Supraspinatus Musculotendinous Architecture: a Cadaveric and in Vivo Ultrasound Investigation of the Normal and Pathological Muscle
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SUPRASPINATUS MUSCULOTENDINOUS ARCHITECTURE: A CADAVERIC AND IN VIVO ULTRASOUND INVESTIGATION OF THE NORMAL AND PATHOLOGICAL MUSCLE by Soo Young Kim A thesis submitted in conformity with the requirements for the degree of Doctor of Philosophy Graduate Department of Rehabilitation Science University of Toronto © Copyright by Soo Young Kim 2009 Supraspinatus musculotendinous architecture: a cadaveric and in vivo ultrasound investigation of the normal and pathological muscle Soo Young Kim Doctor of Philosophy, Graduate Department of Rehabilitation Science Faculty of Medicine, University of Toronto, 2009 Abstract The purpose of the study was to investigate the static and dynamic architecture of supraspinatus throughout its volume in the normal and pathological state. The architecture was first investigated in cadaveric specimens free of any tendon pathology. Using a serial dissection and digitization method tailored for supraspinatus, the musculotendinous architecture was modeled in situ. The 3D model reconstructed in Autodesk MayaTM allowed for visualization and quantification of the fiber bundle architecture i.e. fiber bundle length (FBL), pennation angle (PA), muscle volume (MV) and tendon dimensions. Based on attachment sites and architectural parameters, the supraspinatus was found to have two architecturally distinct regions, anterior and posterior, each with three subdivisions. The findings from the cadaveric investigation served as a map and platform for the development of an ultrasound (US) protocol that allowed for the dynamic fiber bundle architecture to be quantified in vivo in normal subjects and subjects with a full-thickness supraspinatus tendon tear. The architecture was studied in the relaxed state and in three contracted states (60º abduction with either neutral rotation, 80º external rotation, or 80º internal rotation). The dynamic changes in the architecture within the distinct regions of the muscle were not uniform and varied as a function of joint position. Mean FBL in the anterior region shortened significantly with contraction (p<0.05) but not in the posterior. In the anterior region, mean PA was significantly smaller in the middle part compared to the deep (p<0.05). Comparison of the normal and pathological muscle found large differences in the percentage change of FBL and PA with contraction. The architectural parameter that showed the largest changes with tendon pathology was PA. In sum, the results showed that the static and dynamic fiber bundle architecture of supraspinatus is heterogeneous throughout the muscle volume and may influence tendon stresses. The architectural data collected in this study and the 3D muscle model can be used to develop future contractile models. The US protocol may serve as an assessment tool to predict the functional outcome of rehabilitative exercises and surgery. ii Acknowledgements I would first like to give great thanks to my supervisor, mentor, and friend, Dr. Anne Agur, for providing a wonderful opportunity to learn and grow. I am so grateful for the positive and rich learning environment that Dr. Agur has provided. I’d also like to extend a sincere thanks to my committee members Drs Erin Boynton, Robert Bleakney, Tim Rindlisbacher, and Denyse Richardson for their expertise and advice. In particular, thank you Dr. Boynton for your enthusiasm and passion, Dr. Bleakney for your dedication and all the hours of scanning, Dr. Rindlishbacher and Richardson for your encouragement and referrals for the study. To my mother and father, I thank you for all your years of hard work to provide your two daughters with the best. Your love and support have allowed me to be who I am and be where I am today. To my sister Hyon and brother-in-law Peter, I truly could not have done it without your help, encouragement, humor, and prayers. Thank you so very much for bearing some of my burdens with me in the past four years. Most importantly, I give my loving husband, Jae Young, my deepest thanks. Without you, I would have never discovered my passion for teaching, and without your immense sacrifice this dream of becoming a professor could not have come true. Thank you for your love, patience, gentleness, and support. Also, to my precious Noah—you are a true gift from God. To my father-in-law and mother-in-law in Korea, thank you for your constant support from afar. Acknowledgement is made to the Canadian Orthopaedic Foundation, the Division of Anatomy, Faculty of Medicine, University of Toronto for financial support. iii Table of Contents Page Abstract ii Acknowledgements iii Table of Contents iv List of Figures x List of Tables xii List of Abbreviations xvi Chapter 1: Introduction 1 1.1 Contents of thesis 2 Chapter 2: Literature Survey 4 2.1 Structure of