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. 6
Figure 2.2 Muscle architecture: Various arrangements of muscle 10 fibers.
Figure 2.3 Effect of pennation angle. 14
Figure 2.4 Rotator cuff muscles. 20
Chapter 4:
Figure 4.1 Cadaveric investigation: Digitization and dissection of 56 supraspinatus.
Figure 4.2 Cadaveric investigation: MicroscribeTM G2 Digitizer. 57
Figure 4.3 Cadaveric investigation: 3D computer model of 58 supraspinatus.
Figure 4.4 Cadaveric investigation: FBL and PA measurement. 59
Figure 4.5 Ultrasound investigation of normal supraspinatus: 61 Architecturally distinct regions of supraspinatus used to develop US protocol.
Figure 4.6 Ultrasound investigation of normal supraspinatus: 65 Subject arm position for US scanning.
x
Figure 4.7 Ultrasound investigation of normal supraspinatus: 67 Measurement of FBL and PA on US scans.
Figure 4.8 Ultrasound investigation of normal supraspinatus: 68 Measurement of MT and distance of intramuscular tendon to superficial surface of muscle belly (TD).
Figure 4.9 Ultrasound investigation of pathological supraspinatus: 69 US scan of pathological left rotator cuff.
Chapter 5:
Figure 5.1 Cadaveric investigation of normal supraspinatus: 78 Dissection and 3D modeling of the architecturally distinct regions of left shoulder supraspinatus, superior views.
Figure 5.2 Cadaveric investigation of normal supraspinatus: 79 Superior view of left scapula.
Figure 5.3 Ultrasound investigation: US scans of anterior region 87 of right supraspinatus in relaxed and contracted states.
Figure 5.4 Ultrasound investigation: Comparison of US scans of 92 pathological and contra-lateral supraspinatus of same subject.
Figure 5.5 Ultrasound investigation: Comparison of US scans of 99 normal and pathological supraspinatus.
xi List of Tables
Chapter 2: Page
Table 2.1 Summary of fiber types found in skeletal muscles. 8
Table 2.2 Summary of the types of architectural data obtained from 23 cadaveric studies of supraspinatus muscle.
Table 2.3 Comparison of the methodologies used by Jensen et al. (1995), 28-30 Juul-Kristensen et al. (2000), Roh et al. (2000), and Ward et al. (2007).
Table 2.4 Summary of architectural data obtained from cadaveric 34 studies of supraspinatus muscle.
Table 2.5 Summary of architectural data obtained from cadaveric 35 studies of supraspinatus tendon.
Table 2.6 Summary of architectural data obtained from in vivo US 38 studies of normal supraspinatus muscle.
Table 2.7 Summary of findings by Itoi et al. (1995): Architectural 42 data collected through cadaveric investigation of pathological supraspinatus.
Chapter 5:
Table 5.1 Cadaveric investigation of normal supraspinatus: Summary 74 of mean tendon dimensions.
Table 5.2 Cadaveric investigation of normal supraspinatus: Summary 80 of mean architectural parameters for anterior and posterior regions
xii Table 5.3 Cadaveric investigation of normal supraspinatus: Summary 81 of mean architectural parameters for superficial, middle, and deep parts of the anterior and posterior regions of supraspinatus muscle.
Table 5.4 Ultrasound investigation of normal supraspinatus: Mean TD 83
Table 5.5 Ultrasound investigation of normal supraspinatus: Mean MT 84
Table 5.6 Ultrasound investigation of normal supraspinatus: 88 Architectural parameters of the anterior and posterior regions.
Table 5.7 Ultrasound investigation of normal supraspinatus: 89 Architectural parameters of the middle and deep parts of the anterior region.
Table 5.8 Ultrasound investigation of pathological supraspinatus: 90 Summary of tendon pathology on the contra-lateral shoulder.
Table 5.9 Ultrasound investigation of pathological supraspinatus: 91 Comparison of mean TD between pathological and contra-lateral supraspinatus.
Table 5.10 Ultrasound investigation of pathological supraspinatus: 93 Comparison of mean MT between the pathological and contra-lateral supraspinatus
Table 5.11 Ultrasound investigation of pathological supraspinatus: 95 Comparison of mean FLB and percentage change of anterior region between pathological supraspinatus and contra-lateral supraspinatus.
xiii Table 5.12 Ultrasound investigation of pathological supraspinatus: 95 Comparison of mean PA and percentage change between pathological and contra-lateral supraspinatus.
Table 5.13 Ultrasound investigation of pathological supraspinatus: 96 FBL and PA of anterior region for relaxed and contracted states and percentage change for each individual subject.
Table 5.14 Ultrasound investigation of pathological supraspinatus: 97 Comparison of mean FBL of posterior region between pathological and contra-lateral supraspinatus.
Table 5.15 Ultrasound investigation of pathological supraspinatus: 98 Mean FBL for each individual subject.
Table 5.16 Ultrasound investigation: Comparison of mean TD 100 between normal controls and pathological supraspinatus.
Table 5.17 Ultrasound investigation: Comparison of mean MT 101 between normal controls and pathological supraspinatus.
Table 5.18 Ultrasound investigation: Comparison of mean FBL 103 and percentage change of anterior region between normal controls and pathological supraspinatus.
Table 5.19 Ultrasound investigation: Comparison of mean PA 103 and percentage change of anterior region between normal controls and pathological supraspinatus.
Table 5.20 Ultrasound investigation: Comparison of mean 104 FBL of posterior region between normal controls and pathological supraspinatus.
xiv Table 5.21 Summary of mean FBL measurements made on 106 one male fresh cadaveric specimen: US scans and digitized data.
xv List of abbreviations
A actin
Acf acromial correction factor
Acr acromion
AD anterior region deep part
ADP adenosine diphosphate
AM anterior region middle part
AP anterior posterior
AS anterior region superficial part
ATP adenosine triphosphate
CSA cross-sectional area
ER external rotation
F force
F female
FBL fiber bundle length
IR internal rotation
Lat lateral
Lf normalized fiber bundle length
xvi M male
M myosin
Med medial
ML medial lateral
ML muscle length
MRI magnetic resonance imaging
MT muscle thickness
MV muscle volume
PA pennation angle
PD posterior region deep part
Pi inorganic phosphate
PM posterior region middle part
PS posterior region superficial part
PSCA physiological cross-sectional area
SC subcutaneous tissue
SF supraspinous fossa
SK skin
Sup superficial
TD distance of intramuscular tendon to the superficial surface of the muscle
xvii TP trapezius
US ultrasound
V volume
Þ muscle density
ΔL change in length of the myofibril
бl change in length of sarcomere
2D two-dimensional
3D three-dimensional
Units cm centimeters deg degrees
MHz megahertz mm millimeters
xviii Glossary of Terms
*Definition from Stedman’s Medical Dictionary (2000) aponeurosis, pl. aponeuroses*: A flat fibrous sheet of connective tissue that serves to attach muscle to bone or other tissues. endomysium*: A thin sheet of connective tissue consisting principally of reticular fibers that invests each striated muscle fiber and binds the fibers together within a fasciculus. epimysium*: Outermost sheath of connective tissue that surrounds a skeletal muscle. fascia, pl. fasciae*: A fibrous membrane covering, supporting and separating muscles. fascicle (fiber bundle)*: A small bundle of muscle fibers muscle fiber (myofiber)*: A single skeletal muscle cell myofibril*: Component of a skeletal muscle fiber; comprising of many regularly overlapped thick and thin filaments. myofiliament*: The ultramicroscopic threads of filamentous proteins (actin and myosin) making up the myofibrils in striated muscle. perimysium*: The fibrous sheath enveloping each of the fascicles of skeletal muscle fibers. sarcomere*: The segment of the myofibril between two adjacent Z lines, representing the functional unit of striated muscle. skeletal muscle*: A muscle consisting of elongated, multinucleated, transversely striated skeletal muscle fibers together with connective tissues, blood vessels, and nerves.
xix tendon*: A fibrous cord or band of variable length that is the part of the muscle that connects the fleshy (contractile) part of muscle with its bony attachment or other structure; it consists of fascicles of very densely arranged, almost parallel collagenous fibers, rows of elongated fibrocytes, and a minimum of ground substance.
xx Chapter 1: Introduction
Skeletal muscles are responsible for force generation and movement of the body
(Ross, 2006). Muscle architecture is the primary determinant of muscle function and is defined as the arrangement of fiber bundles relative to the line of force (Lieber and Friden,
2001). A detailed understanding of muscle architecture provides insight into the functional role(s) of a muscle (Lieber, 1993). Studying the fiber architecture i.e. fiber bundle length, pennation angle, and muscle thickness, of both normal and pathological muscles can aid in optimizing the outcome of rehabilitative exercises and surgery.
The supraspinatus was chosen for this architectural study because among the shoulder muscles it is most often involved in shoulder pathology (Howell, 1986; Codman 1990,
Harryman, 1991). Rotator cuff tendon impingement, tendinosis, and tears often start in the supraspinatus, and as the pathology worsens it involves the other rotator cuff muscles
(Matsen, 2004).
Understanding the fiber architecture of supraspinatus in normal and pathological states is also needed to better understand the association of the musculotendinous architecture and tendon pathology. Traditionally, the etiology of tendon pathology has been explained by changes in the tendon properties and compression and abrasion by the undersurface of the acromion (Lindblom, 1939; Rothman & Parke, 1976, Matsen et al.,
2004; Bigliani et al., 1990). However, the muscle architecture and changes associated
1 with activity, inactivity, injury, or pain episode may be important factors in the development of tendon tears. Changes in the muscle belly, which have commonly been thought to be compensatory in nature to tendon pathology, may in fact play an important role in the development of tendon tears.
In this thesis, the static and dynamic architecture of supraspinatus throughout its volume has been investigated and quantified using advanced computer modeling techniques and real-time ultrasound. The architectural data was collected from both the normal and pathological supraspinatus in vivo which allowed for novel analysis and comparison.
1.1 Contents of thesis
The present thesis is comprised of eight chapters that are presented in the following
order:
• Chapter 1 introduces the study of skeletal muscle architecture and discusses
the relevance and rationale for this study.
• Chapter 2 is the literature survey that provides background information on the
structure of skeletal muscle, the importance of studying muscle architecture,
methods used to study muscle architecture including cadaveric and in vivo
imaging studies, and muscle modeling. This chapter also discusses previous
2 studies that investigated the musculotendinous architecture of supraspinatus
and outlines their limitations.
• Chapter 3 outlines the hypotheses, objectives, and significance of the thesis.
• Chapter 4 presents the methods used to address the hypotheses and objectives
of this thesis. The first section outlines the methods used in the cadaveric
study. The following sections summarize the methods used to develop and
carry out an ultrasound protocol on subjects with a normal or pathological
supraspinatus muscle.
• Chapter 5 summarizes the results of this thesis. The first section summarizes
the findings from the cadaveric investigation and muscle modeling. In the
following section, the findings from in vivo US investigation are summarized.
In the last section, the architectural data of normal controls and pathological
subjects are compared and contrasted.
• Chapter 6 is a discussion of the results with the functional and clinical
implications.
• Chapters 7 and 8 include the conclusions of this thesis and outline the future
directions for this study.
3 Chapter 2: Literature Survey
The aim of the literature survey is to provide the necessary background information for this architectural study of the human supraspinatus muscle. The chapter is divided into the following sections:
• Section 2.1 discusses the structure of skeletal muscle.
• Section 2.2 provides an overview of muscle architecture and the importance to
function.
• Section 2.3 discusses previous cadaveric, ultrasound, and magnetic imaging
studies of the normal supraspinatus and compares methods and results where
possible.
• Section 2.4 provides a summary of the pathological supraspinatus and previous
cadaveric and imaging investigations.
• Sections 2.5 discusses modeling of skeletal muscles.
• Section 2.6 discusses the role of supraspinatus in abduction and glenohumeral
stabilization as documented in the literature.
• Section 2.7 summarizes the literature survey.
4 2.1 Structure of human skeletal muscle
Skeletal muscles are the “building blocks” of the muscular system (Ganong, 2005). As a muscle contracts, it “delivers work to its outside world by exerting force while changing length” (Huijing, 1998). Skeletal muscles are specifically tailored for force generation at both the mirco- and macroscopic levels (Gans & Gaunt, 1991).
2.1.1 Organization of contractile and connective tissue elements
Architecturally, skeletal muscle is comprised of bundles of muscle fibers called fascicles. Each fascicle is in turn composed of hundreds or even thousands of individual muscle fibers or muscle “cells”. The muscle fiber consists of longitudinally arranged strands called myofibrils which are the fundamental contractile elements within skeletal muscle. Myofibrils are composed of two types of myofilaments: (1) thick filaments composed of the protein myosin and (2) thin filaments composed of the protein actin
(Ross, 2006). The interdigitation of the two types of myofilaments creates a transverse banding pattern of alternating light and dark striations which are visible by light microscopy (Ganong, 2005). Each reiteration of the light-dark-light transverse banding pattern is termed a sarcomere. The sarcomere is the functional contractile unit within a skeletal muscle (Nordin, 2001).
The thick myofilaments are found in the central region of the sarcomere where their volume and density give rise to the dark bands, also known as A bands for their
5 anisotropic appearance on microscopy. The thin myofilaments are found on either side of the central dark band of thick myofilaments. The reduced volume and density of the thin myofilaments manifests as the light bands or I bands for their isotropic appearance.
The thin myofilaments of adjacent sarcomeres are attached to each other and form a boundary structure termed the Z line. Thus, the sarcomere extends from one Z line to the next and contains one iteration of the light-dark-light banding pattern. The thin actin myofilaments of each sarcomere extend from the Z line where they are bound to the thin myofilaments of the adjacent sarcomere, to the central dark band region of the sarcomere where they are unattached and interdigitate with the thick myosin myofilaments. Figure
2.1 illustrates the organization of skeletal muscles.
Figure 2.1 Organization of skeletal muscle.
Skeletal muscles have three connective tissue coverings: the epimysium, the perimysium, and the endomysium (Figure 2.1). The epimysium is the dense connective
6 tissue the surrounds the muscle. The major blood vessels and nerves that supply the muscle will penetrate the epimysium. The perimysium is the connective tissue that surrounds bundles of fibers or fascicles within the muscle. Finally, the endomysium is the delicate connective tissue that covers individual fiber bundles (Ross, 2006).
2.1.2 Contractile mechanism
The contractile mechanism in skeletal muscles depends on the interaction of the myofilaments during a process known as the cross-bridge cycle (Webb and Trentham,
1981). In its simplest form, during the cross-bridge cycle, actin (A) combines with myosin (M) and adenosine triphosphate (ATP) to produce force, adenosine diphosphate
(ADP) and inorganic phosphate (Pi). This can be represented as a chemical reaction:
A + M + ATP A + M + ADP + Pi + Force
Since the muscle fiber is the smallest complete contractile unit, it requires a subsystem for metabolism. During metabolism, nutrients are brought into the cell and oxidized to release energy. The most common examples of this are glycolysis and fatty acid breakdown (Ross, 2006).
There are variations in the metabolism, myosin ATPase activity, and contractile properties of the different fibers that make up muscles (Ganong, 2005). Based on these
7 variations, skeletal muscle can be characterized into three main fiber types: Type I, Type
IIB, and Type IIA (rare in humans). For the most part, human muscles have a mixture of all three fiber types, but the proportions of these fiber types will vary with the functional role of the muscle (Ross, 2006). Muscles that contain a majority of type I fibers respond slowly, have a long latency, and are suited for long, slow, posture- maintaining contractions. Muscles that contain many Type IIB fibers have a short twitch duration and are adapted for fine, skilled movement. The properties of the three main types of fibers found in skeletal muscles are summarized in Table 2.1.
Type I Type IIB Type IIA
Other names Slow oxidative; Fast glycolytic; Fast oxidative; red white red Myosin isoenyzme ATPase Slow Fast Fast activity
Diameter Moderate Large Large
Glycolytic capacity Moderate High High
Oxidative capacity* High Low High
Table 2.1 Summary of fiber types found in skeletal muscles. *correlates with content of mitochondria, capillary density, myoglobin content. Adapted from Ganong, 2005.
8 2.2 Muscle architecture
2.2.1 Overview
While much research has been focused on elucidating the cellular and metabolic properties of muscle (Eisenberg 1983; Goldman 1987; McCray et al., 1980), less attention has been given to the study of the macroscopic properties of human muscle (Lieber &
Frieden, 2001).
The function of skeletal muscles is dependant on its musculotendinous architecture,
“the arrangement of contractile and connective tissue elements within a muscle” (Lieber and Fridén, 2001). Although muscles of different sizes may have a relatively consistent fiber diameter, the arrangements of these fibers and the dimensions of the corresponding tendon can differ significantly (Lieber, 1993).
The contractile elements, the muscle fibers, can be oriented in many ways, but most skeletal muscles associated with the limbs are either parallel or pennate in arrangement
(Kawakami et al., 1993; Narici, 1999). Pennate muscles can be unipennate, bipennate, and multipennate (Hamill, 2009). In muscles with parallel arrangement, the fibers run parallel to the line of force. The line of force is defined as the line to which forces of contracting fiber bundles will be projected (Lieber, 1993). In pennate muscles, the fibers run obliquely to the line of force (Kawakami et al., 1998). The obliquity of the muscle fibers to the line of action is the pennation angle. Figure 2.2 illustrates various
9 arrangements of muscle fibers found in skeletal muscles.
Figure 2.2 Muscle architecture: Various arrangements of muscle fibers
The connective tissue elements in skeletal muscles not only include the epimysium, the perimysium, and the endomysium, but also include tendons and aponeuroses. The primary function of the tendon and aponeurosis are to transmit force from the muscle to the skeleton and to store elastic energy (Enoka, 2002). Tendons are flexible cordlike structures that attach muscle to bone and consist of parallel bundles of collagen fibers
10 interposed with tendinocytes (fibroblasts). The tendon often becomes flattened when it extends into the muscle as an aponeurosis. Aponeuroses are multilayered where the collagen fibers in each layer are arranged at a 90º angle to those in apposing layers (Ross,
2006).
The shape, number, and dimensions of tendons and aponeuroses can also vary significantly (Hamill, 2009). For example, in pennate muscles, tendons are often long and aponeuroses can extend intramuscularly, whereas in parallel fiber muscles, these connective tissue elements tend to be extra-muscular (Griffiths et al., 1991).
2.2.2 Architectural parameters and importance to function
2.2.2.1 Muscle
Specific architectural parameters of the muscle include fiber bundle length (FBL), pennation angle (PA), and muscle volume (MV). Fiber bundle length is defined as the distance between the attachment sites of a fiber bundle, and if often measured with linearly with a ruler or caliper (Keating et al.,1993; Juul-Kristensen et al., 2000a).
