The Role of Scapular Dyskinesis in Rotator Cuff and Biceps Tendon Pathology

235 Pages·2016·5.75 MB·English

UUnniivveerrssiittyy ooff PPeennnnssyyllvvaanniiaa
SScchhoollaarrllyyCCoommmmoonnss
Publicly Accessible Penn Dissertations
2014
TThhee RRoollee ooff SSccaappuullaarr DDyysskkiinneessiiss iinn RRoottaattoorr CCuuffff aanndd BBiicceeppss
TTeennddoonn PPaatthhoollooggyy
Katherine E. Reuther
University of Pennsylvania, [email protected]
Follow this and additional works at: https://repository.upenn.edu/edissertations
Part of the Biomechanics Commons, and the Biomedical Commons
RReeccoommmmeennddeedd CCiittaattiioonn
Reuther, Katherine E., "The Role of Scapular Dyskinesis in Rotator Cuff and Biceps Tendon Pathology"
(2014). Publicly Accessible Penn Dissertations. 1416.
https://repository.upenn.edu/edissertations/1416
This paper is posted at ScholarlyCommons. https://repository.upenn.edu/edissertations/1416
For more information, please contact [email protected].
TThhee RRoollee ooff SSccaappuullaarr DDyysskkiinneessiiss iinn RRoottaattoorr CCuuffff aanndd BBiicceeppss TTeennddoonn PPaatthhoollooggyy
AAbbssttrraacctt
Shoulder tendon injuries including impingement, rotator cuff disease, and biceps tendon pathology are
common clinical conditions and are a significant source of joint pain, instability, and dysfunction. These
injuries may progress into partial tears then to complete tendon ruptures, which have limited healing
capacity even when surgically repaired. These injuries are frequently seen in the presence of abnormal
scapulothoracic joint kinematics (termed scapular dyskinesis). However, the cause and effect relationship
between scapular dyskinesis and shoulder injury has not been directly defined. Additionally, while the
incidence of shoulder injuries and recurrent failure of repairs is well-documented, the mechanisms behind
them are not well-established, making optimal clinical management difficult. Therefore, the objectives of
this study were to examine the effect of scapular dyskinesis on the initiation and progression of
pathological changes in the rotator cuff and biceps tendon and to define the mechanical processes that
lead to these changes. Unfortunately, clinical and cadaveric studies are unable to address the underlying
causes of injury and cannot evaluate the injury process over time. Therefore, a rat model of scapular
dyskinesis (created by denervating the trapezius and serratus anterior) was developed and used, both
alone and in combination with overuse, to investigate the cause and effect relationships between
changes in joint loading and alterations in tendon mechanical, histological, organizational, and biological
properties. We hypothesized that scapular dyskinesis would result in altered joint loading conditions that
would lead to degeneration of the rotator cuff and long head of the biceps. We found that scapular
dyskinesis diminished joint function and passive joint mechanics and significantly reduced tendon
properties. We also investigated the effect of overuse on tendon properties and found that overuse
activity in the presence of scapular dyskinesis resulted in significantly more structural and biological
adaptations than scapular dyskinesis alone. We also investigated the effect of scapular dyskinesis on
supraspinatus tendon healing and found that scapular dyskinesis was detrimental to tendon properties.
These results indicate that scapular dyskinesis is a causative mechanical mechanism of shoulder tendon
injury. Identification of scapular dyskinesis as a mechanism of pathological changes will help inform and
guide clinicians in developing optimal prevention and long-term rehabilitation strategies.
DDeeggrreeee TTyyppee
Dissertation
DDeeggrreeee NNaammee
Doctor of Philosophy (PhD)
GGrraadduuaattee GGrroouupp
Bioengineering
FFiirrsstt AAddvviissoorr
Louis J. Soslowsky
KKeeyywwoorrddss
Animal Model, Biceps, Overuse, Rotator Cuff, Scapular Dyskinesis
SSuubbjjeecctt CCaatteeggoorriieess
Biomechanics | Biomedical
This dissertation is available at ScholarlyCommons: https://repository.upenn.edu/edissertations/1416
THE ROLE OF SCAPULAR DYSKINESIS IN ROTATOR CUFF AND BICEPS
TENDON PATHOLOGY IN A RAT MODEL
Katherine Reuther
A DISSERTATION
In
Bioengineering
Presented to the Faculties of the University of Pennsylvania
in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy
2014
Supervisor of Dissertation
__________________________
Louis J. Soslowsky, PhD, Fairhill Professor, Orthopaedic Surgery

