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Effects of glenohumeral rotations and translations on supraspinatus tendon morphology
Clinical Biomechanics 19 (2004) 579–585 www.elsevier.com/locate/clinbiomech
Effects of glenohumeral rotations and translations on supraspinatus tendon morphology T. Nakajima, R.E. Hughes, K.-N. An
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Orthopedic Biomechanics Laboratory, Mayo Clinic, 200 First Street, S.W., Rochester, MN 55905, USA Received 18 September 2002; accepted 25 February 2004
Abstract Objective. The purpose of this study was to evaluate the effects of glenohumeral rotations and humeral head translations on supraspinatus tendon morphology. Design. A convenience sample of cadaver shoulders was used to measure supraspinatus tendon shape and dimensions from MRI images. Background. Epidemiological evidence has indicated that shoulder elevation and external rotation may be risk factors for rotator cuff tendon pathology, but little is known about how these postures affect tendon morphology. Methods. Measurements of supraspinatus tendon morphology were made from three-dimensional reconstructions based on T2weighted fast spin-echo magnetic resonance images. Seven cadaver arms were imaged at neutral, 45 external and 45 internal rotations at 0, 30, and 60 of glenohumeral abduction. Measurements of the anterior, middle, and posterior portions of the tendon were made using A N A L Y Z E TM software. Results. The supraspinatus tendon was twisted at the muscle–tendon junction of the middle and posterior portions in 45 external and 45 internal axial rotations of the humerus, especially over 30 of abduction. Abduction over 30 shortened the entire supraspinatus tendon. External and internal rotation motions elongated the anterior and posterior portions, respectively. Conclusions. Arm posture affects morphology of the supraspinatus tendon. Relevance The results support the epidemiologic evidence linking external rotation and abduction to supraspinatus tendon disorders. 2004 Elsevier Ltd. All rights reserved. Keywords: Supraspinatus tendon; Rotator cuff; Glenohumeral rotation; MRI; Image processing
1. Introduction Rotator cuff disorders are an important source of musculoskeletal morbidity, with a reported incidence rate of 19.9 per 10,000 full-time equivalent employees per year (Silverstein et al., 1998). Elevated arm posture has been shown to be a risk factor for rotator cuff and shoulder disorders in occupational settings (Herberts et al., 1981; Punnett et al., 2000). The effect of arm posture on shoulder soft-tissue mechanics remains unclear. While elevated arm posture increases the net moment at the shoulder, it also changes the orientations and locations of the humerus and scapula. Although
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Corresponding author. E-mail address: [email protected] (K.-N. An).
0268-0033/$ - see front matter 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.clinbiomech.2004.02.007
much effort has been devoted to understanding the effects of arm posture on rotator cuff muscle forces (Karlsson and Peterson, 1992; van der Helm, 1994; Hughes and An, 1996), less attention has been given to understanding the effect of arm motions on the geometry of the cuff tendons. Two theories of cuff pathology etiology are popular: (1) impaired perfusion to the critical zone of the supraspinatus tendon, and (2) compression and abrasion of the supraspinatus tendon due to impingement from the inferior surface of the acromion. The former theory is predicated on anatomical studies showing limited vascularity in the distal supraspinatus tendon (Lindblom, 1939; Lindblom and Palmer, 1939; Rothman and Parke, 1970), and the effects of poor vascularity are thought to be exacerbated when the tendon is twisted so as to be ‘‘wrung out’’ like a wet towel. In
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contrast, the impingement theory emphasizes the close proximity of the humeral head to the acromion and the reported association between acromial morphology and cuff pathology (Bigliani et al., 1991). Translation of the humeral head may, in theory, trap the tendon between the acromion and humerus, which would represent impingement of the tendon. Finite element modeling has shown that impingement of the supraspinatus tendon, which is the most commonly affected part of the rotator cuff, may cause large compressive stresses (Luo et al., 1998). Compression of tendon, in turn, has been shown to alter gene expression of tenocytes, which may play a role in the biology of rotator cuff pathology (Blevins et al., 1997). Understanding the relationship between arm posture and three-dimensional geometry of the supraspinatus tendon may validate these theories. Magnetic resonance imaging (MRI) may provide information on supraspinatus morphology. MRI has been elegantly used to describe the kinematics of the humerus relative to the scapula in healthy volunteers and rotator cuff patients (Graichen et al., 2000a,b, 2001a,c; von Eisenhart-Rothe et al., 2002) and measure the supraspinatus moment arm (Graichen et al., 2001b) and line of action (Graichen et al., 2001c), but these studies have not directly addressed the complex three-dimensional morphology of the tendon. The purpose of this study was to use MRI to measure the length and thickness of supraspinatus tendons in cadavers with the arm abducted and axially rotated. The hypothesis to be tested was that humeral rotations (abduction and internal/external rotation) and translations resulting from the rotations affect the morphology of the supraspinatus tendon.
supraspinatus (the defects were not detectable on MRI). The remaining five had no evidence of cuff tears at all. The scapula was secured in a prone position on a Plexiglas fixture using plastic screws and methylmethacrylate. This fixture was composed of a round table, a plastic socket, and an attachment device (Fig. 1A). The socket was used to support the humerus and control its axial rotation. The attachment device moved around an edge of the table and could control the glenohumeral abduction angle by rotating the scapula. This device also had three elastomers, each of which was calibrated to generate a uniform tensile load (25 N/cm) depending on an elongation ratio relative to the original length (Fig. 1B). Each scapula rotated from 5 of adduction to its maximum abduction, which averaged 87.3 (11.7 SD).
