Beyond the tissue: The relationship between Structure, Function, and Pain in Achilles Tendinopathy

362 Pages·2017·3.21 MB·English

Beyond the tissue: The relationship between
Structure, Function, and Pain in Achilles
Tendinopathy
By
Seán Mc Auliffe BSc

Supervised by Dr. Kieran O’Sullivan, Dr. Karen Mc Creesh and
Dr. Helen Purtill.
A thesis submitted in fulfillment of the requirements for the degree of
Doctor of Philosophy at the University of Limerick
Submitted: November 2016
DECLARATION
My submission as a whole is not substantially the same as any that I have
previously made or currently am making, whether in published or unpublished
form for a degree, diploma, or similar qualification at any university or similar
institution. I am the author of this doctoral thesis and the principal author of the
five articles, which form its core.

Signature:
Seán Mc Auliffe

ii
ACKNOWLEDGEMENTS:

First and foremost I would like to thank my supervisor, Dr. Kieran O’Sullivan. Kieran
you have been the single biggest influence in my career to date. Your work ethic,
creativity, advice, and wisdom, all whilst maintaining a sense of humour and calmness,
were a massive help. I am uncertain what way my professional career would have gone if
I were not so fortunate to stumble across your path mid way through my undergraduate
degree. Ever since, you have provided me with a role model for which I continually to
strive towards. I am certain there have been times where I have broke your heart over the
past four years with outlandish ideas, sloppy typos and pestering emails, but regardless of
the day, time, or even now time zone, you have been a constant source of support and
guidance throughout this project. Although you have made a massive contribution to the
formation of this thesis, for which I will be eternally grateful, perhaps your greatest
contribution is the influence you have had in my personal development by teaching me
the value of the ability to think critically, and always seek the “why”. I hope this thesis
conveys and reflects my respect, and appreciation for all you have done. UL’s loss is
Aspetars gain for now, and I am sure that your star will continue to rise, I am just grateful
I was able to hitch a ride for a few years!!

My sincere thanks also to my co-supervisors, Dr. Karen Mc Creesh and Dr. Helen Purtill.
Karen, in the midst of your own PhD, family and professional commitments you still
managed the find the time and patience to help, guide, and advise regardless of the topic.
I really appreciate the time taken showing me the technicalities of ultrasound imaging,
which formed a major basis of this thesis. To Helen, the greatest statistician I know! I
cannot thank your enough for your infinite wisdom and constant help with the statistical
aspects of the thesis. No matter the request or idiocy of my questions you always made
the most complex of theories sound so simple and this project would never have been
completed without your substantial contribution. Your email inbox is safe finally!!!

iii
To my co-authors, Dr. Tom Comyns and Seth O’Neill your willingness to share your
extensive expertise and knowledge provided a vital contribution to this thesis. Lets hope
Seth that we can both sit down next year for a drink as Doctors of Philosophy! To Ariane
Tabuena, the biodex queen. Data collection would not have been feasible without your
help and expertise. Although you might not admit it, there is an excellent researcher in
there somewhere!

I would like to acknowledge the contribution made by all the participants who gave up
their time freely to help contribute to this thesis; your efforts are very much appreciated.

To the PG crew John, Eva, Laura, Mary, Bláthin, Dan, Sandra, Bríd and Michelle.
Although our office sometimes resembled a counseling room, your friendship, support
and general humour were a welcome distraction, and a soundboard in times of need.
To the Clinical Therapies Department, and Head of the Department Dr. Norelee
Kennedy, for providing me with the opportunity and funding to pursue my PhD, as well
as a fantastic academic environment over the past 4 years. A special word of thanks to the
technicians in the Clinical Therapies Department, Trish, Jean, and Siobhán. I have no
doubt (which I am constantly reminded of) that I broke your hearts over the past 4 years
with various and constant requests for equipment. I am grateful that no matter the request,
and often with very short notice you always came up trumps for me and always in good
humour.

I would like to thank my employers Abbey Physio, namely Annette Shanahan for your
patience and understanding in allowing me the flexibility I required in getting to this
point. To Mary Fitzgerald, the woman who runs my life. I really appreciate the lengths
that you went to arranging and rearranging my diary at various times over the last 4
years.

iv
A word of thanks to anyone that I have badgered over the past number of weeks,
especially those who kindly gave their time to proof read. Mary, Laura, and Mikey your
help was very much appreciated.

