Professional Documents
Culture Documents
VESTIBULARSusan J. Herdman, Richard Clendaniel-Vestibular Rehabilitation-F.a. Davis Company (2014)
VESTIBULARSusan J. Herdman, Richard Clendaniel-Vestibular Rehabilitation-F.a. Davis Company (2014)
VESTIBULARSusan J. Herdman, Richard Clendaniel-Vestibular Rehabilitation-F.a. Davis Company (2014)
F. A. Davis Company
1915 Arch Street
Philadelphia, PA 19103
www.fadavis.com
Copyright © 2014 by F. A. Davis Company. All rights reserved. This product is protected by copyright. No part
of it may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic,
mechanical, photocopying, recording, or otherwise, without written permission from the publisher.
As new scientific information becomes available through basic and clinical research, recommended treatments
and drug therapies undergo changes. The author(s) and publisher have done everything possible to make this
book accurate, up to date, and in accord with accepted standards at the time of publication. The author(s), editors,
and publisher are not responsible for errors or omissions or for consequences from application of the book, and
make no warranty, expressed or implied, in regard to the contents of the book. Any practice described in this
book should be applied by the reader in accordance with professional standards of care used in regard to the
unique circumstances that may apply in each situation. The reader is advised always to check product information
(package inserts) for changes and new information regarding dose and contraindications before administering any
drug. Caution is especially urged when using new or infrequently ordered drugs.
Authorization to photocopy items for internal or personal use, or the internal or personal use of specific
clients, is granted by F. A. Davis Company for users registered with the Copyright Clearance Center (CCC)
Transactional Reporting Service, provided that the fee of $.25 per copy is paid directly to CCC, 222 Rosewood
Drive, Danvers, MA 01923. For those organizations that have been granted a photocopy license by CCC, a
separate system of payment has been arranged. The fee code for users of the Transactional Reporting Service is:
978-0-8036-3970-6/140/ + $.25.
3970_FM_i-xxvi 01/07/14 12:13 PM Page v
This book is dedicated to “serendipity.” The serendipity that led to me walking into a patient’s
room one weekend and finding there the person who would become my doctoral advisor. The
serendipity that led to that surprising day when, after years of saying “no” to treating patients for
their dizziness, I saw my first patient with BPPV and was forever “hooked” by that patient’s
gratitude. The serendipity that led to me working at Hopkins and NIH. The serendipity that led to
four colleagues sitting down and planning a competency-based course in Vestibular
Rehabilitation that we thought would last maybe 3 or 4 years. The serendipity that put so many
wonderful opportunities in my life. The serendipity that put so many incredible people in my life.
The grace that led me to take advantage of it all.
SJH
I would like to dedicate this book to my family who has supported me throughout, to my
colleagues who have contributed to this book and to my education, and to my friend, colleague,
mentor, and coeditor whose knowledge, guidance, and inspiration have been critical to my
professional growth.
RAC
3970_FM_i-xxvi 01/07/14 12:13 PM Page vi
3970_FM_i-xxvi 01/07/14 12:13 PM Page vii
Foreword
Benjamin Franklin once said, “Life’ s tragedy is that we themselves. Undoubtedly, Dr. Herdman has assembled
get old too soon and wise too late.” While there is substan- the next generation of contributors. Amongst the 34 in-
tial wisdom in that statement, I can think of at least one dividuals whose collective efforts define the 4th edition
exception that might set old Ben on his rear, or is it ear? It of Vestibular Rehabilitation, 14 are first timers and all
is hard to believe that 20 years have passed since the first possess the skill and knowledge to become persistent con-
edition of Vestibular Rehabilitation was published. Yet tributors to subsequent editions. As one reads Chapters 3
even at its birth there w as considerable wisdom in its (Laurie King), 6 (Anne Galgon), 7 (Natalia Ricci), 13
words. At that time the responsibility for e valuating and (Steve Benton), 14 (Rosalyn Schneider), 17 (Yew Ming
rehabilitating patients presenting with dizziness and Chan), 19 (Jeffrey Staab), 20 (Jeff Hoder), 24 (Jennifer
vestibular compromise was restricted to a select few, and Braswell Christy), 26 (Laura Morris and Kim Gottshall),
this area of rehabilitation had not emerged as a specialty. 28 (Courtney Hall and Dara Meldrum) and 30 (Lisa
Susan Herdman recognized a need to train rehabilitation Heusel-Gillig and Courtne y Hall), please kno w that
clinicians to better understand and treat the postural com- while these individuals might not be the sole author of
promise generated through visual def icits, headache or those respective contributions, their effort to revise pre-
other maladies that would adversely impact the quality of vious content was substantial and the resulting quality
life of those unfortunate enough to have acquired vestibu- of their work is outstanding.
lar pathologies. The extent to which this kno wledge has In this edition, all chapters ha ve been updated and
grown over these two decades and with it, the interest of new cases permeate the management chapters to illus-
students and clinicians is truly extraordinary. Throughout trate how patients with specific problems are treated. The
this time Vestibular Rehabilitation has remained the “go thought-provoking and problem solving nature of the
to” text for specialists in this area while also serving as a clinical chapters are supported by the necessity to foster
critical reference source for all neurorehabilitationists. evidence based references, a fundamental tenet of all vol-
All contributors to the Contemporary Perspectives umes in the Contemporary Perspectives in Rehabilitation
in Rehabilitation series have always prided themselves series. While the 3rd edition of Vestibular Rehabilitation
on maintaining the infrastructural inte grity of its foun- was accompanied by 68 videos, this edition has over 100.
dation…….evidence based referencing, problem solving The videos include normal and abnormal e ye move-
presentations and the latest and most novel data or treat- ments, assessment procedures, demonstrations of some
ment techniques. Vestibular Rehabilitation continues to exercises, and gait assessments. Chapters emphasizing
adhere to these principles and undoubtedly the result has tinnitus, novel approaches in the assessment and treat-
been a steadfast allegiance to its content from amongst ment of anterior and horizontal canal benign paroxysmal
its followers…….teachers, clinicians and students. The positional vertigo (BPPV), and data on outcomes in
fact that the content has been updated consistently at patients with unilateral and bilateral vestibular hypofunc-
5 year intervals speaks to the dedication shown by its con- tion are distinctly ne w to the 4th edition. The manage-
tributing authors, many of whom have persisted through ment of patients with chronic subjecti ve dizziness
several editions. Throughout this time, Dr. Herdman has represents another addition to the text. These are patients
amassed a larger international cohort of knowledgeable who present with chronic dizziness and motion sensitiv-
clinicians, many of whom ha ve come to assist her in ity that often is accompanied by variable amounts of anx-
what arguably might be called the most popular (and in- iety and phobic behavior.
tense) vestibular rehabilitation course in the United The text has been further contemporized through
States, if not the world. Many of those once considered the addition of a chapter on the management of patients
novices are now positioned to disseminate information with vestibular problems precipitated from head trauma
vii
3970_FM_i-xxvi 01/07/14 12:13 PM Page viii
viii FOREWORD
including etiologies from post-concussion syndrome restore optimal balance, reduce dizziness or improve the
caused by blast injuries. Regrettably there is ample rea- consequences of migraine, as examples.
son to believe that the incidence of this problem may be The contributions from vestibular neurorehabilitation
profoundly underestimated. If so, then this cate gory of therapists and specialty physicians are woven along a highly
patient will present unique challenges to v estibular re- integrated network. Over each edition, the blend of input
habilitation clinicians and the treatment components from these specialists becomes more tightly coupled. This
may well incorporate a need to foster compliance b e- fluidity may go unrecognized by students, b ut suffice to
cause of concomitant behavioral changes. Additional in- say, there are very few courses, let alone text books, in which
formation is contained in information regarding emerging the content amongst dif ferent specialists, both physician
technologies for the treatment of patients with vestibular and non-physician, can be assembled and transmitted so
disorders. Such rehabilitation includes novel biofeedback smoothly. Herein rests an opportunity to learn from a panel
alternatives, use of virtual reality and gaming, such as of experts who would be very difficult to assemble collec-
the Wii. These advances, while challenging, provoke op- tively. As I concluded in a pre vious Foreword, the sum of
portunities to discover and implement new approaches these parts is truly greater than its whole………
towards enlisting functional plasticity to achie ve en-
hanced quality of life. We can be rest assured that Steven L. Wolf, Ph.D., PT, FAPTA, FAHA
advances in technologies and de vices will continue
Series Editor
to make their way into the armamentarium of tools to
3970_FM_i-xxvi 01/07/14 12:13 PM Page ix
Preface
There are several additions to the fourth edition of Vestibu- since the last edition 7 years ago. So once again, we have
lar Rehabilitation. One change is the addition of Richard extended the material presented to include se veral new
A. Clendaniel as the coeditor. Rick is a clinician, educator, chapters to reflect and to challenge our understanding
and researcher with many years of experience in vestibular of the assessment and treatment of v estibular disorders.
rehabilitation, vestibular function testing, and v estibular One new chapter is on management of patients with
physiology. His contributions to the f ield have been of chronic subjective dizziness and is a nice complement to
benefit to many clinicians and researchers as well as to pa- the chapter of psychological problems in patients with
tients. The other changes in this edition of Vestibular Re- dizziness. Another chapter tackles a current “hot topic”—
habilitation are the e xploration of ne w areas of management of patients with vestibular dysfunction from
“vestibular” rehabilitation including current evidence that concussion. Finally, a third new chapter explores the role
supports the use of the gaze stabilization exercises in pa- of emerging technologies such as virtual reality , sensory
tients with non-vestibular dizziness and the use of ne w substitution devices, and most e xcitedly, vestibular im-
technologies in exercise programs. plants, which will undoubtedly require new treatment ap-
The practice of vestibular rehabilitation faces numer- proaches. Of course, all chapters contain ne w material,
ous challenges in the coming years, as does all health care. from management of tinnitus to the newer treatments that
We must be more ef ficient in our assessments and treat- have been proposed for anterior and horizontal semicircu-
ments. We must provide evidence that the patient is improv- lar canal BPPV. We have added “point and counterpoint”
ing through the application of functional outcome measures. sections in some chapters that highlight the differing opin-
We must be able to defend our choice of treatment based ions about assessment and treatment. The number of
on research establishing the benefits of specific exercises or videos has been increased to include more e xamples of
establishing that a specific exercise is not beneficial. We eye movement abnormalities and to provide visual exam-
must be able to support our recommendation on the need ples of some of the newer treatments.
for further treatment based on measures that suggest the pa- The many chapters in this book are designed to pro-
tient has or has not reached the optimal le vel of recovery. vide you with a foundation for all these challenges, b ut
We need to address the psychological state of the patient as more importantly, the chapters will hopefully gi ve you
well as the physical problems and their consequences. the basis from which you can continue to apply ne w in-
As you should hope, the e vidence supporting the formation in your practice for the betterment of all your
treatment of patients with vestibular deficits has increased patients.
ix
3970_FM_i-xxvi 01/07/14 12:13 PM Page x
3970_FM_i-xxvi 01/07/14 12:13 PM Page xi
Contributors
Steve Benton, AuD Marianne Dieterich, MD, FANA Courtney D. Hall, PT, PhD
Tinnitus Program Manager Professor, Department of Neurology Research Health Scientist
Staff Audiologist University Hospital Audiology and Vestibular Research
VA Medical Center Ludwig-Maximilians University of Enhancement Award Program
Decatur, GA Munich Mountain Home VA Medical Center
Munich, Germany Mountain, Home, TN
Thomas Brandt, MD, FRCP and
Professor, Clinical Neurosciences Michael Fetters, MD Associate Professor
German Center for Vertigo and Associate Professor and Chair Department of Physical Therapy
Balance Disorders Department of Neurology East Tennessee State University
Ludwig-Maximilians-University SRH Klinikum Karlsbad- Johnson City, TN
Munich, Germany Langensteinbach
Teaching Hospital of University of G. Michael Halmagyi, MD, FRACP
Yew Ming Chan, FRCS Edinburgh, Heidelberg Professor, The Department of
FAMS Karlsbad, Germany Neurology
Senior Clinical Lecturer Director, Eye and Ear Research Unit
Department of Otolaryngology Anne K. Galgon, PT, PhD, NCS Royal Prince Alfred Hospital
Yong Loo Lin Medical School, Assistant Professor, Department of Sydney, NSW, Australia
Singapore Senior Otolaryngologist Physical Therapy
Consultant College of Health Professions and Janet Helminski, PT, PhD
Department of Otolaryngology Social Work Professor, Department of Physical
Singapore General Hospital Temple University Therapy
Philadelphia, PA College of Health Sciences
Jennifer Braswell Christy, PT, PhD Midwestern University
Associate Professor Kim Gottshall, PT, PhD, ATC Downers Grove, IL
Department of Physical Therapy Director of Vestibular Assessment
The University of Alabama at and Rehabilitation Lisa Heusel-Gillig, PT, DPT, NCS
Birmingham San Diego Naval Medical Center Adjunct Faculty Member, DPT
Birmingham, AL Dan Diego, CA Program
Emory University School of
Helen S. Cohen, EdD, OTR, FAOTA Timothy C. Hain, MD Medicine
Professor, Bobby R. Alford Professor (Emeritus) Senior Physical Therapist
Department of Otolaryngology – Private Practice Emory Dizziness and Balance
Head and Neck Surgery Chicago Dizziness and Hearing Center
Baylor College of Medicine Chicago, IL Emory University Healthcare
Houston, TX Atlanta, GA
Ian S. Curthoys, PhD
Professor, School of Psychology
Director, Vestibular Research
Laboratory
The University of Sydney, NSW
Sydney, Australia
xi
3970_FM_i-xxvi 01/07/14 12:13 PM Page xii
xii CONTRIBUTORS
Jeffrey M. Hoder, PT, DPT, NCS Gregory F. Marchetti, PT, PhD Rosalyn Schneider, BA
Assistant Professor, Department of Associate Professor Research Assistant
Neurology Department of Physical Therapy Department of Neurology
Virginia Commonwealth University Rangos School of the Health Case Western Reserve School of
Richmond, VA Professions Medicine
and Duquesne University Cleveland, OH
Program Director of Rehabilitation Pittsburgh, PA
and Wellness Michael C. Schubert, PT, PhD
Douglas E. Mattox, MD Associate Professor, Departments of
VCU Parkinson’s and Movement
William Chester Warren Jr., MD Otolaryngology Head and Neck
Disorders Center
Professor of Otolaryngology Surgery and Physical Medicine
Richmond, VA
Chair, Department of Otolaryngology and Rehabilitation
Fay Bahling Horak, PT, PhD – Head & Neck Surgery Johns Hopkins University School of
Professor of Neurology Emory University School of Medicine Medicine
Adjunct Professor of Bioengineering Atlanta, GA Baltimore, MD
Oregon Health and Science
Dara Meldrum, PT, MSc, PhD Neil T. Shepard, PhD
University
Lecturer Professor of Audiology
Portland, OR
School of Physiotherapy Mayo Clinic College of Mediicne
Emily A. Keshner, PT, EdD Royal College of Surgeons in Ireland Chair of Audiology and
Professor and Chair, Department of Dublin, Ireland Director of Dizziness and Balance
Physical Therapy Disorders Program
Laura Morris, PT, NCS
College of Health Professions and Mayo Clinic
Physical Therapist Specialist, Mild
Social Work Rochester, MN
Brain Injury program
Temple University Sinai Hospital of Baltimore Jeffrey P. Staab, MD, MS
Philadelphia, PA Baltimore, MD Associate Professor of Psychiatry
Laurie A. King, PT, PhD Sharon H. Polensek, MD, PhD Mayo Clinic College of Medicine
Assistant Professor, Neurology Chief, Audiology and Speech Department of Psychiatry and
Balance Disorders Laboratory Pathology Psychology
Oregon Health and Science Atlanta VA Medical Center Mayo Clinic
University Decatur, GA Rochester, MN
Portland, OR and Ronald J. Tusa, MD, PhD
Rob Landel, PT, DPT, OCS, CSCS, Assistant Professor of Neurology Professor, Departments of Neurology
FAPTA Dizziness and Balance Center and Otolaryngology-Head and Neck
Professor, Clinical Physical Therapy Emory University Hospital Midtown Surgery, Emory University School
Director, Doctor of Physical Therapy Atlanta, GA of Medicine
Program Natalia A. Ricci, PT, PhD Director, Dizziness and Balance
Director, Clinical Residency Division of Otoneurology, Center, Emory Midtown Hospital,
Programs Division of Biokinesiology Department of Otolaryngology- Atlanta, GA
and Physical Therapy at Head and Neck Surgery,
Herman Ostrow School of Dentistry Susan L. Whitney, DPT, PhD, NCS,
Federal University of Sao Paulo
University of Southern California ATC, FAPTA
Sao Paulo, SP, Brazil
Los Angeles, CA Professor, Departments of Physical
Rose Marie Rine, PT, PhD Therapy and Otolaryngology
R. John Leigh, MD Associate Professor University of Pittsburgh
Blair-Daroff Professor of Neurology Marshall University School of Pittsburgh, PA
Case Western Reserve University Physical Therapy
Cleveland, OH Huntington, WV
and
President, Specialty Therapy Source
LLC
Jacksonville, FL
3970_FM_i-xxvi 01/07/14 12:13 PM Page xiii
Reviewers
Heather D. Anderson, PT, DPT, Yi-Po Chiu, PT, PhD Neeraj Kumar, MS, PT, PhD
NCS Assistant Professor Assistant Professor
Assistant Professor Louisiana State University Health Texas Tech University Health
Neumann University Sciences Center Sciences Center
Aston, PA New Orleans, LA Odessa, TX
Susan Barker, PT, PhD Carolyn K. Craven, PT, DPT Barbara S. Robinson, PT, DPT
Professor Clinical Assistant Professor Associate Professor
Misericordia University University of Oklahoma Health Missouri State University
Dallas, PA Sciences Center Springfield, MO
Oklahoma City, OK
Richard W. Bohannon, EdD, DPT, Rachel D. Trommelen, PT, DPT,
NCS, FAPTA, FAHA, FASNR, Cheryl Ford-Smith, PT, DPT, MS, NCS
CEEAA NCS Assistant Professor
Professor Associate Professor Louisiana State University Health
University of Connecticut Virginia Commonwealth University Sciences Center
Storrs, CT Richmond, VA New Orleans, LA
xiii
3970_FM_i-xxvi 01/07/14 12:13 PM Page xiv
Acknowledgments
I want to share with anyone who finds difficulty in master- I would like to express my sincere gratitude to the au-
ing the information in this book and mastering how to treat thors who shared their kno wledge and expertise in this
people with “dizziness” that it’s not unusual to start with a edition of Vestibular Rehabilitation; it is their contribu-
very real sense of inadequacy! I will always remember that tions that make this text such a v aluable resource for
during my early attempts to learn about “vestibular rehabil- understanding and treating the patient with dizziness.
itation” I visited Fay Horak and w as mystified as to how I would like to also thank the patients, clinicians, and stu-
everyone knew that the patient had a central rather than a dents who question and challenge what we do, forcing
peripheral vestibular deficit. If it’s any encouragement, I us to rethink our assumptions, to continue to learn, and
realize that I have come a “long way” since then but I would continue to investigate the “best” treatments for individ-
also add that I am still learning and I hope I always will be. uals suffering from v estibular disorders. I ha ve been
And so, I w ould like to express my gratitude again to the blessed to learn from some of the v ery best, and recog-
many people it has been my good fortune to meet, w ork nizing all these indi viduals by name w ould fill many
with, teach, treat, and learn from over my years as a physical pages. So I would simply like to offer my thanks to all
therapist. These have included outstanding scientist- who have taught me o ver the years, to fortuitous meet-
clinicians in the field of vestibular rehabilitation (many of ings on Nantucket, and to an atypical insight that k ept
whom have authored chapters in this book), teachers and me from asking a really stupid question. Lastly , an im-
clinicians from all over the world, students, and of course, mense ‘thank you’ to my f amily for their lo ve, support
patients. Thank you all so much. and encouragement over the years.
SJH RAC
xiv
3970_FM_i-xxvi 01/07/14 12:13 PM Page xv
Contents in Brief
Section I Fundamentals of Function, 1 Chapter 17 Surgical Management of Vestibular
Chapter 1 Anatomy and Physiology of the Disorders, 285
Normal Vestibular System, 2 Chapter 18 Management of Psychological
Chapter 2 Vestibulo-ocular Reflex Problems and the Dizzy
Adaptation, 20 Patient, 296
Chapter 3 The Role of Vestibular System in Chapter 19 Management of the Patient with
Postural Control, 29 Chronic Subjective Dizziness, 309
Section II Fundamentals of Dysfunction, 49 Section V Rehabilitation, Assessment and
Chapter 4 Vestibular System Disorders, 50 Management of Peripheral
Chapter 5 Vestibular Lesions of the Central Vestibular Disorders, 323
Vestibular Pathways, 59 Chapter 20 Physical Therapy Management of
Chapter 6 Postural Abnormalities in Benign Paroxysmal Positional
Vestibular Disorders, 85 Vertigo, 324
Chapter 7 Disability in Vestibular Appendix A Differential Diagnosis: BPPV versus
Disorders, 110 Central Positional Nystagmus and
Chapter 8 Vestibular Compensation– Vertigo Mimicking BPPV, 355
Recovery after Unilateral Chapter 21 Physical Therapy Assessment of
Vestibular Loss, 121 Vestibular Hypofunction, 359
Chapter 9 Compensatory Strategies in Appendix 21-A Initial Evaluation Form, 388
Recovery for Vestibulo-ocular Appendix 21-B Dizziness Handicap
Hypofunction, 151 Inventory, 392
Section III Medical Assessment and Vestibular Chapter 22 Physical Therapy Treatment of
Function Tests, 159 Vestibular Hypofunction, 394
Chapter 10 History and Clinical Chapter 23 Physical Therapy Management of
Examination, 160 Bilateral Vestibular Hypofunction
Chapter 11 Vestibular Function Tests, 178 and Loss, 432
Chapter 12 Otolith Function Tests, 195 Chapter 24 Physical Therapy Management of
Chapter 13 Assessment and Management Children with Vestibular
of Auditory Disorders and Dysfunction, 457
Tinnitus, 227 Chapter 25 Physical Therapy Management of
Section IV Medical and Surgical the Older Person with Vestibular
Management, 249 Dysfunction, 480
Chapter 14 Pharmacological and Optical Chapter 26 Physical Therapy Management
Methods to Treat Vestibular of the Patient with Vestibular
Disorders and Nystagmus, 250 Dysfunction from Head Trauma, 504
Chapter 15 Medical Management of Migraine, Chapter 27 Physical Therapy Diagnosis: Clinical
Ménière’s Disease, and Motion Decision-Making for Vestibular
Sensitivity, 266 Disorders, 530
Chapter 16 Medical Management of Mal Chapter 28 The Role of Emerging Technologies
de Débarquement Syndrome, 281 in Vestibular Rehabilitation, 537
xv
3970_FM_i-xxvi 01/07/14 12:13 PM Page xvi
Contents
SECTION I Somatosensory Reflexes, 13
Fundamentals of Function 1 Neurophysiology of Benign Paroxysmal
Positional Vertigo, 13
Chapter 1 Higher-Level Vestibular Processing, 14
Anatomy and Physiology of the Normal Velocity Storage, 14
Vestibular System, 2 Internal Estimation—Going Beyond
Timothy C. Hain, MD, Janet Helminski, PhD, PT
Reflexes, 15
Purpose of the Vestibular System, 2 Higher Level Problems of the Vestibular
The Peripheral Sensory Apparatus, 3 System, 16
Bony Labyrinth, 3 Compensation for Overload, 16
Membranous Labyrinth, 3 Vestibular Ambiguity, 16
Hair Cells, 4 Motion Sickness, 16
Vascular Supply, 5 Repair, 17
Physiology of the Periphery, 6 Summary, 17
Semicircular Canals, 6
Otoliths, 7
Chapter 2
The Vestibular Nerve, 8
Vestibulo-ocular Reflex Adaptation, 20
Michael C. Schubert, PT, PhD
Central Processing of Vestibular Input, 8 Role of Vision and Head Motion in
Vestibular Nucleus, 9 Adaptation—Overview, 20
Vascular Supply, 9 Critical Evidence of VOR Adaptation in
Cerebellum, 9 Animals, 21
Neural Integrator, 11 Consolidation of VOR Learning, 22
Motor Output of the Vestibular System Role of the Peripheral End Organ in VOR
Neurons, 11 Adaptation, 22
Output for the Vestibulo-ocular Reflex, 11 Brainstem versus Cerebellar Site of
Output for the Vestibulospinal Reflex, 11 Adaptation, 22
Vestibular Reflexes, 11 Unique Neuroplasticity Dependent on
Lesion Type, 24
The Vestibulo-ocular Reflex, 11
The Vestibulospinal Reflex, 12 Critical Evidence of VOR Adaptation in
Human, 24
The Vestibulocollic Reflex, 12
Short-term VOR Adaptation in Normal
Cervical Reflexes, 12 Function, 24
The Cervico-ocular Reflex, 12 VOR Gain Retention, 25
The Cervicospinal Reflex, 12 VOR Adaptation in Unilateral Vestibular
The Cervicocollic Reflex, 13 Hypofunction, 25
Visual Reflexes, 13 Summary, 25
xvii
3970_FM_i-xxvi 01/07/14 12:13 PM Page xviii
xviii CONTENTS
Chapter 4 Chapter 6
Vestibular System Disorders, 50 Postural Abnormalities in Vestibular
Michael Fetter, MD Disorders, 85
Benign Paroxysmal Positional Vertigo, 50 Emily A. Keshner, PT, EdD, Anne K. Galgon, PT, PhD, NCS
CONTENTS xix
xx CONTENTS
CONTENTS xxi
xxii CONTENTS
CONTENTS xxiii
Case Study 20-5, 348 Appendix 21-A Initial Evaluation Form, 388
Case Study 20-6, 349 Appendix 21-B Dizziness Handicap
Case Study 20-7, 349 Inventory, 392
Case Study 20-8, 350 Chapter 22
Summary, 350 Physical Therapy Treatment of
Appendix 20-A Differential Diagnosis: Vestibular Hypofunction, 394
BPPV versus Central Postional Nystagmus Susan J. Herdman, PT, PhD, FAPTA, Susan L.Whitney, DPT,
and Vertigo, 355 PhD, NCS, ATC, FAPTA
xxiv CONTENTS
CONTENTS xxv
Subjective Symptom Scales for Assessment Key Concepts Related To Virtual Reality, 538
of mTBI/Concussion, 510 Virtual Reality–Based Vestibular
Neurocognitive Testing, 510 Rehabilitation, 538
Clinical Examination, 511 High-End Systems, 539
Oculomotor Findings in TBI, 511 Off-the-Shelf Systems, 542
Intervention Considerations, 512 Virtual Reality–Based Assessment, 545
Problem-oriented Approach, 512 Technology for Augmented Sensory
Gaze Stability Deficits, 513 Biofeedback, 546
Visual Motion Intolerance, 513 Vestibular Electrical Stimulation, 546
Motion Sensitivity, 513 Tongue Electrotactile Stimulation, 546
Postural Instability, 514 Auditory Biofeedback, 547
Exertion Intolerance, 514 Vibrotactile Biofeedback, 547
Acute Management Issues, 514 Other Technologies, 548
Management Considerations with Chronic Platform Perturbations, 548
TBI, 515 Smart Phones and Tablet Applications, 548
Evidence for Efficacy of Vestibular Case Study 28-1, 549
Rehabilitation with TBI, 516 Summary, 551
Coordination of Care and the Team
Approach, 516
Prognosis: Factors that Contribute to
SECTION VI
Outcome, 517 Non-vestibular Dizziness, 555
Case Study 26-1, 517
Chapter 29
Case Study 26-2, 520 Non-vestibular Dizziness and
Case Study 26-3, 523 Imbalance, 556
Summary, 525 Ronald J. Tusa, MD, PhD
Disuse Disequilibrium (or Deconditioning)
Chapter 27 and Fear of Fall, 556
Physical Therapy Diagnosis: Clinical Description, 556
Decision-Making for Vestibular Useful Outcome Tests, 557
Disorders, 530 Management, 557
Susan J. Herdman, PT, PhD, FAPTA
Leukoaraiosis and Normal-Pressure
Clinical Decision-Making Paradigm for Hydrocephalus, 557
Vestibular Disorders, 531
Description, 557
3970_FM_i-xxvi 01/07/14 12:13 PM Page xxvi
xxvi CONTENTS
ONE
Fundamentals
of Function
3970_Ch01_001-019 25/06/14 11:23 AM Page 2
CHAPTER 1
Anatomy and
Physiology of the
Normal Vestibular
System
Timothy C. Hain, MD ■ Janet Helminski, PhD, PT
2
3970_Ch01_001-019 25/06/14 11:23 AM Page 3
Eye labyrinths, contains the hair cells, which are the motion
movement receptors of the v estibular system. The labyrinth is bor -
dered laterally by the air -filled middle ear and medially
Motor Motor
commands neurons by the temporal bone and is posterior to the cochlea.
Body
movement
Bony Labyrinth
Vestibular Vestibular
proprioceptive nuclear Efference The bony labyrinth consists of three semicircular canals
visual complex copy (SCCs), the cochlea, and a chamber between the tw o
called the vestibule (Fig. 1.3). The bony labyrinth is filled
with perilymphatic fluid, which has chemistry similar to
Adaptive
processor
cerebrospinal fluid (high Na:K ratio). Perilymphatic fluid
(mainly communicates via the cochlear aqueduct with cere-
cerebellum) brospinal fluid. Because of this communication, disorders
that affect spinal fluid pressure (such as lumbar puncture)
Figure 1.1 Block diagram illustrating the organization of
the vestibular system. (Copyright Timothy C. Hain, MD.) can also affect inner ear function.2
Bone
Membrane
Cochlea
Vestibule
Ampulla
Cupula
Figure 1.3 The membranous and bony labyrinths. (Adapted from an illustration by Mary
Dersch from Pender, 1992.)2
of the saccule and the floor of the utricle. Each hair cell
is innervated by an afferent neuron whose cell body lies
in the vestibular (Scarpa’s) ganglion, which is located
close to the ampulla. When hairs are bent toward or away
from the longest process of the hair cell, f iring rate
increases or decreases in the v estibular nerve (see
Fig. 1.4A). A flexible, diaphragmatic membrane called
the cupula overlies each crista and completely seals the
ampulla from the adjacent vestibule. With angular head
motion, endolymphatic pressure differs across the cupula
and causes the cupula to bend back and forth, which
stimulates the hair cells (see Fig. 1.4B).4
The otolithic membranes are structures similar to the
cupulae but are weighted. They contain calcium carbonate
(limestone) crystals called otoconia and have substantially Figure 1.5 The otolithic macula and its overlying
membrane.3
more mass than the cupulae (Fig. 1.5). The mass of the
otolithic membrane causes the maculae to be sensitive to
gravity and linear acceleration. In contrast, the cupulae
normally have the same density as the surrounding en- vestibular artery and the common cochlear artery. The an-
dolymphatic fluid and are insensitive to gravity.3 terior vestibular artery supplies the v estibular nerve, most
of the utricle, and the ampullae of the lateral and anterior
SCCs. The common cochlear artery di vides into a main
Vascular Supply
branch, the main cochlear artery, and the vestibulocochlear
The labyrinthine artery supplies the peripheral v estibular artery. The main cochlear artery supplies the cochlea. The
system (Fig. 1.6; see also Fig. 1.11).The labyrinthine artery vestibulocochlear artery supplies part of the cochlea, the
has a variable origin. Most often it is a branch of the anterior ampulla of the posterior semicircular canal, and the inferior
inferior cerebellar artery (AICA—top of 1.6), but occasion- part of the saccule.5
ally it is a direct branch of the basilar artery. Upon entering The labyrinth has no collateral anastomotic network
the inner ear, the labyrinthine artery divides into the anterior and is highly susceptible to ischemia. Only 15 seconds of
Anterior Inferior
Basilar
Cerebellar Artery Anterior
Artery
Vestibular
Artery
Arteries of
the Canals
Labyrinthine
Artery
Common
Cochlear
Artery
Main
Cochlear
Artery
selective blood flow cessation is needed to abolish audi- a time constant of about 7 seconds. This behavior is due to
tory nerve excitability.6 a springlike action of the cupula that tends to restore it to its
resting position.7
Three important spatial arrangements characterize the
Physiology of the Periphery alignment of the SCC’ s loops. First, each canal plane
The hair cells of the canals and otoliths con vert the me- within each labyrinth is perpendicular to the other canal
chanical energy generated by head motion into neural dis- planes, analogous to the spatial relationship between tw o
charges directed to specific areas of the brainstem and the walls and the floor of a rectangular room (Fig. 1.7). Second,
cerebellum. By virtue of their orientation, the canals and paired planes of the SCCs between the labyrinths conform
otolith organs are able to respond selectively to head mo- very closely to each other. The six individual semicircular
tion in particular directions. Because of differences in their canals become three coplanar pairs: (1) right and left
fluid mechanics, the canals respond to angular v elocity, lateral, (2) left anterior and right posterior, and (3) left pos-
and the otoliths to linear acceleration. terior and right anterior. Third, the planes of the canals are
close to the planes of the extraocular muscles, thus allow-
ing relatively simple connections between sensory neurons
Semicircular Canals (related to individual canals) and motor output neurons
The SCCs pro vide sensory input about head v elocity, (related to individual ocular muscles).
which enables the VOR to generate an eye movement that The coplanar pairing of canals is associated with a
matches the velocity of the head movement. The desired push-pull change in the quantity of SCC output. When
result is that the e yes remain stationary in space during angular head motion occurs within their shared plane,
head motion, enabling clear vision. Neural f iring in the endolymph of the coplanar pair is displaced in oppo-
the vestibular nerve is proportional to head v elocity over site directions with respect to their ampullae, and neural
the range of frequencies in which the head commonly firing increases in one vestibular nerve and decreases on
moves (0.5 to 7 Hz). In engineering terms, the canals are the opposite side. For the lateral canals, displacement of
“rate sensors.” the cupula toward the ampulla (ampullopetal flo w) is
This fact poses a signif icant problem: How do the excitatory, whereas for the vertical canals, displacement
hair cells of the SCCs, which are acti vated by displace- of the cupula away from the ampulla (ampullofugal flow)
ment, produce sensory input proportional to velocity? The is excitatory.
labyrinth must have a method of converting head velocity There are three advantages to the push-pull arrange-
into displacement. Biophysical properties of the semicir- ment of coplanar pairing. First, pairing pro vides sensory
cular canals’ loops accomplish the conversion.7 The mem-
branous canal loops ha ve very thin w alls and a small
lumen diameter relative to the radius of the loop curv a-
ture. These characteristics mak e viscous drag on the
endolymph very powerful. Viscosity, or fluidic friction,
slows down endolymph flow in a w ay similar to ho w
honey slowly runs down the side of a jar. In a frictionless
system with a freely moving cupula, for a step of constant
rotational velocity, endolymph displacement w ould be
proportional to velocity times time, or rotational position.
The viscosity creates resistance to endolymph movement
so that trans-cupular pressure and displacement become
more closely proportional to head v elocity. Because of
these considerations, over the usual frequencies of head
movement, endolymph displacement is proportional to
angular head velocity, and the SCCs transmit a v elocity
signal to the brain.
A second important dynamic characteristic of the
canals has to do with their response to prolonged rotation at Figure 1.7 The spatial arrangement of the semicircular
canals. The canals on each side are mutually perpendicular,
constant velocity. Instead of producing a signal proportional are paired with conjugate canals on the opposite side of
to velocity, the canals respond reasonably well only in the the head, and also are closely aligned with the optimal
first second or so, because output decays exponentially with pulling directions of the extraocular muscles.
3970_Ch01_001-019 25/06/14 11:24 AM Page 7
redundancy. If disease af fects the SCC input from one velocity, we ha ve no sense that we are tra veling at
member of a pair (e.g., as in vestibular neuritis), the central 300 miles per hour. However, in the process of taking off
nervous system will still recei ve vestibular information and ascending to cruising altitude, we sense the change
about head velocity within that plane from the contralat- in velocity (acceleration) as well as the tilt of the plane
eral member of the coplanar pair. on ascent. The otoliths therefore differ from the SCC in
Second, such a pairing allo ws the brain to ignore two basic ways: They respond to linear motion instead
changes in neural firing that occur on both sides simulta- of angular motion, and their output is mainly propor -
neously, such as might occur as a result of changes in body tional to acceleration rather than velocity.7
temperature or neurochemistry. These common changes The otoliths have a simpler task to perform than the
in firing in both nerves are not related to head motion and canals. Unlike the canals, which con vert head velocity
are called common-mode noise. The engineering term for into cupular displacement through hydrodynamic viscos-
the desirable feature of ignoring this type of noise is called ity, the otoliths need no special hydrodynamic system to
common-mode rejection. Third, as is discussed in a later do their job. Exquisite sensitivity to gravity and linear
section, a push-pull configuration assists in compensation acceleration is obtained by incorporating crystals of
for overload. calcium carbonate (limestone), the otoconia, into the
otolithic membrane (see Fig. 1.5). Because force is equal
to mass times acceleration, by incorporating a lar ge
Otoliths mass, a gi ven acceleration produces enough shearing
The otoliths register forces related to linear acceleration force to make the otoliths extremely sensitive. (Shearing
(Fig. 1.8). They respond to both linear head motion and force refers to force that is directed perpendicularly to
static tilt with respect to the gravitational axis. The func- the processes of the hair cells.)
tion of the otoliths is illustrated by the situation of a pas- Like the canals, the otoliths respond to motion in all
senger in a commercial jet. During flight at a constant three dimensions (Fig. 1.9). However, unlike the SCC of
one ear, which have one sensory organ for each axis of an-
gular motion, there are two sensory organs for three axes
of linear motion. In an upright indi vidual, the saccule is
vertical (parasagittal), whereas the utricle is horizontally
oriented (near the plane of the lateral SCC). The saccule
senses linear acceleration in the sagittal plane, such as
might be associated with a forward pitch of the head. The
utricle senses acceleration in its predominantly horizontal
plane, such as might be provoked by a roll (lateral tilt) of
the head.8 The two organs together can encode all possible
vectors of linear acceleration.
Because earth’s gravitational field is a linear accel -
eration field, on earth the otoliths register tilt. For example,
as the head is tilted laterally (which is also called roll; see
Fig. 1.9), shear force is exerted on the utricle, while shear
force is lessened on the saccule. Similar changes occur
when the head is tilted forw ard or backward (pitch). Be-
cause linear acceleration can come from tw o sources—
earth’s gravitational field and linear motion—there is an
ambiguity problem. We discuss strategies that the central
nervous system might use to solve this problem in our sec-
tion on higher-level vestibular processing.
For the otoliths, as in the canals, there is redundancy,
because there are organs similar in orientation and func-
tion located on both sides of the head. Push-pull process-
ing for the otoliths is also incorporated into the geometry
of each of the otolithic membranes. Within each otolithic
Figure 1.8 The otoliths register linear acceleration and macula, a curving zone, the striola, separates the direction
static tilt. of hair cell polarization on each side. Consequently, head
3970_Ch01_001-019 25/06/14 11:24 AM Page 8
tilt results in increased af ferent discharge from one part irregular afferents can be turned off with electrical stimulation
of a macula, while reducing the af ferent discharge from without much change in the VOR of monkeys.10 Irregular
another portion of the same macula. This extra redundancy afferents may be important for the VSR and in coordinating
(compared to the SCC) probably mak es the otoliths less responses between the otoliths and canals.
vulnerable to unilateral vestibular lesions. Regular afferents of the monkey have tonic firing rates
of about 90 spikes per second and sensitivity to head velocity
of about 0.5 spikes per degree per second.11,12 We can spec-
The Vestibular Nerve
ulate about what happens immediately after a sudden change
Vestibular nerve fibers are the afferent projections from in head velocity. Humans can easily mo ve their heads at
the bipolar neurons of Scarpa’s (vestibular) ganglion. The velocities exceeding 300 deg/sec. As noted previously, the
vestibular nerve transmits af ferent signals from the SCC are connected in push-pull, so that one side is al ways
labyrinths along its course through the internal auditory being inhibited while the other is being e xcited. Given the
canal (IAC). In addition to the v estibular nerve, the IAC sensitivity and tonic rate noted earlier , the vestibular nerve
contains the cochlear nerve (hearing), the facial nerve, the that is being inhibited should be dri ven to a firing rate of
nervus intermedius (a branch of the f acial nerve, which 0 spikes per second for head v elocities of only 180° per
carries facial sensation), and the labyrinthine artery . The second! In other words, head velocities greater than 180° per
IAC travels through the dense petrous portion of the tem- second may be unquantifiable by half of the vestibular sys-
poral bone to open into the posterior fossa at the le vel of tem. This cutoff behavior has been advanced as the expla-
the pons. Note that “petrous” is deri ved from the Latin nation for Ewald’s second law, which says that responses to
word petrosus, meaning “stone-like, hard,” and thus the rotations that excite a canal are greater than responses for
inner ear is very well protected! The vestibular nerve en- rotation that inhibits a canal. 13,14 Cutoff behavior explains
ters the brainstem at the pontomedullary junction. Because why patients with unilateral v estibular loss a void head
the vestibular nerve is interposed between the labyrinth motion toward the side of their lesion. More is said about
and the brainstem, some authorities consider this nerve a this when we discuss how the central nervous system may
peripheral structure, whereas others consider it a central compensate for overload.
structure. We consider it a peripheral structure.
There are two patterns of firing in vestibular afferent Central Processing of Vestibular
neurons. Regular afferents usually ha ve a tonic rate and
little variability in interspike intervals. Irregular afferents
Input
often show no firing at rest and when stimulated by head There are two main targets for vestibular input from pri-
motion develop highly variable interspike intervals.9 Regular mary afferents: the vestibular nuclear complex and the
afferents appear to be the most important type for the VOR; cerebellum (see Fig. 1.1). The vestibular nuclear complex
3970_Ch01_001-019 25/06/14 11:24 AM Page 9
is the primary processor of v estibular input and imple- the other nuclei and the cerebellum b ut has no primary
ments direct, fast connections between incoming afferent outflow of its own. The vestibular nuclei between the two
information and motor output neurons. The cerebellum is sides of the brainstem are laced together via a system of
the main adaptive processor—it monitors vestibular per- commissures, which are mutually inhibitory. The commis-
formance and readjusts central v estibular processing if sures allow information to be shared between the two sides
necessary. At both locations, v estibular sensory input is of the brainstem and implement the push-pull pairing of
processed in association with somatosensory and visual canals discussed earlier.15
sensory input. In the vestibular nuclear complex, processing of the
vestibular sensory input occurs concurrently with the pro-
cessing of extravestibular sensory information (propriocep-
Vestibular Nucleus
tive, visual, and efferent (see Fig. 1.1). Extensive connections
The vestibular nuclear complex consists of four major nu- between the vestibular nuclear complex, cerebellum, ocular
clei (superior, medial, lateral, and descending) and at least motor nuclei, and brainstem reticular activating systems are
seven minor nuclei (Fig. 1.10). This large structure, lo- required to formulate appropriately oriented and timed sig-
cated primarily within the pons, also extends caudally into nals to the VOR and VSR effector organs, the extraocular
the medulla. The superior and medial vestibular nuclei are and skeletal muscles.
relays for the VOR. The medial vestibular nucleus is also
involved in vestibulospinal reflexes and coordinates head
Vascular Supply
and eye movements that occur together . The lateral
vestibular nucleus is the principal nucleus for the vestibu- The vertebral-basilar arterial system supplies blood to the
lospinal reflex. The descending nucleus is connected to all peripheral and central vestibular system (Fig. 1.11). The
posterior-inferior cerebellar arteries (PICAs) branch of f
the vertebral arteries. The two PICAs are the most impor-
tant arteries for the central vestibular system. They supply
the surface of the inferior portions of the cerebellar hemi-
spheres as well as the dorsolateral medulla, which includes
the inferior aspects of the vestibular nuclear complex. The
basilar artery is the principal artery of the pons.The basilar
artery supplies central vestibular structures via perforator
branches (which penetrate the medial pons), short circum-
ferential branches (which supply the anterolateral aspect
of the pons), and long circumferential branches (which
supply the dorsolateral pons). The AICA is an important
branch of the basilar artery because it is the sole blood
supply for the peripheral v estibular system via the laby-
rinthine artery. The AICA also supplies blood to the ventro-
lateral cerebellum and the lateral te gmentum of the lower
two-thirds of the pons.
Recognizable clinical syndromes with v estibular
components may appear after occlusions of the basilar
artery, labyrinthine artery, AICA, or PICA. PICA territory
strokes, also called “lateral medullary syndrome, ” cause
purely central balance symptoms as a result of damage to
the vestibular nucleus and inferior cerebellum. AICA ter-
ritory strokes cause a mixed peripheral/cerebellar pattern
because AICA supplies both the labyrinth and part of the
Figure 1.10 The vestibulo-ocular reflex (VOR) and cerebellum.
vestibulospinal reflex (VSR) arcs. S, L, M, and D indicate
the superior, lateral, medial, and descending vestibular
nuclei, respectively. The lateral vestibulospinal and medial Cerebellum
vestibulospinal tracts are shown as heavy lines and light
lines, beginning in the lateral vestibular nucleus and medial The cerebellum (Fig 1.12) is a major recipient of outflow
vestibular nucleus, respectively.15 from the vestibular nucleus complex and is also a major
3970_Ch01_001-019 25/06/14 11:24 AM Page 10
4 3 3 4 Cavity of
fourth ventricle
PCA
SCA SCA Reticular
formation
5
6
Fastigial nucleus
Vestibular
nuclei
7
8
9
10 AICA Labyrinth
12 11
A
PICA Hemisphere Vermis
PICA
Anterior
Primary fissure lobe
Posterior
lobe
Horizontal
fissure
Posterior Uvula
fissure Tonsil
Flocculonodular Flocculus
Vertebral Arteries lobe
Figure 1.11 The vertebral-basilar system. Numerals indi- B Nodulus
cate individual cranial nerve roots. (All nerves are paired, Figure 1.12 The cerebellum and its relationship and
but, for clarity, both sides are not always labeled here.) connections to vestibular structures. (A) Sagittal view. The
AICA = anterior inferior cerebellar artery; PCA = posterior vestibular nuclei are connected to the cerebellar vermis, the
cerebellar artery; PICA = posterior inferior cerebellar artery; labyrinth, the superior colliculus and spinal cord. (B) Poste-
SCA = superior cerebellar artery. (Copyright Timothy C. rior view. Most vestibular connections are to the midline
Hain, MD.) structures (vermis, nodulus).
source of input itself. Although not required for vestibular are found typically in patients with the Arnold-Chiari
reflexes, vestibular reflexes become uncalibrated and in- Malformation or other cerebellum disorders.
effective when the cerebellum is remo ved. Figure 1.12A The cerebellar nodulus adjusts the duration of VOR
and B shows the relationship of the cerebellum to the responses and is also involved with processing of otolith
vestibular nucleus, labyrinth, spinal cord, and ascending input. Patients with lesions of the cerebellar nodulus, such
pathways. as patients with medulloblastoma, sho w gait ataxia and
The cerebellar flocculus is required to adapt the gain often have nystagmus, which is strongly af fected by the
of the VOR.16 Adaptation is initially learned in the floc- position of the head with respect to the gravitational axis.
culus, maintained in “softw are,” and, after a delay , is The nodulus is required for motion sickness.18
downloaded to “hardware”—brainstem flocculus target Lesions of the anterior -superior vermis of the cere-
neurons.17 Lesions of the flocculus reduce the ability bellum affect the VSR and cause a profound gait ataxia
of experimental animals to adapt to disorders that reduce with truncal instability. These patients are unable to use
or increase the gain of the VOR. Flocculus disorders sensory input from their lower extremities to stabilize their
3970_Ch01_001-019 25/06/14 11:24 AM Page 11
posture. These lesions are often related to excessive alco- when shoved from behind, one’s center of gravity might
hol intake and thiamine deficiency. become displaced anteriorly . To restore “balance, ” one
might (1) plantarflex at the ankles, (2) take a step, (3) grab
for support, or (4) use some combination of all three activ-
Neural Integrator ities. The VSR also has to adjust limb motion appropriately
Thus far, we have discussed processing of velocity signals for the position of the head on the body (see the frame of
from the canals and acceleration signals from the otoliths. reference problem discussed in the section on higher-level
These signals are not suitable for driving the ocular motor problems in vestibular processing). The VSR must also use
neurons, which need a neural signal encoding eye position. otolith input, reflecting linear motion, to a greater e xtent
The transformation of velocity to position is accomplished than the VOR. Although the eyes can only rotate and thus
by a brainstem structure called the neural inte grator. The can do little to compensate for linear motion, the body can
nucleus prepositus hypoglossi, located just belo w the me- both rotate and translate.
dial vestibular nucleus, appears to provide this function for There are three major white matter pathways that con-
the horizontal oculomotor system. 19 Although a similar nect the vestibular nucleus to the anterior horn cells of the
structure must exist for the connections with the v estibu- spinal cord. The lateral vestibulospinal tract originates from
lospinal system,20 the location of the VSR neural integrator the ipsilateral lateral vestibular nucleus, which receives the
is presently unknown. Clinically, poor function of the ocu- majority of its input from the otoliths and the cerebellum
lomotor neural integrator causes gaze-evoked nystagmus. (see Fig. 1.10). This pathway generates antigravity postural
motor activity or protective extension, primarily in the lower
extremities, in response to the head position changes, which
Motor Output of the Vestibular occur with respect to gra vity. The medial vestibulospinal
System Neurons tract originates from the contralateral medial, superior, and
descending vestibular nuclei (see Fig. 1.10) and mediates
Output for the Vestibulo-ocular Reflex ongoing postural changes or head righting in response to
The output neurons of the VOR are the motor neurons of semicircular canal sensory input (angular head motion).The
the ocular motor nuclei, which drive the extraocular mus- medial vestibulospinal tract descends only through the cer-
cles. The extraocular muscles are arranged in pairs, which vical spinal cord in the medial longitudinal f asciculus and
are oriented in planes very close to those of the canals (see activates cervical axial musculature.
Fig. 1.7). This geometrical arrangement enables a single The reticulospinal tract receives sensory input from all
pair of canals to be connected predominantly to a single the vestibular nuclei as well as all the other sensory and motor
pair of extraocular muscles. The result is conjugate move- systems involved with maintaining balance. This projection
ments of the eyes in the same plane as head motion. has both crossed and uncrossed components and is v ery
There are two white matter tracts that carry output highly collateralized. As a result, the reticulospinal tract
from the vestibular nuclear complex to the ocular motor through the entire extent of the spinal cord is poorly defined
nuclei. The ascending tract of Deiters carries output from but is probably involved in most balance reflex motor actions,
the vestibular nucleus to the ipsilateral abducens nucleus including postural adjustments made to extravestibular sen-
(lateral rectus) during the horizontal VOR. All other sory input (auditory, visual, and tactile stimuli).
VOR-related output to the ocular motor nuclei is transmit-
ted by the medial longitudinal f asciculus (MLF) (see
Fig. 1.12). Because the MLF is often injured in multiple
Vestibular Reflexes
sclerosis, this connection may account for central vestibu- The sensory, central, and motor output components of the
lar symptoms in these patients (see Fig. 1.12).15 vestibular system have been described. We now discuss
their integration into reflexes called the VOR, VSR, and
VCR. Additionally, we include brief descriptions of cer-
Output for the Vestibulospinal Reflex
vical, visual, and somatosensory refle xes. Although not
The output neurons of the VSR are the anterior horn cells directly mediated by the v estibular apparatus, these
of the spinal cord gray matter, which drive skeletal muscle. reflexes have a close interaction with vestibular reflexes.
However, the connection between the v estibular nuclear
complex and the motor neurons is more complicated than
for the VOR. The VSR has a much more difficult task than
The Vestibulo-ocular Reflex
the VOR because there are multiple strate gies to prevent The VOR normally acts to maintain stable vision during
falls, which involve different motor synergies. For example, head motion. The VOR has two components. The angular
3970_Ch01_001-019 25/06/14 11:24 AM Page 12
VOR, mediated by the SCC, compensates for rotation.The 3. Impulses are transmitted via the lateral and medial
linear VOR, mediated by the otoliths, compensates for vestibulospinal tracts to the spinal cord.
translation. The angular VOR is primarily responsible for 4. Extensor activity is induced on the side to which
gaze stabilization. The linear VOR is most important in the head is inclined, and flexor activity is in-
situations where near tar gets are being vie wed and the duced on the opposite side. The head movement
head is being mo ved at relatively high frequencies. An opposes the movement registered by the vestibu-
example of how the horizontal canal VOR is orchestrated lar system.
is the following:
1. When the head turns to the right, endolymphatic The Vestibulocollic Reflex
flow deflects the cupulae to the left (see Fig. 1.4B). The vestibulocollic reflex (VCR) acts on the neck muscu-
2. The discharge rate from hair cells in the right lature to stabilize the head. The reflex head movement pro-
crista increases in proportion to the velocity duced counters the mo vement sensed by the otolithic or
of the head motion, while the discharge rate semicircular canal organs. The precise pathways mediat-
from hair cells in the left lateral crista decreases ing this reflex have yet to be detailed.
(see Fig. 1.4A).
3. These changes in firing rate are transmitted
along the vestibular nerve and influence the dis- Cervical Reflexes
charge of the neurons of the medial and superior The Cervico-ocular Reflex
vestibular nuclei and cerebellum.
4. Excitatory impulses are transmitted via white The cervico-ocular reflex (COR) interacts with the VOR.
matter tracts in the brainstem to the oculomotor The COR consists of eye movements driven by neck pro-
nuclei, which activate the right (ipsilateral) prioceptors that can supplement the VOR under certain
medial rectus and the left (contralateral) lateral circumstances. Normally, the gain of the COR is v ery
rectus. Inhibitory impulses are also transmitted low.21 The COR is facilitated when the vestibular appara-
to their antagonists. tus is injured. 22,23 Although the COR or lack thereof is
5. Simultaneous contraction of the left lateral rec- generally not recognized as a source of clinical distur -
tus and right medial rectus muscles and relax- bance, it is well known that vibration of the neck muscles
ation of the left medial rectus and right lateral in persons with unilateral v estibular loss induces a v ery
rectus occur resulting in lateral compensatory strong nystagmus, often accompanied by vertigo.24
eye movements toward the left.
6. If the eye velocity is not adequate for the given The Cervicospinal Reflex
head velocity and retina image motion is greater
The cervicospinal reflex (CSR) is defined as changes in limb
than 2° per second, the cerebellar projection to
position driven by neck afferent activity. Analogous to the
the vestibular nuclei (see Fig. 1.12) will modify
COR, which supplements the VOR under certain circum-
the firing rate of the neurons within the vestibu-
stances, the CSR can supplement theVSR by altering motor
lar nuclei to reduce the error.
tone in the body. Like the VSR, the CSR consists of an as-
semblage of several reflexes. Two pathways are thought to
The Vestibulospinal Reflex mediate these reflex signals—an excitatory pathway from
the lateral v estibular nucleus and an inhibitory pathw ay
The purpose of the VSR is to stabilize the body. The VSR
from the medial part of the medullary reticular formation.
actually consists of an assemblage of se veral reflexes
When the body is rotated with head stable, neurons of the
named according to the timing (dynamic vs. static or
excitatory vestibulospinal system increase their rate of firing
tonic) and sensory input (canal vs. otolith). An example
on the side to which the chin is pointed. At the same time,
of a vestibulospinal reflex is the sequence of e vents in-
neurons thought to be in the inhibitory reticulospinal system
volved in generating a labyrinthine reflex.
show a reduced rate of firing. This activity leads to extension
1. When the head is tilted to one side, both the of the limb on the side to which the chain is pointed and flex-
canals and otoliths are stimulated. Endolym- ion of the limb on the contralateral side.Vestibular receptors
phatic flow deflects the cupula, and shear force influence both these systems by modulating the f iring of
deflects hair cells within the otoliths. medullary neurons in a pattern opposite to that elicited by
2. The vestibular nerve and vestibular nucleus are neck receptors. The interaction between the ef fects on the
activated. body of v estibular and neck inputs tends to cancel one
3970_Ch01_001-019 25/06/14 11:24 AM Page 13
another when the head mo ves freely on the body so that Somatosensory Reflexes
posture remains stable.25
Somatosensory mechanisms are involved in postural stabil-
ity as well. Bles and associates documented somatosensory-
The Cervicocollic Reflex induced nystagmus (“stepping around n ystagmus”).28
The cervicocollic reflex (CCR) is a cervical reflex that sta- Interestingly, the subjects with bilateral vestibular loss de-
bilizes the head on the body. The afferent sensory changes veloped a more pronounced n ystagmus than did normal
caused by changes in neck position create opposition to subjects. This implies that subjects with bilateral vestibular
that stretch by way of reflexive contractions of appropriate loss use somatosensory information to a greater extent than
neck muscles.21 The degree to which the CCR contributes normal subjects.
to head stabilization in normal humans is presently uncer- On the other side, indi viduals who have “two hits”—
tain, but it seems likely that it is useful primarily to stabi- somatosensory disturbance and vestibular injuries—naturally
lize head movement in the vertical plane and it may also fare more poorly than persons who ha ve well-functioning
be facilitated after labyrinthine loss. Experimental studies, sensory input. For example, patients with diabetic peripheral
mainly in animals, document that cervical blocks can neuropathy recover from vestibular deficits less well than do
cause imbalance and nystagmus.26 persons without neuropathy.29
DARK CELLS
UTRICLE
SACCULE
COCHLEA
CUPULA
DISPLACED OTOCONIA
OTOCONIA
Figure 1.13 Physiology of benign
paroxysmal positional vertigo. Otoco-
nia become displaced from the utricle
and relocate to the bottom of the
posterior semicircular canal, which
is the lowest part of the inner ear.
(Copyright Timothy C.Hain, MD.)
3970_Ch01_001-019 25/06/14 11:24 AM Page 14
bc = 0.68 mm
Cupular Pressure Pc
1 B
A (mPa)
A B C
0.5
C
0
0 5 10 15 20 25
1 A
C
0
bd = 0.16 mm 0 5 10 15 20 25
A B Time(s)
Figure 1.14 Fluid mechanics of benign paroxysmal positional vertigo. (A) Trajectories of
three otoconia after a sudden change of head position that makes the posterior canal vertical.
Otoconia begin close to the cupula, fall through the ampulla with radius bc, and then enter
the duct with radius bd. (B) Simulated pressure, displacement, and nystagmus due to otoconia
falling with the trajectories of A.30
Figure 1.14, from Squires and colleagues,30 illustrates more accurate, and often are at least partially under con-
the fluid mechanics of BPPV. In this disorder, vertigo and scious control. Because these mechanisms are more modi-
nystagmus begin after a characteristic latenc y of about fiable than vestibular reflexes, they are especially relevant to
5 seconds. The delay in onset of symptoms is caused by rehabilitation. Most of these mechanisms process multiple
movement of detached otoconia through the ampulla, be- sensory inputs.
cause pressure caused by mo ving otoconia is ne gligible
until otoconia enter the narrow duct of the SCC. Figure 1.14
Velocity Storage
also shows that particle-wall interactions can account for
variability in duration and latency of BPPV.30 How good does the VOR have to be? To keep the eye still in
Other results from fluid mechanics have direct bear- space while the head is moving, the velocity of eyes should
ing on our understanding of treatment maneuv ers for be exactly opposite to head movement. When this happens,
BPPV. Under the influence of a full 1 g of gravity, typical the ratio of eye movement to head movement velocity, called
otoconia move at a rate of 0.2 mm/sec, or only about 1% the gain, equals –1.0. To maintain normal vision, retinal
of the circumference of the canal each second. It follo ws image motion must be less than 2° per second. In other
that inertial effects of treatment maneuvers can cause neg- words, for a head velocity of 100° per second, which is easily
ligible movement of otoconia and that, practically, sudden produced by an ordinary head mo vement, the gain of the
jerks of the head or maneuvers that incorporate eccentric VOR must be 98% accurate, because any greater error would
moments (such as the Semont maneuv er) are unlikely to cause vision to be obscured.
have a substantial additional effect in comparison with ma- The normal VOR can deliver this high standard of per-
neuvers that rely on gravity to accomplish canalith repo- formance only for brief head mo vements. In other words,
sitioning (such as the Epley maneuver).30 the VOR is compensatory for high-frequenc y head motion
but is not compensatory for lo w-frequency head motion.
This fact can be most easily demonstrated by the response
Higher-Level Vestibular Processing of the SCC to a sustained head movement, which has a con-
In this section we discuss some of the more sophisticated as- stant velocity. The canals respond by producing an exponen-
pects of central vestibular processing, which are not reflexes tially decaying change in neural firing in the vestibular nerve.
but rather require much more processing, are generally much The time constant of the exponential is about 7 seconds, or,
3970_Ch01_001-019 25/06/14 11:24 AM Page 15
in other words, the firing rate decays to 32% of the initial eyes are closed) or inaccurate (such as when a person
amount in 7 seconds. Ideally, the time constant should be in- with positional v ertigo tilts the head) or is noisy? A
finite, which would be associated with no response decline. mechanism that combines sensory inputs, weights them
Apparently, a time constant of 7 seconds is not long enough, according to their relevance, and provides a reasonable
because the central nerv ous system goes to the trouble estimate of orientation in space, even without any recent
to perseverate the response and replace the peripheral time sensory input, is needed.
constant of 7 seconds with a central time constant of about In engineering terms, we are discussing an “estimator.”
20 seconds. The perseveration is provided via a brainstem Navigating the space shuttle in volves similar problems.
structure called the velocity storage mechanism.31 There are hundreds of sensors and man y actuators (motor
The velocity storage mechanism is a repository for outputs). Some sensors respond quickly and some slo wly.
information about head v elocity derived from se veral They may differ in accuracy, scaling, coordinate frame, tim-
kinds of motion receptors. During rotation in the light, the ing, and noise characteristics. A mechanism is needed to
vestibular nucleus is supplied with retinal slip information. integrate sensors and develop an internal estimate of the
Retinal slip is the dif ference between eye velocity and state of the system (i.e., position, velocity, acceleration) to
head velocity. Retinal slip can dri ve the velocity storage keep the shuttle from crashing.
mechanism and keep vestibular-related responses going The engineering solution to this problem developed
even after v estibular afferent information decays. The out of work done by Kalman at MIT, and is often called
vestibular system also uses somatosensory and otolithic a “Kalman filter.” It is also called an “optimal estima-
information to drive the velocity storage mechanism. 32 tor,” or an “internal model.” We prefer the term “optimal
This example shows how the vestibular system resolves estimator.” The essentials of an optimal estimator are
multiple, partially redundant sensory inputs. shown in Figure 1.15. There is v ery strong e vidence
that mechanisms similar to optimal estimators are used
for human sensorimotor processing 33 and vestibular
Internal Estimation—Going Beyond processing.33,34
Reflexes Estimators are f ar more po werful than simple
Reflexes are simple sensory processors that rapidly con- reflexes. There are several key concepts that need to be
vert sensory input into motor outflo w. What happens introduced to understand how they are different. First, in-
when sensory input is not a vailable (such as when the ternal models of transducers and motor output are used to
Feedforward path
Motor Predicted
Command
Forward Model Next State
of Dynamics
Kalman Gain
Predicted Sensory State
Sensory Error Correction
Model of
Feedback
Gain
Sensory
-
Output +
0 1 2
Time(s)
Feedback path Actual Sensory
Feedback
Figure 1.15 Block diagram showing an optimal estimator such as may be used by the human
body for sensorimotor integration. Sensory inflow and motor outflow are used to estimate the
current state.33 Compare to Figure 1.11.
3970_Ch01_001-019 25/06/14 11:24 AM Page 16
The vestibular apparatus provides partially redundant Although most people are capable of abstract thought
information, and this allo ws for the possibility of intra - and can generalize from one conte xt to another, this is not
labyrinthine conflict. Space motion sickness is thought to be the case for vestibular adaptation—there is a high degree of
caused by intralabyrinthine conflict. About 50% of space context dependency in the repair of peripheral v estibular
shuttle astronauts experience motion sickness during the ini- lesions. In other words, adaptations learned within one sen-
tial 24 to 72 hours of orbital flight. It is currently thought sory context may not work within another. For example, a
that space motion sickness is due to a disturbance in “otolith- patient who can stabilize gaze on a tar get with the head
tilt translation.”36 The otoliths normally function in the con- upright may not be able to do so when making the same head
text of a gravitational field, so that at any moment the total movements from a supine posture. Experimentally , in the
force acting on the otoliths is the v ector sum of that due to cat, VOR gain adaptations can be produced that depend on
gravity and that due to linear acceleration of the head. The the orientation of the head. 40 Similarly, when the VOR of
central nervous system e xpects linear acceleration to be cats is trained using head mo vements of low frequency, no
mainly related to tilt because linear acceleration due to grav- training effect is seen at high frequencies.41
ity is usually much greater than that due to acceleration of Another type of conte xt dependency relates to the
the head. When outside of earth’s gravitational field, such as vestibulospinal reflexes and has to do with the difference
is the situation for astronauts in outer space, the only source in reference frames between the head and body. Because
of otolith stimulation is linear acceleration of the head. In the head can move on the body, information about how the
susceptible individuals, the central nervous system continues head is moving may be rotated with respect to the body .
to interpret linear acceleration as being primarily related to For example, consider the situation when the head is
tilt, which is untrue in this situation, causing the motion sick- turned 90° to the right. In this situation, the coronal plane
ness syndrome.36,37 of the head is aligned with the sagittal plane of the body ,
Structures that are generally required for motion sick- and motor synergies intended to prevent a fall for a given
ness include (1) intact labyrinth and central vestibular con- vestibular input must also be rotated by 90°. For example,
nections, (2) cerebellar nodulus and uvula that coordinate patients with v estibular impairment who under go gait
labyrinthine stimuli,18 (3) the chemoreceptive trigger zone training in which all procedures are performed only in a
located in the area postrema, and (4) the medullary vom- particular head posture (such as upright) may sho w little
iting center.38 Why certain subjects are more prone to improvement in natural situations when the head assumes
motion sickness than others is not completely understood. other postures, such as looking down at one’s feet. Little
is understood about the physiology of context dependency.
Repair of central lesions is much more limited than that
Repair available for peripheral lesions; this is the “ Achilles’ heel”
Thus far, we have described some of the problems posed of the vestibular apparatus. Symptoms due to central lesions
by the limitations of the vestibular apparatus and the con- last much longer than symptoms due to peripheral vestibular
straints of physics. In normal individuals, these problems problems. The reason for this vulnerability is not difficult to
can be resolved by relying on redundancy of sensory input understand. To use a commonplace analogy , if your car
and central signal processing. In addition to these intrinsic breaks down, you can take it to the repair shop and get it
problems, there are also extrinsic problems that are related fixed. If, however, both your car and the repair shop are bro-
to ongoing changes in sensory apparatus, central process- ken, you ha ve a much bigger problem. The cerebellum
ing capabilities, and motor output channels. Because being fulfills the role of the repair shop for the v estibular system.
able to see while one’s head is moving and avoiding falls When there are cerebellar lesions, or lesions in the pathways
are so important to survi val, the repair f acility of the to and from the cerebellum, symptoms of vestibular dysfunc-
vestibular system must be considered as an inte gral part tion can be profound and permanent. Clinicians use this rea-
of its physiology. For this reason, it is our final topic. soning when they attempt to separate peripheral from central
Adaptive plasticity for peripheral v estibular lesions vestibular lesions. A spontaneous nystagmus, which persists
is amazingly competent, even enabling the vestibular sys- over several weeks, is generally due to a central lesion; a
tem to adapt to peculiar sensory situations requiring a re- peripheral nystagmus can be repaired by an intact brainstem
versal of the VOR (see Chapter 2 for more details on and cerebellum.
adaptation).39 Adjustments of internal models and weight-
ing of sensory inputs (e.g., Kalman gain) are likely at least
as important as readjustment of reflexes, because internal
Summary
models provide many important features that reflexes can- The vestibular system is an old and sophisticated human
not (such as functioning in the absence of sensory input). control system. Accurate processing of sensory input
3970_Ch01_001-019 25/06/14 11:24 AM Page 18
about rapid head and postural motion is dif ficult as well 18. Bard P, Woolsey CN, et al. Delimitation of central nervous
as critical to survi val. Not surprisingly, the body uses mechanisms involved in motion sickness. Fed Proc.
1947;6(1 Pt 2):72.
multiple, partially redundant sensory inputs and motor
19. Cannon SC, Robinson DA. Loss of the neural integrator of
outputs, combined with a competent central repair capa- the oculomotor system from brain stem lesions in monkey.
bility. The system as a whole can withstand and adapt to J Neurophysiol. 1987;57(5):1383-1409.
major amounts of peripheral v estibular dysfunction. The 20. Ezure K, Sasaki S, et al. Frequency-response analysis of
Achilles’ heel of the vestibular system is a relative inability vestibular-induced neck reflex in cat, II: functional signifi-
cance of cervical afferents and polysynaptic descending
to repair central vestibular dysfunction.
pathways. J Neurophysiol. 1978;41(2):459-471.
21. Peterson B. Cervicocollic and cervicoocular reflexes.
References In: Peterson B, Richmond F, eds. Control of Head
1. Von Bechterew W. Ergebnisse der Durchschneidung des Movement. New York, NY: Oxford University Press;
N. acusticus nebst Erorterung der Bedeutung der semicir- 1988:90-99.
cularen Canale fur das Korpergewicht. Pflugers Arch. Ges. 22. Kasai T, Zee DS. Eye-head coordination in labyrinthine-
Physiol. 1883;30:312-347. defective human beings. Brain Research. 1978;144(1):
2. Pender D. Practical Otology. Philadelphia, PA: JB Lippincott; 123-141.
1992. 23. Botros G. The tonic oculomotor function of the cervical
3. Baloh R, Honrubia V. Clinical Neurophysiology of the joint and muscle receptors. Adv Otorhinolaryngol.
Vestibular System. Philadelphia, PA: F.A. Davis; 1990. 1979;25:214-220.
4. Bach-Y-Rita P, et al. The control of eye movements. 24. Cherchi M, Hain T. Provocative maneuvers for vestibular
New York, NY: Academic Press; 1971. disorders. In: Eggers DZ, Zee DS, eds. Vertigo and Imbal-
5. Schuknecht H. Pathology of the Ear. Philadelphia, PA: ance: Clinical Neurophysiology of the Vestibular System.
Lea and Ferbiger; 1993. New York, NY: Elsevier; 2010:111-134.
6. Perlman HB, Kimura R, et al. Experiments on temporary 25. Pompeiano O. The tonic neck reflex: supraspinal control. In:
obstruction of the internal auditory artery. Laryngoscope. Peterson B, Richmond F, eds. Control of Head Movement.
1959;69(6):591-613. New York, NY: Oxford University Press; 1988:108-119.
7. Wilson V, Jones M. Mammalian Vestibular Physiology. 26. de Jong PT, de Jong JM, et al. Ataxia and nystagmus in-
New York, NY: Plenum; 1979. duced by injection of local anesthetics in the neck. Ann
8. Barber H, Stockwell C. Manual of Electronystagmography. Neurol. 1977;1(3):240-246.
St. Louis, MO: C.V. Mosby; 1976. 27. Lisberger SG. (1990). Visual tracking in monkeys: evi-
9. Goldberg JM, Fernandez C. Physiology of peripheral dence for short-latency suppression of the vestibuloocular
neurons innervating semicircular canals of the squirrel reflex. J Neurophysiol. 63(4):676-688.
monkey, III: variations among units in their discharge 28. Bles W, de Jong JM, et al. Somatosensory compensation
properties. J Neurophysiol. 1971;34(4):676-684. for loss of labyrinthine function. Acta Otolaryngol.
10. Minor LB, Goldberg JM. Vestibular-nerve inputs to the 1984;97(3-4):213-221.
vestibulo-ocular reflex: a functional-ablation study in the 29. Aranda C, Meza A, et al. Diabetic polyneuropathy may
squirrel monkey. J Neurosci. 1991;11(6):1636-1648. increase the handicap related to vestibular disease. Arch
11. Fernandez C, Goldberg JM. Physiology of peripheral Med Res. 2009;40(3):180-185.
neurons innervating semicircular canals of the squirrel 30. Squires TM, Weidman MS, et al. A mathematical model
monkey, II: response to sinusoidal stimulation and dynam- for top-shelf vertigo: the role of sedimenting otoconia in
ics of peripheral vestibular system. J Neurophysiol. BPPV. J Biomech. 2004;37(8):1137-1146.
1971;34(4):661-675. 31. Raphan T, Matsuo V, et al. Velocity storage in the
12. Miles FA, Braitman DJ. Long-term adaptive changes in vestibulo-ocular reflex arc (VOR). Exp Brain Res.
primate vestibuloocular reflex, II: electrophysiological 1979;35(2):229-248.
observations on semicircular canal primary afferents. 32. Hain TC. A model of the nystagmus induced by off
J Neurophysiol. 1980;43(5):1426-1436. vertical axis rotation. Biological Cybernetics. 1986;54
13. Ewald R. Physiologische Untersuchungen ueber das Endor- (4-5):337-350.
gan des Nervus Octavus. Wiesbaden: Bergman; 1892. 33. Wolpert DM, Miall RC. Forward models for physiological
14. Baloh RW, Honrubia V, et al. Ewald’s second law motor control. Neural Netw. 1996;9(8):1265-1279.
re-evaluated. Acta Oto-Laryngologica. 1977;83 34. Oman CM. Motion sickness: a synthesis and evaluation of
(5-6):475-479. the sensory conflict theory. Can J Physiol Pharmacol.
15. Brodal A. Neurological Anatomy in Relation to Clinical 1990;68(2):294-303.
Medicine. New York, NY: Oxford Press; 1981. 35. Israel I, Berthoz A. Contribution of the otoliths to the
16. Highstein SM. Role of the flocculus of the cerebellum in calculation of linear displacement. J Neurophysiol.
motor learning of the vestibulo-ocular reflex. Otolaryngol 1989;62(1):247-263.
Head Neck Surg. 1998;119(3):212-220. 36. Parker DE, Reschke MF, et al. Otolith tilt-translation
17. Sekirnjak C, Vissel B, et al. Purkinje cell synapses target reinterpretation following prolonged weightlessness:
physiologically unique brainstem neurons. J Neurosci. implications for preflight training. Aviat Space Environ
2003;23(15):6392-6398. Med. 1985;56(6):601-606.
3970_Ch01_001-019 25/06/14 11:24 AM Page 19
37. Oman CM, Lichtenberg BK, et al. M.I.T./Canadian 40. Baker J, Wickland C, et al. Dependence of cat vestibulo-
vestibular experiments on the Spacelab-1 mission, IV: ocular reflex direction adaptation on animal orientation
Space motion sickness: symptoms, stimuli, and pre- during adaptation and rotation in darkness. Brain Res.
dictability. Exp Brain Res. 1986;64(2):316-334. 1987;408(1-2):339-343.
38. Harm D. Physiology of motion sickness symptoms. In: 41. Godaux E, Halleux J, et al. Adaptive change of the vestibulo-
Crampton GH, ed. Motion and Space Sickness. Boca ocular reflex in the cat: the effects of a long-term frequency-
Raton, FL: CRC Press; 1990. selective procedure. Exp Brain Res. 1983;49(1):28-34.
39. Gonshor A, Melvill-Jones G. Extreme vestibulo-ocular
adaptation induced by prolonged optical reversal of vision.
J. Physiol (Lond). 1976;256:381.
3970_Ch02_020-028 25/06/14 11:25 AM Page 20
CHAPTER 2
Vestibulo-ocular
Reflex Adaptation
Michael C. Schubert, PT, PhD
The vestibulo-ocular reflex (VOR) has been created with a robust capability for changing the normal VOR by
an incredible plasticity for the purpose of enabling change coupling head motion with tar get motion. When the
inevitable with disease and aging. In f act, without this viewed targets move in such a manner that the image
adaptation, the normal ef fects of age or the constant slips on the retina, the VOR is recalibrated. The direc-
attacks from disease w ould render us with signif icant tion of the recalibrated VOR (increased or decreased)
functional impairments—namely gaze and gait instability. depends on the direction of the target motion in relation
Some examples of the critical and e xtreme plasticity with the head motion. During head rotation, visual fol-
within the VOR include altered VOR gain with newly fit- lowing of targets that move at a velocity different from
ted glasses and complete reversal of the VOR when fitted the head rotation will create an adaptation (change) in
with lenses that demand it. The focus of this chapter is on the gain of the VOR. This is commonly achieved by one
evidence for VOR adaptation from animal and human of two means: (1) targets are viewed wearing lenses that
studies. In particular, I focus on the rob ustness of VOR maximize the visual world (increases target velocity) or
plasticity, evidence for location sites of such plasticity, and minimize the visual w orld (decreases target velocity)
how this adaptation occurs. F or information concerning or (2) targets are viewed that move in a direction oppo-
oculomotor (e.g., compensatory saccade) and v estibu- site the head rotation (increases target velocity) or move
lospinal compensatory strategies that may assist a def i- in the same direction of head rotation (decreases tar get
cient VOR, please see Chapters 6 and 9. velocity). The difference between the target velocity and
the eye velocity is termed retinal slip and can be quan-
Role of Vision and Head Motion tified. Retinal slip is therefore a v elocity error signal,
thought to be the most ef fective means for changing
in Adaptation—Overview VOR behavior (e.g., VOR gain).1,2
Two sensory stimuli are required for significant adapta-
Eye rotation—angular motion of the eye along a
tion of the VOR: vision and head motion. Traditionally,
specified axis. For example, torsion refers to a
adaptation paradigms designed to enhance the gain of
clockwise or counterclockwise rotation around a
the VOR have been done with short-term (less than
cephalocaudal axis (the line of sight) when the eye
1 hour) or long-term (greater than 1 day) time exposure.
is at its centered and primary position.
A number of VOR adaptation studies have demonstrated
20
3970_Ch02_020-028 25/06/14 11:25 AM Page 21
Adaptation in Animals
Early and seminal studies, critical for establishing thera-
peutic principles of gaze and gait stability, investigated the
role of vision and motion in animals that underwent a uni-
lateral vestibular lesion.3-5 Data suggest when animals
with a lesioned VOR are restrained to a darkened environ-
ment, the VOR does not recover, and imbalance persists.
Once those same animals are released into the light, their
VOR and balance begin to recover. This has been demon- Irregular Afferent
strated across canal plugging, labyrinthectomy, and neurec-
tomy lesions, suggesting that it is a uni versal principle
of VOR adaptation after v estibular hypofunction. It w as
hypothesized that light exposure was critical for VOR re-
covery because it revealed retinal slip, which would occur
when the visual environment blurred during head motion.
This was confirmed when investigators conducted lesion
studies removing the visual corte x (occipital lobes) in
monkeys, and VOR gain adaptation was lost.4 50 msec
Adaptation within the VOR appears to be most robust
Figure 2.1 Classification of the peripheral vestibular
for sinusoid head rotations at frequencies less than 4 Hz afferents is based on the discharge regularity of the affer-
whether the VOR gain is increased or decreased. 6-8 Addi- ent. The discharge regularity is determined by the spacing
tionally, VOR gain tends to be greatest at the frequency of of the interspike intervals between action potentials. The
rotation that was used to change it (e.g., if 1 Hz is used as resting discharge rate is 97 spikes per second for regular
afferents and 98 spikes per second for irregular afferents,
the frequency of head rotation, then the gain change will
though their periodicity is different. (Reprinted with permis-
be greatest at 1 Hz and less at head rotations of 2 Hz or sion from Goldberg JM, Fernandez C. Physiology of periph-
0.5 Hz). Data also suggest that increasing the VOR gain eral neurons innervating semicircular canals of the squirrel
is more prone to frequenc y specificity than is reducing monkey, I: resting discharge and response to constant
VOR gain. The difference in VOR gain for up versus down angular accelerations. J Neurophysiol 1971;34:635-660.9)
adaptation paradigms may be related to dif ferences in af-
ferent physiology. In primates, primary vestibular afferents The VOR has been tested across multiple frequencies
of the healthy vestibular system have a resting firing rate and velocities and shows velocity-dependent nonlineari-
that is typically 70 to 100 spik es per second. 9,10 The dis- ties that may correlate with unique afferent physiology.11
charge regularity of the afferent is determined by the spac- The gain of the VOR remains constant (linear) across mul-
ing of the interspik e intervals between action potentials tiple frequencies of sinusoidal rotation and peak velocities
(Fig. 2.1). This enables classification of afferents into ir- of ±20 deg/sec.11 For rotations at higher frequencies and
regularly and regularly discharging groups. The informa- velocities, the VOR gain rises with increases in stimulus
tion carried by irre gular and regular afferents varies over velocity (nonlinear) and steps of acceleration. Therefore,
the spectral range of frequency and acceleration of natural it may be that the output of theVOR is the combined result
head movements. Irregular afferents tend to be more sen- of linear and nonlinear components.
sitive to rotations during lar ge head accelerations. 10 The Clendaniel et al demonstrated differences in mag-
increased sensitivity of the irregular afferents may be more nitude of VOR gain adaptation dependent on the accelera-
critical for the rapid detection of head movements as well tion or velocity portion of a step rotation.8 A step rotation is
as initiation of the VOR.10,11 Regular afferents, in contrast, named based on its graphed prof ile and refers to a sudden
provide a signal that is proportional to head v elocity over acceleration that then settles at a constant v elocity (see
a wide spectral range. 10 In addition, the re gular afferents Chapter 11 on vestibular function for description). VOR gain
may be the primary source of input to the VOR for low- changes during the acceleration component (~86%) were
frequency and small head accelerations (as measured from nearly double the magnitude of VOR gain changes during
steady-state responses to sinusoidal rotations) because the velocity component (~46%). Based on these properties,
temporarily silencing the irregular afferents had no effect the authors proposed that both a linear pathw ay (tonic)
on the VOR.12 and nonlinear pathway (phasic) mediate the VOR. The
3970_Ch02_020-028 25/06/14 11:25 AM Page 22
nonlinear pathway (irregular afferents) appears more pliable monkeys were exposed to a sum of sines rotation for 3 hours
than the linear pathway of the VOR. In a later study, the same in both heads up (common e xperience) and either left or
authors were able to preferentially adapt the linear and non- right ear-down position (unique experience). Retention only
linear pathways of the VOR using unique frequency and ve- occurred in the ear-down condition. Others have shown sim-
locity profiles, supporting their hypothesis that dif ferential ilar results for short-term adaptation. 20 Head position rela-
adaptive control exists within the VOR.13 tive to gravity is the context in these paradigms. Vertical eye
position,21 vergence angle,22 and head position19,20,23 are all
examples of contexts for which the v estibular system can
Consolidation of VOR Learning be uniquely adapted. For example, the VOR gain can be
Our understanding of consolidation of new motor learning driven up when looking up and down when looking down.
in the VOR is limited. Consolidation refers to a specif ic Context specificity has given insight into plasticity of the
duration of exposure that then enables long-term memory VOR, establishing that the brain can be trained to generate
(retention). A recent study of VOR gain retention showed VOR gains uniquely related to the conte xt it was exposed
that head movements were required for the return to normal to during that training. A second principle important in VOR
of a VOR gain that had been adaptively decreased.14 In this adaptation involves the duration of e xposure time to an
study, investigators adaptively increased (high gain) or de- adapting stimulus. As expected, a longer time e xposure
creased (low gain) the VOR in rhesus monkeys for several leads to a greater magnitude of VOR gain change and usu-
days (long-term experiment). The animals were then placed ally requires more time to recover.24
in the dark (no visual stimulation) and either head re-
strained or allowed to make head movements. Regardless
Role of the Peripheral End Organ
of head motion, animals that had theirVOR gain adaptively
in VOR Adaptation
increased showed little reduction in the magnitude of the
gain. However, monkeys that had the VOR gain decreased Although the cerebellum and brainstem will remain atop
required head movements for the VOR gain to return to the list of regions critical for VOR adaptation, evidence
baseline. This suggests that head mo vements are required suggests that the peripheral end-organ anatomy also has a
for the VOR gain to increase when it is lo w (i.e., patients role. Scarpa’s ganglion has been sho wn to have a change
with vestibular hypofunction) but not required for the VOR in neuronal proteins after unilateral labyrinthectomy (UL)
gain to decrease when it is high.An interesting finding, un- in rat, presumed to provide neuroprotection against oxida-
researched in humans, is the idea that consolidation ofVOR tive damage and thermal signaling for modulation within
motor learning can be enhanced with a break during the the vestibular nerve.25 The proportion of regular and irreg-
training. In studies in which monkeys are exposed to VOR ular vestibular afferents also appears af fected after UL.
adaptation for a period of time (i.e., 1 hour) and then are After UL in monkey, an increase in irregular afferents and
not allowed to move or see light for a period of time, the a decrease in regular afferents occur on the contralesional
learning (adaptation) is more robust and not as susceptible side.26 This may represent an attempt of the brain to im-
to disruption. The prevention of disruption in learning ap- prove the afferent sensitivity for higher acceleration and
pears more robust when the gain is adapted do wn.15 This brief head rotations, belie ved to be mediated primarily
“consolidation rest” benefit appears independent of the fre- from the irregular afferents.27 Finally, as mentioned previ-
quency of training, meaning once the adaptation and rest ously, there appears to be a unique contrib ution from the
period have occurred, the retained learning persisted across peripheral afferents to carry dif ferent velocity and fre-
all tested frequencies—not just the ones that were adapted.16 quency content of information concerning the VOR adap-
This may also e xplain earlier prior long-term adaptation tation. However, we are not certain if this is related to
studies that showed that retention of the adapted VOR gain primary afferent function (peripheral) or to something hap-
is possible when animals are kept in the dark or not allowed pening after synapse occurs in the vestibular nuclei. These
to move their head17,18—conditions that may have enabled cellular changes may represent an attempt to stabilize the
consolidation of learning. ganglionic input to the vestibular nuclei, which in turn may
At least tw o non-error signal principles also af fect initiate the adaptation process.
VOR adaptation: context specificity and duration of expo-
sure. Context specificity implies a unique condition that
Brainstem versus Cerebellar Site
would not normally be expected to affect the performance
of Adaptation
of a motor task. We have demonstrated that VOR adaptation
in squirrel monkeys can be retained for times (days) much The error signals that dri ve VOR adaptation are sent
longer than the adaptive exposure (hours), provided that the to brainstem nuclei (primarily the v estibular Nu) and
context of adaptation is unique to the animal. 19 Squirrel the cerebellum (specifically the floccular and parafloccular
3970_Ch02_020-028 25/06/14 11:25 AM Page 23
lobes).28-31 Unit recordings from both brainstem and cere- placed on the VOR. These changes persist even after the
bellar regions demonstrate that response modulation is horizontal VOR had been e xtinguished by lesioning of
dependent on the magnitude of VOR gain adaptation. In the vestibular nuclei.31 Ablation of the flocculus prevents
the brainstem, neurons that synapse with the flocculus VOR gain adaptation in rabbit 32 and monkey.14 More
(floccular target neurons [FTNs]) show an increased firing specifically, lidocaine injections into the flocculus of
rate when the gain of the horizontal VOR is adapted up macaque monkeys led to an immediate loss only of the
(≥1.6) compared to when the gain of the horizontal VOR adapted VOR, whereas pre-adapted VOR gains were not
is adapted down (≤0.4). Similar evidence exists in the ver- affected (Fig. 2.3).33 These results support the hypothesis
tical VOR.30 The firing rate of these individual neurons can that the flocculus is critical for both adaptive modification
even be reversed (Fig. 2.2). These data suggest that motor and maintenance of VOR adaptation. In contrast, VOR
learning in the VOR is at least partially due to f iring rate gain is unaffected by nodulouvulectomy.
changes of individual FTNs within the vestibular nuclei. Cerebellar-deficient mice show less recovery of VOR
Purkinje cells in the flocculus of the cerebellum gain after UL than do normal mice (wild type). In wild
have been shown to consistently change their f iring rate type, ipsilesional VOR gain recovery is approximately
responsiveness in parallel with the adaptive gain demand 80% by postoperative day 10 and 100% for contralesional
200 200
0 0
60 60
· ·
E 0 E 0
–60 –60
60 · 60
· D 0
D 0
–60 –60
60 · 60
· H 0
A H 0 B
–60 –60
Reversed VOR
VOR Suppression 200
200 iFR 100
iFR 100 0
0 60
·
60 E 0
·
E 0 –60
–60 60
·
D 0
· 60 –60
D 0
–60 60
·
H 0
· 60 –60
C H 0 D
–60 1 sec
Figure 2.2 Behavior and firing rate of a VOR neuron during vertical head rotation under
four unique conditions: (A) Normal VOR with no moving visual target. Note that the vertical
head (Ḣ) and vertical eye (Ė) velocity rotation is opposite each other. (B) Enhanced VOR—
visual target (Ḋ) moving opposite direction of head (as in the X2 VOR exercise). Note the in-
creased eye velocity (Ė) and increased instantaneous firing rate (iFR). (C) VOR suppression with
the visual target moving with the head. Note the reduced iFR and eye velocity. (D) Reversed
VOR with the drum moving at a velocity twice that of head velocity. Note that the direction
of the iFR has reversed! iFR = instantaneous firing rate; Ė = vertical eye velocity in d/s; Ḣ =
head velocity in d/s; Ḋ = the optokinetic drum velocity in d/s. Stimulation parameters are 0.5 Hz,
35 d/s. (Reprinted with permission from Partsalis et al J Neurophysiol. 1995;73:615-631.30)
3970_Ch02_020-028 25/06/14 11:25 AM Page 24
1.1
Injection Lidocaine Critical Evidence of VOR
Ringer’s solution
Adaptation in Human
1.0
Short-term VOR Adaptation in Normal
0.9 Function
HVOR Gain
prior to measuring the VOR with horizontal head rotations Incremental velocity error (IVE) refers to a progressi vely
always led to an increase in the gain of the VOR, even changing visual error signal used to increaseVOR gain. We
though the “priming” e ye movements occurred without investigated how using an IVE coupled with rapid acti ve
head motion.46 These priming eye rotations were applied head impulses might change VOR gain.41 We compared
in both directions. In contrast, neither vertical pursuit nor IVE against a large VOR gain demand ( ×2 viewing). For
vertical saccades had a similar ef fect on the horizontal IVE adaptation, a ×1.1 stimulus was used to boost the VOR
VOR gain. by 10%. After a brief rest, a ×1.2 stimulus demanded greater
adaptation by 10% (20% total), and this was repeated until
the ×2 stimulus was reached. The total adaptation time was
VOR Gain Retention 15 minutes. Both passive and active VOR gain was mea-
Few studies have investigated retention of VOR gain in sured in all subjects before and after training. For both sub-
humans. Recently, new information has elucidated the re- ject groups, traditional all-at-once adaptation resulted in no
tention of an adapted VOR gain using short-term experi- VOR gain increase. IVE adaptation resulted in signif icant
ments and has e xciting implications for v estibular increases in both normal (17.3% active; 14.2% passive) and
rehabilitation. In healthy humans, Yakushin et al docu- UVH subjects (18.2% active). In all the normal and several
mented that only one 1-hour session of VOR adaptation of the UVH subjects, the active IVE training also increased
in a unique position (ear -down, horizontal rotation for the passive VOR gain (Fig. 2.4).
pitch stimulus) was needed to cause a VOR gain change Evidence for VOR adaptation exercises:
to be retained for 2 days (tested in the adapting position).40 • Two sensory stimuli are required for significant
This study suggests that the VOR adaptation can persist adaptation of the VOR: vision and head motion.
when the exposure of the training stimulus is unique. • The VOR retains its adaptive capabilities in the
presence of unilateral hypofunction.
• Retinal slip is thought to be the most effective
VOR Adaptation in Unilateral Vestibular means for changing VOR gain.
Hypofunction • Small errors in retinal slip enable larger VOR gain
The VOR retains its adaptive capabilities in the presence of adaptation than larger errors.
unilateral hypofunction and can be enhanced using visual • The error signals that drive VOR adaptation are sent
and vestibular stimuli that create retinal image slip. 47-49 to brainstem nuclei (primarily the vestibular Nu)
However, improvements in VOR gain after v estibular re- and the cerebellum (specifically the floccular and
habilitation (vestibular physical therapy [VPT])—though parafloccular lobes).
function improves—have been difficult to verify.50,51
Three human studies ha ve demonstrated that the
VOR retains its adaptive capacity in the presence of uni-
Summary
lateral vestibular hypofunction (UVH). 3,41,48 Two of When individuals with vestibular hypofunction (unilat-
these studies measured VOR gain change using passive eral or bilateral) are able to predict timing, direction,
whole body rotation and reported a mean 15% in- and amplitude of an imposed head mo vement, gaze
creased.3,41 Viirre reported that the greatest amount of stability improves relative to an unpredictable head
adaptation occurred at the tw o highest frequencies at movement.55-60 Additionally, the gain of the VOR is
which the authors tested the VOR (0.32 Hz and 0.64 Hz, greater during ipsilesional predictable head motions
50 deg/sec).48 compared with ipsilesional unpredictable head motion
Studies of motor control re veal that retention of in UVH.57,58,60,61 Functionally, visual acuity during
newly learned motor beha vior is most rob ust when the self-generated head rotation is better than it is during
training (adaptation) is presented in an incremental man- unpredictable head rotations.62,63 Although it is believed
ner.52,53 Referred to as “credit assignment,” the brain has that the enhancement of gaze stability and visual acuity
the difficult task of determining where blame resides when during predictable head mo vement is due to central
motor performance is impaired. Smaller error signals may preprogramming or efference copy of the motor com-
“deceive” the brain into believing that the perceived error mand, we do not know whether the augmenting effects
signal is intrinsic and w arrants efforts toward plasticity. of prediction can be deliberately increased. Although
Larger error signals may be interpreted by the brain as we know that VOR gain impro vement is possible in
extrinsic and transient and thus disre garded as invalid.54 hypofunction, less is kno wn about whether such VOR
Thus, the brain attempts a more enduring modif ication gain adaptation can be retained. Long-term VOR adap-
for smaller error signals and ignores lar ge error signals. tation studies have not been conducted in humans with
3970_Ch02_020-028 25/06/14 11:25 AM Page 26
125
Figure 2.4 VOR adaptation
in a subject with unilateral 75
vestibular hypofunction using
an incremental velocity error sig- 25
nal (IVE). Active VOR training for
Velocity (deg/sec)
0
head rotations to both sides was ⫺25
done by gradually increasing the
retinal slip error signal over a POST
225
15-minute period. Passive head 1.38 ⫹ 0.07 0.88 ⫹ 0.04
impulse testing revealed that
175
VOR gain increased for contrale-
sional and ipsilesional head 125
rotations. Black traces represent
head velocity, and grey traces 75
(inverted for ease of comparison)
represent eye velocity. VOR gains 25
are listed in the corner of each 0
plot. Note that the Post ipsile- ⫺25
sional VOR gain is restored,
whereas the Post contralesional 0 50 100 150 200 250 300 0 50 100 150 200 250 300
gain is greater than 1.0. Time (msec)
vestibular hypofunction. Much room e xists for impor- 5. Zennou-Azogui Y, Xerri C, Harlay F. Visual sensory
tant research to be answered: Can we create a behavioral substitution in vestibular compensation: neuronal
substrates in the alert cat. Exp Brain Res. 1994;98(3):
paradigm to improve the VOR gain and k eep that im-
457-473.
provement over time? Can VOR adaptation be unilater- 6. Raymond JL, Lisberger SG. Neural learning rules for
ally applied in the case of UVH? Is there a difference in the vestibulo-ocular reflex. J Neurosci. Nov 1 1998;
VOR gain adaptation in unilateral v ersus bilateral 18(21):9112-9129.
vestibular hypofunction? Because of both e xisting 7. Broussard DM, Bhatia JK, Hong JA. The dynamics of
the vestibulo-ocular reflex after peripheral vestibular
knowledge of the neuronal synapses mediating theVOR
damage, II: Comparison with dynamics after optically
and the latter’s tremendous plasticity, it is expected that induced learning. Exp Brain Res. Apr 1999;125(3):
motor control research in general will continue to rely 365-374.
on the VOR as a model of study for insight. 8. Clendaniel RA, Lasker DM, Minor LB. Horizontal
vestibuloocular reflex evoked by high-acceleration
References rotations in the squirrel monkey, IV: Responses after
spectacle-induced adaptation. J Neurophysiol. Oct
1. Ito M. Cerebellar control of the vestibulo-ocular reflex— 2001;86(4):1594-1611.
around the flocculus hypothesis. Annu Rev Neurosci. 9. Goldberg JM, Fernandez C. Physiology of peripheral
1982;5:275-296. neurons innervating semicircular canals of the squirrel
2. Eggers SD, De Pennington N, Walker MF, Shelhamer M, monkey, I: Resting discharge and response to constant
Zee DS. Short-term adaptation of the VOR: non-retinal-slip angular accelerations. J Neurophysiol. 1971;34:635-660.
error signals and saccade substitution. Ann N Y Acad Sci. 10. Lysakowski A, Minor LB, Fernandez C, Goldberg JM.
Oct 2003;1004:94-110. Physiological identification of morphologically distinct
3. Paige GD. Vestibuloocular reflex and its interactions with afferent classes innervating the cristae ampullares of the
visual following mechanisms in the squirrel monkey, II: squirrel monkey. J Neurophysiol. 1995;73:1270-1281.
Response characteristics and plasticity following unilateral 11. Minor LB, Lasker DM, Backous DD, Hullar TE. Horizon-
inactivation of horizontal canal. J Neurophysiol. Jan 1983; tal vestibuloocular reflex evoked by high-acceleration
49(1):152-168. rotations in the squirrel monkey, I: Normal responses.
4. Fetter M, Zee DS, Proctor LR. Effect of lack of vision and J Neurophysiol. 1999;82:1254-1270.
of occipital lobectomy upon recovery from unilateral 12. Minor LB, Goldberg JM. Vestibular-nerve inputs to the
labyrinthectomy in rhesus monkey. J Neurophysiol. Feb vestibuloocular reflex: a functional-ablation study in the
1988;59(2):394-407. squirrel monkey. J Neurosci. 1991;11:1636-1648.
3970_Ch02_020-028 25/06/14 11:25 AM Page 27
13. Clendaniel RA, Lasker DM, Minor LB. Differential 30. Partsalis A, Zhang Y, Highstein SM. Dorsal Y group in the
adaptation of the linear and nonlinear components of the squirrel monkey, I: Neuronal responses during rapid and
horizontal vestibuloocular reflex in squirrel monkeys. long-term modifications of the vertical VOR. J Neurophysiol.
J Neurophysiol. Dec 2002;88(6):3534-3540. 1995;73:615-631.
14. Cohen H, Cohen B, Raphan T, Waespe W. Habituation and 31. Blazquez P, Partsalis A, Gerrits NM, Highstein SM. Input of
adaptation of the vestibuloocular reflex: a model of differ- anterior and posterior semicircular canal interneurons en-
ential control by the vestibulocerebellum. Exp Brain Res. coding head-velocity to the dorsal Y group of the vestibular
1992;90(3):526-538. nuclei. J Neurophysiol. May 2000;83(5):2891-2904.
15. Titley HK, Heskin-Sweezie R, Chung JY, Kassardjian CD, 32. Nagao S. Effects of vestibulocerebellar lesions upon dy-
Razik F, Broussard DM. Rapid consolidation of motor namic characteristics and adaptation of vestibulo-ocular
memory in the vestibuloocular reflex. J Neurophysiol. and optokinetic responses in pigmented rabbits. Exp Brain
Dec 2007;98(6):3809-3812. Res. 1983;53(1):36-46.
16. Titley HK, Heskin-Sweezie R, Broussard DM. Consolida- 33. Nagao S, Kitazawa H. Effects of reversible shutdown of
tion and disruption of motor memory generalize across the monkey flocculus on the retention of adaptation of
stimulus conditions in the vestibulo-ocular reflex. Brain the horizontal vestibulo-ocular reflex. Neuroscience. 2003;
Res. Apr 24 2009;1267:37-43 118(2):563-570.
17. Lisberger SG, Miles FA, Optican LM, Eighmy BB. 34. Beraneck M, McKee JL, Aleisa M, Cullen KE. Asymmetric
Optokinetic response in monkey: underlying mecha- recovery in cerebellar-deficient mice following unilateral
nisms and their sensitivity to long-term adaptive labyrinthectomy. J Neurophysiol. Aug 2008;100(2):945-958.
changes in vestibuloocular reflex. J Neurophysiol. 35. Dutheil S, Lacour M, Tighilet B. Neurogenic potential of
May 1981;45(5):869-890. the vestibular nuclei and behavioural recovery time course
18. Hirata Y, Lockard JM, Highstein SM. Capacity of vertical in the adult cat are governed by the nature of the vestibular
VOR adaptation in squirrel monkey. J Neurophysiol. Dec damage. PLoS One. 2011;6(8):e22262.
2002;88(6):3194-3207. 36. Dutheil S, Brezun JM, Leonard J, Lacour M, Tighilet B.
19. Schubert MC, Migliaccio AA, Minor LB, Clendaniel RA. Neurogenesis and astrogenesis contribution to recovery of
Retention of VOR gain following short-term VOR adapta- vestibular functions in the adult cat following unilateral
tion. Exp Brain Res. May 2008;187(1):117-127. vestibular neurectomy: cellular and behavioral evidence.
20. Yakushin SB, Raphan T, Cohen B. Context-specific adap- Neuroscience. Dec 29 2009;164(4):1444-1456.
tation of the vertical vestibuloocular reflex with regard to 37. Zheng Y, Masumura C, Chung P, Darlington CL, Smith PF.
gravity. J Neurophysiol. 2000;84:3067-3071. Cell proliferation and survival in the vestibular nucleus fol-
21. Shelhamer M, Tiliket C, Roberts D, Kramer PD, Zee DS. lowing bilateral vestibular deafferentation in the adult rat.
Short-term vestibulo-ocular reflex adaptation in humans, NeurosciLett. Jan 2010;468(1):85-88. Epub 2009 Oct 28.
II: Error signals. Exp Brain Res. 1994;100(2):328-336. 38. Tiliket C, Shelhamer M, Tan HS, Zee DS. Adaptation of
22. Lewis RF, Clendaniel RA, Zee DS. Vergence-dependent the vestibulo-ocular reflex with the head in different orien-
adaptation of the vestibulo-ocular reflex. Exp Brain Res. tations and positions relative to the axis of body rotation.
2003;152:335-340. J Vestib Res. 1993;3(2):181-195.
23. Tan HS, Shelhamer M, Zee DS. Effect of head orientation 39. Tiliket C, Shelhamer M, Roberts D, Zee DS. Short-term
and position on vestibuloocular reflex adaptation. Ann N Y vestibulo-ocular reflex adaptation in humans, I: Effect on
Acad Sci. May 1992;656:158-165. the ocular motor velocity-to-position neural integrator.
24. Kuki Y, Hirata Y, Blazquez PM, Heiney SA, Highstein Exp Brain Res. 1994;100(2):316-327.
SM. Memory retention of vestibuloocular reflex motor 40. Yakushin SB, Palla A, Haslwanter T, Bockisch CJ,
learning in squirrel monkeys. Neuroreport. Apr 29 Straumann D. Dependence of adaptation of the human
2004;15(6):1007-1011. vertical angular vestibulo-ocular reflex on gravity.
25. Kitahara T, Horii A, Kizawa K, Maekawa C, Kubo T. Exp Brain Res. Sep 2003;152(1):137-142.
Changes in mitochondrial uncoupling protein expression 41. Schubert MC, Della Santina CC, Shelhamer M. Incremen-
in the rat vestibular nerve after labyrinthectomy. Neurosci tal angular vestibulo-ocular reflex adaptation to active
Res. Nov 2007;59(3):237-242. Epub 2007 Jul 10. head rotation. Exp Brain Res. Dec 2008;191(4):435-446.
26. Sadeghi SG, Minor LB, Cullen KE. Response of vestibular- 42. Istl-Lenz Y, Hyden D, Schwarz DW. Response of the human
nerve afferents to active and passive rotations under nor- vestibulo-ocular reflex following long-term 2x magnified
mal conditions and after unilateral labyrinthectomy. visual input. Exp Brain Res. 1985;57(3):448-455.
J Neurophysiol. Feb 2007;97(2):1503-1514. 43. Melvill Jones G, Guitton D, Berthoz A. Changing patterns
27. Lasker DM, Hullar TE, Minor LB. Horizontal vestibulooc- of eye-head coordination during 6 h of optically reversed
ular reflex evoked by high-acceleration rotations in the vision. Exp Brain Res. 1988;69(3):531-544.
squirrel monkey, III: Responses after labyrinthectomy. 44. Jones GM, Mandl G. Effects of strobe light on adaptation
J Neurophysiol. May 2000;83(5):2482-2496. of vestibulo-ocular reflex (VOR) to vision reversal. Brain
28. Watanabe, E. Neuronal events correlated with long-term Res. Mar 23 1979;164:300-303.
adaptation of the horizontal vestibulo-ocular reflex in the 45. Scherer M, Schubert MC. High-velocity angular vestibulo-
primate flocculus. Brain Res. 1984;297:169-174. ocular reflex adaptation to position error signals. J Neurol
29. Lisberger SG, Pavelko TA, Broussard DM. Neuronal Phys Ther. Jun 2010;34(2):82-86.
basis for motor learning in the vestibuloocular reflex of 46. Das VE, Dell’Osso LF, Leigh RJ. Enhancement of the
primates, I: Changes in the responses of brain stem neurons. vestibulo-ocular reflex by prior eye movements.
J Neurophysiol. 1994b;72:928-953. J Neurophysiol. Jun 1999;81(6):2884-2892.
3970_Ch02_020-028 25/06/14 11:25 AM Page 28
47. Paige GD. Senescence of human visual-vestibular interac- 56. Tomlinson RD, Saunders GE, Schwarz DWF. Analysis
tions: smooth pursuit, optokinetic, and vestibular control of human vestibulo-ocular reflex during active head move-
of eye movements with aging. Exp Brain Res. 1994;98(2): ments. ActaOtolarygol. 1980;90:184-190.
355-372. 57. Collewijn H, Martins AJ, Steinman RM. Compensatory
48. Viirre E, Draper M, Gailey C, Miller D, Furness T. Adap- eye movements during active and passive head move-
tation of the VOR in patients with low VOR gains. J Vestib ments: Fast adaptations to changes in visual magnifica-
Res. Jul-Aug 1998;8(4):331-334. tion. J Physiol. 1983;340:259-286.
49. Szturm T, Ireland DJ, Lessing-Turner M. Comparison of 58. Jell RM, Stockwell CW, Turnipseed GT, et al. The influ-
different exercise programs in the rehabilitation of patients ence of active versus passive head oscillation and mental
with chronic peripheral vestibular dysfunction. J Vestib set on the human vestibulo-ocular reflex. Aviat Space
Res. Nov-Dec 1994;4(6): 461-479. Environ Med. 1988;59:1061-1065.
50. Herdman SJ, Schubert MC, Das VE, Tusa RJ. Recovery 59. Demer JL. Mechanisms of human vertical visual-vestibular
of dynamic visual acuity in unilateral vestibular hypofunc- interaction. J Neurophys. 1992;68:128-146.
tion. Arch Otolaryngol Head Neck Surg. Aug 2003;129(8): 60. Schubert MC, Hall CD, Das V, Tusa RJ, Herdman SJ.
819-824. Oculomotor strategies and their effect on reducing gaze
51. Herdman SJ, Hall CD, Schubert MC, Das VE, Tusa RJ. position error. OtolNeurotol. Feb 2010;31(2):228-231.
Recovery of dynamic visual acuity in bilateral vestibular 61. Hoshowsky B, Tomlinson D, Nedzelski J. The horizontal
hypofunction. Arch Otolaryngol Head Neck Surg. Apr vestibulo-ocular reflex gain during active and passive high
2007;133(4):383-389. frequency head movements. Laryngoscope. 1994;104:
52. Kagerer FA, Contreras-Vidal JL, Stelmach GE. Adaptation 140-145.
to gradual as compared with sudden visuo-motor distor- 62. Herdman SJ, Schubert MC, Tusa RJ. The role of central
tions. Exp Brain Res. Jul 1997;115(3):557-561. preprogramming in dynamic visual acuity with vestibu-
53. Kilgard MP, Merzenich MM. Order-sensitive plasticity in lar loss. Arch Otolaryngol Head Neck Surg. 2001;127:
adult primary auditory cortex. ProcNatlAcadSci USA. 1205-1210.
Mar 5 2002;99(5):3205-3209. 63. Tian JR, Shubayev I, Demer JL. Dynamic visual acuity
54. Kording KP, Tenenbaum JB, Shadmehr R. The dynamics during unpredictable and self-generated transient head ro-
of memory as a consequence of optimal adaptation to a tation in normal and unilaterally vestibulopathic humans.
changing body. Nat Neurosci. Jun 2007;10(6):779-786. Exp Brain Res. 2002;142(4):486-495.
55. Kasai T, Zee DS. Eye-head coordination in labyrinthine-
defective human beings. Brain Res. 1978;144:123-141.
3970_Ch03_029-048 25/06/14 11:26 AM Page 29
CHAPTER 3
One of the most important tasks of the human postural con- Perceiving Position
trol system is that of balancing the body over the small base
of support provided by the feet. As a sensor of gravity and
and Self-Motion
head acceleration, the vestibular system is one of the nervous The vestibular system pro vides information about the
system’s most important tools in controlling posture. The movement of the head and its position with respect to
vestibular system is both a sensory and a motor system. gravity and other inertial forces (like those generated by
As a sensory system, the v estibular information is closely moving vehicles). Therefore, this system contrib utes
integrated with somatosensory and visual information so that important information to the sensation and perception of
the central nervous system (CNS) can estimate the position the motion and position of the body. Graviceptive infor-
and movement of the entire body as well as the surrounding mation from the v estibular system is combined with
environment. In addition to providing sensory information, information from the somatosensory system to percei ve
the vestibular system also contributes directly to motor con- gravitoinertial forces and use them to orient the body. For
trol. Descending motor pathways such as the vestibulospinal example, the skier in Figure 3.1 maintains equilibrium by
tracts receive vestibular and other types of information to integrating gravitational and centripetal forces from the
control eye, head, and trunk orientation and to coordinate vestibular and somatosensory systems together with ori-
postural movements. entation information from vision. The vestibular system
Because the vestibular system is both a sensory and provides information about the position and motion of the
a motor system, it plays man y different roles in postural head. Because the lar gest head motions during quiet
control. In this chapter, we explore the four most important stance sway and while walking or running usually occur
roles (Fig. 3.1). First, we discuss the role of the vestibular in the sagittal (forward-backward) and frontal (left-right)
system in the perception of body position and self-motion. planes, the vertical canals and otoliths are more critical
Second, we discuss its role in orienting the trunk to verti- for postural control than are the horizontal semicircular
cal using sensory orientation and weighting-appropriate canals. However, the powerful influence of the horizontal
sensory cues under different sensory environments. Third, canals on gaze stability during horizontal head motions
we discuss the role of the vestibular system in controlling (as in shaking the head “no”) also contrib utes to control
the position of the body’s center of mass (COM), both for of posture because a stable visual reference is important
static positions and dynamic mo vements via postural for spatial orientation and balance.
responses. Fourth, we discuss its role in stabilizing the In contrast to the canals, which sense rotational mo-
head during postural movements. tion, the otoliths sense linear accelerations. Vertical linear
29
3970_Ch03_029-048 25/06/14 11:26 AM Page 30
1. Position &
perceiving
self-motion
3. Postural
responses
2. Sensory orientation
Figure 3.1 Four important roles of the vestibular system in postural control. As the skier
leans into a curve, he (1) perceives his body orientation with respect to both gravity and the
mountain, (2) orients his upper body to gravity (sensory orientation), (3) controls his COM
(postural reactions), and (4) stabilizes his head in space.
accelerations of the head, lik e the head translations gen - vestibular inputs can pro vide ambiguous information
erated during heel strike in gait, are sensed by the saccular about body motion. First, the v estibular system only
otoliths. Horizontal linear accelerations, lik e the transla- provides information about head movements and not the
tions of the head generated during walking, are sensed by position or movement of the head on the trunk or any of
the utricular otoliths. The otolith or gans also pro vide the other body se gments. Thus, the v estibular system
information about the direction of gravity. Gravity, which alone cannot distinguish between head tilt on a stationary
is also a linear acceleration, produces an otolith signal that trunk versus whole body tilt over the feet, both of which
changes systematically as the head is tilted.The CNS uses activate the semicircular canals and otolith receptor
this signal to determine head and trunk alignment with organs similarly. Second, the otolith receptor organs can-
respect to gravitational vertical. not distinguish between the acceleration because of grav-
The importance of vestibular otolith function in per- ity and linear acceleration of the head in space. F or
ception of orientation in space can be seen by studies of example, tilting the head to the left can produce the same
perceived vertical and straight ahead in patients with vestibular stimulation as a linear acceleration to the right.
bilateral and unilateral v estibular loss.1 Whereas healthy Resolution of the ambiguity between tilt and linear
subjects can accurately indicate the direction of gra vity motion is important because the postural response nec-
and straight ahead to within 1 degree, patients with bilat- essary to maintain equilibrium and orientation may be
eral vestibular loss make large errors and patients with uni- opposite for these two postural perturbations. Additional
lateral vestibular loss often perceive up and straight ahead information from somatosensory and visual systems is
as tilted to the side of the lesion. 2-4 These asymmetrical required to resolve these ambiguities.
perceptions of spatial orientation in patients with unilateral Each sensory system contributes a different, important
vestibular loss are reflected in the asymmetrical alignment kind of information about body position and motion to the
of their eyes, head, and trunk before compensation for loss CNS, and each sensory system is most sensitive to partic-
of vestibular function on one side.5 ular types of motion. 6-12 The visual system signals the
Vestibular information must be closely inte grated position and mo vement of the head with respect to
with somatosensory and visual inputs to percei ve posi- surrounding objects. The visual system can pro vide the
tion and motion of the body and en vironment because CNS with the information necessary to determine whether
3970_Ch03_029-048 25/06/14 11:26 AM Page 31
Given the vestibular system’s important role in the lesioned side.29-31 The amount of asymmetrical posturing
sensation of self-motion, it is not surprising that patients gradually diminishes over time, and the return to normal
with vestibular disorders often have abnormal perceptions postural alignment is considered a sign of vestibular com-
of self-motion. Patients may report that the y feel them- pensation.32,33 In humans, the vestibular system also plays
selves spinning, dropping, or rocking or that the room an important role in the alignment of the head and body
appears to spin around them. These sensations may be with respect to gravity, although the effect of unilateral
associated with leaning head and trunk postures as the y vestibular lesions on postural alignment is more v ariable
attempt to compensate for perceived body tilt or motion. and short-lived than in lower species.30,31,34 Humans with
Patients with profound loss of v estibular function also sudden loss of v estibular function on one side can also
have difficulty perceiving how they are aligned or moving show lateral flexion of the head to the side of the loss
in environments lacking good visual and somatosensory during the acute phase of the lesion.32-34 However, within
orientation cues, such as walking at night on a sandy beach weeks following total unilateral vestibular loss in humans,
or swimming in murky water. postural alignment and control can be indistinguishable
In summary, the vestibular system, along with other from that of a normal person.35 Bilateral loss of vestibular
sensory systems, provides the CNS with the information function may be associated with a forw ard head posi-
about body motion and position with respect to v ertical, tion.36-38 Altered postural alignment, sometimes associated
which is critical for sensing and perceiving self-motion. No with excessive muscle tension and pain, especially in the
sensory system alone provides all the necessary informa- neck, is a f amiliar problem for patients with v estibular
tion for sensing position and motion of the whole body; dysfunction.39
sensory information from multiple systems must be inte- In addition to head tilts, the entire body seems to shift,
grated and interpreted before being used to ef fect body temporarily, to the side of vestibular loss. Patients with uni-
orientation and equilibrium. In the next section, we explore lateral vestibular lesions shift their weight to the side of
how sensory information is used by the CNS to align the their lesions and then re gain normal weight distribution
body to vertical, and how the CNS selects sensory infor- over the course of several weeks.40,41 Fukuda developed a
mation for body orientation in different environments. stepping-in-place test to document the asymmetry and
gradual compensation that follo w unilateral v estibular
Sensory Orientation; Orienting loss.42 In this test, subjects attempt to step in place with
eyes closed, and patients with unilateral losses typically
the Body to Vertical rotate slowly toward the side of the lesion, although the
Keeping the body properly aligned, parallel to gra vity, effect is quite variable among patients.
and over the base of foot support is one of the most Another way to investigate the role of the vestibular
important goals of the postural control system. The system in aligning the body to gra vity is to stimulate the
vestibular system, which can detect the direction of gravity, vestibular system electrically by deli vering low-level
plays a very important role in maintaining the orientation (<2 mA) direct currents through electrodes on the mastoid
of the whole body to vertical. Because the term “orienta- processes, with an anode placed on one mastoid and a
tion” also includes the alignment of body segments other cathode placed on the other.18,19,22,43-49 Cathodal currents
than the head with respect to each other and with respect increase the tonic firing in the vestibular nerve, and anodal
to vertical, other sensory systems contrib ute to body currents decrease the firing rate.50 With the head f acing
orientation as well. In this section, we discuss the role of forward, sway induced by galvanic current is lateral and
the vestibular system in the alignment of the head and toward the anode, because the galvanic current simulates
body to v ertical, and ho w the nerv ous system selects the vestibular nerve signal, which would result if the body
appropriate sensory information for orientation in differ- was tilted toward the side of the cathode. Subjects sw ay
ent sensory environments. toward the anode to correct the apparent tilt induced by
the galvanic stimulation. Although galvanic stimulation
reliably results in tonic head tilts and weight shifts in nor-
Postural Alignment mal humans,18,19,43-49 these responses are typically absent
Spinal x-rays and fluoroscop y have revealed that most or abnormal in patients with v estibular nerve sections.
vertebrates hold the vertical spine parallel to gravitational However, these responses can be normal in patients with
vertical.29 The vestibular system, which signals the direc- loss of peripheral hair cell receptors, which confirms that
tion of gravity, plays an important, but not exclusive, role the galvanic current directly stimulates the v estibular
in the head and trunk alignment in animals. Unilateral nerve.51-53 Postural responses to electrical stimulation can
vestibular lesions result in head and body tilts toward the be enhanced when subjects stand on a sw ay-referenced
3970_Ch03_029-048 25/06/14 11:26 AM Page 33
surface or have peripheral neuropathy that provides poor galvanically induced sway is forward.18 Thus, the same
somatosensory feedback for orientation or when galvanic vestibular stimulation results in a v ery different and
current is delivered during responses to a platform move- appropriate postural response because it is interpreted
ment.46,51,54,55 These findings suggest that the role of the together with somatosensory signals about body orien-
vestibular system in automatic postural alignment is in- tation.18,56 Thus, equilibrium control centers use infor-
creased when somatosensory information for postural con- mation about body position and motion deri ved from
trol is unreliable. 18 When visual spatial references are proprioceptive afferents from many body segments, not
available with eyes open, postural responses to galv anic just the neck, in combination with v estibular informa-
vestibular stimulation are greatly suppressed, suggesting tion to produce an accurate picture of body sway to trig-
that the importance of v estibular inputs for posture are ger appropriate postural responses.57,58
also increased when visual information is una vailable. One hypothetical explanation for the altered postural
Figure 3.3 shows a person with bilateral v estibular loss alignment of patients with v estibular deficits is that the
attempting to stand on a platform that is rotated up vestibular lesion has resulted in an altered internal map of
5 degrees. With her eyes closed, she is unable to maintain body orientation in space. Gurfinkel and colleagues8 have
her balance because she continued to align her trunk with suggested that the CNS constructs a model or internal map
the surface, rather than with gravity. of the direction of gra vity based on v estibular and other
Studies of postural responses to electrical stimula- sensory information, and that the CNS aligns the body
tion of the v estibular system also show that the nerv ous according to this map. This hypothetical explanation could
system takes both vestibular and somatosensory informa- also account for the body realignments that result from
tion into account when or ganizing these responses. The galvanic stimulation. The galvanic current, which simu-
direction of body sw ay and the corresponding muscle lates the pattern of vestibular nerve firing that results when
activations induced by galvanic stimulation are modulated the body is tilted to ward the cathode, may result in a
by the position of the head on the trunk. With the head change of the central nerv ous system’s estimate of the
facing forward, galvanically induced sway is lateral and position of gravity—that is, that it has shifted toward the
toward the anode. anode.54 Subjects sway toward the anode to realign their
In contrast, when the head is turned on the trunk bodies to the new estimate of the position of gravity. The
so that the ear with the anode is turned forw ard, the tonic body and/or head misalignment in patients with
vestibular disorders may also result from a faulty internal
map based on abnormal information from their malfunc-
tioning vestibular systems.
Vestibular loss patients appear to misinterpret the
movement of external objects as self-motion in the oppo-
site direction. As a result, they may throw themselves into
disequilibrium as the y attempt to maintain a constant
orientation with reference to the mo ving visual object.
Thus, vestibular patients may either align themselves with
a faulty vestibular estimate of the direction of gra vity,
or align themselves with an estimate of the direction of
gravity from another sensory system.
Vestibular information also contributes to another im-
portant internal map for postural control, the map of “sta-
bility limits.” Vestibular pathology may lead to defects in
this map as well. A human standing with feet planted on
the ground may sway forward or backward a small amount
(about 4 deg backward and about 8 deg forward) without
losing balance or taking a step. The boundaries of the area
over which an individual may safely sway are called the
Figure 3.3 This figure represents a patient with bilateral stability limits.59,60 The actual stability limits for an y in-
vestibular loss attempting to stand on a tilted surface dividual in any situation are determined by biomechanical
with eyes closed. Arrows indicate upward rotation of the
surface and his postural alignment with surface tilt. Note constraints, such as range of motion, the firmness and size
he aligns his trunk in relation to the tilted surface rather of the base of support, and by neuromuscular constraints,
than to gravity. such as strength and swiftness of muscle responses. 61,62
3970_Ch03_029-048 25/06/14 11:26 AM Page 34
Vestibular pathology might result in a poor match between water) or uneven (like a ramp or rocky ground), the position
a patient’s actual stability limits and the internal map of of the ankle joints and other somatosensory and proprio-
those limits. The internal map could be smaller or lar ger ceptive information from the feet and legs bears little rela-
than the actual stability limits, or the map could be poorly tionship to the orientation of the rest of the body; that is, the
aligned with respect to gra vity. As a result, patients may body’s COM could be aligned well within the stability lim-
align themselves near the edges of their actual stability its despite lar ge amounts of ankle motion. Figure 3.4 A
limits. Because visual and somatosensory information shows a person standing on an unstable surf ace, without
may substitute for vestibular information, alignment may vision, having to rely on vestibular information for orienta-
be normal in patients with well-compensated v estibular tion. Under such circumstances, the CNS do wn-weights
losses, but may be very abnormal in patients with deficits dependence on the unreliable somatosensory inputs and
in multiple sensory systems or in patients who cannot unavailable visual information, and increases dependence
compensate. on the vestibular inputs for spatial orientation.
The relative dependence on, or weighting of, each
sensory system changes predictably with changes in envi-
Weighting Sensory Information ronmental conditions.27 A change in sensory weighting on
Whether and how vestibular or other sensory information somatosensory, vestibular, and visual information for pos-
is used for postural orientation depends in part on the sen- tural orientation w as shown experimentally by Robert
sory information available in the environment. Under nor- Peterka (Fig. 3.4A to C).65 For example, when blindfolded
mal conditions (i.e., a stable support surf ace and a well-lit subjects are exposed to surface tilts of various amplitudes,
visual environment), postural orientation information from they align themselves to the surface for very small ampli-
all three sensory modalities is a vailable and is congruent; tudes of rotation but orient their posture more with respect
that is, all three modalities yield similar estimates of body to gravity with larger amplitudes of rotation, because they
position and motion. Although a person could theoretically rely more on v estibular information. In contrast, people
rely equally on vestibular, vision, and somatosensory inputs with bilateral loss of vestibular information standing with
for postural orientation, studies suggest they rely primarily eyes closed align their posture with the rotating surf ace
on somatosensory information from the support surface in until they fall. He calculated that healthy subjects standing
these conditions.1,63,64 There are, however, many environ- on a firm surface with vision available normally rely 70%
mental conditions in which the sensory orientation refer - on somatosensory information from the surf ace, 20% on
ences are not congruent. F or example, when the support vestibular information, and 10% on vision for postural ori-
surface is compliant (lik e mud, sand, or a raft floating on entation. However, as surf ace rotation increases from
loss subject
1.0
1.0
Vestibular
Weighting
Control
0.5
0.5
Somatosensory
0 0
Platform 0 2 4 6 8 0 2 4 6 8
A tilt angle B Platform Tilt (deg) C Platform Tilt (deg)
Figure 3.4 (A) Body sway changing in response to platform tilt angle when standing with
eyes closed. (B) As platform tilt increases up to +/–2 degrees, all subjects increase body sway
as they orient their body to the surface. Larger than +/–2 degrees surface tilt, control subjects
stabilize body sway by orienting their bodies to gravity, whereas vestibular loss subjects
continue to orient their bodies to the surface and fall. (C) Normal sensory reweighting as
platform tilt angle increases. Healthy adults gradually increase dependence on vestibular
inputs and decrease dependence on somatosensory inputs. (From Peterka, 2002.65)
3970_Ch03_029-048 25/06/14 11:26 AM Page 35
Vestibular Weight
some existing peripheral vestibular function). The fact that 10
patients with well-compensated vestibular losses can use 0.6 87
either visual or somatosensory information to orient the
* 21
9
body limits the sensitivity and specificity of the standard 0.4 4
* 36
Romberg test as a test of vestibular function.37
In contrast to the v estibular loss pattern, patients 0.2
11
who have uncompensated vestibular disorders may show 5
increased sway in conditions in which somatosensory or vi- 0
0 1 2 4 8
sual information is altered or not available. Their nervous A Surface Rotation Size
system appears to orient their bodies to visual and support 1
surface references even when these inputs are not reliably
indicating motion of their body’s COM in relation to the
environment. Investigators have hypothesized that even
healthy subjects vary in how much they “weigh” (rely 2
more heavily on) sensory information from a particular
source, like vision or somatosensation, so that may affect
how they respond to a v estibular lesion.10,28 Incomplete
Stim Amp
CNS adaptation to a v estibular lesion, particularly in the 3
4°
acute stages, is associated with excessive sway or falls in
8°
many sensory conditions. 72 However, as patients recover
and the CNS adapts to the v estibular loss, patients with
profound bilateral vestibular loss show the vestibular loss 4
pattern, and many patients with total unilateral loss even- B
0 0.2 0.4 0.6 0.8 1
Vestibular Weight
tually return to normal sensory orientation for postural
Figure 3.6 (A) People with unilateral vestibular loss
control.35 (UVL) vary in their sensory reweighting strategies. Solid
A recent study sho ws that patients with unilateral lines show vestibular weight as surface tilt angle increases
vestibular loss vary quite a bit on how much they use their in 11 individual patients with UVL. Asterisks show normal
remaining vestibular function system for postural orienta- vestibular weighting. (B) Correlation between Vestibular
tion, with a group a verage of about 50% of normal Dysfunction ADL by Cohen73 (VDADL) scores and vestibular
weighting. Patients with UVL who had highest vestibular
(Fig. 3.6A).73 Some patients with unilateral vestibular loss weighting for 4 degrees and 8 degrees surface rotations
are able to rely on their one remaining v estibular system had the best ADL scores. (Adapted from Peterka et al,
similar to normal when both vision and the somatosensory 2011, with permission.73)
inputs are unavailable. In contrast, other patients with uni-
lateral vestibular loss behave as if the y cannot use their
remaining vestibular function. The patients who were able even when vision is not pro viding accurate information
to use their remaining v estibular function when standing about body sway. However, when the eyes are closed, they
on the sway-referenced surface with eyes closes showed are able to rely on surface information when standing on
better perceived activities of daily li ving than patients a firm surface and on vestibular information when stand-
who increased weighting on somatosensory inputs ing on a sway-referenced surface.
(Fig. 3.6B).74 People with bilateral or unilateral loss of v estibular
Some vestibular patients who have distorted, but not function can readily substitute alternati ve sensory inputs
absent, vestibular function because of pathologies such as to improve their balance. For example, studies have shown
acute hydrops that alters, but does not eliminate, vestibular that light touch as minimal as that needed to read braille
input may show a Visually Dependent Pattern of sensory is even more effective than vision in stabilizing the pos-
organization.66 These patients show excessive sway when- tural sway of people with bilateral v estibular loss.75,76
ever the visual surround is sway-referenced but show nor- People with bilateral or unilateral vestibular loss can also
mal sway with eyes closed. It is as if the nerv ous system use therapeutic audio-, visual-, or vibrotactile-biofeedback
relies on visual information whenever the eyes are open, about trunk motion to control stance posture, e ven when
3970_Ch03_029-048 25/06/14 11:26 AM Page 37
standing on a compliant foam surf ace with e yes nerves of guinea pigs and monk eys could improve their
closed.71,77 In fact, patients with unilateral loss of vestibu- equilibrium control, so this type of implanted biofeedback
lar function can substitute audio-biofeedback about direc- may one day be applied to patients with vestibular loss.81
tion and e xtent of lateral body sw ay, sensed with an These results suggest that v estibular loss patients who
accelerometer on the trunk, to successfully w alk tandem complain of balance problems will benef it from use of a
with eyes closed, a task normally impossible for them. cane or other augmented sensory feedback to provide sen-
Figure 3.7A illustrates reduced sway during stance with sory information about trunk sway with respect to earth to
eyes closed in a patient with bilateral vestibular loss using substitute for their missing vestibular function, particularly
audio-biofeedback.78 Figure 3.7A shows improvement of when balancing on an unstable surface.
COM stabilization during tandem walking trials with and In summary, these studies show that vestibular infor-
without biofeedback in a group of nine patients with uni- mation for body orientation is most important in environ-
lateral vestibular loss.79 All patients with unilateral ments that lack good somatosensory and/or visual cues for
vestibular loss significantly improved their balance with orientation. Patients attempting to rely on faulty or missing
practice and retained this impro vement the ne xt day. vestibular information in these en vironments may align
Biofeedback immediately improves balance performance themselves poorly and f all. However, they may also
but does not speed motor learning (Fig. 3.7B). choose another source of orientation information when
Even simple sensory feedback such as an alarm vestibular information is missing.
indicating that the trunk has tilted beyond a particular limit
can significantly reduce postural sw ay.80 A study of Controlling Center of Mass—
healthy young adults standing on a rotating surf ace
showed that all modes of biofeedback reduced impro ved
Postural Responses
multisegmental control of posture and stabilized the trunk The previous sections described how the vestibular system
in space, although spontaneous postural motor learning detects the position and motion of the head, and how this
also improved multisegmental postural control (Fig. 3.7C). sensory information is used for postural orientation. This
However, the more information pro vided to the nerv ous section will describe how motor output from the vestibular
system about the direction and magnitude of postural system contributes to static body positions and dynamic
sway, the more sway can be reduced (Fig. 3.7C). Animal postural movements, which help serv e the postural goal
studies have recently shown that galvanic vestibular stim- of maintaining equilibrium, that is, controlling the center
ulation scaled to head rotation applied directly to the 8th of body mass within its limits of stability. We know from
Without ABF
ML-COP SD
60 Without BF 10 Alarm
Magnitiude
COP AP Displacement (mm)
With BF
Direction
ML COM SD (mm)
Direction and
50 9 magnitude
(mm)
40 8
0 20
30 7
COP ML Displacement (mm) Trials Block 1 Block 2 Block 3
A B C
Figure 3.7 Biofeedback can reduce postural sway in subjects with BVL (A) Postural sway is
reduced in a subject with audio-biofeedback (light gray) as compared with no biofeedback
(dark gray) in the same subject. (Adapted from Dozza et al, 2005.)78 (B) Effect of practicing
tandem gait across trials with and without audio-biofeedback (BF). Each value represents the
average among the nine subjects with UVL on three consecutive trials. Error bars represent
standard errors. (Adapted from Dozza et al, 2007.)79 (C) Effects of different types of informa-
tion provided by biofeedback. Averaged SD of ML-COP over the three blocks of trials in all
conditions with and without ABF in 13 healthy controls. (Adapted from Dozza et al, 2011.80)
3970_Ch03_029-048 25/06/14 11:26 AM Page 38
anatomic studies that motor output pathw ays leave the postural responses when surface and visual inputs are not
central vestibular nuclei and descend in the spinal cord, available.7,83-87 Quick displacements directly to the head
where they terminate on the neurons that activate primarily during stance also result in muscle acti vations in the
neck and trunk b ut also limb muscles. 82 However, the neck (45 ms), trunk (85 ms), thigh (90 ms), and ankle
functional significance of the descending v estibular (70 ms).88-90 These responses are absent in patients with
system for the control of orientation and equilibrium in adult-onset vestibular loss, suggesting a vestibular origin.
alert, intact humans and animals is still poorly understood. However, adults who lost v estibular function as inf ants
Nevertheless, there is e vidence that v estibular signals may show normal patterns of response to these head per-
probably play a variety of roles, including stabilizing the turbations, suggesting that cervicospinal responses may
head and trunk in space, scaling postural responses, and adaptively compensate for the loss of vestibular input early
contributing to the selection of appropriate postural strate- in life.89,90
gies for the environmental conditions. Because limb muscles are acti vated in response to
Orientation and equilibrium represent tw o distinct sudden drops, perturbations in head position, and galvanic
postural goals. To accomplish some tasks, greater priority stimulation,43,44,46 investigators have hypothesized that
must be placed on achie ving a specific postural orienta- vestibulospinal mechanisms may also play a role in auto-
tion, at the cost of postural equilibrium. F or example, an matic postural responses to stance perturbations. 91 Two
experienced soccer or volleyball player may make contact types of surface perturbations have been used to test this
with a ball even though making contact requires falling to hypothesis: horizontal translations, which induce body
the ground. Other tasks require equilibrium at the cost of sway such as from a slip or trip, and platform rotations,
postural orientation. For example, balancing across a wire which induce ankle dorsifle xion or plantar fle xion, as
may require rapid hip flexion and extensions to maintain when standing on a boat or pier. Surface translations result
equilibrium. In this task, trunk orientation with respect to in activation of the stretched ankle muscles, which occur
vertical is sacrificed to achieve the goal of equilibrium. at 80 to 100 ms following the onset of platform movement
The way in which the CNS achieves the trade-off between and act to restore the body to initial position. It does not
control of orientation and control of equilibrium in pos- appear, however, that vestibular inputs contribute a great
tural tasks is not well understood. Both static positions and deal to these responses. Human subjects and cats with
dynamic movements require a system that prioritizes complete absence of v estibular function can respond to
behavioral goals and uses all the sensory information surface translations using automatic postural responses
available to effectively and efficiently control the limbs with normal latencies and patterns, e ven when vision is
and trunk to achieve both orientation and equilibrium. not present.72 Proprioceptive information from stretched
muscles appears to be sufficient for recovery from surface
translations. This conclusion is supported by the f inding
Triggering Automatic Postural that automatic postural responses to surf ace translations
Responses are delayed when proprioceptive inputs are disrupted but
If balance is disturbed in a standing human, limb muscles not when v estibular inputs are disrupted. 92-96 Finally,
are activated at short latencies to restore equilibrium. relatively large head accelerations are required to produce
Because the latencies of these muscle acti vations are relatively weak responses in the limbs, and the head
shorter than a v oluntary reaction time, and because the y accelerations that occur in response to platform transla-
act to restore equilibrium, they are called “automatic pos- tions are quite small. 88-90 Therefore, vestibulospinal
tural responses.” Although the most important sensory responses probably do not play a large role in the recovery
trigger for automatic postural responses is somatosensory of equilibrium to slips or trips.
inputs, vestibular inputs may also play a role. Both cats In contrast to responses to translations, responses to
and humans respond to sudden drops from a height with surface rotations rely much more hea vily on the vestibu-
short latency ankle extensor activations (50 to 100 ms in lospinal system. Surface rotations stretch muscles in the
cat; 80 to 200 ms in humans).These muscle responses are lower leg, but do not produce corresponding forw ard or
present with eyes closed, so they can be triggered without backward body sw ay. Responses to platform rotations
visual stimulation. These responses are missing in patients consist of two parts. First to occur is a response in the
with absent vestibular function, but survive procedures in stretched ankle muscle at 70 to 100 ms, which is probably
animals that eliminate the canals b ut spare the otoliths. triggered by proprioceptive inputs.88,91,95,97-99 and which
The magnitude of the responses is also proportional could, if unopposed, actually destabilize the body. Slightly
to head acceleration, all of which suggests a v estibular later, a stabilizing response occurs in the shortened ankle
and, more specifically, an otolith origin for fast, automatic muscle (at 100 to 120 ms), and this corrective response is
3970_Ch03_029-048 25/06/14 11:26 AM Page 39
probably more dependent on vestibular (and visual) inputs. well as different body movements and joint forces, called
Patients with bilateral and unilateral loss of vestibular sys- “postural strategies.”99 Two very different strategies for
tem have reduced magnitudes and delayed latencies of this moving the body’s COM without mo ving the feet ha ve
late, stabilizing response, particularly if the velocity of the been identified: the “ankle strategy” and the “hip strategy”
surface tilt is not so f ast that quick, somatosensory (Fig. 3.9).103 An ankle strategy is used to reco ver from a
responses are triggered, nor too slow such that orientation small postural disturbance when standing on a f irm, flat
to the surface is sufficient for equilibrium.97 The ability to support surface. The body sways roughly as an in verted
adaptively reduce the magnitude of the destabilizing pendulum by exerting force around the ankle joints.A hip
response to repeated surface tilts is also impaired in some strategy, which consists of rapid body motions about the
patients with loss of v estibular function.68 The cause of hip joints, is typically used on narro w support surfaces
this failure to adapt could either be that v estibular infor- (beams), compliant or tilting support surf aces (foam, tilt
mation is required to trigger the adapti ve process or boards), when stance is narrow (one-foot standing or tan-
because patients with absent v estibular function become dem stance), or when COM position must be corrected
dependent on proprioceptive information.100,101 quickly. There is e vidence that these postural control
Surprisingly, complete v estibular loss does not strategies are centrally programmed and can be combined
result in reduced or absent equilibrium responses. In fact, depending on biomechanical conditions, subject expecta-
postural responses to surface translations are larger than tions, and prior experience.36,103,104 A stepping (or grabbing)
normal in animals and humans with complete, bilateral strategy that increases the base of support over the falling
loss of vestibular information, consistent with vestibular center of body mass usually occurs later, after an ankle or
ataxia.102 Figure 3.8 shows the center of pressure change hip strategy is insufficient to recover equilibrium.105,106
in response to a surf ace perturbation. The person with Vestibular information does not seem to be essential
vestibular loss has a response that is too lar ge for the for initiation or e xecution of a normal ankle or stepping
given stimuli compared with a control subject. Thus, pos- strategy, because subjects with complete absence of
tural instability and falls in patients with loss of vestibu- vestibular function sho w normal kinematic and EMG
lar function can be a result of responding too much to patterns, with the exception of neck muscles.36,72,107 This
inappropriate sensory cues and consequently thro wing suggests that proprioceptive information is sufficient to
themselves into disequilibrium. control the ankle and stepping strate gies, albeit with
abnormal activation of neck muscles resulting in lar ger
than normal head accelerations. 108 In contrast, vestibular
Selection of Postural Strategies information appears to be useful in controlling the hip
Not all postural tasks require the same type of movement strategy. Patients with bilateral vestibular loss show poor
for the recovery of equilibrium, and some automatic pos- performance in tasks such as one-foot standing, heel-toe
tural responses require more vestibular involvement than walking, and beam balancing, all tasks requiring hip strat-
others. These different postural responses ha ve different egy for good balance control. 72,107,109,110 Also, subjects
muscle activation patterns (called postural syner gies) as with loss of somatosensory information from the feet
because of ankle ischemia, who presumably must increase
their reliance on the vestibular system, use a hip strategy
when an ankle strategy would be more efficient.109 All of
Vestib loss these findings suggest a critical link between the vestibular
400
system and the use of hip strategy to control posture.
300 Although vestibular loss patients appear to be able to
initiate hip strategy responses to fast surface translations
N cm
200 Control when standing on a firm, flat surface, they take compen-
100
satory steps to maintain balance in response to these faster
translations more frequently than normal subjects.35 They
0 may resort to stepping because hip strate gy may require
0 200 400 600 800 efficient control of the trunk and good stabilization of the
Time (ms)
head with respect to gravity.
Figure 3.8 Postural responses to perturbations are too
Whereas vestibular loss is associated with a f ailure
large in patients with bilateral vestibular loss (BVL). Graph
shows center of pressure changes from plantar flexion in to use hip strate gy in some conditions, some patients
response to a forward fall in a subject with BVL and a with pathology of the vestibular system habitually use hip
control subject. movements to control COM position. 66,107,111 These
3970_Ch03_029-048 25/06/14 11:26 AM Page 40
A B C
D E F
Figure 3.9 Three main postural response strategies used to maintain COM within base of
support for balance control in the sagittal plane (A, B, C) and in the frontal plane (C, D, E).
Ankle strategy can be utilized for small perturbations (A, D), hip strategy is required for larger
perturbations or more challenging stance conditions (B, E), and finally a step is required if per-
turbation is large enough to displace COM the body COM beyond the base of support (C, F).
patients typically report visual motion sensitivity, vertigo, response to a displacement of center of body mass outside
and ataxia consistent with vestibular dysfunction, and have their limits of stability because they perceive themselves to
histories consistent with v estibular pathology, but often be well within their stability limits. In contrast, other
show normal horizontal v estibulo-ocular reflex (VOR) patients may make exaggerated postural responses to small
function during rotation testing; these findings suggest that perturbations well within their limits of stability because
these patients have sustained damage to their v estibular they perceive themselves to be at their limits of stability and
systems, but have not lost a significant amount of horizon- therefore at risk for a fall. The type of response may depend
tal canal vestibular function.66,111,112 Coordination of head both on the type of vestibular dysfunction and the require-
and trunk motions are abnormal in vestibular patients who ments of the task.
use excessive hip strategy. In summary, vestibular information is used, with in-
Patients who perceive themselves to be in a dif ferent formation from other senses, to construct internal maps of
relation to their stability limits than the y actually are the limits of stability, which affect body alignment and
may show inappropriate postural movement strategies in recovery from postural disturbances. The information
response to destabilization.39,112 For example, some patients available from the v estibular system and its relationship
may not take a step necessary to reco ver equilibrium in to information from the other senses changes depending
3970_Ch03_029-048 25/06/14 11:26 AM Page 41
on the movement strategy used in controlling equilibrium. Although there is some mo vement of the head in
We suggest that postural strate gies are specific prescrip- space during most locomotor tasks, the position of the
tions for mapping interactions among sensory and motor head with respect to gra vity is often held relati vely
elements of postural control; these maps are, in essence, a constant, despite the large movements of the body that can
method for solving sensorimotor equilibrium and orienta- occur during tasks lik e hopping or running. 114,117,118 For
tion problems. Indi viduals need a v ariety of dif ferent example, neck muscle activations are observed in normal
movement strategies to choose from depending on current, subjects using a hip strate gy.36,38,107,118 In these studies,
past, and expected environmental conditions. Although the the neck muscle acti vations occurred before an y large
vestibular system may not be prescribing the details of the change in head position, and so the acti vations appear
coordinated motor pattern for postural mo vements, it to be a result of an anticipatory control strate gy. In other
seems to be intimately involved in the appropriate selec- words, these muscle activations serve to prevent the large
tion of movement strategies and in coordination of the tilts of the head with respect to gra vity that could occur
head with the rest of the moving body. during the lar ge trunk mo vements, characteristic of a
hip strategy.
Stabilizing the Head During tasks like walking and running, patients with
profound vestibular loss show increased variability in head
and the Trunk position with respect to gravity.107,119-122 When standing on
The use of visual and vestibular information for the control an oscillating surface with eyes closed, patients with vestibu-
of posture is complicated by the f act that these sense or - lar loss show large oscillations of their heads and trunks in
gans are located in the inertially unstable head. Because space, unlike healthy control subjects who stabilize their
the center of gravity of the head is located abo ve its axis trunks with respect to gravity more and more as the surface
of rotation, any movement of the body will result in head oscillations increase in frequency.123 Figure 3.10 compares
motion. Uncontrolled head motion complicates the use of stable control of the trunk in a control subject compared with
vestibular information to make estimates of body motion large forward and backward drift of the trunk in a patient
and position. Also, if the range of head motions e xceeds with vestibular loss during forward and backward transla-
that which can be compensated for by the VOR, blurred tions of their support surf ace. Some well-compensated
vision could result. For these reasons, investigators have vestibular loss patients, however, can stabilize their trunks
suggested that the nervous system stabilizes the head with in space when their eyes are open, whereas poorly compen-
respect to gravity during postural control to simplify the sated vestibular loss patients cannot use vision to compen-
interpretation of vestibular information and to f acilitate sate for loss of v estibular function. Despite abnormal
gaze stabilization.113-116 In the absence of reliable infor- top-down coordination of the head and the trunk, vestibular
mation about gravity from the vestibular system, or in an loss subjects showed normal coordination of their legs at all
attempt to simplify the control of head on trunk mo ve- frequencies of surface oscillation, even with eyes closed,
ments, the nervous system might stabilize the head with consistent with a bottom-up somatosensory control of pos-
respect to the trunk.113 tural coordination of the legs.124
Figure 3.10 Comparison of stable trunk in space in healthy control subject versus large
trunk instability in a subject with bilateral vestibular loss during fast, anterior-posterior
surface translations. Stick figures show lateral view of trunk, thigh, and legs during surface
oscillations. Solid lines show anterior (up) and posterior (down) trunk displacements in a
representative control subject (gray line) and vestibular loss subject (darker line). Dashed lines
show platform surface oscillations.
3970_Ch03_029-048 25/06/14 11:26 AM Page 42
In summary, the vestibular system plays an important Consider, for example, a task and a set of en viron-
role in head and trunk stabilization with respect to gravity. mental conditions that occur frequently in clinical exami-
In contrast, the v estibular system appears to be less im - nations of postural control: the patient is asked to maintain
portant for the control of the position of the body’s COM verticality in a condition of inaccurate proprioception and
or postural coordination of the legs, especially when good absent or inappropriate visual information. This task is ap-
somatosensory cues about body position are a vailable. propriate to test the ability of the patient to use vestibular
Vestibular loss subjects are very successful in substituting information for the control of posture because visual and
light fingertip touch on a stable surf ace, such as a cane, somatosensory cues for orientation are poor , and normal
for loss of vestibular function to stabilize posture. subjects typically stabilize their heads with respect to grav-
ity while executing such tasks. When asked to perform this
task, patients who ha ve recently lost v estibular function
Clinical Implications will demonstrate abnormalities in the use of v estibular
The vestibular system plays man y potential roles in information in each of its four roles. First, they will have
postural control. The role it plays in any given postural difficulty perceiving and reporting when their bodies or
task will depend both on the nature of the task and on heads are properly oriented to gra vity; that is, the y will
the environmental conditions. When the stabilization have difficulty identifying when they are upright. Second,
of the head or trunk is critical for performance, the they will orient head and body position poorly to gravity,
vestibular system assumes a v ery important role. showing tilts rather than upright orientations when asked
Likewise, when somatosensory (and, to a lesser degree, to right themselves. Third, if the board is tipped suddenly,
visual) information is not available, vestibular informa- they may not be able to recover balance, and fourth, head
tion for postural control assumes a dominant role. Table 3-1 position with respect to gra vity will vary a great deal as
suggests some tasks and conditions in which vestibular they attempt to recover from the perturbation.
information for postural control is important, and some Although the vestibular system has a prominent role in
balance abnormalities that suggest a vestibular disorder. postural control, some aspects of balance do not rely on the
It is also important to note that although this table and vestibular system or may be compensated for by other sys-
this chapter ha ve been de voted to the role of the tems. Figure 3.11 outlines six underlying systems that con-
vestibular system in the control of standing balance, the tribute to postural control; only Anticipatory Postural
vestibular system is equally important during locomo- Adjustments are unaffected by vestibular pathology. These
tion, and problems with sensing mo vement, orienting include Biomechanical constraints (such as neck pain and
to vertical, controlling the position of the COM, and stiffness), Verticality and Limits of Stability (impaired and
stabilizing the head result in impairments in gait as well may be difficult to detect because of compensation), Antic-
as standing balance. ipatory Postural Adjustments (preserved in people with
Role of the Vestibular System Clinical Assessment Findings Suggestive of Vestibular Disorder
Sensing and perceiving self-motion Patient performs head Patient reports abnormal sensations of motion
motions and/or posi- and/or vertigo
tions in different
planes
Orienting to vertical Patient stands on in- Trunk oriented to support surface instead of
clined surface or on gravity; patient falls or sway increases markedly
foam with eyes closed
Controlling center of mass (COM) Patient stands or Patient is not able to use hip strategy to control
walks on a beam COM and falls
Stabilizing the head Patient leans or is Head not stabilized with respect to vertical
tilted
3970_Ch03_029-048 25/06/14 11:26 AM Page 43
Continued
3970_Ch03_029-048 25/06/14 11:26 AM Page 44
discuss its role in orienting the trunk to vertical using sen- muscle vibratory proprioceptive stimulation. Gait & posture.
sory orientation and weighting-appropriate sensory cues 2009;30(1):93.
13. Mauritz KH, Dichgans J, Allum JHJ, Brandt T. Frequency
under different sensory environments. Third, we discuss
characteristics of postural sway in response to self-induced
the role of the vestibular system in controlling the position and conflicting visual stimulation. Pfltigers Arch. 1975;355.
of the body’s COM, both for static positions and dynamic 14. Van Asten WNJC, Gielen CCAM, Van der Gon JJD.
movements via postural responses. Fourth, we discuss its Postural adjustments induced by simulated motion of
role in the v estibular system in the control of standing differently structured environments. Exp Brain Res.
1988;73:371-383.
balance. The vestibular system is equally important during
15. Day BL, Ramsay E, Welgampola MS, Fitzpatrick RC. The
locomotion so problems with sensing movement, orienting human semicircular canal model of galvanic vestibular
to vertical, controlling the position of the COM, and stabi- stimulation. Exp Brain Res. 2011;210(3):561-568.
lizing the head results in similar impairments in gait as in 16. Matthews PBC. Mammalian Muscle Receptors and Their
standing balance. Central Actions. London: Arnold; 1972.
17. Laube R, Govender S, Colebatch JG. Vestibular-dependent
spinal reflexes evoked by brief lateral accelerations of the
References heads of standing subjects. J Appl Physiol. 2012;112(11):
1. Mergner T, Schweigart G, Fennell L, Maurer C. Posture 1906-1914.
Control in Vestibular-Loss Patients. Ann NY Acad Sci. 18. Nashner LM, Wolfson P. Influence of head position and
2009;1164(1):206-215. proprioceptive cues on short latency postural reflexes
2. Bronstein AM, Pérennou DA, Guerraz M, Playford D, evoked by galvanic stimulation of the human labyrinth.
Rudge P. Dissociation of visual and haptic vertical in two Brain Res. 1974;67:255-268.
patients with vestibular nuclear lesions. Neurology. 19. Magnusson M, Johansson R, Wiklund J. Galvanically
2003;61(9):1260-1262. Induced Body Sway in the anterior-posterior plane. Acta
3. Funabashi M, Santos-Pontelli T, Colafêmina J, Pavan T, Otolaryngol. 1990;110:11-17.
Carneiro A, Takayanagui O. A new method to analyze the 20. Dichgans J, Brandt T. Visual-vestibular interaction: effects
subjective visual vertical in patients with bilateral vestibu- on self-motion perception and postural control. In: Held R,
lar dysfunction. Clinics. 2012;67(10):1127-1131. Leibowtz HW, Teuber HL, eds. Handbook of Sensory
4. Ogawa Y, Otsuka K, Shimizu S, Inagaki T, Kondo T, Physiology: Perception. Berlin Heidelberg New York:
Suzuki M. Subjective visual vertical perception in patients Unknown; 1978:755-804.
with vestibular neuritis and sudden sensorineural hearing 21. Trutoiu LC, Mohler BJ, Schulte-Pelkum J, Bülthoff HH.
loss. J Vestib Res. 2012;22(4):205-211. Circular, linear, and curvilinear vection in a large-screen
5. Brandt T, Dieterich M. Cyclorotation of the Eyes and Sub- virtual environment with floor projection. Computers &
jective Visual Vertical in Vestibular Brain Stem Lesionsa. Graphics. 2009;33(1):47-58.
Ann NY Acad Sci. 1992;656(1):537-549. 22. Johansson R, Magnusson M, Akesson M. Identification of
6. Lackner JR. Some mechanisms underlying sensory and human postural dynamics. IEEE Transitions in Biomedical
postural stability in man. In: Held R, Leibowitz HW, Teuber Engineering. 1988;35:858-869.
HL, eds. Handbook of Sensory Physiology: Perception. 23. Pyykko I, Hansson GA, Schalen L, Henriksson NG,
New York: Springer Verlag; 1978:806-845. Wennmo C, Magnusson M. Vibration-induced body sway.
7. Lestienne F, Soechting J, Berthoz A. Postural readjust- In: Computers in Neurootologic Diagnostics. 1st ed.
ments induced by linear motion of visual scenes. Exp 1983:139-155.
Brain Res. 1977;28:363-384. 24. Gurfinkel, VS, and Levick YS. Perceptual and automatic
8. Gurfinkel VS, Levik YS, Popov KE, Smetanin BN, Shlikov aspects of the postural body schema. In: J. Paillard, ed.
VY. Body scheme in the control of postural activity. In: Brain and Space. Oxford: Oxford University Press;
Gurfinkel VS, Yoffe M, Massion J, Roll J, eds. Stance and 1991:147-162.
Motion: Facts and Theories. New York: Plenum Press; 25. Von Holst, E, Mittelstaedt H. Das Raefferenzprinzip.
1988:185-193. Naturwissenschaften. 1957;37:464.
9. Xerri C, Borel L, Barthelemy J, Lacour M. Synergistic in- 26. Longo MR, Azañón E, Haggard P. More than skin deep:
teractions and functional working range of the visual and body representation beyond primary somatosensory
vestibular systems in postural control: neuronal correlates. cortex. Neuropsychologia. 2010;48(3):655-668.
In: Pompeiano O, Allum JHJ, eds. Vestibulospinal Control 27. Macpherson JM, Horak FB. Posture. In: Kandel E,
of Posture and Locomotion: Progress in Brain Research, Schwartz J, Jessell T, Siegelbaum S, Hudspeth A, eds.
Vol. 76. New York: Elsevier; 1988:193-203. Principles of Neural Science. 5th ed. McGraw-Hill;
10. Zacharias GL, Young LR. Influence of combined visual 2013:935-958.
and vestibular cues on human perception and control of 28. Mergner T, Becker W. Perception of Horizontal Self-rotation:
horizontal rotation. Exp Brain Res. 1981;41:159-171. Multisensory and Cognitive Aspects. (Warren R, Wentheim
11. Isableu B, Ohlmann T, Cremieux J, Vuillerme N, Amblard B, A, Erbausen L, eds.).; 1990:219-263.
Gresty MA. Individual differences in the ability to identify, 29. DeWaele C, Graf W, Berthoz A, Vidal PP, De Waele C.
select and use appropriate frames of reference for perceptuo- Vestibular control of skeletal geometry. In: Amblard B,
motor control. Neuroscience. 2010;169(3):1199-1215. Berthoz A, Clarac F, eds. Posture and Gait: Development,
12. Gomez S, Patel M, Magnusson M, et al. Differences Adaptation and Modulation. New York: Excerpta Medica;
between body movement adaptation to calf and neck 1988:423-432.
3970_Ch03_029-048 25/06/14 11:26 AM Page 46
30. Dow RS. The effects of unilateral and bilateral labyrinthec- 47. Kots YM. Decending reflex influences during the organi-
tomy in monkey, baboon and chimpanzee. American Jour- zation of voluntary movement. In: Evarts EV, ed. The
nal of Physiology—Legacy Content. 1938;121(2):392-399. Organization of Voluntary Movement: Neurophysiological
31. Schaefer KP, Meyer DL. Compensation of vestibular lesions. Mechanisms. New York, London: Plenum Press;
In: Handbook of Sensory Physiology. vest comp; review; 1975:181-229.
1974:463-490. 48. Njiokiktjien C, Folkerts JF. Displacement of the body’s
32. Precht W. Recovery of some vestibuloocular and vestibu- centre of gravity at galvanic stimulation of the labyrinth.
lospinal functions following unilateral labyrinthectomy. Stereotactic and Functional Neurosurgery. 1971;33(1):
In: Freund HJ, Buttner U, Cohen B, Noth J, eds. The 46-54.
Oculomotor and Skeletal-Motor Systems: Differences and 49. Storper IS, Honrubia V. Is human galvanically induced
Similarities. Vol 64. Amsterdam - New York, NY: Oxford: triceps surae electromyogram a vestibulospinal reflex
Elsevier Scince Pulishers B.V. (Biomedical Division); response? Otolaryngol Head Neck Surg. 1992;107:
1986:381-389. 527-536.
33. Dieringer N. “Vestibular compensation”: Neural plasticity 50. Goldberg JM, Fernandez C, Smith CE. Responses of
and its relations to functional recovery after labyrinthine vestibular-nerve afferents in the squirrel monkey to exter-
lesions in frogs and other vertebrates. Prog Neurobiol. nally applied galvanic currents. Brain Res. 1982;252:
1995;46(2):97-129. 156-160.
34. Curthoys IS, Halmagyi GM. Vestibular compensation: 51. Tokita T, Al E. Diagnosis of otolith and semicircular-canal
A review of the oculomotor, neural and clinical conse- lesions by galvanic nystagmus and spinal reflexes. In:
quences of unilateral vestibular loss. J Vestib Res. Graham M, Kemink J, eds. The Vestibular System: Neuro-
1995;5:67-107. physiologic and Clinical Research. New York: Raven;
35. Black FO, Shupert CL, Peterka RJ, Nashner LM. Effects 1987:305.
of unilateral loss of vestibular function on the vestibulo- 52. Watanabe Y, Al E. Clinical evaluation of vestibular-
ocular reflex and postural control. Ann Otol Rhinol Laryn- somatosensory interactions using galvanic body sway
gol Suppl. 1989;98:884-889. test. In: Graham M, Kemink J, eds. The Vestibular System:
36. Runge CF, Shupert CL, Horak FB, Zajac FE. Role of Neurophysiologic and Clinical Research. New York:
vestibular information in initiation of rapid postural Raven; 1987:393.
responses. Exp Brain Res. 1998;122(4):403-412. 53. Curthoys IS. A critical review of the neurophysiological
37. Shupert CL, Horak F, Shrank W, Kardonsky K, Black FO. evidence underlying clinical vestibular testing using
Hip sway associated with vestibulopathy: Voluntary hip sound, vibration and galvanic stimuli. Clin Neurophysiol.
strategy? unpublished. 1992. 2010;121(2):132-144.
38. Carpenter M, Allum J, Honegger F. Vestibular influences 54. Hlavacka F, Horak FB. Somatosensory influence on pos-
on human postural control in combinations of pitch and tural response to galvanic vestibular stimulation. Physiol
roll planes reveal differences in spatiotemporal processing. Res. 2006;55(1):S121-S127.
Exp Brain Res. 2001;140(1):95-111. 55. Horak FB, Hlavacka F. Vestibular stimulation affects
39. Shumway-Cook A, Horak FB. Rehabilitation strategies for medium latency postural muscle responses. Exp Brain
patients with vestibular deficits. In: Neurologic Clinics. Res. 2002;144(1):95-102.
Vol 8.; 1990:441-457. 56. Lund S, Broberg C. Effects of different head positions on
40. Takemori S, Ida M, Umezu H. Vestibular training after sud- postural sway in man induced by a reproducible vestibular
den loss of vestibular functions. ORL J Otorhinolaryngol error signal. Acta Physiologica Scandinavica. 1983;117:
Relat Spec. 1985;47:76-83. 307-309.
41. Borel L, Harlay F, Magnan J, Lacour M. How changes in 57. Gurfinkel VS, Lipshits MI, Popov KY. Is the stretch reflex
vestibular and visual reference frames combine to modify a basic mechanism in the system of regulation of human
body orientation in space. Neuroreport. 2001;12(14): vertical posture? Biofizika. 1974;19:744-748.
3137-3141. 58. Horlings CGC, Carpenter MG, Honegger F, Allum JHJ.
42. Fukuda T. The stepping tests. Acta Otolaryngol. Vestibular and proprioceptive contributions to human
1959;50:95-108. balance corrections. Ann NY Acad Sci. 2009;1164(1):1-12.
43. Britton T, Day B, Brown P, Rothwell J, Thompson P, 59. McCollum G, Leen TK. Form and exploration of mechani-
Marsden C. Postural electromyographic responses in the cal stability limits in erect stance. J Mot Behav. 1989;21:
arm and leg following galvanic vestibular stimulation in 225-244.
man. Exp Brain Res. 1993;94:143-151. 60. Riach CL, Starkes JL. Stability limits of quiet standing
44. Fitzpatrick R, Burke D, Gandevia SC. Task-dependent postural control in children and adults. Gait Posture.
reflex responses and movement illusions evoked by 1993;1(2):105-111.
galvanic vestibular stimulation in standing humans. 61. Shumway-Cook A, McCollum G. Assessment and
J Physiol. 1994;478(2):363-372. treatment of balance deficits in the neurologuc patient.
45. Iles JF, Pisini JV. Vestibular-evoked postural reactions in 1991.
man and modulation of transmission in spinal reflex path- 62. Horak FB. Postural orientation and equilibrium: what do
ways. J Physiol. 1992;455:407-424. we need to know about neural control of balance to pre-
46. Inglis JT, Shupert CL, Hlavacka F, Horak FB. Effect vent falls? Age ageing. 2006;35(suppl 2):ii7-ii11.
of galvanic vestibular stimulation on human postural 63. Peterka RJ, Wall Iii C, Kentala E. Determining the effec-
responses during support surface translations. J Neurophys. tiveness of a vibrotactile balance prosthesis. J Vestib Res.
1995;73(2):896-901. 2006;16(1):45-56.
3970_Ch03_029-048 25/06/14 11:26 AM Page 47
64. Peterka RJ. Simplifying the complexities of maintaining 82. Wilson VJ, Peterson BW. Peripheral and central sub-
balance. IEEE Eng Med Biol Mag. 2003;22(2):63-68. strates of vestibulospinal reflexes. Physiological reviews.
65. Peterka RJ. Sensorimotor integration in human postural 1978;58(1):80-105.
control. J Neurophys. 2002;88(3):1097-1118. 83. Greenwood R, Hopkins A. Landing from an unexpected
66. Black FO, Nashner LM. Vestibulo-spinal control differs in fall and a voluntary step. Brain. 1976;99:375-386.
patients with reduced versus distorted vestibular function. 84. Lacour M, Xerri C, Hugon M. Muscle responses and
Acta Otolaryngol. 1984;406:110-114. monosynaptic reflexes in falling monkey: Role of the
67. Black FO, Shupert CL, Horak FB, Nashner LM. Abnormal vestibular system. Journal de Physiologie. 1978;74:
postural control associated with peripheral vestibular dis- 427-438.
orders. In: Pompeiano O, Allum JHJ, eds. Prog Brain 85. Melvill Jones G, Watt DGD. Muscular control of landing
Res.Vol 76. Amsterdam: Elsevier Science Publishers from unexpected falls in man. J Physiol. 1971;219:
BV; 1988:263-275. 729-737.
68. Nashner LM, Black FO, Wall III C. Adaptation to altered 86. Watt DGD. Effect of vertical linear acceleration on
support and visual conditions during stance: Patients with h-reflex in decerebrate cat, I: transient stimuli. J Neuro-
vestibular deficits. J Neurosci. 1982;2:536-544. phys. 1981;45(4):644-666.
69. Shumway-Cook A, Horak FB. Assessing the influence 87. Lin SI, Woollacott MH. Postural muscle responses fol-
of sensory interaction on balance: suggestions from lowing changing balance threats in young, stable older,
the field. Phys Ther. 1986;66(10):1548-1550. Available and unstable older adults. J Mot Behav. 2002;34(1):
at: http://www.ncbi.nlm.nih.gov/entrez/query.fcgi? 37-44.
cmd=Retrieve&db=PubMed&dopt=Citation&list_ 88. Dietz V, Horstmann GA, Berger W. Interlimb coordina-
uids=3763708. tion of leg-muscle activation during perturbation of
70. Romberg MH. A manual of the nervous diseases of man. stance in humans. J Neurophys. 1989;62:680-693.
Printed for the Sydenham Society; 1853. 89. Horak FB, Shupert CL, Dietz V, Horstmann G. Vestibular
71. Dozza M, Horak FB, Chiari L. Auditory biofeedback sub- and somatosensory contributions to responses to head
stitutes for loss of sensory information in maintaining and body displacements in stance. Exp Brain Res.
stance. Exp Brain Res. 2007;178(1):37-48. 1994;100:93-106.
72. Shupert CL, Black FO, Horak FB, Nashner LM. Coordi- 90. Shupert CL, Horak FB. Effects of vestibular loss on head
nation of the head and body in response to support surface stabilization in response to head and body perturbations.
translations in normals and patients with bilaterally J Vestib Res. 1996;6(6):423-437. Available at: http://www
reduced vestibular function. In: Amblard B, Berthoz A, .ncbi.nlm.nih.gov/entrez/query.fcgi?cmd=Retrieve&db=
Clarac F, eds. Posture and Gait: Development, Adaptation PubMed&dopt=Citation&list_uids=8968970.
and Modulation. Amsterdam: Elsevier Sciences Publishers 91. Allum J, Honegger F. A postural model of balance-correcting
BV; 1988:281-289. movement strategies. J Vestib Res. 1992;2:323-347.
73. Peterka RJ, Statler KD, Wrisley DM, Horak FB. Postural 92. Diener HC, Dichgans J, Guschlbauer B, Mau H. The
compensation for unilateral vestibular loss. Front Neur. significance of proprioception on postural stabilization as
2011;2. assessed by ischemia. Brain Res. 1984;296:103-109.
74. Cohen HS, Kimball KT. Development of the vestibular 93. Macpherson JM, Everaert DG, Stapley PJ, Ting LH.
disorders activities of daily living scale. Arch Otolaryngol Bilateral vestibular loss in cats leads to active destabiliza-
Head Neck Surg. 2000;126(7):881. tion of balance during pitch and roll rotations of the
75. Lackner JR, DiZio P, Jeka J, Horak F, Krebs D, Rabin E. support surface. J Neurophys. 2007;97(6):4357-4367.
Precision contact of the fingertip reduces postural sway of 94. Mauritz KH, Deitz V, Haller M. Balancing as a clinical
individuals with bilateral vestibular loss. Exp Brain Res. test in the differential diagnosis of sensory-motor disor-
1999;126(4):459-466. ders. Journal of Neurology, Neurosurgery and Psychiatry.
76. Krishnamoorthy V, Slijper H, Latash ML. Effects of differ- 1980;43:407-412.
ent types of light touch on postural sway. Exp Brain Res. 95. Nashner LM. Fixed patterns of rapid postural responses
2002;147(1):71-79. among leg muscles during stance. Exp Brain Res.
77. Dozza M. Biofeedback systems for human postural con- 1977;30:13-24.
trol. 2007. 96. Welch TDJ, Ting LH. A feedback model explains the
78. Dozza M, Chiari L, Horak FB. Audio-biofeedback im- differential scaling of human postural responses to
proves balance in patients with bilateral vestibular loss. perturbation acceleration and velocity. J Neurophys.
Arch Phys Med Rehabil. 2005;86(7):1401-1403. 2009;101(6):3294-3309.
79. Dozza M, Wall Iii C, Peterka RJ, Chiari L, Horak FB. 97. Allum J, Honegger F, Schicks H. The influence of a bilat-
Effects of practicing tandem gait with and without vibro- eral peripheral vestibular deficit on postural synergies.
tactile biofeedback in subjects with unilateral vestibular J Vest Res. 1994;4:49-70.
loss. J Vestib Res. 2007;17(4):195-204. 98. Diener HC, Dichgans J, Bruzek W, Selinka H. Stabiliza-
80. Dozza M, Chiari L, Peterka RJ, Wall C, Horak FB. tion of human posture during induced oscillations of the
What is the most effective type of audio-biofeedback body. Exp Brain Res. 1982;45:126-132.
for postural motor learning? Gait Posture. 2011;34(3): 99. Nashner LM, McCollum G. The organization of human
313-319. postural movements: a formal basis and experimental
81. Merfeld DM, Lewis RF. Replacing semicircular canal synthesis. Behav Brain Sci. 1985;8:135-172.
function with a vestibular implant. Curr Opin Otolaryngol 100. Horak FB. Comparison of cerebellar and vestibular loss
Head Neck Surg. 2012;20(5):386-392. on scaling of postural responses. In: Brandt T, Paulus IO,
3970_Ch03_029-048 25/06/14 11:26 AM Page 48
Bles W, eds. Disorders of Posture and Gait. Stuttgart: 114. Pozzo T, Berthoz A, Lefort L. Head stabilization during
George Thieme Verlag; 1990:370-373. various locomotor tasks in humans: 1. Normal subject.
101. Horak FB. Postural compensation for vestibular loss. Ann Exp Brain Res. 1990;82:97-106.
NY Acad Sci. 2009;1164(1):76-81. 115. Horak FB, Macpherson JM. Postural orientation and
102. Macpherson JM, Inglis JT. Stance and balance following equilibrium. Compr Physiol. 1996.
bilateral labyrinthectomy. Prog Brain Res. 1993;97: 116. Mergner T. A neurological view on reactive human
219-228. stance control. Annu Rev Control. 2010;34(2):177-198.
103. Horak FB, Nashner LM. Central programming of pos- 117. Assaiante C, Amblard B. Head-trunk coordination and
tural movements: adaptation to altered support-surface locomotor equilibrium in 3- to 8-year-old children. In:
configurations. J Neurophys. 1986;55(6):1369-1381. Berthoz A, Graf W, Vidal PP, eds. The Head-Neck
Available at: http://www.ncbi.nlm.nih.gov/entrez/ Sensory Motor System. New York: Oxford University
query.fcgi?cmd=Retrieve&db=PubMed&dopt= Press; 1992:121-125.
Citation&list_uids=3734861. 118. Grossman GE, Leigh RJ, Bruce EN, Huebner WP, Lanska
104. Park S, Horak FB, Kuo AD. Postural feedback responses DJ. Performance of the human vestibuloocular reflex dur-
scale with biomechanical constraints in human standing. ing locomotion. J Neurophys. 1989;62(1):264-272.
Exp Brain Res. 2004;154(4):417-427. 119. Grossman GE, Leigh RJ. Instability of gaze during loco-
105. Maki BE, McIlroy WE. The role of limb movements in motion in patients with deficient vestibular function. Ann
maintaining upright stance: the “change-in-support” Neurol. 1990;27(5):528-532.
strategy. Phys Ther. 1997;77(5):488-507. 120. Pozzo T, Berthoz A, Lefort L, Vitte E. Head stabilization
106. Maki BE, Mcilroy WE, Fernie GR. Change-in-support during various locomotor tasks in humans. II. Patients
reactions for balance recovery. IEEE Eng Med Biol Mag. with bilateral peripheral vestibular deficits. Exp Brain
2003;22(2):20-26. Res. 1991;85(1):208-217.
107. Shupert CL, Horak FB, Black FO. Effect of peripheral 121. Nashner LM, Shupert CL, Horak FB, Black FO. Organi-
vestibular disorders on head-trunk coordination during zation of posture controls: An analysis of sensory and
postural sway in humans. In: Berthoz A, Graf W, Vidal P, mechanical constraints. Allum JHJ, Hulliger M, eds.
eds. The Head-Neck Sensory Motor System. New York: Prog Brain Res. 1989;80:411-418.
Oxford University Press; 1992:607-610. 122. Horak FB. Postural compensation for vestibular loss and
108. Shupert CL, Horak FB. Adaptation of Postural Control in implications for rehabilitation. Restorative neurology and
Normal and Pathologic Aging: implications for Fall Pre- neuroscience. 2010;28(1):57-68.
vention Programs. JAB. 1999;15(1). 123. Buchanan JJ, Horak FB. Voluntary control of postural equi-
109. Horak FB, Nashner LM, Diener HC. Postural strategies librium patterns. Behav Brain Res. 2003;143(2):121-140.
associated with somatosensory and vestibular loss. Exp 124. Keshner EA, Woollacott MH, Debu B. Neck, trunk and
Brain Res. 1990;82:167-177. limb muscle responses during postural perturbations in
110. Fregly AR. Vestibular ataxia and its measurement in man. humans. Exp Brain Res. 1988;71:455-466.
In: Kornhuber HH, ed. Vestibular System: Handbook of 125. Horak FB, Wrisley DM, Frank J. The balance evaluation
Sensory Physiology. 6th ed. Berlin: Springer Verlag; systems test (BESTest) to differentiate balance deficits.
1974:321-360. Phys Ther. 2009;89(5):484-498.
111. Shupert CL, Horak FB, Black FO. Hip sway associated 126. Berg KO, Maki BE, Williams JI, et al. Clinical and labo-
with vestibulopathy. J Vestib Res. 1994. ratory measures of postural balance in an elderly popula-
112. Shumway-Cook A, Horak FB. Vestibular rehabilitation: tion. Arch Phys Med Rehabil. 1992;73(11):1073.
an exercise approach to managing symptoms of vestibu- 127. Duncan PW, Weiner DK, Chandler J, Studenski S. Func-
lar dysfunction. Seminars in Hearing. 1989;10:196-208. tional reach: a new clinical measure of balance. J Gerontol.
113. Nashner LM. Strategies for organization of human pos- 1990;45(6):M192-M197.
ture. In: Igarashi M BF, ed. Vestibular and Visual Control 128. Shumway-Cook A. Dynamic Gait Index. In: Motor
of Posture and Locomotor Equilibrium. S. Karger, Basel; Control: Theory and Practical Implications. Baltimore:
1985:1-8. Lippincott Williams & Wilkins; 1995.
3970_Ch04_049-058 25/06/14 11:28 AM Page 49
TWO
Fundamentals
of Dysfunction
3970_Ch04_049-058 25/06/14 11:28 AM Page 50
CHAPTER 4
Vestibular System
Disorders
Michael Fetter, MD
Peripheral vestibular dysfunction, which in volves the often appear when a patient rolls from side to side in bed.
vestibular end organs and/or the vestibular nerve, can pro- Patients can usually identify the of fending head position,
duce a variety of signs and symptoms. A thorough evalua- which they often studiously avoid. Many patients also com-
tion by a physician is needed to identify the specif ic plain of mild postural instability between attacks.The ver-
pathology behind the patient’s complaints of vertigo or dis- tigo lasts only 30 seconds to 2 minutes (usually less than
equilibrium. Patient history is the main key for diagnosis, 1 minute) and disappears even if the precipitating position
supported by a careful otoneurologic examination. Deter- is maintained. Hearing loss, aural fullness, and tinnitus are
mining whether vestibular rehabilitation is appropriate and, not seen in this condition, which most commonly occurs
if it is, which approach should be used is based in part on spontaneously in the elderly population but can be seen in
the patient’s diagnosis. This chapter describes the clinical any age group after e ven mild head trauma. Women are
presentation of the more common peripheral vestibular dis- more commonly af fected than men (2:1) and the right
orders. The results of diagnostic tests, and the medical, sur- labyrinth is slightly more often in volved than the left
gical, and rehabilitati ve management of each of these (1.4:1). Bilateral involvement can be found in 7.5%; 90%
disorders is presented as an o verview only, because this of these are traumatic cases. 1 Spontaneous remissions are
material is covered in detail in other chapters. common, but recurrences can occur, and the condition may
trouble the patient intermittently for years with a high
recurrence rate of up to 50% within 10 years.2
Benign Paroxysmal Positional Evaluation should include a careful otoneurologic ex-
amination, the most important part being the history . In
Vertigo the case of the most common posterior canal BPPV, a key
Benign paroxysmal positional vertigo (BPPV) is the most diagnostic maneuver is the Dix-Hallpike positioning test3
common cause of vertigo. Typically, a patient with BPPV while the examiner observes the patient’s eyes with a pair
complains of brief episodes of vertigo precipitated by rapid of Frenzel lenses or in combination with videooculogra-
changes of head posture. Sometimes symptoms are brought phy monitoring. Electronystagmography (ENG) can also
about by assuming very specific head positions. Most com- be used, b ut because the typical response in posterior
monly these head positions involve rapid extension of the BPPV is a combined vertical-torsional nystagmus, record-
neck, often with the head turned to one side (as when look- ings might be hard to interpret, because this technique
ing up to a high shelf or backing a car out of a garage) or cannot measure torsional eye movements and in the verti-
lateral head tilts toward the affected ear. The symptoms cal dimension recordings might be hampered by artifacts.
50
3970_Ch04_049-058 25/06/14 11:28 AM Page 51
A typical response is induced by rapid position changes lateral semicircular canals. F or this maneuver (Pagnini-
from the sitting to the head-hanging right or left position. McClure) the patient lies on his back and the head is moved
Vertigo and nystagmus begin with a latency of 1 or more either to right or left ear-down position about the long body
seconds after the head is tilted toward the affected ear and axis. Two types of lateral canal v ariant BPPV can be
increase in severity within about 10 seconds to a maxi- observed. The canalolithiasis type is usually geotropic
mum accompanied by a sensation of discomfort and ap- (80% of the cases with lateral canal variant) with the nys-
prehension that sometimes causes the patient to cry out tagmus beating toward the lowermost ear being more vig-
and attempt to sit up. The symptoms diminish gradually orous when lying on the offending ear. Sometimes one can
after 10 to 40 seconds and ultimately abate, e ven if the also see an ageotropic (the n ystagmus beating to the up-
precipitating head position is maintained. The nystagmus permost ear) nystagmus, that is transient in canalolithiasis
is mixed upbeat and torsional with a slight horizontal com- or more long lasting without onset latenc y in the case of
ponent: The direction corresponds v ery closely to the cupulolithiasis. In this case the of fending ear is the one
plane of the offending semicircular canal, very similar to where the n ystagmus is less vigorous when lying on
experimental stimulation of the afferents of the posterior that ear.
semicircular canal of the dependent ear.4 Because the ro- The classic explanation of the underlying pathophys-
tation axis of the eye is fixed and parallel to the axis of the iology (cupulolithiasis) was first described by Schuknecht
offending canal, the nystagmus changes with the direction in 1969.5 His study of the temporal bones of two patients
of gaze, becoming more torsional as the patient looks to- afflicted with this disorder showed deposition of otoconial
ward the dependent ear with the gaze line parallel to the material at the cupula of the posterior semicircular canal.
axis of the offending canal and more vertical as the patient The cupulolithiasis theory suggests that the debris adheres
looks toward the higher ear with the gaze line orthogonal to the cupula, making it denser than the surrounding en-
to the axis of the offending canal. dolymph and thereby susceptible to the pull of gra vity.
Sometimes, a low-amplitude, secondary nystagmus, This theory, however, implies that a positioning maneuver
directed in the opposite direction, may occur. If the patient should result in an enhanced positioning response with a
then quickly sits up, a similar b ut usually milder recur- nystagmus initially beating in the direction of an ampul-
rence of these symptoms occurs, the nystagmus being di- lopetal stimulation. This nystagmus should occur imme-
rected opposite to the initial n ystagmus. Repeating this diately after the positioning maneuver, and should change
procedure several times will decrease the symptoms. This direction as gravity drags the cupula do wn. The nystag-
adaptation of the response is of diagnostic value, because mus, however, should not subside as long as the head-
a clinical picture similar to that of BPPV can be created down position is maintained; that is, one w ould expect
by cerebellar tumors. In the latter, though, there is no ha- positional instead of positioning nystagmus. None of these
bituation of the response with repetiti ve testing. Further features are typically seen in posterior canal BPPV b ut
diagnostic criteria indicating a central positional n ystag- sometimes are seen in ageotropic lateral canal BPPV.
mus are as follows: (1) the condition does not subside with Brandt and Steddin emphasized a second theory ,
maintenance of the head in the precipitating position, canalithiasis, which better explains the typical features of
(2) the nystagmus may change direction when dif ferent BPPV.6 It suggests that the debris of a higher density than
head positions are assumed, (3) the nystagmus may occur the endolymph is free-floating in the canal.When the head
as downbeat nystagmus only in the head-hanging position, is moved in the plane of that canal, the debris sinks to the
or (4) the nystagmus direction does not coincide with the lowest point in the canal, causing the endolymph to move
previous stimulation axis. BPPV must also be dif ferenti- and deflecting the cupula by suction or pressure (lik e a
ated from positional nystagmus in Ménière’s disease, per- plunger), depending on the direction it moves. This theory
ilymph fistulas, and alcohol intoxication (positional accords with the direction of the n ystagmus and also
alcohol nystagmus [PAN]) and can also be seen as a tran- allows for a latency.
sient phenomenon in vestibular migraine. If symptoms persist longer than expected or if the po-
A few patients do not display the typical torsional up- sitional nystagmus shows atypical features, further investi-
beat nystagmus but show a strong horizontal n ystagmus, gation, such as magnetic resonance imaging (MRI), should
which nevertheless follows a similar pattern of buildup and be made to assess for unusual causes of positional vertigo,
decline but often o ver a longer period (posterior canal such as acoustic neuroma or tumors of the fourth ventricle.
BPPV: duration <30 s, latency 2–15 s; lateral canal BPPV: BPPV is usually a self-limiting disorder and com-
duration >30 s, latenc y <3 s). This horizontal nystagmus monly resolves spontaneously within weeks to months.
indicates a lateral canal v ariant of BPPV and is best pro- Simple vestibular exercises or maneuvers aimed at dispers-
voked when repositioning tak es place in the plane of the ing the otolithic debris from the cupula or to remo ve the
3970_Ch04_049-058 25/06/14 11:28 AM Page 52
debris from the canal can significantly speed recovery7; an- If examined early, the patient may manifest an irrita-
tivertiginous drugs are usually not helpful, unless used to tive nystagmus from the acute phases of the inflammation.
ease the vertiginous symptoms while performing the liber- Usually the patient is examined after these initial findings
atory maneuvers. In 1988, Semont and colleagues 8 intro- have given way to a more paralytic, or hypofunctional,
duced a single liberatory maneuv er, and Epley,9 in 1992, pattern. Caloric testing invariably shows ipsilateral hy-
proposed a variation, later modified by Herdman and asso- poresponsiveness or nonresponsiveness (horizontal canal
ciates10 (see also Chapter 20). For the lateral canal variant, paresis). The possibility that the three semicircular canals
there also exist meanwhile helpful liberatory maneuv ers and the otoliths (utricle and saccule) may be separately in-
(Lempert, Gufoni). With these newer liberatory maneuvers, volved in partial labyrinthine lesions is suggested by the
most patients can be treated successfully within less than a occasional observation (about 10% of the patients) of an
week. In many cases, immediate recovery after one reposi- acute unilateral vestibulopathy and a BPPV simultane-
tioning maneuver can be seen. Symptoms persist in only a ously in the same ear of a patient (Lindsay-Hemenw ay-
few patients in spite of compliance with v estibular exer- syndrome).12 With three-dimensional measurements of the
cises. For more severe symptoms unresponsive to exercises, vestibulo-ocular reflex in patients with vestibular neuritis,
three surgical options are available for relief. The first is this notion could be conf irmed. Patients with this condi-
transmeatal posterior ampullary nerve section (also known tion most often showed a partial involvement of only the
as singular neurectomy). The other two options are parti- superior vestibular nerve portion (subserving the anterior
tioning of the labyrinth using a laser technique and nonam- and lateral semicircular canals, the utricle, and a small part
pullary plugging of the posterior semicircular canal. of the saccule) leaving part of the saccule and the posterior
Nonampullary plugging seems to be a safe and ef fective semicircular canal afferents intact.13 The symptoms usu-
alternative to singular neurectomy for the small group of ally abate after a period of 48 to 72 hours, and gradual
patients with physically intractable BPPV. return to normal balance occurs o ver approximately
6 weeks. Rapid head movements toward the lesioned side,
however, can still cause slight oscillopsia of the visual
Vestibular Neuritis scene and impaired balance for a short moment. Recovery
Acute unilateral (idiopathic) vestibulopathy, also known is produced by the combination of central compensation
as vestibular neuritis, is the second most common cause of the vestibular tone imbalance, aided by physical e xer-
of vertigo. Although in most cases a definitive etiology is cise, and peripheral restoration of labyrinthine function.
never proved, evidence to support a viral etiology (similar The latter is found in about two-thirds of the patients.
to Bell’s palsy or sudden hearing loss) comes from The differential diagnosis should initially include
histopathological changes of branches of the v estibular other causes of acute v ertigo, and careful history taking,
nerve in patients who ha ve suffered such an illness and physical examination, and an audiogram are required.
the sometimes epidemic occurrence of the condition. 11 Physical examination should include a neurological exam-
Onset is often preceded by the presence of a viral infec- ination with attention to cranial nerv e findings and cere-
tion of the upper respiratory or gastrointestinal tracts.The bellar testing. Careful otoscopy is performed to rule out the
associated viral infection may be coincident with the presence of a potential otologic infectious process as the
vestibular neuritis or may have preceded it by as long as source of a toxic serous labyrinthitis. Fever in the presence
2 weeks. The chief symptom is the acute onset of pro- of chronic ear disease and labyrinthitis suggests suppura-
longed severe rotational vertigo that is e xacerbated by tion and meningitis. Commonly, a toxic labyrinthitis is the
movement of the head, associated with spontaneous hor- result of a well-defined event such as surgery or trauma.
izontal-rotatory nystagmus beating toward the good ear, More recently, the so-called acute v estibular syn-
postural imbalance with a tendenc y to f all toward the drome in elderly patients with at least one risk f actor for
affected side, and nausea. Hearing loss is not usually pres- vascular disease has been carefully ree valuated. Kattah
ent, but when it is then mumps, measles, and infectious and coworkers found that in this situation more than 3/4 of
mononucleosis, among other infections, have been impli- the patients had a central disorder (ischemia, bleeding)
cated. The latter condition should also alert the physician rather than vestibular neuritis.14 They further found, that
to consider other diagnoses (i.e., ischemia of labyrinth with careful e xamination for v ertical skew, direction
artery, Ménière’s disease, acoustic neuroma, herpes zoster changing nystagmus in different directions of gaze (gaze
oticus, Lyme disease, or neurosyphilis). The condition evoked nystagmus) and normal head impulses, a central
mainly affects those aged between 30 and 60 years, with cause could be detected with a sensitivity of 100% and a
a peak for w omen in the fourth decade and men in the specificity of 96%. This important finding for emergency
sixth decade. room evaluation has been summarized with the acron ym
3970_Ch04_049-058 25/06/14 11:28 AM Page 53
HINTS (Head Impulse (normal), Nystagmus (in different normal balance will return. During this recuperation time,
directions), Test for Skew). hearing gradually returns. Hearing may return to the pre-
Initial treatment of v estibular neuritis is accom- attack baseline or there may be residual permanent sen-
plished with the use of vestibular suppressants such as the sorineural hearing loss, most commonly in the lo wer
antihistamine dimenhydrinate or the anticholiner gic frequencies. The rare transient impro vement of hearing
scopolamine. In addition, bed rest is very helpful early on during the attack is known as the Lermoyez phenomenon.
in the course of the disease. After the most severe vertigo Tinnitus will also usually diminish as hearing returns.
and nausea have passed (after 24 to 72 hours), then am- As the disease progresses, hearing fails to return after the
bulation may resume with assistance; independent ambu- attack, and after many years, the symptoms of vertigo may
lation may be achie ved over the next few days. At the gradually diminish in frequenc y and se verity. Some
same time, the administration of v estibular suppressants patients may suddenly fall without warning; these events,
should be greatly diminished or , even better, stopped which may occur in later stages of the disease, are referred
completely because the y prolong the time required to to as Tumarkin’s otolithic crisis and should be differenti-
achieve central compensation. To further speed up the ated from other forms of drop attack.
process of recuperation, vestibular exercises challenge the The typical form of Ménière’s disease is sometimes
compensatory mechanisms of the central nerv ous not complete and is called vestibular Ménière’s disease, if
system (CNS), stimulating adaptation. These exercises only vestibular symptoms and aural pressure are present,
are designed to improve both gaze stability and postural or cochlear Ménière’s disease, if only cochlear symptoms
stability (see Chapter 22).15 and aural pressure are encountered.19
Animal experiments have shown that alcohol, pheno- The disease is about equally distributed between the
barbital, chlorpromazine, diazepam, and ACTH antagonists sexes and usually has its onset in the fourth to sixth
retard compensation; caffeine, amphetamines, and ACTH decades of life. However, there are reports of children as
accelerate compensation.16 Recently Strupp and coworkers young as 6 years of age with classical Ménière’s disease.20
performed, in 141 patients with v estibular neuritis, a About 15 percent of the patients have blood relatives with
prospective randomized trial of methylprednisolone, v ala- the same disease, suggesting genetic f actors. The inci-
cyclovir, and the two in combination within 3 days after the dence of bilateral involvement ranges between 33% after
onset of symptoms.17 The authors showed that methylpred- 10 years and 50% after 20 years.21
nisolone significantly improves the recovery of peripheral A phenomenon fundamental to the de velopment
vestibular function (from 39% in the placebo group to 62% of Ménière’s disease is endolymphatic hydrops. Whether
in the methylprednisolone group), whereas v alacyclovir endolymphatic hydrops itself is the cause of the symptoms
does not. The study sho ws that steroids signif icantly characteristic of Ménière’s disease or whether it is a patho-
improve the recovery of peripheral vestibular function in logical change seen in the disease is still unclear . The
humans with v estibular neuritis. The recurrency rate of development of hydrops is generally a function of malab-
vestibular neuritis is very low (2% within 5 to 10 years) and sorption of endolymph in the endolymphatic duct and sac.
mostly then the other side is in volved. In the rare cases Malabsorption may itself be a result of disturbed function
of recurrence on the same side, this usually happens within of components comprising the endolymphatic duct and
6 months, but symptoms are milder.18 sac, mechanical obstruction of these structures, or altered
anatomy in the temporal bone. Endolymph is produced
Ménière’s Disease and primarily by the stria vascularis and flows both longitudi-
nally (along the axis of the endolymphatic duct toward the
Endolymphatic Hydrops endolymphatic sac) and radially (across the membrane of
Ménière’s disease is a disorder of inner ear function that the endolymphatic space into the perilymph system).
can cause devastating hearing and v estibular symptoms. Ménière’s disease is generally a consequence of altered
The typical attack is e xperienced as an initial sensation longitudinal flow, usually evolving over a course of many
of fullness of the ear, a reduction in hearing, and tinnitus, years. Experimental obstruction of the endolymphatic duct
followed by rotational v ertigo, postural imbalance, n ys- will routinely result in endolymphatic hydrops in man y
tagmus, and nausea and vomiting after a few minutes. This animal models.22 Lesions in the temporal bone that ha ve
severe disequilibrium (vertigo) will persist anywhere from been associated with the development of hydrops include
approximately 30 minutes to 24 hours. Gradually , the fractures of the temporal bone, perisaccular fibrosis, atro-
severe symptoms will abate, and the patient is generally phy of the sac, narro wing of the lumen in the endolym-
ambulatory within 72 hours. Some sensation of postural phatic duct, otitis media, otosclerotic foci enveloping the
unsteadiness will persist for days or weeks, and then vestibular aqueduct, lack of v ascularity surrounding the
3970_Ch04_049-058 25/06/14 11:28 AM Page 54
endolymphatic sac, syphilitic osteitis of the otic capsule, mistaken assumption that diminishing endolymphatic
and leukemic infiltrations, to name just a fe w. Anatomi- hydrops is possible by changing inner -ear blood flo w,
cally, ears af fected by Ménière’ s disease are lik ely to osmotic diuresis, or central sedation. There has never been
demonstrate hypodevelopment of the endolymphatic duct prospective proof of the efficiency of these therapies. The
and sac, periaqueductal cells, and mastoid air cells.There- histamine derivative betahistine has been advocated as the
fore, one can postulate a cause-and-effect relationship be- drug of first choice. Findings from a 1-year prospecti ve
tween constricted anatomy in the temporal bone and double-blind study showed that this treatment is preferable
malabsorption of endolymph. to leaving the disease untreated. 24 Recently, the recom-
Any explanation of the clinical symptoms of mended dosage has been continuously increased up to
Ménière’s disease should account for all the symptoms, 3*48 mg/day for at least 1 year.25 The action is attributed
including rapid or prolonged attacks of v ertigo, disequi- to improvement of microcirculation of the stria vascularis,
librium, positional vertigo during and between attacks, but betahistine also has inhibitory effects on polysynaptic
fluctuating progressive sensorineural hearing loss, tinnitus, vestibular neurons. Adjunct medications in the form of
aural pressure, inability to tolerate loudness, and diplacu- vestibular suppressants other than betahistine are to be
sis. These symptoms probably result from both chemical used primarily during the acute episodes of v ertigo and
and physical mechanisms. Physical factors can tamponade should be discouraged as a chronic daily medication. If
the cochlear duct, contributing to fluctuating progressive the betahistine treatment does not result in a signif icant
sensorineural hearing loss and other cochlear symptoms, reduction of vertigo attacks within 6 months, intratym-
whereas distension of the otolithic or gans can physically panic application of steroids can be tried.26 This procedure
affect the crista ampullaris, resulting in v estibular symp- proved to be ef fective; the e vidence level, however,
toms. The prolonged n ystagmus and v ertigo are com- is low.27
monly believed to be caused by periodic membrane In addition to pharmacologic therapies, man y
ruptures with subsequent transient potassium palsy of patients with Ménière’ s disease require psychological
vestibular nerve fibers. support to help cope with the frustrations and changes
Useful diagnostic tests include the audiogram and brought about by their medical condition. Those patients
ENG. Typically, the audiogram displays an ipsilateral sen- in whom the v ertigo becomes disabling by virtue of in-
sorineural hearing loss involving the lower frequencies. creased severity or frequency of attacks despite maximal
Fluctuation in discrimination scores is often seen, with a medical therapy would be considered candidates for sur-
long-term trend toward poor scores. ENG may demonstrate gical intervention. Only about 1% to 3% of patients ulti-
a unilateral vestibular weakness on caloric testing, again mately require surgical treatment, because the success of
involving the ear symptomatic for pressure, hearing loss, regular endolymphatic sac shunt operations has been
and tinnitus. Electrocochleography is useful in cases that shown to be a placebo effect.28
are unclear. The finding of enlarged summating potentials Sacculotomy has been proposed by a v ariety of
in the suspected ear is diagnostic of endolymphatic hy- authors as a method of relie ving the pressure b uildup
drops. Furthermore, Taylor and colleagues found, in 33% in the endolymphatic chamber. Long-term success rates
of patients with Ménière’s disease, pathological cervical for this procedure are not yet a vailable, but significant
vestibular-evoked myogenic potentials (cVEMP) indicat- hearing loss is observ ed in 50% of patients under going
ing a specific involvement of the saccule in this disease.23 cochleosacculotomy. Advantages are ease of performance,
A brainstem-evoked acoustic response (BAR) must utility in elderly patients as a f irst procedure under local
be done in those cases with f indings of retrocochlear anesthesia, and little risk other than hearing loss.
pathology on routine audiometry to screen for cochlear Intratympanic treatment with ototoxic antibiotics such
nerve or brainstem pathology. If the BAR is found to be as gentamicin sulfate, instilled via a plastic tube inserted
positive, then MRI scanning with the use of intra venous behind the annulus via the transmeatal approach, is ob vi-
gadolinium should be done to assess for central nerv ous ously able to damage selectively the secretory epithelium
system pathology or eighth-nerve schwannoma. (and thereby improve endolymphatic hydrops) before sig-
Treatment in the remission phase aims to reduce the nificantly affecting vestibular and cochlear function.29
frequency of the attacks and preserve hearing without dis- The current treatment most successful is v estibular
tressing tinnitus. Dietetic programs, including restriction nerve section. This procedure is indicated in indi viduals
of salt, water, alcohol, nicotine, and caf feine, are as val- with serviceable hearing in whom maximal medical ther-
ueless in treating the disease as are physical e xercise or apy has been unsuccessful in controlling vertigo. Success
avoidance of exposure to low temperatures. Stellate gan- rates in the range of 90% to 95% ha ve been reported by
glion blocks, diuretics, vasoactive agents, tranquilizers, numerous authors. The newer technique of focused ultra-
neuroleptics, and lithium have been employed under the sound seems to ha ve an advantage over open surgery in
3970_Ch04_049-058 25/06/14 11:28 AM Page 55
that partial ablation of vestibular function (with preserva- variability of signs and symptoms and the lack of a
tion of hearing) can be performed without in vading the pathognomonic test. In the acute phase, medical treatment
labyrinth. is universally recommended because these fistulas usually
In patients with hearing loss, destructive procedures heal spontaneously, and the results of sur gical interven-
are also possible, such as transmeatal, transmastoid, or tions are not encouraging.30
translabyrinthine labyrinthectomy. The success rate is Physical examination, particularly otoscopy, is im-
95%. An extension of this surgery is the translabyrinthine portant. In the cases of head trauma and barotrauma,
vestibular nerve section, shown to eliminate v ertigo in hemotympanum is often seen as an early finding. In cases
98% of cases. However, particularly in elderly patients, of penetrating injury to the ear, a tympanic membrane per-
ablative surgical procedures may cause long-lasting pos- foration makes the likelihood of ossicular discontinuity
tural imbalance because of the reduced ability of central with fistula very high. A useful clinical test consists of
mechanisms to compensate for the postoperative vestibu- applying manual pressure over the tragus or applying pres-
lar tone imbalance. sure to the tympanic membrane with the pneumatic oto-
Vestibular exercises are not appropriate in patients scope; a positi ve test is indicated by the e vocation or
with Ménière’s disease unless there is permanent loss of exacerbation of vertigo (Hennebert’s sign) or the elicita-
vestibular function. Vestibular exercises are designed to tion of nystagmus. Audiometric findings usually demon-
induce long-term changes in the remaining vestibular sys- strate a mixed or sensorineural hearing loss, depending on
tem or to foster the substitution of other strategies to com- the mechanism of injury. This loss may be quite se vere
pensate for the loss of v estibular function. In Ménière’s and usually involves the high frequencies more than the
disease, the vestibular dysfunction is episodic, and be- low frequencies. ENG with caloric testing may be normal
tween episodes the system usually returns to normal func- or show a unilateral weakness in the af fected ear. The
tion. Some patients developed a loss of vestibular function specificity of the clinical f istula tests can be augmented
at the end stages of the disease, and for those patients, by recording eye movements or measuring body sway as
vestibular rehabilitation may be appropriate. Vestibular ex- pressure on the tympanic membrane is increased. Despite
ercises are also beneficial in those patients who have sur- refinements, these tests remain unreliable in detecting all
gical destruction of the inner ear. fistulas. The diagnosis remains essentially a historical one,
and in those patients with a suggestive history and symp-
toms, treatment is indicated. Often the only manner
Perilymphatic Fistula in which the diagnosis is made def initively is at the time
Perilymphatic fistula may lead to episodic vertigo and sen- of surgical exploration by tympanoscopy as the patient
sorineural hearing loss owing to the pathological elasticity performs Valsalva maneuvers.
of the bony labyrinth. Most commonly, these fistulas occur Medical treatment consists of absolute bed rest with
at the round and oval windows of the middle ear. Classi- the head elevated for 5 to 10 days. Mild sedation with tran-
cally, a history of (often minor) head trauma, barotrauma, quilizers; avoidance of straining, sneezing, coughing, or
mastoid or stapes surgery, penetrating injury to the tym- head-hanging positions; and the use of stool softeners is
panic membrane, or vigorous straining precedes the onset important for reduction of further explosive and implosive
of sudden vertigo, hearing loss, and loud tinnitus. The forces that may activate perilymph leakage.31
patients often report a “pop” in the ear during the precip- When symptoms persist for longer than 4 weeks,
itating event. Later on, patients with fistula may complain or if hearing loss w orsens, exploratory tympanotomy is
of imbalance, positional v ertigo, and nystagmus as well indicated. Considerable controversy persists surrounding
as hearing loss. Tullio phenomenon—vestibular symptoms the frequency with which perilymph fistulas are found at
that include vertigo, oscillopsia, nystagmus, ocular tilt surgery. Surgical management consists of middle ear e x-
reaction, and postural imbalance induced by auditory ploration and packing of the oval and round window areas
stimuli—is usually the result of a perilymph f istula, in with fat, Gelfoam, and areolar and/or fibrous tissue. These
most cases because of superior canal dehiscence, b ut areas are pack ed whether or not a clear -cut fistula is
subluxation of the stapes foot plate and other ear pathol- demonstrated. Reported success rates for this treatment
ogy may be responsible. The symptoms will often subside vary between 50% and 70% and lik ely reflect some ele-
while at rest only to resume with activity. Sneezing, strain- ment of variable patient selection.
ing, nose blowing, and other such maneuv ers can elicit More recently, a new variant of perilymphatic fistula
the symptoms after the initial e vent. Perilymph fistulas causing episodic vertigo has been described by Minor and
probably account for a considerable proportion of those coworkers.32 The disease is a result of dehiscence of the
patients presenting with vertigo of unknown origin. Diag- superior semicircular canal. It is probably the most frequent
nosing perilymph fistula is difficult because of the great form of a f istula and probably most often o verlooked.
3970_Ch04_049-058 25/06/14 11:28 AM Page 56
Hallmarks are vertigo spells induced by pressure increase vestibular neuritis, cerebral hemosiderosis, ototoxic drugs,
like coughing, sneezing, or loud noises (T ullio phenome- inner-ear autoimmune disease, or congenital malformations,
non). Vertical-torsional eye movements in the plane of the but in many cases no clear cause can be found (idiopathic
defective superior semicircular canal can be observ ed bilateral vestibulopathy). Autoimmune conditions affecting
in precipitating conditions. Pf ammater and co workers the inner ear are rare b ut distinct clinical entities, 37 charac-
showed in a study with 27 patients that cVEMPs are typi- terized by a progressive, bilateral sensorineural hearing loss
cally altered in this disease.33 Depending on the size of the often accompanied by a bilateral loss of vestibular function.
dehiscence (≥2.5 mm) the stimulation threshold w as sig- Other autoimmune-mediated disease is often present in the
nificantly reduced and the amplitude of the cVEMPs w as afflicted patients; examples include rheumatoid arthritis,
increased. In more than half of the cases symptoms start psoriasis, ulcerative colitis, and Cogan’s syndrome (iritis ac-
after even mild head- or barotrauma. The diagnosis can be companied by vertigo and sensorineural hearing loss). The
made by high-resolution CT of the temporal bone showing history is the most useful diagnostic tool. Support for the di-
a dehiscence of the apical part of the superior semicircular agnosis can be obtained by blood testing for complete blood
canal. Very recently, posterior canal dehiscence and bilat- count, erythrocyte sedimentation rate, rheumatoid factor, and
eral and combined involvement of anterior and posterior antinuclear antibodies. Western-blot precipitation studies
canals have also been reported.34 to look for anticochlear antibodies can be done in some
research centers and may be the future def initive test of
Vestibular Paroxysmia (Disabling choice in these cases.
Little is kno wn about ho w autoimmune disorders
Positional Vertigo) cause otologic symptoms. As with other autoimmune con-
Neurovascular cross-compression of the root entry zone of ditions, the otologic symptoms may occur as a direct assault
the vestibular nerve can elicit disabling positional vertigo.35 by the immune system in the form of humoral and cellular
The term describes a heterogeneous collection of signs and immunity directed at the inner ear. Another mechanism of
symptoms rather than a reliable diagnosable disease entity. injury may be related to the deposition of antibody-antigen
Brandt and Dieterich 36 proposed the following criteria: complex in capillaries or basement membranes of inner ear
(1) short and frequent attacks of rotational or to-and-fro structures. Further immunologic studies of temporal bones
vertigo lasting from seconds to minutes, (2) attacks fre- harvested from deceased patients who had clinical evidence
quently dependent on particular head positions and modi- of autoimmune inner ear involvement may shed some light
fication of the duration of the attack by changing head on the underlying process.
position, (3) hypacusis and/or tinnitus permanent or during Because autoimmune vestibulopathy usually affects
the attack, (4) measurable auditory or vestibular deficits by both ears, therapy is almost exclusively medical. Vestibu-
neurophysiological methods, and (5) positi ve response to lar suppressants are most useful in controlling the more
antiepileptic drugs (carbamazepine). With a special MRI severe exacerbations of vertigo. The use of corticosteroids
technique (CISS-3D), vascular loops around the most prox- and some cytotoxic agents (cytoxan, methotrexate) has
imal part of the v estibular nerve (first 1.5 mm) can often been shown to provide relief in some patients. There is
be detected in this disorder , but there is a considerable some newer evidence to suggest that serum plasmaphere-
amount of false positive and false negative results. sis may play a more prominent role in controlling this dis-
Neurovascular cross-compression can cause local de- ease in the future. The natural history of the disease leads
myelinization of the root entry zone of the eighth nerv e. to eventual bilateral vestibular ablation. This end result is
Ephaptic transmission between bare axons or central almost inevitable unless the underlying process can be
hyperactivity initiated and maintained by the peripheral arrested with treatment or arrests spontaneously.
compression are the suggested mechanisms. Analogous to The most common toxic cause of acute v ertigo is
trigeminal neuralgia, antiepileptic drugs are the f irst ethyl alcohol. We know that positional changes exacerbate
choice of medical treatment of the condition before surgi- the vertigo of a hangover. The reason may be that alcohol
cal microvascular decompression is contemplated. diffuses into the cupula and endolymph at dif ferent rates
and so creates a density gradient, making the cupula sen-
sitive to gravity.38 Other agents that may produce vertigo
Bilateral Vestibular Disorders include organic compounds of hea vy metals and amino-
Bilateral vestibulopathy may occur secondary to meningitis, glycosides. The aminoglycosides are notorious for causing
labyrinthine infection, otosclerosis, Paget’s disease, polyneu- irreversible failure of vestibular function without vertigi-
ropathy, bilateral tumors (acoustic neuromas in neurofibro- nous warning or hearing loss. Thus, monitoring of vestibu-
matosis), endolymphatic hydrops, bilateral sequential lar function may be necessary during such therapy.
3970_Ch04_049-058 25/06/14 11:28 AM Page 57
Independent of vestibulopathies produced by ototox- by recruiting non vestibular sensory capacities such as
ins, single cases of “progressive vestibular degeneration” the cervico-ocular reflex and proprioceptive and visual
of unknown origin have been described, with the follow- control of stance and gait (see Chapters 9 and 23).
ing factors in common: repeated episodes of dizziness
relatively early in life, bilateral loss of vestibular function
with retention of hearing, and freedom from other neuro-
Summary
logical disturbances.39 This chapter describes the clinical presentation of the
Alport’s (inherited sensorineural deafness associated more common peripheral v estibular disorders and the
with interstitial nephritis), Usher’s (inherited sensorineural differential diagnosis to central origins of v ertigo.
deafness associated with retinitis pigmentosa), and Waar- Although the symptomatology of a certain peripheral
denburg’s syndromes (inherited deafness associated with vestibular disorder might be rather specific, as in acute
facial dysplasia) usually cause bilateral labyrinthine defi- unilateral vestibular loss, the cause can be rather differ-
ciency when they affect the vestibular system. Congenital ent, ranging from infection to ischemia to traumatic
vestibular loss is secondary to either abnormal genetic or lesions. A thorough evaluation, therefore, should, in ad-
intrauterine factors including infection (most commonly dition to the specif ic otoneurological in vestigation,
rubella and cytomegalovirus), intoxication (thalidomide), always include a detailed history and a general physical
or anoxia. examination. For a quick review, Table 4-1 summarizes
Controlled physical exercises can improve the con- the hallmarks of the peripheral v estibular disorders
dition in patients with permanent bilateral vestibulopathy treated in this chapter.
Bilateral
Vestibular Ménière’s Nerve Vestibular
BPPV Neuritis Disease Fistula Compression Disorder
Vertigo + + + + + –
Nystagmus + + + + + –
Nausea –/(+) + + – + –
Postural –/(+) + + + + ++
Ataxia
Specific Onset latency, Acute onset Fullness of Loud tinnitus, Frequent at- Gait ataxia
symptoms adaptation ear, hearing Tullio sign, tacks, tinni-
loss, tinnitus Hennebert’s tus, hypacusis
sign
CHAPTER 5
Vestibular Lesions
of the Central
Vestibular Pathways
Marianne Dieterich, MD ■ Thomas Brandt, MD, FRCP
Vestibular pathways run from the eighth nerv e and the Clinical Classification of Central
vestibular nuclei through ascending f ibers, such as the
ipsilateral or contralateral medial longitudinal fasciculus
Vestibular Disorders
(MLF), the brachium conjuncti vum, or the v entral The “elementary” neuronal network of the vestibular sys-
tegmental tract to the ocular motor nuclei, the supranu- tem is the di- or trisynaptic vestibulo-ocular reflex (VOR).
clear integration centers in the rostral midbrain, and the A useful simple clinical classification of central vestibular
vestibular thalamic subnuclei. From there the y reach syndromes is based on the three major planes of action of
several cortex areas through the thalamic projection. the VOR (Fig. 5.1): yaw, roll, and pitch.2-4
Another relevant ascending projection reaches the cor - The plane-specific vestibular syndromes are determined
tex from v estibular nuclei via v estibular cerebellum by ocular motor, postural, and perceptual signs as follows:
structures.