2. Methods Seven (2 right and 5 left) shoulders were harvested from two male and five female fresh cadavers. The age at death ranged 51–79 years (mean: 68.4 years). All of the specimens had full range of motion. They were kept frozen at )40 C and thawed at room temperature before examination. Soft tissues were completely removed from the distal portion of the humerus, leaving the deltoid and cuff muscles and tendons intact. The supraspinatus muscle was detached from its origin in the supraspinous fossa so that the muscle belly could slide without resistance. Care was taken not to rupture the joint capsule. Twenty-pound test nylon lines were sutured to anterior, middle, and posterior portions of the supraspinatus muscle. Following imaging, each specimen was dissected except for the rotator cuff tendons and joint capsule. Cuff tendons were inspected for tears. Five shoulders had intact cuffs, and two had small pinhole-size defects (less than 2 mm in diameter) in the
Fig. 1. Experimental setup. The scapula was fixed in the prone position on a Plexiglas fixture. This fixture was composed of a round table, a plastic socket, and an attachment device. The socket was used to support the humerus and control its axial rotation. The attachment device could control the glenohumeral abduction angle by rotating the scapula (A). The device had three elastomers, each of which was calibrated to generate a uniform tensile load (25 N/cm) depending on an elongation ratio relative to the original length (B). Tensile loads of 5, 25, and 50 Newtons were applied to the supraspinatus muscle by these elastomers in 0, 30, and 60 abduction of the scapula, respectively.
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Since the terminal stage of this motion was not uniform, all specimens were imaged at 0, 30, and 60 of abduction. The glenoid was tilted 20 downward relative to the Plexiglas table to simulate the tilt of the scapula in the sagittal plane. Macroscopically, the center of the humeral head was located at the same level as the center of the glenoid fossa. This initial position produced a motion arc of lateral elevation in the coronal plane, which was called ‘abduction’ in this study (note that this is not the same as the in vivo abduction angle between arm and torso because of scapulothoracic motion). Imaging was conducted with the Plexiglas table inserted longitudinally into a MRI machine. Tensile loads of 5, 25, and 50 Newtons (N) were applied to the supraspinatus muscle by three elastomers in 0, 30, and 60 abduction, respectively. These loads were applied to simulate the muscle forces occurring during arm abduction, and they correspond to values reported in the literature (Wuelker et al., 1994). Two vertical tensile loads, one of which was parallel and the other perpendicular to the humeral shaft, were applied by two calibrated elastomers at the olecranon to simulate the mass of the arm acting 30 cm distal to the glenohumeral joint center of rotation (Poppen and Walker, 1976) (Fig. 2). The magnitudes of two loads were controlled depending on the abduction angle of the scapula, but the net force was 22 N. Sixty degrees of glenohumeral abduction was assumed to correspond to 90 of abduction relative to the torso in vivo, since the ratio of glenohumeral abduction to scapulothoracic motion is approximately 2:1. Therefore, to simulate the effect of gravity on the mass of the arm the 22 N load was applied axially when the humerus was adducted and perpendicularly when it was abducted 60. A 16 N load was
Fig. 2. Two vertical tensile loads, one of which was parallel and the other perpendicular to the humeral shaft, were applied at the olecranon to simulate the mass of the arm acting 30 cm distal to a rotation center of the humeral head. Therefore, to simulate the effect of gravity on the mass of the arm the 22 N load was applied axially when the humerus was adducted and perpendicularly when it was abducted 60. A 16 N load was applied axially and perpendicularly during 30 of glenohumeral abduction to simulate the 45 of abduction in vivo.
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applied axially and perpendicularly during 30 of glenohumeral abduction to simulate the 45 of abduction in vivo. A three-dimensional T2-weighted fast spin-echo (FSE) sequence was implemented on a coronal plane using the Signa 1.5T MR image system (GE Medical Systems, Milwaukee, WI, USA) and a dedicated transmit–receive extremity coil. Each specimen was examined at neutral, 45 external and 45 internal rotation of the humerus in each of 0, 30, and 60 of glenohumeral abduction (total of nine postures). FSE sequence parameters were 2000 ms relaxation time, 90 ms echo time (TEeff ), 160–240 mm field of view (FOV), 256 · 256 pixel acquisition matrix, 1.0-mm section thickness with no gap, number of excitation (NEX) of one, and twosignals averaged. These parameters were determined from pilot testing. A FSE acquisition time for one specimen was less than nine minutes. Each MR image data set, which was stored on digital data tape, was converted to a format readable by the image processing software A N A L Y Z E TM (Version 7.0, Mayo Foundation, Rochester, MN, USA). The supraspinatus tendon, muscle, and humerus were manually traced on two-dimensional MR coronal slices using an image segmentation algorithm. The A N A L Y Z E TM software superimposed these segmented images threedimensionally with the voxel gradient shading algorithm. The tendon, muscle, and humerus were each treated as a separate ‘‘object’’, and they were colored yellow, red, and white, respectively. A 3D image was constructed using the voxel gradient shading algorithm. Geometric measurements of the supraspinatus tendon were made with a line measurement function. Tendon measurements were made for six regions of the supraspinatus. The length of the bursal-side surface (distance between the muscle–tendon junction and the tendon insertion) was examined at neutral, 45 external and 45 internal rotation in each abduction posture. For each of these postures, the tendon was divided into three ‘‘portions’’ in the anteroposterior (AP) direction and two ‘‘segments’’ in the medial–lateral direction. The three AP portions were measured on the bursal-side surface: anterior (3 mm posterior from the anterior tendon margin), middle (10 mm), and posterior (17 mm). Two segments were defined: proximal and distal. A measurement location for the proximal segment of each portion of the tendon was defined as 17 mm proximal to the insertion. For the distal segment, the location was 3 mm proximal to the insertion. Tendon thickness of the whole layer of tendon, including subacromial bursa, was estimated perpendicular to the bursal-side surface at each measurement location (Fig. 3). Therefore, there were a total of six locations at which tendon thickness was measured. Width of the tendon was not a dimension parameter, because the posterior boundary between the supraspinatus and infraspinatus
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Length ðmmÞ ¼ C0 þ C1 ðlocalized tendon indentationÞ þ C2 ðsuperior translationÞ þ C3 ðanterior translationÞ þ C4 ðabductionÞ þ C5 ðexternal rotationÞ þ C6 ðabductionÞ ðexternal rotationÞ External rotation was the rotation of the humerus about its long axis; a positive value was assigned for external rotation and a negative value was for internal rotation. Positive values of the humeral head translations showed superior and anterior distances of the center of the humeral head from that of the glenoid fossa. Tendon thickness was modeled similarly.
