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Orthopaedic Biomechanics in Sports

Medicine Jason Koh


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Jason Koh
Stefano Zaffagnini
Ryosuke Kuroda
Umile Giuseppe Longo
Farid Amirouche
Editors

Orthopaedic
Biomechanics in
Sports Medicine
Orthopaedic Biomechanics in Sports
Medicine
Jason Koh • Stefano Zaffagnini
Ryosuke Kuroda • Umile Giuseppe Longo
Farid Amirouche
Editors

Orthopaedic
Biomechanics
in Sports Medicine
Editors
Jason Koh Stefano Zaffagnini
Department of Orthopaedic Surgery IRCCS – Rizzoli Orthopaedic Institute –
Orthopaedic & Spine Institute 2nd Orthopaedic and Trauma Unit
NorthShore University HealthSystem University of Bologna
Skokie, Illinois Bologna
USA Italy

Ryosuke Kuroda Umile Giuseppe Longo


Department of Orthopaedic Surgery Department of Orthopaedic and
Kobe University Graduate School of Trauma Surgery
Medicine Campus Bio-Medico University
Kobe Trigoria, Rome
Japan Italy

Farid Amirouche
Department of Orthopaedic Surgery
Orthopaedic & Spine Institute
NorthShore University Health System
Evanston, Illinois
USA

ISBN 978-3-030-81548-6    ISBN 978-3-030-81549-3 (eBook)


https://doi.org/10.1007/978-3-030-81549-3

© ISAKOS 2021
This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or
part of the material is concerned, specifically the rights of translation, reprinting, reuse of
illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way,
and transmission or information storage and retrieval, electronic adaptation, computer software,
or by similar or dissimilar methodology now known or hereafter developed.
The use of general descriptive names, registered names, trademarks, service marks, etc. in this
publication does not imply, even in the absence of a specific statement, that such names are
exempt from the relevant protective laws and regulations and therefore free for general use.
The publisher, the authors, and the editors are safe to assume that the advice and information in
this book are believed to be true and accurate at the date of publication. Neither the publisher nor
the authors or the editors give a warranty, expressed or implied, with respect to the material
contained herein or for any errors or omissions that may have been made. The publisher remains
neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This Springer imprint is published by the registered company Springer Nature Switzerland AG
The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland
Foreword

Biomechanics is the bridge between biology and orthopaedic surgery!


Musculoskeletal biomechanics has a very long history. In the fifteenth cen-
tury, Leonardo da Vinci studied biomechanics of muscles and bones in the
human body. Later, Galileo Galilei used mechanics to describe force, motion,
and strength of materials. By the seventeenth century, Sir Isaac Newton gave
us the laws of physics.
Since the 1970s, orthopaedic biomechanics has experienced an explosive
growth as engineers and surgeons began to work together and used biome-
chanical principles to study tissue behaviour and joint motion, to evaluate
body function as well as to develop mathematical models and computation
methods for better implant design. Biomechanics has become a part of the
regular curriculum in orthopaedic education. It became clear that a good
understanding of biomechanics and quantitative data is essential for success-
ful clinical management of patients.
It is so timely for the International Society of Arthroscopy, Knee Surgery,
and Orthopaedic Sports Medicine (ISAKOS) to ask Drs. Jason Koh, Stefano
Zaffagnini, Ryosuke Kuroda, Umile Giuseppe Longo, and Farid Amirouche
to lead the efforts in preparing a textbook entitled Orthopaedic Biomechanics
in Sports Medicine.
These editors are to be congratulated for carefully selecting and assem-
bling a strong list of corresponding authors from around the world. The topics
covered (33 chapters) are relevant and encompassing. These chapters are
logically organized into eight (8) parts that flow seamlessly from Basic
Principles of Biomechanics and Properties of Materials to Biomechanics of
Shoulder, Elbow, Hip, Knee, Ankle, and Foot, and ending with Tissue Repair
Techniques.
Moreover, the materials presented have a strong international flavour. This
writer knows almost all of the corresponding authors personally and has a
high regard for their knowledge and clinical expertise. As such, each chapter
will provide the reader with materials on biomechanics that are comprehen-
sive and clinically relevant as well as translational.

v
vi Foreword

It is without a doubt that this book will be of significant value to the


ISAKOS community, especially for our young and up and coming surgeons
in orthopaedic sports medicine.

Savio L. -Y. Woo


Musculoskeletal Research Center
Department of Bioengineering
Swanson School of Engineering
University of Pittsburgh
Pittsburgh, PA, USA
Preface

On behalf of the editors, contributing authors, and the International Society


of Arthroscopy, Knee Surgery, and Orthopaedic Sports Medicine (ISAKOS),
it is with great pleasure that we invite you to enjoy our book Orthopaedic
Biomechanics in Sports Medicine.
Knowledge of orthopaedic biomechanics is fundamental to understanding
normal function, injury, repair, and recovery in sports medicine. Over the past
several years, there have been many recent advances, spurred by the growth
and development of such areas as image analysis, robotics, and finite element
analysis. Researchers have used these techniques to build upon existing infor-
mation to gain a better understanding of how the body moves and functions.
In this book, an international team of experts has come together to provide
a comprehensive introduction to orthopaedic biomechanics. These clinicians
and researchers have a profound understanding of biomaterials, tissues, and
joint function from the shoulder and elbow to the hip, knee, and ankle. Based
on the newest research and analytical techniques, this book is intended to
assist clinicians, researchers, and students in gaining a background in ortho-
paedic biomechanics as it relates to sports medicine.
As editors and authors, it has been a pleasure to create this work, and we
hope you find this book interesting and informative. We have all been stu-
dents and learned from many pioneers before us and hope that this contrib-
utes to further understanding and future progress in orthopaedic
biomechanics.
Many thanks,

October 2021
Evanston, IL, USA Jason Koh
Bologna, Italy Stefano Zaffagnini
Kobe, Japan Ryosuke Kuroda
Rome, Italy Umile Giuseppe Longo
Chicago, IL, USA Farid Amirouche

vii
Contents

Part I Basic Principles in Orthopaedic Biomechanics

1 Biomechanics of Human Joints������������������������������������������������������   3


Farid Amirouche and Jason Koh
2 Shoulder Muscles Moment Arm Contribution
to Glenohumerol Joint Motion and Stability�������������������������������� 15
Jason Koh, Lorenzo Chiari, and Farid Amirouche

Part II Biomechanical Properties of Orthopaedic Materials

3 Biomechanics of Ligaments������������������������������������������������������������ 27
Jonathan D. Hughes, Calvin K. Chan, Sene K. Polamalu,
Richard E. Debski, and Volker Musahl
4 Biomechanics of Bone Grafts and Bone Substitutes�������������������� 37
Daniel R. Lee and James W. Poser
5 Mechanical and Biologic Properties of Articular
Cartilage Repair Biomaterials�������������������������������������������������������� 57
George Jacob, Kazunori Shimomura, David A. Hart,
Hiromichi Fujie, and Norimasa Nakamura
6 Biomechanical Properties of Fibrocartilage���������������������������������� 73
Jongkeun Seon
7 Tendon Biomechanics-Structure and Composition���������������������� 81
Stefano Zaffagnini, Jason Koh, Umile Giuseppe Longo,
Giovanna Stelitano, Farid Amirouche, and Vincenzo Denaro
8 Biomechanical Properties of Orthopedic Materials: Muscle������ 91
George A. Komnos and Jacques Menetrey
9 FEA Applications for Orthopedics: An Overview������������������������ 99
Umile Giuseppe Longo, Giovanna Stelitano,
Giuseppe Salvatore, Vincenzo Candela, Calogero Di Naro,
Laura Risi Ambrogioni, Farid Amirouche,
and Vincenzo Denaro

ix
x Contents

Part III Shoulder Biomechanics

10 Anatomy and Kinematics of the Shoulder Joint �������������������������� 111


Alfonso Ricardo Barnechea Rey
11 Biomechanics of Rotator Cuff Injury and Repair������������������������ 135
Giacomo Dal Fabbro, Margherita Serra, Giuseppe Carbone,
Alberto Grassi, Khalid Al-Khelaifi, and Stefano Zaffagnini
12 Biomechanics of Shoulder Instability and Repair������������������������ 149
John Fritch, Andre Labbe, Jacques Courseault,
and Felix Savoie
13 Biomechanics of the Throwing Shoulder �������������������������������������� 161
John Fritch, Amit Parekh, Andre Labbe, Jacques Courseault,
Felix Savoie, Umile Giuseppe Longo, Sergio De Salvatore,
Vincenzo Candela, Calogero Di Naro, Carlo Casciaro, and
Vincenzo Denaro
14 Biomechanics of Acromioclavicular Joint Injury and Repair ���� 173
Matthew R. LeVasseur, Michael B. DiCosmo, Rafael Kakazu,
Augustus D. Mazzocca, and Daniel P. Berthold

Part IV Elbow Biomechanics

15 Elbow Anatomy and Biomechanics������������������������������������������������ 193


Andrea Celli, Bartoli Matteo, Peruzzi Marco,
and Luigi Adriano Pederzini
16 Orthopaedics Biomechanics in Sports Medicine
Thrower’s Elbow������������������������������������������������������������������������������ 203
Luigi Adriano Pederzini, A. F. Cheli, F. Nicoletta,
Giovanna Stelitano, and Andrea Celli
17 Elbow Tendon Injury and Repair: Triceps
and Biceps Tendons�������������������������������������������������������������������������� 211
Andrea Celli, Cheli Andrea, Bartoli Matteo,
and Luigi Adriano Pederzini

Part V Hip Biomechanics

18 Biomechanics of Hip Function�������������������������������������������������������� 231


Kyle R. Sochacki and Marc R. Safran
19 Biomechanics of Femoroacetabular Impingement ���������������������� 243
Seper Ekhtiari, Luc Rubinger, Aaron Gazendam,
and Olufemi R. Ayeni
20 Biomechanics of Soft Tissue Injuries about the Hip �������������������� 253
Ran Atzmon and Marc R. Safran
Contents xi

Part VI Knee Biomechanics

21 Biomechanics of the Knee �������������������������������������������������������������� 271


Farid Amirouche and Jason Koh
22 Anatomy and Biomechanics of the Anterior
Cruciate Ligament �������������������������������������������������������������������������� 287
Daniel Guenther, Elmar Herbst, and Volker Musahl
23 Biomechanics of Extra-Articular Ligaments of the Knee and
Extra-­Articular Tenodesis �������������������������������������������������������������� 297
Pablo Besa, Timothy Lording, and Sebastián Irarrázaval
24 Anatomy and Biomechanics of the Collateral Ligaments
of the Knee���������������������������������������������������������������������������������������� 311
Kanto Nagai, Yuta Nakanishi, Kohei Kamada, Yuichi Hoshino,
and Ryosuke Kuroda
25 PCL Biomechanics �������������������������������������������������������������������������� 321
Leonard Tiger Onsen and Jason Koh
26 Biomechanics of Osteotomies around the Knee���������������������������� 331
Dominic T. Mathis and Michael T. Hirschmann
27 Meniscus Biomechanics ������������������������������������������������������������������ 345
Alberto Grassi, Giacomo Dal Fabbro, Stefano Di Paolo,
Gian Andrea Lucidi, Luca Macchiarola, Khalid Al-Khelaifi,
and Stefano Zaffagnini
28 Patellofemoral Biomechanics���������������������������������������������������������� 361
John J. Elias and S. Cyrus Rezvanifar
29 Biomechanics of Cruciate Retaining and Posterior
Stabilised Total Knee Arthroplasty and Return to Sports ������   377
A. Kropelnicki and D. A. Parker
30 Biomechanics of Unicompartmental Knee Replacement ������������ 391
Johanna Elliott and Myles Coolican
Part VII Ankle and Foot Biomechanics
31 Biomechanics of the Ankle Joint������������������������������������������������   401
Krishna C. Ravella, Jamal Ahmad, and Farid Amirouche
32 Biomechanics of the Ankle Joint in Relation to Ankle
Ligament Injuries������������������������������������������������������������������������   415
Marshall Haden, Jamal Ahmad, and Farid Amirouche

Part VIII Biomechanics of Tissue Repair Techniques

33 Biomechanics of Cartilage Repair����������������������������������������������   431


Tomoya Iseki, Benjamin B. Rothrauff, Kazunori Shimomura,
and Norimasa Nakamura
Part I
Basic Principles in Orthopaedic
Biomechanics
Biomechanics of Human Joints
1
Farid Amirouche and Jason Koh

1.1 Introduction Related challenges to TSA include edge


contact-­ friction loading and rim stress due to
The mechanics of the shoulder joint has been the eccentric loading of glenoid implant resulting
subject of numerous studies focusing mostly on from migration and translation of the humeral
three clinical complications such as the glenoid head causing the rocking-horse phenomenon [9],
implant loosening [1–3], rotator cuff repair [4, 5], this is an inherent problem due to implant bone
and total shoulder arthroplasty [6, 7]. TSA has fixation. So, bone–material interface and meth-
consistently provided successful outcomes for ods of fixation including the bony stock condi-
patients with severe arthritis [8], and patients tions for the glenoid dictate the course of success
where rotator cuff repair was unsuccessful result- and become a real challenge to overcome. This is
ing in joint instability and cruciate pain. The GH associated with several contributing parameters
joint is the most mobile joint in the human body, such as glenoid asymmetric bone loss, glenoid
supported and guided by a structure composed of rim defect, bony conditions and depth, and sizing
rotator cuff muscles, ligaments, and an intrinsic of the onlay or inset and bone removal.
cartilaginous glenoid surface that conforms to the It’s obvious that the complexity of the GH joint
humeral head geometry. is one that requires modeling and analysis to gain
insight into its kinematic-kinetic function.
F. Amirouche Modeling of the human joint using a simple 2D or
Department of Orthopaedic Surgery, Orthopaedic & 3D model has usually evolved around the knee,
Spine Institute NorthShore University Health System,
hip and spine but very few models exist for the
Evanston, Illinois, USA
shoulder joint. This is due in part to the shoulder
Department of Orthopeadic Surgery, College of
griddle complexity in terms of articulating sur-
Medicine, University of Illinois,
Chicago, Illinois, USA faces and muscle structures and ligaments that
e-mail: FAmirouche@northshore.org, make up the anatomy of the GH joint. Current
amirouch@uic.edu shoulder models include the one by a group in
J. Koh (*) Sweden [10, 11] related to the model of Hogfors
Department of Orthopaedic Surgery, Orthopaedic & et al. [12, 13], the Newcastle shoulder model [14],
Spine Institute NorthShore University HealthSystem,
the shoulder part of the AnyBody Modeling
Skokie, Illinois, USA
System [15], the open SIMM Stanford model [16],
University of Chicago Pritzker School of Medicine,
and the Delft Shoulder Model (DSM) to name few.
Chicago, Illinois, USA
These complex musculoskeletal models of the
Northwestern University McCormick School of
shoulder and upper arm have been developed to
Engineering, Evanston, Illinois, USA