However, since fiber bundles are often curved, FBL measurement may not be accurate.
Thus, using a method that can account for FBL curvature is important. Pennation angle is defined as the acute angle that a muscle fiber bundle creates with the line of force
(Murray et al., 2000). Specifically, the line of force is the line that intersects the centroids
11 of cross-sections through the muscle volume (Jensen & Davy, 1975). Since this line of force cannot be visualized on a specimen, previous studies have resorted to measuring the surface PA (Lieber et al., 1990; Roh et al., 2000). Surface PA is the angle between the fiber bundle and its attachment sites to bone, tendon, or aponeurosis, which is often not to the line of force. Finally, MV is generally measured by liquid displacement techniques
(Roh et al., 2000) or 3D reconstructions of MRI images (Holzbaur et al., 2007). Muscle volume has also been calculating by dividing muscle mass with a previously published muscle density data (Mendez and Keys, 1960; Ward and Lieber, 2005). However, muscle density has been found to vary with the method and duration of fixation (Ward and Lieber, 2005).
Variations in skeletal muscle architectural properties indicate that muscles are constructed for different functions. That is, the architectural properties allow for muscles to be specialized in force production or excursion.
Functionally, muscle velocity and excursion are proportional to the number of sacromeres in series i.e. FBL (Powell et al., 1984; Bodine et al, 1982; Gans & Gaunt,
1991, Fukunaga et al., 1997). Since FBL reflects the number of sarcomeres in series in the fibers, muscle fiber length can be used to determine the shortening velocity of muscle fibers and the range of lengths over which a muscle can produce active force (Lieber, 1993).
When a muscle contracts, each sacromere shortens proportionately (Enoka, 2002), which
12 in turn results in shortening of the myofibril. This change in length can be described as
ΔL=n(δl)
(ΔL is the change in length of the myofibril, n is the number of sacromeres in series, and
δl is the change in length of a sarcomere). To further illustrate this relationship of muscle fiber length and excursion, consider two hypothetical muscles that only differ in fiber lengths. The muscle with longer muscle fibers has a greater number of sarcomeres in series, thus on contraction it has a greater absolute change in active length and will undergo greater excursion and have a greater shortening velocity.
Muscle force is proportional to the total CSA of sarcomeres. In muscles with parallel fiber arrangement, the force generated is related to the number of myofibrils arranged in parallel. This relationship can be defined as
Fmyofibril= nf
(F is force, n is the number of myofibrils arranged in parallel, and f is the average force exerted by one myofibril). Thus, increasing the number of myofibrils arranged in parallel would increase the muscle force. However, most skeletal muscles in human are pennated which means that each fiber is oriented at an angle to the line of force (Gans and
Bock, 1965). The force transmitted from the muscle fiber to the tendon has been shown to be influenced by the PA of the myofibrils (Roy and Edgerton 1992; Lieber 1993). This relationship can be defined as (Narici, 1999):
13 Ftendon= Fmyofibril cos θ
(Ftendon is the force acting on the tendon, Fmyofibril is the force acting along the fibers, and
θ is PA). Therefore, when muscle fibers are oriented at an angle relative to the line of force, only a portion of their force is transmitted to the tendon. See the schematic illustration of the effect pennation in Figure 2.3.
(θ=0º) (θ=30º) Force=x Force' = cosθ x
θ Force= x Force’=xcosθ =0.87x
Figure 2.3 Effect of pennation angle. Muscle fibers oriented parallel to the axis of force generation transmit all of their force to the tendon. However, muscle fibers oriented at a 30º angle relative to the line of force transmit only a portion of their force (cos θ) to the tendon. Adapted from Lieber and Fridén, 2001.
Using architectural parameters such as FBL, PA, and MV, physiological cross-sectional area (PCSA) can be calculated. Physiological cross-sectional area “represents the sum of the cross-sectional areas of all the muscle fibers within a muscle” and is linearly proportional to the contractile force of a muscle (Lieber et al., 1990). A muscle’s peak isometric force can be calculated by multiplying the PCSA and the maximum stress constant (Lemay & Crago, 1996). Thus, when maximum stress is assumed to be
14 constant between two muscles, PCSA can be used to compare the relative force generating capabilities between different muscles. The formula for physiological cross- sectional area is as follows:
V ∗ cos(PA) PCSA = FBL
(V is the muscle volume).
Physiological cross-sectional area is problematic since the equation assumes that muscle fiber PA is constant during muscle contraction. However, experiments using different techniques have shown that this is not the case. For example, using a photographic technique, Zuurbier and Huijing (1993) examined the PA of the unipennate muscle in rats during isometric contractions at different muscle lengths. They found that when the muscle was relaxed, PA was approximately 30º but when the muscle was contracted the PA increased to about 60º. Through in vivo US investigation of human skeletal muscles, PA has also been found to vary considerably with muscle contraction and when muscle length changed (Chow et al., 2000; Fukunaga et al., 1997; Kawakami et al., 1998).
2.2.2.2 Tendon
In addition to architectural parameters of the muscle, the properties of the tendon are also important to quantify. The width, length, thickness and cross-sectional area (CSA)
15 of tendons provide insight into how the force-generating capabilities of a muscle may be modulated. For example, longer tendons have a greater capacity to store elastic energy
(Hamill, 2009). The properties of the tendon and aponeuroses can also provide insight into the presence of muscular partitions. That is, the distinct regions of skeletal muscles have been defined based on the attachment to distinctive parts of the tendons and aponeuroses (Wickham and Brown, 1998; Segal et al., 1991).
2.2.3 Methods used to study musculotendinous architecture
Musculotendinous architecture has been investigated using cadaveric dissection and various imaging techniques including ultrasound (US) and magnetic resonance imaging
(MRI).
2.2.3.1 Cadaveric dissection
Using cadaveric tissue to study muscle and tendon architecture is advantageous because structural features of the entire muscle and tendon can be observed directly
(Oxorn et al., 1998). However, the majority of previous studies have focused on the gross morphology of the muscle (i.e. volume and muscle lengths). Although MV and muscle length (ML) influence the contractile properties of muscles, accurate predictions of muscle function cannot be obtained from these parameters alone (Lieber et al., 1990).
Previous cadaveric studies that measured FBL and PA are limited because one average value for FBL is usually assigned to the entire muscle despite distinctive divisions within
16 the muscle (Aluisio et al., 2003; Juul-Kristensen et al., 2000b; Jensen et al., 1995; Keating et al., 1993; Bassett et al., 1990). In addition, the number of fiber bundles and location of fiber bundle sampling were not specified. Fiber bundle length was usually measured directly from specimens using a ruler or calipers and PA using a protractor or goniometer.
However, in recent studies, architectural parameters have been quantified algebraically from 3D computer models created from digitized cadaveric data obtain with the muscle in situ (Agur et al., 2003). By digitizing hundreds of fiber bundles throughout the entire volume of the muscle, a comprehensive model can be created through 3D reconstruction and architectural parameters quantified. Using digitized data, FBL curvature is accounted since FBL is quantified by summating the distances between digitized points.
2.2.3.2 Ultrasound
Real-time US enables direct visualization of skeletal muscle architecture in vivo in relaxed and contracted states. Architectural parameters such as FBL and PA associated with muscle contraction and various joint positions can be directly observed and quantified (Fukunaga et al., 1997; Chow et al., 2000). This is an invaluable feature to
US especially since “the architecture of actively contracting muscle fibers differs considerably than that which occurs when movement is passively induced” (Fukunaga et al.,1997). The hypoechoic muscle fiber bundles are dark on US scans and can be well delineated by the pale hyperechoic connective tissue between them.
17 The reliability of US measurements has been tested in numerous studies. For example,
Morse et al. (2008) measured FBL , PA, and MV from US scan of lateral gastrocnemuis on separate days and found the high intra-rater correlation for all the parameters
(FBL=0.90, MV= 0.94; PA=0.80). Kawakami et al. (1998 & 1993) found that the coefficients of variation between two to three different measurements of muscle thickness
(MT), FBL, and PA ranged between 0-2%.
Kawakami et al. (1993) validated the use of US to measure architectural parameters by carrying out the measurements on the triceps brachii of three human cadavers. The results demonstrated that architectural parameters measured from US scans differed from manual measurements from cadavers by 0-1mm for MT and by 0-1º for PA.
2.2.3.3 Magnetic resonance imaging
Magnetic resonance imaging is a validated tool for measuring MV accurately (Narici
1999; Holzbaur et al., 2007). This is achieved through the following steps: (1) contiguous axial images are performed along the muscle belly; (2) each axial image is digitized and its anatomical CSA is calculated; and (3) MV is obtained by summating the individual CSA of each image and multiplying by the sum of slice thickness.
Although MRI can been used to measure PA and MT, the technique has numerous limitations summarized by Narici (1999) who found that “the measurement of pennation angle and muscle thickness by MRI proved to be particularly time-consuming and
18 expensive since repeated scans were required to locate the optimal plane for pennation angle determination”.
2.3 Muscle architecture of normal supraspinatus
2.3.1 Morphology of supraspinatus
Supraspinatus is one of four rotator cuff muscles. The other rotator cuff muscles include the infraspinatus, teres minor, and subscapularis (Figure 2.4). These muscles form a musculotendinous cuff around the glenohumeral joint and blend with the fibrous layer of the joint capsule prior to attaching to the humerus (Moore, 2006). The belly of supraspinatus lies in supraspinous fossa of the scapula and its tendon extends laterally, deep to the acromion, to attach to the superior facet of the greater tubercle of the humerus
(Agur, 2009; Clemente, 2007).
The supraspinatus is reported to act as an abductor of the shoulder that works “in concert” with the deltoid (Moore, 2002). The muscle also works with the other rotator cuff muscles –infraspinatus, teres minor, and subscapularis– to stabilize the glenohumeral joint by forming a musculotendinous cuff. During shoulder movement, the tonic contraction of the rotator cuff muscles holds the humeral head in the shallow glenoid cavity of the scapula (Moore, 2006).
19
Figure 2.4 Rotator cuff muscles. A. Posterior view B. Anterior view.
20 2.3.2 Cadaveric investigation of normal supraspinatus
2.3.2.1 Overview
Based on descriptions found in the literature, the normal supraspinatus muscle and tendon each have anterior and posterior parts. The anterior part of the supraspinatus tendon is “tubular” in shape and lays both intra- and extramuscularly (Roh et al., 2000;
Vahlensieck et al., 1994). In contrast, the posterior part of the supraspinatus tendon is
“flat and broad” in shape and entirely extramuscular (Ward et al., 2006). The muscle belly of supraspinatus has an anterior and posterior region (Roh et al., 2000; Vahlensieck et al., 1994). The fiber bundles of the anterior region of the muscle belly originate from the anterior part of the supraspinous fossa and laterally attach to the anterior part of the supraspinatus tendon. The posterior part of the supraspinous fossa and the spine of the scapula is the origin of the posterior region of the supraspinatus muscle belly. The fiber bundles of the posterior region extend laterally to attach to the posterior part of the supraspinatus tendon.
To date, few studies have quantified the architectural parameters of normal cadaveric supraspinatus. Table 2.2 lists the previous cadaveric studies and the architectural parameters that were examined. Limitations are as follows:
• architectural parameters have mostly been quantified for the muscle as a whole
rather than for anterior and posterior regions
21 • the site of fiber bundle sampling was not stated in some studies and in others fiber
bundles were sampled only from the superficial surface of the muscle
• a variable number of parameters (1-4) are quantified in each study
• often the gender and age of the specimens were not reported making comparison
between studies difficult
22 Author (year) n (sex) Age Part of muscle FBL PA MV ML PCSA
Wood et al. (1989) 1 — X — — * * — (1M)
Keating et al. (1993) 5 — X * — * — *
Vahlensieck et al. (1994) 49 (52-97) X — — — * —
Jensen et al. (1995) 1 — Superficial * * * * — Deep Itoi et al. (1995) 11 — X * — — — —
Juul-Kristensen et al. 9 78.9 X * * * — * (2000b) (F) (55-87) Roh et al. (2000) 25 82 Anterior * * * — * (10M/15F) Posterior Volk and Vangsness 20 (48-76) X — — — * — (2001) (10M/10F)
Ward et al. (2006) 10 Anterior * * — * * Posterior TABLE 2.2 Summary of the types of architectural data obtained from cadaveric studies of supraspinatus muscle. Mean fiber bundle length (FBL), pennation angle (PA), muscle volume (MV), muscle length (ML), physiological cross-sectional area (PCSA). Male (M), female (F), data not collected —, data reported *, not specified X
23 2.3.2.2 Comparison of methodologies
In the following section, architectural parameters investigated in previous cadaveric studies will be discussed and where possible methodologies will be compared. A comparison of the
methodologies used in four studies that investigated the most number of parameters is
provided in Table 2.3.
2.3.2.2.1 Fiber bundle length
In previous studies, the number of fiber bundles sampled was small relative to the total
volume of the muscle. For example, Juul-Kristensen et al. (2000b) sampled three fiber bundles for the entire muscle and Ward et al. (2006) fifteen fiber bundles. In the other studies, the number of fiber bundles sampled was not stated (Jensen et al., 1995; Keating et al., 1993; Itoi et al., 1995; Roh et al., 2000). Keating et al. (1993) and Juul-Kristensen et al.
(2000b) measured FBL in situ, whereas Roh et al., (2000) and Ward et al. (2006) measured
FBL on excised fiber bundles. Furthermore, detail on the location of sampled fiber bundles is often lacking in the literature. For example, Keating et al. (1993) and Jensen at al. (1995) state that FBL were measured at “various locations within the muscle”. Roh et al. (2000) and Ward et al. (2006) stated the general region from which fiber bundles were sampled, but did not provide details on the depth of fiber bundle sampling (Table 2.3). In some studies,
FBL was measured between medial and lateral attachment sites using calipers whereas in
24 other studies FBL was not defined and the measurement tool not specified.
2.3.2.2.2 Pennation angle
Definitions of PA varied among the previous studies. For example, Juul-Kristensen et al.
(2000b) defined PA as the angle between the muscle fibers and the most centrally located tendon of insertion. Ward et al. (2006) defined “surface pennation angle” as the angle between the fibers and the distal tendon. Similarly, Roh et al. (2000) defined the PA as the angle between the axis of the tendinous portion and its inserting muscle fibers. In contrast,
Jensen et al. (1995) defined PA as the angle between the fiber orientation and the line connecting the greater tubercle of the humerus and the medial margin of the scapula in the supraspinatus fossa. Similar to FBL measurements, the number of PA measurements made was small relative to the total volume of the muscle. A goniometer was used by Roh et al.
(2000) and Ward et al. (2006) whereas Juul-Kristensen et al. (2000b) and Jensen et al. (1995) did not state the instrument used to measure PA.
2.3.2.2.3 Muscle volume
Volume of the entire muscle was measured by Wood et al. (1989), Keating et al. (1993),
Jensen et al. (1995), and Juul-Kristensen et al. (2000). In addition to measuring the volume
for the entire muscle, Roh et al. (2000) also separated the anterior and posterior regions to
measure MV for each region. Fluid displacement was used in most of these studies;
25 Jensen et al. (1995) did not report the method.
2.3.2.2.4 Muscle length
Ward et al. (2006) was the only study that provided a definition for ML. It was defined as
“the distance from the origin of the most proximal fiber to the insertion of the most distal fiber”. In the other studies, it was not possible to determine whether ML was the length of the muscle belly or a combination of belly and tendon length.
2.3.2.2.5 Physiological cross-sectional area (PCSA)
Physiological cross-sectional area has been calculated in various ways. For example, Juul-
Kristensen et al. (2000b) used FBL and MV to calculate PCSA. Roh et al. (2000) and
Ward et al. (2006) also included PA whereas Ward et al. (2006) was the only study that normalized FBL with sarcomere length. Keating et al. (1993) did not report the formula used to calculate PCSA.
2.3.2.2.6 Tendon dimensions
Roh et al. (2000), Volk and Vangsness (2001), and Itoi et al. (1995) measured tendon dimensions after removing the muscle and tendon from the specimen. Roh et al. (2000) measured the width and thickness of the anterior and posterior parts of the tendon, Volk and
Vangsness (2001) the lengths, and Itoi et al. (1995) the length of the intramuscular tendon and the width of the extramuscular tendon. Tendon thickness was also measured by Itoi et
26 al. (1995), but the location of measurement was not clearly stated. Dugas et al. (2002), however, measured the tendon dimensions by outlining the attachment of the periphery of the tendon on the humeral head in situ, then measured the dimensions on the marked outline on the humerus after removal of the muscle and tendon.
27
Jensen et al. (1995) Juul-Kristensen et al. (2000b) Roh et al. (2000) Ward et al. (2006)
FBL ·Number of FB measurements: ·Number of FB measurements: ·Number of FB measurements: ·Number of FB measurements: not specified three “Multiple representative FBs” fifteen
·Location of measurements: · Location of measurements: in ·Location of measurements: on ·Location of measurements: on “various locations” situ and “measured on both excised fibers from anterior excised fibers from anterior sides of the most centrally and posterior region of the and posterior region of muscle located muscle tendon and muscle from the superficial fascia of the muscle to the deep fascia”
·Instrumentation: not reported ·Instrumentation: not reported · Instrumentation: calipers ·Instrumentation: digital calipers
ML ·Not defined ·Not measured ·Not measured ·Defined as: “the distance from the origin of the most proximal fiber to the insertion of the most distal fiber”
Table 2.3 Continued on next page
28
Jensen et al. (1995) Juul-Kristensen et al. (2000b) Roh et al. (2000) Ward et al. (2006)
MV ·Method not reported ·Fluid displacement (cm³) ·Fluid displacement (mL) ·Not measured PA · Number of measurements: ·Number of measurements: ·Number of measurements: ·Number of measurements: not specified not specified “Multiple measurements” fifteen
· Location of measurements: · Location of measurements: ·Location of measurements: · Location of measurements: superficial and deep part of “on both sides of the most anterior and posterior regions anterior and posterior regions muscle centrally located muscle of the muscle of the muscle tendon and from the superficial fascia of the muscle to the deep fascia”
· Defined as: “the angle ·Not defined ·Defined as: “the angle ·Defined as: “the angle between the fiber orientation between the axis of each between the fibers the distal and the line connecting the tendinous portion and its tendon” greater tubercle of the inserting muscle fibers” humerus and the medial margin of the suprascapular fossa”
·Instrumentation: not reported · Instrumentation: not reported ·Instrumentation: goniometer · Instrumentation: goniometer
Table 2.3 Continued on next page
29
Jensen et al. (1995) Juul-Kristensen et al. (2000b) Roh et al. (2000) Ward et al. (2006)
PCSA ·Not measured ·Calculated for the entire muscle ·Calculated for the anterior and ·Calculated for the entire muscle posterior muscle belly separately
M(g)g cosθ PCSA(mm) = 2 V 3 PCSA(mm ) = cosθ ρ(g / m )gLf (mm) ·Equation used was not stated. L
where θ is the muscle PA (in where Þ =muscle density (1.112cm²), degrees), V is muscle volume (in θ is the muscle pennation angle (in mL) and L is average muscle degrees), Lf is normalized fiber fiber length (in mm) bundle length
Table 2.3 Comparison of the methodologies used by Jensen et al. (1995), Juul-Kristensen et al. (2000b), Roh et al. (2000), and Ward et al. (2006). Fiber bundle= FB, Fiber bundle length=FBL, muscle volume=MV, muscle length=ML, pennation angle= PA, physiological cross-sectional area= PCSA.