Graduate Group Chairperson
__________________________
Jason A. Burdick, PhD, Professor, Bioengineering

Dissertation Committee
Kristy B. Arbogast, PhD, (Committee Chair)
Research Associate Professor, Pediatrics, Children’s Hospital of Philadelphia
Mary F. Barbe, PhD
Professor, Anatomy and Cell Biology, Temple University
Kurt D. Hankenson, DVM, PhD
Associate Professor, Animal Biology, University of Pennsylvania
Andrew F. Kuntz, MD
Assistant Professor, Orthopaedic Surgery, University of Pennsylvania
Philip W. McClure, PT, PhD, FAPTA
Professor, Physical Therapy, Arcadia University
Acknowledgements
I would like to thank my advisor, Dr. Louis Soslowsky, for providing mentorship
and support throughout my time here. I admire and respect him as a mentor and person
and am grateful for his time, patience, commitment to teaching and mentoring, and
valuable insight. I would like to thank my committee members for guiding me through
my graduate education. I thank Dr. Andrew Kuntz for surgical assistance and clinical
insight throughout the development and duration of this project. I also thank Dr. Philip
McClure, Dr. Mary Barbe, Dr. Kurt Hankenson, and Dr. Kristy Arbogast for their time
and valuable insight and suggestions for this project.
I would also like to thank the entire McKay Orthopaedic Research Laboratory.
Dr. Stephen Thomas has been my mentor, Joint Damage partner, and colleague from the
beginning and continues to be a close friend. His knowledge, advice, and clinical insight
have been instrumental in my graduate education and in this dissertation. I would like to
thank Jennica Tucker, Dr. Sarah Yannascoli, Dr. Adam Caro, and Dr. Joshua Gordon for
their surgical assistance and willingness to help and discuss ideas. I would like to thank
Rameen Vafa for his numerous contributions to this project and for his admirable work
ethic and enthusiasm. I would like to thank Adam Pardes, Stephen Liu, Bob Zanes,
Julianne Huegel, Pankti Bhatt, and Alex Delong for their contributions to this project. I
would like to thank my fellow graduate students, Sarah Rooney, Brianne Connizzo, Ben
Freedman, Cori Riggin, and Adam Pardes, for their support and friendship. I would like
to thank Kris Miller for her friendship and guidance. I would also like to acknowledge
all the past and present graduate students, residents, post-docs, and staff members, for
their friendship and valuable insights and discussions.
ii
Finally, I thank my family for their unwavering love and support throughout my
life, from the athletic field to the classroom. I thank my parents, Jack and Roxanne, and
my sister, Jessica, who have always encouraged and supported me. I thank them for
helping to guide me through the highs and lows and for providing comfort, support, and
understanding. I thank John, whom I was blessed to share this journey with, for his
tremendous understanding and support. I would also like to thank my grandparents,
Anne and Tim, for their constant prayers and love. This would not have been possible
without them.