© ISAKOS 2021 3
J. Koh et al. (eds.), Orthopaedic Biomechanics in Sports Medicine,
https://doi.org/10.1007/978-3-030-81549-3_1
4 F. Amirouche and J. Koh

study the shoulder joint and its muscles during muscles. The relationship between these forces
abduction-adduction. Biomechanical models are can be observed by calculating the absolute force
essential tools for simulation and predictions of of the individual groups of muscle fibers. It was
clinical scenarios not feasible with standard confirmed that a linear relationship between mus-
in vivo studies. cle force and cross-sectional area is found in all
Computer modeling and simulation of human muscles. Hogfors early work [18], investigated
joints has risen to new heights in recent years, the force vectors for different muscles around the
mainly because of the medical needs and advances shoulder joint including greater pectoral muscle,
in imaging and sensors technology. The growing trapezius, deltoid, infraspinatus muscle, and sub-
belief that models can provide more quantitative scalpular muscle. Each muscle is defined as a
explanations of how the neuromuscular and mus- vector with coordinates system defined by the
culoskeletal systems interact to produce move- relative insertion point of each muscle on the
ment is vital to orthopedic surgeons. major bones in the system.
Dynamic models provide knowledge of mus- Pitching in baseball has drawn a lot of interest
cles and joint reaction forces, stress-strain behav- from past and current researchers as the number
ioral responses to load, micromotion injuries of professional athletes became crucial in
measurements and potential pitfalls which are understanding the mechanism of injury due to
invaluable to the clinician. They provide essential high forces and moments produced by the mus-
parameters to the design, validation of orthopedic cles. Andrews et al. [19] study was performed to
implants and patient-specific orthopedic solu- try to understand how the biceps are potentially
tions. Recent studies use computed tomography responsible for the tear of the glenoid labrum.
(CT) images to build patient-specific 3D models Karlsson et al. [20] followed with additional
which are then used to assist the clinicians to work on muscle forces predictions at the shoulder
visualize the pathology more in depth and pro- joint as function of abduction angle in the sagittal
pose new orthopedic solutions. Through different plane. The goal is to create 3D force contribution
simulation studies one can minimize complica- to the joint and understand the balance issue as it
tions by selecting the right size of implants and relates to each muscle. The challenge of validat-
demonstrate a definitive path for best outcome ing these forces is to compare the model data to
solution. This is all virtual allowing for interac- ECG. This is still work in progress but modeling
tion and evaluation of clinical benefits to patients. in 3D is evolving rapidly with the help of imaging
To create realistic shoulder models cadaveric techniques and multibody dynamics software. As
studies are used to improve on the assumptions of is the case most of the 3D models are redundant
the GH joint under different constraints condi- systems and require optimization. Predicted
tions and address the limit of range of motion forces deviate considerably from EMG results.
associated with translation and rotation. The first Delft Shoulder Model [21] consists
Preserving the patient natural motion is key to of a comprehensive 3D inverse-dynamic model
understanding the shoulder joint stability and of the shoulder used to evaluate the muscle and
kinematics. joint contact forces, muscle lengths, and moment
The role of the muscles forces and their cor- arms. The muscle force data was validated using
responding moment arms are crucial in the analy- force–time curves and EMG signals [22]. The
sis of less conforming prostheses designed for the study by Debski et al. [23] was used to measure
replacement of GH joint. Detailed multibody the in situ force distribution inside the glenohu-
muscle forces provide the only feasible method to meral joint capsule as well as the compliance of
quantifying or evaluating the dynamics of the the joint under a load. Ten cadaver shoulders
shoulder joint under different loading conditions. were studied and the in situ force was measured
Early work by Duca et al. [17] used a simple during varying angles of abduction.
2D model to investigate the relationship of the Research by Huang et al. [24] focused on the
forces between the deltoid and supraspinatus supraspinatus muscle and the supraspinatus
1 Biomechanics of Human Joints 5

t­ endon under uniaxial loading. This a load to fail- design of onlay and inset can be addressed as
ure test where strains and stresses are recorded function of the bone quality of the patients.
until the tendon failed. Additional force modeling Modeling and simulations combined leads to bet-
and inverse dynamics can be found in work by ter understanding of the GH shoulder implants
Holzbaur et al. [25] where the muscle force-­ design.
generating characteristics are determined using a
Hill-type muscle model.
Additional experimental work was needed to 1.2 Anatomy of the Shoulder
validate modeling techniques of muscle forces.
The shoulder joint muscles moment arms were The shoulder and its structural support constitute
evaluated by Ackland et al. [26], where eight the human joint with greatest mobility. Its anat-
cadavers were used and the moments for seven omy is such that it possesses motion capabilities
major shoulder muscle groups were recorded for to perform and support extraneous loads and
three different motions: scaption, coronal plane tasks. From pitching in baseball and mastering
abduction, and flexion. the speed of ball delivery to heavy lifting, upper
The contact pressure at the glenoid humeral extremities strength and stability are essential to
interface is critical in determining the effects of successful gymnasts trying to achieve another
rotator cuff repair, total shoulder arthroplasty on high level performance, and therefore, with ver-
the balancing and kinematics of the joints. In satility and strength come injuries and risks. The
essence, reconstruction of the joint affects the glenohumeral joint (GH) has a bony congruity at
contact and hence several studies looked into this its articulating surfaces which render its kinemat-
problem. Hammond et al. [27] used seven cadav- ics and stability a major factor contributing to the
ers to measure the contact area and contact pres- shoulder integrity and longevity. The shoulder
sure of the glenohumeral joint at different joint has to rely on its connective tissues, adja-
abduction angles. Measurements for contact area cent ligaments, and muscles to provide and main-
and pressure were made using Tekscan sensors. tain stability.
There is some evidence that the humeral head The Rotator Cuff is made up of muscles ten-
translation contributes to the instability and con- dons that merge together to form a capsule around
straints resulting from Reverse shoulder con- the shoulder joint used to keep the humeral head
struction surgery of the shoulder joint [28], in the socket joint. Hence, it supports the GH
clinically through X-rays and CT scan one can joint in its rotational motion and constraints its
measure how much translation the humeral head movement to maintain stability. Tendons in the
actually migrates in the superior direction other- rotator cuff can be injured easily because of their
wise we need to use cadaveric shoulders and try limited range of motion and load as they bounded
to measure the humeral head during abduction-­ to limited stretch within a bounded joint space.
adduction of the upper arm and validate the trans- The four important tendons that form the rota-
lation part. Quental et al. [29] assumed an ideal tor cuff are Subscapularis, Supraspinatus,
spherical GH joint and validated the assumptions Infraspinatus, and Teres Minor (see Fig. 1.1).
with cadaver and in vivo studies. He simulated These muscles are made up of numerous muscle
the humeral translation and reported that the GH fibers which in turn are made up of myofibrils.
joint translations can’t be measured experimen- These myofibrils contain regions called Z discs
tally because the limitations of conventional where two adjacent Z discs make up the
motion systems. Sarcomeres. The sarcomeres are the smallest
Finally, it is worth mentioning that the geom- functional unit of a muscle and are responsible
etry of the glenoid bone loss can be evaluated, for the contractile activities of the muscle [31].
and custom glenoid models can be designed and The role each of these muscles play has been
3D printed to address patient-specific orthopedic the subject of a number of investigations, for
problems. Gunther et al. [30] described how the instance the subscapularis is seen to have the
6 F. Amirouche and J. Koh

Tendon for
Supraspinatus
infraspinatus

Tendon for teres


minor

Teres Minor

Infraspinatus

Fig. 1.1 Anterior View of Right Shoulder. A CT based model with Rotator Cuff muscles

highest capacity of force production followed by (2) flat or (3) convex. There are various postero-­
infraspinatus, supraspinatus and, teres minor inferior rim shapes which play a crucial role in
[32]. Subscapularis has upper 60% insertion ten- fitting and keeping the humeral head to be secure
dinous and lower 40% insertion muscular [33]. In within the glenoid cavity. The rim is still not quite
absence of the supraspinatus, Deltoid takes over well understood in terms of whether it should be
the function of shoulder elevation completely preserved during a resurfacing as it is completely
[34] where otherwise the deltoid is only respon- sacrificed during the Onlay resurfacing of the
sible for a 90° abduction before the supraspinatus glenoid. In clinical studies, there are three main
perform the rest. In absence of Supraspinatus, it shapes that have been proposed that best describe
is found that there is 101% increase in middle the rim geometry: triangular, J, and delta. The J
deltoid force generation to initiate the abduction and delta shapes are found to play a key role in
[35]. posterior shoulder instability [36].
In addition to the rotator cuff and its muscles
the humeral head sits in a congruent surface
called the glenoid which forms a cavity that acts 1.3 Kinematics of the Shoulder
as the articular surface at the lateral side of the
scapula. It is concave with a cartilaginous glenoid The humeral head and the glenoid articular sur-
fossa, retroverted and measures 6–8 cm2. face are congruent and rotate similar to a ball
Inferiorly, the articular cartilage may be thin and socket joint within certain range of motion. The
fibrous. Superiorly, intra-articularly, the supra- humeral head is believed to be more convex in
glenoid tubercle serves as the attachment site for the anterior-posterior direction than in the
the long head of biceps tendon. superior-inferior.
There are three main shapes of the glenoid Kinematics is strictly limited to angular dis-
surface described in the literature: (1) concave, placements, angular speed and angular
1 Biomechanics of Human Joints 7

a­ccelerations for rotational motion. It is also 23“anterior to the scapular plane with the arm in
associated with translational motion where dis- 35” of external rotation. Harryman et al. [39]
placement, velocity, and acceleration of specific demonstrated that translation of the humeral head
points such as the humeral head center or any is accompanied by passive movements of the gle-
other points critical to the analysis. These kine- nohumeral joint. The humeral head translates
matical parameters are often affected by the joint either anteriorly or posteriorly and this can be
pathology, geometric properties, kinematical and seen when the arm is in flexion or extension. This
geometrical constraints resulting from muscles forced translation is thought to be induced by the
and ligaments. In the case of the GH joint we are tightening of the capsule-ligamentous structures
mostly concerned by changes in kinematics during motion. Excessive tightness of the ante-
resulting from rotator cuff tears, arthritic condi- rior capsule after anterior capsulorrhaphy leads
tions at the joint or simply the arthroplasty effects to posterior subluxation.
on the joint and patient joint mobility.
The humeral head looks like a sphere and this
was confirmed by Soslowsky et al. [37] in their 1.4 Modeling and Dynamic
experiments where they concluded that the artic- Analysis of the GH Joint
ular surface of the humeral head could be approx-
imated by a sphere with small deviations of less 1.4.1  E Models of Glenohumeral
F
than 1% of the radius. This is further supported Joint Stability
by Boileau and Walch [38] where they estimated
that the difference between the two diameters of The shoulder is the most frequently dislocated
the humeral head assumed is less than 1 mm in joint. The dislocation is usually due to a trau-
88.2% of the tested specimens. They also reported matic injury or loosing of the capsular ligaments.
during the arm elevation that the superior-inferior Anterior dislocation is defined as when the top of
translation of the humeral head is only 0.3– the humerus is displaced forward, toward the
0.35 mm in normal shoulders. front of the body. This is the most common type
Glenohumeral kinematics is driven by con- of shoulder dislocation, accounting for more than
nective forces that have some points of attach- 95% of cases. A shoulder subluxation refers to a
ments to the joint structure mechanism. Any partial dislocation of the shoulder joint. The
changes to the muscles forces result in different 10-year incidence rate of shoulder dislocations
kinematics of the shoulder joint. Tracking the in US Army soldiers is around 3.13%. Complexity
humeral elevation for a healthy human joint can of the GH joint is such that one needs more
provide a base reference from which one can sophisticated tools to examine the shoulder
assess the results of rotator cuff tears which are response to shoulder structural integrity, articular
associated with superior migration of the humeral joint surfaces, and rotator cuff partial and full
head during arm elevation. Motion usually is a tears.
result of drivers such as muscles designed to In the past decade there has been several stud-
achieve certain tasks. In the presence of different ies conducted to investigate the contact problem
pathologies some of these forces effort dimin- and instability of the glenohumeral joint using
ishes resulting in more work to achieve our goal 3D Finite Element (FE) models (see Fig. 1.2).
or simply be limited to certain range of motion. The contact stress is usually indicative of high
Here are some clinical evaluations that pro- peak loads wear and most FE models will pro-
vide some insight into the changes in kinematics vide the stress and strains of the complete meshed
as a result of shoulder instability. For example, in surface or volume which includes bones, carti-
stiff shoulder joints, the humeral head moves lages and ligaments. Buchler et al. [40] built a FE
upward during the first degrees of arm elevation. model which consisted of the major rotator cuff
Browne et al. observed that the maximal gleno- muscles and investigated the contact stresses due
humeral elevation was obtained in a plane to the changes of the geometrical shape of the
8 F. Amirouche and J. Koh

Fig. 1.2 Finite Element shoulder model with onlay prosthesis implant with two pegs

humeral head and the glenoid contact surface in The use of multibody software packages such as
both healthy and pathological conditions. The OPEN SIM allows creating shoulder models
result of the study suggests that the changes in mimicking the natural dynamics of a person. As
shape of the humeral head may lead to joint insta- an option in the analysis an additional FE model
bility. However, one of the drawbacks of this can be used to perform the contact problem using
study as is the case with a large number of FE the loading conditions resulting from the inverse
models is lack of validation. FE model once dynamics solution. Recent FE model of the gle-
developed and the user has determined that it is nohumeral joint used estimated muscle forces as
reliable it can be used for analyzing the biome- the loading condition, and the humerus was
chanical effect of the shapes of prosthetic humeral allowed to move freely with six degrees of free-
heads after shoulder arthroplasty. dom [43]. These loading and boundary condi-
Terrier et al. [41] FE model of the shoulder tions enable the FE analyses to simulate motions
focused on the supraspinatus deficiency as it of the shoulder complex closer to its realistic
relates to osteoarthritis. The result suggested that physiological condition than those with prede-
supraspinatus deficiency increases the upward scribed or artificially defined constraints. This
migration of the humeral head resulting in study provides a useful framework for future FE
increased eccentric loading, and thus decreases studies of the shoulder complex. All models have
GH joint stability. An extension of this FE shoul- limitations and one needs to be aware of what is
der model was by Walia [42] to investigate the perceived as acceptable conditions under which
effect of combined defects of the humeral head a model is being simulated including the geom-
and of the glenoid. It was found that the glenohu- etry and structure of muscles and other soft
meral joint stability was decreased significantly. tissues.
The shoulder joint is a dynamic system that
uses forces generated by the muscles to perform
certain tasks preserving the stability of the joint 1.4.2  E Models of Rotator Cuff
F
and limiting the stress conditions between the Tears
articular surfaces. So in reality the FE models
alone wouldn’t suffice in creating realistic mod- Rotator cuff tendon tears technically can be asso-
els. As is the case in gait and motion analysis, ciated with any of the muscles/tendons that form
inverse dynamics is used to evaluate forces and that capsule which support the humeral head.
that require the solution of equations of motion One of the most common tendon tear is the supra-
with defined constraints and initial conditions. spinatus tendon often a result of trauma injury.
1 Biomechanics of Human Joints 9