30 2.3.2.3 Comparison of results
The architectural parameters that have been quantified in previous studies are summarized
in Table 2.4. The parameters include FBL, PA, MV, ML, and PCSA. It should be noted
that there was variability in the parameters quantified in each study. Tendon dimension data,
width, length and thickness, are summarized in Table 2.5. Comparison of parameters
between studies was difficult because of differences in methodology and treatment of data.
2.3.2.3.1 Fiber bundle length
Mean FBL for the entire muscle was found to be 5.6 cm by Keating et al. (1993) and 6.5
cm by Jensen et al. (1995). When Itoi et al. (1995) normalized their data to scapular length
and Ward et al. (2006) to sarcomere the mean FBL was less than the mean reported by
Keating et al. (1993) and Jensen et al. (1995). Mean FBL for the anterior and posterior
regions of the muscle belly, which was reported only by Roh et al. (2000), was found to be
8.3±0.09 cm and 6.5±1.2 cm respectively.
2.3.2.3.2 Pennation angle
Mean PA for reported for the entire muscle was found to be 11.4º±7.8 º by Juul-Kristensen et al. (2000b) but 5.1º±0.8º by Ward et al. (2006). Roh et al. (2000) found mean PA for the anterior region of the muscle belly to be 14º±3º and 10º±3º for the posterior region. Jensen et al. (1995) reported the range of PA for the superficial and deep part of the muscle be lly.
31 For the superficial part, PA ranged from 20º-25º degrees and 10º-12º for the deep part.
2.3.2.3.3 Muscle volume
Mean MV for the entire muscle belly ranged from 23 cm³ to 39.3 cm³ (Wood et al., 1989;
Keating et al., 1993; Jensen et al., 1995; Itoi et al., 1995; Juul-Kristensen et al., 2000b; Ward et al., 2006). Roh et al. (2000) found the anterior region of the muscle belly to have a volume of 12 cm³ and the posterior region to have a volume of 4 cm³.
2.3.2.3.4 Muscle length
Mean ML for the entire muscle ranged from 8.6 cm to 14.5 cm. It is difficult to comment on the findings since most studies did not define ML.
2.3.2.3.5 Physiological cross-sectional area
Physiological cross-sectional area for the entire muscle was found to be 66±2.6 mm2 by
Juul-Kristensen et al. (2000b) and 66.5 ±5.6 mm2 by Ward et al. (2006). Roh et al. (2000)
found the PCSA for the anterior and posterior regions to be 140±44 mm2 and 62 ±25 mm2
respectively.
2.3.2.3.6 Tendon dimensions
The mean length of the anterior part of the supraspinatus tendon was greater than the
posterior part. Itoi et al. (1995) and Volk and Vangsness (2001) found the mean length of
the anterior tendon to be 4.08±1.03 cm and 5.4 cm respectively, whereas the mean length of
32 the posterior part was found to be 2.8 cm by Volk and Vangsness (2001). Roh et al. (2000)
found the thickness of the anterior tendon (0.31±0.07 cm) to be slightly greater than the posterior (0.25±0.07 cm). The tendon thickness reported by Itoi et al. (1995) was 0.22±0.04 cm, but it is not clear what part of the tendon was measured.
The mean width of the entire supraspinatus tendon (both the anterior and posterior parts)
was reported to be 1.53±0.03 cm by Itoi et al. (1995). Roh et al. (2000) found the mean
width of the anterior tendon (0.84±0.21 cm) was smaller than the posterior tendon (1.28±0.28
cm). The width and length of the tendon insertion on the humerus was found to be
1.63±0.55 cm and 1.27±0.63 cm respectively by Dugas et al. (2002).
33
Author (year) n Part of FBL (cm) PA(deg) MV (cm³) ML (cm) PCSA (mm2) muscle Wood et al. (1989) 1 X — — 39.3 8.6 — Keating et al. (1993) 5 X 5.6 (4.7-6.5) — 23 (15-31) — Vahlensieck et al. 49 anterior — — — 10.6 — (1994) posterior 8.9 Jensen et al. (1995) 1 superficial 6.5 (6.0-7.5) (20-25) 36 11 — deep (10-12) Itoi et al. (1995) 11 X 2.8 ± 0.5 — — — (normalized data) Juul-Kristensen et al. 9 X 4.7 ± 1.1 11.4 ± 7.8 29.7 ± 11.6 — 66±2.6 (2000b) Roh et al. (2000) 25 anterior 8.3 ± 0.9 14 ± 3 12 ± 4 — 140±44 (4.5-11.7) (8-20) (7-25) 62 ±25 posterior 6.5 ± 1.2 10 ± 3 4 ± 2 (3.5-10.1) (2-20) (1-8) Volk and Vangsness 20 X — — — 14.5 — (2001) (12.2-16.8) Ward et al. (2006) 10 X 4.50 ± 0.32 5.1 ± 0.8 — 8.5 ± 0.4 66.5 ±5.6 (normalized data ) TABLE 2.4 Summary of architectural data obtained from cadaveric studies of supraspinatus muscle. Mean fiber bundle length (FBL), pennation angle (PA), muscle volume (MV), muscle length (ML), physiological cross-sectional area (PCSA), ± standard deviation (range), —data not collected, not specified X
34
Author (year) n Part of tendon Length Width Thickness (cm) (cm) (cm) Itoi et al. (1995) 11 intramuscular 4.08±1.03 — —
extramuscular — 1.53±0.03 0.22±0.0.4*
Roh et al. (2000) 25 anterior — 0.84 ± 0.21 0.31 ± 0.07 (0.49-1.34) (0.2-0.42) posterior — 1.28 ± 0.28 0.25 ± 0.07 (0.66-1.57) (0.2-0.43)
Volk and 20 anterior 5.4 — — Vangsness (2001) (4.1-7.7) posterior 2.8 — — (2-3.7)
Dugas et al. 20 area of insertion 1.3 ±0.6 1.6 ± 0.6 — (2002) (0.7-1.5) (1.0-2.1)
TABLE 2.5 Summary of architectural data obtained from cadaveric studies of supraspinatus tendon. Mean tendon length, width, thickness, ± standard deviation (range) when reported. —data not collected. *location of tendon thickness measurement was not clearly stated.
2.3.3 Ultrasound investigation of normal supraspinatus
2.3.3.1 Overview
To date, in vivo US has only been used to investigate gross morphological features of
supraspinatus such as CSA and MT (Juul-Kristensen et al., 2000a; Dupont et al., 2001;
35 Katayose & Magee, 2001). Furthermore, these parameters have only been measured with
the muscle in the relaxed state. Quantitative measurements of architectural parameters such
as FBL and PA of supraspinatus have not been previously investigated with US.
2.3.3.2 Comparison of methodologies
Juul-Kristensen et al. (2000a) and Dupont et al. (2001) investigated the thickness of
supraspinatus using US. The aim of both studies was to determine how measurements taken
by US compared with measurements taken by MRI. It is important to note that the
positioning of patients was different between the two studies. Juul-Kristensen et al. (2000a) measured MT with subjects seated with their arm hanging along the side of the body. In contrast, Dupont et al. (2001) had the subjects positioned in prone with the arms held straight alongside the torso resting on the table.
The location along the muscle belly and position of the US probe differed between the two
studies. Juul-Kristensen et al. (2000a) measured MT at the midpoint of the muscle length with the US probe parallel to the muscle line of force. Dupont et al. (2001), however,
measured MT at various locations along the muscle length with the US probe held
perpendicular to the skin surface with the imaging plane transverse to the muscle line of force.
Both studies used a 5 MHz US transducer.
Juul-Kristensen et al. (2000a) measured the CSA of supraspinatus at the middle and medial
36 fourth of the muscle length with subjects seated in the same position that was used to
investigate MT. The 5 MHz US probe was held transverse to the muscle line of force. In
the study by Katayose & Magee (2001), subjects were also seated with the shoulder in the
neutral position. The CSA was measured at the midpoint of spine of the scapula with the
imaging plane transverse to the line of force. A 7.5 MHz transducer was used and the probe
was angled between 30º and 40 º.
2.3.3.3 Comparison of results
Only three quantitative US studies of supraspinatus were found in the literature. Muscle
thickness was reported in one study and CSA in two (Table 2.6). Juul-Kristensen et al.
(2000a) found the mean MT to be 2.0 cm and the mean CSA of supraspinatus, measured at the middle of the muscle length to be 5.6 cm². The mean CSA for subjects within a similar age range (between 30-39 years of age) was found to be 7.3 cm² by Katayose & Magee
(2001).
37
Author (year) n (sex) Age (range) MT (cm) CSA (cm2)
Juul-Kristensen et al. (2000a) 8 (F) 39.8 2.0 5.6 (27-54)
Dupont et al. (2001) 6 (24-51) NR — (3M/3F)
Katayose & Magee (2001) 72 (M) (30-39) — 7.3
TABLE 2.6 Summary of architectural data obtained from in vivo US studies of normal supraspinatus muscle. Mean muscle thickness (MT), cross-sectional area (CSA), male (M), female (F), data not collected —, date not reported (NR)
2.3.4 Magnetic resonance imaging of normal supraspinatus
Juul-Kristensen et al. (2000) and Dupont et al. (2001) measured MT using both US and
MRI and then compared and correlated the results of the two methodologies. The correlation coefficients in the Juul-Kristensen et al. (2000) study was 0.808 and in the Dupont et al. (2001) study, 0.96. Both Juul-Kristensen et al. (2000) and Dupont et al. (2001) concluded that US, a less expensive imaging technique, could accurately measure supraspinatus MT.
38 2.4 Muscle architecture of pathological supraspinatus
2.4.1 Overview
In individuals over 40 years of age, rotator cuff tears, most commonly involving the supraspinatus, is one of the major causes of shoulder pain and functional deficit (Winter et al.,
1997). The prevalence of tears markedly increases after 60 years of age – the incidence reaching nearly 30% (Lehman et al., 1995). In dissection studies, the incidence of full- thickness tears has been found to range between 19-48% (Itoi et al., 1995; Keyes et al., 1933).
Rotator cuff tears also account for a large percentage of work-related disorders, with a reported incidence rate of 19.9 per 10,000 full-time employees per year (Silverstein et al.
1998). Significant pain, weakness in shoulder elevation, and limited function are typical manifestations of supraspinatus tendon pathology (Bey et al. 2002).
Traditionally, structural deficits of the supraspinatus tendon have been focused on to understand the etiology of supraspinatus tendon tears. Two theories have been popular: (1) impaired perfusion to the critical zone of the supraspinatus tendon, and (2) compression and abrasion of the supraspinatus tendon from the inferior surface of the acromion. The first theory is predicated on anatomical studies that have found limited vascularity of the supraspinatus tendon at and near its bony insertion (Lindblom, 1939; Rothman & Parke,
1976). The second theory, on the other hand, attributes degeneration of the supraspinatus
39 tendon to mechanical compression. According to Neer (1972) and others (Matsen et al.,
1998; Bigliani et al., 1991), the close proximity of the humeral head to the acromion as well
as the shape of the acromion are both associated with tendon tears.
More recently, however, deficits of the neuromuscular system have been highlighted in
the etiology of supraspinatus tendon tears. Muscular imbalance, instability impingement,
muscle overuse, and fatigue are now viewed as important factors in the pathogenesis of
tendon tears (Irlenbusch & Gansen, 2003, McCully et al., 2006).
Complete tears of the rotator cuff tendons are associated with fatty degeneration (Khoury et
al., 2008). Fatty degeneration is characterized by infiltration of fat within the muscle
volume (Goutallier et al. 2003). As the muscle atrophies, spaces are left between the muscle
fibers that become filled with fat. This process is progressive and often irreversible
(Thomazeau et al., 1997). Theses changes in the muscle belly are “negative prognostic
factors for the anatomic and functional results after tendon repair” (Khoury et al., 2008).
2.4.2 Cadaveric investigation of pathological supraspinatus
Previous cadaveric studies of the pathological supraspinatus have mostly been descriptive
(Keyes et al., 1933; Petersson et al 1984) with the exception of one quantitative study by Itoi et al. (1995). In this study of forty-one embalmed cadaveric specimens, mean age of 84 years, thirty had varying degrees of tendon tears and eleven had an intact tendon. The
40 results of the normal specimens have been reported in section 2.3 of this thesis. Once a
tendon tear was identified, the maximal width and length of the tear was measured using
digital calipers. The supraspinatus was then excised from the specimen and the
extramuscular tendon length was measured at the center of the tendon on its articular side
from its lateral end to the musculotendinous junction. “Total tendon length”, was measured
from the lateral margin of the extramuscular tendon to the most medial edge of the
intramuscular tendon. “Functional tendon length” was defined as the sum of the extramuscular tendon length and the tear length. Fiber bundle length was measured at four unspecified locations on the superficial surface of the muscle. Tendon and muscle volumes were measured by water displacement. Cross-sectional area of the muscle was calculated by dividing the MV by FBL.
The mean tendon dimensions, muscle fiber lengths, and cross-sectional areas were organized into four groups: (1) intact cuff- 27%; (2) partial tears comprising partial thickness tears of the supraspinatus-29% (3) small tears comprising full-thickness tears of the supraspinatus-27%, and (4) large tears with tears of more than 2 tendons-17%. All data was normalized by dividing the raw data by the scapular length and multiplying by 100. Table
2.7 provides a summary of the findings by Itoi et al. (1995).
The mean total tendon length and width decreased as the size of the tendon tear increased.
41 Similarly, mean FBL, MV, and CSA decreased as the tendon pathology worsened. Mean
tendon thickness varied little with tendon pathology.
Partial tear (n=12) Small tear (n=11) Large tear (n=7) Tendon length (cm) Extramuscular 1.97 ± 0.45 1.58 ± 0.55 1.53 ±0.38
Total 4.50 ± 0.90 3.51 ±0.78 3.26 ±1.07
Functional 2.46 ± 0.96 3.11 ±0. 88 4.18 ± 0.91 Tendon width (cm) 1.60 ± 0.38 1.58 ± 0.51 1.41 ± 0.24
Tendon thickness (cm) 0.24 ± 0.07 0.25 ± 0.07 0.26 ± 0.06
FBL (cm) 3.10 ± 0.63 2.55 ± 0.60 2.35 ± 0.54
MV (cm3) 26.1 ± 10.4 23.7 ± 9.0 18.5 ± 19.5
Muscle CSA (cm2) 0.7 ± 0.2 0.8 ±0.2 0.9 ±0.3
Tab le 2.7 Summary of findings by Itoi et al. (1995): Architectural data collected through cadaveric investigation of pathological supraspinatus. Fiber bundle length (FBL), muscle volume (MV), cross-sectional area (CSA).
2.4.3 Imaging investigations of pathological supraspinatus
Imaging studies of the pathological supraspinatus tend to focus on two muscle qualities:
(1) muscle atrophy which is reflected by the muscle CSA, and (2) fatty infiltration which is
the replacement of muscle fibers by fat. To study muscle atrophy and fatty infiltration, MRI
42 is considered the gold standard (Thomazeau et al., 1997; Strobel et al; 2005). However, recent
studies have found US to be as reliable and valid to investigate muscle atrophy (Juul-
Kristensen et al., 2000a; Dupont et al., 2001).
Computer tomography (CT) has been used to investigate fatty infiltration (Goutallier et
al.,1994). Goutallier et al. (1994) established a CT based classification system of fatty
infiltration for the supraspinatus that has also been used with T1 weighted MRI scans
(Gladstone et al., 2007).
To date, architectural parameters such as FBL and PA of supraspinatus have not been quantified in vivo with US or MRI.
2.5 Modeling of skeletal muscles
2.5.1 Overview
Modeling of skeletal muscles started in the seventeenth century. Through the use of mathematical formulas, muscle models can create simplified images of what is happening at the muscle level (van den Bogert et al., 1998). By manipulating architectural parameters that
are used in the formula, insight into their effects on muscle properties can be gained (Huijing,
1998).
43 2.5.2 Types of models
Depending on the purpose of modeling, muscle models can be of two general types: phenomenological or structural (Jacobs & Rikkert, 1991). If the purpose of modeling is to
“describe” functional properties, then a phenomological model is developed. However, if the purpose of modeling is to “explain” functional properties, then a structural model is developed.
2.5.2.1 Phenomological models
One of the earliest phenomenological skeletal models was developed by Hill (1938).
Although the model has been modified over the years to account for shortcomings, Hill’s model is the most commonly used muscle model in simulation of human movement (Cole et al., 1996; Winters., 1990). As a phenomenological type of model, Hill’s model provides little insight into the mechanisms of muscular contraction (Cole et al., 1996). Instead, Hill wanted to model the macroscopic contractile phenomenon of whole muscles.
The classic Hill’s model is the three component configuration. The three components, are a contractile element in parallel with a passive elastic element that are both in turn connected in series with another elastic element. The contractile element corresponds to the active characteristics of the muscle fibers, and it includes the force-length and force- velocity behavior of the muscle. The series elastic element represents all elastic components
44 of the muscle-tendon unit (i.e. the tendon and cross-bridge elasticity) in series with the
contractile element. The parallel elastic elements represent the connective tissue around the
muscle fibers and fiber bundles.
2.5.2.2 Structural models
Structural models account for the biochemical reactions during muscle contraction (Otten,
1991). The Distribution Moment model developed by Zahalak (1990) is an example of a structural model that explains the force-velocity characteristics of skeletal muscle. This model incorporates the basics of the cross-bridge model that was initially proposed by
Huxley (1957).