In the majority of cases, central v estibular vertigo • Yaw plane signs are horizontal nystagmus, past
syndromes are caused by dysfunction or a deficit of sen- pointing, rotational and lateral body falls, and
sory input induced by a lesion. In a small proportion of horizontal deviation of perceived straight-ahead.
cases, they are a result of pathological excitation of vari- • Roll plane signs are torsional nystagmus, skew
ous structures, extending from the peripheral v estibular deviation, ocular torsion, and tilts of head, body,
organ to the vestibular cortex. Because peripheral vestibu- and perceived vertical.
lar disorders are always characterized by a combination • Pitch plane signs are upbeat/downbeat nystag-
of perceptual, ocular motor, and postural signs and symp- mus, forward/backward tilts and falls, and verti-
toms, central v estibular disorders may manifest as cal deviations of perceived straight-ahead.
“a complete syndrome” or with only single components.
The defined VOR syndromes allo w for a precise
The ocular motor aspect, for e xample, predominates
topographic diagnosis of brainstem lesions as to their level
in the syndromes of upbeat or do wnbeat nystagmus.
and side, as follows (Fig. 5.2):
Lateral falls may occur without v ertigo in v estibular
thalamic lesions (thalamic astasia) or as lateropulsion in A tone imbalance in yaw indicates lesions of
Wallenberg’s syndrome.1,2 the lateral medulla, including the root entry
59
3970_Ch05_059-084 25/06/14 11:30 AM Page 60
zone of the eighth cranial nerve and/or the There is no primary vestibular cortex, but the parietoinsular
vestibular nuclei. vestibular cortex (PIVC)5 seems to act as a kind of main
A tone imbalance in roll indicates unilateral lesions integration center within a network of multisensory corti-
(ipsiversive at pontomedullary level, contraversive cal areas in the temporoparietal cortex. Dysfunction of this
at pontomesencephalic level). multisensory and sensorimotor cortex for spatial orienta-
tion and self-motion perception may be also in volved
A tone imbalance in pitch indicates bilateral
in spatial hemine glect and rare paroxysmal room-tilt
(paramedian) lesions or bilateral dysfunction
illusions, which belong to disorders of higher v estibular
of the cerebellum, especially the flocculus.
function.6
Most central vertigo syndromes have a specific locus
Some vestibular disorders are characterized by a si-
(Table 5-1) but not a specific etiology. The etiology may,
multaneous peripheral and central vestibular involvement.
for example, be vascular, autoimmunologic as in MS, in-
Examples are large acoustic neurinomas, infarctions of the
flammatory, neoplastic, toxic, traumatic, or degenerative.
anterior inferior cerebellar artery, head trauma, and syn-
dromes induced by alcohol intoxication. Others may affect
the vestibular nerve root in the brainstem, where the tran- Vestibular Disorders in (Frontal)
sition between the peripheral and central nervous systems
has been defined as the Redlich-Oberstein zone (lacunar
Roll Plane
infarction or focal demyelination in multiple sclerosis The “graviceptive” input from the otoliths converges with
[MS] mimicking vestibular neuritis). that from the v ertical semicircular canals (SCCs) at the
Cortical vestibular syndromes include v estibular level of the v estibular nuclei7 and the ocular motor
seizures and lesional dysfunction with tilt of the perceived nuclei8,9 to subserve static and dynamic vestibular func-
vertical, lateropulsion, and, rarely , rotational v ertigo. tion in pitch (up and down in the sagittal plane) and roll
3970_Ch05_059-084 25/06/14 11:30 AM Page 61
Figure 5.2 Vestibular syndromes in roll, pitch, and yaw planes: critical areas are schemati-
cally represented on the basis of our current knowledge of vestibular and ocular motor
structures and pathways, a lesion of which causes a vestibular tone imbalance in one of the
three major planes of action. The mere clinical sign of a vertical, torsional, or horizontal
nystagmus—if central-vestibular—allows a topographic diagnosis of the lesion, although
the particular vestibular structures involved are still under discussion. Whereas a vestibular
tone imbalance in the roll plane indicates unilateral brainstem lesions (a crossing in the
pons), vertical nystagmus indicates bilateral lesions. Two separate causative loci are known
for upbeat nystagmus, medullary and pontomesencephalic. Downbeat nystagmus indicates
a bilateral paramedian lesion of the commissural fibers between the vestibular nuclei or a
bilateral flocculus lesion. Horizontal nystagmus indicates unilateral pontomedullary lesions
involving the vestibular nuclei. The differentiation of vestibulo-ocular motor signs according
to the three major planes of action of the vestibulo-ocular reflex (VOR) and their mapping
to distinct and separate areas in the brainstem are helpful for topographic diagnosis and
for avoiding incorrect assignment of clinical signs to brainstem lesions identified with imag-
ing techniques. INC = interstitial nucleus of Cajal; MLF = medial longitudinal fasciculus;
VN = vestibular nucleus.3
Vestibular cortex Vestibular epilepsy Vestibular seizures are auras (simple or complex partial
(multisensory) multisensory seizures)
Nonepileptic cortical vertigo Rare rotatory vertigo in acute lesions of the PIVC
Continued
3970_Ch05_059-084 25/06/14 11:30 AM Page 62
Tilt of perceived vertical with body Vestibular tone imbalance in roll with acute lesions of
lateropulsion (mostly contraversive) the PIVC
Mesodiencephalic OTR (contraversive; ipsiversive if Vestibular tone imbalance in roll (integrator: OTR with
brainstem paroxysmal) INC lesions)
Mesencephalic Skew torsion (contraversive) Vestibular tone imbalance in roll with MLF lesions
brainstem
Tilt of perceived vertical, lateropul- Vestibular tone imbalance in roll with medial and/or
sion, OTR superior vestibular nuclei lesions
Transient room-tilt illusion Acute severe vestibular tone imbalance in roll or pitch
Familial episodic ataxia (EA1 with EA1 = autosomally dominant inherited potassium
myokymia and EA2 with vertigo) channelopathy
EA2 = autosomally dominant inherited calcium
channelopathy
OTR, perceived tilt of subjective Tone imbalance with ipsiversive or contraversive tilts
vertical caused by lesions of the uvula, flocculus, dentate
nucleus, and cerebellar hemispheric lesions
INC = interstitial nucleus of Cajal; MS = multiple sclerosis; OTR = ocular tilt reaction; riMLF = right medial
longitudinal fasciculus.
(lateral tilt in the frontal plane). In the “normal” position dynamic signs is not surprising if one considers the func-
in the roll plane, the subjecti ve visual vertical (SVV) is tional cooperation of otoliths and vertical SCCs owing to
aligned with the gravitational vertical, and the axes of the their neuronal convergence within “graviceptive” path-
eyes and the head are horizontal and directed straight ways. These signs and symptoms may be found in combi-
ahead. nation or as single components at all brainstem le vels.
Signs and symptoms of a v estibular dysfunction in Unilateral lesions of v estibulo-cerebellar structures
the roll plane can be deri ved from the de viations from (e.g., uvula, nodulus, and dentate nucleus) can also induce
normal function. A lesion-induced vestibular tone imbal- these signs in the roll plane.10,11 A systematic study of 111
ance results in a syndrome consisting of a perceptual tilt patients with acute unilateral brainstem infarctions showed
(SVV), vertical misalignment of the visual axes (skew de- that pathological tilts of SVV (94%) and ocular torsion
viation), ocular torsion, or a complete ocular tilt reaction (83%) are the most sensitive signs.12 Skew deviation was
(OTR; the triad of head tilt, sk ew deviation, and ocular found in one-third and a complete O TR in one-fifth of
torsion). these patients (Table 5-2). Similar frequencies were found
There is convincing evidence that all of the following in the cerebellar lesions.10,11
signs and symptoms reflect v estibular dysfunction in the Current clinical data support the follo wing topo-
(frontal) roll plane: graphic diagnostic rules based on v estibular signs and
symptoms in roll3,4,10,11,13 (Fig. 5.3):
• OTR
• Skew deviation (skew-torsion sign) 1. The fundamental pattern of eye-head tilt in
• Spontaneous torsional nystagmus roll—either complete OTR or skew torsion
• Tonic ocular torsion (monocular or binocular), if without head tilt—indicates a unilateral pe-
not caused by infranuclear ocular motor disorders ripheral deficit of otolith and vertical canal
• Tilt of perceived SVV (with binocular and input or a unilateral lesion of “graviceptive”
monocular viewing) brainstem pathways from the vestibular nuclei
• Body lateropulsion (crossing midline at lower pontine level) to
the interstitial nucleus of Cajal (INC) in the
Ocular motor or postural tilts, as well as maladjust- rostral midbrain and vestibulo-cerebellar
ments of SVV, point in the same direction, either clock- structures.
wise or counterclockwise (as seen from the vie wpoint of 2. Tilts of SVV, resulting from peripheral or cen-
the examiner). The direction of all tilts is reversed if patho- tral vestibular lesions from the labyrinth to the
logical excitation of unilateral “graviceptive” pathways is vestibular cortex, are the most sensitive signs
the cause of vestibular tone imbalance in roll rather than a of a vestibular tone imbalance in roll (~90%).
lesional input def icit. The combination of static and In the acute phase, tilts of SVV are more
3970_Ch05_059-084 25/06/14 11:30 AM Page 64
■ Table 5-2 FREQUENCY OF SUBJECTIVE VISUAL VERTICAL (SVV) TILT, SKEW DEVIATION,
OCULAR TORSION, AND OCULAR TILT REACTION (OTR) IN ACUTE UNILATERAL
BRAINSTEM AND THALAMIC INFARCTIONS
Lesion Patients (No.) SVV Tilt (%) Monocular Binocular Skew (%) OTR (%)
Mesodiencephalic
Brainstem
Mesencephalic 16 94 54 38 37.5 25
Pontomesencephalic 12 92 64 18 25 25
Pontine 34 91 47 33 26.5 12
Medullary (Wallenberg’s 36 94 27 55 44 33
syndrome)
pronounced in patients with lesions of the 5. Brainstem lesions ipsilateral to the vestibular
vestibular nuclei (Wallenberg’s syndrome) than nucleus, near the ascending medial lemniscus
in patients with vestibular neuritis.14 The remis- (ipsilateral vestibule-thalamic tract, IVTT), also
sion of the perceptual deficits over a period of induce isolated ipsilateral deviations of SVV
2 to 4 weeks is very similar in both diseases. without vertical divergence or ocular torsion.15
3. All tilt effects—perceptual, ocular motor, and 6. Depending on the damaged region of the
postural—are ipsiversive (ipsilateral eye low- cerebellum, unilateral lesions of the vestibulo-
ermost) and caused by unilateral peripheral cerebellum induce primarily contraversive
or pontomedullary lesions below the crossing (~60%) and more seldom (~25%) ipsiversive
of the “graviceptive” pathways. They indicate deviations.11 The structure most frequently
involvement of the labyrinth, vestibular nerve, impaired in cases of contraversive signs is the
or medial and/or superior vestibular nuclei; dentate nucleus.
the last are mainly supplied by the vertebral 7. Skew deviation is always combined with ocular
artery. torsion (skew-torsion sign). It manifests without
4. All tilt effects in unilateral pontomesen- head tilt if ascending pontomesencephalic “grav-
cephalic brainstem lesions are contraversive iceptive” pathways are affected rostral to the
(contralateral eye lowermost) and indicate in- downward branching of the vestibulospinal tract.
volvement of the MLF (paramedian arteries 8. Unilateral lesions of ascending vestibular path-
arising from basilar artery) or INC (parame- ways rostral to the INC typically manifest with
dian superior mesencephalic arteries arising deviations of perceived vertical without concur-
from the basilar artery). rent eye-head tilt.
3970_Ch05_059-084 25/06/14 11:30 AM Page 65
9. OTR in unilateral paramedian thalamic infarc- 11. Acute unilateral lesions of the PIVC and the
tions (in ~50%; paramedian thalamic arteries superior temporal gyrus cause moderate ip-
from basilar artery) indicates simultaneous siversive or mostly contraversive SVV tilts
ischemia of the paramedian rostral midbrain, lasting several days (temporal branches of the
including the INC. middle cerebral artery or deep perforators).16,17
10. Unilateral lesions of the posterolateral thala- 12. Some of the patients with lesions of the PIVC,
mus can cause thalamic astasia and moderate the superior temporal gyrus, the operculum,
ipsiversive or contraversive SVV tilts, thereby and the anterior insula simultaneously show a
indicating involvement of the vestibular thala- pusher syndrome.18 There is a positive correla-
mic subnuclei (thalamogeniculate arteries). tion between the extent of pushing and the
This generally resolves within a matter of days SVV deviation.19 This occurs more frequently
or a few weeks. with lesions of the right hemisphere (42%)
3970_Ch05_059-084 25/06/14 11:30 AM Page 66
than of the left hemisphere (25%) and indicates Repeated measurements on subsequent days sho wed a
a close correlation between the control of pos- gradual recovery, mostly within 30 days, both for OT and
ture and stance and the vestibular system. SVV (Fig. 5.5). Some patients, ho wever, maintained a
13. An SVV tilt found with monocular but not residual OT of a few degrees without a corresponding tilt
with binocular viewing is typical for a trochlear of SVV for up to 2 years.
or oculomotor palsy rather than a supranuclear
“graviceptive” brainstem lesion.20 Complicated
ocular motor syndromes are occasionally
induced in midbrain lesions by the combination
of a central vestibular deficit in the roll plane
(caused by the INC lesion) and a concurrent
nuclear or fascicular 3rd cranial nerve or 4th
cranial nerve palsy (“mixed pattern”).
Tilt effects caused by paroxysmal activation of
“graviceptive” pathways point in the opposite
direction to those caused by lesional inhibition,
such as unilateral infarction.21,22
Thus, all clinical signs of v estibular dysfunction in
roll can be helpful when one is determining not only the
level but also the side of the brainstem lesion. If the level
of damage is kno wn from the clinical syndrome, the
vestibular syndrome indicates the more severely affected
side. Conversely, if the side of damage is clear from the A
clinical syndrome, the direction of OTR, skew deviation,
and SVV tilt indicate the level on the brainstem.
Etiology
The two most common causes of tonic OTR are brainstem
ischemia (especially Wallenberg’s syndrome and unilat-
eral paramedian thalamic plus rostral mesencephalic in-
farctions) and brainstem tumors21,23 followed by unilateral
thalamic hemorrhages or lo wer brainstem hemorrhages
(cavernous angioma, lymphomas), se vere brainstem
concussion, MS, or in association with attacks of basilar
migraine.
The overlapping area of these infarctions centered on the induces a tonic contraversive deviation, and therefore a
posterior insula, which, according to functional imaging torsional nystagmus with the fast phases ipsilesional. The
studies,32-36 is homologous to the PIVC in monk eys, and same is true for a lesion of the INC. The only exception
the adjacent superior temporal lobe. 37,38 Further areas in- to these directional rules for tone imbalance along the
volved in the perception of verticality are the superior tem- vestibular graviceptive pathways is the riMLF, a lesion of
poral gyrus, the operculum, the anterior insula, and the which causes an (possibly non vestibular) ocular motor
inferior frontal gyrus.17 SVV tilts caused by vestibular cor- tone imbalance in the opposite direction.
tex lesions can also be associated with (a compensatory)
body lateropulsion. This finding may explain some cases Vestibular Disorders in (Sagittal)
of the cortical phenomenon “pusher” syndrome, 18 which
physical therapists readily recognize.
Pitch Plane
A striking difference between vestibular tone imbalance
in the roll and pitch planes is that roll dysfunction is
Torsional Nystagmus caused by unilateral, and pitch dysfunction by bilateral,
The “graviceptive” input from the otoliths converges with lesions of paired pathways in the brainstem or of the cere-
that from the vertical SCCs to subserve static and dynamic bellar flocculus.4 This structural difference probably ex-
vestibular function in roll. This combination of static and plains why a vestibular tone imbalance in pitch frequently
dynamic effects39 is not surprising if one considers ho w occurs with various intoxications, metabolic disorders, or
these functions are corroborated. Several studies on OTR, degeneration, which is unusual for tone imbalance in yaw
lateropulsion, and SVV were concerned with static effects or roll, unless as a functional decompensation of an earlier
of vestibular dysfunction in roll.11,12 These effects persist (compensated) tone imbalance. Do wnbeat nystagmus
for days to weeks, during which time they spontaneously (DBN) and upbeat nystagmus (UBN) are not merely ocu-
subside. In the acute stage of inf arction, additional dy- lar motor disorders but disorders that also affect orienta-
namic signs and symptoms occur, which consist of hori- tion and balance. A tone imbalance in the pitch plane
zontal rotational vertigo and torsional nystagmus.40,41 Fast manifests as vertical upbeat or downbeat nystagmus, fore-
phases of rotational nystagmus are contraversive in pon- aft head-and-body tilt, and de viation of the subjecti ve
tomedullary lesions, whereas the slow phases correspond straight-ahead toward the direction of the slo w phase of
in direction to the static deviation. the nystagmus.49
Several distinct and separate lesions (see Fig. 5.2) Despite the numerous clinical studies on UBN and
have been associated with torsional nystagmus: for exam- DBN as well as the many hypotheses proposed to explain
ple, lesions of the v estibular nuclei,41,42 the lateral their pathomechanism, so far the pathophysiology of these
medulla,40,43 in rare cases the MLF (as indicated by an as- disorders has not been clarified.50-54 There seem to be var-
sociation with internuclear ophthalmoplegia),44,45 the INC, ious forms of DBN responsible for different aspects of the
and the riMLF.46-48 Fast phases of torsional nystagmus are disorder. Several pathomechanisms that cause an instabil-
contraversive in pontomedullary lesions and ipsiversive in ity in the brainstem-cerebellar networks, which normally
paramedian pontine and mesencephalic (INC) lesions stabilize vertical gaze, are currently being discussed. F or
(rare exception: contraversive in riMLF lesion). example, an asymmetry
Jerk-waveform seesaw nystagmus (a torsional n ys-
• in the vertical neuronal integrator with a disorder
tagmus with elevation of the intorting eye and depression
of the saccade generator, which is conspicuous in
of the extorting eye) is induced by an inacti vation of the
excentric gaze positions;
INC in the rostral midbrain and is also ipsiversive.48
• in the central connections of the VOR for vertical
The different locations of lesions causing dif ferent
eye movements including the otolithic pathways,
directions of torsional nystagmus at first appear to be con-
which explains the frequent dependence on grav-
fusing. They can, ho wever, be e xplained by the tonic
ity; or
torsional shift of eye position along the graviceptive path-
• in the vertical gaze-pursuit system with sponta-
ways from the vestibular nuclei to the INC. A lesion of the
neous upward drift.
(medial or superior) vestibular nucleus causes an ipsiver-
sive tonic deviation (ipsiversive ocular torsion) with com- Here the flocculus/paraflocculus seems to play a spe-
pensatory fast phases of the torsional n ystagmus to the cial role, because its damage leads to a disinhibition of the
contralesional side. In view of the f act that the pathw ay vestibular pathways of the superior v estibular nucleus to
within the MLF crosses to the contralateral side, an MLF the oculomotor nucleus. This fits with findings from func-
lesion in the pontine and pontomesencephalic brainstem tional imaging studies which ha ve proven that patients
3970_Ch05_059-084 25/06/14 11:30 AM Page 69
with idiopathic DBN have a hypometabolism or a reduced the two. Reversals from UBN to DBN ha ve also been
activity in the flocculus/paraflocculus as well as in observed.61
the pontomedullary brainstem. 55-57 In contrast, structural Oscillopsia should be e xpected to cause an impair -
MRI found atrophies of the gray matter not in the floccu- ment of postural balance, because retinal image motion is
lus/paraflocculus but in the lateral portions of the cerebel- a major cue for body stabilization. Ho wever, this kind of
lar hemispheres (lob ule VI) and in the oculomotor “visual ataxia” cannot simply account for the typical pos-
vermis.57 tural imbalance, which is a striking feature of the fore-aft
Clinically, DBN occurs more commonly than UBN body sway and includes a tendency to fall backward. This
and is often permanent (as in idiopathic forms, cerebellar fore-aft postural instability can be interpreted to be a
degeneration, or Arnold-Chiari malformation),58,59 whereas direction-specific vestibulospinal (or cerebellar) imbal-
UBN is usually a transient phenomenon. Lesional sites for ance, because it can be observed when the eyes are closed.
UBN have been more precisely confirmed by clinical stud- We believe that the objecti ve measurable backward tilt
ies (bilateral lesions of the pontomesencephalic junction represents a vestibulospinal compensation in the direction
or the medulla) than those for DBN (bilateral pon- opposite to the perceived lesional “forward vertigo” that
tomedullary lesions or bilateral flocculus dysfunction). corresponds to downbeat nystagmus.63 When the eyes are
Transitions between UBN and DBN have been frequently open, a measurable visual stabilization of body sw ay is
described in paramedian pontomedullary lesions. Whereas preserved, but it does not sufficiently compensate for the
DBN is more typical for congenital craniocervical malfor- visual ataxia. In DBN (more aptly termed “downbeat nys-
mations (Arnold-Chiari malformation) and cerebellar de- tagmus syndrome”), the patient’ s pathological postural
generation, UBN is more typical for MS, bilateral sway with the eyes open depends on the direction of gaze;
brainstem ischemia (basilar artery thrombosis), or brain- it increases with increasing amplitude of the n ystagmus.
stem tumors. UBN and DBN in the primary position of Pathophysiologically, it is secondary to a combination of
gaze may be the result of v arious intoxications (without both vestibulospinal ataxia and reduced visual stabiliza-
structural lesion). tion of posture owing to the nystagmus.
Etiology
Downbeat Nystagmus Idiopathic cases occur most often (38%), degenerative dis-
Box 5-1 summarizes the information given in this chapter orders of the cerebellum in 20% of cases, vascular lesions
about the downbeat nystagmus/vertigo syndrome. in 9%, and malformations in 7%. The more seldom causes
Downbeat nystagmus in the “primary” gaze posi- like toxic drug damage, lesions in MS and paraneoplastic
tion, or more particularly on lateral gaze, is often syndromes, vestibular migraine, vitamin B12 and thiamine
accompanied by oscillopsia and postural instability. This deficiencies, or traumatic and hypoxic injuries occur in
is a clearly defined and, depending on the lesional site, decreasing frequency.58,59
permanent association of symptoms, which often indi- Nutritional cerebellar syndromes owing to thiamine
cates structural lesions of the paramedian craniocervical deficiency, in particular alcoholic cerebellar de generation
junction. DBN is present in darkness and with fixation; (see Box 5-1), not only cause a typical 3-Hz fore-aft oscil-
slow-phase velocity and amplitude increase on lateral lation of body sw ay but also DBN. 59,64-66 Antiepileptic
gaze or with head e xtension or head movements in the drugs, especially phenytoin and carbamazepine, can pro-
sagittal (pitch) plane. It may be present only on do wn- duce a reversible DBN with associated cerebellar signs, de-
ward or lateral gaze. Slow-phase velocity is not consis- pending on the dosage of the drugs. Other rare causes are
tently related to vertical gaze and, contrary to Alexander’s lithium toxicity, 64 felbamate intoxication,67 toluene abuse,68
law, may even be maximal on upward rather than down- and severe magnesium depletion.69 Other conditions asso-
ward gaze. Nystagmus is a jerk, usually with linear slow ciated with DBN are MS,70 familial periodic ataxia, tumors
phases. It may exhibit changes of exponential velocity in of the posterior fossa, cerebellar de generation,71 paraneo-
slow phases, both increasing and decreasing. plastic cerebellar degeneration,72 infratentorial vascular dis-
It has been reported that re versals from DBN to eases such as dolichoectasia of the vertebrobasilar artery,73
UBN can be provoked by upward gaze deviation,60 con- hematomas, cavernomas, syringobulbia,74 and encephalitis
vergence,61 or transitions from sitting to supine position.62 (see Box 5-1).
DBN and UBN may be the directional counterparts of a
vestibular tone imbalance in the pitch plane. The close Management
proximity of the areas causing either UBN or DBN in the DBN caused by drugs, magnesium depletion, or vitamin
medulla agrees with the directional changes between B12 deficiency is usually reversible when the intoxication
3970_Ch05_059-084 25/06/14 11:30 AM Page 70
Box 5-1
or metabolic deficiency is reversed. DBN caused by struc- performed before and ~60 minutes after the first ingestion
tural lesions in the posterior fossa is usually permanent. It of 5 mg 4-aminop yridine to promptly detect an y length-
is therapeutically expedient to try to treat the symptoms ening of the QT interval.76 This is so far a single, nonstan-
of persisting DBN with v arious drugs. In recent years dard therapeutic attempt.
the potassium channel blockers 3,4-diaminopyridine and Because UBN generally slo wly resolves after an
4-aminopyridine have been proven to have a positive ef- acute occurrence, therapy for its symptoms is often not
fect, above all in DBN and also in single cases of UBN.75-78 necessary. In cases of v ery disturbing oscillopsias due
For this reason a therapeutic attempt can be made with to large amplitudes of UBN and in DBN, one can try
5 to 10 mg 4-aminopyridine, 3 times a day (or 10 mg, once 4-aminopyridine (5 to10 mg, three times a day orally), 80
or twice a day in the sustained release form) for DBN memantine (10 to 20 mg, twice a day), 81,82 or gabapentin
(Fig. 5.6). (300 to 600 mg twice a day). 82 If both are inef fective,
Animal experiments have shown that administration one can try baclofen (5 to 10 mg twice a day orally).2
of aminopyridines can increase the resting-state acti vity
and excitability of Purkinje cells 79 and thus improve the
Upbeat Nystagmus (Upbeat Nystagmus
reduced inhibitory GABA-mediated influence of the cere-
Syndrome)
bellum on the superior vestibular nuclei. Because epileptic
attacks or heart rhythm disorders—especially at higher Box 5-2 summarizes the information given in this chapter
dosages—can occur in rare cases, an ECG should be about the upbeat nystagmus syndrome.
3970_Ch05_059-084 25/06/14 11:30 AM Page 71
–5
–10
0 5 10 15
Time (sec)
Up 10
Eye Position (°)
5 3,4-DAP
–5
–10
0 5 10 15
E Time (sec)
Figure 5.6 Effect of 3,4-diaminopyridine on downbeat nystagmus (DBN): influence of
3,4-diaminopyridine (3,4-DAP) on the mean slow phase velocity of DBN (measured with 2D
videooculography). The graphs a-d show the mean slow phase velocity of DBN for each individ-
ual patient. (A) Controls vs. 3,4-DAP, (C) controls vs. placebo. Both graphs (B) and (D) show a
so-called box plot with mean value, median, and 50 percentile as well as standard deviation for
controls vs. 3,4-DAP (B) and controls vs. placebo (D). 3,4-DAP reduced the maximal velocity of
the slow phase of DBN from 7.2 to 3.1 deg/sec 30 min after ingestion of 20 mg 3, 4-DAP
(p < 0.001). (E) shows an original recording of vertical eye position before (top) and 30 min after
(bottom) ingestion of the medicine. (From Strupp et al, 2003,75; with authors’ kind permission.)
3970_Ch05_059-084 25/06/14 11:30 AM Page 72
Box 5-2
Pathomechanism Management
Several hypotheses under discussion: Tone imbal- Medical treatment with 4-aminopyridine, baclofen
ance caused by lesions of the pathways mediating (clonazepam)
(1) signals of the vertical cerebello-vestibular Physical exercise (eye movements and balance training)
neural integrator; (2) central connections of the
vertical VOR, including both the vertical semicir- Differential Diagnosis
cular canal and otolith responses (pitch plane); Acquired pendular nystagmus, gaze-evoked nystagmus,
or (3) signals of the vertical smooth pursuit downbeat nystagmus, spasmus nutans (infants), ver-
system tical congenital nystagmus, reversed ocular bobbing
UBN in the primary position of gaze with concomi- probably indicate bilateral lesions of the pathways me-
tant oscillopsia and postural instability is a pendant of diating (1) signals of the v ertical cerebello-vestibular
DBN and probably reflects either an imbalance of v er- “neural integrator,” (2) the central connections of the
tical VOR tone49 or a downward ocular drift by asym- vertical VOR, or (3) signals of the v ertical smooth-
metrical smooth pursuit commands.50-54 It has the same pursuit system. UBN arising from pontomesencephalic
causes and involves central eye-head coordination in the lesions could result from damage of the superior
pitch plane as mediated by pathw ays from the v ertical vestibular nucleus–ventral tegmental tract pathw ay
SCCs and the otoliths. Because in some cases the man- coursing through the ventral pons and transmitting e x-
ifestations are typically modulated by otolithic input citatory upward vestibular signals to the third nerv e
arising from static head tilt, UBN can in a broader sense nucleus.54 This would lead to an imbalance between
also be a kind of positional nystagmus. As distinct from downward and upward systems and in a downward slow
DBN, brainstem lesions are often found in patients with phase. UBN in lesions af fecting the caudal medulla
UBN. Two separate intra-axial brainstem lesions in the could result from damage in a feedback loop in volved
tegmentum of the pontomesencephalic junction and in in upward gaze-holding.54
the medulla near the perihypoglossal nuclei (Fig. 5.7)
are likely to be responsible for this syndrome, but there Etiology
is insufficient evidence to determine whether the cere- UBN was observed in 26 of 17,900 patients e xamined at
bellar vermis is involved. In analogy to DBN, UBN can a neurotological clinic in Japan. The incidence rate w as
3970_Ch05_059-084 25/06/14 11:30 AM Page 73
Figure 5.7 Partial suppression of upbeat nystagmus by medical treatment with baclofen.
(Top) Vertical electronystagmography recordings. (Bottom) Magnetic resonance image of a
patient with unilateral upbeat nystagmus and a paramedian medullary infarction affecting the
area of PMT neurons near the neurons of the perihypoglossal nuclei.
3970_Ch05_059-084 25/06/14 11:30 AM Page 74
0.145%.83 The etiology of UBN is in general similar to of the eyes, past pointing, rotational and lateral body falls,
that of DBN (see Box 5-2). Malformations of the cranio- and horizontal nystagmus.
cervical junction and cerebellar de generation seem to be Central vestibular syndromes manifesting purely
less common than in DBN, whereas brainstem tumors and in the yaw plane occur less frequently than those caused
MS are more common. UBN can be associated with bilat- by imbalance in the pitch and roll planes, for tw o rea-
eral (paramedian) vascular brainstem lesions, hematoma, sons.4 First, the area of a lesion that can cause a tone
cavernoma, MS, encephalitis, abscess, or head injury . It imbalance in ya w is comparati vely small (root entry
has been repeatedly reported in alcoholic de generation, zone of the v estibular nerve, medial and superior
especially in Wernicke’s encephalopathy84 and in single vestibular nuclei, and the adjacent inte gration center
cases of Fisher’s syndrome,85 central diabetes insipidus,86 for horizontal eye movements—the paramedian pontine
and Pelizaeus-Merzbacher disease, 87 and has even been reticular formation [PPRF]). In contrast, the area of a
associated with middle ear disease. 88 We have seen tran- lesion that can cause v estibular tone imbalance in
sient upbeat nystagmus associated with various intoxica- roll or pitch co vers nearly the entire brainstem from
tions, for example, with antiepileptic drugs. UBN can on the medulla to the rostral midbrain (see Fig. 5.2). The
rare occasions be congenital.89 larger extent of the latter area is a result of the greater
separation of the vestibular nuclei and the ocular motor
Management integration centers for vertical and torsional eye move-
UBN may be associated with se vere vertigo, ataxia, and ments (riMLF and INC). Second, the area of a lesion
nausea, particularly at first. Affected patients may require that can theoretically cause a pure tone imbalance in the
vestibular sedatives (e.g., dimenhydrinate or scopolamine) yaw plane adjoins and o verlaps areas subserving
as long as nausea lasts. Depending on the etiology , the vestibular function in roll and pitch (see Fig. 5.2).There
natural history of this sign usually shows gradual improve- is a multisensory convergence within the parallel neural
ment or disappears, in contrast to DBN, which is fre- network of the v estibular nuclei,92 a lesion of which
quently permanent. Physical e xercise involving fixation, will cause mixed vestibular syndromes in more than one
eye movements, and postural balance accelerates central plane. A study of vestibular nuclei lesion in the monkey
compensation. Medical treatment is possible with baclofen demonstrated a combined n ystagmus: its horizontal
(5 to 10 mg PO daily), which has a benef icial effect on component beat toward the contralateral side after ros-
nystagmus amplitude, oscillopsia, and visual acuity in tral lesions and to ward the ipsilateral side after caudal
some patients (see Fig. 5.7).90 Carbamazepine was found lesions.93
to be ef fective in a single case of upbeat n ystagmus Some of the cases described as central v ariants of
caused by MS. 91 In single patients with UBN, Glasauer vestibular neuritis94-97 caused by lesions of the medial
and colleagues80 have shown that 4-aminopyridine re- vestibular subnucleus or the root entry zone of the vestibu-
duced the peak slow-phase velocity in light from 8.6 to lar nerve were probably not restricted to the ya w plane,
2.0 deg/sec, but UBN in darkness was not affected. These because the case descriptions also contain signs and symp-
investigators concluded that 4-aminopyridine reduces the toms of VOR tone imbalance in other planes of action.
downward drift in UBN by augmenting smooth pursuit There have been frequent reports that cerebellar inf arc-
commands. tions caused by occlusion of the anterior inferior cerebellar
artery (which may also supply the rostral vestibular nuclei)
Summary also mimic vestibular neuritis.98-100 The other main cause
of confusion with disorders at the entry zone of the eighth
These studies in UBN and DBN sho w that a new thera- cranial nerve is MS.95
peutic principle has been de veloped: aminopyridines, as Vestibular syndromes, when caused by unilateral
potassium channel blockers that increase the activity and pontomedullary lesions, commonly result in combined
excitability of Purkinje cells, ha ve a beneficial effect on vestibular tone imbalance in more than one plane, such
several disorders. as a combination of torsional and horizontal nystagmus.
This tone imbalance may manifest not only in sponta-
Vestibular Disorders in neous nystagmus but also in spontaneous or gaze-
evoked ocular deviations. There may be an inappropriate
(Horizontal) Yaw Plane horizontal ocular deviation during attempted v ertical
The clinical signs, both perceptual and motor, of a vestibu- saccades (lateropulsion in Wallenberg’s syndrome) or
lar tone imbalance in the yaw plane include rotational ver- an inappropriate torsional de viation during attempted
tigo, deviation of perceived straight-ahead, lateropulsion horizontal saccades.
3970_Ch05_059-084 25/06/14 11:30 AM Page 75
Vestibular Cortex: Locations, 7 in the inferior parietal lobule,113 and the ventral intra-
parietal area (VIP) in the fundus of the intraparietal
Functions, and Disorders sulcus.114-117 In view of the strong interconnections
The two major cortical functions of the v estibular sys- between PIVC and the other v estibular cortex areas
tem are spatial orientation and self-motion perception. (mainly 3aV and 2v) as well as the vestibular brainstem
These functions, however, are not specifically vestibular; nuclei, Guldin and Grüsser 5 postulate that it is the
they also rely on visual and somatosensory input. All core region within the vestibular cortical system in the
three systems—vestibular, visual, and somatosensory— monkey. About 50% of the neurons in this re gion re-
provide redundant information about the position and spond to vestibular stimulation in addition to somatosen-
motion of the body relati ve to the e xternal space. sory, optokinetic, or visual stimulation. This area is
Although the v estibular cortex function is distrib uted involved in the processing not only of v estibular, so-
among several multisensory areas in the parietal and tem- matosensory, and visual information that is generated
poral cortices, it is also integrated in a larger network for whenever the position of the body changes in relation
spatial attention and sensorimotor control of e ye and to the extra-personal space5 but also of that generated
body motion in space. when stationary human subjects perform optokinetic
The term “disorders of higher visual function” is nystagmus.118,119 Not only do most of these cortical
well established in neuro-ophthalmology. It usually cor- areas receive bilateral vestibular input from the vestibu-
relates circumscribed supratentorial especially cortical lar nuclei, the y in turn directly project do wn to the
lesions with particular dysfunctions of “higher visual vestibular nuclei.5,120,121 Thus, corticofugal feedback
perception,” recognition, and memory as well as spatial may modulate vestibular brainstem function.
orientation along the ventral and dorsal streams.101 Anal- Our knowledge about vestibular cortex function in
ogously one could also def ine disorders of higher humans is less precise. It is derived mainly from stimula-
vestibular function.2 These disorders are characterized tion experiments reported anecdotally in the older litera-
by complex perceptual, sensorimotor, and behavioral cri- ture and from later brain acti vation studies with positron
teria that exceed the basic perceptions like body motion emission tomography (PET) 30,35,122 or functional mag-
and motor responses as well as the vestibulo-ocular and netic resonance imaging (fMRI)32-34,36,118 and lesion stud-
vestibulo-spinal reflexes. There are differences and sim- ies.17,31 The areas in humans that were acti vated during
ilarities between these higher vestibular/visual disorders. caloric or electric v estibular stimulation were located in
A typical difference is that higher v estibular disorders the posterior insula (first and second long insular gyri) and
often involve other sensory modalities, whereas higher retroinsular regions (representing PIVC and the posterior
visual disorders do not. Similarities are that both mani- adjacent visual temporal sylvian area [VTS] in the mon-
fest with cognitive disturbances of spatial orientation, key), the superior temporal gyrus, operculum, the parts of
attention, spatial memory, and navigation. Sometimes, the inferior parietal lobule representing area 7 in monkey,
however, it is not possible to differentiate between them. the depth of the intraparietal sulcus representing monkey
This becomes evident in syndromes lik e visuo-spatial area VIP, the postcentral and precentral gyrus, the anterior
hemineglect102,103 or the room tilt illusion with transient insula and adjacent inferior frontal gyrus, the anterior cin-
episodes of “upside-down vision” induced by a vestibu- gulate gyrus, the precuneus, and hippocampus most often
lar tonus imbalance. 104-106 Not all disorders of higher bilaterally (Fig. 5.8). Simultaneous with these signal
vestibular function are caused by lesions of central increases (activations), signal decreases (deacti vations)
vestibular structures. Peripheral bilateral vestibular loss, of areas within the visual and somatosensory systems of
for example, not only causes oscillopsia and postural both hemispheres were observ ed.32,123 Because opposite
imbalance due to insuf ficient vestibulo-ocular and “activation-deactivation” patterns occurred during visually
vestibulo-spinal reflexes; it also impairs spatial memory induced self-motion perception with activations of parietal
and navigation because of a lack of v estibular input to visual cortex areas and concurrent deacti vations of the
the hippocampal formation. multisensory (vestibular) cortex,118,124 a reciprocal in-
Animal studies have identified several distinct and hibitory cortical interaction between the sensory systems
separate areas of the parietal and temporal cortices that was assumed.124
receive vestibular afferents, such as area 2v at the tip of Activation of the cortical netw ork during vestibular
the intraparietal sulcus,107-109 area 3aV (neck, trunk, and stimulation is not symmetrical in the tw o hemispheres.
vestibular region of area 3a) in the central sulcus, 110 Rather, it depends on three determinants that could be
PIVC at the posterior end of the insula and retroinsular defined in a 2003 study in vestigating healthy right- and
regions, 37,38,111 the periarcuate cortex area 6 pa,112 area left-handers.35 The determinants were (1) the subjects’
3970_Ch05_059-084 25/06/14 11:30 AM Page 76
Right-handers Left-handers
Right-handers
A B
Figure 5.8 (A) Areas activated during caloric stimulation (warm water at 44°C) of the
right ear in right-handed, and of the left ear in left-handed, healthy volunteers (group
analysis ; n = 12; P < 0.001; 15O-labeled H2O bolus, positron emission tomography). Acti-
vations were located in the anterior and posterior insula, the superior temporal gyrus, the
inferior frontal gyrus, the postcentral gyrus, the inferior parietal lobule, and the anterior
cingulum. Note that the activations were more pronounced in right-handers during irriga-
tion of the right ear in the right hemisphere and in left-handers during irrigation of the
left ear in the left hemisphere. This finding indicates dominance of the nondominant
hemisphere in the processing of vestibular information. (B) Lateral views of the surfaces of
both hemispheres showing activated areas during caloric stimulation of the right or left
ear in right-handers in the superior temporal cortex, temporoparietal junction, insular cor-
tex, and inferior frontal cortex. Compared with the activation pattern during caloric irriga-
tion of the right ear, caloric irrigation of the left ear led to activations that were smaller in
both hemispheres and more frequently located within the ipsilateral left hemisphere.
These results represent dominance of the ipsilateral vestibular pathways. (Modified from
Dieterich et al, 2003,35 and Bense et al, 2003125).
handedness, (2) the side of the stimulated ear, and (3) the relevant cortical area for the processing of v estibular
direction of the induced vestibular symptoms. Activation information was located in the posterior insula bilaterally,
was stronger in the nondominant hemisphere, in the hemi- right significantly more than left, including the PIVC. 127
sphere ipsilateral to the stimulated ear , and in the hemi- Recently, a meta-analysis of vestibular stimulation studies
sphere ipsilateral to the f ast phase of v estibular caloric showed convergent activation in a region near the posterior
nystagmus.30,35,126 Furthermore, in right-handed healthy insula, the right posterior operculum (OP2), embedded
volunteers, who performed allocentric visuospatial judg- in a joint v estibular network that seems to represent
ments (line bisection) with and without galv anic the human homologue to the v estibular area PIVC as
stimulation of the right or left v estibular nerve, the most proposed in nonhuman primates.128
3970_Ch05_059-084 25/06/14 11:30 AM Page 77
Studies showing that vestibular (caloric) stimulation textbooks, for example, those by Bumk e and Foerster162
significantly improved spatial functioning ha ve stressed and Penfield and Jasper,153 or from review articles.163,164
the important role of the vestibular system in neglect.148,149 In a later study searching for the human representa-
When vestibular stimulation w as combined with neck tion of “vestibular cortex,” Kahane and associates165 ret-
muscle vibration, the horizontal de viation combined lin- rospectively investigated patients with epilepsy who had
early, adding or neutralizing the ef fects observed during undergone stereotactic intracerebral electroencephalo-
application of both types of stimulation.131 This study also gram recordings before sur gery and looked for patients
showed that the patients with neglect displaced subjective in whom an illusion of rotation w as induced. The inves-
body orientation ipsilesionally, a behavior that does not tigators stimulated at 44 different loci in the temporal and
result from a disturbed primary perception or disturbed parietal cortex and found that electrical stimulation of an
transmission of the vestibular or proprioceptive input from area in the temporo-peri-Sylvian corte x particularly
the periphery. Karnath and associates132,133 argued that the elicited rotatory sensations. This area included Brodmann
transformation process converting the sensory input coor- areas 40, 21, and 22. Of these, the superior temporal
dinates from the periphery into egocentric (body-centered) gyrus (STG) and middle temporal gyrus (MTG) prefer-
coordinates is the critical mechanism leading to hemine- entially caused illusions of rotation around the subjects’
glect. This process must involve multisensory integration yaw axis, whereas the parietal operculum elicited pitch
and motor behavior, including eye and hand mo vements plane illusions. Kahane and associates165 thus confirmed
as well as walking trajectory.150 Spatial hemineglect also earlier findings by Penfield and coworkers,153,166,167 who
includes the back space of the body.151 had observed sensations of dizziness and rotary bodily
movements especially during electrical stimulation of the
STG in epileptic patients.
Vestibular Epilepsy Epileptic nystagmus usually beats contraversive to the
Vestibular epilepsy (vestibular seizures or auras) is a rare seizure focus and may be of vestibular, visual (optokinetic),
cortical vertigo syndrome secondary to focal epileptic dis- or cortical ocular motor origin.168
charges in either the temporal lobe or the parietal associ-
ation cortex152-154; multiple areas of both receive bilateral Management
vestibular projections from the ipsilateral thalamus. Vestibular seizures respond to antiepileptics. First-line
If vestibular seizures arise from dif ferent areas, the drugs are levetiracetam, sodium valproate, carbamazepine,
sensorimotor symptomatology may differ as regards ap- and lamotrigine. If necessary and possible, sur gical pro-
parent rotation or tilt, 155 with or without associated e ye, cedures may be considered.
head, and body deviation or epileptic nystagmus. Clinical
data on the directions of apparent self-motion or surround- Paroxysmal Central Vertigo
motion are mostly incomplete and imprecise. If the de-
Nonepileptic paroxysmal vertigo or other vestibular syn-
scription is e xact, as in rotatory seizures (“v olvular
dromes may result from pathological excitation of various
epilepsy”), then the topographic localization of the under-
vestibular structures.169 Most of them occur in MS, b ut
lying pathology is too ine xact to permit its allocation to
others may be associated with a brainstem abscess (parox-
known vestibular areas.
ysmal OTR) or an arteriovenous malformation with pre-
An acute unilateral functional deficit of the vestibular
vious bleeding (repetiti ve paroxysmal n ystagmus and
cortex (e.g., in medial cerebral artery inf arction) rarely
vertigo42) or brainstem infarction.
manifests with vertigo,156-158 unlike lesions in the vestibu-
The following manifestations of paroxysmal vestibu-
lar area of the brainstem. It is not the functional loss b ut
lar syndromes of the brainstem ha ve been described
the focal discharge that causes central v ertigo. This has
in MS:
been repeatedly demonstrated by stimulation experiments.
Electrical stimulation of the human thalamus during • Paroxysmal dysarthria, ataxia, and vertigo170
stereotactic neurosurgical procedures induced sensations • Paroxysmal OTR171
of movement in space, most frequently described as hori- • Paroxysmal room-tilt illusion172
zontal or v ertical rotation or sensations of f alling or
rising.159 These sensations were similar to those induced Central Vestibular Falls Without Vertigo
by stimulation of the vestibular cortex.152,153 There are a fe w instances of what is probably central
Vertigo has long been considered a manifestation of vestibular dysfunction. In such cases, patients without pare-
epileptic auras.160,161 Most information on auras (vestibular sis or sensory or cerebellar deficits are unable to main-
epilepsy), including case descriptions, comes from older tain an unsupported upright stance. They do not, however,
3970_Ch05_059-084 25/06/14 11:30 AM Page 79
complain of v ertigo. Their conditions include thalamic We hypothesized that the subjective vertigo is missing
astasia, lateropulsion in Wallenberg’s syndrome or in PIVC in patients with this syndrome (despite a striking tendenc y
lesions, and ocular-tilt reaction in pontomedullary or rostral to fall sideways) because individual multisensory postural
midbrain lesions. regulation is adjusted to the deviated vertical. Lateropulsion
then represents postural compensation of an apparent body
Thalamic Astasia tilt contraversive to the lesioned side. Despite the resulting
Postural imbalance with a transient tendenc y to fall has postural imbalance and the conflicting true vertical, the body
been noted after therapeutic thalamotomy.173-175 It has been is continuously adjusted toward what the central nerv ous
attributed to muscle hypotonia or ne glect and has also system erroneously computes as vertical.23,181 This hypoth-
been observed after thalamic inf arctions176 and hemor- esis could explain why patients fall without vertigo or warn-
rhages.28,177 Masdeu and Gorelick27 described 15 patients ing signals from the multisensory spatial orientation system.
with “thalamic astasia,” in the absence of motor weakness, These deficits are centrally compensated during se veral
sensory loss, and cerebellar signs, as a result of lesions of months via brainstem-cerebellar loops. 26 Lateropulsion
different causes, all primarily involving superoposterolat- without hemiparesis also occurs in cortical lesions. Patients
eral portions of the thalamus but sparing the rubral region. with infarctions of the middle cerebral artery territory are
“Typically, when asked to sit up, rather than using the axial well known to physiotherapists, who call them “pushers.” It
muscles, these patients would grasp the side rail of the bed has been demonstrated that acute lesions of the PIVC cause
with the unaffected hand or with both hands to pull them- contraversive tilts of the perceived visual vertical,31 making
selves up.”27 Thalamic astasia is transient and lasts for days it likely that the cortical lateropulsion can also be caused by
or weeks, with the dorsothalamic region being the critical a vestibular tone imbalance in the roll plane.
locus. Because posterolateral thalamic inf arctions cause Lateropulsion in both dorsolateral medullary lesions
tilts of the perceived vertical that are either ipsi versive or and posterior insular lesions spontaneously reco vers
contraversive,24,30 thalamic astasia and tilts of percei ved within days to weeks. 181 The recovery process might be
vertical may both reflect a v estibular tone imbalance. facilitated by physical therapy.
Furthermore, what Masdeu and colleagues 29 described as
astasia and gait f ailure with damage of the pontomesen-
cephalic locomotor region involving the right pontine pe-
Summary
duncle area may be associated with vestibular dysfunction Central vestibular syndromes are characterized by ocular
in roll. Their patient presented with a contra versive skew motor, postural, and perceptual signs. In a simple clinical
deviation of 10 degrees. classification they can be separated according to the three
Thalamic hemiataxia differs from thalamic astasia major planes of action of the VOR: yaw, roll, and pitch. A
and rarely occurs in isolation; it is usually associated with tone imbalance in yaw is characterized by horizontal nys-
hemisensory loss without hemiparesis 178 or hemisensory tagmus, lateropulsion of the eyes, past-pointing, rotational
loss and hemiparesis. 179 The lesions involve the ventral and lateral body falls, and lateral deviation of the perceived
lateral nucleus of the thalamus and the adjacent posterior straight-ahead. A tone imbalance in roll is defined by tor-
limb of the internal capsule and the mid- to posterior thal- sional nystagmus, skew deviation, ocular torsion, and tilts
amus containing the dentatorubrothalamic and ascending of head, body, and the perceived vertical. Finally, a tone
pathways.178,179 imbalance in pitch can be characterized by some forms of
upbeat or downbeat nystagmus, fore-aft tilts and falls, and
vertical deviation of the perceived straight-ahead. The thus
Lateropulsion in Wallenberg’s defined syndromes allow for a precise topographic diag-
Syndrome nosis as regards their level and side. Most signs and symp-
Lateropulsion of the eyes and the body is a well-known toms of central vestibular disorders resolve spontaneously
transient feature of dorsolateral medullary inf arction. within weeks to months owing to either recovery of the le-
Affected patients have irresistible, ipsiversive falls but sion or central compensation and substitution. The predom-
generally no subjective vertigo. Different brainstem le- inantly benign course of these syndromes may be
sions from midbrain to medulla cause ipsi versive devi- facilitated by physical and drug therapy.
ation of the subjecti ve vertical.10,180,181 Transient OTR
and ipsiversive deviations of SVV, which indicate a
pathological shift in the internal representation of the
Acknowledgment
gravitational vector, are typically found in Wallenberg’s The authors wish to thank Ms. J. Benson for cop yediting
syndrome.23,181 the manuscript.
3970_Ch05_059-084 25/06/14 11:30 AM Page 80
References 21. Halmagyi GM, et al. Tonic contraversive ocular tilt reac-
tion due to unilateral meso-diencephalic lesion. Neurology.
1. Brandt T. Vertigo, Its Multisensory Syndromes. 2nd ed. 1990;40:1503.
London: Springer-Verlag; 1999. 22. Lueck CJ, et al. A case of ocular tilt reaction and torsional
2. Brandt T, Dieterich M, Strupp M. Vertigo and Dizziness. nystagmus due to direct stimulation of the midbrain in
Common Complaints. 2nd ed., London, Springer; 2013. man. Brain. 1991;114:2069.
3. Brandt T, Dieterich M. Vestibular syndromes in the roll 23. Brandt T, Dieterich M. Pathological eye-head coordination
plane: topographic diagnosis from brainstem to cortex. in roll: tonic ocular tilt reaction in mesencephalic and
Ann Neurol. 1994;36:337. medullary lesions. Brain. 1987;110:649.
4. Brandt T, Dieterich M. Central vestibular syndromes in the 24. Dieterich M, Brandt T. Thalamic infarctions: differential
roll, pitch, and yaw planes: topographic diagnosis of effects on vestibular function in the roll plane (35 patients).
brainstem disorders. Neuro-Ophthalmology. 1995;15:291. Neurology. 1993;43:1732.
5. Guldin W, Grüsser O-J. The anatomy of the vestibular 25. Bense S, et al. Metabolic changes in vestibular and visual
cortices of primates. In: Collard M, et al. eds. Le Cortex cortices in acute vestibular neuritis. Ann Neurol. 2004;56:
Vestibulaire. Boulogne: Ipsen; 1996:17. 624-630.
6. Brandt T, Dieterich M, Strupp M, Glasauer S: Model 26. Becker-Bense S, et al. Vestibular compensation in acute uni-
approach to neurological variants of visuo-spatial neglect. lateral medullary infarction (FDG-PET study). Neurology.
Biol. Cybern. 2012;106:681-690. 2013;80:1-7.
7. Angelaki DE, et al. Two-dimensional spatio-temporal 27. Masdeu JC, Gorelick PB. Thalamic astasia: inability to
coding of linear acceleration in vestibular nuclei neurons. stand after unilateral thalamic lesions. Ann Neurol.
J Neurosci. 1993;13:1403. 1988;23:596.
8. Baker R, et al. Synaptic connections to trochlear motoneu- 28. Verma AK, Maheshwari MC. Hyperesthetic-ataxic-
rons determined by individual vestibular nerve branch hemiparesis in thalamic hemorrhage. Stroke. 1986;17:49.
stimulation in the cat. Brain Res. 1973;64:402. 29. Masdeu JC, et al. Astasia and gait failure with damage of
9. Schwindt PC, et al. Short latency utricular and canal the pontomesencephalic locomotor region. Ann Neurol.
input to ipsilateral abducens motoneurons. Brain Res. 1994;35:619.
1973;60:259. 30. Dieterich M, et al. Thalamic infarctions cause side-specific
10. Baier B, Bense S, Dieterich M. Are signs of ocular tilt suppression of vestibular cortex activations. Brain. 2005;
reaction in patients with cerebellar lesions mediated by the 128:2052.
dentate nucleus? Brain. 2008;131:1445-1454. 31. Brandt T, et al. Vestibular cortex lesions affect perception
11. Baier B, Dieterich M. Ocular tilt reaction – a clinical sign of verticality. Ann Neurol. 1994;35:528.
of cerebellar infarctions? Neurology. 2009;72:572-573. 32. Bense S, et al. Multisensory cortical signal increases and
12. Dieterich M, Brandt T. Ocular torsion and tilt of subjective decreases during vestibular galvanic stimulation (fMRI).
visual vertical are sensitive brainstem signs. Ann Neurol. J Neurophysiol. 2001;85:886.
1993;33:292. 33. Suzuki M, et al. Cortical and subcortical vestibular
13. Baier B, Thömke F, Wilting J, Heinze C, Geber C, response to caloric stimulation detected by functional
Dieterich M. A pathway in the brainstem for roll-tilt of the magnetic resonance imaging. Cogn Brain Res.
subjective visual vertical: evidence from a lesion-behavior 2001;12:441.
mapping study. J Neurosci. 2012;32(43):14854-14858. 34. Fasold O, et al. Human vestibular cortex as identified
14. Cnyrim CD, Rettinger N, Mansmann U, Brandt T, Strupp M. with caloric stimulation in functional magnetic resonance
Central compensation of deviated subjective visual imaging. NeuroImage. 2002;17:1384.
vertical in Wallenberg’s syndrome. J Neurol Neurosurg 35. Dieterich M, et al. Dominance for vestibular cortical
Psychiatry. 2007;78:527-528. function in the non-dominant hemisphere. Cereb Cortex.
15. Zwergal A, Büttner-Ennever J, Brandt T, Strupp M. An 2003;13:994.
ipsilateral vestibulothalamic tract adjacent to the medial 36. Stephan T, et al. Functional MRI of galvanic vestibular stim-
lemniscus in humans. Brain. 2008;131:2928-2935. ulation with alternating currents at different frequencies.
16. Barra J, Marquer A, Joassin R, et al. Humans use internal NeuroImage. 2005;26:721.
models to construct and update sense of verticality. Brain. 37. Grüsser O-J, et al. Localization and responses of neurons
2010;133:3552-3563. in the parieto-insular vestibular cortex of awake monkeys
17. Baier B, Suchan J, Karnath HO, Dieterich M. Neuronal (Macaca fascicularis). J Physiol. 1990;430:537.
correlate of verticality perception—a voxelwise lesion 38. Grüsser O-J, et al. Vestibular neurons in the parieto-insular
study. Neurology. 2012;78(10):728-735. cortex of monkeys (Macaca fascicularis): visual and neck
18. Johannsen L, Fruhmann, Berger M, Karnath HO. Subjec- receptor responses. J Physiol. 1990;430:559.
tive visual vertical (SVV) determined in a representative 39. Merfeld DM, et al. The dynamic contributions of the
sample of 15 patients with pusher syndrome. J Neurol. otolith organs to human ocular torsion. Exp Brain Res.
2006;253:1367-1369. 1996;110:315.
19. Baier B, Janzen J, Fechir M, Müller N, Dieterich M. 40. Morrow MJ, Sharpe A. Torsional nystagmus in the lateral
Pusher syndrome—its anatomical correlate. J Neurol. 2012; medullary syndrome. Ann Neurol. 1988;24:390.
259:277-283. 41. Lopez L, et al. Torsional nystagmus: a neuro-otological
20. Dieterich M, Brandt T. Ocular torsion and perceived and MRI study of 35 cases. Brain. 1992;115:1107.
vertical in oculomotor, trochlear and abducens nerve 42. Lawden MC, et al. Repetitive paroxysmal nystagmus and
palsies. Brain. 1993;116:1095. vertigo. Neurology. 1995;45:276.
3970_Ch05_059-084 25/06/14 11:30 AM Page 81
43. Büttner U, et al. The localizing value of nystagmus in 63. Brandt T, et al. Postural abnormalities in central vestibular
brainstem disorders. Neuro-Ophthalmology. 1995;15:283. brainstem lesions. In: Bles W, Brandt, T, eds. Disorders
44. Dehaene I, et al. Unilateral internuclear ophthalmoplegia of Posture and Gait. Amsterdam: Elsevier; 1986:141.
and ipsiversive torsional nystagmus. J Neurol. 1996; 64. Halmagyi M, et al. Downbeating nystagmus, a review of
243:461. 62 cases. Arch Neurol. 1983;40:777.
45. Noseworthy JH, et al. Torsional nystagmus: quantitative 65. Costin JA, et al. Alcoholic downbeat nystagmus. Ann
features and possible pathogenesis. Neurology. 1988; Ophthalmol. 1980;12:1127.
38:992. 66. Zasorin NL, Baloh RW. Downbeat nystagmus with alco-
46. Helmchen C, et al. Contralesionally beating torsional holic cerebellar degeneration. Arch Neurol. 1984;41:1301.
nystagmus in a unilateral rostral midbrain lesion. Neurology. 67. Hwang TL, et al. Reversible downbeat nystagmus and
1996;47:482. ataxia in febamate intoxication. Neurology. 1995;45:846.
47. Henn V. Pathophysiology of rapid eye movements in the 68. Malm G, Lyiug-Tunell U. Cerebellar dysfunction related
horizontal, vertical and torsional directions. In: Büttner U, to toluene sniffing. Acta Neurol Scand. 1980;62:188.
Brandt T, eds. Ocular Motor Disorders of the Brain Stem. 69. Saul RF, Selhorst JB. Downbeat nystagmus with magne-
London: Baillière Tindall; 1992:373. sium depletion. Arch Neurol. 1981;38:650.
48. Halmagyi GM, et al. Jerk-waveform see-saw nystagmus 70. Bronstein AM, et al. Down beating nystagmus: magnetic
due to unilateral meso-diencephalic lesion. Brain. resonance imaging and neuro-otological findings. J Neurol
1994;117:789. Sci. 1987;81:173.
49. Dieterich M, et al. Direction-specific impairment of 71. Baloh RW, Yee RD. Spontaneous vertical nystagmus. Rev
motion perception and spatial orientation in downbeat Neurol Paris. 1989;145:527.
and upbeat nystagmus in humans. Neurosci Lett. 1998; 72. Hammack H, et al. Paraneoplastic cerebellar degeneration,
245:29. II: clinical and immunologic findings in 21 patients with
50. Halmagyi GH, Leigh RJ. Upbeat about downbeat nystag- Hodgkin’s disease. Neurology. 1992;42:1983.
mus. Neurology. 2004;63:606. 73. Jacobson DM, Corbett JJ. Downbeat nystagmus associated
51. Glasauer S, et al. Three-dimensional eye position and slow with dolichoectasia of the vertebrobasilar artery. Arch
phase velocity in humans with downbeat nystagmus. J Neurol. 1989;46:1005.
Neurophysiol. 2003;89:338-354. 74. Bertholon P, et al. Syringomyélobulbie posttraumatique et
52. Glasauer S, et al. Effect of 4-aminopyridine on upbeat and nystagmus vertical inférieur. Rev Neurol. 1993;149:355.
downbeat nystagmus elucidates the mechanism of down- 75. Strupp M, Schüler O, Krafczyk S, Jahn K, Schautzer F,
beat nystagmus. Ann NY Acad Sci. 2005;1039:528-531 Büttner U, Brandt T. Treatment of downbeat-nystagmus
53. Marti S, et al. The origin of downbeat nystagmus: an with 3,4-diaminopyridine—placebo-controlled study.
asymmetry in the distribution of on-directions of vertical Neurology. 2003;61:165-170.
gaze-velocity Purkinje cells. Ann N Y Acad Sci. 2005; 76. Strupp M, Thurtell MJ, Shaikh AS, Brandt T, Zee DS,
1039:548. Leigh RJ. Pharmacotherapy of vestibular and ocular
54. Pierrot-Deseilligny C, Milea D. Vertical nystagmus: motor disorders, including nystagmus. J Neurol. 2011;
clinical facts and hypotheses. Brain. 2005;128:1237. 258:1207-1222.
55. Kalla R, Deutschländer A, Hüfner K, Stephan T, Jahn K, 77. Kalla R, Glasauer S, Büttner U, Brandt T, Strupp M.
Glasauer S, Brandt T, Strupp M. Detection of floccular 4-Aminopyridine restores vertical and horizontal neural
hypometabolism in downbeat nystagmus by fMRI. integrator function in downbeat nystagmus. Brain.
Neurology. 2006;66:281-283. 2007;130:2441-2450.
56. Bense S, Best C, Buchholz HG, Wiener V, Schreckenberger M, 78. Tsunemi T, Ishikawa K, Tsukui K, Sumi T, Kitamura K,
Bartenstein P, Dieterich M. 18F-fluorodeoxyglucose Mizusawa H. The effect of 3,4-diaminopyridine on the
hypometabolism in cerebellar tonsil and flocculus in patients with hereditary pure cerebellar ataxia. J Neurol
downbeat-nystagmus. Neuroreport. 2006;17:599-603. Sci. 2010;292:81-84.
57. Hüfner K, Stephan T, Kalla R, Deutschländer A, Wagner J, 79. Etzion Y, Grossman Y. Highly 4-aminopyridine sensitive
Holtmannspötter M, Schulte-Altedorneburg G, Strupp M, delayed rectifier current modulates the excitability of
Brandt T, Glasauer S. Structural and functional MRIs guinea pig cerebellar Purkinje cells. Exp Brain Res.
disclose cerebellar pathologies in idiopathic downbeat 2001;139:419-425.
nystagmus. Neurology. 2007;69:1128-1135. 80. Glasauer S, et al. 4-aminopyridine restores visual ocular
58. Wagner JN, Glaser M, Brandt T, Strupp M. Downbeat motor function in upbeat nystagmus. J Neurol Neurosurg
nystagmus: aetiology and comorbidity in 117 patients. Psychiatry. 2005;76:451.
J Neurol Neurosurg Psychiatry. 2008;79:672-677. 81. Auerbuch-Heller L, et al. A double-blind controlled study
59. Mayfrank L, Thoden U. Downbeat nystagmus indicates of gabapentin and baclofen as treatment for acquired
cerebellar or brainstem lesions in vitamin B12 deficiency. nystagmus. Ann Neurol. 1997;41:818.
J Neurol. 1986;233:145. 82. Thurtell MJ, Joshi AC, Leone AC, et al. Cross over-trail
60. Baloh RW, Spooner JW. Downbeat nystagmus: a type of of gabapentin and memantine as treatment for acquired
central vestibular nystagmus. Neurology. 1981;31:304. nystagmus. Ann Neurol. 2010;67:676-680.
61. Cox TA, et al. Upbeat nystagmus changing to downbeat 83. Tokumasu K, et al. Upbeat nystagmus in primary eye
nystagmus with convergence. Neurology. 1981;31:891. position. Acta Otolaryngol Suppl (Stockh). 1991;481:366.
62. Crevits L, Reynaert C. Posture dependent direction 84. Zumstein HR, Meienberg O. Upbeat nystagmus and vi-
reversal of spontaneous vertical nystagmus. Neuro- sual system disorder in Wernicke’s encephalopathy due
Ophthalmology. 1991;11:285. to starvation. Neuro-Ophthalmology. 1982;2:157.
3970_Ch05_059-084 25/06/14 11:30 AM Page 82
85. Yamazaki K, et al. A case of Fisher’s syndrome with 107. Schwarz DWF, Fredrickson JM. Rhesus monkey vestibu-
upbeat nystagmus. Rinsho-Shinkeigaku. 1994;34:489. lar cortex: a bimodal primary projection field. Science.
86. Fujikane M, et al. Central diabetes insipidus complicated 1971;172:280.
with upbeat nystagmus and cerebellar ataxia. Rinsho- 108. Fredrickson JM, et al. Vestibular nerve projection to
Shinkeigaku. 1992;32:68. the cerebral cortex of the rhesus monkey. Exp Brain Res.
87. Trobe JD, et al. Nystagmus of Pelizaeus-Merzbacher 1966;2:318.
disease: a magnetic search-coil study. Arch Neurol. 109. Büttner U, Büttner UW. Parietal cortex area 2 V neuronal
1991;48:87. activity in the alert monkey during natural vestibular and
88. Gresty MA, et al. Primary position upbeating nystagmus optokinetic stimulation. Brain Res. 1978;153:392.
associated with middle ear disease. Neuro-Ophthalmology. 110. Ödkvist LM, et al. Projection of the vestibular nerve to
1988;8:321. the area 3a arm field in the squirrel monkey (Saimiri
89. Hoyt CS, Gelbert SS. Vertical nystagmus in infants with sciureus). Exp Brain Res. 1974;21:97.
congenital ocular abnormalities. Ophthal Paediatr Genet 111. Chen A, DeAngelis GC, Angelaki DE. Convergence of
(Amsterdam). 1984;4:155. vestibular and visual self-motion signals in an area of the
90. Dieterich M, et al. The effects of baclofen and choliner- posterior sylvian fissure. J Neurosci. 2011;31:11617-
gic drugs on upbeat and downbeat nystagmus. J Neurol 11627.
Neurosurg Psychiatry. 1991;54:627. 112. Ebata S, et al. Vestibular projection to the periarcuate
91. Iwata A, et al. Primary position upbeat nystagmus re- cortex in the monkey. Neurosci Res. 2004;49:55.
versed with carbamazepine. Eur J Neurol. 1996;3:260. 113. Faugier-Grimaud S, Ventre J. Anatomic connections of
92. Leigh RJ, Brandt T. A re-evaluation of the vestibulo- inferior parietal cortex (area 7) with subcortical structures
ocular reflex: new ideas of its purpose, properties, neural related to vestibulo-ocular function in a monkey (Macaca
substrate, and disorders. Neurology. 1993;43:1288. fascicularis). J Comp Neurol. 1989;280:1.
93. Uemura T, Cohen B. Effects of vestibular nuclei lesions 114. Bremmer F, et al. Visual-vestibular interactive responses
on vestibulo-ocular reflexes and posture in monkeys. in the macaque ventral intraparietal area (VIP). Eur
Acta Otolaryngol Suppl (Stockh). 1973;315:1. J Neurosci. 2002;16:1569.
94. Hopf HC. Vertigo and masseter paresis: a new brainstem 115. Klam F, Graf W. Vestibular signals of posterior parietal
syndrome. J Neurol. 1987;235:42. cortex neurons during active and passive head move-
95. Dieterich M, Büchele W. MRI findings in lesions at the ments in macaque monkeys. Ann N Y Acad Sci.
entry zone of the eighth nerve. Acta Otolaryngol Suppl 2004;1004:271.
(Stockh). 1989;468:385. 116. Klam F, Graf W. Vestibular response kinematics in
96. Disher MJ, et al. Evaluation of acute vertigo: unusual posterior parietal cortex neurons of Macaque monkeys.
lesions imitating vestibular neuritis. Am J Otol. Eur J Neurosci. 2003;18:995.
1991;12:227. 117. Schlack A, et al. Multisensory space representations in
97. Francis DA, et al. The site of brainstem lesions causing the macaque ventral intraparietal area. J Neurosci.
semicircular canal paresis: an MRI study. J Neurol 2005;25:4616.
Neurosurg Psychiatry. 1992;55:446. 118. Dieterich M, et al. Horizontal or vertical optokinetic
98. Amarenco P, et al. Infarctus pontin inférolatéral: deux stimulation activates visual motion-sensitive, ocular
aspects cliniques. Rev Neurol (Paris). 1990;146:433. motor, and vestibular cortex areas with right hemi-
99. Kattah JC, Talkad AV, Wang DZ, et al. HINTS to diag- spheric dominance: an fMRI study. Brain. 1998;
nose stroke in acute vestibular syndrome. Three-step 121:1479.
bedside oculomotor examination more sensitive than 119. Bucher SF, et al. Sensorimotor cerebral activation during
early MRI diffusion-weighted imaging. Stroke. 2009; optokinetic nystagmus: an fMRI study. Neurology.
40:3504-3510. 1997;49:1370.
100. Cnyrim CD, Newman-Toker D, Karch C, Brandt T, 120. Abkarian S, et al. Corticofugal connections between the
Strupp M. Beside differentiation of vestibular neuritis cerebral cortex and brainstem vestibular nuclei in the
from central “vestibular pseudoneuritis.” J Neurol macaque monkey. J Comp Neurol. 1994;339:421.
Neurosurg Psychiatry. 2008;79:458-460. 121. Jeannerod M. Vestibular cortex: a network from direc-
101. Goodale MA. Transforming vision into action. Vision Re- tional coding of behavior. In: Collard M, et al, eds.
search. 2011;51:1567-1587. Le Cortex Vestibulaire. Boulogne: Ipsen; 1996:5.
102. Karnath HO , Rorden C. The anatomy of spatial neglect. 122. Bottini G, et al. Identification of the central vestibular
Neuropsychologia. 2012;50:1010-1017. projections in man: a positron emission tomography
103. Brandt T, Dieterich M, Strupp M, Glasauer S. Model activation study. Exp Brain Res. 1994;99:164.
approach to neurological variants of visuo-spatial neg- 123. Wenzel R, et al. Deactivation of human visual cortex
lect. Biol Cybern. 2012;106:681-690. during involuntary ocular oscillations: a PET activation
104. Tiliket C, Ventre-Dominey J, Vighetto A, Grochowicki M. study. Brain. 1996;119:101.
Room tilt illusion. A central otolith dysfunction. 124. Brandt T, et al. Reciprocal inhibitory visual-vestibular
Arch Neurol. 1996;53:1259-1264. interaction: visual motion stimulation deactivates the
105. Brandt T. Cortical matching of visual and vestibular 3-D parieto-insular vestibular cortex. Brain. 1998;
coordinate maps. Ann Neurol. 1997;42:983-984. 121:1749.
106. Sierra-Hidalgo F, Pablo-Fernandez E, Herrero-San M, et al. 125. Bense S, et al. Three determinants of vestibular hemi-
Clinical and imaging features of the room tilt illusion. spheric dominance during caloric stimulation. Ann N Y
J Neurol. 2012; Epub ahead of print. Acad Sci. 2003;1004:440-445.
3970_Ch05_059-084 25/06/14 11:30 AM Page 83
126. Bense S, et al. Three determinants of vestibular hemi- statistical analysis: a study of 140 patients. Cereb Cortex.
spheric dominance during caloric stimulation. Ann N Y 2004;14:1164.
Acad Sci. 2003;1004:440. 148. Cappa S, et al. Remission of hemineglect and anosog-
127. Fink GR, et al. Performing allocentric visuospatial judge- nosia during vestibular stimulation. Neuropsychologia.
ments with induced distortion of the egocentric reference 1987;25:775.
frame: an fMRI study with clinical implications. 149. Vallar G, et al. Exploring somatosensory hemineglect by
NeuroImage. 2003;20:1505. vestibular stimulation. Brain. 1993;116:71.
128. Eulenburg zu P, Caspers S, Roski C, Eickhoff SB. 150. Robertson IH, et al. Walking trajectory and hand move-
Meta-analytical definition and functional connectivity ments in unilateral left neglect: a vestibular hypothesis.
of the human vestibular cortex. NeuroImage. Neuropsychologia. 1994;32:1495.
2012;60:162-169. 151. Vallar G, et al. Spatial hemineglect in back space. Brain.
129. Andersen RA, et al. Encoding of spatial location by pos- 1995;118:467.
terior parietal neurons. Science. 1985;230:456. 152. Foerster O. Sensible Kortikale Felder. In: Bumke O,
130. Galletti C, et al. Parietal neurons encoding spatial orien- Foerster O, eds. Handbuch der Neurologie, vol VI.
tations in craniotopic coordinates. Exp Brain Res. Berlin: Springer; 1936:358.
1993;96:221. 153. Penfield W, Jasper H. Epilepsy and the Functional
131. Karnath H-O. Subjective body orientation in neglect and Anatomy of the Human Brain. Boston: Little Brown; 1954.
the interactive contribution of neck muscle propriocep- 154. Schneider RC, et al. Vertigo and rotational movement in
tion and vestibular stimulation. Brain. 1994;117:1001. cortical and subcortical lesions. J Neurol Sci. 1968;6:493.
132. Karnath H-O, et al. Trunk orientation as the determining 155. Smith BH. Vestibular disturbance in epilepsy. Neurology.
factor of the “contralateral” deficit in the neglect syn- 1960;10:465.
drome and as the physical anchor of the internal represen- 156. Brandt T, et al. Rotational vertigo in embolic stroke of the
tation of body orientation in space. Brain. 1991;114:1997. vestibular and auditory cortices. Neurology. 1995;45:42.
133. Karnath H-O, et al. Decrease of contralateral neglect by 157. Debette S, et al. Transient rotational vertigo as the initial
neck muscle vibration and spatial orientation of trunk symptom of a middle cerebral artery territory infarct in-
midline. Brain. 1993;116:383. volving the insula. Cerebrovasc Dis. 2003;16:97.
134. Watt DGD. Pointing at memorized targets during pro- 158. Naganuma M, Inatomi Y, Yonehara F, et al. Rotational
longed microgravity. Aviat Space Environ Med. vertigo associated with parietal cortical infarction.
1997;68:99. J Neurol Sci. 2006;246:159-161.
135. Vallar G, Perani D. The anatomy of unilateral neglect 159. Hawrylyshyn PA, et al. Vestibulothalamic projections in
after right hemisphere stroke lesions: a clinical CT corre- man—a sixth primary sensory pathway. J Neurophysiol.
lation study in man. Neuropsychologia. 1986;24:609. 1978;41:394.
136. Husain M, Kennard C. Visual neglect associated with 160. Jackson H. Diagnosis of epilepsy. Med Times Gazette.
frontal lobe infarction. J Neurol. 1996;243:652. 1879;1:29.
137. Vuilleumier P, et al. Unilateral spatial neglect recovery 161. Gowers WR. The Borderlands of Epilepsy. London:
after sequential strokes. Neurology. 1996;19:184. Churchill; 1907.
138. Rapcsak SZ, et al. Altitudinal neglect. Neurology. 162. Bumke O, Foerster O, eds. Handbuch der Neurologie,
1988;38:277. vol VI. Berlin: Springer; 1936.
139. Shelton PA, et al. Peripersonal and vertical neglect. 163. Penfield WG, Kristiansen K. Epileptic Seizure Patterns.
Brain. 1990;113:191. Springfield, Ill: Charles C Thomas, 1951.
140. Mesulam M-M. A cortical network for directed attention 164. Karbowski K. Schwindel und Epilepsie. Therapeut
and unilateral neglect. Ann Neurol. 1981;10:309. Umschau. 1984;41:705.
141. Heilman KM, Watson RT, Valenstein E, Damasio AR. 165. Kahane P, et al. Reappraisal of the human vestibular cor-
Localization of lesions in neglect. In: Kertesz A, ed. tex by cortical electrical stimulation study. Ann Neurol.
Localization in Neuropsychology. New York: Academic 2003;54:615.
Press; 1983:471. 166. Penfield W. Vestibular sensation and the cerebral cortex.
142. Mort DJ, Malhotra P, Mannan SK, et al. The anatomy of Ann Otol. 1957;66:691.
visual neglect. Brain. 2003;126:1986. 167. Penfield W, Rasmussen T. The Cerebral Cortex of Man.
143. Samuelsson H, Jensen C, Ekholm S, et al. Anatomical New York: Macmillan; 1957.
and neurological correlates of acute and chronic visu- 168. Kaplan PW, Tusa RJ. Neurophysiologic and clinical corre-
ospatial neglect following right hemisphere stroke. lations of epileptic nystagmus. Neurology. 1993;43:2508.
Cortex. 1997;33:271. 169. Brandt T, Dieterich M. Vestibular paroxysmia (disabling
144. Karnath H-O, Ferber S, Himmelbach M. Spatial aware- positional vertigo). Neuro-Ophthalmology. 1994;14:359.
ness is a function of the temporal not the posterior pari- 170. Andermann F, et al. Paroxysmal dysarthria and ataxia in
etal lobe. Nature. 2001;411:950. multiple sclerosis. Neurology (Minneap). 1959;9:211.
145. Karnath H-O, Himmelbach M, Küker W. The cortical 171. Rabinovitch HE, et al. The ocular tilt reaction: a paroxys-
substrate of visual extinction. Neuroreport. 2003;14:437. mal dyskinesia associated with elliptical nystagmus. Arch
146. Karnath H-O, Fruhmann Berger M, Zopf R, Küker W. Ophthalmol. 1977;95:1395.
Using SPM normalization for lesion analysis in spatial 172. Dogulu CF, Kansu T. Upside-down reversal of vision in
neglect. Brain. 2004;127:E10. multiple sclerosis. J Neurol. 1997;244:461.
147. Karnath H-O, Fruhmann Berger M, Küker W, Rorden C. 173. Hassler R. Thalamic regulation of muscle tone and the
The anatomy of cortical neglect based on voxelwise speed of movement. In: Purpura DP, Yahr MD, eds. The
3970_Ch05_059-084 25/06/14 11:30 AM Page 84
Thalamus. New York: Columbia University Press; 177. Jenkyn LR, et al. Language dysfunction, somesthetic
1966:419. hemi-inattention, and thalamic hemorrhage in the domi-
174. Zoll JG. Transient anosognosia associated with thalamo- nant hemisphere. Neurology. 1981;31:1202.
tomy: is it caused by proprioceptive loss? Confin Neurol. 178. Solomon DH, et al. The thalamic ataxia syndrome.
1969;31:48. Neurology. 1994;44:810.
175. Velasco F, Velasco M. A reticulothalamic system mediating 179. Melo TP, et al. Thalamic ataxia. J Neurol. 1992;239:331.
proprioceptive attention and tremor in man. Neurosurgery. 180. Friedmann G. The judgement of the visual vertical and
1979;4:30. horizontal with peripheral and central vestibular lesions.
176. Cambier J, et al. Lésions du thalamus droit avec syn- Brain. 1970;93:313.
drome de l’hémisphere mineur: discussion du concept 181. Dieterich M, Brandt T. Wallenberg’s syndrome lateropul-
de négligence thalamique. Rev Neurol (Paris). sion: lateropulsion, cyclorotation and subjective visual
1980;136:105. vertical in 36 patients. Ann Neurol. 1992;31:399.
3970_Ch06_085-109 25/06/14 6:43 PM Page 85
CHAPTER 6
Postural
Abnormalities in
Vestibular Disorders
Emily A. Keshner, PT, EdD ■ Anne K. Galgon, PT, PhD, NCS
When this chapter was written for the first edition of this complaints of patients with partial or total destruction
book, the vestibular system was considered to play its of the vestibular labyrinths.10 Despite these fairly consis-
primary role in the control of posture and balance. In tent symptoms, examination of any one patient with
recent years it has been acknowledged that rather than postural abnormalities arising from damage to the vestibu-
initiate automatic postural reactions, the vestibular system lar system could yield an uncertain diagnosis.9,10
is responsible for governing orientation in space. 1-3 The question for the clinician and the clinical inves-
Whereas the somatosensory system provides information tigator is whether any one compensatory strategy would
about the position and motion of the body with respect to prove most ef ficient or ef fective for the population of
the support surface and the body segments with respect to patients with a vestibular deficit. If one compensatory
each other, the vestibular system provides information strategy is best, then a systematic approach to treatment
with respect to gravity and other inertial forces. The cen- could be followed. But to determine the ef fectiveness of
tral nervous system adapts quickly to the loss of peripheral the compensation, we must first determine how to reliably
vestibular inputs from the labyrinths so that it is sometimes indicate whether the patient suffers from postural dyscon-
difficult to objectively identify symptoms of vestibular trol, and whether it is vestibular dysfunction that is respon-
deficit. Identification of the role of the vestibular system sible for the symptoms. Although standard clinical tests
in posture and orientation has relied on findings of of the vestibular system have not changed much, technolo-
postural and orientation disorders in patients and gies such as virtual reality (VR) and vestibular evoked
animals with vestibular abnormalities. 4-8 Most clinical myogenic potentials (VEMP) allow us to explore vestibu-
diagnoses are based on subjective complaints, and patient lar function when combined with other sensory signals
descriptions of a symptom might differ. One might expe- (VR) or to specifically identify what part of the labyrinths
rience a perception of the world spinning about, while an- or vestibular pathways may be affected (VEMP).11,12
other complains of imbalance and falling, yet both could In this chapter, methods available for testing postural
have the same vestibular pathology.9 Since the process of disorders that are associated with vestibular pathology are
central nervous compensation proceeds over a lengthy briefly discussed. Then, postural behaviors that have been
period of time, patients can also have different symptoms quantified and associated with specific vestibular patholo-
when they finally arrive at a clinic, although suf fering a gies are described. Finally, the issue of how the postural
similar deficit. Both clinical and experimental observa- system compensates for loss or damage to vestibular
tions have shown that symptoms of vertigo, past pointing, signals, including the changes that occur with natural
nystagmus, and equilibrium disturbances are the major aging, are discussed.
85
3970_Ch06_085-109 25/06/14 6:43 PM Page 86
Examining the Vestibulospinal transduces linear accelerations and decelerations. The cervi-
System cal VEMP (cVEMP) is a measure of a short-latency response
from a tonically contracted ipsilateral sternocleidomastoid
Advantages and Limitations
(SCM) muscle. The presence, absence, or abnormal ampli-
of Clinical Tests
tude and latency of this muscle response provides diagnostic
Although vestibular disorders continue to be diagnosed information about the function of the saccule, the inferior
through measures of the vestibulo-ocular system such as vestibular nerve,12-15 or the brainstem pathways to the ipsi-
electronystagmography and rotational testing, these cannot lateral SCM.15 The ocular VEMP (oVEMP) test provides
fully describe all disorders of the vestibular system. One diagnostic information about the utricle, the superior vestibu-
problem is that tests of eye movement (vestibulo- ocular) lar nerve, and the associated brainstem pathways to the con-
integrity and postural (vestibulospinal) function may not be tralateral inferior oblique ocular muscle (Fig. 6.1). (For more
correlated.9 First, the well-defined loop of the vestibulo- details on otolith tests see Chapters 11 and 12.)
ocular reflex (VOR) does not reveal the integrity of the more Diagnostic utility of the patterns of oVEMP and
complex vestibulospinal pathways, which are intimately in- cVEMP has been examined for various audiovestibular and
volved in the control of posture and balance. Second, tests neurological disorders, including vestibular labyrinthitis
of the vestibulo-ocular reflex are commonly performed in or neuronitis, Ménière’s disease, vestibular migraine, be-
the plane of the horizontal semicircular canals, whereas nign paroxysmal positional vertigo (BPPV), superior canal
vestibulospinal reflexes are dependent on inputs from the dehiscence, Tullio phenomenon, vestibular schwannoma,
vertical semicircular canals and the otoliths. multiple sclerosis, and spinocerebellar degeneration. 12-16
A clinical test that is able to partially reveal information The relationship between abnormal cVEMP responses and
about vestibulospinal function is the vestibular evoked postural dysfunction (i.e., vestibulospinal mechanisms) is
myogenic potential (VEMP). This is a muscle response gen- still not well studied. Individuals with saccular or inferior
erated from acoustical stimulation of one of the otoliths that vestibular nerve dysfunction and asymmetrical cVEMP
Medial
vestibulo-
spinal tract
Spinal
Sternocleidomastoid accessory
mm nucleus
Ipsilateral Ipsilateral
EMG: Peripheral Central
Short latency
phasic response
Midline Brainstem
Figure 6.1 Diagram of the cervical (cVEMP in black) and ocular (oVEMP in gray) vestibular
evoked myogenic potential pathways from input of an acoustic stimulus to output at the muscle.
3970_Ch06_085-109 25/06/14 6:43 PM Page 87
responses demonstrate abnormal sensory organization tests posturography assesses balance rather than specific
as compared with healthy individuals; however , balance vestibular function, but response patterns that are specific
performance and self-perception of dizziness was not dif- to individuals with vestibular dysfunction can be elicited
ferent from individuals with unilateral caloric weakness with dynamic posturography. Thus, it is a useful adjunct
and normal cVEMP responses.17 to more traditional methods of testing vestibular function.
Although dynamic posturography is not a direct There are tests of the vestibulospinal system that are more
assessment of peripheral or central vestibular function, it easily and inexpensively available to the clinician than
is a useful tool for identifying impairments associated with dynamic posturography and that can be manipulated to
dysfunction of the vestibulospinal system. 18-20 Dynamic better reveal vestibulospinal dysfunction (Table 6-1).
Test Manipulations
(challenge individuals
with vestibular
Advantages Disadvantages compensation)
Static Tests
Vestibular Specific test of the saccule and Requires electromyography of the Can apply a tone or click
Evoked Myogenic inferior vestibular nerve or sternocleidomastoid muscle for the or vibration
Potential (VEMP) utricule and superior vestibular cVEMP and the inferior oblique
nerve. muscle for the oVEMP
Dynamic Tests
Stepping Tests Easily performed in clinic Does not test adaptive responses
Quantified by the number of Has not been shown to be
steps before loss of stability reliable
Virtual Reality Tests the effect of visual infor- Requires expensive technology, a Can manipulate sensory
mation on postural reactions— knowledge of programming, and some signals (haptic, auditory,
incorporates perception with form of kinematic or physiologic visual)
postural responses measurements
3970_Ch06_085-109 25/06/14 6:43 PM Page 88
Dynamic Posturography
Automatic Postural Responses PLANTAR FLEXION ROTATION DORSIFLEXION ROTATION
In the 1970s, Nashner reported stereotypical, automatic Figure 6.2 Four directions of perturbation on the
responses to postural disturbances initiated at the base of dynamic posture platform. Note that in anterior transla-
support, introducing the measurement of postural reac- tions and plantar flexion rotations, ankle angles increase
tions on a moving platform as a powerful experimental as the person compensates for the motion of the platform.
In posterior translations and dorsiflexion rotations, ankle
approach.24,25 Since that time, the majority of studies of
angles decrease.
postural kinematics have concentrated on the electromyo-
graphic (EMG) responses from muscles in the lower limb,
from which most descriptions about restabilizing actions latencies longer than the stretch reflex but shorter than vol-
have been drawn. 24-29 Subjects stand on a platform that untary reactions to bring the body back over the base of
could be translated in an anterior and posterior direction, support. These restabilizing ankle muscle responses (at la-
or rotated so that the ankles are moved into plantar or dor- tencies of 90 to 120 ms) were followed within 10 to 20 ms
siflexion (Fig. 6.2). The expected response to anterior mo- by the muscle in the upper leg on the same side of the body
tion of the platform is backwards sway (base of support (i.e., soleus followed by the hamstrings; tibialis anterior
moved in front of the center of mass), producing a de- followed by the quadriceps). Thus, from these early stud-
creased angle at the ankle and a stretch of the ankle mus- ies, patterns of muscle activation initiated by ankle pro-
cles on the anterior surface of the body (i.e., tibialis prioceptive inputs, and arising from distal to proximal
anterior). If the platform moves posteriorly , the subject lower limb muscles, were identified as ascending muscle
sways forward (base of support moved behind the center synergies responsible for restabilization after platform
of mass), thereby decreasing the ankle angle and stretch- movement.24,25
ing the gastrocnemius and soleus muscles. Rotating the Nashner’s original conclusion that the body acts as a
platform into plantar or dorsiflexion would produce equiv- rigid, inverted pendulum, reliant primarily on ankle pro-
alent changes at the ankle (see Fig. 6.2), but the center of prioceptive inputs to initiate the restabilizing actions, does
mass remains in line with the base of support. not accurately describe the complex, multisegmental ac-
Although the monosynaptic stretch reflex does not tions that occur during postural restabilization.27,29-32 The
act functionally to replace the center of mass over the base “ankle strategy” is most effective when sway is slow and
of support, EMG analysis of the lower limb muscles re- the support surface is firm. When it is impossible to exert
vealed that the muscles being stretched also responded at adequate torque around the ankle joint, as when the base
3970_Ch06_085-109 25/06/14 6:43 PM Page 89
of support is narrow or compliant, balance is recovered were different. When head acceleration and neck and
with flexion at the hip or a “hip strategy.”33 Allum et al34 lower limb muscle EMG responses recorded during both
concluded that all balance corrections result from one of types of perturbation did not exhibit the same response
two basic synergies defined by the timing between the patterns, the investigators concluded that labyrinthine sig-
body segments, and that the amplitude of the selected nals must be directly involved in the generation of lower
synergy was modulated according to the initial movement limb postural reactions. Differences between the two sub-
velocities at all joint segments. Thus, there is a continuous ject groups were greatest and most consistent during plat-
repertoire of movement strategies for balance rather than form rotations,51 leading these researchers to believe that
two discrete strategies. vestibular loss is best diagnosed using a rotation of the
With more demanding stimuli (e.g., rapid perturba- support surface. Further studies using a range of platform
tions and a center of mass moving far beyond the base of translation velocities (5–35 cm/sec) 52 have shown that
support), the ability to take a step has been found to be the equivalent head accelerations produced very different hip
relevant criteria for recovery of balance.35,36 Other studies and knee torques between healthy subjects and patients
have also demonstrated that the initiation of the balance with bilateral vestibular deficit. This suggests that the
reactions is highly dependent both on the ability to predict magnitude and force pattern of the muscles depends very
the occurrence of the perturbation,37-40 and on the location much on the presence of vestibular inputs from early head
of the disturbance on the body.41-44 movements.
system may select a compensatory strategy that relies on experiences with the paradigm are not regulated.A further
enhancing the gains of somatosensory and visual respon- restriction on the interpretation of results is that measure-
siveness to the distorted inputs rather than shifting respon- ment of postural responses should incorporate the mechan-
sibility for the response onto the vestibulospinal system. ics of body sway with the threshold properties and dynamic
Disorientation of labyrinthine-loss patients when visual54 characteristics of the labyrinthine receptors, 29,52,71-76 be-
or somatosensory60,61 information becomes unreliable can cause knowing the mechanics of the head and motions of
also be explained by the fact that neither signal can ade- the center of mass is necessary for predicting the role of
quately specify the orientation of the body in all situations. canal and otolith feedback in restabilization. Despite its
In natural environments we rely on both visual and vestibu- limitations, and the multitude of variables that should be
lar signals to define our orientation in space, and evidence controlled, the posture platform continues to be employed
indicates that labyrinthine-deficient individuals become as a method for obtaining quantitative measures of postural
more sensitive to and dependent on visual inputs with reactions in clinical populations. Many of the results re-
vestibular loss.62-64 ported in this chapter have, in fact, depended on the posture
Clinical researchers have attempted to improve the platform methodology to examine disturbances in postural
sensitivity of distinguishing between postural control in control as a result of vestibular dysfunction.
younger and older adults64-67 and individuals with vestibu-
lar deficits20,68-70 by adding head shaking to dynamic com-
Tests of Quiet Stance
puter posturography and the sensory or ganization test
(SOT). The head shaking SOT (HS-SOT) adds a horizon- Traditional clinical examinations of vestibulospinal func-
tal head shake to conditions 2 (eyes closed; surface fixed) tion include tests of self-localization, such as the Romberg
and 5 (eyes closed; sway referenced). The head shaking test.77 Initially, Romberg’s test of instability was based on
component is accomplished by having the individual per- a population of patients with proprioceptive loss from tabes
form horizontal head turns at a peak velocity of 60 deg/sec dorsalis who were unable to stand with feet together and
for 20 seconds.20 At least one study,69 however, noted ceil- eyes closed. But the Romberg test is insensitive for detec-
ing effects in condition 2 and floor effects in condition 5 tion of chronic unilateral labyrinthine impairment78 and is
of the HS-SOT in individuals with vestibular deficits, highly variable even within a subject. 78,79 Modifying the
which led to a modification that includes head shaking test by having the patient stand in a tandem heel-to-toe
at additional velocities (120 deg/sec in condition 2 and position (sharpened or tandem Romberg) has made the test
15 deg/sec in condition 5).67,69 Lim et al68 showed that the more sensitive, probably because of the narrowed base of
HS-SOT conditions 2 and 5 were related to perception of support. Even so, tests of quiet stance fail to measure the
disability through the Dizziness Handicap Inventory adaptive components of the postural response that are es-
up until 6 months after an acute unilateral hypofunction. sential to dynamic balance during most daily activities.80
The SOT without the head shake only correlated in the Tests of quiet stance may indicate the severity of a
first 1 week after the acute event. Thus the HS-SOT may balance problem because patients with vestibular system
be a valuable outcome measure in vestibular rehabilitation damage will demonstrate increased sway and falling when
for individuals with loss of balance provoked by head the base of support is constrained (e.g., narrow base
movement.68,70 of support or compliant surface) during quiet standing.
In summary, postural responses to support surface Conclusions about the neural processes contributing to
displacements have traditionally been tested by: (1) trans- postural imbalance are severely limited. The effect of al-
lating a standing subject along the earth’s horizontal plane tered proprioceptive and cutaneous information on low-
on a moving platform, (2) rotating the foot about the frequency sway stabilization cannot be determined by tests
horizontal axis of the ankle into dorsiflexion or plantar of quiet standing. Changing velocity of the visual field is
flexion, and (3) keeping the platform fixed to the earth a significant parameter controlling body sway during quiet
horizontal or sway referencing the angle of the platform standing,80 but simple removal of vision does not alter the
or visual field to match the angle at the ankle during quiet temporal or spatial organization of the automatic postural
sway. Experiments using the posture platform have been reactions.45 Furthermore, behavioral measures as to how
performed with a wide range of velocities and amplitudes often a subject falls or to which direction he deviates do
of displacement that alter the transmission of forces from not convey information about the motor and sensory
the lower limb to the head and make the comparison of mechanisms that may be involved in postural control.81,82
vestibular influences on balance difficult across laboratory Thus, attempting to assess the integrity of the vestibular
settings. Instructions to the subjects and monitoring of past system through a test of quiet standing opens the door to
3970_Ch06_085-109 25/06/14 6:43 PM Page 91
many confounding variables and is far from specific to the the classical Romber g test has made the measurement
vestibulospinal disorders that may produce a postural of postural sway during quiet standing more objective,
deficit.83,84 Despite these limitations, the concept of devi- but the mechanisms contributing to the observation of
ation from the vertical during quiet standing continues to increased sway still cannot be identified. One problem
underlie clinical testing of vestibular dysfunction. is that changing the position of the body parts (either
There has been renewed interest in quantifying pos- randomly or through experimenter directive) could shift
tural sway in clinical examination of individuals with the center of pressure without affecting the stability of the
vestibular loss.85-88 A compliant foam surface has been subject.90 In general, because the sensory apparatus of the
shown to be very sensitive for identifying vestibular vestibular system is most responsive to changes in accel-
disorders. Varela et al86 demonstrated increased sway am- eration and orientation in space, 93 and because patients
plitudes between healthy individuals and those with with vestibular deficits tend to have normal Romber g
vestibular involvement in standing on compliant surfaces signs, tests of quiet standing on a stabilometer are not
with eyes open and eyes closed. A large-scale survey of compelling measures of vestibulospinal function.
balance and vestibular function in the United States used
a compliant surface as an indicator of vestibular dysfunc-
Tiltboards
tion and an increased risk of falling, and found that more
than 35% of adults 40 years and older experienced dif fi- Tilt reactions, or reflexes opposing bodily displacement, tra-
culty standing with eyes closed on the compliant surface.89 ditionally were evoked through a lateral tilt or anterior/
Recent development of clinical applicable testing posterior tilt of the supporting surface about a horizontal
systems utilizing inertial sensors may help clinicians in axis.4-6 On tilting the base of support, the reaction to regain
both diagnosing impairments86 and monitoring improve- a stable equilibrium occurred by moving the body against
ments85 with vestibular rehabilitation during tests of quiet the angular momentum and repositioning the center of grav-
stance. Inertial sensors attached to pelvis and trunk 86 or ity within the vertical projection of its base of support. 4-8
sacrum87 may help capture sway amplitudes during clini- These reactions have also been elicited in the clinic by sim-
cal balance and gait tests. Horling et al 85 measured sway ply pushing the patient at the shoulder girdle. Problems with
standing with eyes closed (Romber g test) with firm sur - the accuracy of this test are threefold. First, because the tilt
faces and eyes closed on compliant surfaces in individuals reactions are measured by observational techniques, later
with vestibular loss, extremity proprioceptive loss, and voluntary responses (greater than 150 ms) rather than auto-
healthy individuals. They found that compared with matic postural reactions are being evaluated. Second, the
healthy individuals, those with vestibular loss had increased response pattern alters if the force is applied directly to the
sway in the eye closed and compliant surface standing trunk rather than to the support surface.Third, tilt responses
condition, and those with proprioceptive loss had in- will be organized differently depending on whether your
creased sway in both the eye closed on firm and compliant patient is pushed or trips over an obstacle in the environ-
surface conditions. ment, whether the application of perturbation is predictable,
and whether it is self-induced or elicited.
Stabilometry
Stepping Tests
Stabilometry is a clinical tool that measures anterior -
posterior and lateral excursions of the body in subjects The Unterberger94 or stepping test of Fukuda95 examines the
standing quietly on a force platform, usually over time.90-92 ability of patients to turn about a vertical axis when marching
During that time, the subject stands quietly on a force or stepping in place. Marked variability in the amount of ro-
plate, and the excursion of the center of gravity is mea - tation produced by even the same subject, however, makes
sured across several conditions that can include eyes open, these tests unreliable.9 Patients with severe disruption of the
eyes closed, and eyes closed with head extension. vestibular system may stagger so uncontrollably , that the
Attempts to stress the vestibulospinal system have been stepping tests cannot reliably indicate the side of the lesion.96
incorporated into this system of measurement by altering A battery of tests developed by Graybiel and Fregly 97
signals from other sensory pathways. For example, adding (Ataxia Test Battery) examines subjects standing upright, on
a layer of foam rubber (compliant surface) to the base of one leg, and with feet aligned in tandem position with eyes
support to make somatosensory inputs less effective,53 or open or closed, as well as tandem walking in a straight line
placing the subjects within a visually controlled environ- on the floor or on a narrow rail.This test is useful for patients
ment to modify visual feedback.54 This attempt to quantify who have compensated for a labyrinthine deficit because,
3970_Ch06_085-109 25/06/14 6:43 PM Page 92
resulting mostly in complaints of unsteadiness and insta- that communicate with the vestibular nuclei. In both cases,
bility. Distortion indicates that the signal is present but patients can experience disequilibrium, imbalance, and
disturbed, and does not correspond with expectations ataxia. With unilateral lesions of the peripheral system, the
about the sensory feedback. The result would be inappro- normal symmetry of inputs from the right and left
priate or false motor responses to the existing situation labyrinths become disordered, resulting in a decreased fir-
(e.g., vertigo and ataxia). A summary of postural distur - ing rate of the vestibular nuclei on one side. A unilateral
bances is presented in Table 6-2 for the disorders discussed lesion affects the system as if the intact side were being
in this chapter. stimulated, thus generating an illusion of change in head
orientation and movement. The inherent disequilibrium
then activates the vestibulospinal system to respond inap-
Deficient Labyrinthine Inputs propriately, resulting in vertigo, nystagmus, and postural
Damage along the eighth nerve or within the vestibular instability.
labyrinth produces lost or diminished signals from the Another effect of vestibular system stimulation, main-
peripheral vestibular apparatus. 93 Central disturbances taining tone of the muscles against gravity , appears to be
originate at the vestibular nuclei or in the central pathways directly correlated with labyrinthine inputs because the
Peripheral
Vestibular Disorder Clinical or Functional Expression
Deficient Inputs Need more energy to maintain the upright Complaints of fatigue with sustained upright
position activities
Distorted Inputs Still able to process vestibular inputs Postural response normal when vertigo is not
active
Central Vestibular Impaired perception and location of the Head and trunk tilt
Disorder gravitational vertical
Falling tends to occur in the direction of Lateropulsion results in falls toward the
quick phase nystagmus direction of horizontal nystagmus
activation of extensor muscles in the extremities of both the sensory information provided by the support surface
monkeys108 and humans109 with unilateral deficit were and the visual surround.110
enhanced contralateral to the side of the lesion. But pos- Several problems limit our reliance on these results
tural reactions are more complex than single pathway for clinical diagnosis and measurement. First, patients
vestibular reflexes, and cannot be traced and localized as with unilateral or partial bilateral deficits at times were as
easily as these direct line responses. For example, when unstable as patients with total loss of vestibular function,81
both labyrinths are lesioned, an artificial sense of motion thus rendering this a poor test of graduated function in the
does not occur, and neither do the symptoms of nystag- vestibular system. Second, the authors tested only well-
mus and vertigo. Yet, equilibrium is still disturbed, sug- compensated patients. As will be discussed later, compen-
gesting that the balance function of the vestibular system sation could occur as a central reor ganization in the
is not a simple response to stimulation of the labyrinthine system. Thus, these experiments may not be testing a
receptors. vestibular deficit, but rather a compensatory subsystem
that responds inadequately to the presented stimuli.Third,
patients with postural instability from other, non-vestibular
Indicators of Vestibulospinal Deficiency disorders may have test results similar to those of patients
Unilateral and Bilateral Labyrinthine with vestibular deficits (Hain and Herdman, personal
Deficit communication).
Variability of the responses measured from the many Allum and colleagues examined both the latencies
methods of posturography confirms the complexity of and amplitudes of muscle EMG responses on a platform
control of these disordered postural responses. After re- that dorsiflexed the ankle. 27, 34, 45, 50, 51, 82, 109, 111 Areas
peated attempts to quantify the results of the Romberg test, under the EMG bursts in the ankle muscles, soleus, and
the most reliable effort seems to be measuring ener gy of tibialis anterior, and ankle torque recordings of patients
the power spectral densities of the center of force trajec- with complete bilateral labyrinthine deficit, were sig-
tories when maintaining an upright position. 110 Both in nificantly diminished when compared with normal sub-
this study and in others using force plates to record sway jects with eyes both open and closed. Using these data,
during quiet stance,10,92 intersubject variability and over- the presence of a linear correlation between EMG
lap between normal and clinical populations reduced the amplitudes and the extent of the peripheral vestibular
strength of the findings. Results suggest, however , that deficit was explored. 112 The population measured in-
more energy needs be expended to maintain an upright cluded those with intact labyrinths (normal subjects),
position when visual inputs are removed (eyes closed) acute unilateral labyrinthine deficit patients, chronic
from patients with a labyrinthine deficit. unilateral labyrinthine deficit patients, and bilateral
In a series of papers presented by Black and labyrinthine deficit patients, thus covering a graduated
Nashner,56,106,110 postural sway was recorded through a range of labyrinthine function.
potentiometer placed at the level of the hips. Patients A stepwise discriminant analysis technique per -
stood on a platform that could be either earth fixed, or formed on the data suggested that muscle response ampli-
moved proportional to body sway (sway referenced). tudes in the soleus and tibialis anterior muscles, as well as
The visual environment was then manipulated so amplitude of torque exerted on the platform, were in-
that patients experienced a visual field that was either: versely related to the severity of the labyrinthine deficit.
(1) earth fixed, (2) proportional to body sway, or (3) re- Muscle and torque responses diminished in amplitude as
moved by eye closure. Patients with reduced or absent the reception of labyrinthine inputs decreased. Because
labyrinthine inputs were unstable compared with normal lower limb EMG activity was still present in the patients
controls only when ankle proprioceptive references with complete loss of labyrinthine inputs, a linear corre-
were proportional to body sway and visual references lation of the amount of EMG activity with extent of pe-
were either removed or inappropriate (conditions 2 and ripheral vestibular deficit suggests that lower limb postural
3 above). When the only reliable source of feedback was reflexes could be triggered by proprioceptive stretch re-
the vestibular inputs, it was believed that patients with flexes, but that amplitude modulation is under the control
vestibular deficiencies would fall because they were de- of, or requires the presence of, vestibulospinal signals.
pendent on the somatosensory and visual reference to EMG activity in the neck muscles was not obviously al-
correctly organize their postural responses. From these tered in these patients, implying local control of neck mus-
studies, Black and colleagues suggested that vestibular cle responses. Thus, the effectiveness of the ankle muscle
deficits could be quantified by systematically altering responses to produce a functional forward torque in
3970_Ch06_085-109 25/06/14 6:43 PM Page 95
patients rotated backwards on a platform was diminished, reduced restabilizing torques recorded at the ankle, knee,
and these patients tended to fall backwards. and hip.114
EMG responses of patients with vestibular deficit
during horizontal translations of a platform were also ex- Ménière’s Syndrome
amined.51,61 Although latencies of the postural reactions Ménière’s syndrome, or endolymphatic hydrops, is con-
were produced without significant time delays, segmental sidered to be a vestibular deficiency although it presents
organization of the postural response were disordered. as fluctuating vestibular function. Symptoms of acute
Allum et al 112 found that angular velocity measures of Ménière’s syndrome include hearing loss, tinnitus, and a
rotation of the trunk about the hip were not significantly sensation of fullness or pressure in the ear.9 Patients with
altered in patients with a bilateral peripheral vestibular this syndrome exhibit a negative Romberg sign during re-
deficit, and that a hip strategy was a common component mission,115 but symptoms of dizziness and instability can
in the postural response to platform rotations. These in- occur for several days following intermittent episodes of
vestigators suggested that whichever movement strategy vertigo. These episodes appear at irregular intervals for
was selected depended on the initial direction of trunk and years, and about one-third of the patients eventually
head acceleration (which is oppositely directed in platform develop bilateral involvement.9
rotations and translations), and was executed as if prepro- Objective diagnosis of Ménière’s syndrome has been
grammed from the beginning. Although Horak et al61 pre- dependent on long-term documentation of the fluctuating
viously stated that hip strategies were not seen in patients hearing loss. Quantitative posturography measures have
with vestibular disorders, new measures of hip torques em- been able to identify consistent changes in the postural re-
phasize the importance of identifying the proper response sponse of these patients, even during periods of remission.
variables when using dynamic posturography as a diag- The movement pattern of the center of gravity was mea -
nostic tool. Runge et al 52 found that the joint torques at sured during a stepping test after observing that patients
the hip and knee were abnormal over a range of velocities deviated toward the affected side even during the remis-
during rearward translations for patients with bilateral sion period.115 Stepping was performed in the dark with
deficit. Because head accelerations were the same in the eyes open and closed, and patients were required to per -
patients and healthy subjects, these investigators agreed form at a frequency that was both optimal for normal
with others’ findings27,45 that the magnitude and force pat- walking and that elicited a smooth rhythmical pattern
tern of the muscles depends on vestibular inputs from (i.e., 1.2 Hz). When eyes were closed, the patients exhib-
early head movements. ited angular deviations of 30 degrees or more toward
We can conclude that patients with partial or total the affected side after 8 to 12 seconds of stepping. Time
loss of labyrinthine input exhibit diminished amplitudes to deviation indicated a degrading central motor program
of EMG response and thus require greater energy expen- that was initiated by visual inputs, but which required
diture to maintain balance, particularly when another vestibular inputs (in the absence of vision) to be main-
source of stimulation to the system (e.g., visual inputs) has tained over time.
been removed. These patients also exhibit greater sway in Measures of sway during quiet standing have included
sensory conflict situations, and variability between analyses of the pattern of motion, displacement, and power
patients is a common clinical occurrence because of the spectrum of the center of gravity . With all of these mea -
dynamic central compensatory processes. With unilateral sures, position of the center of gravity changed in an irreg-
deficit, the initial perception of apparent body motion is ular fashion, and deviated primarily toward the af fected
directed away from the side of the lesion. Postural reac- side.116,117 High-frequency components of standing sway
tions are usually in a direction opposite to the direction of were observed during acute phases of Ménière’s syndrome,
vertigo, causing a tendency to fall and deviate toward the but not during remission periods. 117 Patients with
affected side. Severe postural disturbances occur when Ménière’s syndrome who had not developed vestibular hy-
these individuals have to rely on vestibular inputs, but the pofunction, as determined from vestibulo-ocular reflex
deficit is compensated within 2 weeks after the lesion. 113 gains, were also tested under conditions of sensory conflict
Individuals with bilateral deficit exhibit normal postural during quiet standing (see earlier description in section on
sway in quiet stance.61 Removal of vision with eye closure Indicators of Vestibulospinal Dysfunction).110 These pa-
increases this sway by only a small amount. 106 These pa- tients responded very much like well-compensated patients
tients tend to fall backward when their eyes are closed dur- with unilateral or bilateral loss of labyrinthine inputs. The
ing dorsiflexion tilts of a platform. Their diminished group had nearly normal responses on all trials with the
amplitudes of muscle activity presumably result in the platform fixed to earth horizontal. Responses fell outside
3970_Ch06_085-109 25/06/14 6:43 PM Page 96
the normal range when either the platform or the visual place at the level of the vestibular nuclear complex, at the
field was perceptually stabilized, again suggesting depend- adjacent reticular formation, and on spinal interneu-
ence on reliable inputs from the vestibular labyrinths rons120,121 and motoneurons.119 However, increasing evi-
during these test conditions. dence122,123 suggests that correct alignment of the head
with the trunk and with the gravitoinertial vertical 124
requires that the vestibular system receive ascending
Indications of Vestibulospinal Distortion
somatosensory inputs. To attain an appropriate postural re-
Benign Paroxysmal Positional Vertigo sponse, a convergence of sensory information from the
Patients with BPPV have been examined to study the vestibular, somatosensory, and visual systems is needed
effects of distorted labyrinthine inputs on posture.110 The to align the body with respect to earth vertical.Thus, with
key to this syndrome is that brief episodes of vertigo labyrinthine loss, even if the otoliths remain intact, the
(usually less than 1 minute) are generated with position ability to identify the upright orientation may be
change. Paroxysmal positional nystagmus can be observed impaired.125 Inputs from either of these modalities are not
with rapid changes of position. After a period of several necessarily redundant because each represents dif ferent
attacks, symptoms can become more prolonged, and parameters and is effective within a particular frequency
include dizziness and nausea lasting for hours or days. 9 domain.126-128 In fact, the frequency of stimulation is im-
Degeneration of the utricular macula releasing otoconia portant to control with compensated patients because
that influence the cupula of the posterior semicircular motor output of the visual system and the vestibular sys-
canal is strongly implicated as the cause of BPPV , and tem has been found to be frequency dependent. 76,129-132
could result from a variety of etiologies (e.g., trauma, in- Thus, it is unlikely that normal postural responses are
fection, ischemia). The intensity of BPPV depends on the reflective of the isolated labyrinthine and neck reflexes
velocity of the positional changes, and attacks can be observed in the decerebrate animal.133-135 Instead, postural
avoided if positions are assumed very slowly.118 reactions probably emerge from a dynamic coupling of all
Because of the positional component of this syn- available sensory signals. Body posture can be oriented to
drome, postural changes are easily recorded during quiet a visual, somatosensory, or vestibular reference frame
stance by having patients alter the position of their head in depending on the task and behavioral goals. It may also
space. After tilting the head, large amplitudes of anterior- be based on an estimated internal representation of body
posterior sway and sway ipsilateral to the direction of head orientation with respect to the environment from memory,
tilt were observed.118 Instability gradually decreased as the thereby incorporating the expected multisensory inputs
vertigo diminished, but with eyes closed, the sway could and flexible postural reactions occurring for each
not be compensated by other inputs, and falling occurred. task.136,137 A convergence of inputs from more than one
Unlike patients with a loss of vestibular inputs, pa- sensory modality would then be necessary to create this
tients with distorted inputs from BPPV reacted normally estimated postural orientation. Our studies in a virtual en-
on a moving platform when forced to rely only on their vironment138 demonstrated that converging inputs con-
vestibular inputs. More disturbing to this group of patients trolled postural orientation during rotations of the visual
were inappropriate (perceptually stabilized) visual circum- scene in pitch and roll. The head and trunk were linked in
stances whether the platform was earth fixed or moving magnitude and phase, whereas the ankle produced small
proportional to body sway.81,106,110 Patients with BPPV compensations that were lar gely out of phase with the
probably rely primarily on visual information to organize upper body. We inferred, as in a previous study on a
their postural reactions, and have suppressed their posture platform, that the upper body responded to visual-
response to the potentially unreliable vestibular inputs. vestibular signals while the ankle responded to proprio-
ception and changes in ground reaction forces. 30
Postural Reactions in Central Buchanan and Horak139 also reported differential controls
of the head and trunk and of the lower limbs when exam-
Vestibular Lesions ining segmental organization of postural responses. Thus,
One could erroneously assume that function of the vestibu- the cause of instability in labyrinthine-deficient individu-
lar labyrinths is directly representative of the functional in- als may be caused by a disorder of head and trunk spatial
tegrity of the vestibular system. Although receiving direct orientation rather than lower limb instability.140
inputs from the peripheral labyrinths, the vestibular nuclear Several clinical findings have been suggested to
complex also receives visual and somatosensory inputs. 93 differentiate between a peripheral and central disturbance
Convergence of vestibular and somatosensory input onto in the vestibular system. Gradually increasing disturbances
the vestibulospinal and reticulospinal 119 neurons can take of standing, walking, and falling in the direction of the
3970_Ch06_085-109 25/06/14 6:43 PM Page 97
quick phase of spontaneous nystagmus have been identi- the evidence from clinical reports suggests that a central
fied as indications of a central vestibular lesion.141 Balance vestibular dysfunction results in impaired perception and
disorders as a result of abnormalities of the vestibular nu- location of the gravitational vertical exhibited throughout
clear complex have been observed, 142,143 but are poorly the whole body postural system. But with all of these syn-
documented. The majority of the literature about central dromes, other motor structures are af fected as well, and
vestibular brainstem lesions reports only oculomotor ab- may contribute to the impairment.
normalities, but Brandt et al 143 have attempted to relate
well-defined central vertigo syndromes to characteristics
of postural imbalance. Briefly, these investigators reported Postural Dysfunction with
five conditions for which postural imbalance have been Pathology of Other Sensory-
consistently reported: downbeat nystagmus vertigo syn-
drome, ocular tilt reaction, Wallenberg’s syndrome, parox-
Motor Centers
ysmal and familial ataxia, and brainstem lesions that The vestibular nuclear complex communicates with motor
mimic labyrinthine dysfunction. One should recognize, as well as sensory centers.141 In fact, extensive reciprocal
however, that structures other than the vestibular system connections between the vestibular nuclei and thecerebel-
may be damaged and affect balance. lum145 argue for a prominent role of the cerebellum in reg-
Downbeat nystagmus is specific for a lesion of the ulating the output of the vestibulospinal system, and
paramedian craniocervical junction (30% of cases caused lesions of the cerebellum result in severe postural distur -
by Arnold-Chiari malformation), inducing a direction- bances. Three kinds of cerebellar ataxia have been identi-
specific vestibulospinal ataxia. Static head tilts modulate fied, suggesting different pathophysiological mechanisms
the intensity of the nystagmus and the postural sway, sug- that are dependent on the site of the lesion.146 A test of the
gesting involvement of otolith function. The typical pos- sway stabilizing responses on a posture platform of pa-
tural imbalance in this condition is an anterior -posterior tients with late cortical atrophy of the anterior lobe of the
sway with a tendency to fall backwards, but many of these cerebellum revealed that response latencies were within
patients do not complain of vertigo or balance problems. normal limits following dorsiflexion rotations and back-
Brandt et al143 suggest that the backward sway is vestibu- ward translations on a platform, but amplitudes and dura-
lospinal compensation to the forward vertigo resulting tions of response were two to three times greater than
from the downbeat nystagmus. Ocular tilt reaction is normal,147,148 and habituation to the stimulus was ab-
actually a triad of responses, including ipsilateral head- sent.149 Postural response magnitudes of the patients with
trunk tilt, ocular torsion, and ocular deviation. Patients anterior lobe damage were scaled correctly when relying
seem to have a readjustment in their perception of the ver- on current somatosensory feedback, but the patients were
tical that matches the actual tilt deviation of the eye, head, unable to scale their responses when relying on prior ex-
and trunk. This condition has been observed in patients perience. Thus, the major effect of anterior lobe cerebellar
with brainstem abscess, multiple sclerosis, and acute damage on postural responses may be an impairment of
Wallenberg’s syndrome. Wallenberg’s syndrome is an in- responses based on predictive central set.148 This may have
farction of the dorsolateral medulla resulting in ipsilateral implication on motor learning and intervention to improve
dysmetria of the extremities, pain and temperature loss, postural performance. Individuals with cerebellar damage
and a lateropulsion of the eyes and head causing the body may show poor motor learning, show slower recovery of
to deviate toward the side of the lesion and, consequently, postural control, and require more practice.150
fall. A scale was developed that grades the severity of this A characteristic sway frequency of 3 Hz has been
phenomenon and its time course for recovery.144 Classifi- recorded in this population.151 Intersegmental counterbal-
cations of severity are: Grade I: Moderate head-trunk tilt ancing actions were enhanced in these patients, so that
without imbalance; Grade II: Head-trunk tilt with consid- falling was not commonly observed, but they tend to
erable imbalance, but no falls; Grade III: Head-trunk tilt exhibit a stif f-legged gait. Stance ataxia was found to
with imbalance falls with eyes closed; and Grade IV : improve with visual feedback, unlike that appearing with
Head-trunk tilt with imbalance falls with eyes open. vestibulospinal lesions.152, 153 Thus, in these patients, sta-
Paroxysmal and familial ataxias share the broad- bilizing responses occurred, but they lacked the balance
based, unsteady gait that defines ataxia. Finally , pon- between opposing muscle forces and grading of response
tomedullary lesions near the vestibular nuclei at the entry over time.
of the eighth nerve can mimic a peripheral labyrinthine The postural system of patients with lesions of the
disorder, and drop attacks (a sudden, unpredictable for - vestibulocerebellum (flocculus, nodulus, and uvula) may
ward falling) can occur with basilar insuf ficiency. Thus, be so severely impaired that these patients cannot walk.
3970_Ch06_085-109 25/06/14 6:43 PM Page 98
Ataxia of the head and trunk is observed while sitting, disparate responses of agonist and antagonist muscles in
standing, and walking. These patients exhibit unusually the paretic lower limb during postural perturbations on a
large sway in all directions with predominantly low fre- platform.163 With augmented feedback, such as a warning
quencies of less than 1 Hz, and visual stabilization ap- tone and knowledge of perturbation direction, however ,
pears to be reduced when the Romber g test with eyes timing of the postural responses improved. 164 When bal-
open and closed is compared. These patients tend to fall ancing on a seesaw apparatus, patients with spastic hemi-
even when sitting down, which may be a result of dimin- paresis minimized the high-frequency , anteroposterior
ished intersegmental movement for counterbalancing or sway on the affected side with a corresponding reduction
to truncal ataxia.146,152 Neocerebellum lesions produce lit- of the EMG response in tibialis anterior .165,166 Electrical
tle postural instability or disturbance of stance even with stimulation of the tibial nerve in patients on the seesaw re-
eyes closed. Control of position of the body’ s center of vealed a delayed and diminished EMG response of tibialis
mass seems to be disturbed since these patients exhibit anterior in the af fected leg, thereby interfering with the
ataxia during a limb and trunk pursuit task.146 Reports of normal compensatory response to displacement of the sup-
head and trunk deviation to the side of the lesion have port surface. Spastic paraparetic patients were observed
also appeared.152 to produce qualitatively similar results.165,166
With basal ganglia disorders, such as Parkinson’s Children with cerebral palsy were also studied on a
disease, equilibrium reactions are often delayed or absent.4 posture platform.167 Their instability seemed to correlate
An anticipatory postural response in the soleus muscle with the clinical diagnosis so that children with spastic
normally seen in response to a perturbation of the forearm, hemiplegia exhibited reversals in the expected order of
is absent or reduced in these patients, 154 although long muscular activation, whereas children with ataxia demon-
latency responses to direct stretch of a muscle have been strated normal muscle sequencing yet fell frequently. The
observed to be enhanced in the Parkinson population in timing, direction, and amplitude of their postural reactions
both the upper arm155 and lower limb.156 Response laten- were disturbed, particularly when the expected sensory in-
cies to sudden platform displacements were found to be puts had been altered (see paradigm described in section
within the normal range,157,158 although the ability to sup- on Indicators of Vestibulospinal Dysfunction). Thus, pos-
press long-latency muscle reactions to a perturbation was tural abnormalities of children with cerebral palsy were
impaired in these patients even under supported condi- due either to muscle incoordination or instability as a
tions.159 When required to scale the magnitude of their re- result of an inability to deal with sensory conflict.
sponses to amplitude and velocity of backward platform Results of these clinical studies suggest that the long-
translations, patients with Parkinson’s disease produced latency, polysynaptic postural adjustments can be elicited
smaller than normal extensor bursts, lar ger than normal at the spinal level, but require modulation by supraspinal
flexor bursts, and smaller torque responses.160 On a sinu- structures to develop a suf ficient response threshold and
soidally moving treadmill, patients with Parkinson’s dis- gain. Possibly there are an inappropriate number of nerve
ease were able to maintain their balance with eyes open fibers within the damaged motor pathway to excite the mo-
by using their leg flexor muscles whereas healthy subjects toneuron pool, or the damaged pathway sends a reduced
activated their extensor muscles. Timing and amplitude of drive to the interneurons at segmental levels that would
this muscle activity were also impaired. 161 The inability normally facilitate the polysynaptic reflex response.162
to generate adequate force in the stabilizing muscles
appears, therefore, to be hampering successful postural re- Mechanisms for Recovery
actions in these patients. Inferring the contribution of the
basal ganglia or the impairment of vestibular information
of Postural Stability
during dynamic postural reactions in this patient popula- Identification of compensatory mechanisms will improve
tion is difficult, however, because the motor impairments therapeutic interventions that teach compensation for or
could be as much an ef fect of akinesia, rigidity, or aging adaptation to, destabilizing conditions. These mechanisms
as of disruptions in the postural control system. are studied through clinical research, but we must be cau-
Lesions in the motor cortex have also resulted in dis- tious about conclusions drawn about the function of an
turbances to the automatic postural reactions. Patients with anatomical site that are based strictly on the absence of
spastic paresis rarely exhibit disturbances of posture dur- motor control in the presence of specific deficits or dam-
ing quiet standing as in the Romberg test, but reactions to age. We must remember that responses generated in the
rapid displacements of the support surface indicate deficits absence of a sensory or motor signal do not reveal the
in the dynamic postural reactions. 162 Hemiplegic adults function of that input. Rather, these responses demonstrate
demonstrate delayed onsets, a failure to respond, and how the system operates in the absence of certain inputs.
3970_Ch06_085-109 25/06/14 6:43 PM Page 99
AP
0 0
⫺1 ⫺1
⫺2 ⫺2
⫺3 ⫺3
⫺4 ⫺4
⫺4 ⫺2 0 2 4 ⫺4 ⫺2 0 2 4
ML ML
Somatosensory Deficit
• Increased low frequency sway
• Delayed restabilization
• Increased sway with no vision
sway in individuals who have no impairments and in pa- appear.45,55,58 Instead, visual information is thought to be
tients without a functioning vestibular system, even when redundant unless both vestibular and somatosensory inputs
contact force levels are inadequate to provide physical are lost.182 To test the importance of visual inputs in the
support of the body.159,171 When proprioceptive feedback absence of labyrinthine inputs, sway was measured in
from the ankle was excluded or suppressed in normal sub- subjects standing on a stabilometer placed within a later-
jects during perturbations on a posture platform, 21,172 a ally tilting room. 54 At low frequencies of sinusoidal tilt
characteristic low-frequency (1 Hz) sway emer ged. Pos- (0.0025 to 0.1 Hz), patients with unilateral and bilateral
tural abnormalities have been observed with impairment labyrinthine deficits exhibited sway similar to that of nor-
of spinal pathways such as occurs with Friedreich’s ataxia, mal subjects. At higher frequencies (0.2 Hz), the patients’
a hereditary disorder af fecting the spinocerebellar path- sway increased beyond normal limits, indicating that pa-
ways and posterior columns.173 In the absence of feedback tients with vestibular deficit could rely on visual inputs at
from these pathways to the cerebellum, a significant delay lower frequencies, but suffered for the loss of vestibular
of the restabilizing response of the tibialis anterior muscle signals at higher frequencies.80,183 Labyrinthine deficit pa-
following dorsiflexing ankle rotations on a posture plat- tients on a stabilometer were better able to stabilize sway
form has been observed. 147 These patients exhibit lar ge when fixating on a stationary light.184 Patients became un-
lateral sway deviations in the low frequency range (less stable when an optokinetic stimulus was introduced,
than 1 Hz) with eyes closed, as do patients with tabes dor- which indicates that velocity information received through
salis.172 Patients with sensory polyneuropathy of the lower peripheral vision is the cause of the increased sway.
extremities demonstrate ataxia and instability during quiet The influence of velocity of the visual field on pos-
stance. Falls tend to occur when the eyes are closed, 173 tural control was further explored in a three-wall virtual
suggesting that visual inputs are necessary along with environment.185-187 Visual field motion was found to be
vestibular inputs in the absence of lower limb propriocep- very compelling for both healthy young and elder individ-
tor signals. uals, and produced changes in the postural response or-
Finally, cervical proprioceptors have been the focus ganization even when they were standing quietly on a hard
of investigations related to the diagnosis of dizziness surface. This finding justified using a virtual environment
and ataxia.174,175 The neck proprioceptors have intimate to test the effectiveness of a postural training program for
connections with the vestibular system and are probably individuals with labyrinthine disorders. 188 One woman
used both as feedforward and feedback to the vestibulo- had a bilateral labyrinthine deficit, and the other suffered
collic reflexes.176 Cervicogenic dizziness has been a con- from unremitting Ménière’s disease that did not respond
troversial diagnosis, however, because there are no hard to treatment. After being trained to stand in the dark on an
signs to identify the neck as the source of the dizziness.175 increasingly unstable sway referenced platform, these in-
Karlberg and colleagues177-179 have engaged in a series of dividuals were tested on the platform while performing a
studies to verify ataxia or vertigo of cervical origin. Using reaching task in the presence of a rotating visual field.
posturography in which stance was perturbed by a vibra- Center of pressure responses were shown to improve sig-
tory stimulus applied toward the calf muscles, they studied nificantly both immediately and 2 weeks following the
patients with recent onset of neck pain and vertigo but nor- training compared with performance on the task before
mal otoneurological findings. Results demonstrated dis- training.
turbed postural control in the patients with cervical vertigo In summary, patients lacking labyrinthine inputs be-
that differed from patients with vestibular neuritis. In come more dependent on accurate ankle proprioceptive
addition, dorsal neck muscle tenderness and tightness was and visual references to correctly or ganize their postural
found in a majority of the patients with cervicogenic dizzi- responses. Inappropriate or distorted signals along either
ness that was diminished following treatment for neck of these sensory pathways will produce increased sway
pain.180 These results suggest that disorders of the neck and falls in these patients. Although the sensory signals
need to be considered when assessing patients complain- often provide congruent information, inputs from any of
ing of dizziness, vertigo, and balance disturbances. these modalities are not necessarily redundant because
Visual signals are used to accurately detect and each represents different parameters and is effective within
reduce motion relative to the surround. 181,182 In normal a particular frequency range.80,126,127 Thus, falls observed
subjects, vision is very influential, but does not appear to in vestibular deficit patients, particularly following a
be an essential input for the recovery of balance. Many platform perturbation or in the absence of other sensory
studies have shown that simply removing vision will signals, may be caused by uncontrolled or poorly compen-
not produce significant changes in the postural response sated oscillations of intersegmental structures at particular
organization, although greater sway amplitudes may frequencies of sway.
3970_Ch06_085-109 25/06/14 6:43 PM Page 101
system have demonstrated declining function with age,200 increased static sway, and muscle weakness have been
these changes are not present in the central vestibular neu- cited as contributing to falls in the elderly,216,217 but none
rons. The gradual loss of labyrinthine acuity with age of these have been identified as causal factors. Attentional
prompts viewing the elderly population as a model for demands and disorganized postural strategies are more
compensation to vestibular dysfunction, but in the elderly, global parameters that have been tar geted as potentially
sensory loss occurs as a slow process along several feed- generative causes of falls.114,208,218-220 Increased instability
back pathways, not just the vestibular pathways. 199-204 on a moving platform 221,222 and during locomotion 223-225
Thus, their compensatory approach to postural instability has also been attributed to an increasingly rigid trunk with
may not be the same as in those patients who have expe- aging. It has been observed that older adults stif fen their
rienced an acute but sustained loss of a single input (see trunk to decrease the controlled degrees of freedom in an
Table 6-2). effort to make themselves more stable, 219,226 yet they still
Age-related trends in the vestibulo-ocular and opto- produce reduced head stabilization in space.227,228
kinetic reflexes have been shown to correlate well with A longitudinal study of elderly fallers 229 has found
anatomical changes found in the peripheral vestibular sys- significant changes in the mean frequency of postural
tem.202, 203 Declining gains and increased time delays have sway in the medial-lateral direction. A low-frequency
been seen in the optokinetic response (OKR), and de- component was identified in this plane suggesting a slow
creased VOR gains with larger phase leads appeared at postural drift during quiet standing. 230 On a posture plat-
frequencies below 1.5 Hz. This would suggest that elderly form, the stabilizing muscle synergies, found to appear in
subjects have an increased reliance on the visual tracking a temporally consistent fashion in young healthy subjects,
reflexes, and that increased visuomotor processing exhibit a disor ganized order of onset in the elderly .231
time could contribute to feedback delays and poor per- Latencies of EMG responses and of reaction times are
formance.202,204 Thus, elderly individuals will have more increased in the elderly population 218, 231, 232 as is quiet
difficulty detecting sensory signals indicating a loss of sta- sway.233, 234 Although both sway induced by platform per-
bility, and when they do, longer response latencies may turbation and quiet sway measures demonstrated signifi-
well interfere with their ability to produce timely stabiliz- cant aging-related decreases in stability,235 the differences
ing reactions. Older individuals who showed decline in between young and elderly were more pronounced for the
OKN and VOR function also showed poorer performance perturbed sway data. Some of the quiet sway measures,
on clinical measures of balance and gait as compared with however, were more successful in distinguishing elderly
those with less decline of these functions.203 fallers from nonfallers. 235 A study of elderly individuals
If conflicting sensory information is not suppressed, on a rotating posture platform114 has explored whether de-
but instead can influence and modify the weighting of all layed latencies of lower limb muscle responses are respon-
other sensory inputs, then older individuals may be par- sible for the failure to produce torque outputs necessary
ticularly disturbed in the presence of conflicting visual and to compensate for unexpected falling. Results indicate that
somatosensory information. Postural responses of older a disordered temporal relationship between tibialis ante-
subjects were poorly organized during combined support rior and soleus muscles, which are concurrently activated
surface perturbations and mental distraction tasks, 205,206 in younger individuals,45 resulted in decreased stabilizing
and the predictive components of posture were absent.207 ankle torques. Weakness of the tibialis anterior muscle has
Results from a number of studies 208-210 suggested that been described in the elderly,217 and could be a major con-
when two simultaneous tasks were required (e.g., postural tributor to this diminished torque response.
stabilization and manipulation), postural adjustments were Increased stiffening between the head and trunk has
delayed in the elderly. In an elderly subject with disruption also been reported in elderly subjects when attempting to
or deterioration of the mechanisms controlling, any dis- keep the head stationary in space when the trunk was mov-
traction from postural control may be dangerous. In fact, ing226, 227, 236 and during whole body postural control. 42
when maintenance of an upright position and stabilizing Elderly subjects exhibited larger joint torques and greater
gaze were both required, an increased incidence of falling trunk motion than young adults when attempting to stabi-
appeared in the elderly.211-213 lize on a translating platform and when standing on a nar-
Falls among the elderly are a major public health con- row beam,42, 227, 237, 238which could be a result of a stiffer
cern because they are the leading cause of injury-related mechanical system. If the elderly locked their head to their
death and of nonfatal injury in the United States. 214,215 trunk to decrease the controlled degrees of freedom, these
The dynamic process of maintaining an upright posture is greater torques would be transmitted to the head. These
compromised in the elderly as evidenced by this increased data imply that elderly subjects rely on active trunk me-
incidence of falling. Lengthened response latencies, chanics to coordinate head and trunk motion but the stiffer
3970_Ch06_085-109 25/06/14 6:43 PM Page 103
trunk results in less damping of the ascending forces and, 7. Radmark K. On the tipping reaction. Acta Oto-laryngol.
therefore, poorer stabilization. Thus, impaired balance in 1940;28:467.
8. Weisz S. Studies in equilibrium reactions. J Nervous Ment
the elderly may be produced by altered response synergies
Dis. 1938;88:150.
that are generated by delayed vestibulospinal and pro- 9. Norre ME, Forrez G, Beckers A. Functional recovery of
priospinal reflex responses and a postural strategy to posture in peripheral vestibular disorders. In: Amblard B,
increase stiffness of the aging musculoskeletal system. Berthoz A, Clarac F, eds. Posture and Gait: Development,
Adaptation and Modulation. Amsterdam: Elsevier; 1988:291.
10. Baloh RW, Honrubia V. Clinical Neurophysiology of the
Summary Vestibular System. Philadelphia: F.A. Davis; 1979.
11. Keshner EA. Virtual reality and physical rehabilitation:
We can draw the following conclusions about mechanisms a new toy or a new research and rehabilitation tool?
that contribute to postural stability from the existing data. J NeuroEng Rehab. 2004;1:8. http://www.jneuroengrehab
First, central neural processes influence stability in the form .com/content/1/1/8.
12. Curthoys SI. The interpretation of clinical tests of peripheral
of automatic, long-latency reactions, voluntary movements,
vestibular function. Laryngoscope. 2012;122:1342.
and changes in both the passive mechanical properties (e.g., 13. Jacobson GP, et al. Patterns of abnormality in cVEMP,
stiffness) and active force outputs (e.g., joint torques) of the oVEMP, and caloric tests may provide topological infor-
system. Second, the presence or absence of specific sensory mation about vestibular impairment. J Am Acad Audiol.
inputs (e.g., vestibular or proprioceptive) alters the magni- 2011;22:601.
14. Shin B-S, et al. Cervical and ocular vestibular-evoked
tude or temporal onset of the muscle response pattern,
myogenic potentials in acute vestibular neuritis. Clinical
whereas distortion of sensory inputs seems to rearrange the Neurophysiology. 2012;123:369.
directional organization of the muscle response patterns. 15. Colbatch JL. Vestibular evoked myogenic potentials in
Third, learning, attention, and predictive processes influ- multiple sclerosis. Clinical Neurophys. 2012;123:1693.
ence the performance of postural reactions, as does the 16. Gianoli GJ, Soileau JS. Acoustic neuroma neurophysio-
logic correlates: vestibular-preoperative, intraoperative,
motor activity in which the individual is currently engaged
and postoperative. Otolaryngol Clin N Am. 2012;45:307.
when the postural behavior is required. Finally, a particular 17. McCaslin DL, et al. The influence of unilateral saccular
compensatory strategy adopted by a patient may interfere impairment on functional balance performance and self-
with, rather than assist, postural stability. report dizziness. J Am Acad Audiol. 2011;22:542.
Clinicians and researchers need to identify the pre- 18. Furman JM. Role of posturography in the management of
vestibular patients. Otolaryngol Head Neck Surg. 1995;112:8.
planned and automatic components of a postural response
19. DiFabio RP. Sensitivity and specificity of platform postur-
to determine how best to influence the postural response or- ography for identifying patients with vestibular dysfunction.
ganization. Clinicians will need to have knowledge of the Phys Ther. 1995;75:290.
strengths and limitations in tests of postural control and 20. Norre ME. Posturography: head stabilisation compared with
strategies to challenge the postural system (changing visual, platform recording. Application in vestibular disorders.
Acta Otolaryngol Suppl (Stockh). 1995;520:434.
somatosensory cues or altering the complexity of sensory
21. Panosian MS, Paige GD. Nystagmus and postural instabil-
information) with compensation to identify functional- ity after headshake in patients with vestibular dysfunction.
related balance problems. Recognizing the multiple factors Otolaryngol Head Neck Surg. 1995;112:399.
that contribute to the outcome of a postural response should 22. Paloski WH, et al. Destabilization of human balance control
assist clinicians in determining the approach and effective- by static and dynamic head tilts. Gait Posture. 2006;23:315.
23. Paquet N, et al. Effects of fast head turns on head, trunk
ness of their intervention strategies for retraining and
and pelvis motions during standing and walking in patients
restoration of postural function. with unilateral vestibular deficit. J Vestib Res. 2006;16:279.
24. Nashner LM. Adapting reflexes controlling human posture.
Exp Brain Res. 1976;26:59.
References 25. Nashner LM. Fixed patterns of rapid postural responses
1. Barmack NH, Yakhnitsa V. Vestibular signals in the among leg muscles during stance. Exp Brain Res. 1977;
parasolitary nucleus. J Neurophysiol. 2000; 83:3559. 30:13.
2. Guedry FE. Perception of motion and position relative to 26. Nashner LM. Vestibular and reflex control of normal
the earth. An overview. Ann NY Acad Sci. 1992;656:315. standing. In: Stein RB, Pearson KG, Smith RS, Redford JB,
3. Young LR. Vestibular reactions to spaceflight: human eds. Control of Posture and Locomotion. New York:
factors issues. Aviat Space Envion Med. 2000;71:A100. Plenum Press; 1973:2918.
4. Brock S, Wechsler IS. Loss of the righting reflex in man. 27. Allum JHJ, Pfaltz CR. Visual and vestibular contributions
Arch Neurol Psychiat. 1927;17:12. to pitch sway stabilization in the ankle muscles of normals
5. Martin JP. Tilting reactions and disorders of the basal and patients with bilateral peripheral vestibular deficits.
ganglia. Brain. 1965;88:855. Exp Brain Res. 1985;58:82.
6. McNally WJ. Labyrinthine reactions and their relation to 28. Black FO, Shupert CL, Horak FB. Abnormal postural
the clinical tests. Proc Royal Soc Med. 1937;30:905. control associated with peripheral vestibular disorders.
3970_Ch06_085-109 25/06/14 6:43 PM Page 104
In: Pompeiano O, Allum JHJ, eds. Vestibulospinal Control 48. Melvill Jones G, Watt DGD. Observations on the control
of Posture and Movement. Progress in Brain Research. of stepping and hopping movements in man. J Physiol.
Amsterdam: Elsevier; 1988:263. 1971;219:709.
29. Nashner LM, et al. Organization of posture controls: an 49. Wicke RW, Oman CM. Visual and graviceptive influences
analysis of sensory and mechanical constraints. In: Allum on lower leg EMG activity in humans during brief falls.
JHJ, Hulliger M, eds. Afferent Control of Posture and Exp Brain Res. 1982;46:324.
Locomotion. Progress in Brain Research. Amsterdam: 50. Allum JHJ, Honegger F. A postural model of balance-
Elsevier; 1989:411. correcting movement strategies. J Vest Res. 1992;2:323.
30. Keshner EA, Woollacott MH, Debu B. Neck and trunk 51. Allum JHJ, Honegger F, Schicks H. The influence of a
muscle responses during postural perturbations in humans. bilateral peripheral vestibular deficit in postural synergies.
Exp Brain Res. 1988;71:455. J Vest Res. 1994;4:49.
31. Stockwell CW, Koozekani SH, Barin K. A physical model 52. Runge C, et al. Role of vestibular information in initiation
of human postural dynamics. In: Cohen B, ed. Vestibular of rapid postural responses. Exp Brain Res. 1998;122:403.
and Oculomotor Physiology. Ann NY Acad Sci. 1981; 53. Bles W, et al. The mechanism of physiological height
374:722. vertigo, II: posturography. Acta Otolaryngol (Stockh).
32. Nashner LM, McCollum G. The organization of human 1980;89:534.
postural movements: a formal basis and experimental 54. Bles W, et al. Compensation for labyrinthine deficits exam-
synthesis. Brain Behav. 1985;8:135. ined by use of a tilting room. Acta Otolaryngol (Stockh).
33. Horak FB, Nashner LM. Central programming of postural 1983;95:576.
movements: adaptation to altered support-surface configu- 55. Nashner LM, Berthoz A. Visual contributions to rapid motor
rations. J Neurophysiol. 1986;55:1369. responses during postural control. Brain Res. 1978;150:403.
34. Allum JHJ, Honegger F, Schicks H. Vestibular and propri- 56. Black FO, Wall C III, Nashner LM. Effects of visual and
oceptive modulation of postural synergies in normal sub- support surface orientation references upon postural
jects. J Vest Res. 1993;3:59. control in vestibular deficient subjects. Acta Otolaryngol.
35. Maki BE, McIlroy WE. The role of limb movements in 1983;95:199.
maintaining upright stance: the “change-in-support” 57. Sparto PJ, et al. Simulator sickness when performing gaze
strategy. Phys Ther. 1997;77:488. shifts within a wide field of view optic flow environment:
36. Pai YC, Patton J. Center of mass velocity-position predic- preliminary evidence for using virtual reality in vestibular
tions for balance control. J Biomech. 1997;30:347. rehabilitation. J NeuroEng Rehab. 2004;1:14. http://www
37. Bouisset S, Zattara M. Segmental movement as a perturba- .jneuroengrehab.com/content/1/1/14.
tion to balance? Facts and concepts. In: Winters JM, Woo 58. Vidal PP, Berthoz A, Millanvoye M. Difference between
SLY, eds. Multiple Muscle Systems: Biomechanics and eye closure and visual stabilization in the control of
Movement Organization. New York: Springer-Verlag; posture in man. Aviat Space Environ Med. 1982;53:166.
1990:498. 59. Woollacott MH, Shumway-Cook AT, Nashner LM. Postural
38. Burleigh A, Horak FB. Influence of instruction, prediction, reflexes and aging. In: Mortimer JA, ed. The Aging Motor
and afferent sensory information on the postural organiza- System. New York: Praeger; 1982:98.
tion of step initiation. J Neurophysiol. 1996;75:1619. 60. Di Fabio RP, Anderson JH. Effect of sway-referenced
39. Horak FB, Diener HC, Nashner LM. Influence of central visual and somatosensory inputs on human head move-
set on human postural responses. J Neurophysiol. ment and postural patterns during stance. J Vestib Res.
1989;62:841. 1993;3:409.
40. Maki BE, Whitelaw RS. Influence of expectation and 61. Horak FB, Nashner LM, Diener HC. Postural strategies
arousal on center-of-pressure responses to transient postural associated with somatosensory and vestibular loss. Exp
perturbations. J Vestib Res. 1993;3:25. Brain Res. 1990;82:167.
41. Horak FB, et al. Vestibular and somatosensory contribu- 62. Furman JM, Jacob RG. A clinical taxonomy of dizziness
tions to responses to head and body displacements in and anxiety in the otoneurological setting. J Anxiety
stance. Exp Brain Res. 1994;100:93. Disord. 2001;15:9.
42. Gu MJ, et al. Postural control in young and elderly 63. Peterka RJ. Sensorimotor integration in human postural
adults when stance is perturbed: dynamics. J Biomech. control. J Neurophysiol. 2002;88:1097.
1996;29:319. 64. Paquette C, Paquet N, Fung J. Aging affects coordination
43. Massion J, Gahery Y. Diagonal stance in quadrupeds: a pos- of rapid head motions with trunk and pelvis movements
tural support for movement. Prog Brain Res. 1979;50:2196. during standing and walking. Gait Posture. 2006;24:62.
44. Roberts TDM, Stenhouse G. Reactions to overbalancing. 65. Pang MY, et al. Balance performance in head-shake com-
Prog Brain Res. 1979;50:397. puterized dynamic posturography: aging effects and test-
45. Keshner EA, Allum JHJ, Pfaltz CR. Postural coactivation retest reliability. Phys Ther. 2011;9:246.
and adaptation in the sway stabilizing responses of normals 66. Park MK, et al. A head shake sensory organization test to
and patients with bilateral peripheral vestibular deficit. Exp improve the sensitivity of the sensory organization test in
Brain Res. 1987;69:66. the elderly. Otol Neurotol. 2012;33:67.
46. Greenwood R, Hopkins AL. Muscle responses during sud- 67. Honaker JA, Converse CM, Shepard NT. Modified head
den falls in man. J Physiol (Lond). 1976;254:507. shake computerized dynamic posturography. Am J Audiol.
47. Lacour M, Xerri C. Compensation of postural reactions 2009;18:108.
to free-fall in the vestibular neurectomized monkey. Exp 68. Lim HW, et al. Correlating the head shake-sensory
Brain Res. 1980;40:103. organizing test with dizziness handicap inventory in
3970_Ch06_085-109 25/06/14 6:43 PM Page 105
compensation after vestibular neuritis. Otol Neurotol. 88. Mancini M, et al. Postural sway as a marker of progres-
2012;33:211. sion in Parkinson’s disease: a pilot longitudinal study.
69. Mishra A, et al. Head shake computerized dynamic postur- Gait Posture. 2012;36:471.
ography in peripheral vestibular lesions. Am J Audiol. 89. Agrawal Y, et al. Disorders of Balance and Vestibular
2009;18:53. Function in US Adults: Data from the National Health
70. Roma AA. Use of the head shake-sensory organization test and Nutrition Examination Survey, 2001-2004. Arch
as an outcome measure in the rehabilitation of an individual Intern Med. 2009;169:938.
with head movement provoked symptoms of imbalance. 90. Bles W, de Jong JMBV. Uni- and bilateral loss of vestibular
J Geriatr Phys Ther. 2005;28:58. function. In: Bles W, Brandt T, eds. Disorders of Posture
71. Peterka RJ, Benolken MS. Role of somatosensory and and Gait. Amsterdam: Elsevier; 1986:127.
vestibular cues in attenuating visually induced human 91. Kapteyn TS, et al. Standardization in platform stabilome-
postural sway. Exp Brain Res. 1995;105:101. try being a part of posturography. Agressologie. 1983;
72. Bronstein AM, et al. Recovery from bilateral vestibular 24:321.
failure: implications for visual and cervico-ocular function. 92. Norre ME, Forrez G. Posture testing (posturography) in
Acta Otolaryngol Suppl. 1995;520 Pt 2:405. the diagnosis of peripheral vestibular pathology. Arch
73. Guerraz M, et al. Visual vertigo: symptom assessment, Otorhinolaryngol. 1986;243:186.
spatial orientation and postural control. Brain. 2001; 93. Hain T. Chapter 1, this volume.
124:1646. 94. Unterberger S. Neue objektive registrierbare vestibular-
74. Allum JH, et al. The control of head movements during iskorperdrehungen, erhalten durch treten auf der stelle.
human balance corrections. J Vestib Res. 1997;7:189. Der ‘Tretversuch.’ Arch Ohren Nasen Kehlkopfheilkd.
75. Gresty M. Stability of the head: studies in normal subjects 1938;145:478.
and in patients with labyrinthine disease, head tremor, and 95. Fukuda T. Statokinetic Reflexes in Equilibrium and
dystonia. Movement Disorders. 1987;2:165. Movement. Tokyo: Tokyo Univ Press; 1983.
76. Keshner EA, Peterson BW. Mechanisms controlling human 96. Bles W, de Jong JMBV, de Wit G. Somatosensory
head stability, I: head-neck dynamics during random rota- compensation for loss of labyrinthine function. Acta
tions in the vertical plane. J Neurophysiol. 1995;73:2293. Otolaryngol (Stockh). 1984;95:576.
77. Romberg MH. Manual of Nervous Diseases of Man. 97. Graybiel, A and Fregly, AR. A new quantitative ataxia
London: Sydenham Society; 1853:395. test battery. Acta Otolaryngol (Stockh). 1966;61:292.
78. Jacobson GP, et al. Insensitivity of the “Romberg test of 98. Lambrey S, Berthoz A. Combination of conflicting visual
standing balance on firm and compliant support surfaces” and non-visual information for estimating actively per-
to the results of caloric and VEMP tests. Ear Hear. 2011; formed body turns in virtual reality. Int J Psychophysiol.
32:e1-5. 2003;50:101.
79. Wall C III, Black FO. Postural stability and rotational 99. Keshner EA, Kenyon RV. Using immersive technology
tests: their effectiveness for screening dizzy patients. Acta for postural research and rehabilitation. Assist Technol.
Otolaryngol. 1983;95:235. 2004;16:54.
80. Xerri C, et al. Synergistic interactions and functional working 100. Sherman W, Craig A. Understanding Virtual Reality:
range of the visual and vestibular systems in postural control: Interface, Application, and Design. California: Morgan
neuronal correlates. In: Pompeiano O, Allum JHJ, eds. Kaufmann; 2002.
Vestibulospinal Control of Posture and Movement. Progress 101. Riva G, Mantovani F, Gaggioli A. Presence and rehabili-
in Brain Research. Amsterdam: Elsevier; 1988:193. tation: toward second-generation virtual reality applica-
81. Black FO. Vestibulospinal function assessment by moving tions in neuropsychology. J NeuroEng Rehab. 2004;1:9,
platform posturography. Amer J Otology (suppl). 1985;39. http://www.jneuroengrehab.com/content/1/1/9.
82. Allum JHJ, Keshner EA. Vestibular and proprioceptive con- 102. Carrozzo M, Lacquaniti F. Virtual reality: a tutorial.
trol of sway stabilization. In: Bles W, Brandt T, eds. Disor- Electroencephalogr Clin Neurophysiol. 1998;109:1.
ders of Posture and Gait. Amsterdam: Elsevier; 1986:19. 103. Keshner EA, Kenyon RV, Langston J. Postural
83. Allum JHJ, et al. Indicators of the influence a peripheral responses exhibit intra-modal dependencies with dis-
vestibular deficit has on vestibulo-spinal reflex responses cordant visual and support surface motion. J Vestib
controlling postural stability. Acta Otolaryngol (Stockh). Res. 2004;14:307.
1988;106:252. 104. Peitersen E. Measurement of vestibulospinal responses in
84. Cohen H, Keshner EA. Current concepts of the vestibular man. In: Kornhuber HH, ed. Handbook of Sensory Physi-
system reviewed, II: visual/vestibular interaction and ology, Vol. VI (2), Vestibular System. Berlin: Springer-
spatial orientation. Am J Occup Ther. 1989;43:331. Verlag; 1974:267.
85. Horlings CG, et al. Identifying deficits in balance control fol- 105. Baloh RW, Halmagyi GM. Disorders of the Vestibular
lowing vestibular or proprioceptive loss using posturographic System. New York: Oxford Univ Press; 1996.
analysis of stance tasks. Clin Neurophy. 2008;119:2338. 106. Black FO, Nashner LM. Vestibulo-spinal control differs
86. Varela DG, Carneiro JAO, Colafêmina JF. Static postural in patients with reduced versus distorted vestibular func-
balance study in patients with vestibular disorders using a tion. Acta Otolaryngol (Stockh). 1984;406:110.
three dimensional electromagnetic sensor system. Braz J 107. Norre ME. Posture in otoneurology. Acta Oto-Rhino-
Otorhinolaryngol. 2012;78:7. Laryngol Belgica. 1990;44:55.
87. Mancini M, et al. ISway: a sensitive, valid and reliable 108. Dow RS. The effects of bilateral and unilateral labyrinthec-
measure of postural control. J Neuroeng Rehabil. 2012; tomy in monkey, baboon, and chimpanzee. Am J Physiol.
9:59. 1938;121:392.
3970_Ch06_085-109 25/06/14 6:43 PM Page 106
109. Allum JHJ, Pfaltz CR. Postural control in man following 129. Guitton D, et al. Visual, vestibular and voluntary contribu-
acute unilateral peripheral vestibular deficit. In: Igarashi M, tions to human head stabilization. Exp Brain Res. 1986;
Black FO, eds. Vestibular and Visual Control of Posture 64:59.
and Locomotor Equilibrium. Basel: Karger; 1985:315. 130. Keshner EA, Cromwell R, Peterson BW. Mechanisms con-
110. Black FO, Wall C III, O’Leary DP. Computerized trolling human head stability, II: head-neck dynamics during
screening of the human vestibulospinal system. Ann random rotations in the horizontal plane. J Neurophysiol.
Otol Rhinol Laryngol. 1978;87:853. 1995;73:2302.
111. Keshner EA, Allum JHJ. Plasticity in pitch sway stabiliza- 131. Masson G, Mestre DR, Pailhous J. Effects of the spatio-
tion: normal habituation and compensation for peripheral temporal structure of optical flow on postural readjust-
vestibular deficits. In: Bles W, Brandt T, eds. Disorders of ments in man. Exp Brain Res. 1995;103:137.
Posture and Gait. Amsterdam: Elsevier; 1986:289. 132. Dijkstra TMH, Schoner G, Gielen CCAM. Temporal
112. Allum JHJ, et al. Organization of leg-trunk-head coordina- stability of the action-perception cycle of postural control
tion in normals and patients with peripheral vestibular in a moving visual environment. Exp Brain Res. 1994;
deficits. In: Pompeiano O, Allum JHJ, eds. Vestibulospinal 97:477.
Control of Posture and Movement. Progress in Brain 133. Roberts TDM. Reflex balance. Nature. 1973;244:156.
Research. Amsterdam: Elsevier; 1988:277. 134. Suzuki J, Cohen B. Head, eye, body and limb movements
113. Fetter M, Dichgans J. Vestibular tests in evolution, II: from semicircular canal nerves. Exp Neurol. 1964;
posturography. In: Baloh RW, Halmagyi GM, eds. 10:393.
Disorders of the Vestibular System. New York: Oxford 135. Magnus R. Physiology of posture. Lancet. 1926;2:531, 585.
Univ Press; 1996:256. 136. Gurfinkel VS, et al. Kinesthetic reference for human
114. Keshner EA, Allum JHJ, Honegger F. Predictors of less orthograde posture. Neurosci. 1995;68:229.
stable postural responses to support surface rotations in 137. Massion J. Postural control system. Curr Opin Neurobiol.
healthy human elderly. J Vest Res. 1993;3:419. 1994;4:877.
115. Okubo J, et al. Posture and gait in Ménière’s disease. 138. Keshner EA, Kenyon RV. The influence of an immersive
In: Bles W, Brandt T, eds. Disorders of Posture and Gait. virtual environment on the segmental organization of
Amsterdam: Elsevier; 1986:113. postural stabilizing responses. J Vestib Res. 2000;10:
116. Dichgans J, et al. Postural sway in normals and atactic 201.
patients: analysis of the stabilizing and destabilizing 139. Buchanan JJ, Horak FB. Emergence of postural patterns
effects of vision. Agressologie. 1976;17C:15. as a function of vision and translation frequency.
117. Kapteyn TS, De Wit G. Posturography as an auxiliary in J Neurophysiol. 1999;81:2325.
vestibular investigation. Acta Otolaryngol. 1972;73:104. 140. Lacour M, et al. Sensory strategies in human postural
118. Buchele W, Brandt T. Benign paroxysmal positional ver- control before and after unilateral vestibular neurotomy.
tigo and posture. In: Bles W, Brandt T, eds. Disorders of Exp Brain Res. 1997;115:300.
Posture and Gait. Amsterdam: Elsevier; 1986:101-111. 141. Uemura T, et al. Neuro-otological Examination. Baltimore:
119. Brink EE, Hirai N, Wilson VJ. Influence of neck afferents University Park Press; 1977.
on vestibulospinal neurons. Exp Brain Res. 1980;38:285. 142. Rudge P. Clinical Neurootology. London: Churchill
120. Peterson BW. The reticulospinal system and its role in Livingstone; 1983.
the control of movement. In: Barnes CD, ed. Brainstem 143. Brandt T, Dieterich M, Buchele W. Postural abnormalities in
Control of Spinal Cord Function. New York: Academic central vestibular brainstem lesions. In: Bles W, Brandt T,
Press; 1984:27. eds. Disorders of Posture and Gait. Amsterdam: Elsevier;
121. Wilson VJ, Ezure K, Timerick SJB. Tonic neck reflex 1986:141.
of the decerebrate cat: response of spinal interneurons 144. Dieterich M, Brandt T. Wallenberg’s Syndrome: lateropul-
to natural stimulation of neck and vestibular receptors. sion, cyclorotation, and subjective visual vertical in thirty-
J Neurophysiol. 1984;51:567. six patients. Ann Neurol. 1992;31:399-408.
122. Gdowski GT, McCrea RA. Neck proprioceptive inputs 145. Shimazu H, Smith CM. Cerebellar and labyrinthine
to primate vestibular nucleus neurons. Exp Brain Res. influences on single vestibular neurons identified by
2000;135:511. natural stimuli. J Neurophysiol. 1971;34:493.
123. Keshner EA. Head-trunk coordination during linear anterior- 146. Mauritz KH, Dichgans J, Hufschmidt A. Quantitative
posterior translations. J Neurophysiol. 2003;89:1891. analysis of stance in late cortical cerebellar atrophy of the
124. Imai T, et al. Interaction of the body, head, and eyes dur- anterior lobe and other forms of cerebellar ataxia. Brain.
ing walking and turning. Exp Brain Res. 2001;136:1. 1979;102:461.
125. Halmagyi GM, Curthoys IS. Otolith function tests. In: 147. Diener HC, et al. Characteristic alterations of long-loop
Herdman SJ, ed. Vestibular Rehabilitation. 2nd ed. “reflexes” in patients with Friedreich’s disease and late at-
Philadelphia: F.A. Davis; 2000:195. rophy of the cerebellar anterior lobe. J Neurol Neurosurg
126. Bilotto G, et al. Dynamic properties of vestibular reflexes Psychiat. 1984;47:679.
in the decerebrate cat. Exp Brain Res. 1982;47:343. 148. Horak FB, Diener HC. Cerebellar control of postural
127. Peterson BW, et al. The cervicocollic reflex: its dynamic scaling and central set in stance. J Neurophysiol. 1994;
properties and interaction with vestibular reflexes. 72:479.
J Neurophysiol. 1985;54:90. 149. Nashner LM, Grimm RJ. Analysis of multiloop dyscon-
128. Keshner EA, et al. Patterns of neck muscle activation in trols in standing cerebellar patients. In: Desmedt JE,
cats during reflex and voluntary head movements. Exp ed. Cerebellar Motor Control in Man: Long Loop
Brain Res. 1992;88:361. Mechanisms. Basel: Karger; 1978:300.
3970_Ch06_085-109 25/06/14 6:43 PM Page 107
150. Bastian A. Moving, sensing and learning with cerebellar 171. Jeka JJ. Light touch contact as a balance aid. Phys Ther.
damage. Curr Opin Neurobiol. 2011;21:596. 1997;77:476.
151. Dichgans J, Mauritz KH. Patterns and mechanisms of 172. Mauritz KH, Dietz V. Characteristics of postural instabil-
postural instability in patients with cerebellar lesions. In: ity induced by ischaemic blocking of leg afferents. Exp
Desmedt JE, ed. Motor Control Mechanisms in Health Brain Res. 1980;38:117.
and Disease. New York: Raven Press; 1983:633. 173. Kotaka S, Croll GA, Bles W. Somatosensory ataxia. In
152. Diener HC, Dichgans J. Pathophysiology of cerebellar Bles W, Brandt T, eds. Disorders of Posture and Gait.
ataxia. Movement Disorders. 1992;7:95. Amsterdam: Elsevier; 1986:178.
153. Dichgans J, Diener HC. Different forms of postural ataxia 174. Cohen LA. Role of eye and neck proprioceptive mecha-
in patients with cerebellar diseases. In: Bles W, Brandt T, nisms in body orientation and motor coordination.
eds. Disorders of Posture and Gait. Amsterdam: Elsevier; J Neurophysiol. 1961;24:1.
1986:207. 175. de Jong JMBV, Bles W. Cervical dizziness and ataxia.
154. Traub MM, Rothwell JC, Marsden CD. Anticipatory pos- In Bles W, Brandt T, eds. Disorders of Posture and Gait.
tural reflexes in Parkinson’s disease and other akinetic-rigid Amsterdam: Elsevier; 1986:185.
syndromes and cerebellar ataxia. Brain. 1980;103:393. 176. Wilson VJ, Melvill Jones G. Mammalian Vestibular
155. Berardelli A, Sabra AF, Hallett M. Physiological mecha- Physiology. New York: Plenum Press; 1979.
nisms of rigidity in Parkinson’s disease. J Neurol Neurosurg 177. Karlberg M, et al. Dizziness of suspected cervical origin
Psychiat. 1983;46:45. distinguished by posturographic assessment of human
156. Allum JHJ, et al. Disturbance of posture in patients with postural dynamics. J Vestib Res. 1996;6:37.
Parkinson’s disease. In: Amblard B, Berthoz A, Clarac F, 178. Karlberg M, et al. Postural and symptomatic improve-
eds. Posture and Gait: Development, Adaptation and ment after physiotherapy in patients with dizziness of
Modulation. Amsterdam: Elsevier; 1988:245. suspected cervical origin. Arch Phys Med Rehab. 1996;
157. Horak FB, Nutt JG, Nashner LM. Postural inflexibility 77:874.
in parkinsonian subjects. J Neurol Sci. 1992;111:46. 179. Karlberg M, Persson L, Magnusson M. Impaired postural
158. Dick JP, et al. Associated postural adjustments in Parkinson’s control in patients with cervico-brachial pain. Acta
disease. J Neurol Neurosurg Psychiatry. 1986;49:1378. Otolaryngol Suppl (Stockh). 1995;520:440.
159. Schieppati M, Nardone A. Free and supported stance in 180. Malmstrom EM, et al. Cervicogenic dizziness—
Parkinson’s disease: the effect of posture and ‘postural musculoskeletal findings before and after treatment and
set’ on leg muscle responses to perturbation, and its rela- long-term outcome. Disabil Rehabil. 2007;29:1193.
tion to the severity of the disease. Brain. 1991;114:1227. 181. Gantchev GN, Draganova N, Dunev S. Influence of the
160. Horak FB, Frank J, Nutt J. Effects of dopamine on pos- stabilogram and statokinesigram visual feedback upon
tural control in parkinsonian subjects: scaling, set, and the body oscillations. In: Igarashi M, Black FO, eds.
tone. J Neurophysiol. 1996;75:2380. Vestibular and Visual Control of Posture and Locomotor
161. Dietz V, et al. Balance control in Parkinson’s disease. Equilibrium. Basel: Karger; 1985:135.
Gait Posture. 1993;1:77. 182. Paulus W, Straube A, Brandt T. Visual postural perfor-
162. Benecke R, Conrad B. Disturbance of posture and gait in mance after loss of somatosensory and vestibular func-
spastic syndromes. In: Bles W, Brandt T, eds. Disorders tion. J Neurol Neurosurg Psychiat. 1987;50:1542.
of Posture and Gait. Amsterdam: Elsevier; 1986:231. 183. Waespe W, Henn V. Neuronal activity in the vestibular nu-
163. DiFabio RP, Badke MB. Influence of cerebrovascular clei of the alert monkey during vestibular and optokinetic
accident on elongated and passively shortened muscle stimulation. Exp Brain Res. 1977;27:523.
responses after forward sway. Phys Ther. 1988;68:1215. 184. Kotaka S, Okubo J, Watanabe I. The influence of eye
164. Badke MB, Duncan PW, Di Fabio RP. Influence of prior movements and tactile information on postural sway in
knowledge on automatic and voluntary postural adjust- patients with peripheral vestibular lesions. Auris-Nasus-
ments in healthy and hemiplegic subjects. Phys Ther. Larynx, Tokyo. 1986;13(Suppl II):S153.
1987;67:1495. 185. Wang Y, Kenyon RV, Keshner EA. Identifying the control
165. Dietz V, Mauritz KH, Dichgans J. Body oscillations in of physically and perceptually evoked sway responses
balancing due to segmental stretch reflex activity. Exp with coincident visual scene velocities and tilt of the base
Brain Res. 1980;40:89. of support. Exp Brain Res. 2010;201:663-672.
166. Dietz V, Berger W. Interlimb coordination of posture in 186. Dokka K, Kenyon RV, Keshner EA. Influence of visual
patients with spastic paresis. Brain. 1984;107:965. scene velocity on segmental kinematics during stance.
167. Nashner LM, Shumway-Cook A, Marin O. Stance pos- Gait Posture. 2009;30:211.
ture control in select groups of children with cerebral 187. Slaboda JC, Keshner EA. Reorientation to vertical modu-
palsy: deficits in sensory organization and muscular lated by combined support surface tilt and virtual visual
coordination. Exp Brain Res. 1983;49:393. flow in healthy elders and adults with stroke. J Neurol.
168. Allum JHJ, Honegger F. A postural model of balance- 2012;259:2664.
correcting responses. J Vestib Res. 1992;2:323. 188. Haran FJ, Keshner EA. Sensory reweighting as a method
169. Grossman GE, et al. Frequency and velocity of rotational of balance training for labyrinthine loss. J Neurol Phys
head perturbations during locomotion. Exp Brain Res. Ther. 2008;32:186.
1988;70:470. 189. Pfaltz CR. Vestibular habituation and central compensa-
170. Hirasaki E, et al. Effects of walking velocity on vertical tion. Adv Oto-Rhino-Laryngol. 1977;22:136.
head and body movements during locomotion. Exp Brain 190. Igarashi M. Vestibular compensation. Acta Otolaryngol
Res. 1999;127:117. (Stockh) (Suppl). 1984;406:78.
3970_Ch06_085-109 25/06/14 6:43 PM Page 108
191. Curthoys IS, Halmagyi GM. Clinical changes in vestibu- 210. Weeks DL, et al. Interaction between attention demand-
lar function with time after unilateral vestibular loss. ing motor and cognitive tasks and static postural stability.
In: Herdman SJ, ed. Vestibular Rehabilitation. 2nd ed. Gerontology. 2003;49:225.
Philadelphia: F.A. Davis; 2000:172. 211. Tinetti ME, Ginter SF. Identifying mobility dysfunctions
192. Hart CW, McKinley PA, Peterson BW. Compensation fol- in elderly patients. Standard neuromuscular examination
lowing acute unilateral total loss of peripheral vestibular or direct assessment? JAMA. 1988;259:1190.
function. In: Graham MD, Kemink JL, eds. The Vestibular 212. Tinetti ME, Speechley M. Prevention of falls among the
System. Neurophysiologic and Clinical Research. New York: elderly. N Engl J Med. 1989;320:1055.
Raven Press; 1987:187. 213. Skinner HB, Barrack RL, Cook SD. Age-related declines
193. Bouisset S, Zattara M. A sequence of postural movements in proprioception. Clin Orthop. 1984;184:208.
precedes voluntary movement. Neurosci Letters. 1981; 214. Gryfe CI, Amies A, Ashley MJ. A longitudinal study of
22:263. falls in an elderly population, I: incidence and morbidity.
194. Layne CS, Abraham LD. Interactions between automatic Age Aging. 1977;6:201.
postural adjustments and anticipatory postural patterns 215. Sattin RW, et al. The incidence of fall injury events
accompanying voluntary movement. Intern J Neurosci. among elderly in a defined population. Am J Epidemiol.
1991;61:241. 1990;131:1028.
195. Jeannerod M. The contribution of open-loop and closed- 216. Manchester D, et al. Visual, vestibular and somatosen-
loop control modes in prehension movements. In: sory contributions to balance control in the older adult.
Kornblum S, Requin J, eds. Preparatory States and J Gerontol. 1989;44:M118.
Processes. Hillsdale, NJ: Lawrence Erlbaum Assoc; 217. Whipple RH, Wolfson LI, Amerman PM. The relationship
1984:323. of knee and ankle weakness to falls in nursing home resi-
196. Keshner EA, Hain TC, Chen KC. Predicting control dents: an isokinetic study. J Am Geriatr Soc. 1987;35:13.
mechanisms for human head stabilization by altering 218. Stelmach GE, et al. Age related decline in postural con-
the passive mechanics. J Vestib Res. 1999;9:423. trol mechanisms. Int J Aging Hum Develop. 1989;29:205.
197. Viviani P, Berthoz A. Dynamics of the head-neck system 219. Woollacott MH. Age-related changes in posture and
in response to small perturbations: analysis and modeling movement. J Gerontol. 1993;48:56.
in the frequency domain. Biol Cybern. 1985;19:19. 220. Brown LA, Shumway-Cook A, Woollacott MH. Attentional
198. Chen KJ. Identification of Voluntary and Reflex Stabiliza- demands and postural recovery: the effects of aging.
tion Strategies of Head Control [Doctoral Dissertation, J Gerontol A Biol Sci Med Sci. 1999;54:M165.
Department of Biomedical Engineering]. Evanston IL: 221. Allum JH, et al. Age-dependent variations in the direc-
Northwestern University; 2001. tional sensitivity of balance corrections and compensa-
199. Bergstrom B. Morphology of the vestibular nerve, II: the tory arm movements in man. J Physiol. 2002;542:643.
number of myelinated vestibular nerve fibers in man at 222. Wu G. Age-related differences in body segmental move-
various ages. Acta Otolaryngol. 1973;76:173. ment during perturbed stance in humans. Clin Biomech.
200. Richter E. Quantitative study of human Scarpa’s ganglion 1998;13:300.
and vestibular sensory epithelia. Acta Otolaryngol. 1980; 223. Accornero N, et al. Clinical multisegmental posturography:
90:199. age-related changes in stance control. Electroencephalogr
201. Rosenhall U. Degenerative patterns in the aging human Clin Neurophysiol. 1997;105:213.
vestibular neuro-epithelia. Acta Otolaryngol. 1973;76:208. 224. Gill J, et al. Trunk sway measures of postural stability
202. Peterka RJ, Black FO. Age-related changes in human during clinical balance tests: effects of age. J Gerontol
vestibulo-ocular reflexes: pseudorandom rotation tests. Med Sci. 2001;56A:M438.
J Vestib Res. 1990;1:61. 225. Wu Q, et al. Stability and control of human trunk move-
203. Kerber KA, Ishiyama GA, Baloh RW. A longitudinal ment during walking. Comput Methods Biomech Biomed
study of oculomotor function in normal older people. Eng. 1998;1:247.
Neurobiol Aging. 2006;27:1346. 226. Allum JH, Carpenter MG, Adkin AL. Balance control
204. Peterka RJ, Black FO, Schoenhoff MB. Age-related analysis as a method for screening and identifying
changes in human vestibulo-ocular reflexes: sinusoidal balance deficits. Ann N Y Acad Sci. 2001;942:413.
rotation and caloric tests. J Vestib Res. 1990;1:49. 227. Keshner EA. Modulating active stiffness affects head sta-
205. Shumway-Cook AM, et al. The effects of two types of bilizing strategies in young and elderly adults during trunk
cognitive tasks on postural stability in older adults with rotations in the vertical plane. Gait Posture. 2000;11:1.
and without a history of falls. J Gerontol A Biol Sci Med 228. Keshner EA. Head-trunk coordination in elderly subjects
Sci. 1997;52:M232. during linear anterior-posterior translations. Exp Brain
206. Stelmach GE, Zelaznik HN, Lowe D. The influence of Res. 2004;158:213, http://dx.doi.org/10.1007/s00221-
aging and attentional demands on recovery from postural 004-1893-2.
instability. Aging (Milano). 1990;2:155. 229. Maki BE, Holliday PJ, Topper AK. A prospective study
207. Nouillot P, Bouisset S, Do MC. Do fast voluntary move- of postural balance and risk of falling in an ambulatory
ments necessitate anticipatory postural adjustments even and independent elderly population. J Gerontol Med Sci.
if equilibrium is unstable? Neurosci Lett. 1992;147:1. 1994;49:M72.
208. Shumway-Cook A, Woollacott M. Attentional demands 230. McClenaghan BA, et al. Spectral characteristics of ageing
and postural control: the effect of sensory context. postural control. Gait Posture. 1995;3:123.
J Gerontol A Biol Sci Med Sci. 2000;55:M10. 231. Woollacott MH. Gait and postural control in the aging
209. Teasdale NC, et al. On the cognitive penetrability of adult. In: Bles W, Brandt T, eds. Disorders of Posture
posture control. Exp Aging Res. 1993;19:1. and Gait. New York: Elsevier; 1986:325.
3970_Ch06_085-109 25/06/14 6:43 PM Page 109
232. Studenski S, et al. The role of instability in falls among 236. Keshner E, Chen KJ. Mechanisms underlying head stabi-
older persons. In: Duncan PW, ed. Balance. VA: American lization in the elderly during sagittal plane rotations.
Physical Therapy Association; 1990:57. J Motor Behav. 1996;28:324.
233. Hasselkus BR, Shambes GM. Aging and postural sway in 237. Woollacott MH, von Hosten C, Rosblad BP. Relation
women. J Gerontol. 1975;30:661. between muscle response onset and body segmental
234. Overstall PW, et al. Falls in the elderly related to postural movements during postural perturbations in humans.
imbalance. Brit Med J. 1977;1:261. Exp Brain Res. 1988;72:593.
235. Maki BE, Holliday PJ, Fernie GR. Aging and postural 238. Tang PF, Woollacott MH. Inefficient postural responses
control. A comparison of spontaneous- and induced-sway to unexpected slips during walking in older adults.
balance tests. J Am Geriatr Soc. 1990;38:1. J Gerontol A Biol Sci Med Sci. 1998;53:M471.
3970_Ch07_110-120 25/06/14 7:04 PM Page 110
CHAPTER 7
Disability
in Vestibular
Disorders
Natalia A. Ricci, PhD, PT ■ Helen S. Cohen, EdD, OTR, FAOTA
Vestibular disorders are characterized by vertigo, disequi- Society of Physical and Rehabilitation Medicine sponsored
librium, oscillopsia, and autonomic signs. These problems a workshop to identify the health conditions that are most
can contribute to reduced independence in activities of associated with disability and are amenable to rehabilita-
daily living and health-related quality of life (HRQoL). 1-3 tion interventions.9 Participants, who were physicians and
Most vestibular disorders are relatively benign, but they other health-care providers who specialize in rehabilitation,
can still cause significant problems in the ability to func- were generally unaware of vestibular disorders. In total,
tion.1 Vestibular disorders are also burdensome to society participants identified 103 rehabilitation-relevant health
as a drain on the economy ,4 because of lost work hours, conditions, some of which were related to vestibular dis-
decreased participation in society outside the home, and eases, such as hearing loss and falls. Participants failed to
increased health-care costs. Diagnostic testing, alone, does identify disorders of vestibular function or other diseases
not provide information about the need for intervention. of the inner ear as significant and treatable problems. This
The patient’s overall health, functional status, and personal chapter will elucidate the concept of disability, the interface
goals are important in determining the need for care and between disability and vestibular disorders, and the assess-
the type of intervention.5 ment tools used to evaluate functional status.
“Dizziness” and vertigo are among the most common
complaints in medical practice, af fecting approximately
20% to 30% of people in the general population. 6 These
Concepts of Disability
symptoms are relatively more common in the older pop- Confusion in disability terminology impairs communica-
ulation. From the National Health Interview Survey, USA, tion among investigators, clinicians, and patients. 1 The
among 37 million elderly persons, 7 million persons National Institutes of Health (NIH) used the term “func-
(19.6%) reported a problem with dizziness or balance in tional limitations” to refer to limitations in functioning in
the preceding 12 months. 7 On a German survey (n = the immediate environment for basic self-care skills and
1003), dizziness/vertigo had a prevalence of 22.9% within other essential activities of daily living. 10 The NIH used
the last 12 months and an incidence (first episode) of the term “disability” to describe how the individual inter-
3.1%. For vestibular vertigo, the prevalence was 4.8% and acts with the social environment, and used the term “so-
the incidence was 1.4%.8 cietal limitations” to describe how barriers defined by laws
Despite the statistics cited above, the significant im- or social policy restrict functional performance.
pact of vestibular disorders on functional performance is One of the first widely used models, the Nagi disabil-
still not widely recognized. For example, the International ity framework, used basic concepts of active pathology ,
110
3970_Ch07_110-120 25/06/14 7:04 PM Page 111
impairment, functional limitation, and disability .11,12 In In this taxonomy, disability combines impairments, limi-
this framework, disability was defined as “limitation in tations, and restrictions as the negative ef fect between a
performance of socially defined roles and tasks within a health condition and contextual factors (environmental and
sociocultural and physical environment,” 11 similar to the personal factors).17,19 The ICF has been adopted by the
NIH definition of disability. World Report on Disability as the conceptual framework
The International Classification of Impairments, Dis- for understanding functioning and disability.19,21
abilities, and Handicaps (ICIDH)13 was an attempt to de- Using the ICF concepts, reduced vestibular function,
velop a standard terminology for the consequences of as indicated by tests described elsewhere in this book, is
disease.5 The ICIDH classified three central concepts re- impairment. For example, a vestibular impairment caused
lated to disease and health conditions: impairment, dis- by damage to the vestibular nerve might cause a reduced
ability, and handicap. In this model, disability was defined vestibulo-ocular reflex gain. Many people with vestibular
as “any restriction or lack of ability to perform an activity disorders have limitations in performing activities of daily
in the manner or within the range considered normal for a living.8 Natural or man-made environmental factors can
human being.”13 In other words, it defined disability with trigger vestibular symptoms, such as poor lighting, heights,
reference to individual functioning. Handicap was defined open space, sound pollution, or rough terrain. 4,22 Those
as “a disadvantage that limits or prevents the fulfillment environmental interactions can cause anxiety, depression,
of a role that is normal (social and cultural factors) for that and social isolation because of restrictions in participation
individual.” The ICIDH used impairment, defined as ab- outside the home.8
normalities of body structure or system function, as the
cause of disability and handicap.
In the Disablement Process model, 14 disability was
Assessments of Disability
defined as a process of the impacts of chronic and acute Measurements of health status (i.e., function/disability and
conditions on individual function and in society . That quality of life) are crucial components of patient care, the
model combined the concepts of disability and handicap, use of which help the clinician to design rehabilitation pro-
possibly leading to confusion. grams, contribute to policy goals, and monitor the ef fec-
The medical model of disablement is based on the tiveness of health care. 23 Many disability assessments
theory that disability is a consequence of body structure have been developed, some more useful than others. Most
or functional decline, a personal problem. By contrast, the of them are self-assessments, in which the patient rates
social model of disablement is based on the theory that him- or herself. Detailed questions and detailed rating
disability is a result of the lack of opportunities in a per - scales may help the patient to describe performance more
son’s physical and social environment; thus, the problem accurately than open-ended questions. Because disability
is caused by society.5,15,16 Both points of view are valid. is subjective, however, outcomes from self-rating scales
In real life, health conditions and social/environmental have limitations that may reflect the patient’s beliefs more
factors affect many of the same people. The process of dis- than the patient’s actual status. 23 Therefore, self-rating
ablement is probably caused by the complex relationship may not correlate with the impressions of the patient’s sig-
between biological and social factors.16 nificant others, that is, the people closest to the patient. Il-
The biopsychosocial model of disability is currently literacy and use of questions that do not apply to that
the dominant perspective. 12,17 Therefore, the ICIDH was patient’s individual situation can confound assessment and
revised and replaced with the International Classification result in unreliable answers.24
of Functioning, Disability and Health (ICF). 18,19 The ICF Some strategies can be used to address some weak-
complements the International Classification of Diseases, nesses of the self-assessments. Patients can under- or over-
Injuries, and Causes of Death (ICD-10), to give a more estimate their performance skills, so some performance
complete understanding of individual people and popula- tests or direct observation can be useful. 24 For example,
tion health status. 5,16,20 The classification covers any dis - to evaluate difficulty walking, the clinician may ask the
turbance in terms of functional states following the patient about it, use some objective tests in which the pa-
domains: body functions, body structures, activities, and tient may perform as well as possible to impress the clini-
participation.5,15,18 The loss or abnormality of a body part cian, or just observe the patient walking into or out of the
or function is impairment. Difficulties in the ability to ex- office when the patient is unlikely to be aware of being
ecute activities are limitations, and problems in involve- observed. The patient’s significant others may be inti-
ment in life situations are participation restrictions. These mately involved with the diagnostic and rehabilitation
functional states can be influenced positively or negatively process.25 Therefore, evaluating their perceptions of the
by contextual factors, including environmental or personal. patient’s ability to function is important. Families and
3970_Ch07_110-120 25/06/14 7:04 PM Page 112
friends may over - or underestimate patients’ abilities. Disease-specific assessments are designed for special pa-
Sometimes those perceptions are not health related but tient populations with the goal of measuring clinical
reflect some long-established patterns in some people’ s changes after implementing a plan of care. 29 We discuss
interpersonal relationships.26 Patients may perceive them- the most widely used generic and specific assessments for
selves as more independent than their significant others patients with vestibular disorders.
may perceive them, especially for personal care skills, as
suggested by scores on the Vestibular Disorders Activities
Generic Disability Assessments
of Daily Living scale (VADL).26 Similarly, on the Vertigo
Symptom Scale (VSS), spouses tended to overestimate Three generic assessments have been used with patients
vertigo severity compared with patients. 25 So, the chal- who have vestibular disorders. The Short-Form-36 Health
lenge is not to choose one perspective over another, but to Survey (SF-36)30 has been widely used to evaluate
combine them.27 These additional kinds of assessments can HRQoL. The Functional Independence Scale (FIM)31 is a
increase costs and time during evaluations. Some behaviors better choice for a more detailed functional activity level.
may not be observed because they are unique to the pa- The ICF18 has been used for a comprehensive evaluation
tient’s living environment or are too personal, or because of disability.
of the subjective nature of perception of quality of life. The SF-36 was designed as a generic indicator of
The points of view of dif ferent professionals affect health status (functioning and well-being) in any patient
their assessments of disability. For example, physicians group and in population surveys.23 This 36-item scale has
are most concerned with symptoms and signs; physical been used worldwide, with several translations, with good
therapists and occupational therapists are more concerned validity and reliability.30 It is divided into two categories
with the way people perform daily life activities; coun- with four domains per category: physical functioning,
selors and psychologists may be more concerned with the role-physical, bodily pain, general health, vitality , social
emotional and social impacts of the health condition. All functioning, role-emotional, and mental health. The first
of them are concerned about HRQoL. Once the clinician four domains are in physical health; the other four do-
knows what to measure, he or she should identify relevant mains are in mental health. The assessment uses a 5-point
measurement instruments.28 Fortunately, the available scale. For the final score, some norm-based scoring algo-
self-perceived measures are low cost, easy to use, and re- rithms must be used. The final score ranges from 0 to 100,
quire minimal equipment. Some scales are more time con- with 100 indicating the best HRQoL. One study showed
suming than others, and some scales place dif ference that, after vestibular rehabilitation, the SF-36 was less re-
emphases on self-care activities or psychosocial interac- sponsive to change (Physical domain: 6.67% and Mental
tions. Therefore, the clinician should select the level of domain: 4.35%) than the Dizziness Handicap Inventory
detail desired for screening, the specificity of the scale for (DHI), a specific-measure (11.94%).32 Another study re-
different constructs, and the comprehensiveness of the vealed that patients with chronic dizziness had scores 38%
scale. For non–English-speaking patients, the availability to 87% of normative values for the 8 domains, with the
of the scale in the patient’s native language may also affect lowest scores on role-physical and role-emotional do-
the choice of a scale. mains.33 It is an important assessment and reveals poor
Some other factors also affect the selection of a scale. HRQoL for patients with vestibular disorders, but it has
The interests and needs of the individual patient, or target some weaknesses. It does not seem suitable to describe
population, the dif ficulty understanding the items and changes. Some items are not related to symptoms of
questions, the severity of the problem, and the time needed vestibular disorders, such as the domain for bodily pain.
to use the measure are factors to consider . The clinician The scale is cumbersome, and the scoring method can be
should know if the scale is sensitive to change, so that time-consuming in daily practice compared with disease-
treatment results can be quantified, and should know about specific measures.
the psychometric properties of the scale, such as the va- The 18-item FIM is a well-normed scale, developed
lidity and reliability. A good scale has high reliability, sen- by the Uniform Data System for Medical Rehabilitation
sitivity, specificity, and validity. to measure physical and cognitive disability in terms of
Furthermore, the clinician must choose between a level of care required. It is applicable to patients of all ages
generic scale and a disease-specific scale. Generic health and with all diagnoses, and it is especially useful to plan-
status measures are broadly applicable across diverse dis- ning and quantifying rehabilitation outcomes.31 It is not a
eases, disease severity, health status, health interventions, comprehensive scale, because it covers only basic activi-
and demographic subgroups. They summarize concepts ties of daily living and not complex, instrumental activities
that apply to different health conditions and populations. such as shopping or driving. The assessment includes
3970_Ch07_110-120 25/06/14 7:04 PM Page 113
physical and cognitive domains covering self-care, sphinc- be linked to specific ICF categories, most of them related
ter control, mobility, locomotion, communication, and to personal strategies of coping. Alghwiri et al3 described
cognition.23 The FIM uses a 7-point scale. The total score and compared the ICF to the concepts covered by eight
is calculated by summing all the items.The total score can clinical self-report measures used in vestibular rehabilita-
range from 18 to 126; higher scores indicate greater inde- tion. The questionnaires provided 164 items with a total
pendence. The ratings indicate actual performance in daily of 312 meaningful concepts. The concepts were linked to
life rather than the patient’s potential for performance, and 51 different ICF categories: 19 categories related to “body
scores may be based on observation. Using the FIM can functions,” 30 categories to “activities and participation,”
be time-consuming, however, and staff must be trained to and 2 categories related to “environmental factors.” Forty-
administer it. Some items can be performed easily by pa- two concepts could not be linked to any of the ICF com-
tients with vestibular disorders, such as eating and sphinc- ponents, including “moving the head into dif ferent
ter control, which may be the reason why elderly patients directions,” “moving in or out of the bathtub or shower,”
with vestibular disorders presented high FIM total scores and “avoiding certain activities, positions.” These studies
(118.5 points) in one study.34 highlight the importance of the relationship between the
The ICF is a comprehensive assessment with 1,434 individual’s ability to function and the environment. Al-
categories.4,35,36 The ICF uses a 5-point scale, and an item though the ICF has a huge range of categories, some im-
can also be scored 8 (not specified) or 9 (not applicable). portant concepts for understanding disability in people
Evaluating all ICF categories is impossible, so two alterna- with vestibular disorders are not included in the ICF clas-
tive strategies have been developed. ICF categories can be sification system (e.g., transferring into and out of the
linked to related items in disease-specific questionnaires, 3 bathtub or shower).3 Some of those concepts are included
which begs the question of whether the ICF is needed and in one disease-specific assessment, the VADL.40,41 Those
if the diagnosis-specific questionnaires are more useful. concepts should be added to a future revision of the ICF.
Also, core sets have been developed that include only cat- Generic measures have a place in rehabilitation for
egories that are typical and essential to describe a specific comparing outcomes in disparate groups of patients and
health condition.9,20,35 Several core sets have been devel- across facilities and even nations. Unfortunately , these
oped for health conditions that cause common disabilities. measures may not address problems of concern for par-
A vestibular core set was published recently.37 ticular health conditions. Also, they are not sensitive
Two studies examined patients with Ménière’ s dis- enough to vestibular disorders to capture the impact of
ease using the ICF.38,39 Most of the ef fects listed by the vertigo and disequilibrium on the patient’s everyday life.42
patients came from impairments (70%), following by ac- Assessments that are specific to a particular health prob-
tivity limitations (39%), participation restrictions (47%), lem are more likely to be relevant in everyday practice and
environmental factors (16%), and personal contextual fac- for therapeutic treatment planning.
tors (28%). In the category of sensory functions, impair -
ments in hearing, symptoms of vertigo, tinnitus, and
Disability Assessments that Are Specific
imbalance were the most frequent. In the category of ac-
to Vestibular Disorders
tivity limitations, patients reported problems with com-
munication, difficulty walking in the dark, and driving in A wide variety of disability-specific measures are avail-
specific circumstances (long roads, unfamiliar place, and able, but many of them are not comparable because they
dark). In the category of participation, patients were re- assess different aspects of disability.20 Specific self-rated
stricted for work and for performance of recreational and scales have been developed to evaluate patients with
leisure activities. In the category of environmental con- vestibular disorders such as the DHI,43 Vertigo Handicap
textual factors, patients reported changes in diet to manage Questionnaire (VHQ),44 VSS,45 Activities-specific Bal-
their condition. Patients also described problems with un- ance Confidence scale (ABC scale), 46 Dizzy Factor
certainty of life because of the unpredictable course of Inventory (DFI),47 UCLA- Dizziness Questionnaire
their Ménière’s disorder. (UCLA-DQ),48 Vertigo, Dizziness, Imbalance Question-
Müeller et al4 developed an international standard for naire (VDI),49 VADL,40,41 Vestibular Rehabilitation Ben-
the description of functioning and disability in patients efit Questionnaire (VRBQ),50,51 and Vestibular Activities
with vertigo and dizziness based on the ICF. They found and Participation (VAP).52 The questionnaires have dif-
471 concepts in the patients’ interviews that were linked ferent scopes; therefore, they include several dif ferent
to 142 different ICF-categories (40 body functions cate- constructs or specific items.3,4,51
gories, 62 activity and participation categories, and 40 en- The 25-item DHI is the oldest and most widely used
vironmental factors). Four percent of concepts could not self-assessment for patients with vestibular disorders. The
3970_Ch07_110-120 25/06/14 7:04 PM Page 114
DHI evaluates the physical factors and the functional and its responsiveness. The scale has been translated into
emotional consequences of vestibular disease.43 The ques- four languages (German, 65 Afrikaans,66 Turkish,67 and
tionnaire is divided into physical (seven items), emotional Spanish68). This questionnaire is about symptoms; it is not
(nine items), and functional (nine items) subscales. It uses intended to measure other constructs. The VSS may be
a 3-point scale: “yes” (4 points), “sometimes” (2 points) useful when assessing patients who have dif ficulty de-
and “no” (0 points). The total score is obtained by sum- scribing their symptoms.
ming the item scores; the maximum possible score is 100. The 16-item ABC scale is frequently used to evaluate
Higher scores indicate more severe handicap. It has high patients with vestibular disorders, but it is the only scale
internal consistency (␣ = 0.89) and reliability (r = 0.97).43 that was not developed for this purpose. It was developed
It has been translated into several languages including to assess self-perceived balance confidence in performing
some cultural variations (Argentinian Spanish,53 Italian,54 daily activities in community-dwelling seniors. 46 It is
French,55 Arabian,56 Japanese,57 Hebrew,58 Brazilian scored on an 11-point scale, from 0 (“no confidence”) to
Portuguese, 59 Chinese, 60 Spanish, 61 Swedish, 62 and 100% (“complete confidence”) indicating how confident
German63).The three response choices—yes, sometimes, the patient perceives him- or herself to be when perform-
or no—make the DHI quick and easy to use. Interpretation ing activities that involve balance. The total score is the
may seem easy but the meaning of items rated “some- mean of all items. When used with patients with vestibular
times” may be unclear. Also, it does not provide a broad disorders, the ABC scale has a negative moderate corre-
view of the patient, and it is unable to detect small lation with the DHI (r = −0.635), high internal consistency
changes. Despite the DHI’s responsiveness after vestibular (␣ = 0.95), and good reliability for individual items (ICC
rehabilitation, the scale is not useful for treatment plan- = 0.67 to 0.92).71 It is widely used and has been translated
ning, because it does not indicate which tasks or skills into several languages (German, 69 Canadian French,70
should be addressed during rehabilitation.23 In particular, Turkish,71 Chinese,72 and Swedish73). It has been used for
although the DHI items are relevant to symptom context,42 a variety of health conditions including stroke, Parkinson’s
the omission of important self-care skills is a significant disease, and lower limb amputation as well as vestibular
weakness. disorders and disequilibrium of aging. The ABC scale in-
The 22-item VHQ was created to describe common cludes some important activities such as walking up and
social, psychological, and behavioral context experienced down stairs, but it does not address skills that may be af-
by patients with vestibular impairment. It is divided into fected by vertigo such as rolling over in bed. Thus, the
4 domains: restriction of activities, social anxieties, fear ABC scale, alone, may be insufficient for many patients.
of vertigo, and severity of vertigo attacks. It uses a 5-point It is, however, an easy tool to use and may give some
scale, 0 (no handicap) to 4 (maximum handicap).The final patients some insight into their balance problems.24
score is calculated based on the “percentage handicap,” in The 44-item DFI was developed for use as a
which the item average score is multiplied by 25 giving a preliminary screening or as part of a comprehensive as-
maximum score of 100%. The VHQ has high internal con- sessment battery.47 The inventory was based on the Mul-
sistency for the total score (␣ = 0.93) and test-retest reli- tidimensional Pain Inventory and the DHI but with new
ability showed no significant change.44 The questionnaire items added based on the author’s clinical experience. It
has been translated into German. 64 This scale provides a uses a 5-point scale to assess 3 domains (symptom fac-
good understanding of the patient’s anxieties and behav- tors, responses of significant other , and activity level).
ioral restrictions that lead to handicap, so it can be helpful Further testing for reproducibility, validity (discriminant
for psychologists and other professionals who work with and convergent), and responsiveness analysis should be
coping strategies. It is not so useful for physical therapists performed.42 The domain of “responses of significant
and occupational therapists, who are concerned with per- other” is a strength of the scale. The omission of self-
formance of daily life activities. care tasks and the length of time to complete the scale
The 27-item VSS evaluates symptoms related to are weaknesses.
vestibular disorders. It is divided into four subscales: som- The 5-item UCLA-DQ uses a 5-point qualitative
atization, autonomic symptom, acute attack of vertigo, and scale for patients to characterize their vertigo based on fre-
vertigo of short duration. 45 It is scored on a 6-point scale quency, intensity, impact on daily activities, impact on
from 0 (never) to 5 (very often, more than once a week). quality of life, and fear of dizziness. The original paper
The subscale total score is calculated by summing item that described this questionnaire did not provide data
scores and dividing them by the number of items; higher about its psychometric properties. 42 Therefore, the clini-
scores indicate more frequent symptoms. It has good in - cian should use caution when interpreting the results and
ternal consistency and reliability, but less is known about comparing results from different samples and patients in
3970_Ch07_110-120 25/06/14 7:04 PM Page 115
clinical practice. It has been translated into Spanish61 and the VRBQ does not provide new insights into the problem
Swedish.74 The items about daily activities and quality of of disablement, because all the items were derived from
life are generic, putting unrelated concepts together such preexisting scales such as the DHI, VSS, VHQ, DFI,
as “driving” and “taking care of yourself.” The question- UCLA-DQ, and VADL. The omission of self-care activi-
naire has limited utility, because it does not address any ties is a significant weakness.
items in detail,24 but it may be used as a quick screening The 34-item VAP is scored on a 5-point scale. It ex-
before a comprehensive assessment. amines the activities and participation of people with
The 36-item VDI uses a 6-point scale to assess 2 do- vestibular disorders. Its relationship to the ICF is a
mains including 14 questions about symptoms and 22 strength. The total score is obtained by calculating the
questions about HRQoL. Each domain is given a total mean of the item scale values after excluding the “NotAp-
score based on the sum of the items. 42 The scales have plicable” items. The VAP total score had excellent test-
good internal consistency (VDI symptoms: 0.86; VDI retest reliability (ICC = 0.95) and poor to excellent
HRQoL: 0.92) and reliability (VDI symptoms: 0.81; VDI agreement per item ( 0.41–0.80).52 The scale provides a
HRQoL: 0.87),49 but responsiveness was modest. The variety of activities that involves walking and instrumental
VDI has low to moderate correlation with the SF-36 tasks, but the omission of important personal self-care
physical and mental components. No English version is tasks is a significant weakness.
available because it was developed in Spain but aTurkish Many of the scales evaluate frequency and intensity
version75 is available. of symptoms, movements that trigger symptoms, and
The 28-item VADL evaluates the self-perceived im- emotional problems, such as the DHI, VRBQ, and DFI.
pact of vestibular impairment on daily life activities. It is To assess performance of daily life activities, the VADL
divided into three domains: functional (12 items), ambu- and VAP are the best options. A rapid screening can be
lation (9 items), and instrumental (7 items). It is scored on performed using the UCLA-DQ, but a more comprehen-
a 10-point scale from 1 (Independent) to 10 (Too difficult sive evaluation of personal factors can be assessing by the
and no longer performs that activity) with an additional DFI. No scales assess the impact of the physical environ-
rating of “Not Applicable.” Subscores and the total score ment on vestibular disorders. The ideal assessment would
can be based on either the mean or the median of the item include domains for symptoms, self-care activities, mo-
scores. The VADL has high internal consistency for the bility skills, instrumental activities, emotional impact of
total score and for the subscales, and good test-retest reli- symptoms, and the impact of environmental factors.
ability over 2 hours. 40 It has been translated into Brazil-
ian-Portuguese,76 Italian,77 and Korean.78 A Spanish
version is available from the author . The VADL focuses
Disability and Vestibular Disorders
on daily activities and does not address symptoms or emo- Many studies have examined disability in patients with
tional components.24 Strengths of the VADL are the de- vestibular disorders. We review those studies in this sec-
tailed list of self-care skills in the functional domain and tion. Note that some studies used the normed instruments
the use of a detailed scale that provides a specific rating described above, but others did not.
of the patient’s level of performance. The 10-point scale In a study with community-dwelling elderly , the
may be difficult for some patients to select a level of func- prevalence of subjective complaints of dizziness was 45%;
tion.24 Clinical experience suggests that the detailed scale the movements that elicited this symptom were “standing
provides the basis for a useful structured interview during from a lying position” (50%), followed by “turning the
the clinical visit. head” (48%) and “standing from a sitting position” (38%).79
The 22-item VRBQ assesses the subjective sensation All these movements are performed several times a day and
of vertigo and its consequences in 2 domains, symptoms are components of various activities of daily living. People
(11 items) and quality of life (1 1 items), using a 7-point with vestibular disorders often reduce their levels of activity
scale. To obtain the final subscores and the total score, and avoid such movements as they attempt to avoid trig -
some special calculations must be made. The score calcu- gering the symptoms. That habit, however, may cause sec-
lation is an attempt to quantify the difference between the ondary problems such as stiff neck, headache, and muscle
patient’s current state and a state that is normal for the in- weakness,22,80 which then decreases their functional status,
dividual, but is not easy to apply in daily practice. The in a downward spiral.
questionnaire has good internal consistency for the total Aratani et al81 reported that 42% of elderly people
score (0.73), strong reliability (ICC = 0.92), and a moder- with vestibular disorders complained of having dif fi-
ate responsiveness.50,51 Although the attempt to improve culty performing 7 to 15 activities. The most difficult
the value of the subscores and total scores is admirable, task was “walking close to home,” following by “having
3970_Ch07_110-120 25/06/14 7:04 PM Page 116
a bath/shower.” Activity in outdoor environments, such as physical exercises, cause anxiety and avoidance behavior.
walking close to home, required greater attention, head Being inactive and limiting movements and interaction with
and gaze fixation, head and body orientation, and body the environment may limit vestibular compensation and may
stability. Those functions can be impaired by vestibular lead to a cycle of escalating anxiety and disability.80 The an-
disorders. Having a shower can be difficult for people with ticipation of problems is especially anxiety-provoking
vertigo and balance disorders for several reasons. Balance for patients with uncontrollable and unpredictable attacks
is challenged because the floor is slippery and because in- of vertigo, leading them to restrict their participation even
dividuals shift their weight to bend over to wash their hair more.4,22,43
or lower extremities. Vision is challenged when people The influence of contextual factors has not yet been
bathe without their eyeglasses, when they have water or well explored in people with vestibular disorders. 4 Some
shampoo in their eyes, and when the bath or shower stall environmental and seasonal factors, such as temperature
does not have an overhead light.Also, vestibular disorders variations and air pollution, have been shown to be corre-
cause decreased gain of the vestibulo-ocular reflex, result- lated with vertigo events in benign paroxysmal positional
ing in blurred vision. vertigo (BPPV).85,86 The theory, which sounds far-fetched,
People with vestibular disorders sometimes have dif- is that environmental factors may interfere with metabo-
ficulty performing more complex tasks such as shopping lism of endolymph, causing free-floating particles. That
and community-level skills, driving, some work-related theory is not supported by strong evidence.
tasks, and participating in some leisure activities22,80,82,83. Stronger evidence for the role of contextual factors
Cohen et al82 compared healthy subjects and subjects with comes from work by Ganança et al, 87 who found that
vestibular disorders using the Driving Habits Question- 53.1% of elderly people with vestibular disorders had
naire with some additional questions. Patients reported re- fallen inside their homes. The bathroom was the most
duced driving skills compared with healthy subjects, common place to fall (38.1%). The most common tasks in
particularly in challenging driving situations (alone, in the which they were engaged before the fall were walking
rain, at night, during rush hour, on the highway, changing (53.1%), ascending/descending stairs (10.9%), changing
lanes, in ramped garages, and pulling into and out of park- position (9.4%), and taking a shower (6.3%). Those tasks
ing spaces), but driving habits and crashes did not dif fer. could be performed safely and without falls with some
Visual information is very important to spatial orientation minor changes in the environment, such as using a cane
for people with vestibular impairments. They may become while walking and installing grab bars near the toilet and
more disoriented than healthy people in an environment in the shower stall. Clinicians should consider the impor-
with reduced visual stimuli or with visual conflict (such tant role of modifying contextual factors during treatment
as cars passing). Also, when driving, these patients tend planning.
to avoid making head movements, or they move their The social environment in which people live is also
heads slowly, to avoid eliciting vertigo. an important aspect of the environmental context. 18 For
Gutiérrez-Márquez et al. 83 reported that of 139 pa- people with vestibular disorders, the limits to their inde-
tients with vestibular disorders who had paid jobs, 51% pendence in self-care activities and mobility skills, fear
had problems performing their jobs. The median number of falling, avoidance of some tasks, and decreased par-
of days off work was 7 for patients with unilateral weak- ticipation in activities outside the home leads to restricted
ness, 5 for patients with bilateral vestibular weakness, and social networks and consequent decreased sense of well-
12 for patients with central problems. Yardley et al80 found being and quality of life. 22 Wiltink et al 88 found that
that 12.3% of patients who work took days of f work be- 28.3% of people with vertigo reported symptoms of at
cause of vertigo, and 25% had difficulty carrying out a job least one anxiety disorder (generalized anxiety , social
satisfactorily. For people with Ménière’s disease, the un- phobia, or panic) compared with only 5.1% of the control
predictability of the disorder and the hearing loss cause group. Having supportive family and friends might be a
many patients to leave their jobs and either stop working related contextual factor because those people might as-
or find different kinds of work.84 sist the person with vertigo.4 Conversely, the lack of sup-
Most people with vestibular disorders avoid leisure portive significant others, or the presence of people who
activities or reduce their participation, especially activi- are unsupportive because they do not understand the im-
ties related to exercises and body movements. 22 Even a pact of vestibular disorders on function performance, can
simple, sedentary hobby such as crocheting may be be a barrier to participation and developing a sense of
avoided by patients, because the position of the head can self-efficacy and well-being.
trigger symptoms. Thus, even basic daily tasks, such as Health professionals may have different perceptions
taking a shower, and more vigorous activities, such as of patients’ functional limitations, and these dif fering
3970_Ch07_110-120 25/06/14 7:04 PM Page 117
perceptions of disablement could affect treatment plan- peripheral vestibular weakness, balance impairments and
ning. For example, when physicians were asked about the Timed Up and Go test together explained 78% of the
the impact of dizziness on their patients’ quality of life, variance in DHI scores of the patients with bilateral
physicians perceived less impact than patients. 48 A pa- vestibular hypofunction, but they explained only 13% of
tient may continue to perceive him- or herself as disabled the variance in DHI scores of unilateral weakness patients.
because of vertigo, despite the professional’ s objective Thus, balance impairments are probably more closely re-
observation to the contrary. To ameliorate a sense of de- lated to functional limitations in patients with bilateral
creased self-efficacy, that patient will continue to seek vestibular weakness or loss. 95 Their well-known symp-
medical care, if not with the original professional then toms of oscillopsia and reduced dynamic visual acuity
with others.41 This type of behavior has the potential to may lead to particular dif ficulty driving, walking in
increase health-care costs significantly. crowds, and participating in sports. With practice, many
Some vestibular disorders are associated with spe- of those deficits may be reduced or ameliorated.
cific functional limitations and patterns of disability. For Central vertigo is generally associated with severe
example, most people with BPPV (84%) and Ménière’s disequilibrium, oscillopsia, vertigo, and additional neuro-
disease (85%) complain significantly more about vertigo logical signs.6 In a study that compared patients with pe-
than people with unilateral peripheral vestibular weakness ripheral and central vestibular disorders on the VAP and
(39%). Unsteadiness, however, was significantly more the DHI, patients with central involvement had signifi-
common in patients with unilateral peripheral weakness cantly worse scores than did patients with only peripheral
(83%), than in patients with Ménière’s disease (53%) and involvement.52
BPPV (22%).89
In BPPV, the episodes are often provoked by every-
day activities on which patients perform pitch rotations of Summary
the head, such as looking upward, bending forward, and We have pointed out some dif ferences by diagnosis, but
rolling over toward the af fected side.90,91 Those move- having a vestibular disorder, in general, is more significant
ments are often performed during routine activities such for functional limitations than the etiology of the specific
as trying to reach for an object, making the bed, putting disorder.41 Patients, in general, perform tasks more slowly
on socks or shoes, washing the hair at home or at the than normal. They limit their activities within and outside
beauty salon, being reclined in a dentist’s chair, changing the home: they restrict driving to local roads and avoid
a light bulb, or shaving.91 highways, and they may need time of f from work or be
Ménière’s disease is a special case, because many pa- less efficient or effective at work. Many patients also limit
tients have two different states of functioning, either nor- their social activities as a result of visual vertigo elicited
mal or incapacitated. In a survey of functional limitations indoors in large spaces such as some houses of worship,
in Ménière’s disease, patients who considered their attacks some community centers or auditoriums, and in crowds
to be mild (17%) were able to continue working or partic- or unstructured, outdoor spaces because of visual vertigo
ipating in an activity during an attack, but patients who and disequilibrium.
considered the attacks to be moderate (56%) were forced Using a wide range of strategies discussed elsewhere
to stop their activity and lie down. The remaining 27% had in this book, the functional impairments and limitations in
trouble with the attacks even while lying down. 92 Cohen activities and participation that lead to disability in vestibular
et al84 found that during Ménière’s attacks patients have disorders can be prevented or ameliorated. The contextual
difficulty performing activities that require good hearing, factors, especially the physical environment, can sometimes
such as using the telephone and social communication, but be altered or adapted to improve function. In vestibular re-
also activities that involve balance control. Vertigo and habilitation, the clinician’s goal for every patient is always
balance problems mainly influence the physical dimension to reduce symptoms, increase safety and independence, and
of functioning, whereas hearing loss influences the psy- improve the quality of life. The use of valid and reliable stan-
chosocial dimension.93 To modify Helen Keller’s famous dardized assessments can help to achieve those goals.
dictum, vertigo and balance disorders cut you of f from
doing things, but hearing loss cuts you off from people. References
Patients with bilateral vestibular hypofunction have
difficulty maintaining balance and are at risk for falls 1. Cohen H. Defining disablement in otolaryngology. Ear
Nose Throat J. 1995;74:233-237.
when the support surface is unstable, when postural con- 2. Mira E. Improving the quality of life in patients with
trol is challenged, and when ambient light is limited.94 In vestibular disorders: the role of medical treatments and
a study comparing patients with bilateral and unilateral physical rehabilitation. Int J Clin Pract. 2008;62:109-114.
3970_Ch07_110-120 25/06/14 7:04 PM Page 118
3. Alghwiri AA, Marchetti GF, Whitney SL. Content compar- 22. Holmes S, Padgham. A review of the burden of vertigo.
ison of self-report measures used in vestibular rehabilita- J Clin Nurs. 2011;20:2690–2701.
tion based on the international classification of functioning, 23. McDowell I. Measuring Health: a Guide to Rating Scales
disability and health. Phys Ther. 2011;91:346-357. and Questionnaires. 3rd ed. Oxford University Press: New
4. Müeller M, Schuster E, Strobl R, et al. Identification of York; 2006.
aspects of functioning, disability and health relevant to 24. Cohen HS. Assessment of functional outcomes in patients
patients experiencing vertigo: a qualitative study using the with vestibular disorders after rehabilitation. Neuro Reha-
international classification of functioning, disability and bilitation. 2011;29:173-178.
health. Health Qual Life Outcomes. 2012;10:75. 25. Piker EG, Jacobson GP, Tran AT, et al. Spouse perceptions
5. Üstün TB, Chatterji S, Bickenbach J, et al. The Interna- of patient self-reported vertigo severity and dizziness. Otol
tional Classification of Functioning, Disability and Health: Neurotol. 2012;33:1034-1039.
a new tool for understanding disability and health. Disabil 26. Cohen HS, Kimball KT, Adams AS. Application of the
Rehabil. 2003;25:565-571. Vestibular Disorders Activities of Daily Living Scale.