Tears when not treated can cause chronic shoul- parameters to simulate pathological conditions.
der pain, and may lead to secondary degenerative With additional information gained about the
changes in the shoulder. The fundamental rotator cuff tears both these models lacked exper-
­mechanism of what initiate a rotator cuff tear imental data, a common problem with FEA
remains a problem of concern and certainly it is models.
still unclear what are the shear forces that initiate The first 3D FE model of rotator cuff tears was
or produce these tears. A number of studies have reported by Seki et al. [47] in 2008 and was used
been conducted to explore the underlying biome- to analyze similarly to previous 2D models the
chanical stress-strain responses which might stress distribution in the supraspinatus tendon. It
cause rotator cuff tears using FE shoulder was found that the maximum stress occurs in the
models. anterior portion of the articular side of the tendon
Early work in FE addressed the stress-contact insertion rather than at the tendon contact point
relation at the shoulder joint in the presence of with the humeral head as suggested by 2D analy-
rotator cuff tear. For instance, Luo et al. [44] ses. The analysis provided an important informa-
investigated the supraspinatus tear using a 2D FE tion that explains the frequent occurrence of
shoulder model by looking into the tress distribu- rotator cuff tears at this site. The 3D model analy-
tion and how that is related to rotator cuff tear. sis provided an insight that was not possible in
The stress was evaluated at different abduction 2D, where the anteroposterior direction was
angle of 0°, 30° and 60° respectively and also investigated showing that the anterior part of the
under two different acromial conditions with and rotator cuff is not in contact with the superior sur-
without subacromial impingement. It was found face of the humeral head. However, this study
that the high stress concentration due to the sub- only analyzed part of the shoulder at 0° abduction
acromial impingement could initiate a tear. without experimental validation.
Another aspect of their findings also showed that Adams et al. [48] used a 3D FE model of the
this tear may occur on the bursal side, the articu- glenohumeral joint to investigate the effect of
lar side or within the tendon rather than only on moment arms on muscle forces and rotator cuff
the bursal side as previously reported. This 2D tears. An important of this study shows that the
modeling lead to other FE models used to inves- moment arms of infraspinatus and teres minor
tigate this claim further. muscles were generally decreased. Consequently,
Two further studies based on Luo’s model the muscles attached to the torn tendons are
were conducted by first Wakabayashi et al. [45] required to generate more forces for the same
where they applied histological differences at the motions, and the overall strength of the shoulder
tendon insertion in their FE model to analyze the is decreased. This study revealed a potential rela-
stress distribution of the supraspinatus tendon. tionship between shoulder strength reduction and
Their results found that the maximum principal the rotator cuff tears location.
stress of the tendon occurs at the region in contact Another 3D FE study of rotator cuff tears was
with the humeral head rather than at the insertion conducted by Inoue et al. [49] which included the
point. Secondly, Sano et al. [46] in their model rotator cuff muscles as well as the deltoid muscle.
they examined the stress distribution in the path- This model was used to investigating the rotator
ological rotator cuff tendon and revealed poten- cuff tears and stresses at the articular and bursal
tial partial-thickness tears at three different sides of the supraspinatus tendon were found to
locations: on the articular surface, on the bursal cause shearing between the two layers, which is
surface and in the mid-substance close to the believed to initiate partial-thickness tears. As is
insertion. It was found that high stress concentra- the case of other FEA models this 3D model limi-
tion occurs at the articular side of the insertion tation needed further imaging techniques and
and the site of tear. The two studies used same experimental studies to construct soft tissues and
modeling method and conditions as Luo’s origi- muscles to build additional fidelity into the mus-
nal model, but employed different histological cle forces.
10 F. Amirouche and J. Koh

1.5 3D Reconstruction Import Dicom


and Design of Patient-­ files from CT
of a patient
Specific Shoulder Prosthesis

Patient-specific models are today feasible if CT


Masking and
data is available with a sequential imaging file Mesh and FEA
Segmentation
with a minimum of 0.5 mm interval. High resolu-
tions images will provide better rendering and
surface smoothing which allows for a CAD
model and mesh that is close to the actual bony
structure of the patient. Further modeling of the
muscles, tendons, ligaments, and cartilage require CAD Smoothing
MRI images and additional volumetric method- Conversion and Wrapping

ologies to model the muscles associated with the


rotator cuff such as the supraspinatus muscle. Fig. 1.3 Modeling phases in patient-specific implant
The processing of CTs is commonly per- design and analysis
formed by software that uses Hounsfield units as
a contrast to differentiate between soft tissues
and bones to isolate the geometry being formed.
MIMICS. The data conversion method used to
develop the CAD surface model and fill to obtain
a solid model of the shoulder can be obtained
using MIMICS software [50]. The CAD draw-
ings in its final form is exported to either Mimics
own analysis module or other FE software to cre-
ate their corresponding mesh needed for the anal-
ysis. Usually, we perform all the CAD steps in
terms of design of implants such as the onlay in
CAD environment, perform the resurfacing of
the glenoid to accommodate different designs
before the assembly. Once the complete stage of Fig. 1.4 Stress analysis of the implant-scapula assembly
sequential imaging, and CAD steps are complete,
we move into the final stage of analysis where we internal or external rotation of the arm (see
can investigate fixation, stability, cycling loading, Fig. 1.4). The effects of muscle moment arms on
stress, and any outcome that we perceive will be joint stability can also be simulated to assess the
best to evaluate the shoulder implant surgical shoulder joint performance.
success (see Fig. 1.3).
The assignment of material properties for
bone and cartilage are usually assumed based 1.6 Future Biomechanics Work
assumptions one makes on bone quality, thresh- and Clinical Challenges
olding, DEXA, and mathematical bone density
evaluation based on the Hounsfield unit. Isotropic Biomechanics uses mechanics principles to
elastic material properties for bones and cartilage define mathematical equations and functions to
can be used, and soft tissues can be modeled as explain parameters that are used for modeling of
Ogden hyper-elastic material properties [51]. musculoskeletal systems including bones, and
The onlay design with pegs or Keel shape can soft tissues. It employs imaging techniques, test-
be addressed by comparing the contact stress as ing, and experimental studies to validate its
function of loading and different abduction angle, assumptions of its biomaterials. A powerful tool
1 Biomechanics of Human Joints 11

such as FEA which is founded on the first law of muscles. What are the limits of realistic simula-
mechanics is becoming a standard tool used to tions and can Multiphysics provide better
perform mechanical tests accepted by the FDA to understanding of the nonlinearity of material
obtain approval for implants failure analysis, properties. When modeling a human joint is it
quality control, stress, and strains and a number possible to collect and store patient data of bone
of tests that usually are limited to experimental and tissues in healthy conditions so that they
testing. FEA when combined with visual graph- can be compared to joints with pathological
ics can help translate its output in a form that is conditions, including definitions of boundary
understandable and easy to translate. Today we and loading conditions based on individualized
are merging into a multiscale Multiphysics stage physiological data. Special attention should be
integrating several concepts into one framework paid to the consistency between different FE
to be able to investigate the interaction of bone models and models obtaining from multibody
with fluid, investigating bone ingrowth, and con- models used for muscle force estimation
necting our understanding of mechanics from the through inverse dynamics.
cell level to the macroscale so one can model and 2. Define comprehensive models describing the
understand how fractures heal and how different complete joint to capture its complexity
fixations affects its healing process. Simulation including appropriate 3D representations of
and 3D printing provide an even more promising all major connective tissues and their delicate
world to orthopedics as we become patient spe- interactions.
cific to address different pathologies and opti- 3. Define standard testing protocols to validate
mize the treatment protocol including implant these models so that can be developed for
design process. In fact, simulations performed by clinical use.
use of computers through a display of augmented 4. Allow for more group testing of Dynamic FE
reality graphics or virtual simulations are referred simulations so that they are built based on
to as in silico contrary to in vitro and in vivo, physiologically realistic boundary and load-
where all studies are performed on a computer ing conditions that are measurable and can be
via modeling and simulation. In silico medicine used by others. This allows for better simula-
has been in use in orthopedics where surgical tion and understanding of human joints.
planning of complex cases is studied and poten- 5. Develop advanced medical imaging, sensing
tial solutions are examined beforehand giving the techniques tools to quantify in vivo strain and
surgeon the best option for patient-specific rem- stress distributions of soft and hard tissues in
edy and orthopedic solution. In Silico is work in both normal and pathological conditions so as
progress as these models are currently undergo- to validate FE models more rigorously.
ing constant changes to bring these models alive 6. Develop augmented and virtual reality tools to
where they can be biologically driven to show the assist surgeons overcome information redun-
evolution of pathologies and diseases, progres- dancy and improve on real time interaction
sion and bone remodeling, and become dynami- and feedback when needed to improve
cal so when can examine different stages and patient’s outcome.
progress in real time of bone-implant interaction, 7. Develop artificial intelligence and robotics
fracture healing, spine fusion among and poten- platform for minimally invasive procedures,
tial soft tissues and nerve regeneration. complex cases and integrate “savoir faire” and
surgical techniques with validated simulation
What follows are some of the challenges that lie studies.
ahead to orthopedic biomechanics. We need to 8. Improve on in silico Multiphysics and multi
scale modeling to allow for interaction of fluid
1. Address how realistic can a patient-specific and structure interface for better u­ nderstanding
model be represented using CTs and MRI of bone–implants interfaces, and better 3D
imaging and realistic connective tissues such as bioprinting of scaffolding prosthesis.
12 F. Amirouche and J. Koh

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element models of the human shoulder complex: org/10.1088/1361-­6560/ab0137.
Shoulder Muscles Moment Arm
Contribution to Glenohumerol
2
Joint Motion and Stability

Jason Koh, Lorenzo Chiari, and Farid Amirouche

2.1 Introduction 0.05% in 2006. Similarly, anterior crucial liga-


ments reconstruction are among the most com-
Surgeons are now performing more arthroscopic mon sports medicine procedures performed in
rotator cuff repairs than ever before and more of the United States [1, 2]. The focus of many
these repairs are being performed in ambulatory orthopedic surgeons and of rotator cuff-related
surgery settings. The NSAS data from 1996 and research is on the prevention of rotator cuff tears
2006 is indicative of such claim where ambula- and the development of prevention programs
tory surgical procedures increased from and test procedures that help become the identi-
21,236,913 to 34,738,440 and rotator cuff fiers without the burden of cost. What is more at
repairs went from 58,846 (0.3%) to 272,148 stake is the challenge to determine when does a
(0.8%) in respective years [1]. The NHDS data rotator cuff patient be able to return to normal
also shows how the rotator cuff impatient hospi- activities after rehabilitation [3].
talization for the same period decreased by There are several different methods of evaluat-
almost half in 1996 and was reduced further to ing shoulder joint ligament injury, symptoms and
performance before and after surgery. Most are
based on patients’ symptoms performance out-
J. Koh
Department of Orthopaedic Surgery, Orthopaedic &
come measures in a test, and surgeon clinical
Spine Institute NorthShore University HealthSystem, findings [4]. In sports there are specific strength
Skokie, Illinois, USA assessment tests such as arm power which can
University of Chicago Pritzker School of Medicine, discriminate between the injured and non-injured
Chicago, Illinois, USA patients and those who had soft tissue reconstruc-
Northwestern University McCormick School of tion. Other tests used such as isokinetic tests are
Engineering, Evanston, Illinois, USA not always predictors of the functional stability
L. Chiari of the shoulder joint but work well for the knee
IRCCS Istituto Ortopedico Rizzoli, Bologna, Italy [5, 6]. To overcome some of these tests limita-
F. Amirouche (*) tions additional methods were introduced [7–9].
Department of Orthopaedic Surgery, Orthopaedic & In the absence of standardized methods to
Spine Institute NorthShore University Health System, assess joint function and stability after arthro-
Evanston, Illinois, USA
plasty, rotator cuff repair surgeons rely great deal
Department of Orthopeadic Surgery, College of on basic methodologies [10, 11]. Conclusive cor-
Medicine, University of Illinois,
Chicago, Illinois, USA
relations have yet to be completely formulated
e-mail: FAmirouche@northshore.org, between joint function and its kinematics and
amirouch@uic.edu

© ISAKOS 2021 15
J. Koh et al. (eds.), Orthopaedic Biomechanics in Sports Medicine,
https://doi.org/10.1007/978-3-030-81549-3_2
16 J. Koh et al.

