Parkinsons Disease Rating Scales A Literature Rev

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Parkinson’s disease rating scales: a
literature review
Jamir Pitton Rissardo1,2, Ana L. Fornari Caprara1,2

Website: Abstract:
www.aomd.in A scale is critical for an objective and standardized process in which the purpose involves measuring
DOI: differences between various individuals and determining priorities such as primary treatment goals.
10.4103/AOMD.AOMD_33_19 The aim of this study was to describe and analyze the most common Parkinson’s disease (PD)
scales already used for research and clinical practice. We searched three databases in an attempt
Received : 25 Nov, 2019 to locate existing scales about PD published until 2017 in electronic form, only the articles in English,
Revised : 02 Jan, 2020 Spanish, and Portuguese were reviewed. In sum, 114 scales were evaluated and divided into 6 types
Accepted : 13 Jan, 2020 representing a general evaluation, such as staging, health-related quality of life, evaluation of the
Published : 01 Apr, 2020 impact on activities of daily living, loss of functionality aimed at evaluation of the signs and symptoms
of the disease, evaluation of functioning and disability loss, and other specific evaluations. Other
ORCID number specific evaluations include the following: fear of falling, depression, psychosis, sleep, apathy and
https://orcid. anhedonia, anxiety, dysautonomia, dyskinesia, fatigue, motor fluctuations, psychosocial problems,
org/0000-0001-6179-2177
secondary levodopa effects, Scales for Outcomes in Parkinson’s disease (SCOPA) studies, and
cognitive impairment screening. When required, more specific characteristics of each scale were
included: time to apply, the number of items, advantage, and disadvantage. In the literature, there
are a large number of scales, but the majority of them were created for other diseases and only later
studied for PD. Also, more than half have only a small number of studies with psychometric evaluation
and others can be used for only a specific portion of the general population due to their specific
feature assessment or language availability.
Key words:
Parkinson’s disease, rating, review, scale
Key Messages:
(1) In the literature, there are a large number of scales, but the majority of them were created for
other diseases with later study in Parkinson’s disease.
(2) Some of the scales need a lot of training before the application.
(3) None of the scales is perfect, and it would probably be better to use combined scales even though
we know that they overlap in some aspects.

Introduction on a variety of domains. In addition, the


increasing awareness for nonmotor issues of

A scale is critical for an objective and


standardized process in which the
purpose involves measuring differences
PD has prompted a search for instruments
capable of covering a range of symptoms
from neuropsychiatric and autonomic
between various individuals and determining dysfunction to sleep disturbance and other
priorities such as primary treatment goals.[1] nonmotor aspects.[2] It is worth mentioning
Departments of 1Neurology In this context, valid and reliable scales are that the nonmotor assessment is even more
and 2Medicine, Federal needed to monitor, evaluate, and detect difficult to give a clear clinical description
University of Santa Maria,
the impact of Parkinson’s disease (PD) than the motor issues as it involves a
Santa Maria, Brazil
subjective evaluation and the patient’s
Address for cooperation, which sometimes are difficult
correspondence: This is an open access journal, and articles are distributed under to obtain.
Dr. Jamir Pitton Rissardo, the terms of the Creative Commons Attribution-NonCommercial-
Rua Roraima, Santa ShareAlike 4.0 License, which allows others to remix, tweak, and
Maria, Rio Grande do build upon the work non-commercially, as long as appropriate credit
Sul, Brazil. How to cite this article: Pitton Rissardo J,
is given and the new creations are licensed under the identical terms.
E-mail: jamirrissardo@ Fornari Caprara AL. Parkinson’s disease rating scales:
gmail.com For reprints contact: reprints@medknow.com a literature review. Ann Mov Disord 2020;3:3-22.

© 2020 Annals of Movement Disorders | Published by Wolters Kluwer - Medknow 3


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Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

PD is a progressive neurological disorder that gradually screened the titles and abstracts of all papers found from
results in accumulating disabilities. New finds about the initial search. Disagreements between the authors
pathophysiology and levodopa-induced motor were resolved through discussion.
complications have stimulated the development of new
drugs and surgical techniques that have changed, in many Due to a large number of published scales in the
cases, clinical outcomes throughout the last decades. In literature, we prioritized the description of only some
this way, the present therapeutic interventions demand scales in this review. This selection was based on the
valid instruments for research and clinical uses, and number of citations, reviews’ evaluation that compared
these, on their turn, should be effective enough to assess different scales, and task forces by the “The Movement
all the clinical systems of the patient with PD.[3] Thus, Disorder Society” assessing the recommendations of
it was probably the discovery of new techniques in the scales for PD.
management of PD that boosted the designing of new
scales focusing on specific points of PD based on the We excluded scales not related to PD, scales that were
needing evaluation. However, at the same time that the applied only in a small group of individuals, and scales
focus on certain characteristics of PD increased, fewer without at least one article showing the clinimetric. Also,
patients were evaluated, leading many scales to only cases that were not accessible by electronic methods,
extremely specific studies. including after a request to the authors of the study by
email, were excluded.
For the assessment of PD, there are many different
scales that propose to evaluate diverse fields of PD. Data extraction
This evaluation includes the analysis of disease staging, When provided, we extracted the author’s name, year
quality of life, activities of daily living, impairment, of publication, and country of occurrence, and the
disability, and other specific aspects. However, there is scales’ characteristics assessed were type/subtype,
still little evidence on the psychometric characteristics of time to applicate, number of items, advantages, and
most of these instruments used for this disease, and some disadvantages. The majority of the reports did not
are beneficial only for a specific group of individuals.[4] provide sufficient information about the statistical
This is supported, for example, by the fact that many methods to assess the predictive values of the scales.
scales are not appropriated for both research and clinical The data were extracted by two independent authors,
practice. Also, a significant amount of scales have no double-checked to ensure matching, and organized.
validity in most of the countries where they are applied,
for they were not adequately adapted to the reality of Definition
a foreign population, but instead, only translated from The scales are divided into two groups by their
their original language.[5] Furthermore, it is known that methods: qualitative and quantitative methods.[6] This
many instruments destined to evaluate specific aspects study focused only on qualitative methods. These
of the disease, such as cognitive impairment, are not able methods involve subjective evaluations to inventory the
to do this in a non-biased manner. The aim of this study symptoms, signs, and functional loss.
was to describe and analyze the most common PD scales
used for research and clinical practice. In Table 1, PD scales are organized and are divided into
nine columns:
Methods (a) Type (I, II, III, …)/subtype (1, 2, 3, …) of the scale, that
is: staging (I); health-related quality of life (HRQoL) (II);
Search strategy evaluation of the impact on activities of daily living (III);
We searched three databases, Google Scholar, Health loss of functionality aimed at evaluation of the signs and
Sciences Literature (LILACS), and MEDLINE, in an symptoms of the disease (IV); evaluation of functioning
attempt to locate existing scales about PD published and disability loss (V); and other specific evaluations.
until 2017 in electronic form.. Search terms were “scale, Specific evaluations include the following: fear of falling
evaluation instruments, outcome measures, rating (1); depression (2); psychosis (3); sleep (4); apathy and
scales, validation studies, questionnaire, clinimetric, anhedonia (5); anxiety (6); dysautonomia (7); dyskinesia (8);
fatigue (9); motor fluctuations (10); psychosocial problems
reliability, and validity.” These terms were combined
(11); secondary levodopa effects (12); Scales for Outcomes
with “Parkinson and Parkinson’s disease.” in Parkinson’s disease (SCOPA) studies (13); and cognitive
impairment screening (14).
Inclusion and exclusion criteria These types and subtypes were proposed by the authors of
Original articles, case reports, case series, letters to the this review for better comprehension and understanding
editor, task forces, and poster presentations published of the differences of the scales. They represent the main
until 2017 were included in this review in English, characteristic of the scales and their use. Even though some
Spanish, and Portuguese. The two authors independently scales were not aimed for that subtype, the majority of the