Fig. 3. ‘Portions’ and ‘segments’ of the supraspinatus tendon. Length and thickness were measured for the ‘portions’ and ‘segments’, respectively. Tendon length was measured in the medial–lateral direction along the length of the tendon for each portion (anterior, middle, and posterior). Thickness was measured at two locations: 3 mm medial to the insertion (distal segment) and 17 mm medial to the insertion (proximal segment).
tendons could not be clearly identified. Both kinds of geometric data (length and thickness) were measured five times and averaged. These values were converted to millimeters using the scale factor of the volume and recorded as 3D coordinates. Localized tendon indentation was defined to exist if the tendon was thinner than its neighboring area by more than 1 mm. Superior translation was the distance from the mid-slice of the humeral head to the mid-slice of the glenoid oriented perpendicular to the scapular plane. Similarly, the anterior translation was the distance from the mid-slice of the humeral head to the mid-slice of the glenoid in the plane of the scapula. For statistical analysis of the tendon dimensions, length and thickness were dependent variables and scapular abduction and humeral axial rotation angles were independent variables. Localized tendon indentation, superior translation, and anterior translation of the humeral head were also independent variables. The effects of the glenohumeral rotation, localized tendon indentation, and humeral head translations on the tendon length and thickness were statistically analyzed using multiple regression. Tendon length was modeled as
Fig. 4. Top views of the supraspinatus tendon. The top views created by A N A L Y Z E TM showed 3D morphological changes of the supraspinatus tendon depending on axial rotation (internal rotation, neutral, and external rotation) and glenohumeral elevation (0, 30, and 60). Note tendon twisting in neutral and external rotation for the 30 and 60 elevation conditions (arrows denote location of visible tendon twisting).
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3. Results
4. Discussion
Top views made by A N A L Y Z E TM software showed three-dimensional shapes of the supraspinatus tendon in nine positions (Fig. 4). Interestingly, the middle and posterior portions of the tendon appeared twisted at the mid-point of the tendon or muscle–tendon junction. Scapular abduction and external rotation of the humerus made this morphological change more recognizable, even if tensile loads applied to the tendon increased with abduction angle. Abduction motion of the scapula shortened all portions of the supraspinatus tendon more significantly than axial rotation of the humerus (Tables 1 and 3). The shortening with abduction was ranked in the order posterior > middle > anterior. External and internal rotation motions elongated the anterior and posterior portions, respectively. The distal and proximal segments in all portions became thicker with abduction, and the rank of the effect was middle > posterior > anterior (Tables 2 and 3). The anterior portion thickened only with abduction. Thickness of the middle portion increased more significantly with abduction than with external rotation. On the other hand, axial rotation of the humerus had a greater effect on thickness in the posterior portion than abduction did. The posterior portion was thicker than the middle portion when the humerus was externally rotated.
The present study demonstrated the supraspinatus tendon was twisted at the muscle–tendon junction of the middle and posterior portions when glenohumeral abduction was greater than 30 (this level of abduction corresponds to 45 of in vivo arm abduction relative to the torso). This type of folding can be visualized when twisting a wet towel. Rather than folding up along the medial–lateral direction, it twists about its long axis. This twisted shape was more apparent in 45 external rotation postures. In vivo glenohumeral kinematics of bones has been increasingly investigated using electromagnetic tracking systems and MRI, but little is known about how skeletal kinematics affects soft-tissue morphology in the shoulder. Shoulder rhythm during dynamic arm motions has been quantified (Ludewig et al., 1996; McQuade and Smidt, 1998; Ludewig and Cook, 2000; McClure et al., 2001), and MRI has been used to quantify subacromial distances (Graichen et al., 2001a). Our study augments these studies by providing insight into supraspinatus morphology based on MRI measurements. Our results help explain results of epidemiological studies that find external rotation is a risk factor for cuff pathology. Fine et al. reported that employees in jobs having high rates of supraspinatus symptoms worked with arms in external rotation more than employees in
Table 1 Descriptive statistics of tendon length measurements, mean (standard deviation) External rotation angle (degrees)
Glenohumeral abduction angle (degrees)
Anterior tendon portion length (mm) n ¼ 7
Middle tendon portion length (mm) n ¼ 7