Lastly and most notably a word of thanks to my family, in particular my parents, Maxi
and Karen. I am sure there have been times over the years where you have despaired at
my life choices, but despite this you have always encouraged and supported me to pursue
my goals and personal ambitions. I would not be where I am today without you, and I
hope this doctorate is a small recognition and appreciation of the sacrifices you have both
made to allow me pursue everything I have wanted. Rest assured, the eternal student is
finally leaving college…for a while at least!! (cid:45)

v
TABLE OF CONTENTS

DECLARATION.......................................................................................................................II
ACKNOWLEDGEMENTS .....................................................................................................III
LIST OF TABLES ..................................................................................................................VIII
LIST OF FIGURES..................................................................................................................IX
LIST OF PUBLICATIONS .....................................................................................................XI
LIST OF CONFERENCE PRESENTATIONS......................................................................XII
LIST OF ABBREVIATIONS ...............................................................................................XIIII
ABSTRACT: ................................................................................................................................. 2
GENERAL INTRODUCTION: .................................................................................................. 3
CHAPTER 1: INTRODUCTION ................................................................................................ 5
TENDON ANATOMY .............................................................................................................................................................. 5
TERMINOLOGY IN ACHILLES TENDON DISORDERS .................................................................................................... 7
TENDON HEALING AND REPAIR ....................................................................................................................................... 8
EPIDEMIOLOGY OF ACHILLES TENDINOPATHY ........................................................................................................ 10
BURDEN AND IMPACT OF AT IN THE GENERAL POPULATION ............................................................................... 11
RISK FACTORS ..................................................................................................................................................................... 12
PAIN IN AT: TISSUE INJURY, TISSUE SENSITIVITY OR BOTH? ................................................................................ 25
THE ROLE OF IMAGING IN EVALUATING TENDON STRUCTURE ............................................................................. 29
THE ROLE OF STRENGTH IN EVALUATING TENDON FUNCTION ............................................................................. 35
LOADING INTERVENTIONS IN AT: A MULTIFACTORIAL RESPONSE? ................................................................... 41
KEYPOINTS FROM CHAPTER 1 ........................................................................................................................................ 44
AIMS OF THESIS ...................................................................................................................... 46
CHAPTER 2: ARE ALTERATIONS IN TENDON STRUCTURE ASSOCIATED WITH
PAIN? ........................................................................................................................................... 47
STUDY I: A SYSTEMATIC REVIEW OF THE RELIABILITY OF ULTRASOUND IMAGING IN MEASURING
TENDON SIZE: IS THE ERROR CLINICALLY ACCEPTABLE? ...................................................................................... 47
STUDY II: CAN ULTRASOUND IMAGING PREDICT THE DEVELOPMENT OF ACHILLES AND PATELLAR
TENDINOPATHY? A SYSTEMATIC REVIEW AND META-ANALYSIS ....................................................................... 87
CHAPTER 3: FUNCTIONAL DEFICITS IN AT: ARE WE ADDRESSING THE
OBSERVED DEFICITS? ......................................................................................................... 113
STUDY III: ALTERED STRENGTH PROFILE IN ACHILLES TENDINOPATHY: A SYSTEMATIC REVIEW AND
META-ANALYSIS. ............................................................................................................................................................. 113
CHAPTER 4: LOADING INTERVENTIONS IN AT: MORE THAN JUST
STRUCTURAL CHANGE? .................................................................................................... 162
STUDY IV: CLINICAL IMPROVEMENTS FOLLOWING A LOADING INTERVENTION IN ACHILLES
TENDINOPATHY ARE ASSOCIATED WITH A RANGE OF FACTORS: AN UNCONTROLLED PILOT
INTERVENTION STUDY. .................................................................................................................................................. 162
STUDY V: BEYOND THE TENDON: PATIENT EXPERIENCES OF ACHILLES TENDINOPATHY, A
QUALITATIVE STUDY ...................................................................................................................................................... 189