6. Karatas M. Central vertigo and dizziness: epidemiology, Laryngoscope. 2000B;110:1204-1209.
differential diagnosis, and common causes. Neurologist. 27. Madden R, Fortune N, Cheeseman D, et al. Fundamental
2008;14:355-364. questions before recording or measuring functioning and
7. Lin HW, Bhattacharyya N. Balance disorders in the elderly: disability. Disabil Rehabil. 2012. [Epub ahead of print]
epidemiology and functional impact. Laryngoscope. 2012; 28. Fekete C, Boldt C, Post M, et al. How to measure what
122:1858-1861. matters: development and application of guiding princi-
8. Neuhauser HK, Radtke A, von Brevern M, et al. Burden of ples to select measurement instruments in an epidemio-
dizziness and vertigo in the community. Arch Intern Med. logic study on functioning. Am J Phys Med Rehabil.
2008;168:2118-2124. 2011;90:S29-S38.
9. Kohler F, Selb M, Escorpizo R, et al. Towards the joint 29. Patrick DL, Deyo RA. Generic and disease-specific
use of ICD and ICF: a call for contribution. J Rehabil measures in assessing health status and quality of life.
Med. 2012;44:805-810. Med Care. 1989;27:S217-S232.
10. Research Plan for the National Center for Medical Reha- 30. Ware JE Jr. SF-36 health survey update. Spine.
bilitation Research. Bethesda: U.S. Department of Health 2000;25:3130-3139.
and Human Services/ National Institutes of Health/ 31. UDS-Data Management Service. Guide for Use of the
National Institute of Child Health and Human Develop- Uniform Data Set for Medical Rehabilitation Including
ment, 1993; NIH Publication No. 93-3509. the Functional Independence. 3rd ed. Buffalo: State
11. Jette AM. Physical disablement concepts for physical University of New York at Buffalo; 1990.
therapy research and practice. Phys Ther. 1994;74: 32. Enloe LJ, Shields RK. Evaluation of health-related quality
380-386. of life in individuals with vestibular disease using disease-
12. Jette AM. Toward a common language for function, dis- specific and general outcome measures. Phys Ther.
ability, and health. Phys Ther. 2006;86:726-734. 1997;77:890-903.
13. World Health Organization. ICIDH: International Classi- 33. Hsu LC, Hu HH, Wong WJ, et al. Quality of life in elderly
fication of Impairments, Disabilities and Handicaps. A patients with dizziness: analysis of the Short-Form Health
Manual of Classification Relating to the Consequences of Survey in 197 patients. Acta Otolaryngol. 2005;125:55-59.
Disease. Geneva: WHO; 1980. 34. Sousa RF, Gazzola JM, Ganança MM, et al. Correlation
14. Verbrugge LM, Jette AM. The disablement process. Sm between the body balance and functional capacity from
Sci Med. 1994;38:1-14. elderly with chronic vestibular disorders. Braz J Otorhino-
15. Imrie R. Demystifying disability: a review of the Interna- laryngol. 2011;77:791-798.
tional Classification of Functioning, Disability and Health. 35. Riberto M. [Core sets of the International Classification of
Sociol Health Illn. 2004;26:287-305. Functioning, Disability and Health]. Rev Bras Enferm.
16. Sampaio RF, Luz MT. Human functioning and disability: 2011;64:938-946.
exploring the scope of the World Health Organization’s 36. Wiegand NM, Belting J, Fekete C, et al. All talk, no ac-
international classification. Cad Saúde Pública. tion? The global diffusion and clinical implementation of
2009;25:475-483. the International Classification of Functioning, Disability,
17. Roush SE, Sharby N. Disability reconsidered: the paradox and Health. Am J Phys Med Rehabil. 2012;91:550-560.
of physical therapy. Phys Ther. 2011;91:1715–1727. 37. Grill E, Bronstein A, Furman J, et al. International
18. World Health Organization. The International Classification Classification of Functioning. Disability and Health (ICF)
of Functioning. Disability and Health. Geneva: WHO; 2001. core set for patients with vertigo. J Vestib Res. 2012;22:
19. World Health Organization. World Report on Disability. 261-271.
Geneva: WHO, 2011. 38. Levo H, Stephens D, Poe D, et al. Use of ICF in assessing
20. Almansa J, et al; and MHADIE Consortium. The Interna- the effects of Meniere’s disorder on life. Ann Otol Rhinol
tional Classification of Functioning, Disability and Health: Laryngol. 2010;119:583-589.
development of capacity and performance scales. J Clin 39. Stephens D, Pyykkj I, Varpa K, et al. Self-reported effects
Epidemiol. 2011;64:1400-1411. of Ménière’s disease on the individual’s life: a qualitative
21. Von Groote PM, Bickenbach JE, Gutenbrunner C. The analysis. Otol Neurotol. 2010;31:335-338.
World Report on Disability—implications, perspectives 40. Cohen HS, Kimball KT. Development of the Vestibular
and opportunities for physical and rehabilitation medicine Disorders Activities of Daily Living Scale. Arch Otolaryn-
(PRM). J Rehabil Med. 2011;43:869-875. gol Head Neck Surg. 2000;126:881-887.
3970_Ch07_110-120 25/06/14 7:04 PM Page 119
41. Cohen HS, Kimball KT, Adams AS. Application of the 58. Kaplan DM, Friger M, Racover NK, et al. [The Hebrew
Vestibular Disorders Activities of Daily Living Scale. dizziness handicap inventory]. Harefuah. 2010;149:
Laryngoscope. 2000;110(7):1204-1209. 697-700.
42. Duracinsky M, Mosnier I, Bouccara D, et al; and Working 59. Castro AS, Gazzola JM, Natour J, et al. [Brazilian version
Group of the SociétéFrançaised’Oto-Rhino-Laryngologie of the dizziness handicap inventory]. Pro Fono. 2007;19:
(ORL). Literature review of questionnaires assessing ver- 97-104.
tigo and dizziness, and their impact on patients’ quality of 60. Poon DM, Chow LC, Au DK, et al. Translation of the
life. Value Health. 2007;10:273-284. dizziness handicap inventory into Chinese, validation
43. Jacobson GP, Newman CW. The development of the of it, and evaluation of the quality of life of patients with
Dizziness Handicap Inventory. Arch Otolaryngol Head chronic dizziness. Ann Otol Rhinol Laryngol. 2004;113:
Neck Surg. 1990;116:424-427. 1006-1011.
44. Yardley L, Putman J. Quantitative analysis of factors con- 61. Pérez N, Garmendia I, Martín E, et al. [Cultural adaptation
tributing to handicap and distress in vertiginous patients: of 2 questionnaires for health measurement in patients
a questionnaire study. Clin Otolaryngol Allied Sci. with vertigo]. Acta Otorrinolaringol Esp. 2000;51:
1992;17:231-236. 572-580.
45. Yardley L, Masson E, Verschuur C, et al. Symptoms, 62. Jarlsater S, Mattsson E. Test of reliability of the Dizziness
anxiety and handicap in dizzy patients: development of Handicap Inventory and the activities-specific balance
the vertigo symptom scale. J Psychosom Res. 1992;36: confidence scale for use in Sweden. Adv Physiother.
731-741. 2003;5:137-144.
46. Powell LE, Myers AM. The Activities specific Balance 63. Kurre A, Bastiaenen CH, van Gool CJ, et al. Exploratory
Confidence (ABC) scale. J Gerontol A BiolSci Med Sci. factor analysis of the Dizziness Handicap Inventory (German
1995;50:M28-M34. version). BMC Ear Nose Throat Disord. 2010;10:3.
47. Hazlett RL, Tusa RJ, Waranch HR. Development of an 64. Tschan R, Wiltink J, Best C, et al. Validation of the
inventory for dizziness and related factors. J Behav Med. German version of the Vertigo Handicap Questionnaire
1996;19(1):73-85. (VHQ) in patients with vestibular vertigo syndromes or
48. Honrubia V, Bell TS, Harris MR, et al. Quantitative evalu- somatoform vertigo and dizziness. Psychother Psychosom
ation of dizziness characteristics and impact on quality of Med Psychol. 2010;60:e1-e12.
life. Am J Otol. 1996;17:595-602. 65. Tschan R, Wiltink J, Best C, et al. Validation of the
49. Prieto L, Santed R, Cobo E, et al. A new measure for as- German version of the Vertigo Symptom Scale (VSS) in
sessing the health-related quality of life of patients with patients with organic or somatoform dizziness and healthy
vertigo, dizziness or imbalance: the VDI questionnaire. controls. J Neurol. 2008;255:1168-1175.
Qual Life Res. 1999;8:131-139. 66. Rogers C, de Wet J, Gina A, et al. The translation of the
50. Morris AE, Lutman ME, Yardley L. Measuring outcome Vertigo Symptom Scale into Afrikaans: a pilot study. S Afr
from vestibular rehabilitation, part I: qualitative develop- J Commun Disord. 2011;58:6-12.
ment of a new self-report measure. Int J Audiol. 2008;47: 67. Yanik B, Külcü DG, Kurtais Y, et al. The reliability and
169-177. validity of the Vertigo Symptom Scale and the Vertigo
51. Morris AE, Lutman ME, Yardley L. Measuring outcome Dizziness Imbalance Questionnaires in a Turkish patient
from vestibular rehabilitation, part II: refinement and vali- population with benign paroxysmal positional vertigo.
dation of a new self-report measure. Int J Audiol. J Vestib Res. 2008;18:159-170.
2009;48:24-37. 68. Yardley L, Medina SM, Jurado CS, et al. Relationship be-
52. Alghwiri AA, Whitney SL, Baker CE, et al. The develop- tween physical and psychosocial dysfunction in Mexican
ment and validation of the vestibular activities and partici- patients with vertigo: a cross-cultural validation of the ver-
pation measure. Arch Phys Med Rehabil. 2012;93: tigo symptom scale. J Psychosom Res. 1999;46:63-74.
1822-1831. 69. Schott N. [German adaptation of the “Activities-Specific
53. Caldara B, Asenzo AI, BrusottiPaglia G, et al. [Cross- Balance Confidence (ABC) scale” for the assessment of
cultural adaptation and validation of the Dizziness Handi- falls-related self-efficacy]. Z Gerontol Geriatr. 2008;41:
cap Inventory: Argentine version]. Acta Otorrinolaringol 475-485.
Esp. 2012;63:106-114. 70. Salbach NM, Mayo NE, Hanley JA, et al. Psychometric
54. Nola G, Mostardini C, Salvi C, et al. Validity of Italian evaluation of the original and Canadian French version of
adaptation of the Dizziness Handicap Inventory (DHI) and the activities-specific balance confidence scale among
evaluation of the quality of life in patients with acute people with stroke. Arch Phys Med Rehabil. 2006;87:
dizziness. Acta Otorhinolaryngol Ital. 2010;30:190. 1597-1604.
55. Nyabenda A, Briart C, Deggouj N, et al. [Normative study 71. Karapolat H, Eyigor S, Kirazli Y, et al. Reliability, valid-
and reliability of French version of the dizziness handicap ity, and sensitivity to change of Turkish Activities-specific
inventory]. Ann Readapt Med Phys. 2004;47:105-113. Balance Confidence Scale in patients with unilateral
56. Alsanosi AA. Adaptation of the dizziness handicap inven- peripheral vestibular disease. Int J Rehabil Res. 2010;33:
tory for use in the Arab population. Neurosciences 12-18.
(Riyadh). 2012;17:139-144. 72. Mak MK, Lau AL, Law FS, et al. Validation of the
57. Goto F, Tsutsumi T, Ogawa K. The Japanese version of the Chinese translated Activities-Specific Balance Confidence
Dizziness Handicap Inventory as an index of treatment scale. Arch Phys Med Rehabil. 2007;88:496-503.
success: exploratory factor analysis. Acta Otolaryngol. 73. Jarlsater S, Mattsson E. Test of reliability of the Dizziness
2011;131:817-825. Handicap Inventory and the Activities-Specific Balance
3970_Ch07_110-120 25/06/14 7:04 PM Page 120
Confidence scale for use in Sweden. Adv Physiother. 85. Mariani P, Pelagatti M, Hahn A, et al. Epidemiology of
2003;5:137-144. paroxysmal positioning vertigo: correlation with seasons,
74. Kammerlind AS, Bergquist LP, Ledin T, et al. Reliability climate, and pollution. Int Tinnitus J. 2008;14:168-174.
of clinical balance tests and subjective ratings in dizziness 86. Alpini D, Mattei V, Mariani D. Paroxysmal Positioning
and disequilibrium. Adv Physiother. 2005;7:96-107. Vertigo (PPV) and pollution: a ten years correlation. ASN.
75. Yanik B, Külcü DG, Kurtais Y, et al. The reliability and 2011;6.
validity of the Vertigo Symptom Scale and the Vertigo 87. Ganança FF, Gazzola JM, Aratani MC, et al. Circunstân-
Dizziness Imbalance Questionnaires in a Turkish patient cias e conseqüências de quedas em idosos com vestibu-
population with benign paroxysmal positional vertigo. lopatia crônica. Rev Bras Otorrinolaringol. 2006;72:
J Vestib Res. 2008;18:159-170. 388-393.
76. Aratani MC, Ricci NA, Caovilla HH, et al. Brazilian ver- 88. Wiltink J, Tschan R, Michal M, et al. Dizziness: anxiety,
sion of the Vestibular Disorders Activities of Daily Living health care utilization and health behavior: results from a
Scale (VADL). Braz J Otorhinolaryngol. In press. representative German community survey. J Psychosom
77. Salvinelli F, Casale M, Trivelli M, et al. Benign paroxys- Res. 2009;66:417-424.
mal positional vertigo: a comparative prospective study on 89. Tomanovic T, Bergenius J. Different types of dizziness in
the efficacy of Semont’s maneuver and no treatment strat- patients with peripheral vestibular diseases: their preva-
egy. Clin Ter. 2003;154:7-11. lence and relation to migraine. Acta Otolaryngol.
78. Min KK, Ha MJ, Cho CH, et al. Clinical use of subjective 2010;130:1024-1030.
visual horizontal and vertical in patients of unilateral 90. Bhattacharyya N, Baugh RF, Orvidas L, et al; for American
vestibular neuritis. Otol Neurotol. 2007;28:520-524. Academy of Otolaryngology-Head and Neck Surgery
79. De Moraes SA, Soares WJS, Rodrigues RAS, et al. Dizzi- Foundation. Clinical practice guideline: benign
ness in community-dwelling older adults: a population- paroxysmal positional vertigo. Otolaryngol Head
based study. Braz J Otorhinolaryngol. 2011;77:691-699. Neck Surg. 2008;139:S47-S81.
80. Yardley L, Owen N, Nazareth I, et al. Prevalence and 91. Cohen HS, Jerabek J. Efficacy of treatments for posterior
presentation of dizziness in a general practice community canal benign paroxysmal positional vertigo. Laryngoscope.
sample of working age people. Br J Gen Pract. 1998; 1999;109:584-590.
48:1131-1135. 92. Havia M, Kentala E. Progression of symptoms of dizzi-
81. Aratani MC, Perracini MR, Caovilla HH, et al. Disability ness in Ménière’s disease. Arch Otolaryngol Head Neck
rank in vestibular older adults. Geriatr Gerontol Int. Surg. 2004;130:431-435.
2011;11:50-54. 93. Söderman AC, Bagger-Sjöbäck D, Bergenius J, et al. Fac-
82. Cohen HS, Wells J, Kimball KT, et al. Driving disability tors influencing quality of life in patients with Ménière’s
and dizziness. J Safety Res. 2003;34:361-369. disease, identified by a multidimensional approach. Otol
83. Gutiérrez-Márquez A, Jáuregui-Renaud K, Viveros- Neurotol. 2002;23:941-948.
Renteria L, et al. Discapacidad por enfermedad auditiva y 94. McCall AA, Yates BJ. Compensation following bilateral
vestibular en un centro de atención especializada. Gac vestibular damage. Front Neurol. 2011;2:88.
Méd Méx. 2005;141:105-110. 95. Gill-Body KM, Beninato M, Krebs DE. Relationship
84. Cohen H, Ewell LR, Jenkins HA. Disability in Meniére’s among balance impairments, functional performance, and
disease. Arch Otolaryngol Head Neck Surg. 1995;121: disability in people with peripheral vestibular hypofunc-
29-33. tion. Phys Ther. 2000;80:748-758.
3970_Ch08_121-150 25/06/14 11:33 AM Page 121
CHAPTER 8
Vestibular
Compensation—
Recovery after
Unilateral
Vestibular Loss
Ian S. Curthoys, PhD ■ G. Michael Halmagyi, MD
Sudden, complete unilateral loss of vestibular function in function, the permanent loss is clearly sho wn. Neverthe-
normal, healthy individuals results in a dramatic series of less, most patients with permanent UVD reco ver and are
symptoms—strong sensations of turning (vertigo), nausea, happy—they are “well-compensated.” They do not expe-
rapid eye movements (nystagmus), oscillopsia (the illusion rience vertigo, nausea, oscillopsia, or postural unsteadi-
that the visual world is moving as they move their head), ness (see Box 8-1).
falling to the affected side, gait ataxia, postural instability, That the objective tests show the permanent vestibu-
distortions in the perception of body orientation and move- lar loss implies that well-compensated patients must have
ment, and inadequate compensatory responses to head developed some means of o vercoming the loss of this
movement. We will use the term unilateral vestibular deaf- major sensory system. The big question is ho w? What
ferentation (UVD) syndrome to refer to these symptoms. are these patients doing to help themselv es so much?
Such patients are greatly distressed. Over the first few days This puzzle is sharpened by the f act that some patients,
most of the symptoms decline and the patient’ s distress after apparently identical v estibular loss, continue to
correspondingly diminishes. F or most patients, these complain about their UVD syndrome for years after the
symptoms have disappeared within a few weeks, and the event, and are so unhappy they repeatedly visit their cli-
patients return to their normal lifestyle and are happy with nician to attempt to overcome their poor compensation.
their recovery. The term used to describe that general re- It is our contention that the well-compensated patients
covery is v estibular compensation, and superf icially it have learned behaviors to minimize the ef fects of their
seems that there is a full recovery and vestibular function loss—for example, to generate saccades or blinks during
has returned. Indeed, in a few patients this is exactly what head movement—whereas the poorly compenated
does happen: some patients with vestibular neuritis expe- patients have not learned these strategies.
rience all these symptoms, but as their vestibular neuritis The vestibular system has a major role in the control
diminishes, their peripheral vestibular function, as shown of many responses and so the symptoms of the UVD syn-
by new specific, objective tests, is completely restored. drome are complex and varied, and many factors can affect
However, in most patients there is little or no restoration recovery. Simply listing the symptoms and their change
of vestibular function, and when their peripheral vestibular over time does not help in understanding the UVD syn-
function is tested by these ne w tests of canal and otolith drome and its reco very. Vestibular compensation is not a
121
3970_Ch08_121-150 25/06/14 11:33 AM Page 122
vestibular sensory regions project their information to common. However, in patients after gentamicin, the final
the vestibular nucleus in different bundles of fibers within level of residual v estibular function is unkno wn unless
the vestibular nerve. That knowledge is also important for post-procedural testing is undertaken. After the same in-
understanding recovery processes, because if just one divi- tratympanic gentamicin injection procedure, some patients
sion of the vestibular nerve is surgically sectioned (e.g., the may lose almost all v estibular function, whereas others
superior vestibular nerve), then there is still substantial may lose much less.
vestibular input projecting to the v estibular nuclei via the One of the themes of this chapter is to emphasize
inferior vestibular nerve. the importance of ha ving baseline data about the le vel
One procedure, now very widely used to treat unilat- of vestibular function before any therapeutic procedure.
eral peripheral vestibular dysfunction because of its rela- This should be complemented by data about the level of
tive safety, is intratympanic injection of a solution of the vestibular function after the procedure. These data are
ototoxic antibiotic gentamicin—injected via a fine needle especially important for the supposedly healthy ear .
inserted through the eardrum into the middle ear (see After the UVD procedure, it will be the neural output
Carey [2004] for a review).23 from this remaining labyrinth that will be of prime im-
At low doses, gentamicin is taken up into the inner portance for the person’s stability. Is the “healthy” ear
ear through the round window of the cochlea and fairly really healthy? Getting such data is a v ery modest in-
selectively attacks the cilia of vestibular receptors, dis- vestment of time in relation to the possible outcome of
abling their response to natural v estibular stimuli, but a patient who compensates poorly because the suppos-
with little effect on cochlear receptors, so hearing is edly healthy ear w as in fact dysfunctional before the
minimally affected. Gentamicin attacks vestibular recep- UVD. Such patients may spend man y years in therap y
tors in a progressive fashion; Type I receptors at the stri- and rehabilitation in an attempt to overcome their poor
ola of the otoliths and the crest of the crista are most vestibular compensation, which was caused by an inap-
vulnerable.24 Physiological evidence shows these recep- propriate procedure.
tors and the afferent neurons terminating on them con- To measure precisely the pattern and resolution of the
vey information primarily about changes in vestibular UVD syndrome in humans, it is best to study the same pa-
stimulation—the onset of an angular or linear acceleration— tients before and after surgical deafferentation of one in-
and if they are lost, then one would expect that information tact labyrinth. Although such patients and the facilities for
about changes in v estibular stimulation w ould be af- studying them are rare, some long-term quantitati ve data
fected early. Recent evidence shows that there are be- on the precise sensory and motor consequences of UVD
havioral changes that correspond to that progressi ve of such human patients is available.27-29
loss.25 During the course of the gentamicin treatment, The intense disequilibrium after UVD has both sen-
the cell bodies of the receptors may be preserv ed and sory and motor components, which can be categorized into
the receptor cilia on these vestibular receptor cells may static or dynamic symptoms. Static symptoms are present
regrow following the procedure, so that vestibular func- continuously, even when the person is totally stationary .
tion (and possibly vestibular symptoms) may eventually Dynamic symptoms occur during movement. We consider
reappear following gentamicin treatment. 26 In such pa- each category in turn.
tients, what may appear as v estibular compensation is
in fact the return of peripheral v estibular function. A
Static Symptoms
similar situation applies in some cases of vestibular neu-
ritis when the affected peripheral neurons recover from Spontaneous Nystagmus
temporary loss and start to function again. These are not Immediately after UVD, there is a spontaneous, mainly
examples of vestibular compensation but of restoration horizontal, conjugate ocular nystagmus. Both eyes show
of peripheral vestibular function. Until recently, it was rapid eye movements, so that both eyes appear to be beat-
not possible to demonstrate this restoration of function ing away from the affected (lesioned) side. Recordings of
conclusively, but with new selective tests of canal and eye position show that the eye movements consist of slow
otolith function, this vestibular restoration can be clearly eye deviations (called slow phases) toward the affected
identified. The conclusion: one needs to be careful in side, followed by rapid e ye movements (called quick
using data from patients with v estibular neuritis to un- phases) away from the affected side (Fig. 8.2). The slow
derstand vestibular compensation. phases are not apparent to an observer and can only be de-
The intratympanic gentamicin injection procedure is tected by recording the e ye movements. To an observer,
now so successful that surgical UVD procedures are, with both eyes appear to be beating away from the affected ear.
the exception of schw annoma surgery, becoming less This spontaneous nystagmus can be reduced or entirely
3970_Ch08_121-150 25/06/14 11:33 AM Page 125
suppressed by visual f ixation, and such suppression by there are corrective postural responses. In UVD patients,
vision is an important way of identifying that the nystag- over time that neural imbalance decreases, and as it does,
mus is a result of peripheral vestibular dysfunction. Nys- the static symptoms diminish.
tagmus caused by central dysfunction is not reduced or
abolished by vision. To detect spontaneous n ystagmus, Ocular Tilt Reaction
one needs to ha ve a way of viewing eye movements in After UVD, in addition to spontaneous n ystagmus, there
darkness or without an y visual fixation stimuli present. is a static otolith component that is called the ocular tilt
Two ways of doing this are Frenzel glasses or video reaction.30 Just as an angular rotation of the head causes
recordings of eye movements in total darkness while the an imbalance in neural activity between the two vestibular
eye is illuminated by (invisible) infrared light. In the week nuclei, so a maintained head tilt also causes an imbalance.
after the occurrence of the UVD, the strength of the spon- Also, just as the canal-induced post-UVD symptoms can
taneous nystagmus in darkness (the slow phase eye veloc- be seen as compensatory for a head angular acceleration,
ity) declines, but for some patients there is always a very so the post-UVD otolithic responses (skew deviation, oc-
small spontaneous nystagmus present in darkness as a per- ular torsion, and head tilt) can be seen as compensatory
manent legacy of their UVD. for a roll head tilt. It seems that these static otolithic symp-
In spontaneous nystagmus, the vertical eye move- toms are also caused by the neural imbalance between the
ment components are small or absent, presumably because vestibular nuclei.
the two vertical semicircular canals in the labyrinth cause The static otolithic symptoms consist of
essentially opposite vertical eye movements: anterior canal
1. skew deviation of the two eyes. The ipsilesional
activation causes upward movement, and posterior canal
eye is positioned lower in its orbit relative to the
activation causes downward movement. So, the simulta-
(vertical) position of the contralesional eye in its
neous loss of both these sensory or gans in the one
orbit. This can result in double vision (diplopia),
labyrinth will result in the tw o vertical components can-
but the extent of the skew deviation is rarely
celling each other.
large and usually resolves rapidly.30-32
2. conjugate ocular torsion. Both eyes roll in the
Why Does Spontaneous Nystagmus Occur?
orbit (around the line of sight) and adopt a main-
In animals, the UVD causes a total loss of v estibular
tained rolled eye position with the upper pole
afferent input to the v estibular nucleus on the af fected
rolled toward the lesioned ear. This maintained
side (the ipsilesional vestibular nucleus), so there is a
ocular torsional position can be up to 15 degrees
great reduction in neural activity of neurons in that ipsile-
of ocular torsion relative to the pre-operative
sional nucleus. Simultaneously, there is an increase in the
torsional position (Fig. 8.3).31,33,34
resting activity of neurons in the vestibular nucleus on the
3. roll head tilt toward the lesioned side. When
healthy side (the contralesional vestibular nucleus). So,
tested without visual input, the patient has a
the UVD generates an imbalance in neural activity anal-
small roll head tilt toward the lesioned ear.
ogous to that produced by a real head rotation toward the
intact ear. In both cases, the UVD and the rotation, the re- The mechanism by which the unilateral otolithic loss
sponses and the sensations are similar—the person per - causes this ocular tilt reaction is speculative. It is most likely
ceives him- or herself as rotating, there is nystagmus, and similar to the mechanism of the spontaneous nystagmus that
3970_Ch08_121-150 25/06/14 11:33 AM Page 126
of dynamic vestibular function. However, when careful HEAD ROTATION TO INTACT SIDE
measures with specific vestibular tests are made, the clear
EYE
answer is that there is little or no such recovery of dynamic HEAD
purely vestibular function. It can appear that reco very 100
0/
s
takes place, possibly as patients learn ne w modes of re-
sponding to the sinusoidal rotational test stimulus. These
very low sinusoidal frequencies are not physiological;
most natural head movements are high-acceleration, high-
frequency stimuli. The head accelerations during walking
or running, which post-UVD patients complain about,
have high acceleration (2000 to 3000 de g/sec/sec) and 0 0/s
at arm’s length. Then, the clinician turns the patient’s head 100 0/s
in an abrupt unpredictable horizontal head rotation of
about 20 degrees in about half a second, while the patient
is asked to stare at the tip of the clinician’ s nose and
not blink. The head is turned to be pointing at a tar get
location—the movement is “turn and stop”—with no re-
bound. The term used to describe this kind of head rotation
is a “head impulse.” Although it is very brief, this abrupt TIME 100 msec
B
head rotation has a peak angular v elocity of around 200
Figure 8.4 Time series of the eye velocity and head
to 300 deg/sec and a peak angular acceleration of 2500 to velocity response during a single horizontal passive head
4000 deg/sec/sec (or higher). In normal subjects, this head impulse from a patient 3 years after unilateral vestibular
rotation results in a short-latency (about 10 ms), smooth, neurectomy. Head velocity is shown in dashed lines, eye
compensatory eye movement that compensates for the velocity in continuous lines. (A) For rotation to the intact
side, eye velocity mirrors head velocity. (B) In contrast, for
head turn so that the subject’ s gaze remains fixed on the
rotations to the lesioned side, eye velocity is systematically
clinician’s nose irrespective of whether the rotation is to smaller than head velocity from the onset of head rotation.
the left or right (Fig. 8.4). This means that, in normal sub- (From Halmagyi et al, 1990.28)
jects, VOR gain (the ratio of eye velocity to head velocity)
is close to 1.0. For a patient after a unilateral loss, the re-
sult is very different. If the patient’s head is rotated to the Testing over time shows that the ipsilesional VOR
affected side, the UVD causes a marked reduction in VOR gain during the f irst 100 msec, before other sources of
gain for these ipsilesional head rotations, whereas the oculomotor control can affect the eye movement response,
VOR gain for head rotations to the healthy side (contrale- remains (apparently permanently) at around 25% of nor -
sional rotations) is only modestly reduced (Fig. 8.5). mal, whereas the contralesional VOR gain remains at
The inadequate eye movement response during the around 80% of normal values.2,28,48,49-52 A similar asym-
ipsilesional head rotation means that, during the head ro- metry of the VOR is also found in animals.50-53
tation, the patient’s eyes move with the head off the target, After that first report of the overt catch-up saccade in
and so accumulate a position error which is usually cor - 1988, some clinicians complained that in some patients
rected by a saccade at the end of the head mo vement, with a known vestibular loss, it was not possible to detect
which takes the patient’s gaze back to the target, the clin- this saccade at the end of the head turn toward the affected
ician’s nose. It is that corrective saccade (called an “overt” ear. When we measured the responses of UVD patients
saccade) that the clinician can (with a little training and carefully with scleral search coils, we disco vered that
practice) detect, and which is the tell-tale sign of an in- some UVD patients can manage to generate the corrective
adequate VOR.28,47 saccade actually during the head turn. 54 These saccades
3970_Ch08_121-150 25/06/14 11:33 AM Page 128
during the head turn are not detectable by the nak ed eye
EYE VELOCITY (deg/sec)
and so would not be observed by the clinical observation.
We called these hidden saccades “co vert” saccades and
their existence means that it is necessary to actually mea-
100 sure the eye movement response during the head turn,
rather than relying on the unreliable subjecti ve clinical
observation (Fig. 8.6). It is still the case that if an o vert
saccade is detected clinically, then the patient does have a
-200 -100 0 100 200 vestibular loss. However, if no saccade is detected by clin-
ical observation, no conclusion can be drawn—the patient
0
HEAD VELOCITY (deg/sec) may be normal or may have a unilateral vestibular loss and
be generating a covert saccade to conceal that loss. Only
objective measurement of the eye movement can resolve
-100 the latter question, and this was made possible by our de-
velopment of a small, lightweight, high-speed, head-
mounted video camera on minimal slip goggles.When we
HEAD ROTATION TO LESIONED SIDE
measured the eye movement during head turn, this camera
HEAD ROTATION TO INTACT SIDE
successful? In such a UVD patient, if there is no co vert achieve the same result. Belo w we consider the role of
saccade, the image is dragged across the retina at about covert saccades in vestibular compensation.
the same velocity as the velocity of the head turn, and so After UVD, there is a small symmetrical loss ofVOR
causes a smeared, blurred visual image that lasts about as gain for pitch head rotations for both pitch nose down and
long as the head turn—usually 200 msec or so. It is this pitch nose up. There is a larger loss for roll rotations.58-61
smear that is held to be so aversive for UVD patients, who When the roll head movement is toward the lesioned side,
complain about the blur and bounce of their visual expe- there is a lar ge reduction in VOR gain; when the mo ve-
rience during head movements. The perceptual effects of ment is toward the healthy ear, the drop in gain is not as
smear can be reduced or eliminated by a saccade. There great. In fact, when the rapid head rotation is aligned to
are two reasons for this reduction: (1) the v ery high eye be in the plane of one pair of the vertical canals (at about
velocity of a saccade, which lasts only 20 msec or so, will 45 degrees to the main pitch and roll planes) the UVD ef-
reduce the visibility of the smear; and (2) visual percep- fect becomes clear, and the asymmetric VOR can be de-
tion is suppressed by central neural processes just before tected, because each vertical canal forms a synergistic pair
and during a saccade by a phenomenon kno wn as sac- with its opposing partner.62 Impulses in these planes are
cadic suppression.55-57 The combination of these tw o called LARPs (left anterior-right posterior) and RALPs
factors is an effective means of greatly reducing or elim- (right anterior and left posterior).
inating the perceptual effect of the retinal smear. So, the
brief ballistic saccade during the head turn regains the tar- Dynamic Otolithic Responses
get and is probably as effective as the slow, compensatory, After UVD, there are def icits in otolithic dynamic re-
eye velocity correction from v estibular input for gaze sponses. During dynamic otolithic stimulation as the head
maintenance (Fig. 8.7). Of course, a blink will also is rolled at constant v elocity toward the lesioned ear, the
0.2
Position (RV)
0.1 H
E
300 2 3
Velocity (deg/s)
H E
150 1 2 3 1
Time (ms)
Figure 8.7 Time series of eye and head velocity during typical passive (A) and active
(B) head impulses for both ipsilesional and contralesional head rotations. The eye velocity
response has been inverted to allow close comparison to the head velocity. The start of the
head rotation is indicated by the arrow (1), the start of the compensatory saccadic eye move-
ment by (2), and the end of that compensatory saccade by (3). During passive ipsilesional
head rotations, a large gaze error develops during the head rotation, and that error persists
until the saccade occurs after the end of the head rotation and acts to return the patient’s
eyes to the target. With a comparable active head rotation (B) to the ipsilesional side, this
compensatory saccade occurs during the head rotation so that the gaze error is small, and no
corrective saccade is needed after the end of the head rotation. Close inspection of this low-
noise, search-coil record shows the presence of this small but very effective saccade (a covert
saccade) during the active head rotation. (From Black et al, 2005.63)
3970_Ch08_121-150 25/06/14 11:33 AM Page 130
magnitude of the linear acceleration stimulation of the neurons can also be acti vated by BCV (unpublished ob -
otolithic receptors causes a small compensatory ocular tor- servation). This physiological evidence underpins the
sion response—a roll of both e yes around the line of use of moderate intensity BCV and ACS as new ways
sight—called ocular counterrolling (OCR) in the direction of testing dynamic otolith function in the clinic. 77 De-
opposite to the head roll tilt. OCR is one of the fe w livery of 500-Hz BCV to the midline of the forehead at
accepted measures of otolith function. 64,65 Schmid- the hairline—a location called Fz—has been sho wn to
Priscoveanu et al tested patients before and after UVD cause about equal stimulation of both ears simultane-
and found at testing shortly after UVD, there w as an ously and so is a simple clinically ef fective way of si-
asymmetry in their OCR response with smaller OCR for multaneous bilateral dynamic otolith stimulation.78
roll-tilts of the head toward the affected side. This OCR There are very extensive neural projections from the
asymmetry recovers fairly quickly66—it is not lik e the otoliths to many muscle groups throughout the body, and
permanent asymmetry of the angular VOR. thus otolith activation results in myogenic potentials in
Impulses of linear acceleration (so-called head these muscle groups. The two main potentials that ha ve
“heaves”)—in which the patient’s head is given a brief un- been measured for clinical tests of otolith function are the
predictable lateral head mo vement toward or away from cVEMP and oVEMP, although many others have been re-
the affected ear 67,68—also reveal an asymmetrical oculo- ported. In response to 500-Hz Fz BCV, patients with UVD
motor response after UVD.69,70 This lateral or linear head show a marked asymmetry of these VEMPs with little re-
movement causes a horizontal eye rotation in normal sub- covery over time.72,79-81
jects that appears to be caused by the otoliths because an-
gular head rotations are minimal: after UVD, there is an The Cervical Vestibular Evoked
asymmetry with a smaller horizontal eye velocity for lin- Myogenic Potential—the cVEMP
ear accelerations directed to the operated ear (as with Sound-evoked saccular neurons project to and synapse
canals, ipsilesional stimulation re veals the smaller re- on neurons in the ipsilateral v estibular nuclei, and in-
sponse) than for linear accelerations directed to the intact hibitory neurons in the vestibular nuclei project to ipsi-
ear. However, this otolithic response asymmetry also dis- lateral spinal motoneurons and inhibit them. 82,83 So, if
appears fairly quickly.71 the SCM is tensed, and BCV is delivered, there is a short
latency (about 13 msec to peak) positive (inhibitory) re-
Otolithic Responses to Sound sponse recorded by surf ace EMG electrodes o ver the
and Vibration tensed SCM. The stimulus can be either a light tap to Fz
Testing dynamic otolith function, and measuring an y with a tendon hammer or a brief (6 msec) burst of modest
change in otolith function after UVD, has posed a major vibration (about the intensity deli vered by a body mas-
challenge because the usual w ay of delivering the linear sager or an electric toothbrush) delivered by a Bruel and
acceleration stimulus has been to move the whole head (or Kjaer minishaker 4810.79
body) of the patients using a sled or centrifuge. These de- Thus, a short 500-Hz tone burst results in the cervi-
vices are large, very expensive, dangerous, and totally im- cal vestibular evoked myogenic potential—the cVEMP—
practical in a clinic. Ho wever, there is another w ay of consisting of an initial positive potential at about 13 msec
generating linear accelerations: bone conducted vibration latency followed by a ne gative potential at about
(BCV), which is composed of a series of linear accelera- 23 msec.84-86 The cVEMP is mediated by an uncrossed
tions of the mastoids. 72 Physiological evidence from inhibitory sacculo-collic response. In healthy subjects, the
guinea pigs shows that these linear accelerations, although 500-Hz Fz BCV results in symmetrical cVEMPs, and in
brief, are a very effective means of activating one class of patients with complete UVD, there is reduced or absent
otolith neurons—otolith irregular neurons.73 The evidence cVEMP p13 on the ipsilesional SCM in response to Fz
is that 500-Hz BCV is selective for otolith irregular neu- BCV or ACS stimulation of the af fected ear (Fig. 8.8).
rons; few canal neurons are excited at that frequency. The There is little or no recovery over time; this diagnostic in-
sensitivity of these neurons is extraordinarily high; some dicator is clear even in long-term UVD patients.
neurons show clear activation at stimulus levels that are at
or below ABR threshold. The Ocular Vestibular Evoked Myogenic
Similarly, ACS can also activate these same otolith Potential—the oVEMP
irregular afferent neurons, presumably by bending the cilia Similarly, in response to the same 500-Hz Fz BCV stim-
by a mechanism that is still not understood.This selective ulus, the myogenic potential recorded beneath the e yes
response of otolithic afferents to ACS and BCV allows one as the subject looks up (i.e., elevates the eyes to tense the
to use ACS and BCV to index dynamic otolith function in inferior oblique muscles) is called the ocular v estibular
the clinic.74-76 At lower frequencies (e.g., 100 Hz), canal evoked myogenic potential (oVEMP). 86-91 This is a
3970_Ch08_121-150 25/06/14 11:33 AM Page 131
RECOVERY
stimulus-locked ocular VEMP with the small initial neg-
ative (excitatory) potential at about 10 msec (called the
Recovery of Static Symptoms
oVEMP n10), which has since been shown to reflect pre- The static oculomotor and postural components resolv e
dominantly utricular activity.89,90 In healthy subjects, in progressively over the first month or so. In contrast, de-
response to 500-Hz Fz BCV, the oVEMP is of equal am- tailed measures show that the dynamic symptoms do not
plitude beneath both e yes (see Fig. 8.8). Ho wever, in change very much over time. These symptoms may appear
patients after UVD, the oVEMP n10 is reduced or absent to recover, as the patient learns new behaviors to conceal
beneath the eye opposite the affected ear, because the the loss, but careful testing that pre vents patients from
oVEMP n10 is mediated by a crossed utriculo-ocular using these behaviors shows permanent deficit.
3970_Ch08_121-150 25/06/14 11:33 AM Page 132
Recovery of Dynamic Responses the subjective improvements. The evidence from Halmagyi
et al98 shows that neck input seems to ha ve little or no role
Recovery of Dynamic VOR—Slow Phases in generating slow-phase eye velocity responses to unpre-
Early studies of dynamic VOR recovery suggested that there dictable passive, angular high-acceleration head rotations. It
was considerable reco very of the dynamic VOR after may be important for the generation of saccadic corrections.
UVD.94 But for practical reasons, those studies were re- The paradox is that despite this very inadequate recov-
stricted to measuring the slow-phase eye velocity response ery of the VOR to natural dynamic stimuli, many post-UVD
to low-frequency, low-acceleration sine-wave rotations (with patients return to a normal lifestyle and are just not troubled
accelerations of the order of tens of deg/sec/sec). When stud- by the UVD and the VOR loss that our precision measures
ies with natural values of head accelerations (of the order of show that they have. They have “compensated” but evidently
thousands of deg/sec/sec) were used, it became clear that the not by synaptic changes in the v estibular nuclei for natural
recovery of dynamic VOR for ipsilesional head rotations was head accelerations, because their measured eye velocity for
small or none xistent. In patients tested before and after unpredictable passive ipsilesional head rotations remains
UVD, it was found that, for ipsilesional rotations, there was poor. Why then are they not troubled by their inadequate
a large drop in VOR gain immediately after the surgical loss, VOR? Two possibilities, which are not necessarily mutually
and over the ne xt year there w as very little reco very in exclusive, are (1) that the modest reco very of function for
gain. The mean velocity gain at 1 week for 11 patients was low-frequency stimuli is enough, or (2) that the y are using
0.25 +/– 0.21 (sd). The mean velocity gain at 1 year after other strategies, such as different patterns of eye-head coor-
UVD was 0.27 +/– 1.14 (sd).28,47 These patients are very un- dination, to overcome their loss. Our preliminary e vidence
usual, because tests before the UVD showed that their hor- suggests the latter, and that saccades may be the key. In the
izontal canal function w as normal. They underwent the area of vestibular compensation, the main focus has been on
surgical UVD to treat intractable benign paroxysmal posi- the compensatory slow-phase eye velocity without adequate
tioning vertigo, which affected their posterior canal. recognition of the fact that changes in saccadic pattern are a
Is there any recovery of VOR gain at all?Yes, there ap- very effective way of overcoming unilateral vestibular loss
pears to be some improvement in VOR gain for ipsilesional as suggested in 1989 byAlain Berthoz, who coined the term
rotations in the low-frequency, low-acceleration range.95,96 “saccadic substitution.”99 We suggest the focus for future
However, it is not kno wn how functionally effective this studies of plasticity in the compensation of oculomotor re-
small gain recovery is. As shown above, for higher (natural) sponses in human patients after UVD should be on saccades,
head accelerations as encountered during most natural ac- rather than on slow-phase eye velocity.55
tivities such as driving or sport, the evidence is that there is Permanent deficit of dynamic VOR function after
very little or no recovery of VOR gain. Cervical afferent input UVD shows that vestibular rehabilitation of UVD patients
is one of the man y other potential inputs that could modify should be aimed at developing new behaviors that substi-
and substitute for absent v estibular function (see Fig. 8.1). tute for the dynamic vestibular loss—for example, substi-
Potentiation of cervical sensory input may be rele vant for tuting saccades for the inadequate slow compensatory eye
improving responses to low-frequency head movements, es- velocity, rather than trying to restore slo w-phase eye ve-
pecially for active head movements. There is now evidence locity that cannot be restored.
from monkey behavioral studies that sho ws that cervico- These different patterns of saccadic responses after
ocular responses are potentiated after UVD and BVD and UVD lead to the hypothesis that the dif ferent groups of
that potentiation may assist in reco very of oculomotor re- patients using these different saccadic strategies may show
sponses to low-frequency head movements.95-97 Recently, different patterns of v estibular compensation.55 During
there has been evidence of neural mechanisms substituting testing at the stage of the acute attack, some VN patients
for vestibular input at low accelerations.96 In primates, it has already show changes in their pattern of saccades from
been found that extravestibular inputs (neck proprioceptive overt to covert, but it remains to be seen whether these
and efference copy information) substitute for v estibular “early coverters” in fact compensate better.
inputs after vestibular loss and act to stabilize gaze. It is
possible that at low head velocities, especially if actively
generated, these substitution mechanisms impro ve perfor-
Summary
mance. It is clear from the permanent loss of ipsilesional In Box 8-2, we list the permanent le gacies of unilateral
VOR that these mechanisms are not adequate at high (natural) vestibular loss, and in Table 8-1 we summarize the UVD
passive head accelerations, because such tests of long-term, symptoms and the general e xtent of their reco very. Most
well-compensated patients show the permanent loss. How- symptoms are at their maximum within the f irst day after
ever, these mechanisms probably account for a portion of the UVD.
3970_Ch08_121-150 25/06/14 11:33 AM Page 133
Oculomotor symptoms:
Spontaneous nystagmus Rhythmic eye movements with quick Decreased at 1 week
phases directed away from the affected Largely but incompletely recovered at
ear and toward the intact ear 1 year
Visible when all visual fixation has been
removed
Ocular torsion Maintained roll position of both eyes so Largely recovered within 6 months
the upper poles of both eyes roll toward (but not totally—some torsion still
the lesioned side present 12 months after UVD)
Visual perception is affected in a
corresponding fashion
Skew deviation Maintained disconjugate vertical eye posi- Resolves within a few days
tion with the ipsilesional eye being lower
in the orbit than the contralesional eye
Horizontal VOR to passive Reduced VOR gain for low-frequency, Steady improvement over months and
low angular accelerations low-angular-acceleration stimulation in an virtually resolved within 1 year
ipsilesional direction
Horizontal VOR to high Substantially reduced VOR gain (25% of Little change over 1 year and apparently
(natural) angular accelerations normal values) for high-frequency, high- a permanent loss
(head impulses) angular-acceleration stimulation (natural
values) in an ipsilesional direction
Continued
3970_Ch08_121-150 25/06/14 11:33 AM Page 134
Pitch VOR to passive high Reduced VOR gain for both pitch nose- Little change over 1 year—apparently
angular accelerations down and pitch nose-up accelerations permanent
Roll VOR to passive high Substantially reduced VOR gain for high Little change over 1 year
angular accelerations angular acceleration to stimulation in an
ipsilesional direction
Reduced VOR gain for high angular Little change over 1 year
accelerations in a contralesional direction
Canal plane head impulses Substantially reduced VOR gain (25% of Little change over 1 year
(left anterior–right posterior or normal values) for high-frequency, high-
right anterior–left posterior) angular-acceleration stimulation (natural
values) in an ipsilesional direction
Reduced VOR gain (80% of normal
values) for high-frequency, high-
angular-acceleration stimulation (natural
values) in a contralesional direction
Net result—asymmetrical VOR
Ocular counter-rolling Decreased ocular torsion during head Large asymmetry initially and
rotations toward the ipsilesional ear decreased asymmetry over time
Horizontal eye movements Smaller eye rotations for linear Resolution unknown
to impulses of interaural accelerations directed toward the
linear acceleration affected ear
(head heaves)
Vestibulospinal symptoms:
Roll head tilt Roll head tilt toward the affected side pres- Resolves within weeks but a small roll
ent when visual fixation has been removed head tilt may be a permanent legacy
(especially in animals after UVD)
Postural disequilibrium Poor postural stability when vision is Reduces but incompletely resolved
at rest removed within a year
Dynamic postural Poor postural stability when given Reduces over 1 year
disequilibrium dynamic challenges
Perceptual symptoms:
Lateropulsion Sensation of falling or being pushed Improved by 1 week; resolved within
toward the affected side 1 year
Vertigo In darkness: illusion that the patient is Resolved within a few days
rotating in yaw toward the affected side
OR
In light: illusion that the world is rotating
in yaw toward the healthy side
Roll-tilt illusion In darkness, the illusion is that the person Completely resolved within a few days
is roll-tilted toward the affected side
Linear acceleration perception Underestimation of the magnitude of lin- Largely but incompletely resolved at
ear accelerations toward the affected ear 1 year
later, the VOR for these same ipsilesional rotations had for compensation. In humans, v estibular compensation
fully returned. Similarly, the test of utricular function (the takes 3 to 5 days to get under way and a month or more to
oVEMP n10) at the acute attack shows an absent oVEMP achieve a functionally useful level.
n10 contralateral to the lesion, indicating that the utricular
function on the affected side was not present at the acute
Poor Compensation
phase, but 3 months later, utricular function had fully re-
turned. (In this patient, the saccular function w as not af- Most patients recover well after UVD and have an appar-
fected by the neuritis—it w as present at the acute phase ently normal lifestyle with good quality of life. But some
and also at reco very, probably because the neuritis w as patients do not. The reason for the poor reco very is puz-
confined to the superior division of the vestibular nerve). zling. In many cases, they present with similar symptoms
Without the results of the tests of peripheral v estibular to the well-compensated patients: their UVD procedure is
function, these responses would be classed as an excellent similar, but they do not recover as well as others. “Recov-
example of vestibular compensation. However, the objec- ery” has a large subjective component, and it is probable
tive measures of peripheral v estibular function show the that some of these patients had expected a much better out-
improved performance is a result of actual restoration of come. Detailed comparison of the vestibular performance
peripheral vestibular sensory function (Fig. 8.9). of such patients has so f ar not been able to identify an y
The processes of compensation are unlik ely to help clear differences post-UVD between well- and poorly
patients with short recurrent bouts of paroxysmal vestibu- compensated patients (see Box 8-2).
lar dysfunction as occurs in Ménière’ s disease, because Patients with poor compensation exhibit a syndrome
the process of compensation tak es some time (days or called chronic vestibular insufficiency, which consists of
weeks) to be implemented, whereas in patients with fluc- sensations of disequilibrium, gait ataxia (especially with
tuating vestibulopathies such as Ménière’s disease, the at- restricted vision on unstable surfaces), and oscillopsia. The
tacks of vertigo are brief compared with the time required ataxia is particularly evident when vision is disrupted and
3970_Ch08_121-150 25/06/14 11:33 AM Page 136
Horizontal
VOR gain 1.2 Gain Gain
Left 1.2 Left
Right Right
1 1
0.8 0.8
0.6 0.6
0.4 0.4
0.2 0.2
0 0
0 50 100 150 200 250 0 50 100 150 200 250
Peak Head Velocity (deg/s) Peak Head Velocity (deg/s)
oVEMPS oVEMPS
R eye R eye
L eye L eye
5 μV 10 ms 5 μV
10 ms
cVEMPS cVEMPS
R SCM
R SCM
− −
100 μV 100 μV
+ +
10 ms L SCM 10 ms L SCM
3970_Ch08_121-150 25/06/14 11:33 AM Page 137
Figure 8.9 Tests of peripheral vestibular function on the same patient on two occasions,92
separated by about 3 months. On the first occasion the patient was tested during an acute
attack of vertigo, which was diagnosed as superior vestibular neuritis. The tests of horizontal
canal function showed that, for head turns to the left (the affected side), there was a marked
reduction in slow-phase VOR gain (about 0.5) and many covert saccades, indicating a major loss
of function of the horizontal canal. The VOR for head turns to the intact side was minimally af-
fected (gain of 0.8). At testing 3 months later, the VOR gain for left head turns had returned to
normal values, and there were no covert saccades. The test of utricular function showed that
initially the oVEMP n10 was absent beneath the right eye (opposite the affected left ear), but
the oVEMP also returned to normal and symmetrical values at testing 3 months after the attack.
The marked recovery of function shown by tests of peripheral vestibular function justifies the
conclusion that there has been a complete restoration of normal vestibular function within
3 months, without special medication or rehabilitation. (From Manzari et al, 2011.92)
proprioception is challenged (e.g., by asking the patient to procedure is carried out inappropriately. Rehabilitation pro-
stand with eyes closed on a soft, thick, foam rubber mat). cedures are of potential value to such poorly compensated
Oscillopsia refers to the sensation of apparent movement patients, but prevention is preferable to rehabilitation.
of a physically stationary object during head mo vement In human patients, it is unwise to contemplate a UVD
(e.g., the world appears to bounce during jogging, or ap- when the level of vestibular function in the supposedly
pears to slide or smear during a rapid head movement dur- healthy ear is not adequate. For example, in Ménière’s dis-
ing driving). Oscillopsia is evident when the person’s head ease it is frequently the case that both ears are af fected
is moved abruptly (high accelerations) either passively or by the disease, but one ear is more affected than the other.
actively—during running or looking from side-to-side If a UVD procedure is carried out on the more af fected
while crossing a road or during a sudden head turn while ear in such patients, the patient will be relying on a partly
driving. dysfunctional ear to provide full vestibular input.103 It is
Why should this poor compensation occur? In not too surprising that in such cases the e ventual result
some cases, it seems that events (such as postoperative will be poor compensation or chronic v estibular insuffi-
complications) within the first few days after the oper- ciency. The sole remaining labyrinth will provide all the
ation may be important for determining the success or vestibular input for oculomotor, postural, and perceptual
otherwise of the e ventual recovery. There is some e vi- control for that person for the rest of his or her life. Is the
dence that the early stages of compensation—the initia- level of function in that remaining, supposedly healthy
tion of v estibular compensation—are vulnerable and labyrinth adequate to carry that b urden? With the new
may be interrupted by other events. In other words, there tests of peripheral v estibular function (vHIT, oVEMPs,
may be a sensiti ve period for the establishment of and cVEMPs), all peripheral vestibular sense organs can
vestibular compensation.100-101 Certainly there is neural be evaluated.77
and behavioral evidence from animal studies that under-
pins this distinction between the initiation and mainte-
nance of vestibular compensation (Vibert et al). 32 The
Decompensation
UVD procedure itself may inadv ertently generate the An apparently related phenomenon is decompensation.
conditions for poor compensation—if the UVD proce- Decompensation refers to situations in which v estibular
dure leaves some vestibular fibers intact and operational, compensation is nullified and the patient relapses partially
the neural signals from these f ibers may interfere with or completely, and the UVD syndrome returns—the spon-
the vestibular compensation process. taneous nystagmus, the sensations of vertigo, and the pos-
Some poorly compensated patients may have had in- tural disequilibrium reappear. Some situations, such as
adequate vestibular function or even central (e.g., cerebel- highly stressful ones, may trigger decompensation, 104-106
lar) deficits before the UVD procedure. 102 Thus, the UVD but even changing the vestibular environment may also do
procedure is potentially dangerous, and that is why careful so106: Reber et al reported that when well-compensated
pre-procedural testing is needed to ensure there is an ade- rats were exposed to a brief interval of microgravity during
quate level of function of the remaining labyrinth and an parabolic flight, they decompensated and showed sponta-
absence of central deficits before the UVD procedure is un- neous nystagmus and other signs on removal of the gravity
dertaken. Patients may suffer postural disequilibrium and stimulus. That decompensation disappeared within sec-
gait ataxia virtually for the rest of their li ves if the UVD onds of a return to 1 g. This suggests that changing the
3970_Ch08_121-150 25/06/14 11:33 AM Page 138
otolithic stimulation of the intact ear was sufficient to elicit on normal, healthy, young animals and is usually surgical
this brief decompensation. These data and other data sug- and usually complete. There is no attempt in most animal
gest that otolithic input from the remaining ear plays an studies to preserve hearing. The analogous human pa-
important role in compensation.12,107 tients would constitute a tiny minority of patients under-
going a UVD—most patients tend to be middle aged and
have had a chronic progressive disease of one labyrinth
Psychological Factors that has been ongoing for months or years, the other
Of course, psychological factors play a major role in com- labyrinth may be af fected, and the sur geon endeavors
pensation, but it is dif ficult to determine their precise to preserve hearing. One clear result is that dif ferent
role.108 Are psychological factors causal in determining symptoms—oculomotor and postural—recover at differ-
the outcome of UVD, or are they caused by the procedure ent rates.114-115 Blocking of neurogenesis in the vestibu-
itself? Bowman109 measured the personality characteris- lar nuclei of cats after UVD acts to impair reco very of
tics of well- and poorly compensated patients and found their postural balance, but it has no effect on the recovery
that poorly compensated patients showed higher scores on of spontaneous nystagmus.115 This differential rate of re-
tests of somatic awareness (attention to bodily sensations) covery is clearly shown in guinea pig compensation, in
than control subjects. However, it is not clear whether this which the spontaneous n ystagmus recovers quickly, but
result occurred because their poor compensation had en- the roll head tilt (longitudinal twist) is present man y
couraged them to focus attention on themselves or whether months after the UVD (Fig. 8.10).
this personality style had been present before the UVD Again referring to our simple schematic diagram of
procedure and caused their poor compensation. It is not information transmission in the v estibular system (see
surprising that people with a predisposition to hypochon- Fig. 8.1), one can understand how it is that many different
driasis would find the symptoms after UVD distressing. sensory manipulations can influence UVD and the rate of
Patients who ha ve had a UVD for treatment of a life- recovery. Deprivation of all visual input after UVD im-
threatening neuroma may be e xpected to respond more pedes the compensation of dynamic VOR responses to
positively compared with patients who ha ve chosen to low acceleration stimulation 96 and the static component
have a UVD to alleviate a much less threatening condition. of roll head tilt,116,117 but seems to have little effect on the
(See Chapters 18 and 19 for more discussion of psycho- reduction of spontaneous nystagmus after UVD. 94 Visual
logical factors.) inputs do augment the diminished motor responses to lin-
ear acceleration118 and the deficient righting reflexes119
that occur after UVD. Visual motion deprivation delays
Medication recovery of locomotor equilibrium.120-123
At the start of this chapter, we showed the variety of in- Similarly, stimulation of proprioceptive receptors ap-
fluences on transmission of neural information in the pears to facilitate the recovery of dynamic postural equi-
vestibular nucleus. Not only do vestibular neurons them- librium,124 and deprivation of proprioceptive input appears
selves use a v ariety of different neurotransmitters, but to retard the reco very of postural equilibrium. Cervical
they receive input from man y other brain re gions that proprioceptive input could be important in static compen-
can modulate the activity of these neurons and the trans- sation, because head restraint retards resolution of head
mission and processing of v estibular information. Be- tilt and spontaneous nystagmus, at least in guinea pigs.125
cause of the multi-input character of these neurons, a Somatosensory proprioceptive deprivation appears to re-
host of different medications can influence the UVD tard static compensation, 118 whereas somatosensory pro-
syndrome and its recovery. Whether any one neurotrans- prioceptive stimulation appears to facilitate the restoration
mitter is the “key” in such a complex system may well of dynamic postural equilibrium. 124 Acute spinal lesions
be a rather useless question. For reviews of medications can produce a temporary decompensation of static pos-
see references.3,110-113 tural symptoms.104,105
Only scant data exist on the effects of vestibular stim-
ulation or vestibular deprivation on static or dynamic com-
Evidence from Animal Studies pensation. In frogs, otolithic stimulation hastens, whereas
Despite the similar time course of vestibular compensa- otolithic deprivation delays, static compensation of roll-tilt
tion in humans and animals, the data from animal studies of the head. 126 In cats, low-frequency combined visual-
of vestibular compensation do not transfer directly to vestibular stimulation helps reverse the deficit in VOR gain,
human studies. In animal studies, the UVD is carried out which occurs in response to lo w-frequency stimulation
3970_Ch08_121-150 25/06/14 11:33 AM Page 139
Mean n = 6.2
Beats/15 sec
15
0 Hours 52 hr 3 days 4 mo 1 yr
3 24
Mean n = 5.7
60
Degrees
30
0 Hours 52 hr 3 days 4 mo 1 yr
3 24
Longitudinal Twist
90 Mean n = 5.7
60
Degrees
30
0 Hours 52 hr 3 days 4 mo 1 yr
3 24
Time Since Labyrinthectomy
Figure 8.10 Different symptoms of UVD recover at different rates as shown by averaged
measures of nystagmus and posture of guinea pigs over time after UVD. The nystagmus
decays very quickly—within about 52 hours. However, the roll-tilt of the head shows a com-
pletely different recovery profile, and at testing 4 months after UVD, there was still a small
but significant head roll-tilt present.
3970_Ch08_121-150 25/06/14 11:33 AM Page 140
following UVD,127 but has no effect on the asymmetry of The peripheral vestibular function of UVD patients
the VOR at high frequencies. differs substantially from that in normal healthy subjects:
the entire peripheral vestibular input from one labyrinth has
been removed or severely compromised, thereby depriving
VOR Plasticity the brainstem of both the resting discharge of these neurons
There is a long history of studies of v estibulo-ocular re- and its modulation by head mo vement. Possibly, the chal-
sponses that show that the gain of the VOR is modifiable lenge of such a loss for processes of vestibular plasticity is
in normal healthy subjects. Gonshor and Jones 128,129 re- too large: the UVD itself disrupts central vestibular process-
quired subjects to wear re versing spectacles during the ing of vestibular information. In particular, a group of neu-
course of their usual daily activities. To attain a stable reti- rons concerned with perse verating the v estibular neural
nal image in this situation, the VOR gain must decrease response (the velocity storage integrator) is compromised
and even reverse. VOR testing in darkness at re gular in- or disabled, and that may disrupt the neural substrate needed
tervals during this procedure sho wed that the VOR gain for vestibular modification.
did decrease, although not by the full amount required,
and there was no reversal. (Unfortunately, the VOR testing
in this study used predictable low-frequency sinusoidal ro- Rehabilitation
tations rather than pure tests of VOR function using natu-
Vestibular Compensation
ral angular accelerations, so we cannot be sure that the
and Rehabilitation
measured VOR gain increase was purely vestibular.) This
result triggered an explosion of interest in VOR plasticity. Many years ago, Ca wthorne and Cookse y suggested a
It appeared that mechanisms responsible for this VOR number of exercises to assist in the rehabilitation of pa-
plasticity may be used by UVD patients to assist their re- tients with vestibular disorders.130,131 Those exercises are
covery; however, more recent evidence indicates this does similar to those in use today. Doubts about the efficacy of
not happen. such exercises have been largely dispelled.132-135 If there
There is no doubt that the gain of the VOR can be is no change in purely vestibular function, how can these
modified with quite remarkable speed in normal healthy exercises benefit patients? How can patients improve? As
subjects—even within a fe w minutes. However, closer we have shown, substitution of other responses can effec-
consideration shows that such evidence is not really rele- tively conceal the vestibular deficit and so protect the pa-
vant for the situation confronting the UVD patient in tient from receiving smeared retinal images during head
vestibular compensation. Some of the procedures that have movements. Such substitution is possible when there is
been developed for the study of VOR plasticity do assist active control of the response by the patient, and we sug-
patients to improve their normal everyday functioning, but gest that the Cawthorne-Cooksey exercises and other such
we suggest these impro vements are not a result of an y exercises are acting to teach patients ho w to substitute
change in the intrinsic vestibular component of the VOR. these other responses to conceal and thus overcome their
If VOR was as modifiable as the VOR plasticity literature sensory deficit. The results of others136 agree with our own
suggests, then diagnostic tests of vestibular function would results.63 The active VOR gain is enhanced during active
be useless and even unnecessary. Patients would learn to voluntary head movements, and during active head im-
overcome their inadequate v estibular input and generate pulses, patients can learn to preprogram a small eye move-
compensatory responses even when they had total unilat- ment response (a small correcti ve saccade) during the
eral peripheral vestibular loss. ipsilesional head movement that can effectively hide their
It is certainly the case that, during v estibular com- inadequate VOR during that ipsilesional head rotation. 63
pensation, patients do learn a variety of behavioral strate- (See also Chapters 9 and 22.)
gies to minimize the effect of their vestibular deficit, but It is our contention that the development of new eye-
all indications are that an y plasticity of the purely head coordination strategies should be facilitated by train-
vestibular dynamic slow-phase eye velocity response is ing with active head turns. If one asks the same patient to
very modest at natural head angular accelerations. F or maintain gaze in a comparable fashion to the passive head
UVD patients, we think that most of the “plasticity” impulse test described above while they actively turn their
takes place because of contributions of other sensory sys- own head abruptly to left or right, most patients learn to
tems and cognitive control: the patient learns new behav- preprogram a small saccade to correct for inadequateVOR
iors to conceal the v estibular deficit. This achieves the and to insert this saccade during the head movement (see
sought-after goal of returning the patient to a normal Fig. 8.7).63 This is an important observ ation, because it
lifestyle. shows that patients are learning to substitute this (covert)
3970_Ch08_121-150 25/06/14 11:33 AM Page 141
saccade for the deficient vestibular slow phase. Also, it Changes in perception, and also in correcti ve responses
shows that this (covert) saccade acts to minimize the effect (vestibulo-ocular and vestibulo-spinal), are generated by
of the UVD on the patients’ permanent dynamic VOR that neural imbalance. If the acceleration is prolonged,
deficit. Another way of concealing a VOR inadequacy is there is nystagmus.
by a blink, which, by completely remo ving the retinal Another way of generating such an imbalance is by
image, very effectively prevents smear of the retinal silencing the input from one labyrinth in a patient at rest,
image. Blinks are common during head movements in nor- as occurs in a UVD. In both cases, the responses and the
mal healthy subjects and in UVD patients. Ironically, most sensations are similar: the person perceives him- or herself
tests of VOR (including the head impulse test) prevent pa- as rotating, there is a n ystagmus, and corrective postural
tients from using blinks. They require patients to k eep responses occur. Most real-life angular and linear accel -
their eyes wide open during testing. In other w ords, the erations are usually fairly short, and at the end of the ac-
testing procedure itself requires patients to suppress one celeration the system returns to its balanced state. But after
of the strategies (blinks) that they may have learned to as- UVD, the imbalance at rest—without any imposed angu-
sist their vestibular recovery. lar or linear acceleration stimulus—persists for hours or
Patients appear to learn new patterns of eye-head co- days. Recordings of neural acti vity have shown that the
ordination. However, the initial preference of man y pa- imbalance at rest is progressively reduced within the first
tients is to restrict head movements totally—to “lock” the few days; the v ery active cells in the contralesional
head on body. This decreases the opportunity for the pa- vestibular nucleus decrease their acti vity, and silenced
tients to learn any new pattern of eye-head coordination. neurons in the ipsilesional vestibular nucleus start to fire
In our view, patients should be encouraged to e xecute again. As that imbalance is reduced, so the behavioral and
eye-head refixations—for example, by the spouse giving perceptual symptoms decline.142
them passive, unpredictable horizontal head impulses for Why should rebalancing occur? What processes act
a few minutes per day. to remove the imbalance and equalize firing in the two nu-
We suggest that the process of vestibular rehabilitation clei? In the guinea pig after a UVD, this happens in the
should be thought of as an opportunity for other non- space of about one day , and by 52 hours after UVD, the
vestibular sensory inputs and cognitive-behavioral strategies average activity on both sides is about equal.142 The spon-
to increase their role in controlling the patient’s equilibrium. taneous nystagmus disappears, although the dynamic
deficits remain. There is no substantial change of peripheral
vestibular afferents of the remaining ear.143 As the balanced
Neural Evidence Concerning neural activity returns, the static behavioral symptoms dis-
Recovery after UVD appear. Concurrently, other sources of control of neural
transmission through the vestibular nuclei (e.g., cerebellar
Overview input) are changing. The following examines this process
This is a huge area, and in this chapter we refer only to in more detail (Fig. 8.11). This and the following summa-
the major features. F or reviews of neural processing of rize material from references.141,144-150
vestibular sensory input, see references.137-141 The physiological characteristics of primary afferent
There is one simple principle that helps us to under- neurons on the remaining (intact) side do not appear to
stand the neural basis of vestibular responses and vestibu- change after loss of the contralateral labyrinth, which had
lar compensation, and that is “balance.” That term is often been considered as a possible mechanism subserving
used to denote the function of the whole v estibular sys- vestibular compensation.151 However, it does appear that
tem, but it also coincidentally applies to the neural mech- after such a contralateral loss there is a higher proportion
anism of vestibular operation. When a person holds the of irregular afferents on the intact side: 34% post-lesion
head still, the neural activity in the pair of vestibular nu- versus 22% pre-lesion, and the proportion of regular neu-
clei (one on each side of the brainstem) is approximately rons similarly decreases.151
equal—balanced. If there is a horizontal (ya w) angular Within the medial v estibular nucleus, there are tw o
acceleration in one direction, for example, to the person’s types of neurons responding to horizontal (yaw) rotation.
left, then it causes an imbalance in neural activity between Both neuron types discharge spontaneously when the head
the vestibular nuclei. Many neurons in the ipsilateral (left) is stationary. During yaw angular head accelerations in an
vestibular nucleus increase their rate of f iring of action ipsilateral direction, Type I neurons in the ipsilateral
potentials, while many neurons in the right vestibular nu- vestibular nucleus increase their firing, and these neurons
cleus concurrently decrease their f iring. The result is an decrease their firing for yaw head accelerations in the con-
imbalance in neural activation between the tw o nuclei. tralateral direction. These neurons receive direct input
3970_Ch08_121-150 25/06/14 11:33 AM Page 142
Oculomotor
Nucleus
Abducens
Nucleus
Vestibular
Nuclei
Primary
Semicircular
Canal Afferents
from the ipsilateral peripheral vestibular labyrinth. Other head. These indirect connections cross the midline and are
neurons within that same ipsilateral v estibular nucleus called commissural connections, and the y play a major
(Type II neurons) show precisely the opposite pattern of role in vestibular compensation.152 Type II neurons are in-
response: they increase their firing for contralaterally di- hibitory neurons and project their inhibition onto Type I
rected head accelerations and decrease it for ipsilateral neurons. Type I and Type II neurons work synergistically.
head accelerations. These Type II neurons respond in such During an acceleration, Type I neurons increase their fir-
a mirror-image fashion because they are driven (indirectly) ing, because they are receiving activation from the periph-
by cells from the other labyrinth on the other side of the ery and also simultaneously receiving reduced inhibition
3970_Ch08_121-150 25/06/14 11:33 AM Page 143
from Type II neurons. This synergistic mechanism means even though the cells in the ipsilesional nucleus are no
there is enhanced sensitivity of Type I neurons during ac- longer receiving any neural input from its labyrinth. Are
celeration compared with the sensiti vity of peripheral these changes caused only by a neural process such as
vestibular neurons. It is a “push-pull” system, and it func- adaptation, or is there an “error signal” that triggers those
tions to generate a fast, sensitive response. changes? Does the removal of peripheral vestibular input
Immediately after UVD, there are changes in the ac- trigger synaptic or membrane change that acts to restore
tivity of both types of neurons on the lesioned side while the balance between the two nuclei? There is evidence for
the animal is absolutely stationary. The resting discharge changes both at the synaptic and cell membrane level dur-
rate of ipsilesional Type I neurons is substantially de- ing compensation.153-155
creased, and the resting dischar ge of ipsilesional Type II How could the neural balance be restored? Adapta-
neurons is substantially increased.1 These Type II neurons tion is one possibility: that the firing rate of the more active
thus exert even more inhibition than usual on the ipsile- contralesional Type I neurons reduces over time so these
sional Type I neurons, presumably driving them to silence neurons exert less inhibition onto neurons on the ipsile-
and so completely disinhibiting the Type I neurons on the sional side. Another is that the neurotransmitter receptors
intact side. in the ipsilesional Type I neurons become less sensitive to
When the input from one labyrinth is remo ved by a the inhibitory transmitter released by the o veractive in-
UVD, Type I neurons in the ipsilesional nucleus are si- hibitory Type II neurons. Most interest has focused on
lenced, resulting in an imbalance in neural acti vity be- GABA.156-164 A reduction in the efficacy of the neurotrans-
tween the paired vestibular nuclei. Their silence relieves mitter receptor for GABA would allow for greater activity
Type I neurons in the opposite (“contralesional”) vestibu- by ipsilesional Type I neurons. In this w ay, ipsilesional
lar nucleus of inhibition, and so the y can fire at a higher Type I neurons w ould start to return to normal le vels of
rate. As the Type I neurons on the lesioned side progres- resting discharge, because they would not be affected by
sively start to fire again, the neurons in the intact side will as much inhibition as before. This idea is referred to as
receive progressively more inhibition, further enhancing “down regulation of GABA sensitivity” being responsible
the restoration of balanced neural acti vity. So, the de- for the restoration of balanced activity in the two vestibular
creased activity of ipsilesional Type I neurons reflects the nuclei.
loss of peripheral excitatory drive and the increased inhi- The UVD generates a cascade of neural changes—for
bition from the contralateral labyrinth mediated by the in- example, astrocytes and microglia rapidly increase in the
hibitory Type II neurons. vestibular nucleus.165,166 Over time, there are signif icant
How do these neural changes relate to the UVD syn- anatomical changes in the vestibular nuclei,167-170 although
drome and its recovery? The static motor symptoms and it seems that the behavioral effects of compensation occur
the perceptual illusions of v ertigo and roll-tilt are lik ely before sprouting.171 Evidence from Campos-Torres et al
caused by the imbalance in a verage neural activity be- (2005)172 and Lacour et al (2009) 173 indicates that the
tween cells in the v estibular nuclei on each side of the effects of silencing peripheral neurons by chemical means
brainstem. The deficits in dynamic responses are proba- (tetrodotoxin) as opposed to silencing by surgical section-
bly a result of the decreased dynamic sensiti vity of ing of the nerv e, are not identical. Tetrodotoxin does not
vestibular nucleus neurons as documented by Markham cause degeneration, and Campos-Torres et al (2005) 172
et al (1977).145 found it causes no glial changes in the vestibular nuclei, as
It should be noted that, in general, the restoration of opposed to the dramatic increase in glia following section-
static equilibrium (i.e., static compensation) is remarkably ing or damage to the vestibular nerve. Such results suggest
robust: very little appears to hasten or hinder it. That that the “error signal” may well be a chemical f actor re-
robustness is in contrast to the restoration of dynamic leased by the injured neurons.
equilibrium—dynamic compensation—which appears to Recent studies have recorded the characteristics of
depend at least in part on intact visual, vestibular, and pro- neurons in slices of brainstem tissue taken from animals
prioceptive sensory inputs. Dynamic compensation is usu- that have compensated for various durations after UVD.
ally incomplete. Tighilet et al (2007) 115 showed the clear These studies record neurons either e xtracellularly or
dissociation between the recovery of spontaneous nystag- intracellularly from such brainstem slices. In this situa-
mus as opposed to the recovery of postural compensation. tion, it is not possible to identify Type I and Type II neu-
In the hours, days, and weeks that follo w, there is a rons, because there is no peripheral vestibular input. The
remarkable change in the acti vity of vestibular nucleus cells are divided arbitrarily according to their membrane
neurons. The discharge rates of both Type I and Type II characteristics into Type A and Type B neurons, which
neurons on the lesioned side return much closer to normal, have very different action potential prof iles. Type A
3970_Ch08_121-150 25/06/14 11:33 AM Page 144
neurons are tonically firing neurons; Type B neurons tend Neural Network Models of Vestibular
to be phasic. Researchers have reported that, after UVD, Function and Compensation
the membrane characteristics of Type B neurons appear
to change.174,175 These previously phasic neurons appear These physiological changes have been incorporated into
to take on much more tonic characteristics. There have neural network models of the VOR that model the possible
been other reports of very long-lasting changes in intrinsic mechanisms of the UVD syndrome and compensation.
191-195 Cartwright’s physiologically realistic neural net-
membrane characteristics after prolonged inhibition.176,177
It is likely that membrane changes are responsible in part work model was trained on guinea pig eye-movement re-
for the changes in global neural activity to UVD we have sponses before and after UVD and sho wed that changes
described above. in activity in various stages through the neural netw ork
determine the responses.192-195 The model pointed to neu-
rons on the intact side as being especially important, be-
Angular versus Linear Acceleration cause their gain changes most.
Otolithic neurons project to the lateral and descending
vestibular nuclei but also send a branch to the cerebellum.
Recordings from LVN neurons show that most neurons
Summary
show an increase in firing for such ipsilateral roll-tilt stim- The vestibular system is a very fundamental sensory sys-
uli.35 Following a UVD, there is a decrease in the propor- tem whose activity influences many motor systems as well
tion of ipsilesional LVN neurons and a decrease in their as generating perceptual e xperiences. So, disruption of
average resting activity.178,179 So, a similar imbalance oc- vestibular function has f ar-reaching consequences. After
curs to natural linear accelerations as described above for UVD, some symptoms reco ver, but some do not. Ov er
natural angular accelerations. Again, that imbalance is time, patients resume their lifestyle mainly, we think, be-
mimicked by a remo val of all the peripheral v estibular cause of this partial “patchw ork” recovery and because
neural input from one side. they learn a variety of new behaviors to allow normal func-
tion. However, when the appropriate tests are carried out,
probing purely vestibular function and preventing some of
Cerebellum
the other “strategies” that the patient may have learned, the
The cerebellum plays an important role in vestibular com- permanent loss of many vestibular functions is very clear.
pensation,180 which has not been fully recognized because Taking such patients into a clinic and trying to assess
so much focus has been on the v estibular nucleus. Data the mechanism of their recovery, based on a few classical
on the effects of lesions of the cerebellum or its connec- measures of oculomotor performance using unnaturally
tions on v estibular compensation are contradictory . low values of head acceleration and restricting the pa-
Whereas some cerebellar lesion studies sho w a marked tient’s use of other strategies (e.g., excluding blinks dur-
delay in the resolution of spontaneous nystagmus, others ing HIT testing), may not re veal the subtle but effective
show no effect.180-182 Although bilateral occipital lobec- compensatory strategies that patients actually use in real
tomy has no effect on the resolution of spontaneous nys- life. It w as only by using high-speed, high-r esolution
tagmus, it does impede the reco very of the VOR to measures of eye movements that we detected the very small,
low-acceleration stimulation.94 Lesions of the brainstem but very effective, covert saccades during the passive high-
or transcerebellar vestibular commissures do not impede acceleration head movements, and it is these co vert sac-
the vestibulospinal symptoms of static compensation, at cades that we no w think may hold one of the k eys to
least in mammals.183,184 This suggests that input from the understanding compensation of oculomotor symptoms.
contralesional (intact) vestibular nucleus is not essential Saccades are the new frontier in vestibular compensation,
for static compensation. Kitahara et al ha ve shown that and the major question now is what triggers them.
neurons in the flocculus of the cerebellum play an impor- Substitution of other responses can ef fectively con-
tant role in the early stages of v estibular compensation ceal the vestibular deficit and so protect the patient from
for static symptoms.185,186 They have proposed that neu- receiving smeared retinal images during head movements.
rons in the flocculus may inhibit the hyperacti ve Type I The permanent deficit of dynamic VOR function to natural
neurons in the contralesional v estibular nucleus, and so accelerations after UVD shows that vestibular rehabilita-
act to reduce the overactive Type I neurons, which would tion of UVD patients should be aimed at developing new
in turn act to relieve inhibition on the ipsilesional Type I saccadic behavior that substitutes for the dynamic vestibu-
neurons.187-189 Human patients with cerebellar lesions lar loss, rather than trying to restore something that cannot
show slow compensation.190 be restored.
3970_Ch08_121-150 25/06/14 11:33 AM Page 145
The Final Question—Are They Happy? JM, Martini A, Stephens D, eds. Textbook of Audiological
Medicine: Clinical Aspects of Hearing and Balance.
Although vestibular compensation appears to be a simple London: Martin Dunitz; 2003:797-818.
recovery of function, there is overwhelming evidence that 11. Halmagyi GM, Curthoys IS, et al. Clinical applications of
basic vestibular research. In:Highstein SM, Fay RR, Pop-
there are many different processes taking place during
per AN, eds. The Vestibular System. New York: Springer
vestibular compensation. It is also clear that the v arious Verlag; 2004:496-545.
processes recover at different rates, or in some cases, do 12. Straka H, Dieringer N. Basic organization principles of the
not recover at all, while new behaviors are being learned VOR: lessons from frogs. Prog Neurobiol. 2004;73(4):
to substitute for the lost v estibular function. Many pa- 259-309.
13. Dutia MB. Mechanisms of vestibular compensation. In:
tients do learn these new behaviors, and have a satisfac-
Luxon L, Davies R, eds. Handbook of Vestibular Rehabili-
tory recovery—they compensate. But some patients, for tation. London: Whurr Press; 2005.
reasons that we do not yet understand, do not appear to 14. Borel L, Lopez C, et al. Vestibular syndrome: a change in
learn the successful behaviors and are unhappy. The chal- internal spatial representation. Neurophysiologie Clinique-
lenge is to identify ho w these poorly compensated pa- Clinical Neurophysiology. 2003;38(6):375-389.
15. Cullen KE, Minor LB, et al. Neural substrates underlying
tients can be taught to impro ve their lifestyle. With our
vestibular compensation: contribution of peripheral versus
colleagues, we are seeking to teach such patients strate- central processing. J Vestib Res. 2009;19(5-6):171-182.
gies that will help them. 16. Peusner K, Vidal PP, et al. Vestibular compensation: new
clinical and basic science perspectives. J Vestib Res.
2009;19(5-6):143-146.
Acknowledgments 17. Dutia MB. Mechanisms of vestibular compensation: re-
cent advances. Curr Opin Otolaryngol Head Neck Surg.
The revision of this chapter is supported by theAustralian 2010;18(5):420-424.
National Health and Medical Research Council (632746) 18. Halmagyi GM, Weber KP, et al. Vestibular function after
and the Garnett P asse and Rodney Williams Memorial acute vestibular neuritis. Restor Neurol Neurosci. 2010;
28(1):37-46.
Foundation. We thank Ann Burgess for her meticulous
19. Horak FB. Postural compensation for vestibular loss and
proofreading of this manuscript. implications for rehabilitation. Restor Neurol Neurosci.
2010;28(1):57-68.
20. Lacour M, Tighilet B. Plastic events in the vestibular nu-
References clei during vestibular compensation: the brain orchestra-
1. Smith PF, Curthoys IS. Neuronal activity in the contralateral tion of a “deafferentation” code. Restor Neurol Neurosci.
medial vestibular nucleus of the guinea pig following unilat- 2010;28(1):19-35.
eral labyrinthectomy. Brain Res. 1995;444(2):295-307. 21. Balaban CD, Hoffer ME, et al. Top-down approach to
2. Curthoys IS, Halmagyi GM. 1995. Vestibular compensa- vestibular compensation: translational lessons from vestibu-
tion: a review of the oculomotor, neural, and clinical con- lar rehabilitation. Brain Research. 2012;1482:101-111.
sequences of unilateral vestibular loss. J Vestib Res. 1995; 22. Lacour M, Dutheil S, et al. Tell Me Your Vestibular
5(774300)4:67-107. Deficit, and I’ll Tell You How You’ll Compensate. Basic
3. de Waele C, Muhlethaler M, et al. Neurochemistry of the and Clinical Aspects of Vertigo and Dizziness. Ann N Y
central vestibular pathways. Brain Res Brain Res Rev. Acad Sci. 2009;1164:268-278.
1995;20(1):24-46. 23. Carey J. Intratympanic gentamicin for the treatment of
4. Dieringer N. ‘Vestibular compensation’: neural plasticity Meniere’s disease and other forms of peripheral vertigo.
and its relations to functional recovery after labyrinthine Otolaryngol Clin North Am. 2004;37(5):1075-1090.
lesions in frogs and other vertebrates. Prog Neurobiol. 24. Hirvonen TP, Minor LB, et al. Effects of intratympanic
1995;46(2-3):97-129. gentamicin on vestibular afferents and hair cells in the
5. Kitahara T, Takeda N, et al. Unilateral labyrinthectomy chinchilla. J Neurophysiol. 2005;93(2):643-655.
downregulates glutamate receptor delta-2 expression in the 25. Migliaccio AA, Minor LB, et al. Vergence-mediated mod-
rat vestibulocerebellum. Brain Res Mol Brain Res. ulation of the human horizontal vestibulo-ocular reflex is
1998;61(1-2):170-178. eliminated by a partial peripheral gentamicin lesion. Exp
6. Vidal PP, de Waele C, et al. Vestibular compensation revis- Brain Res. 2004;159(1):92-98.
ited. Otolaryngol Head Neck Surg. 1998;119(1):34-42. 26. De Waele C, Meguenni R, et al. Intratympanic gentamicin
7. Curthoys IS, Halmagyi GM. Vestibular compensation. Adv injections for Meniere disease: vestibular hair cell impair-
Otorhinolaryngol. 1999;55:82-110. ment and regeneration. Neurology. 2002;59(9):1442-1444.
8. Curthoys IS. Vestibular compensation and substitution. 27. Dai MJ, Curthoys IS, et al. Linear acceleration perception
Curr Opin Neurol. 2000;13(1):27-30. in the roll plane before and after unilateral vestibular
9. Darlington CL, Smith PF. Molecular mechanisms of re- neurectomy. Exp Brain Res. 1989;77(2):315-328.
covery from vestibular damage in mammals: recent ad- 28. Halmagyi GM, Curthoys IS, et al. The human horizontal
vances. Prog Neurobiol. 2000; 62(3):313-325. vestibulo-ocular reflex in response to high-acceleration
10. Halmagyi GM, Cremer PD, et al. Peripheral vestibular stimulation before and after unilateral vestibular neurec-
disorders and diseases in adults. In: Luxon LM, Furman tomy. Exp Brain Res. 1990;81(3):479-490.
3970_Ch08_121-150 25/06/14 11:33 AM Page 146
29. Curthoys IS, Dai MJ, et al. Human ocular torsional posi- Neurophysiologic and Clinical Research, New York:
tion before and after unilateral vestibular neurectomy. Raven Press; 1987:471-479.
Exp Brain Res. 1991;85(1):218-225. 48. Tabak S, Collewijn H, et al. Gain and delay of human
30. Halmagyi GM, Gresty MA, et al. Ocular tilt reaction with vestibulo-ocular reflexes to oscillation and steps of the head
peripheral vestibular lesion. Ann Neurol. 1979;6(1): 80-83. by a reactive torque helmet. II. Vestibular-deficient subjects.
31. Safran AB, Vibert D, et al. Skew deviation after vestibular Acta Otolaryngol. 1997;117(6):796-809.
neuritis. Am J Ophthalmol. 1994;118(8053470):238-245. 49. Halmagyi GM, Curthoys IS. A clinical sign of canal pare-
32. Vibert D, Hausler R, et al. Diplopia from skew deviation sis. Arch Neurol. 1988;45(7):737-739.
in unilateral peripheral vestibular lesions. Acta Otolaryn- 50. Tabak S, Collewijn H, et al. Gain and delay of human
gol. 1996;116(2):170-176. vestibulo-ocular reflexes to oscillation and steps of the
33. Wolfe GI, Taylor CL, et al. Ocular tilt reaction resulting head by a reactive torque helmet. I. Normal subjects and
from vestibuloacoustic nerve surgery. Neurosurgery. II. Vestibular-deficient. Acta Otolaryngol. 1997;
1993;32(3):417-420. 117(6):785-795 and 796-809
34. Vibert D, Hausler R, et al. Ocular tilt reaction associated 51. Gilchrist DP, Curthoys IS, et al. High acceleration impul-
with a sudden idiopathic unilateral peripheral cochleovestibu- sive rotations reveal severe long-term deficits of the hori-
lar loss. ORL J Otorhinolaryngol Relat Spec.1995;57(6): zontal vestibulo-ocular reflex in the guinea pig. Exp Brain
310-315. Res. 1998;123(3):242-254.
35. Pompeiano O, Xerri C, et al. Central compensation of 52. Lasker DM, Backous DD, et al. Horizontal vestibuloocular
vestibular deficits. II. Influences of roll tilt on different- reflex evoked by high-acceleration rotations in the squirrel
size lateral vestibular neurons after ipsilateral labyrinth monkey. II. Responses after canal plugging. J Neurophys-
deafferentation. J Neurophysiol. 1984;52(1):18-38. iol. 1999;82(3):1271-1285.
36. Wade SW, Curthoys IS. The effect of ocular torsional po- 53. Lasker DM, Hullar TE, et al. Horizontal vestibuloocular
sition on perception of the roll-tilt of visual stimuli. Vision reflex evoked by high-acceleration rotations in the squirrel
Res. 1997;37(8):1071-1078. monkey. III. Responses after labyrinthectomy. J Neuro-
37. Bergenius J, Tribukait A, et al. The subjective horizontal at physiol. 2000;83(5):2482-2496.
different angles of roll-tilt in patients with unilateral vestibu- 54. Weber KP, Aw ST, et al. Head impulse test in unilateral
lar impairment. Brain Res Bull. 1996;40(5-6):385-390. vestibular loss: vestibulo-ocular reflex and catch-up sac-
38. Tribukait A, Bergenius J, et al. Subjective visual horizon- cades. Neurology. 2008;70(6):454-463.
tal during follow-up after unilateral vestibular deafferenta- 55. Macdougall HG, Curthoys IS. Plasticity during vestibular
tion with gentamicin. Acta Otolaryngol. 1998;118(4): compensation: the role of saccades. Front Neurol. 2012;3:21.
479-487. 56. Richards W. Saccadic suppression. J Opt Soc Am. 1969;
39. Friedmann G. The judgement of the visual vertical and 59(5):617-623.
horizontal with peripheral and central vestibular lesions. 57. Matin E. Saccadic suppression: a review and an analysis.
Brain. 1970;93(2):313-328. Psychol Bull. 1974;81(12):899-917.
40. Goto F, Kobayashi H, et al. Compensatory changes in 58. Aw ST, Halmagyi GM, et al. Unilateral vestibular deaf-
static and dynamic subjective visual vertical in patients ferentation causes permanent impairment of the human
following vestibular schwannoma surgery. Auris Nasus vertical vestibulo-ocular reflex in the pitch plane. Exp
Larynx. 2003;30(1):29-33. Brain Res. 1994;102(1):121-130.
41. Hafstrom A, Fransson P-A, et al. Idiosyncratic compensa- 59. Aw ST, Halmagyi GM, et al. Compensation of the human
tion of the subjective visual horizontal and vertical in vertical vestibulo-ocular reflex following occlusion of one
60 patients after unilateral vestibular deafferentation. vertical semicircular canal is incomplete. Exp Brain Res.
Acta Otolaryngol. 2004;124(2):165-171. 1995;103(3):471-475.
42. Black FO, Shupert CL, et al. Effects of unilateral loss of 60. Aw ST, Halmagyi GM, et al. Three-dimensional vector
vestibular function on the vestibulo-ocular reflex and postural analysis of the human vestibuloocular reflex in response
control. Ann Otol Rhinol Laryngol. 1989;98(11):884-889. to high-acceleration head rotations. II. Responses in
43. Borel L, Harlay F, et al. Deficits and recovery of head and subjects with unilateral vestibular loss and selective
trunk orientation and stabilization after unilateral vestibu- semicircular canal occlusion. J Neurophysiol. 1996;
lar loss. Brain. 2002;125(4):880-894. 76(6):4021-4030.
44. Takahashi M, Uemura T, et al. Recovery of vestibulo-ocu- 61. Aw ST, Haslwanter T, et al. Three-dimensional vector
lar reflex and gaze disturbance in patients with unilateral analysis of the human vestibuloocular reflex in response to
loss of labyrinthine function. Ann Otol Rhinol Laryngol. high-acceleration head rotations. I. Responses in normal
1984;93(2 Part 1):170-175. subjects. J Neurophysiol. 1996;76(6):4009-4020.
45. Jenkins HA. Long-term adaptive changes of the vestibulo- 62. Cremer PD, Halmagyi GM, et al. Semicircular canal plane
ocular reflex in patients following acoustic neuroma sur- head impulses detect absent function of individual semi-
gery. Laryngoscope. 1985;95(10):1224-1234. circular canals. Brain. 1998;121(Pt 4):699-716.
46. Paige GD. Nonlinearity and asymmetry in the human 63. Black RA, Halmagyi GM, et al. The active head-impulse
vestibulo-ocular reflex. Acta Otolaryngol. 1989;108 test in unilateral peripheral vestibulopathy. Arch Neurol.
(1-2):1-8. 2005;62(2):290-293.
47. Halmagyi GM, Curthoys IS. Human compensatory slow 64. Diamond SG, Markham CH. Binocular counterrolling in
eye movements in the absence of vestibular function. In: humans with unilateral labyrinthectomy and in normal
Graham MD, Kemink JL, eds. The Vestibular System: controls. Ann N Y Acad Sci. 1981;374:69-79.
3970_Ch08_121-150 25/06/14 11:33 AM Page 147
65. Diamond SG, Markham CH. Ocular counterrolling as an 82. Murofushi T, Curthoys IS, et al. Response of guinea pig
indicator of vestibular otolith function. Neurology. 1983; vestibular nucleus neurons to clicks. Exp Brain Res. 1996;
33(11):1460-1469. 111(1):149-152.
66. Schmid-Priscoveanu A, Straumann D, et al. Vestibulo- 83. Uchino Y, Sasaki M, et al. Otolith and canal integration on
ocular responses during static head roll and three-dimen- single vestibular neurons in cats. Exp Brain Res. 2005;
sional head impulses after vestibular neuritis. Acta Oto- 164(3):271-285.
laryngol. 1999;119(7):750-757. 84. Colebatch JG, Halmagyi GM. Vestibular evoked poten-
67. Crane BT, Tian J, et al. Initiation of the human heave lin- tials in human neck muscles before and after unilateral
ear vestibulo-ocular reflex. Exp Brain Res. 2003;148(2): vestibular deafferentation. Neurology. 1992;42(8):
247-255. 1635-1636.
68. Ramat S, Zee DS. Ocular motor responses to abrupt inter- 85. Colebatch JG, Halmagyi GM, et al. Myogenic potentials
aural head translation in normal humans. J Neurophysiol. generated by a click-evoked vestibulocollic reflex. J Neu-
2003;90(2):887-902. rol Neurosurg Psychiatry. 1994;57(2):190-197.
69. Bronstein AM, Gresty MA, et al. Compensatory otolithic 86. Rosengren SM, Welgampola MS, et al. Vestibular evoked
slow phase eye movement responses to abrupt linear head myogenic potentials: past, present and future. Clinical
motion in the lateral direction. Findings in patients with Neurophysiology. 2010;121(5):636-651.
labyrinthine and neurological lesions. Acta Otolaryngol 87. Weber KP, Rosengren SM, et al. Single motor unit activity
Suppl. 1991;481:42-46. in human extraocular muscles during the vestibulo-ocular
70. Lempert T, Gianna CC, et al. Effect of otolith dysfunction. reflex. Journal of Physiology-London. 2012;590(13):
Impairment of visual acuity during linear head motion in 3091-3101.
labyrinthine defective subjects. Brain. 1997;120(Pt 6): 88. Rosengren SM, Welgampola MS, et al. Vestibular evoked
1005-1013. myogenic potentials: past, present and future. Clin Neuro-
71. Crane BT, Tian J-R, et al. Initiation and cancellation of the physiol. 2010;121(5):636-651.
human heave linear vestibulo-ocular reflex after unilateral 89. Iwasaki S, Chihara Y, et al. The role of the superior
vestibular deafferentation. Exp Brain Res. 2005;161(4): vestibular nerve in generating ocular vestibular-evoked
519-526. myogenic potentials to bone conducted vibration at Fz.
72. Iwasaki S, Smulders YE, et al. Ocular vestibular evoked Clinical Neurophysiology. 2009;120(3):588-593.
myogenic potentials in response to bone-conducted vibra- 90. Manzari L, Tedesco A, et al. Ocular vestibular-evoked
tion of the midline forehead at Fz. A new indicator of myogenic potentials to bone-conducted vibration in supe-
unilateral otolithic loss. Audiol Neurootol. 2008;13(6): rior vestibular neuritis show utricular function. Otolaryn-
396-404. gology-Head and Neck Surgery. 2010;143(2):274-280.
73. Curthoys IS, Kim J, et al. Bone conducted vibration selectively 91. Rosengren SM, McAngus Todd NP, et al. Vestibular-
activates irregular primary otolithic vestibular neurons in evoked extraocular potentials produced by stimulation
the guinea pig. Exp Brain Res. 2006;175(2):256-267. with bone-conducted sound. Clin Neurophysiol. 2005;
74. Curthoys IS, Vulovic V, et al. Irregular primary otolith af- 116(8):1938-1948.
ferents from the guinea pig utricular and saccular maculae 92. Manzari L, Burgess AM, et al. Objective verification of
respond to both bone conducted vibration and to air con- full recovery of dynamic vestibular function after superior
ducted sound. Brain Res Bull. 2012;89(1-2):16-21. vestibular neuritis. Laryngoscope. 2011;121(11):2496-2500.
75. Curthoys IS. A critical review of the neurophysiological 93. Tribukait A, Bergenius J, et al. The subjective visual hori-
evidence underlying clinical vestibular testing using zontal for different body tilts in the roll plane: characteri-
sound, vibration and galvanic stimuli. Clin Neurophysiol. zation of normal subjects. Brain Res Bull. 1996;40(5-6):
2010;121(2):132-144. 375-381; discussion 381-383.
76. Curthoys IS, Vulovic V, et al. The basis for using bone- 94. Fetter M, Zee DS, et al. Effect of lack of vision and of
conducted vibration or air-conducted sound to test occipital lobectomy upon recovery from unilateral
otolithic function. Ann N Y Acad Sci. 2011;1233:231-241. labyrinthectomy in rhesus monkey. J Neurophysiol. 1988;
77. Curthoys IS. The interpretation of clinical tests of peripheral 59(2):394-407.
vestibular function. Laryngoscope. 2012;122(6):1342-1352. 95. Sadeghi SG, Minor LB, et al. Neural correlates of motor
78. Iwasaki S, Smulders YE, et al. Ocular vestibular evoked learning in the vestibulo-ocular reflex: dynamic regulation
myogenic potentials to bone conducted vibration of the of multimodal integration in the macaque vestibular sys-
midline forehead at Fz in healthy subjects. Clinical Neuro- tem. J Neurosci. 2010;30(30):10158-10168.
physiology. 2008;119(9):2135-2147. 96. Sadeghi SG, Minor LB, et al. Multimodal integration after
79. Iwasaki S, McGarvie LA, et al. Head taps evoke a crossed unilateral labyrinthine lesion: single vestibular nuclei neu-
vestibulo-ocular reflex. Neurology. 2007;68(15):1227-1229. ron responses and implications for postural compensation.
80. Iwasaki S, Murofushi T, et al. Ocular vestibular evoked J Neurophysiol. 2011;105(2):661-673.
myogenic potentials to bone-conducted vibration in vestibu- 97. Yakushin SB, Kolesnikova OV, et al. Complementary gain
lar schwannomas. Otol Neurotol. 2010;31(1):147-152. modifications of the cervico-ocular (COR) and angular
81. Manzari L, Burgess AM, et al. Effect of bone-conducted vestibulo-ocular (aVOR) reflexes after canal plugging.
vibration of the midline forehead (Fz) in unilateral Exp Brain Res. 2011;210(3-4):549-560.
vestibular loss (uVL). Evidence for a new indicator of 98. Halmagyi GM, Curthoys IS, et al. Unilateral vestibular
unilateral otolithic function. Acta Otorhinolaryngol Ital. neurectomy in man causes a severe permanent horizontal
2010;30(4):175. vestibulo-ocular reflex deficit in response to
3970_Ch08_121-150 25/06/14 11:33 AM Page 148
high-acceleration ampullofugal stimulation. Acta Oto- 117. Smith PF, Darlington CL, et al. Vestibular compensation
laryngol Suppl. 1991;481:411-414. without brainstem commissures in the guinea pig. Neu-
99. Berthoz A. Cooperation and substitution between the rosci Lett. 1986;65(2):209-213.
saccadic system and reflexes of vestibular origin - should 118. Lacour M, Xerri C, et al. Compensation of postural reac-
we revise the notion of reflex. Revue Neurologique. tions to fall in the vestibular neurectomized monkey. Role
1989;145(8-9):513-526. of the remaining labyrinthine afferences. Exp Brain Res.
100. Horn ER. “Critical periods” in vestibular development 1979;37(3):563-580.
or adaptation of gravity sensory systems to altered 119. Igarashi M, Guitierrez O. Analysis of righting reflex in
gravitational conditions? Arch Ital Biol. 2004;142(3): cats with unilateral and bilateral labyrinthectomy. ORL J
155-174. Otorhinolaryngol Relat Spec. 1983;45(5):279-289.
101. Newlands SD, Dara S, et al. Relationship of static and 120. Xerri C, Zennou Y. Sensory, functional and behavioural
dynamic mechanisms in vestibuloocular reflex compen- substitution processes in vestibular compensation. In: La-
sation. Laryngoscope. 2005;115:191-204. cour M, Toupet M, Denise P, Christen Y, eds. Vestibular
102. Beraneck M, McKee JL, et al. Asymmetric recovery Compensation; Facts, Theories and Clinical Perspec-
in cerebellar-deficient mice following unilateral tives. Paris: Elsevier;1989:35-58.
labyrinthectomy. J Neurophysiol. 2008;100(2): 121. Zennou-Azogui Y, Xerri C, et al. Visual sensory substitu-
945-958. tion in vestibular compensation: neuronal substrates in
103. Black FO, Wade SW, et al. What is the minimal vestibu- the alert cat. Exp Brain Res. 1994;98(3):457-473.
lar function required for compensation? Am J Otol. 1996; 122. Zennou-Azogui Y, Xerri C, et al. Visual experience dur-
17(8817017):401-409. ing a sensitive period plays a critical role in vestibular
104. Jensen DW. Reflex control of acute postural asymmetry compensation: neuronal substrates within Deiters’
and compensatory symmetry after a unilateral vestibular nucleus in the alert cat. Restor Neurol Neurosci. 1995;
lesion. Neuroscience. 1979;4(8):1059-1073. 7(4):235-246.
105. Jensen DW. Vestibular compensation: tonic spinal influ- 123. Zennou-Azogui Y, Xerri C, et al. Vestibular compensa-
ence upon spontaneous descending vestibular nuclear ac- tion: role of visual motion cues in the recovery of
tivity. Neuroscience. 1979;4(8):1075-1084. posturo-kinetic functions in the cat. Behav Brain Res.
106. Reber A, Courjon J-H, et al. Vestibular decompensation 1996; 74(1-2):65-77.
in labyrinthectomized rats placed in weightlessness 124. Igarashi M. Physical exercise and the acceleration of vestibu-
during parabolic flight. Neurosci Lett. 2003;344(2): lar compensation. In: Lacour M, Tighilet B, Denise P, Chris-
122-126. ten Y, eds. Vestibular Compensation: Facts, Theories and
107. Goto F, Straka H, et al. Gradual and reversible central Clinical Perspectives. Paris: Elsevier; 1989:131-144.
vestibular reorganization in frog after selective labyrinthine 125. Pettorossi VE, Petrosini L. Tonic cervical influences on
nerve branch lesions. Exp Brain Res. 2002; 147(3): eye nystagmus following hemilabyrinthectomy: immedi-
374-386. ate and plastic effects. Brain Res. 1984;324(1):11-19.
108. Luxon LM, Furman JM, et al., eds. Textbook of Audiolog- 126. Flohr H. Concepts of vestibular compensation. In: Flohr,
ical Medicine: Clinical Aspects of Hearing and Balance. Precht W, eds. Lesion-induced Neuronal Plasticity in
London: Martin Dunitz; 2003. Sensorimotor Systems. Berlin: Springer-Verlag;
109. Bowman A. Psychological and Visual-Perceptual Ex- 1981:153-172.
planations of Poor Compensation Following Unilat- 127. Maioli C, Precht W. On the role of vestibulo-ocular reflex
eral Vestibular Loss. Sydney: University of Sydney; plasticity in recovery after unilateral peripheral vestibular
2005. lesions. Exp Brain Res. 1985;59(1):267-272.
110. Smith PF, Darlington CL. Neurochemical mechanisms of 128. Gonshor A, Jones GM. Short-term adaptive changes in
recovery from peripheral vestibular lesions (vestibular the human vestibulo-ocular reflex arc.J Physiol.1976;
compensation). Brain Res Brain Res Rev. 1991;16(2): 256(2):361-379.
117-133. 129. Gonshor A, Jones GM. Extreme vestibulo-ocular adapta-
111. Rascol O, Hain TC, et al. Antivertigo medications and tion induced by prolonged optical reversal of vision.
drug-induced vertigo. A pharmacological review. Drugs. J Physiol. 1976;256(2):381-414.
1995;50(5):777-791. 130. Cawthorne T. Vestibular Injuries. Proc R Soc Med. 1946;
112. Lacour M, Sterkers O. Histamine and betahistine in the 39(5):270-273.
treatment of vertigo: elucidation of mechanisms of ac- 131. Cooksey FS. Rehabilitation in vestibular injuries. Proc R
tion. CNS Drugs.2001;15(11):853-870. Soc Med. 1946;39(5):273-278.
113. Hain TC, Uddin M. Pharmacological treatment of ver- 132. Telian SA, Shepard NT. Update on vestibular rehabilitation
tigo. CNS Drugs 17(2):85-100. therapy. Otolaryngol Clin North Am. 1996;29(2):359-371.
114. Curthoys IS, Smith PF, et al. Postural compensation in 133. Strupp M, Arbusow V, et al. Vestibular exercises improve
the guinea pig following unilateral labyrinthectomy. Prog central vestibulospinal compensation after vestibular neu-
Brain Res. 1988;76:375-384. ritis. Neurology. 1998;51(3):838-844.
115. Tighilet B, Brezun JM, et al. New neurons in the vestibu- 134. Strupp M, Arbusow V, et al. Balance training improves
lar nuclei complex after unilateral vestibular neurectomy vestibulospinal compensation after acute one-sided
in the adult cat. Eur J Neurosci. 2007;25(1):47-58. labyrinthian failure. Physikalische Medizin Rehabilita-
116. Putkonen PT, Courjon JH, et al. Compensation of pos- tionsmedizin Kurortmedizin. 2000;10:217-226.
tural effects of hemilabyrinthectomy in the cat. A sen- 135. Strupp M, Arbusow V, et al. Exercise and drug therapy
sory substitution process? Exp Brain Res. 1977; alter recovery from labyrinth lesion in humans. Ann N Y
28(3-4):249-257. Acad Sci. 2001;942:79-94.
3970_Ch08_121-150 25/06/14 11:33 AM Page 149
136. Della Santina CC, Cremer PD, et al. Comparison of head 153. Him A, Dutia MB. Intrinsic excitability changes in
thrust test with head autorotation test reveals that the vestibular nucleus neurons after unilateral deafferenta-
vestibulo-ocular reflex is enhanced during voluntary head tion. Brain Res. 2001;908(1):58-66.
movements. Arch Otolaryngol Head Neck Surg. 2002; 154. Darlington CL, Dutia MB, et al. The contribution of the
128(9):1044-1054. intrinsic excitability of vestibular nucleus neurons to re-
137. Goldberg JM, Fernandez C. The vestibular system. covery from vestibular damage. Eur J Neurosci. 2002;
Sensory Processes. I. Darian-Smith. Bethesda, MD, 15(11):1719-1727.
American Physiological Society.1983;3:977-1022. 155. Ris L, Capron B, et al. Labyrinthectomy changes T-type
138. Smith PF, Curthoys IS. Mechanisms of recovery follow- calcium channels in vestibular neurones of the guinea
ing unilateral labyrinthectomy: a review. Brain Res Brain pig. Neuroreport. 2003;14(12):1585-1589.
Res Rev. 1989;14(2):155-180. 156. Dutia MB, Johnston AR, et al. Tonic activity of rat me-
139. Cirelli C, Pompeiano M, et al. c-fos Expression in the rat dial vestibular nucleus neurones in vitro and its inhibition
brain after unilateral labyrinthectomy and its relation to by GABA. Exp Brain Res. 1992;88(3):466-472.
the uncompensated and compensated stages. Neuro- 157. Magnusson AK, Lindstrom S, et al. GABA(B) receptors
science. 1996;70(2):515-546. contribute to vestibular compensation after unilateral
140. Goldberg JM. Afferent diversity and the organization of labyrinthectomy in pigmented rats. Exp Brain Res. 2000;
central vestibular pathways. Exp Brain Res. 2000; 134(1):32-41.
130(3):277-297. 158. Yamanaka T, Him A, et al. Rapid compensatory changes
141. Highstein SM, Fay RR, et al., eds. The Vestibular System. in GABA receptor efficacy in rat vestibular neurones
New York: Springer-Verlag; 2004. after unilateral labyrinthectomy. J Physiol. 2000;523
142. Smith PF, Curthoys IS. Neuronal activity in the ipsilateral (Pt 2):413-424.
medial vestibular nucleus of the guinea pig following 159. Him A, Johnston AR, et al. Tonic activity and GABA
unilateral labyrinthectomy. Brain Res. 1988; 444(2): responsiveness of medial vestibular nucleus neurons in
308-319. aged rats. Neuroreport. 2001;12(18):3965-3968.
143. Sadeghi SG, Minor LB, et al. Response of vestibular- 160. Johnston AR, Him A, et al. Differential regulation of
nerve afferents to active and passive rotations under nor- GABA(A) and GABA(B) receptors during vestibular
mal conditions and after unilateral labyrinthectomy. compensation. Neuroreport. 2001;12(3):597-600.
J Neurophysiol. 2007;97(2):1503-1514. 161. Tighilet B, Lacour M. Gamma amino butyric acid
144. Precht W, Shimazu H, et al. A mechanism of central com- (GABA) immunoreactivity in the vestibular nuclei of
pensation of vestibular function following hemilabyrinthec- normal and unilateral vestibular neurectomized cats.
tomy. J Neurophysiol. 1966;29(6):996-1010. Eur J Neurosci. 2001;13(12):2255-2267.
145. Markham CH, Yagi T, et al. The contribution of the con- 162. Gliddon CM, Darlington CL, et al. GABAergic systems
tralateral labyrinth to second order vestibular neuronal in the vestibular nucleus and their contribution to vestibu-
activity in the cat. Brain Res. 1977;138(1): 99-109. lar compensation. Prog Neurobiol. 2005;75(1):53-81.
146. Hamann KF, Lannou J. Dynamic characteristics of 163. Shao M, Hirsch JC, et al. Plasticity of spontaneous
vestibular nuclear neurons responses to vestibular and op- excitatory and inhibitory synaptic activity in morpho
tokinetic stimulation during vestibular compensation in logically defined vestibular nuclei neurons during early
the rat. Acta Otolaryngol Suppl. 1987;445:1-19. vestibular compensation. J Neurophysiol. 2012;107(1):
147. Newlands SD, Perachio AA. Compensation of horizontal 29-41.
canal related activity in the medial vestibular nucleus fol- 164. Shao M, Reddaway R, et al. Presynaptic GABA(B) re-
lowing unilateral labyrinth ablation in the decerebrate ceptors decrease neurotransmitter release in vestibular
gerbil. I. Type I neurons. Exp Brain Res. 1990;82(2): nuclei neurons during vestibular compensation. Neuro-
359-372. science. 2012;223:333-354.
148. Newlands SD, Perachio AA. Compensation of horizontal 165. de Waele C, Campos Torres A, et al. Evidence for reac-
canal related activity in the medial vestibular nucleus fol- tive astrocytes in rat vestibular and cochlear nuclei fol-
lowing unilateral labyrinth ablation in the decerebrate lowing unilateral inner ear lesion. Eur J Neurosci. 1996;
gerbil. II. Type II neurons. Exp Brain Res. 1990; 8(9):2006-2018.
82(2):373-383. 166. Campos Torres A, Vidal PP, et al. Evidence for a mi-
149. Ris L, de Waele C, et al. Neuronal activity in the ipsilat- croglial reaction within the vestibular and cochlear nuclei
eral vestibular nucleus following unilateral labyrinthec- following inner ear lesion in the rat. Neuroscience. 1999;
tomy in the alert guinea pig. J Neurophysiol. 1995;74(5): 92(4):1475-1490.
2087-2099. 167. Gacek RR, Lyon MJ, et al. Ultrastructural changes in
150. Ris L, Capron B, et al. Dissociations between behav- vestibulo-ocular neurons following vestibular neurectomy
ioural recovery and restoration of vestibular activity in in the cat. Ann Otol Rhinol Laryngol. 1988;97(1): 42-51.
the unilabyrinthectomized guinea-pig. J Physiol. 1997; 168. Gacek RR, Lyon MJ, et al. Morphologic correlates of
500( Pt 2):509-522. vestibular compensation in the cat. Acta Otolaryngol
151. Sadeghi SG, Minor LB, et al. Response of vestibular- Suppl. 1989;462:1-16.
nerve afferents to active and passive rotations under nor- 169. Gacek RR, Lyon MJ, et al. Ultrastructural changes in
mal conditions and after unilateral labyrinthectomy. contralateral vestibulo-ocular neurons following vestibu-
J Neurophysiol. 2007;97(2):1503-1514. lar neurectomy in the cat. Acta Otolaryngol Suppl. 1991;
152. Bergquist F, Ludwig M, et al. Role of the commissural 477:1-14.
inhibitory system in vestibular compensation in the rat. 170. Gacek RR, Schoonmaker JE. Morphologic changes in the
J Physiol. 2008;586(Pt 18):4441-4452. vestibular nerves and nuclei after labyrinthectomy in the
3970_Ch08_121-150 25/06/14 11:33 AM Page 150
cat: a case for the neurotrophin hypothesis in vestibular 184. Newlands SD, Perachio AA. Effects of commissurotomy
compensation. Acta Otolaryngol. 1997;117(2):244-249. on vestibular compensation in the gerbil. Society for Neu-
171. Aldrich EM, Peusner KD. Vestibular compensation after roscience Abstracts. 1986;12:254.
ganglionectomy: ultrastructural study of the tangential 185. Kitahara T, Takeda N, et al. Molecular mechanisms of
vestibular nucleus and behavioral study of the hatchling vestibular compensation in the central vestibular
chick. J Neurosci Res. 2002;67(1):122-138. system—review. Acta Otolaryngol Suppl. 1998;539:
172. Campos-Torres A, Touret M, et al. The differential re- 19-27.
sponse of astrocytes within the vestibular and cochlear 186. Kitahara T, Fukushima M, et al. Effects of pre-
nuclei following unilateral labyrinthectomy or vestibular flocculectomy on Fos expression and NMDA receptor-
afferent activity blockade by transtympanic tetrodotoxin mediated neural circuits in the central vestibular system
injection in the rat. Neuroscience. 2005;130(4):853-865. after unilateral labyrinthectomy. Acta Otolaryngol.
173. Lacour M, Dutheil S, et al. Tell me your vestibular 2000;120(7): 866-871.
deficit, and I’ll tell you how you’ll compensate. Ann N Y 187. Kitahara T, Takeda N, et al. Role of the flocculus in the de-
Acad Sci. 2009;1164:268-278. velopment of vestibular compensation: immunohistochemi-
174. Beraneck M, Hachemaoui M, et al. Long-term plasticity cal studies with retrograde tracing and flocculectomy using
of ipsilesional medial vestibular nucleus neurons after Fos expression as a marker in the rat brainstem. Neuro-
unilateral labyrinthectomy. J Neurophysiol. 2003;90(1): science. 1997;76(2):571-580.
184-203. 188. Kitahara T, Fukushima M, et al. Role of cholinergic
175. Beraneck M, Idoux E, et al. Unilateral labyrinthectomy mossy fibers in vestibular nuclei in the development of
modifies the membrane properties of contralesional vestibular compensation. Acta Otolaryngol Suppl. 2001;
vestibular neurons. J Neurophysiol. 2004;92(3): 545:101-104.
1668-1684. 189. Johnston AR, Seckl JR, et al. Role of the flocculus in
176. Nelson AB, Krispel CM, et al. Long-lasting increases in mediating vestibular nucleus neuron plasticity during
intrinsic excitability triggered by inhibition. Neuron. vestibular compensation in the rat. J Physiol. 2002;545
2003;40(3):609-620. (Pt 3):903-911.
177. Pettorossi VE, Dutia M, et al. Long-term potentiation and 190. Furman JM, Balaban CD, et al. Vestibular compensation
depression after unilateral labyrinthectomy in the medial in a patient with a cerebellar infarction. Neurology. 1997;
vestibular nucleus of rats. Acta Otolaryngol. 2003; 48(4):916-920.
123(2):182-186. 191. Anastasio TJ. Simulating vestibular compensation using
178. Xerri C, Gianni S, et al. Central compensation of vestibu- recurrent back-propagation. Biol Cybern. 1992;66(5):
lar deficits. I. Response characteristics of lateral vestibu- 389-397.
lar neurons to roll tilt after ipsilateral labyrinth 192. Cartwright AD, Curthoys IS. A neural network simula-
deafferentation. J Neurophysiol. 1983;50(2):428-448. tion of the vestibular system: implications on the role of
179. Lacour M, Manzoni D, et al. Central compensation of intervestibular nuclear coupling during vestibular com-
vestibular deficits. III. Response characteristics of lateral pensation. Biol Cybern. 1996;75(6):485-493.
vestibular neurons to roll tilt after contralateral labyrinth 193. Cartwright AD, Curthoys IS, et al. Testable predictions
deafferentation. J Neurophysiol. 1985;54(4):988-1005. from realistic neural network simulations of vestibular
180. Aleisa M, Zeitouni AG, et al. Vestibular compensation compensation: integrating the behavioural and physiolog-
after unilateral labyrinthectomy: Normal versus cerebellar ical data. Biol Cybern. 1999;81(1):73-87.
dysfunctional mice. J Otolaryngol. 2007;36(6):315-321. 194. Graham BP, Dutia MB. Cellular basis of vestibular com-
181. Courjon JH, Flandrin JM, et al. The role of the flocculus pensation: analysis and modelling of the role of the com-
in vestibular compensation after hemilabyrinthectomy. missural inhibitory system. Exp Brain Res. 2001;
Brain Res. 1982;239(1):251-257. 137(3-4):387-396.
182. Haddad GM, Friendlich AR, et al. Compensation of 195. Cartwright AD, Gilchrist DPD, et al. A realistic neural-
nystagmus after VIIIth nerve lesions in vestibulo- network simulation of both slow and quick phase compo-
cerebellectomized cats. Brain Res. 1977;135(1):192-196. nents of the guinea pig VOR. Exp Brain Res. 2003;
183. Smith PF, Darlington CL, et al. The effect of visual depri- 149(3):299-311.
vation on vestibular compensation in the guinea pig.
Brain Res. 1986;364(1):195-198.
3970_Ch09_151-158 25/06/14 11:34 AM Page 151
CHAPTER 9
Compensatory
Strategies for
Vestibulo-ocular
Hypofunction
Michael C. Schubert, PT, PhD
151
3970_Ch09_151-158 25/06/14 11:34 AM Page 152
120
80
40
Velocity (d/s)
−40
−80
−160
−200
120
Normal VOR
80
40
Velocity (d/s)
−40
−80
−160
−200
−240
B Time (msec)
Figure 9.1 Compensatory (preprogrammed) saccades vs. normal vestibular-ocular reflex
(VOR) in a person with unilateral vestibular hypofunction (UVH). Dark traces reflect head ve-
locity, and lighter traces eye velocity. The vertical line marks the onset of the head rotation.
(A) The slow eye velocity is deficient in relation to the head velocity (low VOR gain), and com-
pensatory saccades (CS) are recruited. Note that the direction of the CS is the same as that of
the slow velocity. (B) The slow eye velocity is similar to the head velocity for a normal VOR gain.
described a type of saccade that corrected for 28% to 59% the gaze position error was reduced when compensatory sac-
of the slow-component error associated with ipsilesional cades were recruited as part of the gaze-stabilizing strategy.20
head thrusts. Later, Bloomberg and colleagues19 reported a The otolith-mediated translational VOR (tVOR) has
similar synergistic relationship between slo w-component also been shown to benefit from the symbiotic relationship
vestibular and saccadic eye movements for the purpose of between VOR and saccades. Shelhamer and associates 21
improving gaze stability. More recently, we have shown that adaptively increased the gain of the tV OR in human
3970_Ch09_151-158 25/06/14 11:34 AM Page 153
subjects (with normal v estibular function) by e xposing head rotation in the place of the def icient vestibular sys-
them to lateral sinusoidal translations and tar get motion tem. The difference, however, is that the eye rotation from
for 20 minutes. These researchers showed that saccades the COR is generated from receptors in the joints and lig-
occurred in the direction of the slow eye movements and aments of the upper cervical v ertebrae.27 For eye move-
accounted for 32% of the tV OR after adaptation. On the ments to be discerned as being generated from the cervical
basis of these pre vious studies, saccades not only ha ve spine and not the vestibular system, the head must remain
been shown to occur in the direction of the vestibular slow still. The COR is quantified from the ratio between e ye
component but also appear to require little time for their and trunk velocities (absolute value of peak eye velocity ÷
recruitment and utility in reducing gaze instability. peak trunk velocity). As a compensatory mechanism for
vestibular loss, the COR should mo ve the eyes in the di-
Saccadic Modifications rection of the moving trunk. When the trunk is rotated to
the left under a still head, the relative head position (static)
A variety of beha vioral modifications to the saccadic
is the same as if the head had rotated to the right. A left-
oculomotor system have been reported for patients with
ward trunk rotation (relative rightward static head posi-
vestibular hypofunction when the experimental paradigms
tion) should therefore elicit a leftw ard eye motion.
have involved a head rotation (a condition that normally
Although the COR is well described in animal models, its
requires a VOR). Three are described here.
presence in humans is controversial.
Kasai and Zee16 reported that when patients with bi-
In 1906, Barany first demonstrated eye motion in ras-
lateral vestibular deficits were asked to shift their gaze to a
cally rabbits when the trunk w as rotated beneath a still
target with the eyes and head, they were found to generate
head.28 In later studies, various researchers demonstrated
an initial saccade to the target of decreased amplitude (un-
that sectioning the dorsal roots from C1 to C4 or injecting
dershoot). The researchers hypothesized that the brain in-
anesthetic into the cervical joints of rabbits produced nys-
tentionally undershoots the target, anticipating the inability
tagmus.29,30 Recording from cat abducens motor neurons,
of the VOR to keep the eyes still during the head rotation.
Hikosaka and Maeda 27 showed in 1973 that stimulating
Through the use of a saccade of insufficient amplitude, the
the second or third cervical dorsal roots caused facilitation
eyes then “drift” to the target with the head motion.
of the ipsilateral abducens motor neurons and increased
Several studies have established that during an ipsile-
firing rate from the contralateral vestibular nucleus. Addi-
sional unpredictable yaw head rotation away from a cen-
tionally, contralateral abducens motor neurons were inhib-
trally positioned visual target, a saccade is generated in the
ited. Stimulation below the fourth cervical joints did not
opposite direction to the head rotation, back to ward the
generate the same f acilitation and inhibition responses.
target.14,18-19,21-24 Most of the investigators agree that these
These researchers demonstrated synapses between second
types of compensatory saccades:
and third cervical vertebral joints and abducens oculomo-
• Are recruited for the purpose of assisting gaze. tor neurons and vestibular nuclei. As a form of control, the
• Improve gaze stability, although they do not com- second or third cervical joints were anesthetized with
pletely match the velocity of head motion. lidocaine injection, after which the n ystagmus could not
• Are inversely correlated with VOR gain.14,18,19,24,25 be elicited.
• May occur more than once during a single head A later study by Gdowski and McCrea,31 in the squir-
rotation.14,21,23-25 rel monkey, yielded further evidence of the influence of
neck proprioceptive information on the vestibular nuclei.
The studies also demonstrate a great deal of variabil-
The investigators compared f iring rates (sensiti vity)
ity in recruitment of CS. Some patients appear to use
recorded from secondary afferents of the horizontal semi-
CS only for high-acceleration or lar ge-amplitude head
circular canals while the primate’s trunk was rotated be-
motions.14,16,19,23-26
neath a still head (passive neck rotation) with those during
It has also been shown that the latency to generate a
whole-body rotation (each rotation parameter was measured
CS during an ipsilesional unpredictable yaw head rotation
at 0.5 Hz, 40 deg/sec and at 2.3 Hz, 20 de g/sec). They re-
away from a centrally located visual target is much shorter
ported the gain of the COR was similar regardless of fre-
than visually guided saccade latencies (70 to 130 msec
quency of the test (0.4 ± 0.04 for 0.5 Hz and 0.33 ± 0.05
versus 200 msec, respectively).14
for 2.3 Hz). This study showed that neurons in the vestibu-
lar nuclei are sensitive to neck rotation in primates.
Cervico-ocular Reflex Similar COR gain v alues were recently reported
The COR parallels the VOR and is thought to contribute a in rhesus monkey.32 Yakushin et al 32 studied COR and
slow-component eye rotation in the direction opposite to VOR gain recovery across frequencies of motion ranging
3970_Ch09_151-158 25/06/14 11:34 AM Page 154
from 0.02 to 6 Hz in monk eys with all six semicircular Pregaze Stabilization Exercises
canals plugged. Before surgery, the measured COR gains 30
Chair velocity trace
were negligible and only observ ed at those frequencies Right Mean eye velocity
Mean head velocity
below 1 Hz. After surgery, the COR gains were signif i-
cantly increased (~0.15) when measured at frequencies 10
below 3 Hz. Over the next 3 months, the COR gains in-
Mean head velocity = 0.23 d/s
creased to ~0.4. When the COR and VOR were summed,
the compensated response gains were ~0.4 to 0.8. 0
Velocity (deg/sec)
response (~0.25 gain).33 −30
10
Subjects with Vestibular Hypofunction Mean head velocity = 0.6 d/s
function was diagnosed from caloric irrigation. 34 The in- B Time (sec)
vestigators reported that the COR gain decreased from Figure 9.2 Cervico-ocular reflex (COR) in a patient with
0.51 to 0.17 as the central vestibular system demonstrated unilateral vestibular hypofunction (UVH). The chair, eye,
recovery of the VOR gain (both VOR and COR measured and head velocities are plotted. The subject’s head was
at 0.2 Hz, 40 deg/sec). This finding implies that the COR fixed in space to prevent head motion. (A) The COR gain
(eye velocity/chair velocity) was at 0.1 before the patient
was a compensatory mechanism transiently useful until started a gaze stabilization exercise program. (B) After the
the gain from the VOR recovered. program, the COR gain had increased to 0.32. Note the
Evidence for the existence of a COR in a person with very low head velocity, demonstrating that this eye velocity
UVH was recently reported in an 81-year-old woman.38 The is not from the vestibular system.
authors described a COR gain of 0.1 ± 0.04 during 0.3-Hz
trunk rotation. In this patient, the COR gain was increased
to 0.32 ± 0.13 after 5 weeks of gaze stabilization exercises toward the defect than during unpredictable head mo ve-
(Fig. 9.2). Oddly, the direction of the COR w as not com- ments toward the defect in indi viduals with v estibular
pensatory. This evidence suggests that the COR can be po- hypofunction.15,17,39-43 Second, visual acuity during head
tentiated, although its functional relevance is still uncertain. motion (dynamic visual acuity [D VA]) is better during
predictable head rotations than during unpredictable head
rotations.12,44 Enhancement of VOR gain (gaze stability)
Effects of Prediction and DVA with predictable head mo vement is believed to
When individuals with vestibular hypofunction can predict be caused by mechanisms such as central preprogramming
head movement, gaze stability improves. This process has and efference copy of the motor command.
been shown in two ways. First, VOR gain (eye velocity ÷ We have found e vidence that indi viduals with
head velocity) is larger during predictable head movements vestibular hypofunction can generate a high-velocity slow
3970_Ch09_151-158 25/06/14 11:34 AM Page 155
phase (HVSP) for ipsilesional predictable head rotations (streptomycin injection) allowed to make active head rota-
(Fig. 9.3A).15 These unique e ye rotations occur with tions, the mean anticipatory slow-phase eye motion latency
velocities greater than the v elocity limit imposed by was 0.1 +/ 2.5 msec. This latency is much shorter than the
inhibitory cutoff (at 100 de g/sec). Additionally, we have latency observed in either a healthy guinea pig (~7 msec)
evidence that the HVSPs occasionally occur before the onset or one with a unilateral vestibular loss (~ ≥15 msec).
of the head rotation and, therefore, are not a v estibular- Recording from neurons in the medial and lateral
generated eye rotation (Fig. 9.3B). vestibular nuclei in the rhesus monkey after bilateral vestibu-
Recently, new evidence has been reported suggesting lar labyrinthectomy, Sadeghi et al confirmed that neuronal
the brain can generate a very short-latency eye rotation.45 sensitivity to active head rotation (compared with passi ve
In guinea pig with bilateral loss of v estibular function head rotation) was increased, verifying the role that efference
copy has as a substitute for absent vestibular information.33
Velocity Plot
Enhanced Smooth Pursuit
Head Velocity
100
93 deg/sec Gaze Velocity
Eye Velocity
Smooth pursuit eye movements are used to track a moving
Right visual target, typically without head rotation. Smooth pur-
50 Onset of suit gain is the ratio of e ye velocity to target velocity (eye
Head Thrust
velocity ÷ tar get velocity). Like the v estibular system,
Velocity (deg/sec)
−1000
Optokinetic Reflex
Left
The optokinetic reflex (OKR) is generated from central
−1500
oculomotor pathways and involves a combined saccade
and smooth pursuit e ye rotation. It is a normal response
B Time (msec)
0 100 200
that typically occurs when an individual follows a moving
Figure 9.3 Velocity and acceleration plots of a high- object that takes up at least 60% of his or her visual field.
velocity slow phase during a predictable head thrust in There is recent evidence that the OKR might be modif i-
a subject with bilateral vestibular hypofunction (BVH). able and able to contrib ute to gaze stability during head
(A) The head is thrust to the left at 124 deg/sec, above rotation. Tilted mice lack otoconia because of a genetic
the level of inhibitory cutoff, yet the subject generates a mutation. Interestingly, these mice have higher OKR gain
slow eye velocity of 93 deg/sec, for a gain of 0.74. (B) The
acceleration plot reveals that the slow eye velocity precedes compared with control mice. The authors presumed this
the head rotation, demonstrating that this type of eye is caused by an adaptation strategy between the otolith and
response is not generated from the vestibular system. visual systems to improve gaze stability.50
3970_Ch09_151-158 25/06/14 11:34 AM Page 156
38. Schubert MC, Das V, Tusa RJ, Herdman SJ. Cervico-ocular 45. Shanidze N, Kim AH, Loewenstein S, Raphael Y, King
reflex in normal subjects and patients with unilateral WM. Eye-head coordination in the guinea pig II. Responses
vestibular hypofunction. Otol Neurotol. 2004;25:65-71. to self-generated (voluntary) head movements. Exp Brain
39. Collewijn H, Martins AJ, Steinman RM. Compensatory eye Res. 2010 Sep;205(4):445-454.
movements during active and passive head movements: fast 46. Fukushima K, Tanaka M, Suzuki Y, et al. Adaptive changes
adaptations to changes in visual magnification. J Physiol. in human smooth pursuit eye movement. Neuroscience
1983;340:259-286. Res. 1996;25:391-398.
40. Demer JL, Oas JG, Baloh RW. Visual vestibular interac- 47. Scheurer W, Ditterich J, Straube A. Adaptation of
tion in humans during active and passive vertical had initial smooth pursuit eye velocity in humans. Neuro-
movement. J Vestib Res. 1993;3:101-114. ophthalmology. 1999;21:223-231.
41. Hoshowsky B, Tomlinson D, Nedzelski J. The horizontal 48. Meyer CH, Lasker AG, Robinson DA. The upper limit
vestibulo-ocular reflex gain during active and passive high of human smooth pursuit velocity. Vision Res. 1985;25;
frequency head movements Laryngoscope. 1994;104: 561-563.
140-145. 49. Bockisch CJ, Straumann D, Hess K, Haslwanter T.
42. Jell RM, Stockwell CW, Turnipseed GT, et al. The influ- Enhanced smooth pursuit eye movements in patients
ence of active versus passive head oscillation, and mental with bilateral vestibular deficits. Neuroreport. 2004;15:
set on the human vestibulo-ocular reflex. Aviat Space 2617-2620.
Environ Med. 1988;59:1061-1065. 50. Andreescu CE, De Ruiter MM, De Zeeuw CI, De Jeu MT.
43. Halmagyi GM, Black RA, Thurtell MJ, Curthoys IS. The Otolith deprivation induces optokinetic compensation.
human horizontal vestibulo-ocular reflex in response to J Neurophysiol. Nov 2005;94(5):3487-3496. Epub Aug 3
active and passive head impulses after unilateral vestibular 2005.
deafferentation. Ann N Y Acad Sci. 2003;1004:325-336.
44. Tian JR, Shubayev I, Demer JL. Dynamic visual acuity
during passive and self-generated transient head rotation
in normal and unilaterally vestibulopathic humans. Exp
Brain Res. 2002;142:486-495.
3970_Ch09_151-158 25/06/14 11:34 AM Page 158
3970_Ch10_159-177 25/06/14 11:35 AM Page 159
THREE
Medical
Assessment
and Vestibular
Function Tests
3970_Ch10_159-177 25/06/14 11:36 AM Page 160
CHAPTER 10
History
and Clinical
Examination
Ronald J. Tusa, MD, PhD
Management of the dizzy patient depends on history, bed- Elements that Help with the Diagnosis
side clinical e xamination, and laboratory testing. This
chapter covers the first two portions of this evaluation. An The tempo, symptoms, and circumstances of the patient’s
accurate history is needed to determine the onset of the primary complaints are the three key items in the history
problem, description of the symptoms, and, most impor - (Table 10-1).
tant, how the symptoms affect the individual’s lifestyle.
This last element is crucial to obtain because some indi- Tempo
viduals may have bedside clinical and laboratory evidence The objective of establishing tempo is to determine
of chronic vestibular loss on one side but may be primarily whether the patient has an acute attack of dizziness (within
affected by some other cause of dizziness, such as mi- 3 days or less), chronic dizziness (more than 3 days), or
graine or anxiety. The bedside clinical examination can be spells of dizziness. To do so, the clinician must be sure the
used to distinguish peripheral from central vestibular prob- patient describes the first onset of the symptoms. Did it
lems, the extent of loss, and how acute the problem may happen suddenly, or did it de velop very slowly? Was it
be. Laboratory testing (see Chapter 11) confirms the pro- provoked by anything, or did it occur spontaneously? Did
visional diagnosis that was based on history and clinical the patient have a cold or some other illness around that
findings, quantifies the degree of loss, provides evidence time? If the patient suffers from spells, the clinician should
of central compensation, and shows evidence of an aphys- try to determine the average duration of the spells in sec-
iological component. onds, minutes, or hours. It is important to have the patient
describe in detail the first spell, the most severe spell, or
the last spell that he or she can clearly recall.
History
The history is by far the most important part of the eval- Symptoms
uation. Unfortunately, taking a good history from the start What the patient means by “dizziness” should be expanded
can be e xtremely tedious, because the patient’ s com- on. Dizziness is an imprecise term used to describe a vari-
plaints are often v ague and also can be complicated by ety of symptoms, each of which has a different pathophys-
anxiety-provoked symptoms. For this reason, I divide the iological mechanism and significance (Table 10-2). If the
history into those elements that help with the diagnosis patient cannot describe the symptoms, the clinician should
and those that lead to goals for management, including ask whether the symptom causes problems primarily in the
physical therapy. head or with balance. It is important to determine if the
160
3970_Ch10_159-177 25/06/14 11:36 AM Page 161
Vestibular neuritis Acute dizziness Vertigo, disequilibrium, nausea and Spontaneous, exacerbated by
vomiting, oscillopsia head movements
Wallenberg’s infarct Acute dizziness Vertigo, disequilibrium, nausea and Spontaneous, exacerbated by
vomiting, tilt, lateropulsion, ataxia, head movements
crossed sensory loss, oscillopsia
Bilateral vestibular Chronic dizziness Dizziness, disequilibrium, occasionally Induced by head movements,
deficit or >7 days oscillopsia walking. Exacerbated when
from a unilateral walking in the dark or on
vestibular defect uneven surfaces
Oscillopsia Chronic dizziness Subjective illusion of visual motion Spontaneous with eyes open
Benign paroxysmal Spells: seconds Vertigo, lightheadedness, nausea Positional: lying down, sitting
positional vertigo up or turning over in bed,
bending forward
Panic attack Spells: minutes Dizziness, nausea, diaphoresis, fear, Spontaneous or situation
palpitations, paresthesias
Motion sickness Spells: hours Nausea, diaphoresis, dizziness Movement induced, usually
visuovestibular mismatch
Ménière’s disease Spells: hours Vertigo, disequilibrium, ear fullness Spontaneous, exacerbated by
from hearing loss and tinnitus head movements
3970_Ch10_159-177 25/06/14 11:36 AM Page 162
Symptoms Mechanism
Disequilibrium: imbalance or unsteadiness while Loss of vestibulospinal, proprioception, visual, and/or motor
standing or walking function, joint pain or instability, and psychological factors
Sense of rocking or swaying as if on a ship (mal de Vestibular system adapts to continuous, passive motion and
débarquement) must readapt once environment is stable
Anxiety
Floating, swimming, rocking, and spinning inside Anxiety, depression, and somatoform disorders
of head (psychologically induced)
Vertigo: rotation, linear movement, or tilt Imbalance of tonic neural activity to vestibular cerebral cortex
symptoms have changed since the onset of the problem. If is then referred to as mal de débarquement.1 The reason
the patient has spells, have him or her describe in detail the for prolonged symptoms in these cases is unkno wn. No
initial spell and the last severe spell. consistent abnormalities are found on magnetic resonance
imaging (MRI) or electronystagmography (ENG) testing.1,2
Disequilibrium When symptoms are prolonged, patients are e xtremely
Disequilibrium is imbalance or unsteadiness while standing bothered to the point that their lifestyle is disrupted. Such
or walking. It is caused by a v ariety of factors, including patients are very difficult to manage. They usually feel better
diminished or double vision, loss of v estibular function, when in motion, and I encourage such patients to engage in
defects in proprioception from peripheral neuropathy or physical activity. Small doses of anti-anxiety medication
spinal cord lesions, defects in motor function from central are sometimes helpful (see Chapters 18 and 29 for further
nervous or peripheral nervous system abnormalities, joint discussion).
pain, and psychological factors.
Motion Sickness
Lightheadedness Motion sickness consists of episodic dizziness, tiredness,
Lightheadedness, or presyncope, is usually related to pallor, diaphoresis, salivation, nausea, and, occasionally,
momentarily decreased blood flo w to the brain. P atients vomiting induced by passive locomotion (e.g., riding in a
with anxiety or depression also commonly use the symp- car) or motion in the visual surround while standing still
tom of lightheadedness to describe their dizziness. (e.g., viewing a rotating optokinetic stimulus). Motion
sickness is believed to be caused by a sensory mismatch
Sense of Rocking or Swaying as if on a Ship between visual and v estibular cues.2 Patients with mi-
Patients can find the sensation of rocking or swaying, as graine disorder are particularly prone to motion sickness,
if on a ship, very disturbing. It frequently occurs for a few especially during childhood. Twenty-six percent to 60%
days after a prolonged sea or air voyage and persists for a of patients with migraine have a history of severe motion
few days. Sometimes, it persists for months to years and sickness, compared with 8% to 24% of people in the
3970_Ch10_159-177 25/06/14 11:36 AM Page 163
normal population3,4 (see Chapter 15 for further discussion). is covered. Vertical diplopia is commonly a result of
The cause for this relationship is not clear. Symptoms of in- a skew eye deviation from peripheral or central otolith
creased motion sensitivity are often reproduced when the dysfunction.
patient is exposed to a moving full-field visual target.
Vertigo
Nausea and Vomiting Vertigo is the illusion of movement of the self or the envi-
Nausea with or without vomiting is a result of stimulation ronment caused by sudden imbalance of tonic neural ac-
of the solitary and vagus centers in the medulla. In periph- tivity in the v estibulocortical pathway (labyrinth–eighth
eral vestibular lesions, these symptoms are usually mild to nerve–vestibular nucleus–vestibular thalamus–vestibular
moderate and in proportion to the degree of vertigo: in be- cortex). It is due either to normal head movements (phys-
nign paroxysmal positional vertigo (BPPV), nausea is usu- iological), lesions that cause loss of function (ablation) of
ally mild and vomiting is rare; in labyrinthitis and vestibular vestibular pathways on one side (e.g., vestibular neuritis),
neuritis, nausea is moderate and vomiting may occur during or mechanical problems of the inner ear (e.g., BPPV).The
rapid head movement. Severity of symptoms varies in cen- direction of vertigo depends on the structures in volved.
tral lesions according to the site of lesion. F or pontine Rotational vertigo in the horizontal plane is caused by
strokes (e.g., anterior inferior cerebellar artery [AICA] syn- horizontal semicircular canal (SCC) dysfunction, which
dromes), the degree of nausea and v omiting is similar to commonly occurs from labyrinthine (e.g., labyrinthitis or
that in peripheral v estibular defects. For dorsal medulla Ménière’s) or eighth nerve dysfunction (vestibular neuri-
strokes (e.g., posterior inferior cerebellar artery [PICA] syn- tis). Rotational vertigo in the torsional plane (clockwise
dromes), nausea and v omiting are e xtreme and out of or counterclockwise direction) is caused by anterior and
proportion to the le vel of v ertigo.5 For all other central posterior SCC dysfunction on one side from a central
vestibular structures (cerebellar, fourth ventricle floor, in- lesion in the dorsal medulla. Tilt—lateral translation or
terstitial nucleus of Cajal, thalamus, and vestibular cortical lateropulsion—is caused by utricle dysfunction, which can
lesions), nausea and vomiting are usually mild or absent. be caused by lesions in the labyrinth or eighth nerv e, but
more commonly occurs from central defects. Lesions in
Oscillopsia central vestibular pathways may cause n ystagmus, skew
Oscillopsia is the subjective illusion of visual motion. It eye deviation, and lateropulsion but rarely cause rotational
differs from vertigo, in that oscillopsia occurs only with vertigo.
the eyes open, whereas vertigo occurs with the eyes open
or closed. P atients occasionally interpret oscillopsia as Circumstance
“dizziness.” There are two types of oscillopsia: (1) Spon- The clinician must determine the circumstances in which
taneous oscillopsia is caused by acquired n ystagmus and the patient’s dizziness occurs. Dizziness may be provoked
is a result of apparent motion of the visual scene caused by only by certain movements, such as standing up after lying
movement of the retina (retinal slip); (2) Head movement– down for at least 10 minutes (orthostatic hypotension)
induced oscillopsia occurs in patients with severe, bilateral or vertical or oblique head movements (lying down, turn-
loss of the v estibular-ocular reflex (VOR), which is fre- ing over in bed, or sitting up, BPPV). If e ye movements
quently experienced after ototoxicity caused by aminogly- without head movement cause dizziness, and there is no
cosides. This form of oscillopsia occurs only during head eye movement disorder (such as ocular misalignment or
movements and is caused by the lack of the gaze-stabilizing an internuclear ophthalmoparesis), the symptom is not
features of the VOR. likely to be caused by a v estibular or neurological prob-
lem. When dizziness occurs without provocation (sponta-
Floating, Swimming, and Spinning inside the neous), and it is v estibular in origin, it is commonly
Head (Psychological Symptoms) exacerbated by head movements.
Sensations of floating, swimming, or swimming “inside
the head” are frequently the symptoms of anxiety (panic International Classification
attacks, agoraphobia, obsessive-compulsive disorder), so- of Vestibular Symptoms
matoform disorders (including conversion), or depression In an attempt to achie ve an international consensus of
(see Chapter 18 for further discussion). vestibular disorders, a committee of the Baran y Society
met and published their f irst document. Their first paper
Vertical Diplopia classified vestibular symptoms.6 Table 10-3 shows a mod-
Vertical diplopia is double vision in which the two images ification of their diagrams based on the concepts we use
line up vertically. The diplopia is not present if either eye at Emory. The main symptoms include dizziness, vertigo,
3970_Ch10_159-177 25/06/14 11:36 AM Page 164
Spontaneous
Classification vs Triggered How Triggered Symptom
vestibular-visual symptoms, and postural symptoms. Each but he just w ants to be reassured that it is nothing seri-
of these may occur spontaneously or may be triggered. ously wrong; this response w ould not require e xtensive
Readers interested in the details of the classification from evaluation and management. A second patient may state
that publication should refer to the original article. that she has no unsteadiness while w alking but can no
longer play golf or tennis because of her balance; this
Other Helpful Elements in the History patient may require only a high-le vel physical therapy
How the Dizziness Affects the Patient’s Life exercise program. A third patient may state that he is com-
One of the most useful questions to ask in order to deter- pletely devastated by the dizziness and will not leave the
mine appropriate management is “How does the dizziness house, drive, or participate in an y social activities. This
affect your life?” Three patients with an incomplete pe- patient requires extensive counseling and physical therapy
ripheral vestibular loss from v estibular neuritis on one by the physician and physical therapist. He may also need
side may give three different responses. The first patient medication and psychological counseling to better cope
may state that he is not af fected at all by the dizziness, with the symptom.
3970_Ch10_159-177 25/06/14 11:36 AM Page 165
Medications with words on both ends. The person rates the symptom
The clinician must make sure to obtain a complete list of intensity while sitting quietly and then while actually per-
all of a patient’s prescription and o ver-the-counter med- forming a task. The results are expressed as the difference
ications. A number of drugs can cause dizziness, some of between the baseline measure and the measure after per -
which also are used to treat dizziness (see Chapter 14). forming the task. In the example (see Fig. 10.1), the results
Some over-the-counter medications, such as diphenhy- are the intensity of dizziness, as measured on a 10-cm line,
dramine and meclizine, also cause dizziness. while sitting quietly and then after 1 minute of horizontal
head movements at a 1-Hz frequenc y. Separate papers
What the Patient Believes Is Causing containing the line are used for each measure.
the Dizziness
Another overlooked question that should be ask ed of a Impact on Functional Activities
patient with dizziness is “What do you think is causing The effect of dizziness on the patient’s functional activities
your dizziness?” Sometimes the patient has a specific con- can be determined from Section A of the Multidimensional
cern that may not be addressed routinely by the health care Dizziness Inventory found on the last page of the P atient
provider. Unless this concern is addressed, the patient may Questionnaire (see Appendix A at the end of the book).
leave the clinic unsatisfied with the visit.
Perceived Disability
The perceived disability caused by a patient’ s dizziness
Elements that Lead to Goals for can be determined from the Disability Scale, sho wn in
Management, Including Physical Box 10-1.7 In this scale, the patient picks the best state-
Therapy ment out of six that best fits how he or she feels. The clini-
Subjective Complaints cian must remember that this is perceived disability or
Two components of the history and examination are help- handicap. The scale has been v alidated for degree of per-
ful in developing treatment goals. The first is obtaining a ceived disability in patients with unilateral v estibular loss
list of the patient’s subjective complaints. One method of (UVL) and bilateral visual loss (BVL).A score of 4 or higher
doing so is to present a written list of symptoms that the is correlated with poor outcome of vestibular rehabilitation;
patient can simply check of f (see Item 1 of the P atient that is, the dizziness is unlikely to change with rehabilitation.
Questionnaire in Appendix A at the back of the book). The This scale has high test-retest reliability (r = 0.97).8
second is to quantify the intensity of specif ic symptoms,
for instance, by using a Visual Analogue Scale (VAS).
Box 10-1
An example would be the head mo vement VAS shown
in Figure 10.1. It consists of a 10-cm line anchored
DISABILITY SCALE*
For the following, please pick the one statement
“Place a mark on the line below corresponding to how dizzy that best describes how you feel:
you feel while you are sitting here” ______ Negligible symptoms (0)
As bad as it can be ______ Bothersome symptoms (1)
______ Performs usual work duties but
symptoms interfere with outside activities (2)
______ Symptoms disrupt performance of
both usual work duties and outside activities (3)
______ Currently on medical leave or had to
change jobs because of symptoms (4)
______ Unable to work for over one year
No dizziness or established permanent disability with
Figure 10.1 Head movement Visual Analogue Scale (VAS). compensation payments (5)
The patient is instructed to place a mark on the line corre-
sponding to how dizzy he or she feels while sitting and then *Numbers in parentheses are individual scores for scale. A score of
while performing a task. For this scale, test-retest reliability 4 or higher is correlated with poor outcome from vestibular rehabilitation;
is r = 0.59, based on a separate sample of patients with that is, that patient’s condition is unlikely to change with rehabilitation.
unilateral and bilateral vestibular loss (n = 25). (Adapted from Shepard et al, 1990.7)
3970_Ch10_159-177 25/06/14 11:36 AM Page 166
Skew eye deviation (vertical eye misalignment) Disruption of peripheral or central utricle pathway
Eye movements and vertigo elicited during Usually, inner ear debris from benign paroxysmal positional vertigo
maneuvers Rarely, central positional vertigo or nystagmus, perilymphatic
fistula, hypermobile stapes, Ménière’s disease, superior semicircular
canal dehiscence
Effect of fixation Nystagmus decreases Nystagmus either does not change or it increases
Direction of gaze Usually mixed plane (horizontal and Usually single-plane horizontal (torsional or
torsional) vertical)
Effect of gaze Nystagmus increases with gaze toward Nystagmus either does not change or reverses
direction of quick phase direction
3970_Ch10_159-177 25/06/14 11:36 AM Page 168
Torsional nystagmus Dorsolateral medulla lesion Decreased tonic neural activity to the INC from
anterior and posterior SCC on one side
Downbeat nystagmus Lesion of cerebellar flocculus or floor Decreased tonic neural activity to the INC from
of fourth ventricle posterior SCC on both sides
Upbeat nystagmus Lesion of brachium conjunctivum or Decreased tonic neural activity to INC from
dorsal upper medulla central anterior SCC on both sides
Seesaw nystagmus Unilateral lesion of INC Unilateral inactivation of INC on one side
Periodic alternating Cerebellar nodulus lesions Unstable (high gain) neural activity in the MVN
nystagmus
Latent nystagmus Loss of cortical binocular visual input Decreased tonic neural activity to MVN from the
to the NOT usually from congenital NOT on one side when one eye is covered. (NOT
esotropia provides all the visual input into the MVN)
INC = interstitial nucleus of Cajal; MVN = medial vestibular nucleus; NOT = nucleus optic tract;
SCC = semicircular canal.
3970_Ch10_159-177 25/06/14 11:36 AM Page 170
X
Figure 10.6 Pathological ocular tilt response from left-
sided peripheral vestibular defect. This defect causes the
head to tilt to the left, the eyes to have a static torsional
component to the left, and a skew eye deviation resulting
in a right hypertropia. In the light during bedside examina-
tion, the only finding that may be readily appreciated is the
skew eye deviation.
Vestibular dynamic Static, distant visual acuity is determined A dynamic visual acuity of 3 or more lines
visual acuity (DVA) with the head still above static visual acuity indicates a vestibular
Dynamic visual acuity is then determined defect
while the patient’s head is oscillated
manually at 2 Hz
Head impulse The patient fixates a distant visual target, A refixation saccade after the head impulse
and eye position is observed immediately indicates decreased VOR
after a small impulse of the head to the left If the head impulse elicits a refixation saccade
and right when the patient is fixating a target at near, the
test should be repeated with the patient looking
at a distant target in order to clearly have a
positive result, especially in older patients
Head-shaking Clinician pitches the patient’s head down Elicitation of jerk nystagmus during this
nystagmus 30 degrees and oscillates the head horizon- procedure indicates a vestibular imbalance
tally 20 times
refixation saccade indicates decreased VOR.18 It is impor- specificity of the head-shaking n ystagmus test with
tant that the patients are tested while they are wearing their respect to the caloric test for UVL. F or a variety of
usual glasses, because the VOR is calibrated for visual in- types of UVL, the o verall sensitivity is 46%, and the
puts through those glasses. Table 10-10 shows the sensi- specificity is 75%. Table 10-13 shows the frequency of
tivity and specificity of the head-impulse test with respect a positive head-shaking nystagmus test with respect to
to the caloric test for UVL. For complete UVL caused by the severity of UVL (canal paresis).22
nerve section, the sensitivity and specificity are 100%. For
incomplete UVL from a v ariety of causes, the median Clinical Vestibular Dynamic
sensitivity is 39%, and the specificity is 95%. Sensitivity of Visual Acuity Test
testing can be impro ved by (1) pitching the head do wn The clinical vestibular dynamic visual acuity test com-
30 degrees to place the horizontal SCC in the plane of move- pares visual acuity with the head still to visual acuity
ment and (2) making the head impulse unpredictable. 19 with the head mo ving. Visual acuity with the head still
Table 10-11 shows how the head impulse test results vary is measured first using a visual acuity chart. The patient
with the severity of UVL. 20 For example, for moderate is then asked to read the smallest possible line on the chart
paresis of the caloric test (50% to 75% weakness), 19 pa- while the examiner manually oscillates the patient’s head
tients had a negative head impulse test (90% of the total horizontally at 2 Hz so the f ace moves 1 or 2 inches in
tested) and 2 patients had a positive test (10% of the total either direction—above the frequency at which pursuit eye
tested). movements can track the target. If the VOR is normal, the
patient’s eyes will move smoothly in the opposite direction
Head-Shaking Nystagmus Test of the head mo vement so that ocular f ixation is always
While wearing Frenzel or IR goggles, the patient is maintained. The patient should be able to read either the
asked to close the eyes, pitch the head down 30 degrees, same line as when the head w as still (initial static visual
and then rapidly oscillate the head 20 times horizon- acuity) or the next line above it, which has larger letters.
tally. After the head oscillation, the patient opens the If the patient can read only lines more than 3 lines abo ve
eyes, which the clinician observes for nystagmus. The the initial static visual acuity line, he or she lik ely has a
presence of nystagmus immediately after this procedure vestibular defect (Fig. 10.7). After vestibular adaptation
indicates a vestibular imbalance.21 This sign may per- exercises, dynamic visual acuity impro ves, possibly be-
sist indefinitely after a peripheral or central unilateral cause of the development of preprogrammed or anticipa-
vestibular lesion. Table 10-12 shows the sensitivity and tory eye movements.23,24
3970_Ch10_159-177 25/06/14 11:36 AM Page 172
■ Table 10-10 BEDSIDE HEAD-IMPULSE TEST COMPARED WITH CALORIC TEST FOR
UNILATERAL VESTIBULAR LOSS (UVL)*
Type or Cause of UVL Specificity (%)* Specificity (%)* No. of Patients Study
95 62 85 Takahashi et al (1990)30
Average: 46 Average: 75
172
3970_Ch10_159-177 25/06/14 11:36 AM Page 173
Figure 10.7 Dynamic visual acuity (DVA) scores in patients with vestibular hypofunction
and normal controls. On the ordinate is the number of letters (optotypes) missed on a stan-
dardized visual acuity (SVA) chart called the ETDRS chart (used in the Early Treatment Diabetic
Retinopathy Study). This chart has five letters on each line. On the abscissa are the rankings
of individual subjects that had the best visual acuity (to the left) to the most impaired (to the
right). Gray bars represent controls or subjects seen in the clinic for dizziness who did not
have a vestibular defect according to bithermal water caloric testing. White bars represent
subjects with unilateral vestibular loss (25% or greater asymmetry). Black bars represent
subjects with bilateral vestibular loss according to caloric testing (<20 degrees of peak
slow-phase velocity on four irrigations) and rotary chair test (gain < 0.1).
3970_Ch10_159-177 25/06/14 11:36 AM Page 174
Target Position
R10deg-
hypermetric. Saccade velocity should be brisk and equal horizontal saccade slowing. Slow saccades can also be
in the two eyes. The patient should also be told to follow caused by internuclear ophthalmoparesis (INO). An INO
an optokinetic drum or tape to assess quick phases of occurs when the pathw ay between the sixth and third
nystagmus. nerve nuclei is disrupted. In an INO, saccades in the e ye
Peripheral vestibular defects do not impair saccades. moving toward the nose (adducting) are slower or limited
In contrast, unilateral lesions of the cerebellum or its af - compared with those in the e ye moving away from the
ferent and efferent connections can cause hypermetria in nose (abducting). Slow saccades can also occur because
one direction and hypometria in the other direction.A uni- of problems in the neuromuscular junction (e.g., myasthe-
lateral lesion involving the cerebellar vermis from a supe- nia gravis, Miller-Fisher syndrome). Finally, slow sac-
rior cerebellar artery inf arction results in contralateral cades may occur because of eye muscle problems (thyroid
hypermetria and ipsilateral hypometria. Inf arction of the eye disease, progressive external ophthalmoplegia).
lateral medulla (Wallenberg’s syndrome) also results in
ipsilateral hypermetria and contralateral hypometria, pre-
Stance and Gait
sumably because of deafferentation of the fastigial nucleus
from infarction of the inferior cerebellar peduncle. The The Romberg test, “Sharpened” Romberg (heel-to-toe tan-
definition of saccade parameters are listed inTable 10-15. dem stance) test, Fukuda’ s Stepping Test (FST), and
Cerebellar vermal lesions result in hypometric sac- retropulsion test should be performed to e valuate stance
cades to the right and to the left. Slo w saccades can be and gait and tandem gait.
caused by a number of different disorders, including a de- In the Romberg tests, the patient is ask ed to stand
crease in the number of burst cells in the paramedian pon- with feet slightly apart and arms folded across the chest
tine reticular formation (PPRF) and rostral interstitial with eyes open for 30 seconds and then with e yes closed
nucleus of the medial longitudinal f asciculus RiMLF. for 30 seconds. A positive Romberg test result is one in
Generally, lesions involving the midbrain cause v ertical which the patient is stable with e yes open b ut loses
saccade slowing, whereas lesions involving the pons cause balance with e yes closed. A positive Romberg result
Latency Time from target step to beginning of Increased latency seen primarily with lesions in
saccade cerebral cortex (visual attention defects) or
brainstem (defects in initiation)
Velocity Peak speed of saccade Decreased velocity seen primarily from lesions in
the pons (burst cells)
occurs in patients with severe proprioceptive defects from important, how the symptoms af fect the indi vidual’s
a peripheral neuropathy and may be found in patients with lifestyle. It is the primary piece of information that deter -
acute vestibular defects. The Romberg test is also useful in mines how the patient should be managed. The bedside
identifying a functional component, suggested when the pa- exam is v ery helpful in determining if the patient has
tient rocks backward on the heels yet, remarkably, does not vestibular hypofunction on one or both sides, BPPV, a cen-
fall or have an exaggerated sway during the test. In the tral defect in the posterior fossa, or psychogenic features.
Sharpened Romberg test, the patient is asked to stand with
feet in heel-to-toe position, f irst with eyes open and then References
with eyes closed. A positive Sharpened Romberg test result 1. Brown JJ, Baloh RW. Persistent mal de débarquement
is found in patients with the same disorders that cause a pos- syndrome: a motion-induced subjective disorder of
itive Romberg result, in those with chronic v estibular de- balance. Am J Otolaryngol. 1987;8:219-222.
fects, and in some normal individuals older than 65 years. 2. Brandt TH, Daroff RB. The multisensory physiological
For the Fukuda Stepping Test, the subject steps in and pathological vertigo syndromes. Ann Neurol. 1980;7:
195-203.
place for 50 steps with arms e xtended and eyes closed.34 3. Kuritzky A, Ziegler DK, Hassanein R. Vertigo, motion
Progressive turning toward one side of more than 30 to sickness and migraine. Headache. 1981;21:227-231.
45 degrees is abnormal. An abnormal Fukuda Stepping 4. Kayan A, Hood JD. Neuro-otological manifestations of
Test can occur from an asymmetric vestibulospinal reflex migraine. Brain. 1984;107:1123-1142.
tone from peripheral or central vestibular tone asymmetry 5. Fisher CM. Vomiting out of proportion to dizziness in
ischemic brainstem strokes. Neurology. 1996;46:267.
or loss. It can also occur from musculo-skeletal asymme- 6. Bisdorff A, Von Brevern M, Lempert T, Newman-Toker
tries including leg-length discrepancy, sciatica, muscle im- DE. Classification of vestibular symptoms: towards an
balance, or asymmetric joint problems from the hip down. international classification of vestibular disorders. J Vestib
Based on 126 consecutive patients with unilateral vestibu- Res. 2009;19:1-13.
lar loss, abnormal deviation toward the side of the lesion 7. Shepard NT, Telian SA, Smith-Wheelock M. Habituation
and balance retraining therapy: a retrospective review.
(45 deg or more deviation) occurred in 50.0% of cases and Neurol Clin. 1990;8:459-475.
toward the intact side in 24.6% of cases. 35 In a study that 8. Hall CD, Herdman SJ. Reliability of clinical measures
measured FST as a function of de gree of caloric weakness used to assess patients with peripheral vestibular disorders.
on ENG, FST w as only sensitive in detecting v estibular J Neurol Phys Ther. 2006;30:74-81.
weakness when the weakness was severe on ENG (greater 9. Powell LE, Myers AM. The Activities-specific Balance
Confidence (ABC) Scale. J Gerontol A Biol Sci Med Sci.
than 75% weakness). Furthermore, the FST abnormality de- 1995; 50:28-34.
creased with time following the vestibular defect.36 10. Whitney SL, Hudak MT, Marchetti GF. The activities-
In the retropulsion test, the patient stands with the feet specific balance confidence scale and the dizziness
slightly spread apart and is instructed to just take one step handicap inventory: a comparison. J Vestib Res. 1999;
backward if pulled backward at the hips by a mild force. 9:253-259.
11. Fetter M, Dichgans J. Vestibular neuritis spares the inferior
The result is positive if the patient must take three or more division of the vestibular nerve. Brain. 1996;119:755-763.
steps backward or falls backward like a log. The retropul- 12. Tusa RJ. The dizzy patient: disturbances of the vestibular
sion test has a positive result in patients with basal ganglia system. In: Tasman WL, Jaeger, EA, eds. Duane’s Clinical
disorders (progressive supranuclear palsy, Parkinson’s dis- Ophthalmology, Vol 2. Philadelphia: Lippincott-Raven;
ease) and disorders that disrupt frontal lobe–basal ganglia 1998.
13. Zee DS. Ophthalmoscopy in examination of patients with
projections (normal-pressure hydrocephalus, leukoareosis). vestibular disorders. Ann Neurol. 1978;3:373-374.
Gait and tandem gait should be e xamined for cere- 14. Brandt T. Vertigo: Its Multisensory Syndrome. London:
bellar ataxia, decreased head-on-body movements during Springer-Verlag; 1991.
turns (vestibular hypofunction), and shuf fling gait in 15. Uchino Y, Sasaki M, Sato H, et al. Utriculoocular reflex
Parkinson’s disease. Other features of gait help identify a arc of the cat. J Neurophysiol. 1996;76:1896-1903.
16. Halmagyi GM, Gresty MA, Gibson WPR. Ocular tilt
functional component, including knee b uckling without reaction with peripheral vestibular lesion. Ann Neurol.
fall, small-amplitude steps, uneconomical posture and 1979;6:80-83.
movement, excessive slowness in gait, and fluctuations in 17. Smith PF, Curthoys IS. Neuronal activity in the contralateral
levels of impairment.37,38 (and ipsilateral) medial vestibular nucleus of the guinea pig
following unilateral labyrinthectomy. Brain Res. 1988;
444:295-319.
Summary 18. Halmagyi GM, Curthoys IS. A clinical sign of canal
paresis. Arch Neurol. 1988;45:737-739.
An accurate history is needed to determine the onset of 19. Schubert M, Tusa RJ, Grine LE, Herdman SJ. Optimizing
the problem, description of the symptoms, and, most the sensitivity and specificity of the head thrust test for
3970_Ch10_159-177 25/06/14 11:36 AM Page 177
identifying vestibular hypofunction. Physical Therapy. 30. Takahashi S, Fetter M, Koenig E, Dichgans J. The clinical
2004;84:151-158. significance of head-shaking nystagmus in the dizzy
20. Beynon GJ, Jani P, Baguley DM. A clinical evaluation of patient. Acta Otolaryngol (Stockh). 1990;109:8-14.
head impulse testing. Clin Otolaryngol. 1998;23:117-122. 31. Jacobson GP, Newman CW, Safadi I. Sensitivity and
21. Hain TC, Fetter M, Zee DS. Head-shaking nystagmus in specificity of the head-shaking test for detecting vestibular
patients with unilateral peripheral vestibular lesions. Am J system abnormalities. Ann Otol Rhinol Laryngol. 1990;
Otolaryngol. 1987;8:36-47. 99:539-542.
22. Asawavichianginda S, Fujimoto M, Mai M, Rutka J. 32. Burgio DL, Blakely BW, Myers SF. An evaluation of the
Prevalence of head-shaking nystagmus in patients accord- head-shaking nystagmus test. Otolaryngol Head Neck
ing to their diagnostic classification in a dizziness unit. Surg. 1991;105:708-713.
J Otolaryngol. 1997;26:20-25. 33. Goebel JA,Garcia P. Prevalence of post-headshake nystag-
23. Herdman SJ, Schubert MC, Das VE, Tusa RJ. Recovery mus in patients with caloric deficits and vertigo. Otolaryn-
of dynamic visual acuity in unilateral vestibular hypo- gol Head Neck Surg. 1992;106:121-127.
function. Arch Otolaryngol Head Neck Surg. 2003; 34. Fukuda T. The stepping test: two phases of the labyrinthine
129:819-824. reflex. Acta Otolaryngol (Stockh). 1959;50:95-108.
24. Herdman SJ, Schubert MC, Tusa RJ. Role of central 35. Zhang YB, Wang WQ. Reliability of the Fukuda stepping
preprogramming in dynamic visual acuity with vestibular test to determine the side of vestibular dysfunction. J Int
loss. Arch Otol Head Neck Surg. 2001;127:1205-1210. Med Res. 2011;39:1432-1437.
25. Foster CA, Foster BD, Spindler J, Harris JP. Functional 36. Honaker JA, Shepard NT. Performance of Fukuda
loss of the horizontal doll’s eye reflex following unilateral Stepping Test as a function of the severity of caloric
vestibular lesions. Laryngoscope. 1994;104:473-478. weakness in chronic dizzy patients. J Am Acad Audiol.
26. Harvey SA, Wood DJ. The oculocephalic response in the 2012;23:616-622.
evaluation of the dizzy patient. Laryngoscope. 1996;106:6-9. 37. Keane JR. Hysterical gait disorders: 60 cases. Neurology.
27. Harvey SA, Wood DJ, Feroah TR. Relationship of the 1989;39:586-589.
head impulse test and head-shake nystagmus in reference 38. Lempert T, Brandt T, Dieterich M, Huppert D. How to
to caloric testing. Am J Otol. 1997;18:207-213. identify psychogenic disorders of stance and gait. J Neurol.
28. Perez N, Rama-Lopez J. Head-impulse and caloric tests in 1991;238:140-146.
patients with dizziness. Otol Neurotol. 2003; 24:913-917.
29. Wei D, Hain TC, Proctor LR. Head shaking nystagmus:
associations with canal paresis and hearing loss. Acta
Otolaryngol (Stockh). 1989;108:362-367.
3970_Ch11_178-194 25/06/14 5:34 PM Page 178
CHAPTER 11
Vestibular
Function Tests
Michael C. Schubert, PT, PhD
The vestibular system senses motion of the head for the neutral) potential difference of 1 millivolt and provided the
purposes of maintaining stability of images on the fo vea first technique useful to record eye motion, called electro-
of the retina and stability of postural control during that oculography (EOG).2,3 By the early 1900s, the CRP had
head motion. In normal function, the vestibular receptors become the standard method to record eye motion.4 Using
provide an elegant and accurate representation of the mo- horizontally and vertically positioned surface electrodes,
tion of the head in three dimensions. This information is the CRP can be detected as the polarity of the eye rotates
then carried along central v estibular pathways to control toward or away from those electrodes. Because a torsional
the reflexes and perceptions that are mediated by the eye rotation (being purely clockwise or counterclockwise)
vestibular system. Disorders of vestibular function result does not cause a v ertical or horizontal deflection of the
in abnormalities in these refle xes and lead to sensations globe within the orbit, the electrodes cannot detect a rela-
that reflect abnormal information. tive change in the CRP. Thus, torsion eye rotations cannot
The output of the v estibular system can grossly be be monitored with EOG.
considered a motor response reflected in an ocular or pos- In addition to a method for recording eye rotation, ENG
tural behavior. The ocular signature of the vestibular sys- also refers to a battery of tests. As a test battery, the ENG
tem is typically measured from the vestibulo-ocular reflex includes measures of oculomotor function (including gaze
(VOR), and the postural beha vior is typically measured stability, smooth pursuit, and saccades), positional and po-
using force plate platform equipment. In this chapter, we sitioning testing, and the caloric exam. With the development
discuss the common testing techniques of the v estibular of video-based recording of eye movements, the test battery
system, categorized by ocular or posturographic behavior. is often referred to as VNG, video nystagmography.
Further delineations are made that incorporate testing the
behavioral outcome of the vestibular function.
Oculomotor Function
Various oculomotor systems and mechanisms can con-
Electronystagmography (ENG) tribute to visual f ixation of a tar get on the fo vea of the
In the 1800s, it was realized that a voltage of the eye ex- retina, in addition to the v estibular system. These non-
isted and varied with eye rotation.1 Because the cornea is vestibular mechanisms include the gaze stability (or gaze
positively charged with respect to the retina, a dipole (i.e., holding), smooth pursuit, and saccadic oculomotor sys-
battery) is formed (Fig. 11.1). This corneo-retinal potential tems. Influences such as tar get position, target velocity,
(CRP) has a baseline (e yes stationary, positioned in and head velocity are the stimulus variables the brain uses
178
3970_Ch11_178-194 25/06/14 5:34 PM Page 179
Smooth Pursuit
The smooth pursuit system is used to stabilize a mo ving
target on the fovea of the retina during lo w velocities and
Cornea
Ocular fundus
frequencies of head motion or target motion. Pursuit is gen-
Retina erated from multiple cortical regions in addition to the brain-
stem and cerebellum. As a result, tests of pursuit are not as
10–30 mV useful for localizing central pathology. Lesions of the pursuit
ⴙ ⴚ
system may present with unilateral or bilateral pursuit
Lens deficits. In cases of unilateral pursuit def icits, the deficits
are most apparent with pursuit to ward the side of lesion.
Although cerebral cortical structures may be in volved, the
lesions typically involve the brainstem pathways.5
Optic nerve The smooth pursuit oculomotor system can be quan-
tified by comparing target velocity with eye velocity (gain
= eye velocity/target velocity) while subjects follo w a
Figure 11.1 Corneo-retinal potential (CRP). The cornea moving target (Fig. 11.2). Abnormality of gain and asym-
of the eye is positive and the retina is negative. As the eyes
move horizontally or vertically toward surface electrodes metry between pursuit to the left and right (or up/do wn)
positioned both horizontally and vertically, the CRP can be are the measures of interest. Most studies agree that the
detected. The electrodes are recording the relative change smooth pursuit system is inef fective at maintaining fixa-
in CRP, not potentials from ocular muscles. Torsional (roll) tion of a moving target when the velocity or frequency of
eye rotations are not recorded, because the CRP does not the target exceeds 60 de g/sec or 1 Hz, respecti vely.6-9
change relative to the electrode position.
However, two studies reveal that the smooth10 pursuit sys-
tem can assist gaze stability at target velocities from 75 to
90 deg/sec.10,11 When analyzing smooth pursuit, the age
to determine which oculomotor system is recruited for of the patient must be considered, because smooth pursuit
gaze stability. The smooth pursuit, saccade, and vestibulo- performance is dependent on age. Other measures of
ocular motor systems each have ranges at which they func- pursuit that may be measured are latency (~125 msec) and
tion most effectively. Each system also has limitations at acceleration (range: 40 to 200 deg/sec/sec).10,12
which point it becomes inef fective. There is o verlap
among the effective ranges such that multiple mechanisms Saccade Oculomotor System
can combine for the purpose of stabilizing gaze. The pur- Saccades are rapid, conjugate e ye rotations that quickly
pose of investigating the oculomotor systems as part of the move the eyes to place the fovea on the target of interest.
ENG test battery is to identify pathology within the central Saccades do not therefore maintain gaze stability during
oculomotor and vestibular systems. Smooth pursuit and head movement, in contrast with the pursuit system, b ut
saccade testing are used to identify pathology within the instead quickly reposition the e yes. They are generated
brainstem and cerebellar regions. The inability to maintain from neurons within the brainstem, basal ganglia, frontal
gaze stability can be caused by either peripheral vestibular eye fields, and cerebellum (and of course require healthy
or central oculomotor pathology. cranial nerve and extraocular muscle function). Saccades
can be useful to locate site of pathology (i.e., internuclear
Gaze Stability ophthalmoplegia) within the central nervous system. Ab-
Gaze stability is the ability to hold the e yes stationary normalities in saccade testing do not occur as a result of
and is tested in primary gaze and after the eyes are moved peripheral vestibular pathology.
30 degrees up, down, right, and left. Gaze stability testing Saccades are tested by asking subjects to move their
is useful to identify problems with the peripheral vestibu- eyes to a newly repositioned target or between tw o sta-
lar or central oculomotor pathw ays. Subjects should be tionary targets. Often, the saccade testing is done using
able to maintain gaze without any eye motion. Abnormal multiple target amplitudes (Fig. 11.3). Horizontal saccades
gaze stability occurs when an eye rotation moves the eye generally occur from excitatory burst neurons within the
off the target (i.e., jerk n ystagmus, ocular flutter). Acute parapontine reticular formation of the pons.13 Vertical and
lesions of the peripheral vestibular system (i.e., vestibular torsional saccades typically occur from e xcitatory burst
neuritis) cause a spontaneous nystagmus that disrupts gaze neurons within the rostral interstitial nucleus of the medial
stability. Various pathologies of the central nervous system longitudinal fasciculus of the midbrain.14 Other central re-
also can disrupt gaze stability (e.g., cerebellar stroke). gions are able to generate horizontal and vertical/torsional
3970_Ch11_178-194 25/06/14 5:34 PM Page 180
R10
0
H
L10
L20
00:20
Sine Horizontal
R20
R10
0
ST
L10
L20
00:57
Tracking Gain
1.25 R gain = 0.60 L gain = 0.55 Frequency = 0.20 Hz Phase shift = –11.1
Velocity Gain
1.00
0.75
0.50
0.25
0.7 0.6 0.5 0.4 0.3 0.2 0.2 0.3 0.4 0.5 0.6 0.7
Rightward Target Frequency (Hz) Leftward
Figure 11.2 Raw trace and analysis plot for smooth pursuit testing. The top two plots
display the target moving in a horizontal sinusoid (left to right) at progressively larger
frequencies. In the bottom analysis plot, the shaded area represents abnormal performance.
The pursuit gain is plotted (y-axis) and is abnormally low for the majority of the testing
frequencies (x-axis).
saccades.5 Important variables in saccade testing are the Positional and Positioning Tests
latency, velocity, and accuracy of the eye rotation. Accel- Positional testing refers to placing the patient into v ari-
eration and amplitude are also considered. The latency to ous head or whole body positions to re veal those posi-
initiate a visually guided saccade is ~200 msec.15 Saccadic tions that cause nystagmus.18,19 Different laboratories use
eye velocities range from 250 to 600 deg/sec. The velocity different protocols. Typically, the patient’s body is placed
of the saccades is proportional to the amplitude the e ye into a minimum of four different positions (i.e., supine,
must move to fixate the target. This relationship between side lying, head right, and head left) to in vestigate nys-
saccade amplitude and v elocity is called the main se- tagmus induced by specif ic head positions relati ve to
quence and is useful to conf irm healthy function of the gravity. Positional testing is considered abnormal if the
saccadic system. Saccades are also typically identified by slow component e ye velocity (SCEV) is greater than
their exceptionally rapid accelerations that range from 5 deg/sec in any position; less than 6 deg/sec and persis-
12,000 to 40,000 deg/sec/sec.15,16 tent in 1/2 of the tested positions; or less than 6 de g/sec
For more in-depth reading on testing of the human ocu- and transient in all positions. The positioning test is
lomotor system, the reader is encouraged to see Jacobsen the Dix-Hallpike. Unlike the positional tests, in which
and Shepard 2008.17 the patient is brought slo wly into the various positions,
3970_Ch11_178-194 25/06/14 5:34 PM Page 181
R10
0
H
L10
L20
00:20
Peak Velocity
800 ***
Degrees/Second
600
400
200
0
30 20 10 0 −10 −20 −30
Rightward Amplitude (deg) Leftward
Accuracy
***
150
120
Percent
90
60
30
30 20 10 0 −10 −20 −30
Rightward Amplitude (deg) Leftward
Latency
***
400
300
Milliseconds
200
100
0
30 20 10 0 −10 −20 −30
Rightward Amplitude (deg) Leftward
Figure 11.3 Raw saccade traces and summary analysis for velocity, accuracy, and latency.
The top plot is for the horizontal channel and shows a random saccade target amplitude
(clean trace) and the subject’s eyes (jagged trace) following the target position. The velocity
and latency of the saccades are normal, and the accuracy is hypometric.
Amplitude (deg)
channel slow component fast component
This is Right
LEFT
Left
beating
nystagmus
Time (seconds)
30°
Vertical
A
Amplitude (deg)
channel
This is Up
DOWN Down Cold water
beating
nystagmus
Time (seconds)
Figure 11.4 Vestibular nystagmus. Nystagmus is named
using the fast component. Eye motion is most commonly
described with the patient as the reference (i.e., their
right/left). The graphing convention denotes the upper A U
1
/2 plot as a right/left rotation, and the lower 1/2 plot is
up/down rotation—depending on the channel.
temporal bone. The change in temperature is the greatest Figure 11.5 Mechanism of the caloric response. The
head must be positioned so the endolymph of the horizon-
for the lateral aspect of the temporal bone and the least for tal SCC can move in the direction of the gravitational vec-
the medial aspect. In the presence of gravity, this temper- tor (A). In this example, water cooled to 30 deg Celsius is
ature gradient results in the convective flow of endolymph flushed into the left external auditory canal ear (and sepa-
that deflects the cupula of the horizontal semicircular rately the right ear) for about 1 minute. This creates a tem-
canal and generates nystagmus (Fig. 11.5). For this reason, perature gradient in the middle ear that causes endolymph
to move within the left horizontal semicircular canal (B).
the position of the head during a caloric e xamination is As a result, the cupula is deflected and right-beating nys-
important. The caloric stimulation also causes some direct tagmus is generated (C). Direct hair cell stimulation and
hair cell stimulation and changes in pressure across the changes in pressure across the middle ear also cause cupu-
middle ear, which will also cause cupular deflection, con- lar deflection, contributing to the resulting nystagmus.
tributing to the resulting n ystagmus.21-23 The caloric test
is particularly useful for determining the side of a def icit
because each labyrinth is stimulated separately . The re- Unilateral weakness (or relative asymmetry) =
sulting nystagmus enables unique data that are analyzed (LC + LW) – (RC + RW)
× 100
by two means: (LC + LW + RC + RW)
1. The peak SCEV from irrigations of the right ear The values are generated from irrigations
are compared with the peak SCEV caused by irri- that are either 7 degrees Celsius above or below
gations from the left ear. These values are used in body temperature (LC – left cool; LW – left
Jongkees formula to determine the relative sym- warm; RC – right cool; RW – right warm). Cold
metry in the response to stimulation of the hori- irrigations inhibit the vestibular afferents of
zontal semicircular canals (SCCs) (Fig. 11.6).24 the stimulated horizontal SCC and create an
3970_Ch11_178-194 25/06/14 5:34 PM Page 183
Right Cool Peak SPV: 16 deg/s Left Warm Peak SPV: 18 deg/s
40 40
Slow Phase Velocity (deg/sec)
20 20
10 10
0 0
−10 −10
−20 −20
−30 −30
−40 −40
Right Warm Peak SPV: −20 deg/s Left Cool Peak SPV: −17 deg/s
0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 140
Seconds Seconds
Caloric weakness: 1% in the left ear
Directional preponderance: 4% to the right
80 80
60 60
Right Beating
Numeric Results
40 40 Right cool 16 deg/s LB
Slow Phase Velocity
Cool irrigation
40 40
Warm irrigation
60 60
80 80
Right Ear Left Ear
Figure 11.6 Summary of ENG analysis. Top plot shows individual peak slow-phase velocity
for warm and cool irrigations chosen by an examiner. The peak SPV values are in the upper
right corner of each plot. The bottom plot is a different rendering of the analysis, known as a
butterfly plot. Values are summarized in the legend. The junction of the irrigation plots (thin
and thicker lines) should be within the center-positioned rectangle representing normal
variability. This is a normal ENG exam.
inhibitory nystagmus pattern on the irrigated remembered using the mnemonic COWS: cold
side. Warm irrigations excite the vestibular opposite warm same—referring to the tempera-
afferents of the stimulated horizontal SCC and ture of the irrigation and the expected direction
create an excitatory nystagmus pattern on the ir- of the fast component of the nystagmus.
rigated side. Therefore, you would expect a right 2. The preference for the nystagmus to beat toward
cool irrigation to generate a left-beating nystag- one direction or another is also of interest.
mus and a right warm irrigation to generate a Directional preponderance (DP) is a measure
right-beating nystagmus (Fig. 11.7). This can be of the difference in the magnitude of nystagmus
3970_Ch11_178-194 25/06/14 5:34 PM Page 184
R10
0
H
L10
L20
01:33
Right Ear/Cool
R20
R10
0
H
L10
L20
01:53
Right Ear/Cool
R20
R10
0
H
L10
L20
02:13
Right Ear/Cool
R20
R10
0
H
L10
L20
02:33
Figure 11.7 Raw tracing of continual nystagmus following cool irrigations for right ear.
Vertical graph lines represent time in 1-sec epochs. Horizontal graph lines represent 10 deg
eye movements. This is a normal caloric response for this irrigation.
much lower than the natural frequencies of head movement extent of central nervous system compensation to vestibu-
(1 to 20 Hz). 25,26 A summary of the critical aspects of the lar hypofunction.20 The rotary chair test provides a phys-
caloric exam is provided in Box 11-1. iological stimulus, because rotating the patient causes
Occasionally, the warm and cool water (or air) irri- endolymph flow (with relative excitation and inhibition)
gations will suggest a 100% loss of vestibular function in from both horizontal SCCs. This form of test is a closer
one or both ears with no n ystagmus having been gener- approximation of natural head velocities as compared with
ated. In this case and others (e.g., the technician suspects the caloric test. The rotational chair test is indicated when
a poor stimulation caused by limited temperature e xpo- bilateral vestibular hypofunction is suspected, when test-
sure), ice water is irrigated into the suspect external audi- ing vestibular function in children, when the caloric test
tory canal, which provides a greater temperature gradient cannot be performed because of tympanic perforations or
and normally causes a robust endolymph flow and inhibi- anatomical asymmetries of the ear, when the caloric exam
tion of the horizontal semicircular canal af ferents. In the is abnormal for function in each horizontal SCC, whenever
case when no nystagmus is generated by the normal warm serial testing is desired, and when trying to determine the
and cool water irrigations, the ice water stimulus may gen- extent of compensation.
erate nystagmus. To confirm that the observed nystagmus In individuals with normal vestibular function, nys-
is caused by horizontal SCC stimulation, the patient is tagmus should be generated during rotational chair testing.
placed in the prone position, which, because of the rever- In individuals with vestibular hypofunction, nystagmus
sal of the canal relati ve to the gravitational vector, will will be generated, b ut the magnitude of the SCEV will
reverse the flow of the endolymph, reverse the cupular de- vary with the extent of the lesion. Data from the rotational
flection, and similarly reverse the direction of the nystag- chair test are collected by tw o means: step v elocity and
mus. If the nystagmus does not reverse or if no nystagmus sinusoid paradigms (Fig. 11.9). In the step velocity para-
is present, then the hypofunction from the horizontal SCC digm, the chair is stationary and accelerates to a predeter-
is considered complete (Fig. 11.8). mined peak velocity, continues to rotate at that v elocity,
and is then stopped suddenly. The test is commonly per-
Rotational Chair Testing formed using peak velocities of 60 and 240 deg/sec in each
The rotational chair test is the “gold standard” for identi- direction. The higher velocity steps can be used to lateral-
fying bilateral v estibular hypofunction (BVH) and the ize the hypofunction caused by inhibitory cutof f. For the
sinusoid tests, the chair oscillates in ya w (left/right) at
varying frequencies (e.g., 0.01, 0.02, 0.04 etc. . . . up to
1.28 Hz), typically with peak v elocities that remain con-
Box 11-1 stant at 50 or 60 deg/sec.
The typical parameters that are measured from the
SUMMARY OF THE CALORIC rotational chair test include Gain, Phase or Time Constant,
EXAM and Asymmetry. The VOR gain is expressed as the ratio
• Nystagmus occurs primarily because of of eye velocity to head velocity (eye velocity/head velocity).
endolymphatic flow caused by convection cur- Under ideal conditions, and when the e yes are not con-
rent and eighth nerve excitation/inhibition. verged, the VOR gain is –1, implying a compensatory eye
• Typical water irrigations involve temperatures velocity equal to the head v elocity but in the opposite
7°C above and 7°C below body temperature. direction. The gain of the VOR during rotational chair test-
• Cold Opposite Warm Same (COWS). ing is typically much lower than –1, for a v ariety of rea-
• Most labs consider UW/RVR and DP to be sons (equipment, alertness) (Fig. 11.10). Each v estibular
abnormal when ≥26%. testing laboratory should determine their normal v alues
• Only examines the horizontal semicircular canal for VOR gain. Generally, the VOR is considered if there
and related afferents. is a gain asymmetry, defined as a greater than 26% differ-
• Ice water irrigation commonly applied only when ence in the response to rotations to the right and left.
an absent response occurs or the technician VOR phase and VOR time constant are measures
suspects a poor irrigation. of the transduction process and velocity storage system.
• Water irrigations more robust, air is useful in the Phase is measured with the sinusoid testing paradigm,
case of perforated TM. and the time constant is measured with the step velocity
testing paradigm. Both measures are useful variables for
UW – unilateral weakness; RVR – reduced vestibular response; assessing the integrity of the vestibular system. Phase is
DP – directional preponderance; TM – tympanic membrane a measure of the timing relationship between the eye and
3970_Ch11_178-194 25/06/14 5:34 PM Page 186
Right Cool Peak SPV: 0 deg/s Left Warm Peak SPV: 0 deg/s
20 20
15 15
Slow Phase Velocity (deg/sec)
5 5
0 0
−5 −5
−10 −10
−15 −15
−20 −20
Right Warm Peak SPV: 0 deg/s Left Cool Peak SPV: −10 deg/s
0 20 40 60 80 100 120 140 0 20 40 60 80 100 120 140
Seconds Seconds
Caloric weakness: 100% in the right ear
A Directional preponderance: 100% to the right
R10
0 H
L10
L20
01:15
Right Ear/Prone - Horizontal
R20
R10
0 H
L10
L20
B 00:20
Figure 11.8 Abnormal ENG and ice water caloric examination. (A) Irrigations into the right ear
(cool and warm) generate no nystagmus. In contrast, note the symbols present for the left cool
and warm water irrigations. (B) Ice water irrigation into the right ear causes no nystagmus—
regardless of supine or prone positioning.
3970_Ch11_178-194 25/06/14 5:34 PM Page 187
Eye Velocity
0 0
−80 −240
0 10 20 30 0 10 20 30
Time (sec) Time (sec)
VOR DATA
At 60 degrees per second At 240 degrees per second
gR = 0.918 gL = 0.896 gR = 0.802 gL = 0.969
tcR = 16.8 tcL = 19.1 tcR = 13.2 tcL = 12.7
GAIN DP = 1.2 TC DP = 6.4 GAIN DP = 9.4 TC DP = 1.9
Figure 11.10 VOR gain and time constant during 60 and 240 deg/sec rotations (step
profile). Note the magnitude of the VOR gain and the duration of the time constant. The
plots appear to normally reduce in velocity over time.
3970_Ch11_178-194 25/06/14 5:34 PM Page 188
−2
−4
−6
5°/s eye velocity
VOR gain = 1.0 VOR Gain = 0.5
−8
Leftward
−10 10°/s eye velocity
0.05 0.15 0.25 0.35 0.45 0.55 0.65 0.75
Time (s)
Figure 11.11 Simulated eye rotation during low-frequency sinusoidal head rotation. Positive
numbers along ordinate indicate rightward velocity rotation; negative numbers indicate leftward
velocity rotation. Arrow line styles match simulated eye velocities. For individuals with healthy
vestibular function, as the head rotates to the right at 10 deg/sec, the eyes move to the left at
10 deg/sec, and the eye and head velocity reach zero at the same time (gain = 1, zero phase
shift). For those with bilateral reduced vestibular function, eye velocity may be one half or less
with respect to head velocity (5 deg/sec in this example, gain = 0.5), and the eyes cross zero
velocity in advance of the head crossing zero velocity (eye position leads the head position—
phase lead). VOR gain = eye velocity/head velocity. (Reprinted from Schubert and Minor.
Vestibulo-ocular physiology underlying vestibular hypofunction. Phys Ther. 2004;84(4):373-385,
with permission from the American Physical Therapy Association. This material is copyrighted,
and any further reproduction or distribution requires written permission from APTA.)
relative to the stationary head, causing the cupulae to de- In peripheral vestibular pathology, there is a decrease
flect in the opposite directions, which causes the e xcita- in the time constant and an abnormal phase lead (at low test-
tion-inhibition pattern within the afferents of the horizontal ing frequencies), which never recover. In central pathologies
SCCs to reverse. For example, a chair rotation to the right (i.e., cerebellar), the time constant can be abnormally long
will excite the right horizontal SCC af ferents by causing and there can be an abnormal phase lag. Although the time
an ampullopetal cupular deflection, and inhibit the left hor- constant and phase measures do not recover, the VOR gain
izontal SCC afferents by causing an ampullofugal cupular to low velocity rotations (i.e., 60 deg/sec) does recover. In
deflection. The resultant nystagmus should be right beat- fact, the rotational chair can be a useful measure of dynamic
ing. Gradually, the nystagmus will stop, at which point the compensation when the VOR gains for the 60 deg/sec step
examiner stops the rotating chair. As soon as the chair stops velocity rotations are normal or when the asymmetry from
its rightward rotation, the endolymph within the left hori- the sinusoid paradigm tests demonstrate an asymmetry less
zontal SCC moves such that the cupula is deflected in an than 25%. In functional reco very from a chronic unilateral
ampullopetal direction. Thus, the left horizontal SCC af - vestibular hypofunction, the VOR gain during 60 de g/sec
ferents are excited, but the right horizontal SCC afferents rotations should be symmetrical. In the case of the f aster
are inhibited because of the ampullofugal cupular deflec- 240 deg/sec step rotations, VOR gain will still be abnormal
tion. The resultant nystagmus should be left beating. This, for ipsilesional rotations.
too, will gradually decline and is used in determining the The extent of pathology from rotation chair data is
time constant of the VOR. determined by comparing VOR gain and phase (or time
3970_Ch11_178-194 25/06/14 5:34 PM Page 189
constant) measures with established normal v alues and recorded from the electrodes. In healthy v estibular func-
comparing the gain values for rotations to the right and to tion, an initial inhibitory potential (occurring at a latency
the left. Rotary chair testing is limited in its diagnostic abil- of 13 msec after the click) is followed by an excitatory po-
ity, because only the horizontal SCCs are assessed to deter- tential (occurring at a latency of 21 msec after the click),
mine extent of pathology. A summary of the critical aspects with symmetric amplitude and threshold waveforms. For
of the rotational chair exam is provided in Box 11-2. patients with vestibular hypofunction, the cVEMPs may
be absent on the side of the lesion.The cVEMP is consid-
Otolith Function ered a test of the saccule and the inferior vestibular nerve
Recent advances in v estibular diagnostic testing ha ve afferents. The saccule has been implicated as the site of
extended the region of identifiable pathology to include afferent stimulation during cVEMP testing, because sac-
the otolith organs.28-30 The vestibular-evoked myogenic cular afferents provide ipsilateral inhibitory disynaptic
potential (VEMP) tests ha ve become an important com- input to the SCM muscle, 31 are responsive to click
ponent of the v estibular function test battery. Two types noise,32-34 and are positioned close to the footplate of
of VEMP studies e xist, cervical and ocular . Each test the stapes. Therefore, the saccular afferents are subject to
examines for the presence and absence of the response, mechanical stimulation.29,32
abnormally low threshold (i.e., 70 to 80 dB nHL), and/or The ocular VEMP (oVEMP) is a ne wer test that
abnormally large amplitude wave form when the stimulus places surface electrodes on the superior cheek re gion,
is applied. positioned over the inferior oblique (IO) muscle. During
The cervical VEMP (cVEMP) in volves recording the test, subjects must be looking up to bring the IO
from electrodes placed over the sternocleidomastoid mus- muscle closer to the electrodes. When clicks to the ear are
cle, which must be contracted during the test.When clicks introduced, or bone vibration to the skull is applied, the
are introduced to the ipsilateral ear, a disynaptic inhibitory contralateral IO muscle is excited and EMG is recorded.
pathway originating from the saccular afferents travels via In individuals with normal vestibular function, the latency
the medial vestibulospinal tract to ipsilateral sternocleido- of the first waveform is excitatory at 10 msec followed by
mastoid (SCM) motoneurons. A transient inhibition of the an inhibitory w aveform with a 16-msec latenc y. The
ipsilateral contracted SCM therefore occurs, which is oVEMP is considered a test of the utricle and the superior
vestibular nerve afferents. The utricle has been implicated
during oVEMP testing based on patients with superior
nerve vestibular neuritis (confirmed abnormal caloric and
Box 11-2 head impulse (thrust) test), who also had absent or reduced
oVEMPs.35 VEMP testing has become particularly useful
SUMMARY OF THE ROTATIONAL in assisting the diagnoses of superior canal dehiscence
CHAIR EXAM syndrome and Ménière’s disease. For further reading on
• Gain at all test velocities should be symmetrical VEMP testing, please see Chapter 12.
in normal function.
• The higher velocity (>100 deg/sec) step rotations Visual Perception Tests
better identify pathologically low VOR gains.
• Lower velocity step rotations are used to determine The subjective visual vertical (SVV) and subjective visual
the time constant and degree of compensation. horizontal (SVH) tests are quantified behavioral tests that
• Increased phase lead (sinusoid test) indicates determine the individual’s perception of v ertical or hori-
reduced time constant (UVH or BVH). zontal. The behavioral response is presumed to assess
• Time constant should be >10 sec. otolith function and the central pathways mediating gravi-
• Only examines the horizontal semicircular canal tational afference. The visual perception tests cannot be
and related afferents. used to uniquely detect saccular or utricular pathology .
• Abnormal high gain and/or long time constant With the SVV test, patients are ask ed to align a dimly lit
indicate cerebellar pathology (lost inhibition). luminous bar (in an otherwise dark ened room) with what
• Low-velocity step rotations should be symmetri- they perceive as being vertical. With the SVH test, patients
cal when central compensation has occurred. are asked to align a similar bar with what they perceive as
being horizontal. Subjects with normal vestibular function
VOR – vestibulo-ocular reflex; UVH – unilateral vestibular hypofunction; align the bar within 2.5 de g of true vertical or horizontal,
BVH – bilateral vestibular hypofunction whereas patients with v estibular pathology (central or
3970_Ch11_178-194 25/06/14 5:34 PM Page 190
Posturography
Recording the postural responses of someone with dizzi-
ness has important functional rele vance. Computerized
dynamic posturography (CDP) uses force plate technology Figure 11.12 The six condition sensory organization
test. Condition 1 does not alter any of the three primary
in measuring center of pressure (COP) under v arious
sensory contributors for balance. Condition 2 measures
challenging conditions. COP represents the location of all center of pressure with eyes closed. Condition 3 distorts
the floor reaction forces from the portions of the body visual feedback. Condition 4 distorts proprioceptive feed-
making contact with the force plate. CDP has its main back. Condition 5 distorts proprioceptive feedback and
value in objectifying postural responses, documenting eliminates vision. Condition 6 distorts visual and proprio-
ceptive feedback, forcing the subject to rely on vestibular
change, and identifying malingering.44 CDP, however, has
input.
no diagnostic capability.
In normal function, the maintenance of equilibrium
occurs with contribution from the long tracts of the corti- The motor component of the CDP commonly includes
cospinal and the shorter tracts of the corticobulbar systems the motor control test (MCT) and the postural e voked
(collectively called the pyramidal system), as well as tracts responses test. The MCT assesses postural responses to
originating from the brainstem nuclei and the basal ganglia sudden forward and backward translations of the support
(the extrapyramidal systems). The pyramidal system is surface. The amplitude of the translation varies depending
primarily responsible for controlling f ine, isolated, and on the test condition. During each translation, the latency
multipurpose volitional movement of the limbs, head, and to the onset of movements to recover the COP, the distri-
neck. The tracts originate in the cortex and run the length bution of weight through the le gs, and the amplitude of
of the spinal cord. The extrapyramidal system is respon- the responses are recorded (Fig. 11.14). It is expected that
sible for controlling large, yet cruder motion patterns that as the translational perturbation increases, so do the re-
are primarily reflexive and postural. These include the sponses. When abnormal, this test indicates possible
vestibulospinal and reticulospinal tracts. lesions within the musculosk eletal or long tracts of the
The CDP exam typically includes both a sensory and neurological system.
motor component. The sensory component involves a bat- Another part of the MCT measures the subject’s abil-
tery of postural control tests used to assess the patient’ s ity to adapt to a repeated stimulus. In this test, the platform
ability to integrate vision, vestibular, and somatosensory is tilted either up or down at the same amplitude. Normally,
inputs to maintain balance. This is typically done by ask- when the platform tilts up, muscle spindles from the gas-
ing subjects to stand for a period of time under six unique trocnemius muscle are stretched, triggering the monosy-
conditions (Fig. 11.12). The subject is ask ed to stand as naptic stretch reflex to the spinal cord and back.This leads
still as possible, while the area and velocity of the patient’s to contraction of the gastrocnemius, which is actually a
COP is recorded (Fig. 11.13). Abnormal patterns are rec- destabilizing response given the tilt of the platform. In time,
ognized based on results from the 6-item sensory e xam a subject should adapt to the stimulus and use less force
(Table 11-1). (smaller amplitude) to maintain balance (Fig. 11.15).
3970_Ch11_178-194 25/06/14 5:34 PM Page 191
Equilibrium Score
100
75
50
Figure 11.13 Sensory organization test report from
the Equitest. Shaded regions represent performance
F outside normal range. Bars outside the shaded region
25
N N N N A denote less sway; bars within the shaded area denote
/ / / / L more sway and abnormal performance. The patient
S S S S L was not able to maintain balance during the more
FALL
1 2 3 4 5 6 Composite challenging fifth and sixth conditions. Image courtesy
Conditions 63 of Natus Medical Incorporated.
Abnormal Test
Abnormal Pattern Condition Interpretation
Visual vestibular dysfunction 4, 5, 6 Suggests difficulty using visual and vestibular input or
vestibular input for stance
M M
L L
0 100 200 0 100 200
160 160
120 120
2 3 4 2 3 4 4 4
80 80
M L M L Composite M L M L
Left Right 165 Left Right
Adaptation Test
150 150
100 100
50 50
0 0
1 2 3 4 5 1 2 3 4 5
Figure 11.15 Adaptation test from Equitest. Shaded regions represent performance outside
normal function. Trials are plotted along the x-axis. This patient is not able to reduce force
production with repeated and identical toes up or toes down perturbations. Image courtesy
of NatusMedical Incorporated.
3970_Ch11_178-194 25/06/14 5:34 PM Page 193
Toes Up - 4 Degrees
625 µv
CH2 LL1 LL2
LL1 LL2 Time (ms) 112 223
Amp (µv) 16 17
CH2
Peak (µv) 387
Figure 11.16 Responses are
IEMG (µvS) 19.8
averaged from surface EMG of
the gastrocnemius (short and
CH3 SL1 SL2 ML1 ML2 medium latencies) and anterior
312 µv
tibialis (long latency) muscles
Time (ms) 36 50 85 118
SL2 during 20 pitch up platform per-
SL1
ML1 ML2 Amp (µv) 20 24 44 32 turbations. SL – short latency;
CH3
Peak (µv) 97 246 ML – medium latency; LL – long
IEMG (µvS) 0.7 4.0 latency. Four channels are used
to record data. Latency, ampli-
625 µv tude, magnitude, and integrated
CH4 LL1 LL2
EMG are presented in table for-
Time (ms) 113 220 mat. (Integrated EMG is defined
LL1 LL2
Amp (µv) 14 23 as the area under the curve
CH4
Peak (µv) 342 of the rectified EMG signal.)
IEMG (µvS) 17.3 Image courtesy of Natus Medical
Incorporated.
17. Jacobsen G, Shepard N. Balance Function Assessment and 32. Young ED, Fernandez C, Goldberg JM. Responses of
Management. San Diego, CA: Plural Publishing; 2008. squirrel monkey vestibular neurons to audio-frequency
18. Ferguson JH, Altrocchi PH, Brin M, et al. Assessment: sound and head vibration. Acta Otolaryngol. 1977;84:
electronystagmography: report of the Therapeutics and 352-360.
Technology Assessment Subcommittee. Neurology. 1996; 33. Murofushi T, Curthoys IS, Topple AN, et al. Responses of
46:1763-1766. guinea pig primary vestibular neurons to clicks. Exp Brain
19. Brandt T. Positional and positioning vertigo and nystagmus. Res. 1995;103:174-178.
J Neurol Sci. Jan 1990;95(1):3-28. 34. Murofushi T, Curthoys IS, Gilchrist DP. Response of
20. Fife TD, Tusa RJ, Furman JM, et al. Assessment: vestibu- guinea pig vestibular nucleus neurons to clicks. Exp Brain
lar testing techniques in adults and children: report of the Res. 1996;111:149-152.
Therapeutics and Technology Assessment Subcommittee 35. Iwasaki S, Chihara Y, Smulders YE, et al.The role of the
of the American Academy of Neurology. Neurology. 2000; superior vestibular nerve in generating ocular vestibular-
55:1431-1441. evoked myogenic potentials to bone conducted vibration
21. Oosterveld WJ, Greven AJ, Gursel AO, de Jong HA. Caloric at Fz. Clin Neurophysiol. Mar 2009;120(3):588-593.
vestibular test in the weightless phase of parabolic flight. Epub Feb 10, 2009.
Acta Otolaryngol. 1985;99:571-576. 36. Bohmer A, Mast F, Jarchow T. Can a unilateral loss of
22. Wit HP, Spoelstra AA, Segenhout JM. Barany’s theory is otolithic function be clinically detected by assessment of
right, but incomplete: an experimental study in pigeons. the subjective visual vertical? Brain Res Bull. 1996;41:
Acta Otolaryngol. 1990;110:1-6. 423-429.
23. Hood JD. Evidence of direct thermal action upon vestibular 37. Tabak S, Collewijn H, Boumans LJ. Deviation of the sub-
receptors in the caloric test: a re-interpretation of the data jective vertical in long-standing unilateral vestibular loss.
of Coats and Smith. Acta Otolaryngol. 1989;107:161-165. Acta Otolaryngol. 1997;117:1-16.
24. Jongkees LB, Philipszoon AJ. Electronystagmography. 38. Dieterich M, Brandt T. Ocular torsion and tilt of subjective
Acta Otolaryngol Suppl. 1964;189:SUPPL 189:1. visual vertical are sensitive brainstem signs. Ann Neurol.
25. Grossman GE, Leigh RJ, Abel LA, et al. Frequency and Mar 1993;33(3):292-299.
velocity of rotational head perturbations during locomo- 39. Min KK, Ha JS, Kim MJ, Cho CH, Cha HE, Lee JH.
tion. Exp Brain Res. 1988;70:470-476. Clinical use of subjective visual horizontal and vertical in
26. Das VE, Zivotofsky AZ, DiScenna AO, Leigh RJ. Head patients of unilateral vestibular neuritis. Otol Neurotol.
perturbations during walking while viewing a head-fixed Jun 2007;28(4):520-525.
target. Aviat Space Environ Med. 1995;66:728-732. 40. Baier B, Dieterich M. Ocular tilt reaction: a clinical sign
27. Goldberg JM, Fernandez C. Physiology of peripheral neu- of cerebellar infarctions? Neurology. Feb 10, 2009;72(6):
rons innervating semicircular canals of the squirrel mon- 572-573. No abstract available.
key, I: resting discharge and response to constant angular 41. Tabak S, Collewijn H, Boumans LJ. Deviation of the sub-
accelerations. J Neurophysiol. Jul 1971;34(4):635-660. jective vertical in long-standing unilateral vestibular loss.
28. Colebatch JG, Halmagyi GM. Vestibular evoked potentials Acta Otolaryngol. 1997;117:1-16.
in human neck muscles before and after unilateral vestibu- 42. Vibert D, Hausler R, Safran AB. Subjective visual vertical
lar deafferentation. Neurology. 1992;42:1635-1636. in peripheral unilateral vestibular diseases. J Vestib Res.
29. Halmagyi GM, Yavor RA, Colebatch JG. Tapping the head 1999;9:145-152.
activates the vestibular system: a new use for the clinical 43. Vibert D, Hausler R. Long-term evolution of subjective
reflex hammer. Neurology. 1995;45:1927-1929. visual vertical after vestibular neurectomy and labyrinthec-
30. Curthoys IS, Dai MJ, Halmagyi GM. Human ocular tomy. Acta Otolaryngol. 2000;120:620-622.
torsional position before and after unilateral vestibular 44. Cevette MJ, Puetz B, Marion MS, Wertz ML, Muenter
neurectomy. Exp Brain Res. 1991;85:218-225. MD. A physiologic performance on dynamic posturogra-
31. Kushiro K, Zakir M, Ogawa Y, et al. Saccular and utricular phy. Otolaryngol Head Neck Surg. Jun 1995;112(6):
inputs to sternocleidomastoid motoneurons of decerebrate 676-688.
cats. Exp Brain Res. 1999;126:410-416.
3970_Ch12_195-226 25/06/14 11:39 AM Page 195
CHAPTER 12
Otolith
Function Tests
G. Michael Halmagyi, MD ■ Ian S. Curthoys, PhD
The balance organs in the inner ear—the v estibular sen- proposed, including the measurement of horizontal, verti-
sory regions—are the gyros of the human body , and un- cal, and torsional eye movements as well as psychophys-
noticed, they function continuously in an almost perfect ical settings in response to linear accelerations produced
fashion, providing the brain with information about head on swings,1 sleds,2 centrifuges,3 tilt-chairs,4 and barbeque
position and head mo vement. Until these or gans fail, no spits.5 For an otolith function test to be clinically useful,
one really appreciates their significance in daily life, and it must be safe, practical, rob ust, and reproducible. The
anyone who has experienced an attack of vertigo will read- test also needs to be specif ic for, and sensitive to, otolith
ily verify their importance. The accelerations involved in dysfunction, particularly unilateral otolith hypofunction.
movements generate forces, and the biological gyros of In our view, only two means of testing otolith function—
the inner ear detect these forces: both the force imposed the subjective visual horizontal or vertical (SVH or SVV)
by gravity and the forces generated when we mo ve. The and the v estibular evoked myogenic potentials—fulfill
vestibular sensors are constructed in such a w ay that dif- these requirements. Both have been regularly used in our
ferent regions detect rotational forces and linear forces in clinical laboratories for many years, and what follo ws is
any direction. The brain synthesizes the information from in part a distillation of our own experience with these tests
these separate force detectors to pro vide a global inte- and of their scientific basis. The SVV and SVH are per-
grated summary of where a person is and how the person ceptual tests that are well known. The newer VEMP tests
is moving. This realization is of clinical importance, be- have been the subject of intense recent interest, and so we
cause it implies that disease affecting only one isolated re- devote detailed discussion of them below. Before consid-
gion of the inner ear has consequences for the o verall ering these tests, however, one must have some familiarity
integration of all the vestibular sensory input. In this chap- with the structure and function of the otoliths.
ter, we deal only with the otoliths, the structures that sense
linear forces, such as the force of gra vity or the “straight
line” acceleration experienced in a v ehicle accelerating
Anatomy
from a stop. The basic element of all vestibular transducers is the re-
The peripheral vestibular system is sensitive to both ceptor hair cell, which is similar in both the angular and
linear and angular accelerations: the semicircular canals the linear force-sensing systems (Fig. 12.1 A to E). The
(SCCs) sense angular acceleration, whereas the otoliths— SCCs and the otoliths detect these tw o different forces,
the saccule and the utricle—sense linear accelerations. not because of any differences in the intrinsic properties
Many different ways of testing otolith function have been of the hair cells themselv es but because of the w ay the
195
3970_Ch12_195-226 25/06/14 11:39 AM Page 196
A B
C E
Figure 12.1 The structure and function of the otolithic system. (A and B) Schematic
representation of the approximate orientation of the utricular and saccular maculae in the
head. Reid’s line is a standard reference line joining the center of the external ear and the
lower edge of the bony orbit. (C) Three drawings show how different linear force stimuli
affect the utricular receptor hair cells. The top diagram (1) shows the back view of a person
at rest with the cilia upright. Head tilts to the right (2) cause the cilia to be deflected to the
right; similarly, a linear acceleration to the left (3, arrow) causes a deflection of the cilia to
the right. (D) Schematic top-down view of a single receptor hair cell to show the polarization
pattern. The kinocilium is located at one extreme of the upper surface of the cell. If the
stereocilia are bent toward the kinocilium, as shown at the right, the receptor cell activity in-
creases. (E) Schematic illustration of the organization of a macular surface. The crystals of
calcium carbonate (the otoliths) are embedded in one side of the gelatinous otolithic mem-
brane, and the tips of the cilia project into the other side of this membrane. Forces cause
the membrane to slide so that the cilia are bent, thus stimulating the receptor cells.
structures that surround the hair cells are affected by the Each labyrinth consists of endolymph-f illed tubes
stimulating force. Each receptor cell has se veral, fine, and sacs containing receptor structures. The two special-
hairlike cilia projecting from the cell body into a gelati- ized sacs are the utricular sac and the saccular sac. A
nous overlying mass, the otolithic membrane. The plate of specialized receptor hair cells and connecti ve
longest cilium is called the kinocilium; it is located at tissue is contained within each of these sacs, and that
one side of the receptor cell and has a specialized cross- plate is called the macula. Each macula takes its name
sectional structure. The remaining cilia, the stereocilia, from the sac in which it is located, so that in each inner
are of uniform cross-sectional structure and are arranged ear there is a utricular macula and a saccular macula.
in a series of increasing height as the y approach the The terms utricle and saccule are often used to refer to
kinocilium. Linear accelerations such as tilts or transla- the utricular and saccular maculae, although strictly
tions cause the otolithic membrane to slide so that the speaking, utricle and saccule refer to the membranous
cilia of the receptor hair cells are bent (Fig. 12.1C). sacs that contain the maculae.