Posterior tendon portion length (mm) n ¼ 7
0 0 0 )45 )45 )45 45 45 45
0 30 60 0 30 60 0 30 60
19.7 19.9 16.3 19.0 17.9 16.7 20.9 20.5 17.1
19.4 17.4 15.2 19.8 17.9 16.7 19.8 16.3 14.1
18.1 15.7 13.5 20.9 19.0 17.0 17.2 13.9 11.9
(3.1) (5.0) (3.5) (2.6) (4.2) (4.1) (3.1) (4.3) (3.6)
(3.5) (4.5) (2.3) (3.1) (4.2) (2.4) (3.1) (2.6) (2.4)
(2.7) (2.7) (2.3) (2.8) (3.8) (2.0) (3.4) (1.3) (2.3)
Table 2 Descriptive statistics of tendon thickness measurements, mean (standard deviation) External rotation angle (degrees)
Glenohumeral abduction angle (degrees)
Anterior tendon portion thickness (mm) n ¼ 7
Middle tendon portion thickness (mm) n ¼ 7
Posterior tendon portion thickness (mm) n ¼ 7
0 0 0 )45 )45 )45 45 45 45
0 30 60 0 30 60 0 30 60
7.3 8.0 8.6 7.3 7.9 8.6 7.3 8.0 9.0
6.7 7.0 8.5 6.5 7.9 8.3 7.4 8.0 9.2
7.0 7.3 9.3 6.8 7.0 8.6 9.0 8.6 9.5
(0.8) (1.3) (1.1) (1.1) (1.6) (1.5) (0.7) (1.0) (0.8)
(0.9) (0.4) (1.3) (0.6) (1.6) (1.2) (1.5) (1.3) (1.1)
(0.9) (1.2) (1.5) (1.1) (1.0) (0.8) (2.1) (1.6) (1.2)
The numbers in parentheses are the p-values for the respective coefficient. Model parameters were C0 (constant), C1 (localized tendon indentation), C2 (superior translation), C3 (anterior translation), C4 (abduction angle), C5 (external rotation angle), and C6 (abduction-external rotation interaction). The bolded numbers indicate changes of the supraspinatus tendon length and thickness were significantly affected by localized tendon indentation (C1 ) and glenohumeral position (C4 and C5 ). R2 is the coefficient of multiple determination.
0.65 0.60 )0.000284 (0.0739) )0.000418 (0.0302) 0.026425 (0.0001) 0.035046 (0.0001) 0.026618 (0.0004) 0.023760 (0.0075) 0.037486 (0.5557) 0.012563 (0.8698) )0.306531 (0.4669) )1.028001 (0.0371) 8.140256 (0.0001) 8.830885 (0.0001) Posterior Dis. Prox.
)0.084382 (0.2728) )0.023548 (0.7965)
0.68 0.62 )5.4661 · 105 (0.6631) )0.000194 (0.2483) 0.012610 (0.0113) 0.019403 (0.0042) 0.034528 (0.0001) 0.024692 (0.0023) 0.055222 (0.2882) )0.044682 (0.5108) )0.481218 (0.0749) )0.590833 (0.0821) 7.695503 (0.0001) 7.549034 (0.0001) Middle Dis. Prox.
)0.056884 (0.3470) 0.002270 (0.9777)
0.74 0.48 )4.0169 · 105 (0.7078) )0.000114 (0.4578) 0.004200 (0.3117) 0.006260 (0.2918) 0.023761 (0.0001) 0.019242 (0.0037) 0.047209 (0.3560) 0.010446 (0.8874) )1.059168 (0.0124) )0.379374 (0.4538) 7.543892 (0.0001) 7.970121 (0.0001) Thickness Anterior Dis. Prox.
)0.122354 (0.0651) )0.097594 (0.3000)
)0.000374 (0.3509) )0.000526 (0.0965) )0.000306 (0.2996) )0.048743 (0.0050) )0.069122 (0.0001) )0.077148 (0.0001) 0.306063 (0.1162) 0.141184 (0.2675) 0.056834 (0.6335) 17.00413 (0.0001) 16.455894 (0.0001) 15.649932 (0.0001) Length Anterior Middle Posterior
)0.321195 (0.1957) )0.161625 (0.2901) )0.115041 (0.4224)
0.033377 (0.0350) 0.000286 (0.9813) )0.041166 (0.0007)
C6 (mm/degree2 ) C5 (mm/degree) C4 (mm/degree) C3 C2 C1 (mm) C0 (mm)
Table 3 Multiple regression model of supraspinatus tendon dimensions
0.65 0.68 0.76
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R2
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jobs having low shoulder injury rates (Fine et al., 1986). Our findings suggest that axial rotation places the tendon in a shape that could impair perfusion when tension is applied to the tendon. There are some limitations in the current study. First, in vitro kinematics of the glenohumeral joint and the scapula may not simulate in vivo conditions. The humeral head was initially located at the center of the Plexiglas table and the glenoid fossa. Although this experiment provides a ‘‘best-case’’ situation in spatial relationships of the supraspinatus outlet, the humeral head translation in this model was found to be different from the in vivo range reported by Poppen and Walker (1976). The humeral head moved inferiorly with increasing arm elevation. This limitation mostly affects the extrapolation of our localized tendon indentation results to the in vivo condition. It is likely that our estimates are conservative. In fact, inferior translation of the humeral head should increase the acromiohumeral distance. Tendon length measurements should be less affected because the humeral head translation direction is orthogonal to the line of action of the supraspinatus. A second limitation of our experimental model was that it did not include muscle contraction forces for all rotator cuff muscles. Modest tension was applied to the supraspinatus tendon, but none was applied to the humeral head depressors. The low levels of supraspinatus tension are likely to produce larger thickness measurements than would occur in vivo because of the tension-induced narrowing of the tendon described by Poisson’s ratio. A third limitation of the study was that the morphological characteristics of the coracoacromial arch were not considered. Fourth, the pinhole-size holes in the tendons of two specimens could have affected how the tendons deformed with changes in humeral posture. However, the reconstructed shapes of tendons from these two specimens did not appear to differ from the intact specimens.