vi
CHAPTER 5: DISCUSSION ................................................................................................... 206
CHANGE IN TENDON STRUCTURE IS ASSOCIATED WITH THE DEVELOPMENT OF PAIN ............................... 207
PAIN IS ASSOCIATED WITH ALTERATIONS IN TENDON FUNCTION .................................................................... 212
CLINICAL IMPROVEMENTS FOLLOWING LOADING INTERVENTIONS IN AT: A MULTIFACTORIAL
RESPONSE ........................................................................................................................................................................... 221
TOP DOWN OR BOTTOM UP: INTEGRATING STRUCTURE, FUNCTION AND PAIN IN AT ............................... 227
REFERENCES: ........................................................................................................................ 233
APPENDICES ........................................................................................................................... 296
APPENDIX 1: SUMMARY OF SELECTED THEORETICAL MODELS IN TENDINOPATHY ............................... 297
APPENDIX 2: CASP CRITERIA ................................................................................................................................. 302
APPENDIX 3: CERT CHECKLIST ............................................................................................................................. 305
APPENDIX 4: DESCRIPTION OF OUTCOME MEASURES FROM PILOT INTERVENTION STUDY.................. 307
APPENDIX 5: PARTICIPANT CONSENT FORM....................................................................................................... 315
APPENDIX 6: PARTICIPANT INFORMATION SHEET ............................................................................................ 316
APPENDIX 7: PILOT INTERVENTION STUDY PRE ASSESSMENT ..................................................................... 318
APPENDIX 8: PILOT INTERVENTION PROGRAMME ............................................................................................ 330
APPENDIX 9: QUALITATIVE STUDY INTERVIEW GUIDE .................................................................................. 342
APPENDIX 10: QAREL CHECKLIST ....................................................................................................................... 346

vii
TABLES

TABLE 1: QUALITY APPRAISAL FOR RELIABILITY STUDIES (QAREL) RESULTS ............................ 56
TABLE 2: DESCRIPTION OF INCLUDED STUDIES .............................................................................. 59
TABLE 3: RELIABILITY STATISTICS AND RESULTS OF THE INCLUDED STUDIES. ............................... 69
TABLE 4: KEYWORDS AND SEARCH STRATEGY .............................................................................. 89
TABLE 5: CHARACTERISTICS OF INCLUDED STUDIES ...................................................................... 95
TABLE 6: CRITICAL APPRAISAL OF INCLUDED STUDIES USING THE CASP CHECKLIST .................... 99
TABLE 7: STUDY III SEARCH STRATEGY ...................................................................................... 116
TABLE 8: STUDY III CHARACTERISTICS AND RESULTS OF INCLUDED STUDIES ............................. 121
TABLE 9: STUDY III QUALITY ASSESSMENT OF INCLUDED STUDIES ............................................. 141
TABLE 10: STUDY III EFFECT SIZES ON STUDIES NOT INCLUDED IN THE META-ANALYSIS ............ 150
TABLE 11: STUDY IV SUBJECTIVE WELLNESS AND PSYCHOSOCIAL OUTCOME MEASURES ........... 167
TABLE 12: STUDY IV DEMOGRAPHICS OF INCLUDED PARTICIPANTS ............................................ 175
TABLE 13: STUDY IV MEAN AND MEDIAN PRE AND POST INTERVENTION RESULTS ...................... 178
TABLE 14: CORRELATIONS OF CHANGE FOLLOWING THE INTERVENTION PERIOD ......................... 182
TABLE 15: EXERCISE DOSE OF THE INCLUDED PARTICIPANTS....................................................... 183
TABLE 16: FREQUENCY OF STATEMENTS AND INTERVIEWS FOR CODES AND CATEGORIES ........... 199
TABLE 17: STUDY V CHARACTERISTICS OF THE STUDY PARTICIPANTS ........................................ 200
TABLE 18: STUDY V IDENTIFIED THEMES .................................................................................... 200