2.5.2.3 Use of architectural parameters in muscle models
Over the years, classic muscle models such as the Hill’s Model and the Distribution
Moment model have evolved to be able to account for different muscle properties (Stensen,
1667; Hill, 1938; Woittiez et al., 1984; Williams & Goldspink et al., 1978; van der Linden et al., 1998). However, as stated by Otten (1991), “A simple rule of thumb is the following: If the model is changed to something closer to the observed structures or characteristics, and the model improves in performance, this may indicate increased insight.”
Despite the availability of new techniques like MRI, data of musculotendinous parameters for muscle modeling is still highly dependent on cadaveric studies (Veeger et al., 1991;
45 Johnson et al., 1996). Since the predictive value of muscle models will heavily depend on the parameters describing the characteristics of the system, the more accurate the architectural data, the greater the predictive value of the muscle model.
2.5.3 Models of shoulder region: source of architectural data
Musculoskeletal models of the glenohumeral joint or shoulder mechanism often rely on cadaveric specimens for architectural data. Veeger et al. (1991) states that due to the complexity of the shoulder mechanism, “assumptions have to be made for muscle characteristics in order to develop an adequate and manageable model.”
When modeling supraspinatus, the architectural data that is used is often based on a limited number of measurements (Wood et al., 1989; Bassett et al., 1983, Poppen and Walker et al., 1978). For example, Bassett et al. (1990) established fiber length of supraspinatus from “one measurement of an individual fiber lying obliquely parallel between tendon plates of origin and insertion using a micrometer.” Thus, fiber bundles throughout the muscle volume were not measured. Johnson et al. (1996) stated that “It (supraspinatus) exhibited no morphological features that justified defining more than a single fascicle.” Second, fiber bundles are often characterized as being straight and linear. In order words, the curvature of fiber bundles is not considered (van der Linden et al., 1998, van Leeuwen and Spoor, 1992).
2.5.4 Use of digitized data for muscle modeling
46 Modeling techniques developed by Agur (2003) and Ng-Thow-Hing (2001) allow for capture and 3D modeling of tendons, aponeuroses, and hundreds of fiber bundles throughout the volume of individual skeletal muscles.
Once the specimen and muscle of interest have been securely mounted and exposed, fiber bundles on the superficial surface of the muscle are identified and digitized in situ from their medial to lateral attachments. Following digitization, the fiber bundles are removed to expose the subsequent layer of fiber bundles. This process is repeated throughout the muscle volume. At each level of dissection, aponeuroses and tendon, if present, are simultaneously digitized. The digitized data is imported into MayaTM (3D computer modeling software) enhanced by plug-ins for three-dimensional visualization and quantification of architectural parameters. Architectural parameters such as FBL and PA can be easily computed, with fiber bundle curvature being accounted for and PA being measured to the line of force.
2.6 Role of supraspinatus in abduction and glenohumeral abduction
Below, studies related to elucidating the role of supraspinatus in glenohumeral abduction will be discussed first followed by an overview of studies that investigated the contribution of supraspinatus relative to the other rotator cuff muscles to joint stabilization.
47 Numerous studies have been carried out to better understand the contribution of
supraspinatus in shoulder abduction. Howell et al. (1986) investigated the torque produced
by supraspinatus within two planes of motion, forward flexion and elevation in the plane of
the scapula, in ten healthy male volunteers between the ages of 24 and 29 years. With the
use of an isokinetic dynamometer, the reduction of torque as a result of isolated paralysis of
the suprascapular and axillary nerves was measured. The study found that with paralysis of
either the suprascapular nerve or the axillary nerve, torque decreased to approximately 50% of the value for the non-paralyzed shoulder in both planes of motion. No significant differences in the mean reduction in torque was found between paralysis of the suprascapular and axillary nerves. Thus, the study concluded that the supraspinatus and deltoid muscles were equally responsible for producing torque about the shoulder joint in the two planes of motion. Sharkey et al. (1994) investigated the contribution of the deltoid, supraspinatus, infraspinatus, teres minor and subscapularis to abduction in five fresh cadaveric specimens.
In this study, the amount of force required to abduct the shoulder was computed for: 1) deltoid only, 2) deltoid and all four rotator cuff muscles, 3) deltoid and supraspinatus, and 4) deltoid and infraspinatus, teres minor, and subscapularis. When the deltoid muscle was concurrently stimulated with the supraspinatus, the average amount of force required by the deltoid reduced significantly (28%), suggesting that the supraspinatus is actively involved in
48 shoulder abduction. The study also found that the contribution of supraspinatus to abduction of the arm was greatest between 30º-60º and insignificant by 120º. McMahon et al. (1995), using a dynamic shoulder testing apparatus, evaluated the muscle forces of supraspinatus and middle deltoid during glenohumeral abduction in the scapular plane. The muscle forces were evaluated with different force ratios applied to the two muscles (i.e. equal force to each tendon; 2:3 ratio of force applied to deltoid/supraspinatus; 3:2 ratio; no force applied to the supraspinatus tendon). The study found that full glenohumeral abduction was achieved in all force ratios, suggesting that the supraspinatus and deltoid can compensate for each other when one is not fully functioning. The study also found that near the beginning of abduction (0-15º), a larger contribution of force from the supraspinatus was required, whereas near the end of the abduction greater activity of the middle deltoid was needed.
There have also been many studies that have aimed at better understanding the contribution of the supraspinatus, relative to the other rotator cuff muscles, to shoulder stabilization and kinematics. In a cadaveric study, Keating et al. (1993) calculated the PCSA of each of the four rotator cuff muscles and the percentage contribution of each muscle to the total PCSA of all four muscles. The study found that the mean percentage contribution of supraspinatus to the total PCSA to be 15%, whereas the infraspinatus contributed 23%, teres minor 10%, and subscapularis 51%. In the studies by Howell et al. (1986) and McMahon et al. (1995)
49 simulated supraspinatus paralysis was not found to affect the normal ball-and-socket kinematics of the glenohumeral joint during abduction. Howell et al. (1986) suggested that
“joint compression through the action of the remaining rotator cuff muscles was sufficient to provide a fixed fulcrum for concentric rotation of the glenohumeral joint during abduction”.
Similarly, in a cadaveric study by Wuelker et al. (1994), the function of the supraspinatus was examined using a dynamic shoulder model. The investigators found that loss of force of the supraspinatus only produced minor changes in the glenohumeral joint mechanics and concluded that the supraspinatus does not have a significant effect on the centering of the humeral head on the glenoid during elevation. However, because of large differences between specimens, the findings were not statistically significant. In an MRI study,
Werner el al. (2006) eliminated supraspinatus and infraspinatus action at the shoulder with paralysis of the suprascapular nerve but found that during active shoulder abduction superior migration of the humeral head could not be provoked.
Few studies have discussed the function of the anterior and posterior regions of the supraspinatus. Vahlensiek et al. (1993) suggested that the anterior region may act as an internal rotator, whereas the posterior region was hypothesized to act as an abductor based on fiber bundle and tendon orientation following dissection of four cadaveric specimens and
MRI scans. Based on PCSA differences for the anterior and posterior regions of
50 supraspinatus, Roh et al. (2000) suggested that the majority of the contractile force was
produced in the anterior region of the muscle.
2.7 Summary:
The supraspinatus, one of the four rotator cuff muscles, is a relatively small muscle that sits
in the supraspinatus fossa and functions with many other muscles to move the shoulder.
Clinically, the supraspinatus is important as its muscle-tendon unit is “the most vulnerable
component of the rotator cuff mechanism” (Howell et al., 1986). Understanding its fiber
architecture has significant clinical implications in the evaluation and management of patients
with shoulder pathology.
A study investigating the static and dynamic fiber bundle architecture throughout the
muscle volume in the normal and pathological supraspinatus is lacking. Fiber bundle
measurements (i.e. FBL and PA) of supraspinatus reported previously in the literature are
limited to a small number of fiber bundle measurements with fibers from only the superficial
region of the muscle belly being investigated. Dynamic investigation of the fiber bundle
architecture of supraspinatus has been limited to qualitative assessment. In vivo architectural data of FBL and PA of supraspinatus has not been collected to date.
51 Chapter 3: Hypotheses and Objectives
3.1 Hypotheses
The hypotheses for this thesis are as follows:
1. A 3D computer model of the musculotendinous architecture of the cadaveric
supraspinatus can be generated and used to quantify the musculotendinous
architecture throughout the muscle volume.
2. From the 3D model of supraspinatus, an US protocol can be developed to investigate
and quantify the in vivo musculotendinous architecture both statically and
dynamically.
3. Fiber bundle lengths, PA and MT throughout the volume of supraspinatus are variable
and can be used to identify architecturally distinct regions.
4. In vivo FBL and PA will change significantly with contraction and the percentage
change will not be uniform throughout the muscle volume.
5. In vivo changes in FBL, PA and MT in the relaxed and contracted state will differ
between the normal and pathological supraspinatus.
52 3.2 Objectives
The objectives for this thesis are as follows:
1. To model the 3D musculotendinous architecture of supraspinatus throughout its
volume in cadaveric specimens.
2. To establish an architectural database from the 3D model of supraspinatus.
3. To develop a comprehensive in vivo US protocol that takes into account the
musculotendinous architecture of the entire supraspinatus based on the findings of the
cadaveric model.
4. To investigate the static and dynamic musculotendinous architecture of supraspinatus,
in vivo, in normal subjects and in subjects with a full-thickness tear of the anterior
supraspinatus tendon.
5. To c ompare the architectural data collected from normal subjects with data from
subjects with a full-thickness tear of the supraspinatus tendon.
53 3.3 Significance
This study will provide detailed architectural data of the static and dynamic
supraspinatus throughout its entire volume. The findings will provide greater insight into
fiber bundle changes as a function of glenohumeral positioning, muscle contraction, and
rotator cuff pathology.
The 3D model will serve as an architectural map for future studies, and the data collected from cadaveric specimens and in vivo may be used to create models that can account for fiber bundle heterogeneity and dynamic changes. Clinically, in vivo US
investigation of the normal and pathological musculotendinous architecture of supraspinatus
may lead to the development of assessment tools capable of planning and predicting the
outcome of rehabilitation, surgery, and training regimens.
54 Chapter 4: Methods
4.1 Cadaveric Investigation
4.1.1 Specimens
Ten formalin embalmed human cadaveric specimens with a mean age of 61.9 ± 16 years were used for this study. Specimens with evidence of visible gross shoulder abnormality, previous surgery, or tendon pathology were excluded. Only male specimens were used in this study since all female specimens were excluded due to tendon pathology. Ethics approval was received from the University of Toronto
(protocol # 20830). See Appendix B.
4.1.2 Dissection and digitization
The supraspinatus was exposed by removing all overlying structures and the acromion.
To prevent movement, the shoulder joint was fixated ˚in of0 abduction, flexion and lateral rotation with a metal plate screwed to the humerus and scapula. Then the specimen was clamped into a securely mounted vice and three reference points (scapular spine, coracoid process, greater tubercle) were demarcated with a screw. These reference points were later used to reconstruct the specimen in 3D. Next, the periphery of the supraspinatus tendon was outlined with points using a paint pen. Each point was digitized using a MicroscribeTM G2 Digitizer to obtain its x, y, and z coordinates. The
55 supraspinatus muscle belly was then serially dissected in situ with the aid of a dissection microscope. At each layer (1.5 -2 mm in thickness), 10-60 fiber bundles were identified and traced from their medial to their lateral attachment sites. The attachment sites and
10-20 intervening points were digitized for each fiber bundle. Following digitization, fiber bundles were sequentially removed to expose the next layer. Digitization of the tendon periphery was repeated at every 3-5 layers of the muscle (Figure4.1).
Figure 4.1 Cadaveric investigation: Digitization and dissection of supraspinatus. Superficial view of supraspinatus with acromion cut. White dots demonstrating the digitized locations along a fiber bundle. Periphery and surface of tendon stippled in black dots.
4.1.3 MicroscribeTM G2 Digitizer
MircroscribeTM G2 Digitizer (Figure 4.2), which was used to digitize the fiber bundles and tendons of supraspinatus, has an accuracy of 0.24mm. For further details on this apparatus see http://www.immersion.com/digitizer/.
56 A. B. C.
Figure 4.2 Cadaveric investigation: MicroscribeTM G2 Digitizer. A: Digitizer. B: Digitizing arm digitizing object. C: Reconstruction of digitized data in 3D.
4.1.4 Modeling
Digitized data was imported into Autodesk Maya™, a 3D modeling and animation software, using plug-ins developed in our laboratory. The plug-ins facilitated the reconstruction of the digitized data of the supraspinatus muscle belly and tendon in 3D by aligning the digitized layers in each specimen using the coordinates of the reference points (screws). The reconstructed model enabled 3D visualization of the muscle belly and tendon throughout its volume (Figure 4.3). From the model, the extent and location of internal and external tendons was documented and the location and attachment sites of the fiber bundles were investigated to determine if there were any architecturally distinct regions.
57 Anterior Medial Lateral Tendon
Anterior region
Posterior region
Posterior
Figure 4.3 Cadaveric investigation: 3D computer model of supraspinatus. Superficial view.
4.1.5 Data analysis
Algorithms were derived and implemented in Python to perform computer-automated calculations of individual fiber bundle parameters. These parameters included FBL, PA,
MV and dimensions of intra- and extramuscular tendons. Fiber bundle length was calculated as the sum of the distances between each of the digitized points along the fiber bundle and the PA as the acute angle between the fiber bundle and line of force (Figure
4.4). Line of force is defined as the line that intersects the centroids of cross-sections through the muscle volume (Jensen and Davy, 1975). To measure MV, the fiber bundles were treated as 3D cylinders. The FBL was used as the height of the cylinder while the radius was calculated as half the average distance to its closest neighboring fiber bundle.
Finally, the volume of each fiber bundle was computed and their sum yielded the MV.
58 Fiber bundle length, PA for the medial and lateral ends of the fiber bundles, and volume of architecturally distinct parts of the muscle were characterized with descriptive statistics
(mean, standard deviation and range). Paired t-tests and ANOVA followed by Tukey’s post-hoc test were carried out to compare means. Statistical significance was set at p<0.05.
Figure 4.4 Cadaveric investigation: FBL and PA measurement
4.2 Ultrasound investigation of normal supraspinatus
4.2.1 Subjects
Seventeen subjects (8M/9F) were recruited for this study. The number of subjects was based on a sample size calculation (Appendix A). The mean age of the subjects was
59 36.4±12.7, with a range of 21-60 years. Subjects with a history of rotator cuff pathology or neuromuscular disease were excluded. Written informed consent was obtained from all subjects. Ethics approval for this study was granted from the University of Toronto
(#15513) and Mount Sinai Hospital Research Ethics Board (05-0235-E). The same musculoskeletal radiologist scanned all subjects. See Appendix B.
4.2.2 Equipment
An HDI 5000, Advanced Technology Laboratories (ATL) real-time US scanner with a linear (38 mm) 12 MHz transducer was used for the study. Information was processed with eFilm Merge PACS system.
4.2.3 Positioning and screening of subjects
Throughout the scanning process, subjects were seated in a chair with their back supported. To ensure there was no pathology at the shoulder, the muscles and tendons of the rotator cuff were scanned bilaterally on all subjects. Provided there was no pathology, the radiologist continued with the in vivo protocol.
4.2.4 Protocol
The US protocol was developed on completion of the cadaveric study. The protocol was based on the architecturally distinct regions of the supraspinatus muscle belly and tendon morphology defined in the cadaveric portion of this thesis. In the cadaveric study, the muscle belly was found to have two distinct regions, anterior and posterior,
60 each consisting of three parts: superficial, middle and deep (Figure 4.5). The tendon consisted two parts: an extramuscular posterior part and an intra- and extramuscular anterior part.
Figure 4.5 Ultrasound investigation of normal supraspinatus: Architecturally distinct regions of supraspinatus used to develop US protocol. Superior views. A: Superficial. B: Intermediate. C: Deep; Anterior part of supraspinatus tendon is reflected. Superficial part of anterior region (AS); middle part of anterior region (AM); deep part of anterior region (AD); posterior region (PR); anterior part of supraspinatus tendon (*); area of acromial shadowing (Acr).
61
4.2.4.1 Protocol development
To develop a protocol, a preliminary study was carried out to determine whether the musculotendinous architecture of each region of the muscle belly and the intramuscular portion of the anterior tendon could be visualized using US. Using panoramic coronal
US images, it was found that fiber bundles of the middle and deep parts of the anterior region could be imaged along with the intramuscular portion of the anterior tendon.
From the scans, FBL and PA of the fiber bundles were measured relative to their attachment sites to the supraspinous fossa and intramuscular portion of the anterior tendon. Fiber bundles of the smaller superficial part could not be consistently visualized, but the distance between the intramuscular tendon and the superficial surface of the muscle belly was measurable and documented as tendon depth (TD). The fiber bundles of the deep part of the posterior region could be visualized until they passed deep to the acromion. Thus, PA could not be measured. Another preliminary study was carried out to determine how much of the FBL is shadowed by the acromion. The superficial and middle parts of the posterior region could not be independently scanned as the fiber bundle planes were difficult to locate consistently. Using sagittal US images, the thickness of the entire muscle (MT) could be visualized and measured along the muscle belly.
62
4.2.4.2 Development of acromial correction factor
To determine the mean length of the fiber bundles of the posterior region that is shadowed by the acromion, ten formalin embalmed cadaveric specimens were used
(9M/1F). The mean age was 75.4±10.3 (53-87) years. Specimens with evidence of tendon or joint pathology were excluded.
4.2.4.2.1 Dissection and Digitization
On each specimen, the supraspinatus muscle, spine of the scapula and the acromion were exposed. Next, the shoulder was stabilized at˚ 0of abduction, flexion , and lateral rotation with a metal plate screwed to the humerus and scapula as in the cadaveric portion of the study. The muscle belly was incised along the medial border of the acromion to demarcate the extent of the acromion. Next, the acromion was excised and the muscle and tendon exposed. In order to determine the length of the fiber bundles that were obstructed by the acromion, fiber bundles lateral to the incision were serially dissected and digitized using the techniques described in section 4.1.2. Mean lengths of the digitized fiber bundle segments were computed for the superficial, middle and deep parts of the posterior region. The “acromial correction factor” will be used to refer to the mean lengths of the fiber bundles shadowed by the acromion. The acromial correction factor was added to in vivo FBL measurements of the posterior region to obtain an
63 estimate of actual FBL.