Acknowledgements This study was supported by grants AR41171 and HD07447 awarded by the National Institutes of Health.
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Effects of glenohumeral rotations and translations on supraspinatus tendon morphology T. Nakajima, R.E. Hughes, K.-N. An
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Orthopedic Biomechanics Laboratory, Mayo Clinic, 200 First Street, S.W., Rochester, MN 55905, USA Received 18 September 2002; accepted 25 February 2004
Abstract Objective. The purpose of this study was to evaluate the effects of glenohumeral rotations and humeral head translations on supraspinatus tendon morphology. Design. A convenience sample of cadaver shoulders was used to measure supraspinatus tendon shape and dimensions from MRI images. Background. Epidemiological evidence has indicated that shoulder elevation and external rotation may be risk factors for rotator cuff tendon pathology, but little is known about how these postures affect tendon morphology. Methods. Measurements of supraspinatus tendon morphology were made from three-dimensional reconstructions based on T2weighted fast spin-echo magnetic resonance images. Seven cadaver arms were imaged at neutral, 45 external and 45 internal rotations at 0, 30, and 60 of glenohumeral abduction. Measurements of the anterior, middle, and posterior portions of the tendon were made using A N A L Y Z E TM software. Results. The supraspinatus tendon was twisted at the muscle–tendon junction of the middle and posterior portions in 45 external and 45 internal axial rotations of the humerus, especially over 30 of abduction. Abduction over 30 shortened the entire supraspinatus tendon. External and internal rotation motions elongated the anterior and posterior portions, respectively. Conclusions. Arm posture affects morphology of the supraspinatus tendon. Relevance The results support the epidemiologic evidence linking external rotation and abduction to supraspinatus tendon disorders. 2004 Elsevier Ltd. All rights reserved. Keywords: Supraspinatus tendon; Rotator cuff; Glenohumeral rotation; MRI; Image processing
1. Introduction Rotator cuff disorders are an important source of musculoskeletal morbidity, with a reported incidence rate of 19.9 per 10,000 full-time equivalent employees per year (Silverstein et al., 1998). Elevated arm posture has been shown to be a risk factor for rotator cuff and shoulder disorders in occupational settings (Herberts et al., 1981; Punnett et al., 2000). The effect of arm posture on shoulder soft-tissue mechanics remains unclear. While elevated arm posture increases the net moment at the shoulder, it also changes the orientations and locations of the humerus and scapula. Although
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Corresponding author. E-mail address: [email protected] (K.-N. An).
0268-0033/$ - see front matter 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.clinbiomech.2004.02.007
much effort has been devoted to understanding the effects of arm posture on rotator cuff muscle forces (Karlsson and Peterson, 1992; van der Helm, 1994; Hughes and An, 1996), less attention has been given to understanding the effect of arm motions on the geometry of the cuff tendons. Two theories of cuff pathology etiology are popular: (1) impaired perfusion to the critical zone of the supraspinatus tendon, and (2) compression and abrasion of the supraspinatus tendon due to impingement from the inferior surface of the acromion. The former theory is predicated on anatomical studies showing limited vascularity in the distal supraspinatus tendon (Lindblom, 1939; Lindblom and Palmer, 1939; Rothman and Parke, 1970), and the effects of poor vascularity are thought to be exacerbated when the tendon is twisted so as to be ‘‘wrung out’’ like a wet towel. In
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contrast, the impingement theory emphasizes the close proximity of the humeral head to the acromion and the reported association between acromial morphology and cuff pathology (Bigliani et al., 1991). Translation of the humeral head may, in theory, trap the tendon between the acromion and humerus, which would represent impingement of the tendon. Finite element modeling has shown that impingement of the supraspinatus tendon, which is the most commonly affected part of the rotator cuff, may cause large compressive stresses (Luo et al., 1998). Compression of tendon, in turn, has been shown to alter gene expression of tenocytes, which may play a role in the biology of rotator cuff pathology (Blevins et al., 1997). Understanding the relationship between arm posture and three-dimensional geometry of the supraspinatus tendon may validate these theories. Magnetic resonance imaging (MRI) may provide information on supraspinatus morphology. MRI has been elegantly used to describe the kinematics of the humerus relative to the scapula in healthy volunteers and rotator cuff patients (Graichen et al., 2000a,b, 2001a,c; von Eisenhart-Rothe et al., 2002) and measure the supraspinatus moment arm (Graichen et al., 2001b) and line of action (Graichen et al., 2001c), but these studies have not directly addressed the complex three-dimensional morphology of the tendon. The purpose of this study was to use MRI to measure the length and thickness of supraspinatus tendons in cadavers with the arm abducted and axially rotated. The hypothesis to be tested was that humeral rotations (abduction and internal/external rotation) and translations resulting from the rotations affect the morphology of the supraspinatus tendon.
supraspinatus (the defects were not detectable on MRI). The remaining five had no evidence of cuff tears at all. The scapula was secured in a prone position on a Plexiglas fixture using plastic screws and methylmethacrylate. This fixture was composed of a round table, a plastic socket, and an attachment device (Fig. 1A). The socket was used to support the humerus and control its axial rotation. The attachment device moved around an edge of the table and could control the glenohumeral abduction angle by rotating the scapula. This device also had three elastomers, each of which was calibrated to generate a uniform tensile load (25 N/cm) depending on an elongation ratio relative to the original length (Fig. 1B). Each scapula rotated from 5 of adduction to its maximum abduction, which averaged 87.3 (11.7 SD).