viii
FIGURES

FIGURE 1: TENDON ULTRASTRUCTURE ............................................................................................ 6
FIGURE 2: COOK AND PURDAM CONTINUUM MODEL .................................................................... 17
FIGURE 3: ABATE’S ICEBERG THEORY ........................................................................................... 17
FIGURE 4: ARNOCZKY MECHANOBIOLOGICAL AETIOPATHOGENESIS .............................................. 17
FIGURE 5: FU’S FAILED HEALING RESPONSE ................................................................................. 17
FIGURE 6: THEORETICAL PARADIGMS ASSOCIATED WITH TENDINOPATHY MODELS ....................... 21
FIGURE 7: MULTIFACTORIAL ASPECTS IN AT ................................................................................. 24
FIGURE 8: GREY SCALE ULTRASOUND SCANNER ............................................................................ 30
FIGURE 9: NORMAL TENDON USING ULTRASOUND IMAGING .......................................................... 31
FIGURE 10: DIFFUSE TENDON THICKENING USING ULTRASOUND IMAGING ..................................... 32
FIGURE 11: ILLUSTRATION OF THE STRETCH SHORTENING CYCLE .................................................. 36
FIGURE 12: ILLUSTRATION OF THE FORCE VELOCITY CURVE .......................................................... 38
FIGURE 13: STUDY I LITERATURE SEARCH STRATEGY ................................................................... 51
FIGURE 14: STUDY I FLOW DIAGRAM ............................................................................................ 54
FIGURE 15: STUDY III FLOWCHART ............................................................................................... 93
FIGURE 16: RISK RATIO FOR PREDICTIVE VALUE OF ULTRASOUND IMAGING ................................ 104
FIGURE 17: STUDY II FUNNEL PLOT ANALYSIS OF STUDY AND PUBLICATION BIAS ....................... 105
FIGURE 18: STUDY III FLOWCHART ............................................................................................. 119
FIGURE 19: STUDY III EFFECT SIZE FOR CONCENTRIC PF PT SLOW ............................................. 143
FIGURE 20: STUDY III EFFECT SIZE FOR CONCENTRIC PF PT FAST ............................................... 144
FIGURE 21: STUDY III EFFECT SIZE FOR ECCENTRIC PF PT SLOW ................................................ 144
FIGURE 22: STUDY III FUNNEL PLOT CONCENTRIC PF PT SLOW ................................................. 145
FIGURE 23: STUDY III FUNNEL PLOT CONCENTRIC PF PT FAST .................................................. 145
FIGURE 24: STUDY III FUNNEL PLOT ECCENTRIC PF PT SLOW ................................................... 146
FIGURE 25: STUDY III EFFECT SIZE FOR TENDON STRAIN ............................................................. 148
FIGURE 26: STUDY III EFFECT SIZE FOR TENDON STIFFNESS ........................................................ 148
FIGURE 27: STUDY IV 12-WEEK LOADING INTERVENTION .......................................................... 173
FIGURE 28: GRAPHICAL ILLUSTRATION FOR CODES AND CATEGORIES EXPRESSED IN THE
INTERVIEWS ......................................................................................................................... 199
FIGURE 29: SUMMARY OF PREDICTIVE ABILITY OF ULTRASOUND IMAGING .................................. 208
FIGURE 30: COMPLEX SYSTEMS THEORY OF AT ........................................................................... 211
FIGURE 31: ASSESSMENT TECHNIQUES IN AT .............................................................................. 215
FIGURE 34: RELATIONSHIP BETWEEN STRUCTURE, FUNCTION AND PAIN IN AT ............................ 221
FIGURE 35: LANGUAGE THAT HARMS IN AT ................................................................................ 226
FIGURE 36: LANGUAGE THAT HELPS IN AT .................................................................................. 226
FIGURE 37: MATURE ORGANISM MODEL OF AT .......................................................................... 228

ix
I would like to gratefully acknowledge the images (1,2,3,4,5,11,29 and 36) used in this thesis
contributed by the following authors: Professor Jill Cook, Dr Bruma Fu, Professor Roberto
Paganelli, Professor Forsgren, Dr. Natalia F.N. Bittencourt, Dr. Caroline Nicol, Dr. Steven P.
Arnoczky, Philippa Tindle,

PUBLICATIONS

(cid:120) Mc Auliffe, S., Mc Creesh. K, Purtill.H, O’Sullivan, K., (2016) “Can ultrasound
technology predict the development of Achilles and patellar tendinopathy? a
systematic review of the literature.” British Journal of Sports Medicine (E pub
ahead of print) doi: 10.1136/bjsports-2016-096288 Impact Factor 6.724
(cid:120) Mc Auliffe, S, Culloty, F., Mc Creesh, K., Purtill, H., O’Sullivan, K., (2016) “A
systematic review of the reliability of diagnostic ultrasound imaging in measuring tendon
size: is the error clinically acceptable?” Physical therapy in Sport. (E pub ahead of
print). DOI: http://dx.doi.org/10.1016/j.ptsp.2016.12.002
(cid:120) Mc Auliffe, S., Casey, H., Mc Creesh, K., Synnott, A., O’Sullivan, K. (2017) “Beyond
the tendon: Patient experiences of Achilles tendinopathy: a qualitative study”.
Musculoskeletal Science & Practice, 29 pp108 – 114.

Planned publications
(cid:120) Mc Auliffe, S., Tabuena, A., Mc Creesh, K., Purtill, H., O’Keeffe, M., Comyns, T.,

Hurley, J., O’Neill, S,O’Sullivan, K. (2016)“Strength and power deficits in Achilles
tendinopathy? a systematic review of the literature with clinical implications.” (Under
review at BJSM)
(cid:120) Mc Auliffe, S., Tabuena, A., Mc Creesh, K., Purtill, H., O’Sullivan, K. (2016) “Clinical
improvements following a loading intervention in Achilles tendinopathy are associated
with a range of factors: an uncontrolled pilot study.” (Under review at Physical Therapy)

x