muscle–ligament forces. This is partly due to the assessment of joint stability, GH range of motion,
complexity of the joint and the reliability of man- and muscle forces joint contribution during
ual measurement collected at the clinic or lab. abduction.
Moment arm is a tool that is mostly used to The four muscles joining together to support
assess the torque relation to lever arm and muscle the humeral head to form the rotator cuff are the
contributing power at the joint. It has a clinical subscapularis (supporting the shoulder anteri-
value in measuring torque producing capacity orly); the supraspinatus (maintains the superior
and its effect on kinematics and joint range of aspect); the infraspinatus and teres minor (located
motion. Moment arm is usually a measure used on the posterior shoulder) [15]. Rotator cuff fail-
when the actual force is not known or difficult to ure usually results from tendinopathy that trans-
measure but the torque and center of the joint forms from partial to full thickness tears involving
rotation is measurable. Since the torque is indica- the supraspinatus tendon and may proceed to
tive of moment which is the product of the force entangle the infraspinatus tendon and/or the sub-
and the distance from the center of rotation, so scapularis tendon [16].
changes in moment arms provide an insight into Surgeons rely on imaging techniques such as
the power capacity produced by individual mus- ultrasound and MRI to identify the cause of ten-
cles and ligaments after rotator cuff repairs and don injuries [17, 18]. The decision-making in the
ACL reconstruction. treatment of the rotator cuff relies mainly upon
The focus of this chapter is to present a study the surgeon diagnosis, patient conditions, and the
on moment and provide detailed look into its cal- extent of the tear. Other factors such as the mus-
culation through experimental investigation of cle quality and patient health conditions includ-
rotator repair techniques using cadaver shoulders ing pain play a role in the development of the
specimens. The experiment provides an insight right protocol for treatment.
how moment arms of the major muscles spanning Moment arm has been used extensively to
the glenohumeral joint during abduction, flexion evaluate the muscle contribution to joint rotation,
and axial rotation are measured and the benefits kinematics, and moment-torque capacity it pro-
we gain from their calculations. Moment arm duces including the different moment contribu-
data for deltoid, supraspinatus, infraspinatus, tions in different planes of rotation. In a vector
subscapularis and teres minor will be reported form the moment is defined by the cross product
when measured using the definition of force-­ of the displacement vector measured from the
moment and intricate geometries of tendons center of rotation to the force line of action. This
insertion points as well using motion capture method is referred in the literature as the geo-
devices to monitor positions during abduction. metrical approach used in calculating the moment
It is important to highlight some of the clinical arm [19–22]. It requires two points to define a
settings where the moment arms can be advanta- vector for the force line of action and the knowl-
geous in comparing surgical outcomes of rotator edge to accurately measure the center of rotation
cuff repair tears. Arthroscopic and open rotator by which the force is driving the body segment
cuff repairs are two procedures with distinct (usually the humerus in case of GH joint). With
advantages and disadvantages. Arthroscopy advances in imaging techniques, geometry recon-
allows for preservation of the deltoid muscle struction using CTs and MRIs combined with
whereas open repair techniques allow for easier motion tracking systems this method is currently
transosseous fixation to better replicate the foot- becoming more popular.
print of the supraspinatus tendon [12]. The other method used in estimating the
Surgeons seem to favor impatient surgery moment arm stems from the concept of virtual
more for rotator cuff and for those with high vol- work where virtual displacement brings in the
ume. Mini-open repair was the most frequently excursion rate of change divided by the joint
used method of repair (46.2%) followed by open angle differential. Essentially it is a direct rewrit-
(36.6%) and arthroscopic (14.5%) [13, 14]. The ing of the virtual displacement used to develop
moment arm will be further explained in the the work performed by a force or a muscle force
2 Shoulder Muscles Moment Arm Contribution to Glenohumerol Joint Motion and Stability 17

vary and experimental validation using imaging


techniques and cadaveric specimens are being
pursued to provide reputable data to assess the
GH repairs.

2.2.1 Imaging Techniques

Previous in vitro and in vivo studies have investi-


gated the GHJ kinematics in the presence of RC
tears and repairs [29–31]. Cadaveric studies have
shown that RC tears size play a crucial role in the
GHJ stability and range of motion [32]. Other
cadaveric experiments showed how the humeral
Fig. 2.1 The model was created from CT scans using
position resulted in an inferior translational shift
Materialise Mimics and imported into SolidWorks. The
coordinate systems (axes) have been extracted at the [33]. Additional studies by Yamaguchi et al. [34]
approximations of glenoid surface and humeral head. (S/I using static radiographs in patients with both
denote superior inferior, M/L medial lateral, A/P anterior asymptomatic and symptomatic rotator cuff tears
and posterior)
found that both groups of patients demonstrated
superior translation of the humeral head with
in this case. It has usually been found advantages increasing arm elevation. As stated by Bey et al.
to the geometric method because you do not need [35], these studies use conventional radiographs
to know the location of the center of rotation collected under static conditions at specific arm
point [23–28]. positions and are limited in scope to understand-
Most kinematic data provide the measurement ing a three-dimensional problem. Other experi-
of the rotation angle and excursion changes asso- ments focused on the correlation between the
ciated with the muscle force line of action (inser- extent to which patient-reported outcomes after
tion points of muscle points). It is unconceivable rotator cuff repair are associated with measures
that an angle can be measured in void. Whether of shoulder function. For example, a study by
assuming a 2D plane motion of 3D general joint Nho et al. [36] reported that shoulder strength
motion a reference axis is usually assumed at the was predictive of patients’ American Shoulder
center joint of rotation and hence one needs to be and Elbow Surgeons (ASES) score. This design
able to position and define the center of rotation experiment is often controversial as successful
(see Fig. 2.1). This is usually performed by mea- RC repairs can lead to poor outcome [37]. In a
suring the intersection of two lines of one moving study by Bey et al. [39], Twenty of 21 rotator cuff
body and one being fixed. repairs appeared intact at 24 months after sur-
gery. Their finding further supports the fact that
the humerus of the patients’ repaired shoulder
2.2  xperimental Methods Used
E was positioned more superiorly on the glenoid
in RC Repairs and Muscles than both the patients’ contralateral shoulder and
Moment Arm Evaluation the dominant shoulder of control participants.
This is another study that differentiate between
Rotator cuff surgical repair techniques are the GHJ kinematics and clinical outcome associ-
reported to fail structurally (20–70%), and the ated with shoulder strength.
belief that they can restore the GHJ normal func- Kozono et al. [38], used X-ray images and
tion has yet to be resolved. Optimum treatment of CT derived digitally reconstructed radiographs
RCT and satisfactory clinical outcomes to restore to evaluate further the kinematics of RCT and
and stabilize the joint during shoulder motion measure the humerus translation relative to the
18 J. Koh et al.

s­ capula. This dynamic analysis of the glenohu- to simulate each muscle’s line of action toward
meral during scapular plane abduction and its origin point on the scapula. This maintained
axial rotation for 11 RCT patients with large to tension to provide support for the shoulder joint
massive full thickness and 10 healthy control throughout abduction.
subjects showed the humeral head center with The three-camera Optotrak Certus (Northern
a medial shift at the late phase of scapular Digital Inc., 2006), along with two Orthopaedic
plane full abduction, and an anterior shift at the Research Pin markers and First Principles soft-
internal rotation position during full axial ware, was used for motion capture. The Optotrak
rotation. was placed lateral to the experimental frame,
allowing cameras to monitor the frontal plane of
the shoulder. The shoulder was placed on an
2.2.2  adaveric Experiments of RC
C adjustable height table to ensure the specimen
Tear and Repairs was positioned at the center of the camera cap-
ture range. Two Optotrak markers were used: one
The experiments conducted in our biomechanics placed on a stationary rod slightly superior to the
laboratory are designed to evaluate the shoulder scapula and one inserted at the insertion site of
kinematics and the changes in muscle forces the deltoid in its musculotendinous. Each
before and after RC repairs techniques in main- Optotrak marker contained three sensors, which
taining a stable joint at different abduction angle. had to be placed within the camera frame of the
The experiment setup follows Hirata et al. [40] Optotrak. During setup, a digitizing probe was
apparatus with the added optotrack and tracking connected and used to assign the digital points
monitoring of muscles insertion and attachment for the origin and insertion sites of the RC mus-
points. This allows for calculation of moment cles. This produced digitized points marked on
arms using the geometric approach or the excur- the shoulder girdle that were relative to the two
sion method as well. Five fresh frozen human markers previously placed.
shoulder specimens were used for this study (all Each shoulder underwent four different
female, age range 60–79 years, two right and motion capture experiments with Optotrack
three left shoulders). Shoulders were thawed and recording conducted for each condition: (1)
carefully dissected removing unnecessary tissues Intact rotator cuff, (2) Complete rotator cuff tear,
and muscles were dissected from their respective (3) SCR, and (4) RSA.
fossa while keeping their insertion tendons intact. A complete tear was created by incising the
Sutures were secured to the tendinous muscle supraspinatus at its humeral insertion. SCR was
insertions. One screw was inserted at the lateral conducted to repair the complete tear then fol-
end of the scapular spine and another at the lowed with an RSA for the same cadaveric model.
humeral neck. These screws served as reference During RSA, the humeral head was incised, and
points in the coronal and sagittal planes respec- the glenoid and humeral shaft were prepared for
tively. The scapula was then placed in a square the reverse prosthesis. The prosthesis was fixed
Plaster of Paris (PoP) mold and PoP was poured with the center of rotation placed infero-­medially,
to confine the medial two-thirds of the scapula following standard surgical procedure.
within a block, while the lateral third of the scap- After the points were digitalized on each
ula remained exposed. model, the humerus was manually abducted in
Muscle-tendon units of all shoulder muscles the coronal plane from 0 to 90° at a constant rate,
were maintained in tension by nylon strings, allowing the Optotrak to capture relative motion
which were attached to muscle-tendon units at in a time frame of 20 s. The Optotrak data output
one end, passed through multiple pulley systems, featured displacement values in millimeters for
and had 3 N free-hanging weights attached to the the digitized points after each of the experiment.
other end. The nylon strings attached to each This was later used to calculate moment arm of
shoulder muscle insertion point were positioned the four RC muscles. (see Fig. 2.2).
2 Shoulder Muscles Moment Arm Contribution to Glenohumerol Joint Motion and Stability 19

a b c

Fig. 2.2 Shoulder experimental apparatus with all four Optotrack was used to track the digitized points during
rotator cuff muscles and deltoid. Three views a, b, and c abduction from 0 to 90°
include the anterior, posterior, and lateral, respectively.

2.2.3 Moment Arm Calculations ing technology allows for 3D analysis and pos-
sibly the calculation of all three joint angles of
Previous techniques for the calculation of rotations. The experimental setup in our experi-
moment arm have been discussed above and their ments relies on pulleys and cables to dictate the
advantages and disadvantages rely great deal on load force direction which is a balancing act to
the accuracy of data measured experimentally. allow for weight adjustment to stabilize the GH
The method of geometric measurement requires t. joint. The pulley system used static weights to
both the joint center of rotation and the force line balance the shoulder joint throughout abduc-
of action. In our experiments we digitized the tion. This system allowed the deltoid to be
muscles insertion points and so the line of action driven by a force sensor dynamometer that
for the forces can be evaluated. However, it is dif- allows for measurement of the abduction arc
ficult to make a point to point map for the evalu- angle and force.
ation of these forces but different combinations The moment arms (MA) of the rotator cuff
of line actions might provide a better insight into muscles were calculated using the origin (O) and
the moment arm contribution to the muscle force insertion (I) digitized points data obtained from
and torque capacity or moment produced at the Optotrak along with the two additional digitized
joint. points on either side of the humeral head used to
The proposed experimental method is well calculate the center of the shoulder joint.
suited for the tendon-joint excursion method as We define the center of the humerus head as O
the different insertion and connecting points of and as the humerus translate during abduction
RC muscles are available throughout the abduc- our optotrack measure of the new center during
tion angle. Hence, one can compute the relative full range of rotation is reevaluated. The line of
change in muscle length as function of the joint action defining the muscle force direction is
angle of rotation. While this method was limited defined by the points denoting the tendon inser-
to 2D plane motion analysis, the optotrack sens- tion and attachment points as depicted in Fig. 2.2
20 J. Koh et al.

Fig. 2.3 Tracking of the Supraspinatus


Humerus head center
before and after
abduction. A and B
points along the muscle
line of action defining
the insertion point and
the origin point used for O′
the computation of the O
moment arm. O and O′ →
r →

and C and C′ denote the F


A
before and after B
abduction positions. F is C′
the force vector along ex
C+ Θ
AB, and r and r’ denote
the projection from O to
AB. The fixed reference ey
frame is given by the ez
unit vectors ex, ey, and ez Subscapularis

Humerus

during the experiment. Let A be a point on laris of the anatomic shoulder was not statisti-
subscapularis as shown
­  in Fig. 2.3 then the cally significantly different than the three models
moment vector arm OA , also referred as r , is (p = 0.148). There was no significant difference
defined as the distance between point O and A. in percent difference testing between model
Consider B another point on the force line of groups (p = 0.814).

action and we define a unit vector
 u along
 that The mean value for the supraspinatus
line. The moment is given by M = r × F . moment arm started with a large abduction
value and features a steady downward trend
into a small adducting moment arm over the
2.3 Results course of shoulder abduction (Fig. 2.5). All
other models also followed a downward trend;
The mean value for the intact subscapularis however, SCR model was the only one to gain
model moment arm starts with a large adducting any adduction moment arm at higher shoulder
ability (Fig. 2.4). As the shoulder is abducted, the abduction angles. Both the complete tear and
mean moment arm shows a steady upward trend, RSA models have moment arm values that
reaching a large abducting moment arm at 90° remained in abduction potential throughout the
abduction. The mean values for the SCR and entire course of shoulder abduction. The RSA
RSA models start with approximately 50% of the model showed the closest alignment with the
adducting ability of the intact model. The SCR intact model, with a largely increased percent
and RSA models then trended upwards, ending difference only at 90° abduction. The SCR
shoulder abduction with a near neutral mean model showed close alignment with the intact
moment arm. Mean moment arm values and per- model for the first 30° and then a larger differ-
cent differences across shoulder abduction ence at angles above 60°.
were −1.9 mm for intact, 5.5 mm (256.3%) for The intact supraspinatus showed slightly dif-
complete tear, −5.5 mm (336.0%) for SCR, ferent behavior between its two muscle fiber
and −4.4 mm (194.4%) for RSA. ANOVA testing groups. Both fiber groups started with large
revealed that moment arms across the subscapu- abducting moment arms, but the anterior fibers
2 Shoulder Muscles Moment Arm Contribution to Glenohumerol Joint Motion and Stability 21

Subscapularis Mean Moment Arm


20
18
16
14
12
10
8
moment arm (mm)

6
4
2
0
−2
−4
−6
−8
−10
−12
−14
−16
−18
0° 30° 60° 90°
Degree of Shoulder Abduction
Intact Complete Tear SCR RSA

Fig. 2.4 The mean values for moment arm of subscapularis at 0, 30, 60, and 90°

Supraspinatus Mean Moment Arm


28
26
24
22
20
18
moment arm (mm)

16
14
12
10
8
6
4
2
0
−2
−4
−6
0° 30° 60° 90°
Degree of Shoulder Abduction
Intact Complete Tear SCR RSA

Fig. 2.5 The mean values for moment arm of supraspinatus at 0, 30, 60, and 90°

moved toward a neutral position during abduc- 2.4 Discussion


tion while the posterior fibers moved into a large
adducting moment toward the end of shoulder Previous work by Hughes et al. [24] among oth-
abduction. After a complete tear, the supraspina- ers have raised the potential or induced from the
tus fibers showed a similar initial large abducting calculation of moment arms related to the
moment arm; however, although the moment arm assumption of the humeral head joint center of
values decreased, there was no transition from an rotation assumed fixed during abduction. This
abducting to adducting moment arm in the poste- limitation was clearly resolved in our study as the
rior fibers. imaging technique employed allowed us to re-­
The SCR and RSA models maintained similar compute the humeral head center of rotation.
trends when compared to the intact model, start- A study by Ruckstuhl et al. also used the
ing with large abducting moment arms that origin-­insertion method for calculating moment
moved into small adducting moments as the arm in specific positions using MRI images to
shoulder was abducted. construct a 3D anatomical reconstruction [41].
22 J. Koh et al.