2. Methods Seven (2 right and 5 left) shoulders were harvested from two male and five female fresh cadavers. The age at death ranged 51–79 years (mean: 68.4 years). All of the specimens had full range of motion. They were kept frozen at )40 C and thawed at room temperature before examination. Soft tissues were completely removed from the distal portion of the humerus, leaving the deltoid and cuff muscles and tendons intact. The supraspinatus muscle was detached from its origin in the supraspinous fossa so that the muscle belly could slide without resistance. Care was taken not to rupture the joint capsule. Twenty-pound test nylon lines were sutured to anterior, middle, and posterior portions of the supraspinatus muscle. Following imaging, each specimen was dissected except for the rotator cuff tendons and joint capsule. Cuff tendons were inspected for tears. Five shoulders had intact cuffs, and two had small pinhole-size defects (less than 2 mm in diameter) in the
Fig. 1. Experimental setup. The scapula was fixed in the prone position on a Plexiglas fixture. This fixture was composed of a round table, a plastic socket, and an attachment device. The socket was used to support the humerus and control its axial rotation. The attachment device could control the glenohumeral abduction angle by rotating the scapula (A). The device had three elastomers, each of which was calibrated to generate a uniform tensile load (25 N/cm) depending on an elongation ratio relative to the original length (B). Tensile loads of 5, 25, and 50 Newtons were applied to the supraspinatus muscle by these elastomers in 0, 30, and 60 abduction of the scapula, respectively.
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Since the terminal stage of this motion was not uniform, all specimens were imaged at 0, 30, and 60 of abduction. The glenoid was tilted 20 downward relative to the Plexiglas table to simulate the tilt of the scapula in the sagittal plane. Macroscopically, the center of the humeral head was located at the same level as the center of the glenoid fossa. This initial position produced a motion arc of lateral elevation in the coronal plane, which was called ‘abduction’ in this study (note that this is not the same as the in vivo abduction angle between arm and torso because of scapulothoracic motion). Imaging was conducted with the Plexiglas table inserted longitudinally into a MRI machine. Tensile loads of 5, 25, and 50 Newtons (N) were applied to the supraspinatus muscle by three elastomers in 0, 30, and 60 abduction, respectively. These loads were applied to simulate the muscle forces occurring during arm abduction, and they correspond to values reported in the literature (Wuelker et al., 1994). Two vertical tensile loads, one of which was parallel and the other perpendicular to the humeral shaft, were applied by two calibrated elastomers at the olecranon to simulate the mass of the arm acting 30 cm distal to the glenohumeral joint center of rotation (Poppen and Walker, 1976) (Fig. 2). The magnitudes of two loads were controlled depending on the abduction angle of the scapula, but the net force was 22 N. Sixty degrees of glenohumeral abduction was assumed to correspond to 90 of abduction relative to the torso in vivo, since the ratio of glenohumeral abduction to scapulothoracic motion is approximately 2:1. Therefore, to simulate the effect of gravity on the mass of the arm the 22 N load was applied axially when the humerus was adducted and perpendicularly when it was abducted 60. A 16 N load was
Fig. 2. Two vertical tensile loads, one of which was parallel and the other perpendicular to the humeral shaft, were applied at the olecranon to simulate the mass of the arm acting 30 cm distal to a rotation center of the humeral head. Therefore, to simulate the effect of gravity on the mass of the arm the 22 N load was applied axially when the humerus was adducted and perpendicularly when it was abducted 60. A 16 N load was applied axially and perpendicularly during 30 of glenohumeral abduction to simulate the 45 of abduction in vivo.
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applied axially and perpendicularly during 30 of glenohumeral abduction to simulate the 45 of abduction in vivo. A three-dimensional T2-weighted fast spin-echo (FSE) sequence was implemented on a coronal plane using the Signa 1.5T MR image system (GE Medical Systems, Milwaukee, WI, USA) and a dedicated transmit–receive extremity coil. Each specimen was examined at neutral, 45 external and 45 internal rotation of the humerus in each of 0, 30, and 60 of glenohumeral abduction (total of nine postures). FSE sequence parameters were 2000 ms relaxation time, 90 ms echo time (TEeff ), 160–240 mm field of view (FOV), 256 · 256 pixel acquisition matrix, 1.0-mm section thickness with no gap, number of excitation (NEX) of one, and twosignals averaged. These parameters were determined from pilot testing. A FSE acquisition time for one specimen was less than nine minutes. Each MR image data set, which was stored on digital data tape, was converted to a format readable by the image processing software A N A L Y Z E TM (Version 7.0, Mayo Foundation, Rochester, MN, USA). The supraspinatus tendon, muscle, and humerus were manually traced on two-dimensional MR coronal slices using an image segmentation algorithm. The A N A L Y Z E TM software superimposed these segmented images threedimensionally with the voxel gradient shading algorithm. The tendon, muscle, and humerus were each treated as a separate ‘‘object’’, and they were colored yellow, red, and white, respectively. A 3D image was constructed using the voxel gradient shading algorithm. Geometric measurements of the supraspinatus tendon were made with a line measurement function. Tendon measurements were made for six regions of the supraspinatus. The length of the bursal-side surface (distance between the muscle–tendon junction and the tendon insertion) was examined at neutral, 45 external and 45 internal rotation in each abduction posture. For each of these postures, the tendon was divided into three ‘‘portions’’ in the anteroposterior (AP) direction and two ‘‘segments’’ in the medial–lateral direction. The three AP portions were measured on the bursal-side surface: anterior (3 mm posterior from the anterior tendon margin), middle (10 mm), and posterior (17 mm). Two segments were defined: proximal and distal. A measurement location for the proximal segment of each portion of the tendon was defined as 17 mm proximal to the insertion. For the distal segment, the location was 3 mm proximal to the insertion. Tendon thickness of the whole layer of tendon, including subacromial bursa, was estimated perpendicular to the bursal-side surface at each measurement location (Fig. 3). Therefore, there were a total of six locations at which tendon thickness was measured. Width of the tendon was not a dimension parameter, because the posterior boundary between the supraspinatus and infraspinatus
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Length ðmmÞ ¼ C0 þ C1 ðlocalized tendon indentationÞ þ C2 ðsuperior translationÞ þ C3 ðanterior translationÞ þ C4 ðabductionÞ þ C5 ðexternal rotationÞ þ C6 ðabductionÞ ðexternal rotationÞ External rotation was the rotation of the humerus about its long axis; a positive value was assigned for external rotation and a negative value was for internal rotation. Positive values of the humeral head translations showed superior and anterior distances of the center of the humeral head from that of the glenoid fossa. Tendon thickness was modeled similarly.