4.2.4.3 Ultrasound investigation
The US protocol developed in the preliminary study was then used to scan fiber bundles of the middle and deep parts of the anterior region and the deep part of the posterior region. All subjects were scanned bilaterally in relaxed and contracted states. For the relaxed state, the muscle was scanned with the arm resting by the subjects’ side and the palm of hand at the side of the chair. For the contracted state, the muscle was scanned with the shoulder in three different positions: 60˚ abduction; 60˚ abduction wi th 80˚ external rotation; 60˚ abduction with 80˚ internal rotation (Figure 4.6). Panoramic coronal
US images were used to capture fiber bundles and the intramuscular tendon; sagittal US images were used to assess the thickness of the muscle. All scans were saved as JPEG images for further analysis.
64
Figure 4.6 Ultrasound investigation of normal supraspinatus: Subject arm positions for US scanning. Contracted states: A: 60º abduction; B: 60º abduction with 80º external rotation; C: 60º abduction with 80º internal rotation
4.2.5 Measurement of architectural parameters from US scans
Architectural parameters were computed using software developed in our laboratory.
Fiber bundle length was computed as the distance along the fiber bundle between the attachment sites. If fiber bundle curvature was observed, the fiber bundle was segmented and the length of each segment was summated to give the total FBL. To compute FBL of the deep part of the posterior region, the acromial correction factor was added to the in
65 vivo FBL measurements (Figure 4.7B). Pennation angle was measured as the angle between the fiber bundle and its attachment to the intramuscular tendon (Figure 4.7A).
Muscle thickness was computed at the midpoint of the muscle belly between the medial border of the acromion and the most medial point of attachment of the muscle belly in the suprascapular fossa (Figure 4.8A). The position of the intramuscular tendon (TD) was computed as the distance between the superficial surface of the muscle belly and the intramuscular tendon at the medial border of the acromion (Figure 4.8B).
66
Figure 4.7 Ultrasound investigation of normal supraspinatus: Measurement of FBL and PA on US scans. Longitudinal US scans of left supraspinatus. Note: images are not uniform in scale. A: One fiber bundle from middle part of the anterior region has been demarcated by a white↔), line pennation ( angle demarcated by (a). B: One fiber bundle from posterior region has been demarcated by a white line↔ ( ). Only a portion of the acromial correction factor (acf) is shown. Fiber bundle length (FBL); pennation angle (*); skin (SK); subcutaneous tissue (SC); trapezius muscle (TP); supraspinous fossa (SF); intramuscular tendon (○ ○ ); middle part of anterior region (AM); deep part of anterior region (AD); acromial shadow (Acr).
67
Figure 4.8 Ultrasound investigation of normal supraspinatus: Measurement of MT and distance of intramuscular tendon to superficial surface of muscle belly (TD). A: Saggital US scan of right supraspinatus at the midpoint of muscle belly. Muscle thickness (MT). B: Longitudinal US scan of right supraspinatus. Distance between the intramuscular tendon and the superficial surface of the muscle belly (TD). Subcutaneous tissue (SC); trapezius muscle (TP); supraspinous fossa (SF); superficial part of anterior region (AS); middle part of anterior region (AM); intramuscular tendon (○ ○); acromial shadow (Acr).
4.2.6 Data analysis
Fiber bundle length, PA, MT and TD data was imported into SPSS. Each architectural parameter was characterized with descriptive statistics (mean, standard deviation and range) for the relaxed and each contracted states (60˚ abduction; 60˚ abduction with 80˚ external rotation; 60˚ abduct ion with 80˚ internal ro tation). Paired t-tests were used to compare means between the anterior and posterior regions, and repeated measures
ANOVA was carried out to compare means between different shoulder positions.
Statistical significance was set at p<0.05.
68 4.3 Ultrasound investigation of pathological supraspinatus
4.3.1 Subjects
Five subjects (2M/3F) with a full-thickness tear of the anterior supraspinatus tendon, as diagnosed by MRI and/or US, were investigated for this study (Figure 4.9). The mean age of the subjects was 59± 7.7 years, with a range of 50-69 years. Subjects with a history of shoulder surgery or neuromuscular disease were excluded. Written informed consent was obtained from all subjects. Ethics approval for this study was granted from the University of Toronto (#19084) and Mount Sinai Hospital Research Ethics Board (06-
0107-E).
Figure 4.9 Ultrasound investigation of pathological supraspinatus: US scan of pathological left rotator cuff. Full-thickness anterior tendon tear. Tendon (T). Dotted line showing extent of tear.
4.3.2 Protocol
The same musculoskeletal radiologist that scanned the normal subjects performed scans on the subjects with rotator cuff tears using the same US equipment (12 MHz transducer).
69 As in the study of normal supraspinatus, subjects were seated in a chair with their back supported.
First, the torn rotator cuff was scanned to document the location and dimensions of the supraspinatus tendon tear. The supraspinatus of the contra-lateral shoulder was also scanned and if any pathology was found, the location and dimensions were documented.
The US protocol as outlined in Section 4.2.4.3 was used to scan the middle and deep parts of the anterior region, the deep part of the posterior region, the thickness of the muscle and the position of the intramuscular tendon. However, the muscle was only scanned in the relaxed state and in one contracted position (60˚ abduction with neutral rotation against gravity). Panoramic coronal US images were used to capture fiber bundles of the middle and deep parts of the anterior region, deep part of the posterior region and tendon position; sagittal US images were used to assess the thickness of the muscle. All data was saved as JPEG images and transferred to a computer in the laboratory for analysis.
4.3.3 Measurement of architectural parameters from US scans
Fiber bundle length, PA, MT and TD, were computed using the same methods were used in section 4.2.3.
4.3.4 Data analysis
The FBL, PA, MT and TD data was imported into SPSS. Each architectural
70 parameter was characterized with descriptive statistics (mean, standard deviation and range) for the relaxed and contracted states. Paired t-tests were used to compare means between relaxed and contracted states. A one-way between groups ANOVA with post- hoc tests was conducted to explore the mean differences between the pathological supraspinatus, contra-lateral supraspinatus, and normal supraspinatus. Statistical significance was set at p<0.05.
4.4 Reliability and validity of measurements
4.4.1 Intra-rater reliability
To determine intra-rater reliability of measurements made on normal subject scans, fiber bundles in all regions of two normal subjects were re-measured eight weeks later by same investigator. To determine intra-rater reliability of measurements made on pathological subject scans, fiber bundles in all regions of all subjects was also re- measured eight weeks later by the same investigator.
4.4.2 Inter-rater reliability
To establish inter-rater reliability of measurements made on normal and pathological subject scans, a second blinded investigator measured FBL and PA on all US scans of two normal subjects and all five pathological subjects.
71 4.4.3 Validity
To validate the measurements of FBL, the US protocol was carried out on the shoulder of a 65 year old male cadaveric specimen. Fiber bundles from the middle and deep parts of anterior region and the visible portion from the deep part of the posterior region were scanned. Three fiber bundles from each region were measured using the methods outlined in section 4.2.3. Following this, three fiber bundles from the corresponding part of the muscle were digitized using the methods outlined in section
4.1.2. The investigator was blinded to the measurements made on US scans when fiber bundles were digitized. Mean FBL measurements computed from the US scans were then compared with the digitized data.
4.4.4 Data analysis
Reproducibility and validity of measurements of FBL and PA were tested by paired t- tests and Pearson product-moment correlations (r) were calculated.
72 Chapter 5: Results
5.1 Introduction
The results of this thesis will be presented in four sections. In the first section, the results of the cadaveric investigation and 3D modeling study will be presented. The second section will present the results from in vivo US investigation of supraspinatus in normal subjects. The following section will present the results from in vivo US investigation of supraspinatus in subjects with a full-thickness tear of the anterior supraspinatus tendon. The final section will present the results of a comparative analysis between five age matched normal subjects and the subjects with rotator cuff pathology.
5.2 Cadaveric investigation of normal supraspinatus architecture
5.2.1 Tendon architecture
The supraspinatus tendon of insertion consisted of an anterior and a posterior tendon found in all ten specimens. See Figure 5.1 for an example.
The quadrangular shaped posterior tendon was found on the lateral aspect of supraspinatus. The posterior tendon blended with the fibrous layer of the capsule of the shoulder joint and terminated by inserting onto the posterosuperior aspect of the greater tubercle of the humerus. The only muscular attachment to the posterior tendon was to its medial aspect. In three of the ten specimens, a distinct short intramuscular tendinous slip
73 (1.0 ± 0.2 cm) extended medially from the posterior tendon into the muscle belly. The average width of the posterior tendon was 1.6 ± 0.3 cm and the average length is 2.9 ± 0.6 cm. (Table 5.1)
The cord-like anterior tendon blended with the joint capsule but then attached to the anterosuperior aspect of the greater tubercle of the humerus. Laterally, the anterior tendon was extramuscular, but became intramuscular medially. The length and width of the entire anterior tendon was found to be significantly longer and narrower than the posterior tendon (p<0.05). The average width of the anterior tendon was 0.8 ± 0.2 cm; the average length 6.1 ± 0.7 cm (Table 5.1).
Part of Tendon n Length (cm) Width (cm)
Anterior 8* 6.1 ± 0.7 (5.0-6.9) 0.8 ± 0.2 (0.6-1.0)
Posterior 8* 2.9 ± 0.6 (2.3-4.0) 1.6 ± 0.3 (1.2-2.1)
TABLE 5.1 Cadaveric investigation of normal supraspinatus: Summary of mean tendon dimensions. Mean length, width, ± standard deviation (range) are reported for the anterior and posterior parts of supraspinatus tendon. * Tendon data was not collected from the first two digitized specimens.
5.2.2 Muscle architecture
The muscle belly was partitioned into two large architecturally distinct regions, anterior and posterior, each of which could be further subdivided into superficial, middle, and
74 deep parts based on attachment sites and architectural parameters (Figure 5.1). In some cases, an additional small anterior part was identified in the posterior region.
Anterior and posterior regions were found in all ten specimens. The average MV of the anterior region was 15.4 ± 5.7 cm3, while the average MV of the posterior region was 2.5
± 0.7 cm3. The large anterior region occupies approximately the anterior three quarters of the supraspinous fossa while the posterior region, located dorsally in the supraspinous fossa, is partially overlapped by the anterior region. These regions were defined by their lateral attachments: fiber bundles of the anterior region attached to the periphery and deep surface of the anterior tendon whereas fiber bundles of the posterior region attached to the medial aspect posterior tendon. In three of the youngest specimens (<50 years of age), the anterior part of the posterior region formed a distinct bipennate muscle segment which attached to the intramuscular tendinous slip of the posterior tendon.
The architecture of the subdivisions of the anterior and posterior regions (superficial, middle, and deep) is described in the next sections of this thesis.
5.2.2.1 Anterior region
The anterior region consisted of superficial (AS), middle (AM) and deep (AD) parts that were superimposed on each other. Each part is described below.
• The fiber bundles of the superficial part of AS attached medially to two sites:
(1) the anteromedial border of the supraspinous fossa and (2) the medial third
75 of the superior border of the scapular spine. The fiber bundles converged to
attach to the periphery and superficial surface of the anterior tendon laterally
(Figure 5.1 A and B).
• The AM that lies deep to the AS extended from the medial two-thirds of the
supraspinous fossa in a bipennate fashion to the periphery and deep surface of
the medial half of the anterior tendon (Figure 5.1 C and D).
• The fiber bundles of AD were parallel in arrangement and spanned between
the lateral third of the supraspinous fossa and the deep surface of the lateral
half of the anterior tendon (Figure 5.1 E and F).
5.2.2.2 Posterior region
The posterior region also consisted of three parts: superficial (PS), middle (PM) and deep
(PD). Each part is described below.
• The fiber bundles of PS were directed anterolaterally from the superficial part
of posterior wall of the supraspinous fossa (Figure 5.2) to the medial border of
the posterior tendon. A cleavage plane separated the PS from the underlying
PM (Figure 5.1G and H).
76 • The fiber bundles of PM attached medially to the posterior wall of the
supraspinous fossa (Figure 5.2), deep to PS, and laterally to the medial border
of the posterior tendon (Figure 5.1 I and J).
• The PD was located deep and anterior to the PM. Fiber bundles attached
medially to the base of the supraspinous fossa (Figure 5.2) and laterally to the
medial border of the posterior tendon (Figure 5.1 I and J).
77
Figure 5.1 Cadaveric investigation of normal supraspinatus: Dissection and 3D modeling of the architecturally distinct regions of left shoulder supraspinatus, superior views. A. and B. Superficial part of anterior region (AS) and entire posterior region (PR). C. and D. Middle part of anterior region (AM). E. and F. Deep part of anterior region (AD). The anterior part (*) of the supraspinatus tendon is reflected. G. and H. Superficial (PS), middle (PM) and deep (PD) parts of the posterior region. I. and J. Middle (PM) and deep (PD) parts of the posterior region. Anterior part of supraspinatus tendon (*); posterior part of supraspinatus tendon (X); medial aponeurosis (+).
78 FIGURE 5.2 Cadaveric investigation of normal supraspinatus: Superior view of left scapula.
5.2.2.3 Fiber bundle length
The mean FBL for the entire anterior and posterior region were very similar: mean
FBL for the anterior and posterior regions were 6.7±0.7 and 6.7±0.5 cm respectively
(Table 5.2). Within the volume of the anterior region, mean FBL of the AS (6.7± 0.5 cm),
AM (6.6± 0.6 cm), and AD (6.6± 0.6 cm) were consistent. In contrast within the posterior region, mean FBL of PM (7.0 ± 0.6 cm) was significantly longer (p<0.05) than PD (6.2 ±
0.5 cm).
5.2.2.4 Pennation angle
The mean lateral PA was greater than the mean medial PA for both the anterior and posterior regions and all their respective parts (Tabl e 5.2). The mean lateral PA of the anterior region (60.0º±12.0º) was smaller than that of the posterior region (82.2º± 4.0º),
79 whereas the mean medial PA for the anterior (11.8º± 2.7º) and posterior (12.4º± 3.6º) regions were similar.
Region of n FBL (cm) Lateral PA Medial PA MV (cm³) muscle (deg) (deg)
Entire 10 6.7±0.6 73.2±14.7 13.2 ±5.7 17.9±6.4 muscle (5.7-7.9) (41.8-85.9) (8.5-18.4) (7.6-30.4)
Anterior 10 6.7±0.7 60.0±12.0 11.8±2.7 15.4±5.7 region (5.8-7.9) (41.8-74.5) (8.5-16.6) (6.2-26.6)
Posterior 10 6.7±0.5 82.2±4.0 12.4±3.6 2.5±0.7 region (5.7-7.6) (74.7-85.9) (7.1-18.4) (1.4-3.8)
TABLE 5.2 Cadaveric investigation of normal supraspinatus: Summary of mean architectural parameters for the anterior and posterior regions. Mean fiber bundle lengths (FBL), lateral and lateral pennation angle (PA), muscle volume (MV), ± standard deviation (range) are reported for the anterior and posterior region.
In the anterior region, the mean lateral PA for the middle part was significantly less than the deep part (p<0.05); however, the superficial part was not different when compared to the middle and deep parts. The mean medial PA of the deep part was significantly greater when compared to both the superficial and middle parts (p< 0.05); there was no statistical difference between the superficial and middle parts (Table 5.3).
In the posterior region, no significant difference was found in the lateral PA among the superficial, middle, and deep parts. However, the mean medial PA of the superficial part was significantly greater than the middle and deep parts (p<0.05); no significant
80 difference was found between the middle and deep parts (Table 5.3). Mean FBL was found to be significantly longer in the middle part compared to the deep part (p<0.05)
Part of n FBL (cm) Lateral PA (deg) Medial PA (deg) muscle Anterior region: Superficial 10 6.7±0.5a (5.7-7.5) 64.6±12.7a (44.6-79.0) 11.4±2.8a (6.6-15.5)
Middle 10 6.6±0.6a (5.7-7.9) 51.4±13.1ab (34.3-70.0) 9.8±2.3a (7.58-14.5)
Deep 10 6.6±0.6a (5.4-7.4) 74.1±10.2ac (54.9-86.0) 16.8±6.1b (9.5-30.6)
Posterior region: Superficial 10 6.9±0.9d (5.2-7.9) 84.4±3.1d (78.6-88.5) 18.6±7.6d (7.9-31.9)
Middle 10 7.0±0.6de (6.2-8.1) 82.0±4.3d (74.0-86.2) 11.3±4.6e (6.7-20.7)
Deep 10 6.2±0.5df (5.4-7.2) 82.5±4.9d (75.6-88.8) 11.2±3.6e (6.6-19.7)
TABLE 5.3 Cadaveric investigation of normal supraspinatus: Summary of mean architectural parameters for superficial, middle, and deep parts of the anterior and posterior regions. Mean fiber bundle lengths (FBL), lateral and medial pennation angle (PA), ± standard deviation (range) are reported for all the architecturally distinct parts of supraspinatus. Superscript letters are used to indicate the presence or absence of statistical significance between the anterior or posterior regions. If the superscript letters in a column block differ, then the result is statistically significant. If the letter is repeated, there is no statistical significance. Note: statistical comparison was only made within each region
5.3 US investigation of normal supraspinatus
5.3.1 Pre-scanning
All recruited subjects were included in the study as no rotator cuff pathology was found
81 in either their right or left shoulders.
5.3.2 Intramuscular tendon
In sixteen of the seventeen subjects investigated, a single intramuscular tendon, a continuation of the extramuscular portion of the anterior tendon, was found extending medially from the acromion. For most of its length, the intramuscular tendon was close and parallel to the superficial surface of the muscle belly. In one subject, two coalescing intramuscular tendons were found. Well-defined fiber bundles of the middle and deep parts of the anterior region were seen in all subjects extending from the supraspinous fossa to the deep surface of the intramuscular tendon. The fiber bundles of the superficial part of the anterior region were seen as a layer superficial to the intramuscular tendon.
However, individual fiber bundles could not be seen and therefore TD (the distance between the intramuscular tendon and the superficial surface of the muscle belly) was measured. The site of measurement was at the medial aspect of the acromion. Mean TD in the relaxed state (0.35±0.07 cm) was significantly smaller than in all contracted states
(p<0.05). In 60° abduction with neutral rotation mean TD increased to 0.40±0.09 cm; in
60° abduction with 80° external rotation it increased to 0.41±0.12 cm and in 60° abduction with 80° internal rotation to 0.56±0.15 cm, see Table 5.4. Mean TD was significantly larger in 60° abduction with 80° internal rotation than in the other contracted positions (p<0.05).