Hamilton et al. used 3D modeling software come and potentially other pathological condi-
and found different RSA reconstructions dis- tions of the shoulder. For clinical relevance,
played similar trends over abduction when com- quantitative assessment of the dynamic kinemat-
pared to our study results [21, 22]. Both the ics of shoulders with RCTs will need imaging
subscapularis and infraspinatus showed large techniques combined with experimental and 3D
negative moment arms which trended toward pos- can lead to development of indicators for achiev-
itive moment arm values over 0–90° abduction. ing functional restoration. Furthermore, our anal-
Additionally, efficiency testing by Hamilton and ysis of fiber divisions within the same muscle
percent difference changes from intact models in illustrate the complex nature of shoulder muscles
our study all failed to reach statistical significance themselves, and future studies should aim to bet-
in all models, secondary to large standard devia- ter explore and model their function. Infraspinatus
tions. However, the large standard deviations in and subscapularis show the greatest variance
our study were likely secondary to a limited num- when comparing RSA and post-reconstruction to
ber of cadaveric models and innate differences intact. It is in these muscles where there is the
between shoulder anatomy and strength [42]. most loss of potential abducting or adducting
An illustration of how the method of discreti- force.
zation of the tendons points at their fixation site
provides an insight into the bundled fibers contri-
bution and how its span area of fixation produces
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Part II
Biomechanical Properties of Orthopaedic
Materials
Biomechanics of Ligaments
3
Jonathan D. Hughes, Calvin K. Chan,
Sene K. Polamalu, Richard E. Debski,
and Volker Musahl

3.1 Introduction 3.2 Histology

Ligaments are soft tissue structures that are com- A fundamental understanding of the underlying
posed of collagen fiber bundles and connect histology is crucial to comprehend the biome-
bone to bone. Ligaments play a vital role in the chanical properties of ligaments and will aid in
stability of joints throughout the body, including designing biomechanical studies. Ligaments are
the shoulder and knee. Ligaments act as individ- composed of water, elastin, proteoglycans, gly-
ual uniaxial restraints on the joint that work colipids, and densely packed collagen fibers that
together to resist a variety of external loads. run in a longitudinal direction. These fibers are
Injury to ligaments disrupts the mobility and sta- arranged into a series of bundles called fascicles
bility of the joint, potentially leading to signifi- and surrounded by a loose connective tissue
cant morbidity and pain for the patient. called paratenon [80]. Fibroblasts, the predomi-
Understanding the histology, joint kinematics, nant cell type, are arranged in rows between sub-
and biomechanical properties of ligaments will units of collagen fibers called fibrils. However, in
help physicians approach injuries to this struc- order to withstand multiaxial loads, the fibrils are
ture and formulate an appropriate treatment plan not uniformly oriented [2]. Ligaments are rela-
for their patients. tively hypovascular and hypocellular [9, 64].
Approximately 70–80% of the dry weight of a
normal ligament is composed of type I collagen,
with smaller amounts of types III (3–10% of dry
J. D. Hughes · V. Musahl (*)
Department of Orthopaedic Surgery, UPMC Freddie weight), V, IX, X, XI, XII, and XIV collagen
Fu Sports Medicine Center, University of Pittsburgh [72]. Type V collagen associates with Type I col-
Medical Center, Pittsburgh, PA, USA lagen to regulate collagen fibril diameter [6].
e-mail: hughesjd3@upmc.edu; musahlv@upmc.edu
Type III collagen has the ability to form intermo-
C. K. Chan · S. K. Polamalu · R. E. Debski lecular disulfide bonds essential for wound heal-
Department of Bioengineering, University of
Pittsburgh, Pittsburgh, PA, USA
ing [13]. Type XII collagen provides lubrication
e-mail: CAC296@pitt.edu; SKP39@pitt.edu; between collagen fibers [52]. Types IX, X, and
genesis1@pitt.edu XI are present at the ligament-bone interface in

© ISAKOS 2021 27
J. Koh et al. (eds.), Orthopaedic Biomechanics in Sports Medicine,
https://doi.org/10.1007/978-3-030-81549-3_3
28 J. D. Hughes et al.

conjunction with Type II collagen [30]. The water tions have superficial and deep fibers. The super-
and proteoglycans provide spacing and lubrica- ficial fibers attach directly to the periosteum,
tion to the ligaments, allowing the collagen fibers while the deep fibers are anchored to the bone via
to glide over each other. Sharpey’s fibers [16]. Various ligaments, includ-
Ligaments are metabolically active, with con- ing the medial collateral ligament, contain both
tinued cell and matrix turnover that occurs at a types of insertions: direct femoral insertion and
slow rate [1]. Since this occurs at a slow rate, indirect tibial insertion [72].
along with the inherent hypovascularity, liga- The collagen fibrils in ligaments are in various
ments heal at a slower rate than other tissues. amounts of crimp, which allows for recruitment
Extra-articular ligaments, such as the medial col- of more fibrils when a high tensile load is applied
lateral ligament, heal in four phases after injury: to the ligament. The ligament responds to tensile
hemorrhage, inflammation, proliferation, and load by elongating, thus allowing normal joint
remodeling [25]. In the initial hemorrhage phase, kinematics during movement by allowing the
there is bleeding at the site of injury with hema- joint to move freely. During high strenuous activ-
toma development between the torn edges. After ities, the stiffness of the ligament increases in
approximately 72 hours, inflammatory cells, order to maintain joint stability and restrict excess
including monocytes, leukocytes, and macro- motion of the joint. When this applied tensile
phages, appear at the site of injury and secrete load exceeds the maximum capacity of the liga-
cytokines and growth factors. This induces an ment, injury and/or rupture of the ligament can
inflammatory reaction and granulation tissue for- occur [72].
mation. Fibroblasts synthesize Type III collagen,
as well as small amounts of Type I collagen,
which forms an immature scar. The cells prolifer- 3.3 Joint Kinematics
ate, creating an immature vascular neo-ligament. and Function
The final phase consists of synthesis of Type I
collagen and further organization of the collagen Evaluation of joint motion is an important method
into a parallel arrangement of fibers along the of understanding joint injury. A joint is con-
functional axis of the ligament. strained by its ligaments, supporting soft tissue
Intra-articular ligaments, such as the anterior structures, and bony geometry. The joint con-
cruciate ligament (ACL), demonstrate minimal straints allow a combination of motion and stabil-
healing potential and do not follow the four ity to a joint along its six degrees of freedom
phases of healing mentioned above. A thin syno- (6-DOF), three translational and three rotational.
vial sheath surrounds the ACL and provides it Traditionally in the knee joint, the three transla-
blood supply. When this is disrupted, blood leaks tional axes are proximal-distal, medial-lateral,
into the surrounding synovial fluid and is unable and anterior-posterior, and the three rotational
to create a hematoma at the site of injury. axes are internal-external, flexion-extension, and
Additionally, cytokines and growth factors are varus-valgus [32]. The knee axes are defined by
unable to reach the site of injury. Due to this, the long axis of the tibial shaft, the line between
there is low healing potential for the ACL after an the femoral insertion points of the lateral and
acute rupture. medial collateral ligaments, and the perpendicu-
Ligament insertions onto bone help dissipate lar line to the long axis of the tibial shaft and the
forces from the soft tissues to the bone [70]. line between the femoral insertions as described
These insertions are classified as either direct or above, respectively. By examining the motion of
indirect. Direct insertions consist of four distinct the 6-DOF joint kinematics, researchers and cli-
zones: ligament, fibrocartilage, mineralized nicians can determine the role and extent of
fibrocartilage, and bone [16]. The indirect inser- injury to individual structures.
3 Biomechanics of Ligaments 29

Measuring kinematics in a laboratory setting ducers, buckle transducers, and strain gauges, to
have been done in a variety of ways. Early tech- directly measure the force in individual ligaments
niques used mechanical loading linkages and in response to external loads [31, 38, 45]. One
weights to measure the motion of the knee in study utilizing direct force measurement found
response to specific external loads [7, 41, 55]. that an internal tibial torque of 10 N-m produced
Biplanar radiography was also used as a way to a force on the order of 100 N in the ACL at 20° of
visually measure the motion of cadaveric knees flexion, while an external tibial torque of 10 N-m
based on radiographs from two known angles produced a smaller force around 50 N by using a
[56, 63]. Another approach involved using elec- load cell attached to the ACL through the tibial
tromagnetic tracking by placing sensors on the insertion [47]. In contrast, noncontact methods of
bones in order to track the joint motion of cadav- measuring in situ force sought to reduce error
ers and patients in a three dimensional space [10, from the interface of the ligament to the measur-
49]. In recent years, robotic technology has ing device. A method using a UFS requires mea-
become the gold standard, in which joint kine- suring the 6-DOF forces and moments applied to
matics are measured by combining a 6-DOF a rigid body connected to the sensor and calculat-
robotic arm with a universal force/moment sen- ing those forces through the joint based on a
sor (UFS) to measure joint motion and forces series of rigid body transformations [26]. A com-
[26, 27]. All of these methods aimed to compare bined robotic/UFS system can measure kinemat-
injured knees to healthy, contralateral knees, in ics and kinetics of an intact joint in response to
order improve injury diagnosis and treatment external loads and then repeat the intact kinemat-
options. ics after a ligament was transected or repaired in
The primary passive stabilizers in multiple order to record a new set of kinetics. The differ-
diarthrodial joints are the ligaments found around ence between the two set of kinetic data (intact
and within the joint. Ligaments act as individual and resected) is the in situ force of the ligament
uniaxial restraints on the joint that work together or graft [33, 59].
to resist a variety of external loads. Prior studies
have outlined the role of individual ligaments in
providing joint stability against certain external 3.4 Biomechanical Properties
forces. The authors examined 6-DOF joint kine-
matics in response to external loads before and 3.4.1 Structural Properties
after resecting the ligament in question in order
to see how the ligament provided stability to the Due to the primary function of ligaments to resist
joint [46, 60]. A separate study performed a sim- tensile loads, several investigations have focused
ulated Lachman test on ACL intact and ACL defi- on their biomechanical properties under uniaxial
cient knees. The authors found ACL deficiency tensile testing. This tensile testing is difficult due
increases knee anterior-posterior laxity from its to a multitude of factors, including the complex
normal 3–5 mm range and could possibly shift composition of ligaments. In order to apply ten-
loads to other structures [29]. sile loads, the ends of the ligament need to be
When one or more ligaments is injured, the properly secured, but issues with slippage are
knee will lose stability and respond to external common. In order to combat slippage, variations
loads differently. Since ligaments normally carry of soft tissue clamping have been created utiliz-
some passive load in the joint to provide stability, ing serrated clamps while freezing the secured
repairing or reconstructing the ligaments will ends [14, 42, 57, 58]. However, slippage can still
restore that native in situ force. Experimental happen, and the stress concentrations that now
measurements of ligament in situ force have used occur near the clamps can cause premature fail-
contact methods, such as implantable force trans- ure and not accurately represent the native tissue.
30 J. D. Hughes et al.

The structural properties of bone-ligament-bone can be obtained from the same uniaxial tensile
complexes in response to tensile loads have been testing. These mechanical properties are obtained
investigated. A benefit of testing the entire com- by normalizing the load by the cross-sectional
plex is the inclusion of the insertion sites of the area of the midsubstance of the ligament, and
ligaments which have different properties than strain, the elongation by the initial length of the
the midsubstance. midsubstance of the ligament. The stress-strain
Structural properties that characterize the curve can be used to determine tensile strength,
response of ligaments to loads along the longitu- the greatest stress in the tissue before failure, ulti-
dinal axis of the ligament include ultimate load, mate strain, the greatest strain before failure,
the greatest load that can be applied to a tissue modulus, the tissue’s resistance to strain in
before failure, ultimate elongation, the response to stress, and strain energy density, the
­deformation of the tissue when failure occurs, energy stored in the tissue before failure
and stiffness, the tissue’s ability to resist defor- (Fig. 3.1a,b). This quantitative data can guide
mation in response to an applied load [70, 75]. clinicians on their graft choice for ligament
These structural properties can be determined reconstructions, as the replacing tissue should
from the load-­elongation curve (Fig. 3.1a). have a similar mechanical response as the native
tissue to best restore intact joint kinematics.
To determine accurate measure of stress, an
3.4.2 Mechanical Properties accurate cross-sectional area (CSA) is needed, as
errors in CSA can cause substantial effects on
The mechanical properties of ligaments refer to stress calculations. CSA measurement falls into
the intrinsic behavioral response of the tissue two general categories: contact and noncontact
based on its composition and micro-structure and methods. Contact methods include the use of

a Ultimate Load Failure b Tensile Strength Failure

Yield Yield

Stiffness Modulus
Stress (MPa)
Load (N)

Energy Strain
Absorbed Energy
Density

Ultimate
Ultimate
Elongation
Strain

Elongation (mm) Strain (%)