3970_Ch12_195-226 25/06/14 11:39 AM Page 197
The two maculae have similar gross features. Dense result is a highly ordered arrangement of polarization
crystals of calcium carbonate, the otoconia (Fig. 12.1E), vectors across each macula (Fig. 12.2). F or both macu-
are embedded on the outer (free) surf ace of the otolithic lae, the preferred directions of cells are opposite on each
membrane. On the inner surface of this membrane, the cilia side of a line in each macula. This line, and the area
of the hair cells project into the membrane. The density of around it, is called the striola. In the utricular macula,
the otolithic membrane itself is similar to that of the sur - the polarization vectors of the receptors point toward the
rounding endolymph, at 1.0 g/cm 3, but the density of the striola, whereas in the saccular macula the vectors point
otoconia is almost three times greater, at 2.7 g/cm3. These away from the striola (Fig. 12.2). At the band around the
two receptor structures are together called the otoliths, be- striola, there is a concentration of type I receptors, with
cause their construction is similar and because both detect large amphora-shaped cell bodies enveloped by a calyx
forces according to the same physical principle—namely, ending. These receptors are in contrast to the other cylin-
that an imposed linear force displaces the relatively dense drical (type II) receptors in the maculae periphery, which
otoliths embedded in the otolithic membrane. The otolithic have a cylindrical cell body and small bouton, af ferent
membrane then tends to slide across the surface of the mac- nerve terminals. Afferents synapsing on type I receptors
ula, displacing the cilia of the receptor hair cells and pro- respond very strongly to changes in linear acceleration,
ducing a change in hair cell resting membrane potential. and so play a major role in otolithic dynamic function:
The displacements of the otolithic membrane generated in afferents synapsing on type II receptors faithfully signal
this way by natural head movements in a 1-g environment maintained linear accelerations.7
are less than one micron.
The utricular and saccular maculae are approximately
perpendicular to each other. With the head erect, the utric-
ular macula is tilted by about 30 de grees (open anterior) Utricles
with respect to the horizontal plane of the head, whereas
the saccular macula is almost v ertical. These different
orientations mean that the receptors on each macula re-
spond maximally to forces in different directions. The sur-
face area of the human utricular and saccular maculae is
only about 4.2 mm 2 and 2.2 mm2, respectively. There are
about 33,000 receptor hair cells in the utricular macula and Striola
about 19,000 in the saccular macula. As in other sensory
systems, there is con vergence of receptors to primary
afferent nerves, so that only about 6,000 primary af ferent Anterior
nerve fibers supply the utricle, and only about 4,000 supply
the saccule.
Intracellular recordings from single isolated otolithic Figure 12.2 Schematic representation of the plates of
receptor hair cells subjected to controlled forces in pre- receptor hair cells in each macula. The arrows show the
preferred orientations of the receptor hair cells on each
cisely defined directions have shown that each receptor macula. On both maculae, hair cells have exactly oppo-
hair cell is polarized 6; that is, (1) it responds most site preferred orientation on either side of an imaginary
strongly to forces in one direction, and (2) as the direc- line (or band) called the striola—shown as a dashed
tion of the force de viates from that optimal direction, line. So, in each macula a linear acceleration will cause
so the response of the receptor declines. This optimum maximal activation of hair cells in one sector and maxi-
mal inhibition of hair cells with the opposite preferred
direction is referred to as the cell’s polarization vector. orientation. Uchino’s group has shown that central in-
This physiological polarization corresponds to a mor- hibitory interaction between afferents from the two
phological polarization, in that receptor cells respond opposing sides acts to enhance sensitivity—cross-striolar
optimally when the imposed force shears the stereocilia inhibition.8 The amphora-shaped type I receptors are
toward the kinocilium. Receptor hair cells are arranged concentrated in the area of the striola, and afferents
from these have an irregular resting discharge and a
in a regular fashion across each macula so that the di- strong response to changes in linear acceleration7 and
rection of the kinocilium of each cell shifts in direction appear to have a major role in generating otolithic
by only a small amount relati ve to its neighbors. The responses to dynamic stimulation—such as VEMPs.
3970_Ch12_195-226 25/06/14 11:39 AM Page 198
Primary afferent neurons synapse on a number of ad- than the decrease in firing rate for the same
jacent receptor hair cells, so that some of the precision of magnitude of acceleration in the opposite,
spatial tuning of the indi vidual receptors is lost: af ferent disfacilitatory direction.
fibers respond to forces over a greater range of directions 5. The spatial distribution of the directional
than the individual receptors. Each afferent fiber exhibits preferences of all otolithic afferents is not
a preference for forces in a particular direction, reflecting uniform. In the squirrel monkey, for example,
the preferred orientation of the receptor hair cells on which there is a directional preponderance so that
the fiber synapses. For afferent fibers, just as for receptors, more otolith afferents prefer ipsilaterally di-
as the force direction deviates from the optimal direction, rected accelerations to contralaterally directed
the fiber’s firing rate declines. Utricular afferents in gen- accelerations. There is 3:1 preponderance of
eral show a preference for forces directed horizontally utricular afferents preferring ipsilateral accel-
across the plane of the macula—in other words, for later- erations, whereas there is about a 1:1 distribu-
ally directed forces—and similarly , saccular af ferents tion of saccular afferents preferring up-and-
show a preference for forces directed vertically across the down accelerations.
plane of the macula.9
The dynamic response characteristics of regular and
irregular otolithic afferents are quite different and indeed
Primary Otolithic almost complementary. Regular neurons show a poor
Afferents—Physiology response to changes in linear acceleration and little adap-
tation to maintained accelerations. Irregular afferents fire
Recordings from primary otolithic afferent neurons in the
vigorously during changes in linear acceleration b ut
vestibular nerve of experimental animals show a number
adapt rapidly (but not completely) for a maintained stim-
of important characteristics (for a review see Goldberg and
ulus.9,11,12 Bone conducted vibration (BCV) consists of
Fernandez.10
many rapidly changing linear accelerations.13,14 Record-
1. Primary otolithic afferents have a resting dis- ings of primary vestibular neurons in guinea pigs sho w
charge rate. They fire at about 50 spikes per that low-intensity 500-Hz BCV activates a high propor-
second even when there is no imposed force tion of otolith irregular neurons from the striolar region
stimulus. of both the utricular and saccular maculae, and man y
2. The spontaneous activity is highly regular in are activated with great sensitivity at very low stimulus
some afferents, whereas in others it is highly values—thresholds of around 0.1g.13-16
irregular. In addition, there is a continuum of BCV at 500 Hz acti vates very few semicircular
regularity between these extremes. Physiologi- canal neurons and then only at high intensities. 13,14
cal responses are closely related to this dimen- However, our recent results show that as the frequency
sion of regularity. Irregular neurons show a is decreased to 100 Hz, canal neurons are also activated
strong response to changes in linear accelera- by vibration (Curthoys 2013, unpublished results). Air-
tions (jerks), whereas regular neurons show conducted sound (A CS) evokes neural responses in
a faithful response to maintained linear many of these same neurons similar to those evoked by
accelerations. BCV, although the stimulus intensities required are very
3. Afferents have a functional polarization high (60 to 80 dB abo ve auditory brainstem response
vector. This means that linear accelerations [ABR] threshold; around 120 to 130 dB sound pressure
oriented in one particular direction will most level [SPL]).14,15 It is still not known just how this trans-
effectively activate the afferent neuron. As duction occurs, but it seems that the pumping of the
the direction of the imposed acceleration is stapes is sufficient to generate displacements of the cilia
deviated from this optimum direction, so the of the receptor cells. Most, but not all, neurons activated
response of the afferent neuron declines. If by BCV can be acti vated by ACS.14 Because 500-Hz
the stimulus is directed exactly opposite to the BCV and ACS are relatively specific stimuli for otolith
preferred direction, then the firing of the cell irregular neurons,13 so myogenic responses to ACS and
is maximally suppressed. BCV have been used to index dynamic otolith function
4. The afferents show a marked asymmetry in in the clinic. 17,18 It is lik ely that responses to lo wer
bidirectional sensitivity. This characteristic frequency stimulation may be contaminated by canal ac-
results in an increase in firing rate for acceler- tivation. This means that even at the level of the afferent
ation in the excitatory direction that is larger neurons leaving the macula, functional specialization
3970_Ch12_195-226 25/06/14 11:39 AM Page 199
has already taken place, in that dif ferent temporal and branches of the vestibular nerve. As we explain below, this
spatial aspects of the force stimulus are being signaled differential vulnerability has been used to identify utricular
by these different parallel pathways. as opposed to saccular function. The schematic f igure
(Fig. 12.3) shows that (1) afferents from the horizontal and
anterior semicircular canals and the utricular macula course
Central Projections in the superior di vision of the v estibular nerve,19,20 and
The projections of otolith neurons are crucial in interpret- (2) most saccular afferents course in the inferior vestibular
ing clinical otolith tests. In addition, the organization of the nerve, except the branch from the small rostral area of the
peripheral neural projections is especially important, be- saccular macula (the “hook” of the saccular macula) called
cause disease (neuritis) may be restricted to indi vidual Voit’s nerve,21 which travels in the superior v estibular
Figure 12.3 Schematic representation of the course of the afferents from each sensory
region of the vestibular labyrinth. The text in the figure describes new clinical tests. Tests of
each sense organ of the vestibular labyrinth and the columns show the pattern of responses
associated with each major disease category. oVEMP is the ocular vestibular-evoked myogenic
potentials; cVEMPs is the cervical vestibular-evoked myogenic potentials (described below).
Fz is the location on the forehead in the midline at the hairline. Reprinted from Curthoys22
“The interpretation of clinical tests of peripheral vestibular function.” Laryngoscope,
122(6):1342-1352, DOI 10.1002/lary.23258, with permission from John Wiley and Sons.
3970_Ch12_195-226 25/06/14 11:39 AM Page 200
nerve. In primates, Voit’s nerve constitutes only about 10% Function of Otolithic Input
of all the afferents from the saccular macula. 23 So, there
are some saccular f ibers coursing in the superior nerv e, Electrical stimulation of the utricular nerv e in the cat
although the evidence is that this is not a large contingent. causes a distinct pattern of e ye movement: a torsion of
Primary otolithic afferent neurons project to second- both eyes so that the upper poles of the e yes roll away
ary vestibular neurons mainly in the lateral, medial, and from the side being stimulated 26 because of activation of
descending vestibular nuclei. In some re gions, these the contralateral inferior oblique and ipsilateral superior
otolithic projections show considerable overlap with the oblique muscles. Complementing that f inding, studies
projections of horizontal SCC af ferents. The predomi- have shown that unilateral section of the vestibular nerve
nant response of lateral vestibular nucleus neurons is an causes a torsion of both eyes toward the operated side.5,27
increase in firing rate in response to ipsilateral tilts. Just Bone conducted vibration elicits eye movements in guinea
as horizontal SCC neurons in the medial v estibular pigs and humans that are analogous to those produced by
nucleus are interconnected to the contralateral medial electrical stimulation of the utricular nerve.28,29 In natural
vestibular nucleus via commissural f ibers, which play head movements, the otoliths are acti vated and generate
a major role in the neural operation of the system, so compensatory eye and postural responses. F or example,
otolith-responsive neurons are interconnected to similar tilting the head to ward one shoulder causes the gra vity
neurons in the opposite vestibular nucleus.8 vector to activate particular regions of the utricular and
However, the interconnections in the otolithic sys- saccular maculae, and as a consequence, the eyeball torts
tem are indirect, and the functional mode of the bilateral (or rolls) around the visual axis in a compensatory direc-
interconnections is predominantly excitatory rather than tion. At the same time, there is a complex pattern of acti-
inhibitory, as is the case with the horizontal SCC system. vation of neck and trunk muscles acting to oppose this
Commissural interaction occurs in the otolithic and the challenge to the equilibrium of the head. The degree of
horizontal canal system. 8 Some cells in each v estibular this countertorsion or ocular counter-rolling is only about
nucleus can be activated both by SCC stimulation and by 10% of the head tilt, but it does depend on otolith function
otolithic.24,25 This is not too surprising—nodding the head because subjects without otoliths do not sho w such
causes activation of both semicircular canals and sectors counter-rolling.6
of both otoliths, and the cooperative interaction of canal
and otolith neurons will generate a smooth compensatory Clinical Tests of Otolith Function
response. These convergent neurons integrate linear and
Static Otolith Tests
angular acceleration input and thus help maintain posture
and equilibrium. However, the existence of these conver- Otolith primary afferents respond to maintained linear ac-
gent neurons means that pathw ays conveying otolith celerations (such as head tilts re gravity) and a number of
signals are not specif ic; many neurons can be acti vated clinical tests examine the responses of patients to main-
by either canal or otolith stimulation. tained linear accelerations. 30,31 We refer to these as tests
The pathways from the otolithic re gions of the of “static” otolith function to contrast them to the tests of
vestibular nuclei to the ocular motor nuclei are poorly “dynamic” otolith function, such as the VEMP tests de-
understood. Trochlear motoneurons can be disynaptically scribed below. Maintained head tilt activates otolith recep-
activated by electrical stimulation of the utricular nerv e, tors and causes both e yes to roll around the line of sight
and increasing attention is being paid to tw o midbrain and maintain that rolled position during the maintained
regions close to the oculomotor nuclei—the interstitial (i.e., static) head tilt. Conversely, if there is unilateral loss
nucleus of Cajal and the rostral interstitial nucleus of the of otolith function, both eyes roll around the line of sight
medial longitudinal fasciculus—that integrate inputs for and adopt a maintained rolled-eye position—rolled toward
torsional and vertical eye movement responses produced the lesioned ear.32 Unilateral otolith loss was probably the
by otolithic stimulation. In particular, it seems that the in- cause of the ocular tilt reaction because of an inadvertent
terstitial nucleus of Cajal has a major role in inte grating vestibular lesion in a patient under going stapes surgery.33
otolithic input for coordinated eye and head responses to On recovery, the patient showed a distinctive pattern of re-
the linear forces detected by the otoliths. The neural sub- sponses that have been taken to indicate otolith function—
strate for the compensatory postural movements required the ocular tilt reaction: (1) both eyes adopted a maintained
by a linear acceleration are mediated by otolith-spinal rolled position around the line of sight toward the affected
projections, the lateral vestibulospinal tract arising in the side; (2) there was a small maintained roll-tilt of the head
lateral vestibular nucleus and the medial v estibulospinal toward the affected side; and (3) there w as a maintained
tract arising in the medial vestibular nucleus. skew deviation between the two eyes—the visual axis of
3970_Ch12_195-226 25/06/14 11:39 AM Page 201
the eye on the side of the lesion was lower in the orbit than the bar toward the UVD side, it is not to null a percei ved
the visual axis of the eye on the intact side. tilt of the bar with the body, toward the intact side. Another
In human subjects with the e yeball in a rolled posi- possible mechanism of the SVH offset is a torsional devia-
tion, visual perception changes in accordance with this new tion of the eyes as a part of the ocular tilt reaction. The oc-
torsional position34 e.g., when a patient with maintained ular tilt reaction is a postural synkinesis consisting of head
ocular torsion is asked to set a visible line—in an otherwise tilt, conjugate ocular torsion, and skew deviation, all toward
darkened room—to where they perceive gravitational hor- the same side. Some patients demonstrate a florid, tempo-
izontal (or vertical) to be, they set it in a direction that is rary, ipsilesional tonic ocular tilt reaction after a unilateral
aligned with their rolled eye position. This test is called the peripheral vestibular lesion,33-51 and others just a partial one
subjective visual horizontal (SVH) or subjective visual ver- with ocular torsion and skew deviation.51-55
tical (SVV).3,29,34-38 Systematic deviations in SVV or SVH We measured torsional ocular position and SVH
greater than about 2 de grees, in patients with peripheral before and after UVD 27 and found that after UVD, there
vestibular dysfunction, are tak en to indicate static otolith was invariably an ipsilesional deviation of torsional ocular
dysfunction. position so that the 12 o’clock meridian of each eye was in-
variably rotated toward the side of the UVD (Fig. 12.4). One
Subjective Visual Horizontal week after UVD, there was up to 15 degrees of ipsilesional
ocular torsion and a close correlation (r = 0.95) between the
or Vertical Testing magnitude of the ocular torsion and the of fset of the SVH
of Otolith Function (Fig. 12.5). Furthermore, the ocular torsion gradually re-
solved with a temporal pattern identical to that of deviation
Peripheral Vestibular Lesions of the SVH. One month after UVD, both the ocular torsion
A normal subject sitting upright in a totally dark ened and the tilting of the SVH were at half the 1-week v alue.
room can accurately set a dimly illuminated bar to within A slight but significant ipsilesional ocular torsion of 4 to
1 degree of the true gra vitational vertical or horizontal. 5 degrees is a permanent le gacy of UVD for Ménière’ s
Friedmann35,36 was the first to show that patients with disease.27 After acute UVD in frogs,56 dogs,57,58 cats,57 and
various unilateral vestibular lesions set such a bar so that horses,59 there is head torsion, which follows the same time
it was no longer aligned with the gravitational vector but course as conjugate eye torsion in humans.
was consistently tilted toward the side of the lesion (see The offset of the SVH is caused by ocular torsion as
Case Study 21-1). We studied the ability of patients with part of the ocular tilt reaction, so that maintained ocular tor-
Ménière’s disease to set such a light-bar to the visual hor- sion can be seen as the equivalent in the otolithic system of
izontal before and after unilateral v estibular neurectomy the spontaneous nystagmus in the semicircular canal sys-
(UVD).3,27 Before UVD, the patients’ settings were within tem. Torsional ocular position and, therefore, the setting of
the normal range. After UVD, patients invariably set the the SVH, depend on relative resting activity in the left and
gravitationally horizontal bar so that it was actually tilted right vestibular nuclei. So, as the brainstem compensates
toward the lesioned side, by 15 de grees or more; the y for the UVD, the SVH returns to ward normal, although a
did this because they actually saw the gravitationally small offset of the SVH appears to be a permanent stigma
horizontal bar as being tilted to ward the intact side. of UVD.27 Therefore, in analogy with spontaneous nystag-
Although their settings of the bar gradually returned to- mus, a return of the SVH to ward normal is ine vitable
ward the true or gravitational horizontal, the settings were whether or not the labyrinth reco vers. It should be noted
still tilted by a mean of 4 de grees 6 months or more that offsets of torsional ocular position and of the SVH
after UVD. Thus a slight ipsilesional tilt, or offset, of the can also occur with SCC stimulation—that is, together with
SVH was a permanent le gacy of a UVD procedure for horizontal or torsional nystagmus.60,61 Nonetheless, ocular
treatment of Ménière’s disease. These findings keep being torsion in the absence of spontaneous n ystagmus is likely
confirmed.39-50 to be otolithic, because it represents a tonic offset of the dy-
What could be the cause of this perceptual error? Is it namic ocular counter-rolling mechanism, which is under
an offset of the internal representation of the gra vitational utricular control (Fig. 12.6).4,62
vertical as a result of the profound asymmetry in otolithic
input to the vestibular nuclei that must occur after UVD?
Central Vestibular Lesions
Arguing against this mechanism is the observation that de-
spite the UVD, the patients do not feel that their own bodies Patients with acute brainstem,63,64 cerebellar,65 and corti-
are tilted, but on the contrary, feel themselves to be normally cal66 lesions (ischemic or demyelinating, 63,66) can show
upright, even in the dark. In other words, although they tilt offsets of the SVH or SVV and of torsional eye position.67
3970_Ch12_195-226 25/06/14 11:39 AM Page 202
Figure 12.4 Ocular torsional position before and after unilateral vestibular deafferentation
(uVD). Fundus photographs of the left and right eyes of a patient before (top row) and one
week after (bottom row) right vestibular neurectomy. After the operation, there is tonic
rightward torsion of the 12 o’clock meridian of each eye toward the patient’s right side. The
torsion measures 17 degrees in the right eye and 15 degrees in the left eye. When the pa-
tient was asked to set a luminous bar to the perceived visual horizontal in an otherwise dark-
ened room, he set the bar tilted down on his right side by 14.2 degrees when viewing with
the right eye and 15.1 degrees when viewing with the left.
Patients with lo wer brainstem lesions in volving the the offset of the SVV. The relationship between the SVV
vestibular nucleus (e.g., lateral medullary inf arcts) offset and ocular torsion is not as tight as with peripheral lesions
the SVV toward the side of the lesion, whereas patients but is nonetheless present. 67 In patients with peripheral
with upper brainstem lesions involving the interstitial nu- vestibular lesions, the ocular torsion and the consequent
cleus (medial thalamic infarcts) or with cerebellar lesions setting of the SVV are almost the same in each eye; in con-
involving the dentate nucleus have offsets of torsional eye trast, there can be significant left eye–right eye differences
position and of the SVV away from the side of the lesion. in both ocular torsion and the SVV in patients with central
In most patients, there is a de viation of torsional ocular vestibular lesions. For example, in patients with lateral
position (also called cyclotorsion) in the same direction as medullary infarcts, the excyclotorsion of the ipsilesional
3970_Ch12_195-226 25/06/14 11:39 AM Page 203
Figure 12.6 Diagrammatic explanation of the possible causes of the changes in torsional
eye position after unilateral vestibular deafferentation (uVD). Normally, second-order afferents
from the vestibular nucleus send excitatory projections to the contralateral inferior oblique and
ipsilateral superior oblique muscles, as well as to the contralateral inferior rectus and ipsilateral
superior rectus muscles (not shown). Left uVD, as shown here, produces reduced tonic activity
in the contralateral inferior oblique (and inferior rectus, not shown) muscles, so that the con-
tralateral eye intorts; it also produces reduced activity in the ipsilateral superior oblique (and
superior rectus, not shown) muscles, so that the ipsilateral eye extorts. One presumes that,
through commissural disinhibition, the left uVD increases tonic activity in the contralateral,
right vestibular nucleus, and therefore increases tonic activity of the contralateral superior
oblique muscle, which also produces intorsion of the contralateral eye. IV = trochlear nucleus;
MLF = medial longitudinal fasciculus. (Courtesy of Ms. Agatha Brizuela.)
3970_Ch12_195-226 25/06/14 11:40 AM Page 204
eye can be larger than the incyclotorsion of the contrale- offset of the SVH or the SVV indicates acute unilateral
sional eye. otolithic hypofunction from a lesion of the end-or gan,
the vestibular nerve, or the vestibular nucleus on the side
to which the patient offsets the bar, above the vestibular
Clinical Significance nucleus on the side opposite to which the patient offsets
Standardized measurement of the SVH, with a dim the bar. The greater the offset, the more acute the lesion;
light-bar in an otherwise totally darkened room, can give a small permanent de viation of the SVV might be a
valuable diagnostic information. In some laboratories, permanent legacy of both central 72 and peripheral46
patients are asked to set a bar to the SVV , but we find vestibular lesions. The SVH test is the single most useful
that most patients have a better intuitive understanding investigation in the acute phase of suspected v estibular
of the horizontal than of the vertical and that the settings neuritis: SVH is of fset, sometimes by more than
of the vertical might not be the same as those of the hor- 20 degrees, always toward the side of the lesion. 43,44
izontal.69,70 In any case, in order for the test to be valid, SVH testing can also be used to follo w the progress of
either the room must be totally dark apart from the light vestibular loss and compensation after intratympanic
bar or there must be some other w ay, such as with a gentamicin treatment for Ménière’s disease.42,45 Offsets
Ganzfeld stimulator or a rotating dome,63 or even a sim- of the SVH seem to correlate better with abnormalities
ple bucket, to exclude all visual cues. 70,71 A significant in oVEMPS than in cVEMPs.73
Continued
3970_Ch12_195-226 25/06/14 11:40 AM Page 206
−
−
−
−
− −
− −
Figure 12.7—cont’d (B) Electronystagmogram and caloric test from the same patient.
There is minimal left-beating gaze-evoked nystagmus in darkness (slow-phase velocity
<1 deg/sec). Bithermal caloric tests show symmetrical slow-phase velocities from each ear.
These findings indicate normal lateral semicircular canal function.
3970_Ch12_195-226 25/06/14 11:40 AM Page 207
Figure 12.7—cont’d (C) Subjective visual horizontal (SVH) from the same patient. The
patient makes 10 settings of the SVH at his own speed, with each eye open and then with
both eyes open. There is a highly significant offset of more than 5 degrees to the left (the
side of the hearing loss). Normal subjects can set the horizontal to within 2 degrees of the
gravitational horizontal.
Continued
3970_Ch12_195-226 25/06/14 11:41 AM Page 208
The Ocular VEMP—oVEMP 500-Hz ACS14-16,81,94 and that saccular neurons also re-
In healthy subjects, short tone b ursts of 500 Hz of either spond to both these stimuli.15,16 So, the response to ACS
high-intensity ACS or moderate BCV result in a stimulus- may indicate either saccular or utricular function depend-
locked, short-latency, negative myogenic potential—the ing on which response, oculomotor or cervical, is being
oVEMP—to be recorded by surface electrodes beneath the measured. Recently, we have found that the stimulus fre-
eyes. The first negative (excitatory) component of which quency is important for this otolithic specificity—if low-
at a latency of about 10 msec, is called oVEMP n10. 83-86 frequency (100-Hz) stimuli are used, canal af ferents and
This component probably indicates primarily the myo- otolithic afferents can be activated with high intensity vi-
genic potential of the inferior oblique. 87 Stimulation bration. However, at 500 Hz only otolith neurons are acti-
of one ear by ACS also elicits oVEMP n10 responses vated (Curthoys et al 2013, unpublished data). So, for
beneath the contralateral eye; however, the sound inten- clinical testing of otolith function, 500 Hz is an almost
sities needed are very high, and the n10 potentials toACS ideal choice.
are typically small. 88-90 In addition to the contralateral The evidence for differential projections of utricular
n10, in some subjects ACS also produces small potentials and saccular maculae is o verwhelming. Uchino’s re-
beneath the ipsilateral e ye,89 but it is the amplitude of search has shown that saccular neurons ha ve a strong
the oVEMP n10 beneath the contralateral eye that is of projection to neck muscles 95-98 and a weak projection
diagnostic value. ACS has the major disadv antage that to the oculomotor system. 99-101 Utricular afferents have
conductive hearing loss renders the test results meaning- a strong projection to eye muscles.101,102 On the basis of
less. The oVEMP is a crossed, excitatory, ascending, many years of research on otolith-ocular and otolith-
utriculo-ocular response.83 spinal projections, Uchino and K ushiro summarize the
differential projections of utricular and saccular afferents
The Interpretation of oVEMP as follows:
and cVEMP Results “Consequently, the neural connections in the sacculo-
The oVEMP and cVEMP tests are v estibular tests, be- ocular system are relatively weak compared to the neu-
cause patients who are totally deaf and cannot hear the ral connections in the utriculo-ocular and sacculo-collic
stimulus show the myogenic potentials to ACS or BCV. systems.”103
Conversely, patients tested after systemic gentamicin
with probably absent vestibular function bilaterally, but
Differentiating Utricular from Saccular
with residual hearing, can hear and feel the stimuli b ut
Function
do not show the myogenic potentials.84,85 In patients with
complete unilateral vestibular loss following vestibular One important source of data conf irming that oVEMPs
schwannoma removal, there is a reduced or absent to 500 Hz probe utricular function and cVEMPs to
oVEMP n10 from beneath the contralateral e ye (as the 500 Hz probe saccular function comes from the pattern
subject looks up) in response to Fz BCV or ACS stimu- of responses of patients with vestibular neuritis, in which
lation of the af fected ear88,91-93 and reduced or absent hearing is not af fected but vestibular function is
cVEMP p13-n23 from o ver the ipsilateral SCM in re- affected.104-109 These patients fall into three main cate-
sponse to Fz BCV. gories: neuritis may affect the entire vestibular nerve, just
In light of the evidence that 500-Hz sound and vibra- the superior division, or just the inferior di vision. The
tion selectively activate otolithic afferents rather than canal consequence of neuritis is that afferents have reduced or
afferents, together with the e vidence of the dif ferential absent function, and that loss of function manifests itself
strengths of the neural projections of the utricle and sac- as a distinctive pattern of deficits on stimuli that activate
cule, Curthoys put forward the hypothesis that measuring various vestibular sense or gans. The results can be
oculomotor responses to 500-Hz ACS and 500-Hz Fz understood in terms of the anatomical projections of the
BCV probes predominantly utricular function, whereas various vestibular sense or gans within the v estibular
measuring neck muscle responses to these stimuli probes nerve shown in Figure 12.9 and their differential projec-
predominantly saccular function (Fig. 12.9). 18 In other tion to oculomotor or cervical regions.
words, it is possible to probe utricular and saccular func- If the neuritis affects the entire vestibular nerve, one
tion separately because of their differential neural projec- would expect a pattern of VEMP deficits matching those
tions, not because the stimuli (ACS and BCV) are specific of a patient after surgical removal of one entire vestibular
selective stimuli for different otolithic sensory regions, be- nerve—loss of ipsilesional cVEMPs and contralesional
cause they are not. 15 The physiological evidence shows oVEMPs (see Fig. 12.9; see also Fig. 12.3). Patients show-
that utricular neurons respond to both 500-Hz BCV and ing such a pattern akin to that of total unilateral vestibular
3970_Ch12_195-226 25/06/14 11:41 AM Page 211
IO IO IO IO
III III
MLF MLF
Right vestibular Left vestibular Right vestibular Left vestibular
nuclei nuclei Utricular nuclei nuclei Utricular
macula macula
Saccular Saccular
macula macula
loss are diagnosed as a total unilateral v estibular neuritis n10 potentials beneath the contralateral eye, because all af-
(TVN).88,110,111 ferents from the utricular macula project in the affected su-
The schema shown in Figure 12.9 implies that patients perior vestibular nerve,19 and the oVEMP n10 is a crossed
with probable unilateral superior vestibular neuritis (SVN) response.83,92 This was demonstrated by Iw asaki et al 92
would have normal cVEMPs, because the saccular afferents (Fig. 12.10) and confirmed in a major study of 133 patients
in the inferior vestibular nerve will not be af fected. How- with SVN in response to 500-Hz Fz BCV.111,112 In response
ever, these patients should have reduced or absent oVEMP to 500-Hz Fz BCV, SVN patients had symmetrical cVEMPs
3970_Ch12_195-226 25/06/14 11:41 AM Page 212
LE LE
Figure 12.10 Examples of oVEMP re-
sponses to bone-conducted vibration at
Fz in healthy subjects (A) and a patient RE RE
with a complete unilateral vestibular
loss (B). In the patient, there is no de-
tectable oVEMP n10 beneath the con- – –
tralesional eye, whereas the oVEMP n10 5 µV 5 µV
beneath the ipsilesional eye is of normal + +
amplitude. (C) The asymmetry ratios
(ARs) for Fz stimulation for healthy sub- 0 10 20 30 40 50 0 10 20 30 40 50
jects (open circles), patients after unilat- A ms B ms
eral vestibular loss (uVL) (crosses), and
patients diagnosed with unilateral supe-
uVL n = 11
rior vestibular neuritis (closed circles). Sup vest neuritis n = 13
The average AR for healthy subjects is Healthy subjects n = 67
about 11%, and all 67 healthy subjects
oVEMP n10 Average Asymmetry Ratio (%)
but asymmetrical oVEMP n10s with the contralateral n10 There is a proviso: in patients with probable inferior
being reduced as predicted.113,114 vestibular neuritis, the superior vestibular nerve is proba-
Patients with probable unilateral inferior vestibular bly intact. So, it is possible that the function of the afferent
neuritis (IVN) as shown by reduced or absent ipsilateral fibers from the “hook” re gion of the saccular macula is
cVEMPs in response to 500-Hz Fz BCV, but with nor- preserved, because these fibers travel in Voit’s nerve and
mal superior nerve function as shown by normal calorics merge with the superior vestibular nerve.20-22 Could these
and by horizontal head impulse testing, would have con- “hook” afferents be responsible for the oVEMP response?
tralateral oVEMP n10 responses that are not detectably That is not a likely possibility (1) because of the relatively
affected. It has been argued that the utricular afferents, small contingent of afferent fibers from the hook re gion
coursing in the superior v estibular nerve, will not be of the saccular macula, 23 (2) because sacculo-ocular path-
affected by IVN. This prediction has recently been ways are polysynaptic, 95,103 and (3) the oVEMP n10 is a
demonstrated in a major study of 59 patients with prob- sharply defined potential at a v ery short latency and ap-
able inferior vestibular neuritis in which, to exactly the pears to be caused by the EMG generated by a synchro-
same stimulus, the cVEMPs were asymmetrical but the nous volley of action potentials arriving at the extraocular
oVEMPs were symmetrical. 115 That result conf irms muscles. It is unlik ely to be caused by action potentials
other independent e vidence of the ef fect of IVN on down a weak polysynaptic pathway95 from the very small
VEMPs.111,116 This is strong evidence that saccular dys- bundle of afferent fibers innervating the hook region of the
function does not affect oVEMPs. saccular macula.
3970_Ch12_195-226 25/06/14 11:41 AM Page 213
Methods—Recording VEMPs source is correctly calibrated and that the background level
of rectified sternocleidomastoid EMG activation is mea -
For details, see Rosengren et al.116 Brief (0.1 msec), loud sured. Two reasons why the cVEMPs could be absent or
(95 db abo ve normal hearing le vel [nHL]), monaural less than 50 µV in amplitude are a conductive hearing loss
clicks74,118 or short tone-b ursts119,120 produce a lar ge and inadequate contraction of the sternocleidomastoid
(60 to 300 µV), short-latency (8 msec), inhibitory potential muscles.
in the tonically contracting ipsilateral sternocleidomastoid For clinical testing, three superimposed averages of
muscle. The initial positive-negative potential, which has 128 stimuli for each ear in response to clicks of 100-dB
peaks at 13 msec (p13) and at 23 msec (n23), is abolished intensity are usually sufficient. The test cannot be done
by selective vestibular neurectomy but not by profound on uncooperative or unconscious patients. The patient
sensorineural hearing loss. In other w ords, even if the lies down and activates the sternocleidomastoid muscles
patient cannot hear the clicks, there can be normal for the averaging period by keeping the head raised from
p13-n23 responses. Later components of the e voked re- a pillow. An alternative method—useful, for e xample,
sponse do not share the properties of thep13-n23 potential in patients with painful neck problems—is to ask the pa-
and probably do not depend on v estibular afferents. tient to turn the head, which continues to rest on the
Failure to distinguish between these early and late com- pillow, to one side. It is then possible to measure the
ponents could explain why earlier work along similar lines VEMP in the sternocleidomastoid muscle on the side
was inconclusive. opposite to the rotation.
For the preceding reasons, we called the p13-n23 The peak-to-peak amplitude of the p13-n23 potential
response the vestibular-evoked myogenic potential from each side can be e xpressed relative to the level of
(VEMP)—more recently known as the cVEMP (cervical background mean-rectified EMG to create a ratio that
VEMP)—to distinguish it from other VEMPs. Unlike a largely removes the effect of differences in muscle activity.
neural-evoked potential such as the brainstem auditory- More accurate, but more time-consuming, correction can
evoked potential, which is generated by the synchronous be made by making repeated observ ations with differing
discharge of nerve cells, the cVEMP is generated by syn- levels of tonic acti vation.118 One ear is best e valuated
chronous discharges of muscle cells or, rather, motor units. through comparison of the amplitude of its cVEMP with
Being a myogenic potential, the cVEMP can be 500 to that of the cVEMP from the other ear. We take asymmetry
1,000 times larger than a brainstem potential,121 for exam- ratios of 2.5:1 to be the upper limit of normal—a v alue
ple, 200 µV rather than less than 1 µV. Single motor unit similar to that obtained by others. 130,131 Minor left-right
recordings in the tonically contracting sternocleidomastoid differences in latency commonly occur and might reflect
muscle show a decreased firing rate synchronous with the differences in electrode placement over the muscle or dif-
surface cVEMP.122 fering muscle anatomy. VEMP amplitude declines after
The amplitude of the cVEMP is linearly related age 60 years.132
to the intensity of the click and to the intensity of stern-
ocleidomastoid muscle activation during the period of
averaging, as measured by the mean rectif ied elec- Methods—oVEMPs
tromyography (EMG) value.118,123 Inadequate sternoclei- For details, see Iwasaki et al.84 Subjects lie supine on a
domastoid contraction produces spurious results by bed with the head supported on a pillow but positioned
reducing the amplitude of the cVEMP.124 A conductive so that the head was horizontal or pitched slightly nose
hearing loss abolishes the response by attenuating the in- down. After thorough cleaning of the skin beneath
tensity of the stimulus 125 (see Fig. 12.9). In such cases, the eyes with alcohol wipes, surface EMG electrodes are
the cVEMP can be elicited by a tap to the forehead,75 by applied to record the responses from beneath both eyes,
a bone vibrator,126-128 or by a direct current applied to as shown in Figure 12.11. F or each eye, the active (+)
the mastoid bone.129 electrode is placed on the infra-orbital ridge about 1 cm
below the lo wer eyelid, and the reference electrode
is placed about 2 cm below that first electrode. The elec-
Methods—cVEMPs trodes are aligned with the center of the pupil as the sub-
Any equipment suitable for recording brainstem auditory ject looks up at a distant tar get in the midline. The
potentials will also record VEMPs. Because the amplitude self-adhesive pads around the electrode are cut to allow
of the cVEMP is linearly related to the intensity of both this very close electrode placement, taking care that
the click and of sternocleidomastoid activation during the no electrical bridge forms between the tw o closely
period of averaging, it is essential to ensure that the sound juxtaposed electrodes.
3970_Ch12_195-226 25/06/14 11:41 AM Page 214
electrode placement or low gaze can negate the oVEMP; or large vestibular aqueduct143 can be differentiated from
insufficient neck muscle tension can ne gate the cVEMP. those caused by middle ear disease using cVEMPs. 144
With ACS stimulation for either test, conducti ve hearing After successful SCD sur gery, both oVEMPS and
loss can nullify the results. Also, some healthy subjects cVEMPs tend to normalize.145,146 SCD patients also have
simply do not have oVEMP n10 to ACS stimuli.135 For abnormally large, low-threshold, click-evoked vestibulo-
these reasons, ACS is a “vulnerable” stimulus that can be ocular reflexes.147
easily affected by f actors apart from the state of the
vestibular receptors. Consequently, BCV is preferable for Ménière’s Disease
clinical testing. In Ménière’s disease143,148-152 and in delayed endolym-
phatic hydrops,153,154 and unlike in acute low-tone hearing
loss,155 VEMPs can be abnormal: too small 156 or too
Clinical Applications large,157 and can have altered tuning properties.148 In some
Superior Semicircular Canal Dehiscence cases, glycerol dehydration or furosemide loading can re-
A third window into the bon y labyrinth allows sound to duce VEMPs that are too large and enlarge the VEMPs that
activate the vestibular system in animals and in humans are too small. 158-163 VEMPs can be used to monitor in-
(for a review, see Halmagyi et al136). Patients with a bony tratympanic gentamicin therapy in patients with Ménière’s
dehiscence from the superior semicircular canal into the disease.164-166 In Ménière’s patients with Tumarkin-type
middle cranial fossa (Fig. 12.12 C) not only have sound- falls, VEMPs might be abnormal, 167,168 perhaps oVEMPs
and pressure-induced v estibular nystagmus but also more than cVEMPs.169 The amplitude of the oVEMP n10
abnormally large, low-threshold cVEMPs and oVEMPs, from the affected ear appears to be selecti vely enhanced
to both air -conducted (AC) and bone-conducted (BC) during attacks in early Ménière’s Disease.170,171
stimulation (Fig. 12.12; Fig. 12.13). It is not yet certain
whether the threshold or the amplitude of the oVEMP or Vestibular Neuritis
cVEMP to AC or BC, or low- or high-frequency stimula- This subject has been comprehensively covered from the
tion has the greatest sensiti vity and specif icity for the physiological viewpoint in the section above “Differenti-
physiological diagnosis of superior semicircular canal ating utricular from saccular function.” Here we deal with
dehiscence (SCD).137-142 Air-bone gaps caused by SCD diagnostic aspects. Usually, vestibular neuritis selectively
A
Figure 12.12 (A) Audiogram. Following the left stapedectomy and two revisions, there is
still a large air-bone gap at 500 and 1,000 Hz on the left and on the unoperated right side.
The contralateral acoustic reflex, the sound stimulus in the operated left ear and the volume
probe in the unoperated right ear, is present at 1 kHz and 2 kHz (A—A) and absent at
0.5 and 4 kHz. It is absent at all frequencies with the stimulus in the unoperated right ear and
the volume probe in the thrice-operated left ear. There is also a severe high-frequency loss
caused by noise damage. Speech comprehension at 65 dB was 95% on the right and 85%
on the left; m = masked; n-r = no response.
Continued
3970_Ch12_195-226 25/06/14 11:41 AM Page 216
C
Figure 12.12—cont’d (B) Vestibular-evoked myogenic potentials (VEMPS). (Left)
Despite the significant air-bone gap, p13-n23 VEMP responses to 110 dB clicks are still
present. The VEMP from the left ear is normal in amplitude but smaller (115 µV) than
from the right (307 µV), indicating that there is some conductive loss on the left (as a
result of the 3 operations) and a conductive gain. The response from stimulating the
right ear is abnormally large and is accompanied by a contralateral inverse response,
n13-p23. (Right) The VEMP threshold is normal from the left ear (with a conductive loss,
the VEMP should be absent) and abnormally low (80 dB; normal > 95 dB) from the right
ear. (C) Left and center, High-resolution spiral computed tomography (CT) scan of the
temporal bones, reconstructed in the plane of each superior semicircular canal, shows a
bilateral superior semicircular canal dehiscence (SCD; arrowheads). CT scan from a normal
subject is shown for comparison. The TORP device is clearly seen abutting the oval window
on the left. (Courtesy of Dr. John Harding-Smith, Central Sydney Imaging.)
affects the superior vestibular nerve. These patients have in response to AC or BC stimulation, b ut preserved sac-
absent or reduced vestibulo-ocular reflexes from the lateral cular function as shown by intact cVEMPs to AC or BC
and anterior (i.e., superior) semicircular canals as sho wn stimulation.83,84,92,104,106-107,111-112,170-173 These patients
by impulsive or caloric stimulation, and absent or reduced can later de velop posterior canal positional v ertigo,174
utricular function as shown by absent or reduced oVEMPs because the inferior vestibular nerve carries posterior canal
3970_Ch12_195-226 25/06/14 11:41 AM Page 217
Healthy Subject posterior canal BPV, especially recurrent BPV, not only
have a higher incidence of abnormal cVEMPs than con-
trols174,183,184 but also a higher incidence of abnormal
R eye
oVEMPs.183
L eye
Vestibular Schwannoma
Although most patients with v estibular schwannoma
SCD Patient (formerly “acoustic neuroma”) present with unilateral
hearing loss, some present with vestibular ataxia. This fact
oVEMP n10 potential is not entirely surprising, because most of these tumors
–
arise not from the acoustic nerv e but from one of the
+
10 µV vestibular nerves, usually the inferior .185 The cVEMP,
which is transmitted via the inferior v estibular nerve, is
oVEMP abnormal—delayed,186 of low amplitude, or absent—in
beneath perhaps four of every five patients with vestibular schwan-
contraSCD
eye
noma.91,187-192 Because the cVEMP does not depend on
cochlear or lateral SCC function, it can be abnormal even
when caloric test results are normal or when brainstem
auditory-evoked potentials cannot be measured because
the hearing loss is too se vere. In patients with bilateral
oVEMP
beneath
vestibular schwannoma caused by neurof ibromatosis
ipsiSCD type 2, loss of cVEMP is unrelated to tumor size. 193 The
eye cVEMP can be preserv ed after vestibular schwannoma
surgery,194 suggesting preservation of the saccular nerve.
0 10 20 30 40 50 The oVEMP is reduced or absent slightly more often than
Time (ms) the cVEMP.92 With other cerebello-pontine angle tumors,
Figure 12.13 Examples of oVEMPs (arrowheads) to brief such as meningiomas, cVEMPs are usually normal.195
500Hz Fz BCV in a healthy subject (a) and a patient with
a CT-verified semicircular canal dehiscence (SCD). The Brainstem Lesions
oVEMP n10 in the patient is extremely large (few healthy
subjects have n10s greater than 10 V), and this enhanced
Unilateral focal brainstem lesions caused by strok e and
oVEMP n10 is a fast simple indicator of probable SCD. multiple sclerosis, especially those that affect the vestibu-
Reprinted from Manzari et al,137 “Ocular and cervical lar nuclei, the accessory nerv e nuclei, and the medial
vestibular-evoked myogenic potentials to 500-Hz Fz bone- vestibulospinal tract or its rostral equi valent, the medial
conducted vibration in superior semicircular canal longitudinal fasciculus, can disrupt ipsilateral cervical195-201
dehiscence,” (Ear and Hearing, 2012;33(4):508-520 by
permission of Wolters Kluwer Health).
and contralateral ocular VEMPs.202,203
Vestibular Test of Normal result Abnormal result Profile of a Profile of a Profile of a Profile of a
sense vestibular in a healthy in a patient with patient with patient with patient with patient
organ sensory subject a vestibular loss unilateral superior inferior with superior
being function vestibular loss vestibular vestibular canal
tested neuritis neuritis dehiscence
UVL SVN IVN SCD
Roll head tilt Roll head tilt Roll head tilt (very few IVN
The maintained Head upright. Head has a small patients tested on
position of the maintained roll these tests)
head, tested toward the
without visual affected ear
cues.
Dynamic H. Ocular I. oVEMP n10 J. Reduced or K. Reduced or L. Reduced or M. Normal n10 of N. Enhanced n10
otolith vestibular beneath the absent n10 of the absent n10 of the absent n10 of the the oVEMP of the oVEMP
function: evoked contralateral eye oVEMP beneath oVEMP beneath oVEMP beneath beneath the beneath the
myogenic of normal the contralateral the contralesional the contralesional contralesional contralateral eye
potential amplitude eye in response eye in response eye in response eye in response to Fz BCV or ipsi
(oVEMP) beneath (5–10µV) and to Fz BCV to Fz BCV to Fz BCV to Fz BCV ACS; also
the contralateral equal amplitude stimulation or stimulation or stimulation or stimulation reduced threshold
eye; the n10 to n10 beneath ipsilateral ACS ipsilesional ACS ipsilesional ACS for n10
Utricular
component in ipsilateral eye in stimulation
macula
response to either response to Fz
bone conducted BCV stimulation
vibration at Fz or or ipsi ACS
ACS to ipsilateral
ear, as the
subject looks up
Figure 12.14 Table showing tests of utricular function and their typical results in healthy
subjects and in patients with vestibular loss. The references for each box are keyed to the
letter and the adjacent table gives the actual references. Reprinted from Curthoys,22 “The
interpretation of clinical tests of peripheral vestibular function,” The Laryngoscope,
122(6):1342-1352, DOI 10.1002/lary.23258, with permission from John Wiley and Sons.
3970_Ch12_195-226 25/06/14 11:41 AM Page 220
37. Goonetilleke SC, Mezey LE, Burgess AM, Curthoys IS. 55. Cosetti MK, Tawfik K, Fouladvand M, Roland JT, Jr.,
On the relation between ocular torsion and visual percep- Lalwani AK. Diplopia due to skew deviation following
tion of line orientation. Vision Res. 2008;48:1488. neurotologic procedures. Otol Neurotol. 2012;33:840.
38. Wade SW, Curthoys IS. The effect of ocular torsional po- 56. Suzuki M, Takahashi H, Yoshida S, Kawaguchi K, Harada
sition on perception of the roll-tilt of visual stimuli. Vision Y. Recovery mechanism of postural disturbance after
Res. 1997;37:1071. vestibular neurectomy. ORL J Otorhinolaryngol Relat
39. Böhmer A, Rickenmann J. The subjective visual vertical Spec. 1991;53:290.
as a clinical parameter of vestibular function in peripheral 57. Brandt T, Strupp M, Benson J. You are better off running
vestibular diseases. J Vestib Res. 1995;5:35. than walking with acute vestibulopathy. Lancet. 1999;
40. Batuecas-Caletrio A, Santacruz-Ruiz S, Munoz-Herrera A, 354:746.
Sousa P, Otero A, Perez-Fernandez N. Vestibular compen- 58. Rossmeisl JH, Jr. Vestibular disease in dogs and cats.
sation after vestibular schwannoma surgery: normalization Vet Clin North Am Small Anim Pract. 2010;40:81.
of the subjective visual vertical and disability. Acta 59. Watrous BJ. Head tilt in horses. Vet Clin North Am Equine
Otolaryngol. 2013. Pract. 1987;3:353.
41. Tabak S, Collewijn H, Boumans LJ. Deviation of the 60. Smith ST, Curthoys IS, Moore ST. The human ocular
subjective vertical in long-standing unilateral vestibular torsion position response during yaw angular acceleration.
loss. Acta Otolaryngol. 1997;117:1. Vision Res. 1995;35:2045.
42. Tribukait A, Bergenius J, Brantberg K. Subjective visual 61. Pavlou M, Wijnberg N, Faldon ME, Bronstein AM. Effect
horizontal during follow-up after unilateral vestibular of semicircular canal stimulation on the perception of the
deafferentation with gentamicin. Acta Otolaryngol. visual vertical. J Neurophysiol. 2003;90:622.
1998;118:479. 62. MacDougall HG, Curthoys IS, Betts GA, Burgess
43. Vibert D, Häusler R, Safran AB. Subjective visual vertical AM, Halmagyi GM. Human ocular counterrolling
in peripheral unilateral vestibular diseases. J Vestib Res. during roll-tilt and centrifugation. Ann N Y Acad Sci.
1999;9:145. 1999;871:173.
44. Vibert N, Beraneck M, Bantikyan A, Vidal PP. Vestibular 63. Dieterich M, Brandt T. Ocular torsion and tilt of subjective
compensation modifies the sensitivity of vestibular neu- visual vertical are sensitive brainstem signs. Ann Neurol.
rones to inhibitory amino acids. Neuroreport. 2000; 1993;33:292.
11:1921. 64. Baier B, Thomke F, Wilting J, Heinze C, Geber C,
45. Takai Y, Murofushi T, Ushio M, Iwasaki S. Recovery of Dieterich M. A pathway in the brainstem for roll-tilt
subjective visual horizontal after unilateral vestibular of the subjective visual vertical: evidence from a lesion-
deafferentation by intratympanic instillation of gentamicin. behavior mapping study. J Neurosci. 2012;32:14854.
J Vestib Res. 2006;16:69. 65. Baier B, Bense S, Dieterich M. Are signs of ocular tilt
46. Hafstrom A, Fransson PA, Karlberg M, Magnusson M. reaction in patients with cerebellar lesions mediated by
Idiosyncratic compensation of the subjective visual horizon- the dentate nucleus? Brain. 2008;131:1445.
tal and vertical in 60 patients after unilateral vestibular 66. Serra A, Derwenskus J, Downey DL, Leigh RJ. Role of
deafferentation. Acta Otolaryngol (Stockh). 2004;124:165. eye movement examination and subjective visual vertical
47. Min KK, Ha JS, Kim MJ, Cho CH, Cha HE, Lee JH. in clinical evaluation of multiple sclerosis. J Neurol.
Clinical use of subjective visual horizontal and vertical in 2003;250:569.
patients of unilateral vestibular neuritis. Otol Neurotol. 67. Frisén L. Ocular torsions and the subjective visual vertical
2007;28:520. with central vestibulo-ocular system lesions: independence
48. Kim HA, Hong JH, Lee H, et al. Otolith dysfunction in disproved. Acta Neurol Scand. 2012;126:205.
vestibular neuritis: recovery pattern and a predictor of 68. Betts GA, Curthoys IS. Visually perceived vertical and
symptom recovery. Neurology. 2008;70:449. visually perceived horizontal are not orthogonal. Vision
49. Ushio M, Iwasaki S, Chihara Y, Murofushi T. Abnormal Res. 1998;38:1989.
deviation of subjective visual horizontal in patients with 69. Pagarkar W, Bamiou DE, Ridout D, Luxon LM. Subjective
vestibular schwannoma. Ann Otol Rhinol Laryngol. visual vertical and horizontal: effect of the preset angle.
2008;117:641. Arch Otolaryngol Head Neck Surg. 2008;134:394.
50. Park H, Shin J, Jeong Y, Kwak H, Lee Y. Lessons from 70. Zwergal A, Rettinger N, Frenzel C, Dieterich M, Brandt T,
follow-up examinations in patients with vestibular neuritis: Strupp M. A bucket of static vestibular function. Neurology.
how to interpret findings from vestibular function tests at a 2009;72:1689.
compensated stage. Otol Neurotol. 2009;30:806. 71. Cohen HS, Sangi-Haghpeykar H. Subjective visual verti-
51. Riordan-Eva P, Harcourt JP, Faldon M, Brookes GB, cal in vestibular disorders measured with the bucket test.
Gresty MA. Skew deviation following vestibular nerve Acta Otolaryngol. 2012;132:850.
surgery. Ann Neurol. 1997;41:94. 72. Cnyrim CD, Rettinger N, Mansmann U, Brandt T, Strupp
52. Safran AB, Vibert D, Issoua D, Häusler R. Skew deviation M. Central compensation of deviated subjective visual
after vestibular neuritis. Am J Ophthalmol. 1994;118:238. vertical in Wallenberg’s syndrome. J Neurol Neurosurg
53. Vibert D, Häusler R, Safran AB, Koerner F. Ocular tilt Psychiatry. 2007;78:527.
reaction associated with a sudden idiopathic unilateral 73. Lin KY, Young YH. Correlation between subjective visual
peripheral cochleovestibular loss. ORL J Otorhinolaryngol horizontal test and ocular vestibular-evoked myogenic
Relat Spec. 1995;57:310. potential test. Acta Otolaryngol. 2011;131:149.
54. Vibert D, Hausler R, Safran AB, Koerner F. Diplopia from 74. Colebatch JG, Halmagyi GM. Vestibular-evoked potentials
skew deviation in unilateral peripheral vestibular lesions. in human neck muscles before and after unilateral vestibu-
Acta Otolaryngol. 1996;116:170. lar deafferentation. Neurology. 1992;42:1635.
3970_Ch12_195-226 25/06/14 11:41 AM Page 222
75. Halmagyi GM, Yavor RA, Colebatch JG. Tapping the head vestibular evoked myogenic potentials in response to
activates the vestibular system—a new use for the clinical bone-conducted vibration of the midline forehead at Fz.
reflex hammer. Neurology. 1995;45:1927. Audiol Neurootol. 2008;13:396.
76. McCue MP, Guinan JJ. Acoustically responsive fibers in 93. Manzari L, Burgess AM, Curthoys IS. Effect of
the vestibular nerve of the cat. J Neurosci. 1994;14:6058. bone-conducted vibration of the midline forehead (Fz)
77. McCue MP, Guinan JJ. Spontaneous activity and frequency in unilateral vestibular loss (uVL). Evidence for a
selectivity of acoustically responsive vestibular afferents in new indicator of unilateral otolithic function. Acta
the cat. J Neurophysiol. 1995;74:1563. Otorhinolaryngol Ital. 2010;30:175.
78. McCue MP, Guinan JJ. Sound-evoked activity in primary 95. Curthoys IS, Vulovic V, Burgess AM, et al. The basis for
afferent neurons of a mammalian vestibular system. Am J using bone-conducted vibration or air-conducted sound
Otol. 1997;18:355. to test otolithic function. In: Rucker J, Zee DS, eds. Basic
79. Murofushi T, Curthoys IS. Physiological and anatomical and Clinical Ocular Motor and Vestibular Research.
study of click-sensitive primary vestibular afferents in the 2011:231-241.
guinea pig. Acta Otolaryngol (Stockh). 1997;117:66. 96. Isu N, Graf W, Sato H, et al. Sacculo-ocular reflex con-
80. Murofushi T, Curthoys IS, Topple AN, Colebatch JG, nectivity in cats. Exp Brain Res. 2000;131:262.
Halmagyi GM. Responses of guinea pig primary vestibu- 97. Kushiro K, Zakir M, Ogawa Y, Sato H, Uchino Y.
lar neurons to clicks. Exp Brain Res. 1995;103:174. Saccular and utricular inputs to sternocleidomastoid
81. Young ED, Fernandez C, Goldberg JM. Responses of motoneurons of decerebrate cats. Exp Brain Res.
squirrel monkey vestibular neurons to audio-frequency 1999;126:410.
sound and head vibration. Acta Otolaryngol (Stockh). 98. Sato H, Imagawa M, Isu N, Uchino Y. Properties of
1977;84:352. saccular nerve-activated vestibulospinal neurons in cats.
82. Murofushi T, Curthoys IS, Gilchrist DP. Response of Exp Brain Res. 1997;116:381.
guinea pig vestibular nucleus neurons to clicks. Exp 98. Uchino Y, Sato H, Sasaki M, et al. Sacculocollic reflex
Brain Res. 1996;111:149. arcs in cats. J Neurophysiol. 1997;77:3003.
83. Iwasaki S, McGarvie LA, Halmagyi GM, Burgess AM, 99. Goto F, Meng H, Bai R, et al. Eye movements evoked by
Kim J, Colebatch JG, Curthoys IS. Head taps evoke selective saccular nerve stimulation in cats. Auris Nasus
a crossed vestibulo-ocular reflex. Neurology. 2007; Larynx. 2004;31:220.
68:1227-1229. 100. Uchino Y, Ikegami H, Sasaki M, Endo K, Imagawa M,
84. Iwasaki S, Smulders YE, Burgess AM, McGarvie LA, Isu N. Monosynaptic and disynaptic connections in the
MacDougall HG, Halmagyi GM, Curthoys IS. Ocular utriculo-ocular reflex arc of the cat. J Neurophysiol.
vestibular evoked myogenic potentials to bone conducted 1994;71:950.
vibration of the midline forehead at Fz in healthy subjects. 101. Uchino Y, Sasaki M, Sato H, Imagawa M, Suwa H, Isu N.
Clin Neurophysiol. 2008;119:2135-2147. Utriculoocular reflex arc of the cat. J Neurophysiol. 1996;
85. Rosengren SM, Todd NPM, Colebatch JG. Vestibular- 76:1896.
evoked extraocular potentials produced by stimulation 102. Goto F, Meng H, Bai RS, et al. Eye movements evoked
with bone-conducted sound. Clin Neurophysiol. 2005; by the selective stimulation of the utricular nerve in cats.
116:1938. Auris Nasus Larynx. 2003;30:341.
86. Todd NPM, Rosengren SM, Aw ST, Colebatch JG. Ocular 103. Uchino Y, Kushiro K. Differences between otolith- and
vestibular evoked myogenic potentials (OVEMPs) produced semicircular canal-activated neural circuitry in the
by air- and bone-conducted sound. Clin Neurophysiol. vestibular system. Neurosci Res. 2011;71:315.
2007;118:381. 104. Aw ST, Fetter M, Cremer PD, Karlberg M, Halmagyi
87. Weber KP, Rosengren SM, Michels R, Sturm V, GM. Individual semicircular canal function in superior
Straumann D, Landau K. Single motor unit activity in and inferior vestibular neuritis. Neurology. 2001;57:768.
human extraocular muscles during the vestibulo-ocular 105. Fetter M, Dichgans J. Vestibular neuritis spares the
reflex. J Physiol (Lond.). 2012;590:3091. inferior division of the vestibular nerve. Brain. 1996;
88. Chiarovano E, Zamith F, Vidal P-P, de Waele C. Ocular 119:755.
and cervical VEMPs: a study of 74 patients suffering from 106. Govender S, Rosengren SM, Colebatch JG. Vestibular
peripheral vestibular disorders. Clin Neurophysiol. 2011; neuritis has selective effects on air- and bone-conducted
122:1650. cervical and ocular vestibular evoked myogenic poten-
89. Chihara Y, Iwasaki S, Ushio M, Murofushi T. Vestibular- tials. Clin Neurophysiol. 2011;122:1246.
evoked extraocular potentials by sound: Another 107. Halmagyi GM, Weber KP, Curthoys IS. Vestibular
clinical test for vestibular air-conducted function. Clin function after acute vestibular neuritis. Restor Neurol
Neurophysiol. 2007;118:2745. Neurosci. 2010;28:37.
90. Piker EG, Jacobson GP, McCaslin DL, Hood LJ. Normal 108. Kim HA, Hong JH, Lee H, et al. Otolith dysfunction in
characteristics of the ocular vestibular evoked myogenic vestibular neuritis—recovery pattern and a predictor of
potential. J Am Acad Audiol. 2011;22:222. symptom recovery. Neurology. 2008;70:449.
91. Iwasaki S, Murofushi T, Chihara Y, Ushio M, Suzuki M, 109. Strupp M, Brandt T. Vestibular neuritis. In: Buttner U,
Curthoys IS, Yamasoba T. Ocular vestibular evoked ed. Vestibular Dysfunction and Its Therapy. Adv Otorhi-
myogenic potentials to bone-conducted vibration in nolaryngol. 1999;55:111.
vestibular schwannomas. Otol Neurotol. 2010;31:147. 110. Goto F, Ban Y, Tsutumi T. Acute audiovestibular deficit
92. Iwasaki S, Smulders YE, Burgess AM, McGarvie LA, with complete ocular tilt reaction and absent VEMPs.
MacDougall HG, Halmagyi GM, Curthoys IS. Ocular Eur Arch Otorhinolaryngol. 2011;268:1093.
3970_Ch12_195-226 25/06/14 11:41 AM Page 223
111. Shin B-S, Oh S-Y, Kim JS, et al. Cervical and ocular 128. Welgampola MS, Rosengren SM, Halmagyi GM, Cole-
vestibular-evoked myogenic potentials in acute vestibular batch JG. Vestibular activation by bone conducted sound.
neuritis. Clin Neurophysiol. 2012;123:369. J Neurol Neurosurg Psychiatry. 2003;74:771.
112. Manzari L, Tedesco A, Burgess AM, Curthoys IS. Ocular 129. Watson SR, Fagan P, Colebatch JG. Galvanic stimulation
vestibular-evoked myogenic potentials to bone-conducted evokes short-latency EMG responses in sternocleidomas-
vibration in superior vestibular neuritis show utricular toid which are abolished by selective vestibular nerve
function. Otolaryngol Head Neck Surg. 2010;143:274. section. Electroencephalogr Clin Neurophysiol.
113. Curthoys IS, Iwasaki S, Chihara Y, Ushio M, McGarvie 1998;109:471.
LA, Burgess AM. The ocular vestibular-evoked myogenic 130. Brantberg K, Fransson PA. Symmetry measures of
potential to air-conducted sound; probable superior vestibular evoked myogenic potentials using objective
vestibular nerve origin. Clin Neurophysiol. 2011;122:611. detection criteria. Scand Audiol. 2001;30:189.
114. Iwasaki S, Chihara Y, Smulders YE, Burgess AM, 131. Young YH, Kuo SW. Side-difference of vestibular evoked
Halmagyi GM, Curthoys IS, Murofushi T. The role myogenic potentials in healthy subjects. Hear Res. 2004;
of the superior vestibular nerve in generating ocular 198:93.
vestibular-evoked myogenic potentials to bone con- 132. Su HC, Huang TW, Young YH, Cheng PW. Aging effect
ducted vibration at Fz. Clin Neurophysiol. 2009; on vestibular evoked myogenic potential. Otol Neurotol.
120:588-593. 2004;25:977.
115. Manzari L, Burgess AM, Curthoys IS. Ocular and cervi- 133. Brantberg K, Tribukait A, Fransson PA. Vestibular evoked
cal vestibular evoked myogenic potentials in response to myogenic potentials in response to skull taps for patients
bone-conducted vibration in patients with probable infe- with vestibular neuritis. J Vestib Res. 2003;13:121.
rior vestibular neuritis. J Laryngol Otol. 2012;126:683. 134. Smulders YE, Welgampola MS, Burgess AM, McGarvie
116. Manzari L, Burgess AM, Curthoys IS. Dissociation LA, Halmagyi GM, Curthoys IS. The n10 component
between cVEMP and oVEMP responses: different of the ocular vestibular-evoked myogenic potential
vestibular origins of each VEMP? Euro Arch Otorhino- (oVEMP) is distinct from the R1 component of the blink
laryngol. 2010;267:1487. reflex. Clin Neurophysiol. 2009;120:1567.
117. Rosengren SM, Welgampola MS, Colebatch JG. Vestibu- 135. Wang S-J, Weng W-J, Jaw F-S, Young Y-H. Ocular and
lar evoked myogenic potentials: past, present and future. cervical vestibular-evoked myogenic potentials: a study
Clin Neurophysiol. 2010;121:636. to determine whether air-or bone-conducted stimuli are
118. Colebatch JG, Halmagyi GM, Skuse NF. Myogenic optimal. Ear Hear. 2010;31:283.
potentials generated by a click-evoked vestibulocollic 136. Halmagyi GM, Curthoys IS, Colebatch JG, Aw ST.
reflex. J Neurol Neurosurg Psychiatry. 1994;57:190. Vestibular responses to sound. Ann N Y Acad Sci.
119. Murofushi T, Matsuzaki M, Wu CH. Short tone burst- 2005;1039:54.
evoked myogenic potentials on the sternocleidomastoid 137. Manzari L, Burgess AM, McGarvie LA, Curthoys IS.
muscle: are these potentials also of vestibular origin? Ocular and cervical vestibular-evoked myogenic poten-
Arch Otolaryngol Head Neck Surg. 1999;125:660. tials to 500Hz Fz bone conducted vibration in superior
120. Welgampola MS, Colebatch JG. Characteristics of tone semicircular canal dehiscence. Ear Hear. 2012;33:508.
burst-evoked myogenic potentials in the sternocleidomas- 138. Zuniga MG, Janky KL, Nguyen KD, Welgampola MS,
toid muscles. Otol Neurotol. 2001;22:796. Carey JP. Ocular versus cervical vemps in the diagnosis
121. Todd N. Evidence for a behavioral significance of saccu- of superior semicircular canal dehiscence syndrome.
lar acoustic sensitivity in humans. J Acoust Soc Am. Otol Neurotol. 2013;34:121.
2001;110:380. 139. Zhang AS, Govender S, Colebatch JG. Tuning of the
122. Colebatch JG, Rothwell JC. Motor unit excitability ocular vestibular evoked myogenic potential (oVEMP)
changes mediating vestibulocollic reflexes in the to air- and bone-conducted sound stimulation in superior
sternocleidomastoid muscle. Clin Neurophysiol. canal dehiscence. Exp Brain Res. 2012;223:51.
2004;115:2567. 140. Zhang AS, Govender S, Colebatch JG. Superior canal
123. Akin FW, Murnane OD, Panus PC, Caruthers SK, dehiscence causes abnormal vestibular bone-conducted
Wilkinson AE, Proffitt TM. The influence of voluntary tuning. Neurology. 2011;77:911.
tonic EMG level on the vestibular-evoked myogenic 141. Brantberg K, Verrecchia L. Testing vestibular-evoked
potential. J Rehabil Res Dev. 2004;41:473. myogenic potentials with 90-dB clicks is effective in the
124. Ferber-Viart C, Dubreuil C, Duclaux R. Vestibular diagnosis of superior canal dehiscence syndrome. Audiol
evoked myogenic potentials in humans: a review. Acta Neurootol. 2009;14:54.
Otolaryngol. 1999;119:6. 142. Janky KL, Nguyen KD, Welgampola M, Zuniga MG,
125. Halmagyi GM, Colebatch JG, Curthoys IS. New tests of Carey JP. Air-conducted oVEMPs provide the best
vestibular function. Baillieres Clin Neurol. 1994;3:485. separation between intact and superior canal dehiscent
126. Sheykholeslami K, Habiby Kermany M, Kaga K. Bone- labyrinths. Otol Neurotol. 2013;34:127.
conducted vestibular evoked myogenic potentials in pa- 143. Taylor RL, Wijewardene AA, Gibson WP, Black DA,
tients with congenital atresia of the external auditory Halmagyi GM, Welgampola MS. The vestibular evoked-
canal. Int J Pediatr Otorhinolaryngol. 2001;57:25. potential profile of Ménière’s disease. Clin Neurophysiol.
127. Sheykholeslami K, Murofushi T, Kermany MH, Kaga 2011;122:1256.
K. Bone-conducted evoked myogenic potentials from 144. Zhou G, Poe D, Gopen Q. Clinical use of vestibular
the sternocleidomastoid muscle. Acta Otolaryngol. evoked myogenic potentials in the evaluation of patients
2000;120:731. with air-bone gaps. Otol Neurotol. 2012;33:1368.
3970_Ch12_195-226 25/06/14 11:41 AM Page 224
145. Welgampola MS, Myrie OA, Minor LB, Carey JP. 162. Magliulo G, Parrotto D, Gagliardi S, Cuiuli G, Novello
Vestibular-evoked myogenic potential thresholds C. Vestibular evoked periocular potentials in Ménière’s
normalize on plugging superior canal dehiscence. disease after glycerol testing. Ann Otol Rhinol Laryngol.
Neurology. 2008;70:464. 2008;117:800.
146. Rinaldi V, Portmann D. Vestibular-evoked myogenic 163. Ban JH, Lee JK, Jin SM, Lee KC. Glycerol pure tone
potentials after superior semicircular canal obliteration. audiometry and glycerol vestibular evoked myogenic
Rev Laryngol Otol Rhinol (Bord). 2011;132:85. potential: representing specific status of endolymphatic
147. Aw ST, Todd MJ, Aw GE, Magnussen JS, Curthoys hydrops in the inner ear. Eur Arch Otorhinolaryngol.
IS, Halmagyi GM. Click-evoked vestibulo-ocular 2007;264:1275.
reflex—stimulus-response properties in superior canal 164. De Waele C, Meguenni R, Freyss G, et al. Intratympanic
dehiscence. Neurology. 2006;66:1079. gentamicin injections for Ménière disease: vestibular hair
148. Rauch SD, Zhou G, Kujawa SG, Guinan JJ, Herrmann cell impairment and regeneration. Neurology. 2002;
BS. Vestibular evoked myogenic potentials show altered 59:1442.
tuning in patients with Ménière’s disease. Otol Neurotol. 165. Gode S, Celebisoy N, Akyuz A, et al. Single-shot,
2004;25:333. low-dose intratympanic gentamicin in Ménière disease:
149. Kim-Lee Y, Ahn JH, Kim YK, Yoon TH. Tone burst role of vestibular-evoked myogenic potentials and caloric
vestibular evoked myogenic potentials: diagnostic criteria test in the prediction of outcome. Am J Otolaryngol.
in patients with Ménière’s disease. Acta Otolaryngol. 2011;32:412.
2009;129:924. 166. Ozluoglu LN, Akkuzu G, Ozgirgin N, Tarhan E.
150. Kingma CM, Wit HP. Asymmetric vestibular evoked Reliability of the vestibular evoked myogenic potential
myogenic potentials in unilateral Ménière patients. test in assessing intratympanic gentamicin therapy in
Eur Arch Otorhinolaryngol. 2011;268:57. Ménière’s disease. Acta Otolaryngol. 2008;128:422.
151. Winters SM, Campschroer T, Grolman W, Klis SF. 167. Ozeki H, Iwasaki S, Murofushi T. Vestibular drop attack
Ocular vestibular evoked myogenic potentials in re- secondary to Ménière’s disease results from unstable
sponse to air-conducted sound in Ménière’s disease. otolithic function. Acta Otolaryngol. 2008;128:887.
Otol Neurotol. 2011;32:1273. 168. Timmer FC, Zhou G, Guinan JJ, Kujawa SG, Herrmann
152. Zuniga MG, Janky KL, Schubert MC, Carey JP. Can BS, Rauch SD. Vestibular evoked myogenic potential
vestibular-evoked myogenic potentials help differentiate (VEMP) in patients with Ménière’s disease with drop
Ménière disease from vestibular migraine? Otolaryngol attacks. Laryngoscope. 2006;116:776.
Head Neck Surg. 2012;146:788. 169. Huang CH, Young YH. Ocular and cervical vestibular-
153. Ohki M, Matsuzaki M, Sugasawa K, Murofushi T. evoked myogenic potentials in Tumarkin falls. Otol
Vestibular evoked myogenic potentials in ipsilateral de- Neurotol. 2012;33:1251.
layed endolymphatic hydrops. ORL J Otorhinolaryngol 170. Manzari L, Tedesco AR, Burgess AM, Curthoys IS.
Relat Spec. 2002;64:424. Ocular and cervical vestibular-evoked myogenic
154. Young YH, Huang TW, Cheng PW. Vestibular evoked potentials to bone conducted vibration in Ménière’s
myogenic potentials in delayed endolymphatic hydrops. disease during quiescence vs during acute attacks. Clin
Laryngoscope. 2002;112:1623. Neurophysiol. 2010;121:1092.
155. Wu CL, Young YH. Vestibular evoked myogenic poten- 171. Wen MH, Cheng PW, Young YH. Augmentation of
tials in acute low-tone sensorineural hearing loss. ocular vestibular-evoked myogenic potentials via bone-
Laryngoscope. 2004;114:2172. conducted vibration stimuli in Ménière disease.
156. de Waele C, Huy PT, Diard JP, Freyss G, Vidal PP. Otolaryngol Head Neck Surg. 2012;146:797.
Saccular dysfunction in Ménière’s disease. Am J Otol. 172. Nola G, Guastini L, Crippa B, Deiana M, Mora R,
1999;20:223. Ralli G. Vestibular evoked myogenic potential in
157. Young YH, Wu CC, Wu CH. Augmentation of vestibular vestibular neuritis. Eur Arch Otorhinolaryngol.
evoked myogenic potentials: an indication for distended 2011;268:1671.
saccular hydrops. Laryngoscope. 2002;112:509. 173. Viciana D, Lopez-Escamez JA. Vestibular evoked
158. Murofushi T, Matsuzaki M, Takegoshi H. Glycerol myogenic potentials and health-related quality of life
affects vestibular evoked myogenic potentials in in patients with vestibular neuritis. Otol Neurotol.
Ménière’s disease. Auris Nasus Larynx. 2001;28:205. 2010;31:954.
159. Seo T, Node M, Yukimasa A, Sakagami M. Furosemide 174. Murofushi T, Halmagyi GM, Yavor RA, Colebatch JG.
loading vestibular evoked myogenic potential for unilat- Absent vestibular evoked myogenic potentials in vestibu-
eral Ménière’s disease. Otol Neurotol. 2003;24:283. lar neurolabyrinthitis—an indicator of inferior vestibular
160. Seo T, Saka N, Sakagami M. Furosemide-loading nerve involvement? Arch Otolaryngol Head Neck Surg.
vestibular evoked myogenic potential testing can suggest 1996;122:845.
developing bilateral involvement of unilateral Ménière’s 175. Halmagyi GM, Aw ST, Karlberg M, Curthoys IS,
disease. Acta Otolaryngol. 2012;132:632. Todd MJ. Inferior vestibular neuritis. In: Kaminski HJ,
161. Magliulo G, Cianfrone G, Gagliardi M, Cuiuli G, Leigh RJ, eds. Neurobiology of Eye Movements: From
D’Amico R. Vestibular evoked myogenic potentials Molecules to Behavior. 2002:306-313.
and distortion-product otoacoustic emissions combined 176. Manzari L, Burgess A, Curthoys IS. Vestibular evoked
with glycerol testing in endolymphatic hydrops: their ocular myogenic potentials (oVEMPS) to Fz bone
value in early diagnosis. Ann Otol Rhinol Laryngol. conducted vibrations in patients with superior vestibular
2004;113:1000. neuritis. Eur J Neurol. 2011;18:292.
3970_Ch12_195-226 25/06/14 11:41 AM Page 225
177. Monstad P, Okstad S, Mygland A. Inferior vestibular evoked myogenic potential during vestibular schwannoma
neuritis: 3 cases with clinical features of acute vestibular surgery. Otol Neurotol. 2003;24:308.
neuritis, normal calorics but indications of saccular 195. Hu YF, Cheng PW, Young YH. Comparison of vestibular
failure. BMC Neurol. 2006;6:45. function between large cerebellopontine angle menin-
178. Zhang D, Fan Z, Han Y, Yu G, Wang H. Inferior vestibular gioma and schwannoma. Acta Otolaryngol. 2009;
neuritis: a novel subtype of vestibular neuritis. J Laryngol 129:161.
Otol. 2010;124:477. 196. Ahn BH, Kim HA, Yi HA, Oh SY, Lee H. Abnormal
179. Kim JS, Kim HJ. Inferior vestibular neuritis. J Neurol. cervical vestibular-evoked myogenic potential in anterior
2012;259:1553. inferior cerebellar artery territory infarction: frequency,
180. Ochi K, Ohashi T, Watanabe S. Vestibular-evoked pattern, and a determinant. J Neurol Sci. 2011;307:114.
myogenic potential in patients with unilateral vestibular 197. Eleftheriadou A, Deftereos SN, Zarikas V, et al. The
neuritis: abnormal VEMP and its recovery. J Laryngol diagnostic value of earlier and later components of
Otol. 2003;117:104. Vestibular Evoked Myogenic Potentials (VEMP) in
181. Murofushi T, Iwasaki S, Ushio M. Recovery of vestibular multiple sclerosis. J Vestib Res. 2009;19:59.
evoked myogenic potentials after a vertigo attack due to 198. Heide G, Luft B, Franke J, Schmidt P, Witte OW, Axer H.
vestibular neuritis. Acta Otolaryngol. 2006;126:364. Brainstem representation of vestibular evoked myogenic
182. Manzari L, Burgess AM, MacDougall HG, Curthoys IS. potentials. Clin Neurophysiol. 2010;121:1102.
Objective verification of full recovery of dynamic 199. Kim S, Lee HS, Kim JS. Medial vestibulospinal tract
vestibular function after superior vestibular neuritis. lesions impair sacculo-collic reflexes. J Neurol. 2010;
Laryngoscope. 2011;121:2496. 257:825.
183. Lee JD, Park MK, Lee BD, Lee TK, Sung KB, Park JY. 200. Patko T, Simo M, Aranyi Z. Vestibular click-evoked
Abnormality of cervical vestibular-evoked myogenic po- myogenic potentials: sensitivity and factors determining
tentials and ocular vestibular-evoked myogenic potentials abnormality in patients with multiple sclerosis. Mult
in patients with recurrent benign paroxysmal postitional Scler. 2007;13:193.
vertigo. Acta Otolaryngol. 2013;133:150. 201. Tseng CL, Young YH. Topographical correlations of
184. Longo G, Onofri M, Pellicciari T, Quaranta N. Benign lateral medullary infarction with caloric- and vestibular-
paroxysmal positional vertigo: is vestibular evoked evoked myogenic potential results. Eur Arch Otorhino-
myogenic potential testing useful? Acta Otolaryngol. laryngol. 2010;267:191.
2012;132:39. 202. Gazioglu S, Boz C. Ocular and cervical vestibular evoked
185. Komatsuzaki A, Tsunoda A. Nerve origin of the acoustic myogenic potentials in multiple sclerosis patients. Clin
neuroma. J Laryngol Otol. 2001;115:376. Neurophysiol. 2012;123:1872.
186. Beyea JA, Zeitouni AG. Vestibular evoked myogenic poten- 203. Rosengren SM, Colebatch JG. Ocular vestibular evoked
tial latencies in Ménière disease and vestibular schwan- myogenic potentials are abnormal in internuclear
noma. J Otolaryngol Head Neck Surg. 2010;39:253. ophthalmoplegia. Clin Neurophysiol. 2011;122:1264.
187. Day AS, Wang CT, Chen CN, Young YH. Correlating 204. Manzari L, Burgess AM, MacDougall HG, Curthoys IS.
the cochleovestibular deficits with tumor size of acoustic Objective measures of vestibular function during an acute
neuroma. Acta Otolaryngol. 2008;128:756. vertigo attack in a very young child. Euro Arch Otorhino-
188. Murofushi T, Matsuzaki M, Mizuno M. Vestibular evoked laryngol. 2012;269:2589.
myogenic potentials in patients with acoustic neuromas. 205. Rosengren SM, Kingma H. New perspectives on vestibu-
Arch Otolaryngol Head Neck Surg. 1998;124:509. lar evoked myogenic potentials. Curr Opin Neurol. 2013;
189. Murofushi T, Shimizu K, Takegoshi H, Cheng PW. 26:74.
Diagnostic value of prolonged latencies in the vestibular 206. Eatock RA, Songer JE. Vestibular hair cells and afferents:
evoked myogenic potential. Arch Otolaryngol Head Neck two channels for head motion signals. In: Hyman SE,
Surg. 2001;127:1069. Jessell TM, Shatz CJ, Stevens CF, Zoghbi HY, eds. Annu
160. Suzuki M, Yamada C, Inoue R, Kashio A, Saito Y, Rev Neurosci, Vol 342011. pp. 501-534.
Nakanishi W. Analysis of vestibular testing in patients 207. Curthoys IS. The role of ocular torsion in visual measures
with vestibular schwannoma based on the nerve of origin, of vestibular function. Brain Res Bull. 1996;40:399.
the localization, and the size of the tumor. Otol Neurotol. 208. Minor LB, Cremer PD, Carey JP, Della Santina CC,
2008;29:1029. Streubel SO, Weg N. Symptoms and signs in superior
191. Tsutsumi T, Tsunoda A, Noguchi Y, Komatsuzaki A. Pre- canal dehiscence syndrome. In: Goebel J, Highstein SM,
diction of the nerves of origin of vestibular schwannomas eds. Vestibular Labyrinth in Health and Disease. 2001:
with vestibular evoked myogenic potentials. Am J Otol. 259-273.
2000;21:712. 209. Carey JP, Migliaccio AA, Minor LB. Semicircular canal
192. Ushio M, Iwasaki S, Murofushi T, et al. The diagnostic function before and after surgery for superior canal
value of vestibular-evoked myogenic potential in patients dehiscence. Otol Neurotol. 2007;28:356.
with vestibular schwannoma. Clin Neurophysiol. 2009; 210. Curthoys IS, Manzari L, Smulders YE, Burgess AM.
120:1149. A review of the scientific basis and practical application
193. Wang CP, Hsu WC, Young YH. Vestibular evoked myo- of a new test of utricular function—ocular vestibular—
genic potentials in neurofibromatosis 2. Ann Otol Rhinol evoked myogenic potentials to bone-conducted vibration.
Laryngol. 2005;114:69. Acta Otorhinolaryngol Ital. 2009;29:179.
194. Magliulo G, Gagliardi M, Ciniglio Appiani G, D’Amico R. 211. Curthoys IS, Burgess AM, MacDougall HG, McGarvie
Preservation of the saccular nerve and of the vestibular LA, Halmagyi GM, Smulders YE, Iwasaki S. Testing
3970_Ch12_195-226 25/06/14 11:41 AM Page 226
human otolith function using bone-conducted vibra- 216. Rosengren SM, Aw ST, Halmagyi GM, Todd NPM,
tion. In: Strupp M, Buttner U, Cohen B, eds. Basic Colebatch JG. Ocular vestibular evoked myogenic
and Clinical Aspects of Vertigo and Dizziness. potentials in superior canal dehiscence. J Neurol
2009:344-346. Neurosurg Psychiatry. 2008;79:559.
212. Curthoys IS. A balanced view of the evidence leads to 217. Welgampola MS, Colebatch JG. Characteristics and
sound conclusions. A reply to JG Colebatch “Sound clinical applications of vestibular-evoked myogenic
conclusions?’’ Clin Neurophysiol. 2010;121:977. potentials. Neurology. 2005;64:1682.
213. Jombik P, Bahyl V, Drobny M, Spodniak P. Vestibulo- 218. Iwasaki S, Takai Y, Ito K, Murofushi T. Abnormal
ocular (oVEMP) responses produced by bone-conducted vestibular evoked myogenic potentials in the presence
sound stimuli applied to the mid-sagittal plane of the of normal caloric responses. Otol Neurotol. 2005;
head. J Vestib Res. 2008;18:117. 26:1196.
214. Curthoys IS, Manzari L. Evidence missed: ocular 219. Streubel SO, Cremer PD, Carey JP, Weg N, Minor LB.
vestibular-evoked myogenic potential and cervical Vestibular-evoked myogenic potentials in the diagnosis of
vestibular-evoked myogenic potential differentiate superior canal dehiscence syndrome. Acta Oto-Laryngol
utricular from saccular function. Otolaryngol Head Suppl. 2001;545:41.
Neck Surg. 2011;144:751.
215. Manzari L, Burgess AM, Macdougall HG, Curthoys IS.
Enhanced otolithic function in semicircular canal
dehiscence. Acta Otolaryngol (Stockh). 2011;131:107.
3970_Ch13_227-248 25/06/14 11:42 AM Page 227
CHAPTER 13
Assessment and
Management of
Auditory Disorders
and Tinnitus
Sharon H. Polensek, MD, PhD ■ Steven L. Benton, AuD
Many patients presenting to a clinician with a possible what environments is hearing most challenging. Infor-
vestibular disorder have underlying auditory impairment. mation such as whether the patient can still talk on the
Because the ear houses the sensory or gans for auditory telephone with either ear or whether the y frequently
and vestibular input, not surprisingly many otologic dis- need to ask for speakers to repeat themselves can be in-
orders (e.g., Ménière’s disease, perilymphatic f istula, dicative of worsening hearing. For more subtle hearing
labyrinthitis, acoustic neuroma, and others) gi ve rise to losses, the patient may report problems only in certain
both auditory and vestibular symptoms. An understand- situations such as listening in church or communicating
ing of clinical methods of assessment and management in a noisy environment such as a restaurant.
of hearing loss and tinnitus is beneficial for the clinician The simplest method for identifying gross hearing
who must diagnose and treat patients with v estibular impairment is for the examiner to occlude one external
impairment. canal by pressing inw ard on the tragus and assessing
whether the patient can hear a vibrating tuning fork, a
whisper, or the examiner’s fingers rubbing together near
History and Physical Examination the other ear. An asymmetric hearing loss can sometimes
A thorough assessment of a patient’ s auditory system be identified by the Weber tuning fork test, which entails
requires obtaining information from a careful history placing a vibrating 512-Hz tuning fork f irmly on the
and physical examination, as well as from audiological patient’s forehead or teeth and determining whether the
testing. A patient whose chief complaint is one of dis- patient perceives the sound emanating from the midline
abling dizziness may not volunteer information about a (Fig. 13.1). If sound perception lateralizes to one side,
mild hearing difficulty, particularly one with an insidi- then hearing loss is present. To determine which ear has
ous onset. At the time of the initial clinical assessment, the loss, the e xaminer can next perform a Rinne test
the examiner should grossly assess hearing acuity of any with the fork (Fig. 13.2). To do this test, the e xaminer
patient presenting with possible vestibular impairment, first places the vibrating fork behind the patient’ s ear,
especially if audiological testing has not yet been per - and when the patient can no longer hear the tone, the
formed. Obtaining a formal audiological assessment on tines of the vibrating fork are placed in front of the e x-
patients with vestibular hypofunction would be a high ternal auditory canal of the same ear. A normal result is
priority. Inquiry should be made as to whether the when the patient can still hear the tone when the fork is
patient has subjective hearing difficulties, and if so, in placed by the ear canal. If the Rinne test is abnormal on
227
3970_Ch13_227-248 25/06/14 11:42 AM Page 228
Audiological Evaluation
and Management
Evaluative Procedures
Tests for Hearing Sensitivity
The most common screen for hearing acuity is the mea -
surement of auditory thresholds to pure tone stimulation
across frequencies from 250 Hz to 8 KHz. An auditory
Figure 13.2 The Rinne Test. See text for explanation. threshold corresponds to the lowest intensity of a sound
stimulus that is detectable some percentage of time.1 The
intensity of the presented sound is typically measured in
the side where the tone perception lateralized with the units of decibels of Hearing Le vel (dB HL), in which
Weber test, then the patient likely has a conductive hear- 0 dB HL is calibrated to the sound pressures that repre-
ing loss in that ear. On the other hand, when the Weber sent hearing sensitivity of young adults with normal hear-
test result is abnormal and the Rinne test yields a normal ing when tested in a reasonably quiet en vironment.2
result, the patient probably has a sensorineural hearing Audiometric thresholds of hearing sensitivity across a spec-
loss in the nonlateralized ear. The Weber and Rinne tests ified frequency range are typically plotted as an individual’s
are screens for hearing loss only . For example, if the audiogram (Fig. 13.3A). The abscissa of the audiogram is
patient has a mix ed hearing loss, these tests can yield in units of dB HL of the presented sound stimulus, and the
inconclusive results. ordinate corresponds to the frequency of the tone presented.
Otoscopic examination is frequently helpful to vi- An audiogram typically shows an individual’s hear-
sualize the outer ear canal and tympanic membrane ing thresholds to pure tone stimuli presented via air con-
when evaluating a patient presenting with dizziness. The duction (AC). Air-conducted sounds are presented using
pinna and external auditory canal should be e xamined either binaural earphones or a loudspeak er, and thus the
for any signs of erythema, edema, or mass and should energy is transmitted through all parts of the ear. For this
be free from any foreign bodies, vesicles, or discharge. reason, measuring auditory thresholds to air -conducted
If the canal is totally occluded with material, such as sounds alone may be suf ficient for diagnosing a hearing
wax or a foreign body , a conductive hearing loss will loss, but provides insufficient information for determining
result in that ear. from which part of the ear the impairment originates. In
Next, the tympanic membrane should be inspected contrast, hearing thresholds to tones presented via bone
for any signs of perforation, b ulging, retraction, or evi- conduction (BC) are obtained by measuring hearing sen-
dence of underlying fluid in the middle ear ca vity that sitivity to pure tones presented with an oscillator placed
could contribute to a conductive hearing loss. Pneumatic on a bony prominence of the skull, typically the mastoid
otoscopy should be performed by insuf flating the ear process behind the auricle. The bone-conducted sounds
canal while otoscopically examining the tympanic mem- are transmitted directly to the bone-encased cochlea, and
brane for normal mobility. Visualization of normal drum thus bypass transmission through the outer and middle ear.
3970_Ch13_227-248 25/06/14 11:42 AM Page 229
Thus, if a hearing loss is identif ied by bone conduction compliance because of a perforation or excessive scarring.
audiometry, it is secondary to a cochlear or retrocochlear A conductive hearing loss can be caused by anything that
problem. occludes the ear canal, such as a mass, impacted w ax or
debris, or e ven a f inger! Etiologies for a conducti ve
Pure Tone Audiogram Interpretation hearing loss include otitis media, otosclerosis, ossicular
and Types of Hearing Loss chain disruption from trauma or chronic otitis media,
When AC thresholds are consistent with a hearing loss, cholesteatoma, hemotympanum (blood in the middle ear
but BC thresholds are normal, an air-bone gap is present, cavity), neoplasm in the outer or middle ear , superior
as shown in the audiogram depicted in Figure 13.3 B of semicircular canal dehiscence, and barotrauma.
Figure 13.3. The presence of an air-bone gap indicates that On the other hand, if AC thresholds indicate a hear-
the hearing loss may be caused by a problem either in the ing loss, and the BC thresholds are the same as those ob-
outer or middle ear. Such a hearing loss is called a con- tained by AC, then no air-bone gap is present and the loss
ductive loss. Causes for conductive losses include fluid in is of sensorineural origin (Fig. 13.3A, Fig. 13.3C). A sen-
the middle ear , disruption or diminished mobility of sorineural loss is therefore a result of a problem either
the ossicular chain, or abnormal tympanic membrane in the cochlea or further proximal in the auditory nerv e
20 20 Tape Speech
PTA SRT/SAT
MLV % % Material
30 30
40 40 Right
1989 Standard
50 50
Left
60 60
70 70 S F Unaided
O I
80 80 U E
N L
90 90 D D Aided
Right
o
1000 ⫹ ⫺
si
C
Left
o
si
C
Figure 13.3 (A) An example of an audiogram. This is from a patient with a mid- to high-
frequency sensorineural hearing loss consistent with presbycusis. Hearing loss is most severe
at the highest frequencies and is less at lower frequencies.
Continued
3970_Ch13_227-248 25/06/14 11:42 AM Page 230
20 20 Tape Speech
PTA SRT/SAT
MLV % % Material
30 30
40 40 Right
1989 Standard
50 50
Left
60 60
70 70 S F Unaided
O I
80 80 U E
N L
90 90 D D Aided
Right
o
1000 ⫹ ⫺
si
C
Left
o
si
C
Figure 13.3—cont’d (B) Audiogram illustrating moderate conductive hearing loss charac-
terized by air-bone gap in the right ear.
or CNS. Frequent etiologies of sensorineural hearing be further classified according to severity, frequencies pre-
losses include presbycusis, ototoxic drugs, congenital dominantly affected, or according to the threshold shape
losses, labyrinthitis, ischemia, acoustic neuroma, tempo- configuration on the audiogram.
ral bone fracture, and Ménière’s disease. Some metabolic The severity of the hearing loss may be described as
or infectious disorders also can cause sensorineural loss mild, moderate, moderately severe, severe, or profound
such as meningitis, congenital syphilis, toxoplasmosis, based on the amount of threshold elevation compared with
cytomegalovirus, rubella, and herpes. Birth complica- normal range (Table 13-1). In general, hearing thresholds
tions such as hypoxia, prolonged mechanical ventilation, are considered normal in adults if less than 20 dB HL. For
and low birth weight also increase the risk for development children under the age of 18, thresholds less than 15 dB
of sensorineural loss. HL are considered within normal limits. Hearing loss is
When BC thresholds show hearing loss, and AC thresh- considered “mild” if thresholds are less than 40 dB, “mod-
olds indicate an air-bone gap, then a mixed-type loss is pres- erate” between 41 and 55 dB, “moderately se vere” be-
ent, meaning the loss has both conductive and sensorineural tween 56 and 70 dB, “severe” between 71 and 90 dB, and
components (Fig. 13.3B). Mixed-typed losses may be seen “profound” if greater than 90 dB HL.
in advanced otosclerosis, severe chronic otitis media, and Many sensorineural hearing losses disproportionately
some genetic forms of auditory impairment. affect higher frequencies, such as those usually associated
In addition to classifying a hearing loss as either con- with aging or noise e xposure, and thus may be described
ductive, sensorineural, or mixed, hearing losses can also as being “down-sloping” on the audiogram. Classically,
3970_Ch13_227-248 25/06/14 11:42 AM Page 231
20 20 Tape Speech
PTA SRT/SAT
MLV % % Material
30 30
40 40 Right
1989 Standard
50 50
Left
60 60
70 70 S F Unaided
O I
80 80 U E
N L
90 90 D D Aided
Right
o
1000 ⫹ ⫺
si
C
Left
o
si
C
■ Table 13-1 CLASSIFICATION noise trauma leads to hearing loss in which sensiti vity to
OF HEARING LOSS 4,000 Hz is most af fected. This kind of hearing loss will
form a V-shape on the audiogram, or what is sometimes
Pure-Tone Audiogram referred to as a “4 KHz notch. ” Individuals with high-
Result (dB) Classification frequency hearing loss have the most difficulty with hear-
ing high-pitched consonants within w ords, although
<20 (adults) <15 (children) Normal hearing
they may hear the lower frequencies of vowels. Therefore,
16–25 Slight loss English-speaking patients may complain that they can hear
speech, but have the most difficulty understanding what is
26–40 Mild loss being said. Languages in which the w ords end in vowels
do not produce the same problems for people with high-
41–55 Moderate loss frequency hearing loss.
Low-frequency sensorineural hearing losses are typ-
56–70 Moderately severe loss
ically seen in patients with Ménière’ s disease and in
71–90 Severe loss some forms of inherited deafness. Audiograms may also
be described as being “ U-shaped” or being a “cookie-
>91 Profound loss bite” audiogram. Thresholds in these audiograms form a
“U shape” by having either a hearing loss with either the
3970_Ch13_227-248 25/06/14 11:42 AM Page 232
least or most severely affected frequencies being in the For routine immittance testing, several types of tym-
mid-portion of the hearing range. panograms exist, as depicted in Figure 13.4. Type A refers
to normal compliance with normal middle ear pressure.
Speech Audiometry Type A deep (or AD) is consistent with eardrum compli-
Another component of a routine hearing evaluation is the ance, which peaks with normal middle ear pressure, b ut
determination of an individual’s ability to detect and rec- with peak compliance being greater than normal.Type AD
ognize speech sounds. The intensity of a speech stimulus pattern is typical for ossicular chain disruption or for a
that is detectable by a listener 50% of the time is called flaccid eardrum. A shallow (or AS) pattern of tym-
the speech detection threshold, or SDT. The SDT should panogram is seen when compliance peaks with normal
closely coincide with the average threshold of hearing sen- middle ear pressure, but with a reduced peak compliance,
sitivity to pure tones at 500, 1,000, and 2,000 Hz, an a v- such as would be expected for ossicular chain fixation or
erage referred to as a pure tone average. The intensity of otosclerosis, tympanic membrane thick ening, or with a
a speech stimulus necessary for a patient to recognize a middle ear mass that dampens ossicular chain mobility .
word is typically around 8 dB greater than the SDT . The Type B tympanograms ha ve compliance measures that
intensity level at which a listener can repeat 50% of the stay constant as the ear canal pressure is changed and are
speech material is referred to as the speech reception consistent with a middle ear effusion, tympanic membrane
threshold, or SRT. perforation, or cerumen impaction. Ne gative middle ear
The ability to recognize w ords presented at a com- pressure gives rise to a Type C tympanogram.
fortable listening le vel is assessed by determining a Another assessment of acoustic impedance is the
patient’s speech recognition score (also referred to as the measurement of the acoustic reflex. The acoustic reflex
speech discrimination score in some te xts). This score is is the contraction of the stapedius muscle in response
obtained by presenting a list of w ords well within the
patient’s audible range and calculating the percentage cor-
rectly recognized. A score that is within normal limits is
dependent on the number and type of words in the list, and Type
Probability
Variants of MEE
normative ranges are available based on the method used. (Jerger,
(Cantekin et al., 1980)4 (Smith et al.,
Speech discrimination scores are more likely to be abnor- 1970)3 2006)5
mal in sensorineural losses and frequently are se verely
1 2 3
affected in retrocochlear losses. In addition to pro viding
information that may be helpful in determining whether a
loss is of sensorineural origin, discrimination test results
A 1%
provide information about the listener’s ability to commu- 9 10 11
nicate effectively and whether hearing aids w ould be
effective management.
12 13 14
Measurements of Acoustic Immittance
A routine audiological e valuation frequently includes B 42%
measurements of acoustic impedance, or resistance to
acoustic energy transmission. The most common tests of 4 5 6
acoustic impedance are tympanometry and stapedial reflex
measures. Tympanometry measures the change in the com-
pliance with changes in air pressure in the external auditory C 80%
7 8
canal. Compliance peaks when air pressure in the outer ear
is equivalent to that in the middle ear. Thus, when negative
pressure applied to the ear canal gives rise to the peak com-
pliance, it may be inferred that negative pressure exists in Figure 13.4 Tympanometric patterns in otitis media. The
the middle ear ca vity. Such would be the case with eu- vertical height of the pressure line is the same throughout
stachian tube dysfunction. On the other hand, when a mid- only for comparison, as the units are arbitrary. Note that
dle ear effusion is present, changing ear canal pressure will the shape of the curve (peaked or gradual), the height of
the curve (proportional to the compliance of the middle
have no significant effect on compliance. Hence, the com- ear), and the middle-ear pressure at peak compliance are
pliance will remain constant at all pressure levels, thereby all related to type of tympanogram classification and to
giving rise to a flat tympanogram (without a peak). likelihood of middle-ear effusion (MEE).
3970_Ch13_227-248 25/06/14 11:42 AM Page 233
to loud sound stimulation, which results in a decrease from points along the pathw ay is dependent on the neu-
in tympanic membrane compliance leading to a reduc- ronal conduction velocity and the delay as the acti vity
tion in the transduction of acoustic ener gy across passes through neuronal synapses. F or this reason, audi-
the tympanic membrane. For the reflex to occur, resid- tory evoked potentials are frequently classif ied by order
ual hearing must be present in the ear being stimulated, of their latencies, which correspond to the duration of time
and the ef ferent fibers to the stapedius muscle must between the presentation of the stimuli and the onset of
be intact. The reflex in normal-hearing indi viduals the electrical potential.
typically occurs when sound is presented 70 to 100 dB
above auditory threshold either in the ipsilateral or Electrocochleography
contralateral ear. Neuroelectric events generated by the cochlea and audi-
The acoustic reflex test battery evaluates for the pres- tory nerve in response to acoustic stimulation are mea -
ence of an acoustic reflex and the threshold at which it oc- sured using electrocochleography. The electrocochlear
curs. If the reflex threshold is less than 70 dB greater than response consists of the cochlear microphonic, the sum-
the hearing threshold, a cochlear lesion is suspected because mating potential (SP), and the whole-nerve action poten-
of the evidence of abnormal loudness growth or sensory re- tial generated by the auditory nerve (AP) (Fig. 13.5). The
cruitment.6 Practically, the presence of the acoustic refle x cochlear microphonic mimics the waveform of the sound
at lower levels above auditory threshold confers a reduced stimulus, and the shift in its baseline (or DC, direct cur -
dynamic range of comfortable hearing, which is useful rent) is called the SP. The AP corresponds to Wave I of the
information in the fitting of appropriate hearing aids. auditory brainstem response (ABR). Ideally , electro-
Middle ear pathology also will inhibit the acoustic cochleography is recorded with an electrode placed as
reflex, although in mild serous otitis media or in some close as possible to the round windo w of the cochlea. A
forms of ossicular chain disarticulation, the reflex may re- transtympanic needle electrode may be used referenced to
main intact. In most cases, both ipsilateral and contralat- another electrode placed on the forehead or tragus, or an
eral reflexes are absent when the patient has a conductive electrode may be placed on the surf ace of the tympanic
hearing loss with an air-bone gap of 20 dB or more in the membrane or in the ear canal.
stimulated ear. The electrocochleogram is particularly useful in iden-
The pattern of abnormal acoustic reflex responses to tifying abnormal cochlear function and has been used ex-
ipsilateral and contralateral stimulation helps to differen- tensively to suggest possible endolymphatic hydrops or
tiate impairment of the se venth or eighth cranial nerv e. Ménière’s disease. Endolymphatic hydrops changes the
Abnormal elevation of the reflex threshold (i.e., more than elasticity of the basilar membrane, causing an increase in
95 dB above the auditory threshold) or absence of the re- amplitude of the SP relative to that of the AP. The SP/AP
flex in the face of normal hearing threshold measurements ratio normally ranges from 10% to 50%, with higher ratios
should raise suspicion of eighth cranial nerv e pathology. in many patients with Ménière’s disease.
Reflex response amplitude that decays to less than half of
the original amplitude within 10 seconds for 500-Hz and Auditory Brainstem Response
1-kHz tones at 10 dB abo ve reflex threshold is also con- Measurement of the auditory brainstem response, orABR,
sistent with neural impairment. Finally , the absence of provides another means of assessing the inte grity of the
contralateral reflexes, with ipsilateral reflexes intact, may auditory pathways from the outer ear to the le vel of the
be seen in patients with brainstem pathology. midbrain. The ABR is a surf ace-recorded, averaged re-
The acoustic reflex threshold should ne ver be less sponse representing the activity of the distal portion of the
than the pure tone threshold. If such is measured, it is most auditory pathway in response to a sound stimulus. Practi-
likely caused by either a nonorganic hearing loss or tech- cal uses for ABR measurement include estimation of au-
nical error. ditory threshold of patients unable to participate in routine
audiometric testing, such as infants or the cognitively im-
Auditory Evoked Potentials paired, and documentation of an audiological threshold in
Electrical activity from the cochlea, auditory nerv e, and those feigning hearing loss. Information regarding site of
auditory centers within the central nerv ous system in re- a lesion along the auditory pathw ay may be inferred by
sponse to presentation of an acoustic stimulus form the the ABR, as waveform morphology may be selecti vely
auditory evoked potentials (AEP). AEPs are most com- abnormal at the site of lesion.ABR monitoring is also use-
monly recorded using noninvasive scalp electrodes and ful intraoperatively when surgery is performed that other-
normally range in humans from one one-thousandth to wise could put the auditory nerv e at risk, such as during
several tenths of a second. The latency of the responses the resection of an acoustic neuroma.
3970_Ch13_227-248 25/06/14 11:42 AM Page 234
Right ECOG
amp
AP (AD) SP/AP = 0.13
Vc
amp
Base (AD) SP (AD)
Nicolet
Left ECOG
amp
amp AP (AS)
SP (AS) SP/AP = 0.81
Vc
Base (AS)
Nicolet
To elicit the ABR, both clicks and brief frequenc y- hence, waves I to V and III to V intervals are routinely
specific tonal stimuli may be used. Electrodes are placed measured.
on the vertex, forehead, and behind each earlobe. The elec- Norms exist for waveform response latencies, and ab-
trode on the earlobe ipsilateral to the ear stimulated is used normally long latencies or widened interw ave intervals
as a reference electrode and the other as a ground elec- may be seen with lesions of the auditory nerv e or brain-
trode. The first five positive polarity peaks within stem. An example of abnormal ABR waveform from a
10 msec are routinely analyzed. Typically, waveforms of patient with multiple sclerosis is shown in Figure 13.6B.
1,000 to 3,000 sweeps are averaged to obtain the ABR.
The morphology of the ABR is sho wn in Middle Latency and Cortical
Figure 13.6A. Wave I originates from the portion of the Event-Related Auditory Evoked
auditory nerve within the internal auditory canal. Wave Potentials
II is from the cochlear nucleus and proximal portion of Middle latency responses (MLR) are thought to be generated
the eighth nerve in the cerebellopontine angle (CP A); by the thalamus and auditory corte x, and unlike electro-
wave III is from the superior olivary complex; wave IV cochleography and ABR, are apparently affected by subject
is from the lateral lemniscus, and wave V is from the in- attention and arousal levels. Latencies of MLRs range from
ferior colliculus. Of note, w aves III to V have bilateral approximately 12 to 65 msec in humans. Responses occur-
crossed inputs and no longer represent a solely ipsilat- ring beyond 75 msec are referred to as slow vertex potentials
eral response. Response latencies normally increase as or late component potentials. Late component potentials,
stimulus amplitude decreases, but interwave intervals re- which are strongly dependent on the arousal and attention
main relatively constant regardless of stimulus intensity; of a subject, are sometimes referred to as e vent-related
3970_Ch13_227-248 25/06/14 11:42 AM Page 235
III
+
I V
II Ri
80dB
Ri 50dB
V
Ri 30dB
V Ri 10dB
Ri 0dB
A −
V-LE
III
I
L
7
Nicolet
potentials (ERP). An ERP called the P300 (named for being Distortion-product otoacoustic emissions are elicited
a positive waveform peak at 300-msec latenc y), may be by two stimulus tones delivered at a 55- to 85-dB sound
elicited only when a subject is attending to an infrequent pressure level, separated by a particular frequency interval.
acoustic stimulus. The most prominent distortion-product otoacoustic emis-
Auditory steady-state responses (ASSR) are brain sion occurs at the cubic difference frequency described by
potentials evoked by steady-state stimuli. Steady-state the expression 2f1-f2, in which f1 represents the lo wer-
stimuli are usually presented as pure tone bursts and must frequency stimulus and f2 the higher -frequency primary
have frequency or amplitude modulation or both. 7 ASSR tone. The resultant emission typically has an amplitude
has the advantage of yielding information that can predict that is 60 dB lower than the primary tones.
more frequency-selective hearing thresholds than ABR,
but be less susceptible to arousal state than MLR or late Tests of Central Auditory Processing
component potentials if the modulation rate is high Audiological assessment of the central auditory nervous
enough. Currently, ASSR is used primarily for estimating system is not yet routine, b ut as increasingly more re-
hearing thresholds in those at risk for hearing loss, espe- search frequently finds association of learning difficulties
cially in infants and young children.8 with auditory perceptual problems, more tests for central
auditory processing disorders are being applied and ad-
Otoacoustic Emissions vocated. Central auditory processing disorder (CAPD)
Otoacoustic emissions (OAEs) are sounds that are gener- was first officially described in 1992 by the American
ated from healthy cochlear outer hair cells. Outer hair cells Speech and Hearing Association (ASHA). Individuals so
are motile and are thought to function as an amplif ier of affected had particular dif ficulties in retrieving, trans-
cochlear partition displacement during acoustic stimula- forming, analyzing, organizing, and storing information
tion, and so generate acoustic by-products, or cochlear from auditory stimuli. 9 Later interpretations of CAPD
echoes. OAEs are obtainable from essentially all patients included subsequent functional def icits involving com-
with normal hearing but may be reduced or absent in ears munication, language, and learning.
with mild hearing loss. Intrasubject variability is minimal Screening for CAPD is not uncommon for audiolo-
in OAEs, and emissions will remain stable o ver several gists and speech pathologists, particularly those who
years for any one ear. OAEs are highly useful in screening work with populations at high risk for ha ving CAPD,
for hearing loss in neonates, because the test is quick, non- such as children with learning disabilities and attentional
invasive, and highly sensitive. disorders and patients who may ha ve sustained a trau-
Otoacoustic emissions may be di vided into sponta- matic brain injury. Results of screening assessments may
neous emission (SO AE), which occur without acoustic lead to possible referral for more comprehensi ve CAPD
stimulation of the ear, and evoked otoacoustic emissions evaluation.
(EOAE), which represent a response to an acoustic stimu- Auditory tasks administered to assess for CAPD
lus. Evoked otoacoustic emissions may be further subdi- consist of monotic (stimuli presented separately to each
vided into transient evoked otoacoustic emissions, elicited ear), diotic (same stimulus presented to both ears simul-
by transient, brief stimulus such as a click or a brief tone taneously), and dichotic (dif ferent stimuli presented to
burst; stimulus-frequency otoacoustic emissions, elicited by each ear simultaneously) tests. Many tests use measures
a pure tone; and distortion-product otoacoustic emissions, of speech (e.g., dichotic digits, staggered spondaic
generated by pure tones separated by a specif ic frequency words) and nonspeech (e.g., temporal gap detection, tone
difference. frequency discrimination) reception.
Otoacoustic emissions are recorded by inserting a
probe tip containing both a miniature loudspeak er and a
Audiological Management
sensitive microphone into the ear canal. The loudspeaker
delivers the stimulus for eliciting evoked OAEs, and the Hearing Loss
microphone samples the emission for approximately Hearing Aids
20 msec. Recorded emissions are then signal-a veraged The majority of individuals with hearing loss are treated
and subsequently deli vered to a sophisticated signal with hearing aids (Fig. 13.7). Hearing aids receive sounds
processor. The transient evoked otoacoustic emissions and convert them either into electrical signals, which are
correspond to a delayed echo of the stimulus and span a then amplified (analogue conversion), or to digital signals.
frequency range of 0.4 to 6 kHz with a latenc y of 5 to Selection of proper amplification systems for hearing loss
20 msec in humans. Emission amplitude typically decreases depends on many factors including type and extent of the
as frequency increases. loss, and whether the loss is bilateral and symmetric. In
3970_Ch13_227-248 25/06/14 11:42 AM Page 237
Figure 13.7 Types of hearing aids. Left, in-the-ear; center, behind the ear; right, in-the-canal.
addition, personal and practical factors such as patient age, Lastly, some hearing aids are specif ically manufac-
cognitive and physical health status, auditory needs, and tured to benefit those with unilateral hearing losses. The
cosmetic concerns also can play a role. Most hearing aid CROS hearing aid delivers sound from an ear with normal
devices are worn either in the ear (ITE) or behind the ear hearing to the contralateral ear with hearing loss. For those
(BTE); rarely a hearing aid may be worn as a device com- with marked asymmetric bilateral hearing loss, a BICROS
bined with eyeglasses. Recent developments in hearing hearing aid may be more appropriate. The BICROS am-
aids have allowed high-powered aids for more severe hear- plifies sounds from both sides and deli vers it to the ear
ing losses to be smaller in size and less conspicuous. The with the better hearing.
smallest hearing aids are w orn in the ear canal (ITC) or The technology of hearing aids has significantly ad-
completely in the ear canal (CIC) so that the y are mini- vanced over the past 20 years. Most modern hearing aids
mally visible, but these are typically not powerful enough are digital and have the advantage of being able to selec-
to amplify for severe hearing loss. Some individuals with tively amplify certain frequencies to suit an indi vidual’s
severe to profound hearing loss use body aids.A body aid needs and hearing loss characteristics. Today’s hearing
consists of a microphone and power supply within a small aids may have multiple programs that a wearer may select
box connected to the earmold with a lead. The power based on the listening environment (e.g., quiet vs. noisy,
supply may be worn in a shirt pocket. Because the power speech or music), or be configured such that the programs
supply may be larger in body aids, they can be quite pow- may change automatically based on the type of acoustic
erful. These aids are not as popular no w as the y were signal received. Such programs reduce acoustic feedback
in the past, but they are still useful in some patients with (whistling), and background noise and may transpose fre-
severe loss or in those patients with vision or de xterity quencies (shift high frequencies that a wearer may not
limitations, which otherwise mak e it dif ficult to use a
conventional hearing aid.
For patients with conductive hearing loss, bone-con-
duction hearing aids may be of benef it. These hearing
aids use an oscillator that contacts skin o verlying the
Sound
mastoid bone, which results in sound being transmitted processor Titanium
via bone conduction and bypassing the middle and outer fixture
ear. They may be worn either attached to a headband or
eyeglasses, or similar to a behind-the-ear hearing aid.An
alternative to traditional bone conduction aids is an im-
planted bone-anchored hearing aid (BAHA). The BAHA
consists of a permanent titanium f ixture or implant,
which is surgically inserted into the mastoid bone. It has
a separate directional microphone and detachable exter- Figure 13.8 The BAHA aid. (Diagram copyright © Entific
nal sound processor (Fig. 13.8). Medical Systems.)
3970_Ch13_227-248 25/06/14 11:42 AM Page 238
hear to lower frequency regions where hearing may be Common risk factors for tinnitus include noise, age,
better). Some hearing aids use directional microphones that ear disease, and hearing loss,12 among others. Noise expo-
selectively amplify sounds originating from in front of the sure is a well-kno wn cause of cochlear sensory cell
user, which may enhance signal-to-noise ratio, particularly damage,13 and as a result, noise e xposure is considered a
in noisy environments. Many hearing aids are equipped primary risk factor for tinnitus.14 The prevalence of tinnitus
with a data logging feature that records the time a hearing among those with high lifetime noise e xposure (20.7%)
aid has been used in certain en vironments (e.g., quiet, is nearly three times greater than that of those with lo w
noisy, musical) and can be useful when an audiologist is lifetime noise exposure (7.5%).15 Veterans are particularly
counseling a wearer on optimal hearing aid usage. at risk for de veloping tinnitus, with 49% of Iraq and
Afghanistan veterans sustaining blast-related injuries having
Aural Rehabilitation it16 and being more than twice as lik ely to have chronic
Aural rehabilitation involves the administration of services tinnitus (12%) as non-veterans (5%).17 For one large audi-
to assist people in adjusting to their hearing loss and mak- ology clinic with the Department ofVeterans Affairs, 26% of
ing the best use of residual hearing and hearing aids. Ex- referrals were for the primary complaint of tinnitus.18
ploring possible assistive devices and providing education The normal effects of aging can result in similar hair
on ways to optimally manage conversations and enhance cell damage,19 and the risk of tinnitus increases with age
communication skills may also be included in aural reha- up to 65 or 70 years, after which the risk decreases. 20
bilitation. Sometimes spouses or other f amily members Although the prevalence of tinnitus increases with increas-
can participate in aural rehabilitation to gain information ing levels of hearing loss, approximately 20% of persons
about hearing loss and the attendant issues of communi- with tinnitus ha ve normal hearing, 14 likely because of
cation. In some aural rehabilitation programs, patients are areas of hair cell damage being too small to be detected
assisted in learning lip reading skills. on a traditional hearing test.21
Research findings indicate that tinnitus is generated
by reduced sensory input related to damage to sensory
Tinnitus cells in the cochlea.22 The discordant dysfunction theory23
Up to 50 million Americans experience tinnitus (pro- postulates that this aberrant nerv e activity is propagated
nounced either tin-NYE-tis or TINN-i-tis),10 which can throughout the auditory nervous system resulting in corti-
be defined simply as ear or head noises (ringing, buzzing, cal perception of tinnitus. Based on the Neurophysiologi-
hissing, etc.) perceived in the absence of an y external cal Model,23 subawareness centers of the brain classify
sound. Approximately 10 to 12 million Americans with sound as either neutral, positive, or negative, and the spe-
tinnitus are so disturbed by it that they seek professional cific classification results in specific activation of the lim-
help and 1 to 2 million report being debilitated by their bic and autonomic nervous systems. In those who merely
tinnitus.10 experience tinnitus, the tinnitus is classif ied as a neutral
Tinnitus can be objective, heard by outside e xam- sound, resulting in minimal, if any, activation of the limbic
iners, or subjective—inaudible to outside examiners. Sub- and autonomic nerv ous systems with no emotional or
jective tinnitus secondary to a serious underlying disorder physiological reaction to the tinnitus. F or those who
is rare, with only 0.4% of patients with either unilateral or experience tinnitus as a signif icant problem, the tinnitus
bilateral tinnitus being diagnosed with acoustic neuroma is classified as negative, as it elicits signif icant negative
in one study.11 Patients reporting subjective tinnitus should limbic and autonomic nervous system reactions, and sub-
be referred to an audiologist for a comprehensive hearing sequent emotional reactions assigned by the limbic system
evaluation. Audiological findings then may determine any (such as anxiety, anger, and/or frustration) and physiolog-
need for referral to an ENT specialist to rule out retro- ical reactions assigned by the autonomic nerv ous system
cochlear pathology. (such as increased muscle tension, release of stress
Objective tinnitus is more rare and may be pulsatile hormones, increased heart rate, and/or increased blood
or non-pulsatile. Pulsatile tinnitus typically arises from pressure). These emotional and physiological reactions
vascular abnormalities near the ear. Non-pulsatile tinnitus cause tinnitus to be a problem for the sufferer, because the
typically arises from less-threatening muscular abnormal- negative limbic and autonomic nerv ous system reactions
ities such as temporomandibular joint (TMJ) dysfunction create physical arousal and alertness. As a result, sleep is
or tensor tympani muscle spasms. Because pulsatile and often adversely affected: 50% of tinnitus patients may re-
non-pulsatile objective tinnitus may respond to medical port sleep problems.24 Sleep deprivation can cause mood
treatment, referral to an ear, nose, and throat (ENT) spe- swings, irritability, and problems with concentration and
cialist is strongly encouraged. attention,21 further reducing overall quality of life.
3970_Ch13_227-248 25/06/14 11:42 AM Page 239
Although multiple herbal, mineral, and homeopathic tinnitus as loud. Hearing aids restore more normal aware-
compounds are marketed as tinnitus treatments, there is ness of ambient environmental sounds, thus reducing ab-
no cure for tinnitus. Although there is no cure, tinnitus can normal auditory gain, increasing lateral inhibition and
be managed successfully, reducing the emotional (limbic reducing the perceived loudness of the tinnitus.
system) and physiological (autonomic nervous system) re- Progressive Tinnitus Management, or PTM, is a
actions to tinnitus. Successful management results in the hierarchical system designed to assist audiologists in iden-
patient feeling less stressed about tinnitus, almost ne ver tifying the least intensive tinnitus management strate gy
thinking about tinnitus, and feeling lik e tinnitus is not adequate to meet a specif ic patient’s needs.28-33 Tinnitus
much of a problem.25 patients proceed to higher PTM levels only if the preced-
Many tinnitus patients can be helped by demystifica- ing level failed to result in adequate tinnitus relief.
tion and en vironmental sound enrichment. Fear of the Table 13-2 summarizes the various levels of PTM.
unknown increases ne gative limbic system acti vation. Tinnitus Retraining Therapy (TRT) combines direc-
Demystification is specific counseling directed toward pro- tive counseling and sound therap y to induce habituation
viding the patient with an understanding of the mechanisms to the tinnitus and has sho wn to result in signif icant
by which tinnitus is generated and by which tinnitus b e- improvement in 85% of patients.34 Regular directive coun-
comes a problem. Counseling focuses both on the patient’s seling sessions focus on demystification and education on
main tinnitus concerns and on information to correct com- the mechanisms of tinnitus generation and tinnitus dis-
mon misperceptions and negative thoughts about tinnitus. tress. Over time, the tinnitus is reclassif ied as a neutral,
Demystification often is suf ficient to reduce limbic and rather than ne gative, stimulus. Full-time use of in-ear
autonomic system engagement and can therefore reduce low-level broadband sound (white noise) generators
tinnitus disturbance to acceptable levels.26 decrease the strength of the tinnitus signal within the brain,
Environmental sound enrichment is the use of sound further facilitating habituation. Successful TRT outcomes
to manage tinnitus. The perceived loudness of a sound is may take up to 24 months, although significant improve-
based on a comparison of the le vel of the target sound to ments may be observed in as few as 3 to 4 months.21
the level of other sounds in the environment.21 Weak signals Neuromonics Tinnitus Treatment (NTT) is a modifi-
in a quiet environment are perceived as louder than the same cation of TRT in which the broadband stimulus is embed-
weak signal in an enriched sound environment. Ordinarily, ded in a relaxing music carrier signal. Both the broadband
excited neurons reduce the activity of neighboring neurons. stimulus and the music are customized using a proprietary
Lateral inhibition is reduced in quiet en vironments. The algorithm based on the individual patient’s hearing profile.
fewer nearby neurons that are stimulated, the more strongly The musical selections provided with the device were cho-
excited neurons respond. In short, the auditory system sen specifically to create positive emotional reactions and
enhances weak tinnitus signals in a quiet en vironment. As to elicit relaxation. Because the broadband treatment sig-
a result, tinnitus patients universally report that their tinnitus nal is customized to the individual, the NTT device can be
seems much louder in quiet environments. used as few as 2 to 4 hours per day with successful NTT
The strength of the ne gative limbic and autonomic outcomes possible in as fe w as 6 to 9 months. Benton 18
nervous system activities is related to the strength of the reported that among a group of patients who had used
tinnitus signal. In an enriched sound environment, lateral NTT for 5 to 8 months, tinnitus a wareness was reduced
inhibition reduces the strength of the tinnitus signal, an average of 72% and tinnitus-related distress w as
thereby reducing the strength of ne gative limbic and reduced an average of 69%.
autonomic nervous system activity: tinnitus is perceived
as less loud and is therefore less disturbing.
Central Auditory Processing Disorders
Tinnitus and Hearing Aids Many interventions may be implemented to assist children
When best practices are used, hearing aids pro vide some and adults with central auditory processing disorders
degree of tinnitus relief for up to 85% of hearing-impaired (CAPD). Compensatory strate gies may include con-
tinnitus patients and moderate to complete tinnitus relief sciously attending to speakers’ faces (i.e., speechreading)
for up to 67%.27 The tinnitus signal typically is generated and having talkers employ “clear speech,” in which the
in the region of the cochlea where outer hair cell damage, goal is to provide the clearest possible sample of the spo-
and resulting hearing loss, is greatest. As a result, the tin- ken utterance.35 Classroom interventions for students with
nitus signal occurs in a hearing region that is always quiet. CAPD include techniques such as preferential seating,
There is minimal, if any, lateral inhibition of the tinnitus having students preview notes before lectures, pro viding
signal, and the hearing-impaired patient percei ves the deliberate clear instructions, listening breaks, and allowing
3970_Ch13_227-248 25/06/14 11:42 AM Page 240
Level 1 Triage Identifies those patients who may require tinnitus-specific services,
most often through the use of screening questionnaires or surveys.
Level 2 Audiological Evaluation Allows the audiologist and patient to distinguish whether tinnitus
and/or other medical issues require intervention. Routine clinical proce-
dures combined with an in-depth case history and validated surveys can
provide this valuable information. Hearing loss may require amplifica-
tion; patients with mental health needs may require referral to appropri-
ate professionals; other health issues that may impact perceived tinnitus
severity, such as hypertension, also may require appropriate referral.
Level 3 Group Education Provides the patient instruction in various tinnitus management strate-
gies, such as sound enrichment, relaxation/stress reduction, and cogni-
tive restructuring in a support group atmosphere. Benton (2010)18
reported that 83% of patients with primary complaint of tinnitus were
able to exit PTM after Level 3 Group education.
Level 4 Tinnitus Evaluation Consists of assessments to determine which patients are likely to
benefit from specific types of treatment, to provide treatment guide-
lines (e.g., spectrum and/or loudness characteristics of broadband de-
sensitization or masking sounds) and to determine if any treatment has
had an effect.36 Measurements most often obtained are quality
(e.g., noise- or tone-like), pitch, loudness, perceptual location
(e.g., right or left ear, both ears, midline), and minimum masking
levels.37 Level 4 may include other disciplines (e.g., mental health,
otolaryngology, neurology) depending on evaluation findings and indi-
vidual patient characteristics.
Level 5 Individualized Management Provides intensive one-on-one sessions for greater patient support. Indi-
vidualized management is reserved for those patients with the most prob-
lematic tinnitus that does not respond to environmental sound enrichment.
In some cases, special devices may be used. Benton (2010)18 reported that
fewer than 6% of tinnitus patients progressed to PTM Level 5.
extra time to complete class work. For students, oftentimes speech in the presence of background noise. Such direct
such compensatory strategies may be included in an indi- auditory therapies, although not yet mainstream, are no w
vidualized education plan (IEP). The speech-language showing significant promise because results show that skills
pathologist frequently is involved in management of lan- learned in therapy do translate into daily skills that patients
guage comprehension and e xpression difficulties, which can successfully employ in their natural environments.
frequently accompany CAPD, and may w ork together
with the audiologist in an interdisciplinary team. Medical Testing in the Evaluation
Different techniques for direct auditory therapy are now
being developed to treat the speech perception difficulties of
of Hearing Loss
CAPD. Some clinicians specifically address decoding diffi- The majority of hearing losses may be attributed to genet-
culties by teaching individual speech sounds and incorpo- ics, age-related, or both, and may be optimally treated by
rating words or nonsense syllables to teach accurate conventional audiological evaluation and management.
speech-sound perception and discrimination. Speech- However, with some clinical presentations, a closer eval-
in-noise sensitization training addresses the common prob- uation to uncover other potential etiologies for the hearing
lem that patients with CAPD encounter understanding loss may be necessary. The clinician needs to recognize
3970_Ch13_227-248 25/06/14 11:42 AM Page 241
common medical causes underlying hearing impairment, frequencies is associated with presbycusis and occurs sec-
and in addition, may need a low threshold of suspicion to ondary to age-related loss of outer hair cells and spiral gan-
look for uncommon, yet potentially treatable, causes of glion cells greatest in the basal turn of the cochlea.38-40 Other
hearing loss. structures in the auditory pathway are also vulnerable such
as the striavascularis, which atrophies with age; cochlear
neurons, which decrease in number; and the middle ear ,
Laboratory Testing auditory brainstem, and cortex, which exhibit degenerative
Some systemic disorders present with hearing loss, such changes. The outcome of age-related changes in the audi-
as autoimmune or infectious disease. For patients present- tory system is characteristically a gradual and progressi ve
ing with sensorineural hearing loss, either the fluorescent loss of hearing in both ears, which initially reduces the abil-
treponemal antibody absorption test (FT A-ABS) or the ity to hear high pitches. Such hearing loss leads to a
microhemagglutination test for Treponema pallidum listener’s complaints of ha ving difficulty discriminating
(MHA-TP) should be obtained, particularly as hearing loss speech and problems hearing in noisy en vironments.
related to syphilis is potentially treatable. Routine screen- Frequently, tinnitus also accompanies presbycusis.
ing for autoimmune disorders is not routinely w arranted,
however, unless disease is suggested from information
obtained from the history and physical e xamination. In
Hearing Loss Associated with Noise
particular, if other cranial neuropathies are present, lumbar
Exposure
puncture is w arranted to check the Venereal Disease Noise exposure can cause either a temporary or permanent
Research Laboratory (VDRL) test for neurosyphilis, and hearing loss. A noise-induced temporary threshold shift
also to evaluate cerebrospinal fluid (CSF) c ytology, cell (NITTS) is a temporary hearing loss that follows exposure
count, levels of glucose and protein, and cultures. In to loud sound and is characterized by a subjective aural full-
endemic geographic areas, L yme’s titers should be ness caused by reduction in the high-frequency sensitivity,
checked. If the history or physical exam findings are oth- and tinnitus. The symptoms of NITTS may be on the order
erwise suggestive of systemic disorders, serological tests of minutes or may last several hours or days. Stimulus fre-
for possible autoimmune etiologies, such as erythroc yte quencies from 2,000 to 6,000 Hz are most effective at pro-
sedimentation rate, rheumatoid factor, ACE level, c-ANCA, ducing NITTS41,42 as are longer stimulus durations and
p-ANCA, and ANA may be helpful. greater stimulus intensities.2,43,44 Noise-induced temporary
threshold shift is associated with swelling of cochlear hair
cells and reduction in stiffness of hair cell cilia.45
Radiological Imaging
Recurrent or chronic e xposure to loud sound may
Radiographical imaging is w arranted in selected patients lead to noise-induced permanent threshold shift (NIPTS).
with hearing loss. Magnetic resonance imaging (MRI) with Swelling of hair cells after noise exposure can lead to cell
gadolinium enhancement is presently the “gold standard” rupture and disruption and permanent loss. In addition,
in evaluating hearing losses of possible retrocochlear origin stereocilia may become fused46 and become unable to ef-
and particularly in making the diagnosis of a tumor on the fectively transmit energy to the hair cells. 47 Progressive
eighth cranial nerve or in the CPA region. Computed to- hair cell damage may subsequently lead to de generation
mography (CT) is useful in patients with suspected of auditory nerve fibers and to changes within the central
labyrinthine congenital anomalies, such as large vestibular auditory system.47
aqueduct syndrome or Mondini dysplasia. CT also is useful Typically, noise-induced hearing loss associated with
in cases with suspected labyrinthine f istula or temporal workplace noise is characterized by having the greatest loss
bone fractures. of hearing from 2,000 to 6,000 Hz, with maximum hearing
loss occurring at 4,000 Hz. This leads to the classic “noise-
induced 4 KHz notch” seen on an audiogram. However, with
Clinical Presentations of Auditory continuing noise exposure, the loss will e xpand to include
Impairment other frequencies outside the 2,000 to 6,000 Hz range.
A single instance of intense loud sound, such as
Presbycusis occurs with an e xplosion, may cause physical trauma to
An estimated 40% to 50% of adults greater than 75 years the ear resulting in permanent hearing loss. Acoustic
of age have hearing loss. The loss associated with aging, trauma may also cause rupture of the tympanic membrane
or presbycusis, is typically of gradual progression and and/or fracture of the ossicular chain. Such hearing loss is
affects both ears symmetrically . Hearing loss for high noticeable immediately.47
3970_Ch13_227-248 25/06/14 11:42 AM Page 242
Sudden Sensorineural Hearing Loss loss and acute vertigo. The route of invasion can be from
(SSNHL) otitis media, via a f istula between the middle ear and the
labyrinth. Alternatively, the route of in vasion can be
The cause of sudden sensorineural hearing loss (SSNHL) meningogenic, through the cochlear aqueduct or internal
is not completely understood and has been hypothesized auditory canal. Suppurative labyrinthitis is the most com-
to be a result of a variety of etiologies: viral, vascular, hy- mon etiology of deafness associated with meningitis.
poxia, intralabyrinthine membrane rupture, inflammatory, Measles and mumps rarely cause hearing and vestibu-
metabolic, and others. SSNHL is considered an otologic lar loss in developed countries because of widespread vac-
emergency, because accepted guidelines for treatment are cination. The hearing loss in measles is usually bilateral
to institute pharmacological agents within 2 weeks to and moderate to profound, and v estibular function is
achieve maximum benefit. Many physicians use the crite- similarly affected. In contrast, mumps typically causes a
ria for SSNHL as minimum loss of 30 dB in three con- unilateral hearing loss. Cytome galovirus (CMV) may
tiguous frequencies measured in routine audiometric cause hearing loss as well, but is typically associated with
evaluation over a period of 3 days or less.The rate of spon- an immunocompromised patient, such as one with acquired
taneous resolution is relatively high at about 65%, but vari- immunodeficiency syndrome (AIDS).
ables such as se verity of loss, flat or do wnsloping
audiograms, age extremes, elevated erythrocyte sedimen- Ramsay Hunt Syndrome
tation rate, time from onset to diagnosis, and the presence If skin vesicles are noted on the pinna or e xternal auditory
of vertigo all portend a poorer prognosis. In general, canal of an ear with ne w onset hearing or v estibular loss,
patients with lower frequency hearing loss ha ve a better herpes zoster infection should be suspected. If accompanied
chance for recovery.48 Steroids administered either orally by an ipsilateral facial weakness, the condition is referred to
or intratympanically is currently the mainstay of treatment as Ramsay Hunt Syndrome caused by a herpes virus. Facial
for SSNHL and have been shown in some studies to be of paralysis is most commonly seen; however, hearing loss and
value.48,49 A recent literature review cautiously concluded vertigo can occur alone or in combination as well. The in-
that application of hyperbaric oxygen therapy may signif- fection probably represents the reactivation of a latent virus,
icantly improve hearing in cases of acute idiopathic such that, after the primary infection, the virus travels to the
SSNHL, but that hyperbaric oxygen was not likely to be of dorsal root ganglion of a cranial nerve, where it remains dor-
benefit in longstanding SSNHL. Various reviews of the mant until reactivated. Incidence and severity is increased
literature have failed to identify clear benef it with other with advancing age associated with an age-related decrease
treatments for SSNHL, for example, vasodilators,50 antivi- in cellular immune response to herpes zoster virus.53
rals,51 or addition of an antiviral agent to steroid treatment.52
Whether other combinations of agents may be more effec- Syphilis
tive remains unclear and is an area of ongoing research. The incidence of hearing loss is as high as 80% in cases
of symptomatic neurosyphilis and 29% in those with
asymptomatic neurosyphilis.39 The mechanism of hearing
Hearing Loss from Infectious Disease loss in syphilis is either a meningolabyrinthitis or an os-
Labyrinthitis teitis of the temporal bone with secondary involvement of
An infectious or inflammatory process within the labyrinth the labyrinth. Pathologically, a resorptive osteitis is seen
can take two forms pathologically: serous or suppurative. in the temporal bone, with endolymphatic hydrops noted
Serous labyrinthitis is defined as an abnormal process within the labyrinth. Clinically, hearing loss caused by
within the labyrinth as a result of the degradation of the tis- syphilis is frequently indistinguishable from Ménière’ s
sue-fluid environment within the inner ear caused by bac- disease, as it may fluctuate and be associated with tinnitus,
terial toxins or contamination of perilymph with blood, aural fullness, or episodic v ertigo. Hennebert’s sign and
products of tissue injury, or air at sur gery. The principal Tullio phenomenon may be seen in otosyphilis.Treatment
abnormal finding in serous labyrinthitis is endolymphatic consists of antibiotics and corticosteroids.
hydrops, with temporary or permanent hearing loss and
vestibular dysfunction. Commonly, labyrinthitis is clinically Rocky Mountain Spotted Fever (RMSF)
diagnosed when patients present with a relati vely sudden Rapidly progressive sensorineural hearing loss has been
onset of sensorineural hearing loss and acute vertigo. Most associated with Rocky Mountain Spotted Fever (RMSF),
commonly, serous labyrinthitis is of viral origin. which is thought to be secondary to a vasculitis involving
Suppurative labyrinthitis is caused by bacterial inva- the auditory system. The hearing loss may be transient.
sion of the inner ear and is manifested by profound hearing RMSF is caused by the tick-borne pathogen Rickettsia
3970_Ch13_227-248 25/06/14 11:42 AM Page 243
rickettsii. Diagnosis is made on the basis of presentation hearing loss. If ultra-high frequencies are tested, then vir-
and confirmed by serologic titers. Treatment is with broad- tually all patients who have received cisplatin probably have
spectrum antibiotics. at least some degree of ototoxicity.58 Occasionally, the hear-
ing loss is accompanied by v ertigo or tinnitus. Other
Lyme Disease chemotherapeutic agents kno wn to cause ototoxicity
Lyme disease is caused by the tick-borne spirochete include the vinca alkaloids vincristine, and to a lesser extent,
Borrelia burgdorferi. Most commonly, it gives rise to vinblastine.
facial paralysis, but it can cause hearing or v estibular
loss and should be considered as a possible etiology in Ototopical Medications
endemic areas. Recommended antimicrobial therapy for Ototopical preparations containing neomycin, gentamicin,
Lyme disease with neurological manifestations is third- and tobramycin are widely used for the treatment of otitis
generation cephalosporins, if no allergy exists. externa and chronic otitis media. However, in experimen-
tal animals and patients, these drugs are no w known to
cause auditory and vestibular loss when they are instilled
Pharmacological Toxicity in the middle ear cavities of normal healthy ears. The toxic
Like the vestibular system, the auditory system is vulner- effect of gentamycin administered transtympanically is
able to the toxic ef fects of a number of pharmacological the mechanism of action of chemical labyrinthectomies
agents. Other than removing the offending agent, no reli- performed to treat patients with refractory Ménière’s dis-
able treatment is kno wn for hearing loss from ototoxic ease.59 Thus, the use of aminoglycoside-containing topical
drug therapy. preparations in uninflamed ears with tympanic membrane
perforations should be a voided. Other ingredients in
Aminoglycosides ototopical preparations that have ototoxic potential include
Probably the most common ototoxic agents encountered in polymyxin B, propylene glycol, acetic acid, and antifungal
clinical practice are the aminoglycoside antibiotics, which agents.60,61
are lethal to hair cells in the inner ear . Kanamycin, Other drugs that have been reported to cause hear-
tobramycin, amikacin, neomycin, and dihydrostreptomycin ing loss include deferoxamine, an iron-chelating agent,
are more cochleotoxic than v estibulotoxic, whereas gen- and eflornithine, used for the treatment of Pneumocystis
tamycin and streptomycin cause disproportionately more carinii pneumonia, trypanosomiasis, cryptosporidiosis,
vestibular damage than cochlear .54 Hearing loss may be leishmaniasis, and malaria. Quinine has long been
asymmetric and progress even after cessation of the therapy. known to cause sensorineural hearing loss, tinnitus, and
Some auditory recovery may occur weeks to months after visual disturbances.55 Loop diuretics alone can cause
treatment. Risk f actors for aminoglycoside ototoxicity reversible hearing loss, which is usually bilateral and
include renal impairment, longer duration or high doses of symmetric.
drug exposure, advanced age, and combined administration
of other ototoxic drugs, particularly loop diuretics.55 Surgical Management
Aspirin of Hearing Loss
Aspirin toxicity may present with tinnitus and re versible Although a thorough review of this topic is be yond the
sensorineural hearing loss, and the toxic effects are typically scope of this chapter, many forms of ear disease can give
dose dependent. The mechanism of injury is most likely al- rise to hearing loss amenable to sur gical treatment. Most
teration of the turgidity and motility of the outer hair cells, often, surgical approaches are used to treat conducti ve
with resultant loss of OAEs and reduction in cochlear action hearing loss, because frequently the loss is secondary to a
potentials.56 Caloric responses can also be reduced by sali- structural problem in the middle or outer ear. When sound
cylates.57 Nonsteroidal anti-inflammatory drugs (NSAIDs) transduction cannot take place because either disease or
such as naprox en, ketorolac, and piroxicam ha ve been trauma has disrupted the ossicular chain, for example, this
known to cause reversible sensorineural hearing loss, b ut can frequently be sur gically corrected either by clearing
this occurs far less frequently than that seen with salicylates. the middle ear ca vity of the structural disease and/or re-
placing the ossicles with a prosthetic device. Disruptions
Chemotherapeutic Agents in the tympanic membrane can also be treated by a tym-
Numerous cancer chemotherapeutic agents have been associ- panoplasty procedure. Rarely do etiologies of conductive
ated with ototoxicity. Cisplatin (cis-diamminedichloroplatinum) hearing loss without a sensorineural component give rise
is associated with irre versible, bilateral, high-frequenc y to vestibular symptoms.
3970_Ch13_227-248 25/06/14 11:42 AM Page 244
Cochlear Implants
Cochlear implants are an option for an increasing number
of hearing-impaired patients. Although the first attempt to
electrically stimulate the auditory system occurred nearly
two centuries ago, the development of a cochlear prosthe-
sis to restore hearing to patients with sensorineural hearing
loss took place only in the past four decades. A deafened
auditory nerve was first electrically stimulated by Djourno
and Eyries in 1957,62 but it was not until 1972 that a com-
mercial device was developed for this purpose. Traditional
criteria for implantation include bilateral profound-to-total B
sensorineural hearing loss, inability to benef it from
conventional hearing aids, good physical and mental Figure 13.9 Cochlear implant. (A) A multichannel
health, and the moti vation and patience to complete a cochlear implant processor, microphone, and magnet coil.
(B) Cochlear implant internal device electrode array and
rehabilitation program.63 ear-level cochlear implant. (Photographs courtesy of
All cochlear implants have several elements in com- Cochlear Corporation.)
mon (Fig. 13.9 A). A microphone, usually at ear le vel,
detects acoustic energy, which is then encoded into an
electrical signal by the external sound processor. The elec- loss, such as connexin 26 mutation,72 Usher syndrome,73,74
trical stimulus is then transmitted to the implanted elec- mitochondrial disorders,75 Waardenburg syndrome,76 and
trode array either in the middle ear or inner ear through Jervell and Lange-Nielsen syndrome.77,78
some form of signal coupler (Fig. 13.9 B). The most The technology of the cochlear implant continues to
commonly used commercially available implants in the improve, particularly in the area of speech processors with
United States are those with 22 active electrodes. increasingly more sophisticated coding strategies. Patient
The criteria for candidacy for cochlear implantation selection criteria have continued to broaden as increasing
has become less rigorous o ver the years. Specif ically, numbers of patients are found to benef it from the proce-
cochlear implants are no w implanted more commonly dure. The rehabilitation process continues to be lengthy ,
bilaterally64 and have now been used in patients with uni- however, because it involves adjustments of the speech
lateral deafness65 and in children less than 2 years of age. processor and extensive aural training.
Children even younger than 12 months of age ha ve been
implanted with good results when hearing loss can be re-
Cerebellopontine Angle (CPA) Tumors
liably confirmed.66 Cochlear implants that are either
shorter than standard lengths or partially surgically inserted Although the acoustic neuroma (acoustic neurinoma,
into the cochlea have been used with success in patients in vestibular schwannoma, acoustic neurilemmoma) is the
which preservation of low-frequency hearing was a goal.67-69 most common lesion found in the cerebellopontine angle, a
Cochlear implants have been advocated as treatment for variety of other benign and malignant lesions may be found
hearing loss associated with enlarged vestibular aqueduct in this region. Patients with these lesions may also present
syndrome.70,71 Implantation criteria continue to broaden as with vertigo, unsteadiness, headache, twitching, weakness,
studies now show success with cochlear implants in or numbness of the face. Unilateral progressive sensorineural
patients with genetic disorders associated with hearing hearing loss is the most common f irst symptom, and
3970_Ch13_227-248 25/06/14 11:42 AM Page 245
predominantly high-frequency sensorineural hearing loss temporal bones. Because the growth rate of these tumors
with poor w ord discrimination ability is characteristic, is generally slow, and malignant transformation is rare, in
although other hearing loss patterns ha ve been described. patients who are otherwise poor operative candidates, the
Little relationship exists between the size of the tumor and most appropriate management may be monitoring the
the audiometric results.79 lesion only. Patients with serviceable hearing with unilat-
Brainstem evoked response audiometry is the single eral tumors that are less than 2.0 cm in diameter may be
most reliable audiometric diagnostic procedure in the diagno- offered either surgical removal with an attempt to sa ve
sis of CPA lesions. Specificity and sensitivity of the ABR hearing or radiographic monitoring, reserving surgery for
ranges from 92% to 96% in the diagnosis of acoustic neuro- an enlarging tumor. For small tumors with poor or no hear-
mas of approximately 1 cm in diameter.80 However, as many ing, either surgical removal or radiographic follow-up may
as 1/3 of patients with smaller tumors on MRI will have nor- be considered. For larger tumors in healthy young and
mal ABRs. Vestibular hypofunction is demonstrated in middle-aged adults, surgical removal is generally recom-
82% to 96% of patients with CP A lesions,81 and positional mended, because the morbidity of sur gical removal is
nystagmus is a very frequent finding.82 MRI of the brain with directly correlated with the size of the tumor, and enlarge-
gadolinium contrast enhancement is the optimal test for diag- ment in healthy patients under 65 years of age is lik ely.
nosing acoustic neurinomas (Fig. 13.10), which may be purely For large tumors in older patients without e vidence of
within the internal auditory canal, and are particularly useful brainstem compression, radiographic monitoring is rec-
for monitoring tumor growth and postoperative recurrence. ommended, reserving surgery for enlarging tumors and
The acoustic neuroma arises most commonly from progressive symptoms. In NF2 cases with bilateral tumors,
the inferior division of the vestibular nerve and next most the goal is to a void bilateral deafness and v estibular
commonly from the superior di vision. In rare cases, it hypofunction, so if hearing is good in both ears, the goal
arises from the cochlear nerve.83 Acoustic neuromas are a is to proceed with sur gical excision of one tumor in the
feature of neurofibromatosis type 2 (NF2). A partial dele- attempt to preserve hearing.84
tion in the long arm of chromosome 22 has been found in
patients with NF2.
Superior Semicircular Canal Dehiscence
Clinically, symptomatic acoustic neuromas are seen
in 1.5 per 100,000 population, which constitute only 0.2% Superior semicircular canal dehiscence is caused by a dis-
of the acoustic neuromas found in postmortem studies of ruption in the bony capsule of the temporal bone overlying
the superior semicircular canal, which renders the vestibular
labyrinth sensitive to loud sounds or pressure changes. The
condition is probably congenital, because it is frequently
bilateral but oftentimes may be asymptomatic. Diagnosis
can be made by demonstration of characteristic torsional
nystagmus induced by application or positi ve or negative
ear canal pressure or by presentation of loud sound.
Frequently, these patients first present with a conduc-
tive hearing loss. Moreover, patients with this condition
may actually be hypersensitive to bone-conducted sounds,
resulting in measurements of audiometric air-bone gaps in
which BC thresholds are lower than normal 0 dB hearing
level and AC thresholds are within normal threshold range.
This hypersensitivity to bone-conducted sounds may gen-
erate patient complaints of hearing their own pulse or eye
movements. Treatment is surgical and may involve block-
ing the affected superior semicircular canal.85,86
Perilymphatic Fistula
Perilymphatic fistulas (PLFs) are associated with a number
Figure 13.10 Post contrast T1-weighted axial image
demonstrating an intense contrast enhancing extraaxial mass of conditions including barotrauma, head injury, heavy lift-
at the left cerebellopontine angle close to the left internal ing or straining, in vasive cochlear procedures, stapedec-
auditory canal (IAC) consistent with an acoustic neuroma. tomies, congenital defects of the middle ear, and labyrinthine
3970_Ch13_227-248 25/06/14 11:42 AM Page 246
8. Cone B, Dimitrijevic A. The auditory steady-state re- 28. Henry JA, et al. A triage guide for tinnitus. J Fam Pract.
sponse. In: Katz J, Medwetsky R, Burkard R, Hood L, eds. 2010;59(7):389-393.
Handbook of Clinical Audiology, 6th ed. Philadelphia, 29. Henry JA, et al. Principles and application of educational
PA: Lippincott Williams & Wilkins; 2009:322-350. counseling used in progressive audiologic tinnitus man-
9. American Speech-Language-Hearing Association (ASHA). agement. Noise Health. 2009;11(42):33-48.
Issues in central auditory processing disorders: a report 30. Henry JA, et al. Using therapeutic sound with progressive
from ASHA Ad Hoc Committee on Central Auditory audiologic tinnitus management. Trends Amplif.
Processing. Rockville, MD: ASHA; 1992. 2008;12(3):188-209.
10. American Tinnitus Association. What You Should Know 31. Henry JA, et al. The role of audiologic evaluation in pro-
about Tinnitus. n.d. [cited 2012]. Available from: http:// gressive audiologic tinnitus management. Trends Amplif.
www.ata.org/sites/ata.org/files/pdf/ATA%20Facts% 2008;12(3):170-187.
20About%20Tinnitus.pdf. 32. Henry JA, Zaugg TL, Schechter MA. Clinical guide
11. Raj-Koziak D, Bartnick G, Fabijanska A, et al. Tinnitus as for audiologic tinnitus management II: treatment.
a symptom of acoustic neuroma. In: International Con- Am J Audiol. 2005;14(1):49-70.
gress Series. Elsevier; 2003:313-315. 33. Henry JA, Zaugg TL, Schechter MA. Clinical guide
12. Baracca G, Del Bo L, Ambrosetti U. Tinnitus and hearing loss. for audiologic tinnitus management I: assessment.
In: Moller A, Langguth B, DeRidder D, Kleinjung T, eds. Text- Am J Audiol. 2005;14(1):21-48.
book on Tinnitus. New York, NY: Springer; 2011:285-292. 34. Jastreboff P, Hazell J, Graham R. Results of tinnitus retrain-
13. NIH, National Institute on Deafness and Other Communi- ing therapy. in Sixth International Tinnitus Seminar. 1999.
cation Disorders. Noise-Induced Hearing Loss. 2008; 35. Medwetsky L, R., L., Katz J. Management of central audi-
Available from: http://www.nidcd.nih.gov/health/hearing/ tory processing disorders. In: Katz J, ed. Handbook of
pages/noise.aspx. Clinical Audiology. Philadelphia: Lippincott, Williams &
14. Davis A, Refaie AE. Chapter 1: Epidemiology of Tinnitus. Wilkins; 2009.
In: Tyler RS, ed. Tinnitus Handbook. New York, NY: 36. Tyler, RS. (1992). The psychophysical measurement o
Thomson Delmar Learning; 2000:15. f tinnitus. In JM Aran & R Dauman (Eds.), Tinnitus 91:
15. Davis A. Hearing in Adults. The Prevalence and Distribu- Proceedings of the Fourth International Tinnitus
tion of Hearing Impairment and Reported Hearing Disabil- Seminar (pp. 17-26). Amsterdam, The Netherlands:
ity in the MRC Institute of Hearing Research’s National Kugler Publications.
Study of Hearing. London: Whurr Publishers, Ltd.; 1995. 37. Tyler, RS. (2000). The psychoacoustical measurement
16. Cave KM, Cornish EM, Chandler DW. Blast injury of of tinnitus. In Tyler, RS (Ed.), Tinnitus Handbook
the ear: clinical update from the global war on terror. Mil (pp. 149-179). Delmar Learning.
Med. 2007;172(7):726-730. 38. Otte J, Schunknecht HF, Kerr AG. Ganglion cell popula-
17. Folmer RL, et al. Audiometric thresholds and prevalence of tions in normal and pathological human cochleae. Implica-
tinnitus among male veterans in the United States: data from tions for cochlear implantation. Laryngoscope. 1978;88
the National Health and Nutrition Examination Survey, (8 Pt 1):1231-1246.
1999-2006. J Rehabil Res Dev. 2011;48(5):503-516. 39. Schuknecht HF, Gacek MR. Cochlear pathology in
18. Benton S. Clinical experience with Progressive Tinnitus presbycusis. Ann Otol Rhinol Laryngol. 1993;
Management (PTM). in American Academy of Audiology. 102(1 Pt 2):1-16.
2010: San Diego, CA. 40. Weinstein WE. Hearing Loss in the Elderly: A New Look
19. McFadden SL, et al. Age-related cochlear hair cell loss is at an Old Problem, in Handbook of Clinical Audiology,
enhanced in mice lacking copper/zinc superoxide dismu- Katz J, ed. Philadelphia: Lippincott Williams & Wilkins;
tase. Neurobiol Aging. 1999;20(1):1-8. 2009:712-725.
20. Moller A, Langguth B, DeRidder D, Kleinjung T. Epi- 41. Ward WE. Adaptation and fatigue. In: Jerger J, ed. Modern
demiology of tinnitus in adults. In: Moller A, Langguth B, Development in Audiology. New York: Academic Press;
Deridder D, Kleinjung T, eds. Textbook of tinnitus. New 1973:241-286.
York, NY: Springer; 2011. 42. Schmiedt RA. Acoustic injury and the physiology of
21. Jastreboff PJ, Hazell JWP. The neurophysiological model of hearing. J Acoust Soc Am. 1984;76(5):1293-1317.
tinnitus. In: Snow JB, ed. Tinnitus: Theory and Management. 43. Hirsh, I.J, Bilger RC, Auditory-threshold recovery after
London: BC Decker, Inc.; 2004:96-106. exposure to pure tones. J Acoust Soc Am. 1955;27(1):
22. Norena AJ, Farley BJ. Tinnitus-related neural activity: the- 1186-1194.
ories of generation, propagation, and centralization. Hear 44. Mills JH, et al. Temporary changes of the auditory system
Res. 2013;295(1-2):161-171. due to exposure to noise for one or two days. J Acoust Soc
23. Jastreboff PJ. Phantom auditory perception (tinnitus): Am. 1970;48(2):524-530.
mechanisms of generation and perception. Neurosci Res. 45. Bohne BA, Harding GW. Degeneration in the cochlea
1990;8(4):221-254. after noise damage: primary versus secondary events. Am
24. Tyler RS, Baker LJ. Difficulties experienced by tinnitus J Otol. 2000;21(4):505-509.
sufferers. J Speech Hear Disord. 1983;48(2):150-154. 46. Durrant JD. Anatomic and physiologic correlates of the
25. Henry J, Zaugg T, Myers P, Kendall C. How to Manage effects of noise on hearing. In: Lipscomb DM, ed. Noise
Your Tinnitus: A Step-by-Step Workbook. 3rd ed. San and Audiology. Baltimore: University Park Press;
Diego, CA: Plural Publishing Inc.; 2010. 1978:109-141.
26. Jastreboff PJ. Tinnitus retraining therapy. Prog Brain Res. 47. Dauman R, Tyler RS. Some considerations on the classifi-
2007;166:415-423. cation of tinnitus. In: Aran JM, Dauman R, eds. Proceed-
27. Benton S. Hearing aid considerations for tinnitus patients. ings of the Fourth International Tinnitus Seminar.
2013: Nashville, TN. Bordeaux, France: Kugler; 1992.
3970_Ch13_227-248 25/06/14 11:42 AM Page 248
48. Eisenman D, Arts HA. Effectiveness of treatment for sud- 70. Bent JP, 3rd, Chute P, Parisier SC. Cochlear implantation
den sensorineural hearing loss. Arch Otolaryngol Head in children with enlarged vestibular aqueducts. Laryngo-
Neck Surg. 2000;126(9):1161-1164. scope. 1999;109(7 Pt 1):1019-1022.
49. Kuhn M, et al. Sudden sensorineural hearing loss: a 71. Miyamoto RT, et al. Cochlear implantation with large
review of diagnosis, treatment, and prognosis. Trends vestibular aqueduct syndrome. Laryngoscope. 2002;
Amplif. 2011;15(3):91-105. 112(7 Pt 1):1178-1182.
50. Agarwal L, Pothier DD. Vasodilators and vasoactive sub- 72. Wiley S, et al. GJB2 mutations and additional disabilities
stances for idiopathic sudden sensorineural hearing loss. in a pediatric cochlear implant population. Int J Pediatr
Cochrane Database Syst Rev. 2009;(4):CD003422. Otorhinolaryngol. 2006;70(3):493-500.
51. Awad Z, Huins C, Pothier DD. Antivirals for idiopathic 73. Liu XZ, et al. Cochlear implantation in individuals with
sudden sensorineural hearing loss. Cochrane Database Usher type 1 syndrome. Int J Pediatr Otorhinolaryngol.
Syst Rev. 2012;8:CD006987. 2008;72(6):841-847.
52. Tucci DL, et al. Treatment of sudden sensorineural 74. Blanchet C, et al. Usher type I syndrome in children:
hearing loss with systemic steroids and valacyclovir. genotype/phenotype correlation and cochlear implant
Otol Neurotol. 2002;23(3):301-308. benefits. Rev Laryngol Otol Rhinol (Bord). 2007;128(3):
53. Oxman MN. Immunization to reduce the frequency and 137-143.
severity of herpes zoster and its complications. Neurology. 75. Yamaguchi T, et al. Cochlear implantation in a patient
1995;45(12 Suppl 8):S41-S46. with mitochondrial disease—Kearns-Sayre syndrome: a
54. Caitlin FI. Prevention of hearing impairment from infec- case report. Adv Otorhinolaryngol. 1997;52:321-323.
tion and ototoxic drugs. Arch Otolaryngol Head Neck 76. Daneshi A, Hassanzadeh S, Farhadi M. Cochlear implan-
Surg. 1985;111:377. tation in children with Waardenburg syndrome. J Laryngol
55. Arts HA. Differential diagnosis of sudden sensorineural Otol. 2005;119(9):719-723.
hearing loss. In: Cummings CW, Fredrickson JM, Harker 77. Daneshi A, et al. Cochlear implantation in children
LA, eds. Otolaryngology Head and Neck Surgery. 3rd ed. with Jervell, Lange-Nielsen syndrome. J Laryngol Otol.
St. Louis: Mosby; 1998:2923-2924. 2008;122(3):314-317.
56. Boettcher FA, Salvi RJ. Salicylate ototoxicity: review and 78. Siem G, et al. Jervell and Lange-Nielsen syndrome in
synthesis. Am J Otolaryngol. 1991;12(1):33-47. Norwegian children: aspects around cochlear implanta-
57. Bernstein JM, Weiss AD. Further observations on salicy- tion, hearing, and balance. Ear Hear. 2008;29(2):261-269.
late ototoxicity. J Laryngol Otol. 1967;81(8):915-925. 79. Nadol JB, Jr, Diamond PF, Thornton AR. Correlation of
58. Kopelman J, et al. Ototoxicity of high-dose cisplatin by hearing loss and radiologic dimensions of vestibular
bolus administration in patients with advanced cancers and schwannomas (acoustic Neuromas). Am J Otol.
normal hearing. Laryngoscope. 1988;98(8 Pt 1):858-864. 1996;17(2):312-316.
59. Nedzelski JM, et al. Chemical labyrinthectomy: local 80. Turner RG, Shepard NT, Frazer GJ. Clinical performance
application of gentamicin for the treatment of unilateral of audiological and related diagnostic tests. Ear Hear.
Meniere’s disease. Am J Otol. 1992;13(1):18-22. 1984;5(4):187-194.
60. Marsh RR, Tom LW. Ototoxicity of antimycotics. Otolaryn- 81. Ojemann RG, Montgomery WW, Weiss AD. Evaluation
gol Head Neck Surg. 1989. 100(2): p. 134-136. and surgical treatment of acoustic neuroma. N Engl J Med.
61. Morizono T. Toxicity of ototopical drugs: animal model- 1972;287(18):895-899.
ing. Ann Otol Rhinol Laryngol Suppl. 1990;148:42-45. 82. Okada Y, et al. Electronystagmographic findings in 147
62. Djourno A, Eyries C, Vallancien P. [Preliminary attempts patients with acoustic neuroma. Acta Otolaryngol Suppl.
of electrical excitation of the auditory nerve in man, by 1991;487:150-156.
permanently inserted micro-apparatus]. Bull Acad Natl 83. Komatsuzaki A, Tsunoda A. Nerve origin of the acoustic
Med. 1957;141(21-23):481-483. neuroma. J Laryngol Otol. 2001;115(5):376-379.
63. Luxford WM. Cochlear implant indications. Am J Otol. 84. Nadol JB. Cerebellopontine angle tumors. In: Surgery of
1989;10(2):95-98. the Ear and Temporal Bone. New York: Raven Press;
64. Litovsky R, et al. Simultaneous bilateral cochlear implan- 1993.
tation in adults: a multicenter clinical study. Ear Hear. 85. Minor LB, et al. Sound- and/or pressure-induced vertigo
2006;27(6):714-731. due to bone dehiscence of the superior semicircular
65. Arndt S, et al. Comparison of pseudobinaural hearing to canal. Arch Otolaryngol Head Neck Surg. 1998;124(3):
real binaural hearing rehabilitation after cochlear implan- 249-258.
tation in patients with unilateral deafness and tinnitus. 86. Baloh RW. Superior semicircular canal dehiscence syn-
Otol Neurotol. 2011;32(1):39-47. drome: leaks and squeaks can make you dizzy. Neurology.
66. Cosetti M, Roland JT, Jr. Cochlear implantation in the 2004;62(5):684-685.
very young child: issues unique to the under-1 population. 87. Stroud MH, Calcaterra TC. Spontaneous perilymph
Trends Amplif. 2010;14(1):46-57. fistulas. Laryngoscope. 1970;80(3):479-87.
67. Gstottner W, et al. Cochlear implantation with preservation of 88. Black FO, et al. The dynamic posturographic pressure
residual deep frequency hearing. HNO. 2005;53(9):784-790. test for the presumptive diagnosis of perilymph fistulas.
68. Kiefer J, et al. Conservation of low-frequency hearing in Neurol Clin. 1990;8(2):361-374.
cochlear implantation. Acta Otolaryngol. 2004. 124(3): 89. Shepard NT, et al. Platform pressure test in identification
p. 272-280. of perilymphatic fistula. Am J Otol. 1992;13(1):49-54.
69. James C, et al. Preservation of residual hearing with 90. Lando M, Hoover LA, Finerman G. Stabilization of hear-
cochlear implantation: how and why. Acta Otolaryngol. ing loss in Paget’s disease with calcitonin and etidronate.
2005;125(5):481-491. Arch Otolaryngol Head Neck Surg. 1988;114(8):891-894.
3970_Ch14_249-265 25/06/14 11:44 AM Page 249
FOUR
Medical
and Surgical
Management
3970_Ch14_249-265 25/06/14 11:44 AM Page 250
CHAPTER 14
Pharmacological
and Optical
Methods to
Treat Vestibular
Disorders and
Nystagmus
Rosalyn Schneider, BA ■ R. John Leigh, MD
Patients with vestibular disease may complain of vertigo, wrote, “During a w alk I found too much motion in my
oscillopsia, or the visual consequences of n ystagmus.1 visual picture of the surroundings to permit recognition
Vertigo means whirling or spinning, b ut the term is also of fine detail. I learned that I must stand still in order to
used to describe other illusions of motion, and implies read the lettering on a sign.”
vestibular imbalance. Oscillopsia consists of illusory , The range of peak velocities and predominant frequen-
oscillatory movements of the seen en vironment. When cies of head rotations measured in 20 normal subjects as
oscillopsia occurs with head movements, it usually implies they walked or ran in place are summarized in Figure 14.1.
loss of v estibular function. Oscillopsia also may occur Note that although peak head velocity is generally below
when the head is stationary in patients with spontaneous 150 deg/sec, the predominant frequencies range from 0.5 to
nystagmus. In this chapter, we review current treatments 5 Hz.3,4 The latter v alue exceeds the frequencies that
for vertigo, oscillopsia, and the visual consequences of nys- vestibular physiologists have conventionally used to test
tagmus from the standpoint of known pathophysiology. patients in the laboratory but generally corresponds to the
In interpreting and treating symptoms resulting bedside head-impulse test.5 Besides head rotations, linear
from vestibular disorders, it is helpful to consider the movements or “translations” occur during locomotion. 6
nature of the demands placed on the v estibular system However, recent studies indicate that head translations are
during natural activities, especially locomotion. The pur- less of a threat to vision than are rotations, unless subjects
pose of the vestibulo-ocular reflex (VOR) is to maintain view near targets during locomotion. 7,8 This information
clear and stable vision during natural head mo vements. about the range and nature of head perturbations that occur
A major threat to clear vision is posed by the head per - during natural activities such as locomotion is useful in
turbations occurring during locomotion. This fact was formulating strategies to rehabilitate patients with vestibu-
pointed out by the anon ymous physician J.C. who had lar disorders, especially if the functional goal of therap y
lost vestibular function because of aminoglycosides2; he is the ability to walk normally, without aids.
250
3970_Ch14_249-265 25/06/14 11:44 AM Page 251
Chapter 14 • PHARMACOLOGICAL AND OPTICAL METHODS TO TREAT VESTIBULAR DISORDERS AND NYSTAGMUS 251
90th PERCENTILE
75th PERCENTILE
MEDIAN
25th PERCENTILE
10th PERCENTILE
Figure 14.1 Summary of the ranges of (A) maximum velocity and (B) frequency of rota-
tional head perturbations that occur during walking or running in place. Distributions of data
from 20 normal subjects are displayed as Tukey box graphs, which show selected percentiles
of the data. All values beyond the 10th and 90th percentiles are graphed individually as
points. Reproduced with permission.1
nystagmus and unsteadiness.1,10 The nystagmus is typi- receptors on Purkinje cells in the cerebellum.19 The phase
cally mixed horizontal-torsional with quick phases beat- of the vestibulo-ocular reflex (timing of eye rotations with
ing away from the side of the lesion. The nystagmus is respect to head rotation) depends on the “velocity storage
more marked when visual fixation is prevented (e.g., with mechanism,” by which the peripheral v estibular signal is
Frenzel goggles) and when the patient looks in the prolonged. This perseveration of the raw vestibular signal
direction of the quick phases, a phenomenon kno wn is achieved by a vestibular commissure that is governed by
as Alexander’s law.1 Past-pointing to the side of the the cerebellar nodulus and uvula. 20 The metabotropic
lesion reflects imbalance of vestibulo-spinal reactions.1 GABAB receptor, which is a mediator of slo w inhibitory
Patients with rotational vertigo caused by acute, periph- postsynaptic potentials, is important in do wn-regulating
eral vestibular lesions are often uncertain as to the direc- velocity storage. Thus, the GABAB agonist baclofen sup-
tion of their vertiginous illusions. This is because there presses the velocity-storage phenomenon in normal mon-
is a conflict between v estibular sensation indicating keys.21 These findings provide an e xplanation for the
self-rotation in one direction and retinal image motion effectiveness of baclofen in treatment of a central form of
(consequent on slow phases of v estibular nystagmus) vestibular nystagmus (periodic alternating nystagmus)22
that, when self-referred, connotes self-rotation in the op- and possibly also in motion sickness.21
posite direction. It is therefore w orthwhile to evaluate The vestibular system also contrib utes to the gaze-
patients’ vestibular sense alone by asking them to report holding mechanism by which the eyes can be held steady
their perceived direction of self-rotation with the e yes in an eccentric position (e.g., f ar right gaze). Thus, the
closed, which will aid localization of the side of the medial vestibular nucleus and adjacent nucleus prepositus
lesion. Although most patients with acute peripheral hypoglossi, along with reciprocal connections with the
lesions recover to become independent for most activities vestibular cerebellum, constitute a “neural integrator” for
within a month or tw o, some are left with recurrent ocular motor signals. This network of neurons receives
vestibular symptoms, and others e xperience benign raw vestibular signals encoding head v elocity and inte-
paroxysmal positional v ertigo. These topics are dis- grates them into the eye position signals required to hold
cussed in detail in other chapters. the eyes steady in eccentric gaze. The network also inte-
grates pre-motor signals for saccades and smooth pursuit;
thus, it is the common neural inte grator for all classes of
Neuropharmacology of the Vestibular eye movements. For vertical eye movements, the intersti-
System and Nystagmus tial nucleus of Cajal also contrib utes to this neural inte-
A broad range of neurotransmitters have been identified grator function. Several neurotransmitters contribute to the
within the vestibular system.13 Vestibular hair cells ex- neural integrator, and nitric oxide appears to perform a
press muscarinic acetylcholine receptors. 14 Primary neuromodulatory stabilizing function within this neural
vestibular afferents in the eighth cranial nerv e, which network.23 Some vestibular inputs to nucleus prepositus
synapse in the v estibular nuclei, express glutamate and hypoglossi are GABAergic and are f acilitated by nitric
histamine as transmitters. 13,15,16 Secondary excitatory oxide.24,25 The projections of nucleus prepositus hypoglossi
projections from the vestibular nuclei to ocular motoneu- (the output of the neural integrator) to the abducens nucleus
rons express glutamate and aspartate as transmitters. 17 are cholinergic.13,26 Further insights into the neurophar-
Secondary inhibitory projections from the vestibular nu- macology of the neural inte grator have been gained
clei to the v ertical ocular motoneurons e xpress gamma- using the technique of pharmacological inactivation.27,28
aminobutyric acid (GABA), whereas those to horizontal Microinjection of the weak GABA antagonist bicuculline
motoneurons are glycinergic.13,17,18 These findings have and the strong GABA agonist muscimol into the MVN-
led to the development of drugs with a range of pharma- NPH region may cause either gaze-e voked nystagmus
cological actions as treatment for acute vestibular imbal- (caused by a “leak y neural integrator”) with centripetal
ance and its associated nystagmus; they are discussed in slow-phase drifts or, occasionally, centrifugal, increasing
the next section. velocity waveforms (caused by an “unstable neural inte-
In addition to the pathways serving the “elementary” grator”). These paradoxical findings may reflect inactiva-
vestibulo-ocular reflex, other systems continuously monitor tion of either the inte grator itself (causing leakiness) or
and optimize the reflex’s performance (see Chapters 1 and 2). cerebellar control of the integrator (causing instability).28
The gain (magnitude of the vestibulo-ocular response) de- Nystagmus with characteristics implying a v estibular
pends on a form of “memory encoding” in the cerebellum imbalance may also be produced during these inactivation
due to metabotropic glutamate receptors and GAB AB experiments. Agents with glutamatergic effects may also
3970_Ch14_249-265 25/06/14 11:44 AM Page 253
Chapter 14 • PHARMACOLOGICAL AND OPTICAL METHODS TO TREAT VESTIBULAR DISORDERS AND NYSTAGMUS 253
compromise the neural integrator, but glycinergic agents course of specific vestibular exercises may be indicated (see
do not.28 Inactivation of the interstitial nucleus of Cajal Chapter 22). Patients in whom enduring v estibular symp-
with muscimol causes neural integrator failure, implying toms develop, such as vertigo with head movement, may
that GABA also contributes to vertical gaze holding. 29 have an underlying central nerv ous system disorder, typi-
Taken together, these findings indicated that GABA and cally of the cerebellum,40 and imaging studies are indicated.
glutamate are not just an important neurotransmitter for Other patients who complain of persistent symptoms may
the horizontal and vertical vestibulo-ocular reflex but are have either a phobic disorder11 or the potential for second-
also involved in the gaze-holding mechanism, malfunction ary gain as a consequence of their injury.
of which may lead to nystagmus.30 Treatment of recurrent vertigo depends on the nature of
Clinical evidence has also supported a role for nico- the underlying disorder. For example, vertigo caused by mi-
tinic acetylcholinergic mechanisms in vertical eye move- graine (including migraine without a headache) can usually
ments. Thus, upbeat n ystagmus may be induced in be successfully managed medically (see Chapter 15). Recur-
darkness in normal subjects by nicotine. 31-33 Functional rent brief episodes of v ertigo—vestibular paroxysmia—
imaging has indicated acti vation by nicotine of the that may be a result of vascular compression of the eighth
nucleus reticularis tegmenti pontis (NRTP),34 suggesting cranial nerve, are often ef fectively treated with carba-
that nicotinic acetylcholinergic mechanisms contribute mazepine.41 Recurrent vertigo caused by a perilymphatic
to vertical smooth-pursuit, although other mechanisms fistula or superior canal dehiscence syndrome may recover
probably also contrib ute. These findings suggest that spontaneously, but some patients require sur gical repair
drugs with actions on nicotinic choliner gic receptors (see Chapters 4 and 17). Less commonly, recurrent attacks
might influence nystagmus. of vertigo are a feature of episodic ataxia type 2
(Case Study 14-1), along with ataxia, vegetative symptoms
Treatment of Vertigo and, sometimes, headache.
The general goals in treatment are to eliminate vertigo and Vertigo caused by Ménière’s syndrome is often dif-
accompanying neurovegetative symptoms (nausea, vom- ficult to manage, although a lo w-salt diet and diuretics
iting, anxiety) and to promote (or, at least, not hinder) the help some patients with the disorder.38 In Europe, betahis-
normal process of v estibular compensation. In certain tidine, which is an H1-agonist and H3-antagonist that
cases, such as viral neurolabyrinthitis and vertigo caused may improve the labyrinthine microcirculation, is gi ven
by migraine, it may be possible to treat the underlying as prophylactic treatment 37; it is not a vailable in the
cause. Often, however, treatment is symptomatic. United States. Because the vestibular imbalance may be
In acute vertigo caused by a peripheral v estibular le- in a continuous state of flux, long-term use of “vestibular
sion, recovery from symptoms and resumption of normal ac- sedatives” such as meclizine is justified in some affected
tivities is the rule in the ensuing weeks. 35 However, if viral patients. Treatment with intratympanic injection of gen-
etiology is suspected and the patient is evaluated within three tamicin, which is toxic to labyrinthine hair cells, can be
days of onset, a short course of methylprednisolone may beneficial when vertigo persists, especially when it arises
speed recovery from symptoms; anti viral agents such as from a deaf ear.38,42 Patients with Menière’s disease tend
valacyclovir offer no therapeutic advantage.36 There is a con- to improve with time, although the second ear may
sensus that drugs exerting a “sedative effect” on the vestibu- become involved.43
lar system should be used for only the first 24 hours.10 Some Central neurological conditions, such as multiple
drugs commonly used for treatment of v ertigo, nausea, sclerosis, vertebrobasilar ischemia, and posterior fossa
and vomiting are summarized in Table 14-1 and are dis- mass lesions, may cause severe, recurrent vertigo. When
cussed more fully in reviews.37,38 Ondansetron, a serotonin treatment of the underlying condition does not pro-
5-hydroxytryptamine3 (5-HT3) antagonist, seems especially duce improvement, “vestibular sedatives” are justified.
helpful in the management of nausea and vomiting in acute Ondansetron helps some patients with vertigo caused
vestibular disorders.39 Most agents probably affect more than by brainstem stroke or multiple sclerosis.44,45 Sometimes
one neurotransmitter system, and in intractable cases, a com- a combination of agents such as an anticholiner gic
bination of different types of agent may be more ef fective (e.g., scopolamine) and an antidopaminergic agent (e.g.,
than one alone. prochlorperazine) are required.
After the first 24 hours, drugs should be used sparingly Benign paroxysmal positional vertigo is effectively
and patients should be encouraged to get out of bed and in- treated in most cases by specif ic vestibular exercises or
crease their activities, because there is evidence that failure maneuvers (see Chapter 20); drugs are seldom indicated
to do so limits recovery of symptoms. During this period, a in this condition.
3970_Ch14_249-265 25/06/14 11:44 AM Page 254
Prochlorperazine Antihistamine Oral: 5–10 mg every 6 hr Sedative and antiemetic Can cause liver disease
(Compazine) Anticholinergic Supp: 25 mg every 12 hr Can cause extrapyrami- when used in combina-
Phenothiazine IM: 5–10 mg every 6 hr; dal reactions tion with CNS depres-
maximum of 60 mg sants, propranolol,
in 24 hr phenytoin, anticoagu-
lants, levodopa, diuretics
CNS = central nervous system; GABA, gamma-aminobutyric acid; IM, intramuscular; IV, intravenous;
supp = suppository.
3970_Ch14_249-265 25/06/14 11:44 AM Page 255
Chapter 14 • PHARMACOLOGICAL AND OPTICAL METHODS TO TREAT VESTIBULAR DISORDERS AND NYSTAGMUS 255
Box 14-1
ETIOLOGY OF OSCILLOPSIA*
Oscillopsia with Head Movements: Abnormal Oscillopsia with Head Stationary: Abnormal spon-
Vestibulo-ocular Reflex taneous eye movements
Peripheral vestibular hypofunction:48 Acquired nystagmus (especially pendular, upbeat,
Aminoglycoside toxicity downbeat, see-saw, dissociated nystagmus)
Ménière’s syndrome Congenital nystagmus (uncommon under natural
Meningitis/encephalitis illumination)
In association with cerebellar degenerations49
Saccadic oscillations (ocular flutter (including
Autoimmune disorders affecting the labyrinth
psychogenic) and opsoclonus
(e.g., Cogan’s syndrome)
Surgical section of eighth cranial nerve Superior oblique myokymia (monocular oscillopsia)
Congenital ear anomalies Oscillopsia with Head Stationary and Normal Eye
Hereditary vestibular areflexia Movements:
Cisplatin therapy Central oscillopsia
Idiopathic With cerebral disorders: seizures, occipital lobe
Central vestibular dysfunction (often with associ- infarction
ated cerebellar disease):
Decreased vestibulo-ocular reflex (VOR) gain
Increased VOR gain
Abnormal VOR phase
direction of the VOR. Some patients with hereditary spino- Nystagmus and Its Visual
cerebellar degeneration may ha ve associated impaired
vestibular responses (Case Study 14-2). Other patients Consequences
with disease of the v estibulocerebellum show vestibular Pathogenesis
hyper-responsiveness; this occurs in patients with the
Arnold-Chiari malformation, and occasionally patients As indicated previously, acquired nystagmus commonly
with cerebellar disorders are reported with increased gain causes impaired vision and oscillopsia (illusory movement
of both the horizontal and vertical VOR.50 In some patients of the environment). These symptoms, which are a result
with vestibulocerebellar dysfunction, the gain of theVOR of excessive drift of images of stationary objects on the
is normal but the phase relationship between head and eye retina, interfere with reading and watching television, and
movements is abnormal, causing retinal image slip. 51 are often distressing to the patient. The relationship be-
Lesions of the medial longitudinal fasciculus (internuclear tween retinal image velocity and visual acuity is a direct
ophthalmoplegia in multiple sclerosis) may cause a one: For higher spatial frequencies (which correspond to
low gain of the vertical VOR and produce oscillopsia with text), image motion in e xcess of about 5 deg/sec impairs
vertical head movements.52,53 vision.66 On the other hand, the relationship between reti-
nal image velocity and the development of oscillopsia is
less consistent; the intensity of oscillopsia is usually less
Treatment of Oscillopsia than the magnitude of nystagmus. For example, in patients
With time, compensation tak es place in some patients with downbeat nystagmus, oscillopsia, on average, was es-
with oscillopsia caused by v estibular loss,2 although timated to be about 1/3 the magnitude of the nystagmus.67
many others remain more permanently disabled.54 When This latter finding suggests that the brain compensates for
compensation occurs, it is a result of a variety of factors, the excessive retinal image motion and so partly maintains
including potentiation of the cervico-ocular refle x, pre- visual constancy, although the mechanism is debated. In
programming of compensatory eye movements, and per- practice, it is often not necessary to reduce retinal image
ceptual changes (see Chapters 8 and 9). 55-58 In general, slip to less than 5deg/sec for patients to report appreciable
drugs have little to offer. Patients should be encouraged benefit, and this can be achieved at drug doses that do not
to resume activities, especially walking, and enroll in ex- produce side effects.
ercise programs (see Chapters 22 and 23). Rarely, oscil-
lopsia caused by a hyperacti ve VOR can be treated
pharmacologically.50 Paradoxically, patients who lack a
Treatments
VOR can read head-fixed visual display during locomo- Drugs
tion better than normal subjects can.59 The reason is that Some of the drugs reported to suppress a range of forms
clear vision of a head-fixed display requires that vestibu- of nystagmus are listed in Box 14-2. Here we re view
lar eye movements be suppressed or canceled. Because medicines that have been evaluated in controlled clinical
such patients have little or no VOR, it is easy to suppress trials. Perhaps the most visually disabling ocular oscil-
vestibular eye movements. This behavior suggests that lations are those of acquired pendular nystagmus, which
head-fixed video displays of images obtained with cam- occurs in two common settings: associated with multiple
eras might be able to compensate for head perturbations sclerosis (Case Study 14-3) or as a component of the
in patients who ha ve lost vestibular function; the tech- syndrome of oculopalatal tremor, which follows brain-
nology required for such devices has been developed but stem stroke (Case Study 14-4). Two medicines ha ve
has not yet been applied to patients with def icient proven useful in the treatment of both forms of acquired
vestibular function.60,61 pendular nystagmus, though the site of action of both
The prospects for treating patients with loss of pe- is uncertain. The first is gabapentin, which was initially
ripheral vestibular function by implanting a v estibular thought to be GAB Aergic but exerts its ef fect via
prosthesis are improving, with some success reported in a subunit of v oltage-dependent calcium channels. 68
restoring vestibular responses in a macaque model.62,63 An Gabapentin was introduced as an anticon vulsant but is
alternative approach is to present tactile sensory stimuli now widely used for the control of chronic pain.
that can substitute for the missing v estibular sense.64,65 Gabapentin suppresses n ystagmus and af fords visual
Future studies will determine how well these devices can improvement in many patients with acquired pendular
overcome the disability following loss of vestibular func- nystagmus, perhaps more frequently when the cause
tion, particularly in elderly patients. is multiple sclerosis.69,70 However, not all such patients
3970_Ch14_249-265 25/06/14 11:44 AM Page 257
Chapter 14 • PHARMACOLOGICAL AND OPTICAL METHODS TO TREAT VESTIBULAR DISORDERS AND NYSTAGMUS 257
Chapter 14 • PHARMACOLOGICAL AND OPTICAL METHODS TO TREAT VESTIBULAR DISORDERS AND NYSTAGMUS 259
25
A B
10
−5
0 1 2 3
Time (seconds)
Position (degrees)
head turns (head impulse test), she made diagonal cor- Eye vertical position
rective saccades that were directed opposite to the di-
rection of head rotation and do wnward (indicated by 0
Chapter 14 • PHARMACOLOGICAL AND OPTICAL METHODS TO TREAT VESTIBULAR DISORDERS AND NYSTAGMUS 261
5 5
Continued
3970_Ch14_249-265 25/06/14 11:44 AM Page 262
Chapter 14 • PHARMACOLOGICAL AND OPTICAL METHODS TO TREAT VESTIBULAR DISORDERS AND NYSTAGMUS 263
19. Broussard DM, Titley HK, Antflick J, et al. Motor learning 37. Strupp M, Thurtell MJ, Shaikh AG, et al. Pharmacother-
in the VOR: the cerebellar component. Exp Brain Res. apy of vestibular and ocular motor disorders, including
2011;210:451-463. nystagmus. J Neurol. 2011;258:1207-1222.
20. Cohen B, Helwig D, Raphan T. Baclofen and velocity stor- 38. Huppert D, Strupp M, Muckter H, et al. Which medication
age: a model of the effects of the drug on the vestibulo- do I need to manage dizzy patients? Acta Otolaryngol.
ocular reflex in the rhesus monkey. J Physiol. 1987;393: 2011;131:228-241.
703-725. 39. Venail F, Biboulet R, Mondain M, et al. A protective effect
21. Cohen B, Dai M, Yakushin SB, et al. Baclofen, motion of 5-HT3 antagonist against vestibular deficit? Metoclo-
sickness susceptibility and the neural basis for velocity pramide versus ondansetron at the early stage of vestibular
storage. Prog Brain Res. 2008;171:543-553. neuritis: a pilot study. Eur Ann Otorhinolaryngol Head
22. Halmagyi GM, Rudge P, Gresty MA, et al. Treatment of Neck Dis. 2012;129:65-68.
periodic alternating nystagmus. Ann Neurol. 1980;8: 40. Rudge P, Chambers BR. Physiological basis for enduring
609-611. vestibular symptoms. J Neurol Neurosurg Psychiatry.
23. Marquez-Ruiz J, Morcuende S, Navarro-Lopez JD, et al. 1982;45:126-130.
Anatomical and pharmacological relationship between 41. Hufner K, Barresi D, Glaser M, et al. Vestibular paroxysmia:
acetylcholine and nitric oxide in the prepositus hypoglossi diagnostic features and medical treatment. Neurology.
nucleus of the cat: functional implications for eye- 2008;71:1006-1014.
movement control. J Comp Neurol. 2007;503:407-420. 42. Lange G, Maurer J, Mann W. Long-term results after
24. Moreno-Lopez B, Escudero M, Estrada C. Nitric oxide interval therapy with intratympanic gentamicin for
facilitates GABAergic neurotransmission in the cat Meniere’s disease. Laryngoscope. 2004;114:102-105.
oculomotor system: a physiological mechanism in eye 43. Huppert D, Strupp M, Brandt T. Long-term course of
movement control. J Physiol. 2002;540:295-306. Meniere’s disease revisited. Acta Otolaryngol. 2010;130:
25. Baizer JS, Baker JF. Neurochemically defined cell 644-651.
columns in the nucleus prepositus hypoglossi of the cat 44. Rice GP, Ebers GC. Ondansetron for intractable vertigo
and monkey. Brain Res. 2006;1094:127-137. complicating acute brainstem disorders. Lancet. 1995;345:
26. Spencer RF, Baker R. Histochemical localization of 1182-1183.
acetylcholinesterase in relation to motor neurons and inter- 45. Macleod AD. Ondansetron in multiple sclerosis. J Pain
nuclear neurons of the cat abducens nucleus. J Neurocytol. Symptom Manage. 2000;20:388-391.
1986;15:137-154. 46. Shaikh AG, Reich S, Zee DS. Pseudonystagmus—clinical
27. Straube A, Kurzan R, Buttner U. Differential effects of features and quantitative characteristics. Nat Rev Neurol.
bicuculline and muscimol microinjections into the vestibu- 2010;6:519-523.
lar nuclei on simian eye movements. Exp Brain Res. 47. Yen MT, Herdman SJ, Tusa RJ. Oscillopsia and pseudonys-
1991;86:347-358. tagmus in kidney transplant patients. Am J Ophthalmol.
28. Arnold DB, Robinson DA, Leigh RJ. Nystagmus induced by 1999;128:768-770.
pharmacological inactivation of the brainstem ocular motor 48. Zingler VC, Weintz E, Jahn K, et al. Causative factors,
integrator in monkey. Vision Res. 1999;39:4286-4295. epidemiology, and follow-up of bilateral vestibulopathy.
29. Helmchen C, Rambold H, Fuhry L, et al. Deficits in verti- Ann N Y Acad Sci. 2009;1164:505-508.
cal and torsional eye movements after uni- and bilateral 49. Zingler VC, Cnyrim C, Jahn K, et al. Causative factors and
muscimol inactivation of the interstitial nucleus of Cajal epidemiology of bilateral vestibulopathy in 255 patients.
of the alert monkey. Exp Brain Res. 1998;119:436-452. Ann Neurol. 2007;61:524-532.
30. Das VE, Oruganti P, Kramer PD, et al. Experimental tests 50. Thurston SE, Leigh RJ, Abel LA, et al. Hyperactive
of a neural-network model for ocular oscillations caused vestibuloocular reflex in cerebellar degeneration:
by disease of central myelin. Exp Brain Res. 2000;133: pathogenesis and treatment. Neurology. 1987;37:53-57.
189-197. 51. Gresty MA, Hess K, Leech J. Disorders of the vestibu-
31. Sibony PA, Evinger C, Manning KA. Tobacco-induced loocular reflex producing oscillopsia and mechanisms
primary-position upbeat nystagmus. Ann Neurol. 1987;21: compensating for loss of labyrinthine function. Brain.
53-58. 1977;100:693-716.
32. Pereira CB, Strupp M, Eggert T, et al. Nicotine-induced 52. Cremer PD, Migliaccio AA, Halmagyi GM, et al.
nystagmus: three-dimensional analysis and dependence Vestibulo-ocular reflex pathways in internuclear
on head position. Neurology. 2000;55:1563-1566. ophthalmoplegia. Ann Neurol. 1999;45:529-533.
33. Kim JI, Somers JT, Stahl JS, et al. Vertical nystagmus in 53. Ranalli PJ, Sharpe JA. Vertical vestibulo-ocular reflex,
normal subjects: effects of head position, nicotine and smooth pursuit and eye-head tracking dysfunction in inter-
scopolamine. J Vestib Res. 2000;10:291-300. nuclear ophthalmoplegia. Brain. 1988;111:1299-1317.
34. Deutschlander A, Stephan T, Riedel E, et al. Nicotine- 54. Zingler VC, Weintz E, Jahn K, et al. Follow-up of
induced nystagmus correlates with midpontine activation. vestibular function in bilateral vestibulopathy. J Neurol
Neuroimage. 2008;41:479-482. Neurosurg Psychiatry. 2008;79:284-288.
35. Brandt T, Huppert D, Hufner K, et al. Long-term course 55. Bronstein AM, Hood JD. Oscillopsia of peripheral
and relapses of vestibular and balance disorders. Restor vestibular origin. Central and cervical compensatory
Neurol Neurosci. 2010;28:65-78. mechanisms. Acta Otolaryngol (Stockh). 1987;104:
36. Strupp M, Zingler VC, Arbusow V, et al. Methylpred- 307-314.
nisolone, valacyclovir, or the combination for vestibular 56. Kasai T, Zee DS. Eye-head coordination in labyrinthine-
neuritis. N Engl J Med. 2004;351:354-361. defective human beings. Brain Res. 1978;144:123-141.
3970_Ch14_249-265 25/06/14 11:44 AM Page 264
57. Schubert MC, Das V, Tusa RJ, et al. Cervico-ocular reflex cross-over treatment study of memantine and gabapentin.
in normal subjects and patients with unilateral vestibular J Neurol. 2010;257:322-327.
hypofunction. Otol Neurotol. 2004;25:65-71. 77. Villoslada P, Arrondo G, Sepulcre J, et al. Memantine in-
58. Schubert MC, Hall CD, Das V, et al. Oculomotor strate- duces reversible neurologic impairment in patients with
gies and their effect on reducing gaze position error. Otol MS. Neurology. 2009;72:1630-1633.
Neurotol. 2010;31:228-231. 78. Strupp M, Schuler O, Krafczyk S, et al. Treatment of
59. Das VE, Thomas CW, Zivotofsky AZ, et al. Measuring eye downbeat nystagmus with 3,4-diaminopyridine: a placebo-
movements during locomotion. Filtering techniques for controlled study. Neurology. 2003;61:165-170.
obtaining velocity signals from a video-based eye monitor. 79. Strupp M, Kalla R, Glasauer S, et al. Aminopyridines for
J Vestibular Res. 1996;6:455-461. the treatment of cerebellar and ocular motor disorders.
60. Schneider E, Bartl K, Dera T, et al. Documentation and Prog Brain Res. 2008;171:535-541.
teaching of surgery with an eye movement driven head- 80. Alvina K, Khodakhah K. The therapeutic mode of action
mounted camera: see what the surgeon sees and does. Stud of 4-aminopyridine in cerebellar ataxia. J Neurosci.
Health Technol Inform. 2006;119:486-490. 2010;30:7258-7268.
61. Schneider E, Villgrattner T, Vockeroth J, et al. EyeSeeCam: 81. Hauser SL, Johnston SC. 4-aminopyridine: new life for an
an eye movement-driven head camera for the examination old drug. Ann Neurol. 2010;68:A8-A9.
of natural visual exploration. Ann N Y Acad Sci. 2009; 82. Cornblath DR, Bienen EJ, Blight AR. The safety profile of
1164:461-467. dalfampridine extended release in multiple sclerosis clini-
62. Rahman MA, Dai C, Fridman GY, et al. Restoring the cal trials. Clin Ther. 2012;34:1056-1069.
3D vestibulo-ocular reflex via electrical stimulation: 83. Sander T, Sprenger A, Marti S, et al. Effect of
the Johns Hopkins multichannel vestibular prosthesis 4-aminopyridine on gravity dependence and neural
project. Conf Proc IEEE Eng Med Biol Soc. integrator function in patients with idiopathic
2011;2011:3142-3145. downbeat nystagmus. J Neurol. 2011;258:618-622.
63. Thompson LA, Haburcakova C, Gong W, et al. Responses 84. Strupp M, Kalla R, Claassen J, et al. A randomized trial
evoked by a vestibular implant providing chronic stimula- of 4-aminopyridine in EA2 and related familial episodic
tion. J Vestib Res. 2012;22:11-15. ataxias. Neurology. 2011;77:269-275.
64. Bach-y-Rita P. Tactile sensory substitution studies. Ann 85. Kumar A, Thomas S, McLean R, et al. Treatment of ac-
NY Acad Sci. 2004;1013:83-91. quired periodic alternating nystagmus with memantine: a
65. Goebel JA, Sinks BC, Parker BE, Jr., et al. Effectiveness case report. Clin Neuropharmacol. 2009;32:109-110.
of head-mounted vibrotactile stimulation in subjects with 86. Yakushiji Y, Otsubo R, Hayashi T, et al. Glucose utilization
bilateral vestibular loss: a phase 1 clinical trial. Otol in the inferior cerebellar vermis and ocular myoclonus.
Neurotol. 2009;30:210-216. Neurology. 2006;67:131-133.
66. Carpenter RHS. The visual origins of ocular motility. In: 87. Young YH, Huang TW. Role of clonazepam in the treat-
Carpenter RHS, ed. Vol 8. Eye Movements. London: ment of idiopathic downbeat nystagmus. Laryngoscope.
MacMillan Press; 1991:1-10. 2001;111:1490-1493.
67. Buchele W, Brandt T, Degner D. Ataxia and oscillopsia in 88. Leigh RJ, Burnstine TH, Ruff RL, et al. Effect of anti-
downbeat-nystagmus vertigo syndrome. Adv Otorhino- cholinergic agents upon acquired nystagmus: a double-
laryngol. 1983;30:291-297. blind study of trihexyphenidyl and tridihexethyl chloride.
68. Thorpe AJ, Offord J. The alpha2-delta protein: an auxil- Neurology. 1991;41:1737-1741.
iary subunit of voltage-dependent calcium channels as a 89. Kim JI, Averbuch-Heller L, Leigh RJ. Evaluation of trans-
recognized drug target. Curr Opin Investig Drugs. dermal scopolamine as treatment for acquired nystagmus.
2010;11:761-770. J Neuroophthalmol. 2001;21:188-192.
69. Averbuch-Heller L, Tusa RJ, Fuhry L, et al. A double-blind 90. Dell’osso LF. Improving visual acuity in congenital nys-
controlled study of gabapentin and baclofen as treatment for tagmus. In: Smith JL, Glaser JS, eds. Neuro-Ophthalmol-
acquired nystagmus. Ann Neurol. 1997;41:818-825. ogy, Volume 7.7 ed. St. Louis: Mosby; 1973:98-106.
70. Thurtell MJ, Joshi AC, Leone AC, et al. Crossover trial of 91. Lavin PJ, Traccis S, Dell’osso LF, et al. Downbeat nystag-
gabapentin and memantine as treatment for acquired nys- mus with a pseudocycloid waveform: improvement with
tagmus. Ann Neurol. 2010;67:676-680. base-out prisms. Ann Neurol. 1983;13:621-624.
71. Thurtell MJ, Leigh RJ. Therapy for nystagmus. 92. Averbuch-Heller L, Leigh RJ. Medical treatments for abnor-
J Neuroophthalmol. 2010;30:361-371. mal eye movements: pharmacological, optical and immuno-
72. Thurtell MJ, Leigh RJ. Nystagmus and saccadic intru- logical strategies. Aust N Z J Ophthalmol. 1997;25:7-13.
sions. Handb Clin Neurol. 2011;102:333-378. 93. Rushton D, Cox N. A new optical treatment for oscillop-
73. Thurtell MJ, Leigh RJ. Treatment of nystagmus. Curr sia. J Neurol Neurosurg Psychiatry. 1987;50:411-415.
Treat Options Neurol. 2012;14:60-72. 94. Yaniglos SS, Leigh RJ. Refinement of an optical device
74. Rogawski MA, Wenk GL. The neuropharmacological that stabilizes vision in patients with nystagmus. Optom
basis for the use of memantine in the treatment of Vis Sci. 1992;69:447-450.
Alzheimer’s disease. CNS Drug Rev. 2003;9:275-308. 95. Stahl JS, Lehmkuhle M, Wu K, et al. Prospects for treating
75. Starck M, Albrecht H, Pollmann W, et al. Drug therapy acquired pendular nystagmus with servo-controlled optics.
for acquired pendular nystagmus in multiple sclerosis. Invest Ophthalmol Vis Sci. 2000;41:1084-1090.
J Neurol. 1997;244:9-16. 96. Smith RM, Oommen BS, Stahl JS. Image-shifting optics
76. Starck M, Albrecht H, Pollmann W, et al. Acquired pendu- for a nystagmus treatment device. J Rehabil Res Dev.
lar nystagmus in multiple sclerosis: an examiner-blind 2004;41:325-336.
3970_Ch14_249-265 25/06/14 11:44 AM Page 265
Chapter 14 • PHARMACOLOGICAL AND OPTICAL METHODS TO TREAT VESTIBULAR DISORDERS AND NYSTAGMUS 265
97. Smith RM, Oommen BS, Stahl JS. Application of adap- 103. Repka MX, Savino PJ, Reinecke RD. Treatment of ac-
tive filters to visual testing and treatment in acquired pen- quired nystagmus with botulinum neurotoxin A. Arch
dular nystagmus. J Rehabil Res Dev. 2004;41:313-324. Ophthalmol. 1994;112:1320-1324.
98. Spielmann AC. Large recession of the four vertical rectus 104. Cestari DM, Chan K, Tajouri N, et al. The use of onabot-
muscles for acquired pendular vertical nystagmus and oscil- ulinum toxin a in the treatment of see-saw nystagmus.
lopsia without a null zone. J AAPOS. 2009;13:102-104. J Pediatr Ophthalmol Strabismus. 2010;47:e1-e3.
99. Wang ZI, Dell’osso LF, Tomsak RL, et al. Combining 105. Di X. Endoscopic suboccipital decompression on
recessions (nystagmus and strabismus) with tenotomy pediatric Chiari type I. Minim Invasive Neurosurg.
improved visual function and decreased oscillopsia and 2009;52:119-125.
diplopia in acquired downbeat nystagmus and in horizontal 106. Baloh RW. Episodic ataxias 1 and 2. Handb Clin Neurol.
infantile nystagmus syndrome. J AAPOS. 2007;11:135-141. 2011;103:595-602.
100. Jain S, Proudlock F, Constantinescu CS, et al. Combined 107. Tsunemi T, Ishikawa K, Tsukui K, et al. The effect of
pharmacologic and surgical approach to acquired nystag- 3,4-diaminopyridine on the patients with hereditary pure
mus due to multiple sclerosis. Am J Ophthalmol. cerebellar ataxia. J Neurol Sci. 2010;292:81-84.
2002;134:780-782. 108. Frohman EM, Frohman TC, Zee DS, et al. The neuro-
101. Tomsak RL, Remler BF, Averbuch-Heller L, et al. Unsat- ophthalmology of multiple sclerosis. Lancet Neurol.
isfactory treatment of acquired nystagmus with retrobul- 2005;4:111-121.
bar injection of botulinum toxin. Am J Ophthalmol. 109. Shaikh AG, Hong S, Liao K, et al. Oculopalatal tremor
1995;119:489-496. explained by a model of inferior olivary hypertrophy and
102. Ruben ST, Lee JP, O’Neil D, et al. The use of botulinum cerebellar plasticity. Brain. 2010;133:923-940.
toxin for treatment of acquired nystagmus and oscillop-
sia. Ophthalmology. 1994;101:783-787.
3970_Ch15_266-280 25/06/14 11:45 AM Page 266
CHAPTER 15
Medical
Management
of Migraine,
Ménière’s Disease,
and Motion
Sensitivity
Ronald J. Tusa, MD, PhD
Migraine is a common cause of episodic vertigo and dis- had one or more migraine headaches per year.4 This study
equilibrium in children and adults. In practices treating used the diagnostic criteria recommended by the Interna-
patients with headaches, 27% to 33% of patients out of a tional Headache Society 5 (IHS, which is now referred to
population of 700 patients with migraine report episodic as ICHD6), which will be described later. Of those individ-
vertigo.1,2 Thirty-six percent of these patients e xperience uals with migraine, approximately 18% e xperienced one
vertigo during their headache-free period; the others e x- or more attacks per month. In both males and females, the
perience vertigo either just before or during a headache. prevalence of migraine w as highest between the ages
The occurrence of vertigo during the headache period is of 35 and 45 years. The type and severity of migraine often
much higher in patients with migraine headaches with varies within the same individual. Migraine with or without
aura (classic migraine) as opposed to migraine without aura frequently begins between 12 and 30 years of age.
aura (common migraine). 3 In this chapter, we describe After the age of 50, migraine is much less common, and it
the incidence of migraine; current classif ication and frequently presents as migraine aura without headache.7
criteria used for diagnosing migraine, neuro-otological
syndromes, and genetics related to migraine; and the
management of migraine. Migraine and International
Classification of Headache
Incidence of Migraine Disorders (ICHD)
Migraine is an extremely prevalent disorder. An epidemi- Migraine disorders are usually subdi vided into several
ological study involving over 20,000 individuals between 12 types. The classification of headache disorders w as ini-
and 80 years of age found that 17.6% of all adult tially published by an Ad Hoc Committee of NIH. 8 This
females, 5.7% of all adult males, and 4% of all children included short descriptions of the headache disorder types
266
3970_Ch15_266-280 25/06/14 11:45 AM Page 267
Chapter 15 • MEDICAL MANAGEMENT OF MIGRAINE, MÉNIÈRE’S DISEASE, AND MOTION SENSITIVITY 267
without a description of the criteria. In 1988, an interna- on the IHS website (http://www .ihs-headache.org/). The
tional committee developed a more comprehensive clas- classification and criteria for headaches pertinent to neuro-
sification with criteria for each headache disorder termed otological disorders is summarized in Box 15-1.
the International Classif ication of Headache Disorders
(ICHD).5 In most cases, the criteria for headache disorder
Migraine without Aura
was based on expert opinion. In 2004, the second version,
the ICHD-II, was published, which was based on clinical re- Migraine without aura (ICHD 1.1), which replaces
search trials published since the 1988 study.6 The ICHD-III “common migraine,” consists of periodic headaches that
version should be published in 2013 and will be accessible are usually throbbing and unilateral, e xacerbated by
Box 15-1
activity, and associated with nausea, photophobia, and Childhood Periodic Syndromes
phonophobia. These headaches are frequently referred
to as “sick” headaches (because of the nausea) or There are two neuro-otological disorders in children as
“sinus” headaches (because of their location). P atients a result of migraine. First, is benign paroxysmal vertigo
usually prefer to lie down in a quiet, dark room during of childhood (ICHD classif ication 1.3.3), which w as
the headache and feel better after sleep.A family history first described by Basser .13 This disorder consists of
for migraine can usually be obtained in the immediate spells of vertigo and disequilibrium without hearing loss
family. or tinnitus.14-18 The majority occurs between 1 and
4 years of age, b ut can occur an ytime during the f irst
decade. Vertigo and disequilibrium typically last for
Migraine with Aura minutes, but can last up to se veral hours. Patients may
Migraine with aura (ICHD 1.2), which replaces “classic experience visual disturbance, flushing, nausea, and
migraine,” is associated with transient neurological symp- vomiting. In the majority of cases, audiograms and
toms consisting of sensory, motor, or cognitive disor- caloric tests are normal. These patients also have a nor-
ders. These neurological disorders usually precede the mal electroencephalogram (EEG), and a normal physi-
headache, but may de velop during or follo wing the cal examination in between spells. Initially, headache is
headache. The neurological disorder usually lasts 5 to usually not a major feature of these spells. Man y of
20 minutes, but can last as long as 1 hour . There are these patients eventually develop migraine with aura
three relevant subtypes. The first is migraine with pro- and there is frequently a positi ve family history for
longed aura, in which neurological symptoms can last migraine. The differential diagnosis includes vestibular
up to 7 days. The second is called basilar migraine, epilepsy, perilymphatic fistula, posterior fossa tumors,
which replaces “basilar artery migraine, ” and presents and psychogenic disorders. The second childhood peri-
with symptoms in the distrib ution of the basilar artery odic syndrome, is benign paroxysmal torticollis (ICHD
including vertigo, tinnitus, decreased hearing, and A1.3.5. This disorder was first described by Snyder, 19
ataxia. The third is called migraine aura without and has now been reported by a number of indi vidu-
headache, which replaces “migraine-equivalent spells” als.20-22 Benign paroxysmal torticollis consists of spells
or “acephalgic migraine.” This presents with the neuro- of head tilt and rotation without vertigo, hearing loss, or
logical disorders found in migraine with aura, e xcept tinnitus. These usually occur in the f irst 5 years of
there is no headache. life and typically last between 10 minutes and se veral
days. They may be associated with nausea, v omiting,
pallor, agitation, and ataxia. In the majority of cases,
Basilar-Type Migraine audiograms and caloric tests are normal between
Basilar-type migraine (ICHD classif ication 1.2.6) was the spells. This syndrome is belie ved to be caused by
first described by Bick erstaff, 9 and has been subse- migraine auras without headache. Some indi viduals
quently reported by a number of indi viduals.10,11 This complain of headache when the y become older. The
disorder consists of two or more neurological problems differential diagnosis includes posterior fossa tumors
(vertigo, tinnitus, decreased hearing, ataxia, dysarthria, and torticollis.
visual symptoms in both hemif ields of both e yes,
diplopia, bilateral paresthesia or paresis, decreased level
of consciousness) followed by a throbbing headache.
Vestibular Migraine
The majority of these occurs before 20 years of age, but This disorder was not formally classif ied by the ICHD.
can occur up until age 60. Vertigo typically lasts Based on the symptoms, it may o verlap basilar-type
between 5 minutes and 1 hour. In the majority of cases, migraine.1,2,6 This was first described by Slater ,23 who
audiograms are normal. Many of these patients eventu- labeled it benign recurrent v ertigo in adults. This disorder
ally develop more typical migraine headaches with aura, consists of spells of v ertigo, and in some indi viduals,
and there is frequently a positi ve family history for jerk nystagmus may occur during the spell. 24,25 (see
migraine. Transient ischemic attacks (TIAs) need to be Case Studies 15-1 and 15-5 at end of the chapter). Vertigo
considered before basilar migraine is diagnosed. TIAs typically lasts from minutes to 72 hours with or without
within the vertebral-basilar circulatory system (v erte- headache. There is no vestibular defect or hearing loss noted
brobasilar insufficiency) may cause the same symptoms on electronystagmography (ENG) and audiogram from the
as basilar migraine, although TIAs usually last less than spell, which rules out vestibular neuritis and Ménière’s dis-
a few minutes.12 ease. The spells usually occur between the ages of 20 and
3970_Ch15_266-280 25/06/14 11:45 AM Page 269
Chapter 15 • MEDICAL MANAGEMENT OF MIGRAINE, MÉNIÈRE’S DISEASE, AND MOTION SENSITIVITY 269
60. Another type of vestibular migraine occurs in some in- Disorders Associated
dividuals who develop exercise-induced spells from a va-
riety of physical activity including sit-ups, heavy lifting, with Migraine
intercourse, and other strenuous aerobic e xercises26 (see Increased motion sickness and anxiety disorders are
Case Study 15-2). One needs to rule out Ménière’s disease, frequent in indi viduals with migraine. Both can cause
benign paroxysmal positional v ertigo (BPPV), TIAs, different types of dizziness that need to be recognized by
vestibular epilepsy, and perilymphatic f istula before the clinician.
making a diagnosis of migraine-induced v ertigo. The
diagnostic criteria for v estibular migraine has recently
been defined by a joint committee of the Baran y Society Motion Sickness
and subcommittee of the International Headache Society 27 Motion sickness consists of episodic dizziness, tiredness,
(Box 15-2). The criteria will appear as an appendix of the pallor, diaphoresis, salivation, nausea, and occasional vom-
third edition of the ICHD (still in discussion; publication iting induced by passive locomotion (e.g., riding in a car)
date unknown). or motion of the visual surround while standing still (e.g.,
viewing a rotating optokinetic stimulus or large screen mo-
tion picture). Motion sickness is partially caused by a visual-
Box 15-2 vestibular conflict or mismatch. 28 Twenty-six to sixty
percent of patients with migraine have a history of severe
DIAGNOSTIC CRITERIA FOR motion sickness compared with 8% to 24% of the normal
VESTIBULAR MIGRAINE population.1,3,29 The cause for this relation is not clear.
1.1 Vestibular Migraine
A. At least 5 episodes with vestibular symptoms Anxiety Disorders (DSM IV)
(vertigo that occurs spontaneously, or with Anxiety disorders are diagnosed using the DSM IV crite-
change in head position, or visually induced, or ria. More detail of these disorders and management can
head motion induced) of moderate or severe be found in Chapter 18.
intensity, lasting 5 min to 72 hr.
B. Current or previous history of migraine with or Generalized Anxiety Disorder
without aura according to the ICHD. This is characterized by generalized and persistent un-
C. One or more migraine features with at least realistic worry with motor tension, autonomic hyperac-
50% of the vestibular episodes: tivity, apprehensive expectation, and vigilance for over
a. Headache with at least 2 of the following 6 months.
characteristics: one-sided location, pulsat-
ing quality, moderate or severe pain inten-
sity, aggravation by routine physical
Panic Attacks
These are discrete spells of intense fear or discomfort and
activity,
greater than 4 symptoms that develop abruptly and peak in
b. photophobia and phonophobia,
10 minutes.
c. visual aura.
D. Not better accounted for by another vestibular • Dizziness, unsteady feelings or faintness
or ICHD diagnosis. • Nausea or abdominal distress
• Shortness of breath (or smothering sensations)
1.2 Probable Vestibular Migraine • Palpitations or tachycardia
A. At least 5 episodes with vestibular symptoms • Trembling or shaking
of moderate or severe intensity, lasting 5 min • Sweating
to 72 hr. • Choking
B. Only one of the criteria B and C for vestibular • Depersonalization or derealization
migraine is fulfilled (migraine history or • Numbness or paresthesias
migraine features during the episode). • Flushes (hot flashes) or chills
C. Not better accounted for by another vestibular • Chest pain or discomfort
or ICHD diagnosis. • Fear of dying
• Fear of going crazy or doing something
Adapted from consensus document of the Barany Society and the IHS.11 uncontrolled
3970_Ch15_266-280 25/06/14 11:45 AM Page 270
Chapter 15 • MEDICAL MANAGEMENT OF MIGRAINE, MÉNIÈRE’S DISEASE, AND MOTION SENSITIVITY 271
Scintillating scotoma 4
Serotonin 5HT1 Receptor and the
Diplopia 2 Headache Phase
Decreased consciousness 2 According to the neurogenic hypothesis, the headache
phase may be mediated by neurons containing serotonin
Chronic Symptoms (5-HT) within the trigeminal nucleus.39 5-HT is an intracra-
nial vasoconstrictor; it rises during the migraine aura and
Motion sickness/vestibular 78% falls during the headache. Platelet 5-HT levels drop rapidly
hypersensitivity during the onset of migraine. Through autoregulation,
blood flow is reduced to this area of neuronal dysfunction.