82
State TD (cm)
Relaxed 0.35 ±0.07a (0.21-0.49)
Contracted*: 0° rotation 0.40 ±0.09b (0.16-0.57)
80° ER 0.41 ±0.12b (0.06-0.72)
80° IR 0.56 ±0.15c (0.22-0.84) TABLE 5.4 Ultrasound investigation of normal supraspinatus: Mean TD. Mean TD, ± standard deviation (range); *, in 60° abduction; ER, external rotation; IR, internal rotation. If the superscript letters in the column differ, then the result is statistically significant. If the letter is repeated, there is no statistical significance.
5.3.3 Muscle architecture
5.3.3.1 Muscle thickness
The thickness of supraspinatus, measured at the midpoint between the medial border of the acromion and the most medial point of attachment of the muscle belly in the suprascapular fossa, increased significantly from the relaxed state and to all contracted states (Table 5.5). Among the contracted states, mean MT in the externally rotated position was significantly larger (2.15±0.35 cm) than in the neutral (2.03± 0.32 cm) and internally rotated (2.01±0.35 cm) positions.
83
State Muscle thickness (cm)
Relaxed 1.74±0.33a (0.91-2.36)
Contracted*: 0° rotation 2.03± 0.32b (1.50-2.77)
80° ER 2.15±0.35c (1.60-2.96)
80° IR 2.01±0.35bd (1.47-2.88)
TABLE 5.5 Ultrasound investigation of normal supraspinatus: Mean MT Mean MT, ± standard deviation (range);*, in 60° abduction; ER, external rotation; IR, internal rotation. Superscript letters are used to indicate the presence or absence of statistical significance between the relaxed and contracted states. If the superscript letters differ, then the result is statistically significant. If the letter is repeated, there is no statistical significance.
5.3.3.2 Anterior region
Ultrasound scans of the relaxed and all contracted states are presented in Figure 5.3 and the architectural parameters in Table 5.6. For all contracted states i.e. 60° abduction with neutral rotation; 60° abduction with 80° external rotation; 60° abduction with 80° internal rotation, the mean FBL was significantly shorter than the mean FBL in the relaxed state
(p<0.05). The percentage of shortening of FBL between the relaxed and contracted states ranged between 9% and 21%, with the smallest percentage of difference found when the arm was held in 60° abduction with internal rotation.
When the muscle was contracted in the 80° internally rotated position, the amount of shortening was significantly less than in neutral and 80° externally rotated positions
(p<0.05). The amount of shortening between the neutral and 80° externally rotated
84 positions were similar, 4.64 ±0.64 cm and 4.87 ±0.90 cm.
Differences in mean PA were also found between the relaxed and contracted states
(Table 5.6). The mean PAs for all contracted states were significantly larger than the mean PA in the relaxed state (p<0.05). The percentage change in mean PA between the relaxed and contracted states ranged between 22% and 44%, with the smallest percentage of change found when the arm was held in 60° abduction with 80° external rotation.
The amount of change when the muscle was contracted in the externally rotated position was significantly less than in neutral and 80° internally rotated positions
(p<0.05). Furthermore, the amount of change in PA between the neutral and internally rotated positions was similar.
When comparing the middle and deep parts of the anterior region, mean FBL was similar in both relaxed and contracted states with no significant difference. In contrast, the mean PA of the deep part was significantly greater than the mean PA of the middle part (p<0.05), see Table 5.7.
5.3.3.3 Posterior region
Fiber bundles of the deep part of the posterior region could be defined in 13 of 17 subjects. The acromial correction factor, to account acromial shadowing of fiber bundles, was determined to be 3.2 cm. Therefore, 3.2 cm was added to each in vivo FBL measurement for the deep part. The lateral attachment of fiber bundles were obscured by
85 the acromion and thus PA could not be measured.
The mean FBLs of the deep part of the posterior region were similar for the relaxed and contracted states (Table 5.6). In the internally rotated position, the mean FBL was slightly longer than in the relaxed state suggesting that the muscle may be eccentrically contracting. Compared to the anterior region, the mean FBL of the posterior region was significantly longer in the relaxed state and in all contracted states (p<0.05).
86
FIGURE 5.3 Ultrasound investigation: US scans of anterior region of right supraspinatus in relaxed and contracted states. Note: images are not uniform in scale. One fiber bundle from each scan has been demarcated by a white line (↔) with the length indicated above. A and B: Relaxed state. C and D: Contracted state (60° abduction with neutral rotation). E and F: Contracted state (60° abduction with 80° external rotation). G and H: Contracted state (60° abduction with 80° internal rotation). Skin (SK); subcutaneous tissue (SC); trapezius muscle (TP); supraspinous fossa (SF); superficial part of anterior region (AS); middle part of anterior region (AM); deep part of anterior region (AD); intramuscular tendon (○ ○); pennation angle (*)
87
n=34 Mean FBL (cm) Mean PA (deg)
Relaxed Anterior region 5.89±0.71a (4.68-7.63) 12.05±3.07a (6.74-21.68)
Posterior region 6.73±0.56b (5.61-7.77) —
Contracted*: 0° rotation Anterior region 4.64±0.64c (3.17-6.12) 17.20±4.29b (8.05-26.62)
Posterior region 6.57±0.57b (5.46-7.79) —
80° ER Anterior region 4.87±0.90c (2.96-6.74) 14.73±3.88c (8.03-22.75)
Posterior region 6.60±0.51b (5.72-7.80) —
80° IR Anterior region 5.36±0.72d (3.91-7.32) 17.36±3.54b (9.67-26.62)
Posterior region 6.90±0.50b (5.86-8.06) —
TABLE 5.6 Ultrasound investigation of normal supraspinatus: Architectural parameters of the anterior and posterior regions. Mean fiber bundle length (FBL), pennation angle (PA) ± standard deviation (range). Note: FBL of posterior region includes acromial correction factor; *, in 60° abduction; ER, external rotation; IR, internal rotation. Superscript letters are used to indicate the presence or absence of statistical significance between the anterior and posterior regions and between relaxed and contracted states. If the superscript letters in a column differ, then the result is statistically significant. If the letter is repeated, there is no statistical significance.
88
n=34 Mean FBL Mean PA (cm) (deg)
Relaxed Middle part 5.94±0.82a (4.69-8.13) 10.87±3.11a (5.48-20.51)
Deep part 5.85±0.89a (3.78-7.91) 14.24±4.26b (6.78-25.33)
Contracted*: 0° rotation Middle part 4.62±0.71bc (3.11-6.00) 16.23±3.97c (8.00-24.64)
Deep part 4.68±0.72bc (3.30-6.42) 18.80±5.26f (8.15-30.57)
80° ER Middle part 4.79±1.06cd (2.73-6.99) 13.38±4.22d (5.63-23.47)
Deep part 5.04±0.87cd (2.90-6.98) 17.29±5.50bf (7.31-29.79)
80° IR Middle part 5.31±0.74d (3.91-7.34) 16.42±3.50ce (8.82-22.71)
Deep part 5.43±0.82ad (3.90-7.63) 19.23±4.73f (10.09-31.55)
TABLE 5.7 Ultrasound investigation of normal supraspinatus: Architectural parameters of the middle and deep parts of the anterior region. Mean fiber bundle length (FBL), pennation angle (PA) ± standard deviation (range); *, in 60° abduction; ER, external rotation; IR, internal rotation. Superscript letters are used to indicate the presence or absence of statistical significance between the middle and deep parts of the anterior region. If the superscript letters in a column differ, then the result is statistically significant. If the letter is repeated, there is no statistical significance.
5.4 Ultrasound investigation of pathological supraspinatus
5.4.1 Pre-scanning
Five of six recruited subjects were included in the study. One subject was excluded because a full-thickness tear of the supraspinatus tendon was not found. On the contra- lateral shoulder, a supraspinatus tendon tear with smaller dimensions was found in four
89 subjects. A summary of the tendon pathology found on the contra-lateral shoulder is provided in Table 5.8.
Subject Age Contra-lateral supraspinatus Pathology and tear (cm) (gender)
1 55 (F) • moderate tendinosis • full-thickness tear (0.9AP, 0.5 ML) 2 50 (M) • mild to moderate tendinosis • no tear 3 65 (F) • moderate tendinosis • partial thickness /bursal sided tear (1.5 AP, 0.8 ML) 4 69 (F) • moderate to severe tendinosis • partial thickness/ articular sided tear (0.8 AP, 1.6 ML) 5 57 (M) • moderate tendinosis, • full-thickness tear (1.0 AP, 1.0 ML) TABLE 5.8 Ultrasound investigation of pathological supraspinatus: Summary of tendon pathology on the contra-lateral shoulder. AP= anterior posterior, ML=medial lateral
5.4.2 Intramuscular tendon
In all five subjects, the intramuscular portion of the anterior tendon was observed.
Fiber bundles of the AM and AD could be seen bilaterally in all subjects extending from the supraspinous fossa to the deep surface of the intramuscular tendon. Similar to normal subjects, TD (the distance between the intramuscular tendon and the superficial surface of the muscle belly) was measured since individual fiber bundles of the AS could not be visualized.
In the relaxed state, the mean TD in the pathological supraspinatus (0.30±0.8 cm) was
90 smaller than in the contra-lateral supraspinatus (0.39±0.15 cm). The difference, however, was not statistically significant. In the contracted state, mean TD of the pathological
(0.44±0.15 cm) and contra-lateral supraspinatus (0.44±0.16 cm) were similar. For the pathological supraspinatus, mean TD increased significantly on contraction (p<0.05).
However, for the contra-lateral supraspinatus mean TD did not change significantly on contraction (Table 5.9).
n=5 Relaxed (cm) Contracted (cm)
Pathological 0.30±0.8a1 0.44±0.15b1 supraspinatus (0.18-0.39) (0.21-0.56)
Contra-lateral 0.39±0.15a1 0.44±0.16a1 supraspinatus (0.21-0.62) (0.22-0.66)
TABLE 5.9 Ultrasound investigation of pathological supraspinatus: Comparison of mean TD between pathological and contra-lateral supraspinatus. Mean distance between the intramuscular tendon and the superficial surface of the muscle belly (TD) ± standard deviation (range). The superscript letters are used to indicate the presence or absence of statistical significance between the relaxed and contracted state, and superscript numbers between the pathological and contra-lateral supraspinatus. If the superscript letters/numbers differ, then the result is statistically significant. If the letter/number is repeated, there is no statistical significance.
5.4.3 Muscle architecture
Fiber bundles on the contra-lateral supraspinatus were generally better defined than the pathological supraspinatus (Figure 5.4).
91 A. B.
FIGURE 5.4 Ultrasound investigation: Comparison of US scans of pathological and contra-lateral supraspinatus of same subject. A. Pathological supraspinatus (Full-thickness tendon tear) B. Contra-lateral supraspinatus
5.4.3.1 Muscle thickness:
The MT of supraspinatus, measured at the midpoint between the medial border of the acromion and the most medial point of attachment of the muscle belly in the suprascapular fossa, did not change significantly from the relaxed to the contracted state in the pathological supraspinatus. However, MT of the contralateral supraspinatus changed significantly (p<0.05) from the relaxed to contracted state. Muscle thickness in the relaxed state of the pathological and contra-lateral supraspinatus did not differ significantly. Muscle thickness in the contracted state also did not differ significantly between the pathological and contra-lateral supraspinatus. A summary of MT is reported
92 in Table 5.10.
n=5 Relaxed (cm) Contracted (cm)
Pathological 1.99±0.29a1 2.30±0.16a1 supraspinatus (1.57-2.34) (2.10-2.54)
Contra-lateral 2.07±0.44a1 2.39±0.33b1 supraspinatus (1.46-2.61) (1.98-2.71)
TABLE 5.10 Ultrasound investigation of pathological supraspinatus: Comparison of mean MT between the pathological and contra-lateral supraspinatus Mean muscle thickness (MT) ± standard deviation (range). The superscript letters are used to indicate the presence or absence of statistical significance between the relaxed and contracted state, and superscript numbers between the pathological and contra-lateral supraspinatus. If the superscript letters/numbers differ, then the result is statistically significant. If the letter/number is repeated, there is no statistical significance.
5.4.3.2 Anterior region
The architectural parameters are presented in Tables 5.11 and 5.12. For both the pathological and contra-lateral supraspinatus, the mean FBL was significantly shorter in the contracted state than in the relaxed state (p<0.05). The percentage of shortening was found to be 21.4% for the pathological supraspinatus and 27.4% for the contra-lateral supraspinatus. The difference in mean FBL between the pathological and contra-lateral supraspinatus in the relaxed and contracted state was not significant.
Mean PA was also found to significantly differ between the relaxed and contracted states. The mean PA for the contracted state was significantly larger than the mean PA in
93 the relaxed state (p<0.05) for the pathological and contra-lateral supraspinatus. The percentage change in mean PA between the relaxed and contracted states was found be
25.8% for the pathological supraspinatus and 42.4% for the contra-lateral supraspinatus.
The difference in mean PA between the pathological and contra-lateral supraspinatus for both the relaxed and contracted states was not significant.
Comparing individual subject data, subject #1 had the smallest percentage change in
FBL, 3%, and the largest percentage change in PA, 49%. Both subjects #4 and #5 had the largest percentage change in FLB of 29%; however, subject #4 had a 38% percentage change in PA whereas subject #5 had a 21% percentage change in PA. Table 5.13 provides a summary of FBL and PA for each subject.
94
n=5 Relaxed (cm) Contracted (cm) % change
Pathological 5.06±0.76a1 3.92±0.0.50b1 21.4% shoulder (4.13-6.14) (3.27-4.42)
Contra-lateral 5.52±0.85a1 3.91±0.56b1 27.4% shoulder (4.79-6.58) (3.48-4.79)
TABLE 5.11 Ultrasound investigation of pathological supraspinatus: Comparison of mean FLB and percentage change of anterior region between pathological supraspinatus and contra-lateral supraspinatus. Mean fiber bundle length (FBL) ± standard deviation (range). The superscript letters are used to indicate the presence or absence of statistical significance between the relaxed and contracted state, and superscript numbers between the pathological and contra-lateral supraspinatus. If the superscript letters/numbers differ, then the result is statistically significant. If the letter/number is repeated, there is no statistical significance.
n=5 Relaxed (deg) Contracted (deg) % change
Pathological 11.93 ± 1.23a1 14.97 ± 2.24b1 25.8% shoulder (10.52-13.09) (12.03-18.15)
Contra-lateral 13.0±1.98a1 18.40±3.55b1 42.4% shoulder (11.21-16.35) (12.90-21.90)
TABLE 5.12 Ultrasound investigation of pathological supraspinatus: Comparison of mean PA and percentage change of anterior region between pathological and contra- lateral supraspinatus. Mean pennation angle (PA), ± standard deviation (range). Superscript letters are used to indicate the presence or absence of statistical significance between the relaxed and contracted state, and superscript numbers between the pathological and contra-lateral supraspinatus. If the superscript letters/numbers differ, then the result is statistically significant. If the letter/number is repeated, there is no statistical significance.
95 Subject Age FBL (cm) % PA (deg) % (gender) change change relaxed contracted relaxed contracted
1 55(F) 4.13 4.0 3% 12.18 18.15 49%
2 50(M) 6.14 4.42 28% 10.76 12.03 12%
3 65(F) 5.02 4.38 13% 13.09 14.33 9%
4 69(F) 5.37 3.57 29% 10.52 14.52 38%
5 57(M) 4.63 3.27 29% 13.07 15.82 21%
TABLE 5.13 Ultrasound investigation of pathological supraspinatus: FBL and PA of anterior region for relaxed and contracted states and percentage change for each individual subject. Fiber bundle length (FBL), pennation angle (PA), male (M), female (F).
5.4.3.3 Posterior region
In four subjects, fiber bundles of the posterior region could be defined bilaterally but in one subject (#4) fiber bundles could only be defined unilaterally in the contracted state.
The acromial correction factor (3.2cm) was added to each in vivo FBL measurement for the deep part. The lateral attachment of fiber bundles were obscured by the acromion and thus PA could not be measured.
The mean FBL for the deep part of the posterior region in the relaxed state was
5.84±0.64 cm (n=4). Mean FBL for the contracted state was slightly shorter 5.66±0.14 cm (n=5) but the difference was not significant. On the contra-lateral supraspinatus, mean FBL in the relaxed state (5.88±0.84 cm) was the same as the mean FBL for the
96 contracted state (5.88±0.43 cm), with the relaxed state having a greater standard deviation
(Table 5.14).
When considering individual subjects, mean FBL for the deep part of the posterior region shortened in two subjects (#2 and #5) and lengthened in two subjects (#1 and #3).
See Table 5.15.
Relaxed (cm) Contracted (cm)
Pathological 5.84±0.64a1 5.66±0.14a1 shoulder (5.18-6.59) (5.49-5.87) n=4 n=5
Contra-lateral 5.88±0.84a1 5.88±0.43a1 shoulder (4.90-6.99) (5.36-6.55) n=5 n=5 TABLE 5.14 Ultrasound investigation of pathological supraspinatus: Comparison of mean FBL of posterior region between pathological and contra-lateral supraspinatus. Mean fiber bundle length (FBL) ± standard deviation (range). Note: FBL of posterior region includes acromial correction factor. Superscript letters are used to indicate the presence or absence of statistical significance between the relaxed and contracted state, and superscript numbers between the pathological and contra-lateral supraspinatus. If the superscript letters/numbers differ, then the result is statistically significant. If the letter/number is repeated, there is no statistical significance.
97
Subject Relaxed (cm) Contracted (cm)
1 5.18 5.60
2 6.14 5.87
3 5.48 5.72
4 - 5.49
5 6.59 5.62
TABLE 5.15 Ultrasound investigation of pathological supraspinatus: Mean FBL of posterior region for each individual subject. Fiber bundle length (FBL), - could not be measured.
5.5 Comparison of pathological and normal data
The architectural data of all five pathological subjects was compared with data from five gender, age, and hand dominance matched normal controls.
5.5.1 Pre-scanning
The middle and deep parts of the anterior region in the pathological supraspinatus had fewer well-defined fiber bundles than in the normal supraspinatus (Figure 5.5).
98 A.
B. B.
FIGURE 5.5 Ultrasound investigation: Comparison of US scans of normal and pathological supraspinatus. Right shoulder. A. Normal supraspinatus B. Pathological supraspinatus (full-thickness supraspinatus tendon tear).