4 Annals of Movement Disorders - Volume 3, Issue 1, January-April 2020


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Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

studies, including the task forces published by the “The caregiver is needed. In this way, when it is obtained
Movement Disorder Society,” evaluated the scale in that by the clinical history that the patient needs his/her
manner. We tried to organize the scales proposed by other caregiver for all basic tasks or is noted a burnout of the
articles, but most of them evaluated only a small number caregiver, this scale could be useful.[23,24]
of scales that were chosen selectively. Also, in an attempt to
use these published organizations, many scales described
The fourth type is about the loss of functionality aimed at
in this article are likely to have more than one classification.
(b) Scale: Sometimes the name was not provided by the authors the evaluation of the signs and symptoms of the disease,
of the article. Therefore, we named according to the reviews which has four scales. They have good reproducibility,
cited or as was commonly named in the literature. but some drawbacks are that some symptoms could not
(c) Reference number. be analyzed. The major sample of this type is UPDRS
(d) Acronym: The acronyms provided are those provided by that captures multiple aspects of PD but fails in the
the clinimetric articles of the scale. evaluation of nonmotor symptoms and in the inadequate
(e) The number of items (items or cognitive domains): Some (ambiguities) instruction for application. Thus, before
scales when used for PD did not assess all the items that applying these scales, the researchers need to spend a
the scale has. Thus, we included only the number of items
significant quantity of time in the development of skills
that were evaluated in PD.
(f) The time required (minutes): The time was obtained from for a uniform and stable evaluation.[24-27]
the review and original articles.
(g) The advantage of the scale was compared with other scales. The fifth type is about functioning and disability, which
(h) The disadvantage of the scale was compared with other has three scales. They are short and easy but only have
scales. few studies in the literature with this type.[24]
(i) Considerations/recommendations already published by
some group in task forces or other reviews. In the sixth type, we resume the scales related to specific
analyses. This category was separated into 14 subtypes.
Discussion The first subtype is about fear of falling, which has four
scales. There are a small number of studies analyzing
The first type of scale is about the staging of PD; the only these scales together, but they have marked differences in
scale until the present moment is Hoehn and Yahr Scale language and some specific details. The articles suggest
that is simple and quick but has low sensitivity in early that FES-I and mSAFFE should be used for the evaluation
stages. These scales are recommended in demographic of activity avoidance due to the risk of falling.[28-35]
presentations of patients and are useful for defining
inclusion and exclusion criteria. In this way, they are one The second subtype is about depression, which has 12
of the fast and easy methods for separating the patients scales. These scales are not specifically made to PD,
in subgroups, when a general analysis is required.[6,7] but the majority of them are easy and quick. Probably,
the best scale to use is the GDS-30 because it is simple,
The second type is HRQoL, which has nine commonly does not have copyright restriction, and is efficient in
used scales. They can be divided into specific and screening depression of PD. However, some have the
generic scales. The specific scales have problems with most specific use: self-administered analysis (BDI),
their restriction in some characteristics of PD as they distinguish depression from dementia (GDS-30), the
superficially or not measure important areas such as severity of depression (IDS-SR, IDS-C), treatment
self-image, sexual function, or the role functionality of efficacy (HAM-D-17), and for more etiological approach
the individual. To be more specific, we cannot take a (MADRS).[36-50]
clear picture of the patient’s overall health. However,
the recommendations are using this type: if an initial The third subtype is psychosis, which has 11 scales. These
evaluation, PDQ-39 and PDQL[8-10] are useful, but if the are divided into specific and generalized scales. The
areas of potential problems need to be identified, PIMS majority of these scales are classified as recommended
should be used.[11] The SIP has the broadest measure or suggested for Parkinson’s psychosis. The most used
among HRQoL. Also, it has important questions about scale is BPRS, but it has some drawbacks when the
writing and sexual dysfunction, but this will be time- characterization of psychotic phenomena is needed.[50,51]
consuming (30 min). It is worth mentioning that PLQ can
be used only in the German population.[12-22] The fourth subtype is about sleep, which has six scales.
These scales are simple and quick. They distinguish in
The third type is an evaluation of the impact on the specific uses such as a focus in nocturnal sleep (PDSS),
activity of daily living, which has four scales. They are sleep habits (PSQI), alertness at time of administration
easy and quick, but the clinimetric properties to PD have (SSS), sleep at a specific point (KSS), sleep in the specific
never been established. The most important use of these eight situations (ESS), and patients at risk of sudden sleep
scales is when an evaluation of the patient and his/her while driving (ISCS).[51-64]

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6
Table  1: Parkinson’s disease rating scales
Types and Scale Reference Acronym Number of Time Advantage Disadvantage Considerations/
Subtypes items (items required recommendations
or cognitive (min)
domains)
(I) Staging (a) Hoehn and Yahr 6,7 HY 1 1 Specific, traditional, simple, and Low sensitivity for early -Used to a
quick stages of the disease demographic
presentation of
patients -Useful for
defining inclusion/
exclusion criteria
(II) Health- (a) Parkinson's Disease 8,9,10 PDQ-39 39 15–20 Specific and validated for many Areas that do not measure: Sensitive to
related quality Questionnaire languages self-image and sexual changes that really
of life (HRQoL) function matter for the
patients, but this
is not the primary
issue in the clinical
evaluation that
focuses primarily
on functionality, so
most appropriate is
HRQoL
(b) Parkinson's Disease 8,9,10 PDQL 37 15–20 Specific and simple Areas that do not measure: Reflects the impact
Quality of Life Questionnaire eating and role function of PD by the own
patient's perspective
(c) Parkinson Impact Scale 8,11 PIMS 10 (two 10 Specific and includes universal Low degree of sensitivity Considered only
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optional precautions in an individual with as a means of


about sexual chronic disease identifying areas of
and financial potential problems
issues)
(d) Parkinson Lebensqualität 11 PLQ 44 15–20 Specific Only for the German Considered as an
population; validity and alternative in areas
sensitivity lower involving German-
speaking patients
(e) EuroQol 12-13 EQ-5D 5 (+visual 4 Generic, brief, simple, and Difficult to get a clear picture
Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

analog scale) attractive to applicate, available of overall health and how it


in many languages has changed within individual
patients
(f) 36-Item Short-Form 14,15 SF-36 36 5 Generic (PD and other
diseases) and multidimensional,
of easy application and
understanding
(g) Nottingham Health Profile 16,17,18 NHP 38 5 Generic and for a patient with Needs further study
chronic diseases in the initial stage of
the PD

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Table  1: Continued
Types and Scale Reference Acronym Number of Time Advantage Disadvantage Considerations/
Subtypes items (items required recommendations
or cognitive (min)
domains)
(h) World Health Organization 19,20,21 WHOQOL-100 100 25 Generic and favors the opinion – –
Quality of Life Questionnaire of the patient
with 100 items
World Health Organization WHOQOL-BREF 26 8 Generic and favors the opinion – –
Quality of Life-BREF of the patient
(i) Sickness Impact Profile 22 SIP 136 30 A broad measure of functional Lengthy-time to applicate The most important
status. questions are about
writing and sexual
dysfunction
(III) Evaluation (a) Schwab and England 23,24 Schwab and 1 1 Easy and simple The clinometric properties of Same researchers
of the impact Activities of Daily Living England ADL this scale have never been are used in the
on activities of Scale established patient and the
daily living caregiver
(b) Northwestern University 24 NUDS or 6 6 – No information about –
Disability Scale NWUDS autonomic dysfunctions,
mental troubles, cognitive
impairment, and social
discomfort
(c) Intermediate Scale for 24 ISAPD x x It has already been
Assessment of PD described

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(d) Extensive Disability Scale 24 EDS 21 15–20 In a clinimetric study, it was It is a modified
considered the best for the version of the
functional status as compared Minimal Record of
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to HY and NUDS Disability


(IV) Loss of (a) Columbia University 24,25 CURS 25 5–10 Good reproducibility with the Early clinical trials
functionality Rating Scale exception of rigidity of L-DOPA
aimed at
evaluation of
the signs and
symptoms of
the disease
Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

(b) Webster Scale 24,26 – 10 – Evaluates better functionality Scarce data on its validity
than disability
(c) Parkinson’s Disease 24 PDIS 10 – Questionable validity It has only one
Impairment Scale study
(d) Unified Parkinson’s 27 UPDRS 42 10–20 A compound scale used to Has absence of screening
Disease Rating Scale capture multiple aspects of questions on several
PD (motor and nonmotor important nonmotor aspects
symptoms) of PD, ambiguities in the
written text, and inadequate
instructions for raters
(V) Evaluation (a) Short Parkinson’s 24 SPES 25 7–10 Short and easy Few studies
of functioning Evaluation Scale
and disability

7
loss
8
Table  1: Continue
Types and Scale Reference Acronym Number of Time Advantage Disadvantage Considerations/
Subtypes items (items required recommendations
or cognitive (min)
domains)
(b) University of California 24 UCLA 21 10–15 Moderate-to-good inter-rater No evidence published, few
Los Angeles Scale reliability studies
(c) New York University 24 NYU 6 7–10 Low validity, few studies
Parkinson’s Disease
Evaluation
(VI) Other
specific
evaluations:
(1) Fear of (a) Falls Efficacy Scale- 28-30 FES-I 16 10 Several languages Evaluates concerns
falling International about falling,
favored the choice
(b) Swedish FES 28,31-32 FES(S) 13 3–5 Used to Swedish people Further studies are needed to Evaluates fall-
verify the validity related self-efficacy;
it is an FES
translated into
Swedish
(c) Activities-Specific Balance 28,33-34 ABC 16 5–10 Wider continuum of activity Ceiling and floor effects in Evaluates balance
Confidence Scale difficulty and more detailed item some reports confidence
descriptors than FES-I
(d) Modified Survey of 28,35 mSAFFE 17 A better choice for active and Less established than FES-I Evaluates activity
Activities and Fear of falling independent community- avoidance due
in the Elderly dwelling older adults to risk of falling,
favored the choice
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(2) Depression (a) Beck Depression 36,46,47 BDI 21 5–10 Assesses the intensity of Does not reflect a particular Designed to be
Inventory depression, today theory of depression administered by
trained interviewers;
it is most often self-
administered.
(b) Center for Epidemiological 37,46,47 CESD-R 20 3 In the past week Few data need more studies
Studies Depression Rating
Scale – Revised
Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