Generalized anxiety 57%
Agonists of these receptors block neuropeptide release and
disorder (GAD)
alter neurotransmission in trigemino vascular neurons.40
GAD + panic attacks 47% Serotonin 5-HT1 receptor agonists such as sumatriptan,
zolmitriptan, frovatriptan, almotriptan, eletriptan, rizatrip-
tan, and naratriptan are effective drugs in aborting migraine
headache.
Calcium Channel Receptor (CACNA1A)
The discovery of the genetic cause of a migraine aura
Management
phase (hemiplegic migraine) has been one of the most Management begins with identifying to what e xtent the
promising breakthroughs in understanding and potentially patient is suffering from spells as a result of vestibular mi-
treating this disorder. This aura causes transient hemi- graine, or more chronic symptoms caused by chronic anx-
paralysis. Familial hemiplegic migraine is an autosomal iety and increased motion sensitivity.
3970_Ch15_266-280 25/06/14 11:45 AM Page 272
■ Table 15-2 CACNA1A GENE DEFECTS THAT CAUSE AUTOSOMAL DOMINANT DISORDERS
Treatment of Vestibular Migraine include biofeedback and relaxation programs, which have
been shown to significantly reduce the frequenc y of re-
Spells of vertigo and disequilibrium secondary to migraine current migraine disorders in clinical trials.45 Patients are
usually respond to the same type of treatment as that used urged to avoid hypoglycemia by eating something at least
for migraine headaches. Migraine is triggered by a number every 8 hours. Many individuals skip breakfast; the need
of factors including stress, anxiety, hypoglycemia, fluctu- to eat breakfast at the same time each morning, including
ating estrogen, certain foods, and smoking.41-43 Treatment weekends, is emphasized. Finally, maintenance of a reg-
of migraine can be di vided into (1) the reduction of risk ular sleep schedule (going to bed and getting up at the
factors, (2) prophylactic medical therapy, and (3) abortive same time each day) is strongly recommended.
medical therapy.
Nicotine
Reduction of Risk Factors Patients who smoke cigarettes are urged to stop smoking.
Sometimes, in practice, patients with migraine are gi ven
a management schedule to follo w, which is e xplained at Estrogen
the time of their first visit (Box 15-3). It may be pointed If patients are taking estrogen supplements (other than
out that there are several triggers for migraine, which can vaginal creams), work with their gynecologist to either
be avoided by following the schedule. eliminate the supplement or reduce the estrogen to the
lowest level possible for a 3-month trial.
Stress
All patients are started on an aerobic e xercise program Diet
to help reduce stress. This program is gradually in- All patients are placed on a diet schedule, which is given
creased until the indi vidual is exercising 3 to 5 times to them in written form (Table 15-3). This diet eliminates
per week for at least 30 minutes at the end of the day foods containing high levels of tyramine and other sub-
(jogging, swimming, fast walk, racquetball, tennis, etc.). stances known to e xacerbate migraine.40,41,45 Some of
Several good aerobic exercise programs can be found in these foods cause migraine almost immediately (red wine,
a paperback book by Cooper.44 If patients are reluctant MSG); most cause migraine the next day (chocolate, nuts,
or unable to participate in an e xercise program, other cheese). Aspartame, found in NutraSweet, can also
stress reduction programs can be v ery helpful. These provoke migraine.46
3970_Ch15_266-280 25/06/14 11:45 AM Page 273
Chapter 15 • MEDICAL MANAGEMENT OF MIGRAINE, MÉNIÈRE’S DISEASE, AND MOTION SENSITIVITY 273
Beverages Chocolate and cocoa. Alcoholic All other beverages including: wine aged in metal
beverages aged in wood containers containers (including chardonnay and red wines of
(red wine, port, sherry, scotch, bour- the “Naked brand”); sugar-free, nonalcoholic with
bon, gin, chardonnay). Sugar-free, saccharin or Splenda
nonalcholic drinks with aspartame
or Nutrasweet)
Aged Cheese Cheeses: Stilton, bleu, cheddar, moz- Cheeses: American, cottage, farmer, ricotta, cream,
zarella, cheese spread, Roquefort, pro- Canadian, processed cheese slice
volone, gruyere, muenster, feta, parmesan,
emmenthal, brie, brick, camembert types,
cheddar, gouda, romano
Smoked Meats Ham, turkey, hot dogs, etc. (look for All meats without nitrates listed in ingredients
nitrates on the package)
Desserts Any product containing chocolate Any sweets without chocolate and nuts
and nuts
Miscellaneous Monosodium glutamate (MSG) in Salt in moderation, lemon juice, butter or mar-
Chinese, Mexican, and seafood. garine, cooking oil, whipped cream, white vinegar,
Also found in soups, Accent seasoning, commercial salad dressings
meat tenderizer, seasoned salt, yeast,
yeast extract
Chapter 15 • MEDICAL MANAGEMENT OF MIGRAINE, MÉNIÈRE’S DISEASE, AND MOTION SENSITIVITY 275
Box 15-4
EVIDENCE-BASED CRITERIA
Class I Evidence provided by a prospective, Level A Established as effective, ineffective,
randomized, controlled clinical trial or harmful for the given condition in
with masked outcome assessment, the specified population. (Level A
in a representative population. The rating requires at least two consistent
following are required: (a) primary Class I studies.)*
outcome(s) is/are clearly defined; Level B Probably effective, ineffective, or
(b) exclusion/inclusion criteria are harmful (or probably useful/predictive
clearly defined; (c) adequate account- or not useful/predictive) for the
ing for drop-outs and crossovers given condition in the specified
with numbers sufficiently low to population. (Level B rating requires
have minimal potential for bias; and at least one Class I study or two
(d) relevant baseline characteristics consistent Class II studies.)
are presented and substantially equiv-
Level C Possibly effective, ineffective, or
alent among treatment groups or there
harmful (or possibly useful/predictive
is appropriate statistical adjustments
or not useful/predictive) for the given
for differences.
condition in the specified population.
Class II Evidence provided by a prospective (Level C rating requires at least one
matched group cohort study in a rep- Class II study or two consistent
resentative population with masked Class III studies.)
outcome assessment that meets a–d
Level U Data inadequate or conflicting; given
above OR a randomized control trial
current knowledge, treatment is
in a representative population that
unproven.
lacks one criteria a–d
Class III All other controlled trials (including Class of evidence for therapy: “Class” refers to
well-defined natural history controls the quality of research methods employed in the
or patients serving as own controls) in reviewed literature.
a representative population, where
outcome assessment is independent of Recommendation Level: “Level” refers to the
patient treatment. strength of the practice recommendation based
Class IV Evidence from uncontrolled studies, on the reviewed literature.
case series, case reports, or expert
opinion.
Short nap usually helps Short naps usually do not help Patient Information
Glaxo Wellcome (1-800-377-0302) and http://www
Visual auras are Visual auras are uncommon
.healthylives.com/. Obtain free pamphlets including “Chart
common
Your Route to Relief: A Personal Migraine Management
Motion sickness is Motion sickness is Program.”
common uncommon For free ne wsletters, contact the National Headache
Foundation at 1-800-843-2256 and http://www.headaches.org/.
Chapter 15 • MEDICAL MANAGEMENT OF MIGRAINE, MÉNIÈRE’S DISEASE, AND MOTION SENSITIVITY 277
Continued
3970_Ch15_266-280 25/06/14 11:46 AM Page 278
Chapter 15 • MEDICAL MANAGEMENT OF MIGRAINE, MÉNIÈRE’S DISEASE, AND MOTION SENSITIVITY 279
3. Kuritzky A, et al. Vertigo, motion sickness and migraine. 30. Peroutka SJ. Dopamine and migraine. Neurology. 1997;
Headache. 1981;21:227. 49:650. 1998;43:711.
4. Stewart WF, et al. Migraine headache: prevalence in the 31. Shukla R, Khanna VK, Vinod P, Sankhwar, Yadav RS.
United States by age, income, race and other sociodemo- Platelet dopamine: D2 receptor binding in patients with
graphic factors. JAMA. 1992;267:64. migraine. Cephalagia. 2009;29:532-538.
5. Headache Classification Committee of the International 32. Peroutka SJ, et al. Comorbid migraine with aura, anxiety,
Headache Society. Classification and diagnostic criteria and depression is associaated with dopamine D2 receptor
for headache disorders, cranial neuralgias and facial pain. (DRD2) Ncol alleles. Mol Med. 1998;4:14-21.
Cephalalgia. 1988;8 (suppl 7):1-96. 33. Breslau N, Schultz LR, Stewart WF, Lipton R, Welch KM.
6. International Headache Society Classification Subcommit- Headache types and panic disorder: directionality and
tee. International Classification of Headache Disorders. specificity. Neurology. 2001;56:350-354.
2nd ed. Cephalalgia. 2004;24 (suppl 1):1-160. 34. Ophoff RA, et al. Familial hemiplegic migraine and
7. Fisher CM. Late-life migraine accompaniments as a cause episodic ataxia type-2 are caused by mutations in
of unexplained transient ischemic attacks. Can J Neurol the Ca2+ channel gene CACNL1A4. Cell. 1996;
Sci. 1980;7:9. 87:543.
8. Ad Hoc Committee on Classification of Headache. 35. May A, et al. Familial hemiplegic migraine locus on
Classification of headache. JAMA. 1962;179:717-718. 19p13 is involved in the common forms of migraine with
9. Bickerstaff ER. Basilar artery migraine. Lancet. 1961; and without aura. Hum Genet. 1995;96:604.
1:15. 36. Elliot MA, et al. Familial hemiplegic migraine, nystagmus
10. Eviatar L. Vestibular testing in basilar artery migraine. and cerebellar atrophy. Ann Neurol. 1996;39:100.
Ann Neurol. 1981;9:126. 37. Main A, Dowson A, Gross M. Photophobia and phonopho-
11. Harker LA, Rassekh CH. Episodic vertigo in basilar artery bia in migraineurs between attacks. Headache.
migraine. Otolaryngol Head Neck Surg. 1987;96:239. 1997;37:492-495.
12. Grad A, Baloh RW. Vertigo of vascular origin: clinical and 38. Vingen JV, et al. Phonophobia in migraine. Cephalalgia.
oculographic features. Arch Neurol. 1989;46:281.12 1998;18:243-249.
13. Basser LS. Benign paroxysmal vertigo of childhood. 39. Moskowitz MA, et al. Neocortical spreading depression
Brain. 1964;87:141. provokes the expression of c-fos protein-like immunoreac-
14. Fenichel GM. Migraine as a cause of benign paroxysmal tivity within trigeminal nucleus caudalis via trigeminovas-
vertigo of childhood. J Pediatr. 1967;71:114. cular mechanisms. J Neurosci. 1993;13:1167.
15. Koenigsberger MR, et al. Benign paroxysmal vertigo of 40. Goadsby PJ, Hoskin KL. Serotonin inhibits trigeminal
childhood. Neurology. 1970;20:1108. nucleus activity evoked by craniovascular stimulation
16. Lanzi G, et al. Benign paroxysmal vertigo of childhood: a through a 5-HT receptor: a central action in migraine?
long-term follow-up. Cephalgia. 1994;14:458. Ann Neurol. 1998;43:711.
17. Parker W. Migraine and the vestibular system in childhood 41. Diamond S. Dietary factors in vascular headache. Neurol
and adolescence. Am J Otol. 1989;10:364. Forum. 1991;2:2.
18. Watson P, Steele JC. Paroxysmal disequilibrium in the 42. Kin T. Discussion, ideas abound in migraine research:
migraine syndrome of childhood. Arch Otolaryngol. consensus remains elusive. JAMA. 1987;257:9.
1974;99:177. 43. Silberstein SD, Merriam GR. Estrogens, progestins,
19. Snyder CH. Paroxysmal torticollis in infancy. Am J Dis and headache. Neurology. 1991;41:786.
Child. 1969;117:458. 44. Cooper KH. The Aerobics Way. New York: Bantam Books;
20. Gourley IM. Paroxysmal torticollis in infancy. Can Med 1997:312.
Assoc J. 1971;105:504. 45. Holroyd KA, Penzien DB. Pharmacological versus
21. Hanukoglu A, et al. Benign paroxysmal torticollis in non-pharmacological prophylaxis of recurrent migraine
infancy. Clin Pediatr. 1984;23:272. headache: a meta-analytic review of clinical trials. Pain.
22. Lipson EH, Robertson WC. Paroxysmal torticollis of in- 1990;42:1.
fancy: familial occurrence. Am J Dis Child. 1978;132:422. 46. Shulman KI, et al. Dietary restrictions, tyramine, and the
23. Slater R. Benign recurrent vertigo. J Neurol Neurosurg use of monoamine oxidase inhibitors. J Clin Psychophar-
Psychiatry 1979;42:363. macol. 1989;9:397.
24. Harker LA, Rassekh CH. Migraine equivalent as a cause 47. van Den Eeden SK, et al. Aspartame ingestion and
of episodic vertigo. Laryngoscope. 1988;98:160. headaches: a randomized crossover trial. Neurology.
25. Moretti G, et al. “Benign recurrent vertigo” and its connec- 1994;44:1787.
tion with migraine. Headache. 1980;20:344. 48. Silberstein SD, Holland S, Freitag F, et al. Evidence-based
26. Imes RK, Hoyt W. Exercise-induced transient visual guideline update: pharmacologic treatment for episodic
events in young healthy adults. J Clin Neuro-ophthalmol. migraine prevention in adults. Neurology. 2012;78;
1989;9:178. 1337-1345.
27. Lembert T, Olesen J, Furman J, Waterston J, et al. Vestibu- 49. Holland S, Silberstein SD, Freitag F, et al. Evidence-based
lar migraine: diagnostic criteria. J Vestibular Res. guideline update: NSAIDs and other complementary
2012;22:167-172. treatments for episodic migraine prevention in adults. Neu-
28. Brandt T, Daroff RB. The multisensory physiological and rology. 2012;78:1346-1353.
pathological vertigo syndromes. Ann Neurol. 1980;7:195. 50. AAN therapeutic classification of evidence scheme
29. Childs AJ, Sweetnam MT. A study of 104 cases of migraine. (appendix e-3 on the Neurology® Web site at www
Br Industr Med. 1961;18:234. .neurology.org).
3970_Ch15_266-280 25/06/14 11:46 AM Page 280
51. Bikhazi P, et al. Efficacy of antimigrainous therapy in the 57. Hinchcliffe R. Headache and Ménière’s disease. Acta
treatment of migraine-associated dizziness. Am J Otol. Otolaryngol (Stockh). 1967;63:384.
1997;18:350. 58. Radtke A, Lempert T, Gresty MA, Brookes GB, et al.
52. Johnson GD. Medical management of migraine-related Migraine and Meniere’s disease. Is there a link?
dizziness and vertigo. Laryngoscope. 1998;108:1. Neurology. 2002;59:1700-1704.
53. Baloh RW, et al. Familial migraine with vertigo and essen- 59. Neuhauseer HK, Radtke A, von Brevern M, et al.
tial tremor. Neurology. 1996;46:458. Migrainous vertigo: prevalence and impact of quality
54. Migraine headache. AAN summary of evidence-based of life. Neurology. 2006;67:1028-1033.
guideline for clinicians. St. Paul, Minn: American 60. Wladslavosky-Waserman P, Facer G, et al. Meniere’s
Academy of Neurology; 2009. https://www.aan.com/ disease: a 30-year epidemiologic and clinical study in
Guidelines/Home/GetGuidelineContent/120. Rochester, MN, 1951-1980. Laryngoscope. 1984;94:
55. Baloh RW. Neuro-otology of migraine. Headache. 1098-1102.
1997;37:615.
56. Dornhoffer JL, Arenberg IK: Diagnosis of vestibular
Ménière’s disease with electrocochleography. Am J Otol.
1993;14:161.
3970_Ch16_281-284 25/06/14 11:47 AM Page 281
CHAPTER 16
Medical
Management
of Mal De
Debarquement
Syndrome
Timothy C. Hain, MD ■ Janet O. Helminski, PhD, PT
Mal de débarquement syndrome (MDDS), literally, “sick- Table 16-2 lists the features that distinguish MDDS
ness of disembarkment,” refers to prolonged and inappro- from simple land-sickness. Land-sickness is common, and
priate sensations of movement after exposure to motion. between 41% and 73% of persons disembarking from seago-
The syndrome typically follows a 7-day sea voyage, but ing voyages experience a brief unsteadiness syndrome. 3-5
it has also been observ ed following extended airplane Common land-sickness typically persists for 2 days or
travel, train travel, and space flight. 1 Symptoms include less. Persons with land-sickness are also likely to have sea-
rocking and swaying accompanied by imbalance. MDDS sickness,5 although persons with MDDS generally are un-
is distinguished from ordinary motion sickness, seasick- troubled by seasickness. Males and females do not appear
ness (mal de mer), and “land-sickness” by persistence of to differ significantly in the incidence, intensity, or duration
symptoms for a month or longer . Additionally, unlike of land-sickness symptoms.3 Land-sickness (or LDS), con-
disorders of the inner ear, most individuals with MDDS fusingly, is also termed “mal de debarquement” by some.
report that their symptoms remit with re-e xposure to Table 16-1 does not include reports or data concerning sub-
motion, such as driving a motor vehicle.2 A typical case jects whose symptoms last less than 1 month (i.e., potential
history is as follows: A 50-year-old woman went on her land-sickness), except for the work of Cha, in whom the du-
first ocean cruise. She had some motion sickness on the ration of symptoms in patients with “classic” MDDS could
cruise, which responded to transdermal scopolamine. not be determined due to study design.2
Immediately after returning from the cruise and getting MDDS also has some similarities to motion sickness
onto solid ground, she developed imbalance and a rocking (mal de mer). However, MDDS again is easily distinguished
sensation, accompanied by fatigue and difficulty concen- by the relatively short duration of motion sickness and gen-
trating. Her description was “Imagine feeling like you are der distribution. Persons with MDDS reliably have relief of
on rough seas 24 hours a day, 7 days a week.” symptoms when in motion, such as driving a car, but expe-
Table 16-1 summarizes the a vailable literature rience recurrence of rocking once motion has stopped.2,6 In
about MDDS. It is a disorder that mainly affects women motion sickness, many persons find driving very difficult.
(87%) in their mid-40s. Symptoms last at least 1 month This is also often true for persons with vestibular disorders.
and most frequently abate before 6 months have elapsed MDDS also overlaps with a little-studied group of
(median 4.1 mo). patients called “rockers,” who develop similar symptoms
281
3970_Ch16_281-284 25/06/14 11:47 AM Page 282
optimal. A potential solution that also explains the persis- affect anticholinergic pathways such as meclizine and
tence of symptoms is that, in MDDS, there is prediction of transdermal scopolamine are not helpful in MDDS. 6
boat motion through an internal model of boat motion— Benzodiazepines, such as clonazepam, are of the most
an internal oscillator. One should ignore ankle inputs that benefit,6,10 and selective serotonin reuptak e inhibitor
are entrained with boat rocking, but one should compen- (SSRI)-type antidepressants are also suggested as being
sate for input that is uncorrelated with boat rocking. An potentially helpful.10 There are also anecdotal reports
internal model of periodic boat motion—an internal oscil- of good responses to gabapentin, amitriptyline, and
lator that is entrained by boat motion—might allo w one venlafaxine—all medications that are also helpful in
to select out salient sensory input (boat surge) and ignore migraine.
the non-salient input (boat pitch). In support of this idea, After 6 months have gone by, if the MDDS patient
some animals e xhibit persistent oscillations in central is no better, there is more pressure to find another inter-
neurons after periodic mo vement ends.12 Also, post- vention. While vestibular physical therapy would seem
movement illusions of rocking can be induced by sinu- reasonable, Cha commented in passing that “only rare
soidal rotation in some indi viduals.13 Such an internal patients seem to be cured by v estibular therapy.”10 In
oscillator might result in persistent rocking when there is fact, the only literature describing physical therapy treat-
no ongoing periodic motion. ment for MDDS is a single case report. 16 Of course, it
With respect to the hypothesis that MDDS is caused is not known how this case would have done without in-
by reweighting of visual, v estibular, or somatosensory tervention. In general, although man y individuals with
input, the data so far is contradictory. Nachum and asso- MDDS undergo vestibular rehabilitation, again because
ciates used posturography to study young males aged 18 of a lack of controls, it is not possible to determine
to 22 with motion sickness and land-sickness (the y con- whether they did any better than persons who were not
sidered land-sickness to be equivalent to mal de debarque- treated.6 Thus the efficacy of vestibular rehabilitation for
ment in their paper). They reported that these young men MDDS is unknown.
developed increased reliance on somatosensory input after Our view is that MDDS was acquired from motion,
motion exposure, and reduced weighting of vision and and it should be possible to f ind an approach that e xtin-
vestibular input.14 Although the accuracy of visual input guishes MDDS too. But what should this procedure in-
depends on whether one is inside the boat or on the deck, clude? Because no compelling or controlled studies have
semicircular canal input is accurate on boats, and so- been published to date, conjectures re garding treatment
matosensory input is intermittently accurate. Accordingly, are speculative.
it is difficult to understand a rationale for this adaptation. Motion sickness has been treated successfully with ha-
An intrinsic problem with this study is that the study group bituation,17 and one might reasonably argue that if MDDS
was young men with motion sickness and land-sickness, is a motion sickness v ariant, it might also respond to a
not middle-aged women with the month or greater MDDS similar approach. Habituation entails a down-weighting of
syndrome. motion input and can reduce the long-duration v estibular
A more reasonable possibility is that indi viduals responses commonly associated with motion sickness sus-
with MDDS may develop an increased reliance on visual ceptibility.18 Although there are well developed self-directed
and vestibular information (and thus decreased so- motion habituation protocols, such as the PUMA e xer-
matosensory weighting). This occurs in normal subjects cises,19 there are presently no reports of their ef ficacy in
who are exposed to situations in which somatosensory MDDS. Because patients with MDDS initially became ill
feedback is distorted and w ould also be a reasonable after repetitive motion exposure, the possibility exists that
adaptation to boat pitch.15 Either adaptation might result more motion exposure as is required for habituation might
in inaccurate land sensorimotor inte gration. Neverthe- worsen MDDS.
less, neither of these adaptations e xplains the rocking Based on the present theories of mechanism, there
sensation of MDDS or the characteristic impro vement are several treatment strategies that might be attempted
on driving a car. in MDDS. As outlined in the section above, two theories
applicable to MDDS dif fer in the conjecture re garding
weighting of somatosensory input (one too much, one
Treatment of MDDS too little), and a third proposes that a central internal os-
The usual treatment strategy for MDDS is to attempt to cillator is the source. Accordingly, if during one’s assess-
make the patient comfortable, while w aiting for the ment of the patient, one determines that somatosensory
MDDS to end by itself (typically within 6 months, see weighting is inappropriate, one might attempt a specific
Table 16-1). Conventional vestibular suppressants that intervention.
3970_Ch16_281-284 25/06/14 11:47 AM Page 284
For example, if the individual disregards propriocep- 2. Cha YH, et al. Clinical features and associated syndromes
tive information in sitting, the indi vidual should practice of mal de debarquement. J Neurol. 2008;255(7):1038-1044.
3. Cohen H. Mild mal de debarquement after sailing. Ann N
detecting joint position sense and kinesthetic a wareness
Y Acad Sci. 1996;781:598-600.
of the toes and ankles with the eyes closed. Once there is 4. Gordon CR, Shupak A, Nachum Z. Mal de debarquement.
heightened awareness of joint position sense, the individ- Arch Otolaryngol Head Neck Surg. 2000;126(6):805-806.
ual should use the sensory information during a dynamic 5. Gordon CR, et al. Clinical features of mal de debarque-
task. While standing on a f irm surface with the e yes ment: adaptation and habituation to sea conditions. J Vestib
Res. 1995;5(5):363-369.
closed, the individual may dynamically shift weight ante-
6. Hain TC, Hanna PA, Rheinberger MA. Mal de debarque-
rior to posterior for 1 to 2 minutes and then side to side ment. Arch Otolaryngol Head Neck Surg. 1999;125(6):
for 1 to 2 minutes. The individual may then be ask ed 615-620.
to walk with e yes closed on mats with objects placed 7. Brown, J. J. and R. W. Baloh (1987). "Persistent mal de
randomly beneath the mat to increase focus on the debarquement syndrome: a motion-induced subjective
disorder of balance."American Journal of Otolaryngology
somatosensory information.
8(4): 219-222.
For persons who o verweight motion information, 8. Murphy, T. P. (1993). "Mal de debarquement syndrome: a
one’s efforts might be reasonably directed to ward down- forgotten entity? "Otolaryngology-Head & Neck Surgery
weighting the inputs. Here, ab undant movement stimuli 109(1): 10-13.
bringing the person to the edge of their tolerance, such as 9. Mair I. The mal de debarquement syndrome. Journal of
Audiological Medicine. 1996;5:21-25.
visual or vestibular habituation protocols, might reduce
10. Cha YH. Less common neuro-otologic disorders.
the size and duration of their motion responses and thus Minneapolis, MN: Continuum. Neuro-otology. 2012;
reduce symptoms. 18(5):1142-1157.
If MDDS is instead caused by an internal oscillator 11. Wassmer E, et al. Clinical spectrum associated with cere-
developed to predict boat motion, one’s treatment strat- bellar hypoplasia. Pediatr Neurol. 2003;28(5):347-351.
12. Barmack NH, Shojaku H. Vestibularly induced slow
egy should be aimed at manipulation of psychological
oscillations in climbing fiber responses of Purkinje cells
variables rather than somatosensory integration. Patients in the cerebellar nodulus of the rabbit. Neuroscience.
need to ignore their aberrant internal signal, in the same 1992;50(1):1-5.
way that most persons with tinnitus eventually develop 13. Lewis RF. Frequency-specific mal de debarquement.
an ability to ignore abnormal internally generated Neurology. 2004;63(10):1983-1984.
14. Nachum Z, et al. Mal de debarquement and posture:
sounds. Treatments that decrease vigilance, obsessi ve-
reduced reliance on vestibular and visual cues. Laryngo-
ness, and anxiety, as well as “tincture of time, ” would scope. 2004;114(3):581-586.
be the optimum strate gy. If this conjecture is correct, 15. Peterka, RJ. Sensorimotor integration in human postural
therapy that focuses attention on the rocking sensation control. J Neurophysiol 2002; 88(3): 1097-118.
could even be counterproductive. 16. Zimbelman JL, Watson TM. Vestibular rehabilitation of
a patient with persistent mal de debarquement. Physical
Therapy Case Reports. 1992;2(4):129-133.
Summary 17. Dai M, Raphan T, Cohen B. Prolonged reduction of mo-
tion sickness sensitivity by visual-vestibular interaction.
MDDS is an uncommon disorder in which indi viduals, Exp Brain Res. 2011;210(3-4):503-513.
mainly women in their mid-40s, develop an inappropriate 18. Dai M, Raphan T, Cohen B. Labyrinthine lesions and
motion sickness susceptibility. Exp Brain Res. 2007;
sensation of rocking, paradoxically relieved by actual mo-
178(4):477-487.
tion such as driving. Research is needed to establish the 19. Puma S. Puma method for prevention of motion sickness.
role of physical therapy in the treatment of MDDS. 2010. [Retrieved 1/12/2013]; Available from: http://www
.pumamethod.com/index.php.
References
1. Stott J. Adaptation to nauseogenic motion stimuli and its
application in the treatment of airsickness. In: Crampton
GH, ed. Motion and Space Sickness. Boca Raton, FL:
CRC Press; 1990.
3970_Ch17_285-295 25/06/14 11:50 AM Page 285
CHAPTER 17
Surgical
Management of
Vestibular Disorders
Yew Ming Chan, FRCS Edinburgh, FAMS ■ Douglas E. Mattox, MD
The diagnosis of v estibular disorders is complicated by unilateral sensorineural hearing loss. Ho wever, some
overlapping symptoms among the v arious disorders and patients first complain of vestibular symptoms, sudden hear-
the lack of pathognomonic diagnostic tests. At times, de- ing loss, or occasionally trigeminal symptoms.2
termining which inner ear is causing the symptoms may An acoustic neuroma should be suspected in any patient
even be difficult. Most patients’ symptoms can be managed with an unexplained unilateral sensorineural hearing loss,
with the medical and physical therapy measures described particularly if the patient has discrimination scores incon-
elsewhere in this book. However, surgical intervention may sistent with pure tone audiometry , abnormal brainstem
be appropriate when the symptoms have failed to respond auditory responses, or hypoactive/absent caloric responses.
to aggressive nonsurgical medical management. Magnetic resonance imaging (MRI) with gadolinium con-
With the exception of acoustic tumors, vestibular dis- trast has become the “gold standard” for the diagnosis of
orders are a matter of lifestyle and comfort and are not life these tumors. Although there are rare instances of f alse-
threatening. Therefore, it must be the patient living with the positive results, usually from arachnoiditis, an enhancing
symptoms who makes the decision whether or not to pro- mass in the cerebellopontine angle e xtending into the
ceed with surgery. The physician should discuss the likeli- internal auditory meatus on MRI is almost al ways an
hood of a successful outcome and the nature and likelihood acoustic neuroma. Meningiomas occasionally occur in the
of potential complications, and must leave the ultimate de- CPA or IAC. Radiologically, they frequently have a dural
cision up to the patient. In the authors’ experience, patients “tail” and are acentric to the IAC.
have a broad spectrum of responses to their symptoms of Once the diagnosis is established, there are three ther-
vertigo. Some patients want immediate intervention; others apeutic options: watchful waiting, microsurgical removal,
consider surgery only when life becomes unbearable. and stereotactic radiosurgery (SRS). Watchful waiting is
indicated only in patients with small intracanalicular
Vestibular Schwannoma (Acoustic tumors for which the diagnosis is inconclusi ve, and in
patients who are elderly or in poor medical condition. Sev-
Neuroma) eral recent series have reported the results of this approach.
Acoustic neuromas are nerve sheath tumors occurring in the Wiet and colleagues3 found that in 40% of 53 patients, con-
internal auditory canal (IA C) or cerebellopontine angle tinued growth of tumors required intervention over a mean
(CPA).1 They are the third most common intracranial tumor, follow-up of about 3 years. More frightening is an experi-
accounting for 8% to 10% of all intracranial tumors. Most ence reported by Charabi and associates. 4 In their series,
patients with acoustic neuromas present with progressi ve 34% of 123 patients follo wed for a mean of 3.4 years
285
3970_Ch17_285-295 25/06/14 11:50 AM Page 286
required intervention for enlarging tumor and 7 died of mastoid air-cell system, and superior semicircular canal are
brainstem compression secondary to the tumor. Therefore, important landmarks. The bone is thinned o ver the entire
it may be concluded that there is a significant risk of tumor extent of the internal auditory canal, and then the dura of
enlargement, and if a “wait-and-see” approach is taken, the the canal is incised. Care is taken not to damage the facial
importance of serial scanning at 6- to 12-month interv als nerve in the anterior superior quadrant of the internal audi-
must be emphasized to the patient. tory canal. The cochlear nerve is anterior-inferior in the
canal and safely out of harm’s way.
The advantage of the middle cranial fossa approach
Surgical Approaches is that it does not destroy the inner ear and hearing. Care
Surgical removal of acoustic tumors has been the treat- must be taken to avoid damaging the facial nerve, because
ment of choice since described by Harv ey Cushing5 in it is superficial in the dissection. Managing tumors that
1917. The three basic approaches used for remo val extend through the porus acusticus into the posterior fossa
of acoustic neuromas are (1) middle fossa craniotomy , with use of the middle cranial fossa approach is v ery
(2) translabyrinthine approach, and (3) suboccipital cran- difficult. This approach, therefore, is indicated only for
iotomy.6,7 The choice of approach is based on the size tumors limited to the internal auditory canal.
and location of the tumor and whether an y attempt will Recovery after middle fossa craniotomy is prompt. Un-
be made to preserve hearing.6,7 less the patient has signif icant vestibular symptoms, he or
she should be up and about the next day. Cerebrospinal fluid
(CSF) leakage is unlikely, but the patient should be checked
Middle Cranial Fossa for both external leak and a leak do wn the eustachian tube
The middle cranial fossa approach is used for tumors con- into the nasopharynx after under going surgery via this
fined to the internal auditory canal in patients who have us- approach and all other approaches described in this section.
able hearing (Fig. 17.1). A vertical incision is made in the
scalp superior to the external auditory canal. The soft tissues
Translabyrinthine Approach
are elevated from the bone and a 3 × 4 cm temporal cran-
iotomy is performed. The dura is elevated from the floor of The translabyrinthine approach is the procedure of choice
the middle cranial fossa. The internal auditory canal is iden- for tumors up to 3.0 cm in diameter when hearing preser-
tified by drilling the bone o verlying it. The facial nerve, vation is not a consideration (Fig. 17.2). The tumor is
Figure 17.1 Middle fossa. This coronal section through the internal auditory canal and
middle ear shows the exposure of the internal auditory canal through the middle fossa. A
drill is shown passing through a small temporal craniotomy. The temporal lobe is elevated
extradurally. The superior semicircular canal is identified, and the internal auditory canal is
exposed by removal of the bone over the auditory canal medial to the superior semicircular
canal.
3970_Ch17_285-295 25/06/14 11:50 AM Page 287
approached as in a standard mastoidectomy. The cortical can be spared in one-third to one-half of the patients in
and pneumatized bone of the mastoid are drilled a way to whom this approach is attempted.8
expose the sigmoid sinus, posterior fossa dura, and middle The suboccipital craniotomy dif fers from the
fossa dura. The facial nerve is protected by identification translabyrinthine approach in that the angle of the ap-
within its bony canal. A complete labyrinthectomy is per- proach is from behind rather than in front of the sigmoid
formed to expose the internal auditory canal. Once the in- sinus. The incision is placed 5 to 6 cm behind the ear, and
tracanalicular portion of the tumor is mobilized, the dura a 5 cm opening is made in the occipital skull.This defect
of the posterior fossa is incised, and the remainder of the is reconstructed with prosthetic mesh at the end of the
tumor is removed. The translabyrinthine approach can be procedure.
extended by combining it with a temporal/retrosigmoid The cerebellum lies between the craniotomy and the
craniotomy for larger tumors. CPA; however, the operation is performed with the patient
Recovery after translabyrinthine removal of acoustic in the lateral position, allowing the cerebellum to fall away
tumors is generally prompt, and patients can be out of bed by itself without additional retraction.
in 2 to 3 days. This rapid recovery is attributable to the After the tumor is identified, the capsule of the tumor
lack of pressure or retraction of the cerebellum during the is incised, and the central core of the tumor is remo ved
procedure. The disadvantage of the translabyrinthine ap- with hand instruments, an ultrasonic aspirator or laser .
proach is that hearing is automatically sacrificed. The ex- After the tumor has been decompressed, the portion of the
posure is excellent for small and medium-sized tumors but tumor within the IAC is removed by drilling away the pos-
is inadequate for tumors more than 3 cm in diameter and terior surface of the canal. The facial nerve is identified in
for those that are adherent to the brainstem. In the ideal the fundus of the IAC where its anatomy is constant. The
case for translabyrinthine removal, computed tomography tumor is mobilized from the brainstem, and the eighth
(CT) or MRI shows a clear separation between the tumor nerve is identified medial to the tumor.
and the brainstem. Recovery time after a suboccipital craniotomy is
longer than from the other two approaches because of the
magnitude of the procedure, but patients are usually ready
Suboccipital Craniotomy (Retrosigmoid for discharge from the hospital within a week. Occasion-
Approach) ally, a patient experiences a postcraniotomy headache that
Suboccipital craniotomy is used for medium and large tu- requires long-term pain management.
mors (Fig 17.3). In rare cases in which there is good hear-
ing preoperatively, the suboccipital approach of fers the
Complications
possibility of preserving hearing. Maintenance of hearing
requires the preservation of both the cochlear nerv e and Severe complications after acoustic neuroma sur gery are
the fragile capillary blood supply of the inner ear. Hearing relatively uncommon. Hearing loss al ways occurs in
3970_Ch17_285-295 25/06/14 11:50 AM Page 288
translabyrinthine procedures and is common after suboc- hearing from 69% pretreatment to 6.7% at a mean of
cipital removal of tumors lar ger than 1.5 cm. Transient 4 years after SRS.
facial paralysis is common with larger tumors. Permanent Despite successful outcome in the majority of
facial paralysis is seen in fewer than 5% of patients. CSF patients treated with SRS, a small fraction of patients
leaks can occur postoperatively but are usually transient have continued growth of the tumor and require surgical
and rarely require secondary surgical correction. salvage. Several authorities ha ve commented on the
increased difficulty of surgical dissection after SRS. A
case-matched study by Limb and colleagues 14 showed
Stereotactic Radiosurgery severely increased fibrosis of the tumor, more difficult
SRS was introduced by Leksell 9 in 1971 and has gained dissection of the facial and lower cranial nerves from the
wide popularity in the last few years. In this procedure, a tumor capsule, longer operative times, and poorer facial
single treatment of high-dose irradiation is administered nerve outcomes for sur gery after irradiation. The ideal
by stereotactically focused multiple radiation sources or indications for microsurgical removal versus stereotactic
arced beams focused on the tumor. The tumor receives an radiosurgery for acoustic tumors remain contentiously
extremely high radiation dose (currently 12 Gy for single debated. I recommend sur gical removal of tumors in
treatment protocols), although the surrounding neural and younger patients, of medially placed tumors, which tend
vascular structures are spared. to grow faster, of tumors larger than 3 cm or with signif-
The results of radiosurgery are encouraging. Tumor icant brainstem compression, and of small tumors in
control is achieved in 70% to 80% of patients, and the patients with a le gitimated chance of hearing preserv a-
procedure has a lo w incidence of complications, espe- tion. SRS is ideal for middle-aged and elderly patients
cially facial paralysis.10,11 Pollock and coworkers12 com- and patients with medical problems that make them poor
pared the results of SRS and microsur gical removal in surgical risks.
87 patients (40 surgery, 47 SRS). The results for surgery
versus SRS, respectively, were as follows: tumor control,
98% versus 94%; preservation of hearing, 14% versus 75%;
Ménière’s Disease
and normal facial function, 63% v ersus 83%. Longer- Although the underlying etiology of Ménière’ s disease is
term follow-up is not as encouraging for hearing preser- unknown, a consistent histopathological finding is hydrops
vation. Lin and associates 13 found a drop in serviceable (dilation) of the endolymphatic spaces. 15 The hydrops
3970_Ch17_285-295 25/06/14 11:50 AM Page 289
presumably results from a malfunction of the resorpti ve therapy achieves better long-term control of v ertigo in
function of the endolymphatic sac. The classic constella- Ménière’s disease.19
tion of symptoms includes fluctuating hearing loss,
episodic vertigo, tinnitus, and a sensation of fullness in the Endolymphatic Sac Surgery
ear.16 These symptoms do not necessarily de velop simul- Endolymphatic sac procedures attempt to reestablish the
taneously, however, and many patients do not e xperience function of the sac as the resorpti ve organ for the en-
all of them. Subcate gories of Ménière’s disease describe dolymph of the inner ear by draining the e xcess endolym-
these other conditions—for instance, cochlear hydrops phatic sac into the mastoid cavity.20 A standard postauricular
(fluctuating hearing loss alone) and v estibular hydrops mastoidectomy is performed, and the sigmoid sinus, mas-
(vestibular symptoms without hearing loss). toid antrum and incus, facial nerve, and lateral and posterior
In most patients, Ménière’s disease is ultimately self- semicircular canals are identified. The endolymphatic sac
limited; over time, the patient suffers deterioration of hear- is found between the posterior surface of the temporal bone
ing and a gradual subsiding of the episodic dizzy spells. and the dura of the posterior fossa.The bone is thinned until
This evolution, however, may require 10 or 20 years. In the the dura and the sac are identif iable through the last layer
interim, the patient’s lifestyle may be severely impaired. of bone. This bone is picked away to expose the dura and
Medical therapy of Ménière’s disease rests on avoid- the overlying endolymphatic sac. The sac is opened, and
ing factors known to exacerbate the symptoms: stress, caf- polymeric silicone (Silastic) sheeting or another shunt
feine, alcohol, nicotine, and foods high in salt. Diuretics device is inserted into the lumen of the endolymphatic sac
and vestibular suppressant drugs are usually prescribed. and allowed to drape into the mastoid cavity. Care must be
This regimen, known as the Furstenberg regimen, can ad- taken to open the endolymphatic sac without puncturing the
equately control the symptoms in up to three-quarters of underlying dura and thereby possibly causing a CSF leak.
patients.17 A few patients, however, cannot be adequately Any endolymph drained by the shunt is resorbed by the
managed by medical means alone, and surgical interven- mucous membranes of the mastoid cavity.
tion must be considered. The surgical procedures for It is an understatement to say that endolymphatic sac
Ménière’s disease may be cate gorized as those designed surgery is controversial. The fluid spaces involved are mi-
to improve the function of the endolymphatic sac and nuscule, and many investigators are skeptical about the
those that ablate the v estibular system, with or without ability of mechanical means to impro ve function of the
preservation of hearing. sac. In a clinical trial, similar results were obtained with
real and sham operations. 21 Nonetheless, the procedure
seems to control the vertiginous attacks in one-half to two-
Surgical Management of Ménière’s thirds of patients and has the adv antage of relative ease,
Disease safety, and preservation of hearing.
Transtympanic Steroids
Transtympanic steroid therapy has been advocated for the
Ablative Procedures—Chemical
treatment of vertigo symptoms in Ménière’s disease and
and Surgical Labyrinthectomy
idiopathic sudden sensorineural loss. An extensive review
had difficulties making definitive recommendations be- In all the ablative procedures described below, the implicit
cause of the heterogeneous nature of the data related to belief is that the disease is unilateral or, if disease is bilat-
individual drugs, drug doses, and frequency of injection.18 eral, the side producing the majority of symptoms can be
Certainly, intratympanic steroid treatment has a role in determined. Surgical procedures are seldom, if ever, indi-
Ménière’s patients with bilateral disease or when the cated in patients who have active bilateral disease.
physician is treating the only hearing ear . The choice of Special care should be taken with any of the abla-
type of steroid injection is between de xamethasone and tive techniques in patients with bilateral or contralateral
methyl prednisolone. We prefer two to three injections labyrinthine hypofunction. A patient left with bilateral
per week for 2 weeks of de xamethasone 4 mg/ml. Usu- vestibular loss may have chronic disequilibrium, significant
ally, 0.4 to 0.5 mL can be injected into the middle ear difficulty walking in the dark, and inability to keep the eyes
space, and the patient is advised to rest in a supine posi- fixed on a target during head movements (oscillopsia).22
tion for 45 minutes with head turned 30 de grees to the
unaffected side.
Chemical Labyrinthectomy
Although middle ear infusion of steroids may have a
role in amelioration of Ménière’s symptoms, our experi- Chemical labyrinthectomy with aminoglycosides has
ence concurs with others that intratympanic gentamicin gained popularity in the management of Ménière’s disease
3970_Ch17_285-295 25/06/14 11:50 AM Page 290
and has almost replaced surgical intervention in some cen- approach (Fig. 17.4). In the retrolabyrinthine approach, a
ters. Several protocols, doses, and dosing schedules have complete mastoidectomy is performed as described for the
been reported, but in essence, a low dose of gentamicin is endolymphatic sac procedure. 27 In addition, all the bone
injected into the middle ear space, either directly through medial to the sigmoid sinus is removed to expose the pos-
the tympanic membrane with topical anesthesia, through terior fossa dura. The dura is opened to e xpose the CPA.
a myringotomy tube, or with a continuous-perfusion de- The vestibular and auditory branches of the eighth nerv e
vice.23,24 This procedure appears to produce good control are directly in the field of view, and the vestibular nerve is
of vertigo attacks but poses a risk to hearing. 25 Cohen- divided. A disadvantage of this approach is that the audi-
Karem and associates 26 performed a meta-analysis of tory and vestibular portions of the eighth nerve are fused
15 studies totaling 627 patients treated with intratympanic as they exit the brainstem and may not have separated be-
gentamicin. Although the doses and dosing schedules fore they enter the internal auditory canal. Some surgeons
varied widely among the studies, these researchers found have advocated a retrosigmoid approach to drill away the
that complete control of v ertigo had been achie ved in posterior lip of the internal auditory canal; this procedure
75% of patients, and complete or substantial control in permits identification of the v estibular nerve after it has
93%. The vertigo control results did not appear to dif fer separated from the auditory nerve.28
for the various treatment regimens. Among multiple stud- If hearing preservation is not a goal, for example, in
ies, progression in hearing loss occurs in about 30% of patients with unilateral Ménière’s disease and severely im-
treated patients. paired hearing or discrimination, a labyrinthectomy is the
Intratympanic administration of aminoglycosides has most effective treatment. Labyrinthectomy can be per -
the great advantage of being a non-operative clinic proce- formed either through the e xternal auditory canal or
dure, thus avoiding the risks of anesthesia, sur gery, and through the mastoid. In the transcanal approach, the tym-
the cost of hospitalization. Ho wever, even though it is a panic membrane is elevated to expose the middle ear. The
simple procedure, it must be taken with the same serious- stapes is removed, and the vestibule is opened between the
ness as any other destructive procedure on the labyrinth. oval and round windows. The saccule, utricle, and ampul-
The risks of chronic post-labyrinthectomy disequilibrium lae of the superior , lateral, and posterior semicircular
and hearing loss must be carefully explained to the patient, canals are removed with an angled pick. Reaching the
and the same rules of informed consent apply to this ampulla of the posterior semicircular canal is a blind
procedure as a surgical intervention. maneuver and may lea ve neuroepithelium behind. F or
this reason, we prefer the transmastoid approach. A stan-
Vestibular Neurectomy dard mastoidectomy is performed, and all three semicir-
and Labyrinthectomy cular canals are identif ied. Each one is drilled a way
Although vestibular neurectomy and labyrinthectomy are in turn, and the neuroepithelium is identified under direct
more complex than endolymphatic sac surgery, control of vision and removed. The three semicircular canals lead
vertigo is predictable and reliable in 90% to 95% of to the vestibule, where once again the saccule and utricle
patients with either procedure. These procedures should are removed.
completely relieve the v ertiginous attacks, because
vestibular input from the operated ear is completely elim- Post-traumatic Vertigo
inated. The loss of all v estibular function on one side
can easily be compensated by an intact labyrinth on the Post-traumatic vertigo is managed in a manner identical
opposite side. to Ménière’s disease, with either a hearing-preserving or
When the hearing is w orth preserving (the ability to hearing-sacrificing form of vestibular ablation. Most au-
detect speech—or speech reception threshold—is better thorities, however, report less reliable control of recurrent
than 60 dB, and the ability to understand speech—or dis- attacks of dizziness after such treatment for this disorder.29
crimination score—is better than 50%), a v estibular The reasons for these results are unknown.
neurectomy through either the middle cranial fossa or
retrolabyrinthine space is the procedure of choice. Benign Paroxysmal Positional
The middle fossa approach is the same as described
previously for acoustic tumors. Once the internal auditory
Vertigo
canal has been identified and exposed, it can be opened, Unlike patients with Ménière’s disease, who experience
and the superior and inferior vestibular nerves divided. spontaneous episodes of dizziness, those suf fering from
The vestibular nerve can also be sectioned through benign paroxysmal positional v ertigo (BPPV) have tran-
either a retrolabyrinthine or retrosigmoid (suboccipital) sient symptoms only when they assume certain positions.16
3970_Ch17_285-295 25/06/14 11:50 AM Page 291
Figure 17.4 Retrolabyrinthine vestibular nerve section. This surgeon’s view of a right ear in
surgical position (anterior-top; superior-left) shows the exposure for a retrolabyrinthine nerve
section. The cerebellopontine angle is exposed by removal of the posterior surface of the
temporal bone between the sigmoid sinus and the posterior semicircular canal. The dura is
opened, and the seventh and eighth nerves are identified. The demarcation between the
vestibular and auditory portions of the nerve is usually marked by a small branch of the
anterior-inferior cerebellar artery (AICA). The vestibular portion of the eighth nerve (superior
half) is divided. Retrolabyrinthine vestibular nerve section. This surgeon’s view of a right ear in
surgical position (anterior-top; superior-left) shows the exposure for a retrolabyrinthine nerve
section. The cerebellopontine angle is exposed by removal of the posterior surface of the
temporal bone between the sigmoid sinus and the posterior semicircular canal. The dura is
opened, and the seventh and eighth nerves are identified. The demarcation between the
vestibular and auditory portions of the nerve is usually marked by a small branch of the
anterior-inferior cerebellar artery (AICA). The vestibular portion of the eighth nerve
(superior half) is divided.
The most common position is in a lateral or head-hanging time. In these cases, two surgical procedures can be con-
position with the diseased ear do wn. The symptoms gen- sidered. The first is singular neurectomy—division of the
erally have a latency of a few seconds before onset, develop branch of the vestibular nerve to the posterior semicircular
in a crescendo-decrescendo pattern, demonstrate torsional canal.30 This procedure is technically dif ficult and has
nystagmus, and habituate on repeated trials. The site of the been described as being performed at only a few centers.
pathology is generally thought to be in the posterior semi- The singular nerve passes just medial to the round window
circular canal. Schuknecht 15 has described debris on the niche before entering the ampulla of the posterior canal.
cupula of the posterior semicircular canal, which he has The lip of the round window is drilled away, but the round
called “cupulolithiasis.” The symptoms could arise from window membrane must be violated. Bone is remo ved
dislodged otoconia floating in the posterior semicircular posterior and inferior to the round window with tiny dia-
canal (canal lithiasis) and from those physically attached mond spurs to e xpose the singular canal. The canal is
to the cupula. opened, and the nerve avulsed.
BPPV is commonly a self-limiting condition that re- Surgical blockade of the flo w of endolymph in the
solves regardless of what treatment is given.16 A number posterior semicircular canal has also been described.31 In
of different physical therapy measures have been designed this procedure, the bon y posterior semicircular canal is
to dislodge the otoconia from the posterior semicircular opened without violation of the membranous labyrinth.
canal. These measures are effective in the vast majority of Flow within the membranous labyrinth is blocked by oc-
patients (see Chapter 20). clusion of the bony and membranous canals with a bone
Rarely, a patient with BPPV has persistent symptoms plug. Reports from several centers confirm this procedure
despite physical therapy intervention and the passage of as an effective and low-risk treatment for those rare cases
3970_Ch17_285-295 25/06/14 11:50 AM Page 292
of BPPV that f ail to respond to particle-repositioning disease may also beha ve with similar symptoms and
maneuvers.32,33 present as a diffuse third-window lesion.35
Surgery to repair superior semicircular canal dehis-
cence is directed at the patient’s needs, presence and severity
Inflammation and Cholesteatoma of the symptoms, and confirmed by the typical hearing pat-
Complications of the middle ear and mastoid infections tern, abnormal VEMPs and CT temporal bone (Fig. 17.5).
can lead to bacterial suppurati ve labyrinthitis and semi- Because there is no indication canal dehiscence is a
circular canal fistula. Management involves early inter- harbinger of dire consequences in the future, sur gical
vention and treatment of bacteria otitis media with intervention is dictated by the patient’s assessment of the
myringotomy and insertion of v entilation tube, cultures severity of symptoms.
of the middle ear aspirate, and appropriate tar geted Various surgical approaches have been described to
antibiotics to the infection. The role of mastoidectomy treat this condition. The middle fossa approach with
surgery in acute otitis media is related to the associated plugging and resurfacing of the dehiscent canal have led
symptoms of complications of acute mastoiditis with to the most lasting results with improvement in the low-
severe pain, facial nerve weakness, mastoid subperiosteal frequency conductive hearing loss. 36 Resurfacing alone
abscess, or intracranial complications. Surgical principles has been less successful. The resurfacing approach with
involve draining mastoid air cells and v entilation of the a bone flap results in recurrence of symptoms. This has
middle ear. led to the plugging technique with the same approach.A
Surgery related to cholesteatoma matrix o verlying transmastoid approach has since been described as a
the dehiscence of semicircular canal in volves careful re- quicker, safer surgical approach with less hospitalization
moval of the matrix, repairing of the f istula with careful stay.37
plugging with bone pâté, and an overlay temporalis fascia. The risk of sensorineural hearing loss following var-
The potential of loss of hearing and labyrinthine function ious surgeries has been reported up to 12% and higher
in large fistula defect is a real concern and risk. following revision surgery. A single lar gest report of
29 surgical repairs suggests that sur gical hearing results
did not differ according to method of canal repair (plug-
Superior Semicircular Canal ging versus resurfacing).34 However, others mentioned
Dehiscence delayed hearing loss in patients who had middle fossa
approach following resurfacing of the canal.38,39
Since Lloyd Minor34 first described superior semicircular
We generally prefer a middle fossa approach, repair-
canal dehiscence syndrome in 1998, a larger group of sim-
ing the defect carefully by gentle plugging of the dehiscent
ilar discrete or diffuse lesions in the temporal bone ha ve
superior canal with hydro set or bone cement, because we
been described as part of the third-window lesions.
believe that this has produced better hearing outcomes as
The symptoms are variable and range from vestibular
had been reported by others.40,41
complaints of vertigo, especially in response to e xternal
loud sounds or straining, autophony, pulsatile tinnitus, and
mild conductive hearing loss.
The positive signs of the third window include sound-
or pressure-induced nystagmus (Tullio’s phenomenon or
Hennebert’s sign, respectively). A tuning fork at 128 Hz
on the ankle or knee may lateralize to the affected ear. The
audiogram will show either a normal hearing or conduc-
tive hearing loss mimicking otosclerosis with lar gest air-
bone gap in the lower frequencies and supernormal bone
conductions threshold below 2 kHz. Acoustic reflexes are
usually present (contrary to otosclerosis), and v estibular
evoked myogenic potentials (VEMPs) are present and
show abnormally low thresholds.
Anatomically discrete lesions may be classif ied by
location: semicircular canals (superior, lateral, or posterior
Figure 17.5 CT scan of superior semicircular canal dehis-
canal dehiscence), bony vestibule (large vestibular aque- cence. This is a parasagittal non-contrast CT of the left su-
duct syndrome), or the cochlea (carotid-cochlear dehis- perior canal in the plane of the canal. An open dehiscence
cence, X-linked deafness with stapes gusher). P aget’s can be seen in the top of the arch of the canal.
3970_Ch17_285-295 25/06/14 11:50 AM Page 293
24. Magnusson H, Padoanm S. Delayed onset of ototoxic 36. Ward BK, Agrawall Y, Nguyen E, et al. Hearing outcomes
effects of gentamicin in treatment of Meniere’s disease: after surgical plugging of the superior semicircular canal
rationale for extremely low dose therapy. Acta Otolaryn- by middle fossa approach. Otol Neurotol. 2012;33:
gol (Stockh). 1991;111:671. 1386-1391.
25. Toth AA, Parnes LS. Intratympanic gentamicin therapy for 37. Deschenes GR, Hsu DP, Megerian CA. Outpatient repair
Meniere’s disease: preliminary comparison of two regi- of superior semicircular canal dehiscence via the trans-
mens. J Otolaryngol. 1995;24:340. mastoid approach. Laryngoscope. Sep 2009;119(9):1765.
26. Cohen-Kerem R, et al. Intratympanic gentamicin therapy 38. Minor LB, Solomon D, Zinerich JS, Zee DS. Sound
for Meniere’s disease: a meta-analysis. Laryngoscope. and/or pressure-induced vertigo due to bone dehiscence of
2004;114:2086. the superior semicircular canal. Arch Otolaryngol Head
27. Silverstein H, Norrell H. Retrolabyrinthine vestibular Neck Surg. 1998;124:249.
neurectomy. Otolaryngol Head Neck Surg. 1982;90:778. 39. Peterson EC, Lazar DA, Nemecek AN, et al. Semicircular
28. Silverstein H, et al. Combined retrolab-retrosigmoid canal dehiscence syndrome: successful treatment with
vestibular nerve neurectomy: an evolution in approach. Am repair of the middle fossa floor: technical case report.
J Otol. 1989;10:166. Neurosurgery. 2008;63(6):E1207-E1208.
29. Kemink, JL et al. Retrolabyrinthine vestibular nerve sec- 40. Crane BT, Minor LB, Carey JP. Superior canal dehiscence
tion: Efficacy in disorders other than Meniere’s disease. syndrome: plugging reduces dizziness handicap. Laryngo-
Laryngoscope. 1991;101:523. scope. 2008;118(10):1809.
30. Gacek RR. Singular neurectomy update. Ann Otol Rhinol 41. Vlastarakos PV, Proikas K, Tavoulari E, et al. Efficacy as-
Laryngol. 1982;91:469. sessment and complications of surgical management for
31. Parnes LS, McClure JA. Posterior semicircular canal superior semicircular canal dehiscence: a meta-analysis of
occlusion for intractable benign paroxysmal positional published interventional studies. Eur Arch Otorhinolaryn-
vertigo. Ann Otol Rhinol Laryngol. 1990;99:330. gol. 2009;266(2):177.
32. Parnes LS. Update on posterior canal occlusion for benign 42. Paugh DR, et al. Identification of perilymph proteins by
paroxysmal positional vertigo. Otolaryngol Clin North two-dimensional gel electrophoresis. Otolaryngol Head
Am. 1996;29:333. Neck Surg. 1991;104-517.
33. Zappia JJ. Posterior semicircular canal occlusion for 43. Mattox DE. Perilymph fistulas. In: Cummings CWC, et al,
benign paroxysmal positional vertigo. Am J Otol. 1996; eds. Otolaryngol Head Neck Surg. St. Louis: Mosby,
17;749. 1986:3113.
34. Limb CJ, Carey JP, Srireddy S, Minor LB. Auditory func- 44. Janetta PJ, et al. Etiology and definitive microsurgical
tion in patients with surgically treated superior semicircu- treatment of hemifacial spasm. J Neurosurg. 1977;47:321.
lar canal dehiscence. Otol Neurotol. 2006 Oct 27(7): 45. Janetta PJ. Neurovascular cross-compensation of the
969-980. eighth cranial nerve in patients with vertigo and tinnitus.
35. Merchant SN, Rosowski JJ. Conductive hearing loss In: Sammi M, Janetta PJ, eds. The Cranial Nerves. New
caused by third-window lesions of the inner ear. Otol York: Springer-Verlag, 1981:552.
Neurotol. 2008 Apr;29(3):282-289.
3970_Ch18_296-308 25/06/14 5:22 PM Page 296
CHAPTER 18
Management
of Psychological
Problems and
the Dizzy Patient
Ronald J. Tusa, MD, PhD
“It is more important to know what kind of patient Yardley and colleagues 2 examined 101 patients at
has the disease than to know what kind of disease onset of dizziness and 7 months later. The best longitudi-
the patient has. nal predictors of poor outcome were autonomic symptoms
The good physician will treat the disease, b ut (heart pounding, excessive sweating, hot or cold spells,
the great physician will treat the whole patient.” feeling faint or short of breath) and somatization (general
—Sir William Osler tendency to complain of a di versity of unrelated health
problems, ranging from pains in the back to difficulty con-
Dizziness can cause e xtreme stress, which may in turn
centrating). These symptoms had a better prediction of
lead to anxiety (including panic attacks and agoraphobia),
poor outcome than did the etiology of true vertigo, severity,
depression, and somatoform disorders. These psycholog-
duration, test results, or medication. High and persistent
ical problems can also cause se vere dizziness. At times,
handicap arose from psychiatric or psychosocial problems
these psychological causes may become the primary cause
unrelated to the vertigo.
of dizziness and may replace the initial or ganic cause of
This chapter summarizes the interaction between
dizziness.
dizziness and psychological problems. It also discusses
Two good longitudinal studies have assessed the role
conversion disorders and malingering. Finally, it presents
of psychological problems in dizziness. Kroenke and asso-
a practical clinical approach to these problems.
ciates1 examined 94 patients at onset of dizziness and then
had the patients complete questionnaires at 4 months and
1 year later. Symptoms improved for 51 patients, stayed the
same for 32, and worsened for 11. Etiology of the dizziness
Psychological Disorders and Their
affected outcome. The majority of patients with benign Prevalence
paroxysmal positional vertigo (BPPV), neuritis, migraine, Dizziness in Patients with Psychological
or presyncope experienced improvement. Less than half of Disorders
those with Ménière’s disease or psychiatric or nonvestibular
disequilibrium showed improvement. The four multivari- Prevalence of Psychological Disorders
ate predictors of poor outcome were (1) primary psychi- The prevalence of psychological problems in the general
atric etiology, (2) dysequilibrium, (3) daily dizziness, and population is very high. Table 18-1 lists the prevalence in
(4) dizziness aggravated by walking. the United States as of 2012.3
296
3970_Ch18_296-308 25/06/14 5:22 PM Page 297
Abnormal Results of Vestibular Tests themselves as much more disabled by their dizziness than
in Patients with Psychological Problems patients with no psychiatric disorder. The prevalence of psy-
To what extent patients with panic disorder have a vestibu- chiatric disorders as the primary cause of dizziness declines
lar defect is contro versial. Several authorities have re- with increasing patient age. 1,12 In patients older than
ported abnormal results on a variety of tests used to assess 60 years, 38% have psychological diagnosis contributing to
dizziness, including caloric testing, rotary chair testing, dizziness, but of these, only 6% were believed to have a pri-
vestibular autorotation, and posturography.4-8 Few articles mary psychological cause for the dizziness. Psychological
have sufficient detail to allow determination whether these problems often coexist with a significant balance disorder.
deficits are truly a result of v estibular dysfunction (high
Patients with and without Peripheral
vestibulo-ocular reflex [VOR] gain on rotary chair testing
Vestibular Deficits
or decreased response on caloric testing). Of these more-
Forty percent of patients with vestibular hypofunction pre-
detailed articles, one article suggests that as man y as
senting to an otolaryngology clinic have an additional panic
14% of patients with panic b ut without agoraphobia and
disorder with and without agoraphobia. 13 Fifty percent of
39% of patients with panic and agoraphobia ha ve com-
patients with vestibular hypofunction evaluated 3 to 5 years
pensated peripheral vestibular defects.6 Another article
after the original referral still had a significant psychiatric
found discrepancies in the VOR but no caloric deficits in
disturbance (panic disorder or major depression). 14 In my
patients with panic disorder.5
experience, panic attacks do occur in a number of patients
with vestibular deficits, but not to the same e xtent as re-
ported in these studies conducted by psychiatrists. Chronic
Psychological Problems in Patients anxiety is much more pre valent. The level of anxiety in
with Dizziness these patients is usually not high enough to w arrant psy-
There is a high pre valence of unrecognized mood and chotherapy or medication. Patients without evidence of pe-
psychological problems in dizzy patients, especially anxiety ripheral vestibular deficit have a greater mean number of
disorders.9,10 Forty percent of all dizzy patients ha ve psy- lifetime psychiatric diagnoses, especially major depression
chological disorders.1 Stein and coworkers11 reported that and panic disorder, than those with a v estibular deficit.10
15% of all dizzy patients meet theDiagnostic and Statistical Patients without vestibular deficits also more frequently
Manual of Mental Disorders (DSM-IV) criteria for panic have somatization disorders as well as more current and
disorder, agoraphobia, or both and that these patients rate lifetime unexplained medical symptoms.
3970_Ch18_296-308 25/06/14 5:22 PM Page 298
Box 18-1
(N) = negative term; (P) = positive term. The patient’s form does not contain these labels. See text for explanation
of scoring. Adapted from Watson et al.17
3970_Ch18_296-308 25/06/14 5:22 PM Page 299
F3. Because of your problem, do you restrict your travel for business or recreation?
P4. Does walking down the aisle of a supermarket increase your problem?
F5. Because of your problems, do you have difficulty getting into or out of bed?
F6. Does your problem significantly restrict your participation in social activities, such as going out to
dinner, movies, dancing, or parties?
P8. Does performing more ambitious activities, like sports, dancing, and household chores such as
sweeping or putting dishes away, increase your problem?
E9. Because of your problems, are you afraid to leave your home without having someone accompany you?
E10. Because of your problem, have you been embarrassed in front of others?
F14. Because of your problem, is it difficult for you to do strenuous housework or yard work?
E15. Because of your problem are you afraid people may think you are intoxicated?
F16. Because of your problem, is it difficult for you to go for a walk by yourself?
F19. Because of your problem, is it difficult for you to walk around your house in the dark?
E20. Because of your problem, are you afraid to stay home alone?
E22. Has your problem placed stress on your relationships with members of your family or friends?
F24. Does your problem interfere with your job or household responsibilities?
For the following, please pick the one statement that best describes how you feel.
Statement Score
Negligible symptoms 0
Bothersome symptoms 1
Performs usual work duties but symptoms interfere with outside activities 2
Symptoms disrupt performance of both usual work duties and outside activities 3
Unable to work for over 1 year or established permanent disability with compensation payments 5
Patient is given a paper with the statements on it and asked, “Please pick the one statement that best describes
how you feel.” See text for scoring.
Adapted from Shepard et al.21
3970_Ch18_296-308 25/06/14 5:22 PM Page 301
in the 37 patients in the Lempert study. This review found Psychological Disorders
psychogenic gait disorders in 9% of their neurological in-
Anxiety
patients. In 5 years, 47% had favorable outcomes.26
Panic Attacks with and without
Aphysiological Spasm of Convergence Agoraphobia
Patients sometimes demonstrate convergence of the eyes Dizziness is the most common symptom in patients with
(cross-eyed) while being examined. This is usually asso- panic disorder, occurring in 50% to 85% of all such pa-
ciated with pupillary constriction. It is aphysiological tients.35,36 Panic attacks consist of discrete spells of intense
(functional) when it is episodic and there are no other fear or discomfort, in which at least four of the symptoms
ocular motor defects. 27 When other dorsal midbrain ab - listed in Box 18-3 de velop abruptly and reach crescendo
normalities are present (chronic pupillary changes, upgaze within 10 minutes. Panic attacks can be unexpected (uncued)
defect), an organic basis should be considered. or situationally bound (cued). An example of the latter is
spells induced when entering a car. Agoraphobia is the aver-
Voluntary Nystagmus sion of open spaces, including leaving the house. Agorapho-
Voluntary nystagmus is a type of nystagmus that some in- bia is commonly found in patients with severe panic attacks.
dividuals can learn to e xhibit volitionally.28 Historically,
it was used by young American men to a void military Obsessive-Compulsive Disorder
draft. It should not be confused with flutter. Voluntary nys- An obsession is a repetitive intrusive thought, impulse, or
tagmus is commonly associated with vergence eye move- image that causes mark ed anxiety. A compulsion is a
ments and pupillary constriction. repetitive ritualistic behavior or mental act that aims to re-
duce anxiety. Examples of the latter include hand washing
and checking to see that doors are locked.
Dynamic Posturography
A number of studies ha ve found characteristic features Generalized Anxiety Disorder
on dynamic posturography in patients with psychogenic Generalized anxiety disorder is characterized by general-
balance disorders.29-34 Box 18-2 lists the k ey patterns ized and persistent anxiety with motor tension, autonomic
3970_Ch18_296-308 25/06/14 5:22 PM Page 302
100 100
75 75
50 50
FF F F FFF FFF
25 AA A A
25
A AA A AA
LL L L LLL LLL
FALL LL L L FALL LLL LLL
1 2 3 4 5 6 Composite 1 2 3 4 5 6 Composite
Sensory Test Condition 38 38
Sensory Test Condition
A B
Trial 1 Trial 2 Trial 3
1
shear
Trial 1 Trial 2 Trial 3
AP sway
1
2
3
3
4
5
6
Box 18-4
of rejection. Using the term psychogenic to describe the from the daily medication group. I usually use the lowest
problem, which is diagnostically neutral, may be preferred dose listed in Table 18-5. After 3 weeks, I either taper the
to “functional” or “hysterical” (Box 18-5). intermittent medication completely or limit its use to 1 or
2 days per week at most.
Medications
Physicians may want to start the patient on medication, as ■ Table 18-5 MEDICATION FOR CHRONIC
listed in Table 18-5. The agents listed as daily medication ANXIETY
are nonaddictive, take up to 3 weeks to become effective,
and can be taken for years. These medications are all an- Half-Life
tidepressants and are approved by the U.S. Food and Drug Medication Dose (hr)
Administration (FDA) for treatment of anxiety. Paroxetine
Intermittent
(Paxil) and sertraline (Zoloft) should be given in the morn-
medication:
ing, because they can impair sleep. Agents listed as inter-
mittent medications are addictive, can cause sedation, act Xanax (alprazolam) 0.2–1 mg tid 11–15
immediately, and are strictly for anxiety. For patients with
severe chronic anxiety or panic attacks, I usually start two Ativan (lorazepam) 0.5–5 mg bid 10–20
drugs, one from the intermittent medication group and one
Klonopin 0.5–10 mg bid 18–50
(clonazepam)
CHAPTER 19
Management
of the Patient
with Chronic
Subjective
Dizziness
Jeffrey P. Staab, MD, MS ■ Neil T. Shepard, PhD
For more than 150 years, the medical literature has con- PPV: (1) obsessive-compulsive personality traits, labile
tained descriptions of patients with chronic dizziness and affect, and mild depression; and (2) anxiety and vegetative
motion sensitivity, accompanied by varying degrees of disturbance.2 Brandt, Dieterich, and colleagues found PPV
anxiety and phobic behaviors. In 1871, Karl Westphal, a to be the second most common cause of vestibular symp-
German neurologist, coined the term agoraphobia to de- toms in their university-based neuro-otology practice, be-
scribe a syndrome of dizziness, spatial disorientation, and hind only benign paroxysmal positional vertigo (BPPV).3
anxiety experienced by individuals in the busy open mar- Diagnostic studies differentiated PPV from panic disorder,
ketplaces of 19th century European villages. 1 Westphal agoraphobia as currently defined in modern psychiatric
considered postural control, spatial orientation, and threat nomenclature, and other psychiatric disorders, suggesting
assessment to be fully integrated components of locomo- that it is a primary neuro-otologic condition with behav-
tion, a view that was lost as clinical neuro-otologic and ioral elements.3 Huppert and colleagues5 found that PPV
psychiatric practice diverged through the 20th century . could be diagnosed quite reliably. They contacted 105 pa-
The term agoraphobia was linked to panic attacks as a pri- tients who were diagnosed with PPV 5 to 16 years earlier
mary psychiatric diagnosis. In the 1980s and 1990s, (average 8.5 years) and reaf firmed the diagnosis in all
neuro-otologists and psychiatrists renewed their interest patients. No patients had been misdiagnosed, and none
in interactions among vestibular and anxiety disorders. had developed other neurological or vestibular conditions.
Brandt and Dieterich described phobic postural vertigo Two other studies showed that the long-term course of
(PPV) in the German medical literature in 1986 2 and in PPV was marked by chronic dizziness and unsteadiness
the English medical literature a decade later.3 They de- that waxed and waned over time. Symptoms tended to de-
fined PPV as a syndrome of postural dizziness and fluc- crease gradually, but rarely resolved.5 Curiously, Westphal
tuating unsteadiness provoked by environmental or social reported this same pattern in his reports in the 1870s. 1
stimuli (e.g., crossing bridges; descending staircases; trav- Behavioral outcomes of PPV were not as good. Two-thirds
eling on busy streets or through crowds). They reported of patients developed clinically significant anxiety or
that PPV could be triggered by vestibular disorders, med- depression.3 Finally, recent studies found that behavioral
ical illnesses, or psychological stress. 4 They included factors may affect the natural course of PPV and outcomes
two behavioral criteria in their original definition of of treatment.6,7
309
3970_Ch19_309-322 25/06/14 5:58 PM Page 310
In the early 2000s, Staab and Ruckenstein defined though they may wax and wane in severity. Asymptomatic
chronic subjective dizziness (CSD), 7,8 which had three periods may occur. CSD often lasts for months or years.
features: (1) persistent nonvertiginous dizziness lasting It may remit spontaneously, but when it does, resolution
3 months or more; (2) hypersensitivity to motion stimuli, is slow and gradual. 5 The unsteadiness experienced by
including a patient’s own movement and motion of objects patients with CSD is subjective. In cases in which un-
in the visual surround; and (3) difficulty with precision vi- steadiness is observable on clinical examination, the pos-
sual tasks such as reading or using a computer. The defini- sibility of comorbid neuro-otologic illnesses (e.g., bilateral
tion of CSD was influenced not only by the original vestibular deficits, movement disorders) or behavioral dis-
concept of PPV, but also by the work of Jacob and col- orders (e.g., phobia of falling, functional gait disorder)
leagues9 on space-motion phobia and Bronstein and col- must be considered.
leagues10 on visual vertigo. Subsequent studies investigated
the relationships between CSD and other neuro-otologic
and psychiatric conditions. 7,11,12 This research found that Relationship to Posture
the behavioral criteria included in the definition of PPV 2 A postural criterion was not part of the original definition
(e.g., obsessive compulsive personality traits, mild depres- of CSD,8 but the core symptoms of dizziness and un-
sion and anxiety) were predisposing factors and behavioral steadiness are usually worse when sitting, standing, or
comorbidities, respectively, not essential components of walking than when recumbent. Postural symptoms occur
CSD. More specifically, anxious, introverted personality when patients are upright, but not when they are reclin-
traits may predispose individuals to developing CSD, and ing. These are to be distinguished from orthostatic and
anxiety or depressive symptoms may coexist with CSD, positional symptoms. As defined by the International
but they are not core elements of the syndrome. 13 Addi- Committee for Classification of Vestibular Disorders,20
tionally, investigators in the United States and Japan com- orthostatic symptoms occur during or immediately after
pleted successful open-label medication trials for CSD patients arise from a recumbent posture (e.g., during or
showing that selective serotonin reuptake inhibitors immediately after standing up). Positional symptoms
(SSRIs) could be used to treat the disorder.7 Other investi- occur when the head or body moves into or through a spe-
gators studied rehabilitative and psychotherapeutic treat- cific orientation in space. Postural symptoms are so com-
ments. They observed that the habituation form of mon in CSD that the diagnosis should be reconsidered
vestibular rehabilitation could be an effective intervention (though not absolutely excluded) if patients report no in-
for CSD. Psychotherapy yielded mixed results. 14 For pa- crease in vestibular symptoms when upright. Patients
tients with long-standing CSD, researchers in Europe and with CSD may have orthostatic or positional problems,
the United States were able to demonstrate short-term re- but these should be part of a generalized pattern of sensi-
ductions in dizziness using cognitive-behavioral therapy tivity to motion in all directions.
(CBT),15,16 but improvements in symptoms were not sus-
tained in long-term follow-up. 17 For patients with new
onset CSD-type symptoms, cognitive-behavioral therapy Provocative Factors
may have more enduring benefits.18
The third row of Table 19-1 lists additional factors that
may provoke CSD symptoms. These include head or
Current Formulation of Chronic body motion that is not direction-specific and visual
Subjective Dizziness stimuli such as large-field visual flow, complex patterns,
or performance of precision visual tasks. These provoca-
The clinical elements of CSD are organized in Table 19-1.
tive factors may not seem to be unique to CSD, but there
They are separated into primary symptoms, relationship to
are important distinctions between the responses of
posture, exacerbating factors, precipitating events, exami-
patients with CSD and those with other neuro-otologic
nation and laboratory findings, and behavioral factors. A
disorders. Patients with Ménière’s disease, vestibular
validation study of this structure is under way at Mayo
migraine, and other vestibular disorders find head move-
Clinic.19 Initial findings from that study support the de-
ments and environmental motion stimuli to be quite
scription given in Table 19-1.
troublesome during acute attacks of their illnesses but
much less problematic or not bothersome at all during
Core Symptoms interictal periods. Patients with most neuro-otologic
The primary symptoms of CSD are persistent, nonvertig- conditions can reduce their symptoms by holding still
inous dizziness or swaying/rocking unsteadiness. For most or removing themselves from motion-rich environ-
patients, these symptoms are present throughout the day, ments. In contrast, patients with CSD are likely to
3970_Ch19_309-322 25/06/14 5:58 PM Page 311
■ Table 19-1 CLINICAL FEATURES SHARED BY PHOBIC POSTURAL VERTIGO AND CHRONIC
SUBJECTIVE DIZZINESS
Primary symptoms Unsteadiness, dizziness, or both are typically Symptoms of phobic postural vertigo
present throughout the day but fluctuate in (PPV) and chronic subjective dizziness
severity. (CSD) are usually quite persistent but
Symptoms are present on most days for wax and wane spontaneously and in
3 months or more. response to provocative factors.
Vertigo is not part of PPV or CSD, but
CSD may coexist with other vestibular
disorders. In those cases, patients may
experience episodic vertigo superimposed
on chronic unsteadiness and dizziness.
Postural relationship Primary symptoms are related to body Some patients with CSD prefer walking
posture. to standing still, although either is more
Symptoms are most severe when walking troublesome than sitting or lying down.
or standing, less severe when sitting, and Postural and orthostatic symptoms are not
absent or very minor when recumbent. the same. Postural symptoms are present
while patients are in upright postures.
Orthostatic symptoms occur as patients
arise into an upright posture.
Orthostatic tremor develops while stand-
ing and improves during walking.
Provocative factors Primary symptoms are present without Symptoms of CSD exist without provoca-
(context-dependent specific provocation but are exacerbated tion but usually reflect the cumulative bur-
symptom exacerbation) by the following: den of exposure to provocative activities
1. Active or passive motion of self that throughout the day. Context-dependent
is not related to a specific direction or factors include motion of self, exposure to
position environments with challenging motion
2. Exposure to large-field moving visual stimuli, or complex visual cues and per-
stimuli or complex (fixed or moving) formance of visual tasks that require pre-
visual patterns cise, sustained focus, such as using a
3. Performance of small-field, precision computer or reading.
visual activities (e.g., reading, using a
computer, fine tasks with hands)
Precipitating factors Precipitating factors include: The most common triggers for CSD are:
(triggering events) 1. Acute or recurrent neuro-otologic dis- • Previous acute vestibular disorders (e.g.,
eases that cause central or peripheral benign paroxysmal positional vertigo,
vestibular dysfunction vestibular neuritis)
2. Acute or recurrent medical problems • Episodic vestibular disorders (e.g.,
that produce unsteadiness or dizziness vestibular migraine, Ménière disease)
3. Acute or recurrent psychiatric disorders • Mild traumatic brain injury or whiplash
that produce unsteadiness or dizziness • Panic attacks, generalized anxiety
• Dysautonomias
• Dysrhythmias
• Adverse drug reactions and other
medical events
Continued
3970_Ch19_309-322 25/06/14 5:58 PM Page 312
■ Table 19-1 CLINICAL FEATURES SHARED BY PHOBIC POSTURAL VERTIGO AND CHRONIC
SUBJECTIVE DIZZINESS—cont’d
Physical examination Physical examination and vestibular labora- CSD may occur as an isolated condition
and laboratory findings tory testing are often normal. Minor, nondi- or coexist with other neuro-otologic or
agnostic abnormalities occur frequently. medical illnesses. Positive examination
Examination and testing may reveal diag- findings do not necessarily exclude CSD.
nostic evidence of a neuro-otologic or They may instead identify comorbid
other medical condition that may be active, conditions.
treated, or resolved but cannot fully ex- At present, there are no established
plain all of the patient’s symptoms. biomarkers for CSD, but emerging data
suggest that patients may have a unique
pattern of sway on static or dynamic
posturography with relatively poorer
performance on simpler tasks.
Behavioral symptoms Behavioral assessment may be normal. Several carefully designed diagnostic
Low levels of anxiety or depression are studies have shown that CSD is a unique
common. clinical entity, not a forme fruste of a
psychiatric illness (see text).
Behavioral assessment also may find clini- However, patients with CSD do have
cally significant psychological distress, an increased prevalence of psychiatric
psychiatric disorders, or adverse changes disorders, typically anxiety or depressive
in activities of daily living. disorders, compared with individuals
with other neuro-otologic illnesses.
* The first three features may be used to make a diagnosis of CSD. The clinical history would include 3 months
or more of persistent, posture-related unsteadiness or dizziness provoked by motion of self and one or both of
the visual stimuli.
experience prolonged exacerbations of unsteadiness and Patients with psychiatric disorders, such as panic
dizziness lasting for hours or days even after minimizing disorder, agoraphobia, and specific phobia of dizziness,
or eliminating exposure to provocative stimuli. In fact, also experience increased symptoms with provocative
the severity of CSD symptoms at a given time reflects stimuli. Here, too, there are important dif ferences be-
the accumulated exposure to motion stimuli over the tween patients with CSD and individuals with these psy-
preceding hours or days, which makes patients continu- chiatric disorders. Fear is not a prominent part of CSD.
ally vulnerable to further exacerbations. Patients with anxiety disorders avoid provocative situ-
ations, because they fear adverse consequences, such as
• Severity of CSD symptoms at a given time reflects
becoming incapacitated or causing a scene in public. In
the accumulated exposure to motion stimuli over
contrast, individuals with CSD avoid provocative situ-
the preceding hours or days.
ations to limit exposure to noxious physical sensations.
• The prevalence of difficulties with visual stimuli
Preliminary results from the Mayo Clinic validation
was significantly greater in patients with CSD
study of CSD 19 are beginning to clarify these dif fer-
(80%) than in patients with other disorders (20%).
ences. Most (75% to 98%) patients with active neuro-
• Vestibular neuritis, BPPV, and other peripheral
otologic conditions reported sensitivity to self-motion
vestibular disorders triggered more cases of CSD
as part of their illnesses, although patients with CSD had
than central vestibular conditions.
prolonged unsteadiness or dizziness rather than time-
• In most cases, CSD has a sudden onset, starting
limited vertigo experienced by those with the other dis-
after a single event.
orders. Furthermore, the prevalence of difficulties with
• The diagnosis of CSD should not be confused with,
visual stimuli was significantly greater in patients with
or attributed to, psychiatric morbidity.
CSD (80%) than in patients with other disorders (20%)
3970_Ch19_309-322 25/06/14 5:58 PM Page 313
and these visual symptoms listed in Table 19-1 appeared testing no longer excludes a diagnosis of CSD, but iden-
to be quite sensitive and specific for CSD. tifies coexisting conditions.
The first 3 rows of Table 19-1 may be used clini-
cally to identify patients with CSD. An individual with Behavioral Predisposition
3 months or more of nonvertiginous dizziness or un- and Comorbidity
steadiness that is postural in nature and exacerbated by
his or her own movements, exposure to large-field visual In addition to their investigations of the core symptoms
stimuli, or performance of small-field precision visual and precipitants of CSD, Staab and Ruckenstein studied
tasks may be given the diagnosis. the role of behavioral factors in its development and clin-
ical course. This research coincided with investigations
Precipitating Events by other clinical scientists6,21-23 to identify three ways the
In two large studies of CSD,8,19 the most common trigger- behavioral factors contribute to CSD.
ing events, accounting for 25% of all cases, were previous • First, individuals with anxious, introverted tem-
acute vestibular disorders. Vestibular neuritis, BPPV, and peraments or preexisting anxiety disorders may
other peripheral vestibular disorders triggered more cases be particularly predisposed to developing CSD.
of CSD than central vestibular conditions, most likely be- • Second, CSD may be more likely to occur in
cause they are more prevalent disorders. Other precipitants individuals who have high levels of anxiety,
included panic attacks, especially in young adults (15% to hypervigilance about vestibular symptoms, and
20%); vestibular migraine, more likely in women (15% to excessive worry about potentially adverse out-
20%); generalized anxiety (15%); mild traumatic brain in- comes during an acute bout of a neuro-otologic
jury (concussion or whiplash), especially in young men illness or other triggering event.
(10% to 15%); and dysautonomias (7%). Other medical • Third, comorbid anxiety and depression occur
problems, such as dysrhythmias and adverse drug reac- in many, but not all, patients with CSD, adding
tions, accounted for about 2% of cases. These problems considerable morbidity.
seemed to trigger CSD because they caused acute bouts of
vertigo, dizziness, or disruption of gait and stance. This last point is important in making accurate clin-
In most cases CSD has a sudden onset, starting after ical diagnoses. Studies from Germany,3 Sweden,24 and the
a single event. It also may begin with recurrent bouts of United States,17 showed that 60% of patients with CSD
self-limited symptoms that consolidate into a persistent had clinically significant anxiety and 45% had clinically
pattern. Most patients are able to identify one or more pre- significant depression. These rates were higher than those
cipitating events, such as a single bout of vestibular neu- encountered in similar studies of patients with Ménière’s
ritis or recurrent episodes of vestibular migraine or panic disease, vestibular migraine, or BPPV, which found psy-
disorder. CSD rarely has an insidious onset.Although such chiatric comorbidity rates of 35% for anxiety and 20% for
cases occur, this presentation warrants reevaluation of the depression.19,25,26 However, 25% of patients with CSD do
clinical history with particular attention to progressive not have significant psychiatric symptoms, and the core
vestibular or degenerative neurological conditions. elements of CSD do not differ in patients with or without
anxiety or depression. Therefore, the diagnosis of CSD
should not be confused with, or attributed to, psychiatric
Medical Comorbidity morbidity.
The original definition conceptualized CSD as a sequela
of a triggering medical or psychological event, not as a Pathophysiological Mechanisms
condition that might coexist with other illnesses.8 This was of CSD—Old and New Hypotheses
an error. Clinical experience and initial data from the
The Old Idea
Mayo Clinic validation study of CSD 19 indicate that the
syndrome coexists with a wide variety of other disorders, Both Brandt and Dieterich, in defining PPV ,3 and Staab
including episodic and chronic neuro-otologic disorders, and Ruckenstein, in defining CSD, 7 hypothesized that
ranging from Ménière’s disease to stroke-related, central classical and operant conditioning were the principal
vestibular deficits. As a result, the original diagnostic cri- pathophysiological mechanisms for this disorder . Acute
terion about normal or insignificant physical examination vestibular events were thought to be particularly potent
and laboratory testing has been revised as shown in the unconditioned stimuli, because they produce strong phys-
fifth row of Table 19-1. Evidence of active neuro-otologic iological responses that sensitize (condition) postural and
deficits on physical examination or vestibular laboratory ocular motor reflexes to subsequent exposures to internal
3970_Ch19_309-322 25/06/14 5:58 PM Page 314
or external motion stimuli. This was thought to trigger High anxiety during the early phase of balance disruption
a heightened awareness of postural control, thereby rein- seems to impair the readaptation process, making it more
forcing (classically conditioning) hypersensitive postural likely that CSD will develop, possibly compounded by
reflexes. At the same time, operant conditioning reinforces anxiety or depressive disorders.
safety behaviors such as avoidance of provocative situations
CSD is now conceptualized as either persistent fail-
and use of safety aids (e.g., going out with a trustworthy
ure to readapt after the initial impairment to posture,
companion). Anxiety that accompanies the triggering events
balance, and oculomotor control resolves or persist-
may augment these conditioning processes. Catastrophic
ent use of high-risk balance control strategies that
thoughts and dysphoric ruminations about the potential con-
are out of proportion to what is necessary to com-
sequences of vestibular symptoms (e.g., crashing the car or
pensate for chronic neuro-otologic deficits.
becoming handicapped) were thought to perpetuate CSD
and increase the likelihood of developing comorbid anxiety The effect of anxiety on balance control strategies
or depression. has been investigated in normal individuals and patients
with CSD. Anxious individuals and patients with CSD do
not tolerate postural disturbances as well as normal indi-
A New Concept viduals. For example, Carpenter and colleagues,27 found
The hypothesis that CSD is caused by classical and oper- that anxious but otherwise normal subjects responded
ant conditioning is based on well-established behavioral more quickly to rotational perturbations while standing
and cognitive theories, but no data specifically support it. on a posture platform than less-anxious subjects. They
Rather, several lines of evidence suggest a different mech- employed a stif fer and more reactive postural control
anism, albeit one that still involves threat systems in the strategy in which they made more postural corrections re-
brain. CSD almost always starts with an acute process, sulting in narrower postural displacements than their
such as an episode of a neuro-otologic disorder , other more relaxed counterparts. In a separate study,28 patients
medical event, or panic attacks with prominent dizziness. with PPV had a similar stiff, highly reactive postural re-
Occasionally, patients will describe insidious onset, but sponse to visual vection stimuli while standing on a pos-
that is uncommon. This means that nearly all triggers for ture platform that produced smaller displacements than
CSD require patients to adapt quickly to an acute disrup- normal subjects.
tion of safe and secure mobility. During the early phases Anxious patients employ several features of high-risk
of acute events, such as the sudden onset of vestibular neu- postural control strategies in situations in which they are
ritis, patients must suppress input from damaged sensory not needed.29 One of these is co-contraction of antigravity
systems and shift preferences to intact sensory systems to muscle groups, which changes the natural sway pattern
maximize detection of accurate spatial orientation cues. during steady stance to one with a higher frequency , but
Patients must also shift into high-risk postural control lower amplitude of movement. This causes anxious indi-
strategies (e.g., moving cautiously, using supports) and viduals to perform worse than normal subjects on simple
maintain a greater degree of vigilance about the environ- postural tasks that do not require high-risk postural control
ment. These changes are adaptive in the short run, but strategies. In situations in which higher risk strategies are
should return to normal when no longer needed (e.g., as needed, anxious and non-anxious individuals perform
vestibular compensation develops). A similar pattern of similarly. For example, healthy college students with high
shifting into high-risk postural control strategies followed anxiety swayed more than their less-anxious classmates
by return to normal would be expected in response to while standing on a posture platform with eyes open but
episodic vestibular illnesses such as Ménière’s disease or not with eyes closed. Both groups swayed more with eyes
vestibular migraine. In these cases, the cycle of response closed, but between-group differences were more notice-
would occur repeatedly. CSD may be caused by panic at- able during the easier task. 29 These studies show that
tacks or other intense stress reactions. These situations threat systems in the brain instinctively alter balance per-
also may disrupt mobility, necessitating a similar shift out formance, depending on the context of the posture control
of and back into normal postural control strategies. Re- task and anxious state of the individual. Patients with CSD
gardless of the nature of triggering events, CSD is now appear to have a reduced tolerance for postural distur -
conceptualized as either persistent failure to readapt after bances, including motion of their bodies and movement
the initial impairment to posture, balance, and oculomotor in the visual surround. They make more high-frequency,
control resolves or persistent use of high-risk balance con- low-amplitude postural corrections (a high-risk postural
trol strategies that are out of proportion to what is neces- control strategy) in routine balance situations when that is
sary to compensate for chronic neuro-otologic deficits. not necessary.
3970_Ch19_309-322 25/06/14 5:58 PM Page 315
The longitudinal development of CSD-type symp- who retained the acute vestibular sway pattern reported
toms has been observed in two prospective studies of chronic dizziness throughout the 9-month study. These
patients enrolled within a few days of acute vestibular longitudinal studies suggest that high anxiety magnifies
events (vestibular neuritis or BPPV).22,23 Thirty percent postural instability and reactivity to motion stimuli dur-
of subjects reported persistent dizziness or unsteadiness ing acute vestibular events and then inhibits readapta-
at 323 and 1222 months after their acute vestibular ill- tion to postural control strategies that are associated
nesses. Importantly, chronic dizziness persisted despite with recovery.
the fact that 90% of symptomatic patients demonstrated Figure 19.132 is a schematic of this new hypothesis.
full compensation or recovery from their peripheral A triggering event induces a necessary switch to a high-
vestibular deficits. Acute behavioral responses distin- risk postural control strategy . Under normal circum-
guished patients who developed chronic dizziness from stances, vestibular, medical, and behavioral recovery (i.e.,
those most likely to recover. In particular, high levels of readaptation) take place over a time course determined by
anxiety at the onset of vertigo, excessive vigilance about the nature of the triggering event. In the presence of pre-
vestibular symptoms, and catastrophic thinking about disposing factors such as an anxious, introverted tempera-
possible adverse outcomes were the best predictors of ment or preexisting anxiety disorders, the re-adaptation
persistent dizziness and unsteadiness.22 Two smaller in- process is disrupted. Instead of recovery, the system enters
vestigations took these studies a step further by meas - a perpetual loop in which continued use of high-risk pos-
uring postural sway in addition to anxiety and physical tural control strategies maintains a heightened reactivity
symptoms during recovery from acute vestibular neuri- to motion stimuli, making previously benign situations
tis.30,31 Patients who had comorbid generalized anxiety highly provocative. Predisposing factors also increase the
swayed more than those without anxiety when standing risk of behavioral comorbidity. In this integrated model of
with eyes closed or when watching an optokinetic stim- CSD, behavioral and neuro-otologic factors are equally
ulus moving toward their damaged ear .31 The postural important elements of the pathophysiological mecha-
sway pattern during the acute period of illness had fre- nisms. Without their interaction, CSD would not exist.
quency content primarily in the vestibular range (i.e., Thus, CSD is a condition that lies at the interface between
dominated by the abnormal vestibular signals). Symp- postural control and threat systems in the brain. Neu-
tomatic recovery coincided with the appearance of a roanatomical links between these systems have been iden-
sway pattern with a broader range of frequencies, in- tified from cortex to brainstem. 33 In health, they support
dicative of a return to a more flexible postural control safe and efficient postural control. In illness, they seem to
strategy making use of multiple sensory inputs. Patients be the neural substrate for CSD.
smaller studies and extensive clinical experience. Most of well beyond the time period for compensation after an acute
the initial research on physical therapy interventions for vestibular injury. This suggests that the first vestibular reha-
vestibular disorders focused on subjects with chronic bilitation protocols were primarily habituation strategies that
dizziness.14 These early studies predated publication of reversed patients’ classically conditioned hypersensitivity to
the definition of CSD. Nonetheless, they have been in- motion stimuli and operantly conditioned alterations in gait
formative for developing vestibular habituation protocols and stance. Some of the early investigators used the term
for CSD, because descriptions of their subjects suggest habituation therapy for their treatment.
that many had CSD. Seven uncontrolled trials of SSRIs To date, there have been no studies of vestibular habit-
and SNRIs for patients with chronic dizziness, most of them uation designed specifically for patients with CSD using
targeting CSD, have been completed in the United States modern clinical trial methods. Therefore, the benefits of
and Japan.35-42 Five CBT trials have been done, including vestibular habituation for patients with CSD must be extrap-
one with 6 and one with 12 months of follow-up. 15-18,43 olated from clinical experience and the early studies of
Vestibular habituation, medication, and CBT may be used mixed groups of patients with chronic nonspecific dizziness.
alone, or more frequently, in combination for CSD. These suggest that vestibular habituation may reduce the
severity of vestibular symptoms, increase mobility , and
enhance daily functioning in 60% to 80% of patients. 14
Vestibular Habituation Exercises Vestibular habituation may also reduce anxiety and depres-
Vestibular and balance rehabilitation therapy is postulated sion in patients with chronic dizziness. 14 Successful treat-
to work by promoting compensation for peripheral or central ment of patients with CSD using vestibular habituation
vestibular deficits (see Chapters 9 and 22). However, a care- requires a gentler approach than what is typically used to
ful review of its formative research suggests that it may exert treat individuals who have just sustained an acute vestibular
its therapeutic benefits through an additional (perhaps en- injury. Habituation exercises must be less intense at the be-
tirely different) mechanism, one that is well suited to treating ginning of therapy and must be increased more gradually, or
CSD.14 The pivotal trials of vestibular rehabilitation were they will exacerbate rather than lessen symptoms. Patients
conducted in the early 1990s on patients with chronic, non- whose vestibular habituation exercises are too vigorous at
specific dizziness. The authors of those studies usually did the beginning are likely to stop therapy prematurely and con-
not report detailed neuro-otologic assessments for their sub- sider it to be a failure. Consistent benefits are usually ob-
jects. Study inclusion criteria were symptomatic in nature, tained after 8 to 12 weeks of daily , home-based exercises,
targeting deficits in function rather than specific diagnoses. but maximum improvement may require 3 to 6 months of
Nevertheless, these investigations certainly included patients diligent therapy. Table 19-2 lists several keys to developing
with CSD, most with symptoms lasting for months to years, successful vestibular habituation strategies for CSD.
Persistence • The habituation process for CSD may take more time than the compensation process for acute
vestibular deficits.
• Full benefits of vestibular habituation may not be realized for 3–6 months.
Visual flow and • Exercises that include visual flow and complex visual stimuli address the visual symptoms of CSD.
visual complexity
Real world settings • Use of indoor and outdoor settings that patients typically encounter promotes reintegration
into daily activities.
3970_Ch19_309-322 25/06/14 5:58 PM Page 318
Fluoxetine 5 to 10 10 to 20 20 to 40 20 to 60
Paroxetine 5 to 10 10 to 20 20 to 40 20 to 60
Citalopram 5 to 10 10 to 20 20 to 40 20 to 40
Escitalopram 2.5 to 5 5 to 10 10 to 20 10 to 20
Duloxetined 20 to 30 40 to 60 40 to 60 40 to 60
a Most patients can be prescribed the higher initial dose to start treatment. Those who do not tolerate that dose
and those who prefer to start treatment more cautiously may be prescribed the lower initial dose.
b Fluvoxamine is typically started at 25 mg once daily for 1 to 2 weeks and then increased to twice-daily
dosing thereafter.
c Milnacipran is typically started at 12.5 mg once daily for 2 to 3 days and then increased to twice-daily
dosing thereafter.
d Duloxetine has not been studied in clinical trials for chronic subjective dizziness (CSD), but it is used clinically.
Desvenlafaxine has not been studied in clinical trials for CSD. It is available only in 50-mg and 100-mg capsules,
which does not permit gradual titration; therefore, it is not used commonly in clinical practice for patients with CSD.
Continued
3970_Ch19_309-322 25/06/14 5:58 PM Page 320
Summary References
A condition of persistent non-vertiginous dizziness and 1. Kuch K, Swinson RP. Agoraphobia: what Westphal really
said. Can J Psychiatry. 1992;37(2):133-136.
unsteadiness was first described as phobic postural vertigo 2. Brandt T, Dieterich M. Phobischer Attacken
27 years ago. Its definition was updated 7 years ago Schwankschwindel, einneues Syndrom? Munch Med
to focus more clearly on its core physical symptoms Wschr. 1986;28:247-250.
(Table 19-1). The streamlined condition was called 3. Brandt T. Phobic postural vertigo. Neurology. 1996;46(6):
chronic subjective dizziness. It is the second most com- 1515-1519.
4. Huppert D, Kunihiro T, Brandt T. Phobic postural vertigo
mon diagnosis made in tertiary neuro-otology centers that (154 patients): its association with vestibular disorders.
recognize it, just behind BPPV and ahead of vestibular mi- J Audiol. 1995;4:97-103.
graine. CSD is defined by persistent (>3 months) symp- 5. Huppert D, Strupp M, Rettinger N, et al. Phobic postural
toms of non-vertiginous dizziness and unsteadiness that vertigo—a long-term follow-up (5 to 15 years) of 106
are worse in an upright position and can be exacerbated patients. J Neurol. 2005;252(5):564-569.
6. Best C, Tschan R, Eckhardt-Henn A, Dieterich M. Who is at
by exposure to provocative motion stimuli in the environ- risk for ongoing dizziness and psychological strain after a
ment or by performance of precision tasks. The clinical vestibular disorder? Neuroscience. 2009;164(4):1579-1587.
course of CSD is typically chronic, but fluctuating in 7. Ruckenstein MJ, Staab JP. Chronic subjective dizziness.
severity over many months or years. CSD is almost al- Otolaryngol Clin North Am. 2009;42(1):71-77.
ways triggered by an acute neuro-otologic, medical, or 8. Staab JP, Ruckenstein MJ. Expanding the differential di-
agnosis of dizziness. Arch Otolaryngol Head Neck Surg.
psychiatric illness. Two large studies have established its 2007;133(2):170-176.
differential diagnosis and identified common comorbidi- 9. Jacob RG, Woody SR, Clark DB, et al. Discomfort with
ties. New hypotheses about its pathophysiological mech- space and motion: a possible marker of vestibular dysfunc-
anisms have been developed. Perhaps most importantly , tion assessed by the Situational Characteristics Question-
studies conducted on three continents suggest that it may naire. J Psychopathol Behav Assess. 1993;15(4):299-324.
10. Bronstein AM. Visual vertigo syndrome: clinical and pos-
be treated successfully with vestibular habituation exer - turography findings. J Neurol Neurosurg Psychiatry.
cises, SSRI and SNRI antidepressants, and CBT. 1995;59(5):472-476.
3970_Ch19_309-322 25/06/14 5:59 PM Page 322
11. Honaker JA, Gilbert JM, Staab JP. Chronic subjective surface rotations. J Neurophysiol. 2004;92(6):
dizziness versus conversion disorder: discussion of 3255-3265.
clinical findings and rehabilitation. Am J Audiol. 28. Querner V, Krafczyk S, Dieterich M, Brandt T. Phobic
2010;19(1):3-8. postural vertigo. Body sway during visually induced roll
12. Eggers SD, Staab JP, Neff BA, et al. Investigation of the vection. Exp Brain Res. 2002;143(3):269-275.
coherence of definite and probable vestibular migraine 29. Ohno H, Wada M, Saitoh J, et al. The effect of anxiety on
as distinct clinical entities. Otol Neurotol. 2011;32(7): postural control in humans depends on visual information
1144-1151. processing. Neurosci Lett. 2004;364(1):37-39.
13. Staab JP, Rohe DE, Eggers SD, Shepard NT. Anxious, 30. Alessandrini M, D’Erme G, Bruno E, et al. Vestibular
introverted personality traits in patients with chronic compensation: analysis of postural re-arrangement as a
subjective dizziness. Journal of Psychosomatic control index for unilateral vestibular deficit. Neuroreport.
Research. 76(1):80-3, 2014 Jan. 2003;14(7):1075-1079.
14. Staab JP. Behavioral aspects of vestibular rehabilitation. 31. Monzani D, Marchioni D, Bonetti S, et al. Anxiety affects
Neuro Rehabilitation. 2011;29(2):179-183. vestibulospinal function of labyrinthine-defective patients
15. Holmberg J, Karlberg M, Harlacher U, et al. Treatment during horizontal optokinetic stimulation. Acta Otorhino-
of phobic postural vertigo: a controlled study of cognitive- laryngol Ital. 2004;24(3):117-124.
behavioral therapy and self-controlled desensitization. 32. Staab JP. Behavioral neurotology. In: Bronstein AM, ed.
J Neurol. 2006;253:500-506. Oxford Textbook of Vertigo and Imbalance. Oxford, UK:
16. Edelman S, Mahoney AE, Cremer PD. Cognitive behavior Oxford University Press; 2013.
therapy for chronic subjective dizziness: a randomized, 33. Balaban CD, Jacob RG, Furman JM. Neurologic bases
controlled trial [published online ahead of print November for comorbidity of balance disorders, anxiety disorders
20, 2011]. Am J Otolaryngol. 2011. and migraine: neurotherapeutic implications. Expert Rev
17. Holmberg J, Karlberg M, Harlacher U, Magnusson M. Neurother. 2011;11(3):379-394.
One-year follow-up of cognitive behavioral therapy for 34. Gerschlager W, Brown P. Orthostatic tremor - a review.
phobic postural vertigo. J Neurol. 2007;254(9):1189-1192. Handb Clin Neurol. 2011;100:457-462.
18. Mahoney AEJ, Edelman S, Cremer PD. Cognitive behav- 35. Staab JP, Ruckenstein MJ. Autonomic nervous system
ior therapy for chronic subjective dizziness: long-term dysfunction in chronic dizziness. Otol Neurotol. 2007;
gains and predictors of disability. Am J Otolaryngology. 28(6):854-859.
34(2):115-120, 2013. 36. Staab JP, Ruckenstein MJ, Solomon D, Shepard NT.
19. Staab J, Eggers S, Neff B, et al. Validation of a clinical Serotonin reuptake inhibitors for dizziness with psychi-
syndrome of persistent dizziness and unsteadiness. Ab- atric symptoms. Arch Otolaryngol Head Neck Surg.
stracts from the XXVI Bárány Society Meeting, Reykjavik, 2002;128(5):554-560.
Iceland, August 18-21, 2010. J Vest Res. 2010;20(3-4): 37. Staab JP, Ruckenstein MJ, Amsterdam JD. A prospective
172-173. trial of sertraline for chronic subjective dizziness.
20. Bisdorff A, von Brevern M, Lempert T, Newman-Toker Laryngoscope. 2004;114:1637-1641.
DE. Classification of vestibular symptoms: towards an 38. Horii A, Mitani K, Kitahara T, et al. Paroxetine, a selective
international classification of vestibular disorders. J Vestib serotonin reuptake inhibitor, reduces depressive symptoms
Res. 2009;19(1-2):1-13. and subjective handicaps in patients with dizziness. Otol
21. Best C, Eckhardt-Henn A, Tschan R, Dieterich M. Psychi- Neurotol. 2004;25:536-543.
atric morbidity and comorbidity in different vestibular 39. Simon NM, Parker SW, Wernick-Robinson M, et al.
vertigo syndromes. Results of a prospective longitudinal Fluoxetine for vestibular dysfunction and anxiety: a
study over one year. J Neurol. 2009;256(1):58-65. prospective pilot study. Psychosomatics. 2005;46:334-339.
22. Godemann F, Siefert K, Hantschke-Bruggemann M, 40. Horii A, Uno A, Kitahara T, et al. Effects of fluvoxamine
et al. What accounts for vertigo one year after neuritis on anxiety, depression, and subjective handicaps of
vestibularis—anxiety or a dysfunctional vestibular chronic dizziness patients with or without neuro-otologic
organ? J Psychiatr Res. 2005;39(5):529-534. diseases. J Vestib Res. 2007;17:1-8.
23. Heinrichs N, Edler C, Eskens S, et al. Predicting contin- 41. Horii A, Kitahara T, Masumura C, et al. Effects of mil-
ued dizziness after an acute peripheral vestibular disorder. nacipran, a serotonin noradrenaline reuptake inhibitor
Psychosom Med. 2007;69(7):700-707. (SNRI) on subjective handicaps and posturography in
24. Holmberg J, Karlberg M, Harlacher U, Magnusson M. dizzy patients. Abstracts from the XXVth Congress of the
Experience of handicap and anxiety in phobic postural Barany Society, Kyoto, Japan, April, 2008. http://www.
vertigo. Acta Otolaryngol. 2005;125(3):270-275. acplan.jp/barany2008/. Accessed July 9, 2011.
25. Warninghoff JC, Bayer O, Ferrari U, Straube A. Co- 42. Staab JP. Clinical clues to a dizzying headache. J Vest Res.
morbidities of vertiginous diseases. BMC Neurol. 2011;21(6):331-340.
2009;9:29. 43. Johansson M, Akerlund D, Larsen HC, Andersson G (2001).
26. Eckhardt-Henn A, Dieterich M. Psychiatric disorders in Randomized controlled trial of vestibular rehabilitation
otoneurology patients. Neurol Clin. 2005;23(3):731-749. combined with cognitive-behavioral therapy for dizziness
27. Carpenter MG, Frank JS, Adkin AL, et al. Influence of in older people. Otolaryngol Head Neck Surg. 125:
postural anxiety on postural reactions to multi-directional 151-156.
3970_Ch20_323-358 25/06/14 1:49 PM Page 323
FIVE
Rehabilitation
Assessment and
Management of
Peripheral
Vestibular
Disorders
3970_Ch20_323-358 25/06/14 1:49 PM Page 324
CHAPTER 20
Physical Therapy
Management of
Benign Paroxysmal
Positional Vertigo
Susan J. Herdman, PT, PhD, FAPTA ■ Jeffrey M. Hoder, PT, DPT, NCS
Benign paroxysmal positional vertigo (BPPV) is a mechan- Patients with BPPV commonly report v ertigo trig-
ical problem of the peripheral v estibular system resulting gered by lying down, rolling over in bed, bending over, and
from otoconia being displaced into the semicircular canals. looking up. Common situations in which v ertigo is pro-
It is the most common cause of recurrent and episodic ver- voked include getting out of bed, gardening, washing hair
tigo from a peripheral v estibular disorder. In the general in the shower, and going to the dentist or beauty parlor .
population, BPPV has an incidence of 64 ne w cases per Other complaints associated with BPPV include balance
100,000 people per year. With such a high incidence in the problems that may last for hours or days after the episodic
general population, an understanding of the disease and its vertigo has stopped and more v ague sensations such as
proper management becomes imperati ve. Treatment of lightheadedness or a feeling of floating (Table 20-1).
posterior semicircular canal BPPV has been studied exten-
sively, and there is considerable research that supports
“best practice” for its assessment and management.We first Historical Mention of BPPV-like Vertigo
describe the proposed mechanisms for BPPV and then ex-
Adler first described the clinical presentation of BPPV in
plore the assessments and various treatment alternatives for
1897 in his paper on “unilateral v ertigo” and recognized
this disorder.
that the posterior and anterior semicircular canals (SCC)
were most likely the affected structures.3 He reported, “Ac-
tive or passive movements of the head toward the diseased
Characteristics and History side . . . elicit severe vertigo, which can be so intense that
BPPV is characterized by brief episodes of vertigo, with the patients become pale, diaphoretic, and strongly resist an y
perception of either the environment or one’s self spinning further head turning . . . illusory movements of the envi-
when the head is mo ved into certain positions. It has been ronment occurred . . . in the respective planes of the ante-
reported in adults of all ages, although it is relatively uncom- rior and posterior semicircular canals of the affected ear.”3
mon in children.1,2 Although BPPV can occur spontaneously The clinical syndrome of recurrent positional nystag-
in many patients, it has been known to follow head trauma, mus was described in further detail by Baran y, a Nobel
labyrinthitis, or ischemia in the distrib ution of the anterior laureate otologist from Sweden, in 1921.4 Barany detailed
vestibular artery.1 Spontaneous remission of this condition the case of a 27-year-old woman who experienced recur-
is common. For those patients in whom the episodic vertigo rent attacks of vertigo for 2 weeks. “. . . these attacks only
persists, this disorder can be annoying, disruptive, and often occurred when the patient lay on her right side. When she
results in significant changes in normal activities. did this, there occurred a strong rotatory nystagmus to the
324
3970_Ch20_323-358 25/06/14 1:49 PM Page 325
326 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Theoretically, with the utricular degeneration that occurs A history of episodic v ertigo with position changes
during acute vestibular neuronitis, otoconia break free and and a positive Dix-Hallpike Test are the clinical practice
float into the still functioning posterior SCC (which is in- guidelines for diagnosis of BPPV.26,27 All tests for BPPV
nervated by the inferior branch of the v estibular nerve). can be performed in room light, b ut the use of Frenzel
The patient presents with vestibular hypofunction and pos- lenses or an infrared camera system to pre vent fixation
terior SCC BPPV. suppression of horizontal and v ertical nystagmus may
increase the likelihood of a correct diagnosis. Torsional
Current Diagnosis and Management nystagmus is not suppressed by fixation.
Three different maneuvers can be used to evaluate an in-
dividual for the presence of BPPV. For all the maneuvers,
observation of the direction and duration of the nystagmus
Tests that Identify BPPV Affecting
by the clinician is critical to determining canal in volve-
the Vertical Canals
ment and to developing a treatment plan. Therefore, it is Dix-Hallpike Test
important that the patient understands what to expect. Dur- The Dix-Hallpike Test, sometimes called the Baran y
ing testing, patients should k eep their eyes open and re- maneuver or the Nylen-Baran y maneuver, is considered
main in the provoking position. To discourage the patient the Gold Standard test for the diagnosis of BPPV
from attempting to mo ve out of the pro voking position (Fig. 20.3)6,26-28 The combination of a history of episodic
once symptoms begin, prior to testing, the clinician should vertigo with position changes and a positive Dix-Hallpike
explain that the vertigo will stop or decrease if the patient Test are the suggested clinical practice guidelines for
remains in the position. If the patient’ s history suggests diagnosis of BPPV.26,27
which side is affected, it is best to test the presumed unaf- This maneuver places the posterior SCC of the down-
fected side first to minimize nausea. For patients with se- side ear in the plane of the pull of gravity. Debris adhering
vere nausea and a history of emesis associated with to the cupula or free-floating in the long arm of the canal
vertigo, the testing maneuvers should be performed more will shift away from the cupula, resulting in v ertigo and
3970_Ch20_323-358 25/06/14 1:49 PM Page 328
328 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
AC
Left
AC PC
HC
PC
Right
nystagmus. In most cases of BPPV, nystagmus and vertigo sensitivity was 79% [95% conf idence interval (CI)
occur within a few seconds of the position change, but oc- 65-94], specificity was 75% (33-100), positive likelihood
casionally the signs and symptoms will ha ve a longer ratio (LR) was 3.17, and the negative LR was 0.28. For
delay until onset, even as much as 30 seconds. If the pa- the Sidelying Test, they reported an estimated sensitivity
tient has BPPV, vertigo and nystagmus will be provoked of 90% [with a 95% CI of 79-100] and a specif icity of
when the affected ear is inferior. The patient may also ex- 75% [95% CI of 33-100]. The positive likelihood ratio
perience vertigo upon returning to the sitting position.The was 3.59 and the negative likelihood ratio was 0.14.28 In
test can then be repeated with the patient’s head turned to a more recent article, unfortunately with only the abstract
the other side. If the debris is within the posterior semi - published in English, the sidelying test demonstrated
circular canal, the resultant nystagmus during testing will concurrent validity with Dix-Hallpik e for identifying
be upbeating and torsional towards the side being tested. both posterior and anterior SCC BPPV.30
A B C D E
Figure 20.5 In the Roll Test, the patient lies supine with the head elevated 15–20 deg (A).
This places the horizontal canals in the plane of the pull of gravity. The head is then quickly
rolled to the left (B) to see if that will provoke the vertigo and nystagmus. Careful observa-
tion of the nystagmus is essential to determine whether the patient has the canalithiasis or
the cupulolithiasis form of HC BPPV. The head can then be brought back to the neutral posi-
tion (C). After waiting until nystagmus ceases, the head is rapidly turned to the right (D).
Vertigo and nystagmus will be elicited in both the head left and head right positions. When
the patient’s vertigo and nystagmus stop, the patient’s head is returned to neutral (E).
3970_Ch20_323-358 25/06/14 1:49 PM Page 330
330 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Bowing position
Cupulolithiasis Canalithiasis
Frontal view right HSCC Frontal view left HSCC Frontal view right HSCC Frontal view left HSCC
Leaning position
Cupulolithiasis Canalithiasis
Frontal view right HSCC Frontal view left HSCC Frontal view right HSCC Frontal view left HSCC
C
3970_Ch20_323-358 25/06/14 1:49 PM Page 331
Figure 20.6 After the Roll Test has been used to determine if the patient has canalithiasis
or cupulolithiasis, the Bow and Lean Test is used to determine which horizontal canal is in-
volved. The starting position is shown in (A). In the “bow” position (B), the nystagmus beats
away from the affected side if the patient has the cupulolithiasis form of BPPV and toward
the affected ear in the canalithiasis form of BPPV. In the “lean” position (C), in cupulolithiasis
the nystagmus beats toward the affected ear but in canalithiasis, the nystagmus beats away
from the affected ear.
using both the Roll Test and the BLT, the direction of nys-
■ Table 20-4 NYSTAGMUS FEATURES BY
tagmus during the BLT was used to determine which side
CANAL AFFECTED IN BPPV
was affected. The additional information provided by the
BLT to determine side of involvement improved the effi- Canal Affected Initial Response in Dix-Hallpike
cacy of treatment of those with HSC-BPPV canalithiasis
from 67.4% to 83.1% after two sessions of canalith repo- Posterior Upbeating and torsional (torsional
sitioning, and those with cupulolithiasis from 61.1% to toward affected ear)
74.7%. This suggests that the BLT may be a useful adjunct
Horizontal: Geotropic (right-beating in head
to perform following the Roll Test, especially when the
canalithiasis right position, left-beating in head
affected side is difficult to determine.38
left position)
332 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Dix-Hallpike test;
if no response to
Dix-Hallpike, do
sidelying test To left
side, which canal is in volved (based on direction of remission exist primarily for the Canalith Repositioning
nystagmus), and whether the problem is caused by Treatment for Posterior SCC BPPV.41-44 Some evidence
canalithiasis or cupulolithiasis leads to specif ic treat- now supports the treatment of Horizontal SCC BPPV .45
ments or to consideration that the nystagmus may be of The results of these studies must be interpreted cautiously,
central origin. however, because of the high incidence of spontaneous
remission that occurs in patients with BPPV . Several
authors report that spontaneous reco very occurs within
Evidence-based Treatments 3 to 4 weeks of onset, 46,47 but others suggest that sponta-
Successful treatment is dependent on identifying which neous recovery may still occur even several months from
canal is involved and whether the debris is free-floating or onset.48 Imai et al reported in 2011 that the natural course
adhering to the cupula. There are three basic bedside treat- of remission in the apogeotropic form of horizontal SCC
ments for BPPV, each with its o wn indications for use: BPPV is an average of 13 days, and the geotropic form is
Canalith Repositioning, and Liberatory and Brandt-Daroff an average of 16 days.49
Habituation Exercises. Variations of these treatments have For a given patient, the choice of which e xercise is
been developed depending on which semicircular canal is most appropriate depends on which canal is involved and
involved. Studies on the ef ficacy of these treatments that whether the patient has the canalithiasis or cupulolithiasis
provide strong e vidence that these treatments result in form of BPPV.
3970_Ch20_323-358 25/06/14 1:49 PM Page 333
334 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
A B C D E
Figure 20.8 Treatment used for the canalithiasis form of both posterior and anterior SCC
BPPV (arrows point to location of debris in the left posterior SCC). In the Canalith Reposition-
ing Treatment, the patient is first taken into the Dix-Hallpike position (A to B) and kept there
until the nystagmus stops or for twice the duration of the initial nystagmus. The patient then
rolls his/her head, with assistance from the clinician, slowly through moderate extension to-
ward the unaffected side (B to C) and kept in the new position until the nystagmus stops or
for twice the duration of the initial nystagmus. The patient is then rolled onto the unaffected
side with the head turned 45 deg down (toward the floor) and kept there until the nystag-
mus stops or for twice the duration of the initial nystagmus (C to D). In each of these posi-
tions, the patient may experience a short spell of vertigo as the otoconia move away from the
cupula through the posterior canal. Finally, keeping the head deviated toward the unaffected
side, the patient then slowly sits up (D to E) and can then straighten the head. The same ma-
neuver would be used for the canalithiasis form of anterior SCC BPPV on the left side. (Modi-
fied from Tusa RJ and Herdman SJ. Canalith Repositioning for Benign Positional Vertigo.
Education Program Syllabus 3BS.002, Amer Acad Neuro, Minnesota, 1998, p 13.5)
or when the four-position maneuver was re- as found by Epley.50 It is useful to know that it is
peated several times, remission was 83%. Sev- not necessary to move the patient through the
eral studies have shown that when patients are different positions quickly. Waiting longer be-
moved through four positions multiple times, a tween changes in positions allows the nausea to
93% remission rate can be achieved.11,55 Wolf decrease and helps to prevent actual emesis.
et al found a 93.4% remission rate in patients 4. Use of vibration during the maneuver: in the
treated with only the first four positions when original procedure, Epley suggested that two dif-
multiple repositioning treatments are performed ferent applications of mechanical vibration to the
during the same clinical visit.55 Therefore, it mastoid of the affected side be used during treat-
seems that either approach—using five posi- ment. During one cycle, a standard electromag-
tions or using four positions but repeating the netic bone conductor vibrator is used, and then in
maneuver multiple times—is effective. How- another cycle of the maneuver, a handheld vibra-
ever, for patient comfort, using the five-position tor (80 Hz) is used.50 The theoretical purpose of
sequence is recommended rather than repeating the vibration was to prevent the debris from ad-
the four-positions maneuver multiple times. hering to the walls of the canal and to aid in the
3. The timing between position changes within the movement of the debris through the canal. Sev-
maneuver: the total timing between the position eral studies have failed to identify any difference
changes in the CRT is based on the combination in outcome whether a vibrator is used or not
of the latency until nystagmus begins plus the used,57-59 and a Cochrane review concluded that
time until the nystagmus stops. Once the pa- there was no evidence that mastoid oscillation
tient’s head has been moved into a new position, was beneficial.60 Epley also advocated the use
that position is maintained until the nystagmus of mastoid vibration in the case of blockage of
slows down. At that point, the head is moved into the SCC by the debris, or “canal jam,” such as
the next position in the sequence. If nystagmus is when a patient has no nystagmus on testing.61
not observed in any given position, which hap- However, it is important to recognize that in a
pens frequently, then the timing is based on the case of a complete “canal jam,” there would be
duration of nystagmus established during the ini- no nystagmus or complaints of vertigo with
tial Dix-Hallpike maneuver. Several studies have change in head position. The debris would essen-
used a longer period between each change in tially block movement of the endolymph, and
position11,55,56 with essentially the same results therefore, the cupula would not be displaced.
3970_Ch20_323-358 25/06/14 1:49 PM Page 335
5. Post-treatment instruction: The last component for posterior canal BPPV , based on the results of 292
of the original CRT was the post-treatment in- patients in five mostly randomized controlled trials with
struction. The patient was advised to keep the the importance of spontaneous remission of BPPV involv-
head upright for 48 hours following the treat- ing the posterior SCC, citing 20% to 38% of control
ment, including sleeping with the head elevated patients were found to ha ve a ne gative Dix-Hallpike
45 degrees. The follow-up visit for reassessment, maneuver at follow-up.41,42 Helminski et al (2010) and
and if necessary another treatment, would be Teixeira et al (2006) performed systematic re views of the
scheduled for 1 week later. Asking patients to literature with similar results related to treatment of poste-
keep the head upright for 48 hours, presumably rior canal BPPV through the use of canalith repositioning
preventing the loose otoconia in the utricle from procedures, including the Epley Maneuver.43,44 Both con-
moving back into the posterior semicircular clude that canalith repositioning procedures are more
canal, is difficult for many patients. Patients effective than controls in managing PC BPPV. Complica-
would report not sleeping well or a sore neck. tions of nausea, vomiting, fainting, or conversion to hori-
Fortunately, these post-treatment instructions do zontal canal BPPV occurred in 6% to 12% of patients. 53
not appear to be necessary to the success of the Most controlled randomized treatments ha ve used re-
treatment60,62,63 Massoud and Ireland62 examined peated repositioning maneuvers within one treatment ses-
the need for post-treatment instructions of stay- sion. Gordon and Gadoth (2004), ho wever, found no
ing upright for 48 hours. Two groups of patients significant difference in outcome between those patients
were given the CRT or another treatment (the treated with repeated maneuvers within a single session
Liberatory maneuver) and were asked to sleep (92% remission) and those patients treated with only one
upright for 2 nights and then on the normal side maneuver (80%).64
for an additional 5 nights. Two other groups were
given the same maneuvers but were not given any CASE: Your patient is a 49-year-old man who experi-
post-maneuver instructions other than to avoid enced vertigo when he was hanging wallpaper about
brisk head movements for 1 week. All patients 24 days ago. He thinks the vertigo is brief but, when
had a follow-up visit at 1 week after treatment. asked, states that he always moves his head when the
They found no statistical difference in the four vertigo starts. He was seen by a physician 2 weeks
groups (analysis of variance, P greater than 0.2). ago and was given a prescription for Valium® but has
The success rate of the maneuvers was 88% to taken it only twice, because it makes him sleepy. He
96%. Similar results were reported by Nuti et al,63 has not returned to work. The physician has referred
who examined 52 patients at 20 minutes, him to you for treatment of his vertigo. On examina-
24 hours, and 7 days after the Liberatory tion today, oculomotor tests are normal except for an
maneuver for posterior canal BPPV. A Cochrane upbeating and rightward torsional nystagmus with
Review found a statistically significant differ- vertigo that lasts for 60 seconds when moved into the
ence in remission rates between patients with right Dix-Hallpike position, at which time you moved
and without post-treatment instructions but con- him out of the Dix-Hallpike position. You decide that
cluded that the clinical impact was insignificant. the patient has the cupulolithiasis form of right poste-
In summary, there does not appear to be a strong rior SCC BPPV because of the persistence of the nys-
benefit to requiring patients to remain upright tagmus and vertigo.
overnight after the canalith repositioning maneu-
In 1988, Semont et al proposed a single “liberatory”
ver. Having patients stay upright for as little as
maneuver designed to move the debris from the posterior
20 minutes after the maneuver may be sufficient
SCC and reposition it back into the utricle (Fig. 20.9). 65
for remission of BPPV.
The technique uses inertia and position changes against
There is strong e vidence to support the use of the gravity to move the debris mechanically. The treatment
canalith repositioning treatments as safe and effective treat- has several names including Semont maneuver, Liberatory
ments compared with no treatment for posterior canal treatment, or brisk treatment.11,65,66 Presumably, the rapid
BPPV (Table 20-5). Cochrane reviews yielded a statisti- acceleration and deceleration of the mo vement from the
cally significant effect in favor of the Epley Maneuver over initial sidelying position to the second (opposite side) side-
control, in terms of complete resolution of symptoms and lying position (Fig. 20.9) can dislodge debris adhering to
conversion from a positive to a negative Dix-Hallpike Test the cupula of the SCC and thus is considered as a treat-
without serious adverse effects.41,42 The reviews support ment for posterior SCC cupulolithiasis as well as a treat-
the use of the Epley Maneuver as a safe, effective treatment ment for posterior SCC canalithiasis.
3970_Ch20_323-358 25/06/14 1:49 PM Page 336
336 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Systematic review Helminski et al Of 10 studies identified Odds in favor of resolution of BPPV were
modified Epley 201044 via literature review, 22 times (95%, CI 3.41–141.73) and 37
vs. Sham 2 RCTs double-blinded, times higher (95%, CI 8.75–159.22) in
2 Quasi-RCTs met persons receiving CRP vs. sham.
inclusion.
Systematic review Teixeira and 5 RCT trials found. Positive evidence of efficacy for Epley’s
Epley vs. Sham Machado 200643 maneuver at 1 week and 1 month.
Systematic review Hilton and Pinter Of 22 studies that met Epley maneuver is safe and effective treat-
modified Epley 200442 inclusion criteria, ment of Posterior canal BPPV vs. sham.
vs. Sham 5 RCTs were included; Patients who received Epley completely re-
others were generally solved symptoms (95%, CI 1.84–13.16) and
poor methodological conversion to negative Dix-Hallpike (95%,
quality. CI 2.21–14.56)
RCT, prospective, Lynn 199547 n = 36 Conversion to 89% cure rate for CRP group vs. 27% cured
single-blinded; negative Dix-Hallpike in Sham group
modified Epley
vs. Sham
RCT, prospective, Froehling et al n = 50 Conversion to 67% cure rate for CRP vs. 38% cure rate
single-blinded 200067 negative Dix-Hallpike for Sham
RCT, modified Munoz 200768 n = 81 Conversion to Single treatment: 34.2% cure rate for CRP
Epley vs. Sham negative Dix-Hallpike group vs. 14.6% in Sham group; Resolution
of dizziness: 31.6% of CRP group and 24.4%
of Sham group. One week later, CRP group
and Sham group both received the CRP, and
61.8% and 57.1%, respectively, had negative
DH test results.
RCT, modified Von Brevern n = 67 Conversion to 80% cure rate for CRP, 10% cure rate for
Epley vs. Sham 200669 negative Dix-Hallpike Sham
RCT, modified Yimtae 200370 n = 58 Conversion to 75.9% cure rate for CRP, 48.2% cure rate for
Epley vs. Sham negative Dix-Hallpike Sham
Semont and colleagues reported on a large cohort of the Liberatory maneuver in a series of patients using the
patients with BPPV (n = 711) treated o ver an 8-year pe- patients as their o wn controls.71 The patients were f irst
riod.65 They found a remission rate of 84% after a single treated with the Liberatory maneuv er but on the unaf-
treatment and of 93% after two treatments. Recurrence of fected side; none of the patients had relief from their
the symptoms was infrequent (4%). In a prospective, ran- symptoms. The patients were then “treated” with just the
domized study that included 30 subjects treated with the post-maneuver instructions to k eep the head upright for
Semont maneuver, Herdman et al (1993) reported remis- 48 hours. Again, at the end of 1 week, all patients were
sion of symptoms and/or signs of signif icant improve- symptomatic. Finally, the patients were treated with
ment in 90% of the cases after a single treatment. 11 In a the Liberatory maneuver on the affected side. At the end
later study, Ireland (1994) examined the effectiveness of of 1 week, all patients were symptom-free. Although the
3970_Ch20_323-358 25/06/14 1:49 PM Page 337
number of subjects in this study is small (n = 10), the re- the cupulolithiasis form of BPPV of the posterior SCC.
sults support the effectiveness of the Liberatory maneu- However, Semont did not describe the nystagmus in his
ver as treatment for BPPV. Other studies have reported large series of patients, and the incidence of cupulolithi-
somewhat lower remission rates. Hausler and Pampurik asis is relatively infrequent. Therefore, it remains un-
(1989) and Le vrat et al (2003) reported remission of clear what the treatment efficacy is for the Liberatory or
symptoms in 51% and 62.6% of their subjects treated, Semont maneuver with the cupulolithiasis form of
respectively.72,73 BPPV. Evidence suggests that it is also appropriate for
The Liberatory maneuv er can also be used in patients with the canalithiasis form of posterior SCC
patients with canalithiasis, in which the success rate BPPV. It is important to note that the Liberatory maneu-
is as high as 86.8% after one treatment. 74 In a placebo- ver may be difficult to perform with elderly patients, be-
controlled, double-blinded study, there was a signifi- cause of the quickness of mo vement required of the
cantly greater rate of remission in patients treated using procedure.
the Liberatory maneuver (86.8%) compared with a sham
treatment (0%) at 1 and 24 hours after treatment.A second Treatment of Anterior SCC BPPV
study showed similar findings at 4 days post-treatment
CASE: Your patient is a 36-year-old female who
with 84% remission in the treated group compared with
needed to be seen urgently in your clinic because
14% in a sham treated group of patients with PC SCC
of complaints of severe vertigo. The patient has
BPPV.75
not gone to a physician at the time of your initial
Because the Liberatory treatment may dislodge ma-
evaluation. She reports that she woke up with
terial adhering to the cupula and move the debris toward
severe complaints of vertigo and vomiting
the utricle, we believe this is the optimal treatment for
3970_Ch20_323-358 25/06/14 1:49 PM Page 338
338 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
yesterday, and although she is no longer vertigi- approximately 20 seconds. She has some nausea
nous, she does not feel well and is somewhat off- but no vomiting, and you proceed to treat her with
balance. Past medical history is not significant; the the CRT for left anterior SCC BPPV.
only medication she is taking is for birth control.
The evidence for treatment ef ficacy for Anterior
She rates her vertigo as of yesterday as a 9/10 on a
SCC BPPV canalithiasis is limited to descripti ve studies
visual analogue scale and her dizziness and imbal-
(Table 20-6). The majority of patients treated seem to
ance today as a 6/10. Oculomotor exam in sitting is
respond to the CR T starting on the af fected side (see
normal. You perform the Dix-Hallpike Test slowly
Fig. 20.8).76,77 Complicating the issue of which might be the
because of the vomiting she had yesterday; she
most effective treatment is the fact that there are at least seven
develops a rapid downbeating and leftward tor-
proposed treatments for Anterior SCC BPPV canalithiasis,
sional nystagmus in the left Dix-Hallpike position,
some with only a few subjects.76-85 Additionally, some studies
and she describes vertigo concurrent with the
used the same treatment for both the canalithiasis and cupu-
nystagmus. The nystagmus and vertigo last for
lolithiasis forms of anterior SCC BPPV.77
Sitting to supine with head hanging Yacovino et al 200931 13 84.6% in one maneuver;
to head flexed 30 degrees in 100% in two
30-second intervals
Dix-Hallpike to unaffected side for Kim et al 200583 30 40.7% after one and
2 minutes; then elevate head to level 5 92.3% after three
1 minute and then return to sitting with maneuvers
chin tucked (30 degrees) Korres et al 200884 60% in one treatment;
100% by two treatments
Forced Prolonged Position (FFP) for toward the healthy ear until he or she is in sidelying with
Horizontal Canal Canalithiasis the healthy ear down. He or she then remains lying on the
Another treatment option for horizontal SCC canalithiasis unaffected side all night. The forced prolonged position
BPPV is Forced Prolonged Position (Fig. 20.12) described can be combined with the roll treatment by having the pa-
by Vannucchi and colleagues. 89 The patient goes to bed tient perform a roll treatment followed by utilizing the FFP
and lies in sidelying on the af fected side (more sympto- at night. Should the client need to get up at night, the
matic side) for 30 to 60 seconds and then slowly rolls over maneuver is repeated.
3970_Ch20_323-358 25/06/14 1:49 PM Page 340
340 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
HC
A B
D C
Figure 20.11 In the Appiani treatment (shown here for
left-sided HC canalithiasis), the patient starts sitting on
the treatment table (A). The patient is quickly brought to HC
a side-lying position on the unaffected side and stays in
this position for 2 min (B). The patient’s head is rapidly
rotated 45 deg down toward the table, again staying in
this position maintained for 2 min (C). The patient is slowly
brought back to sitting and the cervical spine returned to
a neutral position. This treatment has also been referred
to as the Gufoni treatment for canalithiasis (D). (From
Appiani GC, et al, 2001; ).88 L
B
Treatment of Horizontal SCC
Cupulolithiasis HC
342 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Supine with head straight ahead, then three Lempert and 2 100%
rapid 90-deg rolls toward unaffected ear, then sit Tiel-Wilck 199686
(Lempert maneuver)
Lempert maneuver: Supine with head straight Sekine et al 63 At 1 week: treated 78.6%;
ahead, then three rapid 90-deg rolls toward 200696 untreated control group
unaffected ear, then sit (n = 29) 69.1% (no significant
Control: untreated (n = 34; consented but all difference)
at different hospital from treated group)
Forced prolonged positioning: lie supine, rotate Vannucchi et 74 90% remission for FPP in
head and body to unaffected side, lie in that al 199789 3 days
position for 8–12 hours Pseudo randomized; control
group untreated sample of
convenience
Vannuchi maneuver followed by FFP Nuti et al 200597 18 88.8% symptom and nystag-
mus free with one treatment
series; 100% in two
Patient sits w/ head straight ahead, quickly lies Appiani et 32 78.12% with one maneuver;
on unaffected side for nystagmus duration plus al 200188 100% with two maneuvers
1 minute, quickly turns head 45 degrees down
for 2 minutes, slowly sits up
Gufoni maneuver: Patient sits w/ head straight Francesco et 58 79.3% complete resolution
ahead, quickly lies on unaffected side 2 minutes, al 200998 with one session; 13.8%
quickly turns head 45 degrees down for converted to PSCC BPPV;
2 minutes, slowly sits up; then repeated 6.9% no benefit
Randomly assigned to 360 Bar-B-Que roll plus Casani et al 132 Bar-B-Que + FPP: 61% re-
FPP for 12 hr (n = 54) or to 201199 mission with one treatment;
Gufoni (aka Appiani) maneuver for canalithiasis 79.6% with three treatments
(n = 58)
1. Lie on side of weaker nystagmus all Boleas- 22 1. 68% (n = 15) free of vertigo and
night for two weeks (FPP-one); Aguirre nystagmus
2. For those who converted from et al 2009101 2. Converted to canalithiasis (n = 1)
cupulolithiasis to canalithiasis with treat with Lempert or to vertical
FFP-one; Lempert maneuver canal (n = 3) treat with Epley;
3. For those with no responses to FFP-one; 100% resolution
lie on side of greatest nystagmus all 3. No response to FFP-one (n = 3),
night for 2 weeks then treated with FPP-two with
4. If converted to canalithiasis, treated 66% resolution
with Lempert maneuver (n = 1)
Canalithiasis (n = 55) Bar-B-Que roll follo wed Casani et al 82 Resolution in 67.4% with one,
by forced prolonged posi- 200290 80% in two, and 89.1% in three
tioning maneuvers
Cupulolithiasis (n = 9) Seated, quickly lie on Resolution in 44.4% in one,
affected side, turn head 55.5% in two, and 66.6% in
down 45 degrees and stay three maneuvers
in that position for 2–3 Resolution in 16.6% in 1 week;
minutes, rapidly sit up 44.5% in 2 weeks
Control (n = 18) Vestibular suppressant
medication; sample of
convenience
Cupulolithiasis FFP: lie on side of weaker Chiou et al 29 93.1% cases resolved with FFP
Utricular-side nystagmus for 12 hr 2005100
Canalithiasis (n = 36) Bar-B-Que roll for Escher et al 46 74% resolution after one ma-
and Cupulolithiasis 360 degrees in 90-degree 2007102 neuver; 80% after two; 85%
(n = 10) steps; each position held after maximum of three; form of
for 30 sec BPPV had no affect on outcome
344 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Humphriss et al (2003) consider a number of disor - perform the Romberg test for 30 seconds with eyes
ders to be absolute contraindications to performing the open and closed, but her single leg stance time is only
Dix-Hallpike test, and presumably also to performing 3 seconds. Her fall risk score (DGI) is an 18/24, and
some of the treatments (Table 20-10).95 We would suggest her gait speed is slow for age and gender. One possi-
that most individuals with these disorders can be tested bility is that her balance will probably improve over
and treated, but certain precautions must be tak en to en- the next 2 weeks, but you are concerned that with
sure patient safety, especially avoiding extension and ro- her age, gender, single leg stance time, and DGI
tation of the patient’s neck. score, she is at a greater risk for falling than usual.
Therefore, you decide to give her exercises to help
Managing Persistent Imbalance improve her balance.
in Patients with BPPV Over 50% of patients with posterior SCC BPPV sub-
jectively report imbalance.103,104 Imbalance relative to age-
CASE: Your patient is a 76-year-old woman with the
matched controls has been quantified using computerized
canalithiasis form of posterior SCC BPPV. On her
static and dynamic sway platform testing.105-111 The CRT
initial visit, you appropriately treated her with a CRT,
and Liberatory maneuver may completely resolv e posi-
as that was her primary problem. She has returned for
tional nystagmus and vertigo based on repeat Dix-Hallpike
her second visit 7 days later. She reports that she has
Test and improved balance based on repeat computerized
had no vertigo since the treatment but feels very off-
platform testing,105,106,108,111 but 8% to 14% of patients
balance and staggers at times when walking. On her
may still complain of residual imbalance.11,112,113 One pos-
assessment today, she has no nystagmus or vertigo
sibility is that this imbalance is caused by BPPV that
in the right or left Dix-Hallpike positions, and you
is not sufficient to deflect the cupula during testing. An-
conclude that her BPPV is in remission. She rates
other possibility is an underlying vestibular hypofunction
her disequilibrium while walking as a 4.1/10. Her
that was not detected during the initial evaluation. 114 Sev-
balance confidence (ABC score) is a 67%. She can
eral studies have suggested that a concurrent v estibular
3970_Ch20_323-358 25/06/14 1:49 PM Page 345
• Cervical spine instability Unsteadiness with Neck pain, facial pain, headaches, paresthesia in
e.g., atlantoaxial instability walking hands, feet, face, or tongue; head and neck feeling
• Occipitoatlantal instability unstable. Dizziness and vertigo.
e.g., RA, Down’s syndrome
• Prolapsed intervertebral Restricted neck Severe neck pain with referred pain in arm, hand, and
disk with radiculopathy movements. Muscle fingers. Paresthesia and numbness in the arm, hand,
weakness in the arm and fingers, down the line of nerve distribution.
and/or hand
• Cervical myelopathy Unsteadiness on feet • Pain in neck and/or arms. Loss of power in arms,
hands, legs. Numbness or paresthesia in hands
and/or feet. Increased tone in limbs.
• Vascular dissection syndromes Horner’s syndrome • Facial and neck pain, acute retro-orbital pain.
• Acute trauma to neck (“whiplash”) • Neck, arm, facial, trunk pain with restricted neck
– Contraindicated if insufficient movement. Vertigo, dizziness symptoms. Symp-
ROM of cervical spine tom severity will vary.
• Rheumatoid arthritis Arthritic deformities, • Neck pain and restricted movement. May have
especially feet/hands, signs of cervical spine instability
knees/elbows. (see above).
• Aplasia of the odontoid process Cervical spine instability • Neck pain, transient neurological symptoms
Modified from Humphriss RL, Baguley DM, Sparkes V, et al. Contraindications to the Dix-Hallpike
manoeuvre: a multidisciplinary review. International J Audiology. 2003;42:166-173.21
hypofunction is not the underlying cause of this residual CRT. Approximately 66% of the patients did not improve
imbalance. Blatt et al 106 and Di Girolamo et al 105 quanti- to normal values by age after CRT, yet none of the patients
fied the degree of imbalance in patients with posterior had signs or symptoms of BPPV.
canal BPPV who did not ha ve evidence of v estibular So what is the cause of persistent imbalance in pa-
hypofunction (based on bithermal caloric testing) using tients in remission from BPPV? One possibility is the age
computerized dynamic posturography before and after of the patient. In the study by Blatt et al, those patients
3970_Ch20_323-358 25/06/14 1:49 PM Page 346
346 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
who improved to within normal v alues by age were with BPPV. If balance does not improve with treatment of
younger (p < 0.05).106 No difference was found between the BPPV, then patients should be reexamined to rule out
groups for time from onset of BPPV , history of f alls, or vestibular hypofunction or some other cause for imbal-
the patients’ rating of the intensity of vertigo, although the ance. If appropriate, patients should then be referred for
patients’ subjective rating of the intensity of disequilib- specific exercises to improve balance.
rium approached significance. Another possibility is that
the increased postural sway by some individuals on these
tests may be a result of a separate, pree xisting problem
Unraveling Complicated Cases
with balance that occurs in the elderly , such as disuse Unfortunately, not all patients with BPPV ha ve obvious
disequilibrium, which w ould not impro ve after CR T. signs and symptoms, nor do they necessarily have involve-
Alternatively, it is possible that it takes time for the otoliths ment of only one semicircular canal. The cases below
to fully recover following CRT. This latter explanation is illustrate some of the more confusing presentations. All
supported by the study of Giacomini et al, who found that patients in the cases belo w were tested using Frenzel or
balance on a static platform did not fully reco ver in pa- IR goggles. Additionally, Figure 20.15 presents an algo-
tients with BPPV until 12 weeks after CR T.105 This has rithm that may pro vide some assistance in making deci-
significant implications for the rehabilitation of patients sions when confronted by difficult cases.
Results in Do Results in Do
History of
episodic vertigo
Nystagmus is
appropriate and Treat for BPPV
with vertigo
No nystagmus, Dix-Hallpike to
no vertigo symptomatic side Stalwart patient
Nystagmus but no
vertigo
Not BPPV
Downbeating and
torsional nystagmus, No nystagmus, Fear, anxiety,
mild vertigo complains of vertigo conditioned
response
348 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Explanation Resolution
There are two possibilities: either the patient has the Treat the patient for left posterior SCC canalithiasis
canalithiasis form of posterior SCC BPPV on the left BPPV. If the n ystagmus and vertigo resolve on both
side and the canalithiasis form of anterior SCC BPPV sides, then it w as a false bilateral BPPV. If, after you
on the right side, or this is an example of false bilateral achieve resolution of the posterior SCC BPPV on the
BPPV. In the latter situation, the patient actually has left, the patient still has downbeating and rightward tor-
posterior SCC BPPV on the left side; the mild obser- sional nystagmus when in the right Dix-Hallpike posi-
vation of downbeating and torsional n ystagmus ap- tion, then it w as a true case of bilateral BPPV—go
pearing concurrently with mild complaints of v ertigo ahead and treat for the anterior SCC canalithiasis BPPV.
350 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Provoking Dix-Hallpike or Dix-Hallpike or Roll Test, Bow and Lean test; All tests negative,
maneuvers Sidelying tests Sidelying tests may occur with Dix-Hallpike may have occurred
before coming to
clinic
Nystagmus Upbeating and Downbeating and tor- Geotropic and brief if Not observable
torsional toward sional toward affected canalithiasis; apogeotropic and
affected side side persistent if cupulolithiasis
Affected side Torsional toward Torsional toward Canalithiasis – beats toward Could not be
affected side affected side affected side during ‘bow’; determined
cupulolithiasis – beats to-
ward affected side in ‘lean’
Precautions May convert to AC Can be confused with Causes greater nausea, May not be BPPV
or HC BPPV central nystagmus, which vomiting, and imbalance
during treatment is often downbeating,
especially if persistent
3970_Ch20_323-358 25/06/14 1:50 PM Page 351
352 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
37. Baloh RW, Yue Q, Jacobson KM, Honrubia V. Persistent 56. Tirelli G, D’Orlando E, Zarcone O, Giacomarra V. Modi-
direction-changing positional nystagmus: another variant fied particle repositioning procedure. Laryngoscope. 2000;
of benign positional nystagmus? Neurology. Jul 1995; 100:462.
45(7):1297. 57. Hain TC, et al. Vibration does not improve results of the
38. Lee JB, Han DH, Choi SJ, et al. Efficacy of the “bow and canalith repositioning procedure. Arch Otol Head Neck
lean test” for the management of horizontal canal benign Surg. 2000;126:617.
paroxysmal positional vertigo. Laryngoscope. 2010;120 58. Sargent EW, Bankaitis AE, Hollenbeak CS, Currens JW.
(11):2339. Mastoid oscillation in canalith repositioning for paroxys-
39. Choung YH, Shin YR, Kahng H, et al. ‘Bow and Lean mal positional vertigo. Otol Neurotol. 2001;22:205.
Test’ to determine the affected ear of horizontal canal 59. Ruckenstein MJ, Shepard NT. The canalith repositioning
benign paroxysmal positional vertigo. Laryngoscope. procedure with and without mastoid oscillation for the
2006;16:1776. treatment of benign paroxysmal positional vertigo. ORL
40. Cakir BO, Ercan I, Cakir ZA, et al. What is the true J Otorhinolaryngol Relat Spec. 2007;69(5):295-298.
incidence of horizontal semicircular canal benign 60. Hunt WT, Zimmermann EF, Hilton MP. Modifications of
paroxysmal positional vertigo? Otol Head Neck Surg. the Epley (canalith repositioning) manoeuvre for posterior
2006;134(3):451. canal benign paroxysmal positional vertigo (BPPV).
41. Hilton M, Pinder D. The Epley manoeuvre for benign Cochrane Database Syst Rev. Apr 18, 2012;4:CD008675.
paroxysmal positional vertigo—a systematic review. doi:10.1002/14651858.CD008675.pub2.
Clin Otolaryngol Allied Sci. 2002;Dec;27(6):440. 61. Epley JM. Human experience with canalith repositioning
42. Hilton M, Pinder D. The Epley (canalith repositioning) maneuvers. Ann N Y Acad Sci. 2001;942:179-191.
manoeuvre for benign paroxysmal positional vertigo. 62. Massoud EAS, Ireland DJ. Post-treatment instructions
Cochrane Database Syst Rev. 2004;2:CD003162. in the nonsurgical management of benign paroxysmal
43. Teixeira LJ, Machado JN. Maneuvers for the treatment of positional vertigo. J Otolaryngol. 1996;25:121.
benign positional paroxysmal vertigo: a systematic review. 63. Nuti D, Nati C, Passali D. Treatment of benign paroxys-
Braz J Otorhinolaryngol. 2006;72:130-139. mal positional vertigo: no need for postmaneuver restric-
44. Helminski JO, Zee DS, Janssen I, Hain TC. Effectiveness tions. Otol Head Neck Surg. 2000;122:440.
of particle repositioning maneuvers in the treatment of 64. Gordon CR, Gadoth N. Repeated vs single physical
benign paroxysmal positional vertigo: a systematic review. maneuver in benign paroxysmal positional vertigo. Acta
Phys Ther. May 2010;90(5):663. Neurol Scand. Sep 2004;110(3):166-169.
45. Kim JS, Oh SY, Lee SH, et al. Randomized clinical trial 65. Semont A, Freyss G, Vitte E. Curing the BPPV with a lib-
for geotropic horizontal canal benign paroxysmal posi- eratory maneuver. Adv Otorhinolaryngol. 1988;42:290.
tional vertigo. Neurology. 2010;79:700. 66. Harvey SA, Hain TC, Adamiec LC. Modified liberatory
46. Zucca G, Valli S, Valli P, Perin P, Mira E. Why do benign maneuver: effective treatment for benign paroxysmal posi-
paroxysmal positional vertigo episodes recover sponta- tional vertigo. Laryngoscope. 1994;104(10):1206.
neously? J Vestib Res. 1988;8(4):325. 67. Froehling DA, Bowen JM, Mohr DN, et al. The canalith
47. Lynn S, Pool A, Rose D, et al. Randomized trial of the repositioning procedure for the treatment of benign parox-
canalith repositioning procedure. Otol Head Neck Surg. ysmal positional vertigo: a randomized controlled trial.
1995;113:712. Mayo Clinic Proceedings. 2000;75(7):695.
48. Brandt T, Daroff RB. Physical therapy for benign parox- 68. Munoz JE, Miklea JT, Howard M, et al. Canalith reposi-
ysmal positional vertigo. Arch of Otolaryngol. 1980; tioning maneuver for benign paroxysmal positional
106:484. vertigo: Randomized controlled trial in family practice.
49. Imai T, Takeda N, Ito M, Inohara H. Natural course of Can Fam Physician. 2007;53:1048.
positional vertigo in patients with apogeotropic variant of 69. von Brevern M, Radtke A, Lezius F, et al. Epidemiology of
horizontal canal benign paroxysmal positional vertigo. benign paroxysmal positional vertigo: a population based
Auris Nasus Larynx. 2011;30:2. study. J Neurol Neurosurg Psychiatry. 2007;78(7):710.
50. Epley JM. The Canalith Repositioning Procedure. For treat- 70. Yimtae K, Srirompotong S, Srirompotong S. A Randomized
ment of benign paroxysmal positional vertigo. Otol Head Trial of the Canalith Repositioning Procedure. Laryngo-
Neck Surg. 1992;107:399. scope. 2003;113(5):828.
51. Epley JM. Positional vertigo related to semicircular 71. Ireland D. The Semont maneuver. In: Krecjova H, Jerabek J,
canalithiasis. Otol Head Neck Surg. 1996;122:281. eds. Proceedings of the XVIth Bárány Society Meeting,
52. Lynn S, Pool A, Rose D, et al. Randomized trial of the June 2-5, 1992. Prague, Czechoslovakia. 1994:347.
canalith repositioning procedure. Otol Head Neck Surg. 72. Hausler R, Pampurik JC. Die chrirurgische und die physio-
1995;113:712. therapeutische behandlung des benignen paroxysmalen
53. Parnes LS, Price-Jones RG. Particle repositioning maneu- lagerungsschwindels. Laryngol Rhinol Otol. 1989;68:342.
ver for benign paroxysmal positional vertigo. Ann Otol 73. Levrat E, van Melle G, Monnier P, Maire R. Efficacy of
Rhinol Laryngol. 1993;102:325. the Semont maneuver in benign paroxysmal positional
54. Radtke A, Heuhauser H, von Brevern M, et al. A modified vertigo. Arch Otol Head Neck Surg. 2003;129:629.
Epley’s procedure for self-treatment of benign paroxysmal 74. Mandala’ M, Santoro GP, Asprella Libonati C, et al.
positional vertigo. Neurology. 1999;53:1358. Double-blind randomized trial on short-term efficacy
55. Wolf JS, et al. Success of the modified Epley maneuver of the Semont maneuver for the treatment of posterior
in treating benign paroxysmal positional vertigo. Laryngo- canal benign paroxysmal positional vertigo. J Neurol.
scope. 1999;109:900. 2012;259:882.
3970_Ch20_323-358 25/06/14 1:50 PM Page 353
75. Chen Y, Zhuang J, Zhang L, et al. Short-term efficacy 93. Testa D, Castaldo G, De Santis C, et al. Treatment of hor-
of Semont maneuver for benign paroxysmal positional izontal canal benign paroxysmal positional vertigo: A
vertigo: a double-blind randomized trials. Otol Neurotol. new rehabilitation technique. Scientific World Journal.
2012;33:1127. 2012; Published online 2012 April 19.
76. Lopez-Escamez JA, Molina MI, Gamiz M. Anterior semi- 94. Amor-Dorado JC, Barreira-Fernández MP, Aran-Gonza-
circular canal benign paroxysmal positional vertigo and lez I, et al. Particle repositioning maneuver versus
positional downbeating nystagmus. Am J Otolaryngol. Brandt-Daroff exercise for treatment of unilateral idio-
May-Jun 2006;27(3):173. pathic BPPV of the posterior semicircular canal: a ran-
77. Jackson LE, Morgan B, Fletcher JC Jr, Krueger WW. An- domized prospective clinical trial with short- and long-term
terior canal benign paroxysmal positional vertigo: an un- outcome. Otol Neurotol. Oct 2012;33(8):1401.
derappreciated entity. Otol Neurotol. Feb 2007;28(2):218. 95. Humphriss RL, Baguley DM, Sparkes V, et al. Con-
78. Korres S, Riga M, Balatsouras D, Sandris V. Benign traindications to the Dix-Hallpike manoeuvre: a multidis-
paroxysmal positional vertigo of the anterior semicircular ciplinary review. Int J Audiology. 2003;42:166.
canal: atypical clinical findings and possible underlying 96. Sekine K, Imai T, Sato G, et al. Natural history of benign
mechanisms. Int J Audiol. May 2008;47(5):276. paroxysmal positional vertigo and efficacy of Epley and
79. Tevzadze N, Shakarishvili R. Effectiveness of canalith Lempert maneuvers. Otolaryngol Head Neck Surg. Oct
repositioning manoeuvers (CRM) in patients with benign 2006;135(4):529.
paroxysmal positional vertigo (BPPV). Georgian Med 97. Nuti D, Vannucchi P, Pagnini P. Lateral Canal BPPV:
News. Jul-Aug 2007;(148-149):40. Which is the affected side? Audiol Med. 2005;3(1):16.
80. Zapala DA. Down-beating nystagmus in anterior canal 98. Francesco R, Francesco D, Salvatore G, et al. Management
benign paroxysmal positional vertigo. J Am Acad Audiol. of benign paroxysmal positional vertigo of lateral semicir-
Mar 2008;19(3):257. cular canal by Gufoni’s manoeuvre. Am J Otol – Head
81. Honrubia V, Baloh RW, Harris MR, Jacobson KM. Parox- Neck Medicine and Surg, 2009;30:106.
ysmal Positional Vertigo Syndrome. Am J Otol. 1999; 99. Casani AP, Nacci A, Dallan I, et al. Horizontal semicircular
20(4):465. canal benign paroxysmal positional vertigo: effectiveness
82. Rahko T. The test and treatment of benign paroxysmal of two different methods of treatment. Audiol Neurotol.
positional vertigo and an addition to the management of 2011;16:175.
vertigo due to the superior vestibular canal (BPPV-SC). 100. Chiou W-Y, Lee H-L, Tsai S-C, et al. A Single therapy
Clin Otolaryngol. 2002;27:392. for all subtypes of horizontal canal positional vertigo.
83. Kim YK, Shin JE, Chung JW. The effect of canalith repo- Laryngoscope. 2005;115:1432.
sitioning for anterior semicircular canal canalithiasis. ORL 101. Boleas-Aquirre MS, Perez N, Batuecas-Caletrio A. Bed-
J Otorhinolaryngol Relat Spec. 2005;67(1):56. side therapeutic experiences with horizontal canal benign
84. Korres S, Riga M, Balatsouras D, Sandris V. Benign paroxysmal positional vertigo (cupulolithiasis). Acta
paroxysmal positional vertigo of the anterior semicircular Otolaryngol. 2009;129:1217.
canal: atypical clinical findings and possible underlying 102. Escher A, Ruffieux C, Maire R. Efficacy of the barbecue
mechanisms. Int J Audiol. May 2008;47(5):276. manoeuvre in benign paroxysmal vertigo of the horizon-
85. Crevits L. Treatment of anterior canal benign paroxysmal tal canal. Eur Arch Otorhinolaryngol. Oct 2007;264
ositional vertigo by a prolonged forced position procedure. (10):1239.
J Neurol Neurosurg Psychiatry. 2004;75:779. 103. Tusa RJ, Herdman SJ. Canalith repositioning for benign
86. Lempert T, Tiel-Wilck K. A positional maneuver for treat- paroxysmal positional vertigo. Publication 319-American
ment of horizontal-canal benign positional vertigo. Laryn- Academy of Neurology, pg 19, 1996.
goscope. 1996;106:476. 104. Herdman SJ, Tusa RJ. Diagnosis of benign paroxysmal
87. Lempert T, Wolsley C, Davies R, et al. Three hundred positional vertigo. ENG Report. Illinois: ICS Medical;
sixty-degree rotation of the posterior semicircular canal 1998.
for treatment of benign positional vertigo: a placebo- 105. Di Girolamo S, Paludetti G, Briglia G, et al. Postural
controlled trial. Neurology. 1997;49:729. control in benign paroxysmal positional vertigo before
88. Appiani GC, Catania G, Gagliardi M. A liberatory maneu- and after recovery. Acta Otolaryngol (Stockh).
ver for the treatment of horizontal canal paroxysmal posi- 1998;118:289.
tion vertigo. Otol Neurotol. 2001;22(1):66. 106. Blatt PJ, Georgakakis GA, Herdman SJ, et al. Effect of
89. Vannucchi P, Giannoni B, Pagnini P. Treatment of horizontal canalith repositioning maneuver on resolving postural in-
semicircular canal benign paroxysmal positional vertigo. stability in patients with BPPV. Am J Otol. 2000;21:356.
J Vestib Res. 1997;7:1. 107. Black FO, Nashner LM. Postural disturbance in patients
90. Casani AP, Vannucci G, Fattori B, Berrettini S. The treat- with benign paroxysmal positional nystagmus. Ann Oto
ment of horizontal canal positional vertigo: our experience Rhino Laryngol. 1984;93:595.
in 66 cases. Laryngoscope. 2002;112:172. 108. Norré ME, Forrez G, Beckers A. Benign paroxysmal
91. Appiani GC, Catania G, Gagliardi M, Cuiuli G. Reposi- positional vertigo. Clinical observations by vestibular
tioning maneuver for the treatment of the apogeotropic habituation training and by posturography. J Laryngol
variant of horizontal canal benign paroxysmal positional Otol. 1987;101:443.
vertigo. Otol Neurotol. Mar 2005;26(2):257. 109. Voorhees RL. The role of dynamic posturography in
92. Kim JS, Oh SY, Lee SH, et al. Randomized clinical trial neurotologic diagnosis. Laryngoscope. 1989;99:995.
for geotropic horizontal canal benign paroxysmal posi- 110. Katsarkas A, Kearney R. Postural disturbances in
tional vertigo. Neurology. 2010;79(7):700. paroxysmal positional vertigo. Am J Otol. 1990;11:444.
3970_Ch20_323-358 25/06/14 1:50 PM Page 354
354 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
111. Giacomini P, Alessandrini M, Magrini A. Long-term 116. Prokopakis E, Vlastos IM, Tsagournisakis M, et al.
postural abnormalities in benign paroxysmal positional Canalith Repositioning Procedures among 965 Patients
vertigo. ORL. 2002;64:237. with Benign Paroxysmal Positional Vertigo. Audiol
112. Welling DB, Barnes DE. Particle repositioning maneuver Neurootol. Nov 6, 2012;18(2):83.
for benign paroxysmal positional vertigo. Laryngoscope. 117. Kansu L, Avci S, Yilmaz I, Ozluoglu LN. Long-term
1994;104:946. follow-up of patients with posterior canal benign parox-
113. Dlugaiczyk J, Siebert S, Hecker DJ, et al. Involvement ysmal positional vertigo. Acta Otolaryngol. Sep 2010;
of the anterior semicircular canal in posttraumatic benign 130(9):1009.
paroxysmal positioning vertigo. Otol Neurotol. Oct 2011; 118. Ahn SK, Jeon SY, Kim JP, et al. Clinical characteristics
32(8):1285. and treatment of benign paroxysmal positional vertigo
114. Beynon GJ. A review of management of benign paroxys- after traumatic brain injury. J Trauma. Feb 2011;
mal positional vertigo by exercise therapy and by reposi- 70(2):442.
tioning manoeuvres. Br J Audiol. 1997;31:11. 119. Suarez H, Alonso R, Arocena M, et al. Clinical character-
115. Mandala M, Santoro GP, Awrey J, Nuti D. Vestibular istics of positional vertigo after mild head trauma. Acta
neuritis: recurrence and incidence of secondary benign Otolaryngol. Apr 2011;131(4):377.
paroxysmal positional vertigo. Acta Otolaryngol. 2010;
130(5):565.
3970_Ch20_323-358 25/06/14 1:50 PM Page 355
APPENDIX 20-A
Differential Diagnosis: BPPV
versus Central Postional
Nystagmus and Vertigo
Richard A. Clendaniel, PT, PhD
Although benign paroxysmal positioning vertigo (BPPV) including Chiari malformation, multiple sclerosis, oli vo-
is a common finding that is relatively easy to diagnose and pontocerebellar atrophy, and brainstem infarction.3 These
treat, there are causes of positional n ystagmus and posi- patients had other oculomotor signs such as impaired
tional vertigo that are a result of either abnormalities smooth pursuit and impaired VOR cancellation. The actual
within the central nerv ous system or other peripheral pathophysiology causing the downbeating nystagmus is
vestibular conditions. These conditions will not respond not well understood at this point, but it is thought that the
to the conservative measures described for the treatment downbeating nystagmus results from an imbalance be-
of BPPV. The goal of this appendix is to help the clinician tween the anterior and posterior semicircular canal path-
identify the signs and symptoms of positional nystagmus ways. Recall that the semicircular canal inputs are
and positional vertigo that are not consistent with BPPV separated at the level of the vestibular nuclei into vertical
and are suggestive of other disorders. (pitch), horizontal (yaw), and roll pathways. A lesion that
causes either an increase in the central anterior semicircu-
lar canal pathways or a decrease in the central posterior
Central Positional Nystagmus semicircular canal pathways would lead to downbeating
Two types of central positional nystagmus have been iden- nystagmus.
tified: central positional nystagmus without vertigo (CPN) The upbeating spontaneous n ystagmus and CPN
and central positional n ystagmus with vertigo (CPV).1,2 have been associated with central disorders such as tumor,
Central positional nystagmus without vertigo is character- stroke, and multiple sclerosis affecting brachium conjunc-
ized by nystagmus that persists as long as the head is held tivum or the v entral tegmental tract.4 Many of these pa-
in the provoking position.1 The nystagmus is typically in tients also had findings of abnormal smooth pursuit. The
one direction (vertical, horizontal, or torsional), unlike the presumed pathophysiology for the upbeating n ystagmus
mixed vertical torsional nystagmus seen in posterior and is thought to be the opposite of that for the do wnbeating
anterior semicircular canal BPPV. Central positional nys- nystagmus. The upbeating n ystagmus is caused by a
tagmus may be seen in elderly patients when the y are in higher level of neural activity in the central posterior semi-
supine. The elicited nystagmus is typically vertical. In the circular canal pathw ays relative to the central anterior
absence of other findings on the examination, the CPN is semicircular canal pathways.
thought to be benign. In other indi viduals, the CPN may Given the lack of symptoms of vertigo with the posi-
be seen in conjunction with either upbeating or downbeat- tional tests, the unidirectionality of the positional nystag-
ing spontaneous nystagmus while the patient is seated. mus, and the other oculomotor f indings, it should not be
The CPN in these cases is typically greater than the spon- difficult for the clinician to dif ferentiate between CPN
taneous nystagmus observed in sitting. and BPPV.
The downbeating spontaneous nystagmus and CPN Central positional nystagmus with vertigo can pre
have been associated with a v ariety of central disorders sent with persistent, positional-induced n ystagmus and
355
3970_Ch20_323-358 25/06/14 1:50 PM Page 356
356 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
vertigo. In this type of CPV, the nystagmus is downbeating vertical (downbeating or upbeating), pure torsional, pure
without a torsional component, and the n ystagmus and horizontal (either apogeotropic, or geotropic), and mixed
vertigo persist as long as the head is in the provoking po- vertical and horizontal patterns of n ystagmus.2,8,13-15 In
sition. The nystagmus and vertigo do not fatigue, nor do animals with experimental lesions to the cerebellar nodu-
they habituate with repeated testing. This pattern of CPV lus, downbeat, downbeat with torsion, and horizontal pat-
has been attributed to cerebellar tumors or to hemorrhage terns of n ystagmus have been observ ed.11,12 Although
dorsolateral to the fourth ventricle.5,6 most of these patterns of nystagmus do not fit with BPPV,
Unlike CPN, CPV may present in a manner remark- downbeating torsional nystagmus could be caused by an-
ably similar to BPPV. Central positioning nystagmus with terior semicircular canal BPPV, and horizontal nystagmus
vertigo is often characterized by brief episodes of posi- could be caused by horizontal semicircular canal BPPV ,
tioning vertigo and n ystagmus, which has been called making accurate diagnosis difficult. In addition, there are
pseudo-BPPN.2,7 Based on clinical findings and experi- instances when the n ystagmus seen in indi viduals with
mental animal studies, there is a lar ge degree of overlap BPPV may not appear to f it the mixed vertical and tor-
in the signs (latency, duration, and fatigability) as well as sional nystagmus seen in posterior and anterior semicir-
the symptoms associated with BPPV and CPV. For exam- cular canal BPPV. For example, the horizontal position of
ple, the latency to the onset of nystagmus in cases of CPV the eye in the orbit will accentuate either the v ertical or
has been reported to be between 0 and 5 seconds, and in torsional component of the nystagmus, which may make
the case of experimental lesions to the cerebellar nodulus, it difficult to determine if the nystagmus is mixed vertical
up to 50 seconds.8-12 Likewise, the duration of the elicited and torsional, pure vertical, or pure torsional. Also, lid clo-
nystagmus and symptoms is typically relati vely brief sure or rapid blinking may mak e it difficult to assess the
(5–60 sec) and mimics that seen in BPPV canalithiasis.8,13 pattern of nystagmus. Either scenario would increase the
Unlike the duration of BPPV canalithiasis, the duration of difficulty in making an accurate diagnosis.
the nystagmus in the animals with e xperimental lesions Another differentiating feature between CPV and
to the nodulus could persist up to 3 minutes, similar to BPPV is the presence of other neurological f indings and
that seen in BPPV cupulolithiasis.12 Fatigability of the re- symptoms, which w ould not be e xpected in cases of
sponse to repeated testing within a short time frame, al- BPPV. Associated symptoms, such as sudden hearing loss,
though not always tested in the clinic, is another hallmark tinnitus, fainting sensations, progressive imbalance, and
of BPPV and may also be seen in indi viduals with vomiting have been reported in individuals with paroxys-
CPV.8,11,14 However, fatigability of the response is not seen mal, positioning vertigo of central origin (CPV). 16,17 An
in all patients with CPV, just as it is not seen in all patients abnormal oculomotor exam is often seen in indi viduals
with BPPV.2,8 with CPV.7 The presence of other neurological signs and
Although there are similarities in the latenc y, dura- symptoms, however, is not a requirement for CPV. There
tion, and fatigability of BPPV and CPV, there do appear are numerous reports of indi viduals with CPV and no
to be differences in the patterns of the elicited nystagmus. other signs or symptoms.8,10,13,15 The similarities and dif-
The pattern of n ystagmus in CPV can tak e a variety of ferences between BPPV, CPV, and CPN are summarized
forms. Findings from clinical studies ha ve reported pure in Table 20-A.
Duration 5–60 seconds (longer in horizontal 5–60 seconds Persistent as long as the head is
canal and in cupulolithiasis) in the provoking position
Direction of In the plane of the stimulated Pure vertical, pure tor- Typically pure downbeat, may
nystagmus canal. Most commonly mixed up- sional, or horizontal be pure upbeat or horizontal
beating and torsion, may be down-
beating and torsion, or horizontal
3970_Ch20_323-358 25/06/14 1:50 PM Page 357
Nausea and Unusual with a single test; may More frequently seen No
vomiting develop with repeat testing with a single test
Various causes of CPV have been reported in the lit- changes such as Valsalva maneuvers, or the Dix-Hallpike
erature, including cerebellopontine angle tumors, lesions Test, where the head is hanging below the horizontal plane.
affecting the cerebellar vermis or the fourth ventricle, and These conditions are typically accompanied by hearing
an infarction of the cerebellar nodulus. 15-17 A more com- loss. The production of nystagmus and symptoms are not
mon form of CPV is migrainous v ertigo and positional dependent on the position of the head in space and can
nystagmus. Spontaneous, positional, or a combination often be reproduced in an upright (seated) position with the
of spontaneous and positional n ystagmus can be seen Valsalva maneuver.
during an acute migraine with associated symptoms of Lastly, positional nystagmus may be seen following
dizziness.18 In these cases the nystagmus can be vertical, a unilateral vestibular loss. The nystagmus is horizontal
horizontal, or torsional and may change with dif ferent (geotropic or apogeotropic), and the pattern of nystagmus
positional tests. In patients with a history of migrainous will remain constant (geotropic or apogeotropic) in each
vertigo that were assessed when they were asymptomatic, Dix-Hallpike or Roll Test. Thus the n ystagmus may
12% to 28% (depending on the time of assessment) appear similar to horizontal semicircular canal BPPV
demonstrated significant positional nystagmus.19 (canalithiasis or cupulolithiasis). Whereas individuals
with horizontal semicircular canal BPPV are very symp-
Other Causes of Positional tomatic, individuals with positional nystagmus as a result
of unilateral vestibular loss are either asymptomatic or
Nystagmus/Vertigo have mild symptoms.
Vertebrobasilar insufficiency (VBI) has been reported to
produce episodic bouts of v ertigo and n ystagmus.20,21
These findings have been seen in both positional testing
Summary
as well as in sitting with cervical rotation. Symptoms There are causes of positional vertigo and nystagmus not
associated with VBI would be dependent of the position caused by BPPV. The challenge to the clinician is to iden-
of the head on the trunk (neck position), rather than the tify the cause of the positional vertigo, such that appropri-
position of the head in space (positional testing). Conse- ate treatment can be initiated. There are differences in the
quently, nystagmus and vertigo seen in the Dix-Hallpik e clinical presentation of the v arious causes of positional
Test should be reproducible in sitting with cervical exten- vertigo, but at times it may be dif ficult to determine
sion and rotation if the cause of the signs and symptoms whether the positional vertigo is a result of BPPV or an-
were a result of VBI. Vertiginous symptoms are common other cause, such as CPV . The latency, duration, and
in cases of VBI, but isolated episodes of vertigo in VBI is symptoms may be very similar in cases of BPPV and CPV.
controversial, with conflicting reports as to the incidence There are generally differences in the pattern of elicited
of this finding.22,23 nystagmus in BPPV and CPV. The one consistent differ-
Perilymphatic fistula and superior canal dehiscence ence between BPPV and CPV is that BPPV will respond
can make the membranous labyrinth susceptible to pressure to maneuvers such as the canalith repositioning maneuver
3970_Ch20_323-358 25/06/14 1:50 PM Page 358
358 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
or Semont maneuver, but CPV will not respond to these 12. Fernandez C, Alzate R, Lindsay JR. Experimental obser-
treatments. If the presumed BPPV is not responding to the vations on postural nystagmus. II. Lesions of the nodulus.
The Annals of otology, rhinology, and laryngology.
therapeutic maneuvers, the clinician should be suspicious
1960;69:94-114.
of possible CPV. 13. Barber HO. Positional nystagmus. Otolaryngol Head Neck
Surg. 1984;92(6):649-655.
Appendix References 14. Kattah JC, Kolsky MP, Luessenhop AJ. Positional vertigo
and the cerebellar vermis. Neurology. 1984;34(4):527-529.
1. Harrison MS, Ozsahinoglu C. Positional vertigo: aetiology 15. Kim HA, Yi HA, Lee H. Apogeotropic central positional
and clinical significance. Brain. 1972;95(2):369-372. nystagmus as a sole sign of nodular infarction. Neurologi-
2. Sakata E, Ohtsu K, Shimura H, Sakai S. Positional nystag- cal sciences:official journal of the Italian Neurological
mus of benign paroxysmal type (BPPN) due to cerebellar Society and of the Italian Society of Clinical Neurophysi-
vermis lesions. Pseudo-BPPN. Auris, nasus, larynx. ology. 2012;33(5):1189-1191.
1987;14(1):17-21. 16. Dunniway HM, Welling DB. Intracranial tumors mimick-
3. Baloh RW, Spooner JW. Downbeat nystagmus: a type ing benign paroxysmal positional vertigo. Otolaryngol
of central vestibular nystagmus. Neurology. 1981;31(3): Head Neck Surg. 1998;118(4):429-436.
304-310. 17. Shoman N, Longridge N. Cerebellar vermis lesions and
4. Fisher A, Gresty M, Chambers B, Rudge P. Primary tumours of the fourth ventricle in patients with positional
position upbeating nystagmus. A variety of central posi- and positioning vertigo and nystagmus. J Laryngol Otol.
tional nystagmus. Brain. 1983;106(Pt 4):949-964. 2007;121(2):166-169.
5. Harrison MS, Ozsahinoglu C. Positional vertigo. Arch 18. von Brevern M, Zeise D, Neuhauser H, et al. Acute
Otolaryngol. 1975;101(11):675-678. migrainous vertigo: clinical and oculographic findings.
6. Brandt T. Positional and positioning vertigo and nystagmus. Brain. 2005;128(Pt 2):365-374.
J Neurol Sci. 1990;95(1):3-28. 19. Radtke A, von Brevern M, Neuhauser H, et al. Vestibular
7. Buttner U, Helmchen C, Brandt T. Diagnostic criteria migraine: long-term follow-up of clinical symptoms and
for central versus peripheral positioning nystagmus and vestibulo-cochlear findings. Neurology. 2012;79(15):
vertigo: a review. Acta Otolaryngol. 1999;119(1):1-5. 1607-1614.
8. Gregorius FK, Crandall PH, Baloh RW. Positional vertigo 20. Strupp M, Planck JH, Arbusow V, et al. Rotational vertebral
with cerebellar astrocytoma. Surgical neurology. artery occlusion syndrome with vertigo due to “labyrinthine
1976;6(5):283-286. excitation”. Neurology. 2000;54(6):1376-1379.
9. Jacobson GP, Butcher JA, Newman CW, Monsell EM. 21. Grad A, Baloh RW. Vertigo of vascular origin. Clinical and
When paroxysmal positioning vertigo isn’t benign. electronystagmographic features in 84 cases. Arch Neurol.
J Am Acad Audiol. 1995;6(4):346-349. 1989;46(3):281-284.
10. Watson P, Barber HO, Deck J, Terbrugge K. Positional 22. Gomez CR, Cruz-Flores S, Malkoff MD, et al. Isolated
vertigo and nystagmus of central origin. The Canadian vertigo as a manifestation of vertebrobasilar ischemia.
journal of neurological sciences. Le journal canadien des Neurology. 1996;47(1):94-97.
sciences neurologiques. 1981;8(2):133-137. 23. Wityk RJ, Chang HM, Rosengart A, et al. Proximal
11. Allen G, Fernandez C. Experimental observations in pos- extracranial vertebral artery disease in the New England
tural nystagmus. I. Extensive lesions in posterior vermis Medical Center Posterior Circulation Registry. Arch
of the cerebellum. Acta Otolaryngol. 1960;51:2-14. Neurol. 1998;55(4):470-478.
3970_Ch21_359-393 25/06/14 6:04 PM Page 359
CHAPTER 21
Physical Therapy
Assessment
of Vestibular
Hypofunction
Susan L. Whitney, DPT, PhD, NCS, ATC, FAPTA ■
Susan J. Herdman, PT, PhD, FAPTA
Patients with peripheral vestibular hypofunction dif fer that includes both positive experiences and negative
with respect to the onset and clinical course of their dis- consequences of disease.12 This scheme consists of three
ability and to the final level of recovery , depending domains that can be used to describe the effects of differ-
on the type and extent of vestibular deficit. Despite ent disorders or diseases on a person’s health, with a num-
these differences, such patients have many of the same ber of environmental and personal factors that affect each
symptoms—dizziness, lightheadedness, vertigo, nystag- of those domains (Box 21-1).
mus, blurred vision, postural instability , fear of move- The ICF model differs from other models of disable-
ment, gait disturbances, and occasional falling. 1 In ment in that it provides a more comprehensive depiction
addition, these patients may experience anxiety, depres- of the health of an individual. The model shifts the em-
sion, and fear related to their disability.2-6 In fact, people phasis away from impairment and disability to a more
with vestibular dysfunction report that they are signifi- balanced perspective that includes “health.” Table 21-1
cantly impaired by their disability .7-9 As a result of one provides a description of how one can choose a self-
or more of these symptoms, patients with peripheral report tool for use with persons with vestibular dysfunc-
vestibular hypofunction often cope with their disability tion based on which areas of the ICF are included in the
by avoiding certain movements and decreasing their ac- measure (Fig. 21.1). Use of the ICF enables comparison
tivity level.10 This habit, if not treated, will lead to the un- of similar constructs across cultures to better describe re-
fortunate results of physical deconditioning and an habilitation outcomes.
alteration of the patient’s lifestyle.10,11
The purpose of this chapter is to provide an overview Normal Structure and Function
of patient problems and the key components of the clinical
examination as well as the more comprehensive exami-
versus Impairment
nation. We use the International Classification of Func- Patients with vestibular hypofunction may express a mul-
tioning, Disability and Health (ICF) scheme for the titude of symptoms. These symptoms emerge from func-
organization of this chapter .12 The ICF was developed tional deficits in vestibulo-ocular and vestibulospinal
by the World Health Organization specifically to provide systems (Box 21-2) and from the results of sensory mis-
a framework for the “description of health-related states” match and physical deconditioning.13
359
3970_Ch21_359-393 25/06/14 6:04 PM Page 360
360 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Box 21-1
HEALTH CONDITION
Normal Function and Structure versus Activities versus Participation versus
Impairment (body level) Limitations (individual level) Restriction (societal level)
Contextual Factors
Environmental Factors: Personal Factors:
e.g. Natural environment e.g. Gender, age
Support and relationships Comorbidities
Attitude of family Social background
Attitude of society Education and profession
Services, systems, policies Past experience
Products and technology Coping and character style
ICF Domain
Normal/Abnormal Activity/ Participation/
Tool Structure and Function Limitation Restriction
Head-thrust test X
Dix-Hallpike test X
Strength X
Range of motion X
Endurance X
Gait speed X
ICF Domain
Normal/Abnormal Activity/ Participation/
Tool Structure and Function Limitation Restriction
Dizziness Handicap Inventory X
Disability Score X
Vestibulo-ocular Function function, of course, the brain interprets this abnormal sig-
and Dysfunction nal as continuous movement of the head. The patient then
experiences a spinning sensation even when he or she is
The vestibulo-ocular reflex (VOR) is the primary mecha- not moving at all. Within a week, this asymmetry resolves
nism for gaze stability during head movement. During and the spontaneous spinning sensation ceases. However,
movements of the head, the VOR stabilizes gaze (eye po- in patients with chronic vestibular dysfunction, the loss of
sition in space) by producing an eye movement of equal a vestibular response to head movement becomes a per-
velocity and opposite direction to the head movement.The sistent problem with actual movement of the head.
ratio of eye velocity to head velocity is referred to as the According to Norré, 17 the disturbed vestibular
gain of the VOR. The ideal gain in a normal subject would function produces a sensory input different from the one
equal 1. VOR gain has been shown to be reduced to 25% expected under normal conditions. This abnormal
in human beings immediately after unilateral labyrinthine vestibular signal is in conflict with normal signals pro-
lesions for head movements toward the affected side.14,15 vided by the visual and somatosensory systems, and the
During the acute stage, VOR gain is also reduced to 50% resultant “sensory conflict” is thought to produce the
for head movements toward the unaffected side. symptoms associated with motion misperception. 17
Other eye movements, such as saccades and pursuit, Clinically, patients complain of lightheadedness or
are not affected by vestibular loss. Saccadic eye move- dizziness associated with particular head or body move-
ments are rapid movements that allow refoveation of ments. Norré17 has referred to this condition as “pro-
stationary targets. Pursuit eye movements enable the in- voked vertigo,” which is attributable to the asymmetry
dividual to visually follow a moving object across the vi- in the dynamic vestibular responses following a unilat-
sual field (smooth pursuit) without making compensatory eral vestibular lesion.
head movements. Normally, the vestibulo-ocular, pursuit,
and saccade systems work cooperatively to stabilize gaze
Postural Instability
during head movements.16 If impaired smooth pursuit or
hypermetric saccades are identified during the examina- Independent and safe ambulation depends on the ability
tion, the clinician should strongly consider that the person to successfully perceive the relevant features of one’s en-
has central dysfunction. vironment while maintaining appropriate orientation of
the body with respect to the support surface and gravity.18
Information necessary for postural control is derived from
Perception of Head Movement an integration of sensory inputs from the visual, so-
and Position matosensory, and vestibular systems.19
Normally, signals from the labyrinth provide accurate in- Impairment in the function of vestibulospinal reflex
formation concerning head movement and position. These (VSR) itself is believed to contribute to postural distur -
vestibular signals are synchronized with visual and bances in patients with peripheral vestibular disorders.
somatosensory inputs, and the nervous system is able to Lacour and associates20 showed that unilateral vestibular
appropriately interpret the combination of signals. When- neurotomy induces asymmetrical excitability in ipsilateral
ever there is an acute or sudden asymmetry of vestibular and contralateral spinal reflexes in baboons. Similarly ,
3970_Ch21_359-393 25/06/14 6:04 PM Page 362
362 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Box 21-2
364 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
psychiatric comorbidities, a history of migraines, and pre- while walking. The scale is anchored at one end as “no
existing or long-term visual dysfunction (e.g., strabismus) imbalance at all” and at the other end as “the worst it can
are examples of disorders that affect the ability of the per- be.” Another scale can be used for the intensity of head
son to compensate for the vestibular loss. Obtaining a movement-induced dizziness. In that assessment, the pa-
complete medication history from the patient also is vital tient rates the intensity of his/her dizziness while sitting
because many medications can produce or enhance dizzi- quietly and then again after 1 minute of horizontal head
ness (see Chapters 10 and 14). Some people may be taking movement at 1 Hz (see Appendix 21-A). These visual ana-
certain medications that act to reduce the patient’s symp- logue scales have only moderate reliability .42 It is very
toms by depressing the vestibular system. These medica- helpful to have patients rate their symptoms, yet not all pa-
tions may also delay vestibular adaptation and therefore tients are able to provide a number . Those who are con-
may prolong the recovery period. The therapist should fused have great dif ficulty rating their symptoms, and
consult with the physician to determine the possibility of family members often attempt to “help” the patient, which
reducing the dose of such a medication or even eliminat- is not useful. When it is impossible for the patient to pro-
ing it completely. Other people need medication to pro- vide a numerical rating, a “little, medium, or lot of dizzi-
ceed with rehabilitation, especially those with anxiety and ness” rating scale can help guide intervention. Finally, the
persons with central vestibular dysfunction. Persons with patient can be asked the percentage of time in the last week
central vestibular disorders who have constant dizziness that his/her dizziness has interfered with daily activities.
complaints may benefit from a central vestibular suppres- Questions related to the patient’s perceived disabil-
sant so that their symptoms, especially severe nausea, are ity and psychosocial status should also be included in
better under control.38,39 They may not be able to tolerate the initial assessment. Many different tools can be used
rehabilitation efforts without such medication to control to measure perceived disability, and most of them in-
their symptoms. clude items that assess function at the activity/limitation
and participation/restriction levels. Using the Medical
Subjective History Outcomes Study 36-Item Short-Form Health Survey
The subjective history of the patient’s condition is critical (SF-36) is one method that could be used to determine
in the evaluation of the patient with a peripheral vestibular whether the patient is doing more in the home or com-
problem. Questions that go beyond those usually asked by munity after therapy.43-49 Other therapists may use the
a physical therapist should be considered (see Box 21-2). Sickness Impact Profile or other health status mea -
The use of a questionnaire that the patient can complete sures.50 These tools help the therapist determine whether
before the initial visit is also helpful and saves time (see the patient is feeling better and is more active. Use
Appendix 21-A). A complete description of the patient’ s of health status inventories is an excellent way to
symptoms should be documented, so that functional determine whether the patient has actually improved. 51
progress can be later assessed. Think about documenting Shepard and colleagues 52 have suggested the use of a
which symptom(s) the patient is experiencing, the duration disability scale to objectively document a patient’s per-
of the symptoms(s), and the circumstance(s) in which ceived level of disability (T able 21-2). The Disability
the symptoms occur (e.g., spontaneous versus position- Scale is quick and easy to use and a change in the score
specific). Knowing what positions, movements, or situa- of one point is significant. Test-retest reliability is high
tions aggravate the patient’ s symptoms is important in (ICC 1.0).42 This 6-point Disability Scale has descrip-
treatment planning. In addition, the patient should be tors that range from having no disability (negligible
asked questions about the type, frequency , duration, and symptoms) to having long-term disability . Long-term
intensity of symptoms and whether symptoms are of a disability is defined as the inability to work for more
fluctuating nature. Knowing the type of onset and fre- than 1 year.52 The Disability Scale can be incorporated
quency of the symptoms is very helpful in determining the into the initial and dischar ge physical therapy evalua-
physical therapy diagnosis and prognosis. tions to document treatment outcome. As an alternative,
Intensity of symptoms like vertigo and disequilib- the Post-Therapy Symptoms Scale, also developed by
rium can be measured by means of a visual or verbal ana- Shepard and colleagues, 52 can be used at dischar ge to
log scale similar to that used in the assessment of pain.40-42 determine whether the patient perceives a change in dis-
Some therapists use a 0 to 10 scale, and others use a 0 to ability (Table 21-3). The Disability Scale is also useful
100 scale.41,43 One commonly used technique is to ask the in predicting treatment outcome; Shepard and col-
patient to rate symptom intensity using a visual analogue leagues52 found that patients who rated their disability
scale. For instance, disequilibrium (the patient’ s sense as a 4 or 5 were less likely to show significant improve-
of being off-balance) is rated while sitting quietly and ment with rehabilitation.
3970_Ch21_359-393 25/06/14 6:05 PM Page 365
366 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
important issues include: (1) whether the patient has been may have a limited ability to interact with their environ-
injured during a fall, (2) the conditions under which the ment and, over time, tend to adopt a more sedentary
fall(s) occur, (3) how the patient has modified his or her lifestyle. Occasionally, patients develop phobias associ-
lifestyle after a fall or fall-related injury, and (4) whether ated with their symptoms, including fears of elevators and
the patient sought medical intervention as a result of the of heights. Whitney and colleagues 77 have reported that
fall. Unexplained falls are always of concern.The treating 50% of the people referred to the investigators’ tertiary
physician should be notified immediately if the person is care physical therapy clinic stated that they were always
falling with no known provocative cause. Fortunately, cer- wary of heights.
tain exercise programs can reduce fall risk, even in the
frail older adult. 66,67 Others68-71 have demonstrated that Patient Goals
fall risk is reduced after vestibular rehabilitation in persons At the beginning of the assessment, the patient should be
with unilateral hypofunction. asked about expectations of physical therapy and func-
tional goals.78 After the assessment is complete, the ther-
Functional History apist and the patient should discuss whether these goals
To obtain a complete picture of functional status, the ther- are realistic and attainable. The patient’s goals may have
apist should question the patient about previous and cur - to be mutually modified by the therapist and the patient.
rent activity levels (Box 21-3). A history of the patient’s The final level of recovery for most patients with unilat -
activity level is an important component of the assess- eral vestibular hypofunction (UVH), without other com -
ment, which often characterizes the extent of the patient’s plications, should be a return to full activities. Conditions
disability. The Vestibular Activities of Daily Living Scale that may make recovery more dif ficult, and therefore
is an excellent example of a tool that will assist the thera- need to be recognized in the setting of goals, include the
pist in identifying limitations in activity and participation patient’s premorbid physical condition and personality
(Box 21-3).10,72 profile.6 Occasionally, patients with significant vestibular
Some patients avoid leaving their homes because ex- dysfunction make remarkable functional gains but still
posure to highly textured visual stimulation, such as light experience significant symptoms at the conclusion of
flickering through trees or walking in stores, increases rehabilitation.
their disequilibrium.73-76 This common experience is re-
ferred to as the “shopping aisle syndrome.”These patients
Clinical Examination
The clinical examination of a patient with vertigo and dis-
Box 21-3 equilibrium is usually comprehensive (Box 21-4) and
therefore is time-consuming. Discretion should be used as
CURRENT FUNCTIONAL STATUS to which portions of the examination must be performed
on each patient. The full examination is described here
Are you independent in self-care activities? but, where possible, conditions are described for which
Can you drive: different portions of the examination would be unneces-
• In the daytime? sary. Many of the elements of the therapist’ s assessment
• In the nighttime? are also discussed in Chapter 10. Key elements of the clin-
Are you working? If yes, occupation: ical examination are listed in Box 21-5.
________________________
Are you on medical disability? Oculomotor and Vestibulo-ocular Testing
Can you perform all your normal parenting
The oculomotor examination is one part of the overall as-
activities?
sessment of the “dizzy” patient that may have been per -
Do you have difficulty: formed by a neurologist or otolaryngologist before
• Watching TV? referral for physical therapy. It is therefore not always in-
• Reading? cluded in the physical therapy assessment. If the patient
• Being in stores or malls? is self-referred, it is an essential aspect of the physical
• Being in traffic? examination.
Do you have difficulty walking up and down First, the patient is observed for the presence of
ramps, stairs, walking on grass? spontaneous nystagmus in room light. In patients with
unilateral peripheral vestibular hypofunction, spontaneous
3970_Ch21_359-393 25/06/14 6:05 PM Page 367
Box 21-4
nystagmus will be observable in room light during the same regardless of eye-in-orbit position) is consistent
acute stage after onset of the lesion and is the result of the with acute unilateral vestibular hypofunction. Direction-
imbalance in the tonic or resting firing rate of the vestibu- changing gaze-holding nystagmus is consistent with a
lar neurons. Within a few days of onset, the patient should central lesion, usually in the posterior fossa.
suppress the nystagmus with visual fixation. Patients in Patients can also be tested for ocular alignment, par-
this acute stage often complain of having difficulty read- ticularly for skew deviations that can occur during the
ing and watching television. In later stages, with infrared acute stage of a unilateral vestibular loss (UVL). Skew de-
goggles in place, the therapist may still be able to visualize viations, in which the eye opposite the side of the lesion
the spontaneous nystagmus that is absent in room light. is elevated, occur because of the loss of the tonic otolith
Next, the patient is examined for gaze-holding nys- input from one side. Normally , the tonic input holds the
tagmus, the inability to keep the eyes steady when looking eyes level within the orbit; when there is a unilateral
about 15 to 20 degrees eccentrically. Direction-fixed gaze- vestibular loss, the eye on the side of the lesion drops in
holding nystagmus (the direction of the nystagmus is the the orbit and the patient complains of vertical diplopia.As
3970_Ch21_359-393 25/06/14 6:05 PM Page 368
368 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Box 21-5
with spontaneous nystagmus from UVL, skew deviations disconjugant smooth pursuit, which can confound the re-
from UVL should resolve within 3 to 7 days after onset. sults of the testing.
Smooth pursuit is tested by asking the patient to Saccadic eye movements are tested by simply asking
track, with the eyes, an object moving in the central the patient to look back and forth between two horizontal
20 degrees of the visual field while the head is stationary. or two vertical tar gets. In healthy individuals, the tar get
Typically, this test assesses central pathways involved in can be reached with a single eye movement or with one
smooth pursuit and the motor function of cranial nerves small corrective saccade. It is important to have discrete
III, IV, and VI. Smooth pursuit is abnormal if, during targets to observe so that the clinician can definitively
tracking, the eye movements are disrupted by saccades. determine if they consistently overshoot the target position
One important thing to remember is that abnormal (see Chapters 10 and 11 for more details).
smooth pursuit is never a sign of a peripheral vestibular The patient can then be asked to voluntarily fixate
deficit. on a moving target while the head is moved in the same
For the patient with nystagmus, determining the qual- direction. This procedure tests the ability to suppress
ity of pursuit eye movements may be difficult. In addition, or “cancel” the vestibulo-ocular reflex (VORc) and is a
care must be taken to distinguish gaze-evoked nystagmus function of the parietal lobe. Results should agree with
from end-point nystagmus. End-point nystagmus, which the observations made during the smooth-pursuit test. If
is normal, occurs when the eyes are at the extreme end of VORc is impaired, one should suspect a central nervous
their range of motion. It is also important to determine, in system disorder.
the initial patient history, whether the patient has any pre- Next, the VOR itself is tested. The head-thrust or
morbid eye disorder, including asking about a history of head impulse test is one test that an experienced physi-
strabismus. Patients with “lazy eye” disorders may have cal therapist can perform to assess the function of the
3970_Ch21_359-393 25/06/14 6:05 PM Page 369
vestibular system itself. The test traditionally involves an Then the patient is asked to read the chart while the head
unpredictable, high-acceleration, small-amplitude head is oscillated at 2 Hz by the examiner. Using a metronome
thrust in the horizontal plane,81,82 although the head thrust helps standardize the test.86,87 In normal individuals, visual
test can be performed in the planes of the each of the semi- acuity changes by one line in younger individuals or by
circular canals.83 The patient sits with the head pitched in two lines in older individuals. In patients with uncompen-
30 degrees of cervical flexion (using an imaginary line sated, unilateral vestibular loss, visual acuity degrades by
from the inferior rim of the ocular orbit to the external three or four lines. Computerized systems for measuring
acoustic meatus). The patient is instructed to maintain visual acuity during head movement are now available
visual fixation on the examiner’s nose. The patient’s head (see Chapter 11) and have the added benefit of being able
is then gently grasped, and a small-amplitude (5 to 10 deg) to determine dynamic visual acuity for rightward and left-
but high-acceleration (3,000 to 4,000 deg/sec 2) thrust is ward head movements separately. The NIH Toolbox has
applied horizontally. When the head impulse stops, the a DVA test and has established test-retest reliability.
eyes are observed to see if they are still directed toward Brandt and colleagues88 suggest that distance acuity
the target (the nose). If there is a decrease in vestibular poorer than 20/50 has a significant effect on postural sta-
function, a corrective “overt” saccade, a rapid eye move- bility. Additionally, balance can also be affected by visual
ment that returns the eyes to the target, will be observed. field loss89; patients with monocular vision may have par-
If the head impulse test at near distance is abnormal (cor- ticular difficulty with depth perception, which would af-
rective saccade is present), the test is repeated with the fect their ability to walk up and down stairs. The test
participant looking at a target place more than 2 m away. becomes much more difficult to perform with progressive
Repeating the test with a distant tar get helps reduce the or bifocal lenses, especially in the pitch plane.
false-positive results seen in some older individuals be- Eye movements can also be observed with the use of
cause of poor ability to accommodate to a near tar get. Frenzel lenses or video oculography (VOG). Frenzel
Testing should be performed with appropriate visual cor- lenses magnify the eyes, with light inside them to help
rection (glasses) for the distance tested although some- with visualization, enabling the clinician to observe eye
times it is difficult to visualize the eyes. The sensitivity of movements and greatly decreasing the patient’s ability to
the test has been reported to be 54%, and specificity to be stabilize the eyes with visual fixation. The VOG systems
100%.84 During the acute stage, corrective saccades occur permit the examiner to visualize the eyes in all positions
even with slow head rotations. In the chronic stage, people because infrared cameras record eye movements and
with vestibular deficits often are able to maintain fixation transmit the image to either a computer or television mon-
during slow head movements using the pursuit eye move- itor. Either one or both eyes may be visualized, depending
ment system but make corrective saccades to regain the on the system used. Clinical assessment of oculomotor
target with rapid head movements. In addition, the pres- function using Frenzel lenses should include spontaneous
ence of corrective saccades is dependent on the severity and gaze-evoked nystagmus, head shaking–induced nys-
of the deficit, and in general the head impulse test is most tagmus,90 tragal pressure–induced nystagmus, hyperven-
likely to be positive with deficits greater than 75%. It is tilation-induced nystagmus, and positional nystagmus (see
imperative that the examiner carefully view the eyes during Chapter 10). The VOG systems allow the playback of the
the first head thrust maneuver , because they may be able eye movements, permitting the patient to visualize their
to generate “covert” saccades on subsequent repetitionsof eye movements, and also permitting the clinician to per-
the test that will be missed by the examiner. manently record what was seen. There are significant
Another evaluation of VOR function is to measure advantages to being able to record eye movements with
the degradation of visual acuity that occurs with head complex eye movements and conditions. In addition, the
movement.40,85 We use a modified ETDRS chart with ability to determine if the nystagmus changes with fixation
SLOAN letters (Lighthouse Distance Visual Acuity Tests, can significantly help determine if you are dealing with a
Long Island City, New York) for the clinical version of peripherally or centrally generated nystagmus.
this test. A handheld Snellen card is not as appropriate, be- During the assessment of eye movement function,
cause it measures the patient’s vision at a distance of only the patient is asked to report any symptoms of blurred
18 inches, a distance that older patients in particular have vision or dizziness. Tests that involve repeated head move-
difficulty accommodating. In addition, the letters on the ments (VOR, head shaking–induced nystagmus, and dy-
Snellen card are not balanced for difficulty nor is there an namic visual acuity testing) may exacerbate the patient’s
equal decrease in letter size from line to line. In the clinical symptoms. If there is a significant increase in symptoms,
Dynamic Visual Acuity (DVA) test, the patient is first the patient may be unable or may refuse to continue with
asked to read a wall eye chart with the head stationary . the testing. Explaining the importance of the information
3970_Ch21_359-393 25/06/14 6:05 PM Page 370
370 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
to be gained from the test and acknowledging the patient’s from pathological changes. 93 Furthermore, certain disor-
symptoms often helps the patient to accept the discomfort ders that can affect perception, such as cataract formation,
caused by the test. If the patient is experiencing significant are more likely to occur in the older person.There is some
symptoms, some of the testing can be deferred, because if evidence that a decrease in VOR gain occurs with aging,
the patient becomes too sick, he or she may not return for at least at higher frequencies, and there is a more limited
a follow-up visit. adaptive capability with increased age.14,15
Multisystem involvement can impede the patient’ s
Sensory Evaluation functional progress. A patient with reduced vestibular
Sensation of the extremities can be tested to rule out con- function and a deficit in somatosensory cues is likely to
current pathology and assist in treatment planning. Per - compensate by using visual mechanisms. This patient is
haps the most important of these is the assessment of limited functionally if placed in a situation devoid of vi-
kinesthesia and proprioception, although profound sensory sual information. For example, many patients with re-
loss affecting touch and pressure sensitivity would also af- duced somatosensory cues and a peripheral vestibular
fect postural stability and raise the risk of a fall.91,92 These deficit have difficulty walking in the dark. A treatment
tests may not be performed in all subjects but should be plan that does not consider the patient’s sensory loss may
considered, especially in older individuals and in patients be ineffectual, and the patient’s functional independence
with diabetes or peripheral neuropathy. could suffer.
Proprioception can be assessed by having the patient
close the eyes and then moving the patient’s great toes ei- Coordination
ther up or down and asking the patient to identify the po- Vestibular deficits per se do not result in poor coordination
sition of the toe. Care must be taken to make these or in limb ataxia. Assessment of coordination is especially
relatively small movements, or the test becomes too easy. important, however, as part of the preoperative and post-
The patient must also be instructed not to guess at the an- operative examination of patients with cerebellar angle tu-
swer. This traditional test of proprioception does not ap- mors. Finger-to-nose and heel-to-shin movements and the
pear to be very sensitive, and patients are quite accurate ability to perform rapid alternating movements of fingers
in perceiving whether the toe is up or down even when or feet are gross tests that may be used to subjectively as-
other tests indicate sensory deficiencies. Kinesthesia can sess the patient’s coordination. Other tests of cerebellar
be tested by slowly moving the toe either up or down and function include truncal stability and tests of tone, such as
asking the patient to state the direction of the movement postural fixation and the rebound phenomenon; however,
as soon as he or she first perceives movement. Again, the surgery for vestibular schwannoma usually does not cause
patient should be instructed not to guess. Perception of the these deficits.
direction of the movement should occur before the toe is
moved more than 10 to 15 degrees, although each clinician Range of Motion and Strength
must develop his or her own internal standard for what is Range of motion and strength is not assessed in every pa-
normal. Vibration can be tested with application of a tun- tient. However, in some patients it is an important part of
ing fork to a bony prominence. One method is to ask the the assessment, such as in patients with neck pain. Al-
patient to identify when the vibratory sensation stops, and though the neck, trunk, and extremities can be included in
then to dampen the tuning fork unexpectedly . Another this assessment, special attention should be paid to the
method is to let the vibration diminish naturally and to neck’s range of motion. Patients in whom head movement
time the difference between when the patient and the cli- exacerbates symptoms may voluntarily restrict active neck
nician stop feeling the vibration. Again, each clinician motion and may eventually lose that range of motion. Fur-
must develop his or her own sense of normal. Devices are thermore, many of the other assessments involve passive
also available that quantify vibration thresholds. These de- movement of the neck (e.g., Head Impulse Test, head
vices enable the clinician to compare the patient with age- shaking–induced nystagmus, dynamic visual acuity, posi-
matched normal subjects and to follow changes over time. tional testing), and any limitations in movement or pain
Diminished sensation in the toes may not af fect postural associated with neck movement should be identified be-
stability; if a patient appears to have no sensation in the fore those tests are attempted. In some patients, when neck
toes, then the clinician should perform the same tests on range of motion increases, there appears to be an associ-
the ankles. ated decrease in dizziness symptoms.25 A detailed exami-
The visual, vestibular, and somatosensory systems nation of extremity strength and range of motion is often
all show decrements with age, and the clinician should be unnecessary; however, a quick screen indicates whether
familiar with these normal changes to dif ferentiate them more-detailed testing would be appropriate. It is common
3970_Ch21_359-393 25/06/14 6:05 PM Page 371
372 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
nystagmus during the Dix-Hallpike maneuver. Haynes and level of suspicion that the person has vertebrobasilar com-
associates reported that 86% of those with “subjective” promise, they should be referred out for blood flow studies.
BPPV reported significant improvement in symptoms Examples of other movements that can be tested are
after treatment with the Semont maneuver.96 Recognizing rolling, supine to sit, reaching in sitting toward the floor ,
BPPV and providing the proper intervention can signifi- and sit to stand. All these movements can be tested at var-
cantly enhance the patient’s quality of life (Fig. 21.2).97 ious speeds and with the patient’ s eyes open and closed.
BPPV is a common cause of vertigo. 98 This periph- The therapist should exercise care when having patients
eral vestibular deficit is easily and effectively treated with perform these maneuvers while standing with the eyes
physical therapy.99,100 In contrast, vertebral artery compres- closed, because this is often very difficult for patients and
sion is relatively rare, and unfortunately , clinical tests may cause them to lose their balance, especially if the
for vertebral artery compression are not reliable (see patient experiences severe vertigo. A more formalized
Chapter 31). Vertebral artery compression often causes assessment of what positions and movements induce
some symptoms that are like those of BPPV. Occlusion of symptoms in patient is the Motion Sensitivity Quotient
blood flow with compression of the vertebral artery pro- (MSQ). The MSQ is typically used to determine what po-
duces neurological symptoms, such as numbness, weak- sitions result in an increase in symptom intensity and to
ness, slurred speech, and mental confusion, as well as quantify the patient’s symptom intensity and duration. The
vertigo and nystagmus. Persons with BPPV do not expe- test consists of 16 changes in position, and the results are
rience neurological symptoms such as slurred speech, used to develop a treatment program to reduce symptom
mental confusion, weakness, or numbness. If there is any intensity (see Chapter 22).
The speed at which movement is performed can af-
fect the patient’s symptoms. For example, a quickly per -
formed movement could increase the patient’s symptoms,
whereas the same movement performed at a slower speed
may not. Varying the speed and the conditions under
which the patient performs the task may af fect the pa-
tient’s functional ability. Positional and movement testing
is limited only by the imagination of the therapist. For one
patient seen in our clinic, the only position that increased
her symptoms was the “all-fours” position, which she
would assume for looking under the bed (Fig. 21.3).
Head Movement Induced Symptoms: In addition
to testing positions and movements that incorporate mul-
tiple body segments, the patient is asked to perform head
movements. The head movements are typically tested with clinical examination. The Ottawa Sitting Scale may be help-
the patient sitting. These movements are performed at ful in the acute care setting to quantify sitting abilities.101
various speeds and with the eyes open and closed.The pa-
tient is asked to report whether these movements provoke Static Balance
symptoms and whether the symptoms are of a mild, mod- Static balance tasks have been used clinically to objec-
erate, or severe intensity. Verbal and visual analog scales tively document balance function.102-106 Single-leg stance
have been used in an attempt to better quantify the pa- (SLS), Romberg, and Sharpened or tandem Romberg tests
tient’s symptom intensity.40,41 The same movements are are often included in a static balance test battery and can
tested in the standing position or during gait, if the patient be performed with the patient’s eyes open or closed.106-108
can tolerate further testing. Traditionally, the variable of interest in this testing has
been the time that the patient maintains the position.
Normative data for dif ferent ages have been established
Balance Assessment for SLS, Romber g, and sharpened Romber g tests.106
Sitting Balance The Romberg test has been shown to have low intra-
Few patients with chronic vestibular disorders have diffi- subject variability when measures are repeated over a
culty with balance in sitting, but for some patients, includ- 5-day period.107
ing an assessment of sitting balance may be appropriate. Patients with vestibular deficits may have normal
Acutely, people will have deficits in sitting balance in performance on these tests. 109 Tests of static balance,
the first few days post-acute peripheral vestibular insult. such as the Romber g, are fairly easy. Patients may have
Patients should be tested while they are leaning anteriorly difficulty with this test only during the acute stage after
and posteriorly as well as right and left; tests should be onset of the vestibular deficit or if they have a coexisting
performed both actively and passively. The patient can be peripheral neuropathy. It is also important to remember
observed for weight-shifting ability, head righting, equi- that patients with balance disorders other than from vestibu-
librium reactions in the upper and lower extremities, and lar dysfunction may have difficulty with these tests. Hav-
the ability to recover to a trunk vertical position. Having ing difficulty maintaining stance with the Romber g test
the patient reach in sitting in all directions without support does not necessarily mean the subject has vestibular dys-
is also valuable information that can be gained in the function. Table 21-5 lists the expected results for static and
■ Table 21-5 EXPECTED TEST RESULTS IN PATIENTS WITH UNILATERAL VESTIBULAR LOSS (UVL)
Nystagmus Spontaneous and gaze-evoked in light and Spontaneous in dark; may have
dark; head shaking–induced nystagmus head-shaking–induced nystagmus
Vestibulo-ocular reflex (VOR) Abnormal with both slow and rapid head Abnormal with rapid head thrusts
thrusts toward side of lesion
Turn head while walking Cannot keep balance Normal; some may slow cadence
3970_Ch21_359-393 25/06/14 6:05 PM Page 374
374 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
dynamic balance tests in patients with acute and compen- with other vestibular diagnoses. Yoneda and Tokumasu113
sated UVL. reported that sway patterns seem to be dif ferent among
patients with Ménière’s disease, BPPV, and vestibular
Measures of Sway neuronitis, and that these patterns differed from those of
During performance of static balance tasks, medial-lateral a normal comparison group.
or anterior-posterior stability can be objectively docu-
mented with the use of “high-tech” tools such as force Altering Sensory Cues
platforms, accelerometers,110-112 or of simple tools such The modified Clinical Test for Sensory Interaction in Bal-
as a sway grid.112,113 When one is assessing and attempting ance (CTSIB) should be included in the rehabilitation as-
to replicate standing sway measures, the distance the sub- sessment.28,115-117 In some ways this test is an extension
ject stands from a stable visual target, upper extremity po- of the Romberg test, which assesses the effect of removing
sitioning, type or lack of footwear, and foot position of the visual cues on postural stability. Referred to formerly as
patient should be standardized. Brandt88 hypothesizes that the “foam and dome” test (Fig. 21.4), the CTSIB assesses
one explanation for the variability often found on the the influence of vestibular, somatosensory, and visual in-
Romberg test is the inconsistent positioning of the patient puts on postural control. In the modified version, the
with respect to a tar get used for visual fixation. The dis- “dome” portion of the test is no longer used.
tance that the patient stands from the tar get should be In the modified CSTIB (mCTSIB), standing on the
standardized and should be within 1.5 meters. Kirby and foam surface and closing the eyes alters somatosensory
associates114 employed five dif ferent foot positions to input and eliminates visual input. In this situation, vestibu-
determine the effect of foot position on sway. They deter- lar input is the most accurate information about postural
mined that subjects standing in double-limb stance were stability. Patients with uncompensated unilateral periph-
most stable in the 25-degree toe-out position. In addition, eral vestibular loss may have dif ficulty maintaining an
they observed that subjects had the greatest medial-lateral upright posture when both visual and support-surface in-
sway when their feet closely approximated each other. The formation are altered.19 Subjects with unilateral peripheral
standard Romberg position is with heel and toes together. vestibular dysfunction often lose their balance when
Postural sway correlates well with measures of the standing on foam with the eyes closed (using the mCTSIB
DHI.21,56 Of course, both postural sway and the responses protocol).
to the DHI questionnaire are under “voluntary control,” According to Nashner,19 symmetry and constancy of
and what is measured is subject to errors according to vestibular information are critical in providing an absolute
what the patient wants to convey . Sway patterns of pa- reference for reorganization of senses in conflicting con-
tients with central disorders dif fer from that of patients ditions. The inability of the vestibular system to provide
this information may explain why patients with unilateral self-initiated task. The subject is asked to reach as far for-
vestibular lesions often report postural instability when ward as possible. The extent of movement is measured
riding on an escalator or when walking on thick carpet with a simple yardstick (Fig. 21.5). Duncan and cowork-
across a dimly lit room. If a patient is unstable when ers124 have shown that functional reach, as a measure of a
both visual and somatosensory cues are altered, a treat- subject’s margin of stability, correlates well with center of
ment plan might be designed to improve the function pressure measures obtained from a force platform. This
of the remaining vestibular system. Depending on the test can be modified so that reaches in different directions
patient, an alternative treatment strategy may focus on are documented (Fig. 21.6). 121 Functional reach has also
altering the patient’s environment so that visual and so- been shown to be related to falls in older male veterans.124
matosensory cues are maximized, in an effort to overcome Generally, scores of 6 inches or less indicate that the per-
the vestibular loss.118-120 son is at high risk for falling.110 This test has been shown
to have concurrent validity with certain items of the Func-
Self-Initiated Movements tional Independence Measure and is useful in determining
In addition to static tests of balance function, self-initiated the risk of falling in older adults. It has also been shown
movements and dynamic tests of balance should be exam- to demonstrate change over the course of rehabilitation,126
ined. Self-initiated weight shifts performed in different di- although Wernick-Robinson and colleagues 127 suggest
rections can be assessed to determine whether the patient that functional reach measures have less value in patients
moves freely and symmetrically.121 Self-initiated move- with vestibular dysfunction.
ments should also be tested in functionally relevant and The standing reach test is administered easily and re-
rich contexts—for example, having the patient reach to quires very little equipment. Such a functional measure of
pick an object from the floor or place an object on a high balance can easily be used in the clinic or home care
shelf. Altering the environment so that there are many setting to document whether the patient has made gains in
visual distractions may also be a way to make the task physical therapy. The mini-BESTest might be considered
more difficult. Reaching for an object on the floor among to assess balance in persons with vestibular disorders, be-
many objects on the floor might make the task more dif- cause the test is promising but has not yet been validated
ficult for the patient. in persons with vestibular disorders.128
The functional reach test has been developed as
a way to assess the subject’ s balance and willingness Movement Strategy
to reach outside the base of support. 56,122-127 This test During the balance assessment, the therapist should ob-
functionally and reliably documents performance on a serve and document the patient’ s movement strategy .