iii
ABSTRACT
THE ROLE OF SCAPULAR DYSKINESIS IN ROTATOR CUFF AND BICEPS
TENDON PATHOLOGY IN A RAT MODEL

Katherine Reuther
Dr. Louis J. Soslowsky

Shoulder tendon injuries including impingement, rotator cuff disease, and biceps
tendon pathology are common clinical conditions and are a significant source of joint
pain, instability, and dysfunction. These injuries may progress into partial tears then to
complete tendon ruptures, which have limited healing capacity even when surgically
repaired. These injuries are frequently seen in the presence of abnormal scapulothoracic
joint kinematics (termed scapular dyskinesis). However, the cause and effect relationship
between scapular dyskinesis and shoulder injury has not been directly defined.
Additionally, while the incidence of shoulder injuries and recurrent failure of repairs is
well-documented, the mechanisms behind them are not well-established, making optimal
clinical management difficult. Therefore, the objectives of this study were to examine
the effect of scapular dyskinesis on the initiation and progression of pathological changes
in the rotator cuff and biceps tendon and to define the mechanical processes that lead to
these changes. Unfortunately, clinical and cadaveric studies are unable to address the
underlying causes of injury and cannot evaluate the injury process over time. Therefore,
a rat model of scapular dyskinesis (created by denervating the trapezius and serratus
anterior) was developed and used, both alone and in combination with overuse, to
iv
investigate the cause and effect relationships between changes in joint loading and
alterations in tendon mechanical, histological, organizational, and biological properties.
We hypothesized that scapular dyskinesis would result in altered joint loading conditions
that would lead to degeneration of the rotator cuff and long head of the biceps. We found
that scapular dyskinesis diminished joint function and passive joint mechanics and
significantly reduced tendon properties. We also investigated the effect of overuse on
tendon properties and found that overuse activity in the presence of scapular dyskinesis
resulted in significantly more structural and biological adaptations than scapular
dyskinesis alone. We also investigated the effect of scapular dyskinesis on supraspinatus
tendon healing and found that scapular dyskinesis was detrimental to tendon properties.
These results indicate that scapular dyskinesis is a causative mechanical mechanism of
shoulder tendon injury. Identification of scapular dyskinesis as a mechanism of
pathological changes will help inform and guide clinicians in developing optimal
prevention and long-term rehabilitation strategies.
v
TABLE OF CONTENTS

Acknowledgements ........................................................................................................ ii
Abstract .......................................................................................................................... iv
Table of contents ........................................................................................................... vi
List of tables.................................................................................................................. xii
List of figures ............................................................................................................... xiii
Chapter 1 : Introduction ...............................................................................................1
A. Introduction ...........................................................................................................1
B. Background ...........................................................................................................4
1. Shoulder anatomy ............................................................................................4
a. Glenohumeral Joint ....................................................................................5
b. Scapulothoracic Joint .................................................................................6
2. Normal Shoulder function................................................................................6
a. Role of the Glenohumeral Joint .................................................................6
b. Role of the Scapulothoracic Joint ..............................................................7
c. Scapulohumeral Rhythm ............................................................................9
3. Scapular Dyskinesis .........................................................................................9
a. Classification ..............................................................................................9
b. Causes ......................................................................................................10
c. Associated Injuries and Impairments .......................................................11
d. Treatment .................................................................................................11
4. Tendon properties ..........................................................................................12
vi
a. Biology and composition .........................................................................12
b. Structure and function ..............................................................................13
c. Mechanics ................................................................................................14
d. Injury and healing ....................................................................................15
e. Responses to changes in loading ..............................................................16
5. Cartilage properties ........................................................................................17
a. Biology and composition .........................................................................17
b. Structure, Function, and Mechanics.........................................................17
c. Responses to changes in loading ..............................................................18
6. Rat Model System ..........................................................................................19
a. Justification ..............................................................................................19
b. Investigations for Scapular Dyskinesis in Animal Models ......................20
C. Specific aims .......................................................................................................20
D. Study design ........................................................................................................23
E. Chapter overview.................................................................................................26
F. References............................................................................................................27
Chapter 2 : Scapular dyskinesis is detrimental to shoulder tendon properties and
joint mechanics in a rat model ...............................................................................35
A. Introduction .........................................................................................................35
B. Methods ...............................................................................................................37
1. Study design and surgical technique ..............................................................37
2. Quantitative ambulatory assessment ..............................................................39
3. Passive joint mechanics .................................................................................39
vii
4. Sample preparation for mechanical testing ....................................................39
5. Tendon mechanical testing ............................................................................40
6. Tendon histology ...........................................................................................41
7. Tendon immunohistochemistry .....................................................................41
8. Cartilage mechanical testing ..........................................................................44
9. Serum biomarkers ..........................................................................................47
10. Statistical analysis ........................................................................................47
C. Results .................................................................................................................48
1. Ambulatory data.............................................................................................48
2. Passive joint mechanics .................................................................................51
3. Tendon mechanics .........................................................................................52
4. Tendon histology ...........................................................................................55
5. Tendon immunohistochemistry .....................................................................58
6. Cartilage mechanics and thickness ................................................................61
7. Serum biomarkers ..........................................................................................62
D. Discussion ...........................................................................................................66
E. References ...........................................................................................................72
Chapter 3 : Overuse activity in the presence of scapular dyskinesis leads to
shoulder tendon damage in a rat model ................................................................77
A. Introduction .........................................................................................................77
B. Methods ...............................................................................................................78
1. Study design ...................................................................................................78
2. Quantitative ambulatory assessment ..............................................................79
viii