(c) 30-Item Geriatric 40,46,47 GDS-30 30 3 Simple and fast, the most Only elderly people, limited Designed to
Depression Scale efficient depression screening content validity, and appears identify depression
scale to use in PD and no insensitive at the end of the in the elderly by
copyright restriction depression severity spectrum distinguishing
symptoms of
depression and
dementia. -Not used
in severe cognitive
impairment

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Table  1: Continue
Types and Scale Reference Acronym Number of Time Advantage Disadvantage Considerations/
Subtypes items (items required recommendations
or cognitive (min)
domains)
(d) Inventory of Depressive 38,39,46 IDS-SR 30 10–15 Patients may have difficulty To assess the
Symptoms – Patient comprehending severity of,
and change
in, depressive
symptoms
(e) Inventory of Depressive 38,39,46 IDS-C 30 15–20 To assess the
Symptoms Clinician severity of,
and change
in, depressive
symptoms
(f) Patient Health 40,46,50 PHQ-9 9 3 Easy and fast, excellent to use Low sensitive to detect a An algorithm based
Questionnaire-9 in primary care to measuring major depressive disorder on Diagnostic
depression (severity and and Statistical
responsiveness to treatment) Manual Of Mental
Disorders, Fourth
Edition criteria
(g) 17-Item Hamilton 41,46,47 HAM-D-17 17 15–20 Measures the severity of The construction of
Depression Rating Scale depressive symptoms a depression rating
scale designed
to be particularly
sensitive to

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treatment effects is
described.
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(h) Montgomery–Asberg 41,46,47 MADRS 10 15 Measures the of severity of Further studies are required More etiological
Depression Rating Scale depressive symptoms approach
(i) Zung Self-Rating 44,45,47 SDS 20 10 Short and more easily More confusing than GDS-30,
Depression Scale comprehended few studies confirm validity
to PD, and a large number
of somatic items are likely to
infiltrate depression rates
(j) Hospital Anxiety and 40,47 HADS 14 1–2 Easy and fast, excellent to use Has large effect sizes as Evaluates 7-item
Depression Scale in primary care to measuring compared to others and depression and
Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

depression (severity and measures depression 7-item anxiety


responsiveness to treatment)
(k) Cornell Scale for the 43,47 CSDD 19 20–30 It is used with moderate-to- Further studies are required Uses information
Assessment of Depression in severely impaired elders with from an interview
Dementia dementia and shows the with the patient and
effectiveness of interventions, caregiver
especially antidepressant
treatment

9
Table  1: Continue

10
Types and Scale Reference Acronym Number of Time Advantage Disadvantage Considerations/
Subtypes items (items required recommendations
or cognitive (min)
domains)
(l) Major Depression 42,48 MDI 10 5–10 Better than SDS to measure the Emphasizes the intensity of Diagnosis of
Inventory ICD-10 severity of the depression mood symptoms rather than major depression,
its frequency according to either
the DSM-IV criteria
or the ICD-10
criteria.
(3) Psychosis (a) Parkinson Psychosis 50 PPRS 7 5–15 Specifically to assess psychosis Fails to capture Suggested
Rating Scale in PD, short heterogeneous psychosis
in PD
(b) Parkinson Psychosis 50 PPQ 14 5–15 Specifically to PD, cataloging Does not include all Suggested
Questionnaire discrete psychotic phenomena hallucination phenomena;
delusions are more detailed
than hallucinations, although
they are less common in PD
(c) Rush Hallucination 50 – 53 >30 Covers the past 1 month Severity is based on Listed
Inventory emotional association;
delusions are not included
(d) Baylor Parkinson’s 50 – 6 5–15 Easy and quick Rate symptom’s frequency Listed
Disease Hallucination seems disproportionate
Questionnaire
(e) Neuropsychiatric 50 NPI 12 15–30 Many strengths: efficient Its development as an Recommended
Inventory administration, separating instrument to evaluate
symptom’s frequency, some patients with dementia limits
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questions to specific psychotic its application to patients with


phenomena PD who are not demented
(f) Behavioral Pathology in 50 Behave-AD 25 15–30 The delusions and Constructed to Alzheimer’s Suggested
Alzheimer’s Disease Rating hallucinations items detailed disease
Scale rating to the PD
(g) Brief Psychiatric Rating 50 BPRS 18 15–30 It is the most widely used scale Does not provide a detailed Recommended
Scale characterization of the
psychotic phenomena that
occur in PD
Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

(h) Positive and Negative 50 PANSS 30 >30 Detailed definitions, the positive Constructed specifically to Recommended
Syndrome Scale scale also includes behavioral schizophrenia, long and
phenomena complex
(i) Schedule Assessment of 50 SAPS 34 >30 Easy and clear Developed to patients with Recommended
Positive Symptoms schizophrenia
(j) Nurses’ Observation Scale 51 NOSIE-30 30 5–15 Brief and simple, largely used Described to schizophrenic; Listed
for Inpatient Evaluation studies some of the items can be
confounded

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Table  1: Continue
Types and Scale Reference Acronym Number of Time Advantage Disadvantage Considerations/
Subtypes items (items required recommendations
or cognitive (min)
domains)
(l) Clinical Global Impression 51 CGIS 3 <5 A few seconds to complete, Assessment of single items Suggested
Scale maybe be a useful addition to can be confusing
the more sophisticated scales.
(4) Sleep (a) Parkinson’s Disease 54,60,62 PDSS 15 (more an 5 Good to assess potential Insufficient to screen for Focus in nocturnal
Sleep Scale analog scale) causes of “bad-sleep” to specific sleep disorders sleep
differentiate in early and
advanced stages
(b) Pittsburg Sleep Quality 55,61,62 PSQI 19 5–10 More closely related to Is not likely to be useful as To assess sleep
Index psychological symptom ratings screening measures for habits and
and sleep diary measures than polysomnographic sleep disturbances during
the ESS abnormalities; some items are the previous month.
ambiguous and confusing
(c) Stanford Sleepiness Scale 51,56,62 SSS 1 1–2 Simple and quick Never been properly validated The measure of
alertness at the time
of administration.
(d) Karolinska Sleepiness 51,57,63,64 KSS 1 5 Simple and quick Problems with validity and The measure of
Scale too short to assess sleep sleepiness at a
problems specific point in
time.
(e) Epworth Sleepiness Scale 51,58 ESS 8 2–5 Many publications Unsuitable for screening for A measure of how

Annals of Movement Disorders - Volume 3, Issue 1, January-April 2020


episodes of sudden sleep likely the subject
onset in patients with PD. is to a dozen off in
eight situations
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(f) Inappropriate Sleep 62 ISCS 12 2–5 The ISCS is used to capture The clinimetric properties of Identifies patients at
Composite Score excessive daytime sleepiness the ISCS are unknown and risk of sudden onset
appearing even in active it has not been used in a of sleep (SOS)
situations non-PD population, restricted while driving
to evaluating severe daytime
sleepiness.
(5) Apathy and (a) Apathy Evaluation Scale 66,67 AES 18 10–20 Assesses the severity of Problems with validation Suggested
anhedonia apathetic symptoms and may due to lack of consensus on
also be used to follow changes diagnostic criteria
Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

in apathy during treatment


(b) Apathy Inventory 66 AI 3 Undefined Assesses the severity and quick Problems with validation Listed
due to lack of consensus on
diagnostic criteria
(c) Apathy Scale 66 AS 14 Undefined It was developed specifically for Problems with validation Recommended
patients with PD due to lack of consensus on
diagnostic criteria
(d) Lille Apathy Rating Scale 66,68 LARS 33 10 Specifically designed for Longest scale to apathy Suggested
patients with PD

11
Table  1: Continue

12
Types and Scale Reference Acronym Number of Time Advantage Disadvantage Considerations/
Subtypes items (items required recommendations
or cognitive (min)
domains)
(e) Chapman Scales 65,66 – 61 Undefined Most widely used instrument to Problems with validation Listed
for Physical and Social measure anhedonia in patients due to lack of consensus on
Anhedonia with psychiatric diseases diagnostic criteria. The single
study that used the scales in
PD patients concluded that
the scale was not useful
(f) Snaith–Hamilton Pleasure 66 SHAPS 14 Undefined Shorter and simple Problems with validation Suggested
Scale due to lack of consensus on
diagnostic criteria
(6) Anxiety (a) Anxiety Status Inventory 69 ASI 20 Undefined More commonly used in Poorly clinimetric properties Suggested
epidemiological studies of recording the
anxiety in PD presence of anxiety
(b) Zung Self-Rated Anxiety 69,71 SAS 20 5–10 Poorly clinimetric properties Suggested
Scale recording the
presence of anxiety
(c) Beck Anxiety Inventory 69 BAI 21 5–10 Used to screening for symptoms Less suitable to screen for Suggested
of panic attacks in patients with other anxiety disorders
PD
(d) Spielberger State-Trait 69,70 STAI 40 10 Brief and easy No validation for PD and does Suggested
Anxiety Inventory not cover all symptoms of
GAD and panic disorder
(e) Hamilton Anxiety Rating 69,71 HAS It has already been
Scale described
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(f) Hospital Anxiety and 69,70 HADS It has already been