376 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Three types of movement strategies have been described documenting whether the patient’s individual strategy is
for controlling anterior-posterior displacements of the cen- efficient, safe, and successful with respect to achieving the
ter of mass. 129 The ankle strategy produces shifts in the task goal. With this approach, the clinician’s expectations
center of mass via rotation of the body about the ankle of the patient’s responses are not as biased. This notion
joints. According to Horak and Nashner,130 the ankle strat- also has implications for treatment. Current motor learning
egy elicits a distal-to-proximal firing pattern of ankle, hip, theory suggests that the learner will be more successful
and trunk musculature. This activation pattern exerts com- in the task when the learner , not the teacher or therapist,
pensatory ankle torques, which are believed to correct for selects the appropriate movement strategy.131
small postural perturbations. The hip strategy controls
movement of the center of mass by flexing and extending
Gait Evaluation
the hips. Unlike the ankle strategy, the muscle activation
sequence associated with the hip strategy occurs in a prox- Evaluation of the patient’s gait provides a dynamic and
imal-to-distal fashion. This strategy produces a compen- functional assessment of the patient’ s postural control
satory horizontal shear force against the support surface. mechanism. The gait assessment can be obtained through
The hip strategy occurs in situations in which the ankle is clinical observation, videotape analysis, computerized gait
unable to exert the appropriate torque necessary to restore mats, or computerized motion analysis (there is evidence
balance. This situation arises when the task of maintaining of reliability for each).132-134 A videotape record of the pa-
balance is more dif ficult, such as when an individual tient’s gait is easily obtained clinically and can be ex-
stands on a small, narrow support surface. Finally, a step- tremely useful for documentation and patient education.
ping strategy is used when the center of mass is displaced The patient’s gait should be assessed in as many sit-
outside the base of support. This strategy is employed in uations as are realistically accessible to the therapist.
response to fast, large postural perturbations. Analysis of the patient walking down a crowded versus a
To function safely and independently throughout the non-crowded hallway may yield very dif ferent informa-
life span, humans are required to respond, through their tion about the patient’s gait function. Similarly, the patient
movements, to a variety of task situations and environ- should be instructed to walk at a normal speed, slowly ,
mental contexts. Postural strategies may be task-specific, and quickly. Common clinical observations indicate that
and therefore categorizing postural strategies can prove to patients with vestibular disorders, like other patients, have
be difficult. In addition, individuals vary greatly with re- greater gait instability when asked to walk at a non-
spect to body size, proportion, and weight. These consid- preferred speed. They also often have difficulty changing
erations, taken together with age-related changes, make gait speed while they are walking.
the task of categorizing postural strategies dif ficult. In- During gait assessment, the physical therapist docu-
stead, the physical therapist may be more successful in ments the patient’s movement strategy, the presence of
3970_Ch21_359-393 25/06/14 6:05 PM Page 377
gait deviations, and whether the patient reports any abnor- progress. The functional gait assessment is often used for
mal sensation of movement. The patient with a peripheral younger people rather than the DGI, as the test was de-
vestibular disorder may select an overall strategy for gait signed to negate a possible ceiling effect of the DGI.28 The
that limits movement of the head and trunk. Clinically, this HiMat has also been used recently for patients with higher
gait is characterized as being stif f or robot-like, and the level gait disorders, although none of the tests appear op-
patient may use excessive visual fixation while walking. timal for those persons with blast injuries and vestibular
Some of the typical gait deviations demonstrated by these complaints.137-140
patients include inconsistent step lengths, veering to the Many patients with unilateral peripheral vestibular
right or left, a widened base of support, a listing of the loss experience difficulty when asked to perform gait tasks
head and/or trunk to one side, decreased rotation through that require an anticipatory mode of motor control. One
the trunk and neck (and decreased arm swing), and “en such task requires the patient to walk quickly and then to
bloc”135 movements and slow turns. In addition to observ- stop immediately on the therapist’s command. To maintain
able gait deviations, patients with a unilateral peripheral a level of uncertainty, the patient should not be informed
vestibulopathy may associate dizziness with their gait ahead of time of the required pivot direction. The speed
instability. of the pivot is another factor that must be considered.The
A complete assessment of the patient’s gait function patient may also slow gait speed as a strategy to avoid dis-
should include having the patient perform a variety of equilibrium during the task. The patient may also slow gait
tasks while walking. Many of these tasks cause the patient speed to avoid the anticipatory requirements of the task.
to lose balance; therefore, during this portion of the gait In such instances, the patient should perform the task at a
assessment, the physical therapist may need to guard the faster speed so that the therapist obtains a more complete
patient but without becoming a part of the patient’ s pos- picture of the patient’s gait function.
tural control system. The goal of this assessment is to learn Observing the ability of the patient to negotiate an
how the patient, not the therapist, solves the problem of obstacle course may also provide valuable information
postural control. about his or her functional balance (Fig. 21.7) and the pa-
One of the gait tasks performed by the patient is to tient’s ability to function in an anticipatory mode of con-
walk while moving the head, either to the left and right or trol. To assess the patient’s functional balance, the patient
up and down. Head movements up/down and right/left are self-selects the path to negotiate the obstacle course. In
components of the Dynamic Gait Index (DGI), 136 a very addition, the patient decides whether or not to pick up or
helpful tool for use in the quantification of gait dysfunc- step over an object in the course. The patient also decides
tion. The therapist documents whether the patient experi- to negotiate the course quickly or slowly . If, on the
ences symptoms (dizziness, lightheadedness, etc.), loss of other hand, the patient’s anticipatory control is of interest,
balance, or an exaggeration of gait deviations. Such a de- the therapist directs which path the patient should follow.
tailed assessment facilitates documentation of the patient’s Task variability and uncertainty are manipulated by the
378 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
therapist. For example, the therapist may decide at which associates27,30,136,141-143 is very helpful in quantifying gait
point in the course to throw a ball toward the patient dysfunction in people with vestibular disease (Box 21-6).
(Fig. 21.8). A temporal constraint may also be added to It is currently undergoing a revision that is not available
the task. Asking the patient to negotiate the course as at the time of publication (personal communication, A
quickly as possible enhances task difficulty and provides Shumway-Cook). This eight-item test takes less than
a means to subjectively document the patient’s progress. 10 minutes to perform and requires little equipment (a
The ability of the patient to perform gait tasks while shoebox, two cones, and stairs). Scoring is based on the
manipulating an object with the hands should also be as- concept of no, minimal, moderate, or severe gait dysfunc-
sessed. Patients with unilateral vestibular loss frequently tion when performing the eight gait tasks. It has been re-
complain of increased gait instability when carrying a bas- lated to scores on the Berg Balance Scale,141,142 a tool to
ket of laundry up a flight of stairs or when carrying a bag assess balance. Scores of 19 or less on the DGI have been
of groceries. Clinically, the patient’s ability to monitor pos- related to falls in community-living elderly adults. 138 In
tural control while manipulating an object can be tested in patients with severe vestibular disability , we have seen
a variety of ways. The patient can be asked to walk, pick scores as low as 3 out of 24! The DGI is very useful for
up one or more objects off the floor, and continue walking. quantifying gait dysfunction in people with vestibular dys-
Documenting the strategy used by the patient to perform function and can be easily used to determine whether the
this task is important. Many patients with vestibular loss therapy intervention is effective.
bend at the knees and avoid flexing the head or bending at The Berg Balance Scale (BBS) is also a useful tool
the hips. This strategy may be selected in an attempt to min- to use if the patient has balance dysfunction.143-146 Not all
imize provocation of symptoms or loss of balance.A patient patients with peripheral vestibular disorders have balance
may also be asked to negotiate a flight of stairs while car- disorders.97 Scores of 36 and less on this test indicate a
rying objects of varying weight or size. This task is impor- 100% risk of falling in older adults.141,143,147,148 This scale
tant to include in the gait assessment, because a patient who consists of 14 items that include sitting, standing, and
demonstrates little difficulty with other gait tasks may ex- reaching activities with a total point value of 56. It has
press extreme postural instability with this task. been shown to be a reliable and valid test with many dif-
Other gait tasks that the therapist can assess are side- ferent patient populations and is very useful in assessing
stepping, backward walking, tandem walking, walking in change in a patient’s balance over time. Concurrent valid-
a figure of eight, and marching and/or jogging in place. If ity of the BBS and the DGI has been established in a
feasible, the patient should be asked to perform these tasks mixed group of patients with vestibular dysfunction.143
at various speeds with the eyes open and closed. Another tool that might be helpful to assess gait over
Additional tests can be used to assess functional time is the Timed “Up and Go” (TUG) test. 149 This test
balance in subjects with peripheral vestibular dysfunc- consists of having the subject rise from a standard height
tion. The DGI, as developed by Shumway-Cook and chair with armrests, walk 3 m, turn, and return to sit in the
Box 21-6
Continued
3970_Ch21_359-393 25/06/14 6:05 PM Page 380
380 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Box 21-6
chair. It is closely related to speed of gait and is a quick aligned at 90-degree angles to each other, similar to a plus
method to assess gait performance over time in any phys- sign. The subject is asked to step into each block twice,
ical setting. In people with vestibular dysfunction, it is going forwards and then repeating the pattern backwards
often helpful to have the subject turn to the right and also as they are timed and instructed to perform the task as
to the left to detect any asymmetry. The test takes less than quickly as possible. The test was originally designed to
1 minute to complete and requires only a chair and a stop- assess risk of falling in older adults. It functionally pro-
watch. In a mixed group of patients with vestibular disor- vides information about the ability to make quick changes
ders, scores of 11.1 seconds or greater were 5 times more of direction and tests the ability to step backwards.
likely to have reported a fall in the previous 6 months. 30
At 11.1 seconds, the sensitivity of the test was 80% and
Red Flags
the specificity was 56%, suggesting that the tool may be
helpful for use in persons with vestibular dysfunction. 30 As the assessment is being performed, certain “red flags”
The TUG has been modified to include components that may appear. Signs and symptoms of central nervous sys-
assess an individual’s ability to allocate attention. 148,150 tem pathology must be recognized and reported to the re-
Although the modified TUG has not yet been validated in ferring physician (Box 21-7). It is possible for individuals
patients with vestibular deficits, it adds an important com- to be referred to a balance and vestibular clinic with undi-
ponent to balance testing—that of the ef fect of cognitive agnosed central nervous system disease. Multiple sclerosis,
impairments on balance. brainstem transient ischemic attacks (TIAs), Parkinson’ s
The four-square-step test has been validated with per- disease, cerebellar disorders, and migraines are but a
sons with vestibular disorders. 151,152 Straight canes are few of the disorders that have been diagnosed in patients
3970_Ch21_359-393 25/06/14 6:05 PM Page 381
382 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
but not when they are sitting), with central nervous system the patient’s perspective. Some studies have begun to de-
lesions, or with other medical problems such as low blood fine change according to criteria that may be more clini-
pressure, or as a side effect of medications. Vertigo, most cally relevant, but the criteria can vary considerably
frequently associated with peripheral vestibular deficits, among studies. Brown and colleagues118 defined clinically
can occur with central lesions (often, patients with central significant change for the DHI as a change greater than 18
lesions may not complain of vertigo) and with other med- points, but the investigators did not describe how they ar-
ical problems, such as presyncope. These patients may rived at these criteria.
have balance problems and may need an individualized A second method of examining improvement has been
exercise program but not necessarily exercises designed to determine whether the patient’s performance has returned
to improve vestibular function. It is not known what in - to within normal values for age. This information exists for
terventions are optimal for persons with central vestibular only some of the outcome measures we use, such as the
dysfunction, although there is some evidence that they computerized DVA test and gait speed.40,157 A third method
tend to improve with rehabilitation.154 would be to use values based on comparisons with other in-
formation. For example, the cutof f value for low risk for
falls using the DGI was established by comparing test
Assess and Reassess scores against the person’s history of falling.142,143 A fourth
The initial assessment is directed at identifying problems approach has been to combine the scores for several tests
associated with the vestibular deficit, such as increased and then define outcome on the basis of the total or
dizziness or decreased visual acuity with head movements, weighted score. Whitney and colleagues61 used a composite
and with the functional limitations of the patient. The ex- score based on the ABC, DHI, and DGI scores. Finally, cri-
ercise plan, therefore, may include vestibular exercises but teria for improvement can be based on change in score that
must also address the specific problems and level of func- is beyond the within-subject variability of the measures. 68
tion of the individual patient. Developing a problem list Clearly, more research is needed in this important area.
enables the therapist to set goals and devise specific exer-
cises for each of those goals. As the patient responds to Summary
the exercises, reassessment is necessary to allow modifi-
cation of the treatment program. The participation of the The physical therapy assessment is multifaceted and aimed
patient is key in developing a plan of care that is mutually toward identifying the patient’s specific functional deficits
agreed on and feasible for the patient’s lifestyle. and to quantitatively establish the effects of the vestibular
deficit on the patient’s vestibulo-ocular and vestibulospinal
systems and subjective complaints of disequilibrium and
Quantify the Assessment vertigo. The results of the assessment are used to identify
Although not all components of the assessment yield quan- specific patient problems and to develop treatment goals
tifiable data, many tests do, such as the patient’s subjective for the patient. The results of the assessment also provide
complaints, DVA, measures of postural stability, and most the basis for determining whether the interventions used
of the gait and balance measures. Taking the time to objec- are successful. The aim of exercise in the rehabilitation of
tively measure the patient’s performance is important for patients with vestibular disorders is to promote vestibular
the therapist to determine the outcome of the patient’ s in- compensation and functional recovery.
tervention, to modify the intervention, to justify further in-
tervention, and to determine when to terminate intervention. Acknowledgments
The authors wish to acknowledge the contribution of
Diane F. Borello-France, PhD, PT , who cowrote this
Determining Whether There Has Been chapter in the first edition of Vestibular Rehabilitation.
Improvement Some of the work described here was supported by NIH
grant DC05384 (SLW) and NIH grant DC03196 (SJH).
One of the most difficult parts of the assessment is decid-
ing what criteria to use in determining whether the pa-
References
tient’s problem has actually improved. Many studies that
examine changes in patients with performance of vestibu- 1. Herdman SJ, Blatt P, Schubert MC, Tusa RJ. Falls in
lar exercises use a statistically significant change in test patients with vestibular deficits. Am J Otol. 2000;21:847.
2. Eagger S, Luxon LM, Davies RA, Coelho A, Ron MA.
score as the criteria for “improvement.” 33,43,155-157 How- Psychiatric morbidity in patients with peripheral vestibular
ever, statistically significant change does not necessarily disorder: a clinical and neuro-otological study. J Neurol
indicate a clinically meaningful change, especially from Neurosurg Psychiatry. 1992;55:383.
3970_Ch21_359-393 25/06/14 6:05 PM Page 383
3. Eckhardt-Henn A, Breuer P, Thomalske C, Hoffmann SO, 23. Allum JH, Pfaltz CR. Influence of bilateral and acute uni-
Hopf HC. Anxiety disorders and other psychiatric sub- lateral peripheral vestibular deficits on early sway stabiliz-
groups in patients complaining of dizziness. J Anxiety ing responses in human tibialis anterior muscles. Acta
Disord. 2003;17:369. Otolaryngol. Suppl. 1984;406:115.
4. Tos T, Caye-Thomasen P, Stangerup SE, Tos M, Thomsen 24. Karlberg M, Magnusson M, Malmstrom EM, Melander A,
J. Long-term socio-economic impact of vestibular Moritz U. Postural and symptomatic improvement after
schwannoma for patients under observation and after physiotherapy in patients with dizziness of suspected
surgery. J Laryngol Otol. 2003;117:955. cervical origin. Arch Phys Med Rehabil. 1996;77:874.
5. Whitney SL, Hudak MT, Marchetti GF. The activities- 25. Wrisley DM, Sparto PJ, Whitney SL, Furman JM.
specific balance confidence scale and the dizziness handi- Cervicogenic dizziness: a review of diagnosis and treat-
cap inventory: a comparison. J Vestib Res. 1999;9:253. ment. J Orthop Sports Phys Ther. 2000;30:755.
6. Yardley L. Contribution of symptoms and beliefs to handi- 26. Patten C, Horak FB, Krebs DE. Head and body center of
cap in people with vertigo - a longitudinal-study. Br J Clin gravity control strategies: adaptations following vestibular
Psychol. 1994;33:101. rehabilitation. Acta Otolaryngol. 2003;123:32.
7. Badke M, Pylke G, Shea T, Miedaner J. Outcomes in 27. Whitney SL, Hudak MT, Marchetti GF. The dynamic gait
vestibular ablative procedures. Otol Neurotol. 2002; index relates to self-reported fall history in individuals
23:504. with vestibular dysfunction. J Vestib Res. 2000;10:99.
8. Furman JM, Hsu LC, Whitney SL, Redfern MS. Otolith- 28. Wrisley DM, Marchetti GF, Kuharsky DK, Whitney SL. Re-
ocular responses in patients with surgically confirmed liability, internal consistency, and validity of data obtained
unilateral peripheral vestibular loss. J Vestib Res. 2003; 13:143. with the functional gait assessment. Phys Ther. 2004;84:906.
9. Whitney S, Wrisley DM, Brown KE, Furman JM. Is 29. Wrisley DM, Walker ML, Echternach JL, Strasnick B. Re-
Perception of handicap related to functional performance liability of the dynamic gait index in people with vestibular
in persons with vestibular dysfunction? Otol Neurotol. disorders. Arch Phys Med Rehabil. 2003;84:1528.
2004;25:1. 30. Whitney SL, Marchetti GF, Schade A, Wrisley DM. The
10. Cohen HS, Kimball KT, Adams AS. Application of the sensitivity and specificity of the Timed “Up & Go” and
vestibular disorders activities of daily living scale. the Dynamic Gait Index for self-reported falls in persons
Laryngoscope. 2000;110:1204. with vestibular disorders. J Vestib Res. 2004;14:397.
11. Cohen H, Kane-Wineland M, Miller LV, Hatfield CL. Oc- 31. Gall RM, Ireland DJ, Robertson DD. Subjective visual
cupation and visual/vestibular interaction in vestibular re- vertical in patients with benign paroxysmal positional
habilitation. Otolaryngol Head Neck Surg. 1995;112:526. vertigo. J Otolaryngol. 1999;28:162.
12. World Health Organization. 2001; www.cdc.gov.hchs/ 32. Gill-Body KM, Krebs DE. Locomotor stability problems
about/otheract/ic99/icfhome.htm. associated with Vestibulopathy: assessment and treatment.
13. Shumway-Cook A, Horak FB. Rehabilitation strategies Physical Therapy Practice. 1994;3:232.
for patients with vestibular deficits. Neurologic clinics. 33. Krebs DE, Gill-Body KM, Riley PO, Parker SW. Double-
1990;8:441. blind, placebo-controlled trial of rehabilitation for bilateral
14. Allum JH, Yamane M, Pfaltz CR. Long-term modifica- vestibular hypofunction: preliminary report. Otolaryngol
tions of vertical and horizontal vestibulo-ocular reflex Head Neck Surg. 1993;109:735.
dynamics in man. I. After acute unilateral peripheral 34. Jeka JJ, Lackner JR. Fingertip contact influences human
vestibular paralysis. Acta Otolaryngol. 1988;105:328. postural control. Exp Brain Res. 1991;100:495.
15. Paige GD. Nonlinearity and asymmetry in the human 35. Lackner JR. Some proprioceptive influences on the per-
vestibulo-ocular reflex. Acta Oto-laryngol. 1989;108:1. ceptual representation of body shape and orientation.
16. Baloh RW. The Essentials of Neurology. Philadelphia: Brain. 1988;111(Pt 2):281.
F.A. Davis; 1984. 36. Jeka JJ. Light touch contact as a balance aid. Phys Ther.
17. Norré M. Treatment of Unilateral Vestibular Hypofunc- 1997;77:476.
tion. London: John Wiley & Sons; 1984. 37. Cohen H. Vestibular rehabilitation reduces functional dis-
18. Shumway-Cook A, Patla A, Stewart A, Ferrucci L, Ciol ability. Otolaryngol Head Neck Surg. 1992;107:638.
MA, Guralnik JM. Environmental components of mobility 38. Hain TC, Uddin M. Pharmacological treatment of vertigo.
disability in community-living older persons. Journal of CNS Drugs. 2003;17:85.
the American Geriatrics Society. 2003;51:393. 39. Johnson GD. Medical management of migraine-related
19. Nashner LM. Adaptation of human movement to altered dizziness and vertigo. Laryngoscope. 1998;108:1.
enviroments. Trends Neurosci. 1982;5:358. 40. Herdman SJ, Schubert MC, Das VE, Tusa RJ. Recovery of
20. Lacour M, Roll JP, Appaix M. Modifications and develop- dynamic visual acuity in unilateral vestibular hypofunc-
ment of spinal reflexes in the alert baboon (Papio papio) tion. Arch Otolaryngol Head Neck Surg. 2003;129:819.
following an unilateral vestibular neurotomy. Brain 41. Wrisley DM, Whitney SL, Furman JM. Vestibular rehabil-
Research. 1976;113:255. itation outcomes in patients with a history of migraine.
21. Robertson DD, Ireland DJ. Dizziness Handicap Inventory Otol Neurotol. 2002;23:483.
correlates of computerized dynamic posturography. 42. Hall CD, Herdman SJ. Reliability of clinical measures
J Otolaryngol. 1995;24:118. used to assess patients with peripheral vestibular disor-
22. Alghwiri AA, Marchetti GF, Whitney SL. Content compari- ders. J neurol phys ther. 2006;30:74.
son of self-report measures used in vestibular rehabilitation 43. Horak FB, Jones-Rycewicz C, Black FO, Shumway-Cook
based on the international classification of functioning, A. Effects of vestibular rehabilitation on dizziness and
disability and health. Phys Ther. 2011;91:346. imbalance. Otolaryngol Head Neck Surg. 1992;106:175.
3970_Ch21_359-393 25/06/14 6:05 PM Page 384
384 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
44. Ware JE, Jr., Sherbourne CD. The MOS 36-item short- and vestibular dysfunction with history of migraine.
form health survey (SF-36), I: conceptual framework and Laryngoscope. 2000;110:1528.
item selection. Med Care. 1992;30:473. 62. Pothula VB, Chew F, Lesser TH, Sharma AK. Falls and
45. McHorney CA, Ware JE, Jr., Raczek AE. The MOS 36-Item vestibular impairment. Clin Otolaryngol. 2004;29:179.
Short-Form Health Survey (SF-36), II: psychometric and 63. Agrawal Y, Carey JP, Della Santina CC, Schubert MC,
clinical tests of validity in measuring physical and mental Minor LB. Disorders of balance and vestibular function in
health constructs. Med Care. 1993;31:247. US adults: data from the National Health and Nutrition
46. McHorney CA, Ware JE, Jr., Lu JF, Sherbourne CD. The Examination Survey, 2001-2004. Archives of internal
MOS 36-item Short-Form Health Survey (SF-36), III: medicine. 2009;169:938.
tests of data quality, scaling assumptions, and reliability 64. Studenski S, Duncan PW, Chandler J, et al. Predicting
across diverse patient groups. Med Care. 1994;32:40. falls: the role of mobility and nonphysical factors. Journal
47. McHorney CA, Kosinski M, Ware JE, Jr. Comparisons of of the American Geriatrics Society. 1994;42:297.
the costs and quality of norms for the SF-36 health survey 65. Sattin RW, Easley KA, Wolf SL, Chen Y, Kutner MH. Re-
collected by mail versus telephone interview: results from duction in fear of falling through intense tai chi exercise
a national survey. Med Care. 1994;32:551. training in older, transitionally frail adults. Journal of the
48. Ware JE, Jr., Kosinski M, Bayliss MS, McHorney CA, American Geriatrics Society. 2005;53:1168.
Rogers WH, Raczek A. Comparison of methods for the 66. Wolf SL, Sattin RW, O’Grady M, et al. A study design to
scoring and statistical analysis of SF-36 health profile and investigate the effect of intense Tai Chi in reducing falls
summary measures: summary of results from the Medical among older adults transitioning to frailty. Controlled
Outcomes Study. Med Care. 1995;33:AS264. clinical trials. 2001;22:689.
49. Enloe LJ, Shields RK. Evaluation of health-related quality 67. Summary of the updated American Geriatric Society/
of life in individuals with vestibular disease using disease- British Geriatric Society clinical practice guideline for
specific and general outcome measures. Phys Ther. the prevention of falls in older persons. JAGS. 2011;
1997;77:890. 59:148.
50. Bergner M, Bobbitt RA, Carter WB, Gilson BS. The Sick- 68. Hall CD, Schubert MC, Herdman SJ. Prediction of fall
ness Impact Profile: development and final revision of a risk reduction as measured by dynamic gait index in indi-
health status measure. Med Care. 1981;19:787. viduals with unilateral vestibular hypofunction. Otol
51. Patrick DL, Deyo RA. Generic and disease-specific mea- Neurotol. 2004;25:746.
sures in assessing health status and quality of life. Med 69. Kao CL, Chen LK, Chern CM, Hsu LC, Chen CC, Hwang
Care. 1989;27:S217. SJ. Rehabilitation outcome in home-based versus super-
52. Shepard NT, Telian SA, Smith-Wheelock M. Habituation vised exercise programs for chronically dizzy patients.
and balance retraining therapy. A retrospective review. Archives of gerontology and geriatrics. 2010;51:264.
Neurologic clinics. 1990;8:459. 70. Horning E, Gorman S. Vestibular rehabilitation decreases
53. Reishen S. A career in the balance. Sports Illustrated. fall risk and improves gaze stability for an older individual
1991:36. with unilateral vestibular hypofunction. J Geriatr Phys
54. Polensek SH, Sterk CE, Tusa RJ. Screening for vestibular Ther. 2007;30:121.
disorders: a study of clinicians’ compliance with recom- 71. Macias JD, Massingale S, Gerkin RD. Efficacy of vestibu-
mended practices. Medical science monitor: international lar rehabilitation therapy in reducing falls. Otolaryngol
medical journal of experimental and clinical research. Head Neck Surg. 2005;133:323.
2008;14:CR238. 72. Cohen HS, Kimball KT. Development of the vestibular
55. Jacobson GP, Newman CW. The development of the disorders activities of daily living scale. Arch Otolaryngol
Dizziness Handicap Inventory. Arch Otolaryngol Head Head Neck Surg. 2000;126:881.
Neck Surg. 1990;116:424. 73. Bronstein AM. Vision and vertigo: some visual aspects of
56. Mann GC, Whitney SL, Redfern MS, Borello-France DF, vestibular disorders. J Neurol. 2004;251:381.
Furman JM. Functional reach and single leg stance in 74. Sparto PJ, Whitney SL, Hodges LF, Furman JM, Redfern
patients with peripheral vestibular disorders. J Vestib Res. MS. Simulator sickness when performing gaze shifts
1996;6:343. within a wide field of view optic flow environment:
57. Gill-Body KM, Popat RA, Parker SW, Krebs DE. Rehabil- preliminary evidence for using virtual reality in vestibular
itation of balance in two patients with cerebellar dysfunc- rehabilitation. J Neuroengineering Rehabil. 2004;1:14.
tion. Phys Ther. 1997;77:534. 75. Pavlou M, Lingeswaran A, Davies RA, Gresty MA,
58. Jacobson GP, Newman CW, Hunter L, Balzer GK. Bronstein AM. Simulator based rehabilitation in refractory
Balance function test correlates of the Dizziness Handicap dizziness. J Neurol. 2004;251:983.
Inventory. J Am Acad Audiol. 1991;2:253. 76. Pavlou M, Quinn C, Murray K, Spyridakou C, Faldon M,
59. Powell LE, Myers AM. The Activities-specific Balance Bronstein AM. The effect of repeated visual motion stim-
Confidence (ABC) Scale. J Gerontol A Biol Sci Med Sci. uli on visual dependence and postural control in normal
1995;50A:M28. subjects. Gait Posture. 2011;33:113.
60. Myers AM, Fletcher PC, Myers AH, Sherk W. Discrimina- 77. Whitney SL, Jacob RG, Sparto PJ, et al. Acrophobia and
tive and evaluative properties of the Activities-specific pathological height vertigo: indications for vestibular
balance confidence (ABC) scale. J Gerontol Med Sci. physical therapy? Phys Ther. 2005;85:443.
1998;53A:M287. 78. Sullivan M. The new subjective medicine: taking the
61. Whitney SL, Wrisley DM, Brown KE, Furman JM. patient’s point of view on health care and health. Soc Sci
Physical therapy for migraine-related vestibulopathy Med. 2003;56:1595.
3970_Ch21_359-393 25/06/14 6:05 PM Page 385
79. Morris AE, Lutman ME, Yardley L. Measuring outcome efficacy in patients presenting without nystagmus.
from vestibular rehabilitation, part II: refinement and Laryngoscope. 2002;112:796.
validation of a new self-report measure. International 97. Gamiz MJ, Lopez-Escamez JA. Health-related quality
journal of audiology. 2009;48:24. of life in patients over sixty years old with benign parox-
80. Morris AE, Lutman ME, Yardley L. Measuring outcome ysmal positional vertigo. Gerontology. 2004;50:82.
from Vestibular Rehabilitation, Part I: Qualitative devel- 98. Furman JM, Cass SP. Benign paroxysmal positional
opment of a new self-report measure. International jour- vertigo. N Engl J Med. 1999;341:1590.
nal of audiology. 2008;47:169. 99. Brandt T, Daroff RB. Physical therapy for benign parox-
81. Halmagyi GM, Curthoys IS. A clinical sign of canal ysmal positional vertigo. Archives of otolaryngology.
paresis. Archives of neurology. 1988;45:737. 1980;106:484.
82. Cremer PD, Halmagyi GM, Aw ST, et al. Semicircular 100. Herdman SJ. Advances in the treatment of vestibular dis-
canal plane head impulses detect absent function of indi- orders. Phys Ther. 1997;77:602.
vidual semicircular canals. Brain. 1998;121 ( Pt 4):699. 101. Thornton M, Sveistrup H. Intra- and inter-rater reliability
83. Migliaccio AA, Schubert MC, Clendaniel RA, et al. Axis and validity of the Ottawa Sitting Scale: a new tool to
of eye rotation changes with head-pitch orientation during characterise sitting balance in acute care patients. Dis-
head impulses about earth-vertical. Journal of the Associa- ability and rehabilitation. 2010;32:1568.
tion for Research in Otolaryngology : JARO. 2006;7:140. 102. Bohannon RW, Larkin PA, Cook AC, Gear J, Singer J.
84. Oliva M, Martin Garcia MA, Bartual J, Ariza A, Garcia Decrease in timed balance test scores with aging. Phys
Teno M. [The head-thrust test (HTT): physiopathological Ther. 1984;64:1067.
considerations and its clinical use in daily practice]. Acta 103. Fregly AR, Graybiel A, Smith MJ. Walk on floor eyes
Otorrinolaringol Esp. 1998;49:275. closed (WOFEC): a new addition to an ataxia test battery.
85. Herdman SJ, Tusa RJ, Blatt P, Suzuki A, Venuto PJ, Aerospace medicine. 1972;43:395.
Roberts D. Computerized dynamic visual acuity test in 104. Fregly AR, Smith MJ, Graybiel A. Revised normative
the assessment of vestibular deficits. Am J Otol. 1998; standards of performance of men on a quantitative ataxia
19:790. test battery. Acta oto-laryngologica. 1973;75:10.
86. Dannenbaum E, Paquet N, Chilingaryan G, Fung J. Clinical 105. Fregly AR, Graybiel A. An ataxia test battery not requir-
evaluation of dynamic visual acuity in subjects with uni- ing rails. Aerospace medicine. 1968;39:277.
lateral vestibular hypofunction. Otol Neurotol. 106. Ekdahl C, Andersson SI. Standing balance in rheumatoid
2009;30:368. arthritis. A comparative study with healthy subjects.
87. Dannenbaum E, Paquet N, Hakim-Zadeh R, Feldman AG. Scandinavian journal of rheumatology. 1989;18:33.
Optimal parameters for the clinical test of dynamic visual 107. Black FO, Wall C, 3rd, Rockette HE, Jr., Kitch R. Nor-
acuity in patients with a unilateral vestibular deficit. J mal subject postural sway during the Romberg test.
Otolaryngol. 2005;34:13. Am J Otolaryngol. 1982;3:309.
88. Brandt T. Visual acuity, visual field and visual scene char- 108. Thyssen HH, Brynskov J, Jansen EC, Munster-Swendsen
acteristics affect postural balance. In: Igarashi M, Black J. Normal ranges and reproducibility for the quantitative
FO, eds. Vestibular and Visual Control on Posture and Romberg’s test. Acta neurologica Scandinavica. 1982;
Locomotor Equilibrium. Basel: Karger; 1985. 66:100.
89. Paulus WM, Straube A, Brandt T. Visual stabilization of 109. Horak FB. Clinical measurement of postural control in
posture. Physiological stimulus characteristics and clinical adults. Phys Ther. 1987;67:1881.
aspects. Brain. 1984;107(Pt 4):1143. 110. Whitney SL, Roche JL, Marchetti GF, et al. A compari-
90. Hain TC, Fetter M, Zee DS. Head-shaking nystagmus son of accelerometry and center of pressure measures
in patients with unilateral peripheral vestibular lesions. during computerized dynamic posturography: a measure
Am J Otolaryngol. 1987;8:36. of balance. Gait Posture. 2011;33:594.
91. Richardson JK, Ashton-Miller JA, Lee SG, Jacobs K. 111. Mancini M, Salarian A, Carlson-Kuhta P, et al. ISway: a
Moderate peripheral neuropathy impairs weight transfer sensitive, valid and reliable measure of postural control.
and unipedal balance in the elderly. Arch Phys Med Journal of neuroengineering and rehabilitation. 2012;
Rehabil. 1996;77:1152. 9:59.
92. Richardson JK, Hurvitz EA. Peripheral neuropathy: a true 112. Nashner LM, Black FO, Wall C, 3rd. Adaptation to altered
risk factor for falls. J Gerontol A Biol Sci Med Sci. 1995; support and visual conditions during stance: patients with
50:M211. vestibular deficits. The Journal of neuroscience : the offi-
93. Kenshalo DR. Age changes in touch, vibration, tempera- cial journal of the Society for Neuroscience. 1982;2:536.
ture, kinethesis and pain sensitivity. In: Birren JE, Schaie 113.Yoneda S, Tokumasu K. Frequency analysis of body sway
K, eds. Handbook of Psychology of Aging. New York: Van in the upright posture . Statistical study in cases of periph-
Nostrand Reinhold; 1977. eral vestibular disease. Acta Otolaryngol. 1986;102:87.
94. Dix MR, Hallpike CS. The pathology, symptomatology 114. Kirby RL, Price NA, MacLeod DA. The influence of foot
and diagnosis of certain common disorders of the vestibu- position on standing balance. Journal of biomechanics.
lar system. The Annals of otology, rhinology, and laryn- 1987;20:423.
gology. 1952;61:987. 115. Shumway-Cook A, Horak FB. Assessing the influence of
95. Herdman SJ. Treatment of benign paroxysmal positional sensory interaction of balance. Suggestion from the field.
vertigo. Phys Ther. 1990;70:381. Phys Ther. 1986;66:1548.
96. Haynes DS, Resser JR, Labadie RF, et al. Treatment of 116. Weber PC, Cass SP. Clinical assessment of postural
benign positional vertigo using the semont maneuver: stability. Am J Otol. 1993;14:566.
3970_Ch21_359-393 25/06/14 6:05 PM Page 386
386 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
117. Whitney SL, Wrisley DM. The influence of footwear 136. Shumway-Cook A, Woollacott MH. Motor Control:
on timed balance scores of the modified clinical test of Theory and Practical Applications. Baltimore: Williams
sensory interaction and balance. Arch Phys Med Rehabil. & Wilkins; 1995.
2004;85:439. 137. Williams GP, Morris ME. Tests of static balance do not
118. Brown KE, Whitney SL, Wrisley DM, Furman JM. predict mobility performance following traumatic brain
Physical therapy outcomes for persons with bilateral injury. Physiotherapy Canada. Physiotherapie Canada.
vestibular loss. Laryngoscope. 2001;111:1812. 2011;63:58.
119. Whitney SL, Rossi MM. Efficacy of vestibular rehabili- 138. McCulloch KL, Buxton E, Hackney J, Lowers S. Balance,
tation. Otolaryngologic clinics of North America. 2000; attention, and dual-task performance during walking after
33:659. brain injury: associations with falls history. The Journal
120. Whitney SL, Wrisley DM. Vestibular Rehabilitation. of head trauma rehabilitation. 2010;25:155.
Boston: MIT Press; 2003. 139. Williams G, Robertson V, Greenwood K, Goldie P,
121. Newton RA. Validity of the multi-directional reach test: Morris ME. The high-level mobility assessment tool
a practical measure for limits of stability in older adults. (HiMAT) for traumatic brain injury, Part 1: item genera-
J Gerontol A Biol Sci Med Sci. 2001;56:M248. tion. Brain injury: [BI]. 2005;19:925.
122. Duncan PW, Chandler J, Studenski S, Hughes M, 140. Williams GP, Robertson V, Greenwood KM, Goldie PA,
Prescott B. How do physiological components of balance Morris ME. The high-level mobility assessment tool
affect mobility in elderly men? Arch Phys Med Rehabil. (HiMAT) for traumatic brain injury. Part 2: content valid-
1993;74:1343. ity and discriminability. Brain injury: [BI]. 2005;19:833.
123. Duncan PW, Studenski S, Chandler J, Prescott B. Func- 141. Shumway-Cook A, Baldwin M, Polissar NL, Gruber W.
tional reach: predictive validity in a sample of elderly Predicting the probability for falls in community-
male veterans. Journal of gerontology. 1992;47:M93. dwelling older adults. Phys Ther. 1997;77:812.
124. Duncan PW, Weiner DK, Chandler J, Studenski S. Func- 142. Shumway-Cook A, Gruber W, Baldwin M, Liao S. The
tional reach: a new clinical measure of balance. Journal effect of multidimensional exercises on balance, mobil-
of gerontology. 1990;45:M192. ity, and fall risk in community-dwelling older adults.
125. Weiner DK, Bongiorni DR, Studenski SA, Duncan PW, Phys Ther. 1997;77:46.
Kochersberger GG. Does functional reach improve with 143. Whitney S, Wrisley D, Furman J. Concurrent validity of
rehabilitation? Arch Phys Med Rehabil. 1993;74:796. the Berg Balance Scale and the Dynamic Gait Index in
126. Weiner DK, Duncan PW, Chandler J, Studenski SA. people with vestibular dysfunction. Physiotherapy re-
Functional reach: a marker of physical frailty. Journal of search international : the journal for researchers and
the American Geriatrics Society. 1992;40:203. clinicians in physical therapy. 2003;8:178.
127. Wernick-Robinson M, Krebs DE, Giorgetti MM. Func- 144. Berg K. Balance and its measure in the elderly: a review.
tional reach: does it really measure dynamic balance? Physiotherapy Canada. 1989;41:240.
Arch Phys Med Rehabil. 1999;80:262. 145. Berg KO, Maki BE, Williams JI, Holliday PJ, Wood-
128. King LA, Priest KC, Salarian A, Pierce D, Horak FB. Dauphinee SL. Clinical and laboratory measures of pos-
Comparing the Mini-BESTest with the Berg Balance tural balance in an elderly population. Arch Phys Med
Scale to Evaluate Balance Disorders in Parkinson’s Rehabil. 1992;73:1073.
Disease. Parkinson’s disease. 2012;2012:375. 146. Bogle Thorbahn LD, Newton RA. Use of the Berg Bal-
129. Fukuda T. The stepping test: two phases of the ance Test to predict falls in elderly persons. Phys Ther.
labyrinthine reflex. Acta Otolaryngol. 1959;50:95. 1996;76:576;discussion 584.
130. Horak FB, Nashner LM. Central programming of pos- 147. Lajoie Y, Gallagher SP. Predicting falls within the elderly
tural movements: adaptation to altered support-surface community: comparison of postural sway, reaction time,
configurations. Journal of neurophysiology. 1986; the Berg balance scale and the Activities-specific Bal-
55:1369. ance Confidence (ABC) scale for comparing fallers and
131. Higgins S. Motor skill acquisition. Phys Ther. 1991; non-fallers. Archives of gerontology and geriatrics.
71:123. 2004;38:11.
132. Borel S, Schneider P, Newman CJ. Video analysis soft- 148. Lundin-Olsson L, Nyberg L, Gustafson Y. Attention,
ware increases the interrater reliability of video gait as- frailty, and falls: the effect of a manual task on basic
sessments in children with cerebral palsy. Gait Posture. mobility. Journal of the American Geriatrics Society.
Apr 2011;33(4):727. 1998;46:758.
133. Leddy AL, Crowner BE, Earhart GM. Functional gait 149. Podsiadlo D, Richardson S. The timed “Up & Go”: a test
assessment and balance evaluation liability, validity, of basic functional mobility for frail elderly persons.
sensitivity, and specificity for identifying individuals Journal of the American Geriatrics Society. 1991;39:142.
with Parkinson disease who fall. Phys Ther. Jan 2011; 150. Shumway-Cook A, Woollacott M. Attentional demands
91(1):102. and postural control: the effect of sensory context. J
134. Krebs DE, Edelstein JE, Fishman S. Reliability of obser- Gerontol A Biol Sci Med Sci. 2000;55:M10.
vational kinematic gait analysis. Phys Ther. Jul 1985; 151. Whitney SL, Marchetti GF, Morris LO, Sparto PJ. The
65(7):1027. reliability and validity of the Four Square Step Test for
135. Kerber KA, Enrietto JA, Jacobson KM, Baloh RW. people with balance deficits secondary to a vestibular
Disequilibrium in older people: a prospective study. disorder. Arch Phys Med Rehabil. 2007;88:99.
Neurology. 1998;51:574.
3970_Ch21_359-393 25/06/14 6:05 PM Page 387
152. Dite W, Temple VA. A clinical test of stepping and acute stage after acoustic neuroma resection.
change of direction to identify multiple falling older Otolaryngol Head Neck Surg. 1995;113:77.
adults. Arch Phys Med Rehabil. 2002;83:1566. 156. Szturm T, Ireland DJ, Lessing-Turner M. Comparison
153. Zwergal A, Rettinger N, Frenzel C, Dieterich M, Brandt of different exercise programs in the rehabilitation of
T, Strupp M. A bucket of static vestibular function. patients with chronic peripheral vestibular dysfunction.
Neurology. 2009;72:1689. J Vestib Res. 1994;4:461.
154. Brown KE, Whitney SL, Marchetti GF, Wrisley DM, 157. Topuz O, Topuz B, Ardic FN, Sarhus M, Ogmen G, Ardic
Furman JM. Physical therapy for central vestibular dys- F. Efficacy of vestibular rehabilitation on chronic unilat-
function. Arch Phys Med Rehabil. 2006;87:76. eral vestibular dysfunction. Clinical rehabilitation.
155. Herdman SJ, Clendaniel RA, Mattox DE, Holliday MJ, 2004;18:76.
Niparko JK. Vestibular adaptation exercises and recovery:
3970_Ch21_359-393 25/06/14 6:05 PM Page 388
APPENDIX 21-A
Initial Evaluation Form
Evaluation Pertinent Past Medical History
Initial: Yes No Follow-up: Yes No Do you have:
Date: ____________ Diabetes: Yes No
Patient: _______________ Medical Record #: _______ Heart disease: Yes No
D.O.B. _______ Age: ____ Hypertension: Yes No
Referring physicians and physicians to whom we Headaches: Yes No
should send report (please give addresses): Arthritis: Yes No
Describe the major problem or reason you are seeing us: Migraines Yes No
When did this problem begin? __________________ Neck problems: Yes No
Specifically, do you experience spells of vertigo (a sense Back problems: Yes No
of spinning)? Yes No Pulmonary problems: Yes No
If yes, how long do these spells last? _______________ Weakness or paralysis: Yes No
When was the last time the vertigo occurred? ________ Hearing problems: Yes No
Is the vertigo: If yes, describe _________________________
spontaneous: Yes No Visual problems: Yes No
induced by motion: Yes No If yes, describe _________________________
induced by position changes: Yes No Have you been in an Yes No
Do you experience a sense of being off-balance (disequi- accident?
librium)? Yes No If yes, please describe ____________________
If yes, is the feeling of being off-balance: When did it occur? ______________________
constant: Yes No What medications do you take?
spontaneous: Yes No ______________________________________
induced by motion: Yes No ______________________________________
induced by position changes: Yes No ______________________________________
worse with fatigue: Yes No
worse in the dark: Yes No
Social History
worse outside: Yes No
worse on uneven surfaces: Yes No Do you live alone? Yes No
Does the feeling of being off-balance occur when you are: If No, who lives with you?_______________________
lying down Yes No Do you have stairs in your home? Yes No If yes, how
sitting Yes No many? _______
standing Yes No Do you smoke? Yes No If yes, please indicate how
walking Yes No much per day____________
Do you or have you fallen (to the ground)? Yes No Do you drink alcohol? Yes No If yes, please indi-
If yes, please describe _______________________ cate how much ____________
How often do you fall? __________________________ Do you have trouble sleeping? Yes No
Have you injured yourself? Yes No
If yes, please describe: ______________________
PANAS
Do you or have you had “near falls”? Yes No
(Positive and Negative Affective Scale)1
Do you stumble, stagger, or side-step while
walking? Yes No The scale below consists of a number of words that de-
Do you drift to one side while you walk? Yes No scribe different feelings and emotions. Read each item and
If yes, to which side do you drift? Right Left then mark the appropriate answer in the space next to that
388
3970_Ch21_359-393 25/06/14 6:05 PM Page 389
word. Indicate to what extent you generally feel this ___ Symptoms disrupt performance of both usual work
way—that is, how you feel on the average. Use the duties and outside activities
following scale to record your answers: ___ Am currently on medical leave or had to change jobs
1 2 3 4 5 because of symptoms
very slightly a little moderately quite a bit extremely ___ Have been unable to work for more than 1 year or
or not at all have established permanent disability with compen-
_____ interested _____ irritable _____ jittery _____ sation payments
strong _____ nervous
_____ enthusiastic _____ distressed _____ alert _____ Final Visit
active _____ excited Please pick the one statement from the following list that
_____ ashamed _____ afraid _____ upset _____ best describes how you feel:2
inspired _____ hostile _____ No symptoms remaining at the end of therapy
_____ guilty _____ determined _____ proud _____ _____ Marked improvement remaining at the end of
scared _____ attentive therapy
_____ Mild improvement, definite persistent symptoms at
How would you describe your functional level of activi-
the end of therapy
ties before this problem developed?
_____ No change in symptoms in relation to therapy
______________________________________________
_____ Symptoms worsened with therapy activities on a
persistent basis compared with pretherapy period
Current Functional Status
Are you independent in self-care activities: Yes No Assessment
Can you drive: In the daytime? Yes No In the nighttime?
Subjective Complaints
Yes No
Have you modified your driving habits? If yes, in what PANAS1 Score/significance: ______________________
way? ____________________ Rate the following symptoms from 0 (none) to 10 (as bad
Are you working? Yes No Not applicable If yes, as it can be):
occupation: ____________________ Vertigo: (0–10) _____ Disequilibrium: (0–10) _____
Are you on Medical Disability? Yes No Oscillopsia (0–10) ______
Can you perform all your normal parenting activities?Yes What time of day do you feel best: ______________
No Not applicable worst: ______________
Are you able to: How many times per day do you experience symptoms?
Watch TV comfortably? Yes No ____________
Read? Yes No Major problems: ________________________
Go shopping? Yes No Disability score: _____________ (pre-therapy)
Be in traffic? Yes No _____________ (post-therapy)
Use a computer? Yes No
Motion Sensitivity Quotient:2
Initial Visit: Disability Scale2 __________________
Please pick the one statement from the following list that
best describes how you feel:2 MSQ = {(Total score) × (# of positions with symptoms)}
___ Have negligible symptoms ÷ 20.48.
___ Have bothersome symptoms (Don’t forget to adjust for baseline intensity so MSQ is
___ Perform usual work duties but symptoms interfere based on change in intensity.)
with outside activities MSQ: 0–10 = mild; 11–30 = moderate; 31–100 = severe.
3970_Ch21_359-393 25/06/14 6:05 PM Page 390
390 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
1. Sitting to supine
4. Supine to sitting
5. Left Dix-Hallpike
7. Right Dix-Hallpike
*Duration: 5–10 sec = 1 point; 11–30 sec = 2 points; >30 sec = 3 points.
Caloric Test: __________________________ F. Walk, turn head and count backwards out loud by
____________:
Stance Postural Control Cadence: ____________ Base of support:
A. Alignment eyes open: _______________ ____________
(erect, head still, base of support) Path: Straight? Y N Drifts: R L
B. Self-initiated weight-shifting: _______________ Staggers: Y N Side-steps: Y N
(strategy) G. Walk, turn around rapidly:
C. Reactive responses (sternal shove): ______________ Normal: ____________
(strategy) Has difficulty/loses balance turning right _________
turning left ____________
H. Fall Risk (Dynamic Gait Index or Functional Gait
Balance Tests Assessment): _______________________
A. Romberg: eo ________ ec _______ Normal/
abnormal for age? _________ Functional Gait
B. Sharpened Romberg: eo _____ ec _____ Normal/
abnormal for age? _____ Independent: min/mod/max assist
C. Single leg stance: eo _____ ec _____ Normal/ Dependent: slow, cautious
abnormal for age? ______ Stairs ________ Inclines ________
D. Functional reach: _______(normal ≥12 inches) Uneven surfaces ________ Carpet ________
Gait Subsystems
Assistive devices: ____________ Orthoses? _________ A. ROM:
A. At self-initiated pace: Cervical___________________________________
Speed: ____________ Normal for age? __________ R- UE ________ L- UE ________ R- LE ________
Cadence: ___________ Base of support: _________ L- LE ________
Step length: ____________ (equal, each foot passes B. Strength: R- UE ________ L- UE ________ R- LE
the other) ________ L-LE ________
Arm swing: ____________ C. Soft tissue problems: Y N Location: ________
Head and trunk rotation: ____________ Nature: (spasm?) ________
Path: Straight? Y N Swerves: R L D. Sensation: (vibration, proprioception, kinesthesia)
Staggers: Y N Side-steps: Y N LEs ________
B. As fast as possible: Can perform Cannot perform E. Muscle tone: UEs ______________________ LEs
Speed: ____________ Normal for age? __________ _______________________
Cadence: ___________ Base of support: _________ F. Cerebellar: Finger to nose R ________ L ________
Step length: ____________ (equal, each foot passes Rapid alternating movement: R ________
the other) L ________
Arm swing: ____________ Optic ataxia R ________ L ________
Head and trunk rotation: ____________ Tremor R ________ L ________
Path: Straight? Y N Drifts: R L Heel to shin—looking R ________ L ________
Staggers: Y N Side-steps: Y N Heel to shin—not looking R ________ L ________
C. Gait deviations: (20 foot path, 12 inches wide) Rapid alternating movement R ________ L
________________________ ________
D. Walk, turn head: Can perform Cannot perform G. Pain: Y N Location ______________
Cadence: ____________ Base of support:
____________ Appendix References
Path: Straight? Y N Drifts: R L 1. Watson D, et al. Positive and negative affectivity and their
Staggers: Y N Side-steps: Y N relation to anxiety and depressive disorders. J Abnorm
E. Walk, move head vertically Psychol. 1988;97:346.
Cadence: _________ Base of support: ___________ 2. Shepard NT, et al. Habituation and balance retraining
therapy: a retrospective review. Neurol Clin. 1990;8:459.
Path: Straight? Y N Drifts: R L
Staggers: Y N Side-steps: Y N
3970_Ch21_359-393 25/06/14 6:05 PM Page 392
APPENDIX 21-B
Dizziness Handicap
Inventory1
Name: _________________ Date: _________________ unsteadiness. Please check Yes, No, or Sometimes for
The purpose of this scale is to identify dif ficulties that each question. Answer each question as it pertains to your
you may be experiencing because of your dizziness or dizziness or unsteadiness only.
Yes No Sometimes
E2. Because of your problem, do you feel frustrated? _____ _____ _____
F3. Because of your problem, do you restrict your travel for business _____ _____ _____
or recreation?
P4. Does walking down the aisle of a supermarket increase your _____ _____ _____
problem?
F5. Because of your problem, do you have difficulty getting into _____ _____ _____
or out of bed?
F6. Does your problem significantly restrict your participation in _____ _____ _____
social activities such as going out to dinner, the movies, dancing,
or to parties?
F7. Because of your problem, do you have difficulty reading? _____ _____ _____
P8. Does performing more ambitious activities like sports or _____ _____ _____
dancing or household chores such as sweeping or putting dishes
away increase your problem?
E9. Because of your problem, are you afraid to leave your home _____ _____ _____
without having someone accompany you?
E10. Because of your problem, are you embarrassed in front of others? _____ _____ _____
P11. Do quick movements of your head increase your problem? _____ _____ _____
F12. Because of your problem, do you avoid heights? _____ _____ _____
P13. Does turning over in bed increase your problem? _____ _____ _____
392
3970_Ch21_359-393 25/06/14 6:05 PM Page 393
Yes No Sometimes
F14. Because of your problem, is it difficult for you to do strenuous _____ _____ _____
housework or yardwork?
E15. Because of your problem, are you afraid people may think you _____ _____ _____
are intoxicated?
F16. Because of your problem, is it difficult for you to walk by _____ _____ _____
yourself?
P17. Does walking down a sidewalk increase your problem? _____ _____ _____
E18. Because of your problem, is it difficult for you to concentrate? _____ _____ _____
F19. Because of your problem, is it difficult for you to walk around _____ _____ _____
your house in the dark?
E20. Because of your problem, are you afraid to stay home alone? _____ _____ _____
E21. Because of your problem, do you feel handicapped? _____ _____ _____
E22. Has your problem placed stress on your relationships with _____ _____ _____
members of your family or friends?
E23. Because of your problem, are you depressed? _____ _____ _____
F24. Does your problem interfere with your job or household _____ _____ _____
responsibilities?
P25. Does bending over increase your problem? _____ _____ _____
Appendix Reference
1. Jacobson GP, Newman CW. The development of the dizziness
handicap inventory. Arch Otolaryngol Head Neck Surg.
1990;116:424. Copyright © 1990 The American Medical
Association.
3970_Ch22_394-431 25/06/14 12:31 PM Page 394
CHAPTER 22
Physical Therapy
Treatment of
Vestibular
Hypofunction
Susan J. Herdman, PT, PhD, FAPTA ■
Susan L. Whitney, DPT, PhD, NCS, ATC, FAPTA
Vestibular rehabilitation is considered an appropriate and the patient’s overall general physical condition, (5) enable
valuable treatment approach for patients with v estibular the patient to return to a more normal level of activity and
hypofunction. This chapter provides the reader with the participation in society, and (6) reduce the patient’s social
background necessary to treat patients with vestibular hy- isolation. Patients are usually seen by the physical thera-
pofunction. The chapter covers mechanisms of reco very pist on an outpatient basis, although the initial interv en-
as the basis for the exercise approaches used and similar- tions often occur while the patient is in the hospital.
ities and differences among the v arious treatments and Several centers within the United States and England em-
guidelines for the progression of the exercises. We provide ploy physical therapists who screen for vestibular dysfunc-
a review of literature that supports the use of these e xer- tion in the emer gency room. An important part of the
cises. Finally, we provide case studies to illustrate the de- rehabilitation process is the establishment of a home e x-
cision-making process in developing exercise programs. ercise program. The physical therapist must motivate the
patient and ensure e xercise compliance. To do so, the
The previously used nomenclature to describe the
physical therapist must identify the patient’ s own goals
exercises used in the treatment of v estibular hypo-
and clarify to the patient the treatment goals as well as the
function needs to be revised in light of recent find-
potential effects of exercise.
ings on the mechanisms underlying improvement in
physical function. The previously described “Adap-
tation” and “Substitution” e xercises are together
called “Gaze Stabilization” exercises. Mechanisms of Recovery
Several different mechanisms are involved in the recovery
of function following unilateral vestibular loss (UVL).
Goals of Treatment These mechanisms include cellular recovery, spontaneous
The goals of physical therap y intervention are to (1) de- reestablishment of the tonic-firing rate centrally, adapta-
crease the patient’s disequilibrium (sense of being off-bal- tion of residual vestibular function, the substitution of al-
ance) and oscillopsia (visual blurring during head ternative strategies for the loss of vestibular function, and
movement), (2) improve the patient’s functional balance habituation of unpleasant sensations. The following sec-
especially during ambulation, (3) improve the patient’s tion relates the changes that are seen follo wing UVL to
ability to see clearly during head movement, (4) improve the mechanisms of recovery.
394
3970_Ch22_394-431 25/06/14 12:31 PM Page 395
396 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
section presents a brief o verview of some of the mecha- dark. At an extreme, some patients may modify their be-
nisms that contribute to the impro vement in function in havior to avoid situations in which visual or somatosen-
patients with vestibular hypofunction. For more details, sory cues are diminished, such as going out at night.
see Chapters 2 and 9. These mechanisms do not adequately substitute for the
It was initially believed that the recovery of the signs lost vestibulo-ocular function, which functions across fre-
and symptoms associated with unilateral vestibular hypo- quencies of 8 Hz or more25,26 for activities such as walking
function or loss was due solely to the adaptive capability and running and gaze stabilization during unpredictable and
of the vestibular system—that is, the ability of the vestibu- predictable head movements. Preprogrammed saccades and
lar system to make long-term changes in the neuronal re- anticipatory eye movements occur primarily with pre-
sponse to input. Several studies have demonstrated that dictable head movements and not during unpredictable head
adaptation can be induced during the acute stage after movements. Other types of eye movements do not function
UVL. Pfaltz16 used optokinetic stimulations and increased across the necessary frequency range (Fig. 22.2). F or ex-
VOR gain in patients with UVL compared with untreated ample, pursuit eye movements are limited to less than 1 Hz
patients. Szturm et al 17 reported increased VOR gain in and a maximum eye velocity of 60 degrees per second. 27
patients following a course of vestibular adaptation exer- Saccadic eye movements would not be a particularly useful
cises but not in a control group. The primary signal for in- alternative for a poor VOR, because patients would not be
ducing vestibular adaptation is retinal slip, or the able to see the tar get clearly during the actual e ye move-
movement of a visual image across the retina. 18 This slip ments.28 The cervico-ocular reflex also does not operate in
results in an error signal that the brain attempts to mini- the appropriate frequency range, and well-controlled studies
mize by increasing the gain of the v estibular responses have failed to identify a cervico-ocular reflex in which the
(see Chapter 2). However, adaptation is probably not the eye movements are in the compensatory direction.29,30 Sim-
only mechanism behind recovery in patients with vestibu- ilar limitations exist for the substitution of somatosensory
lar hypofunction.19 Recent research suggests that the sub- and visual cues for lost v estibular function (Fig. 22.3).
stitution of alternati ve strategies may be the basis for Again, the vestibular system operates through a wider fre-
functional recovery (see Chapter 9). Enhancement of gaze quency and velocity range than do vision and somatosen-
stability and dynamic visual acuity during predictable sation.25,26,31-33
head movement is believed to be from central preprogram-
ming, but during passive head movements, adaptation may
be the primary mechanism of impro vement.19,20 For ex-
ample, patients with vestibular hypofunction may make a
saccade during the head thrust itself. These prepro-
grammed saccades occur at a latenc y that is too short to
be voluntary or reflexive21 and are not present in normal
subjects.22 There is evidence that they can be “uncovered”
by making the amplitude of the head thrust unpre-
dictable.23 Another mechanism that has been described is
anticipatory slow-phase eye movement. These slow-phase
eye movements are initiated more than 5 milliseconds
(ms) before the initiation of predictable head thrusts, are
in the appropriate direction for the direction of the head
movement, and are initiated centrally . Other slow-phase
eye movements probably are initiated by the intact
vestibular system, based on the latenc y to onset of these
eye movements (less than 10 ms after the head thrust),
which is within the range for the VOR.24
Recovery of postural stability may be caused by the Figure 22.2 Frequency range over which the COR,
use of visual and somatosensory cues instead of remaining smooth-pursuit eye movements, and the VOR can contribute
vestibular cues. Although the substitution of visual or so- to gaze stability compared with the frequency and velocity
matosensory cues as a strategy may provide sufficient in- ranges for daily activities, walking, and running. Only the
normal VOR operates over the frequency and velocity ranges
formation for postural stability in man y situations, the of normal activities. (Modified from Herdman SJ. The role of
patient will be at a disadv antage if trying to w alk when adaptation in vestibular rehabilitation. From Otolaryngol
those cues are inaccurate or not a vailable, such as in the Head Neck Surg. 1998;119:49-54, with permission.)
3970_Ch22_394-431 25/06/14 12:31 PM Page 397
Treatment Approaches
Several different approaches ha ve been adv ocated in
the management of patients with vestibular hypofunction.
Three different approaches—gaze stabilization exercises,
habituation exercises for the reduction of symptomatic
complaints, and postural stabilization exercises—are pre-
Figure 22.3 Frequency ranges over which somatosensory, sented. A summary and comparison of these different ex-
visual, semicircular canal, and otolith inputs contribute to ercise approaches (T able 22-1) sho ws that there are
postural stability. This information has been determined elements common to all. Case studies are used to demon-
only for stability during quiet stance and following sudden
perturbations. (Modified from Herdman SJ. The role of strate the basis for specific exercises used in treatment and
adaptation in vestibular rehabilitation. From Otolaryngol the progression of the patient’s exercise program.
Head Neck Surg. 1998;119:49-54, with permission.)
Gaze Stabilization Exercises
Three different exercises are used to enhance gaze stability
Patients may also restrict head mo vements as a in patients with vestibular hypofunction. In all, the chal-
means of seeing clearly or maintaining their balance. lenge is for the e yes to stay on a tar get during a head
This strategy is not particularly desirable, because it movement. The mechanism by which the appropriate eye
would result in limited activity and would not provide a movement is generated varies from patient to patient. The
mechanism for seeing clearly or for maintaining balance first exercise is based on ha ving the patient attempt to
during head movements. Restricting head mo vements maintain fixation on a target while moving his or her head
can also lead to musculosk eletal impairments, which (Figure 22.4). These exercises were originally based on
serve to compound the acti vity limitations from the inducing adaptation of residual vestibular function by cre-
vestibular deficit. ating a small amount of retinal slip. The best stimuli
■ Table 22-1 COMPARISON OF DIFFERENT EXERCISE APPROACHES FOR THE PATIENT WITH
A PERIPHERAL VESTIBULAR DISORDER
Movement Gaze Stabilization Postural Stabilization Habituation
398 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
appear to be those that incorporate movement of the head (e.g., X and Z) are placed on a w all about 2 feet apart
and a visual input. Optokinetic stimulation (movement of (the two targets are placed close enough together that
visual world only) by itself also can increase the gain when the patient is looking directly at one, he/she can
of the vestibular system, although perhaps not be as effec- see the other tar get out of the corner in the periphery).
tively as head movement combined with a visual stimu- The patient is instructed to look directly at the X, being
lus.18,34-36 Nevertheless, optokinetic stimuli ha ve been sure that the head is also lined up with the X (the nose
used in the treatment of patients with vestibular hypofunc- should point at the X). Then the patient shifts gaze to the
tion16 or with chronic vestibular symptoms.37 other target, keeping the head still. The patient turns
Although there is e vidence that these e xercises do his/her head toward the second tar get with the goal of
enhance recovery, mechanisms other than adaptation keeping the target in focus. In patients with a poor or no
may underlie the improved gaze stability. The second ex- VOR, other mechanisms must de velop if the e yes are
ercise involves repeated eye and then head mo vements to remain on target during the head movement. Presum-
between two targets with the goal of maintaining fixation ably, in this exercise, the underlying mechanism is central
on the tar get during the head mo vement. Two letters preprogramming.
3970_Ch22_394-431 25/06/14 12:31 PM Page 399
The third exercise involves imagining fixation on a Cawthorne was treating patients with unilateral vestibu-
stationary target during a head movement performed with lar deficits and postconcussive disorders. In conjunction
eyes closed. In this exercise, called the remembered target with Cooksey, Cawthorne developed a series of e xer-
exercise, the patient looks at a tar get placed directly in cises that addressed their patients’ complaints of vertigo
front of him/her. Then the patient closes his/her eyes and, and impaired balance. The Cawthorne-Cooksey exer-
while trying to keep the eyes on the remembered target lo- cises include pursuit and saccadic e ye movements,
cation, turns the head. The patient then opens the eyes to movements of the head, tasks requiring coordination of
see if he/she is looking at the tar get. The exercise is re- eyes with the head, total body movements, and balance
peated with the head starting in the center position. This tasks (Box 22-1). Ca wthorne and Cookse y recom-
exercise may enhance the use of cervical inputs to gener- mended that the exercises be performed in v arious po-
ate the eye movement that will keep the eye on the target, sitions and at various speeds of movement. In addition,
or it may enhance cortical co-acti vation, producing the patients were required to perform the e xercises with
head movement and the eye movement. their eyes open and closed. According to Cawthorne and
Cooksey,38,39 performing the e xercises with the e yes
closed decreased the patient’s reliance on visual infor-
Habituation Exercises mation and possibly forced more effective compensation
These exercises are based on the concept that repeated by vestibular and somatosensory mechanisms. Addition-
exposure to a pro vocative stimulus will result in a re- ally, patients were trained to function in noisy and
duction in the pathological response to that treatment. crowded environments. To encourage active participa-
The first to develop exercises based on habituation were tion, Cawthorne and Cooksey had patients exercise to-
Cawthorne and Cooksey38,39 in the 1940s. At the time, gether in daily group sessions. Cawthorne and Cooksey
Box 22-1
Source: Cawthorne-Cooksey exercises for patients with vestibular hypofunction. Reprinted with permission
from Dix, MR. The rationale and technique of head exercises in the treatment of vertigo. Acta Oto-rhino-laryng
(Belg). 33;370:1979.
3970_Ch22_394-431 25/06/14 12:31 PM Page 400
400 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
believed a group e xercise format would be more eco- Paroxysmal Positional Vertigo (BPPV). Calculation of
nomical and more fun for the patients, and would make the MSQ score involves:
it easier to identify a malingerer. Hecker et al40 used the
• For each of the sixteen movements, the patient
Cawthorne-Cooksey exercises to treat a group of pa-
rates the intensity of symptoms on a scale of
tients with vestibular disorders and reported that 84% of
0 to 5 after the movement is completed.
the patients responded favorably. They also emphasized
• The therapist calculates the number of seconds
the importance of performing the exercises regularly.40
until the patient’s symptoms return to baseline
In addition, they noted that emotional stress seemed to
and applies the following criteria: less than
affect the patient’s progress.
5 seconds = a score of 0; 5 to 10 seconds = a
In the 1980s, Norre 41,42 proposed a different series
score of 1, 11 to 30 seconds is given a score of 2,
of exercises for v estibular habituation training in the
and greater than 30 seconds is given a score of 3.
treatment of patients with unilateral peripheral vestibular
• The Intensity + Duration scores for all 16 move-
loss. According to these investigators, an asymmetry in
ments is summed (added across Columns 1 and 2)
labyrinth function results in a “sensory mismatch. ” The
and written down in Column 3.
disturbed vestibular signal produces an input to the brain
• The numbers in Column 3 are added. That sum is
that conflicts with information received from intact visual
multiplied by the number of positions that cause
and somatosensory systems. This conflict, they believed,
an increase of symptoms.
produced the symptoms experienced by patients with uni-
• The results of that multiplication are divided by
lateral peripheral vestibular loss.
20.48 for the final score.
More recently, habituation exercises are based on
the Motion Sensitivity Quotient (MSQ) as a means for If the final score is 0 to 10, it indicates a mild motion
evaluating initial problems and documenting out- sensitivity, 11 to 30 a moderate motion sensitivity, and 31
come.43 The MSQ, developed by Shepard and Telian, to 100 a severe motion sensitivity.
uses a series of mo vements and positions as the basis In the Habituation approach, up to four movements
for establishing an indi vidualized exercise program are chosen from the MSQ results to form the basis for
for patients with chronic unilateral vestibular hypofunc- the exercises. The patient performs these movements 2
tion (Table 22-2).43-45 Note that the Dix-Hallpike posi- or 3 times, twice a day . It is important that the patient
tion is part of the MSQ; it is important to realize that perform the mo vements quickly enough and through
the MSQ is not used in patients who ha ve Benign sufficient range to produce mild to moderate symptoms.
■ Table 22-2 MOTION SENSITIVITY QUOTIENT TEST FOR ASSESSING PATIENTS WITH
DIZZINESS*
Baseline Symptoms Intensity Duration Score
1. Sitting to supine
4. Supine to sitting
5. Left Dix-Hallpike
7. Right Dix-Hallpike
■ Table 22-2 MOTION SENSITIVITY QUOTIENT TEST FOR ASSESSING PATIENTS WITH
DIZZINESS*—cont’d
Baseline Symptoms Intensity Duration Score
*MSQ = {(Total score) × (# of positions with symptoms)} + 20.48 MSQ score 0–10 + mild; 11–30 = moderate;
31–100 = severe. Duration: 5–10 sec + 1 point; 11–30 sec = 2 points; >30 sec = 3 points.
Source: From Shepard NT, Telian SA. Programmatic vestibular rehabilitation. Otolaryngol Head Neck Surg.
1995;112:173.45
As habituation occurs, the movements can be performed by having the person walk with a more narrow base of sup-
more rigorously. The patient should rest between each port, by adding head mo vement, or with unpredictable
movement for the symptoms to stop. The symptoms changes in direction of w alking. The primary concerns
should decrease within a minute after each e xercise or when developing an exercise program to improve postural
within 15 to 30 minutes after all exercises have been per- stability is how to challenge the patient’s balance without
formed. It may take 4 weeks for the symptoms to begin causing the patient to f all. Fall risk should be determined
to decrease. The exercises may be performed for a week before choosing the most appropriate exercises for a person
to 2 months before they are modified. with postural control deficits.
The habituation approach is not advocated for all pa-
tients. The elderly, especially, should not perform mo ve-
ments in which the y rise quickly. Precautions include Treatment
orthostatic hypotension and orthostatic intolerance. The General Considerations
habituation approach is often not tolerated well, because
it takes time to decrease the symptoms, does not work on 1. Treatment should begin early. Most evidence
all patients, and compliance is dif ficult because of the suggests that patients will still improve even
symptoms that are exacerbated with the exercises. If treat- with long periods of time between the onset of
ment fails, counseling is advisable regarding changing ac- the vestibular hypofunction to the initiation of
tivities or reorganizing the work area. exercises.46,47 Logically, however, it is safer for
the patient if fall risk can be decreased as
quickly as possible. Furthermore, there is evi-
Postural Stabilization Exercises
dence that early intervention with vestibular ex-
Exercises should synthesize the use of visual and so- ercises facilitates a decrease in symptoms and
matosensory cues with the use of v estibular cues as well improves gait stability compared with no exer-
as the possibility of central preprogramming to impro ve cise in patients post resection of vestibular
postural stability. For example, balance exercises should schwannoma.48-50 In a prospective, randomized
“stress” the system by ha ving the patient w ork with and controlled trial (n = 53), an early customized
without visual cues or while altering somatosensory cues vestibular rehabilitation exercise program in
by having the patient stand on foam. Removing or altering older adults (age greater than 50 years) post
cues forces the patient to use the remaining sensory cues. acoustic neuroma resection was more effective at
Thus, if the patient is ask ed to stand on foam with e yes enhancing postural control at 3 months and was
closed, the use of vestibular cues will be fostered. The in- maintained at 1 year compared with those who
tensity of balance exercises while walking can be increased were provided general instructions.49 In another
3970_Ch22_394-431 25/06/14 12:31 PM Page 402
402 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
recent randomized trial in 40 persons with an Nevertheless, patients should be told that dur-
acute vestibular disorder, Teggi et al reported ing physical therapy, there might be a period
that early vestibular exercises resulted in better when they may feel worse before they feel
Dizziness Handicap Inventory scores, less anxi- better. To assist the patient through this period,
ety, less reliance on visual cues, and better walk- the physical therapist should be accessible. For
ing, as assessed by the Dynamic Gait Index.50 example, the patient should be instructed to
The exercise group means were all “better” than telephone the therapist if the symptoms be-
the control subjects group outcome means at come severe or long lasting. In such instances,
25 days post onset of the exercise program. Both the physical therapist determines if the exer-
studies suggest that the use of a supervised exer- cises can be modified or if the exercises
cise program can enhance outcomes in should be discontinued until the patient is for-
persons with vestibular disorders. mally reevaluated. Excessive exacerbation of
2. Exercise can be for brief periods of time ini- the patient’s symptoms can also be avoided by
tially. Pfaltz’s study16 is important for showing careful exercise prescription. Initially, the pa-
that even brief periods of stimulation can pro- tient may be provided with only a few key
duce VOR gain changes that would be particu- exercises. The patient is instructed to attempt
larly useful in the treatment of patients during the exercises 3 to 5 times per day; the number
the acute stage of recovery. of repetitions is based on the therapist’s as-
3. Patients with chronic peripheral vestibular sessment of the patient’s exercise tolerance.
deficits may have limited their movements, or It is a good idea to have the patient perform all
at least their head movements, in an attempt to exercises completely during the clinic visit in
avoid precipitating the symptoms of dizziness order to assess the response to the exercises. In
and disequilibrium. Head movements must be some ways, the increase in symptoms is good,
encouraged in these patients both to induce im- because there is some evidence that perform-
proved function and to habituate the symptoms ing these exercises will result in a decrease in
provoked by movement. symptom intensity over the course of several
4. The goal for each gaze stabilization exercise weeks.43-45,47,48,51 However, if the increase in
is to maintain fixation on a target. In the X1 intensity is great or if it persists for longer
and X2 viewing paradigms, the patient is than 10 to 20 minutes after the exercise is fin-
asked to move the head at a rate that is at the ished, the patient may avoid performing the
top of their ability to see clearly (Fig. 22.4). exercise or he/she may be less active for the
In fact, there should be a slight blurring of rest of the day. Patients who become
the target image indicating that there is some excessively “dizzy” while performing the
retinal slip. As mentioned before, the best exercises may even refuse to continue with
stimulus to induce adaptation is one produc- rehabilitation.
ing an error signal that the central nervous 6. For optimal recovery, exercises must stress the
system attempts to reduce by modifying the system in different ways.46 For example, adapta-
gain of the remaining vestibular function. tion of the vestibular system is frequency de-
In the eye-head movement, the patient must pendent.52,53 If the system is adapted at a
be reminded that the goal is to see clearly as specific frequency, gain will improve most at
the head moves to the target. Finally, in the that frequency. Because normal movement oc-
remembered target paradigm, the patient’s curs over a wide range of frequencies of head
goal is to see the target clearly when he/she movement, the patient should perform the head
open the eyes. movement exercises at many different frequen-
5. Exercises may cause an increase in the inten- cies for optimal effects. Different head positions
sity of the patient’s dizziness and disequilib- can also be used to vary the exercise. Patients
rium. This is because the exercises involve need to be instructed to gradually increase the
head movement, which the patient has been speed of their head movements either from
avoiding, because moving the head provokes exercise session to exercise session or within a
the patient’s dizziness. This situation may be session. This creates a challenge to the central
threatening to patients who are extremely nervous system and may improve the effective-
fearful of experiencing their symptoms. ness of the exercise.53
3970_Ch22_394-431 25/06/14 12:31 PM Page 403
404 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
control. The general treatment progression includes the the acute stage following unilateral vestibular loss. In this
following: stage, the patient may complain of severe vertigo and may
be nauseated and v omiting. Head movement will make
1. Increasing and alternating the speed of the
these symptoms worse and the patient usually prefers to lie
exercises
quietly, often in a dark ened room or with e yes closed. At
2. Performing exercises in various positions and
this stage, the patient may also be taking medications to
activities (i.e., head movements performed while
suppress these vegetative responses and may be receiving
sitting, then standing, during walking)
intravenous fluid replacement. Slo w, easy head mo ve-
3. Performing exercises in situations of decreasing
ments, such as turning the head to look at someone, should
visual and/or somatosensory input (i.e., balance
be encouraged first. Good visual inputs (bright room lights,
exercises with eyes open and eyes closed, walk-
curtains open, television on) also should be encouraged
ing with eyes closed)
during the first days after the acute onset of a v estibular
4. Performing balance exercises while distracted
deficit. Getting up out of bed may require assistance and
(e.g., mental tasks)57
sometimes an assistive device, because many people are
5. Exposing the patient to a variety of task and en-
unstable early after an acute vestibular event.
vironmental situations and contexts (i.e., walk-
After 1 to 3 days, the symptoms of nausea and vertigo
ing in the home to walking at a shopping mall)
should have diminished or resolved, and the spontaneous
nystagmus should be decreasing as the resting state of the
Problem: Visual Blurring and Dizziness vestibular neurons recovers. Patients can begin exercises to
When Performing Tasks that Require facilitate gaze stabilization as early as 1 to 3 days after the
Visual Tracking or Head Stabilization onset of the vestibular loss using gentle, active head move-
Visual blurring and dizziness when performing tasks that ment. The X1 viewing paradigm exercise with horizontal
require visual tracking or gaze stabilization during head head movement would be an appropriate starting point. The
movements is most likely a result of decreased VOR gain exercise would be performed while fixating a small (foveal),
resulting in visual blurring during head movement and also stationary target for 1 minute followed by a period of rest
a visual-vestibular sensory mismatch. Some caution should and would be done 5 times/day (see Fig. 22.4 and
be taken when gaze stabilization exercises are used during Box 22-3).
Box 22-2
Box 22-2
The next stage would be to add performing the exer- the exercises can be expanded to include use of a full-field
cise using vertical head movements. As the patient im- stimulus (checkerboard) in addition to the small target he
proves, he or she should try to perform the e xercises for or she had been using. Within 1 or 2 weeks after onset,
up to 2 minutes each. Although the patient may complain patients can be gin the gaze stabilization e xercises that
of increased dizziness or disequilibrium with head move- require them to maintain fixation on a visual target that is
ments, neither is a reason to stop the e xercises unless, as moving in the opposite direction as their head movement
mentioned earlier, the symptoms persist for 10 to 20 min- (X2 viewing; see Fig. 22.4 and Box 22-3). This exercise
utes or more each time the patient performs the e xercise. should be performed with smaller head mo vements (and
Vomiting or significant nausea, however, would be reasons comparably small target movements), because the tar get
for terminating or modifying the exercises. cannot be kept in focus while vie wing out of the corner
VOR gain in the acute stage after unilateral vestibular of an eye. The head movements may have to be slower
loss is poor (0.25 to 0.5), and relatively slow head veloci- as well for the patient to maintain f ixation. Both the X1
ties and low frequencies should be used so that the patient and X2 viewing paradigms should be performed at in-
can keep the visual tar get in focus at all times. As the creasing head velocities as the patient impro ves. Within
patient improves (within a few days to a week or more), 2 or 3 days after onset, patients can be gin to perform the
3970_Ch22_394-431 25/06/14 12:31 PM Page 406
406 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
gaze stabilization exercises while standing, as a prepara- 3 to 5 times. It is particularly important that the initial
tion for turning the head while walking. The eye-head ex- prescription of these exercises should avoid those move-
ercise and the remembered target exercise are added to the ments/positions that produce se vere symptoms. Man y
patient’s exercise program as he or she progresses. therapists have experienced that too aggressi ve an ap-
Ultimately, the eye-head exercise should be incorpo- proach may lead to patient noncompliance. Instead, ther-
rated into gait and other functional activities. Patients with apists should select movements and positions that produce
vestibular deficits should also be instructed to perform a moderate level of symptoms.
functional tasks or games that require visual tracking or Attempts are also made to include habituation e xer-
gaze fixation. For example, laser tag requires the patient to cises into the patient’s daily routine. For example, the pa-
move the head while focusing the eyes on a moving target. tient is instructed to incorporate neck diagonals into the
The Wii, discussed in Chapter 28 has games that incorpo- task of loading and unloading the dishw asher. This task
rate eye-head tracking activities that can be incorporated requires the patient to focus on the object and mo ve the
into the treatment program. Bouncing and catching a ball body, head, and arm synchronously to either pick up or
may be another appropriate task for some patients.The pa- place the object on a high shelf.
tient could be advised to bounce the ball off the floor, wall,
and/or ceiling in an attempt to v ary the task by changing Problem: Static and Dynamic
direction of object motion and/or neck position. Alterna- Postural Instability
tively, the patient can play kickball against a w all, which The balance and gait exercises prescribed for a patient are
would require following the ball with e yes and head and based on the problems identif ied during assessment and
rapid shifts in balance. Using multicolored or highly pat- will vary considerably depending on patient history and
terned balls may also increase task dif ficulty, because the medical diagnosis. Recovery from unilateral v estibular
moving pattern or high color contrast may greatly increase neuronitis, labyrinthitis, or from a surgical procedure, such
the patient’s symptoms. Mental activities (counting back- as vestibular nerve section, typically tak es 6 weeks, al-
wards by three or seven) should also be incorporated during though recovery may take up to 6 months in some patients.
standing and gait as the patient improves. Patients with vestibular nerve section, for example, often
Exposing the patient to highly te xtured visual envi- return to work within 3 weeks. Reco very from resection
ronments may also assist in the remediation of visuo- of acoustic neuroma typically takes longer, although most
vestibular interaction deficits. For example, the patient of the recovery occurs within the f irst few weeks. After
may be instructed to gradually perform tasks such as gro- the first 2 or 3 weeks, the main complaints are fatigue, in-
cery shopping or walking through a shopping mall. Opto- stability when turning quickly, and some increased diffi-
kinetic stimulation can be incorporated into the treatment culty walking in the dark. Patients may also complain of
program to simulate complex visual environments.37 greater instability when w alking on uneven surfaces or
when there is a change in light intensity (opening a door
Problem: Exacerbation of Symptoms to the outside or w alking through intermittent shadows,
If a patient experiences exacerbation of symptoms during such as trees).
the head movement assessment, habituation exercises can Although many patients with peripheral v estibular
be incorporated into the e xercise program. Ho wever, hypofunction perform below the norm on static tests of
there is sufficient evidence that the gaze stabilization ex- balance during the acute stage, the most common com-
ercises also result in a decrease in symptom intensity . plaint is imbalance during dynamic acti vities such as
During the physical therap y assessment, positions or walking, especially with head turning. Rarely do these pa-
movements that provoke the patient’s symptoms are iden- tients report an inability to stand on one leg or to walk with
tified based on the results of the Motion Sensiti vity Test eyes closed. Instead, the y may complain of dif ficulty
or during the history taking (see Chapter 21). These walking on an uphill grade, through a cluttered room, or
positions and movements are then incorporated into the into a movie theater. Because of the nature of the patient’s
patient’s exercise program. Initially, if the patient has sig- deficits, balance training should address the dynamic as-
nificant symptoms, habituation e xercises may be modi- pects of gait and be task directed. Balance and gait training
fied so they can be performed in the supine or sitting are inseparable and therefore considered together in this
position. Later, the patient can perform e xercises while discussion.
standing or even while walking. During the habituation Based on the e valuation, the therapist identif ies the
exercises, the patient is instructed to hold the position for patient’s functional balance deficits. Therapeutic exercise
at least 10 seconds, or until the symptoms dissipate. In prescription should address the patient’s specific deficits.
addition, the patient is instructed to perform each exercise For example, a patient may e xperience disequilibrium
3970_Ch22_394-431 25/06/14 12:31 PM Page 407
when the opportunity to use visual and/or somatosensory control system. To overcome this challenge, the patient is
input for balance is minimized (e.g., walking at night). In first instructed to walk down a corridor while moving the
this situation, emphasizing exercises and tasks that require head left and right, or up and down. Later, the patient per-
the patient to focus on vestibular, instead of visual or so- forms the same task, while avoiding objects placed in the
matosensory, input is important. Such e xercises can in- walking path. The most difficult condition would be to per-
clude walking backward, sidestepping, and braiding form this exercise in an area with a comple x visual envi-
performed with the e yes closed, marching in place on ronment (similar to a shopping aisle with people and carts).
foam performed first with the eyes open and later with the The last deficit to be discussed is the dif ficulty pa-
eyes closed (Fig. 22.6 and Box 22-3), and walking across tients with vestibular deficits experience when their gait
an exercise mat or mattress in the dark. is unexpectedly disrupted. One seldom w alks through a
Another functional deficit is the instability e xperi- busy shopping mall without experiencing a sudden head-
enced by patients when faced with situations that require on encounter with another person. Such tasks require the
movements of the head while walking. For instance, many postural control system to respond quickly. In some cases,
patients indicate having difficulty shopping for groceries. the patient may need to impro ve the ability to anticipate
To scan the grocery shelv es for the desired item, the forthcoming events. As indicated in the gait evaluation, an
patient must walk while moving the head left, right, or obstacle course can be devised to assess the patient’s abil-
diagonally. At the same time, the patient must continue ity to anticipate or respond quickly to changes in task con-
to monitor the en vironment to prevent a collision with text. The obstacle course can also be used in treatment.
another shopper. As a result, this rather ordinary task cre- The patient should be instructed to v ary the course in as
ates an overwhelming challenge to the patient’ s postural many ways as possible. Having a family member verbally
direct the patient on the path to follow is helpful with ver-
bal cueing for sudden changes of direction during amb u-
lation. Commands are gi ven at the moment the patient
must encounter or avoid an obstacle, thereby maintaining
a level of task uncertainty. Another task that requires the
patient to respond quickly to e xternally imposed con-
straints is walking and pivoting to the left or right. Again,
a family member directs the patient on when and in what
direction to pivot. Family members can also quickly give
the command to “stop.”
Patients with vestibular disorders can experience dif-
ficulty with many different balance and gait tasks. This
discussion considered only a few. With a thorough evalu-
ation, the therapist may identify the patient’ s specific
motor control problem. In such cases, the therapy program
should not be limited to specific balance or gait exercises.
Instead, the therapist should provide the patient with bal-
ance and gait activities that challenge the patient’s postural
control system in a v ariety of ways in different environ-
ments and on various surface areas to maximally challenge
the patient’s abilities.
408 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Box 22-3
increased sway. Gait will be grossly ataxic for the f irst through a series of e xercises that stress their balance by
week, but patients should be walking independently, albeit gradually decreasing their base of support or by altering
with a widened base of support, within 1 week. During visual and somatosensory cues. Even if they are unable to
this initial stage of recovery, several different balance and maintain the position successfully for the required period
gait exercises are appropriate. Goals include increasing of time, practicing will impro ve their balance. P atients
the patient’s endurance while walking, improving stability with complete unilateral v estibular loss, however, rarely
while standing with a more narro w base of support perform the sharpened Romberg with eyes closed at any
(Romberg position) with eyes open and closed, and begin- age. More difficult dynamic balance exercises may include
ning to turn the head while walking. Exercises to improve walking and turning suddenly or walking in a circle while
balance in sitting or other positions are usually not neces- gradually decreasing the circumference of the circle, first
sary, but for postoperative patients, bending over must be in one direction and then in the other . The patient needs
avoided for several weeks. the practice of walking in different environments, such as
Gait exercises can be more challenging for patients on grass, in malls (walking in an empty mall is easier than
with chronic v estibular disorders, although, again, the in a crowded mall, walking with the crowd is easier than
starting point depends on the problems identif ied during against the crowd), and walking at night. Precautions to
the assessment (see Box 22-2). P atients can be tak en prevent falls should always be taken until the patient no
3970_Ch22_394-431 25/06/14 12:31 PM Page 409
longer needs them, but it is important to avoid letting the walking program to other situations and contexts. Walk-
patient become dependent on assisti ve devices for walk- ing in a park and at a shopping mall are frequently rec-
ing. Assistive devices may only be necessary the first few ommended as the patient impro ves. When walking in
days after the vestibular event but are rarely used later in these situations, patients are advised to e xperience as
the rehabilitation process. many challenges as possible. For example, riding an es-
calator in a shopping mall may pro vide an interesting
Problem: Physical Deconditioning challenge to the patient. The patient must remain bal-
Physical deconditioning because of inacti vity may be a anced while standing on a moving support surface. In ad-
significant problem for many patients with UVL. Many dition, the motion of other people toward or to the side of
patients are advised to begin a regular walking program. the patient may create a sense of dizziness or imbalance,
The purpose of the walking program is twofold: first, to enhancing the difficulty of the task. Such challenges are
prevent deconditioning of the patient; second, to provide necessary to overcome if the patient is to manage safely
realistic balance challenges to the patient’ s central ner - in a variety of contexts without experiencing an exacer-
vous system. Tasks such as w alking on uneven terrain, bation of symptoms.
walking through a shopping mall, or crossing the street Patients can also be encouraged to return to other ac-
challenge the patient in w ays that cannot be simulated tivities, such as tennis or golf, which will help impro ve
by a therapeutic e xercise program (Fig. 22.7). When their overall fitness. These activities need to be added
crossing the street, the patient must conform to the tem- gradually. Activities such as using a stationary bik e, al-
poral constraints imposed by mo ving vehicles. Specifi- though it should help impro ve fitness, will not help im-
cally, the patient must determine at what moment to step prove postural stability e xcept indirectly by increasing
off the curb to avoid confronting a vehicle. When cross- strength or range of motion. Swimming can be safely per-
ing the street at a busy intersection, this requirement be- formed by patients with UVL and is a good f itness exer-
comes more difficult to fulfill. In addition, the patient’s cise. If the patients w ant to return to ocean swimming,
postural control system must make quick adjustments to they should be advised that the y might have some diffi-
offset perturbations caused by changes in terrain or mo- culty initially walking on the sand or standing on the sand
tion of other people. in the water. (Patients with bilateral v estibular loss must
The initial program requires the patient to w alk for be more cautious because, without visual cues, the y will
15 to 20 minutes four or more times per week. Ov er the have difficulty knowing “which way is up” when under-
subsequent weeks, the patient is instructed to increase to water. Ocean swimming in particular may not be advis-
a 30-minute walk. Initially, the patient may be advised to able. Swimming with goggles will help, but not in murky
walk in a f amiliar environment with fe w challenges. water.) For all patients, the precautions we all should fol-
Later, the therapist encourages the patient to e xpand the low need to be observed: never swim alone.
410 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Problem: Return to Driving additional information related to dri ving and vestibular
One of the more commonly ask ed questions is when the disorders.
patient may begin to drive again. The legal ramifications
may vary from state to state, but essentially patients should Information the Physical Therapist
not drive if they cannot see clearly during head movements
or if head mo vements result in significant dizziness (or
Should Send the Physician
disorientation). One guideline, that patients should be able The physical therapy evaluation should be aimed at iden-
to see clearly when making rapid and abrupt head mo ve- tifying the specific problems that patients with vestibular
ments, can be tested using the dynamic visual acuity test. hypofunction often have (Table 22-3). Once the problems
If a patient decides to return to dri ving, he or she should have been identified, the actual treatment plan is de vel-
be encouraged to begin on quiet, local streets or in a park- oped with an emphasis on the home e xercise program.
ing lot when it is empty . Driving at night and dri ving on Reevaluation should occur mid-rehabilitation process and
high-speed roads should be delayed until the patient is again at the end of the rehabilitation process.The referring
comfortable with the quieter roads. Drivers’ training may physician therefore should be provided with objective as-
be beneficial but may or may not be co vered through in- sessment results that show whether or not progress has oc-
surance. It is somewhat controversial as to whether per - curred. With the electronic medical record, sending reports
sons with bilateral vestibular hypofunction should drive. to the physician hopefully becomes easier . Continued
A recent report suggests that persons with bilateral loss communication, especially if the patient is being managed
are safe to drive, yet patients have reported reductions in with a pharmacological intervention, is very helpful to the
their perceived ability to dri ve.59,60 See Chapter 7 for referring physician. Adjustments in the medication can be
■ Table 22-3 SPECIFIC PROBLEMS AND APPROPRIATE MEASUREMENT TOOL (SEE CHAPTER
21 FOR DETAILS)
Potential Problem Measurement Tool
Subjective Complaints
Dizziness with head movement Visual analogue scale – 1 minute of head movement
Low confidence in balance Activities Specific Balance Confidence Scale (ABC), Falls
Efficacy Scale,61 or the Falls Efficacy Scale International62
Decreased walking speed Timed walking at preferred speed compared with age and gender norms
Poor physical condition 6-minute walk test; Heart Rate, Respiratory Rate
more easily made if symptom reports are objecti vely improved. Again, quantified data should be
reported to the physician. presented.
The goals of physical therap y intervention are to 2. The number of clinical visits/week and the
(1) decrease the patient’s disequilibrium (sense of being number of weeks that physical therapy will be
off-balance) and oscillopsia (visual blurring during head required.
movement), (2) improve the patient’s functional balance
Final note should:
especially during ambulation, (3) improve the patient’s
ability to see clearly during head movement, (4) improve 1. Itemize what goals the patient has achieved.
the patient’s overall general physical condition and activity 2. Provide the data that demonstrates the change
level, (5) enable the patient to return to a more normal (baseline and discharge measures).
level of activity and participation in society, and (6) reduce 3. Explain why the patient is being discharged
the patient’s social isolation. These goals should be di- from physical therapy if the goals have not been
rectly linked to the e xercises and the outcome measures achieved.
used by the therapist.
Patients are usually seen by the physical therapist
on an outpatient basis, although, in some cases, the
Evidence that Exercise Facilitates
initial treatments will occur while the patient is in the Recovery
hospital. An important part of the rehabilitation process Animal studies provided us with the f irst evidence that vi-
is the establishment of a home e xercise program. suomotor experience facilitated the rate of recovery and im-
The physical therapist must motivate the patient and ob- proved the f inal level of reco very following vestibular
tain compliance. To do so, the physical therapist must dysfunction.13-15 Furthermore, several studies suggested that
identify the patient’s own goals and clarify to the patient exercise facilitated the process of vestibular compensation.
the treatment goals as well as the potential ef fects of For example, Igarashi et al 64 found locomotor equilibrium
exercise. compensation occurred faster (7.3 days as compared with
The initial note should contain the following: 13.7 days) in a group of squirrel monkeys exercising in a ro-
1. Quantification of the patient’s subjective tating cage compared with a none xercise group. Similar
complaints and of the results of the examina- findings have been observed in cats follo wing unilateral
tion. At a minimum, there should be one labyrinthectomy.12
measure of subjective complaints, a measure Fortunately, there is now considerable evidence in
of gait speed and of fall risk, and a measure human patients that the use of specific exercises facilitates
of the patient’s ability or inability to partici- the level of recovery in patients with unilateral vestibular
pate in societal activities. Normal values for hypofunction.
age (and gender where appropriate) should Availability of supporting e vidence is important
be included for comparison with the patient’s because supervised physical and occupational
performance, therapy adds to the health care costs of the patient.
2. A list of problems specific for that patient, the Current health care pro viders (insurance compa-
goals for the patient, and a timeframe by which nies) are be ginning to require that treatments
those goals should be met. are supported by e vidence and that continuation
3. The specific exercises the patient will be of patient visits is supported by documentation
performing related to the patient’s goals. of progress through the use of v alid assessment
4. An indication that the patient is expected to tools. It is necessary, therefore, to demonstrate the
perform a home exercise program (HEP). effectiveness of these e xercise approaches in
5. The number of clinical visits/week and the the rehabilitation of patients with v estibular
number of weeks that physical therapy will be hypofunction.
required.
6. The expected ability of the patient to improve A Cochrane Review in 2011 on vestibular rehabil-
should also be included in the note. itation identified six additional studies that compared
vestibular rehabilitation therapy for patients with unilat-
A request for continuation of the therapy should: eral peripheral vestibular hypofunction with sham treat-
1. Show evidence that the patient has shown im- ments, no treatment, and other forms of v estibular
provement toward reaching those goals or gives rehabilitation therapy to the 21 identif ied in the 2007
an explanation as to why the patient has not review.65,66 Exercises used in these articles include
3970_Ch22_394-431 25/06/14 12:31 PM Page 412
412 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
habituation, adaptation, and substitution. The patients in exercises) to general conditioning e xercises
all studies were either community dwelling or patients and to the use of v estibular suppressant medica-
hospitalized for sur gery who had been community tions in patients with chronic vestibular dysfunc-
dwelling before admission to the hospital. The authors tion. Patients were randomly assigned to one
concluded that: of the groups and were follo wed for 6 weeks.
The investigators found a significant decrease
1. moderate to strong evidence exists that vestibu- in dizziness only in the group of patients receiving
lar rehabilitation is a safe and effective treatment vestibular rehabilitation. Similarly, only the
for patients with unilateral vestibular hypofunc- vestibular exercise group had a significant
tion or loss. improvement in postural stability as indicated
2. moderate evidence exists that vestibular by decreased anterior -posterior sway and in-
rehabilitation is an effective treatment of creased single leg stance time. The group receiv-
patients during the acute period onset of ing vestibular suppressant medications did
vestibular neuritis or after resection of not show improvement.17
vestibular schwannoma. This randomized study compared the
3. improvements have been reported in dizziness, effectiveness of unsupervised exercises and
gait and balance, vision during head move- vestibular rehabilitation supervised by physical
ments, activities of daily living, and quality therapists. The patients in the unsupervised ex-
of life. ercise group were given a handout and were in-
4. and moderate evidence exists that these im- structed to “go home and do them.” This group
provements are sustained for months after the of patients was compared with a group of pa-
rehabilitation process ends. tients who performed a customized, supervised
Several key studies are summarized belo w under program of vestibular adaptation exercises.
headings that represent the evidence provided. As with The authors found that a greater percentage of
many investigations, these studies are limited in certain patients improved in the vestibular adaptation
ways: exercise group than in the unsupervised exercise
group. Similarly, Topuz et al compared a super-
1. In many of these studies the exercise approaches vised program of habituation exercises to home
were not described in sufficient detail to allow exercises only and reported a significant im-
replication of the exercises used. provement in subjective complaints and self-
2. Although the study designs included analysis of perceived handicap in the supervised exercise
group data, in most studies no information was group only.68
provided on the individual level (e.g., the num- These studies provide some support for
ber of participants within a group who failed to why it is not sufficient to simply provide pa-
improve). tients with a list of what they could do to foster
3. With few exceptions, these randomized con- return to normal activities. For the most part,
trolled trials did not examine the effect of spe- patients with vestibular hypofunction who end
cific factors, such as exercise approach, gender, up in a neurologist’s office are those patients
time from onset, comorbidities, or environment who have not recovered on their own. Typi-
on recovery. cally, they have avoided activities that involve
head movement, because it increases their
I. Specific vestibular exercises result in a de-
symptoms, they may be fearful of provoking
crease in symptoms, improvement in postural
another episode of vertigo, or they may be
stability, and improvement in gaze stability in
sedentary by habit or nature. Giving these pa-
patients with chronic unilateral vestibular
tients a handout of exercises to perform will
hypofunction:67
not overcome these barriers to recovery.
This prospective, randomized, controlled Pavlou et al recently reported that their drop-
study compared the ef fectiveness of v estibular out rate was 55% in a group of people provided
exercises (customized exercise programs consist- a home DVD for exercise versus a 10% drop-
ing of gaze stability , habituation, and balance out rate for a group of people with visual
3970_Ch22_394-431 25/06/14 12:31 PM Page 413
414 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
vestibular exercise group showed this gait dis- with subacute (2 weeks post onset) patients
turbance. This resulted in the patients in the with UVH. Ten healthy volunteers were also
vestibular exercise group being safer while studied. After 6 weeks of therapy, patients
walking at the time they were discharged performing the combined computerized postur-
home than were the patients in the control ography and Cawthorne-Cooksey exercises
group.72 improved significantly in most measures
This prospective, randomized study examined (modified clinical test of sensory organization
the effectiveness of gaze stabilization exercises and balance [mCTSIB] and limits of stability
performed beginning 3 days after surgery on [LOS] tests), and there were no significant
reducing the patients’ perception of dizziness/ differences between these patients and a group
imbalance. They examined a cohort of 65 pa- of healthy volunteers. In contrast, the untreated
tients (30 exercise patients, 27 control patients, group differed from healthy controls on several
and -8 balance exercises only). The main finding LOS parameters.
was that there was less dizziness in those pa- These studies are important, because they
tients who performed vestibular exercises, provide the evidence that vestibular exercises
based on the scores of the Dizziness Handicap result in improved function when compared
Inventory.49 with no treatment control group.
This randomized, controlled trial IV. Are different treatment approaches equally ef-
found that patients over the age of 50 years fective for vestibular hypofunction?75
who performed a customized exercise program
performed significantly better on standing Only one study has compared the differ-
balance, Timed Up and Go test, and Tandem ent vestibular exercises (habituation and gaze
Gait when compared with patients over 50 stabilization exercises) in the treatment of
years of age who received only instructions patients with UVH. The results should be con-
to go about their normal activities. This effect sidered as preliminary, because the study had
persisted up to 12 weeks and also became a small number of subjects (n = 7). The study
apparent on the Dynamic Gait Index. used disability, motion sensitivity, and visual
acuity during head movement (computerized
III. Exercises versus no exercises:73 dynamic visual acuity, DVA) as the outcome
Yardley et al reported on a comparison of measures but not gait and balance measures.
customized home exercise programs based on Study patients were treated with either habitu-
habituation exercises with a control group who ation exercises or gaze stabilization exercises
performed no exercises. In this prospective ran- (adaptation and substitution exercises), and
domized study, patients with dizziness from a both groups improved in all outcome mea-
variety of causes (including non-vestibular) sures. These finding were unanticipated, be-
were assigned to one of the two groups. Out- cause although habituation exercises are
come measures included scores of symptom designed to reduce symptoms, they theoreti-
severity, anxiety, provocative movements, and cally should not result in an improved DVA.
the sharpened Romberg test. The results of that Similarly, gaze stabilization exercises are
prospective study showed that there was signifi- expected to improve DVA but not necessarily
cantly greater improvement in the patients who reduce symptoms, although this has been
were on the vestibular habituation exercise pro- shown in at least one previous study.46 The
gram than on no exercises. Vestibular exercises, author suggests that the important factor for
even when unsupervised, thus appear to be ben- successful outcome for patients with UVH
eficial.74 may be the inclusion of head movements in
The purpose of this prospective, random- the exercises.
ized controlled study was to assess the role of a An important part of treatment is the
computerized posturography-assisted training education of the patient about the possible
protocol combined with a home-based exercise final level of recovery. This enables the pa-
program to spontaneous recovery in patients tient (and the therapist) to set realistic goals.
3970_Ch22_394-431 25/06/14 12:31 PM Page 415
It is possible that treatment efficacy is not results showed that although most patients
only dependent on matching the exercise ap- improve with a course of vestibular exercises,
propriate to the patient’s problems but also some patients do not improve or improve in
is dependent on the characteristics of the indi- only certain areas (Table 22-5). This study
vidual patient. examined the relationships between patient
characteristics, pretreatment measures of sub-
V. Are there factors that can be identified that are
jective complaints and physical function, and
associated with who will and who will not show
treatment outcome. The primary findings of
improvement?47
the study were:
Several studies on treatment of patients • Age and gender did not affect which patients
with vestibular hypofunction clearly state would improve.47 However, the study showed
the reality that some patients do not that older patients walked more slowly and
improve.75,76 For patients with UVH, be- had poorer visual acuity during head movement
tween 12% and 25% of subjects do not im- (DVA) than did younger patients at discharge.
prove, depending on what outcome measure is This was expected, because there is a naturally
used (Table 22-4).47 Of patients with BVH, occurring decrement in gait speed and in DVA
overall outcomes are worse, with between with age. Older patients were also more likely to
18% and 72% of patients failing to show im- remain at risk for falls, based on the DGI score,
provement (see Chapter 23).77 Identifying and than were younger patients. This simply may be
assessing these non-responding patients is a reflection of the slower gait speed as that is a
extremely important because, as clinicians, component of scoring the DGI test, or it may in-
we are obligated to identify these patients, dicate a lesser degree of recovery in older pa-
seek the reasons for poor outcome, and de- tients. Results from several other studies have
velop methods to reverse poor outcome. identified the fact that age is not a factor in
Herdman et al (2012) examined data achieving improvement in subjective complaints,
from 209 patients with UVH, all of whom had visual acuity during head movement, gait speed,
been treated with similar courses of vestibular and fall risk in patients following a course of
adaptation, substitution, and balance and gait vestibular exercises.46,51,79-81 Less is known
exercises.47 As with several other studies, the about the role of gender in recovery. Within
Nystagmus Spontaneous and gaze-evoked in light Spontaneous in dark; may have head-
(NOT affected and dark; head shaking induced in- shaking–induced nystagmus
by exercises) creases nystagmus; with visual fixa-
tion, the spontaneous nystagmus
decreases
Head Impulse Test of Positive with a corrective saccade May have covert saccades toward the
the VOR side of the lesion; overt corrective sac-
cade more likely when >75% asymmetry
Imbalance – especially Present with all walking and early on, Essentially only with rapid turns toward
while walking during standing: slow, cautious gait affected side and sometimes in the pitch
plane
Continued
3970_Ch22_394-431 25/06/14 12:31 PM Page 416
416 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Oscillopsia with head May or may not be significant Little or no complaints, may be affected
movement complaint by depression47
Walking speed ~50% slow for age Only 14.6% abnormally slow for age47,78
Risk for falling DGI score ≤19 indicating risk for falling 67% no longer at risk; 22% improved
but still at risk; 11% no improvement;47
Vision during head Abnormal for age 78% improve significantly with major-
movements ity to within normal for age47
Participation in normal Disability scores range from bother- Disability scores shift to 0–2 except for
societal interactions some1 – out of work or on long-term those out of work for >1 year or are on
disability5 long-term disability51
Sharpened Romberg Cannot perform Normal with eyes open; cannot perform
with eyes closed
CSTIB—foam, eyes Most cannot maintain balance on foam, Normal with eyes open; may be normal
closed eyes open with eyes closed
Gait Wide-based, slow cadence, decreased Normal except for very rapid turns
rotation, may need help for a few days toward affected side or in pitch plane
Turn head while walking Cannot keep balance Normal; some may slow cadence
and veer
3970_Ch22_394-431 25/06/14 12:31 PM Page 417
■ Table 22-5 MEAN (SD) IN OUTCOME MEASURES FOR PATIENTS WITH CHRONIC
UNILATERAL VESTIBULAR HYPOFUNCTION BEFORE (BASELINE) AND AFTER
A COURSE OF GAZE AND POSTURAL STABILIZATION EXERCISES (DISCHARGE).
ADAPTED FROM HERDMAN ET AL, 2012.47 MEAN AGE OF SUBJECTS WAS
59.3 + 14.9 YEARS.
% of Time Gait
Outcome Symptoms DVA Speed
Measures oVAS dVAS ABC Interfere Disability (Ipsilesional) (meter/sec) DGI
# of 65 113 69 20 68 67 59 119
pre-post
comparisons
418 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
patients who all had surgical removal of acoustic were more likely to return to normal DVA for
neuroma, gender was a significant factor in the age.47 Degree of deficit was not related to im-
patients’ perception of handicap postoperatively, provement in other outcome measures. The ex-
with male patients reporting a greater perception tent to which the rate of development of the
of handicap at 3 months postoperatively, but problem (e.g., sudden unilateral, slowly progres-
there was no gender effect at 1 year after sur- sive loss as in vestibular schwannoma) affect the
gery.69 In patients with a variety of diagnoses, final level of recovery remains unclear. There is
male patients reported worse disability scores some evidence that points to the importance of
than female.44 the underlying etiology in outcome. For instance,
• Time from onset: Time from onset was not re- within subjects who all had surgical removal of
lated to any outcome, supporting the use of acoustic neuroma, tumor size and degree of pre-
these exercises in patients regardless of the operative canal paresis were significant factors in
chronicity of their vestibular dysfunction. Pa- the patients’ perception of handicap postopera-
tients in this study had a mean time from onset tively.80 In contrast, patients with surgically in-
of 14.5 months (range 1 week to 12 years; me- duced vestibular loss have a similar level of
dian 5.0 months). Findings from studies on pa- recovery as do patients with unilateral vestibular
tients with acute UVL are different and suggest neuritis and labyrinthitis.49
that delaying the initiation of vestibular exer- • The presence and number of different comor-
cises results in a delay in the initiation of recov- bidities did not affect whether or not improve-
ery/slows compensation.1,72 In one relatively ment occurred. This was in contrast to a study
small study (n = 23), patients with acute loss that showed that patients with migraine often
of vestibular function following resection of improve physically but continue to perceive that
acoustic neuroma started a vestibular rehabilita- they are disabled by their vestibular com-
tion program at 3 days postoperatively and had plaints.83 In the Herdman et al study, the only
better postural stability and less disequilibrium comorbidity that affected outcome was the pres-
than a control group who performed placebo ence of anxiety and/or depression. Patients with
exercises by 6 days postoperatively.48 Another anxiety and/or depression were more likely to
randomized controlled trial with a larger cohort have lower balance confidence and a higher per-
of subjects (n = 65) confirmed these findings.72 centage of time for which symptoms interfered
Even this result is somewhat controversial, be- with activities at discharge. As with many if not
cause a third study found no difference in out- all chronic illnesses, the presence of depression
come between patients performing vestibular and/or anxiety can impact quality of life. In
exercises and a placebo group during the acute some populations, depression is the variable
stage post removal of acoustic neuroma.82 most likely to influence quality of life.84 How-
There were differences, however, in the out- ever, Grunfeld et al noted that the presence of a
come measures and the exercises used, which vestibular lesion per se is not associated with
may explain the different conclusions, but depression.85 Somewhat in contrast, Yardley
clearly more research is needed on the effect et al found that negative mood, rather than true
of time from onset on recovery. depression, was a factor contributing to self-
perceived handicap in patients with dizziness.86
A different issue is whether there is a critical period
Although there may be no direct association
during which exercises must be initiated. The evidence
between vestibular deficits and depression, the
seems to suggest that there is no critical period—that
presence of depression can have a serious
vestibular exercises are beneficial even for patients with
impact on the potential for recovery. Krebs
chronic problems.17,56 This has been sho wn directly
et al noted that some patients with vestibular
through analysis of time from onset as a factor that might
hypofunction developed depression that pre-
be involved in recovery.46,51,77
vented participation in vestibular rehabilita-
• The vestibular deficit itself: The only relationship tion.77 This observation is supported by others
this study identified between degree of deficit, as who noted that treatments that appear to de-
defined as percent asymmetry, was that patients crease quality of life have low adherence by
with smaller asymmetries in vestibular function patients,87 while better outcomes and improved
3970_Ch22_394-431 25/06/14 12:31 PM Page 419
quality of life are associated with increased had a history of falls, had poor baseline fall
treatment adherence.88 Factors that have been risk scores initially, and were older. These
identified as contributing to the self-perception three factors accounted for 42.5% of DGI at
of handicap or disability in patients with dizzi- discharge. Interestingly, initial DVA score,
ness include somatization, negative mood, satis- which has previously been shown to predict
faction with social support, self-esteem, and fall risk at discharge, was not a significant
anxiety.89,90 Psychiatric/psychological factors factor.93
also help predict outcome. Symptoms of somatic
These results provide some guidelines that therapists
anxiety predict an increase in handicap over a
and other clinicians can use to de velop expectations for
7-month study of people with recurrent dizzi-
recovery.
ness.90 Another factor, maladaptive coping
Several other f actors must be tak en into account
strategies, was not examined in the Herdman
when considering the potential for recovery of a patient.
et al (2012) study but has been documented by
others as being associated with decreased qual- • Medication: Several authors have suggested that
ity of life and with greater depression in patients vestibular-suppressant medications such as di-
with chronic medical illness.91,92 azepam may delay or slow recovery,44,94 but
few studies actually have examined the influ-
One study of patients with episodic vertigo identified
ence of medication on the level of recovery.
four primary strategies for coping with vertigo: (1) problem-
One randomized controlled study found that pa-
focused information seeking, (2) distraction, (3) denial,
tients taking meclizine did not show an im-
and (4) relinquishing responsibility.91 The investigators
provement in symptoms or in balance, whereas
found that “relinquishing responsibility” predicted hand-
patients performing vestibular exercises did im-
icap, even when the analysis controlled for other f actors
prove.67 Patients treated with steroids for
such as emotional distress. Because of the non-episodic
vestibular neuritis, on the other hand, appear to
nature of the symptoms in the patients with vestibular hy-
have less perception of handicap after treatment
pofunction, the relationship of coping strategies and psy-
than those patients who were not treated with
chological factors to outcome may be different than what
steroids.95 The use of medication appears to be
has been already reported.
influenced by performing exercises. In a separate
Several patterns were identif ied in which multiple
randomized trial, Venosa and Bittar suggested
factors accounted for a signif icant percentage of the re-
that persons who performed exercises acutely
covery of some of the outcome measures.47
(symptoms that began less than 5 days before
1. Patients who indicated that symptoms interfered the start of the study) were significantly less
with performance of their usual activities at a likely to use medication at 3 weeks than those
high level (greater percentage of the day) at dis- who were not provided vestibular exercises.96
charge were those who had anxiety and/or de- Those in the vestibular exercise group also had
pression and who indicated a high percentage a greater number of normal Fukuda step tests
of time symptoms interfered with activities and post head shake testing results recorded by
(5TSI) at the time of the baseline assessment. a blinded tester. At 3 weeks post exercise in
These two factors together accounted for 83.7% acute persons with vestibular disorders com-
of the outcome. Similarly, patients who rated pared with a control group, they had similar
their disability as high at discharge had higher symptom reports. However, only 13% continued
baseline %TSI, worse baseline disability scores, to take medication in the exercise group, while 82%
and poor baseline DVA score. These three fac- of subjects in the control group were taking
tors accounted for 47.8% of the disability score medication daily.
at discharge. • Recovery may be delayed or limited if the patient
2. Patients who walked more slowly at discharge restricts head movement or if visual inputs are
had slower baseline gait speed and were older. minimized.10,14,15 Patients with vestibular lesions
Approximately 55% of gait speed at discharge often prefer to keep their eyes closed and their
was accounted for by advanced age and slow heads still to minimize symptoms. Another factor
walking at onset of symptoms. that may delay recovery or limit the final level of
3. Patients had lower (poorer) fall risk scores at recovery may be the use of medications that sup-
discharge, as measured by the DGI test, if they press vestibular function.94
3970_Ch22_394-431 25/06/14 12:31 PM Page 420
420 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Continued
3970_Ch22_394-431 25/06/14 12:32 PM Page 422
422 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
the day but had not attempted to dri ve at night. She ability to perform the Romberg with eyes closed most
was able to go to church but had not yet resumed her likely reflects her peripheral neuropathy, because most
evening social activities. people with UVH can perform the Romberg eyes open
and eyes closed. A home program of exercises would
be continued until the patient’s recovery had plateaued.
Comment The use of a straight cane at night was recommended
This patient is now showing good progress toward re- because of her combined peripheral neuropathy and
covery following her unilateral vestibular loss. Her in- vestibulopathy.
Continued
3970_Ch22_394-431 25/06/14 12:32 PM Page 424
424 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Continued
3970_Ch22_394-431 25/06/14 12:33 PM Page 426
426 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Continued
3970_Ch22_394-431 25/06/14 12:33 PM Page 428
428 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
8. Halmagyi GM, et al. Vestibular neurectomy and the man- 29. Schubert MC, Das V, Tusa RJ, Herdman SJ. Cervico-
agement of vertigo. Curr Opinion Neurol Neurosurg. ocular reflex in normal subjects and patients with unilat-
1988;1:879. eral vestibular hypofunction. Otology Neurotology. 2004;
9. Yagi T, Markham CH. Neural correlates of compensation 25:65.
after hemilabyrinthectomy. Exp Neurol. 1984;84:98. 30. Sawyer RN, et al. The cervico-ocular reflex of normal
10. Fetter M, Zee DS. Recovery from unilateral labyrinthec- human subjects in response to transient and sinusoidal
tomy in Rhesus monkeys. J Neurophysiol. 1988;59:370. trunk rotations. J Vestib Res. 1994;4:245.
11. Allum JHJ, et al. Long-term modifications of vertical and 31. Diener HC, et al. The significance of proprioception on
horizontal vestibulo-ocular reflex dynamics in man. Acta postural stabilization as assessed by ischemia. Brain Res.
Otolaryngol (Stockh). 1988;105:328. 1984;296:103.
12. Mathog RH, Peppard SB. Exercise and recovery from 32. Diener HC, et al. Stabilization of human posture during
vestibular injury. Am J Otolaryngol. 1982;3:397. induced oscillations of the body. Exp Brain Res. 1982;
13. Igarashi M, et al. Further study of physical exercise and 45:126.
locomotor balance compensation after unilateral 33. Dichgans J, Brandt T. Visuo-vestibular interaction. Effects
labyrinthectomy in squirrel monkeys. Acta Otolaryngol. on self-motion perception and postural control. In: Held R,
1981;92:101. et al, eds. Handbook of Sensory Physiology. Berlin:
14. Courjon JH, et al. The role of vision on compensation of Springer; 1978:755.
vestibulo ocular reflex after hemilabyrinthectomy in the 34. Istl-Lenz Y, et al. Response of the human vestibulo-ocular
cat. Exp Brain Res. 1977;28:235. reflex following long-term 2X magnified visual input. Exp
15. Lacour M, et al. Modifications and development of spinal Brain Res. 1985;57:448.
reflexes in the alert baboon (Papio papio) following an 35. Davies P, Jones GM. An adaptive neural model compatible
unilateral vestibular neurectomy. Brain Res. 1976; with plastic changes induced in the human vestibulo-
113:255. ocular reflex by prolonged optical reversal of vision. Brain
16. Pfaltz CR. Vestibular compensation. Acta Otolaryngol. Res. 1976;103:546.
1983;95:402. 36. Collewijn H, et al. Compensatory eye movements during
17. Szturm T, et al. Comparison of different exercise pro- active and passive head movements: fast adaptation to
grams in the rehabilitation of patients with chronic periph- changes in visual magnification. J Physiol. 1983;340:259.
eral vestibular dysfunction. J Vestib Res. 1994;4:461. 37. Pavlow M, Bronstein AM, Davies RA. Randomized trial
18. Miles FA, Eighmy BB. Long-term adaptive changes in pri- of supervised versus unsupervised optokinetic exercise in
mate vestibuloocular reflex, I: behavioral observations. J persons with peripheral vestibular disorders. Neurorehabil
Neurophysiol. 1980;43:1406. Neural Repair. 2013;27(3):208.
19. Schubert MC, Migliacco AA, Clendaniel RA, Allak A, 38. Cawthorne T. The physiological basis for head exercises.
Carey JP. Mechanism of dynamic visual acuity recovery Journal of the Chartered Society of Physiotherapy.
with vestibular rehabilitation. Arch Phys Med Rehabil. 1944;30:106.
2008;89(3):500. 39. Cooksey FS. Rehabilitation in vestibular injuries. Proc
20. Scherer M, Migliaccio AA, Schubert MC. Effect of Royal Soc Med. 1946;39:273.
vesibular rehabilitation of passive dynamic visual acuity. 40. Hecker HC, et al. Treatment of the vertiginous patient
J Vestib Res. 2008;18(2-3):147. using Cawthorne’s vestibular exercises. Laryngoscope.
21. Schubert MC, Hall CD, Das V, Tusa RJ, Herdman SJ. 1974;84:2065.
Oculomotor strategies and their effect of reducing gaze 41. Norre ME, Beckers A. Vestibular habituation training for
position error. Otology Neurotology. Feb 2010;31(2):228. positional vertigo in elderly patients. J Am Geriatr Soc.
22. Tian J, Crane BT, Demer JL. Vestibular catch-up saccades 1988;36:425.
in labyrinthine deficiency. Exp Brain Res. Apr 2000;131 42. Norre ME, De Weerdt W. Treatment of vertigo based on
(4):448. habituation, I: physio-pathological basis. J Laryngol Otol.
23. Tierstrom F, Nystrom A, Magnuss M. How to uncover the 1980;94:689.
covert saccade during the head impulse test. Otol Neuro- 43. Shepard NT, et al. Habituation and balance retraining ther-
tol. 2012;33(9):1583. apy. Neurol Clin. 1990;5:459.
24. Minor, et al. Horizontal vestibuloocular reflex evoked by 44. Shepard NT, et al. Vestibular and balance rehabilitation
high-acceleration rotations in the squirrel monkey, I: nor- therapy. Ann Otol Rhinol Laryngol. 1993;102:198.
mal responses. J Neurophysiol. Sep 1999;82(3):1254. 45. Shepard NT, Telian SA. Programmatic vestibular rehabili-
25. Grossman GE, et al. Frequency and velocity of rotational tation. Otolaryngol Head Neck Surg. 1995;112:173.
head perturbation during locomotion. Exp Brain Res. 1988; 46. Herdman SJ, Schubert MC, Das VE, Tusa RJ. Recovery
70:470. of dynamic visual acuity in unilateral vestibular hypo-
26. Grossman GE, et al. Performance of the human vestibu- function. Arch Otolaryngol Head Neck Surg. 2003;
loocular reflex during locomotion. J Neurophysiol. 1989; 129:819.
62:264. 47. Herdman SJ, Hall CD, Delaune W. Variables associated
27. Leigh RJ, et al. Supplementation of the vestibulo-ocular with outcome in patients with unilateral vestibular hypo-
reflex by visual fixation and smooth pursuit. J Vestib Res. function. Neurorehabil Neural Repair. 2012;26(2):151.
1994;4:347. 48. Herdman SJ, Clendaniel RA, Mattox DE, Holliday M,
28. Segal BN, Katsarkas A. Long-term deficits of goal-directed Niparko JK. Vestibular adaptation exercises and recovery:
vestibulo-ocular function following total unilateral loss of acute stage following Acoustic Neuroma Resection.
peripheral vestibular function. Acta Otolaryngol (Stockh). Otolaryngol-Head and Neck Surg. 1995;113:71.
1988;106:102.
3970_Ch22_394-431 25/06/14 12:33 PM Page 430
430 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
49. Vereeck L, Wuyts FL, Truijen S, De Valck C, Van de 68. Topuz O, Tupuz B, Ardic FN, Sarhus M, Ogmen G,
Heyning PH. The effect of early customized vestibular Ardic F. Efficacy of vestibular rehabilitation on chronic
rehabilitation on balance after acoustic neuroma resection. unilateral vestibular dysfunction. Clin Rehabilitation.
Clin Rehabil. 2008;22(8):698. 2004;18:76.
50. Teggi R, Caldirola D, Fabiano B, Recanati P, Bussi M. 69. Pavlou M, Bronstein AM, Davies RA. Randomized trial of
Rehabilitation after acute vestibular disorders. J Laryngol supervised versus unsupervised optokinetic exercise in
Otol. 2009;123(4):397. persons with peripheral vestibular disorders. Neurorehabil
51. Telian SA, et al. Habituation therapy for chronic vestibular Neural Repair. Mar 2013;27(3):208.
dysfunction: preliminary results. Otolaryngol Head Neck 70. Cohen HS, Kimball KT. Increased independence and de-
Surg. 1990;103:89. creased vertigo after vestibular rehabilitation. Otolaryngol
52. Lisberger SG, et al. Frequency-selective adaptation: Head Neck Surg. 2003;128(1):60.
evidence for channels in the vestibulo-ocular reflex. 71. Herdman SJ, Hall CD, Schubert M, Das VE, Tusa RJ.
J Neurosci. 1983;3:1234. Recovery of dynamic visual acuity in patients with bilat-
53. Schubert MC, Della Santina CC, Shelhamer M. Incremen- eral vestibular hypofunction. Arch Otolaryngol Head Neck
tal angular vestibulo-ocular reflex adaptation to active Surg. Apr 2007;133(4):383.
head rotation. Exp Brain Res. Dec 2008;191(4):435. 72. Enticott JC, O’Leary SJ, Briggs RJ. Effects of vestibulo-
54. Demer JL, Porter FI, Goldberg J, Jenkins HA, Schmidt K. ocular reflex exercises on vestibular compensation after
Adaptation to telescopic spectacles: vestibulo-ocular re- vestibular schwannoma surgery. Otol Neurotol.
flex plasticity. Invest OphthalmolVisual Sci. 1989;30:159. 2005;26:265.
55. Cohen HS, Kimball KT. Changes in a repetitive head 73. Yardley L, et al. A randomized controlled trial of exercise
movement task after vestibular rehabilitation. Clin Rehabil. therapy for dizziness and vertigo in primary care.
Mar 2004;18(2):125. Br J Gen Pract. 1998;48:1136.
56. Kirby SE, Yardley L. The contribution of symptoms of 74. Marioni G, Fermo S, Zanon D, Broi N, Staffieri A. Early
posttraumatic stress disorder, health anxiety and intoler- Rehabilitation for unilateral peripheral vestibular disor-
ance of uncertainty to distress in Ménière’s disease. ders: a prospective, randomized investigation using com-
J Nerv Ment Dis. May 2009;197(5):324. puterized posturography. Eur Arch Otorhinolaryngol.
57. Bessot N, Denise P, Toupet M, Van Nechel C, Chavoix Feb 5, 2012; [Epub ahead of print]
C.Interference between walking and a cognitive task is 75. Clendaniel RA. The effects of habituation and gaze
increased in patients with bilateral vestibular loss. Gait stability exercises in the treatment of unilateral vestibular
Posture. Jun 2012;36(2);319. hypofunction: preliminary results. J Neurol Phys Ther.
58. Bessot N, Denise P, Toupet M, Van Nechel C, Chavoix C. 2010;34:111.
Interference between walking and a cognitive task is in- 76. Krebs DE, Gill-Body KM, Parker SW, Ramirez JV.
creased in patients with bilateral vestibular loss. Gait Vestibular rehabilitation: Useful but not universally so.
Posture. Jun 2012;36(2):319. Otolaryngol Head Neck Surg. 2003;128:240.
59. MacDougall HG, Moore ST, Black RA, Jolly N, Curthoys 77. Brown KE, Whitney SL, Wrisley DM, Furman JM. Physi-
IS. On-road assessment of driving performance in bilateral cal Therapy outcome for persons with bilateral vestibular
vestibular-deficient patients. Ann N Y Acad Sci. May loss. Laryngoscope. 2001;111:1812.
2009;1164:413. 78. Bohannon RW. Comfortable and maximum walking speed
60. Cohen HS, Wells J, Kimball KT, Owsley C. Driving of adults aged 20-79 years: reference values and determi-
disability and dizziness. J Safety Res. 2003;34(4):361. nants. Age Ageing. 1997;26:15.
61. Tinetti ME, Richman D, Powell L. Falls efficacy as a 79. Cohen HS, Kimball KT. Changes in repetitive head
measure of fear of falling. J Gerontol. Nov 1990;45 movement task after vestibular rehabilitation. Clin
(6):P239. Rehabil. 2004;18(2):125.
62. Yardley L, Beyer N, Hauer K, Kempen G, Piot-Ziegler C, 80. Humphriss RL, Baguley DM, Moffat DA. Changes in
Todd C. Development and initial validation of the Falls Dizziness Handicap after vestibular schwannoma excision.
Efficacy Scale-International (FES-I). Age Ageing. Nov Otol Neurotol. 2003;24:661.
2005;34(6):614. 81. Whitney SL, Wrisley DM, Marchetti GF, Furman JM.
63. Washburn RA, Smith KW, Jette AM, Janney CA. The The effect of age on vestibular rehabilitation outcome.
Physical Activity Scale for the Elderly (PASE): develop- Laryngoscope. 2000;112:1785.
ment and evaluation. J Clin Epidemiol. Feb 1993;46:153. 82. Cohen HS, Kimball KT, Jenkins HA. Factors affecting
64. Igarashi M, et al. Effect of physical exercise on nystagmus recovery after acoustic neuroma resection. Acta Otolaryn-
and locomotor dysequilibrium after labyrinthectomy in ex- gol. 2002;122:841.
perimental primates. Acta Otolaryngol. 1975;79:214. 83. Wrisley DM, Whitney SL, Furman JM. Vestibular rehabil-
65. Hillier SL, McDonnell M. Vestibular rehabilitation for uni- itation outcomes in patients with a history of migraine.
lateral peripheral vestibular dysfunction. Cochrane Data- Otol Neurotol. Jul 2002;23(4):483.
base Syst Rev. Feb 16, 2011;(2):CD005397. 84. Jia H, Uphold CR, Wu S, Reid K, Findley K, Duncan PW.
66. Hillier SL, Hollohan. Vestibular rehabilitation for unilater- Health-related quality of life among men with HIV infec-
all peripheral vestibular dysfunction. Cochrane Database tion: Effects of social support, coping, and depression.
Syst Rev. 2007;(2):CD05397. AIDS Patient Care and STDs. 2004;18:594.
67. Horak FB, et al. Effects of vestibular rehabilitation on 85. Grunfeld EA, Gresty MA, Bronstein AM, Jahashati M.
dizziness and imbalance. Otolaryngol Head Neck Surg. Screening for depression among neuro-otology patients
1992;106:175.
3970_Ch22_394-431 25/06/14 12:33 PM Page 431
with and without identifiable vestibular lesions. INT J 95. Kitahara T, Kondoh K, Morihana T, Okumura S, Horii A,
Audiology. 2003;42:161. et al. Steroid effects on vestibular compensation in
86. Yardley L, Masson E, Verschern C, Haacke, Luxon L. human, Neurol Res. 2003;25(3):287.
Symptoms, anxiety and handicap in dizzy patients: devel- 96. Venosa AR, Bittar RS. Vestibular rehabilitation exercises
opment of the vertigo symptom scale. J Psychosom Res. in acute vertigo. Laryngoscope. 2007;117(8):1482.
1992;36(8):731. 97. Nardone A, Godi M, Artuso A, Schieppati M. Balance re-
87. Fallowfield L. Acceptance of adjuvant therapy and quality habilitation by moving platform and exercises in patients
of life issues. Breast. 2005;14(6):612. with neuropathy or vestibular deficit. Arch Phys Med
88. Studenski S, Duncan PW, Perea S, Reker D, Lai SM, et al. Rehabil. Dec 2010;91(12):1869.
Daily functioning and quality of life in a randomized con- 98. Winkler PA, Esses B. Platform tilt perturbation as an in-
trolled trial of therapeutic exercise for subacute stroke sur- tervention for people with chronic vestibular dysfunction.
vivors. Stroke. 2005;36:1764. J Neurol Phys Ther. 2011;35(3):105.
89. Yardley L. Contribution of symptoms and beliefs to handi- 99. Rossi-Izquierdo M, Santos-Perez S, Soto-Varela A. What
cap in people with vertigo: a longitudinal study. is the most effective vestibular rehabilitation technique in
Br J Clin Psychol. 1994;33:101. patients with unilateral peripheral vestibular disorders?
90. Yardley L. Prediction of handicap and emotional distress Eur Arch Otorhinolaryngol. 2011;11:1569.
in patients with recurrent vertigo: symptoms, coping 100. Whitney SL, Wrisley DM, Brown KE, Furman JM.
strategies, control beliefs and reciprocal causation. Soc Sci Physical therapy for migraine-related vestibulopathy
Med. 1994;39:573. and vestibular dysfunction with a history of migraine.
91. Myaskowsky L, et al. Avoidant coping with health prob- Laryngoscope. 2000;110:1528.
lems is related to poorer quality of life among lung trans- 101. Wrisley DM, Whitney SL, Furman JM. Vestibular reha-
plant candidates. Prog Transplant. Sep 2003;13(3):183. bilitation outcome inpatients with a history of migraine.
92. Rothrock NE, Lutgendorf SK, Kreder KJ. Coping strate- Otol Neurotol. 2002;23:483.
gies in patients with interstitial cystitis: relationships with 102. Wrisley DM, Whitley SL, Furman JM. Measurement
quality of life and depression. J Urol. Jan of Health Status in patients with dizziness and a history
2003;169(1):233. of migraine. J Neurol Phys Ther. 2004;28(2):84.
93. Hall CD, Schubert MC, Herdman SJ. Prediction of fall 103. VanSwearingen JM, Brach JS. Changes in facial move-
risk reduction in individuals with unilateral vestibular ment and synkinesis with facial neuromuscular reeduca-
hypofunction. Otol Neurotol. Sept 2004;25(5):746. tion. Plast Reconstr Surg. Jun 2003;111(7):2370.
94. Zee DS. The management of patients with vestibular
disorders. In: Barber HO, Sharpe JA, eds. Vestibular
Disorders. Chicago: Year Book;1987:254.
3970_Ch23_432-456 25/06/14 1:59 PM Page 432
CHAPTER 23
Physical Therapy
Management of
Bilateral Vestibular
Hypofunction
and Loss
Susan J. Herdman, PT, PhD, FAPTA ■
432
3970_Ch23_432-456 25/06/14 1:59 PM Page 433
Chapter 23 • PHYSICAL THERAPY MANAGEMENT OF BILATERAL VESTIBULAR HYPOFUNCTION AND LOSS 433
Etiology
unknown 38.4% 51% 21% 38.5% 5.7%
Progressive 20.2%
Autoimmune 7% 9% 5.7%
Tumor 5.7%
receiving a vestibulotoxic medication such as gentamicin, patients with BVH under the age of 65 reported falls related
often do not know they have a balance problem until they get to their bilateral hypofunction and 58% of those 65 to
out of bed. Typically, these patients have been treated with 74 years of age reported falls related to their BVH.9 In both
the ototoxic medication because of a serious infection. They cases the incidence of falls exceeded the fall rate of healthy
are often debilitated, and their balance problems are initially individuals of the same age. Interestingly , patients age
attributed to weakness. Other patients, such as those with a 75 years and older had a lo wer fall rate than do healthy in-
progressive loss, may not notice their gradually w orsening dividuals; this was attributed to their use of assistive devices
balance until it reaches a critical point and they start falling. and limited activity level. Most patients are able to pre vent
Even with full compensation, balance problems will falls even though they may side-step or stagger occasionally.
persist. Although the other sensory and motor systems do However, even after a course of v estibular and balance re-
help compensate for the vestibular loss, these systems cannot habilitation, 20% to 30% of patients with BVH are still at
substitute completely for the loss of vestibular function (see risk for falling when they are discharged.3,10
Chapters 6 and 9). Normal postural stability while w alking
requires the combined use of at least tw o of three sensory
cues (visual, vestibular, somatosensory). Patients who have
Oscillopsia
no vestibular function, therefore, will ha ve difficulty when Another problem for patients with bilateral vestibular loss is
either visual or somatosensory cues are also significantly de- the visual blurring that occurs during head mo vements. Al-
creased (e.g., walking in the dark). Although balance may most 70% of all patients with BVH complain of oscillopsia
be poor, it is not known what the actual frequency of falling even after a course of gaze stabilization exercises.10 Greater
is for patients with BVL. One study reported that 70% of intensity of oscillopsia occurs in patients with absence of both
3970_Ch23_432-456 25/06/14 1:59 PM Page 434
434 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
inferior and superior vestibular nerve function. In addition to described by patients with terms such as “dizziness” and
the subjective complaint, patients also ha ve a documented “spaciness” is also heightened by head movement and per-
decrement in visual acuity during head movements. Interest- sists in as many as 60% of all patients. This head movement–
ingly, several studies have demonstrated that the subjecti ve induced dizziness is e xacerbated by repeated head
complaints of oscillopsia does not correlate with the actual movement and may cause patients to avoid movement.
decrement in visual acuity during head movement.5,11,12
Initially, loss of vestibular function results in a decre-
Physical Deconditioning
ment in visual acuity even when the patient is stationary,
if the head is not supported. 13 Even following the best Poor physical condition can be a signif icant problem for
compensation, some patients say that objects that are f ar patients with BVL. This can be caused directly by a de-
away appear to be jumping or bouncing. This visual blur- creased activity level because of the patient’ s fear of
ring, or oscillopsia, increases with irre gular or unpre- falling or because of the increased dizziness that occurs
dictable head mo vements such as w ould occur while with movement. It is especially a problem for patients
walking. As a result, patients may not be able to read street whose vestibular loss is secondary to ototoxic medica-
signs or identify people’s faces as they walk, or they may tions. These patients are already debilitated because of se-
have difficulty seeing clearly while in a moving car. Severe vere infection. Many patients on peritoneal dialysis, for
oscillopsia will also impact postural stability because de- example, develop infections that are treated with genta -
creased visual acuity will affect the person’s ability to use micin, a vestibulotoxic aminoglycoside.
visual cues for stability.14
Assessment
Sense of Disequilibrium, Imbalance, The assessment of patients with BVL is similar to that for pa-
and Dizziness tients with unilateral vestibular deficits; therefore, only certain
Patients often complain of a sense of being “of f-balance” aspects of the assessment will be described here. Physical
that is separate from their actual postural instability . This therapy assessment of patients with BVL must address sub-
feeling lessens or disappears when the person is lying down jective complaints, postural instability and oscillopsia, the pa-
or sitting with the head supported. It increases dramatically tient’s overall physical condition, and their ability to perform
when the person is moving. Although disequilibrium may activities of daily living (ADLs). This assessment must also
decrease as a result of compensation, for up to 80% of pa- identify other factors that might affect recovery, especially
tients it remains a serious and debilitating problem.10 It can visual and somatosensory deficits. A summary of the assess-
lead to decreased physical activity, social isolation, and de- ment and the usual findings for patients with chronic bilateral
pression. Another disturbing sensation that is more vaguely vestibular loss is presented in Box 23-1.
Box 23-1
Chapter 23 • PHYSICAL THERAPY MANAGEMENT OF BILATERAL VESTIBULAR HYPOFUNCTION AND LOSS 435
Box 23-1
436 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
great as 10% to 20%, however, in those patients with renal In certain cases, vestibular function tests can also be
impairment, over the age of 65 years, taking loop diuretics, used to follow the course of the vestibular loss and of any
or with previous vestibular loss. This percentage increases recovery of vestibular function that might occur.26,27 Cer-
to 40% among persons on renal dialysis who receive gen- tain aminoglycoside antibiotics are selectively taken up by
tamicin. Furthermore, the patient who has a loss of vestibular hair cells and result in a gradual loss of vestibu-
vestibular function, with its resultant balance and visual lar function. Typically, there is continued loss of vestibular
problems, secondary to ototoxic medication may ha ve to function even after the medication is stopped. Some im-
deal with significant anger and depression. provement in vestibular function may occur in hair cells
While taking the patients’ histories, the clinician should that were affected by the ototoxic drug but did not die. Po-
identify the presence of specific comorbidities such as mac- tentially, an increase in gain may also occur with the use
ular degeneration and cataracts. These disorders result in a of vestibular adaptation exercises. This has been demon-
gradual decrease in available visual cues and will ha ve an strated in patients with unilateral vestibular loss but not in
adverse effect on balance in the future. Similarly, disorders patients with BVL.28,29
that frequently result in peripheral neuropathies should be
noted, such as diabetes or chronic alcohol abuse. Other co- Visual System
morbidities that influence outcome in patients with BVH had Assessment of visual function should include a measure
fair to strong correlations with specific outcomes.10 Of par- of visual acuity, because this can affect postural stability.14
ticular interest was that a history of headaches correlates with Measuring visual acuity during head movement is partic-
a higher percentage of time that symptoms interfere with ularly important. The vestibulo-ocular system normally
life, a greater intensity of oscillopsia and head mo vement– stabilizes the eyes during head movements; when there is
induced dizziness, and a lo wer balance confidence at dis- no vestibulo-ocular reflex (VOR) to stabilize the eyes dur-
charge. Furthermore, the total number of comorbidities also ing head movement, small amounts of retinal slip (move-
influences outcome.2,10 Gillespie and Minor (1999) found ment of image across the retina) will de grade vision. For
that poor outcome following a course of vestibular rehabil- instance, 3 deg/sec of retinal slip would cause visual acuity
itation was related in part to having more than four comor- to change from 20/20 to 20/200.30 As such, in patients with
bidities,2 and Herdman et al reported that poor outcome, as absent vestibular function, the head movement that occurs
indicated by higher disability scores at dischar ge, was in a moving car can cause a de gradation of visual acuity
correlated with greater numbers of comorbidities.10 that would make driving unsafe.
Chapter 23 • PHYSICAL THERAPY MANAGEMENT OF BILATERAL VESTIBULAR HYPOFUNCTION AND LOSS 437
0.80
0.70
0.60
0.50
CVA (LogMAR)
0.40
0.30
0.20
0.10
0.00
1 13 25 37 49 61 73 85 97 109 121 133 145 157 169 181 193 205 217 229 241
Subjects
NL UVH BVH
Figure 23.1 Distribution of dynamic visual acuity scores (LogMAR) using the computerized
test in patients with unilateral and bilateral vestibular loss and in normal subjects. In the
methodology used to determine these values, static visual acuity (SVA) had a minimal score of
LogMAR 0.000, which is different from newer commercial versions of the test (see Herdman
et al31 for details on the methodology used). DVA is the expression of the decrement in visual
acuity during head movement.
Scores
(LogMAR)
on postural stability in otherwise healthy individuals, in the patient can hold the position for the normal time for
patients with vestibular loss, somatosensory deficits may their age. Although some patients will be able to perform
have profound effects on balance and on the potential for the Sharpened Romberg with eyes open, they will not be
functional recovery. As with visual system disorders, able to perform the Sharpened Romberg with eyes closed.
being aware of potentially progressive disorders affecting Patients with bilateral vestibular deficits will also have dif-
somatosensory information is important. ficulty performing tests in which both visual and so-
matosensory cues are altered. An example of this w ould
Balance and Gait be Fukuda’s Stepping Test in which the e yes are closed
Patients with BVL must be given a detailed assessment of and the patient is marching in place. P atients may have
balance and gait. Obviously, static balance should be as- normal tests with eyes open but will fall with eyes closed.
sessed first. In the acute stage, patients with bilateral Determining whether patients use both visual and so-
vestibular deficits may have positive Romberg tests. In the matosensory cues to maintain balance or whether they de-
compensated stage, the Romberg is usually normal in that pend on particular sensory cues is critical. It is important
3970_Ch23_432-456 25/06/14 1:59 PM Page 438
438 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
to recognize that this may vary considerably from patient unless challenged by the need to perform an unanticipated
to patient and that it can change over the course of recov- head or body movement. Patients decrease their trunk and
ery. Bles et al34 found that patients with BVL are initially neck rotation in an ef fort to improve stability by avoiding
more dependent on visual cues than on somatosensory head movements. Arm swing is similarly decreased. Patients
cues for balance. With time, there is an impro vement in may use e xcessive visual fixation and therefore ha ve in-
the ability of patients to use somatosensory cues.This im- creased difficulty if asked to look up or turn the head while
provement varies from patient to patient, ho wever, and walking. Patients typically turn “en bloc” and may even stop
needs to be carefully assessed (Fig. 23.2). If a patient is before they turn. Asking patients to turn their heads while
dependent on one sensory cue for balance (e.g., vision), walking results in increased ataxia and, often, loss of balance.
then exercises that foster the ability to use the under-used One of the main characteristics of gait of people with
sensory cues are appropriate (e.g., somatosensory). bilateral vestibulopathy it that is has sudden changes in
The gait of man y patients with bilateral v estibular trajectories compared with gait of healthy indi viduals.35
deficits can be described as wide-based, slow, and ataxic. In That is, the patient may appear to w alk normally at one
other patients, gait may appear to be essentially normal moment and then staggers at the next moment.
A B
C D
Figure 23.2 Posturography test results from patients with bilateral vestibular loss demon-
strating the differences in ability to maintain postural stability when different sensory cues are
altered or removed. Patients are tested using six different conditions:
Available Cues Unavailable or Altered Cues
Results show patients who have difficulty when both visual and somatosensory cues are altered
(A), when somatosensory cues only are altered (B), when visual cues only are altered (C), and
when either visual or somatosensory cues are altered (D).
3970_Ch23_432-456 25/06/14 1:59 PM Page 439
Chapter 23 • PHYSICAL THERAPY MANAGEMENT OF BILATERAL VESTIBULAR HYPOFUNCTION AND LOSS 439
440 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
they were followed, they recovered the ability to maintain to move around places with busy visual environments such
their balance to within normal limits in the testing para- as shopping malls and grocery stores. F or some patients,
digm except at high frequencies. The vestibular system moving in busy environments may require the use of some
functions at higher frequencies than do the visual or type of assistive device, such as a shopping cart or a cane,
somatosensory systems, which w ould account for why but for many patients with BVL, no assistive devices are
neither visual nor somatosensory cues can substitute com- needed after the patient becomes comfortable walking in
pletely for loss of vestibular cues. that environment.
The contribution of somatosensory inputs from the
cervical region to postural stability in patients with com- Evidence that Exercise Facilitates
plete BVL is not clearly understood. Bles et al47 found that
changes in neck position did not af fect postural stability
Recovery
in patients with complete BVL. They concluded that so- Support for the use of exercises to improve physical func-
matosensory signals from the neck do not contrib ute to tion in patients with bilateral v estibulopathy was based
postural stability. We do not know, however, if kinesthetic originally on the result of studies of nonhuman primates
signals from the neck that occur during head mo vement (Igarashi et al). 52 Evidence now exists in people with
would affect postural stability. Certainly patients with bi- BVH that supports the use of specific exercises (adapta-
lateral vestibular dysfunction become less stable when tion, substitution, balance and gait; see Chapter 22) to de-
asked to turn their heads while walking. Another interpre- crease subjective complaints, impro ve visual acuity
tation is that these patients are more reliant on visual cues during head movement, and improve postural stability
to maintain postural stability , and thus, when the head during functional activities. Krebs et al, 1 in a double-
moves and visual cues are de graded, their balance be- blinded, placebo-controlled trial, found those patients
comes worse. The contribution of somatosensory cues performing customized vestibular and balance exercises
from the lower extremities to postural stability in patients had better stability while walking and during stair climb-
with BVL is also not well understood. Certainly some pa- ing than did patients performing isometric and condi-
tients are dependent on somatosensory cues rather than on tioning exercises, such as using an e xercise bicycle.
visual cues. Perhaps more importantly, we do not yet know Furthermore, the patients who had vestibular rehabilita-
how the degree of somatosensory loss affects postural sta- tion were able to walk faster. They used vestibular adap-
bility in these patients. tation and eye-head exercises as well as balance and gait
The loss of either visual or somatosensory cues in ad- training. In a continuation of this study , Krebs et al 4
dition to vestibular cues has a de vastating effect on pos- again demonstrated that, as a group, those indi viduals
tural control. Paulus et al 48 reported a case in which the performing the vestibular rehabilitation exercises had in-
patient had a complete bilateral vestibular loss plus a loss creased gait velocity, improved stability while walking,
of lower extremity proprioception. This patient relied on and decreased vertical excursion of the center of mass
visual cues to maintain his balance. When the effective- while walking. They noted a moderate correlation be-
ness of the visual cues w as degraded (i.e., by fixating on tween improved gait measures at 1 year and the fre-
a visual target more than 1 meter away), his postural sta- quency of performing the home e xercise program over
bility deteriorated significantly. Visual and somatosensory the preceding year. When the patients with BVL (n=51)
cues will not substitute fully for the lost vestibular contri- were combined with those with a UVL (n=33), 61% of
bution to postural stability.49-51 the patients demonstrated signif icant improvements in
their gait. Another study of patients with BVH demon-
strated improved visual acuity during head movement in
Compensatory Strategies patients with BVH. 5 In this double-blinded study, pa-
Patients can be taught, and often de velop on their own, tients were randomly assigned to either perform gaze sta-
strategies to use when in situations in which their balance bilization exercises (adaptation and substitution) or
will be stressed. For example, they learn to turn on lights placebo exercises (saccades, without head mo vement,
at night if they have to get out of bed. They may also wait, against a featureless background). As a group, patients
sitting at the edge of the bed, before getting up in the dark who performed the vestibular exercises had a significant
to allow themselves to awaken more fully and for their improvement in visual acuity during head movement, but
eyes to adjust to the dark ened room. They should be ad- the control group did not impro ve. Furthermore, 7 of 8
vised to use lights that come on automatically and to have patients who performed the e xercises improved com-
emergency lighting inside and outside the house in case pared with only 1 of 5 patients in the control group. Only
of a power failure. Patients may need to learn how to plan type of exercise was significantly correlated with change
3970_Ch23_432-456 25/06/14 1:59 PM Page 441
Chapter 23 • PHYSICAL THERAPY MANAGEMENT OF BILATERAL VESTIBULAR HYPOFUNCTION AND LOSS 441
in DVA. Other f actors examined, including age, time of visual and somatosensory information to impro ve pos-
from onset, and initial DVA, were not significantly cor- tural stability and the development of compensatory strate-
related with change in DVA. gies that can be used in situations where balance is stressed
The fact that not all patients with BVH improve with maximally (Boxes 23-3 and 23-4). This approach is also
a course of vestibular rehabilitation is documented in several used in the treatment of patients with unilateral v estibular
studies. Brown and colleagues noted that, as a group, the hypofunction (see Chapter 22).
patients (n=13) had significant improvements in various Once the patient’ s specific problems ha ve been
measures (Dizziness Handicap In ventory, Activities- identified, the exercise program can be established. Dur-
specific Balance Confidence Scale, Dynamic Gait Inde x, ing the initial sessions, particular attention should be paid
Timed “Up and Go” test, and Sensory Or ganization Test to the degree to which the exercises increase the patient’s
component of dynamic posturography).3 However, not all complaints of dizziness. The patient’s perception of
patients benefited to the same de gree. Brown and col- dizziness can be the major deterrent (limiting f actor) to
leagues noted that 33% to 55% of the patients demon- the patient’s eventual return to normal acti vities. Head
strated what were considered clinically significant changes movement, a component of all e xercises, may increase
on the different measures.3 In another retrospective study, that dizziness. Also, the home exercise program typically
Gillespie and Minor found that only 63% of the patients requires that the patient perform e xercises many times
with BVL that received vestibular rehabilitation demon- daily. Patients may find that they become increasingly
strated improvements (defined as reported increased activ- dizzy with each performance of the e xercises. It is im -
ity levels, reduced symptoms, and demonstrated normal portant to explain to the patient that some increase in
gait velocity, normal Romberg test, or normal DVA).2 More dizziness is expected when they begin the exercises and
recently, a study e xamined the outcome of v estibular with any increase in the intensity of the e xercises. One
rehabilitation in 69 patients with BVH. 10 They found a guideline to follo w is that an y increase in dizziness
significant improvement for the group as a whole for should decrease to pre-e xercise levels within 10 to
each outcome measure e xcept oscillopsia and disability 20 minutes. Additionally, limit the exercises that involve
(Table 23-3). However, for balance confidence, percentage head movement to only one exercise initially. Other ex-
of time symptoms interfered with acti vities, visual acuity ercises can be added and the frequenc y and duration of
during head movement, gait speed, and fall risk, a majority the exercises can be increased as the patient impro ves.
of, but not all, patients impro ved. The percentage of pa- Have the patient perform at least one complete set of all
tients who improved varied from 3.9% for head mo ve- exercises at the time of the clinic visit. P atients should
ment–induced dizziness to 81.3% for percentage of time also be taught how to modify the e xercises if the dizzi-
symptoms interfered with activities, depending on the spe- ness becomes overwhelming (Box 23-5). They should be
cific measurement (Table 23-3). The percentage of subjects strongly encouraged to contact the therapist if they con-
who had worse scores at dischar ge varied from 0% for tinue to have difficulty. In those patients in whom dizzi-
DVA, DGI, and dynamic posturography, to 28.6% for dis- ness continues to be a problem, we suggest medication
equilibrium intensity (Table 23-3). and stress reduction techniques, such as w alking, to try
Not all exercise approaches are appropriate for pa- to reduce the effect of the dizziness on the patient’s life.
tients with BVL. Telian et al53 studied the effectiveness of
a combination of balance exercises, vestibular habituation
Progression of Exercises
exercises, and general conditioning exercises for patients
with bilateral v estibular deficits. They were unable to Changing the duration of an y given exercise, the fre-
demonstrate a significant change in functional activity in quency of performance, and ho w many different exer-
these patients following treatment. Thus, vestibular habit- cises are given (Table 23-4) can modify the intensity of
uation exercises do not appear to be appropriate for these the exercise program to improve gaze stability. Patients
patients. This makes sense, because habituation exercises will find the exercises more challenging if they have to
are designed to decrease unwanted responses to vestibular perform them while standing as opposed to sitting.
signals rather than improve gaze or postural stability. Exactly which exercises are given initially and the pro-
gression itself will depend on the indi vidual patient.
Concurrent with the exercises to improve gaze stability,
Treatment of course, the patient should be instructed in e xercises
The treatment approach for patients with complete loss of to improve postural stability. Again, the initial exercise
vestibular function involves the combined use of gaze sta- program and the rate of progression should be cus-
bilization exercises and exercises that foster the substitution tomized for each patient.
■ Table 23-3 MEAN (5D) IN OUTCOME MEASURES FOR THE GROUP AT BASELINE AND AT DISCHARGE
442
% of Time Gait
Outcome Symptoms Disability DVA Speed
Measures oVAS dysVAS dzVAS ABC Interfere Score (LogMAR) (m/sec) DGI CDP
# of pre-post 28 35 26 32 16 23 23 31 47 15
comparisons
Baseline 2.7 ± 2.8 4.2 ± 2.2 3.1 ± 2.1 49.4 ± 20.5 72.7 ± 27.0 2.9 ± 1.1 0.323 ± 0.69 ± 0.22 13.5 ± 3.6 42.1 ± 9.9
0.107
Discharge 1.1 ± 1.5 2.1 ± 2.2 1.7 ± 2.5 68.3 ± 18.7 31.4 ± 24.9 2.1 ± 1.4 0.195 ± 0.84 ± 0.18 18.1 ± 3.0 53.1 ± 8.8
3970_Ch23_432-456 25/06/14 1:59 PM Page 442
0.102
Pre-post 0.006 (NS) 0.00002 0.0004 0.00004 0.0001 0.006 (NS) 0.00001 0.00001 0.00001 .00003
paired
comparison:
p value
% of 42.9% 45.7% 3.9% (n=1) 56.3% 81.3% 43.5% 73.9% 54.8% 61.7% 6.7% (n=1)
subjects (n=12) (n=16) (n=18) (n=13) (n=10) (n=17) (n=17) (n=29)
with
significant
improvement
% subjects 32.1% 17.1% 34.6% 28.1% 6.3% (n=1) 13.0% 52.2% 25.8% 36.2% 6.7% (n=1)
who (n=9) (n=6) (n=9) (n=9) (n=3) (n=12) (n=8) (n=17)
returned to (score (score (score
normal < 0.2) < 0.2) < 0.2)
Total 53.6% 45.7% 38.5% 62.5% 81.3% 47.8% 78.3% 61.3% 70.2% 6.7% (n=1)
subjects (n=15) (n=16) (n=10) (n=20) (n=13) (n=11) (n=18) (n=19) (n=33)
who
improved
or returned
to normal
Chapter 23 • PHYSICAL THERAPY MANAGEMENT OF BILATERAL VESTIBULAR HYPOFUNCTION AND LOSS 443
Box 23-3
Box 23-4
Continued
3970_Ch23_432-456 25/06/14 1:59 PM Page 444
444 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Box 23-4
X1 viewing paradigm against plain Maybe for less than Two or three times Sitting until can per-
stationary background; horizontal or 1 minute each time daily form the head move-
horizontal and vertical head movement ments easily and then
standing
X1 viewing paradigm against plain Increase to 1 minute Increase to five times Standinga
stationary background; horizontal or each exercise daily
horizontal and vertical head movement
3970_Ch23_432-456 25/06/14 1:59 PM Page 445
Chapter 23 • PHYSICAL THERAPY MANAGEMENT OF BILATERAL VESTIBULAR HYPOFUNCTION AND LOSS 445
X1 with target held in hand against a plain 1 minute each exercise Up to five times daily Standinga
background; horizontal and then vertical
head movements
Add eye-head exercises, horizontally and No specific duration Two to three times Sitting at first and then
vertically daily standing
X1 with target held in hand and also with 1 minute each exercise Two or three times Standinga
target at distance daily
Eye-head exercises, horizontally and No specific duration Two or three times Standinga if possible
vertically daily
X1 with target held in hand and also with 1 minute each exercise Four times daily Standinga
target at distance
Eye-head exercises, horizontally and No specific duration Four times daily Standinga
vertically
Add imaginary target exercise No specific duration Four times daily Sitting at first and then
standing
X1 with target held in hand and also with 1 minute each exercise Four times daily Standinga
target at distance
Eye-head exercises, horizontally and No specific duration Four times daily Standinga
vertically
Some patients may be able to progress to 1 minute each exercise Four times daily Standinga
X2 with target held in hand and also with
target at distance
Eye-head exercises, horizontally and No specific duration Four times daily Standinga
vertically
X1 with target held in hand and also with 1 minute each exercise Four times daily Standinga
target at distance
Eye-head exercises, horizontally and No specific duration Four times daily Standinga
vertically
Add finding numbers written randomly on No specific duration Twice daily Stand and step to touch
large (6 ft by 5 ft) checkerboard pattern number
placed on wall
aThe exercise can be made more difficult by changing the base of support (e.g., from feet apart to feet together).
3970_Ch23_432-456 25/06/14 1:59 PM Page 446
446 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
recovery of visual acuity during head mo vement.5 A that he or she w ould like to enjoy these activities more,
more comprehensive study examined the relationship of then the clinician can look at the initial measures of dise-
patient characteristics, subjective complaints, and phys- quilibrium and fall risk (DGI) scores as a guide as to what
ical function to outcome. 10 In agreement with other to expect for outcome. Values that initially are closer to
studies, they found that age did not contrib ute to normal would suggest that the patient should impro ve in
whether a patient impro ved or returned to normal— the primary goal.
older patients were just as likely as younger patients to
improve. Several specific comorbidities had f air to
strong correlations with certain outcome measures. For Comparison with Patients with
example, a history of headaches w as correlated with a Chronic Unilateral Vestibular
higher percentage of time symptoms interfered with ac- Hypofunction (UVH)
tivities, with lower balance confidence and a greater in- One of the surprising findings is that patients with BVH
tensity of head mo vement–induced dizziness at and patients with UVH have similar results on initial as-
discharge. When lower extremity sensory def icits or sessment (Table 23-5).10,54 The only differences appear
Ménière’s disease were present, patients w alked more to be that patients with BVH walk more slowly and have
slowly at discharge. In addition to the presence of spe- a greater percentage of time that symptoms interfere
cific comorbidities correlating with outcome, the num- with activities. The primary difference is in the level of
ber of comorbidities af fected outcome such that the recovery reached by the tw o groups (Table 23-6). For
greater the number of comorbidities, the worse the dis- most measures of subjective complaints, a smaller per-
ability at discharge. Another important finding was that centage of patients with BVH impro ve significantly
the longer the time from onset until the initiation of compared with patients with UVH.
vestibular rehabilitation, the poorer the balance conf i-
dence at discharge. Loss of both superior and inferior
nerve function was correlated with worse complaints of Guidelines to Treatment and Prognosis
oscillopsia at discharge. Higher intensity of disequilib- There are several factors to remember when working with
rium initially was correlated with worse balance confi- patients with bilateral vestibular deficits:
dence, poorer disability, and higher percentage of time
symptoms interfered with activities at discharge. Simi- 1. The patient’s perception of dizziness can be the
larly, poor DGI score initially correlated with lower bal- major deterrent to the patient’s return to normal
ance confidence, poorer disability scores, and poorer the activities.
DGI scores at discharge. 2. Recovery following bilateral deficits is slower
How do you use this information? One way is to first than for unilateral lesions and can continue to
identify your patient’s primary goal(s). For example, if the occur over a 2-year period,
patient states that his or her main problem is that the symp- 3. Recovery is easily upset by other medical prob-
toms (dizziness with head movement, oscillopsia, disequi- lems such as having a cold or receiving
librium) interfere with both leisure and work activities and chemotherapy.
Outcome
measures oVAS dysVAS DRS % TSI ABC GS DGI DVA
UVH: 3.1 ± 2.7 3.97 ± 2.5 2.9 ± 0.95 59 ± 29.8 51.5 ± 16.9 0.80 ± 0.15 14.2 ± 4.0 .327 ± 0.134
Baseline
score
BVH: 3.0 ± 2.2 4.2 ± 2.2 2.9 ± 1.1 72.7 ± 27.0 49.4 ± 20.5 0.69 ± 0.22 13.5 ± 3.6 .323 ± 0.107
Baseline
score
Chapter 23 • PHYSICAL THERAPY MANAGEMENT OF BILATERAL VESTIBULAR HYPOFUNCTION AND LOSS 447
■ Table 23-6 COMPARISON OF OUTCOMES FOR PATIENTS WITH BVH AND UVH
Outcome
Measures oVAS dysVAS DRS % TSI ABC GS DGI DVA
UVH:
discharge 0.79 ± 1.65 1.58 ± 1.91 1.39 ± 1.4 24 ± 30.1 78.5 ± 16.0 1.01 ± 0.17 19.8 ± 3.0 0.210 ± 0.138
BVH: 1.1 ± 1.5 2.1 ± 2.2 2.1 ± 1.4 31.4 ± 24.9 68.3 ± 18.7 0.84 ± 0.18 18.1 ± 3.0 0.195 ± 0.102
discharge
4. To maintain recovered function, patients may al- have been emplo yed in an attempt to replace the lost
ways need to be doing some exercises, at least vestibular function. Although these devices have shown
intermittently. potential benefits, the devices are solely focused on im-
5. Postural stability will never be completely nor- proving postural control, not on improving gaze stability
mal. The patient may have a negative Romberg during head movements. With the success of cochlear im-
and may be able to maintain the Sharpened plants, several labs have been working on developing a
Romberg position with eyes open, but not with vestibular prosthesis. The basic design is that sensors will
eyes closed. detect and measure the directions of rotation and then
6. Initially, the patient may need to use a cane or electrically stimulate the appropriate ampullary nerv es.
a walker while ambulating. Some patients, es- The majority of the w ork to date has been performed in
pecially older patients, need to use a cane at bilaterally vestibular–deficient chinchillas and monkeys.
least some of the time. Most patients, however, Della Santina and colleagues ha ve demonstrated partial
are eventually able to walk without any assis- restoration of the angular VOR to horizontal, as well as
tive devices. Ambulation during the acute stage RALP (right-anterior, left-posterior) and LARP (left-
will be wide-based and ataxic with shortened anterior, right-posterior) rotations with unilateral implan-
stride length and side-stepping to the right and tation of the v estibular prosthesis in chinchillas treated
left. The patient will turn en bloc, and turning with gentamicin.55 In addition to the angular VOR im-
the head will cause increased instability. Am- provements, they noted improved postural stability in the
bulation will improve, but again, it will not be animals as well. Similar impro vements in angular VOR
normal. responses were observed in rhesus monkeys with bilateral
7. Patients will be at increased risk for falls when vestibular deficits after unilateral implantation of the
walking in low-vision situations, over uneven vestibular prosthesis.56 Even though the responses were
surfaces, or when they are fatigued. not normal, the responses were strong and had similar dy-
namics to normal animals, and the implanted animals had
not undergone any adaptation treatments with the vestibu-
Future Treatment lar prosthesis. These studies bode well for future implan-
Various devices and technologies, such as auditory cues, tation of a vestibular prosthesis in humans with bilateral
tactile cues applied to the torso, and stimulation of the vestibular hypofunction, which may, in combination with
tongue (see Chapter 28: The Role of Emerging Technolo- rehabilitation, lead to impro ved function and decreased
gies in Vestibular Rehabilitation for a detailed re view) disability.
3970_Ch23_432-456 25/06/14 2:00 PM Page 448
448 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Chapter 23 • PHYSICAL THERAPY MANAGEMENT OF BILATERAL VESTIBULAR HYPOFUNCTION AND LOSS 449
Figure 23.3 Results from bithermal caloric irrigation of the external auditory canals in a
patient with profound bilateral vestibular hypofunction. SCV = Slow component velocity.
Continued
3970_Ch23_432-456 25/06/14 2:00 PM Page 450
450 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Chapter 23 • PHYSICAL THERAPY MANAGEMENT OF BILATERAL VESTIBULAR HYPOFUNCTION AND LOSS 451
Comment
0.0
This patient’s signs and symptoms (vertigo, disequi-
librium, oscillopsia, spontaneous n ystagmus, and
poor VOR) certainly were suggestive of a vestibular
disorder. Furthermore, her history included multiple VOR 240
treatments with gentamicin, an ototoxic medication.
With bilateral dysfunction from treatment with an 0 10 20 30
ototoxic drug, the symptoms of oscillopsia and dis - Time, sec
equilibrium develop over time and may not appear
until after the drug treatment is f inished. Once the Figure 23.4 Plot of the decay in slow-phase eye ve-
symptoms appear, they may continue to become locity with time during VOR after nystagmus. Patient
is first rotated in a chair in complete darkness for
worse for several weeks. With some patients, there is 2 minutes, and then the chair is stopped. The slow-
a partial reversal of symptoms with time. Depending phase eye movements that occur are caused by the dis-
on the aminoglycoside used, v estibular symptoms charge of the velocity storage system and represent the
may be accompanied by hearing loss. Gentamicin has function of the vestibular system. These results show
primarily vestibulotoxic effects. It is unusual for the poor peak slow-phase eye velocity (35 deg/sec) and
the short time constant (less than 2 sec) in a patient with
systemic gentamicin to result in v ertigo and nystag- bilateral vestibular loss. A step rotation at 240 deg/sec
mus, because that indicates asymmetrical v estibular was used. Eye movements were recorded using
function. Although gentamicin usually results in electro-oculography.
Continued
3970_Ch23_432-456 25/06/14 2:01 PM Page 452
452 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Chapter 23 • PHYSICAL THERAPY MANAGEMENT OF BILATERAL VESTIBULAR HYPOFUNCTION AND LOSS 453
Figure 23.5 Hearing test results from patient with gentamicin ototoxicity. Circles and trian-
gles indicate right ear, and Xs and squares indicate left ear, respectively. Note asymmetry in
hearing loss for this patient.
Continued
3970_Ch23_432-456 25/06/14 2:01 PM Page 454
454 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Summary 3. Brown KE, Whitney SL, Wrisley DM, Furman JM. Physical
therapy outcomes for persons with bilateral vestibular loss.
Studies have shown that the worse disability is in part de- Laryngoscope. 2001;111:1812.
pendent on the number of comorbidities the patient has as 4. Krebs DE, Gill-Body KM, Parker SW, et al. Vestibular
rehabilitation: Useful but not universally so. Otolaryngo
well as greater initial intensity of disequilibrium, lo wer Head Neck Surg. 2003;128:240.
balance confidence, and poor fall risk scores. Patients with 5. Herdman SJ, Hall CD, Schubert M, Das VE, Tusa RJ.
bilateral vestibular problems can be expected to return to Recovery of dynamic visual acuity in patients with
many activities but will continue to have problems in cer- bilateral vestibular hypofunction. Arch Otolaryngol Head
tain areas. They will be able to ambulate without the use Neck Surg. Apr 2007;133(4):383.
6. Zingler VC, Cnyrim C, Jahn K, Weintz E, Fernbacher J,
of a cane or walker, at least when they are in well-lighted Frenzel C, et al. Causative factors and epidemiology of
environments.59 Patients should be able to return to work, bilateral vestibulopathy in 255 patients. Ann Neurol. Jun
but it may be necessary to find a different occupation. Pa- 2007;61(6):524.
tients often report difficulty driving, particularly in the rain 7. Rinne T, Bronstein AM, Rudge P, Gresty MA, Luxon LM.
or snow or at night or on high-speed roads, but actual driv- Bilateral loss of vestibular function: clinical findings in 53
patients. J Neurol. Jun-Jul 1998;245(6-7):314.
ing habits and accidents do not dif fer from subjects with 8. Rinne T, Bronstein AM, Rudge P, Gresty MA, Luxon LM.
normal vestibular function.60,61 Treatment approaches in- Bilateral loss of vestibular function. Acta Otolaryngol
clude increasing the function of the remaining v estibular Suppl. 1995;520 Part 2:247.
system, inducing the substitution of alternati ve mecha- 9. Herdman SJ, Blatt PJ, Schubert MC, Tusa RJ. Falls in pa-
nisms to maintain gaze stability and postural stability dur- tients with vestibular deficits. Am J Otology. 2000;21:847.
10. Herdman SJ, Hall, et al. 2013 (submitted for publication).
ing head movements, and modifications of the home and 11. Schubert MC, Herdman SJ, Tusa RJ. Vertical dynamic vi-
working environment for safety. sual acuity in normal subjects and subjects with vestibular
hypofunction. Otology Neurotology. 2002;23:372-377.
12. Guinand N, Pijnenburg M, Janssen M, Kingma H. Visual
References acuity while walking and oscillopsia severity in healthy
1. Krebs DE, et al. Double-blind, placebo-controlled trial of subjects and patients with unilateral and bilateral vestibu-
rehabilitation for bilateral vestibular hypofunction: Prelimi- lar function loss. Arch Otolaryngol Head Neck Surg.
nary report. Otolaryngol Head Neck Surg. 1993;109:735. Mar 2012;138(3):301.
2. Gillespie MB, Minor LB. Prognosis in bilateral vestibular 13. Crawford J. Living without a balance mechanism. New
hypofunction. Laryngoscope. 1999;109:35. Engl J Med. 1952;246:458.
3970_Ch23_432-456 25/06/14 2:01 PM Page 455
Chapter 23 • PHYSICAL THERAPY MANAGEMENT OF BILATERAL VESTIBULAR HYPOFUNCTION AND LOSS 455
14. Brandt T, et al. Visual acuity, visual field and visual scene Zee DS, (eds). Vertigo and Imbalance: Clinical Neuro-
characteristics affect postural balance. In: Igarashi M, physiology of the Vestibular System. Amsterdam: Elsevier;
Black FO, eds. Vestibular and Visual Control on Posture 2009:181.
and Locomotor Equilibrium. Karger: Basel; 1985:93. 34. Bles W, et al. Compensation for labyrinthine defects
15. Hewitt WL. Gentamicin toxicity in perspective. Postgrad examined by use of a tilting room. Acta Otolaryngol.
Med J. 1974;50(suppl 7):55. 1983;95:576.
16 Fee WE. Aminoglycoside otoxicity in the human. 35. Cavanaugh JT, Goldvasser D, McGibbon CA, Krebs DE.
Laryngoscope. 1980;90:1. Comparison of head- and body-velocity trajectories during
17. Lerner SA, Schmitt BA, Seligsohn R, Matz GJ. Compara- locomotion among healthy and vestibulopathic subjects
tive study of ototoxicity and nephrotoxicity in patients ran- J Rehab Res and Development. 2005;42:2, March/April
domly assigned to treatment with amikacin or gentamicin. 2005:191.
Am J Med. 1986;30:98. 36 Kasai T, Zee DS. Eye-head coordination in labyrinthine-
18. Schacht J. Aminoglycoside ototoxicity: Prevention in defective human beings. Brain Res. 1978;144:123.
sight? Otolaryngol Head Neck Surg. 1998;118:674. 37 Barnes GR. Visual-vestibular interaction in the control of
19. Hall CD, Herdman SJ. Reliability of clinical measures head and eye movement: The role of visual feedback and
used to assess patients with peripheral vestibular disorders. predictive mechanisms. Prog Neurobiol. 1993;41:435.
J Neurol Phys Ther. 2006;30:74. 38. Tian J, Crane BT, Demer JL. Vestibular catch-up
20. Jacobson GP, Newman CW. The development of the saccades in labyrinthine deficiency. Exp Brain Res.
dizziness handicap inventory. Arch Otolaryngol Head 2000;131:448.
Neck Surg. 1990;116:424. 39. Tian J, Jr, Shubayev I, Demer JL. Dynamic visual acuity
21. Morris AE, Lutman ME, Yardley L. Measuring outcome during passive and self-generated transient head rotation
from vestibular rehabilitation, part II: refinement and in normal and unilaterally vestibulopathic humans. Exp
validation of a new self-report measure. Int J Audiol. Brain Res. 2002;142:486.
Jan 2009;48(1):24. 40. Schubert MC, Hall CD, Das V, Tusa RJ, Herdman SJ.
22. Myers AM, Powell LE, Maki BE, Holliday PJ, Brawley LR, Oculomotor strategies and their effect of reducing
Sherk W. Psychological indicators of balance confidence: gaze position error. Otology Neurotology. Feb
relationship to actual and perceived abilities. J Gerontol. 2010;31(2):228-231.
1996; 51A(1):M37. 41. Weber KP, Aw ST, Todd MJ, McGarvie LA, Curthoys IS,
23. Myers AM, Fletcher PC, Myers AH, Sherk W. Halmagyi GM. Head impulse test in unilateral vestibular
Discriminative and evaluative properties of the loss: vestibulo-ocular reflex and catch-up saccades.
Activities-specific balance confidence (ABC) scale. Neurology. Feb 5 2008;70(6):454.
J Gerontol Med Sci. 1998;53A:M287. 42. Macdougall HG, Curthoys IS. Plasticity during vestibular
24. Cohen HS, Kimball KT, Adams AS. Application of compensation: the role of saccades. Front Neurol.
the vestibular disorders activities of daily living scale. 2012;3:21.
Laryngoscope. Jul 2000;110(7):1204. 43. Bockisch CJ, Straumann D, Hess K, Haslwanter T. En-
25. Alghwiri AA, Whitney SL, Baker CE, Sparto PJ, Marchetti hanced smooth pursuit eye movements in patients with
GF, et al. The development and validation of the vestibular bilateral vestibular deficits. Neuroreport. 2004;15:2617.
activities and participation measure. Arch Phys Med Rehabil. 44. Bronstein AM, Hood JD. The cervico-ocular reflex in nor-
Oct 2012;93(10):1822. mal subjects and patients with absent vestibular function.
26. Black FO, et al. Vestibular reflex changes following Brain Res. 1986;373:399.
aminoglycoside induced ototoxicity. Laryngoscope. 45. Chambers BR, et al. Bilateral vestibular loss, oscillopsia,
1987;97:582. and the cervico-ocular reflex. Otolaryngol Head Neck
27. Esterhai JL, et al. Gentamicin-induced ototoxicity compli- Surg. 1985;93:403.
cating treatment of chronic osteomyelitis. Clin Orth Related 46. Bronstein AM, Morland AB, Ruddock KH, Gresty MA.
Res. 1986;209:185,. Recovery from bilateral vestibular failure: implications for
28. Szturm T, et al. Comparison of different exercise programs visual and cervico-ocular function. Acta Otolaryngol
in the rehabilitation of patients with chronic peripheral Suppl. 1995;520 Pt 2:405.
vestibular dysfunction. J Vestib Res. 1994;4:4614. 47. Bles W, et al. Postural and oculomotor signs in
29. Scherer M, Schubert MC. High-velocity angular vestibulo- labyrinthine-defective subjects. Acta Otolaryngol (Stockh).
ocular reflex adaptation to position error signals. J Neurol 1984;406:101.
Phys Ther. Jun 2010;34(2):82. 48 Paulus WM, et al. Visual stabilization of posture. Brain.
30. Westheimer G, and McKee SP. Visual acuity in the presence 1984;107:1143.
of retinal-image motion. J Optical Soc Am. 1975;65:847. 49 Diener HC, et al. The significance of proprioception on
31. Herdman SJ, et al. Computerized dynamic visual acuity postural stabilization as assessed by ischemia. Brain Res.
test in the assessment of vestibular deficits. Am J Otol. 1984;296:103.
1998;19:790. 50. Diener HC, et al. Stabilization of human posture during
32. Venuto PJ, et al. Interrater reliability of the clinical dynamic induced oscillations of the body. Exp Brain Res.
visual acuity test. Scientific Meeting and Exposition of 1982;45:126.
the American Physical Therapy Association. Orlando, FL, 51. Dichgans J, Brandt T. Visuo-vestibular interactions.
June 6, 1998. Effects on self-motion perception and postural control.
33. Herdman SJ. Computerized Dynamic Visual Acuity Test In: Held R, et al, eds. Handbook of Sensory Physiology.
in the assessment of vestibular deficits. In: Eggers S, Berlin: Springer; 1978:755.
3970_Ch23_432-456 25/06/14 2:01 PM Page 456
456 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
52. Igarashi M, et al. Physical exercise and balance compensa- 56. Dai C, Fridman GY, Davidovics NS. Restoration of 3D
tion after total ablation of vestibular organs. In: Pompeiano vestibular sensation in rhesus monkeys using a multichan-
O, Allum JHJ, eds. Progress in Brain Research. Amsterdam: nel vestibular prosthesis. Hear Res. 2011;281(1-2):74.
Elsevier; 1988:395. 57. Bohannon RW. Comfortable and maximum walking speed
53. Telian SA, et al. Bilateral vestibular paresis: Diagnosis of adults aged 20-79 years: reference values and determi-
and treatment. Otolaryngol Head Neck Surg. 1991; nants. Age Aging. 1997;26(1):15.
104:67. 58. Shepard NT, et al. Vestibular and balance rehabilitation
54. Herdman SJ, Hall CD, Delaune W. Variables associated therapy. Ann Otol Rhinol Laryngol. 1993;102:198.
with outcome in patients with unilateral vestibular 59. McCall AA, Yates BJ. Compensation following bilateral
hypofunction. Neurorehabil Neural Repair. 2012;2 vestibular damage. Front Neurol. 2011;2:88.
6(2):151. 60. Cohen HS, Wells J, Kimball KT, Owsley C. Driving
55. Della Santina CC, Migliaccio AA, Hayden R, et al. Current disability and dizziness. J Safety Res. 2003;34(4):361.
and future management of bilateral loss of vestibular 61. MacDougall HG, Moore ST, Black RA, Jolly N, Curthoys
sensation – an update on the Johns Hopkins Multichannel IS. On-road assessment of driving performance in bilateral
Vestibular Prosthesis Project. Cochlear Implants Int. vestibular-deficient patients. Ann N Y Acad Sci. 2009
2010;11(Suppl 2):2. May;1164:413.
3970_Ch24_457-479 25/06/14 12:34 PM Page 457
CHAPTER 24
Physical Therapy
Management of
Children with
Vestibular
Dysfunction
Rose Marie Rine, PT, PhD ■ Jennifer Braswell Christy, PT, PhD
The vestibular system develops relatively early in gesta- impairments, the development of postural control and ocu-
tion.1-4 The vestibular system is composed of v estibulo- lomotor abilities, and appropriate testing and intervention
ocular and vestibulospinal subsystems, each with distinct for this population.
tasks and each requires different methods of assessment.
Labyrinthine reflexes, which are mediated by the vestibu- Incidence of Vestibular Deficits in
lospinal system, provide postural tone necessary for the
emergence of early motor milestones (e.g., rolling, sitting, Children and Related Functional
standing).5-7 The role of the v estibulo-ocular system in Impairments
visual stabilization, acuity, and the development of visual
Common Diagnoses of Vestibular
spatial and perception abilities has been well docu-
Dysfunction and the Etiology of Vertigo
mented.8-11 It is therefore logical to deduce that individuals
in Children
with deficits of the v estibular system since birth or v ery
early in life will present with dif ficulties in either motor In the last decade, there is increased evidence in the liter-
or visuospatial abilities or both.12,13 ature of vestibular dysfunction or v ertigo of various eti-
The functional integrity of the v estibular system is ologies and consequent functional impairments in children
rarely tested in young children, and thus impairments can (Table 24-1).15-24 Lesions of the vestibular system may be
be undetected and untreated. This may be in part a result peripheral (either unilateral or bilateral) or central in na-
of the child’s inability to describe symptoms or even know ture. Each has dif fering signs and symptoms that can
that what they are experiencing is not “normal.”14,15 One change from the acute to chronic stage.
of the major difficulties in the identification of vestibular
dysfunction in children has been the unavailability or the Vertigo
omission of the use of traditional and more recently de- Vertigo is typical of acute unilateral peripheral v estibular
veloped tests of vestibular function with this population. hypofunction but is not common in bilateral peripheral
This chapter will provide a review of the types and inci- deficits. Furthermore, symptoms can be acute, progressive,
dence of v estibular deficits in young children, related or chronic. The most comprehensive study completed to
457
3970_Ch24_457-479 25/06/14 12:34 PM Page 458
458 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
AUTHORS
Causes of Vertigo
Metabolic — 6.0% — — —
Demyelination — — — — 5.0%
date regarding the varying etiologies of vertigo and their Many children and/or parent(s) may not identify v ertigo
incidence was done by Wiener-Vacher,15 who investigated or imbalance, which suggests an underestimation of the
the causal mechanisms of v ertigo in over 2,000 children problem.20
seen in otolaryngology. Similar to other reports, 15-17,27
Wiener-Vacher15 reported that the most common causes of BPVC, BPPV, and Migraine
vertigo and/or imbalance were migraine-associated dizzi- BPVC has been identified as a common cause of v ertigo
ness (25%) and benign paroxysmal vertigo of childhood in young children. It is therefore important to note that
(BPVC; 20%). It should be noted that in all these studies, BPVC is not the same as benign paroxysmal positional
only children referred to otolaryngology were included. vertigo (BPPV). BPVC typically is seen in children less
3970_Ch24_457-479 25/06/14 12:34 PM Page 459
than 7 years of age, with vertigo lasting less than 10 minutes Jacot et al 44 followed over 200 children who recei ved
and no associated headache. Vestibular and otological cochlear implants. Fifty percent had normal v estibular
exams are typically normal. A child may not complain of function before sur gery. Cochlear implantation altered
dizziness, but autonomic signs (pallor , nausea) may be vestibular function in 71% of the children who previously
noted. Children may or may not present with typical mi- had vestibular function (10% had areflexia). Cochlear im-
graine later in life.28 Although BPPV has been reported in plantation altered vestibular function in 51% of the entire
children,21,29 its incidence is much lower in children than cohort of children with and without vestibular function be-
in adults.30 Vestibular migraine is a common cause of ver- fore surgery. This necessitates that v estibular function
tigo in children. 15,27,30,31 Vertigo may last hours or days testing should be performed both before and after
and might be independent of headache. A double-blind, cochlear implantation so that functional impairments can
dose-comparison trial showed that preventative therapy be addressed.
with topiramate reduced the frequency of basilar migraine
attacks in children by 50% and the duration of attacks by Developmental Disabilities
as much as 89 minutes.32 and Prematurity
Recent reports suggest that learning disabilities and other
Otitis Media diagnoses may have vestibular involvement.45,46 Franco
Otitis media with effusion (OME) is typically associated and Panboca45 examined vestibular function in children
with conductive hearing loss and speech delay in children. underperforming in school and found that 67.4% of them
However, evidence exists that OME may also cause bal- had unilateral or bilateral irritati ve peripheral vestibular
ance impairments and dizziness. The mechanism for these deficits. Compared with children without learning disor -
impairments is unclear.33,34 Balance impairments in chil- ders, these children had v alues above the normal range
dren with OME are often reversed following insertion of with cold thermal stimulation and abnormal accuracy with
tympanostomy tubes.33,35-38 Abnormal electronystagmog- saccadic testing. In another study,46 children with learning
raphy (ENG) to include spontaneous and positional disabilities and irritative peripheral vestibular findings also
nystagmus in children with acute OME also resolved fol- had behavioral abnormalities to include difficulties skip-
lowing insertion of tympanostomy tubes. 35,38 However, ping, playing hopscotch, and riding a bic ycle. Although
Casselbrandt et al 39 reported that children with a history the exact neural mechanism behind v estibular hyperex-
of OME had persistent decreased gain for rotary stimuli citability has not been studied, the behaviors exhibited by
at 0.1 Hz compared with controls without a history these children are similar to those with developmental co-
of OME. This demonstrates that OME, even when treated ordination disorder (DCD). Children with DCD have poor
with tympanostomy tubes, might cause long-lasting balance, poor coordination, and dif ficulty organizing
changes to the vestibular system. movements. Imaging studies have shown that the corti-
cospinal pathways, posterior thalamic pathways, and the
Sensorineural Hearing Loss parietal lobe are affected in children with DCD.47,48 How-
Often, children with se vere or profound sensorineural ever, peripheral vestibular function has not been tested in
hearing loss (SNHL) have concurrent bilateral vestibular this population. Eviatar and Eviatar49 used per-rotary and
hypofunction.15,22 Tribukait et al 22 reported that 70% of cold caloric stimulation to examine vestibular function in
children with SNHL since birth had some form of periph- full-term and premature infants. They reported that in pre-
eral vestibular dysfunction, typically hypofunction, mature, low birth weight infants, there was a maturational
(as confirmed by rotary, caloric, and v estibular evoked delay in vestibular system function evidenced by longer
myogenic potential [VEMP] tests. Unfortunately, these in- latency and smaller frequenc y, amplitude, and speed of
vestigators did not report associated impairments in func- slow component eye movements compared with the nor-
tion. Others have reported motor and balance def icits in mative sample. Complete maturation w as attained in all
young children with SNHL and evidence of vestibular hy- infants by 12 months of age.
pofunction as measured by rotary, caloric, and/or VEMP
tests).13,40-43 Because children with sensorineural hearing Other Potential Causes of Vertigo
impairment (SNHI) typically have bilateral vestibular hy- or Vestibular Related Impairments
pofunction, this group does not present with nystagmus or One of the risks of aminoglycoside antibiotics is periph-
vertigo. In spite of these reports, children with SNHI are eral vestibular hypofunction.50-52 In one study,51 peripheral
not routinely tested for v estibular function. The impor- hypofunction, as measured by ENG with caloric irrigation,
tance of testing is particularly rele vant for the children was reported in 30.4% of young adults (mean age
with SNHI who are candidates for cochlear implantation. 23 years) with c ystic fibrosis who received tobramycin
3970_Ch24_457-479 25/06/14 12:34 PM Page 460
460 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
(0.87% unilateral and 21.7% bilateral). Another study of presented with delayed maturation of v estibular and vi-
infants who received gentamicin at birth52 reported no sig- sion ratios on posturography testing (Fig. 24.1). These
nificant differences in vestibular responses as measured children also had a progressive delay in gross motor de-
by rotary chair between patients and controls at 12 months velopment as measured by the Peabody De velopmental
of age. The conclusion was that the vestibulotoxic effects Motor Scales Test. Inoue et al43 published a retrospective
of gentamicin in controlled doses at birth had less of a chart review of 89 children with profound SNHI who
vestibulotoxic effect than in older children or adults. were to undergo cochlear implant surgery. The children
Benign paroxysmal torticollis of inf ancy (BPTI) is were tested using rotary chair , caloric, and cervical
characterized by recurrent episodes of head tilt with asso- VEMP tests. Twenty percent showed abnormal rotary
ciated vomiting, pallor, agitation, and ataxia that subsides chair tests, 41% had an abnormal caloric test, and 42%
within a few hours or days. After 5 years of age, BPTI typ- had an abnormal VEMP test. Children with abnormal
ically evolves into a migraine syndrome such as benign vestibular function tests developed head control and in-
paroxysmal vertigo of childhood (BPVC). 53,54 Formal dependent walking significantly later than typically de-
vestibular function testing has not been done in this veloping children. Shall 13 reported that children with
population. hearing loss since birth and def icits on VEMP testing
Although children can ha ve vestibular dysfunction, scored lower on tests of motor de velopment than those
the results of some reports should be questioned, because with hearing loss and normal saccular function based on
they lack diagnostic vestibular testing or lack positive test VEMP testing. These findings concur with the report by
results. Furthermore, identification of vestibular dysfunc- Weiner-Vacher,4 who reported that the acquisition of
tion may be confounded by the plasticity of the nerv ous walking ability was related to measures of otolith, not
system in response to injury. canal, vestibular function.
Horak et al59 found that adults with bilateral periph-
Plasticity of the Nervous System eral vestibular hypofunction since birth did not demon-
Confounds Identification strate the lack of le g muscle responses to perturbations
of Vestibular Dysfunction evident in adults who had adult onset bilateral v estibular
Investigations of plasticity and recovery of function sup- loss. However, activation of trunk muscles w as delayed
port the idea that age at the time of injury and age at the and smaller in amplitude in the early onset group as com-
time of testing af fect results obtained on tests of func- pared with either those without a def icit, or those with
tion.55 Recovery of function is well documented and evi-
denced on vestibular tests of adults with unilateral lesions
of the peripheral vestibular apparatus, in spite of the f act 1
Comparison of Mean Ratio Scores - All Ages
that the peripheral apparatus does not re generate or re-
cover. Based on evidence that neural changes occur in in- 0.9
adult onset deficit. These results suggest that somatosen- suggests sensory organization impairment of a central
sory inputs from the cervical and upper trunk areas com- nature. Nashner, Shumway-Cook, and Marin 64 and
pensated for the vestibular loss in the early onset b ut not others61,65 reported similar results, as well as a re versal
the adult onset group. In contrast, Rine et al 41 noted de- of muscle activation patterns in children with cerebral
layed leg muscle responses on dynamic balance testing, palsy. However, in none of these studies w as vestibular
and deficient re-weighting of sensory cues during postur- function formally tested.
ography testing in young children with bilateral vestibular Benign Paroxysmal Vertigo of Childhood (BPVC) is
hypofunction since birth (see Fig. 24.1). a migraine-related vertigo syndrome occurring most often
In addition to the motor and balance impairments, in children between 2 and 6 years of age. It causes vertigo
Braswell and Rine11 reported that children with confirmed lasting seconds to minutes with associated n ystagmus,
vestibular hypofunction (rotary testing) f ailed tests of postural imbalance, and nausea and v omiting. Vestibular
dynamic visual acuity and had impaired reading acuity . impairments are not evident between attacks.66 However,
This impairment of gaze stability may contrib ute to the a study by Zhang et al 30 showed that of 56 children with
problems in school performance that have been reported. BPVC studied, 14.3% had abnormal bithermal caloric
Despite the documented functional relationship of the tests and 32.1% had abnormal cervicalVEMP tests. High-
visual and vestibular systems, and the effect vestibular de- stimulus auditory brainstem responses and Transcranial
ficiency may have on gaze stability and oculomotor con- Doppler sonography tests were abnormal in 48.2% of the
trol,10,11 children with visuomotor deficits on educational cases. These results suggest that BPVC is a vascular event
or developmental testing are rarely tested for concurrent and related to migraine syndrome. Authors also suggest
vestibular function or gaze stabilization deficits. However, that the inferior vestibular pathway is more damaged than
interpretation of test results may be compounded by the superior vestibular pathway.
changes caused by adaptation or plasticity. The identification of a vestibular deficit is important
The variation of clinical symptoms seen with a pe- to the development of appropriate interv ention and for
ripheral vestibular deficit sustained early in life, versus in prognostic purposes. Further research is needed in this
adulthood, may also be e vident in children with central area, particularly because early identif ication and inter-
vestibular deficits. vention during critical periods may affect recovery.
In summary, children, like adults, can and do ha ve
central and peripheral v estibular deficits. Reportedly, a
Impairments with Central
delay in acquisition of motor skills and learning disabili-
Vestibular Deficits
ties is e vident in children with peripheral and central
Although vestibular and postural control def icits have
vestibular dysfunction. To understand the implication of
been documented in adults with central nerv ous system
vestibular deficits early in life, and to enable the selection
involvement, similar investigations of children are scarce
and interpretation of testing and the de velopment of ap-
(see Chapter 5 on central v estibular disorders).60-63 It is
propriate intervention for children, a review of the devel-
logical to assume that children with traumatic brain injury
opment of postural and oculomotor control as they relate
or other acquired central nerv ous system conditions will
to vestibular function is warranted.
present with vestibular deficits similar to those of adults.
However, because of maturation issues in volved in the
development of postural control, and particularly the
effectiveness of vestibular function in postural control, the
Development of Postural
consequences to motor reco very may differ, and varied and Oculomotor Control
mechanisms of compensation and adaptation may mask as They Relate to Vestibular
vestibular deficits.
Liao et al 63 reported poor static postural control
System Function
under various sensory en vironments in children with Functional maturation of the vestibular and visual systems
spastic cerebral palsy. The children had normal vision for postural control continues through 15 years of age67,68
and somatosensation. Although it is e xpected that the with the following noted: (1) although visual system ef-
muscle tone impairment involved is to a great deal re- fectiveness in postural control is less mature than that of
sponsible, the fact that postural sw ay was significantly the somatosensory system before age 7.5 years, it is the
different between children with and without impairment dominant source of information for postural control in
only on the sw ayed surface (SS), eyes closed—swayed standing69-71; (2) vestibulo-ocular mechanisms are intact
surface (ECSS), and sw ayed vision—swayed surface and mature by 1 year of age 72; (3) vestibular system ef -
conditions (SVSS), and similar in all other conditions, fectiveness for gaze stabilization is mature by 3 years of
3970_Ch24_457-479 25/06/14 12:34 PM Page 462
462 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
is a vestibular pathology requires a team effort and compre- have normative data and are standardized for children
hensive testing. include:
• Functional Reach Test,85,86
Evaluation of Children with • Locomotion subscale of the Peabody Develop-
Vestibular Dysfunction mental Motor Scales, 2nd edition (PDMS-2),87
• Balance subscale of the Bruininks-Oseretsky Test
A comprehensive examination of vestibular function in- of Motor Proficiency, 2nd edition (BOT-2),88
cludes functional and diagnostic tests of vestibulo-ocular • Pediatric Balance Scale,89,90
(VO) and vestibulospinal (Vsp) function.82,83 Because di- • Dynamic Gait Index,91
agnostic procedures are costly and may be uncomfortable, • Pediatric Clinical Test of Sensory Interaction for
particularly for young children, screening for appropriate Balance.92,93
referrals for in-depth testing is w arranted. Based on the
literature, the following children should be tested with re- Care should be taken in the selection of tests, because
gard to motor and balance de velopment and oculomotor not all are appropriate for all ages (Table 24-2). The BOT-
control.19 Children with: 2 and PDMS-2 are valuable in documenting general gross
and fine motor developmental status and pro viding more
• SNHI, specific measures of balance and visual motor de velop-
• identified learning disability with evidence of ment. Tests of sensory integration dysfunction (i.e., The
functional impairments related to Vsp or VO Test of Sensory Functions in Inf ants94 and the DeGangi-
function, Berk Test of Sensory Integration95) are appropriate for chil-
• recurrent and chronic inner ear infections who dren with only mild motor delays. Specifically, these tests
also present with difficulties of coordination, examine for the persistence of primiti ve reflexes, such as
reading, or developmental delay, and the tonic labyrinthine and asymmetric tonic neck refle xes
• complaints of dizziness or visual stabilization (see Figs. 24.3 and 24.4). Persistence of these responses
difficulties. purportedly suggests involvement of the vestibular system.
Therapists can complete developmental functional However, the literature remains unclear on the relationship
testing of motor and postural control abilities, perceptual between peripheral and central vestibular function and sen-
and oculomotor abilities, and screening of VO and Vsp sory integration dysfunction as measured by these tests.
function.14,84,85 The purpose of these tests is to: Therefore, the use of the tests of sensory inte gration dys-
function and intervention for motor planning, dyspraxia,
1. establish that a functional balance and/or oculo- and sensory inte grative dysfunction will not be further
motor deficit(s) exists, addressed in this chapter. However, these issues are appro-
2. isolate the contributions of the various compo- priately and completely reviewed elsewhere.5
nents of the postural control and gaze stability For children with or without balance impairments,
systems, and thus determine which component(s) gaze stability should be examined. The functional measure
is (are) problematic, and of gaze stability, and more specifically, the contribution of
3. provide a basis for referral for further diagnos- vestibular information to gaze stability, is the dynamic vi-
tic testing and the development of remedial sual acuity (DVA) test.14,96,97 For children, visual acuity
programs. charts are available with symbols (Fig. 24.5) to complete
Dynamic Visual Acuity Testing, which has excellent sen-
Children who attain scores belo w age-appropriate
sitivity and specificity for the identification of vestibular
levels and those in whom screening identif ies VO or
hypofunction in children. 14 In addition, a computerized
Vsp dysfunction should be referred for more compre-
DVA test was recently developed. Normative data was
hensive testing (e.g., oculomotor, rotary chair, caloric,
gathered for children, and the test w as determined to be
VEMP).
reliable and valid.96
Children who present with deficits in balance or gaze
stability on any of the tests noted above, or more specifi-
Testing Balance and Gaze Stability
cally, on the balance, refle xive, or visual motor subtests,
Normal postural control for balance requires intact or dynamic visual acuity test, should be further examined
vestibulospinal abilities and inte grated labyrinthine for sensory (i.e., vision, somatosensory , and vestibular)
reflexes. Clinical functional measures of balance that and postural control system ef fectiveness, to include
3970_Ch24_457-479 25/06/14 12:34 PM Page 464
464 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Bruininks- Balance and gross motor Vsp 4 through Balance on beam in tandem and
Oseretsky Test ability VO 21 years single leg stance
of Motor Manual dexterity, upper- of age Single leg eyes opened and
Proficiency, limb coordination, bilat- closed
2nd edition88 eral coordination, Dribbling a ball, target
balance, running speed finger to nose, bilateral
and agility, strength coordination tasks
subtests
DeGangi-Berk Sensory integration and Vsp 3 through Pivot prone and supine flexion
Test of Sensory motor planning VO 5 years of age Postural tone
Integration95 Postural control, bilat- Dysdiadochokinesi
eral motor and reflex Tapping, jumping, and bilateral
integration subtests tasks
ATNR and STNR testing
(Figs. 24.3 and 24.4)
The Sensory Sensory integration and Vsp 4 through Form and space perception
Integration and motor planning abilities VO 8 years of age Praxis
Praxis Tests98 Visual perception Tactile discrimination
Vestibular integration
Prone extension test
Pediatric Clinical Balance under varying Vsp 4 through Measures of sway in double leg
Test of Sensory sensory conditions 9 years of age stance with eyes opened and
Interaction for closed while standing on foam
Balance102 or floor, or with conflict dome
Dynamic Visual Gaze stabilization VO 3 years Visual acuity with head stable
Acuity Test through adult and moving at 2 Hz.
(Clinical);14
Computerized
(NIH toolbox)96,97
Abbreviations: VFx = Vestibular Function; Vsp = Vestibulospinal system; VO = Vestibulo-ocular system; ATNR
= Asymmetrical Tonic Neck Reflex; STNR = Symmetrical Tonic Neck Reflex; SOT = Sensory Organization
Test; DPT = Dynamic Perturbation Test (i.e., toes up tip test)
screening of neurological, oculomotor, and musculoskele- measures may assist in dif ferential diagnosis of normal
tal systems. central nervous system response to an abnormal muscu-
loskeletal system or an abnormal central nerv ous system
response to a normal musculoskeletal system. Subtests of
Screening Motor and Sensory Systems the PDMS-2, BOT-2, and the sensory integration tests can
The musculoskeletal system must be examined to determine provide screening of neurological status (e.g., Romber g
if restrictions in range of motion, pain, reduced strength, testing with eyes open and closed, finger to nose with eyes
or limited endurance are present, because any of these may open and closed, developmental tonic reflex integration).
affect postural alignment or the a vailability of movement Sensory screening should include an e xamination of the
strategies to maintain equilibrium. Furthermore, these visual, somatosensory, and vestibular systems.106
3970_Ch24_457-479 25/06/14 12:34 PM Page 466
466 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
SENSORY AND MOTOR SCREENING and inexpensive version of the test of subjective visual ver-
tical (SVV). If a balance or a visuomotor deficit is evident,
• Lower extremity strength concomitant with evidence of VO or Vsp deficit, further
• Manual muscle testing diagnostic testing of vestibular function is warranted.
• BOT-2 strength subtest
• Coordination
• Heel to shin and rapid alternating toe taps Diagnostic Postural Control Testing
• Finger to nose with eyes opened and closed To test postural control, dynamic posturography testing is
• BOT-2 coordination subtests used.41,73,79,103,109 Dynamic posturography testing involves
• Deep tendon reflexes both a sensory organization test (SOT) and dynamic pertur-
• Equilibrium reactions bation test (DPT), which complement and e xpand on the
• Tilting information provided by traditional clinical testing, and
• Postural fixation yield an objective, functional measure of postural cont rol.
• Protective extension 71,73,103,109 Although sensory and motor tests enable the
• Somatosensory screening in lower extremities clinician to isolate the integrity of the different components
• Light touch of postural control, they do not measure the functional use
• Proprioception (i.e., position sense) and effectiveness of the sensory modalities, the inte grative
• Cortical sensation (e.g., graphesthesia) capabilities necessary for postural control, which the SO T
• Visual screening provides (see Chapter 11 for details on the SOT). In addition,
• Visual field capabilities sensory system ratios calculated from results obtained from
• Oculomotor tests the SOT may be used to monitor dominance or maturation
• Saccades, smooth pursuit of sensory system ef fectiveness in postural control. 71
• Clinical Vestibulo-ocular Reflex Testing (see Normative values of SOT measures have been reported for
Table 24-2) children 3 through 15 years of age (Table 24-3).70,71,103,109,110
Clinically, vestibular screening can be done by noting A clinical, less-sophisticated form of the sensory or ganiza-
the presence of abnormal responses such as gaze-evoked or tion test, one that requires ine xpensive materials and is
positional nystagmus and corrective saccades on the head portable, has been developed.92,102,111 The Pediatric Clinical
thrust test.83,107 Other screening tools for v estibular canal Test of Sensory Interaction for Balance (P-CTSIB) has f air
function include the DVA and the Emory Clinical Vestibular to good reliability when combined sensory conditions scores
Chair Test (ECVCT, Box 24-1). Unlik e the Southern were used.102 Using the P-CTSIB, the examiner documents
California Post Rotary Nystagmus Test (SC-PRNT), the duration of balance (up to 30 seconds) and body sw ay
ECVCT is measured with f ixation removed and has been under the six SOT conditions using a dome and medium-
proposed as a clinical measure of pure vestibular hypofunc- density foam. Recently, the National Institutes of Health
tion.100,101 Screening of vestibular otolith function is typically (NIH) developed the NIH toolbox, which includes a reliable
done by testing the perception of v ertical.108 The Bucket and valid balance test called the Balance Accelerometry
Test108 was recently developed for adults as a reliable, valid, Measure (BAM).112 The BAM uses an accelerometer and
A B
Figure 24.4 One method of testing whether the asymmetrical tonic neck reflex is interfer-
ing with function is to request that the child maintain quadruped with elbows extended as
he/she looks to the left or right: (A) the child without deficit is able to do so without diffi-
culty; (B) the arms collapse as the child attempts to look to his right.
medium-density foam to objectively measure sway. Norma- neuromotor component of postural control can be meas-
tive data has been collected for children.97 ured and monitored. Muller and colleagues 2 and Dichi-
The DPT component of posturography may be used gans and associates79 reported that responses are evident
to determine if neurological dysfunction is e vident, and with minimal maturation changes e vident in the v ery
at what level, and provides an indirect measure of Vsp early stages of learning to stand and walk. Harcourt114 re-
function.59,79,113 Furthermore, maturation changes in the ported that although posturography testing may not be as
468 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Box 24-1
sensitive as caloric testing in the identification of individ- weekly for 30 minutes, under the direction of a physical
uals with peripheral vestibulopathy, it does provide addi- therapist (Table 24-4). The previously noted progressive
tional information and is most v aluable for identifying motor development delay was halted and visual and so-
patients with central abnormalities. matosensory effectiveness ratios that were pre viously
deficient improved to within normative ranges. Braswell
and Rine122 reported improved scores on dynamic visual
Diagnostic Testing of Vestibular Function acuity tests and improved subjective reports of gaze sta-
Diagnostic tests of canal v estibular function include bility following exercise intervention in children with
caloric and rotary chair testing. Normati ve values are vestibular hypofunction. Medeiros and colleagues also
available for children as young as 1 year .49,110,119 Otolith showed improvement of symptoms and balance on SOT
vestibular testing for children, to include vestibular evoked conditions 5 and 6 in children with peripheral vestibular
myogenic potentials (VEMP), off-vertical axis rotation, hypofunction who received vestibular rehabilitation.123
and SVV, has also been reported.4,22,110,120,121
Once appropriate testing identif ies functional im- Benign Paroxysmal Positional Vertigo
pairments related to vestibular dysfunction, appropriate (BPPV)
intervention can be developed and administered. Evidence on treatment ef ficacy in children with BPPV
is limited to case studies. D’Agostino, Melagrana, and
Taborelli21 reported a case of horizontal canal BPPV in a
Treatment of Vestibular 10-year-old child, with “spontaneous” recovery following
Dysfunction short-term hospitalization and repeated mobilization (e.g.,
Peripheral Disorders roll side to side) in supine. Saka et al 124 published two
cases with BPPV. An 11-year-old boy presented with apo-
As with adults with peripheral dysfunction, once a diag- geotropic nystagmus following the roll test, implying
nosis is complete, medical management and rehabilitation cupulolithiasis in the horizontal canal. A 3-year-old girl
should begin. This may include medication, sur gery, or presented with geotropic nystagmus following the roll test,
gaze stability and balance training activities (see Chapters implying canalithiasis of the horizontal canal. In both
17, 21, 22, and 23). cases, treatment was not done and positional n ystagmus
disappeared 1 week later at the follo w-up visit. Shetye
et al125 reported about a 13-year -old girl who developed
Evidence of Treatment Efficacy BPPV following fairground rides. She had cochlear im-
Peripheral Vestibular Hypofunction plant surgery 2 years prior . The case w as successfully
Rine and colleagues58 completed a randomized double- treated using the Eple y maneuver and Brandt Darof f
blind controlled study to determine the efficacy of ex- exercises. In a retrospecti ve chart review, Song et al 126
ercise intervention for the impro vement of motor reported that five patients including three children with
development and postural control in children with bilat- enlarged vestibular aqueduct syndrome also presented
eral vestibular hypofunction. Children participated in an with recurring BPPV and multiple canal in volvement.
exercise intervention focused on substitution three times They were treated successfully with the Epley maneuver.
3970_Ch24_457-479 25/06/14 12:34 PM Page 470
470 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Sessions are 30 minutes; 3X/week; 12 weeks. For each session, choose 1 exercise from 3 categories and spend
10 minutes working on the exercise. Document success and progression.
Categories Examples of Specific Exercises Progression (80% Success of Trials)
Eye-hand Tap small pictures on a balloon as it moves; Balloon: begin with balloon still, then move it
coordination bat a balloon with a badminton racket; throw with increasing speed and direction;
bean bags to a target; pick up Velcro pictures Badminton: begin with a balloon and progress to a
with a tennis ball (bouncing it on the floor); birdie;
catching balls Bean Bag Target & Velcro ball: begin close to the
target and progress to standing further away;
Catch: begin with larger balls, progress to small
rubber ball.
General Side-stepping; braiding; dancing; running, Begin with side-stepping, easy dance steps,
coordination skipping, galloping, and hopping races; galloping and progress to more advanced steps
obstacle courses that include crawling, (e.g., braiding, skipping);
climbing, and jumping Time the obstacle course and race and try to beat
the previous time; measure the distance of long
jump and try to increase it.
Visual-motor Identify pictures, letters, and numbers while: Decrease the optotype size; increase the speed of
training (1) swinging in a net swing; (2) jumping on a head movement
trampoline; (3) spinning on a sit-and-spin;
(4) walking quickly.