human skeletal muscle 5 2.1.1 Organization of contractile and connective tissue elements 5 2.1.2 Contractile mechanism 7 2.2 Muscle architecture 9 2.2.1 Overview 9 2.2.2 Architectural parameters and importance to function 11 2.2.2.1 Muscle 11 2.2.2.2 Tendon 15 2.2.3 Methods used to study muscle architecture 16 2.2.3.1 Cadaveric dissection 16 2.2.3.2 Ultrasound 17 2.2.3.3 Magnetic resonance imaging 18 iv 2.3 Muscle architecture of normal supraspinatus 19 2.3.1 Morphology of supraspinatus 19 2.3.2 Cadaveric investigation of normal supraspinatus 21 2.3.2.1 Overview 21 2.3.2.2 Comparison of methodologies 24 2.3.2.2.1 Fiber bundle length 24 2.3.2.2.2 Pennation angle 25 2.3.2.2.3 Muscle volume 25 2.3.2.2.4. Muscle length 26 2.3.2.2.5 Physiological cross sectional area 26 2.3.2.2.6 Tendon dimensions 26 2.3.2.3 Comparison of results 31 2.3.2.3.1 Fiber bundle length 31 2.3.2.3.2 Pennation angle 31 2.3.2.3.3 Muscle volume 32 2.3.2.3.4 Muscle length 32 2.3.2.3.5 Physiological cross sectional area 32 2.3.2.3.6 Tendon dimensions 32 2.3.3 Ultrasound investigation of normal supraspinatus 35 2.3.3.1 Overview 35 2.3.3.2 Comparison of methodologies 36 2.3.3.3 Comparison of results 37 2.3.4 Magnetic resonance imaging of normal supraspinatus 38 2.4 Muscle architecture of pathological supraspinatus 39 2.4.1 Overview 39 2.4.2 Cadaveric investigation of pathological supraspinatus 40 2.4.3 Imaging investigation of pathological supraspinatus 42 2.5 Modeling of skeletal muscles 43 2.5.1 Overview 43 2.5.2 Type of models 44 2.5.2.1 Phenomenological models 44 2.5.2.2 Structural models 45 v 2.5.2.3 Use of architectural parameters in muscle 45 models 2.5.3 Models of shoulder region: sources of architectural data 46 2.5.4 Use of digitized data for muscle modeling 47 2.6 Role of supraspinatus in abduction and glenohumeral stabilization 47 2.7 Summary 51 Chapter 3: Hypotheses and Objectives 52 3.1 Hypotheses 52 3.2 Objectives 53 3.3 Significance 54 Chapter 4: Methods 55 4.1 Cadaveric investigation of normal supraspinatus 55 4.1.1 Specimens 55 4.1.2 Dissection and digitization 55 4.1.3 MicroscribeTM G2 Digitizer 56 4.1.4 Modeling 57 4.1.5 Data analysis 58 4.2 Ultrasound investigation of normal supraspinatus 59 4.2.1 Subjects 59 4.2.2 Equipment 60 4.2.3 Positioning and screening of subjects 60 4.2.4 Protocol 60 4.2.4.1 Protocol development 62 4.2.4.2 Development of acromion correction factor 63 4.2.4.2.1 Dissection and digitization 63 4.2.4.3 Ultrasound investigation 64 4.2.5 Measurement of architectural parameters from US scans 65 4.2.6 Data analysis 68 vi 4.3 Ultrasound investigation of pathological supraspinatus 69 4.3.1 Subjects 69 4.3.2 Protocol 69 4.3.3 Measurement of architectural parameters from 70 US scans 4.3.4. Data analysis 70 4.4 Reliability and validity of measurements 71 4.4.1 Intra-rater reliability 71 4.4.2 Inter-rater reliability 71 4.4.3 Validity 72 Chapter 5: Results 73 5.1 Introduction 73 5.2 Cadaveric investigation of normal supraspinatus 73 5.2.1 Tendon architecture 73 5.2.2 Muscle architecture 74 5.2.2.1 Anterior region 75 5.2.2.2 Posterior region 76 5.2.2.3 Fiber bundle length 79 5.2.2.4 Pennation angle 79 5.3 Ultrasound investigation of normal supraspinatus 81 5.3.1 Pre-scanning 81 5.3.2 Intramuscular tendon 82 5.3.3 Muscle architecture 83 5.3.3.1 Muscle thickness 83 5.3.3.2 Anterior region 84 5.3.3.3 Posterior region 85 5.4 Ultrasound investigation of pathological supraspinatus 89 5.4.1 Pre-scanning 89 5.4.2 Intramuscular tendon 90 5.4.3 Muscle architecture 91 vii 5.4.3.1 Muscle thickness 92 5.4.3.2 Anterior region 93 5.4.3.3 Posterior region 96 5.5 Comparison of pathological and normal data 98 5.5.1 Pre-scanning 98 5.5.2 Intramuscular tendon 99 5.5.3 Muscle architecture 100 5.5.3.1 Muscle thickness 100 5.5.3.2 Anterior region 101 5.5.3.3 Posterior region 104 5.6 Reliability and validity of measurements 104 5.6.1 Intra-rater reliability 104 5.6.2 Inter-rater reliability 105 5.6.3 Validity 105 5.7 Summary of main results 106 Chapter 6: Discussion 109 6.1 Cadaveric investigation of normal supraspinatus 109 6.1.1 Three-dimensional modeling 109 6.1.2 Measurement of architectural parameters 110 6.1.3 Comparison of architectural parameters 111 6.1.3.1 Fiber bundle length 111 6.1.3.2 Pennation angle 112 6.1.3.3 Muscle volume 113 6.1.3.4 Tendon architecture 113 6.2 Ultrasound investigation of normal supraspinatus 114 6.2.1 Measurement of architectural parameters 116 6.2.2 Muscle architecture 117 viii 6.3 Functional implications of cadaveric and in vivo findings 118 of normal subjects 6.4 Ultrasound investigation of pathological supraspinatus 123 6.5 Functional implications of in vivo findings of pathological 125 subjects 6.6 Clinical implications 126 6.7 Summary 128 Chapter 7: Conclusions 130 Chapter 8: Future Directions 133 References 135 Appendix A: Sample size calculation 145 Appendix B: Ethics approval 146 ix List of Figures Chapter 2: Page Figure 2.1 Organization of skeletal muscle.