Depression Scale described
(7) (a) Autonomic Dysfunction in 72 – 29 Undefined Specifically to PD This questionnaire has not yet Listed; a global
Dysautonomia Parkinson’s Disease been used in other studies survey of autonomic
and validation is needed symptoms in PD
(b) Composite Autonomic 72 COMPASS 73 20–30 High accuracy in the definition Complex and large Recommended
Symptoms Scale of autonomic symptoms. (with some
limitations)
Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

(c) Freiburg Questionnaire 72,76 – 5 Undefined Short and easy Was not used in other studies Listed
and not validated
(d) Hobson Scale 72,73 – 23 Undefined Designed to estimate the Listed
prevalence of bladder and
autonomic symptoms
(e) l-threo-3,4- 72,74 l-threo-DOPS 10 Undefined Has not yet been used by Listed
Dihydroxyphenylserine Scale other groups
(f) Non-Motor Symptoms 72 NMS-Quest 30 5–7 Easy to score It is not a rating scale It is the first
Questionnaire for Parkinson’s validated tool to
Disease screen for the
presence of NMS
in PD

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Table  1: Continue
Types and Scale Reference Acronym Number of Time Advantage Disadvantage Considerations/
Subtypes items (items required recommendations
or cognitive (min)
domains)
(g) Non-Motor Symptoms 72 NMSS 30 10–15 Questionnaire to quantify NMS The NMSS has not yet been Suggested
Scale and easy to score used by groups other than the
developers
(h) Senard 72,75 – 8 Undefined Does not include frequency Prevalence of
and severity OH and nature of
postural events
related to a fall in
BP in patients with
PD
(i) Orthostatic Grading Scale 72 OGS 5 5 Short, frequency and severity of Has not yet been used Suggested
orthostatic symptoms specifically in patients with
PD
(8) Dyskinesia (a) Abnormal Involuntary 87,94 AIMS 10 14 Does not allow the impact of Clinimetric problems, score Recommended;
Movement Scale dyskinesia on the quality of life to designed other dyskinesia assesses the
besides PD severity of abnormal
movements in
different parts of the
body
(b) Clinical Dyskinesia Rating 87,92 CDRS 10 (five 10 Useful to clinician Has not been used outside of Suggested;
Scale hyperkinesia the developing group independently

Annals of Movement Disorders - Volume 3, Issue 1, January-April 2020


and five evaluates
dyskinesia) hyperkinesia and
dystonic posture
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(c) Lang-Fahn Activities of 87,93 LFADLDS 5 5 Brief and easy On the basis of retrospective Suggested
Day Living Dyskinesia Scale recall of patient, no quality of
life assessment of the impact
of dyskinesia is provided
(d) Obeso Dyskinesia Rating 87,90 CAPIT 3 2 Easy and clear Problems with time frame Suggested
Scale
(e) Parkinson Disease 87,91 PDYS-26 26 10 Specifically made for patients Potential redundancy on Suggested as
Dyskinesia Scale with PD and easy to use modalities of activity a measure for
assessing the
Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

patient’s perception
of functional impact
from dyskinesia
in PD
(f) Rush Dyskinesia Rating 87,88 RDRS 3 5 Assesses functional disability of Assessments are performed Recommended
Scale dyskinesia at the single time points and
the evaluation time point may
or may not reflect the rest, no
consideration made for pain
or discomfort of the day.
(g) Unified Dyskinesia Rating 87,89 UDysRS 26 15 Comprehensive rating tool Has not been studied by Suggested
Scale other groups

13
Table  1: Continue

14
Types and Scale Reference Acronym Number of Time Advantage Disadvantage Considerations/
Subtypes items (items required recommendations
or cognitive (min)
domains)
(9) Fatigue (a) Chalder Fatigue 77,81,86 CFQ 14 3–5 Rather than a measure of Few studies to Parkinson Developed to
Questionnaire impact or consequence, and assess disabling
has physical and mental fatigue severity
domains. in hospital and
community
populations
(b) Clinical Global Impression 78 CGIS x x It has already been
Scale described. Listed to
evaluate fatigue
(c) Fatigue Assessment 78,79 FAI 29 5–10 Various aspects of fatigue and Insufficient data to support Suggested,
Inventory allows comparison between the validity expanded version of
different disease groups the FSS
(d) Fatigue Impact Scale for 78,80 D-FIS 8 2–3 Emphasizes the impact of Little validation studies in PD D-FIS is a listed
Daily Use fatigue rather than the perceived scale for screening
severity for fatigue and
suggested a
measure for daily
assessment of
fatigue severity
(e) Fatigue Severity Inventory 78 FSI 33 5 Diversity of aspects related to Has not been formally Listed
fatigue validated and most of its
psychometric properties are
unknown.
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(f) Fatigue Severity Scale 78,82 FSS 9 2–3 Brief and easy to use, and Does not provide a definition Recommended
translates to various language of the underlying variable it scale for screening
intends to measure. and severity rating
(g) Functional Assessment 78,85 FACIT-F 13 5–10 Brief and easy to use, and Does not provide a clear Recommended
of Chronic Illness Therapy translates to various language definition of the underlying scale for screening
Fatigue Scale variable it intends to measure and suggested
scale for severity
rating.
(h) Multidimensional Fatigue 78 MFI 20 10 Short scale with good The proposed factor structure Suggested
Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

Inventory psychometric properties has not always been


confirmed in independent
studies and there are no data
on the reliability of the scale
in PD.
(i) Parkinson Fatigue Scale- 78,84 PFS-16 16 5 Brief and easy to use, Does not define fatigue Recommended
16 developed specifically for use in scale for screening
patients with PD and suggested
scale for severity
rating

Annals of Movement Disorders - Volume 3, Issue 1, January-April 2020


Table  1: Continue
Types and Scale Reference Acronym Number of Time Advantage Disadvantage Considerations/
Subtypes items (items required recommendations
or cognitive (min)
domains)
(j) Visual Analog Scales 78 VSA Brief and easy to use, and PD has not been validated Listed
generally easy for the subject to
understand
(10) Motor (a) Assessment of Parkinson 97 APDS
fluctuations Disease Scale
(b) Core assessment 97,98 CAPSIT-PD diary Registry for patients with Needs continuum evaluation Recommended;
Program for Surgical PD subjected to functional and few studies it was published
Interventional Therapies in neurosurgery providing the
Parkinson's Disease minimum
requirements for
a common patient
evaluation protocol
(c) Hauser Parkinson’s 102 PD Home Diary Easy and simple Needs more studies Recommended
Disease Home Diary
(d) Intermediate Scale for 99 ISAPD 13 7 Easy to apply and valid Needs more studies
Assessment of PD
(e) Wearing-off 100,101 WOQ-19 19 5 Easy and brief Few studies Recommended
Questionnaire-19
(11) (a) Belastungsfragebogen 95 BELA-P-k 19 Undefined Useful for evaluation of Few studies
Psychosocial Parkinson Kurzversion psychosocial problems

Annals of Movement Disorders - Volume 3, Issue 1, January-April 2020


problems
(12) Secondary(a) Parkinson’s Disease 96 PDSI 51 Undefined Useful patient evaluation tool to Few studies Informative to
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levodopa Symptom Inventory help clinicians assess and track measure changes
effects the symptom-related disease in symptoms and
status of patients. side effects over
time as treatment
progresses.
(13) SCOPA (a) Scale for Outcome in 104 SCOPA-AUT 25 10 Focused on the content and
studies Parkinson's Disease – the clinical applicability of the
Autonomic Dysfunction questionnaire, specifically made
to PD
Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

(b) Scale for outcome in 105,109 SCOPA-COG 10 10–15 Short, reliable, and valid,
Parkinson's Disease – specifically to PD
Cognition
(c) Scale for Outcome in 108 SCOPA- Motor 21 8 Shorter as compared with
Parkinson’s Disease – Motor Scale UPDRS, specifically made to
Scale PD
(d) Scale for Outcome 108 SCOPA-PC 12 10 Shorter, specifically made to Although SCOPA-COG was
in Parkinson's Disease - PD, more likely to be sensitive developed specifically for
Psychiatric Complication to early cognitive changes in the a PD population, it has not
PD population than the MMSE been used extensively in PD.