Fig. 3.1 (a) Load-elongation response of a bone-­ response of a ligament displaying the mechanical proper-
ligament-­bone complex displaying the structural proper- ties that can be interpreted from the curve
ties that can be interpreted from the curve. (b) Stress-strain
3 Biomechanics of Ligaments 31

calipers and molding [4, 28, 54, 61, 82]. However, their longitudinal direction due to their highly
these methods involve touching the soft tissue parallel collagen fibers. This fiber alignment
and thus risk causing deformation or incorrect causes the mechanical response of ligaments to
assumptions of rectangular shape. Noncontact differ when loads are applied in directions other
methods have developed from shadow amplitude than along the longitudinal axis of the ligament.
and light profile methods [20, 39] to the use of Thus, it is pertinent to be mindful of the orienta-
laser micrometers, which have been found to be tion of the ligament with respect to external loads
the most accurate and reproducible [67]. when measuring mechanical properties.
However, issues with concavity exist for all of
these noncontact measurements. In order to
address these issues, a laser reflectance system 3.4.4 Viscoelasticity
has been developed [12].
Strain accuracy has similar difficulties as A distinct property of ligaments and biological
stress, in which an accurate measure of tissues is their viscoelasticity, meaning their
elongation is needed, otherwise the strain mea- mechanical response is load and rate dependent.
surements are unreliable. Contact and noncon- Ligaments demonstrate both viscous and elastic
tact tissue elongation methods have been properties during deformation. Elastic response
developed as well. Contact methods include the refers to a substance’s ability to return to its origi-
use of a differential variable reluctance trans- nal shape and size after deformation, while vis-
ducer (DVRT) [5, 22, 48]. A DVRT outputs a cous response refers to a substance’s ability to
voltage that has a linear relationship with the dis- resist flow. Viscoelastic substances display differ-
tance and elongation of tissue between the barbs. ent properties from elastic materials in isometric,
The limitations of DVRT measurements include isotonic, and cyclical loading. In isometric load-
not measuring strain throughout the ligament ing, or applying a constant deformation, the tis-
and possibly damaging the tissue by inserting sue displays a decreased stress response over
metallic barbs. Noncontact strain measurements time, known as a stress relaxation (Fig. 3.2a). In
involve the use of optical video tracking of either isotonic loading, or applying a constant force, the
markers or strain, and address both of the limita- tissue deforms more with time (Fig. 3.2b). When
tions of the contact methods [68, 77]. The posi- applying cyclical loading to a biological tissue,
tion of the markers or strain can be tracked, and the unloading curve is below the loading curve,
strain can be calculated by determining the dif- which represents energy dissipating from fluid
ference in their position before and after apply- friction of the water moving in the ligament
ing a load. (Fig. 3.2c). When analyzing the strain response
over time during this cyclic loading, the peak
stresses to reach the same strain decrease with
3.4.3 Contributing Properties each cycle as the curve becomes more repeatable
(Fig. 3.2d). Viscoelasticity is important clinically
Ligament compositions vary within different por- as the tissue relaxes during daily activities such
tions of the tissue from the insertion site to the as walking or jogging.
midsubstance and have a complex three-­
dimensional heterogeneous architecture [53, 66].
This variation has an impact on the mechanical 3.5 Factors Affecting Mechanical
properties and thus the mechanical response. Properties of Ligaments
Stress and strain response near the insertion sites
are different than that experienced at the midsub- Numerous biological factors determine the
stance [11, 43]. Furthermore, a distinct quality of mechanical properties of different ligaments
ligaments is their ability to resist tensile loads in within the body. The same tissue from two
32 J. D. Hughes et al.

a b

Stress (MPa)
viscoelastic elastic
Strain (%)

elastic viscoelastic

Time (s) Time (s)

c d
Stress (MPa)

Stress (MPa)
Loading
Unloading

Strain (%) Time (s)

Fig. 3.2 (a) Creep of viscoelastic and elastic materials rial in response to loading and unloading. (d) Stress
and in response to isotonic loading. (b) Stress relaxation relaxation of a viscoelastic material in response to cyclic
of viscoelastic and elastic materials in response to isomet- loading demonstrating a decreased peak stress at each
ric loading. (c) Stress-strain curve of a viscoelastic mate- cycle

different sources can present two different com- sion, whereas mature specimens fail midsub-
peting sets of data due to differences in skeletal stance [78]. Among skeletally mature specimens,
maturation, age of the source, location of the lig- ligaments from younger sources (aged
ament, and physical activity of the source [65, 66, 22–35 years) will demonstrate significantly
76, 78]. When evaluating which mechanical higher stiffness and ultimate load values
properties to use for individual ligaments, (242 ± 28 N/mm and 2160 ± 157 N, respectively)
researchers should pay attention to these biologi- than older specimens [69].
cal factors to ensure an accurate comparison can The location of the ligament sample plays an
be made. important role in determining the mechanical
properties of the tissue being investigated.
Different areas of a ligament demonstrate differ-
3.5.1 Biological Factors ent degrees of fiber organization, mineralization,
and protein composition. Initially, authors
Age and skeletal maturation play a significant defined ligaments as homogenous-appearing tis-
role in determining the mechanical property of a sues and used the mechanical properties of an
ligament [78, 79]. Younger and skeletally imma- entire tissue complex [23, 77]. However, authors
ture specimens still have open physes that allow later examined the properties of individual parts
growth of the bone compared to older and skele- of the ligament in order to understand the func-
tally mature specimens with closed physes. tional properties of the tissue [11, 24, 81].
Specimens from younger animals exhibit lower Through this later examination, the anteromedial
ultimate load, cross-sectional area, and stiffness bundle of the anterior cruciate ligament was
compared to skeletally mature specimens. found to have larger moduli, maximum stresses,
Younger specimens tend to fail due to tibial avul- and strain energy densities than the posterolateral
3 Biomechanics of Ligaments 33

bundle [11]. Tissue closer to the insertion sites of cycles [50, 71]. Researchers should be mindful
the ligament will exhibit different strain distribu- about limiting the number of freeze-thaw cycles
tion than tissue at the midsubstance [81]. ligament samples undergo in order to accurately
Physical activity levels of the tissue donor can measure mechanical properties.
affect the properties of the tissue in two ways. Due to the viscoelastic nature of ligaments,
Some swine exercise models showed femur-­ the mechanical behavior of ligaments varies
MCL-­tibia complexes have increases in ultimate greatly due to their surrounding temperature and
load, linear stiffness, tensile strength, and ulti- hydration. There are established effects of vary-
mate strain after 12 months of physical exercise ing degrees of hydration on the mechanical prop-
when compared to the sedentary group [74]. erties of different ligaments [15, 36, 37, 62].
However, joint immobilization, which usually During experimental procedures, specimens
results from musculoskeletal injuries, has been should either be immersed in a saline solution or
shown to cause decreases in ultimate loads, elas- constantly kept moist in order to accurately cor-
tic moduli, and cross-sectional area in studies relate measurements to in vivo mechanical prop-
done on rabbit ACL midsubstance and canine erties. Studies that examined the relationship
femur-MCL-tibia complexes [51, 73]. between temperature and the mechanical proper-
ties of ligaments yielded varying results. One
study reported a decline in elastic modulus and
3.5.2 Environmental Factors stiffness with increasing temperature [3].
Another study showed an inverse relationship
When investigating the role of ligaments in an between stiffness and temperature, and the liga-
in vitro setting, researchers should keep in mind ment relaxed to lower values under cyclic load-
several external factors that affect the mechanical ing performed at higher temperatures [44]. In
properties of ligaments. Some of these factors, order to minimize variance between data sets,
such as specimen orientation, should be consid- experimental procedures should also dictate
ered long before testing begins [21, 34, 35, 50, temperature.
71]. Other properties, such as hydration and sur- When designing an experiment, researchers
rounding temperature, are important factors that should pay attention to the strain rate used to
should be monitored during an actual experiment apply loads. One study examined rates of
[3, 15, 36, 37, 62, 66]. 0.003 mm/s, 0.3 mm/s, and 113 mm/s in mature
Before testing begins, specimens will often rabbit ACL and patella tendons and found that
need to be stored frozen in order to preserve their increasing strain rates increase modulus by 31%
biomechanical properties as much as possible. in the ACL and 94% in the patella tendon [19].
Studies have found differing results on the effects One study tried to emulate the rates at which
of freezing on ligaments. One study that put a injuries occur in vitro with rates as high as 500%
bone-patella-tendon-bone complex through mul- per second [18]. However, a different study
tiple freeze-thaw cycles found the tissue can examining rabbit MCLs found that increasing
undergo 8 freeze-thaw cycles without affecting strain rate from 0.01 to 155% per second increases
any biomechanical properties [40]. Other studies the ultimate strength of the tissue by 40% [79].
found that fresh harvested rabbit medial collat- Two studies found loading different ligaments
eral ligaments have little to no structural biome- (rabbit MCL and canine LCL) at a faster rate than
chanical difference when compared to ligaments >1% /s, even up to physiological injury rates
that were properly frozen and then thawed. (>1000% /s), will not drastically affect mechani-
However, these studies did find that during the cal properties from the medium rates of loading
first few cycles of cyclical loading, frozen speci- [8, 17]. At higher speeds, failure mode usually
mens had a significant decrease in the area of shifts from midsubstance to the insertion points
hysteresis that became insignificant with more of the specimen [83].
34 J. D. Hughes et al.

3.6 Summary 9. Bray R, Rangayyan R, Frank C. Normal and heal-


ing ligament vascularity: a quantitative histological
assessment in the adult rabbit medial collateral liga-
Ligaments are soft tissue structures that govern ment. J Anat. 1996;188:87.
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Biomechanics of Bone Grafts
and Bone Substitutes
4
Daniel R. Lee and James W. Poser

Several comprehensive reviews have been pub- nomics are all considerations that should be
lished on bone graft substitutes and provide valu- weighed in the choice to achieve the desired clin-
able background information on the vast array of ical outcome. Most bone grafts and bone substi-
available materials and products [1–3] Rather tutes initially provide very little clinically relevant
than provide yet another product or materials structural stability and ultimately rely on biology
review to add to this comprehensive collection, to restore structural stability and function.
the focus here is to catalog the attributes of these Deciding which bone graft material to select
materials in a context that may help guide the sur- can be a confusing and daunting process. How
geon’s selection of the bone graft substitutes for does one differentiate between the products? Are
particular clinical applications. product claims supported by reliable science and
Achieving the best possible clinical outcome clinical experience? How should variables such
while satisfying the patient’s expectations of as composition, handling, mechanical and bio-
return to functionality should be the principal logical properties, patient clinical presentation,
determinants in choosing which of the myriad of intended outcomes and price are all factors that
bone graft substitutes is the best option for any weigh in decision-making?
clinical application. It is known that the structural The objective in this chapter is to provide
requirements should be considered in the choice some of the information that will be useful for the
of the appropriate bone graft [4]. Many times the clinician in making that decision. Several publi-
choice of bone graft is relegated to availability in cations provide general reviews of the bone graft-
the surgical setting, commercial representation or ing options that are available to the clinician [6,
historic clinical experiences of the clinicians. The 7]. In the current paper, particular emphasis will
choice of a bone graft may also be dependent on be placed on the mechanical properties along
a delicate balance between biology and biome- with material and biological properties of the
chanical stability [5]. Patient age, health status, bone graft with respect to short- versus long-term
and activity level, coupled with clinical presenta- outcomes and patient satisfaction. With this
tion, compliance, rehabilitation options, and eco- objective we will discuss bone grafting options
from the following clinical perspectives and con-
siderations, see Fig. 4.1.
D. R. Lee (*)
CellRight Technologies, LLC, Bone grafts are used to repair and rebuild
Universal City, TX, USA missing, damaged, or diseased bones in a human
J. W. Poser body where the clinical situation where the bone
RegenTX Partners, LLC, San Antonio, TX, USA may not heal by itself or healing might be

© ISAKOS 2021 37
J. Koh et al. (eds.), Orthopaedic Biomechanics in Sports Medicine,
https://doi.org/10.1007/978-3-030-81549-3_4
38 D. R. Lee and J. W. Poser

the structural support to the body, while cancel-


lous bone is extremely porous as it is more
involved in bone remodeling. The turnover rate
of trabecular bone is 25% per year versus only
STRUCTURAL CLINICAL
3% for cortical bone [10]. With respect to
mechanical properties, the compressive strength
of human cortical bone ranges between 90 and
230 MPa and the tensile strength ranges between
90 and 190 MPa [11]. The compressive strength
of human cancellous bone ranges from 2 MPa for
osteopenic cancellous bone to 45 MPa for dense
REGENERATIVE AND cancellous bone [12]. The Young’s modulus of
LONG-TERM
cancellous bone is 10.4–14.8 GPa, while cortical
bone measures 18.4–20.7 GPa [9]. These physi-
cal differences also manifest themselves in bio-
Fig. 4.1 Bone Grafting Considerations logical remodeling and the susceptibility to
pathologies such as osteoporosis. For cortical
bone to be remodeled, osteoclasts and osteoblasts
c­ ompromised. It has been reported that there are are required so the greater surface area of cancel-
over two million bone grafting procedures per- lous bone allows for more rapid revascularization
formed annually [8]. The considerations for the and remodeling.
selection of the optimal bone graft involve bio- Bone regeneration has been defined to involve
mechanical, biomaterial, and biological consid- three pillars: osteogenesis, osteoinduction, and
erations. Among the many options available to osteoconduction [13]. Osteogenesis is the synthe-
the surgeon it is safe to say that the ideal bone sis of new bone by cells derived from either the
graft that performs as well as the patient’s own graft or the host. Osteoinduction is the process
bone (i.e., autograft) has yet to be developed, but where mesenchymal stem cells (MSCs) are
many of the available bone grafting options do recruited and induced to differentiate into func-
have desirable and often suitable properties for a tionally competent osteoblasts and chondroblasts.
particular situation. Osteoconduction is the ability process where bio-
logical interactions along the graft result in fusion
of the graft with the host’s bone. The overall func-
4.1  one Basics: Basic Properties
B tionality of a bone graft is dependent on the graft’s
and Concepts ability to perform these three processes.
The timeline for normal bone regeneration and
Human bone consists of 80% cortical bone and repair involves three distinct phases: inflamma-
20% cancellous bone. Cortical or compact bone tory, proliferative and then remodeling [14]. The
is 70% inorganic material (principally hydroxy- inflammatory stage (weeks 1–3) occurs after the
apatite), 22% organic material (e.g., collagen, insult or injury (hours to days, postoperatively)
non-collagenous proteins, cells, hyaluronic acid), and involves the recruitment and proliferation of
and the rest is water [9]. Cancellous or trabecular inflammatory cells and growth factors and differ-
bone has the same constituents as cortical bone entiation into repair cells and the formation of cal-
but has a lower calcium content, tissue density lus. The proliferative phase (weeks to months,
and ash fraction [10]. Cancellous bone also has post operatively) causes the callus to organize
higher water content (27% compared to 23% for together with a periosteal response which replaces
cortical bone) [10]. Cortical bone is dense, strong, the callus with immature woven bone predomi-
and difficult to fracture and thus provides most of nated with vascular ingrowths and collagen
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CAPITOLO XVIII.
Ambrogio lo stregone.