Balance Walking on a narrow path; walking or stand- Decrease the size of the path to a tandem walk;
training ing on a balance beam; single legged stance; balance in various lighting conditions (e.g., dim
walking on various surfaces (e.g., thick mat); light, Vaseline goggles, eyes closed, varying depth
sitting on a T-stool (i.e., a stool with a single of compliant surface); T-stool: begin with feet
leg); assuming a posture on a scooter board apart while catching large balls and progress to
and holding a position while being pulled feet together catching smaller balls.
around the room.
stabilization regime, balance, and movement activities to central deficits have been delineated elsewhere in this vol-
resume age-appropriate levels of activity). ume. Reportedly, postural control def icits are the most
consistent finding. Therefore, children with deficits of bal-
ance, postural control ability, and visual motor function
Central Vestibular and Postural Control should be evaluated for VO and Vsp function and differ-
Deficits ential diagnosis of the multiple factors involved. Treatment
Few studies have been conducted to e xamine vestibular can then be developed to either facilitate the use and inte-
function in children with central nervous system disorders. gration of systems intact but not used, or to facilitate com-
However, reports in the literature do note the follo wing: pensatory mechanisms. F or example, a child with
children with autism spectrum disorder and dyslexia pre- hypertonicity and developmental delay, as well as e vi-
sent with sensory organization and balance deficits,127,128 dence of VO and Vsp dysfunction, should participate in
postural control deficits are evident in children with cere- programs that include facilitation and improvement of vi-
bral palsy, and vestibular stimulation does improve motor sual stabilization ability, movement tolerance and balanc-
and visual abilities in children with central nervous system ing during visual stabilization, and balance training under
deficit, autism, and lo w birth weight premature in- varying sensory environments to encourage the use of
fants.9,57,129-131 Specific clinical signs and symptoms of intact systems and facilitate integration of information.
472 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
However, with use of hearing aids, audiological testing single leg stance eyes opened for 6 seconds,
was within normal limits and the child did comprehend with eyes closed for 3 seconds; he was able to
spoken language and spoke clearly. He also had a his- walk 3.5-inch balance beam, but not balance
tory of frequent ear infections with drainage tubes in- standing across the beam in double or single leg
serted twice (bilaterally). This child had been recently stance; on Balance subtest of BOTMP achieved
placed in a special education program for learning dis- age-equivalent score of 4 years 11 months;
ability because of poor reading test results (f alling on visual-motor coordination subtest, age-equiv-
below grade level). He was referred for testing to estab- alent score of 7 years 8 months. Significant de-
lish vestibular functional status and to determine if fur- velopmental delay in balance abilities evident.
ther testing or treatment was warranted. Parent reported ■ Neurological Screening (to rule out confound-
typical activity levels until recently to include playing ing factors and determine appropriate treatment
T-ball and basketball with peers (intramural sports). Re- approach): Deep tendon reflexes within normal
view of records indicated treatment with gentamicin and limits, as were rapid alternating movements,
amoxicillin during the past few years. (Although amox- integration of labyrinthine reflexes, and finger-
icillin does not affect the vestibular apparatus, genta- to-nose test.
micin is known to be ototoxic in children, similar to what ■ Posturography (SOT) results: Patient relied on
Continued
3970_Ch24_457-479 25/06/14 12:35 PM Page 474
474 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
■ Table 24-5 CASE STUDY 24-4 PRE AND POST INTERVENTION OUTCOMES
Name of Test Result Pre-intervention Result Post-intervention Published Normative Data
Clinical DVA test 5.5 lines of difference 4.5 lines of difference <3 lines of difference
between SVA and DVA14,118
BOT-2 <10th percentile for bal- 50th percentile for balance Standardized test88
ance and bilateral coordina- and bilateral coordination
tion subscales. subscales
P-CTSIB Foam EO (15 sec); Foam Foam EO (30 sec); Foam 30 seconds for all
(modified) EC (unable) all other EC (25 sec) conditions102
conditions 30 sec
Single-Legged Stance EO (8 sec); EC (2 sec) EO (10 sec); EC (6 sec) 10 seconds EO and EC87
Toes Up Tip Increased latency for Continued to have abnor- No stepping; adult-like EMG
with EMG tibialis anterior response; mally increased latency for responses.
stepped tibialis anterior; no stepping
SUMMARY References
Children presenting with vertigo, delays in motor devel- 1. Kodama A, Sando I. Postnatal development of the vestibular
aqueduct and endolymphatic sac. Annals of Otolaryngology
opment and postural control, learning disabilities, and/ Rhinology and Laryngology. 1982;91(Suppl 96):3-12.
or impaired gaze stability may have vestibular dysfunc- 2. Muller K, Homberg V, Coppenrath P, Lenard HG. Matura-
tion. Children suspected of ha ving vestibular dysfunc- tion of set-modulation of lower extremity EMG responses
tion should be screened for oculomotor , motor, and to postural perturbations. Neuropediatrics. 1992;23:82-91.
sensory impairments. The peripheral vestibular system 3. Nadol JB, Hsu W. Histopathologic correlation of spiral gan-
glion cell count and new bone formation in the cochlea fol-
should be screened using the Head Thrust Test, Emory lowing meningogenic labyrinthitis and deafness. Ann Otol
Clinical Vestibular Chair Test, and Bucket Test. Gaze Rhinol Laryngol. 1991;100:712-716.
stability and balance should be tested using the Clinical 4. Wiener-Vacher SR, Toupet F, Narcy P. Canal and otolith
Dynamic Visual Acuity Test, Modified Clinical Test vestibulo-ocular reflexes to vertical and off vertical axis
of Sensory Interaction on Balance, and balance sub- rotations in children learning to walk. Acta Otolaryngol.
1996;116:657-665.
scales of the BOT-2 or PDMS-II. Children with abnor - 5. Ayres J. Sensory Integration and Learning Disorders.
mal tests should be referred for diagnostic testing. Gaze Los Angeles, CA: Western Psychological Services; 1983.
stability, balance, and motor impairments can be treated 6. Montgomery P. Assessment of vestibular function in chil-
using adaptation and substitution exercises, modified for dren. Physical & Occupational Therapy in Pediatrics.
children. 1985;5(2/3):33-56.
3970_Ch24_457-479 25/06/14 12:35 PM Page 476
476 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
7. Wiener-Vacher SR, Ledebt A, Bril B. Changes in otolith 25. Riina N, Ilmari P, Kentala E. Vertigo and imbalance in
VOR to off vertical axis rotation in infants learning to children. Arch Otolaryngol Head Neck Surg. 2005;131:
walk. Annals of New York Academy of Sciences. 1996;19 996-1000.
(781):709-712. 26. Gruber M, Cohen-Kerem R, Kaminer K, Shupak A.
8. Cioni G, Favilla M, Ghelarducci B, La Noce A. Develop- Vertigo in children and adolescents: Characteristics and
ment of the dynamic characteristics of the horizontal outcome. The Scientific World Journal. 2012;10:1-6.
vestibulo-ocular reflex in infancy. Neuropediatrics. 27. Balatsouras DG, Kaberos A, Assimakopoulos D,
1984;15(3):125-130. Katotomichelakis M, Economou NC, Korres SG. Etiology
9. Slavik BA, Kitsuwa-Lowe J, Danner PT, Green J, Ayres of vertigo in children. Int J Pediatr Otorhinolaryngol.
AJ. Vestibular stimulation and eye contact in autistic 2007;71(3):487-494.
children. Neuropediatrics. 1984;15:33-36. 28. Batson G. Benign paroxysmal vertigo of childhood: a
10. Von Hofsten C, Rosander K. The development of gaze review of the literature. Paediatric Child Health.
control and predictive tracking in young infants. Vision 2004;9(1):31-34.
Research. 1996;36(1):81-96. 29. Uneri A, Turkdogan D. Evaluation of vestibular function
11. Braswell J, Rine RM. Evidence that vestibular hypofunc- in children with vertigo attacks. Arch of Dis Child.
tion affects reading acuity in children. International 2003;88:510-511.
Journal of Pediatric Otorhinolaryngology. 2006;70:1957- 30. Zhang D, Fan Z, Han Y, et al. Benign paroxysmal vertigo
1965. of childhood: diagnostic value of vestibular test and high
12. Rine RM, Cornwall G, Gan K et al. Evidence of progressive stimulus rate auditory brainstem response test. Int J Pedi-
delay of motor development in children with sensorineural atr Otorhinolaryngol. 2012;76(1):107-110.
hearing loss and concurrent vestibular dysfunction. Percep- 31. Bisdorff AR. Management of vestibular migraine.
tual and Motor Skills. 2000;90:1101-1112. Therapeutic Advances in Neurological Disorders.
13. Shall MS. The importance of saccular function to motor 2011;4(3):183-191.
development in children with hearing impairments. Inter- 32. Lewis D, Paradiso E. A double-blind, dose comparison
national Journal of Otolaryngology. 2009;2009:1-5. study of topiramate for prophylaxis of basilar-type mi-
14. Rine RM, Braswell J. A clinical test of dynamic visual graine in children: a pilot study. Headache.
acuity for children. Int J Pediatr Otorhinolaryngol. 2003; 2007;47(10):1409-1417.
69(11):1195-1201. 33. Golz A, Netzer A, Angel-Yeger B, Westerman ST, Gilbert
15. Wiener-Vacher SR. Vestibular disorders in children. LM, Joachims HZ. Effects of middle ear effusion on the
International Journal of Audiology. 2008;47:578-583. vestibular system in children. Otolaryngol Head Neck
16. Choung Y-H, Park K, Moon S-K, Kim C-H, Ryu SJ. Surg. 1998;119(6):695-699.
Various causes and clinical characteristics in vertigo in 34. Engel-Yeger B, Golz A, Parush S. Impact of middle ear
children with normal eardrums. Int J Pediatr Otorhino- effusion on balance performance in children. Disabil
laryngol. 2003;67:889-894. Rehabil. 2004;26(2):97-102.
17. Erbek SH, et al. Vertigo in childhood: a clinical experi- 35. Golz A, Westerman T, Gilbert LM, Joachims HZ, Netzer
ence. Int J Pediatr Otorhinolaryngol. 2006;70:1547-1554. A. Effects of middle ear effusion on the vestibular
18. McCaslin DL, Jacobson G, Gruenwald JM. The predomi- labyrinth. J Laryng and Otol. 1991;105:987-989.
nant forms of vertigo in children and their associated 36. Casselbrant ML, Furman JM, Rubinstein E, Mandel EM.
findings on balance function testing. Otolayngology Effect of otitis media on the vestibular system in children.
Clinics of North America. 2011;44:291-307. Annals of Otology Rhinology Laryngology. 1995;104:
19. Rine RM. Growing evidence for balance and vestibular 620-624.
problems in children. Audiological Medicine. 37. Jones NS, Radomskij P, Prichard AJN, Snashall SE. Im-
2009;99999:1. balance and chronic secretory otitis media in children:
20. Weiss AH, Phillips JO. Congenital and compensated effect of myringotomy and insertion of ventilation tubes
vestibular dysfunction in childhood: an overlooked entity. on body sway. Ann Otolaryngology Laryngology.
Journal of Child Neurol. 2006;21:572-579. 1990;99:477-481.
21. D’Agostino R, Melagrana A, Taborelli G. Benign posi- 38. Koyuncu M, Saka MM, Tanyeri Y, et al. Effects of otitis
tional paroxysmal vertigo of horizontal semicircular canal media with effusion on the vestibular system in children.
in the child: case report. Int J Pediatr Otorhinolaryngol. Otolaryngol Head Neck Surg. 1999;120(1):117-121.
2003;67:549-551. 39. Casselbrant ML, Furman JM, Mandel EM, Fall PA,
22. Tribukait A, Brantberg K, Bergenius J. Function of semi- Kurs-Lasky M, Rockette HE. Past history of otitis media
circular canals, utricles and saccules in deaf children. and balance in four-year-old children. Laryngoscope.
Acta Otolaryngol. 2004;124:41-48. 2000;110:773-778.
23. Cushing SL, Gordon KA, Rutka JA, James AL, Papsin 40. Kaga K. Vestibular compensation in infants and children
BC. Vestibular end-organ dysfunction in children with with congenital and acquired vestibular loss in both ears.
sensorineural hearing loss and cochlear implants: an Otorhinolaryngology. 1999;49:215-224.
expanded cohort and etiologic assessment. Otol Neurotol. 41. Rine RM, Spielholz NI, Buchman C. Postural control
2013;34(3):422-428. in children with sensorineural hearing loss and vestibular
24. Cushing SL, Papsin BC, Rutka JA, James AL, Gordon KA. hypofunction: deficits in sensory system effectiveness
Evidence of vestibular and balance dysfunction in children and vestibulospinal function. In: Duysens J, Smits-
with profound sensorineural hearing loss using cochlear Engelsman BCM, Kingma H, eds. Control of Posture
implants. Laryngoscope. 2008;118(10):1814-1823. and Gait. Amsterdam: Springer-Verlag; 2001:40-45.
3970_Ch24_457-479 25/06/14 12:35 PM Page 477
42. Rajendran V, Roy FG, Jeevanantham D. Postural control, 59. Horak FB, Shupert CL, Dietz V, Horstmann G. Vestibular
motor skills, and health-related quality of life in children and somatosensory contributions to responses to head
with hearing impairment: a systematic review. Eur Arch and body displacements in stance. Experimental Brain
Otorhinolaryngol. 2012;269(4):1063-1071. Research. 1994;100:93-106.
43. Inoue A, Iwasaki S, Ushio M, et al. Effect of vestibular 60. Barron S, Irvine J. Effects of neonatal cocaine exposure on
dysfunction on the development of gross motor function two measures of balance and coordination. Neurotoxicol-
in children with profound hearing loss. Audiol Neurootol. ogy and Teratology. 1994;16(1):89-94.
2013;18(3):143-151. 61. Brogen E, Hadders-Algra M, Forssberg H. Postural con-
44. Jacot E, Van Den AT, Debre HR, Wiener-Vacher SR. trol in children with spastic diplegia: muscle activity dur-
Vestibular impairments pre- and post-cochlear implant ing perturbations in sitting. Developmental Medicine and
in children. Int J Pediatr Otorhinolaryngol. 2009;73(2): Child Neurology. 1996;38:379-388.
209-217. 62. Bundy AC, Fisher AG, Freeman M. Concurrent validity
45. Franco ES, Panboca I. Vestibular function in children of equilibrium tests in boys with learning disabilities with
underperforming at school. Brazilian Journal of Otorhino- and without vestibular dysfunction. Am J Occup Ther.
laryngology. 2008;74(6):815-825. 1987;41:28-34.
46. Franco ES, Panhoca I. Otoneurologic evaluation in chil- 63. Liao HF, Jeng SF, Lai JS, Cheng CK, Hu MH. The
dren with school difficulties: vestibular function investiga- relation between standing balance and walking
tion. Braz J Otorhinolaryngol. 2007;73(6):803-815. function in children with spastic diplegic cerebral
47. Zwicker JG, Missiuna C, Harris SR, Boyd LA. Develop- palsy. Developmental Medicine & Child Neurology.
mental coordination disorder: a pilot diffusion tensor 1997;39:106-112.
imaging study. Pediatr Neurol. 2012;46(3):162-167. 64. Nashner LM, Shumway-Cook A, Marin O. Stance posture
48. Kashiwagi M, Iwaki S, Narumi Y, Tamai H, Suzuki S. control in select groups of children with cerebral palsy:
Parietal dysfunction in developmental coordination deficits in sensory organization and muscular coordina-
disorder: a functional MRI study. Neuroreport. tion. Exp Brain Res. 1983;49:393-409.
2009;20(15):1319-1324. 65. Reid DT, Sochaniwskyj A, Milner M. An investigation of
49. Eviatar L, Eviatar A. The normal nystagmic response of postural sway in sitting of normal children and children
infants to caloric and perrotatory stimulation. Laryngo- with neurological disorders. Physical & Occupational
scope. 1979;89:1036-1045. Therapy in Pediatrics. 1991;11(1):19-35.
50. Ariano RE, Zelenitsky SA, Kassum DA. Aminoglycoside- 66. Jahn K. Vertigo and balance in children—diagnostic ap-
induced vestibular injury: maintaining a sense of balance. proach and insights from imaging. Eur J Paediatr Neurol.
Ann Pharmacother. 2008;42(9):1282-1289. 2011;15(4):289-294.
51. Scheenstra RJ, Rijntjes E, Tavy DL, Kingma H, 67. Kimball JG. Normative comparison of the Southern
Heijerman HG. Vestibulotoxicity as a consequence of California Postrotary Nystagmus Test: Los Angeles vs.
systemically administered tobramycin in cystic fibrosis pa- Syracuse data. American Journal of Occupational
tients. Acta Otolaryngol. 2009;129(1):4-7. Therapy. 1981;35(1):21-25.
52. Aust G. Vestibulotoxicity and ototoxicity of gentamicin in 68. Dichigans J, Diener HC. The contribution of vestibulo-
newborns at risk. Int Tinnitus J. 2001;7(1):27-29. spinal mechanisms to the maintenance of human upright
53. Giffin NJ, Benton S, Goadsby PJ. Benign paroxysmal posture. Acta Otolaryngology. 1989;107:338-345.
torticollis of infancy: four new cases and linkage to 69. Foudriat BA, DiFabio RP, Anderson JH. Sensory organiza-
CACNA1A mutation. Dev Med Child Neurol. 2002;44(7): tion of balance responses in children 3-6 years of age: a
490-493. normative study with diagnostic implications. Internat
54. Drigo P, Carli G, Laverda AM. Benign paroxysmal J Ped Otorhinolaryng. 1993;27:225-271.
torticollis of infancy. Brain Dev. 2000;22(3):169-172. 70. Hirabayashi S, Iwasaki Y. Developmental perspective of
55. Villablanca JR, Hovda DA, Jackson GF, Infante C. Neuro- sensory organization on postural control. Brain and
logical and behavioral effects of a unilateral frontal corti- Development. 1995;17:111-113.
cal lesion in fetal kittens, II: visual system tests, and 71. Rine RM, Rubish K, Feeney C. Measurement of sensory
proposing an “optimal developmental period” for lesion system effectiveness and maturational changes in postural
effects. Behavioral Brain Research. 1993;57:79-92. control in young children. Pediatric Physical Therapy.
56. Tsuzuku T, Kaga K. Delayed motor function and results 1998;10:16-22.
of vestibular function tests in children with inner ear 72. Nandi R, Luxon LM. Development and assessment of
anomalies. Int J Pediatr Otorhinolaryngol. 1992;23: the vestibular system. Int J Audiol. 2008;47(9):566-577.
261-268. 73. Ferber-Viart C, Ionescu E, Morlet T, Froehlich P, Dubreuil C.
57. Horak FB, Shumway-Cook A, Crowe TK, Black FO. Balance in healthy individuals assessed with Equitest:
Vestibular function and motor proficiency of children maturation and normative data for children and young
with impaired hearing or with learning disability and adults. International Journal of Pediatric Otorhinolaryn-
motor impairments. Developmental Medicine Child gology. 2007;71(7):1041-1046.
Neurology. 1988;30:64-79. 74. Shumway-Cook A, Woollacott MI. The growth of stabil-
58. Rine RM, Braswell J, Fisher D, Joyce K, Kalar K, Shaffer ity: postural control from a developmental perspective.
M. Improvement of motor development and postural con- Journal of Motor Behavior. 1985;17:131-147.
trol following intervention in children with sensorineural 75. Woollacott MH, Debu B, Mowatt M. Neuromuscular con-
hearing loss and vestibular impairment. Int J Pediatr trol of posture in the infant and child: is vision dominant?
Otorhinolaryngol. 2004;68(9):1141-1148. Journal of Motor Behavior. 1987;19:167-168.
3970_Ch24_457-479 25/06/14 12:35 PM Page 478
478 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
76. Haas G, Diener HC, Bacher M, Dichigans J. Development 95. Berk RA, DeGangi GA. DeGangi-Berk Test of Sensory
of postural control in children: short-, medium-, and long- Integration. Los Angeles: Western Psychological
latency EMG responses of leg muscles after perturbation Services; 1983.
of stance. Exp Brain Res. 1986;64:127-132. 96. Rine RM, Roberts D, Corbin BA, et al. A new portable
77. Woollacott MH, Shumway-Cook A. Changes in postural tool to screen vestibular and visual function: National
control across the life span—a systems approach. Physical Institutes of Health Toolbox Initiative. Journal of
Therapy. 1990;70(12):799-807. Rehabilitation Research and Development. 2012;49
78. Forssberg H, Nashner LM. Ontogenetic development of (2):209-220.
postural control in man: adaptation to altered support and 97. Rine RM, Schubert MC, Whitney SL, et al. Vestibular
visual condition during stance. Journal of Neuroscience. function assessment using the NIH Toolbox. Neurology.
1982;2:545-552. 2013;80(Suppl 3):S25-S31.
79. Dichigans J, Deiner HC. The use of short- and long-latency 98. Ayres AJ. Sensory Integration and Praxis Test. Los
reflex testing in leg muscles of neurological patients. In: Angeles: Western Psychological Services; 1996.
Struppler A, Weindl A, eds. Clinical Aspects of Sensory 99. Ayres AJ. Southern California Postrotary Nystagmus
Motor Integration. Berlin: Springer-Verlag; 1987:165-175. Test. Los Angeles, Ca: Western Psychological Services;
80. Riach CL, Starkes JL. Visual fixation and postural sway. 1989.
Journal of Motor Behavior. 1989;21:265-276. 100. Hall CD, Abbott KN, Lane EC, et al. Measurement of
81. Riach CL, Hayes KC. Maturation of postural sway in vestibular hypofunction: validity of the Emory clinical
young children. Developmental Medicine and Child vestibular chair test (ECVCT). Journal of Neurologic
Neurology. 1987;29:650-658. Physical Therapy. 2007;31(4):210-211.
82. Phillips JO, Backous DD. Otolaryngol Clin North Am. 101. Hall CD, Hoover J, Jacobs M, et al. A new measurement
2002;35(4):765-790. tool for vestibular hypofunction: validity of the Emory
83. Valente LM. Assessment techniques for vestibular evalua- Clinical Vestibular Chair Test. Journal of Neurologic
tion in pediatric patients. Otolaryngol Clin North Am. Physical Therapy. 2009;33(4):232.
2011;44(2):273-290. 102. Westcott SL, Crowe TK, Dietz JC, Richardson P. Test-
84. Westcott SL, Burtner PA. Postural control in children: retest reliability of the Pediatric Clinical Test of Sensory
implications for pediatric practice. Phys Occup Ther Interaction for Balance (P-CTSIB). Physical and
Pediatr. 2004;24(1-2):5-55. Occupational Therapy in Pediatrics. 1994;14(1):1-22.
85. Donahoe B, Turner D, Worrell T. The use of functional 103. Charpiot A, Tringali S, Iionescu E, Vital-Durand F,
reach as a measurement of balance in boys and girls Ferber-Viart C. Vestibulo-ocular reflex and balance
without disabilities ages 5 to 15 years. Pediatric Physical maturation in healthy children aged from six to twelve
Therapy. 1994;6:189-193. years. Audiolo Neurootol. 2010;15(4):203-210.
86. Norris RA, Wilder E, Norton J. The functional reach test 104. Furman JM. Role of posturography in the management
in 3- to 5-year-old children without disabilities. Pediatr of vestibular patients. Otolaryngology-Head and Neck
Phys Ther. 2008;20(1):47-52. Surgery. 1995;112(1):8-15.
87. Folio MR and Fewell RR. Peabody Developmental Motor 105. Carswell A, McColl MA, Baptiste S, Law M, Polatajko
Scales-2. 2nd ed. Austin: pro-ed, Inc.; 2000. H, Pollock N. The Canadian Occupational Performance
88. Bruininks RH, Bruininks BD. Bruininks-Oseretsky Test of Measure: a research and clinical literature review.
Motor Proficiency. 2nd ed. Minneapolis: NCS Pearson, Canadian Journal of Occupational Therapy. 2004;71(4):
Inc; 2005. 210-222.
89. Franjoine M, Gunther J, Taylor M. Pediatric balance scale: 106. Westcott SL, Lowes L, Richardson PK. Evaluation of
a modified version of the Berg Balance Scale for the postural stability in children: current theories and assess-
school-age child with mild to moderate motor impairment. ment tools. Physical Therapy. 1997;77(6):629-645.
Pediatric Physical Therapy. 2003;15:114-128. 107. Schubert MC, Tusa RJ, Grine LE, Herdman SJ. Optimiz-
90. Franjoine MR, Darr N, Held SL, ott K, oung BL. The perfor- ing the sensitivity of the head thrust test for identifying
mance of children developing typically on the pediatric bal- vestibular hypofunction. Physical Therapy. 2004;84(2):
ance scale. Pediatric Physical Therapy. 2010;22(4):350-359. 151-158.
91. Lubetzky-Vilnai A, Jirikowic TL, McCoy SW. Investiga- 108. Zwergal A, Rettinger N, Frenzel C, Dieterich M, Brandt
tion of the Dynamic Gait Index in children: a pilot study. T, Strupp M. A bucket of static vestibular function.
Pediatr Phys Ther. 2011;23(3):268-273. Neurology. 2009;72(19):1689-1692.
92. Deitz JC, Richardson P, Crowe TK, Westcott SL. Perfor- 109. Casselbrant ML, Mandel EM, Sparto PJ, et al. Longitudi-
mance of children with learning disabilities and motor de- nal posturography and rotational testing in children three
lays on the Pediatric Clinical Test of Sensory Interaction to nine years of age: normative data. Otolaryngol Head
for Balance (P-CTSIB). Physical & Occupational Therapy Neck Surg. 2010;142(5):708-714.
in Pediatrics. 1996;16(3):1-21. 110. Valente M. Maturational effects of the vestibular system:
93. Deitz JC, Richardson P, Atwater SW, Crowe T, Odiorne. a study of rotary chair, computerized dynamic posturog-
Performance of normal children on the pediatric clinical raphy, and vestibular evoked myogenic potentials with
test of sensory integration for balance. The Occupational children. J Am Acad Audiol. 2007;18(6):461-481.
Therapy Journal of Research. 1991;11(6):337-357. 111. Shumway-Cook A, Horak FB. Assessing the influence
94. DeGangi GA, Greenspan SI. Test of Sensory Function in In- of sensory interaction on balance. Physical Therapy.
fants. Los Angeles: Western Psychological Services; 1989. 1986;66:1548-1550.
3970_Ch24_457-479 25/06/14 12:35 PM Page 479
112. Reuben DB, Magasi S, McCreath HE, et al. Motor as- 123. Medeiros I, Bittar R, Pedalini M, Lorenzi M, Kii M,
sessment using the NIH Toolbox. Neurology. 2013;80 Formigoni L. Evaluation of the treatment of vestibular
(Suppl 3):S65-S75. disorders in children with computerized dynamic
113. Shepard NT. The clinical use of dynamic posturography posturography: preliminary results. Jornal de Pediatria.
in the elderly. Ear Nose and Throat. 1989;68:940-957. 2003;79(4):337-342.
114. Harcourt JP. Posturography—applications and limitations 124. Saka N, Imai T, Seo T, et al. Analysis of benign paroxys-
in the management of the dizzy patient. Clin Otolaryn- mal positional nystagmus in children. Int J Pediatr
gol. 1995;20:299-302. Otorhinolaryngol. 2013;77(2):233-236.
115. Cohen H. Testing vestibular function: problems with the 125. Shetye A. Benign paroxysmal positional vertigo in a
Southern California Postrotary Nystagmus Test. Am J child: an infrequent complication following a fairground
Occup Ther. 1989;43(7):475-477. ride and post-cochlear implant surgery. Cochlear
116. Wiss T, Clark F. Validity of the Southern California Implants Int. 2012;13(3):177-180.
Postrotary Nystagmus Test: misconceptions lead to incor- 126. Song JJ, Hong SK, Kim JS, Koo JW. Enlarged vestibular
rect conclusions. American Journal of Occupational aqueduct may precipitate benign paroxysmal positional
Therapy. 1990;44(7):658-660. vertigo in children. Acta Otolaryngol. 2012;132(Suppl 1):
117. Rine RM, Lindblad S, Donovan P, Vergara K, Gostin J, S109-S117.
Mattson K. Balance and motor skills in young children 127. Barela JA, Dias JL, Godoi D, Viana AR, de Freitas PB.
with sensorineural hearing impairment: a preliminary Postural control and automaticity in dyslexic children:
study. Pediatric Physical Therapy. 1996;8:55-61. the relationship between visual information and body
118. Christy JB, Payne J, Azuero A, Formby C. Reliability and sway. Res Dev Disabil. 2011;32(5):1814-1821.
diagnostic accuracy of clinical tests of vestibular function 128. Bhat AN, Lands RJ, Galloway JC. Current perspectives
for children. Pediatr Phys Ther. 2014;26:180-190. on motor functioning in infants, children, and adults
119. Staller SJ, Goin DW, Hildebrandt M. Pediatric vestibular with autism spectrum disorders. Phys Ther. 2011;91(7):
evaluation with harmonic acceleration. Otolaryngology- 1116-1129.
Head and Neck Surgery. 1986;95(4):471-476. 129. Gregg CL, Haffner ME, Korner AF. The relative efficacy
120. Kelsch TA, Schaefer LA, Esquivel CR. Vestibular of vestibular-proprioceptive stimulation and the upright
evoked myogenic potentials in young children: Test position in enhancing visual pursuit in neonates. Child
parameters and normative data. Laryngoscope. Development. 1997;309-314.
2006;116:895-900. 130. Barela JA, Focks GM, Hilgeholt T, Barela AM, Carvalho
121. Cakrt O, Slaby K, Viktorinova L, Kolar P, Jerabek J. Sub- RP. Perception-action and adaptation in postural control
jective visual vertical in patients with idiopathic of children and adolescents with cerebral palsy. Res Dev
scoliosis. Journal of Vestibular Research. 2011;21(3): Disabil. 2011;32(6):2075-2083.
161-165. 131. Nelson MN, White-Traut RC, Vasan U, et al. One-year
122. Braswell J, Rine RM. Preliminary evidence of improved outcome of auditory-tactile-visual-vestibular intervention
gaze stability following exercise in two children with in the neonatal intensive care unit: effects of severe pre-
vestibular hypofunction. International Journal of maturity and central nervous system injury. Journal
Pediatric Otorhinolaryngology. 2006;70:1967-1973. of Child Neurol. 2001;16(7):493-498.
3970_Ch25_480-503 25/06/14 12:38 PM Page 480
CHAPTER 25
Physical Therapy
Management
of the Older Person
with Vestibular
Dysfunction
Susan L. Whitney, DPT, PhD, NCS, ATC, FAPTA ■
The complaint of dizziness is one of the most common Normal Changes of Aging
reasons that older adults visit the doctor’s office.1 The in-
cidence of dizziness increases with age and accounts for Vestibular Function
1.3% of all visits to internists in people 45 to 64 years old, To appreciate the effect of aging on the mechanisms and
2.9% in people older than 65, and 3.8% in people older potential for recovery in vestibular disease, one must un-
than 75. Although dizziness can be caused by man y dif- derstand the normal anatomy and physiology of the
ferent medical conditions, it is estimated that as man y as vestibular system (see Chapters 1–4). Several concepts are
45% of cases are a result of v estibular disorders.2 Aktas particularly important and will be emphasized here.
and colleagues3 have reported that in 31% of their subjects
with hip fracture, vestibular disease was a comorbidity. In
80% of their patients with falls of unknown cause, Pothula
Semicircular Canal Function
and associates4 found symptoms of vestibular dysfunction. The input from the receptors in the semicircular canals
In a recent report of persons who reported dizziness who produces compensatory oculomotor responses (v estibulo-
were over the age of 40 (n = 5,086), there w as a 12-fold ocular reflex [VOR]) and compensatory postural responses
increase in their odds of falling within the last year.5 The (vestibulospinal reflex [VSR]). In the ideal situation, the eye
vestibular insult or injury may be the same as in a younger movement produced by the head mo vement is equal (but
individual, but the functional consequences may be v ery opposite) to the head mo vement, and the VOR is said to
different because of the person’s comorbid health status. have a gain (eye velocity ÷ head velocity) equal to 1. With
Older adults with v estibular disorders, therefore, often aging, there is a decrease in the numbers of both hair cells
present with very different problems from those of their and vestibular neurons.6-8 Functionally, VOR gain de-
younger counterparts. This chapter provides information creases, resulting in reduced visual compensation in re-
about the normal changes in the vestibular, visual, and so- sponse to head movement. These changes, however, appear
matosensory systems with aging as well as the pathologi- to be frequenc y- and v elocity-dependent.9,10 Baloh and
cal changes that can occur in each system. Practical coworkers11 found that older subjects had lo wer visual-
suggestions are made as to ho w older adults may be VOR gain as velocity increased than younger subjects. If
treated differently because of their age. the visual-VOR gain decreases with age, especially at
480
3970_Ch25_480-503 25/06/14 12:38 PM Page 481
Chapter 25 • PHYSICAL THERAPY MANAGEMENT OF THE OLDER PERSON WITH VESTIBULAR DYSFUNCTION 481
higher velocities,12 it would lead to greater retinal slip and that driving is not compromised with persons with bilateral
therefore poorer visual acuity during head movement. The vestibular hypofunction.19 On the road, driving did not ap-
changes in vestibular function have been compared with a pear to be impaired in three people with long-term bilateral
progressive bilateral vestibular deficit10,11,13 and may con- loss (range of bilateral loss was 7 to greater than 20 years).19
tribute to the complaints of disequilibrium (an “off-balance”
sensation) and to the gait ataxia, without an y true vertigo,
that many older people have. Paige12 suggests that this grad-
Utricular and Saccular Function
ual, mild bilateral v estibular loss results in a mismatch in The presence of calcium carbonate crystals (otoconia) on
the visual and vestibular mechanisms. Interestingly, Nadol the maculae of the utricle and saccule mak e these struc-
and Schuknecht13 suggested that de generative changes tures sensitive to the pull of gravity and to linear acceler-
might occur in only one labyrinth, producing sudden, severe ation. These crystals are held in place by a glue-lik e
vertigo or leading to chronic vertigo and disequilibrium. substance, and in all people there is a normal de genera-
Another change related to aging is a decreased ability tion and regeneration of the crystals.20 In addition, degen-
to adapt the gain of the v estibular system.10 This would erative changes in the otoconia of the utricle and saccule
affect the ability of the system to adjust to loss of function increase with aging, 20,21 with less otoconia present in
or other stresses of the system. older adults.22 This process may contrib ute to the rela-
Preexisting vestibular disorders can cause balance tively high incidence of benign paroxysmal positional
problems that manifest slightly dif ferently in older indi- vertigo (BPPV, see Chapter 20) in the elderly . The inci-
viduals. Subclinical vestibular dysfunction may have de- dence of idiopathic BPPV has been reported as peaking
veloped in an older adult when he or she w as younger. in the sixth and se venth decades of life. 23 Baloh and
Then, with the decrease in the number of hair cells and coworkers11 reported that, of 116 patients aged 70 or
vestibular neurons with rising age, along with the changes older that they saw for complaints of “dizziness, ” 25%
in the vestibular and other systems’ ability to compensate, had BPPV. Whitney and colleagues 24 found that 23% of
the patient experiences symptoms of vestibular dysfunc- patients referred to a v estibular clinic had the diagnosis
tion. Thus, the problems are caused by decompensation of BPPV and a mean age of 61 years.
rather than to a new vestibular disorder. Oghalai and associates25 suggest that older persons
Bilateral vestibular disorders are associated with oto- with undiagnosed BPPV ha ve more reports of f alls, are
toxicity, autoimmune, otologic, and neoplastic disorders more likely to have had past depression, and have impair-
plus ototoxicity.5 The previous conditions that are associ- ments of activities of daily living (ADLs). In their sample
ated with bilateral vestibular disorders are more common of older persons seen in a general medical clinic, 9% had
in older than in younger adults. The most common cause a positive Dix-Hallpike test result, although none of the
of bilateral v estibular loss is antibiotic therap y after a older adults were being seen for a balance or v estibular
major infection (see Chapters 4 and 23). The presence of disorder. Gamiz and Lopez-Escamez26 found that 82% of
visual and somatosensory changes with aging complicates the adults in their surv ey older than 60 years who were
the functional recovery for patient with a bilateral vestibu- treated for BPPV had a negative Dix-Hallpike test result
lar loss. Older patients who present with instability of gait at 30-day checkup, suggesting that older persons are suc-
and functional mobility are more likely than younger pa- cessfully treated with canalith repositioning. They also
tients to require the use of a walker or cane and will always reported that older adults with BPPV showed significant
have difficulty walking in the dark. 14,15 These functional changes in the Medical Outcomes Short-F orm Medical
deficits may require environmental and behavioral adap- Survey (SF-36) and short-form Dizziness Handicap In-
tations to prevent falls and injuries in the older person. ventory (DHI) v alues 30 days after under going the
One practical suggestion is that the older person increase canalith repositioning maneuver, suggesting that they had
the lighting in the house, especially nightlights and power- improved. Symptoms of BPPV are often missed in the
outage lights, and that he or she have numerous flashlights elderly, because the Dix-Hallpik e test is often not per -
available at night so as never to have to walk in total dark- formed even when the older adult complains of positional
ness.14 Installation of grab bars in the bathroom, especially dizziness/vertigo.27,28
in the tub or shower, has been shown to be helpful in de- Several theories have been suggested in relation to
creasing falls in older persons. Older persons with bilateral why older persons appear to ha ve a higher incidence of
vestibular loss often e xperience limitations in activities BPPV than younger persons. BPPV has now been associ-
and participation, because man y persons with bilateral ated with higher rates of mild head trauma and diabetes,29
vestibular loss either choose not to drive or by law are lim- osteoporosis and osteopenia, 30 fissures in the otoconia, 21
ited in their driving abilities.16-18 Others have suggested and giant cell arteritis.31 All of these conditions are more
3970_Ch25_480-503 25/06/14 12:38 PM Page 482
482 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
common in older adults. Cause-ef fect relationships with addition, Bhattacharyya et al suggest that concern should
BPPV are very difficult to determine in older adults, be- be exercised with persons with Down syndrome, cervical
cause aging affects many systems, and many older people radiculopathies, ankylosing spondylitis, those with lo w
have a tendency to develop BPPV. Gizzi and colleagues32 back pain, and older adults with morbid obesity.34
have even suggested that the presence of BPPV is f ive It is important to move more slowly with the reposi-
times more common in persons for whom a blood relative tioning maneuvers in adults older than 80 years and with
also had reported BPPV in the past, suggesting that BPPV the adult who has multiple medical problems. 35 The ulti-
may be associated with a genetic link. mate success rate of repositioning in older adults is similar
A newly developed BPPV subscale of the DHI may to that in younger persons but may require more than one
be helpful in identifying BPPV in older persons who present visit. We think that the reason for the dif ference is that it
to a balance clinic.24 Determining whether the older patient is difficult to obtain sufficient neck extension and/or rota-
becomes dizzy or experiences vertigo when moving from tion for an ef fective treatment in older patients. Care
supine to sitting position or while rolling o ver are two of should also be taken with individuals who have metastatic
the key questions included in the new subscale; a “yes” an- cancer to avoid pathological fractures or who have had a
swer significantly increases the lik elihood that the person cerebrovascular accident to a void vascular insufficiency.
has BPPV. We often perform the repositioning maneuv er with two
Even if a patient does not present with a diagnosis clinicians present to help the patient with position changes
of BPPV or with complaints consistent with BPPV , it is if he or she is severely impaired.
recommended that the older adult always be assessed for Another special group is older adults with mental
BPPV during the clinical e xamination, because of its and/or physical disabilities. Ha ving a f amily member
prevalence.25 Because the Dix-Hallpike test result may be present is helpful to assure the older adult that he or she
false-negative in some patients, Viirre and coworkers33 will not be harmed by the maneuvers. It is very frighten-
have suggested that clinicians perform the Dix-Hallpik e ing for older persons with mental challenges to undergo
test, then the roll test, and then repeat the Dix-Hallpik e the canalith repositioning maneuver. As a precaution, we
test if results of the f irst two tests are negative. Whitney also routinely monitor blood pressure in people older
and associates24 also suggest repeating the Dix-Hallpike than 75 years who ha ve abnormally high or lo w blood
maneuver as well as performing the test at dif ferent pressure.
speeds with older adults to dislodge the otoconia. Also,
the examiner is more likely to find evidence of BPPV ear- Vestibular Function Tests
lier in the day.24 It is difficult to determine whether dizziness is truly be-
When performing assessment or treatment for BPPV cause of a vestibular deficit without sophisticated testing
in older persons, however, it is important to consider the (see Chapters 10 and 11). The results of these tests in
possibility that the patient may have cervical spine, lum- older persons must be interpreted carefully and should be
bar spine, and cardiopulmonary disorders as well. Cervi- based on age-related normal v alues.36 For example, in
cal spine range of motion should be assessed before people in their 90s, caloric testing may document bilateral
position testing. Great care should be exercised in extend- vestibular loss, but they may not actually have a bilateral
ing and rotating the older adult’s head because of possible vestibular deficit.
structural changes caused by arthritis or other cervical
disorders, or the position used should be modified by tilt-
Visual Deficits
ing the treatment table so the labyrinth is below the hor-
izontal but the neck is not e xtended. Alternatively, the Visual acuity, the ability to accommodate, and smooth pur-
side-lying test may be used. Also, the patient should be suits normally decline with age.37,38 These normal changes
questioned about vertebral basilar compromise, because associated with aging can mak e rehabilitation after a
great care should be used when deciding how to position vestibular insult more difficult.
the older adult to both test and treat BPPV in someone An inability to adjust to the dark has been sho wn in
with suspect vertebra-basilar insufficiency. If the patient the literature to be one of the reasons why older adults may
presents with a long history of cervical disease (e.g., fall.39 Combining the dark adaptation problem with
rheumatoid arthritis or Paget’s disease), a tilt table is use- vestibular dysfunction can mak e it dangerous for older
ful during the testing and repositioning maneuvers. For a adults with vestibular disorders to move from areas with
patient with normal-pressure hydrocephalus, the neuro- ample light to darkened areas or vice v ersa. This change
surgeon should be consulted about possible problems in light has been sho wn to cause temporary blindness in
with placing the patient in the head-do wn position. In older adults for more than a minute.39
3970_Ch25_480-503 25/06/14 12:38 PM Page 483
Chapter 25 • PHYSICAL THERAPY MANAGEMENT OF THE OLDER PERSON WITH VESTIBULAR DYSFUNCTION 483
In addition to dark adaptation, visual acuity and A home inspection w ould be very helpful for the
contrast sensitivity have been related to f alls in older person with a visual disorder to ensure that the home is
adults40-44 and may contrib ute to imbalance after a free of hazards. The Home Safety Checklist de veloped
vestibular disorder. Older adults may have other eye dis- by the U.S. National Safety Council is an excellent tool
orders, including cataracts, glaucoma, and macular de- for identifying fall hazards in the home (Box 25-1). 46
generation that impair vision.45 Cataracts typically cloud Any of the visual disorders described can potentially
the lens and may cause blurred vision. In patients who raise the risk of f alls and complicate the patient’s reha-
have macular degeneration, near and distant vision are bilitation course. A home visit by the physical or occu-
affected without adversely affecting peripheral vision.45 pational therapist (lo w vision specialists) to reduce
Individuals with glaucoma have difficulty with peripheral hazards may be a v ery helpful intervention for people
vision.45 Depth perception disorders, such as cataracts in who have visual impairments.45
one eye, and double vision mak e maintaining upright
stance more difficult. Multifocal lenses ha ve also been
Somatosensory Changes
implicated in falls in older persons. 41,44 Lord and asso-
ciates44 reported that wearers of progressive, bifocal, or Older adults appear to have a greater chance of reduced
trifocal lenses were more likely to have described a fall, somatosensory function. Age-related electrophysiologi-
especially descending stairs, as well as more trips and cal and functional declines in the peripheral nervous sys-
falls outside their homes. tem have been described in groups of healthy subjects
Box 25-1
Continued
3970_Ch25_480-503 25/06/14 12:38 PM Page 484
484 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Box 25-1
Chapter 25 • PHYSICAL THERAPY MANAGEMENT OF THE OLDER PERSON WITH VESTIBULAR DYSFUNCTION 485
Box 25-1
This checklist was developed by the U.S. National Safety Council in cooperation with AARP, Itasca, IL, 1982.
(Used with permission.)
and patients with neuropathological disorders. These age- that there are changes in static standing balance (sw ay
related somatosensory changes can result in diminished profiles), because one has less sensation distally from pe-
vibratory and passive motion sense and an increase in ripheral neuropathy.
lower extremity reaction times.47,48 Pathological changes Older adults have more difficulty sensing vibration
such as axonal degeneration because of neuropathy result in the distal extremities and less sensitivity for detecting
in abnormalities in distal somatosensation.49,50 These so- smaller monofilaments. Diabetes is one of the most com-
matosensory changes have functional implications. Ducic mon conditions in older adults that causes changes in dis-
and colleagues51 and Reid and associates52 have reported tal somatosensation and vision.53
3970_Ch25_480-503 25/06/14 12:38 PM Page 486
486 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Chapter 25 • PHYSICAL THERAPY MANAGEMENT OF THE OLDER PERSON WITH VESTIBULAR DYSFUNCTION 487
associates73 suggest that therapists work with patients to Both cognition and depression af fect the ability of
reduce their fear of falling, thus also enhancing their func- the patient to follow through with an e xercise program.
tion. Older adults with vestibular disorders who expressed The older adult who is depressed or who has little support
fear of falling also report a history of depression.76 at home may have to be seen more frequently in the clinic
When asking a patient about a fall, the therapist must and will need closer monitoring by the therapist. The pa-
make sure to be using the same definition of a “fall” as the tient who displays an indif ferent or negative attitude to-
patient. In a recent systematic re view, no standardized ward therapeutic interv ention should not be merely
method was noted for the definition, measurement, or doc- dismissed as “lacking motivation.” Coexisting depression
umentation of injurious falls.77 The therapist should deter- may be the cause of the indifference. Anxiety has been re-
mine whether the patient has many “near falls”—coming ported to be more common than depression in persons
close to, but not actually, hitting the ground. Falls with no with vestibular disorders.86 Jacob87 and Clark and associ-
known cause are of concern to the therapist and must be ates88 have suggested that anxiety is strongly related to
investigated further to determine their cause. Noting vestibular dysfunction. The Dizziness Handicap Inventory
whether the patient was injured during a fall and required appears to relate to the Beck Depression In ventory and
medical attention is also very important to a better under- may be helpful for screening persons with vestibular dis-
standing of the seriousness of the fall reports. orders who might be experiencing depression.89
488 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Box 25-2
Chapter 25 • PHYSICAL THERAPY MANAGEMENT OF THE OLDER PERSON WITH VESTIBULAR DYSFUNCTION 489
Box 25-2
Continued
3970_Ch25_480-503 25/06/14 12:38 PM Page 490
490 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Box 25-2
Chapter 25 • PHYSICAL THERAPY MANAGEMENT OF THE OLDER PERSON WITH VESTIBULAR DYSFUNCTION 491
Box 25-2
Berg K, Wood-Dauphinee S, Williams J, Gayton D. Measuring balance in the elderly: preliminary development of
an instrument. Physiotherapy Canada. 1989;41(6):304-311.
Another tool that is helpful for assessing risk of Questionnaires for Balance
falls in older individuals is the functional reach test.103
The test was developed in older male veterans. It yields Assessment
a difference score in the patient’s willingness to reach The Activities-Specific Balance Confidence (ABC) Scale
forward without taking a step. To be able to perform the is a 16-item questionnaire that can be completed by the
test, the patient must be able to stand for 30 seconds patient or administered by the caregiver (Box 25-3).114,115
without support in flat or no shoes and must ha ve at The patient’s perceived confidence in performing 16 ac-
least 90 degrees of shoulder flexion. Patients are typi- tivities that are performed in and outside the house are
cally instructed to raise the arm, mak e a fist, and then rated by the patient from a range of 0 (no conf idence) to
reach forward along a yardstick as far as they can with- 100 (100% confident). Scores that are closer to 100 are a
out touching the wall or the yardstick. They are permit- better score on this scale. The ABC scale and the DHI have
ted to use any strategy they choose to complete the trial. been shown to ha ve a moderately ne gative correlation
Duncan and associates 104 have determined that scores (r = 2.64), indicating that the ABC scale is a valid tool for
of 6 inches or less on the functional reach test sho w a use in persons with v estibular dysfunction.116 The ABC
significant increase in the risk of falling in older adults. scale has shown to be sensitive to change over the course
Individuals who reach between 6 and 10 inches are at of rehabilitation.92,117,118
moderate risk for f alling.104 This test has some dra w- The ABC scale has been compared with the Mod-
backs. Functional reach is related to height; taller pa- ified Falls Efficacy Scale. 75 Both scales are sensiti ve
tients have longer functional reach scores than those tools that can be used in community-based older
who are shorter in stature. Functional reach scores have adults, and both discriminate individuals who are high-
been shown to change o ver the course of rehabilita- functioning from those who are low-functioning. Lajoie
tion.108 Functional reach is sometimes administered to and Gallagher119 have reported that older adults who
the patient who has dizziness, 105 although Wernick- score 66% or less on the ABC are at high risk for
Robinson and colleagues113 have suggested the test may falling. Myers and co workers114 previously reported
have little value in persons with vestibular dysfunction. that persons who scored less than 80% on the ABC
The functional reach test appears to be helpful in older scale were some what impaired and that those who
adults who complain of balance problems, b ut it may scored less than 50% were often home-bound indi vid-
have less discriminative value in persons with vestibular uals. Older adults should be able to perform most of the
disorders. 16 ABC activities with great confidence.
3970_Ch25_480-503 25/06/14 12:38 PM Page 492
492 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Box 25-3
From: Powell and Myers, 1995.86 Reprinted with permission of the Gerontological Society of America, 1030
15th Street, NW, Suite 250, Washington, DC 20005, via Copyright Clearance Center, Inc.
3970_Ch25_480-503 25/06/14 12:38 PM Page 493
Chapter 25 • PHYSICAL THERAPY MANAGEMENT OF THE OLDER PERSON WITH VESTIBULAR DYSFUNCTION 493
The Vestibular Activities of Daily Li ving (VADL) The Modified Fast Evaluation of Mobility, Balance,
Scale is another questionnaire that is helpful in determining and Fear Baseline (MFEMB AF) questionnaire is e x-
the functional capabilities of people living with vestibular tremely helpful in determining risk f actors for falling
disorders.120,121 The VADL scale is further discussed in the (Box 25-4).122,123 The therapist fills out “yes” or “no”
chapter by Cohen on disability (see Chapter 7). answers to the risk f actor questions either as he or she
Box 25-4
Risk Factors
YES NO
1. Needs aid for two (or more) basic activities of daily living (washing, cooking, dressing,
walking, continence, feeding) ____ ____
2. Needs aid for two (or more) instrumental activities of daily living (money management,
shopping, telephone, medications) ____ ____
3. Has had a fracture or articular problems at hips, knees, ankles, feet ____ ____
4. Has visible articular sequela in the mentioned joints ____ ____
5. Uses a walking device (e.g., cane, walker) ____ ____
6. Limits physical activity to basic activities of daily living at home ____ ____
7. Self-defines as anxious ____ ____
8. Complains of vertigo ____ ____
9. Complains of imbalance ____ ____
10. Makes complaints suggesting an existing postural hypotension ____ ____
11. Fell one or two times in the current year ____ ____
12. Fell more than twice in the current year ____ ____
13. Required nursing after the fall ____ ____
14. Had a fracture after the fall ____ ____
15. Is afraid of falling in general ____ ____
16. Is afraid of falling indoors (e.g., bathtub, kitchen) ____ ____
17. Is afraid of falling outdoors (e.g., bus, stairs, street) ____ ____
18. Avoids going outside for fear of falling ____ ____
19. Presents three or more somatic pathologies that require regular medical supervision ____ ____
20. The pathologies require home-based medical-social supervision ____ ____
21. Shows a specific pathology likely to induce falls: ____ ____
• neurological (e.g., cancer, peripheral neuropathy, multiple sclerosis, lupus)
• cardiovascular (e.g., postural hypotension)
• musculoskeletal (e.g., total joint replacements, arthritis)
• sensory (e.g., visual impairment)
• other (amputation, Parkinson’s disease, Alzheimer’s disease)
Continued
3970_Ch25_480-503 25/06/14 12:38 PM Page 494
494 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Box 25-4
From DiFabio and Seavy, 1997.94 With permission of the American Physical Therapy Association.
3970_Ch25_480-503 25/06/14 12:38 PM Page 495
Chapter 25 • PHYSICAL THERAPY MANAGEMENT OF THE OLDER PERSON WITH VESTIBULAR DYSFUNCTION 495
interviews the patient or after having obtained informa- faster gait speeds related to better health. 128 Others have
tion from the patient’s medical chart. This questionnaire suggested that faster gait speeds improve survival rates at
has a comprehensive list of fall risk questions, answers 8-year follow-up.129 Generally, gait speed is recorded from
to which help guide intervention. 3 to 5 meters with a stop watch.
The Vestibular Activities and P articipation (VAP) If the patient is complaining of balance problems, the
scale124 was developed using only activity and participa- single-leg stance (SLS), Romberg, and tandem Romberg
tion items from the International Classif ication of Func- tests are also performed. Bohannon and associates130 have
tioning (ICF). The VAP consists of 55 items b ut is found that SLS times significantly decrease as people get
currently undergoing analysis to determine if the scale can older.130 Single-leg stance, Romberg, and tandem Romberg
be shortened. The ICF core set for vertigo, dizziness, and tests help the therapist determine what kind of functional
balance disorders was recently developed at a consensus movements might be difficult for the patient.130-134 Gener-
in 2012, and the core sets should have value in future de- ally, the patient who is unable to stand in SLS usually has
sign of studies so that the w orld is using the same termi- great difficulty going up and down stairs without holding
nology for function.125 The largest number of items chosen onto the railing. Such a patient may also ha ve strength
were in the activities and participation area (40) followed deficits if unable to stay in SLS. The strength deficits can
by environmental items (29), body functions (25), and be determined through further testing. The patient who has
body structures (6).125 difficulty with the Romber g and tandem Romber g test is
often challenged while w alking through tight spaces.
Standing with the feet close together may be very destabi-
Dizziness Assessment lizing for such a patient. Some older adults may li ve in
The Dizziness Handicap In ventory (DHI) is e xtremely homes with narrow hallways or small rooms with little
helpful in determining what type of intervention will most clearance, and the therapist must consider the patient’s en-
benefit the patient with vestibular dysfunction.72 This tool vironment in designing the treatment program.
helps determine the self-perceived handicap of the indi- The Short Physical Performance Battery (SPPB) was
vidual completing the form. The patient answers 25 ques- developed to assess risk of f alling in older adults. 135 The
tions related to dizziness and/or handicap. There are three SPPB has 3 components: (1) the Romber g, semi-tandem
subdivisions of the test, and sub-scores can be calculated. Romberg, tandem Romberg, (2) repeated sit to stand, and
The test has been di vided into emotional, physical, and (3) gait speed. Scores range from 0 to 12, which has been
functional subsets. Information from this tool can signifi- norm-based on over 10,000 older adults (higher scores in-
cantly direct the treatment of the patient. If the patient dicate better function). 136 The SPPB is easy to complete
checks only the physical symptoms, one needs to look at and provides important information about overall health,
assessing positions and specif ic movements that predis- balance, and strength.
pose or increase the patient’s dizziness and/or falls.
Older adults who ha ve lost mobility as a result of
dizziness often check a signif icant number of the emo-
Home Assessment
tional questions on the DHI. One then must determine the Preparing the patient to function independently in his or
actual activity level of the person. Scores on the DHI have her own home is v ery important. Occasionally, a home
also been related to falls in persons with vestibular disor- visit is necessary for older persons with v estibular dys-
ders.118 Scores of 60 or higher were associated with in- function, if the therapist is concerned about their safety .
creased reports of f alls in persons with v estibular Determining how many stairs the patient must ascend or
disorders. Use of the SF-36 form can be helpful in assess- descend is critical. Some extrinsic environmental hazards
ing the activity level of the patient; the DHI, ho wever, is that have been identified are items such as poor lighting,
more responsive to changes after a 6- to 8-week course of uneven or slippery surf aces, loose rugs, steep stairs, ob-
vestibular rehabilitation.126,127 jects in the pathway, long bathrobes, inappropriate furni-
ture, and lack of handrails, especially in the bathroom.137
Modification of the home environment so that the pa-
Typical Balance Tests tient does not have to reach excessively either up or down
Gait speed is the most powerful measure of balance avail- to perform ADLs is helpful. The investigators at the Center
able and should be recorded on all older adults seen in a for Studies in Aging in Toronto developed a device to as-
balance clinic.128 A recent prospective study of 34,000 sist persons in the bathroom or kitchen who are v ery un-
people over the age of 65 suggests that gait speed, age, steady. The device, made of a material that makes it easy
and gender can predict how long a person will li ve, with to grip, is secured easily without damaging walls. Persons
3970_Ch25_480-503 25/06/14 12:38 PM Page 496
496 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
who have difficulty reaching without holding on may sig- documentation with description of state-by-state unsafe
nificantly benefit from this type of appliance in the home. driver reporting standards can be obtained at http://www
Primary care physicians, especially in managed care .ama-assn.org/go/olderdrivers. Cohen et al 142 have re-
situations, should be made a ware that such services are ported that some persons with vestibular disorders have
available to their patients. difficulty with driving, yet a recent report of 3 persons
Many of the older adults seen in our clinic with com- with bilateral vestibular loss over the age of 60 suggests
plaints of dizziness and balance dysfunction do not ha ve that people with bilateral loss may be capable of driving
a specific diagnosis. A total vestibular workup and a neu- without additional risk. When uncertain about the capa-
rology assessment of such patients are helpful and should bility of the person’s ability to drive, a driver examina-
be performed so that the physical therapist kno ws what tion is warranted.
interventions may be most effective.
Duration of Treatment
Driving Function in Older Adults Older adults frequently need to be treated for a longer time
According to the National Highway Traffic Safety Admin- than a younger patient. The longer duration of treatment
istration (NHTSA), the proportion of drivers in the United is related to the number of risk factors present in such pa-
States who were age 65+ increased 13% between 2000 tients and to their fear. They may be seen on a more tradi-
and 2009. Older drivers accounted for 12% of fatal traffic tional schedule of one to three times per week because of
crashes and 8% of all injuries nationwide. 138 Fatal crash their multiple medical problems and the risk of f alling
rates per mile traveled increase starting at age 75 and in- when unsupervised at home. Many older patients have dif-
crease significantly after age 80.139 ficulty being transported to physical therapy. This fact can
Many of the age-related issues that can contribute to complicate rehabilitation; the older adults’ cancellation
increased likelihood of imbalance and falling, such as vi- rate is often higher. If their transportation system breaks
sion, cognition, physical function, and medical f actors, down or if the weather is bad, man y older adults will be
may also contribute to the decline in driving skills.140 Be- forced to cancel their appointments; referral to a local
cause driving helps older adults remain mobile and inde- agency for the aging may be indicated to help the patient
pendent, issues related to dri ving safety often create obtain dependable transportation. Evidence now suggests
difficult decisions for older adult patients, their f amilies, that treatment outcomes in older adults are similar to those
and clinicians. These issues are further complicated by a in younger persons with the same vestibular disorder.117
lack of precise, easily administered and validated clinical
screening tools for driver safety, insufficient resources and
expenses for on-road evaluation, and poorly understood What to Do Once the Risk Factor
guidelines for clinicians in reporting unsafe dri vers that Has Been Identified in an Older
differ between states.
Against this background of clinical uncertainty, the
Adult
American Medical Association and the NHTSA ha ve After the older person with v estibular dysfunction has
jointly published guidelines that can assist physicians been assessed, it is important to determine what problems
and other clinicians to identify impairments that identified in the e valuation must be addressed, referral
may limit driving safety.141 These guidelines include the being one alternative. Patients who have visual problems
Assessment of Dri ving Related Skills (ADReS). The should be referred to an appropriate physician for further
ADReS is an easily administered battery that allo ws eye testing. People with undiagnosed vestibular disorders
screening of vision (acuity and peripheral fields), cogni- should be referred to a neurologist or otolaryngologist. If
tion (clock dra wing and trail-making) and motor/ a neuropathy is suspected, a referral to a neurologist, a
somatosensory function (walking speed, strength, range physical therapist specializing in electromyography, or a
of motion, and proprioception). Scoring standards for the physiatrist is recommended.
ADReS are provided as well as recommendations for fur- The physical or occupational therapist can also pro-
ther evaluation on substandard patient performance. It is vide an environmental assessment with specific recom-
important to note that results of ADReS screening have mendations, determine whether the patient needs an
not been specifically validated against crash outcomes. assistive device, and teach the patient about safety and
Thus, the results cannot be used to specifically infer risk clothes to wear to reduce the risk of f alling. In addition,
of a future crash but does identify limitations that could shoe type and wear can be determined, and recommenda-
potentially increase crash risk. The complete guideline tions can be made to the patient.The older adult who may
3970_Ch25_480-503 25/06/14 12:38 PM Page 497
Chapter 25 • PHYSICAL THERAPY MANAGEMENT OF THE OLDER PERSON WITH VESTIBULAR DYSFUNCTION 497
have chosen to wear inappropriate shoes can sometimes Motor weakness is most often assessed by performance
be counseled to change. of a manual muscle test or through the use of a dynamome-
During the environmental assessment, lighting in the ter. Strength deficits can be addressed, because older patients
patient’s home may be identif ied as a major risk f actor. have the potential to improve their strength, although it may
Many older adults use low-wattage light bulbs or keep the take 6 to 10 weeks for impro vement to be e vident.143-145
lights off most of the day to save money. Use of nightlights Range of motion is a major f actor that can be impro ved
is strongly suggested, especially in the bathroom. Motion through rehabilitation. Patients can be significantly at risk
detector lights, which are automatically acti vated when for falls if they lack adequate distal range of motion in their
one passes through the plane of the sensor, may also have feet.146 Having normal plantar flexion and dorsiflexion is ex-
some value. Additionally, the layout of some patients’ tremely helpful in preventing falls and achieving normal gait,
homes may cause significant changes in contrast of light because the feet are the only part of the body touching the
levels, which has been identif ied as a contrib utor to ground when one is walking. Assessing flexibility of the toes
falls.42,43 It is also advisable to have battery-operated lights and foot musculature may be of added benefit; having strong
that will come on when there is a po wer outage placed dynamic stabilizers distally may make the patient more sta-
around the house. Proper lighting must be addressed with ble.57 If the patient has an extremely immobile foot, perform-
the patient and family. ing normal balance reactions will be difficult.
Continued
3970_Ch25_480-503 25/06/14 12:38 PM Page 498
498 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Chapter 25 • PHYSICAL THERAPY MANAGEMENT OF THE OLDER PERSON WITH VESTIBULAR DYSFUNCTION 499
500 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Summary 16. Cohen HS. Disability and rehabilitation in the dizzy patient.
Curr Opin Neurol. 2006;19:49.
Older adults with vestibular disorders have some unique 17. Guerraz M, et al. Visual vertigo: symptom assessment, spa-
differences from younger adults. The normal physiological tial orientation and postural control. Brain. 2001;124:1646.
18. Page NG, Gresty MA. Motorist’s vestibular disorientation
changes associated with aging in the vestibular apparatus, syndrome. J Neurol Neurosurg Psychiatry. 1985;48:729.
the eye, and somatosensation can complicate the rehabil- 19. MacDougall HG, et al. On-road assessment of driving per-
itation of the older adult with a vestibular disorder. Older formance in bilateral vestibular-deficient patients. Ann N Y
adults can improve with vestibular rehabilitation but may Acad Sci. 2009;1164:413.
need special care. Comorbid medical problems that may 20. Ross MD, et al. Observations on normal and degenerating
human otoconia. Ann Otol Rhinol Laryngol. 1976;85:310.
be seen in older adults with v estibular disorders require 21. Jang YS, et al. Age-related changes on the morphology of
the physical therapist to think carefully before initiating the otoconia. Laryngoscope. 2006;116:996.
an intervention program. Patient safety and encouraging 22. Igarashi M, et al. Otoconia in young and elderly persons: a
compliance with the interv ention are essential. Careful temporal bone study. Acta Otolaryngol Suppl. 1993;504:26.
identification of the patient’s functional limitations enables 23. Baloh RW, Honrubia V, Jacobson K. Benign positional
vertigo: clinical and oculographic features in 240 cases.
a therapeutic program to be de vised to restore the older Neurology. 1987;37:371.
adult’s function safely. 24. Whitney SL, Marchetti GF, Morris LO. Usefulness of
the dizziness handicap inventory in the screening for
References benign paroxysmal positional vertigo. Otol Neurotol.
2005;26:1027.
1. Kroenke K, Mangelsdorff AD. Common symptoms in am- 25. Oghalai JS, et al. Unrecognized benign paroxysmal posi-
bulatory care: incidence, evaluation, therapy, and outcome. tional vertigo in elderly patients. Otolaryngol Head Neck
Am J Med. 1989;86:262. Surg. 2000;122:630.
2. Collard M, Chevalier Y. Vertigo. Curr Opin Neurol. 26. Gamiz MJ, Lopez-Escamez JA. Health-related quality of
1994;7:88. life in patients over sixty years old with benign paroxysmal
3. Aktas S, Celik Y. An evaluation of the underlying causes positional vertigo. Gerontology. 2004;50:82.
of fall-induced hip fractures in elderly persons. Ulus 27. Ekvall Hansson E, Mansson NO, Hakansson A. Benign
Travma Derg. 2004;10:250. paroxysmal positional vertigo among elderly patients in
4. Pothula VB, et al. Falls and vestibular impairment. Clin primary health care. Gerontology. 2005;51:386.
Otolaryngol. 2004;29:179. 28. Polensek SH, Sterk CE, Tusa RJ. Screening for vestibular
5. Rinne T, et al. Bilateral loss of vestibular function: clinical disorders: a study of clinicians’ compliance with recom-
findings in 53 patients. Journal of Neurology. 1998; mended practices. Med Sci Monit. 2008;14:CR238.
245:314. 29. Cohen HS, Kimball KT, Stewart MG. Benign paroxysmal
6. Bergstrom B. Morphology of the vestibular nerve, II: the positional vertigo and comorbid conditions. ORL J Otorhi-
number of myelinated vestibular nerve fibers in man at nolaryngol Relat Spec. 2004;66:11.
various ages. Acta Otolaryngol. 1973;76:173. 30. Vibert D, Kompis M, Hausler R. Benign paroxysmal
7. Richter E. Quantitative study of human Scarpa’s ganglion positional vertigo in older women may be related to
and vestibular sensory epithelia. Acta Otolaryngol. osteoporosis and osteopenia. Ann Otol Rhinol Laryngol.
1980;90:199. 2003;112:885.
8. Rosenhall U. Degenerative patterns in the aging human 31. Amor-Dorado JC, et al. Giant cell arteritis: a new associa-
vestibular neuro-epithelia. Acta Otolaryngol. 1973;76:208. tion with benign paroxysmal positional vertigo. Laryngo-
9. Wall C, 3rd, Black FO, Hunt AE. Effects of age, sex and scope. 2004;114:1420.
stimulus parameters upon vestibulo-ocular responses to 32. Gizzi M, Ayyagari S, Khattar V. The familial incidence of
sinusoidal rotation. Acta Otolaryngol. 1984;98:270. benign paroxysmal positional vertigo. Acta Otolaryngol.
10. Paige GD. Vestibular-ocular reflex (VOR) and adaptive 1998;118:774.
plasticity with aging. Soc Neurosci Abstr. 1989. 33. Viirre E, Purcell I, Baloh RW. The Dix-Hallpike test
11. Baloh RW, Sloane PD, Honrubia V. Quantitative vestibular and the canalith repositioning maneuver. Laryngoscope.
function testing in elderly patients with dizziness. Ear 2005;115:184.
Nose Throat J. 1989;68:935. 34. Bhattacharyya N, et al. Clinical practice guideline: benign
12. Paige GD. Senescence of human visual-vestibular interac- paroxysmal positional vertigo. Otolaryngol Head Neck
tions, 1.: vestibulo-ocular reflex and adaptive plasticity Surg. 2008;139:S47.
with aging. J Vestib Res. 1992;2:133. 35. Epley JM. The canalith repositioning procedure: for treat-
13. Nadol JB, Jr, Schuknecht HF. The pathology of peripheral ment of benign paroxysmal positional vertigo. Otolaryn-
vestibular disorders in the elderly. Ear Nose Throat J. gol Head Neck Surg. 1992;107:399.
1989;68:930. 36. Furman JM, Cass SP. A practical work-up for vertigo.
14. Brown KE, et al. Physical therapy outcomes for persons Contemp Intern Med. 1995;7:24.
with bilateral vestibular loss. Laryngoscope. 2001; 37. Spooner JW, Sakala SM, Baloh RW. Effect of aging on
111:1812. eye tracking. Arch Neurol. 1980;37:575.
15. Herdman SJ, et al. Falls in patients with vestibular deficits. 38. Sharpe JA, Sylvester TO. Effect of aging on horizontal
Am J Otol. 2000;21:847. smooth pursuit. Invest Ophthalmol Vis Sci. 1978;17:465.
3970_Ch25_480-503 25/06/14 12:38 PM Page 501
Chapter 25 • PHYSICAL THERAPY MANAGEMENT OF THE OLDER PERSON WITH VESTIBULAR DYSFUNCTION 501
39. McMurdo ME, Gaskell A. Dark adaptation and falls in the 61. Gill-Body KM, et al. Rehabilitation of balance in two pa-
elderly. Gerontology. 1991;37:221. tients with cerebellar dysfunction. Phys Ther. 1997;77:534.
40. Duncan PW, et al. How do physiological components of 62. Brown KE, et al. Physical therapy for central vestibular
balance affect mobility in elderly men? Arch Phys Med dysfunction. Arch Phys Med Rehabil. 2006;87:76.
Rehabil. 1993;74:1343. 63. Syrjala P, et al. Neurological diseases and accidental falls
41. Lord SR, Dayhew J. Visual risk factors for falls in older of the aged. J Neurol. 2003;250:1063.
people. J Am Geriatr Soc. 2001;49:508. 64. Whitman GT, et al. A prospective study of cerebral white
42. Arend O, et al. Contrast sensitivity loss is coupled with matter abnormalities in older people with gait dysfunction.
capillary dropout in patients with diabetes. Invest Neurology. 2001;57:990.
Ophthalmol Vis Sci. 1997;38:1819. 65. Kerber KA, et al. Disequilibrium in older people: a
43. Hirvela H, Koskela P, Laatikainen L. Visual acuity and prospective study. Neurology. 1998;51:574.
contrast sensitivity in the elderly. Acta Ophthalmol Scand. 66. Nutt JG, Marsden CD, Thompson PD. Human walking
1995;73:111. and higher-level gait disorders, particularly in the elderly.
44. Lord SR, Dayhew J, Howland A. Multifocal glasses im- Neurology. 1993;43:268.
pair edge-contrast sensitivity and depth perception and in- 67. Sudarsky L, Ronthal M. Gait disorders among elderly
crease the risk of falls in older people. J Am Geriatr Soc. patients. A survey study of 50 patients. Arch Neurol.
2002;50:1760. 1983;40:740.
45. McNulty L. Low vision impact on rehabilitation. Geriatr 68. Rosano C, et al. A regions-of-interest volumetric analysis
Notes. 1998;5:5. of mobility limitations in community-dwelling older
46. Council USNS. U.S. National Safety Council, Home adults. J Gerontol A Biol Sci Med Sci. 2007;62:1048.
Checklist: For detection of Hazards, Itaska, IL. 1982. 69. Peters A, Sethares C. Aging and the myelinated fibers
47. Brockelhurst Jea. Clinical correlation of sway in old in prefrontal cortex and corpus callosum of the monkey.
age-sensory modalities. Age Aging. 1982;11:1. J Comp Neurol. 2002;442:277.
48. Stelmach GE, Worringham CJ. Sensorimotor deficits re- 70. Legters K. Fear of falling. Phys Ther. 2002;82:264.
lated to postural stability. Implications for falling in the 71. Hatch J, Gill-Body KM, Portney LG. Determinants of
elderly. Clin Geriatr Med. 1985;1:679. balance confidence in community-dwelling elderly people.
49. Richardson JK, Ashton-Miller JA. Peripheral neuropathy: Phys Ther. 2003;83:1072.
an often-overlooked cause of falls in the elderly. Postgrad 72. Jacobson GP, Newman CW. The development of the
Med. 1996;99:161. Dizziness Handicap Inventory. Arch Otolaryngol Head
50. Richardson JK, et al. Moderate peripheral neuropathy im- Neck Surg. 1990;116:424.
pairs weight transfer and unipedal balance in the elderly. 73. Tinetti ME, Richman D, Powell L. Falls efficacy as a
Arch Phys Med Rehabil. 1996;77:1152. measure of fear of falling. J Gerontol. 1990;45:P239.
51. Ducic I, Short KW, Dellon AL. Relationship between loss 74. Tinetti ME, Williams CS. Falls, injuries due to falls, and
of pedal sensibility, balance, and falls in patients with the risk of admission to a nursing home. N Engl J Med.
peripheral neuropathy. Ann Plast Surg. 2004;52:535. 1997;337:1279.
52. Reid VA, et al. Using posturography to detect unsteadiness 75. Hill KD, et al. Fear of falling revisited. Arch Phys Med
in 13 patients with peripheral neuropathy: a pilot study. Rehabil. 1996;77:1025.
Neurol Clin Neurophysiol. 2002;2002:2. 76. Marchetti GF, et al. Factors associated with balance confi-
53. Braun E, et al. Balance abilities of older adults with and dence in older adults with health conditions affecting the
without diabetes. Issues Aging. 1996;19:19. balance and vestibular system. Arch Phys Med Rehabil.
54. Rossiter-Fornoff JE, et al. A cross-sectional validation 2011;92:1884.
study of the FICSIT common data base static balance 77. Schwenk M, et al. Definitions and methods of measuring
measures. Frailty and Injuries: Cooperative Studies of and reporting on injurious falls in randomised controlled
Intervention Techniques. J Gerontol A Biol Sci Med Sci. fall prevention trials: a systematic review. BMC Med Res
1995;50:M291. Methodol. 2012;12:50.
55. Bohannon RW. Hand-grip dynamometry predicts future 78. Shumway-Cook A, et al. The effects of two types of cog-
outcomes in aging adults. J Geriatr Phys Ther. 2008;31:3. nitive tasks on postural stability in older adults with and
56. Horak FB, Nashner LM. Central programming of postural without a history of falls. J Gerontol A Biol Sci Med Sci.
movements: adaptation to altered support-surface configu- 1997;52:M232.
rations. J Neurophysiol. 1986;55:1369. 79. Lundin-Olsson L, Nyberg L, Gustafson Y. “Stops walking
57. Mickle KJ, et al. ISB Clinical Biomechanics Award 2009: when talking” as a predictor of falls in elderly people.
toe weakness and deformity increase the risk of falls in Lancet. 1997;349:617.
older people. Clin Biomech (Bristol, Avon). 2009;24:787. 80. Lajoie Y, et al. Upright standing and gait: are there
58. Waddington GS, Adams RD. The effect of a 5-week changes in attentional requirements related to normal
wobble-board exercise intervention on ability to discrimi- aging? Exp Aging Res. 1996;22:185.
nate different degrees of ankle inversion, barefoot and 81. Maki BE, McIlroy WE. Influence of arousal and attention
wearing shoes: a study in healthy elderly. J Am Geriatr on the control of postural sway. J Vestib Res. 1996;6:53.
Soc. 2004;52:573. 82. Lundin-Olsson L, Nyberg L, Gustafson Y. Attention,
59. Mathias CJ. Orthostatic hypotension: causes, mechanisms, frailty, and falls: the effect of a manual task on basic
and influencing factors. Neurology. 1995;45:S6. mobility. J Am Geriatr Soc. 1998;46:758.
60. Mosnaim AD, et al. Etiology and risk factors for develop- 83. Lundin-Olsson L, Nyberg L, Gustafson Y. The Mobility
ing orthostatic hypotension. Am J Ther. 2010;17:86. Interaction Fall chart. Physiother Res Int. 2000;5:190.
3970_Ch25_480-503 25/06/14 12:38 PM Page 502
502 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
84. Bessot N, et al. Interference between walking and a cog- 105. Mann GC, et al. Functional reach and single leg stance in
nitive task is increased in patients with bilateral vestibu- patients with peripheral vestibular disorders. J Vestib Res.
lar loss. Gait Posture. 2012;36:319. 1996;6:343.
85. Yesavage J. Development and validation of a geriatric 106. Studenski S, et al. Predicting falls: the role of mobility
depression screening scale: a preliminary report. and nonphysical factors. J Am Geriatr Soc. 1994;42:297.
J Psychiatr Res. 1983;17:37. 107. Weiner DK, et al. Functional reach: a marker of physical
86. Grunfeld EA, et al. Screening for depression among frailty. J Am Geriatr Soc. 1992;40:203.
neuro-otology patients with and without identifiable 108. Weiner DK, et al. Does functional reach improve with
vestibular lesions. Int J Audiol. 2003;42:161. rehabilitation? Arch Phys Med Rehabil. 1993;74:796.
87. Jacob RG. Panic disorder and the vestibular system. 109. Thorbahn LD, Newton RA. Use of the Berg Balance Test
Psychiatr Clin North Am. 1988;11:361. to predict falls in elderly persons. 1996;76:576.
88. Clark DB, et al. Panic in otolaryngology patients present- 110. Godi M, et al. Comparison of reliability, validity, and
ing with dizziness or hearing loss. Am J Psychiatry. responsiveness of the Mini-BESTest and Berg Balance
1994;151:1223. Scale in patients with balance disorders. Phys Ther.
89. Hong SM, et al. Influence of Vestibular Disease on Psy- 2013;93:158.
chological Distress: A Multicenter Study. Otolaryngol 111. Hall CD, Herdman SJ. Reliability of clinical measures
Head Neck Surg. 2013. used to assess patients with peripheral vestibular disor-
90. Whitney SL, Hudak MT, Marchetti GF. The dynamic gait ders. J Neurol Phys Ther. 2006;30:74.
index relates to self-reported fall history in individuals 112. Wrisley DM, et al. Reliability of the dynamic gait index
with vestibular dysfunction. J Vestib Res. 2000;10:99. in people with vestibular disorders. Arch Phys Med
91. Hall CD, Schubert MC, Herdman SJ. Prediction of fall Rehabil. 2003;84:1528.
risk reduction as measured by dynamic gait index in 113. Wernick-Robinson M, Krebs DE, Giorgetti MM.
individuals with unilateral vestibular hypofunction. Otol Functional reach: does it really measure dynamic
Neurotol. 2004;25:746. balance? Arch Phys Med Rehabil. 1999;80:262.
92. Whitney SL, et al. Physical therapy for migraine-related 114. Myers AM, et al. Psychological indicators of balance
vestibulopathy and vestibular dysfunction with history confidence: relationship to actual and perceived abilities.
of migraine. Laryngoscope. 2000;110:1528. J Gerontol A Biol Sci Med Sci. 1996;51:M37.
93. Gananca FF, et al. Elderly falls associated with benign 115. Powell LE, Myers AM. The Activities-specific Balance
paroxysmal positional vertigo. Braz J Otorhinolaryngol. Confidence (ABC) Scale. J Gerontol A Biol Sci Med Sci.
2010;76:113. 1995;50A:M28.
94. Berg K, Norman KE. Functional assessment of balance 116. Whitney SL, Hudak MT, Marchetti GF. The activities-
and gait. Clin Geriatr Med. 1996;12:705. specific balance confidence scale and the dizziness hand-
95. Berg K, et al. Measuring balance in the elderly: Prelimi- icap inventory: a comparison. J Vestib Res. 1999;9:253.
nary development of an instrument. Physiother Canada. 117. Whitney SL, et al. The effect of age on vestibular rehabil-
1989;41:304. itation outcomes. Laryngoscope. 2002;112:1785.
96. Berg K, Wood-Dauphinee S, Williams JI. The Balance 118. Whitney SL, et al. Is perception of handicap related
Scale: reliability assessment with elderly residents and to functional performance in persons with vestibular
patients with an acute stroke. Scand J Rehabil Med. dysfunction? Otol Neurotol. 2004;25:139.
1995;27:27. 119. Lajoie Y, Gallagher SP. Predicting falls within the elderly
97. Berg Kea. Clinical and laboratory measures of postural community: comparison of postural sway, reaction time,
balance in an elderly population. Arch Phys Med Rehabil. the Berg Balance Scale and the Activities-specific Bal-
1992;73:1073. ance Confidence (ABC) scale for comparing fallers and
98. Wood-Dauphinee Sea. The balance scale: responsiveness non-fallers. Arch Gerontol Geriatr. 2004;38:11.
to clinically meaningful change. Canadian J Rehab. 120. Cohen HS, Kimball KT, Adams AS. Application of the
1997;10:35. vestibular disorders activities of daily living scale. Laryn-
99. Bogle Thorbahn LD, Newton RA. Use of the Berg goscope. 2000;110:1204.
Balance Test to predict falls in elderly persons. Phys 121. Cohen HS, Kimball KT. Development of the vestibular
Ther. 1996;76:576. disorders activities of daily living scale. Arch Otolaryn-
100. Shumway-Cook A, et al. Predicting the probability for gol Head Neck Surg. 2000;126:881.
falls in community-dwelling older adults. Phys Ther. 122. Arroyo Jea. Fast evaluation test for mobility, balance, and
1997;77:812. fear: a new strategy for the screening of elderly fallers.
101. Whitney S, Wrisley D, Furman J. Concurrent validity of the Arthritis Rheum. 1994;3:S416.
Berg Balance Scale and the Dynamic Gait Index in people 123. Di Fabio RP, Seay R. Use of the “fast evaluation of mo-
with vestibular dysfunction. Physiother Res Int. 2003;8:178. bility, balance, and fear” in elderly community dwellers:
102. Shumway-Cook A, Woollacott M. Motor Control. Theory validity and reliability. Phys Ther. 1997;77:904.
and Practical Applications, 1st ed. Baltimore: Williams 124. Alghwiri AA, et al. The development and validation of
and Wilkins; 1995. the vestibular activities and participation measure. Arch
103. Duncan PW, et al. Functional reach: a new clinical mea- Phys Med Rehabil. 2012;93:1822.
sure of balance. J Gerontol. 1990;45:M192. 125. Grill E, et al. International Classification of Functioning,
104. Duncan PW, et al. Functional reach: predictive validity Disability and Health (ICF) Core Set for patients with
in a sample of elderly male veterans. J Gerontol. vertigo, dizziness and balance disorders. J Vestib Res.
1992;47:M93. 2012;22:261.
3970_Ch25_480-503 25/06/14 12:38 PM Page 503
Chapter 25 • PHYSICAL THERAPY MANAGEMENT OF THE OLDER PERSON WITH VESTIBULAR DYSFUNCTION 503
126. Ware JE, Jr, Sherbourne CD. The MOS 36-item short- 137. Baraff LJ, et al. Practice guideline for the ED manage-
form health survey (SF-36), I: conceptual framework and ment of falls in community-dwelling elderly persons.
item selection. Med Care. 1992;30:473. Kaiser Permanente Medical Group. Ann Emerg Med.
127. Enloe LJ, Shields RK. Evaluation of health-related qual- 1997;30:480.
ity of life in individuals with vestibular disease using 138. United Stated Department of Transportation NHTSA.
disease-specific and general outcome measures. Phys Traffic Safety Facts, 2010 [cited 2013 Feb 21]: http://
Ther. 1997;77:890. www-nrd.nhtsa.dot.gov/Pubs/811391.PDF.
128. Studenski S, et al. Gait speed and survival in older adults. 139. Insurance Institute for Highway Safety (IIHS). Fatality
Jama. 2011;305:50. facts 2009, Older people, 2010 [cited 2013 Feb 21]:
129. Hardy SE, et al. Improvement in usual gait speed predicts http://www.iihs.org/research/fatality_facts_2009/
better survival in older adults. J Am Geriatr Soc. 2007; olderpeople.html.
55:1727. 140. Owsley C. Driver Capabilities in Transportation in an
130. Bohannon RW, et al. Decrease in timed balance test Aging Society: A Decade of Experience. Technical Pa-
scores with aging. Phys Ther. 1984;64:1067. pers and Reports from a Conference, 2004, Washington,
131. O’Loughlin JL, et al. Incidence of and risk factors for DC Transportation Research Board.
falls and injurious falls among the community-dwelling 141. Carr DB, et al. Physician’s Guide to Assessing and
elderly. Am J Epidemiol. 1993;137:342. Counseling Older Drivers, NHTSA, Editor 2010.
132. Vellas BJ, et al. One-leg balance is an important predictor 142. Cohen HS, et al. Driving disability and dizziness.
of injurious falls in older persons. J Am Geriatr Soc. J Safety Res. 2003;34:361.
1997;45:735. 143. Province MA, et al. The effects of exercise on falls in
133. Black FO, et al. Normal subject postural sway during the elderly patients. A preplanned meta-analysis of the
Romberg test. Am J Otolaryngol. 1982;3:309. FICSIT Trials. Frailty and Injuries: Cooperative Studies
134. Newton R. Review of tests of standing balance abilities. of Intervention Techniques. Jama. 1995;273:1341.
Brain Inj. 1989;3:335. 144. Lichtenstein MJ, et al. Exercise and balance in aged
135. Quadri P, et al. Lower limb function as predictor of falls women: a pilot controlled clinical trial. Arch Phys Med
and loss of mobility with social repercussions one year Rehabil. 1989;70:138.
after discharge among elderly inpatients. Aging Clin Exp 145. Lord SR, Castell S. Physical activity program for older
Res. 2005;17:82. persons: effect on balance, strength, neuromuscular
136. Guralnik JM, et al. A short physical performance battery control, and reaction time. Arch Phys Med Rehabil.
assessing lower extremity function: association with self- 1994;75:648.
reported disability and prediction of mortality and nurs- 146. Kemoun G, et al. Ankle dorsiflexion delay can predict
ing home admission. J Gerontol. 1994;49:M85. falls in the elderly. J Rehabil Med. 2002;34:278.
3970_Ch26_504-529 25/06/14 12:41 PM Page 504
CHAPTER 26
Physical Therapy
Management
of the Patient
with Vestibular
Dysfunction from
Head Trauma
Laura Morris, PT ■ Kim Gottshall, PT, PhD
Traumatic Brain Injury (TBI) has been def ined as damage The term concussion, used interchangeably with mild
to the brain, resulting from an external force such as an im- traumatic brain injury (mTBI), describes a complex patho-
pact, penetration from a projectile object, rapid acceleration/ physiological process that affects the brain. This process is
deceleration forces, or blast w aves. Brain function can be induced by traumatic biomechanical forces, but does not re-
disrupted temporarily or permanently, and structural damage quire direct contact to the head. For example, blast exposure
may or may not be identif ied using current imaging tech- can cause concussion, as can a f all that results in rapid
niques. Given the trauma to the head and the location of the acceleration/deceleration of the head but no direct contact
vestibular end organs, TBI can result in v estibular impair- between the head and the ground. Concussion causes a
ment. The impairment may be caused by peripheral damage rapid onset of short-lived impairments of neurological func-
to the end organ, central damage at the cerebellar or corte x tion that usually resolve spontaneously. Loss of conscious-
level, or a combination of both. This chapter outlines the ness may or may not be present with a concussion.2,3
unique considerations for the management of those with The diagnostic criteria for post-concussive syndrome
vestibular impairment and TBI. (PCS) have been defined by several groups, including the
Traumatic brain injury results in damage that ranges World Health Organization (WHO) for the ICD-10 cod-
from mild to se vere injury. Classification of the se verity ing system, and the American Psychiatric Association for
of TBI can be described as mild, moderate, or severe based the DSM-IV. These criteria differ in their inclusi veness
on Glasgow Coma Scale (GCS) ratings, the presence of (Box 26-1) and ha ve since been found to be fla wed.4-6
loss of consciousness (LOC), or post-traumatic amnesia The Centers for Disease Control (CDC) def ines PCS as
(PTA). See Table 26-1 for the classification structure that having a prolonged recovery, and generally the period of
is most commonly described. Neither the location of the 3 months is used to separate acute concussion from PCS.3
lesion, nor the nature of resulting impairment factors into There is little consensus or published literature that states
the severity classification.1 a clear delineation between mTBI or concussion and PCS.
504
3970_Ch26_504-529 25/06/14 12:41 PM Page 505
Chapter 26 • PHYSICAL THERAPY MANAGEMENT OF THE PATIENT WITH VESTIBULAR DYSFUNCTION 505
Loss of consciousness 0–30 minutes <30 minutes to <24 hours >24 hours
Post-traumatic amnesia <1 day >1 day but <7 days >7 days
Classification of the severity of TBI can be described as mild, moderate, or severe based on Glasgow Coma
Scale ratings, presence of loss of consciousness, or post-traumatic amnesia.
Box 26-1
Continued
3970_Ch26_504-529 25/06/14 12:41 PM Page 506
506 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Box 26-1
Second Impact Syndrome (SIS) is an unusual and neurotransmitters such as glutamate cause neuronal depo-
often fatal phenomenon in which an indi vidual sustains a larization that leads to an ef flux of potassium from the
second head injury before the resolution of the f irst head neuron and an influx of calcium into the neuron. The
injury. The first concussion may have been minutes, days, sodium-potassium pump in the cell membrane must then
or weeks prior. The second blow may be minor, with a di- work overtime to restore proper ionic balance within the
rect blow to the head, or an indirect injury that results in cell. The pump requires increased amounts of adenosine
accelerative forces to the brain. The patient will suddenly triphosphate (ATP). The increased demand for ATP causes
collapse and undergo rapid neurological decline and res- a large metabolic requirement for glucose. This sudden
piratory failure in the first few seconds to minutes after the metabolic need is accompanied by a general decrease in
injury. SIS results in death or se vere neurological impair- cerebral blood flow. The resulting decrease in the supply
ment. The pathophysiology of SIS is thought to be caused of energy in the form of glucose, and the increased demand
by either a subdural hemorrhage and/or dysautoregulation by the NA/K pump leads to a cellular metabolic crisis.
of the cerebral vasculature that causes widespread hyper- Once the initial period of ener gy crisis has passed,
emic brain swelling and increased intracranial pressure. the concussed brain enters a period of depressed metabo-
Adolescents and young adults are primarily affected.7-10 lism. Persistently high le vels of calcium in the cell are
toxic, leading to intracellular edema and dif fuse axonal
Pathophysiology of Mild TBI death. In addition, higher calcium levels have been shown
to disrupt posttraumatic neural connectivity.11,12
Injury to the brain following a mild TBI has been studied
extensively over the past decade. Our understanding of the
pathophysiology of mTBI is based on the work of Giza and Mechanism of Injury: Blast Injury
colleagues, which was described in 2001 (Fig. 26.1). 11,12
Unlike moderate to severe injuries, which cause focal vas-
Versus Blunt Head Trauma
cular or axonal lesions, mild injury results in a cascade of Blast wave exposure occurs from e xplosions of all
neurometabolic events that damage the brain’s processing types, including industrial accidents and military oper-
ability. Upon onset of a biomechanical injury , excitatory ations. Blast-induced injuries have been recognized as
3970_Ch26_504-529 25/06/14 12:41 PM Page 507
Chapter 26 • PHYSICAL THERAPY MANAGEMENT OF THE PATIENT WITH VESTIBULAR DYSFUNCTION 507
Decrease in Diffuse
Increase in Metabolic Axonal Lack of
demand + ATP
(energy)
= crisis swelling + perfusion = axonal
injury
B C
Figure 26.1 Pathophysiology of mTBI. (A) Acute effects of a mild TBI caused by disruption of neuronal membranes.
(B) A metabolic crisis occurs because of a rapid increase in energy needs, coupled with a decrease in available adenosine
triphosphate (ATP). (C) Once the initial period of energy crisis has passed, metabolism is depressed. Persistently high
levels of calcium in the cell are toxic, leading to intracellular edema and diffuse axonal death.
a major cause of head trauma in recent combat opera- Symptomatology in Head Trauma
tions, accounting for more than 80% of all battlef ield
injuries.13 Blast exposure is def ined as an e vent in Unlike the focal neurological changes that occur with mod-
which the individual feels or is e xposed to a pressure erate to severe brain injury, the diffuse nature of the meta-
wave before they hear a noise. The pressure wave may bolic impairment and axonal death leads to the broad symptom
be regarded as a primary causati ve factor of much of picture that occurs with mild brain injury. Figure 26.2 details
the brain injury seen after the e xposure. Individuals the symptoms that are typically described, and highlights
who experience this type of injury experience different the broad categories of impairment. 18 Dizziness is a very
symptoms and injury patterns than those who ha ve common symptom after traumatic brain injury , present in
blunt head trauma.13-17 23% to 81% of cases in the f irst few days after injury.19-22
The patterns of injury in survi vors of blast injury In the sports population, 55% of athletes report dizziness
can be complex because of multisystem in volvement
and the severity of injury. A large percentage of these
individuals suffer limb loss, orthopedic trauma, burns,
gastrointestinal injury, visual impairment and post- Somatic
traumatic stress disorder.16 The pressure wave from the • Dizziness
• Imbalance
blast can cause signif icant middle and inner ear dam- • Headaches
age, with resulting vestibular pathology. Shupak studied • Nausea
Israeli soldiers following blast exposure, and found that • Sensitivity to
light, sound
hearing loss, tinnitus, and tympanic membrane perfo- • Neck pain
ration occurred in 80% of subjects, and 60% had per-
sistent dizziness.17 Hoffer et al found that 98% of those
individuals experiencing blast injury reported dizziness Sleep Emotional
acutely, and 80% of the indi viduals reported dizziness • Hyper/hyposomnia • Anxiety
• Difficulty initiating • Lability
in the subacute and chronic phases. 13 Hoffer and col- sleep • Depression
leagues also reported that those indi viduals with blast • Irritability
injuries had increased rates of headache and greater
symptoms of disequilibrium than those with blunt head Cognitive
trauma. There was a reported dif ference in the nature • Attention
of the symptoms, as the individuals who suffered blast • Memory
injuries reported that their symptoms tended to be con- • “Fogginess”
• Cognitive
stant, as compared with the indi viduals with blunt endurance
head trauma, who had more intermittent symptoms. In- • Delayed
dividuals with blast injuries also showed higher rates of processing
hearing loss, post-traumatic spatial disorientation, and
cognitive dysfunction as compared with those with Figure 26.2 Symptoms from m (mild) TBI: Categories of
blunt head trauma.13 impairment and typical symptoms associated with mTBI.
3970_Ch26_504-529 25/06/14 12:41 PM Page 508
508 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
after concussion.23 When military personnel report symp- mTBI. In one group of non-military subjects with mTBI,
toms following blast-related mTBI, dizziness is the most 41% reported anxiety 5 years after injury.32 In military stud-
common post-injury symptom.13 ies, as many of 44% of soldiers in the Iraqi conflict that had
The etiology of dizziness following head trauma is di- a loss of consciousness during their head injury met the cri-
verse. The vestibular pathology found in head trauma can teria for post-traumatic stress disorder and endorsed symp-
be from temporal bone fractures, labyrinthine concussion, toms of anxiety.33 The pathophysiology of anxiety-related
benign paroxysmal positional vertigo (BPPV), vascular le- dizziness has been well described, and is belie ved to be
sions, central lesions, and perilymphatic f istula.14,24,25 caused by common central pathways in the brainstem that
Gottshall studied service members to describe type of in- perceive dizziness and vertigo and also control anxiety.34,35
jury and potential for recovery. She found that impairments Migraine–anxiety related dizziness has also been suggested
in gaze stability during head movement and disequilibrium as a separate entity , which may be seen as a sequela of
were common, as was exertional dizziness.14 Scherer et al mTBI.36,37 Careful interviewing of the patient and collabo-
studied blast exposure in service members with the inten- ration with other team members may help identify anxiety
tion of determining the etiology of dizziness.26 Using scle- in patients referred for v estibular rehabilitation, and the
ral search coil methods to study e ye movements during presence of anxiety will ha ve implications in the rehabili-
rapid head rotations, they found impairment in the angular tation process.
VOR (aVOR), and hypothesized that this could be caused Post-traumatic headache, both migrainous and non-
by differential destruction of Type I hair cells, or a disrup- migrainous, is a common sequela of mTBI.38 In addition to
tion of the irre gular afferent VOR pathways. This would photophobia, phonophobia, nausea, and visual changes,
account for normal v estibular function for lo w-velocity dizziness and vertigo are common symptoms in migraine,
movements that are detected by Type II cells, and lo wer occurring in 25% to 30% of the individuals with migraine.37
than normal aVOR gain with high-v elocity movements. These symptoms can occur without or without the headache.
Significantly, elevated symptom severity during exertion In the military population, Hof fer et al found that 41% of
was also found, consistent with w ork by Gottshall and soldiers with mTBI met criteria for migraine-related dizzi-
Hoffer. Scherer and colleagues found deficits in pitch plane ness.13 The pathophysiology of migrainous v ertigo is not
aVOR, which may contribute to the elevated dizziness dur- well understood, but may be a result of neuroanatomical
ing running, because running invokes greater head move- connections between the trigeminal nuclei and v estibular
ments in the pitch plane as compared with w alking, and nuclei.37 The presence of migrainous headache in athletes
thus places more of a demand on the pitch plane aVOR.26 with mTBI has been identified as being associated with sig-
There are other causes of dizziness withTBI that are not nificantly decreased neurocognitive function, as compared
related directly to peripheral v estibular loss. Post-traumatic with those with non-migrainous headache or no headache.38
BPPV, anxiety related dizziness, migraine-associated dizzi- The management of migraine by the medical team is impor-
ness, autonomic dysregulation, and cervicogenic dizziness tant to the o verall positive outcome of the rehabilitation
have all been implicated as sequelae of mTBI. The ortho- process. Well-managed migraine will allow patients to par-
pedic injuries associated with head injury often involve the ticipate more fully in the rehabilitation process.
cervical spine, so a cervical etiology to dizziness should be Dizziness may also occur in mTBI caused by auto-
assessed.27-29 The evaluation and management of cervico- nomic dysregulation. Patients with autonomic dysregula-
genic dizziness is discussed in Chapter 31. tion typically report dizziness with position changes such
Post-traumatic BPPV is a common occurrence follow- as sit to stand, bending over, and climbing stairs and often
ing head trauma. The estimated incidence of post-traumatic note that any form of exertion may provoke dizziness. The
BPPV in the TBI population with symptoms of dizziness symptoms experienced from autonomic changes may
varies widely, from less than 5% to 28%. 13-30 The differ- mimic BPPV or mo vement intolerance, so care must be
ences in the reported incidence rates may be a result of the taken to assess symptoms closely . There is occasionally
nature and extent of the TBI (concussion vs. blast exposure), clear evidence of orthostatic hypotension, but more often
as well as length of time between the head trauma and the the changes are transient and may not be detectable with
time that patients are first assessed. Spontaneous resolution blood pressure monitoring. Later in the recovery process,
can occur with BPPV, which may account for the lower in- patients may have better tolerance for position changes but
cidence of BPPV reported in some studies. The incidence may experience dizziness during exercise or any activity
of bilateral BPPV is higher in post-traumatic as compared that increases heart rate.39
with idiopathic BPPV.31 Postural instability and impaired balance reactions
Anxiety-related dizziness has been found to be present may be caused by sensory organization dysfunction and/or
in both military and non-military populations follo wing vestibulospinal reflex impairment. Sensory or ganization
3970_Ch26_504-529 25/06/14 12:41 PM Page 509
Chapter 26 • PHYSICAL THERAPY MANAGEMENT OF THE PATIENT WITH VESTIBULAR DYSFUNCTION 509
impairment may be a result of abnormal central processing dysfunction may be less clear, and may be difficult to de-
of the input from peripheral end or gan, or impairment of termine in the presence of se vere oculomotor deficits or
the end organ itself in the case of peripheral vestibular le- central patterns of nystagmus. In mild brain injury, the di-
sions. Guskiewicz et al studied concussed athletes and agnostic process is less clear, and a standard of assessment
found impairment in sensory organization using comput- has been developing over the past two decades.
erized and clinical assessment tools.40,41 Numerous imaging techniques hold promise as diag-
In addition to somatic symptoms, cognitive symptoms nostic tools and as measures of reco very. Diagnostic im-
are a hallmark sign of mild brain injury. Typical impairments aging, using standard CT or MRI scanning, is not sensitive
include limited attention, a sensation of mental “fogginess,” enough to reveal mTBI/concussion in most cases. Because
impaired immediate and delayed recall, decreased cognitive the injury is metabolic in nature and the dysfunction is dif-
endurance, and delayed cognitive processing. Multitasking fuse rather than focal, no abnormalities can be identified.
and the ability to alternate tasks are also impaired. Because There are several imaging techniques that can be used to
of decreases in metabolism and increased energy demands, reveal changes associated with mTBI. The development
new learning is often difficult.42 of single-photon emission CT (SPECT) imaging has al-
Sleep disturbance complicates many other functions, lowed researchers to identify changes in blood flo w and
and sleep is often impaired in indi viduals with mTBI. The perfusion of cortical tissue. Abu-Judeh et al, were able to
disturbances may be in initiating sleep, maintaining sleep, identify abnormal perfusion as part of the pathophysiolog-
or sleeping too much (hypersomnia). 43 Lack of adequate ical changes following mild to moderate TBI.47 Positron
sleep exacerbates many of the same symptoms that are emission tomography (PET scans) measures metabolic
caused by the initial brain injury , including irritability and changes in the brain. This makes PET scans particularly
anxiety, depression, decreased concentration and attention, helpful in identifying the changes that occur in mTBI. In
delayed reaction time, decreased energy levels, and fatigue.44 one study by Chen et al, subjects with mTBI appeared nor-
Emotional symptoms are also widely described with mal at rest. 48 When PET scans were measured after per -
concussion; these symptoms include irritability , anxiety, forming a cognitively difficult task, there was a significant
depression, and emotional lability. Healthy adolescents difference in images between controls and the subjects
tend to have difficulty regulating their emotions, which is with mTBI. The use of fMRI, which sho ws local blood
often worsened with concussion.45 The strong comorbidity flow and metabolic changes in real time, was used as well
between anxiety and dizziness should trigger therapists to and found the same results.49 In a study performed on high
pay close attention to the presence and persistence of anx- school athletes, there was a positive correlation between
iety in their patients.6,46 the extent of abnormal brain hyperactivation found on the
As therapists managing individuals with brain injury, fMRI studies and the length of the clinical reco very, as
we must take into account these other areas of symptoms measured by cognitive testing and reported symptoms. 50
that may affect our patients’ abilities to recover from their In the future, it may be possible to use fMRI to give more
vestibular impairment. Assessing the patient in a holistic objective data to support return to play , or removal from
manner should improve treatment effectiveness and ulti- play, for athletes.
mately result in better outcomes and less frustration during Proton magnetic resonance (MR) spectroscopy mea-
the rehabilitation process. Managing all aspects of the pa- sures brain metabolites, and this has provided an objective
tient’s impairments are not within our scope of practice, basis to confirm the presence of a metabolic imbalance in
but knowledge of a patient’s symptom picture and overall brain tissue. Vagnozzi et al imaged concussed athletes via
challenges will allow us to refer patients, as appropriate, proton MR spectroscop y and found the ratio between
to other practitioners and allow for more realistic e xpec- N-acetylaspartate (NAA) to creatinine (Cr) w as reduced
tations of the patient. Working with a multidisciplinary for 30 days after the f irst mild brain injury, and 45 days
team will also allow for better management of this broad after two injuries.51,52 Diffusion Tensor Imaging (DTI) is
scope of recovery. an imaging technique that measures white matter changes
in the brain. In a recent prospective study by Mayer et al,
those with mTBI were found to ha ve abnormal DTI im-
Examination aging that was sensitive to change over time, and this may
serve as a potential objective biomarker of recovery in the
Diagnostic Imaging future.53
The process of identification of moderate to severe brain Although most patients do not recei ve these ad-
injury is relatively straightforward, using imaging and vanced imaging techniques, the tests may be used more
clinical neurological testing. The presence of v estibular commonly as technology impro ves and more is learned
3970_Ch26_504-529 25/06/14 12:41 PM Page 510
510 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
about the diagnostic utility of these imaging techniques in problems, but are not as specific as the Dizziness Handicap
the future. Inventory62 or the Activities-specific Balance Confidence
Scale.63 The Rivermead Post Concussion Symptom Ques-
tionnaire,64 the Post Concussion Symptom Scale (PCSS),65
Acute Testing
the Graded Symptom checklist, 56 and the Concussion
Accurate and objecti ve clinical assessment of mTBI Symptom Inventory65 are all used to measure symptom
should be multifactorial to be sensitive to the broad range severity. These assessment tools vary from 12 to 22 items
of dysfunction that is commonly found in this popula- and use either 5 or 7 point Likert scales. Caution should
tion. Much of the w ork in developing assessment tools be used when making management decisions based
has been focused on athletic injuries, with the goals of solely on a patient’s symptoms, because symptoms may
(1) establishing an on-field test to determine if an athlete be under- or over-reported, depending on the patient’ s
has sustained an mTBI, and (2) establishing a test to de- situation.66,67
termine whether the athlete should return to play follow-
ing an mTBI. An international group of practitioners
Neurocognitive Testing
developed a consensus statement that outlined the man-
agement of concussion in sport. As part of this consensus Assessment of neurocognitive function is an integral part
statement, the Sports Concussion Assessment Tool, or of the management of the post-concussive patient, and has
SCAT3, was recommended for sideline assessment. It been endorsed by leaders in the field as part of the assess-
consists of se ven subtests: (1) the Glasgo w coma scale ment battery.2,68 There are many forms of assessment, both
(GCS), (2) an orientation to game/play called the Maddocks computerized testing and paper and pencil testing. Regard-
score, (3) a structured symptom scale, (4) cogniti ve less of the actual test, the testing domains are the same and
assessment, (5) cervical examination, (6) balance assess- are listed in Box 26-2. The testing can provide information
ment using either the modif ied BESS (Balance Error on changes in cogniti ve function if performed serially .
Scoring System) test or a tandem gait test, and (7) a co - Some practice models endorse regular testing to determine
ordination test. Imbedded in the SCAT3 is the Sideline improvement in function o ver time. There is, however,
Assessment of Concussion, or SAC, which is a cognitive some controversy over whether pain, emotional distress,
assessment test. It consists of tests of basic orientation, and depression may influence the outcomes of neurocog-
immediate memory, concentration, and delayed recall. A nitive assessment.69-72 There is a trend toward performing
pediatric version of the test has also been de veloped, baseline testing, which allo ws for pre- and post-injury
called the Child SCAT3. The seven areas of assessment comparison. This data may be helpful in determining level
are similar, with modifications to appropriately assess of impairment and management of the patient.73 There has
children from 5 to 12 years old.18,54-58 been some suggestion that the baseline data and subse-
One limitation in the currently used assessment is the quent neurocognitive post-injury data are not always used
lack of dynamic balance tasks as opposed to static testing, effectively when making return-to-play decisions, and that
and the lack of dual task assessment. Catena et al ha ve
proposed that dual-task balance testing may be a better
screening tool for identifying dysfunction in the concussed
athlete.59-61 This research focused on dual tasks such as
Box 26-2
answering questions while w alking and during obstacle
TYPICAL COGNITIVE
crossing tasks. In these studies, walking while answering
FUNCTIONS THAT ARE
questions was found to be sensitive to concussive impair-
ASSESSED IN STANDARDIZED
ment if assessed within 6 days of injury.
NEUROCOGNITIVE TESTING
• Attention Span
Subjective Symptom Scales for • Working Memory
Assessment of mTBI/Concussion • Sustained Attention
In addition to the subjecti ve scale mentioned previously, • Selective Attention
there are several subjective symptom scales that are used • Nonverbal Problem Solving
for both acute and subacute assessment of TBI. These • Reaction Time
scales measure the global symptoms of post-concussi ve • Visual Memory and Verbal Memory
symptoms and are not focused on v estibular symptoms. • Response Variability
They all contain some reference to dizziness and balance
3970_Ch26_504-529 25/06/14 12:41 PM Page 511
Chapter 26 • PHYSICAL THERAPY MANAGEMENT OF THE PATIENT WITH VESTIBULAR DYSFUNCTION 511
symptom report, rather than objecti ve data, guides deci- these various components in a more global balance assess-
sion making. As the f ield of concussion management ment tool.83
grows and education impro ves, the use of the objecti ve Two balance tests have been designed specifically
data should increase.74 As with all assessment tools used for this patient population. The Balance Error Scoring
for concussion diagnosis and management, neurocognitive Scale (BESS) is recommended for sideline assessment
testing should not be used as a single measure, but as part for individuals with suspected concussion, and mTBI
of a comprehensive patient assessment.65 and can be used later in the recovery process as well. 84
The HiMAT test was specifically developed for assess-
ing people with traumatic brain injury . It is a measure
Clinical Examination of high-level mobility, such as dynamic w alking tasks,
Physical therapy assessment of patients with suspected the ability to ne gotiate stairs, running, skipping, hop-
vestibular impairment caused by mild to severe TBI follows ping, and bounding. 85,86 This measure can be uniquely
a similar practice pattern to those without TBI, although helpful in determining return to sport or return to active
care must be taken to attend to possible comorbidities. For work duty for physically challenging jobs.
subjective assessment of symptoms, there are a v ariety of
tools that can be used to assess the impact of the vestibular
Oculomotor Findings in TBI
impairment on the indi vidual’s ability to function. Two
commonly used tools are the Dizziness Handicap Inventory, A variety of oculomotor abnormalities can be observed in
which can be used to measure the impact of the dizziness individuals as a result of TBI. Some of these findings may
on specific tasks,62 and the Activities-specific Balance Con- be related to a loss of v estibular function; other findings
fidence Scale, which assesses balance conf idence over a may be related to deficits in the central oculomotor path-
number of conditions.63 The Vestibular Rehabilitation Bal- ways or damage to the e xtraocular muscles. Some of the
ance Questionnaire (VRBQ) can be used to monitor sub- patient’s symptoms may be attributable to these oculomo-
jective dizziness and also to measure changes in quality of tor deficits. The dynamic visual acuity test (DVA), which
life.75 The Vestibular Activities of Daily Living scale mea- assesses an individual’s ability to see clearly during head
sures functional difficulty with various tasks and is one of movements, is a functional measure of presumed VOR
the few scales that also addresses the issue of participa- function. Dynamic visual acuity testing can be measured
tion.76 Visual-motion induced symptoms can be quantified by a clinical test or with a computerized system.Although
using the Situational Vertigo Questionnaire77 or the Visual either method allows for insight into gaze stability , the
Vertigo Analog Questionnaire.78 computerized DVA is more sensitive than the clinical DVA
Because a wide v ariety of people ha ve traumatic test. Computerized testing may include a battery of tests
brain injuries, from the young athlete to the elderly person that are thought to measure perception time (PT), tar get
with TBI as a result of a f all, there is no uni versally ac- acquisition (TA), target following (TF), gaze stabilization
cepted objective measurement tool that will meet the (GST), and dynamic visual acuity (DVA). Dynamic visual
needs of this patient population. Selection of the appro- acuity is measured as the difference between static and dy-
priate assessment tools should take into account the needs namic visual acuity, and is typically reported as a logMAR
and goals of the individual patient. For the athlete, the tests score (log minimal angle of resolution). Computerized
must be challenging enough to make return to play deci- testing has been used to identify gaze stability impair -
sions; for the nonathlete, the tests should determine f all ments in those with mTBI and to track changes with re-
risk and the ability to return to pre vious activity levels. covery.14 Computerized DVA testing has been found
The ability to use dif ferent sensory signals for postural sensitive and reliable for identifying v estibular impair-
control can be measured using computerized dynamic pos- ment.87 This type of testing may be helpful in identifying
turography (CDP) testing or the modified Clinical Test of subtle impairments in elite athletes or young, higher-level
Sensory Interaction in Balance (mCTSIB).79,80 The Func- patients.
tional Gait Assessment (FGA) measures gait tasks that in- In addition to the assessment of gaze stability, a thor-
corporate head movement, narrow base of support, and ough oculomotor assessment is critical. There is evidence
changing speeds.81,82 The test is similar to the Dynamic for saccadic and smooth pursuit deficits with TBI, caused
Gait Index (DGI), but includes more challenging tasks that by central nervous system impairment. These impairments
avoid the ceiling effects found with the DGI when testing are not sensitive as a diagnostic tool, but may have impli-
higher-functioning patients. The FGA also has an identi- cations for rehabilitation and reco very. A person with
fied fall risk cutoff of 22/30, which is helpful for assessing saccadic or smooth pursuit def icits may have difficulty
lower level TBI patients.82 The mini-BESTest combines reading, tracking people or objects in his/her environment,
3970_Ch26_504-529 25/06/14 12:41 PM Page 512
512 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
or visually scanning. 88,89 There is very limited evidence convergence spasm is similar to other dystonias and that
(only small-size case studies without control groups) to botulinum toxin treatment may be ef fective.97 There is
suggest that an oculomotor training program (fixation, sac- no evidence that any oculomotor exercise will help with
cades, smooth pursuit, and simulated reading) could lead recovery from convergence spasm.
to improvement in reading function in subjects with TBI As in patients with symptoms of dizziness not related
and CVA.89 to head trauma, findings of oculomotor abnormalities dur-
Vergence and accommodative abnormalities have also ing the clinical exam should be discussed with the refer -
been identified as oculomotor impairments in TBI.90 Con- ring physician or medical team because of the implications
vergence insufficiency, or the inability to generate the ap- for central nervous system involvement.
propriate amount of ocular convergence to maintain clear
and single binocular vision with a near tar get, has been
identified in TBI, but the specific etiology of the impair - Intervention Considerations
ment is unknown. The neurons that control v ergence are
Problem-oriented Approach
located near the oculomotor nucleus in the mesencephalic
reticular formation, and may be implicated because of in- Those patients with physical therapy needs following trau-
jury at the brainstem level during TBI.91 Some individuals matic brain injury progress at different rates. Following a
with vergence disorders following TBI endorse symptoms problem-oriented approach and assessing patients care-
of dizziness that are non-vestibular in nature and have vi- fully may maximize recovery in the most efficient manner.
sual motion–provoked dizziness.90 It is not clear in these When developing a treatment plan, the therapist may need
cases if the individual’s symptoms are a result of the con- to prioritize the impairments, because of the diversity and
vergence insufficiency (dizziness caused by blurred vision number of impairments associated with TBI (Fig. 26.3).
or diplopia) or because of other underlying deficits as a re- In addition, the therapist will need to maintain fle xibility
sult of the TBI. Screening for convergence insufficiency is and be able to modify the interv entions to maintain an
important for accurate assessment and ef ficient manage- optimal level of challenge to the patient.
ment of the rehabilitation process. Headache, fatigue, and Recovery typically happens in a progressi ve fashion,
loss of concentration are also symptoms reported with non- and the rehabilitation process follows in a similar progressive
vestibular oculomotor deficits.92 There has been some ev- fashion (Fig. 26.4). The general process starts with medical
idence to suggest that vision therapy designed to improve management and physical therapy intervention as appropri-
the near point for con vergence can be ef fective.89,92,93 ate, incorporating musculoskeletal intervention and vestibu-
Vision therapy often consists of clinical visits with a neuro- lar rehabilitation techniques. The next step in the process is
optometrist and home e xercise programs. If convergence aerobic conditioning and the addition of strength/po wer
insufficiency is identified during the oculomotor exam, and training as appropriate. Once the patient is able to tolerate
the patient reports an increase in dizziness with convergence aerobic training and strength/power exercises without exac-
tasks, it may be beneficial to incorporate some convergence erbation of his or her symptoms, functional training for
tasks into the intervention plan. If symptoms or oculomotor return to sport or w ork can be initiated. This may take the
abnormalities persist, a discussion with the referring physi- form of high-velocity ball tasks, hopping, jumping, running,
cian and possible recommendation to neuro-ophthalmology climbing ladders, or repetitive tasks that require rapid move-
or neuro-optometry would be appropriate. ment. Customization and creativity are necessary to individ-
Convergence Spasm is defined as an inappropriate or ualize the intervention to the patient’s specific functional
excessive convergence, accompanied by pupillary miosis, needs. This is often the last step in the physical therapist’ s
lasting seconds to minutes, and occasionally longer. This involvement with the patient.
impairment was first described as a psychosomatic phe- The recovery process is not necessarily o ver at this
nomenon, often accompanied by anxiety or panic. An or- point for athletes, members of the military, or other indi-
ganic etiology to convergence spasm was implicated with viduals, depending on their job requirements. Athletes will
TBI, likely caused by brainstem in volvement.94-96 The likely need to w ork on sport-specific training. Return to
spasm is brought on most often by v ertical eye move- practice with the team may be appropriate if symptom-
ments. Patients who experience convergence spasm de- free. There should be no return to play until symptoms are
scribe symptoms of vague discomfort, disequilibrium, or fully resolved and neurological and cogniti ve testing is
dizziness, especially with reading or looking down. Until normal. For service members, combat-specif ic training
recently, the standard treatments involved atropine, which will be needed, incorporating virtual reality with a moving
dilates the pupil and breaks the spasmodic pattern, correc- support surface to simulate combat situations. F or those
tive lenses, or occlusion. There has been suggestion that who work at heights, like electrical workers, iron workers,
3970_Ch26_504-529 25/06/14 12:41 PM Page 513
Chapter 26 • PHYSICAL THERAPY MANAGEMENT OF THE PATIENT WITH VESTIBULAR DYSFUNCTION 513
514 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
symptoms with the same time-to-resolution as discussed Leddy et al studied both athletes and nonathletes who were
above. As head motion tolerance increases, the e xercises more than 1 month post-concussion. The symptoms that pa-
can be increased in terms of v elocity, number, and com- tients identified upon exertion assessment were headache,
plexity. The exercises may be performed in standing and dizziness/balance, sadness/depression, irritability, fatigue,
may involve trunk and whole-body mo vements. One of and concentration/memory impairments. The investigators
the challenges in treating motion sensitivity in individuals found that these symptoms could be reduced or alle viated
with TBI is that the exertion level is often increased as one by an individualized, controlled aerobic exercise program
moves with greater speed and larger body movements. Be- that trains patients with a sub-symptom threshold paradigm.
cause exertion can provoke symptoms as well, these tw o The subjects underwent an exertion assessment on a tread-
problems can interfere with one another. Cervical dysfunc- mill, in which the exertion level (as measured by heart rate)
tion and migraine can complicate the treatment of motion that provoked symptoms (symptom threshold) was identi-
sensitivity, and occasionally, habituation exercises must fied. Exercise was started at 80% of symptom threshold for
be postponed. 5 to 6 days per week, with the exertion level increased grad-
ually as long as symptoms stayed under control. Duration
was also increased within the patient’s tolerance. Using this
Postural Instability intervention plan, Leddy et al found that 72% of patients
Postural demands vary across individuals and will v ary returned to full daily functioning.
with age, lifestyle demands, and acti vity levels. An indi- In following a training program like this, it is impor-
vidual involved in athletic endeavors will have greater pos- tant to ensure that patients are being honest in the report-
tural stability needs that an individual who has a sedentary ing of symptoms, because many individuals are motivated
lifestyle. For individuals with TBI, recovery of postural sta- to return to sport or normal activity levels and may under-
bility can be a complicated issue gi ven the diffuse nature report symptoms. If patients ha ve persistent baseline
of their injuries. Whereas individuals with peripheral symptoms of any sort before the aerobic exercise training,
vestibular disorders generally have difficulty with the ap- these symptoms need to remain stable without e xacerba-
propriate use of the different sensory cues for the mainte- tion for multiple treatment sessions before progression of
nance of balance, individuals with TBI and damage to the the intensity or duration of the training program.
central nervous system may also experience disruption of
the automatic postural responses and anticipatory postural
Acute Management Issues
adjustments. Treatment of postural stability deficits in these
cases will need to move beyond the typical exercises used Immediately after injury and for the f irst few days, those
to promote the utilization of v estibular cues for balance, with concussion should be monitored closely and encour-
and will need to incorporate exercises to work on balance aged to rest if symptoms are present. Rest includes both
reactions to expected and unexpected perturbations. Static physical and cognitive rest, which includes avoiding social
and dynamic balance e xercises using the dual-task para- interaction, as well as not using telephones and television.
digm are often beneficial. In developing interventions to Playing video games should be avoided because of the cog-
treat the postural instability, the therapist should be mindful nitive engagement and visual motion stimulation. Because
of the needs of the patient in terms of the postural demands of impairments in sensory processing and limited cognitive
of work and normal activity levels. resources for managing complex environments, busy com-
munity or social events may cause space and motion dis-
comfort or visual motion intolerance. These environments
Exertion Intolerance may be overwhelming and cause increased symptoms, and
Exertion intolerance is a unique problem in TBI. It is un- as such, these experiences should be avoided in the early
clear whether the dizziness reported is a result of movement stage. As symptoms resolve, graded exposure to complex
in the pitch plane or caused by the e xertion itself. Scherer sensory environments is recommended. Majersk e et al
and colleagues found that service members with mild to found that individuals who returned to play or w ork and
moderate TBI secondary to blast exposure and complaints experienced high levels of exertion had increased symp-
of dizziness had greater exertion-induced symptoms and de- toms and cognitive impairments.100 Limiting activity in the
creased angular VOR gains to pitch plane head impulses, short term after concussion will lik ely result in a quick er
as compared with those without symptoms of dizziness fol- resolution of symptoms and return to full function.
lowing blast exposure.26 Leddy and colleagues39,99 theorize Education is a critical component of successful recov-
that there is ongoing central and systemic physiological ery at this stage. When written information about concussion
regulatory dysfunction that causes symptoms with exertion. was supplied to injured subjects at the onset, the subjects
3970_Ch26_504-529 25/06/14 12:41 PM Page 515
Chapter 26 • PHYSICAL THERAPY MANAGEMENT OF THE PATIENT WITH VESTIBULAR DYSFUNCTION 515
reported significantly less stress 3 months post-injury.101 A tests automatically with any report of dizziness, but others
clear understanding of the risks of repeated concussions and wait until there is clear delineation between v estibular
the physiological rationale behind appropriate levels of rest symptoms and non-vestibular dizziness. If there is an y in-
will help to a void prolonged or incomplete reco very. In- dication that a v estibulopathy is present during physical
volvement of parents, coaches, and trainers in the education therapy assessment, a referral may be appropriate. If a pa-
process, as appropriate, should impro ve the consistency of tient has dizziness that is vestibular in origin, it is appropri-
the activity restrictions. Because of the cogniti ve and pro- ate to initiate physical therap y intervention at this time as
cessing deficits, both written and v erbal communication long as the interventions are within the patient’s tolerance.
should be used to improve information retention. In clinical A conservative approach may be wise initially , to ensure
settings, patients may appear to understand and assimilate that the patient does not experience a marked and prolonged
your verbal recommendations, but delayed recall may still exacerbation of symptoms. If a patient demonstrates motion
impair their ability to remember the recommendations when sensitivity and postural stability impairments, initiating bal-
they leave the clinic. When exercises are prescribed for a ance tasks is a good place to start the intervention. Eye-head
patient, written instructions and an exercise log may be ben- coordination tasks may be recommended if the y are well
eficial to enhance compliance with the exercise program. tolerated. Exercises will most likely provoke symptoms, but
In the acute stage, activity level (such as returning to the resulting dizziness should measure no more than a 3 to
school), exercise, or social interaction should only be re- 4 (out of 10) using either a numerical rating scale or visual
stricted if the individual reports symptoms. Progression of analog scale, and the symptoms should resolv e within a
the individual’s activities should occur when the individual few minutes after completion of the task.
is symptom-free with the current level of activity. Although
exertion should be restricted if exacerbation of symptoms
Management Considerations
occurs, all types of activity should be moderated according
with Chronic TBI
to symptom levels. If, for e xample, brisk walking causes
an increase in symptoms but static postural control activi- There is no clear delineation for what is considered an
ties do not, then the static postural control acti vities tasks acute or chronic phase of recovery with TBI. The medical
should be recommended. All subjective symptoms should literature generally categorizes the chronic phase as any-
be considered, including headache, mental “fogginess, ” thing longer than 1 to 3 months. Although metabolic
dizziness, blurred vision, fatigue, or nausea. processes may still be slo wed, the true metabolic crisis
In the acute and subacute stages, function may be that is present post-injury has resolved by approximately
limited secondary to pain from musculosk eletal involve- 3 months.11 The resulting symptoms and functional impair-
ment. Occasionally, back and neck pain are not identified ments may be caused by axonal death, or altered neural
until the patient be gins to move more in therap y. Upper connectivity.
cervical spine instability can be a consequence of head The rehabilitation process continues, again following
injury, so a careful assessment of the cervical spine is im- a problem-oriented approach. The therapist should be
portant.102 If cervical involvement is noted, a cervicogenic aware that individuals with TBI often have problems be-
basis for symptoms may be present. See Chapter 31 for yond those seen in the typical patient with a unilateral or
more information on the management of cervicogenic bilateral vestibular deficit. Migraine headaches are com-
contributions to dizziness. If vestibular exercises are indi- mon, and if present, medical management is important for
cated, they may need to be postponed, or modif ied, until resolution of the headache, which would otherwise inter-
cervical limitations allow freer movement. Smaller ampli- fere with exercise and activity tolerance. If musculoskele-
tude cervical movements that remain within the indi vid- tal injuries exist, especially cervical, one must address
ual’s pain-free range may be performed, which will still them via physical therap y and/or medical management.
allow for appropriate stimulation of the vestibular system. Emotional distress tends to be evident at this point, because
BPPV should be ruled out in all patients following head people experiencing a prolonged recovery may be affected
trauma, because head trauma is a common cause of BPPV.31 by long periods of inacti vity or a lack of producti vity. If
Patients may move slowly and carefully after TBI and may anxiety issues are present, medical or psychological man-
not be aware of their positional symptoms right a way, so agement may be indicated.
therefore may not report dizziness with position changes. Stress management, which is usually situational be-
For individuals with symptoms of dizziness following cause of the recent injury, but can be a result of pre-injury
head trauma, referral for v estibular function testing may factors, can become integral to recovery. Hanna-Plady et al
occur at this time, depending on the practice pattern of the monitored individuals with mild TBI and post-concussive
program. Some facilities will perform vestibular function symptoms exposed to high stress and low stress conditions
3970_Ch26_504-529 25/06/14 12:41 PM Page 516
516 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
as compared with non-injured indi viduals.103 The investi- from blast injury. The subjects underwent physical therapy
gators found increased symptoms, decreased speed of in - utilizing vestibular rehabilitation techniques for gaze stabi-
formation processing, and subtle memory def icits during lization training, balance training, and habituation exercises
the high stress condition that were greater in the individuals for motion sensitivity.14 The investigators documented sig-
with mild TBI as compared with the non-injured individu- nificant improvement in gaze stability, gait, and balance after
als. Although relaxation training and stress-management 12 weeks.
training are not typical functions of the physical therapist, There is only one study thus far that includes subjects
there are resources available that may help patients manage that were not exclusively athletes or the military. Alsalaheen
these issues. A myriad of relaxation training resources are et al reviewed 84 patients in a retrospective study of those
available in podcast and CD formats. Mantra repetition, the referred for vestibular rehabilitation following mTBI.30 The
use of a short w ord or phrase as part of meditation, may patients underwent customized physical therap y interven-
be incorporated into meditation training and then be avail- tions using vestibular rehabilitation techniques, such as eye-
able for use when patients f ind themselves in stressful or head coordination exercises, habituation exercises, static
symptom-producing situations. and dynamic postural control training, and dynamic gait
tasks involving walking with head turns and direction
changes. The patients improved significantly in the areas of
Evidence for Efficacy of Vestibular subjective dizziness, gait, and balance within 5 weeks.
Rehabilitation with TBI There is clearly a need for continued research in the
The literature related to mild TBI has been growing but has area of vestibular rehabilitation for those with traumatic
primarily been focused on sports-related injuries and trauma brain injury. Studies with appropriate control groups are
in the military. There is still much to be learned in the areas needed to determine treatment efficacy. In addition, studies
of diagnostic imaging, etiology of dizziness, measurement related to dosage of the exercises, timing of the exercises,
of recovery, efficacy for medical management, standards of and progression of the rehabilitation program are needed.
medical care, and rehabilitation. The studies re garding
vestibular rehabilitation for individuals with TBI have thus
Coordination of Care and the Team
far been retrospective studies without control groups or
Approach
descriptive studies without control groups.
In two studies that focus on service members in the mil- Given the diverse nature of impairments that can occur
itary with mild TBI, Hoffer et al characterized patients by with TBI, a multidisciplinary team approach that addresses
the etiology of their dizziness and then monitored their re- all aspects of reco very is an important aspect in the care
covery following vestibular rehabilitation.13,104 In the first and rehabilitation of the individual with a TBI. In a multi-
study, 58 military members post-injury were cate gorized disciplinary team, neurologists and physiatrists may work
by the etiology of their dizziness into three cate gories: to control headaches and manage pain and orthopedic co-
BPPV, migraine-related dizziness, and spatial disorientation. morbidities, and psychiatrists can manage preexisting men-
Twenty-eight percent of the indi viduals had BPPV, which tal health needs or developing anxiety. Neuropsychologists
was cleared in 1 week via canalith repositioning maneuvers, may monitor and address cognitive deficits, and counseling
with resulting resolution of their symptoms. Forty-one per- psychologists can work with patients on anxiety manage-
cent of the individuals were categorized as having migraine- ment, relaxation training, and issues related to adjustment.
related dizziness, and 19% of the individuals were diagnosed Occupational therapists and speech therapists may w ork
with spatial disorientation. These two groups underwent on executive level skills and address cogniti ve and com-
physical therapy with a customized interv ention program munication deficits. Physical therapists address the dizzi-
using vestibular rehabilitation techniques. The migraine- ness, balance, e xertion, and orthopedic components of
related dizziness group had resolution of symptoms within rehabilitation. Case managers assist in bringing team mem-
8 weeks. The spatial disorientation group required up to bers together for regular collaboration or conferences, and
39 weeks for resolution of symptoms. In this study , 9% of also act as liaison for external case management, employ-
subjects could not be classified. In the second study, a fourth ers, team trainers, teachers, and school officials.
etiological category was identified: exercise-induced dizzi- With the increased incidence of TBI among service
ness, which accounted for 7% of the indi viduals.104 This personnel as a result of recent armed conflicts, the military
group was also treated with customized physical therap y has developed an integrated, multidisciplinary team ap-
interventions and required approximately 4 weeks for reso- proach that may serve as a model for comprehensive care.
lution of symptoms. In a prospecti ve study, Gottshall and Patients presenting to a military vestibular clinic with mTBI
Hoffer studied soldiers returning from combat with mildTBI and symptoms of dizziness undergo a detailed history and
3970_Ch26_504-529 25/06/14 12:41 PM Page 517
Chapter 26 • PHYSICAL THERAPY MANAGEMENT OF THE PATIENT WITH VESTIBULAR DYSFUNCTION 517
standardized physical examination by a team composed of that was associated with a protracted recovery, which was de-
a neurotologist and a physical therapist. In addition to the fined as greater than 20 days.107 Ten to fifteen percent of those
physical examination, the patients undergo complete audi- diagnosed with concussion will ha ve a prolonged recovery
tory and vestibular test batteries, including rotational chair (greater than 7 days).108,109 Several factors have been associ-
testing, VNG test battery including caloric e xamination, ated with longer recovery times and greater impairments:
vestibular-evoked myogenic potentials (VEMP), an audio-
• Age: Adolescents require more time and rehabili-
gram, and electrocochleography (ECOG). MRI is obtained
tation services following mild TBI.23,110,111
as indicated by the patient’s physical examination and test
• Amnesia: There is some evidence to suggest that
results. Military centers have instituted a program called the
loss of consciousness is not a predictor for recov-
POWER: Program Of Wellness Education and Recovery.
ery.112 However, amnesia (retrograde or antero-
The program uses medical pro viders from physiatry, neu-
grade) on the sideline is a predictor for longer
ropsychology, primary care, physical therapy, occupational
recovery and presence of neurocognitive deficits.112
therapy, speech therapy, mental health, and case manage-
• Exertion: High levels of exertion or activity level
ment. There are many program goals, but through organized
post-injury is associated with greater impairment
and coordinated services as well as structured programs, the
in neurocognitive scores and greater symptoms
overriding goal for the program is to focus on wellness and
1 month post-concussion.100
education with a positive expectation for recovery and re-
• Headaches: Athletes with post-concussion
turn to duty. As part of the educational program, theVestibu-
headaches or migraines have higher rates of am-
lar Balance Awareness and Safety Course includes an
nesia, lower neurocognitive scores, and higher
overview of vestibular anatomy and function, factors con-
reported symptoms.38,113
tributing to balance, strategies for decreasing dizziness and
• Symptoms: Individuals with symptoms of “foggi-
unsteadiness, how drugs affect motion sickness, and ho w
ness” following a concussion have higher scores
alcohol affects vertigo. The physical program includes ex-
for other symptoms and lower scores on neu-
ercises specific to the individual’s impairments and strate-
rocognitive testing.114
gies for relaxation, acti vities to increase endurance and
• History: Amateur athletes with multiple concus-
decrease fatigue, exercises and activities to promote core
sions (3 or more) have greater baseline symp-
strengthening, overall strength and flexibility, and agility.
toms, have increased chance of a significant drop
in memory performance with subsequent concus-
sions, are more likely to sustain another concus-
Prognosis: Factors That Contribute sion, and have prolonged recovery times.115,116
to Outcome • Gender: Female athletes report more post-
According to several studies of sports concussion, mTBI concussive symptoms compared with males and
resolves in most cases within 2 weeks. 23,105,106 Dizziness demonstrate more impairment on computerized
at the time of injury was the sole on-field sign or symptom neurocognitive testing.117,118
Continued
3970_Ch26_504-529 25/06/14 12:41 PM Page 518
518 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
creased gains with rotation to the left. Subjective Visual looking at a fixed object in front of him on the
Vertical (SVV) testing w as abnormal, consistent with wall. The patient’s task was to maintain focus on
left utricular dysfunction. the object while doing a push-up against the wall.
The patient completed the Dizziness Handicap Inven- ■ Active slow convergence: The patient started
tory (DHI) and Activity-specific Balance Confidence looking at the tip of his finger held at arm’s
Scale (ABC). Computerized dynamic posturography length. He slowly brought the finger closer to
was performed, including the Sensory Organization Test his nose, trying to keep it in focus. This was
(SOT), the SOT Head Shake Test, Motor Control Test practiced for 1 minute, first in sitting and then
(MCT), and Adaptation Test. The Functional Gait As- progressed to a standing position.
sessment (FGA) and High-level Mobility Assessment ■ Active fast convergence: looking from far to
Tool (HiMAT) were performed as clinical measures of near targets of varying sizes
dynamic balance. Functional assessment of theVOR was ■ Brock string exercises
performed using the Dynamic Visual Acuity Test (DVA) To improve standing balance:
and Gaze Stabilization Test (GST). ■ Standing balance exercises with arms crossed, eyes
The patient’s test results indicated abnormalities in closed, and a decreasing base of support. Performed
VOR function, deficits in somatosensory integration, initially with head level and then with head tilted back.
impaired gait, and motion sensitivity. ■ Standing balance exercises with arms crossed,
Chapter 26 • PHYSICAL THERAPY MANAGEMENT OF THE PATIENT WITH VESTIBULAR DYSFUNCTION 519
■ Turning corners and pivot turns while walking ary bike, and was then progressed to an elliptical ma-
■ Skipping, hopping, lunging chine, and finally to swimming, with steadily
■ Stair ascent and descent increasing demands. Progression from one activity
To decrease motion sensitivity: was based on the patient’s ability to perform the activ-
ity without provocation of dizziness.
■ Visual tracking: To decrease visual motion sen-
■ Job specific activities: Given the patient’s job re-
sitivity, the patient held a visual target at arm’s
quirements, the swimming exercises progressed
length, and then moved the target side to side,
from distance swims to sprints with flip turns in
up and down, and in diagonal directions, track-
daylight and in dark. In addition, the patient at-
ing the object with his eyes and keeping his
tended surf clinic and used the surf kayak, stand-
head still. This exercise was performed initially
up paddle board, and surfboard.
in sitting, but progressed to standing, and then to
walking. The patient w as also follo wed by audiology ,
■ Rapid, large-amplitude head movements: To de- where he was fit with hearing aids and was taught tin-
crease the symptoms of dizziness that occurred nitus adaptation strategies.
with head movements and position changes, the
patient performed the following movements: sit Outcomes
to supine; sit to bending forward, sit to stand After 9 weeks of vestibular physical therapy, the patient
with head turn, standing full body diagonals, had met his short-term goal, and had partially met his
and standing pivot turns. long-term goal. Table 26-2 summarizes the changes in
Continued
3970_Ch26_504-529 25/06/14 12:42 PM Page 520
520 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Chapter 26 • PHYSICAL THERAPY MANAGEMENT OF THE PATIENT WITH VESTIBULAR DYSFUNCTION 521
results were as follows: ENG test battery re vealed a ■ Able to tolerate 60 seconds of gaze stabilization
38% asymmetry to caloric testing with decreased re- task with dizziness rated as less than 4/10
sponses in the right ear, persistent direction changing, ■ Able to exercise on stationary bike for 15 minutes
gaze-evoked nystagmus; rotary chair testing re vealed at a level of intensity 80% of the symptom thresh-
low VOR gain for rotations to the right and a right di- old level
rectional preponderance. LONG-TERM GOALS (12 WEEKS)
■ FGA improved to 30/30
Plan of Care ■ A 2-line or less difference between static and
The patient verbalized the following goals: resolution dynamic visual acuity in the clinical DVA test
of dizziness and unsteadiness, return to e xercise, be ■ HiMAT score greater than 46
able to participate in daughter’ s sports activities, and ■ Able to exercise via jogging for 30 minutes
return to full-duty police officer. The following short- without an increase in dizziness or headache
and long-term goals were set: ■ Able to tolerate 30 minutes of complex visual
SHORT-TERM GOALS (4 WEEKS) environments that include noise and visual mo-
■ FGA improved to 27/30 tion without increase in dizziness and headache
■ Static standing eyes closed in semi-tandem for ■ Return to all work duties
30 seconds
Continued
3970_Ch26_504-529 25/06/14 12:42 PM Page 522
522 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
ical therapy twice a week for 3 weeks, once a week for sual motion exercises at 4 weeks. The initial exer-
5 weeks, then once every 2 weeks for 4 weeks. Ther- cises consisted of watching videos taken while
apy sessions were 1 hour in duration. The patient was individuals walked through busy urban environ-
retested at 4 weeks, 8 weeks, and 12 weeks.The patient ments. Initial exposure time was 5 minutes, which
cancelled two appointments because of migraine; was progressed to 15 minutes. When the patient
the sessions were rescheduled within the week. He could tolerate this visual motion exposure, he
attended 13 sessions total. started graded exposure to community environ-
A portion of the first four visits was devoted to patient ments including the grocery store, observing
education regarding migraine management, rationale for daughter’s lacrosse practice, watching his daugh-
vestibular rehabilitation, pacing, and reinforcement of ter’s game, and then busy restaurants.
previously recommended relaxation techniques. All the ■ Head motion exercises: The habituation exer-
information was also provided in the form of written cises consisted of progressively more complex
handouts. and challenging movements—gait with head
A 10-point symptom scale to assess dizziness and turns and whole body turns, combined eye and
headache was used at the be ginning and end of each head tracking in standing then while walking,
session. The scale was used periodically during the ball toss in standing and then while walking. As
session to monitor the patient’s tolerance of symptom- the patient progressed, repetitive motion tasks
exacerbating tasks. The specific physical therapy in- using high and low surfaces, agility drills, and
terventions are listed below. rapid random direction changes were added to
To improve convergence: walking activities.
■ Brock string exercises To decrease e xertion-induced symptoms and im-
■ Pencil push-ups prove aerobic conditioning:
■ Note: Near point of convergence resolved to ■ Stationary bicycle: 10 minutes duration. The dura-
10 cm without symptoms within 2 weeks. tion was increased when the patient had dizziness
The patient still reported dizziness with com- rated as no more than a 3/10 that lasted for less
puter scrolling but found that reading on the than 10 minutes after completion of the stationary
paper or phone had improved. Based on the bicycle exercise.
normal performance on convergence, no further ■ Jogging on a treadmill: This was progressed by
referral was recommended for this condition. increasing the speed and duration of the exer-
To improve gaze stability during head movements: cise, using the same guidelines as described for
the stationary bicycle exercise. Jogging outside:
■ X1 and X2 viewing exercises: The gaze stability
Once patient was able to jog 15 minutes on
exercises were started in standing with feet apart.
treadmill with good tolerance, he began to jog
As the patient progressed, the exercises were per-
outside.
formed with a narrow base of support and then
■ High-level agility tasks were added for the last
while walking. Increasing the velocity of the head
6 weeks, including hopping, jumping, obstacle
movement, the use of busy backgrounds, and per-
climbing (low wall), and carrying up to 50 lb.
forming the exercises in complex visual and audi-
■ NOTE: Patient was instructed to avoid these
tory environments were added to the exercise
exercises if he was experiencing a migraine.
program as tolerated.
To improve standing balance: Outcomes
■ Standing balance exercises with eyes closed on
During the course of recovery, patient’s headaches re-
firm and compliant surfaces: Decreasing the base solved gradually with 1 to 2 headaches per month by
of support, weight shifting with eyes closed, the discharge, which he was able to control with Zolmitrip-
use of a rocker board and bosu ball were used as tan. He reported significant irritability, lack of patience
exercise progressions.
3970_Ch26_504-529 25/06/14 12:43 PM Page 523
Chapter 26 • PHYSICAL THERAPY MANAGEMENT OF THE PATIENT WITH VESTIBULAR DYSFUNCTION 523
Continued
3970_Ch26_504-529 25/06/14 12:43 PM Page 524
524 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
bilization exercise with busy background with firm and compliant surfaces: Decreasing the base
provoked symptoms of dizziness less than 4/10 of support and weight shifting with eyes closed
■ Able to tolerate 10 minutes of watching an were used as exercise progressions.
urban walking video with provoked dizziness To decrease motion sensitivity:
less than 4/10 ■ Visual motion exercises: The initial exercises
■ Able to exercise on stationary bike for 15 minutes consisted of watching videos taken while individ-
at a level of intensity 80% of the symptom thresh- uals walked through busy urban environments.
old level Initial exposure time was 5 minutes, which was
LONG-TERM GOALS (4 WEEKS) progressed to 15 minutes. When the patient could
■ FGA improved to 30/30 tolerate this visual motion exposure, she started
■ A 2-line or less difference between static and graded exposure to community environments in-
dynamic visual acuity on the clinical DVA test cluding walking through the grocery store, at-
■ HiMAT score greater than 52 tending a basketball game, and then using the
■ Able to exercise via jogging for 30 minutes subway.
without an increase in dizziness ■ Head motion exercises: The habituation exer-
■ Able to tolerate 30 minutes of complex visual cises consisted of progressively more complex
environments that include noise and visual and challenging movements—gait with head
motion without an increase in dizziness turns and whole body turns, combined eye and
■ Return to training with team, progression head tracking in standing then while walking,
toward return to play ball toss in standing and then while walking. As
the patient progressed, repetitive motion tasks
Intervention using high and low surfaces, agility drills, and
The patient was scheduled to receive vestibular phys- rapid random direction changes were added to
ical therapy twice a week for 4 weeks. Therapy ses- walking activities. Finally, she began sport-
sions were 1 hour in duration. She attended se ven specific training that included tossing a basket-
sessions total. ball with rapid turns, hopping, and jumping.
Initial visits included patient education re garding To decrease e xertion-induced symptoms and im-
the rationale for v estibular rehabilitation and pacing prove aerobic conditioning:
recommendations to avoid excessive exertion. The pa- ■ Stationary bicycle: 10 minutes duration. The dura-
tient began a general stretching and 20-minute daily tion was increased when the patient had dizziness
walking program. All information and instructions rated as no more than a 3/10 that lasted for less
were also provided as written handouts. than 10 minutes after completion of the stationary
A 10-point symptom scale to assess dizziness w as bicycle exercise.
used at the be ginning and end of each session. The ■ Jogging on a treadmill: This was added after
scale was used periodically during the session to mon- 2 weeks of using the stationary bicycle, and was
itor her tolerance to symptom-exacerbating tasks. The progressed by increasing the speed and duration
specific physical therapy interventions are listed below. of the exercise, using the same guidelines as de-
To improve gaze stability during head movements: scribed for the stationary bicycle exercise.
■ X1 and X2 viewing exercises: The gaze stability ex- ■ Jogging outside: Once patient was able to jog
ercises were started in standing with feet apart. As 15 minutes on treadmill with good tolerance,
the patient progressed, the exercises were performed she began to jog outside.
3970_Ch26_504-529 25/06/14 12:43 PM Page 525
Chapter 26 • PHYSICAL THERAPY MANAGEMENT OF THE PATIENT WITH VESTIBULAR DYSFUNCTION 525
Dizziness Severity (0–10) 0 to 5/10 (frequently with typical tasks) 0 to 3/10 (occasionally with rapid
movements)
526 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
6. Moore EL, Terryberry-Spohr L, Hope DA. Mild traumatic 24. Herdman SJ. Treatment of vestibular disorders in traumati-
brain injury and anxiety sequelae: a review of the literature. cally brain-injured patients. Journal of Head Trauma
Brain Inj. 2006;20(2):117-132. Rehabilitation. 1990;5(4):63-76.
7. Byard RW, Vink R. The second impact syndrome. 25. Furman JM Whitney SL. Central causes of dizziness.
Forensic science, medicine, and pathology. Sci Med Physical therapy. 2000;80(2):179-187.
Pathol. 2009;5(1):36-38. 26. Scherer MR, Shelhamer MJ, Schubert MC. Characterizing
8. Cantu RC, Gean AD. Second-impact syndrome and a high-velocity angular vestibulo-ocular reflex function in
small subdural hematoma: an uncommon catastrophic service members post-blast exposure. Experimental Brain
result of repetitive head injury with a characteristic Research. 2011;208(3):399-410.
imaging appearance. Journal of Neurotrauma. 27. Malmstrom EM, Karlberg M, Melander A, Magnusson
2010;27(9):1557-1564. M, Moritz U. Cervicogenic dizziness–musculoskeletal
9. Wetjen NM, Pichelmann MA, Atkinson JL. Second impact findings before and after treatment and long-term
syndrome: concussion and second injury brain complica- outcome. Disability and Rehabilitation. 2007;29(15):
tions. Journal of the American College of Surgeons. 1193-1205.
2010;211(4):553-557. 28. Wrisley DM, Sparto PJ, Whitney SL, Furman JM.
10. McCrory P, Davis G, Makdissi M. Second impact syn- Cervicogenic dizziness: a review of diagnosis
drome or cerebral swelling after sporting head injury. and treatment. J Orthop Sports Phys Ther. 2000;30(12):
Current Sports Medicine Reports. 2012;11(1):21-23. 755-766.
11. Giza CC, Hovda DA. The Neurometabolic Cascade 29. Karlberg M, Johansson R, Magnusson M, Fransson PA.
of Concussion. J Athl Train. 2001;36(3):228-235. Dizziness of suspected cervical origin distinguished by
12. Giza CC, Difiori JP. Pathophysiology of sports-related posturographic assessment of human postural dynamics.
concussion: an update on basic science and translational J Vestib Res. 1996;6(1):37-47.
research. Sports Health. 2011;3(1):46-51. 30. Alsalaheen BA, Mucha A, Morris LO, Whitney SL,
13. Hoffer ME, Balaban C, Gottshall K, Balough BJ, Furman JM, Camiolo-Reddy CE, et al. Vestibular rehabili-
Maddox MR, Penta JR. Blast exposure: vestibular conse- tation for dizziness and balance disorders after concussion.
quences and associated characteristics. Otol Neurotol. J Neurol Phys Ther. 2010;34(2):87-93.
2010;31(2):232-236. 31. Katsarkas A. Benign paroxysmal positional vertigo
14. Gottshall KR, Hoffer ME. Tracking recovery of vestibular (BPPV): idiopathic versus post-traumatic. Acta Oto-
function in individuals with blast-induced head trauma laryngol. 1999;119(7):745-749.
using vestibular-visual-cognitive interaction tests. J Neurol 32. Masson F, Maurette P, Salmi LR, Dartigues JF, Vecsey J,
Phys Ther. 2010;34(2):94-97. Destaillats JM, et al. Prevalence of impairments 5 years
15. Hoffer ME, Gottshall KR, Moore R, Balough BJ, Wester after a head injury, and their relationship with disabilities
D. Characterizing and treating dizziness after mild head and outcome. Brain Inj. 1996;10(7):487-497.
trauma. Otol Neurotol. 2004;25(2):135-138. 33. Hoge CW, McGurk D, Thomas JL, Cox AL, Engel
16. Scherer MR, Schubert MC. Traumatic brain injury and CC, Castro CA. Mild traumatic brain injury in
vestibular pathology as a comorbidity after blast exposure. U.S. Soldiers returning from Iraq. N Engl J Med.
Physical Therapy. 2009;89(9):980-992. 2008;358(5):453-463.
17. Shupak A, Doweck I, Nachtigal D, Spitzer O, Gordon CR. 34. Balaban CD. Neural substrates linking balance control and
Vestibular and audiometric consequences of blast injury to anxiety. Physiol Behav. 2002;77(4-5):469-475.
the ear. Arch Otolaryngol Head Neck Surg. 1993;119(12): 35. Balaban C, Jacob, R. Background and history of the inter-
1362-1367. face between anxiety and vertigo. Journal of Anxiety
18. McCrory P, et al. Consensus statement on concussion Disorders. 2001;15:27-51.
in sport: the 4th International Conference on Concus- 36. Balaban CD, Jacob RG, Furman JM. Neurologic bases for
sion in Sport held in Zurich, November 2012, published comorbidity of balance disorders, anxiety disorders and
2013. migraine: neurotherapeutic implications. Expert Review
19. Kisilevski V, Podoshin L, Ben-David J, Soustiel JF, of Neurotherapeutics. 2011;11(3):379-394.
Teszler CB, Hafner H, et al. Results of otovestibular tests 37. Furman JM, Balaban CD, Jacob RG, Marcus DA. Migraine-
in mild head injuries. The International Tinnitus Journal. anxiety related dizziness (MARD): a new disorder? J Neurol
2001;7(2):118-121. Neurosurg Psychiatry. 2005;76(1):1-8.
20. Maskell F, Chiarelli P, Isles R. Dizziness after traumatic 38. Mihalik JP, Stump JE, Collins MW, Lovell MR, Field M,
brain injury: overview and measurement in the clinical Maroon JC. Posttraumatic migraine characteristics in
setting. Brain Inj. 2006;20(3):293-305. athletes following sports-related concussion. J Neurosurg.
21. Maskell F, Chiarelli P, Isles R. Dizziness after traumatic 2005;102(5):850-855.
brain injury: results from an interview study. Brain Inj. 39. Leddy JJ, Kozlowski K, Donnelly JP, Pendergast DR,
2007;21(7):741-752. Epstein LH, Willer B. A preliminary study of subsymptom
22. Terrio H, Brenner LA, Ivins BJ, Cho JM, Helmick K, threshold exercise training for refractory post-concussion
Schwab K, et al. Traumatic brain injury screening: syndrome. Clin J Sport Med. 2010;20(1):21-27.
preliminary findings in a US Army Brigade Combat 40. Guskiewicz KM. Assessment of postural stability follow-
Team. The Journal of Head Trauma Rehabilitation. ing sport-related concussion. Current Sports Medicine
2009;24(1):14-23. Reports. 2003;2(1):24-30.
23. Lovell M, Collins M, Bradley J. Return to play 41. Guskiewicz KM. Balance assessment in the manage-
following sports-related concussion. Clin Sports Med. ment of sport-related concussion. Clin Sports Med.
2004;23(3):421-441, ix. 2011;30(1):89-102,ix.
3970_Ch26_504-529 25/06/14 12:43 PM Page 527
Chapter 26 • PHYSICAL THERAPY MANAGEMENT OF THE PATIENT WITH VESTIBULAR DYSFUNCTION 527
42. Lau B, Lovell MR, Collins MW, Pardini J. Neurocognitive data for the post-concussion scale. Applied Neuropsychol-
and symptom predictors of recovery in high school ath- ogy. 2006;13(3):166-174.
letes. Clin J Sport Med. 2009;19(3):216-221. 59. Catena RD, van Donkelaar P, Chou LS. Altered balance
43. Leddy JJ, Kozlowski K, Fung M, Pendergast DR, Willer B. control following concussion is better detected with an at-
Regulatory and autoregulatory physiological dysfunction tention test during gait. Gait Posture. 2007;25(3):406-411.
as a primary characteristic of post concussion syndrome: 60. Catena RD, van Donkelaar P, Chou LS. Cognitive task ef-
implications for treatment. NeuroRehabilitation. fects on gait stability following concussion. Experimental
2007;22(3):199-205. Brain Research. 2007;176(1):23-31.
44. Alhola P, Polo-Kantola P. Sleep deprivation: impact on 61. Catena RD, van Donkelaar P, Halterman CI, Chou LS.
cognitive performance. Neuropsychiatric Disease and Spatial orientation of attention and obstacle avoidance
Treatment. 2007;3(5):553-567. following concussion. Experimental Brain Research.
45. Zeman J, Cassano M, Perry-Parrish C, Stegall S. Emotion 2009;194(1):67-77.
regulation in children and adolescents. J Dev Behav 62. Jacobson GP Newman CW. The development of the Dizzi-
Pediatr. 2006;27(2):155-168. ness Handicap Inventory. Arch Otolaryngol Head Neck
46. Jacob RG, Furman JM. Psychiatric consequences Surg. 1990;116(4):424-427.
of vestibular dysfunction. Curr Opin Neurol. 2001;14(1): 63. Powell L, Myers A. The Activities-Specific Balance
41-46. Confidence Scale. Journal of Gerontology. 1995;50A(1):
47. Abu-Judeh HH, Parker R, Aleksic S, Singh ML, Naddaf S, M28-M34.
Atay S, et al. SPECT brain perfusion findings in mild 64. King NS, Crawford S, Wenden FJ, Moss NE, Wade DT.
or moderate traumatic brain injury. Nuclear Medicine The Rivermead Post Concussion Symptoms Question-
Review. 2000;3(1):5-11. naire: a measure of symptoms commonly experienced
48. Chen SH, Kareken DA, Fastenau PS, Trexler LE, Hutchins after head injury and its reliability. J Neurol. 1995;242(9):
GD. A study of persistent post-concussion symptoms in 587-592.
mild head trauma using positron emission tomography. 65. Randolph C, Millis S, Barr WB, McCrea M, Guskiewicz
J Neurol Neurosurg Psychiatry. 2003;74(3):326-332. KM, Hammeke TA, et al. Concussion symptom inventory:
49. McAllister TW, Saykin AJ, Flashman LA, Sparling MB, an empirically derived scale for monitoring resolution of
Johnson SC, Guerin SJ, et al. Brain activation during work- symptoms following sport-related concussion. Arch Clin
ing memory 1 month after mild traumatic brain injury, a Neuropsychol. 2009;24(3):219-229.
functional MRI study. Neurology. 1999;53:1300-1308. 66. Williamson IJ, Goodman D. Converging evidence for
50. Lovell MR, Pardini JE, Welling J, Collins MW, Bakal J, the under-reporting of concussions in youth ice
Lazar N, et al. Functional brain abnormalities are related hockey. British Journal of Sports Medicine.
to clinical recovery and time to return-to-play in athletes. 2006;40(2):128-132;discussion 128-132.
Neurosurgery. 2007;61(2):352-359;discussion 9-60. 67. McCrea M, Hammeke T, Olsen G, Leo P, Guskiewicz K.
51. Vagnozzi R, Signoretti S, Tavazzi B, Floris R, Ludovici A, Unreported concussion in high school football players:
Marziali S, et al. Temporal window of metabolic brain implications for prevention. Clin J Sport Med. 2004;14(1):
vulnerability to concussion: a pilot 1H-magnetic reso- 13-17.
nance spectroscopic study in concussed athletes—part III. 68. Guskiewicz KM, Bruce SL, Cantu RC, Ferrara MS, Kelly
Neurosurgery. 2008;62(6):1286-1295;discussion 95-96. JP, McCrea M, et al. National Athletic Trainers’ Associa-
52. Vagnozzi R, Signoretti S, Cristofori L, Alessandrini F, tion Position Statement: Management of Sport-Related
Floris R, Isgro E, et al. Assessment of metabolic brain dam- Concussion. J Athl Train. 2004;39(3):280-297.
age and recovery following mild traumatic brain injury: a 69. Grossman I, Kaufman AS, Mednitsky S, Scharff L, Dennis
multicentre, proton magnetic resonance spectroscopic study B. Neurocognitive abilities for a clinically depressed sam-
in concussed patients. Brain. 2010;133(11):3232-3242. ple versus a matched control group of normal individuals.
53. Mayer AR, Ling J, Mannell MV, Gasparovic C, Phillips Psychiatry Research. 1994;51(3):231-244.
JP, Doezema D, et al. A prospective diffusion tensor 70. Rohling ML, Green P, Allen LM, 3rd, Iverson GL.
imaging study in mild traumatic brain injury. Neurology. Depressive symptoms and neurocognitive test scores in
2010;74(8):643-650. patients passing symptom validity tests. Arch Clin
54. McCrea M. Standardized mental status assessment of Neuropsychol. 2002;17(3):205-222.
sports concussion. Clin J Sport Med. 2001;11(3):176-181. 71. Austin MP, Mitchell P, Goodwin GM. Cognitive deficits in
55. Maddocks DL, Dicker GD, Saling MM. The assessment of depression: possible implications for functional neu-
orientation following concussion in athletes. Clin J Sport ropathology. Br J Psychiatry. 2001;178:200-206.
Med. 1995;5(1):32-35. 72. Iezzi T, Archibald Y, Barnett P, Klinck A, Duckworth M.
56. McCrea M, Kelly JP, Randolph C, Kluge J, Bartolic E, Neurocognitive performance and emotional status in
Finn G, et al. Standardized assessment of concussion chronic pain patients. Journal of Behavioral Medicine.
(SAC): on-site mental status evaluation of the athlete. The 1999;22(3):205-216.
Journal of Head Trauma Rehabilitation. 1998;13(2):27-35. 73. Schatz P, Pardini JE, Lovell MR, Collins MW, Podell K.
57. Guskiewicz KM, Register-Mihalik J, McCrory P, et al. Sensitivity and specificity of the ImPACT Test Battery for
Evidence-based approach to revising the SCAT2: intro- concussion in athletes. Arch Clin Neuropsychol.
ducing the SCAT3. British Journal of Sports Medicine. 2006;21(1):91-99.
2013;47(5):289-293. 74. Covassin T, Elbin RJ, 3rd, Stiller-Ostrowski JL, Kontos
58. Lovell MR, Iverson GL, Collins MW, Podell K, Johnston AP. Immediate post-concussion assessment and cognitive
KM, Pardini D, et al. Measurement of symptoms follow- testing (ImPACT) practices of sports medicine profession-
ing sports-related concussion: reliability and normative als. J Athl Train. 2009;44(6):639-644.
3970_Ch26_504-529 25/06/14 12:43 PM Page 528
528 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
75. Morris AE, Lutman ME, Yardley L. Measuring outcome 92. Adler P. Efficacy of treatment for convergence insuffi-
from vestibular rehabilitation, part II: refinement and vali- ciency using vision therapy. Ophthalmic Physiol Opt.
dation of a new self-report measure. International Journal 2002;22(6):565-571.
of Audiology. 2009;48(1):24-37. 93. Jainta S, Bucci MP, Wiener-Vacher S, Kapoula Z.
76. Cohen HS Kimball KT, Adams AS. Application of the Changes in vergence dynamics due to repetition. Vision
vestibular disorders activities of daily living scale. Research. 2011;51(16):1845-1852.
Laryngoscope. 2000;110(7):1204-1209. 94. Dagi LR, Chrousos GA, Cogan DC. Spasm of the near
77. Guerraz M, Yardley L, Bertholon P, Pollak L, Rudge P, reflex associated with organic disease. American Journal
Gresty MA, et al. Visual vertigo: symptom assessment, of Ophthalmology. 1987;103(4):582-585.
spatial orientation and postural control. Brain. 2001; 95. Chan RV, Trobe JD. Spasm of accommodation associated
124(Pt 8):1646-1656. with closed head trauma. J Neuroophthalmol. 2002;
78. Dannenbaum E, Chilingaryan G, Fung J. Visual vertigo 22(1):15-17.
analogue scale: an assessment questionnaire for visual 96. Knapp C, Sachdev A, Gottlob I. Spasm of the near reflex
vertigo. J Vestib Res. 2011;21(3):153-159. associated with head injury. Strabismus. 2002;10(1):1-4.
79. Pickett TC, Radfar-Baublitz LS, McDonald SD, Walker 97. Kaczmarek BB, Dawson E, Lee JP. Convergence
WC, Cifu DX. Objectively assessing balance deficits after spasm treated with botulinum toxin. Strabismus.
TBI: Role of computerized posturography. J Rehabil Res 2009;17(1):49-51.
Dev. 2007;44(7):983-990. 98. Pavlou M. The use of optokinetic stimulation in
80. Guskiewicz KM. Postural stability assessment following vestibular rehabilitation. J Neurol Phys Ther. 2010;
concussion: one piece of the puzzle. Clin J Sport Med. 34(2):105-110.
2001;11(3):182-189. 99. Baker JG, Freitas MS, Leddy JJ, Kozlowski KF, Willer BS.
81. Wrisley DM, Marchetti GF, Kuharsky DK, Whitney SL. Return to full functioning after graded exercise assess-
Reliability, internal consistency, and validity of data ment and progressive exercise treatment of postconcus-
obtained with the functional gait assessment. Physical sion syndrome. Rehabilitation Research and Practice.
Therapy. 2004;84(10):906-918. 2012;2012:705309.
82. Wrisley DM, Kumar NA. Functional gait assessment: 100. Majerske CW, Mihalik JP, Ren D, Collins MW, Reddy
concurrent, discriminative, and predictive validity in CC, Lovell MR, et al. Concussion in sports: postconcus-
community-dwelling older adults. Physical Therapy. sive activity levels, symptoms, and neurocognitive
2010;90(5):761-773. performance. J Athl Train. 2008;43(3):265-274.
83. Franchignoni F, Horak F, Godi M, Nardone A, Giordano A. 101. Ponsford J, Willmott C, Rothwell A, Cameron P, Kelly
Using psychometric techniques to improve the Balance AM, Nelms R, et al. Impact of early intervention on
Evaluation Systems Test: the mini-BESTest. J Rehabil outcome following mild head injury in adults. J Neurol
Med. 2010;42(4):323-331. Neurosurg Psychiatry. 2002;73(3):330-332.
84. Riemann BL, Guskiewicz KM. Effects of mild head injury 102. Mathers KS, Schneider M, Timko M. Occult hypermobil-
on postural stability as measured through clinical balance ity of the craniocervical junction: a case report and re-
testing. J Athl Train 2000;35(1):19-25. view. J Orthop Sports Phys Ther. 2011;41(6):444-457.
85. Williams GP, Greenwood KM, Robertson VJ, Goldie PA, 103. Hanna-Pladdy B, Berry ZM, Bennett T, Phillips HL,
Morris ME. High-Level Mobility Assessment Tool Gouvier WD. Stress as a diagnostic challenge for post-
(HiMAT): interrater reliability, retest reliability, and inter- concussive symptoms: sequelae of mild traumatic brain
nal consistency. Physical Therapy. 2006;86(3):395-400. injury or physiological stress response. Clin Neuropsy-
86. Williams G, Robertson V, Greenwood K, Goldie P, Morris chol. 2001;15(3):289-304.
ME. The concurrent validity and responsiveness of the 104. Hoffer ME, Balough BJ, Gottshall KR. Posttraumatic
high-level mobility assessment tool for measuring the balance disorders. The International Tinnitus Journal.
mobility limitations of people with traumatic brain injury. 2007;13(1):69-72.
Arch Phys Med Rehabil. 2006;87(3):437-442. 105. McCrea M, Barr WB, Guskiewicz K, Randolph C,
87. Herdman SJ, Tusa RJ, Blatt P, Suzuki A, Venuto PJ, Marshall SW, Cantu R, et al. Standard regression-based
Roberts D. Computerized dynamic visual acuity test in methods for measuring recovery after sport-related con-
the assessment of vestibular deficits. Am J Otol. cussion. J Int Neuropsychol Soc. 2005;11(1):58-69.
1998;19(6):790-796. 106. Pellman EJ, Viano DC, Casson IR, Arfken C, Powell J.
88. Heitger MH, Jones RD, Macleod AD, Snell DL, Frampton Concussion in professional football: injuries involving
CM, Anderson TJ. Impaired eye movements in post- 7 or more days out—Part 5. Neurosurgery. 2004;55(5):
concussion syndrome indicate suboptimal brain function 1100-1119.
beyond the influence of depression, malingering or 107. Lau BC, Kontos AP, Collins MW, Mucha A, Lovell MR.
intellectual ability. Brain. 2009;132(10):2850-2870. Which on-field signs/symptoms predict protracted recov-
89. Ciuffreda KJ, Han Y, Kapoor N, Ficarra AP. Oculomotor ery from sport-related concussion among high school
rehabilitation for reading in acquired brain injury. football players? The American Journal of Sports
NeuroRehabilitation. 2006;21(1):9-21. Medicine. 2011;39(11):2311-2318.
90. Kapoor N, Ciuffreda KJ. Vision Disturbances Following 108. McCrea M, Guskiewicz K, Randolph C, et al. Inci-
Traumatic Brain Injury. Current Treatment Options in dence, clinical course, and predictors of prolonged re-
Neurology. 2002;4(4):271-280. covery time following sport-related concussion in high
91. Lepore FE. Disorders of ocular motility following head school and college athletes. J Int Neuropsychol Soc.
trauma. Arch Neurol. 1995;52(9):924-926. 2013;19(1):22-33.
3970_Ch26_504-529 25/06/14 12:43 PM Page 529
Chapter 26 • PHYSICAL THERAPY MANAGEMENT OF THE PATIENT WITH VESTIBULAR DYSFUNCTION 529
109. Makdissi M, Cantu RC, Johnston KM, McCrory P, in high school athletes. The American Journal of Sports
Meeuwisse WH. The difficult concussion patient: Medicine. 2003;31(2):168-173.
what is the best approach to investigation and 114. Iverson GL, Gaetz M, Lovell MR, Collins MW. Relation
management of persistent (>10 days) postconcussive between subjective fogginess and neuropsychological
symptoms? British Journal of Sports Medicine. testing following concussion. J Int Neuropsychol Soc.
2013;47(5):308-313. 2004;10(6):904-906.
110. Iverson GL, Brooks BL, Collins MW, Lovell MR. Track- 115. Iverson GL, Gaetz M, Lovell MR, Collins MW. Cumula-
ing neuropsychological recovery following concussion in tive effects of concussion in amateur athletes. Brain Inj.
sport. Brain Inj. 2006;20(3):245-252. 2004;18(5):433-443.
111. Field M, Collins MW, Lovell MR, Maroon J. Does age 116. Guskiewicz KM, McCrea M, Marshall SW, Cantu RC,
play a role in recovery from sports-related concussion? Randolph C, Barr W, et al. Cumulative effects associ-
A comparison of high school and collegiate athletes. ated with recurrent concussion in collegiate football
J Pediatr. 2003;142(5):546-553. players: the NCAA Concussion Study. JAMA. 2003;
112. Collins MW, Iverson GL, Lovell MR, McKeag 290(19):2549-2555.
DB, Norwig J, Maroon J. On-field predictors of 117. Broshek DK, Kaushik T, Freeman JR, Erlanger D, Webbe F,
neuropsychological and symptom deficit following Barth JT. Sex differences in outcome following sports-
sports-related concussion. Clin J Sport Med. 2003; related concussion. J Neurosurg. 2005;(5):856-863.
13(4):222-229. 118. Colvin AC, Mullen J, Lovell MR, West RV, Collins MW,
113. Collins MW, Field M, Lovell MR, Iverson G, Johnston Groh M. The role of concussion history and gender in
KM, Maroon J, et al. Relationship between postconcus- recovery from soccer-related concussion. The American
sion headache and neuropsychological test performance Journal of Sports Medicine. 2009;37(9):1699-1704.
3970_Ch27_530-536 25/06/14 12:44 PM Page 530
CHAPTER 27
Physical Therapy
Diagnosis: Clinical
Decision-Making for
Vestibular Disorders
Susan J. Herdman, PT, PhD, FAPTA
The advent of direct access for physical and occupational occupational therapy diagnosis for a vestibular disorder
therapists means that clinicians must be able to screen for or to the decision to refer the patient to a physician.
and identify for a multitude of problems and mak e deci- The diagnostic schematic presented here is a “w ork in
sions about treatment and referral. At a minimum, thera- progress” and is meant as a guide only for the therapist.
pists need to know when they should refer the patient to a It is offered as a framework for arriving at a physical di-
more qualified therapist or to a physician. Sometimes the agnosis for patients with vestibular problems. Each of the
decision to refer to another health-care pro vider is made physical therapy diagnoses presented should demonstrate
easily, such as when the patient’s problems are clearly not commonalities across all persons with that diagnosis.
under the purview of a therapist (e.g., headache or hearing There are two phases to making the physical therapy (PT)
loss). In other situations, the patient’s problem may or may diagnosis. The first is in the history of the patient’s com-
not be something appropriate for physical or occupational plaints; the second consists of some simple clinical tests
therapy, but the underlying cause needs to be managed of the vestibulo-ocular system.
by a physician. “Dizziness” is one of those patient prob- Diagnosis can be defined as “the art of distinguishing
lems. “Dizziness” is one of the most prevalent complaints one disease from another.”3 In medicine, the identification
for which people seek medical help, 1 with an estimated of a particular disease leads to specific medical and/or sur-
90 million Americans over the age of 16 years having ex- gical treatment. A physical or occupational therapy diag-
perienced it.2 It can have significant consequences for an nosis differs from a medical diagnosis in that, rather than
individual, with 33% of patients reporting that their pro- attempting to identify a particular disease, a constellation
fessional activities are af fected by dizziness and 14% of symptoms and signs toward which physical and occu-
changing or abandoning their profession.2 Although dizzi- pational therapy will be directed is identified. Once the PT
ness can be caused by many different medical conditions, diagnosis is achieved, the vestibular exercise approach can
it is estimated that as much as 45% is caused by vestibular be identified (Table 27-1). Certainly, there will be times
disorders.2 when the medical diagnosis and the PT diagnosis are the
In this chapter, we discuss an updated paradigm for same—for example, benign paroxysmal positional vertigo
helping the therapist arri ve at the proper physical or (BPPV). However, there will be times when the diagnoses
530
3970_Ch27_530-536 25/06/14 12:44 PM Page 531
Chapter 27 • PHYSICAL THERAPY DIAGNOSIS: CLINICAL DECISION-MAKING FOR VESTIBULAR DISORDERS 531
532 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Chapter 27 • PHYSICAL THERAPY DIAGNOSIS: CLINICAL DECISION-MAKING FOR VESTIBULAR DISORDERS 533
BENIGN PAROXYSMAL
POSITIONAL VERTIGO
History Central vestibular Refer to
Nystagmus/vertigo neurology
+ Test
No Migraine, fistula
Vertigo? Yes ⫺Test
Yes Positional? Test for BPPV Possible BPPV
Yes Check hypotension
No
Episodic
Lasts <1 minute
dizziness? Yes Yes Fistula Refer to
No Pressure-induced?
No not appropriate neurology
Lasts 1–2 hrs Yes
Yes Is the problem No Yes
disequilibrium? Yes Episodic vertigo
Spontaneous? Also has persistent No
not appropriate for PT
No imbalance
No recheck for BPPV
Yes Does pt have Yes
+ head thrust No
No Lasted >12 hrs Yes + Head thrust ? Migraine
bilaterally ? Meniere’s
No longer present Yes
+ HT
GO TO unilaterally UNILATERAL VESTIBULAR LOSS
No Spontaneous?
UVL Yes Peripheral or level of Vestibular Nu
Yes
No Yes
No Direction fixed In room
BILATERAL Lasted >12 hrs Acute
Nystagmus light
VESTIBULAR LOSS Still present Nystagmus
Yes
Not No In the
really Yes dark Subacute Expect SVV
Chronic lateropulsion
Motion
Direction Yes ipsilaterally
sensitivity Refer to
changing
Movement- in room light neurology
SVV, OTR induced,
Lateropulsion? Yes
No other? No
No
Yes Refer to
Yes neurology SYMPTOM
Neck pain MIGRAINE
CENTRAL Dizziness MIGRAINE EQUIVALENT TEMPO
Figure 27.2 This flow diagram begins with the history (center). The patients should be
asked if they have experienced vertigo (a sense of spinning). If the answer is “yes,” the next
series of questions deals with the temporal nature of that vertigo. (Column to the right:
<1 minute, 1 to 2 hours, >12 hours, continuous). The temporal quality of the vertigo then
leads to diagnoses of BPPV, episodic vertigo, UVL, continuous vertigo, and motion sensitivity.
Note that some of these diagnoses are appropriate for PT treatment, and others are not. If,
on history, the patient states that he or she has not experienced vertigo but rather has com-
plaints of disequilibrium, the path leads to diagnoses that must be distinguished based on
clinical examination. Note how the presence or absence of corrective saccades to rapid head
thrusts is used to identify unilateral and bilateral vestibular loss. (UVL = unilateral vestibular
loss, SVV = subjective visual vertical, OTR = ocular tilt reaction.)
3970_Ch27_530-536 25/06/14 12:44 PM Page 534
534 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
does not mean that the patient does not have BPPV. The experiencing vertigo continuously or may be misusing
appearance of vertigo and nystagmus during testing is the word vertigo. For example, the patient may be expe-
notoriously inconsistent. A diagnosis of BPPV may be riencing movement-provoked symptoms or motion sen-
reached, at least tentatively, by history alone. Also note sitivity. This implies that movement of the individual or
that the possibility of a diagnosis of BPPV is raised re- movement of the environment produces symptoms that
gardless of the patient’s description of the duration of may include lightheadedness, nausea, and e ven an illu-
the spell of v ertigo. Patients are often poor historians sion of movement. Although this can occur follo wing
and may believe the vertigo lasted for extended periods unilateral or bilateral vestibular loss, it can also occur in
of time because they continue to feel poorly e ven after patients with other , non-vestibular problems such as
the actual spinning has stopped. In f act, all patients migraine. Finally, complaints of continuous vertigo of long
should be tested for BPPV, including those without com- duration suggest problems for which the patient should
plaints of true v ertigo. BPPV is v ery common and has be referred to a neurologist.
been identified in patients who also have UVH or BVH The patient may den y a history of v ertigo but may
(see Chapters 22 and 23). complain of episodic dizziness. Note that episodic dizzi-
Vertigo that lasts for a fe w hours is most lik ely to ness leads back to Tempo and specifically “last less than
be from Ménière’s disease or may be a migraine-related 1 minute.” The patient may also complain of disequilib-
event (see Chapters 4 and 15). These disorders are not rium. There are many underlying etiologies for the com-
appropriate for treatment using vestibular rehabilitation, plaint of disequilibrium, both vestibular and non-vestibular.
and must be managed medically . The exception would The head-thrust test can be used to identify whether the
be the patient who has persistent complaints of imbal- patient has chronic UVH (positive to one side only) or bi-
ance between these episodes of vertigo who might have lateral vestibular loss (positive with head thrusts in both
developed UVH with repeated episodes of Ménière’s dis- directions). Patients with apparently normal VOR to rapid
ease. The head-thrust test may help to identify this prob- head thrusts may still ha ve a vestibular deficit, so further
lem, although formal v estibular function tests may be testing (vestibular function tests) may be needed to reach
necessary. this diagnosis.7
Vertigo lasting 12 hours to days typically signif ies The complaint of disequilibrium (a sense of imbal-
the sudden onset of UVH (see Chapter 4). During the ance) may also be an aspect of motion sensiti vity. If
acute period following onset, spontaneous nystagmus in patients with disequilibrium specifically have complaints
the light and possibly a sk ew deviation would be of lateropulsion (and also have an abnormal ocular tilt re-
observed. Both should resolve within 1 to 2 weeks. Fail- action and abnormal subjective visual vertical), they prob-
ure of spontaneous nystagmus, or of a skew deviation, to ably have a central v estibular problem above the level
resolve strongly suggests central in volvement of the of the vestibular nuclei (see Chapters 5, 10, and 12). The
structures responsible for compensation. Thus, the pres- complaint of disequilibrium may be used by patients to
ence of spontaneous nystagmus in the light should be cor- describe motion sensiti vity, leading to questions as to
related with time from onset to determine if there is whether the patient is experiencing migraine or migraine-
central involvement. Continuous vertigo has several pos- equivalent events. Finally, disequilibrium may be related
sible explanations. First, the patient may be in the acute to other neuromuscular problems.
phase following onset of unilateral dysfunction. This can
be easily v erified by determining when the v ertigo
started. Additionally, if the problem is acute, the patient
Identification of Modifiers
should still ha ve spontaneous n ystagmus that follo ws Once a PT diagnosis has been achieved, based on history
Alexander’s Law (Chapter 10). Second, if the patient de- and elements of the clinical examination, it is necessary
scribes vertigo but there is no n ystagmus when fixation to perform other assessments to identify other problems
is blocked (with Frenzel lenses or infrared goggles), it is that will modify the exercise program for each individual
not likely that the patient has a v estibular deficit that is patient. These modifiers include comorbidities, subjec-
treatable with exercises. Therefore, the patient should be tive complaints, psychological factors, and the patient’s
referred to a neurologist. Unfortunately, looking for nys- premorbid activity level (Box 27-1). Finally, there are
tagmus with the patient looking at a Ganzfeld (unstruc- specific assessments that must be performed to establish
tured, uniform visual background) may not be suf ficient the patient’s baseline performance so that changes in sta-
for this e xamination unless you can truly attest that tus can be assessed following treatment and the patient’s
the patient could not be suppressing nystagmus by fixat- return to improved or normal participation at the societal
ing on a tar get. Third, the patient may not be actually level can be evaluated (Table 27-3).
3970_Ch27_530-536 25/06/14 12:44 PM Page 535
Chapter 27 • PHYSICAL THERAPY DIAGNOSIS: CLINICAL DECISION-MAKING FOR VESTIBULAR DISORDERS 535
Box 27-1
MODIFIERS OF TREATMENT
Activity Level Psychological
Basic ADL—bath, dress, meals, clean Coping strategy
Balance—gait speed, fall risk, endurance Anxiety, depression
Fall history—circumstance, frequency, injury Perception of disability
Driving—day, night Somatoform, conversion
Work—harder to perform, changed jobs, not working Severity of subjective complaints
Personal factors Secondary gain issues
Visual—cataracts, macular degeneration, field Environmental factors
Somatosensory—peripheral neuropathy Family support
Musculoskeletal—cervical, back, arthritis, strength, Availability of transportation
range of motion Location of stairs, bedroom, bathrooms
Central nervous system—stroke (e.g., brainstem),
cerebellar disease
Gender
Problem Tests
Visual acuity during head movement Computerized Dynamic Visual Acuity Test Clinical
Dynamic Visual Acuity Test
536 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
CHAPTER 28
The Role
of Emerging
Technologies
in Vestibular
Rehabilitation
Courtney D. Hall, PT, PhD ■ Dara Meldrum, PT, MSc, PhD ■
It is an exciting time in rehabilitation. In the past decade, creates opportunities that did not previously exist for im-
there has been a proliferation of novel technologies designed proving patient care. In addition, the use of smart phones,
to enhance rehabilitation outcomes. Virtual reality is one of which have sophisticated b uilt-in sensors (e.g., ac-
those emerging technologies that has been applied to a vari- celerometers, gyroscopes, global positioning systems, and
ety of medical purposes including medical education and compasses), may be used to provide feedback and deliver
training, primary care, psychiatry, surgery, radiology, and and track precise rehabilitation programs. More recently,
more recently, rehabilitation. There is considerable excite- applications (apps, as the y are commonly kno wn) have
ment surrounding virtual reality across a multidisciplinary been developed that can be used on smart phones and
group of scientists and clinicians who are de veloping this tablets to record gait speed, demonstrate the labyrinth and
new technology for physical, psychological, cognitive, and how the vestibulo-ocular reflex (VOR) works, and even
social rehabilitation purposes. Telehealth, the delivery of to employ a metronome for use during assessment (e.g.,
health-care services at a distance, has emerged as a signifi- dynamic visual acuity) and treatment. Additional apps for
cant component of the health-care delivery system with the eye movements and demonstration of v estibular treat-
advent of high-speed, high-bandwidth telecommunication ments are in the process of being de veloped. With the
networks. The combination of virtual reality with telereha- use of YouTube, one can sho w patients how to perform
bilitation holds great promise in increasing our ability to vestibular exercises and even the canalith repositioning
work with patients at a distance, of fering greater access to maneuvers. As with anything, one must always ensure the
care for rural patients. Although telerehabilitation incorpo- accuracy of what is being taught or demonstrated. In the
rating virtual reality to train balance in patients following a future, part of our job may be to identify for our patients
stroke has been recently tested with good outcomes, 1 there the appropriate technology to optimize education concerning
have been no studies to date that ha ve validated the use of their specific condition.
telerehabilitation for patients with vestibular disorders. The goal of this chapter is to highlight new technolo-
It is currently estimated that 90% of the world’s pop- gies, focusing on virtual reality b ut also including aug-
ulation now has access to a mobile network. This access mented sensory biofeedback and rele vant apps that are
537
3970_Ch28_537-554 25/06/14 2:12 PM Page 538
538 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
currently being tested or newly available to clinicians. These not severe, symptoms. Initially, patients may feel worse as
apps may be a useful adjunct to vestibular rehabilitation for they experience those situations that they may have previ-
improving outcomes or for widening our reach to include ously avoided. Little is known about the mechanism of ha-
patients with limited clinic access. This is a burgeoning area bituation. One hypothesis is that active movement presents
of research that is e xponentially expanding as technology a sensory mismatch to the brain that promotes compensa-
costs decrease and research capacity increases. tion and adaptation for vestibular disorders.10
Visually complex environments, such as grocery
stores, frequently induce symptoms in patients with vestibu-
Key Concepts Related lar deficits. The difficulty for the therapist is in creating gra-
to Virtual Reality dations of the visual environment from relatively simple to
One of the challenges facing therapists is identifying ac- complex. Virtual reality of the en vironment can be finely
tivities that are appealing, meaningful, and motivating so controlled, thus “dosed” to match the stage of reco very of
that patients will engage in these acti vities at a level that the patient. As mastery is achieved, the complexity of the
is of sufficient intensity and duration to produce long-term virtual environment is systematically increased. For exam-
compensation. Some of our patients complain that vestibu- ple, with the virtual grocery store, shelv es can be sparsely
lar exercises are boring. The use of virtual reality technol- populated with products initially, and then as the patient
ogy for rehabilitation has the potential to enhance progresses to comple x visual en vironments, the virtual
rehabilitation outcomes by being engaging and interesting. shelves can be more densely populated.6
Virtual reality is an immersive, interactive experience that There are numerous reports of using virtual reality ,
occurs in real time and is created by a computer interface.2 specifically using a game-based platform, for dynamic bal-
Specific assets of virtual reality related to rehabilitation ance training to impro ve postural stability in indi viduals
include the opportunity for e xperiential learning in chal- with neurological impairments or older adults. 11,12 It is
lenging but safe environments and the ability to objec- only recently that an application of virtual reality has been
tively measure behavior while maintaining control o ver developed specifically to incorporate vestibular adaptation
stimulus delivery and measurement.2 Nazareth et al iden- exercises that involve head movement while focusing on
tified three factors that predicted chronic dizziness: a his- a visual target.13
tory of fainting (probably a symptom of panic), v ertigo, Although virtual reality systems ha ve great potential,
and avoidance of situations that pro voked dizziness.3 By most of them are not commercially available, require exten-
allowing patients to carefully control the level of exposure, sive space or specially trained staf f, and are prohibitively
thus symptoms, to situations that pro voke their dizziness, expensive; thus, virtual reality is inaccessible to the ma -
virtual reality may encourage early training in provocative jority of clinicians involved in vestibular rehabilitation and
situations, which may result in improved outcomes. their patients. Recently, the gaming industry has de vel-
Virtual reality systems specific to vestibular rehabil- oped portable, low-cost interactive game systems, such as
itation have been de veloped to achie ve three primary Nintendo Wii Fit® (Nintendo, Kyoto, Japan) and Microsoft
goals: (1) reduction of symptoms (vertigo, dizziness, space Xbox 360 Kinect ® systems (Microsoft, Redmond, WA),
and motion discomfort/visual v ertigo), (2) adaptation of which monitor movement. The use of these of f-the-shelf
the VOR and optokinetic responses, and (3) retraining of video games as an adjunct to rehabilitation has garnered
postural stability. There is preliminary support for the use much interest with physical therapists o ver the past fe w
of virtual reality to meet these goals.4-6 In addition, studies years. In addition, there is increasing e vidence that older
have reported that participants enjoy interacting with vir- adults experience a high level of enjoyment from video game
tual environments,7 and importantly, achieve a high num- experiences. A recent study showed that 20% of seniors over
ber of repetitions,2,8 which may lead to greater motivation the age of 65 reported playing video games and, in fact, they
to exercise more, especially if the virtual environment can played more often than their younger counterparts.14
be used in the home.
One of the approaches commonly used in vestibular re- Virtual Reality–Based Vestibular
habilitation, habituation, is v ery well suited to the virtual
reality platform. Habituation is used to reduce symptoms by
Rehabilitation
repeated, graded exposure of the patient to situations that There has been a considerable increase in research explor-
elicit symptoms.9 The therapist guides the patient through sit- ing the use of virtual reality in v estibular rehabilitation in
uations or positions that provoke the patient’s symptoms and the past decade 15,16 coinciding with a general acceptance
prescribes a home-based program that involves repetitions of that virtual reality has a place in rehabilitation.17-19 Thus far,
these situations in a graded fashion to provoke moderate, but the research has been primarily laboratory-based because
3970_Ch28_537-554 25/06/14 2:12 PM Page 539
of the expensive equipment and multiple disciplines (clini- Two main types of virtual reality systems have been in-
cians, computer scientists, engineers) required for this tech- vestigated in patients with v estibular pathology: high-end
nically demanding process. To date, investigations of virtual systems consisting of head-mounted display and wide field
reality have involved physiological responses, acceptability of vision, and of f-the-shelf systems including Nintendo
of virtual reality to patients, and ef ficacy of treatment, Wii®, Microsoft Kinect®, and Hybrid systems (Table 28-1).
although efficacy research has been limited to small non- Hybrid systems employ different combinations of compo-
controlled, non-randomized studies. nents, usually from low-cost systems (such as the Nintendo
Virtual reality has demonstrated profound effects on Wii® remote controller or Microsoft Kinect ®) to create
the visual and v estibular systems and can induce both vestibular-specific exercises. These systems are differenti-
wanted and unwanted oculomotor and postural effects in ated by levels of immersion, technical specifications, front-
healthy subjects. For example, virtual reality can cause end flexibility, availability, cost, and the evidence supporting
motion sickness20-22 and transient oculomotor changes. 23 their application to rehabilitation.
Increased postural sway15,22,24 and gait deviations have
also been observed with virtual reality.21 Further research
High-End Systems
is needed to quantify these ef fects and identify how they
may be applied therapeutically in patients with compro- High-end systems are highly immersi ve and have front-
mised vestibular systems before recommendations of vir- end flexibility (i.e., the therapist can control and adapt
tual reality for mainstream clinical use. delivery of stimuli, such as the speed and direction of
Examples Examples
Head-Mounted Display systems • Nintendo Wii
• Balance Rehabilitation Unit (BRU) • Microsoft Kinect
Wide Field of View • Hybrid systems (using elements of low-cost
• Computer Assisted Rehabilitation Environment (CAREN) systems and specially developed software)
• Balance Near Automatic Virtual Environment (BNAVE)
• Virtual Environment and Postural Orientation (VEPO)
Laboratory
Advantages Advantages
• Precise measurement of motion and postural stability • Low cost
parameters • Readily available
• Highly immersive • High usability
• Front-end flexibility • Easy to incorporate into clinical/home environment
Disadvantages Disadvantages
• High cost • Not highly immersive
• Not readily available • Minimal front-end flexibility
• Not for home use • Measurement not as precise
• Technically demanding • Narrow field of view (no optokinetic stimuli/visual
• Multiple disciplines required for use flow)
*Quasi-experimental design—subjects are not randomized but measured pre and post intervention/exposure
**RCT—Randomized controlled trial
3970_Ch28_537-554 25/06/14 2:12 PM Page 540
540 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
optokinetic stimulus). In addition, these systems allo w disorders suggesting that virtual reality could be used to
for precise measurement of motion and postural stability. adapt visual scenes to a person’s capabilities, thereby fa-
The disadvantages of these systems are the high cost, tech- cilitating faster adaptation. Viirre and Sitarz used the time
nical demands of the systems, and the multiple disciplines lag between image update and head movement therapeu-
that are needed to operate the equipment and interpret tically in patients with v estibular disorders.5 As the user
data. There are two basic types of high-end systems— moves the head, thus the HMD, the virtual scene updates
head-mounted display and wide f ield of view—that will to correspond to the new point of view. The virtual scene
be discussed below. motion was altered by slo wing the visual scene to just
slightly faster than the patient’s VOR gain (i.e., the virtual
Head-Mounted Displays scene moved proportionally slower than the head moved),
Head-mounted displays (HMDs) are considered com- and then as VOR gain improved, the virtual scene w as
pletely immersive. When wearing an HMD, the e xternal gradually speeded up. Nine subjects performed the virtual
world is no longer visible and is replaced by a virtual world reality exercises twice a day for 30 minutes for f ive days,
projected onto two internal liquid crystal display screens and six controls completed the same exercises but without
(LCD) in the HMD (Fig. 28.1A, B, and C). Head position alteration of the scene speed. The exercise program entailed
is tracked and the image on the screens is updated in real active search tasks, necessitating active head movements.
time (i.e., if the patient turns the head left, the virtual scene There was a significant increase in VOR gain for the virtual
moves accordingly). HMDs can be hea vy and typically reality group compared with controls immediately after the
result in a narrow field of view (30 to 60 de grees). The intervention, which partially remained after 1 week. In
lack of peripheral field of view has been associated with contrast, Di Girolamo et al found a transient decrease in
“cybersickness” or “simulator sickness.”25 Simulator sick- VOR gain in healthy subjects playing a virtual game with
ness can include symptoms of nausea, dizziness, faintness, HMD.29 They postulated that as the computer was updating
headache, double vision, and/or f atigue and is thought to the visual scene and doing the w ork of the semicircular
be a result of sensory conflict. The time lag between head canals, the VOR gain w as adaptively reduced. Thus, it
movement and the visual display update is also kno wn to appears that VOR gain can be adapted, at least transiently,
cause simulator sickness. using HMDs.
Viirre26,27 and Kramer et al 28 were the first to dis- In a new application of HMD technology , Pothier
cuss the use of virtual reality with persons with vestibular and colleagues used immersive virtual reality glasses in
A B C
Figure 28.1 (A) Head-mounted displays block the person from viewing the external world
and replace it with a virtual world that is projected onto internal display screens. Head
position is tracked and the image on the screens is updated in real time (i.e., if the patient
turns the head left, the virtual scene moves accordingly). (B) The head-mounted display is
connected via cable to a computer system so that the virtual image is displayed inside the
lenses and updated in real time. (C) In this application, the patient is navigating through a
virtual forest to reach the target tree (with swirls on the trunk) while avoiding obstacles:
rocks, holes, and other trees. (Forest Virtual Environment developed by Kathleen Turano,
Johns Hopkins University, and Ronald Schuchard, Stanford University/VAPAHCS.)
3970_Ch28_537-554 25/06/14 2:13 PM Page 541
542 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Off-the-Shelf Systems
The computer gaming industry has inadvertently made it
possible for the advanced technologies present in some of
the high-end virtual reality de vices to be made a vailable
to clinicians at a lo w cost. These gaming systems, dis- patients needed a nearby chair for support when using the
cussed below, have the capacity to track three-dimensional Wii. It has also been reported that older adults across a
movement and/or center of pressure (COP). Although con- wide range of ages (62 to 90 years old) can safely mount
sidered to be non-immersive (they were developed to con- the balance board and quickly learn Wii Fit games.45
nect to a television or computer monitor), they can provide One key component of balance training is learning to
auditory and visual feedback in real-time and generate so- control the center of gravity during a variety of movements.
phisticated virtual environments. Furthermore, these com- The WBB detects vertical forces applied to the board and
mercially available gaming systems have a wide repertoire then calculates COP, a surrogate measure for center of
of games and exercises. The potential of gaming systems gravity. The WBB is sensitive enough to detect even small
has been realized by the rehabilitation community , and changes in COP that occur during e ye movement tasks
many groups are investigating using these systems off-the- while standing.46 By moving and shifting COP, the player
shelf (i.e., as-is) as well as adapting them to meet the spe- controls an avatar in the game environment, which is then
cific needs of rehabilitation patients (hybrid systems). One displayed in real time on the monitor. For example, the ski
major disadvantage of these systems is that the y have a slalom game involves the player shifting his or her weight
smaller field of view and thus lack the ability to generate side-to-side to move the avatar laterally or anterior-posterior
visual flow and optokinetic stimuli that are important in to control speed down the mountain with the goal of skiing
postural control and in rehabilitation.15,41,42 Another major down a virtual ski slope and passing through as many gates
disadvantage for the rehabilitation community is that the as possible.
gaming systems were designed for healthy populations Through the use of balance games that involve control
and lack front-end flexibility; thus, many of the games, as of COP, the Wii Fit may be a useful adjunct to therap y
developed, are not appropriate for clinical use. (Fig. 28.6A and B). However, Duclos and colleagues found
that performing the Wii 50/50 balance challenge using the
Nintendo Wii® football game and ski slalom game did not challenge bal-
Nintendo released the Wii in 2006, and it has become the ance (as determined by the distance between COP and the
best-selling gaming console of all time. The Wii consists limits of the base of support where a smaller distance is
of a computer interf ace; a controller (W iimote), which less stable) as much as w alking at a f ast pace in a small
houses an accelerometer; gyroscope and infrared camera; sample of healthy elderly subjects. 47 The static nature of
and a sensor that detects motion in three planes. In 2007, the balance games (feet in place) may not be optimal for
Nintendo released the Wii Fit Plus system, which incor- retraining dynamic balance. Another important component
porated a balance board. The balance board is a force plate of balance rehabilitation is multisensory training to im-
incorporating four force transducers that compute center prove the ability to integrate sensory input for balance. The
of pressure displacement in the mediolateral and antero- incorporation of unstable surf aces and reduced or absent
posterior directions. Wii Fit Plus has man y exercise and vision (eyes closed conditions) is thought to be a critical
balance games that purport to challenge balance and pro- aspect in balance training exercises.48 The limitation of the
vide visual and auditory feedback of the COP. The accu- firm, non-movable surface of the Wii balance board can be
racy of the Wii balance board (WBB) to detect center of overcome by incorporation of a rocker bottom device (Frii
pressure is comparable to a laboratory force plate.43,44 Board; Fig. 28.6C) that transforms the WBB into a multi-
A recent study e xamined perceived usability of the directional unstable surface (Swiit Game Gear) or the Wii
Wii system in patients with balance impairment. 7 In this Real Balance board (CTA Digital; Fig. 28.6D). The games
study, 26 subjects with impaired balance caused by neu- and balance exercises on the Nintendo Wii do not factor in
rological disease underwent a single, 30-minute session the requirement for performing exercises with eyes closed,
on the Wii using selected exercises and balance games (see although auditory feedback of the COP is built in and can
Case Study 28-1) and afterwards scored the system on us- provide feedback regarding postural sway. Some of the ex-
ability. Scores indicated high usability, but there was a ten- ercises/games provide a visual image of COP e xcursion,
dency for older patients to rate the system less usable. which provides knowledge of results feedback. As yet, no
Nearly 90% of patients indicated a preference to use the studies have investigated these add-on boards or auditory
Wii in future therapy, and 70% reported that the Wii was feedback for their impact on rehabilitation.
more enjoyable and motivating than conventional balance One randomized controlled trial has demonstrated pos-
retraining. Factors such as feedback and motivation were itive outcomes using a non-modified WBB for balance re-
frequently cited as perceived benefits of Wii. Mild adverse habilitation after acute vestibular neuritis compared with a
events (nausea, headache, and increased dizziness) were no-exercise control group. 49 The experimental group per-
reported in a minority of patients. The majority of these formed a variety of exercises including yoga, strengthening,
3970_Ch28_537-554 25/06/14 2:13 PM Page 544
544 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
A B
C D
Figure 28.6 (A) Patient with bilateral vestibular loss exercises on the Nintendo Wii Fit Plus®
playing the Table Tilt game. The patient stands on the Wii Balance Board (WBB) and, by
moving her center of pressure, rolls virtual balls into virtual holes on a virtual tilt table.
(B) Center of pressure is displayed providing visual feedback to the user. (C) A progression
of the exercise in which the Frii Board is placed under the WBB to transform it into an
unstable (rocker) board. (D) The Wii Real Balance Board is another method to transform
the WBB into an unstable surface.
and balance games for 10 training sessions, none of which intensity than conventional rehabilitation. These aspects,
involved specific head movement or gaze stability activities. plus the low cost of Nintendo Wii and ease of use, mak e
Sensory organization test and Dizziness Handicap Inventory it likely that Wii will have a growing place in v estibular
scores for the e xperimental group (n = 34) were signif i- rehabilitation, although there is limited evidence at present
cantly improved compared with the control group (n = 33). to support its effectiveness.51
Another randomized controlled trial using the unmodif ied
Wii in vestibular rehabilitation is under way.50 Microsoft Kinect®
The Nintendo Wii is currently being used in clinics Microsoft Kinect® for Sony Xbox was released in 2010 as
for a variety of rehabilitation applications. The motiva- a computer gaming system. It uses an embedded webcam
tional and enjoyment aspects of Wii-based programs may and infrared system to detect motion, so no handheld con-
result in better adherence to exercise resulting in a higher troller is required. The accuracy of the Microsoft Kinect
3970_Ch28_537-554 25/06/14 2:13 PM Page 545
546 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
reach, lateral reach, and single-leg stance with eyes closed), including vestibular electrical stimulation, electrotactile
but there was a tendency for error to be present in lar ger- feedback, auditory feedback, and vibrotactile feedback.
magnitude movements.
Use of a simple, ine xpensive gaming system may
provide an alternati ve method for testing balance in Vestibular Electrical Stimulation
community-dwelling older adults when other resources Recent work suggests that “vestibular electrical stimulation”
are not available. The components of the Wii Fit balance (VES) was as effective as oculomotor rehabilitation in per-
board and Kinect sensors are v alid and reliable for col- sons with acute peripheral v estibular disorders.58 The VES
lecting force and motion data when compared with lab- consisted of electrical stimulation that w as applied to the
oratory force plates and motion analysis systems and paravertebral nuchal muscles, which is purported to stimu-
thus may have utility in measuring postural control. In late the af fected vestibular nuclei through the crossed
addition, off-the-shelf games appear to capture similar vestibulospinal pathway. Participants in the electrical stim-
information as standard physical performance measures ulation group (n = 14) w alked while VES was applied for
of balance and gait and the gold standard computerized 40 minutes over a 10-day period. The oculomotor group
dynamic posturography. Additionally, there is no w a (n = 14) performed saccadic e ye movements to a tar get,
commercially available low-cost alternative to comput- smooth pursuit eye movements, reading a moving paper, and
erized dynamic posturography that incorporates the optokinetic stimulation (moving stripes of different colors at
WBB as the force platform component and is paired with a velocity of 30deg/sec) while standing for the same amount
customized software to perform assessment of limits of of time as the electrical stimulation group. Barozzi and col-
stability and modified clinical test of sensory interaction leagues found that both groups impro ved on measures of
on balance (CSMI Solutions). Benef its of gaming sys- static posturography and dizziness handicap inventory scores
tems include availability, minimal cost, nonclinical ap- with no differences between the two types of interventions.58
pearance, and potential for assessment of f all risk in VES might be an option in the future, but the technology is
community-dwelling older adults. not readily available for use in the clinic at this time.
Auditory Biofeedback
Auditory biofeedback to enhance postural control is an in-
expensive technology66-68 that uses accelerometers and has
A
been demonstrated to improve balance in healthy control
subjects66 and in persons with bilateral vestibular hypofunc-
1 2 3 tion.67 Subjects stood with eyes closed on a foam pad on a
force platform while wearing headphones. The pitch and
volume of the auditory signal increased when subjects
moved away from vertical (outside the ±1-deg sway thresh-
old) in any direction. Subjects with bilateral v estibular hy-
FG 0 0
pofunction demonstrated less trunk accelerations, a smaller
X X
X Y
sway area, and greater time spent within the ±1-de g sway
4 threshold after training with the device (Fig. 28.8). Hegeman
et al reported that audio biofeedback did not improve sway
on a foam pad with e yes closed in people with bilateral
vestibular hypofunction but did report that single leg stance
Y time improved with audio feedback. 68 This approach has
also been successfully applied to indi viduals with isolated
5 otolith organ dysfunction.69,70
4
Vibrotactile Biofeedback
1 2 3
Vibrotactile feedback has advantages over lingual, audi-
tory, and visual feedback in that it does not directly com-
FG
5 Y
pete with tasks that involve speaking, hearing, or seeing.
Vibrotactile feedback is similar to the vibration that you
B
would feel from a cell phone in your pocket and is usually
Figure 28.7 (A) Tongue electrotactile device and provided around the w aist area. When vibrotactile feed-
intraoral device; (B) stimulus position and movement back was first developed, the vibrotactile de vices were
as a function of head angular motion. (From Danilov et al, quite cumbersome and not user friendly . These research
2007. Used with permission.)62
devices used as man y as 64 tactors imbedded in a v est
worn by subjects.71,72 Testing of alternative array designs
healthy people, suggesting that the device might be helpful to determine optimal design and signal ha ve resulted in
for persons with neck or vestibular pathologies.61 Proposed more streamlined products with fewer tactors.
uses for the tongue electrotactile feedback de vice include One can think of vibrotactile feedback as an early
the prevention of pressure sores,61 fall risk reduction in older motion detector system or a “body alarm” that provides the
3970_Ch28_537-554 25/06/14 2:13 PM Page 548
548 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
COP AP displacement (mm)
Other Technologies
Platform Perturbations
Typical rehabilitation of patients with vestibular disorders
involves balance training with altered visual and/or so-
matosensory information to improve postural stability in
a variety of environments. This training is typically per -
formed on foam cushions and rock er boards; however,
there is emer ging evidence that the use of computer -
driven, motorized force platforms is effective in improving
Sensor postural stability and in reducing symptoms. 78-80 The ra-
tionale is that the subject is not able to rely on somatosen-
sory input, because the platform is mo ving, and so is
forced to rely on vestibular input to maintain balance. This
Laptop may force reweighting of sensory input so that remaining
COP AP
vestibular function is used to determine position in space
and respond to loss of balance.
One paradigm uses a continuously mo ving platform,
Foam
translating in the anterior-posterior or medial-lateral direc-
tion, on which the subject attempts to maintain balance78,79
These studies demonstrated that the platform training w as
Forceplate
as effective as performance of Ca wthorne–Cooksey exer-
Figure 28.8 A patient with bilateral vestibular
hypofunction had less sway while processing the auditory cises in terms of postural stability with eyes open or closed
cue than with no auditory cueing while standing on a on a firm surface and in terms of subjecti ve symptoms of
foam pad. (Modified from Dozza M, Chiari L, Horak FB. steadiness and dizziness handicap inventory scores. Another
Audio-biofeedback improves balance in patients with perturbation paradigm involves tilt perturbations of the plat-
bilateral vestibular loss. Arch Phys Med Rehabil. 2005;86: form.80 The perturbations involve discrete angular move-
1401-1403.)
ments of the platform at a range of directions, speeds, and
amount of tilt. Winkler and Esses used random tilt pertur-
brain with additional input about body in space and en- bations of increasing speed and tilt angle in a small random-
hanced feedback about a person’ s limits of stability. The ized controlled trial. 80 In this study, subjects with chronic
amount of sway that is “tolerated” by the system can be pre- vestibular dysfunction were assigned to one of three groups:
set for each patient based on his or her abilities and the goal (1) perturbation only, (2) perturbation + home program of
of therapy. To date, most of the studies conducted with the vestibular rehabilitation (including gaze and postural stabil-
vibrotactile feedback devices have tested subjects in static ity exercises), and (3) v estibular rehabilitation only. The
stance.71-74 There has been concern that the de vices make perturbation and perturbation + v estibular rehabilitation
people stand stiffly; thus, for the devices to have clinical util- groups made the greatest improvements in subjective symp-
ity they must also be effective during walking or have car- toms and perceived function as well as f all risk reduction
ryover from standing to walking. There is some evidence to measured by the dynamic gait inde x. There has been no
support the usefulness of vibrotactile feedback during gait.75 direct comparison of the dif ferent types of perturbation
There are at least two commercially available devices training, so it is not clear what the optimal training param-
developed in Europe for use with patients (V ertiGuard® eters are. Further research is needed to clarify the role of
and SwayStarTM). Randomized controlled trials suggest perturbation training in vestibular rehabilitation. Equipment
that postural control is enhanced while wearing the is commercially available that can be used for this type of
Vertiguard® device, which is worn around the waist and training: Equitest (NeuroCom®, a di vision of Natus®) or
registers angular deviations and angular velocities of the Proprio® Reactive Balance Systems (Perry Dynamics).
trunk.76,77 It is not clear whether future vibrotactile de-
vices will be used at home or only in the clinic to retrain
postural control. If they can assist as an early detection
Smart Phones and Tablet Applications
system for fall risk, they have great value, especially for The increasing penetration of smartphones, tablets, and
the frail elderly, who are at the greatest risk of f all- mobile computing in daily life will lik ely revolutionize
related injury. health care in the future. These systems are capable of both
3970_Ch28_537-554 25/06/14 2:13 PM Page 549
storing information and measuring physiological signals dynamic visual acuity. “OptOK” also provides visual dis-
in ways that were neither accessible nor portable in the plays of optokinetic stimuli (i.e., mo ving stripes). There
past. They provide opportunities for both patients and pro- are fewer apps available on Android systems, but devel-
fessionals to access information readily, and thus have po- opers have devised a balance assessment system using the
tential to impro ve the diagnosis and management of accelerometer in a smart phone. The phone is secured to a
vestibular disorders. They can capture, store, and facilitate body segment (such as the shank) and the amplitude of
sharing of multiple types of patient data (e.g., patient data- movement is recorded o ver a period of time. These bal-
bases and reported outcomes, videos, pictures, physiolog- ance assessments include sitting balance, standing on one
ical signals). Most smartphones and tablets ha ve sensors leg, and standing on an unstable surface. However, no de-
such as accelerometers, GPS, and gyroscopes that could tails on the validity or reliability of this app are available.
have numerous uses in vestibular rehabilitation. Thus far The University of Sydney, in partnership with Liberty
only a small number of apps specif ic to vestibular reha- Technology and the Neurology Department at the Prince
bilitation have been developed. There is no go vernance Alfred Hospital Sydney, have recently developed a free
concerning apps; thus, health professionals should assess app for medical education, “aVOR” (angular VOR), that
each one for merit and applicability before emplo ying can be downloaded from iTunes. It presents a virtual pa-
them with patients. tient showing the semicircular canals in the head in three
At present, apps related to v estibular rehabilitation dimensions. It is interactive in three dimensions allowing
can be categorized as either measurement or educational. translation, rotation, zooming, and pivoting of the virtual
In the measurement cate gory, an iPhone application, head by moving the phone or using the touch screen. The
“Visual Vertical,” is commercially available to measure push-pull responses of the canals are demonstrated in re-
subjective visual v ertical (www.clearhealthmedia.com) sponse to head movement. The resultant eye responses to
based on the bucket test.81 The iPhone is secured to the in- moving the head in the presence of various combinations
side of the bottom of a b ucket. The phone presents a red of semicircular canal and/or cerebellar dysfunction are
line against a black background that the subject has to shown, including BPPV and canal repositioning maneu-
align to vertical and then degrees off-vertical are provided. vers. A quiz is available to test knowledge. This applica-
Two other iPhone apps, “Eye Chart Pro” and “OptOK” tion is highly useful for any professional wishing to learn
provide visual acuity charts that can be used to measure more about the vestibular system.
Continued
3970_Ch28_537-554 25/06/14 2:13 PM Page 550
550 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
Vestibular Rehabilitation
Benefits Questionnaire
Free Stepping Advance to step basics, then step plus and incorporate head movements
in the yaw and pitch planes.
Yoga Tree Raised foot placed lightly on other foot if full pose not possible.
*Instructions were given to have a high-backed chair within reach when exercising to provide haptic
support.
was given gaze stabilization exercises and a progres- At a 6-month follow-up, he reported one further at-
sive walking program. tack of v ertigo that had resolv ed over a 2-week
Post-treatment he felt much improved, rating both period, and he w as out walking dogs and felt able
vertigo and dizziness at 2/10. Dynamic visual acuity to return to golf. His gait speed at this session w as
had not changed. His gait speed had increased to 1.35 m/sec, and his SO T was 80 indicating he had
1.48 m/sec and his DGI was 24/24 (see Table 28-2). maintained his improvements.
552 Section FIVE • REHABILITATION ASSESSMENT AND MANAGEMENT OF PERIPHERAL VESTIBULAR DISORDERS
8. Deutsch JE, Merians A, Adamovich S, et al. Development 29. Di Girolamo S, Picciotti P, Sergi B, et al. Vestibulo-ocular
and application of virtual reality technology to improve reflex modification after virtual environment exposure.
hand use and gait of individuals post-stroke. Restor Neurol Acta Oto-Laryngologica. 2001;121:211.