15
Table  1: Continue

16
Types and Scale Reference Acronym Number of Time Advantage Disadvantage Considerations/
Subtypes items (items required recommendations
or cognitive (min)
domains)
(e) Scale for Outcome in 103 SCOPA-Sleep 11 8 A specific PD rating scale Without exploring potential Asses nocturnal
Parkinson's Disease – Sleep causes of sleep disorders and sleep disorders
Scale somnolence and daytime
somnolence
(14) Cognitive (a) Addenbrooke’s Cognitive 109,119 ACE 6 CD 15–20 Not specifically to PD
impairment Examination
screening
(b) Cambridge Cognitive 117,119 CAMCOG 8CD 25–30 Not specifically to PD, lengthy Assesses cognitive
Assessment function and
screening for
dementia
(c) Dementia Rating Scale 112,113,119 DRS 5CD 15–30 Available in many languages
(d) Mini-Mental Parkinson 118,119 MMP 7CD 10 Quick and useful in detecting an Heavy representation of the
early cognitive change orientation item, which is also
the item contributing least to
scale variance, and a lack
of cortical items, and needs
more studies
(e) Mini-Mental State 111,112,119 MMSE 11 10 Easy and clear, most widely Has not adequate
Examination used screening tool for psychometric to detect mild
detecting dementia cognitive impairment in PD
and does not measure some
cognitive functions that are
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commonly impaired in PD
(f) Montreal Cognitive 110,111,119 MOCA 1CD 10 Easy and clear, has adequate Needs a population with
Assessment psychometric to detect mild greater knowledge than for
cognitive impairment in PD, and the MMSE
available in many languages
(g) Parkinson 115,116,119 PANDA 5CD 8–10 Specifically made to PD, Needs more clinimetric
Neuropsychometric Dementia superiority to MMSE evaluation
Assessment
Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

Annals of Movement Disorders - Volume 3, Issue 1, January-April 2020


Table  1: Continue
Types and Scale Reference Acronym Number of Time Advantage Disadvantage Considerations/
Subtypes items (items required recommendations
or cognitive (min)
domains)
(h) Parkinson’s Disease 114,119 PD-CRS 2CD 15–30 Specifically made to PD Characterized by
Cognitive Rating Scale the addition of
cortical dysfunction
on a predominant
and progressive
fronto-subcortical
impairment recently
conducted a
systematic review
of cognitive scales
used in PD and
identified the
PD-Cognitive Rating
Scale (PD-CRS)
as the optimal
PD-specific scale
for detecting early
cognitive deficits
in PD and tracking
the transition to PD
dementia.

Annals of Movement Disorders - Volume 3, Issue 1, January-April 2020


(i) Parkinson’s Disease 120,122 PDD-SS 8CD 5–7 Specifically made to PD, Quick
Dementia – Short Screen and appears as the first brief
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screening tests for diagnosing


Parkinson’s disease with
dementia as compared MDRS
and MMSE
(j) Repeatable Battery 121,122 RBANS 5CD 20–30 These data suggest that the Not specifically to PD
for the Assessment of RBANS is effective at both
Neuropsychological Status detecting and characterizing
dementia of different etiologies
Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

CD = cognitive domains, I = items, min = minutes, MDRS = mattis dementia rating scale, PD = Parkinson’s disease

17
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Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

The fifth subtype is about apathy and anhedonia, need more studies. CAPSIT-PD diary has a registry for
which has six scales. These are divided into specific patients with PD subjected to functional neurosurgery; it
and generalized scales. The majority of the scales have is recommended and was published providing minimum
problems with their validation and they have been used requirements for a common patient evaluation control.
in a few studies. The only recommended scale is AS that The other two classified as recommended scales and easy
also has problems with validation, but it is specifically to apply are HPDD and WOQ-19.[97-102]
developed for PD. The scales AES and AI are used to
assess the severity, and the AES is used to follow the The 13th subtype is about SCOPA studies. SCOPA
changes of apathy during treatment.[65-67] is a large research project on Scales for Outcomes in
Parkinson’s disease. This study has five scales. SCOPA-
The sixth subtype is about anxiety, which has six scales. AUT is an autonomic scale, which focuses on the clinical
These scales have poorly clinimetric properties. One of applicability of the questionnaire. SCOPA-COG is to
the most used scales is ASI that has 20 items and whose evaluate cognition, which is short, reliable, and valid.
application time is undetermined. The BAI is more used SCOPA-Motor Scale is to evaluate motor symptoms
to assess panic attacks in PD.[68-71] and is quick compared with UPDRS. SCOPA-PC is to
evaluate psychiatric complications; it is relatively short
The seventh subtype is about dysautonomia, which has and is more likely to be sensitive to early cognitive
nine scales. These scales were used only in a few studies, changes in the PD population than the MMSE. SCOPA-
so their clinimetric properties are not consolidated. Sleep assesses nocturnal sleep disorders and daytime
The recommended (but with some limitations) scale to somnolence.[60,103-108]
evaluate dysautonomia are COMPASS, because it has
high accuracy in the definition of autonomic symptoms The 14th subtype is about cognitive impairment screening,
in PD but is much complex and large as compared to the which has 10 scales. These scales are easy and quick.
other scales of evaluation of dysautonomia.[72-76] The best scales are PDD-SS, mattis dementia rating
scale (MDRS), and MMSE. The MMSE is the widely
The eighth subtype is dyskinesia, which has seven scales. used screening measure for detecting dementia, but the
All of them can assess dyskinesia and are useful to clinimetric evaluation in PD to detect mild cognitive
clinician, brief, and simple to apply. The problems with impairment has not been adequately stabilized. The MOCA
these scales are that these are used only in a few studies has more adequate clinimetric properties, but a higher
and their clinimetric properties are not consolidated. The formal knowledge is required compared to the MMSE.[109-122]
recommended scales are AIMS and RDS. The AIMS is
best to assess the severity of dyskinesia and the RDS to
Conclusion
assess functional disability, but the time spent to apply
the AIMS is about twice the RDS.[77-84] In sum, 114 scales are evaluated in Table 1 and divided
into 6 types. In the literature, there are a large number of
The ninth subtype is about fatigue, which has 10 scales.
scales and every year more and more scales are published
These scales are brief and easy, but have problems with
for the assessment of PD. However, the majority of them
clinimetric evaluation because of few studies and not
have only a small number of studies with psychometric
clearly defining the variable that it intends to measure.
evaluation, and others can be used for only a specific
The recommended scales to screening the fatigue are
portion of the general population due to their characteristic
FSS, FACIT-F, and PFS-16 (made specific to PD); the
features such as language availability. Also, some of the
only one scale recommended to evaluate the severity
newly developed scales are incorporating part of other
is FSS.[85-94]
ratings instead of only citing them; this gives the medical
The 10th subtype is about psychosocial problems. This literature a confusing assessment, when evaluating these
subtype has only one scale, the Belastungsfragebogen grading systems, and turns them into long, confusing,
Parkinson Kurzversion (BELA-P-k). This scale has only and difficult to apply clinically. Therefore, we believe
a few studies and is in German.[95] that instead of developing new scales, the studies should
focus on the clinimetric evaluation, and assess these
The 11th subtype is about levodopa secondary effects. scales in different ethnic origins translating the scales and
This subtype has only one scale, the Parkinson’s Disease evaluating their quality.
Symptom Inventory (PDSI). It is useful for helping
clinicians to measure changes in symptoms and side Financial support and sponsorship
effects over the treatment time, but it has few studies.[96] Nil.

The 12th subtype is about motor fluctuations, which Conflicts of interest


has five scales. All of them have little evidence and There are no conflicts of interest.
18 Annals of Movement Disorders - Volume 3, Issue 1, January-April 2020
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Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

References WHO quality of life assessment instrument (WHOQOL-100).