V’era un fatto semplicissimo, vestito dalle fantastiche forme


dell’immaginazione in tutto il grande avvenimento che susurravano a
bassa voce compiutosi nella casa della valle nella quale gli spiriti
eran tornati ad abitare.
Verso la mezzanotte vi entrava un uomo tutto avvolto in un mantello
andaluso, quell’uomo veniva da una casuccia che è situata tra il
vicolo bargello e la taverna del Gallo Nero.
Nessuno forse vi poneva mente, era una casa bassa, le finestre
n’eran sempre chiuse... pareva ch’essa fosse disabitata ma non
l’era.
Consentimi, lettore, ch’io te la faccia conoscere, sarà un capitolo di
più che avrò aggiunto al mio romanzo, e dopo tutto, la noja di
leggerne uno invece d’un altro tu l’avresti avuta ugualmente... Aperta
la piccola porta il cui battente di bronzo rappresenta un pipistrello
colle ali tese, si salgono tre gradini di marmo, i gradini erano
rozzamente scolpiti, ed eran forse qualche pezzo di granito lavorato
tolto chi sa da qual luogo per farlo servire all’uopo, e ciò lo desumo
perchè nulla del restante della casa era in armonia con quel non so
di stranamente artistico che vi si scorgeva al primo fissarvi lo
sguardo. In una vasta sala dalle nere pareti, ardeva un fornello su
cui arroventavasi un bastone di ferro, v’era presso al fornello un
bacile contenente una sostanza liquida, e presso al bacile una storta
di vetro... sopra un tavolo situato nel mezzo della sala vedeansi due
maschere di vetro opaco, vicino alle maschere due grandi manopole
di pelle di camoscio, in un angolo varii alambicchi di rame... di fianco
al fornello un seggiolone a bracciuoli; nel mezzo, sospesa ad una
corda annerita dal tempo e dal fumo, una lanterna spargeva
d’intorno una semiluce; che dava a quel luogo un aspetto cupo e
fantastico.
Ambrogio lo stregone se ne stava abbandonato dentro alla sua
seggiola assorto nella lettura d’un grosso libro che avea d’innanzi, e
sovra cui fissava il suo sguardo avido ed attento.
Quell’uomo aveva circa cinquant’anni, di fattezze regolari, ma
alterate dalle strane vicende di quella sua vita d’astrazione e d’orgia,
cose che egli alternava come un vero filosofo tedesco alla cui
scienza avea attinte le sue cognizioni in fatto di diavoleria nelle quali
lo si teneva riputatissimo dal volgo, che l’avea veduto più volte in
relazione con Paride Ceresara il mago della casa della valle.
Era esistito in fatti tra Paride Ceresara il distinto alchimista ed
Ambrogio lo stregone, quella relazione che suol correre tra persone
che professino l’arte istessa e che i rapporti della scienza non
possono a meno di avvicinare per quanto dispari possa anche
essere lo stato della loro posizione sociale.
Pel volgo e l’uno e l’altro eran gente perduta che patteggiando col
diavolo avevangli venduta l’anima per comperare i godimenti della
terra... in faccia alla scienza, l’uno era maestro all’altro, e Ambrogio
avea di lui quel rispetto che suole imporre il genio in chi vorria col
pensiero elevarsi tanto alto quanto quelli a cui l’animo tributa il senso
della propria ammirazione... In faccia a sè stessi, Paride Ceresara
era contento d’insegnare al suo discepolo, come questo era lieto
d’imparare; siccome però, dice il proverbio, nelle cose di questo
mondo il diavolo ci vuol sempre mettere la coda, così avvenne che la
sfortuna cacciate le mani ne’ suoi affari e scompigliatili per ogni
verso, lo portò dal campo dell’astrazione poetica in quello della
realtà... vale a dire che ridotto a non aver altri mezzi di sussistenza
dovette lasciar l’estasi delle contemplazioni e far della scienza un
mestiere che gli fornisse di che vivere. Il suo maestro moriva verso
quell’epoca, e se la sua morte gli portò fortuna aumentandogli il
numero degli avventori, non per questo ei men riguardava con
occhio di compianto quei beati giorni passati nei vaghi studii fatti per
dar pascolo al loro desiderio di spaziare in quel vasto campo della
scienza, non circoscritta come or la vedea a servire basse e stolte
superstizioni, senza le quali ei non avrebbe cavato una moneta.
I tempi correvan tristi affè!... e l’esser fabbro di sortilegi in modo
d’averne lucro non era la posizione più sicura del mondo, nè la meno
scevra di pericoli, nè quella in cui fosse facile tirar dritto per la via,
con una mano sulla coscienza.
Il professo d’allora nelle scienze, dovea essere un uomo in relazione
cogli spiriti e votato al diavolo fin dal suo nascere. Era medico, era
astronomo, era mago insomma, e non troppo raramente avveniva
che a qualche vecchia comare saltasse in mente ch’ei dovesse
risuscitare qualche morto e a qualche marrano che dovesse alla
spiccia far morire qualche vivo... Era un navigare tra Scilla e Cariddi,
colla prospettiva poco seducente di urtare un giorno o l’altro in uno di
questi scogli, e farla finita, o coll’onestà... o forse con qualch’altra
cosa che a seconda dei casi può valere di più o di meno.
Nel momento in cui noi poniamo piede nel vasto stanzone
dell’alchimista, egli tolse lo sguardo dal libro e si volse con atto di
mal umore.
Erano stati battuti alcuni colpi alla porta della casa.
Egli attese un istante.... il battente martellò di nuovo; si alzò ed andò
ad aprire!... Fu un’esclamazione di sorpresa e di disgusto che suonò
sul suo labbro — Voi!...
— Io!... rispose con voce franca e quasi impudente il visitatore.
— Se avete bisogno dei miei servigi nel modo in cui ve li ho ricusati
altra volta, vi prevengo essere affatto inutile che noi ci tratteniamo...
— Non è la morte che vengo a chiedervi, maestro Ambrogio... è la
vita.
— Ho io il potere di Dio?...
— Avete la facoltà della scienza.
— Cosa chiedete?..
— Un farmaco che renda la vita ad una donna.
— E perchè volete farla vivere?... gli domandò il negromante
fissando sul suo interlocutore uno sguardo a cui pareva non potesse
sfuggire un men che menomo attimo del pensiero.
— Che v’importa?... rispose questi confuso.
— Importa molto... a colui a cui si venga a dire, fate vivere un’anima,
fate palpitare un cuore!... la morte è la cessazione delle sensazioni
umane, perchè dovrei io far vivere? per permettervi forse la
tortura?...
— Maestro Ambrogio, siete molto bisbetico questa notte... affè...
parmi vi passino ben strambe idee pel capo...
— Spicciamoci dunque?.. È la vita che voi volete?..
— La vita.
— Per utilizzarla come una merce?..
— No; per rendere la pace ad una famiglia.
— È questo il vostro pensiero?..
— Questo...
Il negromante stette alcuni istanti meditabondo, si volse verso un
uscio che metteva ad una scaletta e chiamò: Bianca, Bianca...
Una vaga giovinetta pallida, pallida, dallo sguardo color cielo, dai
capelli d’ebano, dai labbri di cinabro, bella come uno di quegli angioli
che il pennello del Buonarotti dipinse, tipi eterni di bellezza sulle
immortali sue tele, si affacciò alla soglia.
— Eccomi, diss’ella.
Il visitatore la contemplò affascinato, poi volse il pensiero sul
negromante che muto non vi fe’ risposta: fissava immoto la
giovinetta e puntandogli le mani stese verso il petto la fe’ ristare
come sotto l’influenza magica di un fascino strano... Bianca.... gli
domandò egli poichè la vide calma, tranquilla ed immobile a sè
d’innanzi, serena la fronte, sorridente il viso, e seduta con dolce
abbandono sovra una sedia vicina.
La fanciulla provò un tremito.
— Bianca, ripetè Ambrogio, vedi tu?..
— Sì... vedo, rispose la fanciulla con voce dolce e soave.
— Leggi tu nel mio pensiero?..
— Vi leggo.
— Sai chi sia a me d’innanzi in questo momento?..
La fanciulla pronunciò il nome dello straniero, con un atto appena
percettibile di disgusto.
— Perchè ti agiti?... cos’è che ti fa male?...
— Nulla.
Il vecchio Ambrogio guardò inquieto lo straniero che sorrise con
piglio di disprezzo.
Il negromante non gli badava più. Tutto assorto come era nella sua
operazione, tutto il fuoco della sua anima parea fosse passato nella
sua pupilla, larga, fissa ed immota... Il lume della lampada oscillava
sprizzando all’intorno pallidi raggi di luce. Il vecchio girava intorno
alla giovinetta agitando le braccia, descrivendo colla mano scarna
magici circoli intorno alla sua bella testa che sorrideva; lo straniero si
sentiva suo malgrado dominato dallo strano svilupparsi di quella
scena, egli si trovava in faccia a quell’apparenza del soprannaturale
alla cui impressione si dovettero i fatti più strani e più terribili che
lasciarono pagine di sangue sul libro della storia di tutti i popoli.
La scienza vestiva a quei tempi una forma atta a colpire lo spirito,
incapace come era di rivelarsi alla ragione, ond’è che quelli che ne
traevan lucro assumevan in faccia al volgo qualità strane di enti
diabolici ed altro.... Nè per volgo s’intenda quella parte di popolo che
costituiva la plebe. Nelle case di maggior locazione non si pensava
diversamente che dalle donnicciuole di piazza.... si accettava un
fatto... per non analizzarlo; si avea paura del demonio e lo si
evocava per trarne gli oroscopi a mezzo di qualche suo
rappresentante.
— Presto, sbrigati!... o che il malanno ti porti!... borbottò lo straniero,
mal potendo frenare un senso d’impazienza e nello stesso tempo
impedito da una panica apprensione a dar sfogo al suo mal umore.
Il vecchio non fe’ moto... dalla pupilla della giovinetta parve uscisse
un lampo di luce, egli passò ambe le mani sulle sue ciglia, ne
premette le tempia, e raccogliendo tutta la forza della sua volontà, le
domandò con voce chiara:
— Vedi?...
— Come è bella!... mormorò la giovinetta, e sulle sue labbra corse
un sorriso quasi salutasse col cuore l’imagine che le vagava nel
pensiero. Come è bella! ripetè ancora fra sè.
— È quella che vedi la donna ch’egli vuol salvare? interrogò il
negromante.
La fanciulla si raccolse un istante. — Sì, rispose ella con voce
debole... si agitò, alzò la mano come accennasse a seguire un
pensiero fatto vivo nella sua mente, e disse con accento d’indicibile
tristezza: — Muore...
Lo straniero fremette, e interrogò Ambrogio con uno sguardo
inquieto.
Questi continuava a fissare la fanciulla.
— Guarda, guarda... Bianca... gli replicò egli con forza.
— No, no... diss’ella rasserenandosi in viso, vi è ancora della vita nel
suo petto!.... Oh ella è forte!... aspetta...
I due testimoni di questa scena bizzarra ascoltavano assorti con
tutte le facoltà della loro anima in ogni parola che usciva dalle labbra
della giovinetta, in ogni atto che palesasse un pensiero.
Pel negromante era il miracolo della scienza che si svolgeva ai suoi
occhi abbagliati.
Nello straniero v’era un senso di avida curiosità che andava
svolgendosi a norma che si incalzavano quelle rivelazioni a cui
parea fosse annesso chi sa qual misterioso interesse.
Era successo un istante di pausa... si sentiva l’ansia dei loro petti
alitare con febbrile violenza. Il negromante parea che raddensasse
con forza crescente la vigoria d’un pensiero che dovesse soffiare
sulla vita artificiale che parea accendersi nella mente della fanciulla.
— Aspetta, continuò essa, io la vedo... Come è bella!... quanto
soffre!... La fanciulla mandò un debole grido, stette anelante
incerta... indi proseguì accennando tutti i sintomi di una emozione
vera: Aspetta... C’è una frase di convenzione, una specie di modo di
dire di tutti i magnetizzati. Il suo occhio è infossato... Dio!... come
soffre da tanto tempo!... Sua madre veglia al suo letto... essa
l’interroga... l’ammalata sorride.... ella non crede di guarire!... Eppure
la sua famiglia aspetta... Un uomo ha promesso di salvarla...
quell’uomo... Essa ristette un momento come oppressa dalla foga
del pensiero; aspetta... mormorò a bassa voce usando di quella
formula come di una sosta onde riprender lena. Quell’uomo....
Lo straniero sentì un brivido corrergli per l’ossa.
— Ebbene?... ebbene?... domandò con ansia il negromante.
— È qui, seguitò la giovinetta. Ti ha chiesto un farmaco... salvala!...
Essa muore... La fanciulla come sfinita dallo sforzo operato lasciò
cadere con abbandono il capo sul guanciale della poltrona.
— Sono con voi, disse Ambrogio allo straniero, facendogli segno
colla mano che andasse seco.
Lo straniero obbedì. Il negromante s’avvicinò ad una scansia chiusa
a chiave e scelse una fiala di vetro ermeticamente chiusa fra le tante
che v’erano dentro accatastate.
— Sul vostro onore, gli diss’egli, è la verità ciò che ha detto Bianca?
— Lo giuro, rispose lo straniero.
— Sta bene!.... Poche goccie è la vita, qualche goccia di più è la
morte.
— Iddio vi guardi!
Ambrogio consegnò la fiala allo straniero, questi porse al
negromante una borsa ed uscì fuori da quella casa fantasticando
bizzarre immagini di diavoli e di streghe, che gli parea avesser
dovuto ronzare intorno al suo letto a turbarne le notti insonni agitate
forse da un pensiero che dal fondo dell’animo sorgeva a giudicarlo
inesorabile e severo.
CAPITOLO XIX.
Presentimenti.

Nella famiglia del marchese Gian Paolo si aspettava intanto colla più
viva impazienza il ritorno dello straniero. In quella notte che dovea
precederne la venuta, e madre e padre e fratello aveano avuto per la
povera fanciulla uno sguardo in cui eravi espressa tutta l’ansia d’una
speranza cara come un sogno di felicità.
La fanciulla sorrideva col suo mesto sorriso di rassegnata, e volgeva
il raggio de’ suoi belli occhi celesti verso un angolo della stanza da
dove Adolfo stava contemplandola triste ed abbattuto. Parea che
non una di quelle soavi illusioni facesse velo alla fatalità d’una
sinistra previsione che gli stava fissa nel cuore. Egli aveva tanto
combattuto contro sè stesso, si era detto pazzo, avea cercato di
sorridere ad Angela quando parea richiesto di un pensiero che ella
avrebbe accarezzato con fede!
Quel senso indefinito, indefinibile era là.... s’era cacciato nel suo
cuore e non valeva a strapparvelo!... Esso sfuggiva all’analisi, era
vago come un sogno... Era nulla... era un’ombra nel vuoto.... ma era
tale da gelargli il sorriso sulle labbra contratte da un amaro
dispetto.....