Neurosci. 2004;22:371. 30. Pothier DD, Hughes C, Dillon W, et al. The use of real-
9. Norre ME, De Weerdt W. Treatment of vertigo based time image stabilization and augmented reality eyewear in
on habituation. 2. Technique and results of habituation the treatment of oscillopsia. Otolaryngol Head Neck Surg.
training. J Laryngol Otol. 1980;94:971. 2012;146:966.
10. Norre ME, Beckers A. Vestibular habituation training: 31. Herdman SJ, Hall CD, Schubert MC, et al. Recovery of
exercise treatment for vertigo based upon the habituation dynamic visual acuity in bilateral vestibular hypofunction.
effect. Otolaryngol Head Neck Surg. 1989;101:14. Arch Otolaryngol Head Neck Surg. 2007;133:383.
11. Lange B, Flynn S, Proffitt R, et al. Development of an 32. Mora R, Mora F, Crippa B, et al. Virtual Reality and vestibu-
interactive game-based rehabilitation tool for dynamic lar rehabilitation. Arch Sensol Neurootol Sci Prac. 2003
balance training. Top Stroke Rehabil. 2010;17:345. (Proceedings XXX Congress of the GNA-NES- Oporto,
12. Lange BS, Requejo P, Flynn SM, et al. The potential of Portugal).
virtual reality and gaming to assist successful aging with 33. Suárez H, Suárez A, Lavinsky L. Postural adaptation in
disability. Phys Med Rehabil Clin N Am. 2010;21:339. elderly patients with instability and risk of falling after
13. Che PY, Hsieh WL, Wei SH, Kao CL. Interactive wiimote balance training using a virtual-reality system. Int Tinnitus
gaze stabilization exercise training system for patients with J. 2006;12:41.
vestibular hypofunction. J Neuroeng Rehabil. 2012;9:77. 34. Cusin FS, Gananca MM, Gananca FF, et al. Balance Reha-
14. Lenhart A. Adults and Video Games. www.pewinternet bilitation Unit (BRU) posturography in Meniere’s disease.
.org/~/media//Files/Reports/2008/PIP_Adult_gaming_ Braz J Otorhinolaryngol. 2010;76:611.
memo.pdf. Accessed January 19, 2012. 35. Kasse CA, Santana GG, Scharlach RC, et al. Results from
15. Keshner E, Kenyon R. Using immersive technology the balance rehabilitation unit in benign paroxysmal posi-
for postural research and rehabilitation. Assist Technol. tional vertigo. Braz J Otorhinolaryngol. 2010;76:623.
2004;16:54. 36. Jacobson J, Redfern MS, Furman JM, et al. Balance
16. Whitney SL, Sparto PJ, Alahmari K, et al. The use of NAVE: a virtual reality facility for research and rehabilita-
virtual reality for people with balance and vestibular tion of balance disorders. Conf Proc ACM symposium
disorders: the Pittsburgh experience. Phys Ther Rev. Virtual Reality Software Tech. Alberta, Canada. 2001:103.
2009;14:299. 37. Whitney SL, Sparto PJ, Brown KE, et al. The potential use
17. Rizzo A, Kim GJ. A SWOT analysis of the field of virtual of virtual reality in vestibular rehabilitation: preliminary
reality rehabilitation and therapy. Presence: Teleoper findings with the BNAVE. J Neurol Phys Ther. 2002;26:72.
Virtual Environ. 2005;14:119. 38. Sparto PJ, Whitney SL, Hodges LF, et al. Simulator sick-
18. Schulteis M, Rizzo A. The application of virtual reality ness when performing gaze shifts within a wide field
technology in rehabilitation. Rehabil Psychol. 2001;46:296. of view optic flow environment: preliminary evidence
19. Kenyon RV, Leigh J, Keshner EA. Considerations for for using virtual reality in vestibular rehabilitation.
the future development of virtual technology as a J Neuroengineering Rehabil. 2004;1:14.
rehabilitation tool. J Neuroeng Rehabil. 2004;1:13. 39. Whitney SL, Sparto PJ, Brown KE, et al. The potential use
20. Ohyama S, Nishiike S, Watanabe H, et al. Autonomic of virtual reality in vestibular rehabilitation: preliminary
responses during motion sickness induced by virtual findings with the BNAVE. Neurol Report. 2002;26:72.
reality. Auris Nasus Larynx. 2007;34:303. 40. Gottshall KR, Bartlett J, Sessoms P. Vestibular physical
21. Ohyama S, Nishiike S, Watanabe H, et al. Effects of optoki- therapy comparing the CAREN: Computer Assisted
netic stimulation induced by virtual reality on locomotion: a Rehabilitation Environment with clinical vestibular
preliminary study. Acta Oto-Laryngologica. 2008;128:1211. physical therapy rehabilitation. Conf Proc 27th Barany
22. Stanney KM, Kennedy RS, Drexler JM, Harm DL. Motion Society Meeting. Uppsala, 2012.
sickness and proprioceptive aftereffects following virtual 41. Vitte E, Sémont A, Berthoz A. Repeated optokinetic stim-
environment exposure. Appl Ergon. 1999;30:27. ulation in conditions of active standing facilitates recovery
23. Howarth PA. Oculomotor changes within virtual environ- from vestibular deficits. Exp Br Res. 1994; 102:141.
ments. Appl Ergon. 1999;30:59. 42. Pavlou M, Quinn C, Murray K, et al. The effect of
24. Cobb SV. Measurement of postural stability before and repeated visual motion stimuli on visual dependence
after immersion in a virtual environment. Appl Ergon. and postural control in normal subjects. Gait Posture.
1999;30:47. 2011;33:113.
25. Moss JD, Muth ER. Characteristics of head-mounted 43. Clark R, Bryant A, Pua Y, et al. Validity and reliability
displays and their effects on simulator sickness. Hum of the Nintendo Wii Balance Board for assessment of
Factors. 2011;53:308. standing balance. Gait Posture. 2010;31:307.
26. Viirre E. In: Sieburgh H, Weghorst S, Morgan K, eds. 44. Hubbard B, Pothier D, Hughes C, Rutka J. A portable,
Health Care in the Information Age. Studies in Health low-cost system for posturography: a platform for longitu-
Technology Informatics. Vol 29. Vestibular telemedicine dinal balance telemetry. J Otolaryngol Head Neck Surg.
and rehabilitation applications for virtual reality. 1996. 2012;41(Suppl 1):S31.
27. Viirre E. Virtual reality and the vestibular apparatus. IEEE 45. Hall CD, Clevenger CK, Wolf RA, et al. Feasibility of a
Eng Med Biol. 1996;2:41. Low-cost, Interactive Gaming System to Assess Balance
28. Kramer PD, Roberts DC, Shelhamer M, Zee DS. A versatile in Older Adults. Combined Sections Meeting of the
stereoscopic visual display system for vestibular and oculo- APTA. Chicago, IL, February 8-11, 2012. Phys Ther
motor research. J Vestib Res. 1998;8:363. Abstract. 2128.
3970_Ch28_537-554 25/06/14 2:13 PM Page 553
46. Koslucher F, Wade MG, Nelson B, et al. Nintendo Wii 64. Bittar RS, Barros CG. Vestibular rehabilitation with
Balance Board is sensitive to effects of visual tasks on biofeedback in patients with central imbalance. Braz J
standing sway in healthy elderly adults. Gait Posture. Otorhinolaryngol. 2011;77:356.
2012;36:605. 65. www.wicab.com\balance.html. Accessed October 21, 2012.
47. Duclos C, Miéville C, Gagnon D, Leclerc C. Dynamic 66. Chiari L, Dozza M, Cappello A, et al. Audio-biofeedback
stability requirements during gait and standing exergames for balance improvement: an accelerometry-based system.
on the Wii Fit® system in the elderly. J Neuroeng Rehabil. IEEE Trans Biomed Eng. 2005;52:2108-2111.
2012;9:28. 67. Dozza M, Chiari L, Horak FB. Audio-biofeedback im-
48. Horak FB. Postural compensation for vestibular loss. Ann proves balance in patients with bilateral vestibular loss.
N Y Acad Sci. 2009;1164:76-81. Arch Phys Med Rehabil. 2005;86:1401-1403.
49. Sparrer I, Duong Dinh TA, Ilgner J, Westhofen M. 68. Hegeman J, Honegger F, Kupper M, Allum JH. The balance
Vestibular rehabilitation using the Nintendo® Wii Balance control of bilateral peripheral vestibular loss subjects and its
Board—a user-friendly alternative for central nervous improvement with auditory prosthetic feedback. J Vestib
compensation. Acta Otolaryngol. 2013;133:239. Res. 2005;15:109-117.
50. Meldrum D, Herdman S, Moloney R, et al. Effectiveness 69. Basta D, Singbartl F, Todt I, et al. Vestibular rehabilitation
of conventional versus virtual reality based vestibular re- by auditory feedback in otolith disorders. Gait Posture.
habilitation in the treatment of dizziness, gait and balance 2008;28:397-404.
impairment in adults with unilateral peripheral vestibular 70. Ernst A, Singbartl F, Basta D, et al. Short-term rehabilita-
loss: a randomised controlled trial. BMC Ear Nose Throat tion of patients with posttraumatic otolith disorders by
Disord. 2012;12:3. auditory feedback training: a pilot study. J Vestib Res.
51. Fitzpatrick M, Harding L. Using the Wii for Vestibular 2007;17:137-144.
Rehabilitation. http://www.vestibular.org. Accessed 71. Wall C, 3rd, Weinberg MS. Balance prostheses for pos-
10/18/2012. tural control. IEEE Eng Med Biol Mag. 2003;22:84.
52. Clark RA, Pua YH, Fortin K, et al. Validity of the 72. Wall C, 3rd, Weinberg MS, Schmidt PB, Krebs DE.
Microsoft Kinect for assessment of postural control. Balance prosthesis based on micromechanical sensors
Gait Posture. 2012;36:372-377. using vibrotactile feedback of tilt. IEEE Trans Biomed
53. Wang PC, Chang CH, Su MC, et al. Virtual reality rehabil- Eng. 2001;48:1153.
itation for vestibular dysfunction. Otolaryngol Head Neck 73. Sienko KH, Balkwill MD, Wall C, 3rd. Biofeedback
Surg. 2011;145 (2 suppl):P158-P159. improves postural control recovery from multi-axis
54. Young W, Ferguson S, Brault S, Craig C. Assessing and discrete perturbations. J Neuroeng Rehab. 2012;9:53.
training standing balance in older adults: a novel approach 74. Wall C, 3rd, Kentala E. Effect of displacement, veloc-
using the ‘Nintendo Wii’ Balance Board. Gait Posture. ity, and combined vibrotactile tilt feedback on postural
2011;33:303-305. control of vestibulopathic subjects. J Vestib Res.
55. Albiol-Pérez S, Gil-Gómez JA, Alcañiz M,et al. Use of the 2010;20:61.
Wii balance board system in vestibular rehabilitation. Proc 75. Wall C, 3rd, Wrisley DM, Statler KD. Vibrotactile tilt
13th Int Conf Interacción Persona-Ordenador; 2012: ACM. feedback improves dynamic gait index: a fall risk indicator
56. Gascuel JD, Payno H, Schmerber S, Martin O. Immersive in older adults. Gait Posture. 2009;30:16.
virtual environment for visuo-vestibular therapy: preliminary 76. Allum JHJ, Zamani F, Adkin AL, Ernst A. Differences
results. Stud Health Technol Inform. 2012;181:187-191. between trunk sway characteristics on a foam support
57. Yamada M, Aoyama T, Nakamura M, et al. The reliability surface and on the Equitest ankle-sway-referenced support
and preliminary validity of game-based fall risk assessment in surface. Gait Posture. 2002;16:264-270.
community-dwelling older adults. Geriatr Nurs. 2011;32:188. 77. Basta D, Rossi-Izquierdo M, Soto-Varela A, et al. Efficacy
58. Barozzi S, Di Berardino F, Arisi E, Cesarani A. A compar- of a vibrotactile neurofeedback training in stance and gait
ison between oculomotor rehabilitation and vestibular conditions for the treatment of balance deficits: a double-
electrical stimulation in unilateral peripheral vestibular blind, placebo-controlled multicenter study. Otol Neurotol.
deficit. Int Tinnitus J. 2006;12:45. 2011; 32:1492-1499.
59. Bach-y-Rita P, Kaczmarek KA, Tyler ME, Garcia-Lara J. 78. Corna S, Nardone A, Prestinari A, et al. Comparison of
Form perception with a 49-point electrotactile stimulus Cawthorne-Cooksey exercises and sinusoidal support
array on the tongue: a technical note. J Rehabil Res Dev. surface translations to improve balance in patients with
1998;35:427. unilateral vestibular deficit. Arch Phys Med Rehabil.
60. Danilov Y, Tyler M. Brainport: an alternative input to the 2003;84:1173.
brain. J Integr Neurosci. 2005;4:537. 79. Nardone A, Godi M, Artuso A, Schieppati M. Balance
61. Vuillerme N, Chenu O, Pinsault N, et al. Pressure sensor- rehabilitation by moving platform and exercises in patients
based tongue-placed electrotactile biofeedback for balance with neuropathy or vestibular deficit. Arch Phys Med
improvement—biomedical application to prevent pressure Rehabil. 2010;91:1869.
sores formation and falls. Conf Proc IEEE Eng Med Biol 80. Winkler PA, Esses B. Platform tilt perturbation as an inter-
Soc. 2007;6114. vention for people with chronic vestibular dysfunction.
62. Danilov YP, Tyler ME, Skinner KL, Hogle RA, Bach-Y- J Neurol Phys Ther. 2011;35:105.
Rita O, J Vestib Res. 2007:17:119-130 used with 81. Zwergal A, Rettinger N, Frenzel C, et al. A bucket of static
permission. vestibular function. Neurology. 2009;72:1689.
63. Barros CG, Bittar RS, Danilov Y. Effects of electrotactile
vestibular substitution on rehabilitation of patients with
bilateral vestibular loss. Neurosci Lett. 2010;476:123.
3970_Ch28_537-554 25/06/14 2:13 PM Page 554
3970_Ch29_555-568 25/06/14 12:46 PM Page 555
SIX
Non-vestibular
Dizziness
3970_Ch29_555-568 25/06/14 12:46 PM Page 556
CHAPTER 29
Non-vestibular
Dizziness and
Imbalance
Ronald J. Tusa, MD, PhD
Non-vestibular dizziness and imbalance can be v ery the outcomes scores are re viewed to determine whether
frustrating to the clinician, because the symptoms are the patient needs more rehabilitation and/or a follo w-up
often vague and the vestibular test results are normal. This appointment in 6 to 12 months. The latter is especially
chapter discusses the more common causes of these dis - important in patients who have progressive problems (spino-
orders. Disuse disequilibrium with fear of f all, the most cerebellar degeneration, progressive peripheral neuropathy,
common cause of imbalance, readily responds to gait and and progressive supranuclear palsy).
balance therapy. Other disorders that cause imbalance
are leukoaraiosis, normal-pressure hydrocephalus (NPH), Disuse Disequilibrium
progressive supranuclear palsy, Parkinson’s disease, large
fiber peripheral neuropathy, and cerebellar ataxia. Man y (or Deconditioning) and
of these disorders are associated with disuse disequilib- Fear of Fall
rium (or deconditioning) and, therefore, respond to phys-
ical therapy (PT) to a certain e xtent. Some individuals
Description
with these disorders do not have disuse disequilibrium, be- Each year, approximately one-third of elderly individuals
cause they are very active or are too incapacitated to per- in the general population experience a fall.1 In elderly in-
form PT. In these individuals, one must concentrate on dividuals, there is progressive decline in muscle bulk, joint
reducing fall risk through the use of assistive devices and range of motion, and reflex time.2 Increased exercise can
education. Finally, we discuss a group of disorders that are reduce the rate of this decline. Man y individuals stop
best described as dizziness in the head without severe im- walking and exercising because of recent surgery, fatigue,
balance that are triggered primarily by specific situations. chronic illness, or a fall to the ground or a near fall. Lack
It is best to ha ve any patient with chronic dizziness of exercise in the elderly leads to disuse disequilibrium. 3
first assessed by a physician to determine the diagnosis. Fear of fall can occur as a result of disuse disequilibrium
After this assessment, PT can be started the same day or and can also exacerbate disuse disequilibrium by reducing
as soon as possible. During PT, there is an initial assess- the patient’s willingness to participate in a home exercise
ment to identify the patient’s specific problems. Then the program.4
patient is started on a daily home gait and balance program Figure 29.1 sho ws the age distrib ution of fear of
that is reviewed and revised by the physical therapist every fall and disuse disequilibrium in patients at our Dizziness
week. At each visit, outcomes scores are reassessed. The and Balance Clinic. The diamonds indicate all patients
patient is then reevaluated by the physical therapist, and seen in the clinic (left axis) based on decade of age of the
556
3970_Ch29_555-568 25/06/14 12:46 PM Page 557
Management
There are no large, controlled studies of the management
800 50%
of disuse disequilibrium, but in our experience, imbalance
600
40% in individuals with disuse disequilibrium and fear of f all
Total Dizzy
■ Table 29-1 OUTCOME MEASURES USED IN PATIENTS WITH IMBALANCE AND DEMENTIA
Pre-Drain 2 hr Post-Drain
Date:
Fall risk:
(DGI ≤ 19 = fall risk; BBS ≤ 49 = fall risk; <36 = 95% fall risk)
Posturography:
SOT composite score (normal for age = _________)
in a chair and is instructed to stand up and walk as quickly improved blood flow to the brain stabilizes or improves
and as safely as possible for 3 meters, turn around, w alk function.
back to the chair , and sit do wn. Then the patient is in- All patients with NPH and leuk oaraiosis should be
structed to perform the test while counting backwards by referred for PT. These patients are usually at high risk for
threes from a randomly selected number between 20 and falls, especially backwards. For patients with leukoaraio-
100 (TUG – cognitive). Finally, the patient is asked to per- sis, some balance impro vement may occur with PT , but
form the test while carrying a full cup of w ater (TUG many patients must be given an aid (cane, walker, or rol-
manual). A difference between TUG manual and TUG lator) when amb ulating inside or outside the house. A
(TUG manual – TUG) greater than 4.5 sec indicates home health evaluation may also be necessary to reduce
fall risk. the risk for f alls at home. This may be true for patients
In the Walk While Talk test, subjects are timed while with NPH as well, if shunting does not impro ve balance.
they walk at self-selected speed for 20 feet, turn around Case Study 29-2 describes a patient with NPH, and Case
and return (40 feet total). On the second trial (WWT - Study 29-3 a patient with leukoaraiosis.
simple) the subject walks the same course and recites let-
ters of the alphabet. On the third trial (WWT-complex) the Progressive Supranuclear Palsy,
subject walks the same course and recites every other letter
of the alphabet (e.g., “a-c-e”). The gait speed for each of Parkinson’s Disease, Large-Fiber
those trials can indicate risk for falling as follows: Peripheral Neuropathy, and
Spinocerebellar Ataxia
WWT (40 ft): greater than 18 sec at risk for falls
WWT-simple: greater than 20 sec at risk for falls Description
WWT-complex: greater than 33 sec at risk for falls The neurological disorders progressive supranuclear palsy,
Parkinson’s disease, lar ge-fiber peripheral neuropathy,
Table 29-1 lists three columns for data insertion. F or and spinocerebellar ataxia are usually progressi ve and
patients with NPH, we use the table as it e xists. “Drain” are associated with imbalance and falls.
in the headings refers to performance of a lar ge-volume Supranuclear palsy (PSP) and Parkinson’s disease are
CSF drainage procedure, as described earlier. For patients a result of degeneration of different portions of the basal
with leukoaraiosis, one can substitute the following head- ganglia and forebrain. Both manifest as rigidity and masked
ings: “Pre-PT,” “1 week of PT,” and “4 weeks of PT.” facies. Retropulsion is mild in P arkinson’s disease but se-
vere in PSP. To perform the retropulsion test, the examiner
has the patient stand with feet slightly apart and instructs
Management the patient to take no more than one step backwards when
Non-controlled studies have suggested improved cognition the examiner suddenly pulls the patient backw ards at the
and balance from 65% to 77% in patients with NPH after hips using a mild force. The result is positive if the patient
insertion of a permanent shunt system to drain the hydro- must take three or more steps backwards or falls backwards
cephalus.13,14 At our center, the shunt is inserted only if “like a log.” A resting and sometimes action tremor is found
cognitive and gait tests performed after a lar ge-volume in Parkinson’s disease but is absent in PSP. Both disorders
CSF drainage procedure ha ve a positive outcome com- have some degree of upgaze defect, but it is profound in pa-
pared with baseline. tients with PSP. PSP can be devastating because the average
Unfortunately, randomized, prospective clinical trials life span of affected patients is 7 years, death being caused
are lacking. In a Cochrane review published in 2002 and by aspiration or complications from falls to the ground.
updated in 2009,15 there is no evidence to indicate whether Large-fiber peripheral neuropathy results in loss of
placement of a shunt to remo ve fluid is effective in the vibration perception and proprioception. Se vere loss of
management of normal pressure hydrocephalus. proprioception, especially in the ankles, leads to se vere
Current evidence suggests that in patients with imbalance. Individuals with this disorder are e xtremely
leukoaraiosis, vigorous treatment of cardio vascular dependent on vision to maintain balance. They usually
disease risk f actors may pre vent the de velopment or have a positive Romberg test result on clinical e xamina-
progression of the process as well as the associated tion. Common causes of lar ge-fiber neuropathy are dia-
cognitive and balance decline.16 Therefore, hypertension, betes mellitus, alcohol ab use, inflammatory neuropathy,
elevations of cholesterol, diabetes mellitus, and smoking and hereditary neuropathy.
should be controlled in these patients. Unfortunately , Spinocerebellar ataxia (SCA) is a genetic disorder
there are no prospecti ve trials to determine whether that causes de generation of dif ferent portions of the
3970_Ch29_555-568 25/06/14 12:46 PM Page 560
cerebellum and structures outside the cerebellum, includ- randomized controlled trials of the ef fectiveness of exer-
ing peripheral nerve and brainstem structures. These result cise therapy to improve function in patients with neuropa-
in imbalance, difficulty with gait, and incoordination of thy. The studies found improvement in muscle strength but
the eyes, arms, and legs. There have been up to 60 differ- not in reduction of disability . Currently, the standard of
ent types of SCA identified, and at least 29 different gene care for patients with proprioception defects caused by pe-
mutations.17 Some patients with SCA type 3 have bilateral ripheral neuropathy or dorsal root/dorsal column disease
vestibular hypofunction as well. Other patients with is to encourage them to use visual cues while standing and
SCA have normal vestibular function but are not able to walking.
cancel their vestibulo-ocular reflex (VOR) because of a A randomized clinical trial of 42 patients with pure
defect in the cerebellar v ermis; this inability can cause cerebellar degeneration revealed that rehabilitation with
greater motion sensitivity during head movements. physical and occupational therapies can significantly im-
prove functional gains in ataxia, gait, and ADLs. In this
study, the patients were randomized into an immediate
Useful Outcome Scores treatment arm or a delayed-entry control arm. Some level
Patients with PSP and some with P arkinson’s disease of improvement was shown to be maintained for 24 weeks
demonstrate cognitive decline as the disease progresses, after treatment stopped. 20 Case Study 29-4 describes a
so the outcome measures in Table 29-1 become relevant. patient with SCA that improved with rehabilitation.
Phobic postural vertigo 1986, 1994 Subjective imbalance in individuals with obsessive- 26
compulsive personality that have no balance defect
traveling downhill. Some consider this a form of space discussed in the English language in 1994. 26 In the
phobia or visual vertigo.25 neuro-otology clinics, the incidence of this syndrome may
be as high as 17%. It consists of a subjective sense of im-
balance in individuals that have an obsessive-compulsive
Phobic Postural Vertigo
personality but no balance problems. These patients do not
This term was first used in 1986 by German neurologists, show psychogenic signs of a gait disorder .26 Treatment
Drs. Thomas Brandt and Marianne Dieterich, and later has included reassurance, description of the mechanism,
Box 29-1
and repeat exposure with regular exercise. In a 2.5-year Chronic Subjective Dizziness
follow-up, symptoms of dizziness were reduced, but as a
whole there were still significant psychological problems This term was first used in 2007 by Staab and Ruckenstein
requiring psychotherapeutic intervention.27 based on a series of studies of patients in the USA that re-
sembled phobic postural vertigo.32 It consists of unsteadi-
ness or dizziness present for most days for 3 months or
Mal de Débarquement more. Symptoms are most severe when walking or stand-
The term mal de débarquement syndrome (MdDS) w as ing and exacerbated by motion of objects in the visual sur-
initially used and described in the English literature in round or self-motion. Triggering factors may be acute or
1987.28 It consists of the sense of rocking as if on a boat, recurrent problems that cause dizziness or unsteadiness in-
most noticeable when the indi vidual is still. This sensa- cluding (1) peripheral vestibular dysfunction, (2) medical
tion is masked when the indi vidual is moving (e.g., in problems, and (3) psychiatric disorders. Exam and testing
the car). It usually is induced after continuous passi ve are either normal or consist of features that do not explain
transportation for several days (cruise ship). Enhanced ac- the symptoms. These patients have an increased pre va-
tivity in certain limbic areas that may be in volved in vi- lence of psychiatric disorders, usually anxiety or depres-
sual motion has been found on functional MRI of sion, but they also may not sho w these features. Case
individuals with MdDS.29 Study 29-6 describes a patient diagnosed with Chronic
Subjective Dizziness. See also Chapter 19.
Visual Vertigo
Bronstein used this term to describe indi viduals with
Management
peripheral vestibular, central lesions in posterior fossa, or There is no reliable treatment for an y of these chronic,
strabismus that have abnormally high dependence of full situation-related dizziness disorders.
field visual motion.30 As a result, they report dizziness and What is generally suggested is reassurance, increased
show signs of imbalance when e xposed to certain visual activity, and discussion of the problem with the health
situations. Since then, this nomenclature has been used to provider. One can also add cogniti ve behavioral therapy,
include all individualsß including those with migraine or desensitization, and medication including lo w-dose sero-
anxiety that appear to ha ve an “over reliance on visual tonin selective reuptake inhibitors and long-acting benzodi-
cues for perception and postural control. ”31 Case Study azepines. The role of physical therap y is discussed in
29-5 describes a patient diagnosed with visual vertigo. Chapter 19.
Back extension ask to lean backwards (2) Good extensions w'o holding on, staggering
(1) Tries but decreased ROM or holds on
(0) Will not attempt or staggers
Reaching up high (2) Able to take down object w/o holding on or becoming unsteady
(1) Able to reach but needs to hold on
(0) Unable or unsteady
Step length (1) Right foot passes left foot by foot length
(0) Right foot does not pass left by full foot length
(1) Left foot passes right foot by foot length
(0) Left foot does not pass right by full foot length
Average gait speed (ft/sec) (normal) age/gender = 3.08) 2.32 ft/sec 2.20 ft/sec
3970_Ch29_555-568 25/06/14 12:47 PM Page 565
WWT (40 ft) ( ≥18 sec = at risk for falls) 18.24 21.64
8-ft Up & Go Test 22.4 sec with cane 11.4 sec without cane
SOT composite score on computerized 36/72; 6/6 falls 70/72; 1/6 falls
dynamic posturography
CHAPTER 30
Physical Therapy
Management
of People with
Non-vestibular
Dizziness
Lisa Heusel-Gillig, PT, DPT, NCS ■ Courtney D. Hall, PT, PhD
Dizziness is among the most pre valent complaints for After excluding patients who have dizziness caused
which people seek medical help, and the incidence by cardiovascular pathology or medication side effects,
increases with advancing age.1 Dizziness represents a patients with non-vestibular dizziness can be di vided
diagnostic and treatment challenge, because it is a sub- into two major cate gories: those with neurological
jective sensation, refers to a v ariety of symptoms (un- pathology and those without. Individuals with neurolog-
steadiness or imbalance, spinning, sense of motion, or ical involvement include peripheral neuropathy affecting
lightheadedness), and has man y potential contributory large fibers with impaired proprioception or kinesthesia
factors. As many as 45% of indi viduals with dizziness in toes or ankles, cerebellar/brainstem disorders (e.g.,
are diagnosed with peripheral v estibular disorders;2 spinocerebellar ataxia, multiple sclerosis, and strok e),
therefore, the majority of individuals have non-vestibular ischemic white matter disease (leukoaraiosis), and mild
causes for their dizziness and imbalance. Although these head injuries and concussions. (See Chapter 26 for
patients have similar signs and symptoms to those with assessment and management of indi viduals with head
inner ear dysfunction, v estibular function testing does injuries and concussions; see Chapter 29 for medical
not reveal vestibular pathology. It is essential that pa- management of patients with non-vestibular dizziness.)
tients with non-vestibular dizziness and imbalance be Individuals with non-vestibular dizziness without neu-
referred to specialists in v estibular rehabilitation to rological involvement include older adults with disuse
achieve optimal outcomes. Man y assessments that we disequilibrium and/or fear of f alls and indi viduals
recommend, including a thorough oculomotor e xam in with motion sensiti vity caused by migraines and/or
both room light and with fixation removed, are identical anxiety.
to those used to e valuate vestibular patients. Although This chapter identifies components of the physical
they are not commonly performed in inpatient or out - therapy assessment that are the most important as well
patient settings, they provide important information to as outcome measures which are appropriate. Secondly ,
the clinician. There is considerable evidence that vestibu- we discuss therapeutic interv entions for patients with
lar exercises are important in the rehabilitation of pa- non-vestibular dizziness including gait and balance
tients with vestibular pathology.3 There is also evidence training, vestibular rehabilitation including habituation
that vestibular rehabilitation is benef icial for patients and gaze stability exercises, and dual-task activities. We
with non-vestibular dizziness.4-11 suggest recreational activities that are both enjoyable and
569
3970_Ch30_569-589 01/07/14 12:09 PM Page 570
challenging for the patient to continue after discharge to what is meant by the w ord “dizzy.” Many may report
maintain gains achieved with formal physical therap y. being “off balance,” and others may complain that
Each section identif ies specific treatments that ha ve movements cause their head to feel “lightheaded,
been shown to improve balance and mobility, as well as woozy, foggy, fuzzy, full, spacey, cloudy” or e ven ex-
dizziness. Finally, we discuss expected recovery time and press that they are “inside a cotton ball. ” The therapist
factors that may limit functional progress. needs to ask questions such as “Is there something that
makes your symptoms w orse?” “Better?” “Is there a
time in the day when you ha ve no symptoms?” Addi-
Assessment tionally, the therapist should ha ve the patient identify
A comprehensive evaluation is essential to identify the the primary goal for physical therapy.
underlying impairments and functional deficits and de- After discussing the questionnaire and history with
termine the best treatment approach for patients with the patient, reliable and valid outcome measures to assess
non-vestibular dizziness. Our dizziness and balance both symptoms and performance-based balance and mo-
clinic uses a six-page questionnaire (that is mailed to bility should be performed (Table 30-1). Strength, sensa-
each patient before the f irst appointment). This allows tion, and coordination also need to be e valuated, but will
the patient adequate time to record relevant history and not be discussed in this chapter.
describe symptoms that help the clinician prioritize the
evaluation. A questionnaire should include date of onset,
characteristics of symptoms (e.g., acute or chronic,
Therapeutic Interventions
spells or constant), past medical history , medications, Gait and balance training, vestibular rehabilitation includ-
and a scale to assess anxiety and depression. Reviewing ing habituation and gaze stability exercises, and dual-task
physicians’ notes and pre viously performed tests also activities have been shown to improve function, postural
helps the therapist decide which specific assessments to stability, and symptoms in patients with non-v estibular
perform. dizziness. Studies have shown that including these treat-
Taking a good history is the most important part of ment approaches are beneficial to this population and will
the assessment. The patient needs to identify e xactly be discussed in each section below.
Functional Reach25 x
A
Stepping forward with left foot
B
Stepping backward with left foot
Figure 30.1 Many patients with fear of falls have decreased foot clearance and heel strike.
In the “Step-over” exercise, the patient is required to (A) step over an object (rolled towel)
and shift his or her weight forward as if preparatory to taking another step. The patient then
steps backward (B) with the same leg and repeats sequence 10-15 times on each leg.
based on outcomes measures, have fallen at least once in the forces the use of the remaining somatosensory input, but
past year, or have gradually become more cautious and seden- helps the patient use v estibular and visual inputs more
tary. Many individuals report holding onto the walls or furniture effectively.
inside their homes. In the community , the older adults be gin
Exercises for Fall Prevention—Supportive
using a cane plus the support of their spouse or other f amily
Evidence
member, or a rollator walker. A combination of slowed motor
A meta-analysis of f all prevention exercise pro-
responses, impaired sensory input, and decreased strength con-
grams in o ver 9,000 older adults demonstrated
tributes to falls in older adults.27
that a program combining a moderate to high
Balance deficits caused by poor sensory integration
level of challenging balance exercises, including
are common in patients with mild cogniti ve decline, cere-
reduced base of support, controlled movements of
bellar ataxia, and peripheral neuropathy .27,39 To maintain
the center of mass, and minimal upper e xtremity
postural stability, the brain must quickly process inputs
support, as well as an increased dose of e xercise
from the visual, somatosensory, and vestibular systems.28
time (at least 50 hours) had the greatest ef fect
When one or more of these sensory systems fail, imbalance
on fall prevention.40 Modified single-leg stance
and incidence of f alls increase.28 Therefore, balance re-
(Fig. 30.2), an e xercise in which one foot rests
training designed to improve the integration of the three
lightly on a book or cushion while the patient fo-
sensory systems should be included as an interv ention for
cuses straight ahead, progressing to head rota-
non-vestibular dizzy patients. Initial assessments frequently
tions or e yes closed, impro ves the indi vidual’s
show abnormal findings on the modified clinical test for
ability to step up on curbs or over obstacles with-
sensory interaction of balance (mCTSIB) with eyes closed
out support. Exercises that facilitate dynamic pos-
on foam (condition 4) or on conditions 5 and 6 of the SOT
tural reactions are also important to prevent falls.
using computerized dynamic posturography (CDP).
The activities should be safe b ut challenging
Balance training for these individuals should focus
enough to force the patient to use appropriate au-
on increasing the use of the vestibular system by engag-
tomatic balance reactions including ankle, hip,
ing, reducing, or remo ving visual input (e.g., focusing
and stepping strategies. If these strategies are not
on a moving object, using dim lighting, or closing eyes)
automatic or quick enough to be ef fective, they
and reducing somatosensory input (e.g., foam surface).
need to be practiced initially with v oluntary ac-
If Romberg position with e yes closed (condition 2 on
tivities and progressing toward involuntary (or re-
the mCTSIB) is difficult for someone with somatosen-
active) until the patient is able to do them in
sory deficits, the patient should be instructed to “feel
unpredictable situations.
your weight on the balls of your feet” and practice with
feet apart with e yes open and closed and gradually Patients with fear of falls are afraid to shift volun-
narrow the base of support. This intervention not only tarily near their limits of stability as determined by
Figure 30.2 Certain activities while walking can require that the patient stand on one
foot for brief periods of time without loss of balance. In the “modified single-legged
stance” exercise, patients place one foot lightly on a book, or foam or cup, and maintain
their balance for a specified period of time. Variations include performing slow head
turns with eyes open, or keeping the head stationary and closing the eyes as well as
performing cognitive tasks.
3970_Ch30_569-589 01/07/14 12:09 PM Page 574
the functional reach test or limits of stability on CDP . stance, unpredictable perturbations by the thera-
From our e xperience, these patients respond well pist in all directions, and whole-body movements
to practicing automatic acti vities including passing to train trunk and limb coordination. Study results
a ball, tapping a balloon, or performing weight shifts demonstrated that static balance on both firm and
using visual feedback (e.g., Equitest or Wii System; compliant surfaces improved.8 Many individuals
Fig. 30.3). with ataxia cannot stand on one foot; therefore,
Ataxia, Falls, and Fear of Falling they are prescribed a modif ied single-leg stance
For individuals with ataxia, falls are a major prob- (mod SLS) exercise (see Fig. 30.2) to gradually
lem: in one retrospecti ve study, 93% reported improve stability.
falling in the previous year.41 In addition, patients Migraineurs with motion sensitivity are often visually
with ataxia report higher le vels of fear of f alling dependent and sway more than normal when e xposed to
than healthy controls (43% compared with 2%).41 visually stimulating environments.42 This group of patients
Fortunately, patients with truncal and limb ataxia should practice static balance on compliant surf aces
can benefit from balance retraining.8 In a random- with eyes closed forcing them to use their v estibular and
ized controlled trial, subjects with de generative somatosensory inputs. Pavlou and colleagues 15 demon-
cerebellar ataxia who underwent an intensi ve strated that a group of subjects with motion sensiti vity
coordination training program that focused on who performed customized vestibular rehabilitation (gaze
balance improved static and dynamic balance stability and dynamic balance acti vities) plus simulator
and maintained gains with a prescribed home pro- training (involving videos of optokinetic stimulus) im-
gram at 8-week follo w-up testing.8 Static and proved to a greater e xtent on both postural stability and
dynamic balance e xercises included single-le g visual vertigo as determined by SOT and Situational Ver-
tigo Questionnaire (SVQ; Appendix 30-1) than the group
that performed customized v estibular training without
simulator training. These findings suggest that the use
of optokinetic stimulation is benef icial for this group of
patients with motion sensitivity.
Habituation Exercises
Many individuals become dizzy and imbalanced with
self-movement and others experience discomfort, imbal-
ance, and disorientation in stimulating (visual) environ-
ments, often described as a visual-vestibular mismatch,43
visual vertigo,44,45 or space and motion discomfort. 46
Patients with a new onset or exacerbation of motion sen-
sitivity with either self or environmental stimulation re-
spond well to habituation e xercises. With repeated
exposure to the provoking stimulus, the central nervous
system habituates so that tolerance of motion improves.9
Initially, intensity of symptoms may increase with these
exercises but decrease over time with repetition. Persons
with oculomotor def icits because of neurological in-
volvement and migraineurs frequently experience motion
sensitivity.6,47,48
Motion-provoked dizziness should be assessed with
valid and reliable measures (see Table 30-1). Suggested
scales include Motion Sensitivity Quotient (MSQ),9 Dizzi-
ness Handicap In ventory (DHI),13 Situational Vertigo
Questionnaire (SVQ),15 and Visual Vertigo Analog Scale
Figure 30.3 Wii Practice: patients with difficulty shifting
weight or who have a fear of falls can benefit from partici- (VVAS).16
pating in activities that allow them to have fun and focus These assessments help determine appropriate
on visual feedback to help them improve balance. exercises for the home e xercise program. The MSQ
3970_Ch30_569-589 01/07/14 12:09 PM Page 575
determines the specific movements that cause the symp- is prescribed a specif ic number of repetitions and sets
toms to increase. This 16-item scale includes mo ve- depending on his symptoms. Duration of the response
ments including rolling, bending o ver to right and should last less than 30 seconds per set, and the patient
left knees, horizontal and v ertical head rotations, and should return to baseline within 15 to 20 minutes of doing
180-degree turns in standing (see Chapter 21). The SVQ all the exercises in the session. Habituation e xercises are
and VVAS help the therapist pinpoint environments and customized to address the specific provoking stimulus of
situations that provoke symptoms that can be simulated each patient, and the patient is educated that the mo ve-
in therapy and home exercise program (HEP) to reduce ments need to be performed f ast enough to pro voke the
symptoms of visual v ertigo (see Appendices 30-1 and symptoms to ultimately reduce the dizziness. The therapist
30-2). The SVQ and VVAS include items such as walk- should start conservatively, so that the patient can carry
ing through a supermarket, watching a movie or action out his or her daily acti vities. The exercises need to be
TV, walking on patterned floors, and going on escala- done with eyes open and at a speed that provokes mild to
tors. If the patient is sensitive to self-movements based moderate symptoms. Rest breaks between each set allow
on MSQ, up to 4 mo vements are chosen depending on for the symptoms to return to baseline, and ideally , the
the severity of symptoms (Table 30-2). symptoms after subsequent sets should be less than the
Exercises should not pro voke more than a mild to first set. If headaches or nausea occur , exercises should
moderate intensity for each repetition or set. Each patient be modified (Appendix 30-3).
1. Sitting to supine
4. Supine to sitting
5. Left Hallpike-Dix
7. Right Hallpike-Dix
*MSQ = {(Total score) × (# of positions with symptoms)} + 20.48 MSQ score 0–10 = mild; 11–30 = moderate;
31–100 = severe. Duration: 5–10 sec = 1 point; 11–30 sec = 2 points; greater than 30 sec = 3 points.
3970_Ch30_569-589 01/07/14 12:09 PM Page 576
If the patient is sensitive to stimulating environments tunnels, and panoramic views while the patient’s
as determined by the DHI, SVQ, or VVAS, the therapist postural sway is measured on a platform. Lo w-
can systematically introduce situations that pro voke the tech methods that ha ve been used include disco
symptoms. balls, twirling umbrellas, mo ving stripes or b usy
Visual Vertigo and Habituation Exercises tablecloths on the wall, and action videos (Fig. 30.5).
Visual vertigo has been sho wn to respond to Therapists can either pro vide a list of appropriate
habituation exercises using a similar paradigm to videos from YouTube (Appendix 30-4) or design a
habituation of self-movements.15 Habituation of customized program of videos of appropriate levels
visual vertigo involves brief doses of visual stim- of difficulty.
ulation for a specif ic amount of time to pro voke Patients with migraines may be sensitive to both
mild to moderate symptoms (e.g., 1 minute of an self-motion and movements in the environment. These
action video), followed by a rest period to allo w individuals need to be gin their HEP at a slo w pace so
the individual to return to baseline before intro- that the movements do not provoke headaches or nausea.
ducing another epoch of visual stimulation. Walking short distances outdoors or balance training
Patients can also begin viewing a small screen and with slow head movements may be all that can be toler-
progress to a larger screen. Pavlou suggested that ated initially. Migraineurs need to be educated that
optokinetic stimulation is beneficial but needs to habituation exercises should not be performed during
be gradual, progressive, and structured.15 Sugges- migraine spells. Habituation e xercises, in addition to
tions for interventions include high- and low-tech medical management for migraines and stress reduction,
options. If the clinic has a CDP, the therapist can are essential to optimal outcomes (see Chapter 15).
use it for training by gradually changing the pa- Many patients with cerebellar degeneration experi-
rameters of the surround mo vements (Fig. 30.4). ence dizziness as a result of oculomotor impairments
Other high-tech systems include virtual reality including abnormal smooth pursuit, VOR cancellation
systems such as the “grocery store”49 and Balance deficits, and gaze-evoked nystagmus.31,50 When these
Rehabilitation Unit (BRU) system.42 The grocery individuals turn their heads, the en vironment may be-
store model consists of a simulation of w alking come distorted, causing dizziness, imbalance, and un-
through an aisle of a supermark et searching for steady gait.31 Habituation exercises including head turns
specific items. During assessment and intervention while scanning the en vironment can decrease motion
on the BRU system, the patient wears goggles and
watches virtual scenes with mo ving objects,
sensitivity.33,51 These patients can be trained to f ind the acuity (DVA) and functional mobility.6,11 However, few
“null” position of the eyes where nystagmus is the least, studies have looked at the use of gaze stability e xercises
as well as to turn their head and eyes at the same time to for patients without neurological pathology.
look peripherally while preventing gaze-evoked nystag-
Gaze Stabilization and Non-vestibular
mus. Following a target with head and eyes together hor-
Dizziness—Supportive Evidence
izontally at a speed at which the target remains in focus
In a randomized controlled pilot study of older
(simulating the VOR cancellation testing) can be used as
adults with non-vestibular dizziness (i.e., normal
a habituation e xercise to decrease dizziness. 11 Cohen
vestibular function based on clinical e xam and
demonstrated that patients’ gait improved by focusing
caloric testing), subjects in the gaze stability
the intervention on balance exercises and habituation ex-
group (n = 20) performed vestibular gaze stability
ercises to reduce dizziness.52
exercises, and subjects in the placebo group (n = 17)
Based on our experience, habituation exercises can
performed placebo e ye exercises (saccadic e ye
also help older adults with disuse disequilibrium, white
movement against a plain background). 7 Both
matter disease, or a history of BPPV who are hesitant to
groups performed gait and balance e xercises
look upward or bend o ver for fear of pro voking dizzi-
based on impairments identified at initial evalua-
ness. When this behavior is observed during initial as-
tion. Both groups improved on measures of symp-
sessment, the therapist needs to include habituation
toms, balance confidence, gait speed, and sensory
exercises with head and body mo vements in the home
integration. The only significant interaction (p = 0.026)
exercise program.
was for f all risk as measured by dynamic gait
We inform patients with motion sensitivity that they
index (DGI) with 90% of the gaze stability group
may experience more symptoms with the HEP the f irst
demonstrating clinically significant improvement
week, because they are doing movements that they have
in DGI scores versus 50% of the placebo group.
been avoiding. Smith-Wheelock suggested that habitua-
These studies suggest that incorporating vestibu-
tion exercises should be performed only 2 times a day
lar gaze stability e xercises in the rehabilitation
initially to avoid overloading the compensatory system
of individuals with non-v estibular dizziness is
and make symptoms worse.9 Subjective and objective
beneficial.
outcome measures should be repeated in 1 month be-
cause motion sensitivity has been shown to significantly
Dual-Task Training
improve within 4 to 6 weeks of initiation of habituation
exercises.51 Smith-Wheelock suggested that a decrease Many patients with non-v estibular dizziness, especially
in sensitivity and duration of symptoms can occur as older adults, have difficulty walking while performing sec-
quickly as 2 weeks, but may take as long as 6 months. 9 ondary tasks.53 Woollacott and Shumway-Cook suggest that
In our experience, patients who may not respond to ha- the problem with dual-task ability in older adults can be the
bituation exercises include those individuals who expe- result of inability to shift attention, a reduction in attentional
rience constant vague symptoms of dizziness that do not capacity, impairments in the postural control system, or a
change with self or environmental movement. Individu- combination of these factors.53 In fact, an impaired ability
als who do not adhere to the prescribed HEP or have psy- to allocate attentional resources to balance during dual-task
chological causes for their dizziness that ha ve not been situations is a powerful predictor of falls.20 Outcome mea-
addressed may also not impro ve. For habituation exer- sures such as the modif ied Timed Up and Go (mTUG) or
cises to be the most effective, the therapist needs to per- Walk While Talk (WWT) test can be used to identify diffi-
form a thorough e valuation, design an indi vidualized culty walking and dividing attention (see Table 30-1).
treatment plan based on the findings, and educate the pa-
Single-Task to Dual-Task Balance Training—
tient of the purpose of the intervention. When there is no
Supportive Evidence
improvement or symptoms worsen even with modifica-
Few studies have compared single-task to dual-
tions, the patient should discontinue the exercises and re-
task balance training. One such study demon-
turn to the referring physician.
strated that only participants trained under dual-
task conditions sho wed improvements for gait
Gaze Stabilization Exercises speed tested under dual-task conditions.54 In con-
trast, a retrospective study demonstrated that stan-
Two studies have evaluated the use of vestibular gaze sta-
dard balance rehabilitation with no specif ic
bility exercises for patients with neurological (cerebellar)
dual-task training improved gait under dual-task
involvement and have shown improved dynamic visual
3970_Ch30_569-589 01/07/14 12:09 PM Page 578
individuals who live alone may not be able to 3. Absence of neurological pathology. Older
do the challenging balance exercises safely, patients with disuse disequilibrium or fear of
may be fearful of doing the exercises alone, or fall without neurological pathology typically
may not be disciplined enough to do them can decrease fall risk and reach goals within
alone. Also, patients who are themselves care- 1 month of weekly visits (average of 3.7 visits7).
givers for spouses or parents often do not take Those with cerebellar ataxia8 and central
the time needed to perform the home program vestibular6 require more visits to reach goals
as prescribed. (range: 5 to 12 visits).
ABC (%) 54 90
Gait speed (m/sec) 0.72 m/sec (abnl ≤ 1.09 m/sec) 1.25 m/sec
ABC (%) 32 58
Disability 3/5 (symptoms interfere with both usual and 1/5 (symptoms are bothersome)
outside activities)
ABC (%) 56 92
4. Perlman SL. Symptomatic and disease-modifying therapy 24. Anacker SL, Di Fabio RP. Influence of sensory inputs on
for the progressive ataxias. Neurologist. 2004;10:275. standing balance in community-dwelling elders with a
5. Badke MB, Shea TA, Miedaner JA, Grove CR. Outcomes recent history of falling. Phys Ther. 1992;72:575.
after rehabilitation for adults with balance dysfunction. 25. Duncan PW, Weiner DK, Chandler J, Studenski S.
Arch Phys Med Rehabil. 2004;85:227. Functional reach: a new clinical measure of balance.
6. Brown KE, Whitney SL, Marchetti GF, Wrisley DM, J Gerontol. 1990;45:M192.
Furman JM. Physical therapy for central vestibular 26. Bootsma-van der Wiel A, Gussekloo J, De Craen AJ,
dysfunction. Arch Phys Med Rehabil. 2006;87:76. Van Exel E, Bloem BR, et al. Common chronic diseases
7. Hall CD, Heusel-Gillig L, Tusa RJ, Herdman SJ. Efficacy and general impairments as determinants of walking
of gaze stability exercises in older adults with dizziness. disability in the oldest-old population. J Am Geriatr Soc.
J Neurol Phys Ther. 2010;34:64 2002;50:1405.
8. Ilg W, Synofzik M, Brötz D, Burkard S, Giese MA, et al. 27. Baloh RW Yue Q, Socotch TM, Jacobson KM. White mat-
Intensive coordinative training improves motor perfor- ter lesions and disequilibrium in older people. Case con-
mance in degenerative cerebellar disease. Neurology. 2009; trol comparison. Arch Neurol. 1995;52:970.
73:1823. 28. Kerber KA, Enrietto JA, Jacobson KM, Baloh RW. Dise-
9. Smith-Wheelock M, Shepard NT, Telian SA. Physical quilibrium in older people: a prospective study. Neurology.
therapy program for vestibular rehabilitation. Am J Otol- 1998:51;574.
ogy. 1991;12:218. 29. Baezner H, Blahak C, Poggesi A, Pantoni L, Inzitari D,
10. Martin CL. Effectiveness of physiotherapy for adults with et al. Association of gait and balance disorders with
cerebellar dysfunction: a systematic review Clin Rehabil. age related white matter changes. The LADIS study.
2009;23:15. Neurology. 2008;70:935.
11. Gill-Body KM, Popat RA, Parker SW, Krebs DE. Rehabil- 30. Norton R, Campbell AJ, Lee-Joe T, Robinson E, Butler M.
itation of balance in two patients with cerebellar dysfunc- Circumstances of falls resulting in hip fractures among
tion. Phys Ther. 1997;77:534. older people. J Am Geriatr Soc. 1997;45:1108.
12. Powell LE, Myers AM. The Activities-Specific Balance 31. Gilan S, Bloedel JR, Lechtenberg R. In: Disorders of the
Confidence (ABC) scale. J Gerontology: Medical Science. Cerebellum. Philadelphia, Pa: FA Davis; 1981:189-215,243.
1995;50:M28. 32. Leigh RJ, Zee DS. In: The Neurology of Eye Movements.
13. Jacobson GP, Newman CW. The development of the 3rd ed. New York NY: Oxford University Press; 1981:189.
Dizziness Handicap Index. Arch Otolaryngol Head Neck 33. Shepard NT, Smith-Wheelock M, Telian SA, Raj A.
Surg. 1990;16:424. Vestibular and balance rehabilitation therapy. Ann Otol
14. Hall CD, Herdman SJ. Reliability of clinical measures Rhinol Laryngol. 1993;102:198.
used to assess patients with peripheral vestibular 34. Nutt JG, Marsden CD, Thompson PD. Human walking
disorders. J Neurol Phys Ther. 2006;30:74. and higher level gait disorders, particularly in the elderly.
15. Pavlou M, Lingeswaran A, Davies R, Gresty MA, Neurology. 1993;43:268.
Bronstein AM. Simulator based rehabilitation in 35. Hornbrook MC, Stevens VJ, Wingfield DJ, Hollis JF,
refractory dizziness. J Neurol. 2004;251:983 Greenlick MR, et al. Preventing falls among community-
16. Dannenbaum E, Chilingaryana G, Fung J. Visual Vertigo dwelling older persons: Results from a randomized trial.
Analogue Scale: an assessment questionnaire for visual Gerontologist. 1994;34:16.
vertigo. J Vestib Res. 2011;21:153. 36. O’Loughlin JL, Robitaille Y, Boivin J, Suissa S. Incidence
17. Bohannon RW. Comfortable and maximum walking speed of and risk factors for falls and injurious falls among the
of adults aged 20–79 years: reference values and determi- community-dwelling elderly. Am J Epidem. 1993;137:342.
nants. Age Ageing. 1997;26:15. 37. Downton JH, Andrews K. Prevalence, characteristics and
18. Shumway-Cook A, Baldwin M, Polissar NL, Gruber W. factors associated with falls among the elderly living at
Predicting the probability for falls in community-dwelling home. Aging (Milano). 1991;3:219.
older adults. Phys Ther. 1997;77:812. 38. Hausdorff JM, Rios DA, Edelber HK. Gait variability
19. Shumway-Cook, A, Brauer S, Woollacott, M. Predicting and fall risk in community-living older adults: a 1-year
the probability for falls in community-dwelling older adults prospective study. Arch Phys Med Rehab. 2001;82:1050.
using the timed up and go test. Phys Ther. 2000;80:896 39. Baloh RW, Jenkins HA, Honrubia V, Yee RD, Lau CG.
20. Verghese J, Buschke H, Viola L, Katz M, Hall C, et al. Visual-vestibular interaction and cerebellar atrophy.
Validity of divided attention tasks in predicting falls in Neurology. 1979;29:116.
older individuals: a preliminary study. J Am Geriatr Soc. 40. Sherrington C, Whitney JC, Lord SR, Herbert RD, Cum-
2002;50:1572. ming RG. Effective exercise for the prevention of falls: a
21. Tinetti ME. Performance oriented assessment of mobility systematic review and meta-analysis. J Am Geriatri Soc.
problems in elderly patients. J Am Geriatr Soc. 1986;34:119. 2008;56:2234.
22. Lord SR, Murray SM, Chapman K, Munro B, 41. Van de Warrenburg BPC, Steijns JA, Munneke M, Kremer
Tiedemann A. Sit-to-stand performance depends on BP, Bloem BR. Falls in degenerative cerebellar ataxias.
sensation, speed, balance, and psychological status in Mov Disord. 2005;20:497.
addition to strength in older people. J Gerontol A Biol 42. Suarez H, Suarez A, Lavinsky L. Postural adaptation in
Sci Med Sci. 2002;57:M539. elderly patients with instability and risk of falling using a
23. Ford-Smith CD, Wyman JF, Elswick RK, Fernandez T, virtual-reality system. Int Tinnitus J. 2006;12:41.
Newton RA. Test-retest reliability of the sensory organiza- 43. Longridge NS, Mallinson AI, Denton A. Visual Vestibular
tion test in noninstitutionalized older adults. Arch Phys mismatch in patients treated with intratympanic gentam-
Med Rehab. 1995;76:77. icin for Meniere’s disease. J Otolaryngol. 2002;31:58.
3970_Ch30_569-589 01/07/14 12:09 PM Page 583
44. Bronstein AM. Visual Vertigo syndrome: clinical and 56. Earhart GM. Dance as therapy for individuals with
posturography findings. J Neurol Neurosurg Psychiatry. Parkinson’s disease. Eur J Phys Med Rehab. 2009;
1995;59:472. 45:231.
45. Guerraz M, Yardley L, Bertholon P, Pollak L, Rudge P, 57. Simmons V, Hanson PD. Effectiveness of water exercise
et al. Visual vertigo: symptom assessment, spatial on postural mobility in the well elderly: an experimental
orientation and postural control. Brain. 2001;124:1646. study on balance enhancement. J Gerontol. 1996;51A:
46. Jacob RG, Redfern MS, Furman JM. Space and motion M233.
discomfort and abnormal balance control in patients with 58. Young W, Ferguson S, Brault S, Craig C. Assessing and
anxiety disorders. J Neurol Neurosurg Psychiatry. training standing balance in older adults: A novel ap-
2009;80:74. proach using the ‘Nintendo Wii’ Balance Board. Gait
47. Whitney SL, Wrisley DM, Brown KE, Furman JM. Posture. 2011;33:303.
Physical therapy for migraine-related vestibulopathy 59. Wolfson L, Whipple R, Derby C, Judge J, King M, et al.
and vestibular dysfunction with a history of migraine. Balance and strength training in older adults: intervention
Laryngoscope. 2000;110:1528. gains and tai chi maintenance. J Am Geriatr Soc. 1996;
48. Waterston J. Chronic migrainous vertigo. J Clin Neurosci. 44:498.
2004;11:384. 60. Gatts SK, Woollacott M. How tai chi improves balance:
49. Sparto PJ, Whitney SL, Hodges LF, Furman JM, Redfern biomechanics of recovery to a walking slip in impaired
MS. Simulator sickness when performing gaze shifts seniors. Gait Posture. 2007;25:205.
within a wide field of view optic flow environment: pre- 61. Lin M, Hwang H, Wang Y, Chang S, Wolf SL. Community-
liminary evidence for using virtual reality in vestibular based Tai Chi and its effect on injurious falls, balance,
rehabilitation. J Neuroeng Rehabil. 2004;1:14. gait, and fear of falling in older people. Phys Ther. 2006;
50. Kheradmand A, Zee DS. Cerebellum and ocular motor 86:1189.
control. Front Neurol. 2011;2:1. 62. Oken BS, Zajdel D, Kishiyama S, Flegal K, Dehen C,
51. Telian SA, Shepard NT. Update on vestibular rehabilita- et al. Randomized, controlled, six- month trial of yoga in
tion therapy. Otolaryngol Clin North Am. 1996;29:359. healthy seniors: effects on cognition and quality of life.
52. Cohen H, Kimball KT. Decreased ataxia and improved Altern Ther Health Med. 2006;12:40.
balance after vestibular rehabilitation. Otolaryngol Head 63. Smith K, Smith E. Integrating Pilates-based core strength-
Neck Surg. 2004;130:418. ening into older adult fitness programs: implications for
53. Woollacott M, Shumway-Cook A. Attention and the con- practice. Topics Geriatr Rehabil. 2005;21:57.
trol of posture and gait: a review of an emerging area of 64. Cass SP, Borello-France D, Furman JM. Functional
research. Gait Posture. 2002;16:1. outcomes of vestibular rehabilitation in patients with ab-
54. Silsupadol P, Ka-Chun Siu, Shumway-Cook A, Woollacott normal sensory-organization testing. Am J Otol. 1996;
M. Training of balance under single and dual-task condi- 17:581.
tions in older adults with balance impairment. Phys Ther. 65. Mohler PJ. Enhancing compliance with screening mam-
2006;86:269. mography recommendations: a clinical trial in a primary
55. Hall CD, Heusel-Gillig L. Balance rehabilitation and care office. Fam Med. 1995;27:117.
dual-task ability in older adults. J Clin Geriatr Gerontol.
2010;1:22.
3970_Ch30_569-589 01/07/14 12:09 PM Page 584
APPENDIX 30-1
Situational Vertigo
Questionnaire
Situational Vertigo Questionnaire Please circle a number to indicate the degree to which each
of the situations listed below causes feelings of vertigo, or
Vertigo is the medical term used for symptoms which pa- makes your vertigo worse. If you have never been in one
tients often describe as feelings of unusual disorientation, of the situations, then for that item ring “N.T .” for “Not
dizziness, giddiness, lightheadedness, or unsteadiness. Tried.”
(Pavlou, 2004)15
*A lift is an elevator.
584
3970_Ch30_569-589 01/07/14 12:09 PM Page 585
APPENDIX 30-2
Visual Vertigo Analog
Scale
Indicate the amount of dizziness you experience in the following situations by marking off the scales below.
0 represents no dizziness, and 10 represents the most dizziness.
Walking through a supermarket aisle
____________________________________________________________________
0 10
Being a passenger in a car
____________________________________________________________________
0 10
Being under fluorescent lights
____________________________________________________________________
0 10
Watching traffic at a busy intersection
____________________________________________________________________
0 10
Walking through a shopping mall
____________________________________________________________________
0 10
Going down an escalator
____________________________________________________________________
0 10
Watching a movie at the movie theatre
____________________________________________________________________
0 10
Walking over a patterned floor
____________________________________________________________________
0 10
Watching action television
____________________________________________________________________
0 10
586
3970_Ch30_569-589 01/07/14 12:09 PM Page 587
APPENDIX 30-3
Sample Home Exercise
Program
These sample home programs are for a patient with motion sensitivity.
HABITUATION EXERCISES Do ______daily
1. In a sitting position:
_______Bend over and sit up ___________times in a row
_______Wait until symptoms resolve and repeat one more set of ______
2. In a sitting position:
_______Turn head side to side __________times in a row
_______Wait until symptoms resolve and repeat one more set of ______
3. In a sitting position:
_______Move head up and down ________times in a row
_______Wait until symptoms resolve and repeat one more set of ______
4. Stand in a corner:
_______ Turn a FULL 1/2 turn to the right ______times,
waiting for symptoms to resolve each time
_______Turn a FULL 1/2 turn to the left ________times,
waiting for symptoms to resolve each time
5. Practice walking in hallway ______times
_____Move head side to side slowly, focusing on the walls each time
_____Move head up and down slowly, focusing on the ceiling and floor each time
_____Move head diagonally slowly, crossing in the center each time
6. Practice tossing a ball hand to hand following it with head and eyes ___________
7. Practice handing ball to a person behind you to right and left while walking.
Make sure you rotate your head and body and watch the ball with your eyes
8. Practice rolling in bed
_____roll to the right______ times, wait for symptoms to resolve
_____roll to the left________ times, wait for symptoms to resolve
9. Other_______________________________________________
587
3970_Ch30_569-589 01/07/14 12:09 PM Page 588
APPENDIX 30-4
Suggested Videos to Use
in Clinic and Home Program
This sample program is for patients with visual vertigo Walk through Harry Potter World: 3:11
based on VVAS or SVQ. These videos will make you http://www.youtube.com/watch?v=-434p3l-2EA
dizzy and uncomfortable—make sure your symptoms
Trail Running (start at 1:00 mark; some pauses
are only mild when you watch these videos. Start with
built in) 7:16
the less-stimulating videos first for only 30 seconds or
less, let the symptoms return to baseline before watch- http://www.youtube.com/watch?v=ENj2yXDMGng
ing another 30 seconds or less. Build up from there. Skiing down mountain in Italy: 12:58
Everyone is different, so do not expose yourself for http://www.youtube.com/watch?v=fPZNahPtUD4
too long or it will not be beneficial. Do only as pre-
Driving: I-95 New Jersey & Henry Hudson Pkwy
scribed by your PT. Sessions should last no more than
New York City 5:31
10 minutes with symptoms resolving within 20 minutes
after stopping. If the symptoms provoked are moderate http://www.youtube.com/watch?v=-eQHl9T0W8U&
to severe, do not continue. feature=related
Driving: Fort Pitt Tunnel Pittsburgh Pa 1:40
EASY http://www.youtube.com/watch?v=C-Ui0gxYVCg&
Driving in Manhattan New York: 5:10 feature=related
http://www.youtube.com/watch?v=Lv0OgDmwC3 A stroll through the casino at the Monte Carlo hotel
Q&feature=related in Las Vegas 4:33
Cruising Lake Erie via Motorcycle 3:06 http://www.youtube.com/watch?v=AHt_iTuzQNY
http://www.youtube.com/watch?v=h2Jz6IdS-iM& Women’s Hockey Practice 3:53
feature=related http://www.youtube.com/watch?v=ZXX
An evening stroll in the Paris Opera quarter 22:33 wIiHdrQs
http://www.youtube.com/watch?v=i6bDAWqf2RY Men’s hockey w/ helmet cam 7:40
&feature=related http://www.youtube.com/watch?v=DqjNyy-ONCU&
Ice Skating in High Sierra 6:11 feature=related
http://www.youtube.com/watch?v=-EG7kLjpzsM
DIFFICULT
Rue Saint Severin and Rue de la Harpe 4:50
Walking through lobby of Venetian hotel Las Vegas
http://www.youtube.com/watch?v=PD_RikPVmyY
0:54
&feature=related
http://www.youtube.com/watch?v=4imxlc1xEO0&
MEDIUM feature=related
An Afternoon Stroll through the Latin Quarter: 14:54 Walking through Winn Dixie (grocery store): 6:53
http://www.youtube.com/watch?v=csJupEA1lCI http://www.youtube.com/watch?v=2ojMWHCJKhc
Just Walking Down The Street In Akihabara Japan:
4:40
http://www.youtube.com/watch?v=5tl-mo2Ob0o
588
3970_Ch30_569-589 01/07/14 12:09 PM Page 589
A walk through Times Square: 6:52 Walking through: New Cosmopolitan Casino Hotel
http://www.youtube.com/watch?v=5nRVIPyHGR8 Las Vegas 7:24
Maui: The Road to Hana Timelapse 7:19 http://www.youtube.com/watch?v=NsI0vSPKBxs&
feature=related
http://www.youtube.com/watch?v=5ER2K-
ERLlk&feature=fvwrel
3970_Ch31_590-609 25/06/14 5:39 PM Page 590
CHAPTER 31
Physical Therapy
Management of
Cervicogenic
Dizziness
Richard A. Clendaniel, PT, PhD ■
Rob Landel, PT, DPT, OCS, CSCS, FAPTA
Cervicogenic dizziness is a contro versial subject at best. the anatomical and physiological bases for cervicogenic
The term tends to be used to describe a v ariety of entities, dizziness, to summarize the scientif ic findings related to
some of which are theoretically more likely than others, in- cervicogenic dizziness, to address the clinical methods of
cluding cervical ataxia, cervical n ystagmus, and cervical assessing cervicogenic dizziness, and to discuss possible
vertigo. Because vertigo is defined as the illusion of move- management strategies for this condition.
ment (rotation, tilt, or linear displacement) and is therefore
restrictive, the term cervicogenic dizziness, rather than the Proposed Etiologies
older term “cervical vertigo,” is used in this chapter to refer
to symptoms of dizziness (including vertigo, disequilibrium, Posterior Cervical Sympathetic
and lightheadedness) arising from the cervical spine. Syndrome
Several different processes have been hypothesized Barré1 suggested that cervical problems could irritate the
to be the cause of cervicogenic dizziness. These patho- sympathetic vertebral plexus, leading to constriction of
physiological mechanisms include irritation of the sym- the internal auditory artery and decreased perfusion of
pathetic vertebral plexus, vertebrobasilar insufficiency the labyrinth, which would induce vertigo. There is little
(VBI), and altered proprioceptive afferent signals from the objective evidence, however, to support this hypothesis.
upper cervical spine. This latter potential cause of dizzi- In addition, the intracranial circulation is controlled in-
ness is of particular interest because of the lar ge number dependently of the cervical sympathetic system. There-
of patients with either whiplash injuries or neck pain that fore, it is difficult to see how a cervical injury could lead
are seen by physical therapists. This particular cause of to restricted blood flow to the inner ear.
dizziness is also perhaps the most controversial.
One of the major problems in identifying patients
Vertebrobasilar Insufficiency
with cervicogenic dizziness is the lack of a concrete test
that is sensitive and specific to this entity. From a thera- Another possible cause of dizziness arising from the
peutic standpoint, however, the controversy surrounding cervical spine is occlusion of the v ertebral arteries by
cervicogenic dizziness may be academic. If an individual osteoarthritic spurs2 or occipitoatlantal instability.3 VBI
presents with cervical symptoms and dizziness, the holis- and vertebrobasilar ischemia can arise from a v ariety of
tic approach would be to treat the cervical problem as well causes, including embolism, large artery atherosclerosis,
as the dizziness. The aim of this chapter is to re view small artery disease, and arterial dissection, and can occur
590
3970_Ch31_590-609 25/06/14 5:39 PM Page 591
at numerous sites along the course of the v ertebral Given the typical mixed signs and symptoms of VBI,
and basilar arteries. 4 There are two sites where physical the presence of episodic, isolated bouts of v ertigo in the
occlusion, or in the e xtreme, dissection of the v ertebral absence of associated symptoms for more than 3 weeks is
artery can occur. One is in the upper cervical spine, after believed to be rarely caused by vertebrobasilar disease.9 In
the vertebral artery e xits the transv erse foramen and addition, drop attacks, which have been attributed to tran-
courses around the mobile upper cervical v ertebrae. The sient ischemia of the posterior circulation, were never found
other potential site for occlusion is in the initial se gment in isolation in the New England Medical Center–Posterior
of the vertebral artery before it enters the transverse fora- Circulation Registry cases.4,11 In summary, although it
men.5 In theory, the vertebral arteries can be compressed is unlikely that dizziness as the sole symptom arises from
during cervical rotation or e xtension, as occurs when a vertebrobasilar ischemia, the possibility of VBI should at
person reaches for an object on an o verhead shelf, turns least be considered on the basis of the patient’s history and
the head while backing up a vehicle, or undergoes cervical symptoms. Clinical tests for VBI, and their usefulness, are
spine manipulations. In normal individuals, the carotid ar- described in detail later in this chapter.
teries provide sufficient collateral circulation to pre vent
symptoms.6 In individuals with atherosclerotic vascular
disease, the cerebrovascular circulation may be compro-
Altered Proprioceptive Signals
mised to the e xtent that compression of the v ertebral The mechanism by which cervical pain or dysfunction
arteries could lead to VBI. could lead to symptoms of dizziness has not been identi-
Although there is an anatomical substrate that could fied. One hypothesis is that inflammation or irritation of
link cervicogenic dizziness with VBI, it is not clear that the the cervical roots or facet joints would lead to a mismatch
symptoms of VBI match those of cervicogenic dizziness. among vestibular, visual, and cervical inputs. This multi-
The symptoms associated with VBI can be quite di verse. sensory mismatch would lead to the symptoms attributed
In a study of 65 patients diagnosed withVBI, Williams and to cervicogenic dizziness, and the symptoms w ould be
Wilson7 found that vertigo was the initial symptom in 48% most apparent during head mo vements (Fig. 31.1). In
of the cases. Vertigo caused by VBI is generally abrupt in theory, once the central nervous system (CNS) has adapted
onset, is of short duration (se veral minutes), and may be
associated with nausea and vomiting.8 These symptoms are
similar to those of someone with a v estibular deficit, but
the vertigo in patients with VBI is generally associated with
other symptoms related to ischemia of areas supplied by
the posterior circulation—typically including visual hallu-
cinations, loss of vision, ataxia, drop attacks, numbness or
weakness affecting both sides of the body, visceral sensa-
tions, visual field defects, diplopia, and headaches.7,9
Vertigo may be an isolated initial symptom but is typ-
ically intermixed with the other symptoms of VBI.10 Of
the more than 400 patients with vertebrobasilar ischemia
whose data are entered in the Ne w England Medical
Center–Posterior Circulation Re gistry, fewer than 1%
presented with a single sign or symptom, and the initial
symptom was not necessarily vertigo or dizziness.4,11 In-
dividuals with v ertebrobasilar ischemia secondary to
stenosis or occlusion of the vertebral arteries typically ex-
perience transient ischemic attacks (TIAs) with symptoms
of dizziness, impaired vision, and loss of balance, which Figure 31.1 Schematic diagram of the multisensory
are consistent with ischemia in the v estibulocerebellum mismatch hypothesis. Peripheral inputs (vestibular, cervical,
and medulla.12 In cases of dissection of the v ertebral ar- and visual) converge on central vestibular structures and
tery, the primary symptom is posterior cervical pain that affect oculomotor function, balance function, vestibulo-
may radiate to the shoulder re gion. In addition, these in- ocular reflex (VOR), and perceptions of dizziness. Cervical
dysfunction (represented by the curved line) would lead to
dividuals typically experience occipital headaches, dizzi- a mismatch among vestibular, visual, and cervical inputs.
ness, diplopia, and lateral medullary and cerebellar signs This multisensory mismatch would lead to the symptoms
including unsteadiness and ataxia.5,13,14 attributed to cervical dizziness.
3970_Ch31_590-609 25/06/14 5:39 PM Page 592
to the altered somatosensory inputs (just as the system is light of the physiological f indings and the anatomical
capable of adapting to altered vestibular inputs), the symp- convergence of cervical and v estibular inputs, the fol-
toms of cervicogenic dizziness w ould abate even though lowing sections explore whether cervical proprioceptive
the underlying dysfunction remained. Because the symp- signals can contribute to symptoms of v ertigo or dise-
toms attributed to cervicogenic dizziness can continue quilibrium and influence vestibular system function or
for extended periods, this explanation, although enticing, postural stability.
remains controversial. The following sections review the
literature that addresses the role of altered cervical propri- Findings after Cervical Spine Lesions
oceptive signals in the generation of signs and symptoms A number of studies in animals and humans ha ve investi-
of dizziness. gated oculomotor and balance changes follo wing either
experimentally induced lesions in the upper cervical spine
Anatomy and Physiology or cervical injuries. With regard to the cervical injuries, the
There is a con vergence of cervical propriocepti ve and primary research focus has been on whiplash associated
vestibular information throughout the spinal cord, brain- disorders (WADs), which cause a diverse set of symptoms
stem, cerebral cortex, and cerebellum.15 A detailed review (including headache, dizziness, paresthesia, anesthesia,
of the anatomical e vidence is beyond the scope of this and cervical, thoracic, lumbar, and upper extremity pain)
chapter; however, a brief review of the pertinent physio- following a flexion-extension cervical injury.26 Although
logical evidence, which suggests that cervical inputs may most individuals recover from WAD, the symptoms, which
play a role in dizziness, is warranted. Cervical propriocep- can be severe, persist in a signif icant proportion of these
tive signals important for postural neck reflexes arise from individuals. On the basis of the findings of various studies,
the joint and tendon receptors located in the deep struc- cervical injury seems to have little effect on the oculomotor
tures of the upper cervical spine. 16 McCouch and col- and vestibular system but may lead to disturbances in pos-
leagues16 demonstrated that the tonic neck reflexes in cats tural control.
were mediated through the joint receptors rather than the
cervical musculature. The role of the deep para vertebral Oculomotor Findings
muscle spindles in this re gion is not clear and may be Cervical proprioceptive ablation has been performed
species dependent.17-22 by both sectioning of the dorsal roots and injection of
In addition to its influence on postural neck re- local anesthetics into the neck. Igarashi and coworkers27
flexes, upper cervical spine proprioception is thought to reported on the oculomotor ef fects seen after local
be responsible for the generation of the cervico-ocular anesthetic injections, or unilateral transection of the
reflex (COR), which, when present, complements the C1 and C2 dorsal roots in squirrel monk eys. Lidocaine
vestibulo-ocular reflex (VOR) at lower frequencies of (Xylocaine) (1 mL of 1% solution) without epinephrine
movement.23 Rubin and associates24 recorded from neu- was injected into the deep neck re gions unilaterally in
rons in the vestibular nucleus of cats that responded to the experimental animals, and into either the superficial
both vestibular stimulation (whole-body rotation) and posterior neck region or abdominal wall in control sub-
movements of the trunk on a fixed head. Further support jects. The animals were placed in the dark, and their eye
for the hypothesis that cervical proprioception can in- movements were recorded. There was no evidence of
fluence vestibular function comes from the w ork of spontaneous nystagmus in either the e xperimental or
Hikosaka and Maeda. 25 These investigators reported control groups after injection. Optokinetic n ystagmus
that, in the cat, v estibular excitation of the abducens was used as a measure of v estibular function in this
nerve was inhibited by contralateral and f acilitated by study. Optokinetic nystagmus, the reflexive eye move-
ipsilateral electrical stimulation of the cervical dorsal ment response to a moving full-field visual stimulus, is
roots or facet joints. In addition, they reported that these a visually mediated response that tra vels through the
effects were seen with stimulations at C2 and C3 but not accessory optic system, a subcortical neural pathway, to
with stimulations at C5 or lower. the vestibular nuclei. Here the signals are processed
These studies indicate that cervical proprioception, in conjunction with the v estibular afferent input to
particularly from the upper cervical spine, may play a generate compensatory e ye movements. Optokinetic
role in postural control and may ha ve an ef fect on nystagmus was measured pre-injection and postinjection
vestibular function. It is important to remember that the in 10 animals by means of a rotating optokinetic stimu-
studies were performed in anesthetized or decerebrate lus (1 deg/sec2 acceleration up to 200 deg/sec). Igarashi
animal preparations and that responses in a wake, nor- and coworkers27 reported bidirectional declines in both
mally functioning humans may be entirely different. In the slow-component and fast-component eye velocities
3970_Ch31_590-609 25/06/14 5:39 PM Page 593
of the optokinetic n ystagmus in the e xperimental sub- In addition to the questionable statistical signif i-
jects. The control groups also demonstrated declines in cance, the responses these in vestigators noted to the
the slow-component eye velocity postinjection. The in- optokinetic stimuli and the rotational stimuli were not
vestigators stated that there was a statistically significant consistent. Clockwise optokinetic stimulation induces
difference in slow-component eye velocity changes be- nystagmus with slo w-component eye velocity to the
tween the experimental and control groups, and the y right and the f ast-component eye velocity to the left
infer from this f inding that cervical proprioception (left-beating nystagmus). In humans, this stimulation
contributes to oculomotor behavior. also induces a sense of rotation in a counterclockwise
Two issues raise questions about their conclusion. direction. The post-rotatory nystagmus following coun-
First, the investigators reported a statistically signif icant terclockwise rotation is right-beating (slow-component
difference using a P value equal to 0.066, which exceeds eye velocity to the left and fast-component eye velocity
the generally accepted probability le vel for statistical to the right), and it would be accompanied by a sense of
significance. Most investigators would not reject the null clockwise rotation in humans. If the dorsal root sections
hypothesis that there is no difference between groups with were to have an asymmetrical effect on vestibular func-
this P value. Second, the declines in v elocity of the f ast tion, one would expect that the response to optokinetic
component of the n ystagmus in the e xperimental group stimulation would be diminished during clockwise
and in the velocity of the slow component of the nystag- rotations and that post-rotatory n ystagmus would be
mus seen in the control groups would argue that the local diminished after a clockwise rotation of the chair. Both
anesthetic has a diffuse, systemic effect on the nervous of these conditions would elicit left-beating nystagmus
system rather than a specif ic effect on the v estibular as well as inducing a sense of leftw ard rotation in
or optokinetic system through cervical propriocepti ve humans. Although Ishigara and coworkers27 suggest that
pathways. If the anesthetic were to have a localized effect their findings support the role of cervical proprioception
on vestibular function mediated through the cervical in normal oculomotor and v estibulo-ocular function,
proprioceptive pathways, one w ould not e xpect to see their interpretations should be taken cautiously in light
changes in the fast component of the nystagmus, which is of the data.
not mediated through the v estibular system. In addition, Care must be taken in extrapolating from the animal
one would not expect to see changes in the control groups, studies cited here to humans, because there appear to be
in which the anesthetic was administered at a site distant species-specific differences. Injection of local anesthetics
from the deep cervical structures. in the posterior, upper cervical musculature in animals and
The same group of in vestigators recorded similar humans yields different oculomotor responses. De Jong
measures in f ive monkeys following left C1 and C2 and associates 28 reported that injection of a local anes-
dorsal root section. They reported no spontaneous nys- thetic in the cat, monk ey, and rabbit induced n ystagmus.
tagmus but did observ e asymmetrical optokinetic The induced nystagmus in the cat and rabbit lasted from
responses as compared with preoperati ve responses, several minutes to an hour or more. The nystagmus in the
which had been symmetrical. Slo w-component eye monkey lasted for only se veral minutes and w as sup-
velocity was diminished during clockwise optokinetic pressed by vision. In rabbits with bilateral labyrinthec-
stimulation (P values ranging from 0.03 to 0.09). The tomies, injection of the local anesthetic did not induce
post-rotatory nystagmus (rotation velocity 200 deg/sec) nystagmus, indicating that the n ystagmus is generated
was measured in four monkeys preoperatively and after through the vestibular system.29 In monkeys, the local
left C1 and C2 dorsal root sections. During the f irst anesthetic had no effect on optokinetic nystagmus, opto-
2 postoperative days, the monk eys demonstrated a de- kinetic after-nystagmus, or caloric n ystagmus. These in-
crease in the maximum slo w-component eye velocity vestigators also injected local anesthetic into tw o human
after counterclockwise rotations. The investigators state subjects and observ ed no n ystagmus in either subject.
that this was a statistically significant decrease, and that Therefore, the nature of the cervical-induced n ystagmus
the effect was likely a result of the loss of proprioceptive appears to be species specific.
input from the cervical spine to v estibular nuclei. As On the basis of the anatomical con vergence of
in the previous experiment, however, they used a P value vestibular, cervical proprioceptive, and visual signals from
equal to 0.06 as the level of significance. This response the accessory optic tract on type II neurons in the vestibular
difference was short-lived. By the f ifth day after the nuclei,30,31 Karlberg and Magnusson32 proposed that asym-
dorsal root section, the slo w-component eye velocity metrical cervical proprioception may af fect optokinetic
responses were greater than the control values, and there after-nystagmus (OKAN), the n ystagmus present in the
was no apparent asymmetry in the responses. dark following the cessation of the optokinetic stimulus.
3970_Ch31_590-609 25/06/14 5:39 PM Page 594
These researchers measured OKAN in normal, healthy were found frequently. The incidence of individual central
individuals with the head in neutral, passi vely rotated signs ranged from 26% to 43%. The investigators also
70 degrees to either side, and acti vely rotated 60 to reported that cervical nystagmus was present in 168 pa-
70 degrees to either side. They found that initial velocity, tients, which may simply be the normal manifestation of
duration, and cumulative eye position of OKAN were the COR. Because there is no indication of the incidence
significantly decreased when the optokinetic stimulus of cervical nystagmus in normal individuals, one cannot
was rotated in the direction of passi ve head rotation in ascertain whether this finding is abnormal. On the basis
comparison to the OKAN with the head in neutral.When of results of their oculomotor studies, the in vestigators
the optokinetic stimulus was in the direction opposite to contended that cervical whiplash injuries induce diffuse,
the head rotation, there w as no decrease in the OKAN rather than well-localized, lesions within the CNS.
response. A similar decrease in OKAN duration and Toglia34 reported ENG and rotational chair results in
cumulative eye position occurred during acti ve head 309 patients who had primary symptoms of dizziness after
rotation. The researchers suggest that this cervical influ- flexion–extension acceleration injury to the cervical spine.
ence on OKAN may play a role in the pro vocation of Of these patients, 57% had abnormal caloric test results
symptoms of dizziness in individuals with cervical pain (40% had significant canal paresis, and 22.5% a significant
and dysfunction. directional preponderance), and 51% had abnormal rota-
Although Karlberg and Magnusson32 conducted their tional test results. These data support the idea that periph-
study in normal humans, the results may support the find- eral vestibular system deficits are frequently present in
ings of Igarashi and co workers27 after unilateral C1 and individuals who experience whiplash injuries. One might
C2 dorsal root section in squirrel monk eys. Recall that make the argument that the caloric weaknesses and rota-
the latter investigators reported a decrease in the slo w- tional asymmetries were due not to peripheral v estibular
component eye velocity of post-rotatory nystagmus when dysfunction but to impaired cervical input to the vestibular
the slow component was directed toward the side of the nuclei. This possibility is unlik ely, however, given the
dorsal root section. Karlberg and Magnusson32 reported a relatively small input from the cervical spine to the vestibu-
decrease in slow-component velocity when the optokinetic lar nuclei compared with the input from the v estibular
nystagmus was in the same direction as the head rotation. labyrinth. In addition, because there was no cervical move-
If one assumes that head rotation to the left induces an ment during the caloric or rotational tests, one would have
asymmetrical input from the cervical proprioceptors no physiological reason to e xpect that the asymmetrical
(greater on the right than the left because of stretching of responses arose from the cervical spine.
the muscle spindles), the results of the tw o studies are The smooth pursuit neck torsion test (SPNT) has
qualitatively similar. In both cases, the slo w-phase eye been proposed to identify cases of cervicogenic dizziness.
velocities were decreased to ward the side of decreased This laboratory test e valuates the smooth pursuit e ye
cervical proprioceptive input. Whether this asymmetrical movement system and is conducted with the neck in
OKAN test can be used to identify individuals with cervi- neutral and rotated 45 degrees to the left and to the right.
cal vertigo remains to be seen. Smooth pursuit e ye movements are recorded in each
Several other studies have assessed oculomotor and position. The gain (the ratio of e ye velocity to tar get
vestibular function in humans after flexion–extension in- velocity) of the response is determined for each neck po-
juries to the cervical spine. Oosterveld and colleagues33 sition, and the difference between the smooth pursuit gain
conducted electronystagmographic (ENG) studies in in neutral and the average gain in the rotated positions is
262 patients who had symptoms of cervical or cervical calculated (the SPNT difference). Several studies have
and upper extremity pain after experiencing acceleration demonstrated a significant increase in the SPNT dif fer-
injuries to the cervical spine. Eighty-five percent of these ence values between subjects with WAD and normal sub-
patients had symptoms of lightheadedness or a floating jects, as well as between subjects with WAD and those
sensation. The investigators report that none of the pa- with Ménière’s disease or central vertigo.35-37 In addition,
tients had rotational vertigo. Spontaneous nystagmus was these studies have shown a significantly greater increase
reported in 165 patients (63%); 110 of these patients in the SPNT dif ference in subjects with WAD and con-
(67%) also had positional nystagmus. On the basis of the current complaints of dizziness as compared with subjects
pattern of spontaneous and positional nystagmus in these with WAD but no dizziness, suggesting that the dizziness
165 patients, the nystagmus was thought to be of central is a critical component.
origin in 159 cases (96%). Central oculomotor f indings, It is possible that the severity of cervical pain is the
including direction-changing nystagmus, saccadic smooth critical component in the SPNT dif ference values. Both
pursuit, and impaired visual suppression of the VOR, Tjell and Rosenhall 35 and Treleaven and colleagues 36
3970_Ch31_590-609 25/06/14 5:39 PM Page 595
noted that patients with WAD and dizziness had greater WAD and cervicogenic dizziness and indi viduals with
complaints of pain than patients with WAD but no dizzi- WAD and another cause of dizziness.
ness. Treleaven and colleagues36 evaluated the role of pain In a second study, Tjell and colleagues 37 compared
levels in their analyses of the SPNT . They found mixed individuals with WAD to individuals with cervical spondy-
results: if they grouped data from all patients with WAD, losis, cervical vertigo, or fibromyalgia. They found signif-
there was a weak b ut statistically significant correlation icant differences in the SPNT dif ference values between
(Spearman rank correlation [ρ] = 0.27) between pain lev- the individuals with WAD and each of the other condi-
els and SPNT differences, such that with increasing pain tions, suggesting that the SPNT test may be more appro-
levels, there was an increase in the SPNT dif ference. On priate as a test for WAD than cervicogenic dizziness.
the other hand, there w as a significant negative relation- Another point to k eep in mind is that the SPNT , as
ship between SPNT dif ferences and reported le vels of described, is a laboratory test where the analysis of the eye
pain/disability in patients with WAD but no dizziness, movements is performed off-line, and the identification of
such that those with greater pain tended to have a smaller saccades within the smooth pursuit mo vements is made
SPNT difference. Although the SPNT difference values by visual inspection of the e ye movement data. It is not
were greatest in patients with WAD, individuals with other clear that this test can be replicated with the typical e ye
causes of cervical pain, such as cervical spondylosis and movement recording systems used in v estibular function
fibromyalgia, had signif icant SPNT dif ference values testing clinical laboratories. Kongsted and colleagues38,39
when compared with normal individuals.37 Regardless of were unable to identify a signif icant SPNT difference in
the exact etiology of the changes in SPNT, either nocicep- individuals with WAD using computerized eye movement
tive or proprioceptive factors, the results do suggest a re- analyses similar to those used in clinical v estibular labs.
lationship between cervical pain, cervical proprioception, There were other methodological differences between the
and CNS oculomotor control. studies performed by the tw o groups. In the studies per -
Attempts have been made to determine the sensitivity formed by Kongsted and colleagues, a chin rest was used
and specificity of the SPNT. Tjell and Rosenhall32 deter- to stabilize the head, which may have had an influence on
mined the sensitivity and specificity of the SPNT using head movements that occurred during the test and poten-
2 standard deviations from the mean of the SPNT dif fer- tially altered the cervical af ferent input. There were also
ence value found in healthy controls as the threshold to differences in the parameters of the smooth pursuit stim-
determine a normal/abnormal test result. F or the control ulus. The SPNT test shows promise, but it has not been
group, they combined the healthy controls, subjects with adequately validated for use in identifying individuals with
Ménière’s disease, and those with central vertigo, because cervicogenic dizziness. In addition, although some ha ve
there were no dif ferences in the results among these indicated that SPNT can be performed as part of the clin-
groups. Comparison of individuals with WAD and dizzi- ical bedside exam, to date there are no published data to
ness with the “normal” group gave the SPNT a sensitivity support this claim.40
of 90% and a specificity of 91%. Comparing the individ- In summary, although there are kno wn cervical in-
uals with WAD but no dizziness with the “normal” group puts to the vestibular nuclei and a convergence of cervical,
gave the SPNT a sensiti vity of 56% and a specif icity of visual, and vestibular inputs in the CNS, it does not appear
91%. Based on these results, the authors concluded that that ablative cervical lesions ha ve a profound ef fect on
the SPNT test is useful for diagnosing cervicogenic dizzi- the oculomotor or vestibular systems in humans. Cervical
ness in individuals with WAD. However, they did not ad- disorders have been shown to induce changes in smooth
dress the issue of discriminating between individuals with pursuit, but the studies to date ha ve not been able to dif -
WAD and cervicogenic dizziness and folks withWAD and ferentiate between individuals with cervical pain only and
dizziness arising from another cause, such as a concurrent those with cervical pain plus dizziness.
vestibular problem. Using the reported sensiti vity and
specificity values, one can determine the positive and neg- Postural Control Findings
ative predictive values of the SPNT test for comparing In contrast to the inconclusi ve results of v arious oculo-
WAD with dizziness and WAD without dizziness. The motor tests in indi viduals with suspected cervicogenic
positive predictive value (PPV) is 62%, and the ne gative dizziness, the tests of balance and cervical kinesthetic
predictive value (NPV) is 81%. With these values, the ab- sense may be more beneficial in the diagnosis of this dis-
sence of a significant SPNT difference value does a fairly order. De Jong and associates 28 described ataxia in all
good job of eliminating cervicogenic dizziness as the species following injections of a local anesthetic in the
cause of symptoms. However, a significant SPNT differ- cervical region. Cats demonstrated ataxia and hypotonia
ence is unlikely to differentiate between individuals with ipsilateral to the injection and had a tendenc y to fall to
3970_Ch31_590-609 25/06/14 5:39 PM Page 596
that side. Rabbits also displayed a complex behavior after researchers found differences between groups and with
unilateral injection; they first fell and rolled to the side of different cervical positions. All three subject groups gen-
the injection, then de veloped lateropulsion, and then erally demonstrated increased sw ay when the cervical
demonstrated ipsilateral hypotonia. Similarly, when uni- spine was out of anatomically neutral position. The pa-
lateral cervical root sections were performed in rabbits tients with cervical pain and dizziness had signif icantly
that had previously undergone unilateral labyrinthectomy, greater sway than the healthy controls when the cervical
the rabbits fell to the side of the labyrinthectomy and spine was in neutral. The subjects with cervical pain and
rolled along the long axis of their bodies. The direction dizziness had greater sway than subjects with cervical pain
of the rolling depended on the side of the labyrinthectomy but no dizziness when the cervical spine w as held in the
and was independent of the side of the cervical root sec- most painful positions. On the basis of these findings, the
tion. Although the nystagmus induced by the local anes- researchers concluded that dynamic posturography may
thetic in monkeys was small compared with that in the be an appropriate method of determining the presence of
cat, the ataxia was greater. The monkeys displayed a head cervicogenic dizziness. They did not determine the speci-
and trunk tilt of approximately 10 degrees toward the side ficity and sensitivity of the test, which must be examined
of the lesion and mark ed ataxia of the ipsilateral limbs. before the test can be clinically useful.
Injection of a local anesthetic in human subjects resulted Karlberg and colleagues42,43 have described changes
in lightheadedness and a sense of lateropulsion. There in postural control in individuals with suspected cervico-
was a deviation of stance toward the side of the injection genic dizziness and in indi viduals with cervical and
and ipsilateral past-pointing. When human subjects were radiating upper extremity pain. They did not mention
in supine, the injection produced a sense that the bed was whether the individuals with upper quarter pain had com-
rolling over toward the side of the injection.Although the plaints of dizziness or imbalance. Postural control in
injection of local anesthetic w as no doubt an unusually these studies was assessed using a force platform and
potent stimulus, it yielded both postural and perceptual measuring the motion (sway velocity and sway variance)
findings that one might e xpect to see in cases of altered of the center of pressure. These investigators induced
cervical proprioceptive inputs. body sway with vibrators attached to the gastrocnemius
Several studies have examined balance control in in- muscles or the posterior cervical musculature. Compared
dividuals with cervical symptoms both with and without with age- and gender-matched controls, the individuals
associated complaints of dizziness. These studies have with upper quarter pain had greater sw ay velocity and
used various manipulations and measurement modes to increased variance of sway with eyes closed when either
determine the role that cervical pain may play in standing site was vibrated.42
balance and to establish a test for cervicogenic dizziness. In a subsequent study , Karlberg and colleagues 43
For the most part, these studies have documented that cer- evaluated postural dynamics (measures of swiftness, stiff-
vical pain leads to a disruption of standing balance, which ness, and damping determined from an inverted pendulum
has been postulated to be the result of a disruption of the model of stance control) for three groups. Using the
proprioceptive inputs. vibration-induced body sway described previously, they
Alund and colleagues 41 measured standing balance measured the postural control parameters in indi viduals
in patients with chronic cervical pain and associated symp- with suspected cervicogenic dizziness, individuals with a
toms of vertigo or imbalance, which were compared with recent bout of v estibular neuritis, and in normal healthy
those obtained in age-matched, normal healthy controls individuals. The group with a suspected cervical cause of
and to patients with chronic cervical pain but no associated dizziness demonstrated lo wer values of stif fness than
vertigo or imbalance. Postural sw ay was measured with either the normal or vestibular neuritis groups. In addition,
computerized dynamic posturography. The subjects were the cervicogenic dizziness group had higher v alues for
tested with eyes open in both stable and sw ay-referenced damping than the normal group. Using Fisher linear
platform conditions (sensory organization tests 1 and 4). discriminant analysis and the swiftness, stif fness, and
The subjects performed the tests with the cervical spine in damping values, the investigators were able to distinguish
neutral, flexion, extension, lateral flexion to the right and subjects with cervicogenic dizziness from both the normal
left, and rotation to the right and left. The subjects with subjects and those with vestibular neuritis. They were also
cervical pain also performed the tests with the cervical able to differentiate the subjects with v estibular neuritis
spine in the most painful position. When the subjects from the normal subjects.
performed the tests on a stable platform, there w as no The results of these tw o studies give further support
difference among groups or test positions. However, with to the hypothesis that cervical disorders in general lead to
the test performed on a sw ay-referenced platform, the disturbances in postural control, possibly through distortion
3970_Ch31_590-609 25/06/14 5:39 PM Page 597
of the propriocepti ve information. Karlber g and col- aimed at reducing the cervical pain, impro ving range of
leagues43 report that a naïve tester using this method could motion, and extensor muscle endurance resulted not only
correctly classify 78% of indi viduals with cervicogenic in reduced f atigability, but improved postural sw ay
dizziness, so evaluation of postural control may be a test following the f atiguing isometric contractions. These
for cervicogenic dizziness. However, as the investigators findings suggest that cervical e xtensor muscle f atigue
note, the specificity of the test has not yet been determined. may have a role in the increased postural sw ay and that
Two other points should be raised regarding this test. First, the cervical muscle fatigue testing and treatment may be
the sensitivity of this test w as calculated using data from important components in the treatment of individuals with
individuals previously identified with cervicogenic dizzi- WAD. At this point, it is not clear if cervical e xtensor
ness, rather than in a mixed population with the examiner fatigue has a role in cervicogenic dizziness.
blinded to the diagnosis. Second, although this test may
hold promise as a diagnostic tool, it incorporates compu- Cervical Kinesthesia Findings
tations and measures that are not currently part of commer- Another line of investigation provides additional support
cially available balance assessment tools. to the hypothesis that cervical problems, WAD in partic-
Finally, Treleaven and colleagues44 assessed stand- ular, can lead to altered cervical kinesthetic sense. Several
ing balance using the Clinical Test for Sensory Interac- studies have demonstrated a decrease in cervical kines-
tion in Balance in normal indi viduals and individuals thesia in individuals with complaints of cervical pain.
with WAD, half of whom had associated complaints of Revel and coworkers46 reported that subjects with chronic
imbalance and dizziness. The amount of postural sw ay cervical pain, compared with normal subjects, had a
was recorded by means of a force platform and analyzed diminished ability to relocate the head on the trunk
with wavelet analysis. As a group, the indi viduals with (in the absence of visual cues) after an acti ve head rota-
WAD had greater sw ay than the age-matched normal tion. Using a threshold v alue of 4.5 de grees, these re-
individuals. In addition, the indi viduals with WAD and searchers determined that the test had a sensitivity of 86%
complaints of dizziness had greater sw ay than the in - and a specificity of 93%. In a subsequent study, Revel and
dividuals with WAD but no dizziness. As noted previ- coworkers47 found that patients with chronic cervical pain
ously by these investigators, individuals with WAD and and impaired kinesthetic sense, who were enrolled in
dizziness had greater complaints of pain than individuals a kinesthetic retraining program in combination with
with WAD but no dizziness. The investigators noted sta- medical analgesic therapy, experienced improvements in
tistically significant, moderate correlations (Spearmans kinesthetic sense and cervical rotation range and a de-
rho correlation coefficients 0.32 to 0.41, P < 0.01) be- crease in pain in comparison with patients who recei ved
tween pain levels and sway energy in the v arious test only medical analgesic therap y. The training program
conditions for the indi viduals with WAD (combined used in this study is described later in this chapter.
dizzy and nondizzy groups). No attempt was made to de- Subsequent studies have assessed cervical kinesthe-
termine sensitivity or specificity for this test. The results sia in individuals with WAD and dizziness. Similar to the
of this study further support the proposition that altered findings reported by the Re vel group, Heikkilä and
cervical proprioceptive input or cervical pain can lead to Wenngren48 found that indi viduals with WAD had
disturbed balance responses. Care should be taken in in- greater cervical repositioning errors than normal individ-
terpretation of these results, however, because vestibular uals. They also noted that indi viduals with WAD and
lesions were not ruled out in the subjects of the study complaints of dizziness had greater cervical reposition-
except by patient history. ing errors than individuals with WAD and no complaints
There is other e vidence to suggest that WAD can of dizziness. It is not clear whether this greater error is
contribute to imbalance and postural sw ay, but it should caused by the associated dizziness (and presumed influ-
be noted that in this study there w as no mention of ence on the vestibular system) or the increased cervical
whether the patients with WAD had symptoms of dizzi- pain that is typically found in individuals with WAD and
ness. Stapley et al 45 found that, following whiplash in- dizziness. Heikkilä and Wenngren48 did not report the
juries, some patients (7 of 13) were more susceptible to pain levels in the tw o subgroups with WAD. They did
fatigue in the neck e xtensor musculature. These seven observe, however, that individuals with WAD and radic-
subjects showed an increase in postural sw ay following ular symptoms also had greater cervical repositioning
isometric contractions designed to fatigue the cervical ex- errors than individuals with WAD and no radicular symp-
tensor musculature. The subjects who were not suscepti- toms, suggesting that the extent of injury, and the result-
ble to fatigue showed no changes in their postural sw ay ing pain levels, may be the critical factor in determining
following the same isometric contractions. Interventions the extent of the cervical repositioning errors.
3970_Ch31_590-609 25/06/14 5:39 PM Page 598
Treleaven and colleagues 49 also noted greater cer- musculature could create a sensory mismatch between the
vical repositioning errors for rotation and e xtension in vestibular and proprioceptive inputs, which could lead to
individuals with WAD than in normal individuals. When symptoms of dizziness and altered postural control. 55
these investigators compared results in individuals with Third, rather than creating a sensory mismatch, the altered
WAD and dizziness and indi viduals with WAD but no cervical kinesthetic sense could lead to inaccurate repre-
dizziness, they noted that the individuals with the asso- sentation of head position relati ve to the trunk. Because
ciated dizziness had significantly greater cervical repo- the vestibular system is physically located in the head, the
sitioning errors (4.5 degrees vs. 2.9 degrees) for rotation output of the v estibular system must be modulated in
in one direction. The difference in cervical repositioning relation to head position on the trunk to properly control
errors between these tw o groups approached statistical balance. If the CNS receives inaccurate information about
significance (3.9 degrees vs. 2.8 degrees) for rotation in head position relative to the trunk, the modulation of the
the opposite direction. There was no difference between vestibular responses may be inappropriate, resulting in the
the two WAD groups in the repositioning error for cer- observed imbalance. In both of these instances, the symp-
vical extension movements. These investigators reported toms would be greatest during head mo vements, when
that the subjects with WAD plus dizziness had higher vestibular and cervical propriocepti ve inputs would be
scores on the neck pain inde x, but made no attempt to changing.
correlate the level of pain with the extent of the cervical Finally, it may not be disruption of the cervical kines-
repositioning error. thetic receptors, but the actual pain in the cervical region,
The results of these studies suggest that cervical that leads to the observ ed balance and proprioception
kinesthesia is disturbed after injury to the cervical spine. deficits. Studies by Rossi and colleagues56,57 have shown
Similar kinesthetic impairments have been reported with that chemically induced tonic muscle pain can alter the
pain or injury to other joints, such as the ankle, 50 position sense of the affected limb in the absence of an y
knee,51,52 and shoulder.53 The disruption of cervical actual damage to muscle or joint receptors. The studies
kinesthetic sense has been used as a possible e xplana- have also demonstrated changes in somatosensory-evoked
tion for the mechanism behind cervicogenic dizziness. potentials at a cortical level, rather than at the spinal cord,
Although this is a plausible mechanism for cervicogenic following chemical induction of muscle pain. 57 On the
dizziness, the fact that not all individuals with WAD and basis of the nature of the stimuli used and the measured
impaired cervical kinesthesia have complaints of dizzi- effects, these researchers concluded that alteration in the
ness detracts from the argument. Certainly the extent of somatosensory-evoked potentials reflected changes in the
the injury and the le vel of cervical kinesthetic impair - proprioceptive pathways. A third study demonstrated in-
ment may be a factor in determining which individuals hibition of both cortical and spinal level motor excitability
experience dizziness. as a result of chemically induced muscle pain.58
From the results of these studies, one could hypoth-
Possible Mechanisms esize that cervical pain will alter the proprioceptive sense
The lesion-induced ataxia in humans, the changes seen in in the neck, leading to inappropriate control of the head
stance control in individuals with cervical pain, and the cer- on the trunk. Recall from the previously discussed clinical
vical repositioning errors associated with cervical disorders studies that the postural control deficits and cervical repo-
lend support to the hypothesis that cervical proprioception sitioning errors increased with rising le vels of cervical
has a role in balance control and, possibly , cervicogenic pain. Regardless of the actual mechanisms in volved, it
dizziness. The mechanism of the postural disturbance is appears that cervical disorders can lead to alterations in
unresolved. There are several possible explanations for the balance and cervical position sense that may be related
observed balance/proprioceptive deficits. First, individuals to symptoms of dizziness. It remains to be seen, however,
with cervical spine disease or cervical disc disease may have whether any of these tests can be used to identify individ-
compression of the spinal cord and the spinal tracts relaying uals with cervicogenic dizziness.
the proprioceptive information from the lo wer extremities,
which could cause the observed postural disturbances. Many
of the individuals with cervical pain or dizziness, ho wever,
Examination
have no findings of spinal cord compression on radiological With the lack of a definitive test for cervicogenic dizzi-
or clinical e xamination, making this f inding an unlik ely ness, the diagnosis is based on the individual’s signs and
cause of the postural deficits.54 symptoms and on the absence of otologic or neurologi-
Second, inaccurate proprioceptive input from sensi- cal causes for the clinical f indings. A patient with sus-
tized receptors in either the joint capsules or the cervical pected cervicogenic dizziness typically presents with
3970_Ch31_590-609 25/06/14 5:39 PM Page 599
disequilibrium or lightheadedness, cervical pain, ataxia spine is initiated. We should emphasize one point regard-
or unsteadiness, and limited cervical motion. Head ing VBI testing in the clinic. Studies to date ha ve shown
movements typically aggra vate the symptoms. Other that the clinical tests for v ertebral artery compression
disease processes, such as cerebellar and spinal ataxia, do not have adequate sensitivity to rule out the disorder
bilateral vestibular loss, benign paroxysmal positioning (see Richter and Reinking 60 and Childs and colleagues 61
vertigo (BPPV), and chronic unilateral v estibular loss, for in-depth reviews of this issue). Therefore, a negative
can also manifest similar signs and symptoms. These test result does not rule out the possibility of v ertebral
otologic and neurological causes of dizziness may also artery compromise.
cause restricted cervical motion and neck pain as a result Despite its lack of utility as a screening test, local
of muscular guarding of the neck to limit head mo ve- statutes and practice patterns may dictate the performance
ments. Consequently, the presence of disequilibrium or of VBI testing. Testing for VBI often consists of the
lightheadedness, cervical pain, ataxia or unsteadiness, vertebral artery compression test (cervical e xtension and
and limited cervical motion is not conclusi vely indica- rotation), typically performed in the supine position. It
tive of a cervical cause of the dizziness, and the clinical should be noted that this test position is similar to the final
decision-making process should first rule in or rule out position in the Dix-Hallpike test used to assess for BPPV.62
otologic and neurological causes of the symptoms. If the There are differences in the two tests, at least in patients
symptoms are because of an otologic or neurological with normal cervical range of motion. The test for
cause, this fact should become apparent with a compre- VBI involves full e xtension and rotation, whereas the
hensive clinical examination, vestibular function tests, Dix-Hallpike test in volves 45 de grees of rotation and
or radiological evaluation. 10 to 20 de grees of cervical e xtension. In patients with
If there are no apparent neurological or otologic limited cervical range, however, the Dix-Hallpike test may
causes for the symptoms, one should conduct a more involve movements at the limits of extension and rotation.
detailed evaluation of the upper quarter . Malmstrom If a patient with complaints of cervical pain and
et al59 examined patients with suspected cervicogenic dizziness experiences symptoms of dizziness with either
dizziness for musculosk eletal impairments. Subjects the Dix-Hallpike test or the vertebral artery compression
were excluded if they had a history of central nerv ous test, differentiating between BPPV and VBI can be prob-
system disease, head-neck trauma, major injuries of lematic. As discussed previously, it is unlik ely that VBI
the lower limbs, cerebrovascular diseases, ear diseases, would produce isolated symptoms of dizziness or the char-
psychiatric disorders, pregnancy, or hyperthyroidism. acteristic patterns of nystagmus one sees in patients with
Vestibular causes of dizziness were excluded via clinical BPPV. However, given the nature and se verity of the
examination, electronystagmography, and pure tone deficits that can result from VBI, one would like to be able
audiometry. Common findings included good cervical to differentiate between these two entities. This differen-
mobility but reduced cervical-thoracic mobility. There tiation can be made if one remembers the follo wing
were postural alignment de viations, and e vidence of two facts: (1) BPPV is brought about by changes in head
postural imbalance. Dorsal neck muscle tenderness and position relative to gravity, regardless of the position of
tightness was evident in the majority of the subjects, and the cervical spine, and (2) VBI caused by cervical motion
there was local tenderness at se veral zygapophyseal is brought on by the position of the cervical spine, regard-
joints. It follo ws that an appropriate e valuation of less of head position relative to gravity.
patients with suspected cervicogenic dizziness should Consequently, one can test for BPPV by positioning
include assessment of postural alignment and control, an individual’s head (relative to gravity) in a position
active and passive cervical and cervico-thoracic range identical to that for the Dix-Hallpike test without extend-
of motion, tests for instability in the upper cervical ing the neck by ha ving the person lie supine on a table
spine, neurological examination of the upper extremities that is in the modif ied Trendelenburg position (foot of
(strength, sensation, and reflexes), palpation of the cer- the table elevated relative to the head). Another method
vical spine musculature and facet joints, and segmental is to perform the side-lying test for BPPV .63 If cervical
mobility testing of the cervical spine. A detailed descrip- rotation must be avoided as well, the indi vidual can lie
tion of these e xamination procedures is be yond the down in a partial side-lying position. Because the neck
scope of this chapter; three specif ic test maneuv ers, is maintained in a neutral position with these test modi-
however, are addressed here. fications, symptoms brought on with the tests would not
The first specific test is the test for VBI. Some be attributed to VBI. In an analogous f ashion, one can
authorities recommend testing for VBI during the cervical position the individual’s cervical spine in a position iden-
screening examination before treatment of the cervical tical to the Dix-Hallpik e position without changing the
3970_Ch31_590-609 25/06/14 5:39 PM Page 600
orientation of the head relati ve to gravity. The patient example, the head and trunk move as a unit, as in a stand-
sits, forward flexes at the hips, and at the same time ing pivot or with the patient sitting in a chair or on a stool
extends and rotates the neck. This sequence of mo ve- that will rotate (Fig. 31.2C). The examiner must stabilize
ments places the cervical spine in a position identical to the head in relationship to the trunk with this test. Provo-
that obtained in the Dix-Hallpik e and vertebral artery cation of symptoms by this test suggests a vestibular com-
compression tests, but the patient’s head position remains ponent to the disorder . With this test sequence, it is
unchanged relative to gravity. Maintaining the v ertical important to perform the complete sequence to determine
orientation of the patient’s head prevents the occurrence whether the symptoms originate from the cervical spine,
of the signs and symptoms of BPPV (which are provoked the vestibular system, or both. A similar approach can be
by changes in head position relati ve to gravity). There- used to dif ferentiate between v estibular and cervical
fore, any symptoms associated with this position change causes of dizziness induced by v ertical head movements
may be attrib uted to v ertebral artery compression (cervical flexion-extension).
and VBI. Another method of assessing whether the symptoms
Another method of testing for VBI, which is rec- originate from the cervical spine is a trial of manual
ommended by the Australian Physiotherapy Association, cervical traction. The theory behind this examination tech-
involves having the patient acti vely assuming the fol- nique is that unloading the cervical spine may alter
lowing positions in a sequential manner: e xtension, the cervical somatosensory inputs to the CNS. Although
rotation, and quadrant position (rotation and e xten- unloading of the cervical spine can be performed in vari-
sion).64 Each position is maintained for 10 seconds ous ways, application of traction while the patient is sitting
while the e xaminer monitors the patient’ s status. If causes minimal disturbance of the v estibular system. A
results of these positions are ne gative (no dizziness, reduction in symptoms during the traction would suggest
nausea, tinnitus, headache, blurred vision, slurred a cervical component to the disorder . The test can be
speech, slowed responses, or facial or tongue paresthe- modified by placing the patient in a symptom-pro voking
sia), the examiner repeats the positions by using passive position before applying the manual traction to test for al-
movements with o verpressure. This testing method, leviation of the symptoms. This examination technique has
when done in sitting, avoids the severe position changes not yet been validated in the literature, but we have found
of the head relative to gravity and may help differentiate it clinically useful.
between BPPV and VBI. In particular , if this test is The third test is a test of cervical kinesthetic sense.
performed first and no signs or symptoms are noted, This test has been performed in laboratory settings, 46
subsequent Dix-Hallpike test findings can be attributed but can be performed clinically. The patient starts sitting
to BPPV. in a chair with a backrest with the neck in a neutral, rest-
The second test is a test to differentiate between cer- ing position. The patient closes his or her e yes and
vical- and vestibular-provoked symptoms. When patients makes a full range cervical rotation to the right or left.
complain of dizziness associated with head movements on After the full range rotation, the patient attempts to re-
a fixed trunk, one cannot differentiate, from that statement, locate his or her head to the initial starting position, still
whether the symptoms are attrib utable to a v estibular with the eyes closed. The accuracy of this movement is
disorder, cervicogenic dizziness, or a combination of the assessed (the actual process will be described in the next
two. To differentiate between a cervical cause of the dizzi- paragraph), and the patient will open the eyes and return
ness and a v estibular cause of the dizziness, one must to the initial starting position. The process will be re-
isolate the two systems. One method is to perform the peated with cervical rotation to the other side, as well
Head-Neck Differentiation test, a clinical variation of the as for cervical extension and flexion.
neck torsion nystagmus test,65-67 in which one looks for There are three clinical methods that can be used to
provocation of symptoms, not for nystagmus, as individu- assess the accuracy of the relocation task. One method is
als without a cervical disor der can have nystagmus with to use a laser pointer that is attached to a headband or the
this test. To test the cervical spine in isolation, one must brim of a baseball cap. The laser pointer is positioned such
move the patient’s body under a stable head. For example, that the “spot” will appear at eye level, in front of the pa-
the patient rotates the trunk in one direction while the tient. Another method is to use fo veal glasses, which are
examiner stabilizes the head in space (Fig. 31.2A and B). glasses that block peripheral visual input and only allo w
Symptom provocation (dizziness) with this test w ould vision through a small (1 mm square) aperture. These
indicate a cervical component to the disorder. To test the glasses are constructed by f irst covering one lens com-
vestibular system in isolation, the head and body must pletely with opaque tape. Then, with the patient wearing
move together (en bloc). To test for horizontal rotation, for the glasses and looking at a small object located directly
3970_Ch31_590-609 25/06/14 5:39 PM Page 601
A B
C
Figure 31.2 (A) The patient complains of symptoms of dizziness with head rotation to the
left. (B) To assess the cervical contribution to her symptoms, her head is stabilized in space,
and she turns her body to the right. (C) To assess the vestibular contribution to her symp-
toms, she is rotated en bloc to the left. In this example, the patient is sitting on a stool that
rotates. The same examination procedure could be performed with the patient standing.
in front of him or her, the peripheral portions of the other will perform the cervical relocation task described above.
lens are obscured with opaque tape, leaving a small aper- To evaluate the accurac y of the repositioning task, the
ture such that the patient can still see the object. To per- examiner measures the location of the laser spot before the
form the test with the laser pointer, an appropriately sized patient opens the eyes. To perform the test with the fo veal
target is placed in front of the patient, such that the laser glasses, an appropriately sized tar get is placed in front of
pointer is pointing at the center of the tar get. The patient the patient, such that the patient can see the center of the
3970_Ch31_590-609 25/06/14 5:39 PM Page 602
target. The patient will perform the cervical relocation task address restricted mobility (because of joint restrictions
described above. To assess the accuracy of the repositioning or muscle tightness), hypermobility, increased muscle
task, the examiner holds the patient’s head stationary, and tone, trigger points, poor cervical posture, and impaired
asks the patient to open the eyes and tell the examiner what cervical kinesthesia. Detailed descriptions of the treat-
he or she can see through the glasses. The third method ment approaches for upper quarter dysfunction are
is to attach the Cervical Range of Motion de vice (CROM; beyond the scope of this chapter; the therapeutic treat-
Performance Attainment Associates) to the patient’s head ments may include cervical spine mobilization, range-
and measure the position of fle xion/extension/rotation the of-motion exercises, cervical strengthening e xercises,
patient is in when he or she has f inished the repositioning cervical proprioception exercises, soft tissue mobilization,
maneuver.68 and therapeutic agents.
The size of the target that is used will vary with the Because of the apparent role of the upper cervical
distance between the patient and the target. Using 4.5 de- spine in the generation of cervicogenic dizziness, treat-
grees as the cutoff for normal cervical joint repositioning ment may need to be focused on this area. Numerous tech-
error and trigonometry, one can determine the appropri- niques are available to increase joint mobility in the upper
ate distance and target size. The relationship between tar- cervical spine. The treatment techniques described here
get size and distance can be expressed by the following are examples of those that ha ve been well tolerated by
formula: patients, are relatively easy to perform, and appear to be
effective in improving cervical mobility and reducing pain.
Tangent (4.5 degrees) = (0.5W)/D
In addition, the patients may note a reduction in dizziness.
where W = width of the target, and D is the distance from The first technique is occipito-atlas distraction, which can
the axis of rotation (top of the head) to the tar get. Note be performed in various manners. In one technique, the
that we use one-half the width of the tar get to allow for patient lies supine, and the patient’s head is supported by
error to either side of the center of the tar get. Because the therapist. The therapist positions his or her hands such
the tangent of 4.5 degrees is 0.0787 and the width of the that the superior nuchal line of the patient’s skull is resting
target can be measured, the equation can be rearranged on the therapist’s fingertips (Fig. 31.3A). The therapist can
to determine the necessary distance of the patient from simply allow the patient’s head to rest on the fingertips or
the target: can apply gentle traction to the upper cervical spine by ei-
ther flexing the metacarpal phalangeal joints or leaning
D = (0.5W)/0.0787
away from the patient. Another method of performing the
For example, using a standard “stick y-note,” which traction is for the therapist to cup the patient’ s occipital
is 3 inches square, the distance that the patient should be region in the palm and fingers (Fig. 31.3B). The therapist
from the target is applies traction by leaning away from the patient.
The second technique is designed to increase rotation
D = (0.5 × 3)/0.0787
between C1 and C2 (Fig. 31.4). The patient lies supine.
D = 19 inches
The therapist prepositions the patient’ s lower cervical
If one used a sticky-note for the target and the patient spine into flexion. This position can be combined with lat-
could perform the cervical relocation test such that the eral flexion (not shown). While maintaining the cervical
laser pointer was within the sticky-note, or if the patient flexion, the therapist then passi vely rotates the patient’s
could see the sticky-note through the foveal glasses, then head in the direction of restricted mobility to the end of
the test would be within normal limits. Note that with the passive, pain-free motion. If the prepositioning of the
foveal glasses, the field of view increases as the distance lower cervical spine is maintained, this cervical rotation
between the patient and tar get increases. Consequently, occurs only in the upper cervical spine. At end range, the
one should use small targets (such as sticky-notes) located patient attempts to gently rotate in the opposite direction.
closer to the patient. This is not a concern when using a This motion is block ed by the therapist’ s hand. After
laser pointer. 10 to 15 seconds, the patient relax es, and the therapist
gently rotates the patient’ s neck in the direction of the
restricted motion. This treatment technique is analogous
Management to the hold-relax stretching techniques often used to
Treatment in cases of supposed cervicogenic dizziness stretch limb musculature. The force generated by the pa-
is directed to the clinical f indings and the patient’ s tient during the active, resisted rotation in this technique
symptoms. Treatment of the cervical spine should is minimal. Telling the patient to look in the direction of
3970_Ch31_590-609 25/06/14 5:39 PM Page 603
A
B
Figure 31.5 Cervical kinesthesia training exercises.
(A) Foveal glasses. (B) Eyes maintain gaze on a fixed target
(indicated by straight arrow) while the trunk is rotated to
the right. The foveal glasses necessitate disassociation of
head and trunk movements. Similar exercises can be per-
formed with hip and trunk flexion and extension in the
sitting position.
36. Treleaven J, Jull G, Lowchoy N. Smooth pursuit neck 53. Smith RL, Brunolli J. Shoulder kinesthesia after anterior
torsion test in whiplash-associated disorders: relationship glenohumeral joint dislocation. Phys Ther. 1989;69:106.
to self-reports of neck pain and disability, dizziness and 54. de Jong JMBV, Bles W. Cervical dizziness and ataxia.
anxiety. J Rehabil Med. 2005;37:219. In: Bles W, Brandt T, eds. Disorders of Posture and Gait.
37. Tjell C, Tenenbaum A, Sandstrom S. Smooth pursuit neck Amsterdam: Elsevier; 1986:185.
torsion test: a specific test for whiplash associated disor- 55. Brandt T, Bronstein AM. Cervical vertigo. J Neurol
ders? J Whiplash Relat Disord. 2002;1:9. Neurosurg Psychiatry. 2001;71:8.
38. Kongsted A, Jørgensen LV, Bendix T, Korsholm L, 56. Rossi A, Decchi B. Changes in Ib heteronymous inhibition
Leboeuf-Yde C. Are smooth pursuit eye movements to soleus motoneurones during cutaneous and muscle
altered in chronic whiplash-associated disorders? A nociceptive stimulation in humans. Brain Res. 1997;
cross-sectional study.Clin Rehabil. 2007;21:1038. 774:55.
39. Kongsted A, Jorgensen LV, Leboeuf-Yde C, Qerama E, 57. Rossi S, della Volpe R, Ginanneschi F, et al. Early
Korsholm L, Bendix T. Are altered smooth pursuit eye somatosensory processing during tonic muscle pain in
movements related to chronic pain and disability follow- humans: relation to loss of proprioception and motor
ing whiplash injuries? A prospective trial with one-year ‘defensive’ strategies. Clin Neurophysiol. 2003;114:1351.
follow-up. Clin Rehabil. 2008;22:469. 58. Le Pera D, Graven-Nielsen T, Valeriani M, et al. Inhibition
40. Treleaven J. Sensorimotor disturbances in neck disorders of motor system excitability at cortical and spinal level by
affecting postural stability, head and eye movement tonic muscle pain. Clin Neurophysiol. 2001;112:1633.
control. Man Ther. 2008;13:2. 59. Malmstrom E-M, Karlberg M, Melander A, Magnusson
41. Alund M, Ledin T, Odkvist L, Larsson SE. Dynamic M, Moritz U. Cervicogenic dizziness—musculoskeletal
posturography among patients with common neck findings before and after treatment and long-term out-
disorders: a study of 15 cases with suspected cervical come. Disability & Rehabilitation. 2007;29:1193.
vertigo. J Vestib Res. 1993;3:383. 60. Richter RR, Reinking MF. Evidence in practice: how
42. Karlberg M, Persson L, Magnusson M. Impaired postural does evidence on the diagnostic accuracy of the vertebral
control in patients with cervico-brachial pain. Acta artery test influence teaching of the test in a professional
Otolaryngol Suppl (Stockh). 1995;520(Pt 2):440. physical therapist education program? Phys Ther. 2005;
43. Karlberg M, Johansson R, Magnusson M, Fransson PA. 85:589.
Dizziness of suspected cervical origin distinguished by 61. Childs JD, Flynn TW, Fritz JM, et al. Screening for verte-
posturographic assessment of human postural dynamics. brobasilar insufficiency in patients with neck pain: manual
J Vestib Res. 1996;6:37. therapy decision-making in the presence of uncertainty.
44. Treleaven J, Jull G, Lowchoy N. Standing balance in J Orthop Sports Phys Ther. 2005;35:300.
persistent whiplash: a comparison between subjects with 62. Dix M, Hallpike C. The pathology, symptomatology and
and without dizziness. J Rehabil Med. 2005;37:224. diagnosis of certain common disorders of the vestibular
45. Stapley PJ, Beretta MV, Dalla Toffola E, Schieppati M. systems. Ann Otol Rhinol Laryngol. 1952;61:987.
Neck muscle fatigue and postural control in patients 63. Cohen HS. Side-lying as an alternative to the Dix-Hallpike
with whiplash injury. Clinical Neurophysiology. test of the posterior canal. Otol Neurotol. 2004;25:130.
2006;117:610. 64. Grant R. Vertebral artery testing—the Australian Physio-
46. Revel M, Andre-Deshays C, Minguet M. Cervicocephalic therapy Association Protocol after 6 years. Man Ther.
kinesthetic sensibility in patients with cervical pain. Arch 1996;1:149.
Phys Med Rehabil. 1991;72:288. 65. Philipszoon AJ, Bos JH. Neck torsion nystagmus. Pract
47. Revel M, Minguet M, Gregoy P, et al. Changes in cervico- Otorhinolaryngol (Basel). 1963;25:339.
cephalic kinesthesia after a proprioceptive rehabilitation 66. Fitz-Ritson D. Assessment of cervicogenic vertigo.
program in patients with neck pain: a randomized con- J Manip Physiol Ther. 1991;14:193.
trolled study. Arch Phys Med Rehabil. 1994;75:895. 67. Norré ME. Cervical vertigo: diagnostic and semiological
48. Heikkilä HV, Wenngren BI. Cervicocephalic kinesthetic problem with special emphasis upon “cervical nystag-
sensibility, active range of cervical motion, and oculomo- mus.” Acta Otorhinolaryngol Belg. 1987;41:436.
tor function in patients with whiplash injury. Arch Phys 68. Rix GD, Bagust J. Cervicocephalic kinesthetic sensibility
Med Rehabil. 1998;79:1089. in patients with chronic, nontraumatic cervical spine pain.
49. Treleaven J, Jull G, Sterling M. Dizziness and unsteadi- Arch Phys Med Rehabil. 2001;82:911.
ness following whiplash injury: characteristic features and 69. Reid SA, Rivett DA. Manual therapy treatment of
relationship with cervical joint position error. J Rehabil cervicogenic dizziness: a systematic review. Man Ther.
Med. 2003;35:36. 2005;10:4.
50. Bullock-Saxton JE. Local sensation changes and altered 70. Lystad RP, Bell G, Bonnevie-Svendsen M, Carter CV.
hip muscle function following severe ankle sprain. Phys Manual therapy with and without vestibular rehabilita-
Ther. 1994;74:17. tion for cervicogenic dizziness: a systematic review.
51. Barrack RL, Skinner HB, Buckley SL. Proprioception Chiropractic & Manual Therapies. 2011;19:21.
in the anterior cruciate deficient knee. Am J Sports Med. 71. Karlberg M, Magnusson M, Malmstrom EM, et al. Postural
1989;17:1. and symptomatic improvement after physiotherapy in
52. Barrack RL, Skinner HB, Cook SD, Haddad RJ, Jr. Effect patients with dizziness of suspected cervical origin. Arch
of articular disease and total knee arthroplasty on knee Phys Med Rehabil. 1996;77:874.
joint-position sense. J Neurophysiol. 1983;50:684.
3970_App A_610-616 25/06/14 2:35 PM Page 610
APPENDIX A
Questionnaire for History
and Examination
Describe your major problem or the reason why you are seeing us.
Please describe in detail the circumstances and date in which the problem be gan and what were your initial symptoms
and problems. Was there any stress or anxiety around the onset of the problem?
If you have spells, please describe a typical spell in as much detail as possible and describe the frequency and duration of
the spells.
Duration (please check which most closely fits what you experience):
_____ less than two minutes; _____ 20 – 30 minutes; _____ 2 – 4 hours; _____ 12 – 24 hours;
_____ 1 – 3 days; _____ always present; _______ other (please write in duration)
1. Please check the symptoms which characterize your problem and grade their severity from 2 (marked), 1 (mod-
erate) to 0 (none). Put 0 if you do not have these symptoms.
a. Sensation of imbalance
( ) Trouble with walking. Do you use a cane, walker or wheel chair, touch walls or furniture, or use a person for
balance inside buildings (If yes, please circle all that apply).
( ) Poor balance.
( ) F alls. How many falls have you had in the past 6 months, in which you une xpectedly lost your balance and
landed on the floor or ground _______? Please circle all that apply: indoors, outdoors, poor lighting, due toatigue,
f
while turning, while standing up or sitting down.
Check ( ) if the fall(s) were due to your dizziness
610
3970_App A_610-616 25/06/14 2:35 PM Page 611
Standing up
Loud noises
Menstrual periods
Do or did you have moderate-severe motion (car or boat) sickness. If yes when did it start?
Do or did you avoid situations in which you were tumbled or spun (amusement rides, merry-go-
rounds)? When did this start?
Can you sit in the back seat of a moving car and read without feeling ill?
3970_App A_610-616 25/06/14 2:35 PM Page 612
YES NO
Hearing test
Evaluation by a neurologist
7. ALLERGIES TO MEDICATIONS and please note if drug causes rash or difficulty breathing.
8. MEDICATIONS
What are your current medications, include hormones, birth control pills, special diet, etc. (Name and Amount/Day)?
1. 5.
2. 6.
3. 7.
4. 8.
3970_App A_610-616 25/06/14 2:35 PM Page 613
YES NO
History of irregular periods now?
If yes, for how long? _______________________________________________
Are you taking any hormone supplements now (e.g., Provera, Estratest, birth control pill)?
If yes, how long have you been taking it? ______________________________
Did you stop taking hormones prior to the onset of your dizziness?
If yes, which hormone(s) were you taking previously? _____________________
PERSONAL INFORMATION
DOB _____-_____-_____ AGE: _________
RACE ❑ Caucasian ❑ African American ❑ Asian ❑ Hispanic ❑ Other
HANDEDNESS ❑ Right Handed ❑ Left Handed Primary Language:
HOME PHONE ___-____-_____ FAMILY CONTACT ___________________ PHONE ___-____-____
WORK PHONE ___-____-_____ PRIMARY CAREGIVER ___________________ PHONE ___-____-____
CELL PHONE ___-____-_____ EMERGENCY CONTACT ___________________ PHONE ___-____-____
PHARMACY ___-____-_____ EMAIL if you want note sent to you ___________________
SOCIAL HISTORY
Education: ❑ High School ❑ College ❑ Graduate Degree Marital Status: Currently Employed:
❑ Single ❑ Married ❑ Yes ❑ No
Present Occupation: _________________________________ Disability Claims: ❑ Yes ❑ No
2.
3.
4.
REVIEW OF SYSTEMS Please check if you have had any of these symptoms IN THE PAST MONTH
Neurological Ocular Gastrointestinal Constitution Cardiovascular
❑ Dizziness ❑ Glasses ❑ GI bleed ❑ Weakness ❑ Heart attack
❑ Headaches ❑ Redness ❑ Nausea/Vomiting ❑ Tiredness ❑ Chest pain/angina
❑ Muscle pain/cramps ❑ Dryness ❑ Hepatitis ❑ Loss of appetite ❑ Dizziness
❑ Double vision ❑ Tearing ❑ Hiatal hernia ❑ Increased appetite ❑ Fainting
❑ Droopy eyes ❑ Pain ❑ Heartbrurn ❑ Weight loss ❑ Aneurysm
❑ Muscle twitching ❑ Infection ❑ Diarrhea ❑ Weight gain ❑ Palpitations
❑ Weakness ❑ Constipation ❑ Chills ❑ Calf/leg pain at rest
❑ Numbness Ear, Nose, Throat ❑ Difficulty chewing ❑ Fever ❑ Calf/leg pain walking
❑ Tingling ❑ Pain or soreness ❑ Abdominal pain ❑ Night sweats ❑ Swelling of ankles
❑ Loss of memory/ ❑ Discharges ❑ Bright red blood ❑ Discoloration of
concentration ❑ Hearing loss in stool Psychiatric hands/feet
❑ Blackouts/Seizures ❑ Bleeding gums ❑ Psychosis ❑ Poor circulation
❑ Unsteadiness ❑ Hoarseness Rheumatologic ❑ Addictions ❑ Heart murmur
❑ Head injury ❑ Tinnitus ❑ Joint pain ❑ Anxiety ❑ Heart failure
❑ Slurred speech ❑ Joint swelling ❑ Hallucinations
❑ Trouble swallowing Respiratory ❑ Severe stress Hematologic
❑ Snoring ❑ Cough Dermatologic ❑ Depression ❑ Easy bruising
❑ Daytime sleepiness ❑ Blood in cough ❑ Rash ❑ Mental illness ❑ Bleeding disorder
❑ Insomnia ❑ Wheezing ❑ Skin color change ❑ Mood swings
❑ Restless legs ❑ Pneumonia ❑ Hair loss ❑ Phobias Lymph
❑ Leg movements ❑ Bronchitis ❑ Skin ulcer ❑ Frequent infections
during sleep ❑ Node enlargement
2. Since the time your dizziness began, how much has your dizziness changed your ability to work? (___Check here, if
you have retired for reasons other than your dizziness.)
1 2 3 4 5
not at all slightly moderately quite a bit extremely
3. How much has your dizziness changed your ability to do household chores?
1 2 3 4 5
not at all slightly moderately quite a bit very much
4. Does your dizziness significantly restrict your participation in social activities such as going out to dinner, going to
movies, dancing or to parties?
1 2 3 4 5
not at all slightly moderately quite a bit very much so
5. To what extent does dizziness prevent you from driving your car?
1 2 3 4 5
not at all slightly moderately markedly severely
MDI Section B
This scale consists of a number of words that describe different feelings and emotions. Read each item and then mark
the appropriate answer in the space next to that word. Indicate to what extent you generally feel this way, that is, how
you feel on the average. Use the following scale to record your answers.
1 2 3 4 5
very slightly a little moderately quite a bit extremely
or not at all
_____ interested _____irritable _____jittery
_____ distressed _____alert _____active
_____ excited _____ashamed _____afraid
_____ upset _____inspired _____hostile
_____ strong _____nervous _____enthusiastic
_____ guilty _____determined _____proud
_____ scared _____attentive
3970_Index_617-630 25/06/14 12:53 PM Page 617
Index
Anatomy Assessment of Driving Related Skills
A cervical proprioception, 592 (ADRes), 496
Abducens nerve palsy, 255
otolith organs, 195–197, 196f Astasia, 67–68, 79
Abducens nucleus VI, 65f
peripheral sensory apparatus, 3–6, 3f, 4f, 5f Ataxia
Acceleration. See also Otolith organs
Ankle strategy, postural response, 39–40, 40f, Case Study, 259, 260, 260f
otoliths, response to, 7–8, 7f, 8f, 195–199,
88–89, 88f, 94–95, 375–376 central vestibular lesions, 97
196f
Anterior horn cells, spinal cord, 11 chronic vestibular insufficiency, 135, 137
perceiving position and self-motion, 29–31,
Anterior inferior cerebellar artery (AICA), 5, dysfunction of sensory motor centers, 97–98
30f, 31f
5f, 9, 10f episodic ataxia, 63t
Acetazolamide, 257b, 259
Anterior semicircular canal, 4f falls and fear of falling, exercises for, 573f, 574
Acetic acid, 243
Anterior vestibular artery, 5, 5f Friedreich’s ataxia, 100
Acetylcholine receptors, 252–253
Anticholinergic medications, 253, 254t gait assessment, 176
Acoustic neuroma
Antidepressant medication, 318–319, 318t, 319t peripheral vestibular disorders, 93–96, 93t
auditory brainstem response (ABR), 235f
Antifungal agents, 243 spinocerebellar ataxia, 559–560
bilateral vestibular disorders, 56
Antihistamines, 254t treatment of, 257, 257b, 571–572
central vestibular disorders, 60
Antivert, 254t unilateral vestibular deafferentation (UVD),
diagnosis of, 51, 52
Anxiety 121
surgical management, 123–124, 244–245,
agoraphobia and, 309 vertigo, treatment of, 253
245f, 285–288, 286f, 287f, 288f
anxiety disorders and migraine, 269 Ataxia Test Battery, 91–92
Acoustic reflex, 232–233
Case Studies, 306–307 Ativan (lorazepam), 304t
Acquired pendular nystagmus, 256, 260–261,
chronic subjective dizziness and, 311t, Audiogram, 54, 228–232, 229f, 230f, 231f, 231t
261f
312–315, 312t, 315f Audiometry, speech, 232
Activities of daily living
dizziness and, 296–298, 297t Auditory biofeedback systems, 547, 548f
assessments, 114–115, 362f, 493
head trauma, 508 Auditory brainstem response (ABR), 233–234,
integration of exercise, 578
patient history, 116, 161t, 163 235f
patient history, 164–166, 165b, 165f
treatment for, 304, 304b, 304t Auditory disorders. See also Sensorineural
vestibular disorders and, 115–117
types of disorders, 301–302, 302b hearing loss
Activities-Specific Balance Confidence Scale
Appiani maneuver, 339, 340f, 341, 342t, 343t acoustic immittance measures, 232–233, 232f
(ABC), 113, 114, 166, 360t, 362f, 365,
Aps, smart phones and tablets, 548–549 audiograms, hearing loss types and, 229–232,
491–492, 492b
Arnold-Chiari malformation, 10, 10f, 69, 97, 229f, 230f, 231f, 231t
Activity of Daily Living Questionnaire
256, 258 auditory brainstem response (ABR), 233–234,
(ADQL), 360t, 362f
Arteries. See Vascular supply 235f
Acute unilateral vestibulopathy, 52–53
Aspartate, 252–253 auditory evoked potentials (AEPs), 233,
Adaptation
Aspirin toxicity, 243 234, 236
animal studies of, 21–24, 21f, 23f, 24f
Assessment. See also Children with vestibular aural rehabilitation, 238
human studies, 24–25, 26f
hypofunction; Elderly persons; Psycho- central auditory processing tests, 236
overview, 20
logical disorders; specific condition and electrocochleography, 233, 234f
sensory substitution, posture and, 99–101,
test names hearing aids, 236–238, 237f
99f
auditory disorders, overview, 227–228, 228f hearing loss, infectious disease and, 242–243
Ageotropic nystagmus, 51
clinical decision-making paradigm, 530–531, hearing loss, noise exposure associated, 241
Aging. See Elderly persons
531t hearing sensitivity tests, 228–229, 229f
Agoraphobia, 163, 297t, 301, 302b, 309
clinical examination, 366, 367b, 368b history and physical examination, 227–228,
AIDS, 242
diagnosis, modifiers and, 534, 535b, 535t 228f
Air-bone gap, 229–232, 229f, 230f, 231f, 231t
diagnosis and IFC model of disablement, middle latency responses (MLR), 234, 236
Air-conducted sound (ACS), 198–199, 228–232,
531–532, 531f, 532t otoacoustic emissions (OAEs), 236
229f, 230f, 231f, 231t
diagnostic flowchart, 532–534, 533f pharmacological toxicity, hearing loss, 243
Alcohol use, effects of, 11, 51, 56, 60, 72–74,
evaluation forms, 388–391 presbycusis, 241
72b, 73f, 257b
fall, risk in elderly, 487–491, 488b, 489b, speech audiometry, 232
Alexander’s law, 69, 252
490b, 491b sudden sensorineural hearing loss (SSNHL),
Alport’s syndrome, 57
functional history, 366, 366b 242
Alprazolam (Xanax), 304t
home assessment, elderly persons, 495–496 surgical management, hearing loss, 243–246,
Ambiguity, resolving of, 16
patient goals, 366 244f, 245f
Amblyopia, 458t
patient history, 160–166, 161t, 162t, 164t, tinnitus, 238–240, 240t
Aminoglycosides, 56, 243, 289–290, 459
165b, 165f, 363–364 Auditory evoked potentials (AEPs), 233, 234,
4-aminopyridine, 257, 257b
physical examination, 166–176, 166t 236
Amitriptyline, 283
red flags, 380–381, 381b Auditory nerve
Ampulla, 4f, 6–7, 6f
subjective history, patient, 364–365, 365t electrocochleography, 233, 234f
Ampullofugal flow, 6–7, 6f
treatment decisions and, 381–382 sensorineural hearing loss, 229–232, 229f,
Ampullopetal flow, 6–7, 6f
virtual reality-based assessment, 545–546 230f, 231f, 231t
Ampyra, 257, 257b
617
3970_Index_617-630 25/06/14 12:53 PM Page 618
618 INDEX
Auditory steady-state responses (ASSR), 236 Balance Evaluation Systems Test, 43 Bilateral vestibular disorders, 56–57
Auditory threshold, 228 Balance Near Automatic Virtual Environment assessment of, 161t, 434–438, 434b, 435b,
Augmented sensory biofeedback, 546–548, (BNAVE), 541–542, 542f 437f, 437t, 438f
547f, 548f Balance Rehabilitation Unit (BRU) systems, Case Studies, 448–454, 449f, 451f, 453f
Aural rehabilitation, 238 576 etiology, 432, 433t
Autoimmune disease, 56, 255b Barany maneuver, 327–328, 328f exercise, evidence for, 440–441, 442t
Ayres, Jean, 468 Barbiturates, 257b mechanisms of recovery, 439–440, 439b
Bar-B-Que Roll treatment, 339, 339f physical therapy treatments, 441–447, 443b,
Barotrauma, 55 444b, 445t, 446t, 447t
B Basal ganglia disorders, 98, 176 primary complaints, 432–434
Baclofen, 252, 257, 257b
Basilar artery, 5, 5f, 9, 65 rotational chair test, 185, 186–189, 187f,
Balance. See also Physical therapy; Posture;
Basilar migraine, 66 188f, 189b
specific condition names
Basilar-type migraine, 267b, 268. See also Biofeedback
Activities-specific Balance Confidence
Migraine postural sway and, 36–37, 37f
(ABC) scale, 113, 114
BCV (bone conducted vibration), 130 technology for, 546–548, 547f, 548f
aging and, 101–103
Beck Anxiety Inventory, 300 Bipolar disorder, 297t
assessment, children, 463–469, 464t, 465t,
Beck Depression Inventory, 300 Blast injury, 506–507. See also Head trauma
466f, 467f, 468b, 468t, 469t
Benign paroxysmal positional vertigo (BPPV), 4. Blood vessels. See Vascular supply
assessment, elderly patients, 491–495, 492b,
See also Clinical decision making paradigm Body aid, hearing loss management, 237
493b, 494b, 495
activities of daily living, 117 Body movement, vestibular system overview,
assessment of, 166, 373–376, 373t, 374f,
aging, effects of, 481–482 2–3, 3f
375f, 376f, 435b, 437–438, 438f
anterior SCC canalithiasis treatment, Bone-anchored hearing aid (BAHA), 237, 237f
center of mass, postural responses, 37–41,
337–338, 338t Bone-conducted sounds, 228–232, 229f, 230f,
39f, 40f
assessment and diagnosis, 50–52, 57t, 86–88, 231f, 231t
cervical injury studies, 595–597
86f, 161t, 327–331, 328f, 329f, 330f, 346, Bone conducted vibration (BCV), 130, 198–199
classification of vestibular symptoms,
346f, 355–357, 356t, 357t Bone-conduction hearing aids, 237, 237f
163–164, 164t
Brandt-Daroff exercises, 341, 344f Bonine, 254t
clinical applications and case studies, 42–44,
canalithiasis, treatment of, 339, 339f Bony labyrinth, 3–6, 3f, 4f, 5f
42t, 43b, 44b
Case Studies, 347–350 Borrelia burgdorferi, 243
clinical tests of, 86–88, 86f, 87t, 374–375,
characteristics and history of, 324–326, Botulinum toxin, 258
374f, 597
325f, 325t, 326f Bow and Lean Test, 329–331, 330f
dynamic posturography, 88–90, 88f
chronic subjective dizziness and, 310, 311t, Brainstem. See also Head trauma; stroke
falls, risk of, 487–491, 488b, 489b, 490b,
312t auditory brainstem response (ABR), 233–234,
491b
cupulolithiasis, treatment of, 340, 341f 235f
Modified Fast Evaluation of Mobility, Bal-
environmental causes of, 116 central vestibular lesions, 97
ance, and Fear Baseline (MFEMBAF),
etiology, 116, 326–327, 326t lesions, diagnosis of, 59–60, 60f, 217
493–495, 493b, 494b
imbalance, management of, 344–346 otolith function tests, 201–204, 203f
non-vestibular dizziness, exercises for,
maneuver-induced vertigo and eye reflex adaptations and, 22–24, 23f
572–574, 573f, 574f
movements, 173–176, 174f, 175f, 175t roll plane dysfunction, 63–66, 64t, 65f
patient history, 166
nausea and vomiting, 163 treatment of disorders, evidence for, 572
perceiving position and self-motion, 29–31,
neurophysiology of, 13–14, 13f, 14f unilateral vestibular deafferentation (UVD),
30f, 31f
postural abnormalities, 96 122
postural alignment, 32–34, 33f
repositioning treatment, posterior SCC upbeat nystagmus, 72–74, 72b, 73f
posturography, 190–191, 190f, 191f, 191t,
canalithiasis, 333–337, 334f, 336t, 337f vestibular disorders, pitch plane, 68–74,
192f, 193f
surgical management, 290–291 70b, 71f, 72b, 73f
progression of balance and gait exercises,
treatment of, 253, 331–332, 332t, 340–341, vestibular inputs, processing of, 9, 9f
407–409
342t, 343t, 344, 345t, 346, 346f, 350t vestibulo-ocular reflex and, 12
recovery after UVD, 141–144, 142f
VEMP tests for, 217 vestibulospinal system tests, 86–88, 86f, 87t
sensory information, weighting of, 34–37,
Benign paroxysmal torticollis, 268 visual perception tests, 189–190
34f, 35f, 36f, 37f
Benign paroxysmal torticollis of infancy Brainstem-evoked acoustic response (BAR), 54
sensory substitution, 99–100, 99f
(BPTI), 460 Brandt-Daroff exercises, 341, 344f
somatosensory reflexes, 13–14, 13f, 14f
Benign paroxysmal vertigo of childhood Brisk treatment, 335–337, 336t, 337f
stabilizing head and trunk, 41–42, 41f
(BPVC), 268, 326, 458–459, 458t, 460, Bruininks-Oseretsky Test of Motor Proficiency,
stabilometry, 91
461, 469–470 463, 464t
stepping tests, 91–92
Benzodiazepine, 254t Bucket Test, 466
tests of quiet stance, 90–91
Benztropine, 257, 257b
thalamic and cortical astasia, 67–68
Berg Balance Scale (BBS), 43, 378, 487–491,
tiltboards, 91
488b, 489b, 490b, 491b
C
vestibular system overview, 2–3, 3f Calcium carbonate, 5, 7–8, 7f, 8f
BESTest, 43
vestibulospinal reflex, 11–12 Calcium channel receptor CACNA1A, 271,
Betahistidine, 253
virtual reality environment tests, 92, 92f 272t
Bias test, 126
Balance Accelerometry Measure (BAM), Caloric test, 182–185, 182f, 183f, 184f, 185b,
Bicuculline, 252
466–467 186f, 228
3970_Index_617-630 25/06/14 12:53 PM Page 619
INDEX 619
Canadian Occupational Performance Measure vestibular compensation, 144 modifiers, identification of, 534, 535b, 535t
(COPM), 465t, 473–474 vestibular disorders, pitch plane, 68–74, overview, 530–531, 531t
Canalithiasis 70b, 71f, 72b, 73f Clinical Test for Sensory Interaction in Balance
anterior SCC treatment, 337–338, 338t vestibular inputs, processing of, 8–11, 9–11, (CTSIB), 374–375, 374f, 597
benign paroxysmal positional vertigo, 13–14, 9f, 10f Clinical vestibular dynamic visual acuity test,
13f, 14f, 325–326, 326f vestibulo-ocular reflex and, 12 171, 173f
Bow and Lean Test, 329–331, 330f visual perception tests, 189–190 Clonazepam (Klonopin), 257, 257b, 262, 304t
Case Studies, 347–350 visual tracking, 174 Cochlea
horizontal SCC canalithiasis, treatment of, Cerebral hemosiderosis, 56 anatomy, 3–5, 3f, 4f
339, 339f, 340f Cerebral palsy, 98, 461 audiogram, 229–232, 229f, 230f, 231f, 231t
repositioning treatment, posterior SCC Cerebrospinal fluid, 3 blood vessels, 5, 5f
canalithiasis, 333–337, 334f, 336t, 337f Cervical kinesthesia exercises, 603–605, 604f, cochlear implants, 244, 244f
treatment efficacy, 340–341, 342t, 343t 605f electrocochleography, 233, 234f
Canalith repositioning treatment (CRT), Cervical kinesthesia studies, 597–598 hearing loss in children, 459
333–337, 334f, 336t, 337f Cervical range of motion, 362 otoacoustic emissions (OAEs), 236
Carbamazepine, 253, 257b Cervical reflexes, 12–13 Cochlear aqueduct, 4f
CAREN (Computer Assisted Rehabilitation Cervical traction, 600–603, 603f Cochlear echoes, 236
Environment), 542, 542f Cervical vestibular evoked myogenic potential Cochlear implants, 459
Casani maneuver, 340, 341, 341f, 342t, 343t (cVEMP), 86–88, 86f, 87t, 130, 131f, Cochlear Ménière’s disease, 53–55. See also
Cataracts, 436 189, 209–210, 209f Ménière’s disease
Cautious gait, 572 Cervicocollic reflex (CCR), 13 Cochlear nerve, 8
Cawthorne-Cooksey habituation exercises, Cervicogenic dizziness Cochlear ramus, 5, 5f
399–401, 399b, 400t, 401t Case Studies, 606–607 Cochleosacculotomy, 54
Center of mass, postural responses, 37–42, 39f, etiologies, proposed, 590–598 Cogan’s syndrome, 56, 255b
40f, 41f management of, 602–605, 603f, 604f, 605f Coma. See Head trauma
Central auditory processing disorder (CAPD), overview, 590 Common cochlear artery, 5, 5f
236, 239–240 patient examination, 598–602, 601f Common-mode noise, 7
Central auditory processing tests, 236 Cervico-ocular reflex (COR) Common-mode rejection, 7
Central positional nystagmus, 355–357, 356t, anatomy and physiology, 12, 592 Communication, physical therapist and
357t bilateral vestibular hypofunction, treatment physician, 410–411, 410b
Central vestibular deficits, in children, 461 of, 439, 439f Compazine/Prochlorperazine, 254t
Central vestibular falls, without vertigo, 78–79 vestibulo-ocular reflex hypofunction, Concussion. See Head trauma
Central vestibular lesions, otolith function response to, 151, 153–154, 154f Conductive hearing loss
tests, 201–204, 203f Cervicospinal reflex (CSR), 12–13 audiogram interpretation, 229–232, 229f,
Central vestibular pathways Chemical labyrinthectomy, 289–290 230f, 231f, 231t
disorders, classification of, 59–60, 60f, 61f, Chemotherapeutic agents, hearing loss and, 243 hearing aids, 237, 237f
61t, 62t, 63t Children with vestibular hypofunction Congenital vestibular loss, 57
pitch plane (sagittal) disorders, 68–74, 70b, Case Studies, 471–474, 475t Contact lenses, nystagmus treatments, 257–258,
71f, 72b, 73f common causes of dysfunction, 457–461, 258f
Cerebellar artery infarction, 175, 175t 458t, 460f Convergence prisms, 257–258, 258f
Cerebellar degeneration, 576–577 evaluation and assessment, 463–469, 464t, Convergence spasm, 512
Cerebellar flocculus, 10, 10f, 68–74, 70b, 71f, 465t, 466f, 467f, 468b, 468t, 469t Conversion disorders, 303, 307
72b, 73f overview, 457 Coplanar pairs, semicircular canals, 6–7, 6f
Cerebellar nodulus, 10, 10f postural and oculomotor control, development COR. See Cervico-ocular reflex (COR)
Cerebellopontine angle (CPA) tumors, 244–245, of, 461–463, 462f Corneo-retinal potential (CRP), 178, 179f.
245f treatment of, 469–471, 470t See also Electronystagmography (ENG)
Cerebellum Cholesteatoma, 292 Cortical astasia, 67–68
aging, effects of, 486 Chronic subjective dizziness (CSD) Covert saccade, 151–153, 152f
case study, stroke, 261–262, 261f case studies, 319–321 Craniotomy, middle fossa, 286, 286f
cerebellar degeneration, 69 differential diagnosis, 316 Craniotomy, suboccipital, 287–288, 288f
neuropharmacology of vestibular system, overview, 309–313, 311t, 312t, 561t, 562 Crista ampullaris, 4–5, 5f
252–253 pathophysiology, 313–315, 315f CSR. See Cervicospinal reflex (CSR)
nystagmus, assessment of, 169f, 169t treatment of, 316–319, 317t, 318t, 319t CT scans, head trauma, 509–510
otolith function tests, 201–204, 203f Chronic vestibular insufficiency, 135, 137 Cupula, 4f, 5–7, 6f, 185, 186–189, 187f, 188f,
postural dysfunction and, 97–98 Cilia. See Hair cells 189b
reflex adaptations and, 22–24, 23f Cisplatin therapy, 255b Cupular deflection, 4–5, 4f
roll plane dysfunction, 64 Citalopram, 318t Cupulolithiasis
saccadic eye movements, 175, 175t Clinical decision making paradigm. See also benign paroxysmal positional vertigo, 13–14,
treatment of disorders, evidence for, 572 Assessment 13f, 14f, 51, 325, 325f
unilateral vestibular deafferentation (UVD), diagnosis and IFC model of disablement, Bow and Lean Test, 329–331, 330f
122–123, 123f 531–532, 531f, 532t Case Studies, 347–350
vascular supply, 9, 10f diagnostic flowchart, 532–534, 533f horizontal SCC treatment, 340, 341f
3970_Index_617-630 25/06/14 12:53 PM Page 620
620 INDEX
Liberatory treatment, 335–337, 336t, 337f Disuse disequilibrium, 556–557, 557f, 558t, 577 supranuclear palsy, Parkinson’s disease,
position testing, 173–174, 174f Dix, Margaret, 325 large-fiber peripheral neuropathy,
treatment efficacy, 340–341, 342t, 343t Dix-Hallpike positioning test spinocerebellar ataxia, 559–560
Cushing, Harvey, 286 benign paroxysmal positional vertigo, 50, Dizziness Handicap Inventory (DHI)
cVEMP(p13), 122b, 130, 131f 327–328, 328f, 331, 331t aging, report results, 481–482
Cyclotorsion, 202 cervicogenic dizziness, testing for, 599–600 elderly patients, assessment of, 495
Cystic fibrosis, medication toxicity, 459–460 overview, 180–181 form for, 392–393
Cytomegalovirus, 57, 242 physical therapy assessments, 371–373, non-vestibular dizziness, 574
371t, 372f overview, 112, 113–114
treatment precautions, 341, 344, 345t patient history, 166
D Dix-Hallpike test posture abnormalities, 90
Decibels of Hearing Level (db HL), 228
overview, 173–174, 174f psychological disorders, 298–300, 299t
Deferoxamine, 243
Dizziness. See also Clinical decision making vestibular hypofunction, 361t, 365
Deficiency disorders, defined, 92–93
paradigm; Psychological disorders; Dizzy Factor Inventory (DFI), 113, 114
DeGangi-Berk Test of Sensory Integration,
Vestibular function tests; specific Dopamine, migraine and, 270
463, 464t
condition names Downbeat nystagmus
Deiters, Tract of, 11
Case Studies, 304–307 assessment of, 169f, 169t
Demystification, tinnitus, 239
classification of vestibular symptoms, treatment of, 257, 257b
Depression
163–164, 164t vestibular disorders, 68–74, 70b, 71f, 72b, 73f
aging, effects of, 487
head trauma, 507–509 vestibular lesions, 62t, 63t
Case Studies, 306–307
incidence of, 110 Downbeat nystagmus vertigo syndrome, 97
chronic subjective dizziness and, 309–310
maneuver-induced vertigo and eye Dramamine, 254t
overview of, 302, 303b
movements, 173–176, 174f, 175f, 175t Driving, 410, 496, 560–562, 561t
patient history, 161t, 163
patient history, 160–166, 161t, 162t, 164t, Drop attacks, 97
prevalence of, 297t
165b, 165f Drug toxicity, 69, 70b, 72–74, 72b, 73f
Descending vestibular nuclei, 9, 9f
physical examination, 166–176, 166t Dual-task training, 577–578
Desipramine (Norpramin), 304t
skew eye deviation, 168, 170, 170f Duloxetine, 319t
Developmental coordination disorder (DCD), 459
spontaneous nystagmus, 166–168, 167f, Dynamic Gait Index (DGI)
Developmental disabilities, 459, 460–461
167t, 168f, 168t, 169f, 169t in children, 463, 464t
Dexamethasone, 289
stance and gait assessment, 175–176 in elderly patients, 487
Diabetes insipidus, 74
symptoms of, 162t overview, 377, 378–380, 379b, 380b
Diagnosis. See Assessment
use of term, 160, 161t, 162t postural control, 43
3, 4-diaminopyridine, 257, 257b
vestibular-ocular reflex (VOR), assessment Dynamic perturbation test (DPT), 466, 467
Diazepam (Valium), 304t
of, 170–172, 171t, 172t, 173f, 173t Dynamic posturography, 88–90, 88f, 465t,
Diet, migraine and, 272–273, 274t
visual blurring and, exercises for, 404–406, 466–469, 466f, 467f, 468b, 468t, 469t
Diffusion Tensor Imaging (DTI), 509–510
404b, 405b Dynamic visual acuity (DVA) test, 369, 436,
Dimenhydrinate, 254t
Dizziness, cervicogenic 437f, 437t, 463, 465t
Diphenhydramine, 254t
Case Studies, 606–607 Dysthymic disorder, 297t
Directional preponderance (DP), 183–184
etiologies, proposed, 590–598
Disability
management of, 602–605, 603f, 604f, 605f
activities of daily living and, 115–117 E
overview, 590
aging populations, 115–116 Eflornithine, 243
patient examination, 598–602, 601f
assessment of, 111–115 Elderly persons
Dizziness, chronic subjective
definitions of, 110–111 balance tests, typical, 495
Case Studies, 319–321
diagnosis and IFC model of disablement, Case Studies, 497–499
differential diagnosis, 316
531–532, 531f, 532t disability, 113–116
features of, 310–313, 311t, 312t
dizziness and, 298 driving function, 496
overview, 309–310
Dizziness Handicap Inventory (DHI), falls, risk assessment, 487–491, 488b, 489b,
pathophysiology, 313–315, 315f
298–300, 299t 490b, 491b
treatment of, 316–319, 317t, 318t, 319t
International Classification of Functioning, hearing loss, audiogram interpretation,
Dizziness, non-vestibular
Disability and Health (ICF), 359, 360b, 230–232, 230f, 231f, 231t
assessment of, 570, 570t, 571t
360t, 361t home assessment, 495–496
Case Studies, 562–567, 579–581
overview of, 110–111 incidence of vertigo, 110
disuse disequilibrium, 556–557, 557f, 558t
patient perception of, 165, 165b normal changes of aging, 480–487, 483b,
habituation exercises, 574–577, 575t, 576f
subjective history, patient, 364–365, 365t 484b, 485b
leukoaraiosis and normal-pressure
Disability Scale, 165, 165b, 300, 300t, 364, 365f peripheral vestibular disorders, 93–96, 93t
hydrocephalus, 557–559
Disablement Process model, 111 posture and, 101–103
overview, 556, 569–570
Disabling positional vertigo, 56 tinnitus, 238
physical therapy exercises, 570–578, 572f,
Discordant dysfunction theory, 238 Electrocochleography, 233, 234f
573f, 574f, 575t, 576f
Disequilibrium. See also Balance Electronystagmography (ENG)
recovery time course, 578–579
bilateral vestibular hypofunction, 434 benign paroxysmal positional vertigo, 50
situation-related dizziness, chronic, 560–562,
patient history, 162 caloric test, 182–185, 182f, 183f, 184f,
561t
Distortion disorders, defined, 92–93 185b, 186f
3970_Index_617-630 25/06/14 12:53 PM Page 621
INDEX 621
cervical injury studies, 594 maneuver-induced vertigo and eye Fukuda’s Stepping Test (FST), 175–176,
Ménière’s disease, 54 movements, 173–176, 174f, 175f, 175t 437–438, 438f
oculomotor function, 178–181, 180f, 181f motion sickness, 16–17 Functional Independence Scale (FIM), 112–113,
otolith function tests, 189 neuropharmacology of vestibular system, 375–376, 375f, 376f
overview of, 178, 179f 252–253 Functional polarization vector, 198
rotational chair test, 185, 186–189, 187f, ocular counterrolling (OCR), 130, 200 Functional Reach Test, 43, 463, 465t
188f, 189b ocular tilt reaction, 97 Function tests. See Vestibular function tests
semicircular canal function tests, 181–182, ocular VEMP (oVEMP), 209, 209f, 210 Furstenberg regimen, 289
182f oculomotor and vestibulo-ocular testing,
Electrooculography (EOG), 178, 179f 366–370, 367b, 368b G
Emory Clinical Vestibular Chair Test oculomotor control, development of, GABA (gamma-aminobutyric acid), 252–253
(ECVCT), 463, 464t, 466 461–463, 462f Gabapentin, 256, 257b, 261, 262, 283
Encephalitis, oscillopsia, 255b optical devices, 257–258, 258f Gait. See also Physical therapy; Vestibular
Endolymph oscillopsia, 163, 255–256, 255b pathways, lesions of
caloric test, 182–185, 182f, 183f, 184f, otolith, response to, 199f, 200 assessment of, 437–438, 438f
185b, 186f overload, compensation for, 16 ataxia, 10, 10f, 121
rotational chair test, 185, 186–189, 187f, semicircular canals and, 6–7, 6f bilateral vestibular hypofunction, 435b,
188f, 189b sensory substitution, 99–100, 99f 441–447, 443b, 444b, 445t, 446t, 447t
semicircular canals, function of, 6–7, 6f, 12 skew eye deviation, 168, 170, 170f Case Study, 260, 260f
surgical blockade of flow, 291–292 static otolith tests, 200–201 elderly patients, assessment of, 495
Endolymphatic duct, 4f velocity storage, 14–15 evaluation of, 376–380, 377f, 378f, 379b,
Endolymphatic fluid, 4 vertigo and, 51 380b
Endolymphatic hydrops, 53–54, 56, 95–96, vestibular compensation and rehabilitation, non-vestibular dizziness, therapy for,
233, 234f, 458t 140–141 571–572, 572f
Endolymphatic sac, 4f, 289 vestibular inputs, processing of, 8–11, 9f, patient assessment, 175–176
Environmental causes, vestibular disorders, 116 10f, 77 progression of balance and gait exercises,
Environmental sound enrichment, tinnitus, 239 vestibular system overview, 2–3, 3f 407–409
Epidemic vertigo, 63t visual-motor training, children, 469–471, psychogenic stance and gait disorders,
Epilepsy, 61t, 78, 458t 470t 300–301, 301b, 301t, 302f
Episodic ataxia, 63t visual reflexes, 13 thalamic and cortical astasia, 67–68
Epley maneuver, 14, 333–337, 334f, 336t, 337f VOR plasticity, 140 Gamma-aminobutyric acid (GABA),
Equitest, 192f Eye rotation, defined, 20 252–253
Escitalopram, 318t Ganzfeld, 168t
Estimators, 15–16, 15f F Gaze stability
Estrogen, migraine and, 272 Facial nerve, 8 bilateral vestibular hypofunction, treatment
Eustachian tube dysfunction, assessment for, Factitious disorder, 303 of, 439, 439f, 441–446, 443b, 444b,
232 Falls 445t
Event-related potentials (ERP), 236 bilateral vestibular hypofunction, 432–433 children, assessment of, 463–465, 464t,
Evidence-based practices defined, 365–366 465t, 467f
bilateral vestibular hypofunction, 440–441, disuse disequilibrium, 556–557, 557f, 558t compensatory strategies, 151–153, 152f
442t exercises for prevention, 573–574, 573f, exercises for, 397–399, 398f, 577
cerebellar/brainstem disorders, 572 574f head trauma, 511–512, 513, 513f
for children, 469–471, 470t fear of falling, elderly patients, 486–487 mechanisms of recovery, 395–397, 395f,
exercises, benefits of, 411–420, 415t, 416t, history of, 365–366 396f, 397f, 439, 439f
417t home environment assessment, 483b, 484b, neuropharmacology of vestibular system,
Evoked otoacoustic emissions (EOAEs), 236 485b, 495–496 252
Ewald’s second law, 8 patient history, 166 static and dynamic postural instability,
Exercise, stress reduction and, 272 Familial ataxias, 63t, 97 exercises for, 406–407, 407f, 408b
Exertion intolerance, head trauma and, 514 Fampridine, 257, 257b, 259 tests of, 180
Eye movement. See also Gaze stability; Fastigial nucleus, cerebellum, 10, 10f Generalized anxiety disorder, 269, 297t,
Nystagmus; Smooth pursuit eye Felbamate intoxication, 69, 70b 301–302, 302b
movements; Vestibulo-ocular reflex Fisher’s syndrome, 74 Gentamicin
(VOR); specific condition names Floating, sensation of, 163 balance, effect on, 432–433
adaptations, 20–24, 21f, 23f, 24f, 26f Flocculus, cerebellum, 10, 10f, 23–24, 24f, bilateral vestibular hypofunction, 435–436
ambiguity, resolving, 16 97–98 Case Study, 451–452, 451f
cervical reflexes, 12–13 Fluoxetine, 318t in children, 460
clinical vestibular dynamic visual acuity Fluvoxamine, 318t effects of, 123, 124, 243, 253
test, 171, 173f Forced prolonged position (FFP), 339, 340f Ménière’s disease, 289, 290
corrective saccade, 127–129, 128f, 129f Four-square step test, 380 Geriatric Depression Screening Scale, 487
dynamic posturography, sensory cues, 89–90 Frenzel lenses, use of, 167t, 168t, 369 Glasgow Coma Scale, 504, 505t
gaze stabilization exercises, 151–153, 152f, Friedreich’s ataxia, 100 Glutamate, 252–253
397–399, 398f Frontal cortex, visual tracking, 174 Gufoni maneuver, 340, 341, 341f, 342t, 343t
3970_Index_617-630 25/06/14 12:53 PM Page 622
622 INDEX
INDEX 623
Kinesthesia, cervical exercises, 603–605, 604f, Measles, 242 classification of, 266–269, 267b, 269b
605f Meclizine, 253, 254t clinical presentation, 270–271, 270f, 271t
Kinocilum, 196, 197 Medial longitudinal fasciculus (MLF), 11 downbeat nystagmus, 69, 70b
Klonopin (clonazepam), 304t Medial rectus muscle, 12 habituation exercises and, 576
Medial vestibular nuclei, 9, 9f head trauma, 508
L Medical assessment. See Assessment incidence of, 266
Labyrinth Medical Outcomes Study 36-Item Short-Form management of, 271–273, 273b, 274t, 275b,
aging and, 101–103 Health Survey (SF-36), 364, 481–482 275t
anatomy, 3–6, 3f, 4f, 5f, 196–197 Medications. See Pharmacological treatments Ménière’s disease and, 273, 276, 276t
central vestibular lesions, 96–97 Medulla motion sensitivity, exercises for, 574
deficiencies, response to, 90, 92, 92f central vestibular syndromes, 62t motion sickness and, 162–163, 269
deficient labyrinthine inputs, 93–96, 93t lateropulsion, infarction and, 79 patient history, 161t
dynamic posturography, 88–90, 88f nystagmus, 72–74, 72b, 73f, 169f, 169t roll plane dysfunction, 66
head movement, response to, 6–7, 6f vascular supply, 9, 10f tests for, 86–88, 86f, 87t
infections of, 52 vestibular disorders, roll, pitch, and yaw vertigo and, 51, 253, 254t
neural projections, 199–200, 199f planes, 61f Miller-Fisher syndrome, 175
sensory substitution, 99–100, 99f vestibular nuclear complex, 9, 9f Millon Behavioral Medicine Diagnostic
vertigo, pathophysiology, 251–252 Medullary brainstem, infarctions in, 63–66, (MBMD), 298, 305f
vestibulospinal reflex, 12 64t, 65f Milnacipran, 319t
Labyrinthectomy, 289–290, 291f Medulloblastoma, 10, 10f Minor, Lloyd, 292
Labyrinthine artery, 5, 5f, 8, 52 Memantine, 257, 257b, 261, 262 Mixed-type hearing loss, 230–232, 230f, 231f,
Labyrinthitis Membranous labyrinth, 3–6, 3f, 4f, 5f 231t
Case Study, 204–208, 205f, 206f, 207f, 208f Memory, vestibulo-ocular reflex and, 22 Modified Fast Evaluation of Mobility, Balance,
in children, 458t Ménière’s disease and Fear Baseline (MFEMBAF), 493–495,
hearing loss from, 242 activities of daily living, 117 493b, 494b
nausea and vomiting, 163 assessment, 52, 53–55, 57t, 113 Modified Semont maneuver, 340, 341f
patient history, 161t case studies, 276–278 Mondini malformation, 458t
skew eye deviation, 168, 170, 170f in children, 458t Mood disorders, 297t, 302, 303b
Land-sickness, 281. See also Mal de chronic subjective dizziness and, 310, 311t, Motion-provoked dizziness, exercises for,
débarquement 312t 574–577, 575t, 576f
Large-fiber peripheral neuropathy, 559–560 electrocochleography, 233, 234f Motion receptors, hair cells, 3f, 4–5, 4f
Latent nystagmus, assessment of, 169f, 169t hearing loss, 231–232 Motion sensitivity, exercises for, 574
Lateral medullary syndrome, 9 migraine and, 273, 276, 276t Motion Sensitivity Quotient (MSQ), 372, 400,
Lateral rectus muscle, 12 nystagmus and, 174 400t, 401t, 574, 575t
Lateral semicircular canal, 4f oscillopsia, 255b Motion sickness, 10, 10f, 16–17, 161t, 162–163,
Lateral vestibular nuclei, 9, 9f patient history, 161t 252, 269. See also Mal de débarquement
Lateropulsion, 63, 79, 126 postural abnormalities, 95–96 Motor control test, 190–191, 190f, 191f, 191t,
Learning, vestibulo-ocular reflex and, 22 sensory substitution, 100 192f, 193f
Leg-length discrepancy, 176 subjective visual horizontal (SVH), 201, 202f Motorist disorientation syndrome, 560–562,
Lermoyez phenomenon, 53 surgical management, 288–290, 291f 561t
Leukoaraiosis, 176, 557–559 tests for, 86–88, 86f, 87t Motor neurons, 11–12
Liberatory treatment, 335–337, 336t, 337f, transtympanic steroids, 289 Motor skills
339, 340f VEMP tests for, 215 assessment in children, 463–466, 465t, 466t
Lightheadedness, 162 vertigo and, 51, 253 center of mass, postural responses, 37–41,
Linear acceleration, response to, 7–8, 7f, 8f vestibular compensation and, 135 39f, 40f
Lithium toxicity, 69, 70b Meningioma, 285 perceiving position and self-motion, 29–31,
Loop diuretics, 243 Meningitis, 56, 242, 255b 30f, 31f
Lorazepam (Ativan), 254t, 304t Mesencephalic brainstem, 61f, 62t, 63–66, postural alignment, 32–34, 33f
Lumbar puncture, 3 64t, 65f posturography, 190–191, 190f, 191f, 191t,
Lyme disease, 52, 243 Mesodiencephalic brainstem, 62t 192f, 193f
Methylprednisolone, 253, 254t, 289 visual-motor training, children, 469–471,
Microsoft Xbox 360 Kinect, 538–546, 539t, 470t
M 545b Movement strategy, assessment of, 375–376
Maculae, 4–5, 5f, 7–8, 7f, 8f, 196–197, 197f, Middle ear, anatomy, 3–5, 3f, 4f MRI (magnetic resonance imaging), 285,
199–200, 199f Middle fossa craniotomy, 286, 286f 509–510
Macular degeneration, 436 Middle latency responses (MLR), 234, 236 Multiple sclerosis (MS)
Magnesium deficiency, 69, 70b Migraine case study, 260–261, 261f
Main cochlear artery, 5, 5f anxiety disorders and, 269 central vestibular disorders, classification of,
Mal de débarquement, 161t, 162, 281–284, Case Studies, 276–278 60, 62t
282t, 561t, 562 in children, 458–459, 458t, 461 downbeat nystagmus, 69, 70b
Malingering, 303 chronic subjective dizziness and, 310, 311t, nystagmus, treatment of, 256–257, 257b
Mastoidectomy, 292 312t ocular tilt reaction, 97
3970_Index_617-630 25/06/14 12:53 PM Page 624
624 INDEX
oscillopsia, 256 oculomotor and vestibulo-ocular testing, patient history, 161t, 163
paroxysmal central vertigo, 78 366–370, 367b, 368b unilateral vestibular deafferentation (UVD),
roll plane dysfunction, 66, 67 oscillopsia, 163, 255–256, 255b 121
tests for, 86–88, 86f, 87t pathogenesis of, 256 Otitis media, 459
upbeat nystagmus, 72–74, 72b, 73f perilymphatic fistula, 55 Otoacoustic emissions (OAEs), 236
vertigo, treatment of, 253 recurrent positional nystagmus, 324–325 Otoconia, 5, 7–8, 7f, 8f, 13–14, 13f, 14f, 196f,
vestibular disorders, pitch plane, 69 somatosensory reflexes, 13–14, 13f, 14f 197
vestibulo-ocular reflex, 11 Southern California Post Rotary Nystagmus Otolithic membrane, 7–8, 7f, 8f, 196
Mumps, 242 Test, 466, 468 Otolith organs
Muscarinic acetylcholine receptors, 252–253 spontaneous nystagmus, 124–125, 125f, anatomy of, 3–4, 4f, 195–197, 196f
Muscimol, 252 166–168, 167f, 167t, 168f, 168t, 169f, Case Study, function tests, 204–208, 205f,
Muscles. See Somatosensory reflexes 169t, 395 206f, 207f, 208f
Musculoskeletal system, aging and, 486 torsional nystagmus, 68 central vestibular lesions, 97
Myasthenia gravis, 175 treatment of, 256–258, 257b, 258f cerebellum, input processing, 10, 10f
vertigo, pathophysiology, 252 function of, 12, 29–31, 30f, 31f, 197–198,
vestibular disorders, pitch plane, 68–74, 197f, 200
N 70b, 71f, 72b, 73f function tests, 189–190, 195, 200–201, 219f
Naproxen, 243
vestibular neuritis, 52–53 Ménière’s disease, 215
National Health Interview Survey, 110
motion sickness, 16–17
National Institutes of Health (NIH), disability
neural projections, 199–200, 199f
term usage, 110 O ocular counterrolling (OCR), 130
Nausea, 163, 253, 254t Obsessive-compulsive disorder, 163, 297t, 301,
ocular tilt reaction, 125–126, 126f
Near falls, defined, 365–366 309–310
physiology, 7–8, 7f, 8f, 198–199
Neck muscles, posture and, 41–42, 41f Occipito-atlas distraction, 602, 603f
semicircular canal dehiscence, tests for, 215,
Neocerebellum lesions, 98 Ocular counterrolling (OCR), 130, 200
215f, 216f, 217f
Neomycin, 243 Ocular motor nuclei, 9, 9f, 11–12, 65f
skew eye deviation, 168, 170, 170f
Nervus intermedius, 8 Ocular tilt reaction (OTC)
subjective visual horizontal and vertical
Neural integrator, 11 skew eye deviation, 168, 170, 170f
(SVH, SVV), 201–208, 202f, 203f , 205f,
Neurectomy, singular, 291 Ocular tilt reaction (OTR)
206f, 207f, 208f
Neurofibromatosis type 2 (NF2), 245, 245f central vestibular lesions, 62t, 97
unilateral vestibular deafferentation (UVD),
Neurolabyrinthitis, case study, 204–208, 205f, peripheral vestibular lesions, 201, 202f
125–126, 126f, 129–130
206f, 207f, 208f roll plane dysfunction, 63–68, 64t, 65f,
VEMP testing (oVEMP, cVEMP), 209–215,
Neuromonics tinnitus treatment (NTT), 239 66f, 67f
211f, 212f, 214f
Neurosyphilis, 52 static otolith tests, 200–201
vertigo, pathophysiology, 251
Nicotine, 72–74, 72b, 73f, 253 unilateral vestibular deafferentation (UVD),
vestibular syndromes, roll plane, 65f
NIH Toolbox, 466–467 125–126, 126f
Otosclerosis, 56
Nintendo Wii Fit, 543–544, 544f Ocular torsion, 63, 125–126, 126f
Otoscopic examination, 228
Nodulus, cerebellum, 10, 10f, 97–98 Ocular vestibular evoked myogenic potential
Ototopical medications, 243
Noise exposure, 238, 241 (oVEMP), 86–88, 86f, 87t, 130–131,
Oval window, 293, 293f
Nonepileptic cortical vertigo, 61t 131f
oVEMP(n10), 122b, 130–131, 131f
Nonsteroidal anti-inflammatory drugs Oculomotor control. See also Cervicogenic
Overload, compensation for, 16
(NSAIDs), 243 dizziness
Non-vestibular dizziness. See Dizziness, cervical injury and, 592–598
non-vestibular development of, 461–463, 462f P
Noradrenic system, migraine and, 271 Oculomotor function, tests of, 178–181, 180f, Paget’s disease, 56, 292
Norpramin (desipramine), 304t 181f, 366–370, 367b, 368b, 434b Pagnini-McClure maneuver, 51
Nucleus prepositus hypoglossi, 11 Oculomotor nuclei, 12 Pain, cervical, 594–595, 597–598
Nucleus reticularis tegmenti pontis (NRTP), 253 Oculomotor palsy, 66 Panic attack
Nutritional syndromes, 69, 70b Oculopalatal tremor, 256, 257, 261–262, 261f agoraphobia and, 309
Nylen-Barany maneuver, 327–328, 328f Ondansetron, 253, 254t Case Studies, 306–307
Nystagmus. See also Electronystagmography Ophthalmoscope, use of, 168t chronic subjective dizziness and, 311t,
(ENG); specific condition names Optical devices, nystagmus treatment, 257–258, 312–313, 312t
Case Study, 260–261, 260f, 261f 258f overview of, 269, 301, 302b
central positional nystagmus, 355–357, 356t, Optimal estimator, 15–16, 15f patient history, 161t, 163
357t Optokinetic response (OKR), 102, 155 prevalence of, 297–298, 297t
cerebellar lesions, 10, 10f Orthostatic hypotension, patient history, 161t treatment for, 304, 304b, 304t
cervico-ocular reflex and, 12 Orthostatic symptoms, chronic subjective Paramedian pontine reticular formation
head-shaking nystagmus test, 170–172, dizziness, 310, 311t, 312t (PPRF), 74
171t, 172t, 173t Oscillopsia Parietoinsular vestibular cortex (PIVC), 60,
jerk-waveform seesaw nystagmus, 68 bilateral vestibular hypofunction, 433–434 65, 65f
maneuver-induced eye movements, 173–176, chronic vestibular insufficiency, 135, 137 Parkinson’s disease, 98, 114, 176, 559–560
174f, 175f, 175t downbeat nystagmus, 69, 70, 70b Paroxetine (Paxil), 304, 304t, 318t
neuropharmacology, 252–253 pathogenesis, 255–256, 255b Paroxysmal ataxia, 97
3970_Index_617-630 25/06/14 12:53 PM Page 625
INDEX 625
Paroxysmal central vertigo, 78 coordination assessments, 370 Pontomedullary brainstem, 62t, 63–66, 64t, 65f
Paroxysmal room-tilt illusions, 62t diagnosis, modifiers and, 534, 535b, 535t Pontomesencephalic brainstem, 63–66, 64t,
Peabody Developmental Motor Scales Test, diagnosis and IFC model of disablement, 65f, 72–74, 72b, 73f
460, 463, 464t 531–532, 531f, 532t Positional alcohol nystagmus (PAN), 51
Pediatric Balance Test, 463, 465t diagnostic flowchart, 532–534, 533f Position testing, 173–174, 174f, 180–181
Pediatric Clinical Test of Sensory Interaction dizziness, non-vestibular, 570–578, 572f, Positive and Negative Affective Scale
for Balance, 463, 465t, 466–467 573f, 574f, 575t, 576f (PANAS), 298, 298b
Pediatric patients. See Children with vestibular elderly patients, 496–499 Positron emission tomography (PET) scans,
hypofunction evidence for recovery, 411–420, 415t, 416t, 509–510
Pelizaeus-Merzbacher disease, 74 417t Post-concussive syndrome. See Head trauma
Perihypoglossal nuclei, 72–74, 72b, 73f exacerbation of symptoms, 406 Posterior cervical sympathetic syndrome, 590
Perilymphatic fistula gait evaluation, 376–380, 377f, 378f, 379b, Posterior-inferior cerebellar arteries (PICA),
assessment, 245–246 380b 9, 10f
in children, 458t gaze stabilization exercises, 397–399, 398f Post-Therapy Symptoms Scale, 364, 365f
overview, 55–56, 57t habituation exercises, 399–401, 399b, 400t, Post-traumatic stress disorder, 297t
position testing, 173–174, 174f 401t Postural hypotension, aging and, 486
surgical management, 293, 293f head trauma, 512–525, 513f Postural orthostatic tachycardia syndrome
vertigo, treatment of, 253 initial evaluation form, 363, 388–391 (POTS), 486
Perilymphatic fluid, 3 mechanisms of recovery, 394–397, 396f, Posture. See also specific condition names
Peripheral neuropathy, 176 397f aging and, 101–103, 487
Peripheral sensory apparatus, 3–6, 3f, 4f, 5f physical deconditioning, 409, 409f center of mass, postural responses, 37–41,
Peripheral vestibular lesions, 201–208, 202f, positional and movement testing, 371–373, 39f, 40f
203f , 205f, 206f, 207f, 208f 371t, 372f central vestibular lesions and, 96–97
Pharmacological treatments. See also postural examination, 371 cervical injury studies, 595–597
Gentamicin postural stabilization exercises, 401 children, assessment of, 463–469, 464t,
bilateral vestibular hypofunction, 435–436 problem-oriented approach, overview, 465t, 466f, 467f, 468b, 468t, 469t
chemical labyrinthectomy, 289–290 403–404 children, treatment of, 469–471, 470t
chronic subjective dizziness and, 310, progression of balance and gait, 407–409 classification of vestibular symptoms, 85,
318–319, 318t, 319t range of motion and strength assessments, 163–164, 164t
mal de débarquement, 283 370 clinical applications and case studies, 42–44,
migraine, 271, 273, 274t, 275t recovery time course, 578–579 42t, 43b, 44b
nystagmus, 256–257, 257b return to driving, 410 clinical tests, 86–88, 86f, 87t
patient history, 165, 166 sample home exercise program, 587 dysfunction of other sensory motor centers,
psychological disorders, 304, 304b, 304t sensory evaluation, 370 97–98
toxicity, hearing loss and, 243 static and dynamic postural instability, examination of, 371
transtympanic steroids, 289 406–407, 407f, 408b mechanisms of recovery, 395
vertigo, 253, 254t subjective history, patient, 364–365, 365t perceiving position and self-motion, 29–31,
Phenergan, 254t treatment decisions, 381–382, 401–403 30f, 31f, 34–37, 34f, 35f, 36f, 37f
Phenothiazine, 254t treatment goals, 394 peripheral vestibular disorders, 92–96, 93t
Phobic postural vertigo (PPV), 309, 561–562, videos, list for clinic and home use, 588–589 postural alignment, 32–34, 33f
561t Physicians, communication with, 410–411, postural control, development of, 461–463,
Physical deconditioning, 434 410b 462f
Physical deconditioning, exercises for, 409, 409f Physiology postural instability, 361–362
Physical therapy cervical reflexes, 12–13 postural stabilization exercises, 401, 404–406,
assessment red flags, 380–381, 381b higher-level vestibular processing, 14–17, 15f 404b, 405b, 406–407, 407f, 408b
balance assessment, 373–376, 373t, 374f, motor outputs, vestibular system, 11 postural sway, measures of, 374
375f, 376f otoliths, 7–8, 7f, 8f, 198–199 sensory substitution, 99–100, 99f
bilateral vestibular hypofunction, treatment semicircular canals, 6–7, 6f stability, mechanisms for recovery, 98–103,
of, 441–447, 443b, 444b, 445t, 446t, 447t vestibular inputs, processing of, 8–11, 9f, 10f 99f
blurred vision and dizziness, 404–406, 404b, vestibular nerve, 8 stabilizing head and trunk, 41–42, 41f
405b vestibular reflexes, 11–12 stabilometry, 91
BPPV, treatment of, 331–346, 332t, 334f, visual reflexes, 13–14, 13f, 14f stepping tests, 91–92
336t, 337f, 338t, 339f, 340f, 341f, 342t, PICA (posterior-inferior cerebellar arteries), tests of quiet stance, 90–91
343t, 344f 9, 10f thalamic and cortical astasia, 67–68
Case Studies, 420–428, 471–474, 475t Piroxicam, 243 tiltboards, 91
cervicogenic dizziness, 602–605, 603f, 604f, Pitch, 7–8, 7f, 59–60, 60f, 68–74, 70b, 71f, virtual reality environment tests, 92, 92f
605f 72b, 73f, 122b Posturography
children, treatment of, 469–474, 470t Platform perturbations, technology for, 548 advantages and disadvantages, 87t
clinical decision-making paradigm, 530–531, Polarization vector, hair cell, 197 bilateral vestibular hypofunction, 438, 438f
531t Polymyxin B, 243 chronic subjective dizziness and, 316
communication with physicians, 410–411, Polyneuropathy, 56 computerized dynamic posturography,
410b Pons, 9, 9f, 10f, 61f, 175, 175t 190–191, 190f, 191f, 191t, 192f, 193f
3970_Index_617-630 25/06/14 12:53 PM Page 626
626 INDEX
INDEX 627
Sensory information, postural control and, sensory substitution, 99–100, 99f central vestibular disorders, classification
34–37, 34f, 35f, 36f, 37f, 89–90, shipboard motion, 282–283 of, 60
99–100, 99f stabilometry, 91 cerebellar artery, 175, 175t
Sensory Integration and Praxis Test, The, 463, stepping tests, 91–92 nausea and vomiting, 163
464t tests of quiet stance, 90–91 nystagmus, treatment of, 256
Sensory organization test (SOT), 35, 89–90, tiltboards, 91 thalamic and cortical astasia, 67–68, 79
466–469, 466f, 467f, 468b, 468t, 469t vestibular cortex and, 75–78, 76f upbeat nystagmus, 72–74, 72b, 73f
Serotonin, 271, 318–319, 318t, 319t virtual reality environment tests, 92, 92f vertigo, treatment of, 253
Serous labyrinthitis, 242 Southern California Post Rotary Nystagmus vestibular disorders, pitch plane, 69–74,
Sertraline (Zoloft), 304, 304t, 318t Test, 463, 464t, 466, 468 70b, 71b, 72b, 73b
Sharpened Romberg test, 176, 437–438, 438f Space motion sickness, 17 vestibular disorders, roll plane, 63–66, 64f,
Shearing force, 7–8, 7f, 12 Space phobia, 560, 561t 65f, 66f
Shipboard motions, body response to, 282–283 Spastic cerebral palsy, 461 vestibular disorders, yaw plane, 74
Short-Form-36 Health Survey (SF-36), 112 Spastic hemiplegia, case study, 472–473 vestibular vascular supply, 9
Short Physical Performance Battery (SPPB), Spastic paresis, 98 Wallenberg’s syndrome, 79, 97
495 Spatial hemineglect (contraversive), 62t, Structured Clinical Interview for DMS-IV, 300
Sickness Impact Profile, 364 75–78, 76f Subjective visual horizontal (SVH), 201–208,
Sidelying test, 328, 329f, 331, 331t Spatial orientation, vestibular cortex and, 202f, 203f , 205f, 206f, 207f, 208f
Singular neurectomy, 291 75–78, 76f Subjective visual vertical (SVV)
Sitting balance assessment, 373 Speech audiometry, 232 otolith function tests, 201–208, 202f, 203f ,
Situational Vertigo Questionnaire (SVQ), Speech detection threshold (SDT), 232 205f, 206f, 207f, 208f
574–575, 584–585 Speech discrimination score, 232 roll plane, 63, 65, 65f
Skew eye deviation Speech reception threshold (SRT), 232 thalamic and cortical astasia, 67–68
mechanisms of recovery, 395 Speech recognition score, 232 unilateral vestibular deafferentation (UVD),
oculomotor and vestibulo-ocular testing, Spinal cord, 10, 10f, 11–12 126
366–370, 367b, 368b Spinning, sensation of, 163 Suboccipital craniotomy, 287–288, 288f
physical examination, 168, 170, 170f Spinocerebellar ataxia, 559–560 Sudden sensorineural hearing loss (SSNHL),
Skew torsion (contraversive), 62t Spinocerebellar degeneration, tests for, 86–88, 242
Skew-torsion sign, 63, 64 86f, 87t Superior canal dehiscence, 86–88, 86f, 87t,
Smart phone aps, 548–549 Spontaneous emission otoacoustic emissions 253
Smooth pursuit eye movements (SOAE), 236 Superior cerebellar artery, 10f
bilateral vestibular hypofunction, treatment Stability, gaze. See Gaze stability Superior colliculus, 10, 10f
of, 439, 439f Stability, mechanisms for recovery, 98–103, 99f Superior oblique myokymia, 255b
neuropharmacology of vestibular system, Stability limits, 33–34 Superior semicircular canal dehiscence, 245,
252 Stabilometry test, 87t, 91 292, 292f
oculomotor and vestibulo-ocular testing, Stance, patient assessment, 175–176 Superior vestibular neuritis (SVN), 211, 211f
366–370, 367b, 368b Stapedial reflex measures, 232–233, 232f Superior vestibular nuclei, 9, 9f
vestibular function tests, 174, 179, 180f Stapedius muscle, 232–233 Support groups, 365
Smooth pursuit neck torsion test (SPNT), Stapes, 174, 189, 198–199 Support surfaces, sensory information, 34–37,
594–595 Static balance assessment, 373–374, 373t, 35f, 36f, 37f
Social assessment, 114–115, 296–297, 297t 435b Suppurative labyrinthitis, 242
Social environment, disability and, 116 Static defects, 166–168, 167f, 167t, 168f, 168t, Supranuclear palsy (PSP), 559–560
Somatoform disorders, 303 170–172, 171t, 172t, 173f, 173t Surface translations and rotations, posture and,
Somatosensory reflexes. See also Vestibulo- Steady-state stimuli, 236 38–41, 39f, 40f
ocular reflex (VOR) Step-over exercise, 423f, 571, 572f Surgery
aging and, 101–103, 483, 485 Stepping strategy, postural response, 39–40, acoustic neuroma, 123–124, 285–288, 286f,
anatomy and physiology, 13–14, 13f, 14f 40f, 375–376 287f, 288f
assessment of, 370, 436–438, 438f Stepping tests, 87t, 91–92 benign paroxysmal positional vertigo, 52
bilateral vestibular hypofunction, treatment Step rotation, defined, 21 hearing loss management, 243–246, 244f,
of, 441–447, 443b, 444b, 445t, 446t, 447t Stereocilia, 196, 197 245f
center of mass, postural responses, 37–41, Stereotactic radiosurgery, 288 inflammation and cholesteatoma, 292
39f, 40f Sternocleidomastoid muscles, 86, 189, 213 Ménière’s disease, 54–55, 288–290, 291f
central vestibular lesions and, 96–97 Steroids, transtympanic, 289 nystagmus, treatment of, 258
clinical tests of, 86–88, 86f, 87t Strength assessments, 370 perilymphatic fistula, 55, 293, 293f
dynamic posturography, 88–90, 88f Stress reduction, 272 stereotactic radiosurgery, 288
dysfunction of other sensory motor centers, Striola, otoliths, 7–8, 7f, 8f, 197, 197f superior semicircular canal dehiscence, 292,
97–98 Stroke 292f
peripheral vestibular disorders, 92–96, 93t Activities-specific Balance Confidence unilateral vestibular loss, 123
posturography, 190–191, 190f, 191f, 191t, (ABC) scale, 114 vascular loops, surgical management,
192f, 193f brainstem and thalamic infarctions, 63–66, 293–294, 294f
sensory information, weighting of, 34–37, 64t, 65f vestibular schwannoma, 285–288, 286f,
34f, 35f, 36f, 37f Case Study, 261–262, 261f 287f, 288f
3970_Index_617-630 25/06/14 12:53 PM Page 628
628 INDEX
Sway, 35, 35f, 162, 374. See also Balance; Tumors. See also Schwannoma Utricular sac, 196–197
Posture bilateral vestibular disorders, 56 Uvula, lesions of, 97–98
Swimming, sensation of, 163 cerebellopontine angle (CPA) tumors,
Symptom Checklist-90 (SCL-90-R), 300 244–245, 245f
V
Syphilis, 242 in children, 458t Valacyclovir, 253
roll plane dysfunction, 66 Valium (Diazepam), 304t
surgical management, schwannoma,
T Valproate, 257b
285–288, 286f, 287f, 288f
Tablet aps, 548–549 Vascular supply
surgical management, stereotactic
Technology, role of anterior inferior cerebellar artery (AICA),
radiosurgery, 288
augmented sensory biofeedback, 546–548, 9, 10f
upbeat nystagmus, 72–74, 72b, 73f
547f, 548f benign paroxysmal vertigo of childhood,
vertigo and, 51
balance exercises and, 574, 574f 461
vestibular disorders, pitch plane, 69
Case Study, 549–551 brainstem and thalamic infarctions, 63–66,
Tuning fork tests, 227–228, 228f
overview, 537–538 64t, 65f
Tympanic membrane, 228. See also Auditory
platform perturbations, 548 central vestibular disorders, classification
disorders
smart phone and tablet aps, 548–549 of, 60
Tympanometry, 232–233, 232f
virtual reality tools, 538–546, 539t, 540f, cerebellar artery infarction, 175, 175t
Tympanotomy, 55
541f, 542f, 544f, 545b infarction, saccadic eye movement and, 175,
visual vertigo, habituation exercises, 576, 175t
576f U internal auditory canal (IAC), 8
Temporal bone, 3, 3f, 8 UCLA-Dizziness Questionnaire (UCLA-DQ), ischemia of labyrinth artery, 52
Test of Sensory Function in Infants, 463, 113, 114–115, 362f peripheral sensory apparatus, 4–6, 5f
464t Uniform Data System for Medical posterior-inferior cerebellar arteries (PICA),
Thalamic arteries, infarction in, 64–65, 64t Rehabilitation, 112 9, 10f
Thalamic astasia, 59, 62t, 65, 67–68, 79 Unilateral vestibular deafferentation (UVD) thalamic and cortical astasia, 79
Thalamic hemiataxia, 79 animal studies, 138–140, 139f upbeat nystagmus, 72–74, 72b, 73f
Thalamus, 62t, 63–66, 64t, 65f causes of, 123–124 vascular loops, surgical management,
Thalidomide, 57 decompensation, 137–138 293–294, 294f
Thiamine deficiency, 11, 69, 70b medication, 138 vertebral artery compression, 372
Tick-borne illness, 242–243 overview of, 121–123, 122b, 123f vertebral-basilar arterial system, 9, 10f
Tiltboards, 87t, 91 permanent legacies of, 133b vertebrobasilar insufficiency, 327, 590–591,
Tilt of perceived vertical, 62t, 63, 77 poor compensation, 135, 137 599–607
Timed Up and Go (TUG) test, 117, 378, 380, psychological factors, 138 vestibular disorders, pitch plane, 69–74,
559, 577–578 recovery, 131–132, 141–144, 142f 70b, 71b, 72b, 73b
Tinnitus, 53–55, 227–228, 228f, 238–240, 240t sensory components, 131 vestibular disorders, yaw plane, 74
Tinnitus retraining therapy (TRT), 239 summary table, 133t, 134t, 135t vestibular neuritis, 52–53
Tobramycin, 243, 459–460 symptoms of, 124–131, 125f, 126f, 127f, VCR. See Vestibulocollic reflex (VCR)
Tofranil (imipramine), 304t 128f, 129f, 131f Velocity storage mechanism, 14–15
Toluene abuse, 69, 70b vestibular restoration, 133, 135 Venlafaxine, 283, 319t
Tongue electrotactile stimulation, 546–547, VOR plasticity, 140 Vermis, cerebellum, 10, 10f
547f Unilateral vestibular hypofunction (UVH) Vertebral artery compression, 372
Torsional nystagmus, 62t, 68, 169f, 169t adaptation to, 25 Vertebral-basilar arterial system, 9, 10f
Toxic serous labyrinthitis, 52 caloric test, 182–185, 182f, 183f, 184f, Vertebrobasilar artery insufficiency, 327,
Traction, cervical, 600, 602–603, 603f 185b, 186f 590–591, 599–600
Tract of Deiters, 11 compensatory strategies, 151–153, 152f Vertebrobasilar ischemia, 253
Transdermal scopolamine, 254t, 257, 257b patient history, 161t Vertical alignment, posture, 32–34, 33f
Transient ischemic attacks, patient history, Upbeat nystagmus. See also Nystagmus Vertical diplopia, 163
161t assessment of, 62t, 169f, 169t Vertigo. See also Benign paroxysmal
Transient room-tilt illusions, 62t vestibular disorders, pitch plane, 68–74, positional vertigo (BPPV); Clinical
Translabyrinthine approach, acoustic neuroma, 70b, 71f, 72b, 73f decision making paradigm; Disability;
286–287, 287f vestibular upbeat syndrome, 70–74, 72b, 73f Ménière’s disease
Translabyrinthine vestibular nerve section, 55 Usher syndrome, 57, 244 activities of daily living, 117
Transtympanic steroids, 289 Utricle bilateral vestibular disorders, 56–57
Traumatic brain injury. See Head trauma aging, effects of, 481–482 Case Study, 259, 259f
Trihexyphenidyl, 257b anatomy, 3–4, 4f, 196–197 central vestibular disorders, classification of,
Trochlear nucleus IV, 65f function tests, summary table, 219f 60, 61t, 62t, 63t
Trochlear palsy, 66 function tests, unilateral vestibular cervico-ocular reflex and, 12
Truncal stability, 10–11, 10f deafferentation syndrome, 133, 135 in children, 457–458, 458t
Trunk, posture and, 41–42, 41f head motion, response to, 7–8, 7f differential diagnosis, 355–357, 356t, 357t
Tullio phenomenon, 55, 56, 57t, 86–88, 86f, otolith neuron projections, 199–200, 199f environmental causes of, 116
87t, 174 VEMP testing, 210–215, 211f, 212f, 214f epilepsy and, 78
Tumarkin’s otolithic crisis, 53 vestibulospinal system tests, 86–88, 86f, 87t incidence of, 110
3970_Index_617-630 25/06/14 12:53 PM Page 629
INDEX 629
maneuver-induced vertigo, 173–176, 174f, cervical (cVEMP), 130, 131f, 189, 209–215, normal structure and function vs. impairment,
175f, 175t 211f, 212f, 214f 359, 361–362
Ménière’s disease, 53–55 Ménière’s disease, tests for, 215 overview, 359, 360b, 360t, 361t, 362f
migraine and, 266 methods, 213–215, 214f patient goals, 366
nausea and vomiting, 163 ocular (oVEMP), 130–131, 131f, 189, physical therapy, 406
neuropharmacology, 252–253 209–215, 211f, 212f, 214f physical therapy evaluation, overview, 363
paroxysmal central vertigo, 78 schwannoma, 217 positional and movement testing, 371–373,
pathophysiology of, 251–252 semicircular canal dehiscence, 215, 215f, 371t, 372f
patient history, 161t, 163, 251–252 216f, 217f postural examination, 371
perilymphatic fistula, 55–56 uses of, 85, 189, 215–218 postural stabilization exercises, 401
post-traumatic vertigo, treatment of, 290 vestibular neuritis, tests for, 215–217 problem-oriented treatment approach,
Situational Vertigo Questionnaire (SVQ), Vestibular function tests 403–404
584–585 benign paroxysmal positional vertigo, 217 range of motion and strength assessment,
summary chart, disorders, 57t brainstem lesions, 217 370
surgical management, 290–291 caloric test, 182–185, 182f, 183f, 184f, rotational chair test, 185, 186–189, 187f,
tests for, 86–88, 86f, 87t 185b, 186f 188f, 189b
treatment of, 253, 254t electronystagmography (ENG), overview, sensory evaluation, 370
unilateral vestibular deafferentation (UVD), 178, 179f treatment decisions and goals, 381–382,
121, 131 Ménière’s disease, 215 394, 401–403
VEMP tests for, 217 oculomotor function, 178–181, 180f, 181f Vestibular hypofunction, bilateral
vestibular neuritis, 52–53 otolith function tests, 189, 195, 219f assessment of, 434–438, 434b, 435b, 437f,
vestibular paroxysmia, 56 overview, 178 437t, 438f
Vertigo, Dizziness, Imbalance Questionnaire peripheral vestibular disorders, 436 Case Studies, 448–454, 449f, 451f, 453f
(VDI), 113, 115 posturography, 190–191, 190f, 191f, 191t, etiology, 432, 433t
Vertigo Handicap Questionnaire (VHQ), 113, 192f, 193f exercise, evidence for, 440–441, 442t
114, 362f rotational chair test, 185, 186–189, 187f, mechanisms of recovery, 439–440, 439b
Vertigo Symptom Scale (VSS), 112, 113, 114 188f, 189b physical therapy treatments, 441–447, 443b,
Vestibular Activities and Participation (VAP), schwannoma, VEMP tests for, 217 444b, 445t, 446t, 447t
113, 115 semicircular canal dehiscence, 215, 215f, Vestibular insufficiency (VBI), 357
Vestibular Activities of Daily Living scale 216f, 217f Vestibular labyrinthitis, tests for, 86–88, 86f, 87t
(VADL), 112, 113, 115, 362f, 366, 366b, semicircular canal function, 181–182, 182f Vestibular Loss Pattern, 35–36
493 static otolith tests, 200–201 Vestibular Ménière’s disease, 53–55. See also
Vestibular cerebellum, 62t subjective visual horizontal and vertical Ménière’s disease
Vestibular compensation (SVH, SVV), 201–208, 202f, 203f , 205f, Vestibular migraine, 268–269, 269b. See also
animal studies, 138–140, 139f 206f, 207f, 208f Migraine
decompensation, 137–138 VEMP testing (oVEMP, cVEMP), 209–215, in children, 458t, 459
medication, 138 211f, 212f, 214f chronic subjective dizziness and, 310, 311t,
overview of, 121–123, 122b, 123f vestibular neuritis, 215–217 312t
permanent legacies of UVD, 133b visual perception tests, 189–190 tests for, 86–88, 86f, 87t
poor compensation, 135, 137 Vestibular ganglion, anatomy, 4–5, 5f treatment of, 272–273, 273b, 274t, 275b, 275t
psychological factors, 138 Vestibular hypofunction Vestibular nerve. See also Vestibular pathways,
recovery, neural evidence of, 141–144, 142f adaptation to, 25 lesions of
rehabilitation and, 140–141 assessment red flags, 380–381, 381b head movement, response to, 6–7, 6f
sensory components, 131 balance assessment, 373–376, 373t, 374f, Ménière’s disease, 54–55
summary table, 133t, 134t, 135t 375f, 376f neurectomy, 123–124
symptom recovery, 131–132 caloric test, 182–185, 182f, 183f, 184f, otolith neuron projections, 199–200, 199f
unilateral vestibular loss, causes of, 123–124 185b, 186f physiology of, 8
vestibular loss, symptoms of, 124–131, Case Studies, physical therapy, 420–428 velocity storage, 14–15
125f, 126f, 127f, 128f, 129f, 131f clinical examination, 366, 367b, 368b vertigo and, 56, 57t, 251–252
vestibular restoration, 133, 135 coordination assessments, 370 vestibulo-ocular reflex and, 12
VOR plasticity, 140 exercise, evidence for recovery, 411–420, vestibulospinal reflex, 12
Vestibular cortex, 75–78, 76f 415t, 416t, 417t vestibulospinal system tests, 86
Vestibular Disorders Association (VEDA), 365 fall history, 365–366 Vestibular neurectomy, 123–124, 290, 291f
Vestibular electrical stimulation (VES), 546 functional history, 366, 366b Vestibular neuritis
Vestibular epilepsy, 61t, 78 gait evaluation, 376–380, 377f, 378f, 379b, benign paroxysmal positional vertigo,
Vestibular-evoked myogenic potential 380b 326–327, 326t
(VEMP) gaze stabilization exercises, 397–399, 398f bilateral vestibular disorders, 56
advantages and limitations of, 86–88, 86f, 87t habituation exercises, 399–401, 399b, 400t, in children, 458t
benign paroxysmal positional vertigo, test 401t chronic subjective dizziness and, 310, 311t,
for, 217 initial evaluation form, 388–391 312t
brainstem lesions, tests for, 217 mechanisms of recovery, 394–397, 396f, 397f clinical presentation and diagnosis, 52–53, 57t
case study, 204–208, 205f, 206f, 207f, 208f medical history, patient, 363–365, 365t nausea and vomiting, 163
3970_Index_617-630 25/06/14 12:53 PM Page 630
630 INDEX
patient history, 161t Vestibulo-ocular reflex (VOR) motion-provoked dizziness, exercises for,
pseudo-vestibular neuritis, 62t abnormal functioning, 151 574–577, 575t, 576f
semicircular canal redundancy, 7 adaptation, animal studies of, 21–24, 21f, motion sickness, 16–17
skew eye deviation, 168, 170, 170f 23f, 24f optical devices, 257–258, 258f
spontaneous nystagmus, 166–168, 167f, adaptation, human studies of, 24–25, 26f overload, compensation for, 16
167t, 168f, 168t, 169f, 169t adaptation, overview, 20 sensory substitution, 99–100, 99f
VEMP tests, 211–212, 211f, 212f, 215–217 aging and, 102–103 visual-motor training, children, 469–471,
yaw plane disorders and, 74 anatomy and physiology, 592 470t
Vestibular nuclear complex. See also Vestibular bilateral vestibular hypofunction, treatment visual perception tests, 189–190
pathways, lesions of of, 439, 439f visual reflexes, 13
central vestibular lesions and, 96–97 central vestibular disorders, classification of, Visual acuity test, 171, 173f, 369
neuropharmacology, 252–253 59–60, 60f, 61f, 61t, 62t, 63t Visual Analogue Scale (VAS), 165, 165f
peripheral vestibular disorders, 93–96, 93t clinical tests of, 86–88, 86f, 87t Visually Dependent Pattern of Sensory
unilateral vestibular deafferentation (UVD), compensatory strategies, 151–154, 152f, 154f Organization, 36
122 function and dysfunction, 2–3, 3f, 361 Visual tracking assessments, 174
vestibular inputs, processing of, 8–11, 9f, 10f function testing, 366–370, 367b, 368b Visual vertigo, 561t, 562, 576, 576f
vestibulo-ocular reflex and, 12 hypofunction, effects of prediction, 154–155, Visual Vertigo Analog Scale (VVAS), 574–575,
vestibulospinal reflex, 12 155f 586
Vestibular paroxysmia, 56, 57t hypofunction, enhanced smooth pursuit, 155 Vitamin deficiencies, 69, 70b
Vestibular pathways, lesions of mechanisms of recovery, 395–397, 395f, Voit’s nerve, 199–200, 199f
central vestibular falls without vertigo, 396f, 397f Volvular epilepsy, 61t, 78
78–79 motor outputs, 11–12 Vomiting
classification of central vestibular disorders, neuropharmacology, 252–253 patient history, 163
59–60, 60f, 61f, 61t, 62t, 63t normal functioning, 151 vertigo, treatment of, 253, 254t
pitch plane (sagittal) disorders, 68–74, 70b, oculomotor and vestibulo-ocular testing,
71f, 72b, 73f 366–370, 367b, 368b W
roll plane (frontal) disorders, 60, 63–68, 64t, oscillopsia, 163, 255–256, 255b Waardenburg syndrome, 57, 244
65f, 66f, 67f otolith-mediated translational VOR (tVOR), Walk While Talk test (WWT), 558–559, 577–578
thalamic astasia, 79 152–153 Wallenberg’s syndrome
vestibular cortex, 75–78, 76f plasticity of, 140 central vestibular lesions, 59, 77, 97
yaw plane disorders, 74 smooth pursuit, patient assessment, 174 lateropulsion, 79
Vestibular Rehabilitation Benefit Questionnaire vestibular dysfunction, roll plane, 65f patient history, 161t
(VRBQ), 113, 115, 362f vestibular inputs, processing of, 9, 9f roll plane dysfunction, 64–66, 64t, 65f
Vestibular schwannoma VOR cancellation, 174 saccadic eye movements, 175, 175t
surgical management, 285–288, 286f, 287f, Vestibulospinal reflex (VSR) skew eye deviation, 168, 170, 170f
288f clinical tests of, 86–88, 86f, 87t Weber tuning fork test, 227–228, 228f
tests for, 86–88, 86f, 87t function of, 2–3, 3f Wernicke’s encephalopathy, 72–74, 72b, 73f
Vestibular system motor outputs, 11–12 Westphal, Karl, 309
cervical injury and, 592–598 peripheral vestibular disorders, 92–96, 93t Whiplash associated disorders (WAD),
cervical reflexes, 12–13 vestibular inputs, processing of, 9, 9f 592–598, 606–607. See also Cervicogenic
child development and, 461–463, 462f Vibration tests, 370 dizziness
classification of symptoms, 163–164, Vibriotactile biofeedback, 547–548 White matter disease, 486, 571
164t Video infrared (IR) camera, use of, 167t, 168t Wide field of view systems, 541–542, 542f
higher-level processing and problems, Video oculography (VOG), 369 Wii, Nintendo, 543–544, 544f
14–17, 15f Videos, list for clinic and home use, 588–589 World Health Organization (WHO), self-report
inputs, processing of, 8–11, 9f, 10f Virtual reality (VR) technology instruments, 359, 360t, 361t, 362f
motor outputs, 11–12 advantages and disadvantages, 87t World Report on Disability, 111
neuropharmacology, 252–253 overview, 85, 92, 92f, 538–546, 539t, 540f,
peripheral sensory apparatus, 3–6, 3f, 4f, 5f 541f, 542f, 544f, 545b
physiology, periphery, 6–8, 6f, 7f, 8f uses of, 85 X
purpose of, 2–3, 3f visual vertigo, habituation exercises, 576, Xbox 360 Kinect, Microsoft, 538–546, 539t,
repair of, 17 576f 544f, 545b
somatosensory reflexes, 13–14, 13f, 14f Vision. See also Eye movement
visual reflexes, 13 aging, visual deficits, 482–483 Y
Vestibular system disorders. See specific aging and postural reactions, 102 Yaw, defined, 122b
disorder names assessment of, 436 Yaw plane, 59–60, 60f, 74, 131, 141–144, 142f
Vestibule, anatomy, 3–5, 4f, 5f cataracts, 436
Vestibulocerebellum, lesions of, 97–98 cervical kinesthesia exercises, 603–605,
Vestibulocochlear artery, 5, 5f 604f, 605f
Z
Zofran, 254t
Vestibulocollic reflex (VCR), 12 macular degeneration, 436