Braz J Psychiatry 1999; 21:19-28.
1. Pocinho M, Figueiredo JP. Methods and Techniques of Scientific 20. Bittencourt ZZLC, Alves Filho G, Mazzali M, Santos NR. Quality
Research. Coimbra, Portugal: Escola Superior Tecnologia da Saúde of life in kidney transplant recipients: Importance of a functioning
de Coimbra; 2004. graft. Rev Saúde Pública 2004;38:732-4.
2. Chaudhuri  KR, Odin  P, Antonini  A, Martinez-Martin  P. 21. Hirayama MS, Gobbi S, Gobbi LT, Stella F. Quality of life (QoL)
Parkinson’s disease: The non-motor issues. Parkinsonism Relat in relation to disease severity in Brazilian Parkinson’s patients
Disord 2011;17:717-23. as measured using the WHOQOL-BREF. Arch Gerontol Geriatr
2008;46:147-60.
3. Martínez-Martín P, Rodríguez-Blázquez C, Mario A, Arakaki T,
Arillo VC, Chaná P, et al. Parkinson’s disease severity levels and 22. Longstreth WT Jr, Nelson L, Linde M, Muñoz D. Utility of the
MDS-unified Parkinson’s disease rating scale. Parkinsonism Relat sickness impact profile in Parkinson’s disease. J Geriatr Psychiatry
Disord 2015;21:50-4. Neurol 1992;5:142-8.
4. Rito  M. Parkinson's disease: assessment tools. Arq Fisioter 23. McRae C, Diem G, Vo A, O’Brien C, Seeberger L. Reliability of
2006;2:27-45. measurements of patient health status: A comparison of physician,
patient, and caregiver ratings. Parkinsonism Relat Disord
5. Martinez‐Martin P, Schrag A, Weintraub D, Rizos A, Rodriguez‐
2002;8:187-92.
Blazquez C, Chaudhuri KR, et al. Pilot study of the International
Parkinson and Movement Disorder Society‐sponsored Non‐Motor 24. Ramaker C, Marinus J, Stiggelbout AM, Van Hilten BJ. Systematic
Rating Scale (MDS‐NMS). Mov Disord Clin Pract 2019;6:227-34. evaluation of rating scales for impairment and disability in
Parkinson’s disease. Mov Disord 2002;17:867-76.
6. Levy A. Parkinson's Disease: A Practical Guide. Lisboa, Portugal:
Técnicas; 2003. 25. Harder  S, Baas  H. Concentration‐response relationship of
levodopa in patients at different stages of Parkinson’s disease.
7. Goetz  CG, Poewe  W, Rascol  O, Sampaio  C, Stebbins  GT,
Clin Pharmacol Ther 1998;64:183-91.
Counsell C, et al.; the Movement Disorder Society Task Force on
Rating Scales for Parkinson’s Disease. Movement Disorder Society 26. Geminiani  G, Cesana  BM, Tamma  F, Contri  P, Pacchetti  C,
Task Force report on the Hoehn and Yahr staging scale: Status and Carella F, et al. Interobserver reliability between neurologists in
recommendations. Mov Disord 2004;19:1020-8. training of Parkinson’s disease rating scales: A multicenter study.
8. Damiano  AM, Snyder  C, Strausser  B, Willian  MK. A review Mov Disord 1991;6:330-5.
of health-related quality-of-life concepts and measures for 27. Disease MDS. The Unified Parkinson’s Disease Rating Scale
Parkinson’s disease. Qual Life Res 1999;8:235-43. (UPDRS): Status and recommendations. Mov Disord 2003;18:738-
9. Peto  V, Jenkinson  C, Fitzpatrick  R. PDQ-39: A  review of the 50.
development, validation and application of a Parkinson’s disease 28. Jonasson SB, Nilsson MH, Lexell J. Psychometric properties of four
quality of life questionnaire and its associated measures. J Neurol fear of falling rating scales in people with Parkinson’s disease.
1998;245:S10-4. BMC Geriatr 2014;14:66.
10. Hobson  P, Holden  A, Meara  J. Measuring the impact of 29. Yardley L, Beyer N, Hauer K, Kempen G, Piot-Ziegler C, Todd C.
Parkinson’s disease with the Parkinson’s disease quality of life Development and initial validation of the Falls Efficacy Scale-
questionnaire. Age Ageing 1999;28:341-6. International (FES-I). Age Ageing 2005;34:614-9.
11. Marinus  J, Ramaker  C, van  Hilten  JJ, Stiggelbout  AM. Health 30. Tinetti ME, Richman D, Powell L. Falls efficacy as a measure of
related quality of life in Parkinson’s disease: A systematic review fear of falling. J Gerontol 1990;45:P239-43.
of disease specific instruments. J Neurol Neurosurg Psychiatry 31. Hellström K, Lindmark B, Fugl-Meyer A. The Falls-Efficacy Scale,
2002;72:241-8. Swedish version: Does it reflect clinically meaningful changes
12. Luo  N, Chew  LH, Fong  KY, Koh  DR, Ng  SC, Yoon  KH, et  al. after stroke? Disabil Rehabil 2002;24:471-81.
Validity and reliability of the EQ-5D self-report questionnaire 32. Nordell E, Andreasson M, Gall K, Thorngren K-G. Evaluating the
in English-speaking Asian patients with rheumatic diseases in Swedish version of the Falls Efficacy Scale-International (FES-I).
Singapore. Qual Life Res 2003;12:87-92. Adv Physiother 2009;11:81-7.
13. Devlin  NJ, Parkin  D, Browne  J. Patient-reported outcome 33. Powell LE, Myers AM. The Activities-specific Balance Confidence
measures in the NHS: New methods for analysing and reporting (ABC) Scale. J Gerontol Ser A 1995;50:28-34.
EQ-5D data. Health Econ 2010;19:886-905. 34. Kressig  RW, Wolf  SL, Sattin  RW, O’Grady  M, Greenspan  A,
14. Pagani TCS, Junior CRP. Health-related quality of life assessment Curns  A, et  al. Associations of demographic, functional, and
instruments. Ensaios Ciência 2006;1:32-7. behavioral characteristics with activity-related fear of falling
15. Brazier  JE, Harper  R, Jones  NM, O’Cathain  A, Thomas  KJ, among older adults transitioning to frailty. J Am Geriatr Soc
Usherwood  T, et  al. Validating the SF-36 health survey 2001;49:1456-62.
questionnaire: New outcome measure for primary care. BMJ 35. Li F, Fisher KJ, Harmer P, McAuley E, Wilson NL. Fear of falling
1992;305:160-4. in elderly persons: Association with falls, functional ability, and
16. Teixeira-Salmela  LF, Magalhães  LC, Souza  AC, Lima  MC, quality of life. J Gerontol B Psychol Sci Soc Sci 2003;58:P283-90.
Lima RCM, Goulart F. Nottingham Health Profile adaptation: a 36. Beck AT, Steer RA, Carbin MG. Psychometric properties of the
simple tool for assessing the quality of life. Cad Saúde Pública Beck Depression Inventory: Twenty-five years of evaluation. Clin
2004;20:905-14. Psychol Rev 1988;8:77-100.
17. Hagell  P, Whalley  D, McKenna  SP, Lindvall  O. Health status 37. Van  Dam  NT, Earleywine  M. Validation of the Center for
measurement in Parkinson’s disease: Validity of the PDQ‐39 and Epidemiologic Studies Depression Scale–Revised (CESD-R):
Nottingham Health Profile. Mov Disord 2003;18:773-83. Pragmatic depression assessment in the general population.
18. Ebrahim S, Barer D, Nouri F. Use of the Nottingham health profile Psychiatry Res 2011;186:128-32.
with patients after a stroke. J Epidemiol Community Health 38. Rush AJ, Carmody T, Reimitz PE. The Inventory of Depressive
1986;40:166-9. Symptomatology (IDS): Clinician (IDS‐C) and Self‐Report (IDS‐
19. Fleck MP, Leal OM, Louzada SN, Xavier MK, Chachamovich E, SR) ratings of depressive symptoms. Int J Methods Psychiatr Res
Vieira GM, et al.Development of the Portuguese version of the 2000;9:45-59.

Annals of Movement Disorders - Volume 3, Issue 1, January-April 2020 19


[Downloaded free from http://www.aomd.in on Monday, May 11, 2020, IP: 10.232.74.22]

Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

39. Rush  AJ, Gullion  CM, Basco  MR, Jarrett  RB, Trivedi  MH. The 60. Martinez-Martin P, Visser M, Rodriguez-Blazquez C, Marinus J,
Inventory of Depressive Symptomatology (IDS): Psychometric Chaudhuri  KR, van  Hilten  JJ; SCOPA-Propark Group; ELEP
properties. Psychol Med 1996;26:477-86. Group. SCOPA-Sleep and PDSS: Two scales for assessment of
40. Smarr  KL, Keefer  AL. Measures of depression and depressive sleep disorder in Parkinson’s disease. Mov Disord 2008;23:1681-8.
symptoms: Beck Depression Inventory-II (BDI-II), Center for 61. Shulman  LM, Taback  RL, Rabinstein  AA, Weiner  WJ. Non-
Epidemiologic Studies Depression Scale (CES-D), Geriatric recognition of depression and other non-motor symptoms in
Depression Scale (GDS), Hospital Anxiety and Depression Scale Parkinson’s disease. Parkinsonism Relat Disord 2002;8:193-7.
(HADS), and Patient Health Questionnaire-9 (PHQ-9). Arthritis 62. Högl B, Arnulf I, Comella C, Ferreira J, Iranzo A, Tilley B, et al.
Care Res (Hoboken) 2011;63:S454-66. Scales to assess sleep impairment in Parkinson’s disease: Critique
41. Montgomery SA, Asberg M. A new depression scale designed to and recommendations. Mov Disord 2010;25:2704-16.
be sensitive to change. Br J Psychiatry 1979;134:382-9. 63. Chaudhuri  KR, Pal  S, DiMarco  A, Whately-Smith  C,
42. Bech P, Rasmussen NA, Olsen LR, Noerholm V, Abildgaard W. Bridgman K, Mathew R, et al. The Parkinson’s Disease Sleep
The sensitivity and specificity of the major depression inventory, Scale: A  new instrument for assessing sleep and nocturnal
using the present state examination as the index of diagnostic disability in Parkinson’s disease. J Neurol Neurosurg Psychiatry
validity. J Affect Disord 2001;66:159-64. 2002;73:629-35.
43. Ownby RL, Harwood DG, Acevedo A, Barker W, Duara R. Factor 64. Marinus J, Visser M, van Hilten JJ, Lammers GJ, Stiggelbout AM.
structure of the Cornell scale for depression in dementia for Anglo Assessment of sleep and sleepiness in Parkinson disease. Sleep
and Hispanic patients with dementia. Am J Geriatr Psychiatry 2003;26:1049-54.
2001;9:217-24. 65. Isella V, Iurlaro S, Piolti R, Ferrarese C, Frattola L, Appollonio I,
44. Zung WW, Richards CB, Short MJ. Self-rating depression scale et  al. Physical anhedonia in Parkinson’s disease. J Neurol
in an outpatient clinic: Further validation of the SDS. Arch Gen Neurosurg Psychiatry 2003;74:1308-11.
Psychiatry 1965;13:508-15. 66. Leentjens  AF, Dujardin  K, Marsh  L, Martinez-Martin  P,
45. Yesavage JA, Brink TL, Rose TL, Lum O, Huang V, Adey M, et al. Richard  IH, Starkstein  SE, et  al. Apathy and anhedonia rating
Development and validation of a geriatric depression screening scales in Parkinson’s disease: Critique and recommendations.
scale: A preliminary report. J Psychiatr Res 1982;17:37-49. Mov Disord 2008;23:2004-14.
46. Williams  JR, Hirsch  ES, Anderson  K, Bush  AL, Goldstein  SR, 67. Marin  RS, Biedrzycki  RC, Firinciogullari  S. Reliability and
Grill S, et al. A comparison of nine scales to detect depression in validity of the apathy evaluation scale. Psychiatry Res 1991;38:
Parkinson disease: Which scale to use? Neurology 2012;78:998- 143-62.
1006. 68. Sockeel P, Dujardin K, Devos D, Denève C, Destée A, Defebvre L.
47. Schrag A, Barone P, Brown RG, Leentjens AF, McDonald WM, The Lille Apathy Rating Scale (LARS), a new instrument for
Starkstein S, et al. Depression rating scales in Parkinson’s disease: detecting and quantifying apathy: Validation in Parkinson’s
Critique and recommendations. Mov Disord 2007;22:1077-92. disease. J Neurol Neurosurg Psychiatry 2006;77:579-84.
48. Bech  P, Wermuth  L. Applicability and validity of the Major 69. Leentjens AF, Dujardin K, Marsh L, Martinez-Martin P, Richard IH,
Depression Inventory in patients with Parkinson’s disease. Nord Starkstein SE, et al. Anxiety rating scales in Parkinson’s disease:
J Psychiatry 1998;52:305-10. Critique and recommendations. Mov Disord 2008;23:2015-25.
49. Manea L, Gilbody S, McMillan D. A diagnostic meta-analysis of the 70. Julian  LJ. Measures of anxiety: State-Trait Anxiety Inventory
patient health questionnaire-9 (PHQ-9) algorithm scoring method (STAI), Beck Anxiety Inventory (BAI), and Hospital Anxiety
as a screen for depression. Gen Hosp Psychiatry 2015;37:67-75. and Depression Scale-Anxiety (HADS-A). Arthritis Care Res
(Hoboken) 2011;63:S467-72.
50. Fernandez HH, Aarsland D, Fénelon G, Friedman JH, Marsh L,
71. Zung  WW. A rating instrument for anxiety disorders.
Tröster AI, et al. Scales to assess psychosis in Parkinson’s disease:
Psychosomatics 1971;12:371-9.
Critique and recommendations. Mov Disord 2008;23:484-500.
72. Pavy‐Le  Traon  A, Amarenco  G, Duerr  S, Kaufmann  H,
51. Thorpy  MJ, Billiard  M. Sleepiness: Causes, Consequences and
Lahrmann H, Shaftman SR, et al. The movement disorders task
Treatment. Cambridge, UK: Cambridge University Press; 2011.
force review of dysautonomia rating scales in Parkinson’s disease
52. Ellis BW, Johns MW, Lancaster R, Raptopoulos P, Angelopoulos N, with regard to symptoms of orthostatic hypotension. Mov Disord
Priest RG. The St. Mary’s hospital sleep questionnaire: A study 2011;26:1985-92.
of reliability. Sleep 1981;4:93-7.
73. Hobson P, Islam W, Roberts S, Adhiyman V, Meara J. The risk of
53. Parrott AC, Hindmarch I. Factor analysis of a sleep evaluation bladder and autonomic dysfunction in a community cohort of
questionnaire. Psychol Med 1978;8:325-9. Parkinson’s disease patients and normal controls. Parkinsonism
54. Chaudhuri KR, Pal S, DiMarco A, Whately-Smith C, Bridgman K, Relat Disord 2003;10:67-71.
Mathew  R, et  al. The Parkinson’s Disease Sleep Scale: A  new 74. Mathias  CJ. L-dihydroxyphenylserine (droxidopa) in the
instrument for assessing sleep and nocturnal disability in treatment of orthostatic hypotension: The European experience.
Parkinson’s disease. J Neurol Neurosurg Psychiatry 2002;73:629- Clin Auton Res 2008;18:25-9.
35.
75. Senard JM, Raï S, Lapeyre-Mestre M, Brefel C, Rascol O, Rascol A,
55. Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ. The et al. Prevalence of orthostatic hypotension in Parkinson’s disease.
Pittsburgh Sleep Quality Index: A new instrument for psychiatric J Neurol Neurosurg Psychiatry 1997;63:584-9.
practice and research. Psychiatry Res 1989;28:193-213. 76. Magerkurth C, Schnitzer R, Braune S. Symptoms of autonomic
56. Saadat S, Sadeghian F, Fayaz M. Sleepiness and fatigue among failure in Parkinson’s disease: Prevalence and impact on daily
night-shift nurses with three-hour nap and day-shift nurses. Int life. Clin Auton Res 2005;15:76-82.
J Health Stud 2016;2:24-30. 77. Colosimo  C, Martínez-Martín  P, Fabbrini  G, Hauser  RA,
57. Akerstedt T, Gillberg M. Subjective and objective sleepiness in Merello M, Miyasaki J, et al. Task force report on scales to assess
the active individual. Int J Neurosci 1990;52:29-37. dyskinesia in Parkinson’s disease: Critique and recommendations.
58. Johns MW. A new method for measuring daytime sleepiness: The Mov Disord 2010;25:1131-42.
Epworth Sleepiness Scale. Sleep 1991;14:540-5. 78. Goetz  CG, Stebbins  GT, Shale  HM, Lang  AE, Chernik  DA,
59. Douglass AB, Bornstein R, Nino-Murcia G, Keenan S, Miles L, Chmura TA, et al. Utility of an objective dyskinesia rating scale for
Zarcone VP Jr, et al. The sleep disorders questionnaire. I: Creation Parkinson’s disease: Inter- and intrarater reliability assessment.
and multivariate structure of SDQ. Sleep 1994;17:160-7. Mov Disord 1994;9:390-4.

20 Annals of Movement Disorders - Volume 3, Issue 1, January-April 2020


[Downloaded free from http://www.aomd.in on Monday, May 11, 2020, IP: 10.232.74.22]

Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

79. Goetz  CG, Nutt  JG, Stebbins  GT. The unified dyskinesia A comprehensive and sensitive instrument to measure disease
rating scale: Presentation and clinimetric profile. Mov Disord symptoms and treatment side-effects. Parkinsonism Relat Disord
2008;23:2398-403. 1999;5:93-8.
80. Langston JW, Widner H, Goetz CG, Brooks D, Fahn S, Freeman T, 97. Defer  GL, Widner  H, Marié  RM, Rémy  P, Levivier  M. Core
et al. Core assessment program for intracerebral transplantations Assessment Program for Surgical Interventional Therapies in
(CAPIT). Mov Disord 1992;7:2-13. Parkinson’s Disease (CAPSIT-PD). Mov Disord 1999;14:572-84.
81. Katzenschlager  R, Schrag  A, Evans  A, Manson  A, Carroll  CB, 98. Reimer  J, Grabowski  M, Lindvall  O, Hagell  P. Use and
Ottaviani D, et al. Quantifying the impact of dyskinesias in PD: interpretation of on/off diaries in Parkinson’s disease. J Neurol
The PDYS-26: A  patient-based outcome measure. Neurology Neurosurg Psychiatry 2004;75:396-400.
2007;69:555-63. 99. Group TC, Martínez-Martin P, Gil-Nagel A, Gracia LM, Gómez JB,
82. Hagell P, Widner H. Clinical rating of dyskinesias in Parkinson’s Martínez-Sarriés  FJ, et  al. Intermediate scale for assessment of
disease: Use and reliability of a new rating scale. Mov Disord Parkinson’s disease: Characteristics and structure. Parkinsonism
1999;14:448-55. Relat Disord 1995;1:97-102.
83. Group  PS. Evaluation of dyskinesias in a pilot, randomized, 100. Stacy M, Hauser R. Development of a patient questionnaire to
placebo-controlled trial of remacemide in advanced Parkinson facilitate recognition of motor and non-motor wearing-off in
disease. Arch Neurol 2001;58:1660-8. Parkinson’s disease. J Neural Transm (Vienna) 2007;114:211-7.
84. Whall  AL, Engle  V, Edwards  A, Bobel  L, Haberland  C. 101. Abbruzzese  G, Antonini  A, Barone  P, Stocchi  F, Tamburini  T,
Development of a screening program for tardive dyskinesia: Bernardi  L, et  al. Linguistic, psychometric validation and
Feasibility issues. Nurs Res 1983;32:151-6. diagnostic ability assessment of an Italian version of a 19-item
85. Cho HJ, Costa E, Menezes PR, Chalder T, Bhugra D, Wessely S. wearing-off questionnaire for wearing-off detection in Parkinson’s
Cross-cultural validation of the Chalder Fatigue Questionnaire disease. Neurol Sci 2012;33:1319-27.
in Brazilian primary care. J Psychosom Res 2007;62:301-4. 102. Hauser RA, Friedlander J, Zesiewicz TA, Adler CH, Seeberger LC,
86. Friedman JH, Alves G, Hagell P, Marinus J, Marsh L, Martinez- O’Brien  CF, et  al. A home diary to assess functional status in
Martin P, et al. Fatigue rating scales critique and recommendations patients with Parkinson’s disease with motor fluctuations and
by the movement disorders society task force on rating scales for dyskinesia. Clin Neuropharmacol 2000;23:75-81.
Parkinson’s disease. Mov Disord 2010;25:805-22. 103. Visser M, Marinus J, Stiggelbout AM, Van Hilten JJ. Assessment of
87. Schwartz JE, Jandorf L, Krupp LB. The measurement of fatigue: autonomic dysfunction in Parkinson’s disease: The SCOPA-AUT.
A new instrument. J Psychosom Res 1993;37:753-62. Mov Disord 2004;19:1306-12.
88. Fisk JD, Doble SE. Construction and validation of a Fatigue Impact 104. Marinus J, Visser M, Verwey NA, Verhey FR, Middelkoop HA,
Scale for Daily Administration (D-FIS). Qual Life Res 2002;11:263- Stiggelbout  AM, et  al. Assessment of cognition in Parkinson’s
72. disease. Neurology 2003;61:1222-8.
89. Chalder  T, Berelowitz  G, Pawlikowska  T, Watts  L, Wessely  S, 105. Martínez-Martín  P, Benito-León  J, Burguera  JA, Castro  A,
Wright D, et al. Development of a fatigue scale. J Psychosom Res Linazasoro  G, Martínez-Castrillo  JC, et  al. The SCOPA-Motor
1993;37:147-53. Scale for Assessment of Parkinson’s disease is a consistent and
90. Kleinman L, Zodet MW, Hakim Z, Aledort J, Barker C, Chan K, valid measure. J Clin Epidemiol 2005;58:674-9.
et al. Psychometric evaluation of the fatigue severity scale for use 106. Martínez-Martín P, Carroza-García E, Frades-Payo B, Rodríguez-
in chronic hepatitis C. Qual Life Res 2000;9:499-508. Blázquez  C, Forjaz  MJ, de  Pedro-Cuesta  J; Grupo ELEP.
91. Martinez-Martin  P, Catalan  MJ, Benito-Leon  J, Moreno  AO, [Psychometric attributes of the SCales for Outcomes in
Zamarbide  I, Cubo  E, et  al. Impact of fatigue in Parkinson’s PArkinson’s disease – Psychosocial (SCOPA-PS): Validation in
disease: The Fatigue Impact Scale for Daily Use (D-FIS). Qual Spain and review]. Rev Neurol 2009;49:1-7.
Life Res 2006;15:597-606. 107. Marinus  J, Visser  M, Martínez-Martín  P, van  Hilten  JJ,
92. Brown  RG, Dittner  A, Findley  L, Wessely  SC. The Parkinson Stiggelbout AM. A short psychosocial questionnaire for patients
fatigue scale. Parkinsonism Relat Disord 2005;11:49-55. with Parkinson’s disease: The SCOPA-PS. J Clin Epidemiol
2003;56:61-7.
93. Yellen  SB, Cella  DF, Webster  K, Blendowski  C, Kaplan  E.
Measuring fatigue and other anemia-related symptoms with the 108. Reyes  M, Lloret  S, Gerscovich  E, Martin  M, Leiguarda  R,
functional assessment of cancer therapy (FACT) measurement Merello M. Addenbrooke’s Cognitive Examination validation in
system. J Pain Symptom Manage 1997;13:63-74. Parkinson’s disease. Eur J Neurol 2009;16:142-7.
94. Hewlett  S, Dures  E, Almeida  C. Measures of fatigue: Bristol 109. Nasreddine  ZS, Phillips  NA, Bédirian  V, Charbonneau  S,
Rheumatoid Arthritis Fatigue Multi-Dimensional Questionnaire Whitehead V, Collin I, et al. The Montreal Cognitive Assessment,
(BRAF MDQ), Bristol Rheumatoid Arthritis Fatigue Numerical MOCA: A brief screening tool for mild cognitive impairment. J
Rating Scales (BRAF NRS) for severity, effect, and coping, Chalder Am Geriatr Soc 2005;53:695-9.
Fatigue Questionnaire (CFQ), Checklist Individual Strength 110. Hoops S, Nazem S, Siderowf AD, Duda JE, Xie SX, Stern MB, et al.
(CIS20R and CIS8R), Fatigue Severity Scale (FSS), Functional Validity of the MOCA and MMSE in the detection of MCI and
Assessment Chronic Illness Therapy (fatigue) (FACIT-F), Multi- dementia in Parkinson disease. Neurology 2009;73:1738-45.
Dimensional Assessment of Fatigue (MAF), Multi-Dimensional 111. Aarsland D, Andersen K, Larsen JP, Perry R, Wentzel-Larsen T,
Fatigue Inventory (MFI), Pediatric Quality of Life (PedsQL) Multi- Lolk A, et al. The rate of cognitive decline in Parkinson disease.
Dimensional Fatigue Scale, Profile of Fatigue (ProF), Short Form Arch Neurol 2004;61:1906-11.
36 Vitality Subscale (SF-36 VT), and Visual Analog Scales (VAS). 112. Llebaria  G, Pagonabarraga  J, Kulisevsky  J, García-Sánchez  C,
Arthritis Care Res (Hoboken) 2011;63:S263-86. Pascual-Sedano B, Gironell A, et al. Cut-off score of the Mattis
95. Spliethoff-Kamminga  NG, Zwinderman  AH, Springer  MP, Dementia Rating Scale for screening dementia in Parkinson’s
Roos  RA. Psychosocial problems in Parkinson’s disease: disease. Mov Disord 2008;23:1546-50.
Evaluation of a disease-specific questionnaire. Mov Disord 113. Pagonabarraga  J, Kulisevsky  J, Llebaria  G, García-Sánchez  C,
2003;18:503-9. Pascual-Sedano  B, Gironell  A. Parkinson’s disease-cognitive
96. Hogan  T, Grimaldi  R, Dingemanse  J, Martin  M, Lyons  K, rating scale: A new cognitive scale specific for Parkinson’s disease.
Koller W. The Parkinson’s Disease Symptom Inventory (PDSI): Mov Disord 2008;23:998-1005.

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Pitton Rissardo and Fornari Caprara: Parkinson’s disease rating scales

114. Kalbe E, Calabrese P, Kohn N, Hilker R, Riedel O, Wittchen HU, Group. A recommended scale for cognitive screening in clinical
et  al. Screening for cognitive deficits in Parkinson’s disease trials of Parkinson’s disease. Mov Disord 2010;25:2501-7.
with the Parkinson Neuropsychometric Dementia Assessment 119. Pagonabarraga  J, Kulisevsky  J, Llebaria  G, García-Sánchez  C,
(PANDA) instrument. Parkinsonism Relat Disord 2008;14:93-101. Pascual-Sedano B, Martinez-Corral M, et al. PDD-Short Screen:
115. Dávila G, Berthier ML, Kulisevsky J, Asenjo B, Gómez J, Lara JP, A  brief cognitive test for screening dementia in Parkinson’s
et  al. Structural abnormalities in the substantia nigra and disease. Mov Disord 2010;25:440-6.
neighbouring nuclei in Tourette’s syndrome. J Neural Transm 120. Thaler  NS, Hill  BD, Duff  K, Mold  J, Scott  JG. Repeatable
(Vienna) 2010;117:481-8. Battery for the Assessment of Neuropsychological Status
116. Kulisevsky J, Pagonabarraga J. Tolerability and safety of ropinirole (RBANS) intraindividual variability in older adults:
versus other dopamine agonists and levodopa in the treatment Associations with disease and mortality. J Clin Exp
of Parkinson’s disease: Meta-analysis of randomized controlled Neuropsychol 2015;37:622-9.
trials. Drug Saf 2010;33:147-61. 121. Randolph  C, Tierney  MC, Mohr  E, Chase  TN. The Repeatable
117. Pagonabarraga J, Corcuera-Solano I, Vives-Gilabert Y, Llebaria G, Battery for the Assessment of Neuropsychological Status
García-Sánchez  C, Pascual-Sedano  B, et  al. Pattern of regional (RBANS): Preliminary clinical validity. J Clin Exp Neuropsychol
cortical thinning associated with cognitive deterioration in 1998;20:310-9.
Parkinson’s disease. PLoS One 2013;8:e54980. 122. Chaudhuri  KR, Odin  P, Antonini  A, Martinez-Martin  P.
118. Chou KL, Amick MM, Brandt J, Camicioli R, Frei K, Gitelman D, Parkinson’s disease: The non-motor issues. Parkinsonism Relat
et  al.; Parkinson Study Group Cognitive/Psychiatric Working Disord 2011;17:717-23.

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