· · · · · · · · · · · · · · · ·

Lo straniero è ritornato, egli ha recato seco il prezioso farmaco. Il


marchese non si sazia dall’attestargli la sua riconoscenza, la madre
di Angela piange di gioia baciando le guancie della giovinetta, che
vanno riprendendo il lor colorito vitale. Angela sorride più vaga e più
bella al giovane suo amico nel cui animo tutto ciò mette un arcano
sbigottimento, e che ella si sforza a cancellare con tutte le
dimostrazioni del più tenero affetto.
La gioia, quella vaga silfide dal volo leggiero, ha ripreso il suo posto
in quel campestre romitaggio; la primavera lo adorna col suo manto
di verzura, l’aria lo circonda dell’olezzo dei fiori rapito alle ricche alee
del giardino, la rondine stridendo vi volteggia intorno, e dal trave
ospitale saluta il diletto suo nido; s’ode alla sera l’allegra canzone dei
campagnoli che ritornano ai loro casolari dove li allieterà il sorriso
delle loro donne ed il bacio dei loro figli. Non più quel tetro squallore,
non più sugli incolti viali cadono le foglie degli alberi disseccate, nè i
fiori dagli steli; non più il paesano riguarda le chiuse imposte e si
dice mestamente: là si soffre... e pensa che colei che soffre era
l’angelo che si recava al letto delle sue figlie ammalate a portarvi il
conforto di una parola; il brodo della sua mensa, il farmaco della sua
casa, il fiore del suo giardino!...
È una bella mattina del mese di aprile... l’aria è imbalsamata di
profumi... piena di melodie... l’usignuolo ed il capinero gorgheggiano
di mezzo alle verdi siepi e si ricambiano le loro canzoni d’amore; la
cingallegra volteggia vispa e gaia di ramo in ramo.
Sotto ad un verde chiosco del giardino era raccolta la famiglia del
marchese intenta ad un gaio confabulare; Angela appoggiavasi
tutt’ora debole per la passata malattia, al braccio del padre; sua
madre la contemplava seduta vicino a lei con un lungo sguardo di
amore; Adolfo discorreva col fratello d’Angela appoggiati entrambi
alla spalliera del chiosco. Lo straniero vi entrava dopo aver colto un
fiore da una vicina alea e lo porse alla giovinetta.
Angela gettò uno sguardo sopra Adolfo, il cui occhio avea seguito lo
straniero con palese inquietudine.
— È il fiore dell’addio che vi reco, madamigella, disse lo straniero ad
Angela; ne avvisai già il marchese; alcuni affari mi chiamano a
Mantova onde reclamare dai Gonzaga un appoggio contro le
angherie di cui mi fa scopo la Corte dei duchi di Milano.
— Voglio sperare che non sarà un congedo, gli rispose il marchese
con confidente premura, non è vero, dottore?
— V’assicuro, marchese, che ho ben poche volte in vita mia fatto
uso di pozioni, e lasciai per solito la cura ad altri di guarire qualche
parte del corpo a cui l’armatura non sia stata bastevole riparo, gli
ribattè lo straniero sorridendo.
— In ogni modo è il titolo che vi fa più caro alla mia amicizia, poichè i
vostri colpi di spada non avrebbero salvata la mia Angela. Mi
permetto quindi di ripetervi di nuovo: Dottore, la mia casa è sempre
aperta per voi, alla mia tavola vi è un posto che vi aspetta.
Lo straniero s’inchinò.
— Il mio cavallo è sellato, diss’egli accommiatandosi coll’atto.
Tutti si alzarono, il marchese passò amichevolmente il suo sotto al di
lui braccio e rifecer la via intrattenendosi gajamente.
Angela si strinse al braccio della madre; il suo sguardo scontrossi in
quello di Adolfo e mandò un lampo di felicità.
— Avrò il piacere di rivedervi presto, madamigella, gli disse lo
straniero che si era rivolto verso lei in quel momento.
Vi era una strana accentazione in quelle parole. Angela se le sentì
vibrare sinistramente nell’anima come la minaccia d’una sventura, e
guardò quasi impaurita sua madre, che volgendosi allo straniero
dicevagli colla sua voce più calma:
— Ella sarà sempre il benvenuto, signore.
Adolfo raccolse tutto il fuoco della sua anima avvampante nello
sguardo, e fissò lo straniero; questi parea non si fosse neppur
accorto della presenza del giovane, che si morse le labbra di
dispetto.
Si era arrivati al cortile della casa; un paesano teneva per la briglia il
cavallo dello straniero. Era un magnifico baiardo che nitriva
salutando il suo signore. Ei gli si fe’ vicino, lo accarezzò, in un salto
snello e leggiero fu in sella, strinse di nuovo la mano al marchese,
salutò colla mano Angela, Alberto e la madre, e dopo alcuni istanti
non si sentiva che il lontano scalpitare del suo cavallo sulla strada di
Mantova, verso cui correva a tutta briglia.
— È partito!... mormorò con senso di rincrescimento il marchese,
volgendo lo sguardo per dove era scomparso il cavaliere.
— Finalmente!... mormorarono con un sospiro Angela ed Adolfo.
La marchesa Isabella, la madre di Angela, non disse nulla. Essa
guardava Angela, il cui volto s’era fatto sorridente di felicità. Il cuore
della madre si arrestava d’innanzi un quesito di cui non sapeva
trovare la soluzione. Il cuore della donna rispettava uno di quei mille
sentimenti per cui l’analisi non trova che il mistero d’un’impressione
che alle volte è rivelatrice dei più terribili arcani della vita.
V’era diffatti una strana contradizione nel vincolo di quei varii
sentimenti che si erano svolti sotto a’ suoi occhi ed innanzi al suo
cuore nella durata di quella breve scena. Donna Isabella era madre,
e madre in tutta la santità di quella soave parola, che compendia in
sè quanto v’ha di grande e di nobile nell’anima umana!... Se v’ha
qualche cosa in questo vasto organismo della creazione, così strano
per le sue inconseguenze.... nei suoi rapporti... nelle sue
stravaganze inqualificabili... atto a far ricredere dall’ateismo da
questo pensiero per cui si sconoscerebbe anche sè stessi, per non
maledire a tutto ciò che è intorno a noi, saria il sublime mistero, che
è il cuore d’una madre!... Donna Isabella dunque, come dicemmo,
compendiava in sè una delle mille fasi di questo misterioso enigma.
Esser madre è avere in sè la divinazione di quei non nulla che sono
il tutto dell’esistenza!... è leggere col pensiero nel sorriso del labbro
per strappare di sotto a quella forma che è una menzogna il gemito
dell’anima... L’esser madre è il non vivere per sè, ma è l’identificarsi
nell’esistenza de’ suoi figli, è quasi un fondersi con essi con tal
legame d’affetto, che i dolori di questi gli sieno proprj... è il rendere
impossibile la menzogna del labbro, come quella della mente, è
sentire quell’uniformità di sensazioni mediante le quali il cuore non
ha bisogno della parola per rivelarsi.
E Angela... quel tenero virgulto cresciuto ai miti raggi di quel sole
fecondatore si svolse lussureggiante e bello; si svolse anima nobile
e peregrina interrogando il gorgheggio dell’usignuolo che cantava tra
le rose del suo giardino; interrogando lo schiudersi del fiore che non
volea spiccare perchè gli incresceva vederlo sì tosto appassire,
fissando gli occhi in quelli della madre per cercarvi un conforto a
quel sentimento che serpeggiava fuoco sottile, ma ardente nelle sue
vene, ed allorchè le informi larve della sua fantasia modellate a poco
a poco dalle arcane indagini del pensiero ridessero ai suoi occhi una
forma, indefinita sì, ma che vestivasi di ognor più potente attraenza,
allora ella sentì il bisogno d’una parola che diversa da quella della
madre gli mormorasse all’anima avida di emozioni la prima nota del
sublime poema della vita...
Come era bella, appoggiata talvolta al suo balcone illuminata dalla
mistica luce di qualche astro gentile, a cui la sua anima sembrava
favellare misteriose parole!
Era pur bella!... china la fronte sul suo seno d’alabastro, simile alla
Margherita di Goethe che sfoglia il fiore della rivelazione, sfogliava
essa i fiori del suo pensiero cercandovi il più bello ed il più olezzante.
Era pur bella, assorta in melanconico atto eppur raggiante di vita e di
speranza... stretto l’esile corpiccino dalla bianca sua veste, puro
giglio fragrante che mano impudica avria dovuto arrestarsi dal
toccare, che alito umano non avria dovuto avvizzire!..
Perchè si agita così il tuo seno di neve?.. perchè balbetta inarticolati
accenti il tuo labbro?.. forse un nome... il suo!... prima ancora che tu
lo sapessi, chi sa quante volte hai sognato una larva vanescente...
ma che importa?.. la tua anima la vestiva d’un’immagine... nel
silenzio delle tue notti di vergine, tu ascoltavi un’arcana melodia a
cui univi il tuo sospiro, il tuo voto, puro come la prima preghiera che
insegnava tua madre al tuo labbro di fanciulla, al tuo cuore di
donna... santo come tutto ciò che è giovinezza, perchè giovinezza è
fede... Giovinezza è amore... ed al senso arcano che molcea le tue
fibbre di diciassette anni rispondevi con un suono indefinito... ti
sovvenivi della prima parola con cui chiamandoti ti baciava tua
madre e l’hai mormorata stemperando la tua anima in un sospiro. —
Mio Angelo...
La marchesa aveva compreso quel suo cuore di fanciulla, ne aveva
seguito fin dalla culla il rapido sviluppo. L’avea veduta crescere sotto
i suoi baci, interrogando ogni palpito del suo petto... in lei non potea
esservi atto nel quale non leggesse l’impronta del pensiero come il
senso del cuore... Eppure le pareva strana quell’impossibilità di
interrogare un sentimento che ella non arrivava a comprendere,
forse perchè era un mistero anche per l’animo istesso della
giovinetta... Una di quelle sensazioni che sono in noi, che ci
dominano, che vivono d’una vita loro propria, che interrogate
svaniscono, che assopite ritornano, che ci assediano, ci tormentano,
e contro cui la ragione trova l’inutilità de’ suoi sforzi, per l’impotenza
appunto di questi!..
Perchè mai sentiva Angela un senso d’avversione dirò così, per un
uomo che l’aveva sottratta alla morte?.. per un uomo al quale il
marchese avrebbe data la vita?... che sua madre avrebbe baciato
qual figlio?... L’irriconoscenza non è per sè stessa una colpa?... e
come poteva quel bel cuore d’angelo schiuso ai più puri affetti, alle
più nobili aspirazioni, nutrire un senso che fosse una violazione di
queste sante leggi della natura?... No, si dicea essa, in queste leggi
istesse che agli animi incorrotti tracciano la via delle loro azioni, deve
essere la causa di questa sensazione, che un’altra sensazione
attutisce nel suo sviluppo... Il pensiero non le rendeva conto di ciò,
ma vagamente la madre si faceva sue le indefinite sensazioni che
s’agitavano nel cuore d’Angela...
Ella osservò che Angela avea impallidito ricevendo dallo straniero
quel fiore che ei le porgeva in segno d’addio come in lei volesse
lasciare una memoria. Avea notato lo sguardo furtivo, inquieto che la
giovinetta avea lanciato verso Adolfo, e come questi impiegasse
tutta la vigoria della sua volontà per imporre una calma artificiale alla
segreta tortura del suo animo. Angela si era appoggiata a lei come
ricorrendo ad un conforto allorchè lo straniero le avea fatto
presentire la possibilità del suo ritorno; Angela temeva quello
straniero appunto perchè sentiva che egli voleva attaccarsi alla vita
che aveagli resa in modo sì strano!... ma lo temeva essa nel dubbio
che un giorno egli potesse reclamare un diritto?.. oppure questo
timore istesso accusava in lei un affetto già formatosi nel cuore e
che avea paura d’ogni ombra che potesse frenarne lo slancio?..
Nel pensiero della madre, sorse uno di quei lampi che sono la parola
della rivelazione parlata al cuore colle mille voci dell’animo; ella sentì
che Angela avea scelto tra l’uomo che l’avea resa alle braccia del
padre, e l’uomo che l’avea resa all’amore dei suoi cari... Quel
sentimento di freddezza verso lo straniero che l’avea salvata dalla
morte, proveniva dall’aver lo slancio del suo cuore assorbite tutte le
facoltà sensuali della sua anima vergine d’affetti, che s’era
abbandonata tutta intera alla sua prima e pura rivelazione!..
Angela amava!.. amava un cuore devoto che l’avea conquistata con
un eroismo; più che con un eroismo!... con un atto di disinteresse
tutto umano!.. affrontando un pericolo per salvare una vittima che
era uno straniero per lui, e che era suo padre!.. V’era la fatalità!..
questa figlia della poesia delle menti giovani e vergini in
quell’avvenimento che avea segnato una meta sul sentiero della sua
esistenza!..
Angela amava!.. era un affetto a cui sorrideva come una benedizione
il pensiero di sua madre!.. Ella accarezzò più dolcemente la sua
vaga bambina dalle belle chiome di corvo, dal bel guardo celeste e
soave; essa strinse con più affetto la mano di Adolfo!.. Essa lo
chiamò figlio collo slancio più tenero del suo cuore!... ed Angela le si
gettò confidente tra le braccia, mormorando col cuore ebbro
d’affetto!.. Oh come l’amo, madre mia!...

FINE DEL PRIMO VOLUME.


INDICE

VOLUME PRIMO

CAPITOLO
I. Che può servire d’introduzione Pag. 5
II. Una notte infernale 19
III. La taverna del Gallo Nero 27
IV. La ballata dei morti 39
V. Il Testamento 43
VI. Il fratricidio 47
VII. In cui si parla di ciò che si dice 51
VIII. Giulietta 55
IX. Il vendicatore 65
X. Schiarimenti 75
XI. La trama 81
XII. La capanna del carbonaro 89
XIII. L’agguato 95
XIV. Dieci anni dopo 109
XV. Adolfo 115
XVI. In cui il Romanzo s’imbroglia
maledettamente 125
XVII. Ancora il Palazzo del Diavolo 151
XVIII. Ambrogio lo stregone 157
XIX. Presentimenti 169
Nota del Trascrittore

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errori tipografici.
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