5.5.2 Intramuscular tendon
The mean TD in the relaxed state of the normal controls (0.36±0.09 cm) tended to be larger than in the pathological supraspinatus (0.30±0.8 cm). In the contracted state, mean
TD of the pathological supraspinatus (0.44±0.15 cm) was slightly larger than in the normal controls (0.41±0.1 cm). These differences, however, were not significant. Mean
99 TD did not significantly change between the relaxed and contracted state in the normal controls, whereas in the pathological supraspinatus the mean distance did change significantly (p<0.05).
n=5 Relaxed (cm) Contracted (cm)
Normal 0.36±0.09a1 0.41±0.1a1 supraspinatus (0.25-0.47) (0.29-0.53)
Pathological 0.30±0.8a1 0.44±0.15 b1 supraspinatus (0.18-0.39) (0.21-0.56)
TABLE 5.16 Ultrasound investigation: Comparison of mean TD between normal controls and pathological supraspinatus. Mean distance between the intramuscular tendon and the superficial surface of the muscle belly (TD) ± standard deviation (range). The superscript letters are used to indicate the presence or absence of statistical significance between the relaxed and contracted state, and superscript numbers between the normal controls and pathological supraspinatus. If the superscript letters/numbers differ, then the result is statistically significant. If the letter/number is repeated, there is no statistical significance.
5.5.3 Muscle architecture
5.5.3.1 Muscle thickness
Mean MT between the normal controls and the pathological subjects did not differ significantly in either the relaxed or contracted state. In the normal controls, mean MT in the contracted state (2.07±0.38 cm) was significantly larger than in the relaxed state
(1.71± 0.34). In contrast, mean MT in the contracted state of the pathological
100 supraspinatus was not significantly larger than in the relaxed state. The percentage change in mean MT between the relaxed and contracted states was 21.9% in the normal controls, whereas it was 17.4% in the pathological supraspinatus (Table 5.17).
n=5 Relaxed (cm) Contracted (cm) % change
Normal 1.71± 0.34a1 2.07±0.38b1 21.9% supraspinatus (1.28-2.14) (1.59-2.54)
Pathological 1.99±0.29a1 2.30±0.16a1 17.4% supraspinatus (1.57-2.34) (2.10-2.54)
TABLE 5.17 Ultrasound investigation: Comparison of mean MT between normal controls and pathological supraspinatus. Mean muscle thickness (MT) ± standard deviation (range). Superscript letters are used to indicate the presence or absence of statistical significance between the relaxed and contracted state, and superscript numbers between the normal controls and pathological supraspinatus. If the superscript letters/numbers differ, then the result is statistically significant. If the letter/number is repeated, there is no statistical significance.
5.5.3.2 Anterior region
The mean FBL significantly changed between the relaxed and contracted state in both the normal controls and pathological supraspinatus (p<0.05). In the relaxed state, the mean FBL of the normal controls was 6.02±0.83 cm, and 4.30±0.83 cm in the contracted state. The mean percentage change was 28.4%. In the pathological supraspinatus, the mean FBL in the relaxed state was 5.06±0.76 cm, and 3.92±0.50 cm in the contracted
101 state. The mean percentage change was 21.4%. Mean FBL did not significantly differ between the normal controls and pathological supraspinatus for either the relaxed or contracted state. Table 5.18 summarizes these findings.
The mean PA also significantly changed between the relaxed and contracted state in both the normal controls and pathological supraspinatus (p<0.05). In the normal controls, mean PA in the relaxed state was 12.42º±1.89º and increased to 17.54º±2.59º in the contracted state. The mean percentage change was 44.9%. In the pathological supraspinatus, the mean percentage change was 25.8%. Mean PA in the relaxed state was
11.93º±1.23º and increased to 14.97º±2.24º in the contracted state. The difference in mean PA between the normal controls and pathological supraspinatus in either the relaxed and contracted state was not statistically significant (Table 5.19).
102 % n=5 Relaxed (cm) Contracted (cm) change
Normal 6.02±0.83a1 4.30±0.83b1 28.4% supraspinatus (4.68-6.88) (3.17-5.35)
Pathological 5.06±0.76a1 3.92±0.50b1 21.4% supraspinatus (4.13-6.14) (3.27-4.42)
TABLE 5.18 Ultrasound investigation: Comparison of mean FBL and percentage change of anterior region between normal controls and pathological supraspinatus. Mean fiber bundle length (FBL) ± standard deviation (range). The superscript letters are used to indicate the presence or absence of statistical significance between the relaxed and contracted state, and superscript numbers between the normal controls and pathological supraspinatus. If the superscript letters/numbers differ, then the result is statistically significant. If the letter/number is repeated, there is no statistical significance.
% n=5 Relaxed (deg) Contracted (deg) change
Normal 12.42±1.89a1 17.54±2.59b1 44.9% supraspinatus (9.29-14.13) (14.04-20.82)
Pathological 11.93 ± 1.23a1 14.97 ± 2.24b1 25.8% supraspinatus (10.52-13.09) (12.03-18.15)
TABLE 5.19 Ultrasound investigation: Comparison of mean PA and percentage change of anterior region between normal controls and pathological supraspinatus. Mean pennation angle (PA) ± standard deviation (range). Superscript letters are used to indicate the presence or absence of statistical significance between the relaxed and contracted state, and superscript numbers between the normal controls and pathological supraspinatus. If the superscript letters/numbers differ, then the result is statistically significant. If the letter/number is repeated, there is no statistical significance
103
5.5.3.3 Posterior region
Fiber bundle lengths of the deep part of the posterior region did not significantly change between the relaxed and contracted state in the normal controls and pathological supraspinatus. The difference between the mean FBL for the normal controls and pathological supraspinatus was statistically significant in the contracted state (p<0.05) but not in the relaxed state. See Table 5.20.
Relaxed (cm) Contracted (cm)
Normal 6.70±0.33a1 (6.35-7.07) 6.47±0.59a1 (6.01-7.27) supraspinatus n=5 n=4
Pathological 5.84±0.64a1 (5.18-6.59) 5.66±0.14a2 (5.49-5.87) supraspinatus n=4 n=5
TABLE 5.20 Ultrasound investigation: Comparison of mean FBL of posterior region between normal controls and pathological supraspinatus. Mean fiber bundle length (FBL) ± standard deviation (range). Note: FBL of posterior region includes acromial correction factor. Superscript letters are used to indicate the presence or absence of statistical significance between relaxed and contracted state, and superscript numbers between the normal controls and pathological supraspinatus. If the superscript letters/numbers differ, then the result is statistically significant. If the letter/number is repeated, there is no statistical significance.
5.6 Reliability and validity of measurements
5.6.1 Intra-rater reliability
No statistical difference was found between the two measurements for any variable at
104 any site (paired t-tests: p<0.05) for both the normal and pathological subject scans. The
Pearson product-moment correlation coefficients were calculated for FBL (r=0.93 normal subjects; r=0.87 pathological subjects) and PA (r=0.88 normal subjects; r=0.84 pathological subjects), indicating a good correlation.
5.6.2 Inter-rater reliability
Paired t-tests were used to determine if measurements by investigator 1 and 2 were significantly different. There was no statistical significant difference in measurements
(p<0.001). There was a good positive correlation between the measurements of the two independent raters; FBL (r=0.74 normal subjects; r=0.87 pathological subjects) PA
(r=0.76 normal subjects; r=0.89 pathological subjects).
5.6.3 Validity
Table 5.21 shows US measurements and digitized data of FBL on the fresh male human cadaver. Ultrasound measurements of FBL differed from digitized data by <0.1 cm.
105 US measurements Digitized data Mean FBL (cm) Mean FBL (cm) Anterior region
Middle part 5.4±0.3 5.4±0.9
Deep part 5.7±0.5 5.8±0.4
Posterior region
Deep part 3.0±0.2 3.0±0.2
TABLE 5.21 Summary of mean FBL measurements made on one male fresh cadaveric specimen: US scans and digitized data.
5.7 Summary of main findings
Cadaveric investigation:
• The supraspinatus muscle belly has two architecturally distinct regions that vary
significantly in their volumes (p<0.05).
• Within the anterior and posterior regions, there are three architecturally distinct
parts: superficial, middle and deep.
• Mean FBL for the entire anterior and posterior region were very similar.
• Within the anterior region, mean lateral PA for the middle part was significantly
less than the deep part (p<0.05).
US investigation of normal subjects:
• Mean FBL changes with active contraction and abduction to 60º differed between
the anterior and posterior regions.
106 • In the anterior region, mean FBL significantly shortened with active contraction
(p<0.05), but not in the posterior region.
• For the anterior region, the smallest percentage change in mean FBL between the
relaxed and contracted state was found when the arm was in the internally rotated
position.
• Mean PA significantly increased with active contraction in the anterior region
(p<0.05).
• The change in mean PA was significantly less in the externally rotated position
compared to the internally rotated and neutral positions (p<0.05).
• Within the anterior region, mean PA was significantly greater in the deep part than
in the middle part for the relaxed and all contracted states (p<0.05).
US investigation of pathological subjects:
• Muscle thickness did not change with active contraction on the pathological
supraspinatus.
• For the anterior region, the percentage change in mean FBL of the pathological
supraspinatus was less than the contra-lateral supraspinatus.
• A large difference in percentage change of mean PA was found between the
pathological and contra-lateral supraspinatus.
• Mean FBL of the posterior region did not significantly change with active
107 contraction and abduction to 60º.
Comparison of normal and pathological subjects:
• Mean TD in the relaxed state was smaller in the pathological supraspinatus than in
the normal controls.
• Mean FBL and PA were smaller in the pathological supraspinatus than in the
normal controls.
• Mean percentage change in FBL and PA varied between the pathological and
normal supraspinatus.
108 Chapter 6: Discussion
This cadaveric and in vivo study of the normal and pathological architecture of supraspinatus is the first of its kind. The findings of this study show that supraspinatus is a complex muscle; the fiber bundle architecture is not uniform throughout the muscle volume and dynamic changes are affected by tendon pathology. In this chapter, the findings of the cadaveric and in vivo investigation will be discussed relative to the previous literature and the functional and clinical significance will be elaborated.
6.1 Cadaveric investigation of normal supraspinatus
6.1.1 Three-dimensional modeling
To date, no previous study has modeled the detailed musculotendinous architecture of supraspinatus in situ throughout its volume. Computer modeling techniques that were initially developed by Agur (2003) and Ng-Thow-Hing (2001) were specifically customized for study of the supraspinatus. The enhanced technique enabled 1200-1600 fiber bundles spread throughout the muscle volume of supraspinatus and the intra- and extra-muscular portions of the tendon to be captured in 3D.
Previous studies that have identified distinct regions relied on gross dissection or 2D images (Roh et al., 2000; Vahlensieck et al., 2000). However, in this study, the architecturally distinct regions could be defined precisely within the volume of the muscle
109 using the 3D model. The model allows for fiber bundles to be viewed individually, in layers, and regionally. Furthermore, architecturally distinct parts within the anterior and posterior regions that were not previously documented in the literature could also be identified and defined.
6.1.2 Measurement of architectural parameters
This study is the first of its kind to quantify and document architectural parameters of the supraspinatus, in situ, using 3D data. In previous cadaveric studies of supraspinatus, architectural parameters have been quantified by sampling a small number of fiber bundles, often from the superficial surface of the muscle.
Fiber bundle lengths were computed in this study by summating the distance between closely digitized points, thus accounting for any fiber bundle curvature. In previous studies, FBL was usually measured with calipers placed at each attachment site, which does not capture fiber bundle curvature.
Pennation angle has been defined as the angle the fiber bundle creates at the intersection with line of force (Murray et al., 2000). Since the line of force (the line that intersects the centroids of cross-sections through the muscle volume) cannot be visually determined on a specimen, previous cadaveric studies have measured the surface PA, between the fiber bundle and its attachment sites to bone, tendon, or aponeurosis. In this study, PA was measured, as initially defined, relative to the line of force. Using the 3D
110 computer model, the line of force could be computed mathematically from the digitized data and used to determine PA.
The digitized data set could be sorted into separate files for the fiber bundles and tendon, thus enabling calculation of MV using only fiber bundle data. On cadaveric specimens, it is impossible to selectively remove the tendon alone without including some of the fiber bundles. In addition, the digitized data of the fiber bundles could be easily separated into regions based on attachment sites, FBL and PA. Roh et al. (2000) separated the anterior and posterior regions by visual observation and dissection.
6.1.3 Comparison of architectural parameters
The results of this cadaveric study will be discussed and compared, when possible, with data available in the literature.
6.1.3.1 Fiber bundle length
In this study, mean FBL for the entire muscle (6.7±0.64 cm) was found to be larger than those reported in the literature (mean FLB ranged from 2.8-6.5 cm). The shorter mean FBL reported by Itoi et al. (1995) and Ward et al. (2006) may be due to normalization of data (Tables 2.4 & 5.2).
Roh et al. (2000) was the only study to report separate mean FBLs for the anterior and posterior regions. The mean FBL for the anterior region found in this study was smaller
(6.7±0.7 cm) than what Roh et al. (2000) reported (8.3±0.9 cm). Mean FBL for the
111 posterior region found in this study (6.7 ± 0.5 cm) was similar with the mean Roh et al.
(2000) reported (6.5± 1.2 cm). It should be noted that mean FBL reported by Roh et al.
(2000) was based on “multiple representative muscle fibers excised from each muscle belly” which could have resulted in differences in the mean FBL for the anterior region.
Unique to this study, architecturally distinct parts (superficial, middle, deep) were observed within the anterior and posterior regions of the muscle belly. Within the anterior region, the mean FBL among all the three parts did not differ significantly.
Within the posterior region, the shortest mean FBL was found in the deep part (6.2 ± 0.5) and the longest in the middle part (7.0 ± 0.6 cm). The difference was significant
(p<0.05).
6.1.3.2 Pennation angle
In previous studies, PA was measured at only one attachment site relative to the tendon. In this study, both the medial and lateral PA were computed for fiber bundles relative to the line of force making comparison of results difficult. In this study, the mean medial PA was significantly less than the lateral PA. This difference may be explained by the orientation of the fiber bundles. The fiber bundles attach medially to a large area of bone, i.e. supraspinous fossa, resulting in a small PA, whereas, laterally the fiber bundles are more obliquely oriented and converge on the tendon.
112 6.1.3.3 Muscle volume
The combined volumes of the anterior and posterior regions in this study and the study by Roh et al. (2000) were similar, 17.9 cm3 and 16 cm3 respectively. Muscle volume of 39.3 ml reported by Wood et al. (1989) and 36 ml by Jensen et al. (1995) were the largest, but these were based on only one male cadaveric specimen.
When compared to Roh et al. (2000) the volume of the anterior region found in this study was larger (this study 15.4 ± 5.7 cm3; Roh et al. (2000) 12 ± 4 ml) and the posterior region was smaller (this study 2.5 ± 0.7 cm3; Roh et al. (2000) 4 ± 2 ml). These differences may be explained by the manual techniques used by Roh et al. (2000) to separate the anterior region from the posterior.
6.1.3.4 Tendon architecture
The anterior and posterior parts of the supraspinatus tendon were also documented by
Volk and Vangsness (2001) and Roh et al. (2000). These studies measured either tendon length (Volk and Vangsness, 2001) or tendon width (Roh et al, 2000), but not both (Table
2.5).
In this study, as with previous studies, the length of the anterior tendon was found to be greater than the posterior. The mean length of the anterior tendon (6.1 ± 0.7 cm) found in this study was longer than the length Volk and Vangsness (2001) found (5.4 cm).
However, the mean length of the posterior tendon in this study (2.9±0.6 cm) was
113 comparable to data reported by Volk and Vangsness (2001) who found the length to be
2.8 cm. The mean length of the “intramuscular tendon” reported by Itoi et al. (1995) was normalized to scapular length and was shorter than all other studies (4.08 ±1.03 cm).
The width of the anterior tendon found in this study (0.8±0.2 cm) was the same as that found by Roh et al. (2000). The widths of the posterior tendon were similar (in this study 1.6±0.3 cm; Roh et al. (2000) 1.3±0.3 cm). In this study, a small tendinous slip, extending approximately 1 cm from the posterior tendon, was found in three of the youngest (<50 years of age) specimens. Vahlensieck et al. (1993), in an MRI study of subjects with a mean age of 40.5 ± 13.9 years, found similar tendinous slips. Other cadaveric studies have not documented this structure. This may be explained by differences in the mean age of specimens used in this study and in previous cadaveric studies (Table 2.2). The mean age in this study was 61.9±16 years, whereas the mean age was 78.9 and 82 years in the studies by Juul-Kristensen et al. (2000b) and Roh et al.
(2000). Furthermore, since the intramuscular tendinous slip was short and found deep to the anterior region of the muscle belly it also could have been overlooked if the entire muscle volume was not dissected.
6.2 Ultrasound investigation of normal supraspinatus
On longitudinal US scans of suprspinatus, the pennate pattern created by the
114 hyperechoic fibroapdipose septa of the perimysium surrounding the hypoechoic muscle fiber bundles was visible. As Fornage et al. (1983) stated, the pennate pattern appeared as “multiple parallel lines forming oblique angles with the echogenic myotendinous junction”. Despite the visibility of the pennate pattern, US has not previously been used to quantify architectural parameters.
This is the first US study in which architectural parameters (i.e. FBL, PA, MT and
TD) were quantified in vivo. The development of the US protocol would not have been possible without the anatomical study which was integral in identifying the regions and their subdivisions in vivo.
The musculotendinous architecture of supraspinatus was observed in four different glenohumeral joint positions (0º abduction with neutral rotation, 60º abduction with neutral rotation; 60º abduction with 80º external rotation; 60º abduction with 80º internal rotation) with the contracted muscle working isometrically. Glenohumeral abduction of
60º was chosen because it is similar to the loose pack position (Trew & Everett, 2001).
The loose or “open” pack position is the position where the joint surfaces are least congruent, where the ligaments are least tight, and where the greatest amount of joint play is possible (Petersen, 2002). Thus, the loose pack position is a vulnerable position that relies on the dynamic function of muscles such as the supraspinatus. Different degrees of rotation at the glenohumeral joint in the loose pack position were investigated to gain
115 insight into the effect of joint position on musculotendinous architecture.
Shoulder abduction of 90º may have also been a good position to investigate since it is a functional position in many sports. However, to ensure that architectural comparison could be later made between the normal subjects and subjects with tendon pathology, this position was not investigated. Shoulder abduction of 90º may have elicited discomfort or pain in subjects with tendon pathology.
6.2.1 Measurement of architectural parameters
Since US has never been previously used to quantify FBL and PA of the supraspinatus, the reliability and validity of measurements were rigorously tested. Intra- and inter-rater measurements for FBL and PA in the normal and pathological subjects were found to have good correlations (r=0.74 - 0.87 for FBL; r=0.76-0.89 for PA).