Fig. 3. ‘Portions’ and ‘segments’ of the supraspinatus tendon. Length and thickness were measured for the ‘portions’ and ‘segments’, respectively. Tendon length was measured in the medial–lateral direction along the length of the tendon for each portion (anterior, middle, and posterior). Thickness was measured at two locations: 3 mm medial to the insertion (distal segment) and 17 mm medial to the insertion (proximal segment).
tendons could not be clearly identified. Both kinds of geometric data (length and thickness) were measured five times and averaged. These values were converted to millimeters using the scale factor of the volume and recorded as 3D coordinates. Localized tendon indentation was defined to exist if the tendon was thinner than its neighboring area by more than 1 mm. Superior translation was the distance from the mid-slice of the humeral head to the mid-slice of the glenoid oriented perpendicular to the scapular plane. Similarly, the anterior translation was the distance from the mid-slice of the humeral head to the mid-slice of the glenoid in the plane of the scapula. For statistical analysis of the tendon dimensions, length and thickness were dependent variables and scapular abduction and humeral axial rotation angles were independent variables. Localized tendon indentation, superior translation, and anterior translation of the humeral head were also independent variables. The effects of the glenohumeral rotation, localized tendon indentation, and humeral head translations on the tendon length and thickness were statistically analyzed using multiple regression. Tendon length was modeled as
Fig. 4. Top views of the supraspinatus tendon. The top views created by A N A L Y Z E TM showed 3D morphological changes of the supraspinatus tendon depending on axial rotation (internal rotation, neutral, and external rotation) and glenohumeral elevation (0, 30, and 60). Note tendon twisting in neutral and external rotation for the 30 and 60 elevation conditions (arrows denote location of visible tendon twisting).
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3. Results
4. Discussion
Top views made by A N A L Y Z E TM software showed three-dimensional shapes of the supraspinatus tendon in nine positions (Fig. 4). Interestingly, the middle and posterior portions of the tendon appeared twisted at the mid-point of the tendon or muscle–tendon junction. Scapular abduction and external rotation of the humerus made this morphological change more recognizable, even if tensile loads applied to the tendon increased with abduction angle. Abduction motion of the scapula shortened all portions of the supraspinatus tendon more significantly than axial rotation of the humerus (Tables 1 and 3). The shortening with abduction was ranked in the order posterior > middle > anterior. External and internal rotation motions elongated the anterior and posterior portions, respectively. The distal and proximal segments in all portions became thicker with abduction, and the rank of the effect was middle > posterior > anterior (Tables 2 and 3). The anterior portion thickened only with abduction. Thickness of the middle portion increased more significantly with abduction than with external rotation. On the other hand, axial rotation of the humerus had a greater effect on thickness in the posterior portion than abduction did. The posterior portion was thicker than the middle portion when the humerus was externally rotated.
The present study demonstrated the supraspinatus tendon was twisted at the muscle–tendon junction of the middle and posterior portions when glenohumeral abduction was greater than 30 (this level of abduction corresponds to 45 of in vivo arm abduction relative to the torso). This type of folding can be visualized when twisting a wet towel. Rather than folding up along the medial–lateral direction, it twists about its long axis. This twisted shape was more apparent in 45 external rotation postures. In vivo glenohumeral kinematics of bones has been increasingly investigated using electromagnetic tracking systems and MRI, but little is known about how skeletal kinematics affects soft-tissue morphology in the shoulder. Shoulder rhythm during dynamic arm motions has been quantified (Ludewig et al., 1996; McQuade and Smidt, 1998; Ludewig and Cook, 2000; McClure et al., 2001), and MRI has been used to quantify subacromial distances (Graichen et al., 2001a). Our study augments these studies by providing insight into supraspinatus morphology based on MRI measurements. Our results help explain results of epidemiological studies that find external rotation is a risk factor for cuff pathology. Fine et al. reported that employees in jobs having high rates of supraspinatus symptoms worked with arms in external rotation more than employees in
Table 1 Descriptive statistics of tendon length measurements, mean (standard deviation) External rotation angle (degrees)
Glenohumeral abduction angle (degrees)
Anterior tendon portion length (mm) n ¼ 7
Middle tendon portion length (mm) n ¼ 7
Posterior tendon portion length (mm) n ¼ 7
0 0 0 )45 )45 )45 45 45 45
0 30 60 0 30 60 0 30 60