Validity of measurements was demonstrated by comparison of FBL measurements made from US scans and digitized data of the same specimen. The measurement error was found to be <0.1cm.
In this study, the location of the intramuscular tendon relative to the superficial muscle belly surface (TD) was also measured. Similar to MT, TD can be used to assess muscle atrophy. However, TD can provide insight into whether muscle atrophy has occurred in the area above the intramuscular tendon. Meyer et al. (2005) suggested that atrophy of the supraspinatus following tendon tears may not be uniform throughout the
116 muscle volume and that muscle atrophy is more likely to occur in the muscle volume found above the intramuscular tendon.
6.2.2 Muscle architecture
The only architectural parameter that can be compared with previous US studies is
MT (Table 2.6). Mean MT in the relaxed state of normal subjects (1.74 ± 0.33 cm) found in this study was similar to the reported mean by Juul-Kristensen et al. (2000) 2.0 cm. It should be noted that the mean age of subjects were similar (in this study
36.4±12.7 years; Juul-Kristensen et al. (2000) 39.8 years. The effect of aging on MT is not clear. In a US study, Kubo et al. (2003) investigated 224 female subjects ranging in
20-79 years of age and found MT of vastus lateralis but not gastrocnemius and triceps brachii to significantly decline with advanced aging.
Since there are no other in vivo studies that have quantified architectural parameters, the findings from the cadaveric portion of this study will be compared with the findings from the US portion. Mean FBL of the middle and deep parts of the anterior region in vivo in the relaxed state, 5.94±0.82cm; 5.85±0.89cm respectively, were slightly shorter than the mean FBLs found in the cadaveric specimens in this study (6.7±0.7cm for middle,
6.7±0.5 cm for deep). However, the mean FBL in vivo was still within the range of mean FBL found in the cadaveric specimens (5.8-7.9 cm). For the deep part of the posterior region, mean FBL in vivo in the relaxed state (6.73±0.56 cm) was slightly longer
117 than the mean found in the cadaveric specimens (6.2± 0.5cm) but was still within the range of mean FBL (5.4-7.2cm).
On contraction, mean FBL significantly shortened for all positions in the anterior region, whereas no significant shortening occurred in the posterior. Among the different arm positions, mean FBL shortened the least in the internally rotated position and the most in the neutral. On contraction, mean PA significantly increased for all positions but was significantly less in the externally rotated position compared to the other contracted positions. The functional implications of these findings are discussed in the following section.
6.3 Functional implications of cadaveric and in vivo findings of normal subjects
To date, the dynamic function of supraspinatus has been inferred from static architectural data most often obtained from cadaveric specimens. In this study, however, the static and dynamic architecture were directly visualized and quantified. The muscle architecture was investigated in vivo in the relaxed state (arm resting by the subjects’ side) and three different contracted states (60˚ abduction; 60˚ abduction with 80˚ external rotation; 60˚ abduction with 80˚ internal rotation) with the muscle working isometrically.
Making inferences on other glenohumeral positions and functional contexts which involve
118 different types of contraction, however, are limited. Furthermore, since the entire length of fiber bundles from the posterior region could not be visualized, functional inferences of the posterior region require further support with EMG analysis or possibly MRI analysis.
The anterior and posterior parts of the supraspinatus tendon allow for two distinct fiber bundle arrangements to be found within the muscle volume. The long cord-like anterior tendon allows for fiber bundles of the anterior region to be arranged in a pennate fashion, whereas the broad posterior tendon allows for a more parallel arrangement of fiber bundles in the posterior region. In a pennate muscle, fiber bundles are orientated at an angle to the line of force, which allows for a greater number of fiber bundles to be packed within a given volume. Thus, a pennate muscle can often produce greater forces than a muscle of similar length with a more parallel arrangement. Based the overall fiber bundle arrangements of the anterior and posterior regions, the anterior region is more likely to be involved in force production.
The significantly larger volume of the anterior region of muscle belly also suggests that much of the muscle’s force is produced by this region. As a result, the anterior tendon may undergo greater stress than the posterior tendon during contraction. This difference in volume and possible greater stress may explain the higher incidence of anterior tendon tears (Huang et al., 2005).
Significant differences in PA between the middle and deep parts of the anterior region,
119 may suggest that stresses throughout the anterior tendon are heterogeneous.
Intratendinous shear has been found to occur within the supraspinatus tendon, and the strain within the tendon has been found to increase as the joint angle increases (Bey et al.,
2002). Both Huang et al. (2005) and Fukada et al. (1994) found that there is higher strain on the articular (deep) side of the tendon. Although joint position has been found to have a pronounced effect on intratendinous strain, and shear within the tendon has been thought to be responsible for pathogenesis of tendon injuries (Bey et al., 2002; Fukada et al., 1994), the possible influence of the musculotendinous architecture on tendon shearing has not been previously investigated or discussed. Based on the findings of this study, the larger PA of the deep part when compared to the middle part of the anterior region suggests that the middle part will generate greater force than the deep part under similar activation conditions. As a result, the different contraction forces stressing the tendon simultaneously may contribute to greater shear stresses to the articular surface of the anterior tendon.
The results obtained in vivo indicate that the musculotendinous architecture of supraspinatus significantly changes as a function of muscle contraction and that these changes may not be uniform for the anterior and posterior regions. For example, mean
FBL and PA of the anterior region were different between the relaxed and contracted states. The mean FBL was significantly shorter and the mean PA was significantly
120 greater in the contracted states compared to the relaxed state. Contrary to what was found for the anterior region, the mean FBL of the posterior region did not significantly change with muscle contraction.
Differences in the percentage of mean FBL shortening between the anterior and posterior regions also suggest that these regions may have different functional roles. The significantly greater percentage of fiber bundle shortening in the anterior region from the relaxed to contracted states, in addition to volume differences previously discussed, further suggests that the anterior region is more involved in force production than the posterior region. In contrast, the small percentage of FBL change of the posterior region from the relaxed to contracted states may suggest that this region has an important role in maintaining tension on the tendon. In other words, the posterior region, which laterally attaches to a wider portion of the tendon than the anterior region, may aid in maintaining tension on the cuff and capsule to prevent impingement and help maintain joint stability.
To better elucidate the role of the posterior region further investigations are needed such as US investigation with different glenohumeral joint positions. Fiber bundle length may be found to significantly change with different joint positions.
Electromyography (EMG) analysis with needles placed within the posterior region may also aid in better understanding the functional role. It would be interesting to investigate
FBL changes in 90º abduction with movement from external to internal rotation. This is
121 a functional position for overhead athletes who tend to have posterior tendon pathology
(Blevins, 1997). Finally, examination of the intramuscular innervation pattern of the suprascapular nerve would provide important insight into whether the anterior and posterior regions are independently innervated by separate branches of the nerve and thus functionally distinct.
As found in the cadaveric specimens, mean PA in normal subjects in vivo was not uniform throughout the anterior region. In the relaxed and all the contracted states, mean
PA of the middle part was significantly greater than the deep part. These differences in mean PA between the middle and deep parts of the anterior region further suggest that forces along the intramuscular tendon are heterogeneous. Since the mean PA of the middle part was significantly smaller, the contracting force may be greater than the deep part. This difference in resultant forces may result in shearing stresses along the articular side of the intramuscular tendon which was previously discussed.
The musculotendinous architecture of supraspinatus also significantly changes as a function of glenohumeral joint position with muscle contraction. For example, when the muscle was contracted, the percentage of mean FBL shortening of the anterior region was significantly less with the arm held in the internally rotated position than in the neutral or externally rotated positions. In addition, mean PA was significantly smaller with the arm held in the externally rotated position than in the neutral or internally rotated positions.
122 Architectural differences found between the various joint positions suggest that the amount of force the supraspinatus is able to produce depends on the glenohumeral joint position. Under similar activation conditions, the anterior region of the supraspinatus may be able to produce less force in the internally rotated position than if the joint was positioned in neutral or external rotation. In the internally rotated position, not only was the mean PA greatest but the percentage of mean FBL shortening was also smallest.
6.4 Ultrasound investigation of pathological supraspinatus
The pennate pattern of the pathological supraspinatus was still visible on US scanning although the sharp contrast between the muscle fiber bundles was often less distinct compared to the normal subjects and to the contra-lateral supraspinatus.
It is not surprising that the contra-lateral supraspinatus tendon was found to have pathology in four or the five subjects. In fact, Booth and Marvel (1975) state that “it is unusual, by the fifth decade of life, to find rotator cuffs in which thinning and fibrillation of the tendons has not begun.” Whether changes in the tendon precede or result in changes of the muscle architecture remains unknown.
Ultrasound investigation of the pathological supraspinatus allowed for comparison of architectural data not only between the pathological and contra-lateral shoulder but also between age and gender matched normal controls. As the tendon pathology worsens (i.e.
123 partial thickness tear to full-thickness tear), the percentage change in MT, FBL and PA with muscle contraction in the anterior region decreases. The impact was greatest to the PA. For the posterior region, mean FBL changed very little from the relaxed to contracted state for both the pathological and contra-lateral shoulder. This may be related to the fact that the tear was located in the anterior not posterior tendon.
Comparison between the pathological and normal controls revealed more pronounced differences in mean percentage change of MT, FBL and PA on contraction than between the pathological and contra-lateral muscles of the same individual. Again, PA changes were found to be impacted the most by the tendon pathology. Mean TD, the distance between the intramuscular tendon and the superficial surface of the muscle belly, was smallest in the pathological supraspinatus suggesting that muscle atrophy in this area of the muscle had occurred.
Although the sample of pathological subjects was small (n=5), the results provide preliminary data that suggest that architectural changes do occur with tendon pathology.
Quantification of architectural parameters with US of the pathological muscle in vivo may provide additional functional and diagnostic information.
6.5 Functional implications of in vivo findings of pathological subjects
124 Differences in the percentage change in FBL and PA of the anterior region and MT on contraction between the normal and pathological supraspinatus suggest that the muscle is not functioning optimally. Since PA appears to be the architectural parameter that is most affected by tendon pathology, changes in the force producing capabilities of the anterior region are likely.
In the posterior region, the relatively small differences in the mean FBL on contraction between the pathological, contra-lateral, and normal controls suggest that the function of the posterior region, which is presently unclear, may be preserved with anterior tendon tears.
As discussed earlier, shearing stresses along the intramuscular tendon may occur as a result of significant differences in mean PA between the middle and deep parts of the anterior region. If muscle atrophy that occurs with tendon pathology is not uniform and affects the area of the muscle above the intramuscular tendon more than other areas, then the contraction force generated by this area of the muscle will be less. Thus, in the pathological supraspinatus, the shearing stress that may normally occur along the tendon is likely to change.
125 6.6 Clinical implications
Rotator cuff tears involving the supraspinatus are one of the most common clinical problems associated with the shoulder (Matsen, 2004). Unfortunately, as Harryman et al. (2003) states, “the effectiveness and appropriateness of rotator cuff tear treatment across multiple practices is essentially unknown.” The architectural data collected in this study along with the US protocol has numerous clinical implications that may aid in improving the outcome of rotator cuff treatment and in better understanding the etiology of tendon tears.
Presently, therapeutic exercises for supraspinatus, such as the empty and full-can exercises, aim at improving the force generating capability of the muscle. These exercises, which involve shoulder abduction (0-90˚) with either internal or external rotation at the glenohumeral joint, likely target the anterior region based on architectural changes seen with US. Ultrasound investigation found significant changes in mean FBL in the anterior region with active shoulder abduction but not in the posterior. Although further investigation is needed to clarify the role of the posterior region, if the posterior region’s role is more for proprioception and/or eccentric control, exercises that focus on these aspects may be helpful to maximize functional properties.
The three-dimensional model of supraspinatus and the architecturally distinct region and parts of the muscle could serve as an architectural map for future clinical studies.
126 For example, EMG analysis with accurately placed needles may be carried out to better monitor the activity of distinct regions during different functional activities.
The US protocol developed in this study could be used as an outcome measure of adaptive changes of muscle function following therapeutic exercises, athletic training, or surgery. For example, although EMG and MRI studies have found the empty-can exercise to be just as appropriate as the full-can exercise in activating supraspinatus, the in vivo architectural data seems to suggest otherwise (Malanga et al., 1996; Takeda et al., 2002).
In the internally rotated position, which is the position of the glenohumeral joint with the empty-can exercise, the in vivo architecture shows that the anterior region likely cannot produce as much force as compared to the neutral or externally rotated positions.
Additionally, although athletes undergo rigorous training regimes that involve repetitive overhead activities, little is known about the effects of training on the musculotendinous architecture. Thus, a combination of US and EMG could be used to compare changes in muscle architecture and make inferences regarding muscle function as a result of different exercises and intensities of athletic training or surgery.
For patients with articular sided partial thickness tears, supraspinatus exercises within the range of 60º of glenohumeral abduction may increase shearing stress on the articular surface of the tendon caused by differences in PA between the middle and deep parts of the anterior region. This is also supported by Bey et al. (2002) who found that
127 intratendinous strain “profoundly” increased with 60º abduction of the glenohumeral joint.
In these patients, avoiding exercises that involve abduction around or greater than 60º may be important to prevent further progression of these kinds of tears.
In the case of more severe pathology of the supraspinatus tendon, US may also be used by surgeons to determine the best intervention. Currently, the severity of the rotator cuff tear and muscle atrophy are used to help determine the suitability for surgical repair
(Goutallier et al., 2003). However, as shown by Boehm et al. (2005), patients with an identical clinical diagnosis (i.e. full thickness tears of the supraspinatus with the same amount of fatty atrophy) can have significant variability in muscle contraction patterns.
Therefore, US investigation may assist surgeons detect muscles that may have atrophy but still show potential to produce adequate forces based on quantitative analysis of architectural parameters. Pre and post-operative investigation could also provide surgeons with greater insight into how the repair of the tendon has influenced the musculotendinous architecture and thus its function.
6.7 Summary
The supraspinatus is architecturally complex. In vivo investigation and quantification of the musculotendinous architecture with US is feasible and can provide important insight into the dynamic function of the normal and pathological muscle.
128 Traditionally, structural deficits of the tendon have been focused on to understand the etiology of supraspinatus tendon tears (Rothman & Parke, 1965, Bigliani et al., 1990).
However, as shown in this study, quantification of architectural parameters of the muscle belly may provide important insight into the pathomechanics, prevention, and treatment of tendon pathology.
129 Chapter 7: Conclusions
The conclusions of this thesis are divided into three sections. The first section outlines the conclusions derived from the cadaveric investigation, the second section from the US investigation of normal subjects and the third from the US investigation of pathological subjects.
Conclusions related to cadaveric investigation and three-dimensional modeling of supraspinatus:
1. The supraspinatus muscle and tendon architecture is complex.
• The tendon has two distinct parts: an anterior tendon which is extra- and
intramuscular in its course; a posterior tendon which is entirely extramuscular.
The lengths of the anterior and posterior tendon are significantly different
(p<0.05).
• The muscle belly has two distinct regions: anterior and posterior. The
volume of each region is significantly different (p<0.05).
• Within the anterior and posterior regions, there are three distinct subdivisions:
superficial, middle, and deep.
• Mean PA between the middle and deep parts of the anterior region differ
significantly (p<0.05).
130
Conclusions related to US investigation of the normal supraspinatus:
1. Fiber bundle changes on contraction were not uniform throughout the muscle
volume.
• Fiber bundle length changes on contraction were significant (p<0.05) in the
anterior region but not in the posterior.
• Pennation angle changes on contraction in the anterior region were significant
(p<0.05).
• The mean PA between the middle and deep parts of the anterior region differed
even with muscle contraction and with different shoulder positions.
2. Fiber bundle architecture changes as a function of joint position. Among the
different positions investigated, the internally rotated position appears to be
the least optimal for force production.
131 Conclusions related to US investigation of the pathological supraspinatus:
1. The in vivo US protocol can be used to investigate and quantify the
musculotendinous architecture i.e. FBL, PA, MT and TD of supraspinatus in
subjects with a full-thickness anterior tendon tear.
2. Comparison of architectural parameters between the pathological and normal
controls suggests that the mean percentage change in FBL and PA on contraction
differ.
3. Based on differences between MT and percentage change in FBL and PA with the
normal controls, the pathological supraspinatus does not appear to be functioning
optimally.
4. The size of the tendon tear (i.e. partial thickness or full-thickness) appears to be
related to the mean MT and percentage change in FBL and PA on contraction.
The supraspinatus is a complex muscle that is architecturally partitioned. If clinicians use the traditional perspective of a uniform muscle with an origin and insertion as the only rationale to characterize supraspinatus function, it may limit optimal evaluation and treatment of dysfunction associated with supraspinatus tendon tears.
132 Chapter 8: Future Directions
The findings of this study could be used as the basis for future anatomical, biomechanical, imaging, and clinical studies. Below is an outline of some of the possible future directions.
1. Use the architectural data base collected in this study to develop more advanced
computer models of supraspinatus such as a contractile model of the normal and
pathological supraspinatus that also accounts for tissue properties of muscle,
tendon and bone.
2. Use the architectural map to
a. Investigate correlation between the intramuscular innervation pattern of
the suprascapular nerve and architecturally distinct region of supraspinatus
b. Investigate and model the fiber type distribution throughout the muscle
volume of supraspinatus and discuss the functional and clinical
implications.
133 3. Use the US protocol developed in this study to investigate the musculotendinous
architecture of supraspinatus pre- and post- rotator cuff tendon repair surgery to
better understand the functional implications of surgical techniques.
4. Use the US protocol to investigate the musculotendinous architecture of
supraspinatus in other patient populations i.e. hemiplegic patients, overhead
athletes.
5. Plan EMG studies to investigate the activity of architecturally distinct regions of
supraspinatus with different exercise regimens.
6. Explore the feasibility of using other advanced imaging modalities i.e. MRI to
investigate the fiber bundle architecture of the posterior region of supraspinatus.
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144 Appendix A Sample Size Calculation
Fiber bundle length was used to calculate the sample size because it is the most commonly measured architectural parameter.
1. Null Hypothesis: Mean FBL (cm) of the anterior region of supraspinatus is the same
as the mean of the posterior region.
2. Alternative Hypothesis: Mean FBL (cm) of the anterior region of supraspinatus is
different from the mean of the posterior region.
3. Effect size = 0.651cm (10% X 6.51 cm)
4. Standard Deviation of fiber bundle length = 0.47 cm
5. Standardized effect size = effect size÷standard deviation = 0.651÷0.47= 1.38
6. α (two-sided) = 0.05; β= 1-0.80 =0.20
7. Therefore, sample size required is 17
145 Appendix B Ethics Approval
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