19.7 19.9 16.3 19.0 17.9 16.7 20.9 20.5 17.1
19.4 17.4 15.2 19.8 17.9 16.7 19.8 16.3 14.1
18.1 15.7 13.5 20.9 19.0 17.0 17.2 13.9 11.9
(3.1) (5.0) (3.5) (2.6) (4.2) (4.1) (3.1) (4.3) (3.6)
(3.5) (4.5) (2.3) (3.1) (4.2) (2.4) (3.1) (2.6) (2.4)
(2.7) (2.7) (2.3) (2.8) (3.8) (2.0) (3.4) (1.3) (2.3)
Table 2 Descriptive statistics of tendon thickness measurements, mean (standard deviation) External rotation angle (degrees)
Glenohumeral abduction angle (degrees)
Anterior tendon portion thickness (mm) n ¼ 7
Middle tendon portion thickness (mm) n ¼ 7
Posterior tendon portion thickness (mm) n ¼ 7
0 0 0 )45 )45 )45 45 45 45
0 30 60 0 30 60 0 30 60
7.3 8.0 8.6 7.3 7.9 8.6 7.3 8.0 9.0
6.7 7.0 8.5 6.5 7.9 8.3 7.4 8.0 9.2
7.0 7.3 9.3 6.8 7.0 8.6 9.0 8.6 9.5
(0.8) (1.3) (1.1) (1.1) (1.6) (1.5) (0.7) (1.0) (0.8)
(0.9) (0.4) (1.3) (0.6) (1.6) (1.2) (1.5) (1.3) (1.1)
(0.9) (1.2) (1.5) (1.1) (1.0) (0.8) (2.1) (1.6) (1.2)
The numbers in parentheses are the p-values for the respective coefficient. Model parameters were C0 (constant), C1 (localized tendon indentation), C2 (superior translation), C3 (anterior translation), C4 (abduction angle), C5 (external rotation angle), and C6 (abduction-external rotation interaction). The bolded numbers indicate changes of the supraspinatus tendon length and thickness were significantly affected by localized tendon indentation (C1 ) and glenohumeral position (C4 and C5 ). R2 is the coefficient of multiple determination.
0.65 0.60 )0.000284 (0.0739) )0.000418 (0.0302) 0.026425 (0.0001) 0.035046 (0.0001) 0.026618 (0.0004) 0.023760 (0.0075) 0.037486 (0.5557) 0.012563 (0.8698) )0.306531 (0.4669) )1.028001 (0.0371) 8.140256 (0.0001) 8.830885 (0.0001) Posterior Dis. Prox.
)0.084382 (0.2728) )0.023548 (0.7965)
0.68 0.62 )5.4661 · 105 (0.6631) )0.000194 (0.2483) 0.012610 (0.0113) 0.019403 (0.0042) 0.034528 (0.0001) 0.024692 (0.0023) 0.055222 (0.2882) )0.044682 (0.5108) )0.481218 (0.0749) )0.590833 (0.0821) 7.695503 (0.0001) 7.549034 (0.0001) Middle Dis. Prox.
)0.056884 (0.3470) 0.002270 (0.9777)
0.74 0.48 )4.0169 · 105 (0.7078) )0.000114 (0.4578) 0.004200 (0.3117) 0.006260 (0.2918) 0.023761 (0.0001) 0.019242 (0.0037) 0.047209 (0.3560) 0.010446 (0.8874) )1.059168 (0.0124) )0.379374 (0.4538) 7.543892 (0.0001) 7.970121 (0.0001) Thickness Anterior Dis. Prox.
)0.122354 (0.0651) )0.097594 (0.3000)
)0.000374 (0.3509) )0.000526 (0.0965) )0.000306 (0.2996) )0.048743 (0.0050) )0.069122 (0.0001) )0.077148 (0.0001) 0.306063 (0.1162) 0.141184 (0.2675) 0.056834 (0.6335) 17.00413 (0.0001) 16.455894 (0.0001) 15.649932 (0.0001) Length Anterior Middle Posterior
)0.321195 (0.1957) )0.161625 (0.2901) )0.115041 (0.4224)
0.033377 (0.0350) 0.000286 (0.9813) )0.041166 (0.0007)
C6 (mm/degree2 ) C5 (mm/degree) C4 (mm/degree) C3 C2 C1 (mm) C0 (mm)
Table 3 Multiple regression model of supraspinatus tendon dimensions
0.65 0.68 0.76
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R2
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jobs having low shoulder injury rates (Fine et al., 1986). Our findings suggest that axial rotation places the tendon in a shape that could impair perfusion when tension is applied to the tendon. There are some limitations in the current study. First, in vitro kinematics of the glenohumeral joint and the scapula may not simulate in vivo conditions. The humeral head was initially located at the center of the Plexiglas table and the glenoid fossa. Although this experiment provides a ‘‘best-case’’ situation in spatial relationships of the supraspinatus outlet, the humeral head translation in this model was found to be different from the in vivo range reported by Poppen and Walker (1976). The humeral head moved inferiorly with increasing arm elevation. This limitation mostly affects the extrapolation of our localized tendon indentation results to the in vivo condition. It is likely that our estimates are conservative. In fact, inferior translation of the humeral head should increase the acromiohumeral distance. Tendon length measurements should be less affected because the humeral head translation direction is orthogonal to the line of action of the supraspinatus. A second limitation of our experimental model was that it did not include muscle contraction forces for all rotator cuff muscles. Modest tension was applied to the supraspinatus tendon, but none was applied to the humeral head depressors. The low levels of supraspinatus tension are likely to produce larger thickness measurements than would occur in vivo because of the tension-induced narrowing of the tendon described by Poisson’s ratio. A third limitation of the study was that the morphological characteristics of the coracoacromial arch were not considered. Fourth, the pinhole-size holes in the tendons of two specimens could have affected how the tendons deformed with changes in humeral posture. However, the reconstructed shapes of tendons from these two specimens did not appear to differ from the intact specimens.
Acknowledgements This study was supported by grants AR41171 and HD07447 awarded by the National Institutes of Health.
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