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A Cadaveric Study of Strain on the Subscapularis Muscle
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ORIGINAL ARTICLE
A Cadaveric Study of Strain on the Subscapularis Muscle Takayuki Muraki, PT, PhD, Mitsuhiro Aoki, MD, PhD, Eiichi Uchiyama, MD, PhD, Hiroshi Takasaki, PT, MS, Gen Murakami, MD, PhD, Shigenori Miyamoto, PT, PhD ABSTRACT. Muraki T, Aoki M, Uchiyama E, Takasaki H, Murakami G, Miyamoto S. A cadaveric study of strain on the subscapularis muscle. Arch Phys Med Rehabil 2007;88:941-6. Objectives: To measure the strain on 3 fiber groups of the subscapularis muscle at various glenohumeral joint positions and to determine the appropriate shoulder position for subscapularis muscle stretching. Design: Repeated-measures design. Setting: Biomechanics laboratory. Specimens: Nine frozen-thawed glenohumeral joints obtained from 9 fresh cadavers. Interventions: Not applicable. Main Outcome Measure: The strain on the upper, middle, and lower fiber groups of the subscapularis were measured by precise displacement sensors during 14 different glenohumeral joint positions. Results: The glenohumeral joint position that showed the largest strain varied among the 3 fiber groups. Although no position showed significantly large strain on the upper and middle fiber groups, external rotation at 30°, 60°, and 90° of elevation, abduction, flexion, and horizontal abduction revealed significantly greater strain on the lower fiber groups (P⬍.005). Additionally, except for external rotation at 0° of elevation, the strain on the lower fiber group was significantly greater than that on the upper and middle fiber groups in external rotation (P⬍.005). Conclusions: The stretching position of each fiber group of the subscapularis differs depending on the glenohumeral joint position. External rotation at 30° to 60° of glenohumeral elevation, abduction, flexion, and horizontal abduction can significantly stretch the lower fiber group of the subscapularis muscle. Key Words: Cadaver; Muscles; Rehabilitation; Sprains and strains. © 2007 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation UNCTIONS OF THE SUBSCAPULARIS muscle, such as flexibility and strength, are essential for the normal shoulF der motion required for daily activities and for the high per-
formance necessitated by overhead sports.1-3 The flexibility of the muscle could be reduced due to muscle contracture.4-6 Moreover, the subscapularis muscle strength has been reported
From the Doctoral Course of Physical Therapy, Graduate School of Health Sciences, Sapporo Medical University, Sapporo, Japan (Muraki, Takasaki); and Departments of Physical Therapy (Aoki, Miyamoto) and Anatomy (Uchiyama, Murakami), Sapporo Medical University School of Health Sciences, Sapporo, Japan. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to Takayuki Muraki, PT, PhD, Doctoral Course of Physical Therapy, Graduate School of Health Sciences, Sapporo Medical University, South-1, West-17, Chuo-ku, Sapporo, Japan, e-mail: [email protected]. 0003-9993/07/8807-11250$32.00/0 doi:10.1016/j.apmr.2007.04.003
to be compromised by subscapularis tendon tear7-11 and muscle damage due to repetitive overload.12,13 In rehabilitation, muscle stretching is an important technique for restoring the flexibility of shortened musculotendinous units.14 This technique is also frequently used as part of both warming-up and cooling-down procedures in order to prevent muscle injury while participating in sports-related activities.15 If it is applied effectively, muscle injury occurring during strenuous activities may be avoided. Generally, the most effective shoulder position for stretching the subscapularis muscle is considered to be unclear. Although, based on the anatomic characteristics of the subscapularis muscle, some authors have reported the use of shoulder external rotation for the selective stretching positions of the subscapularis muscle; other authors have reported the use of other shoulder elevation angles at which the external rotation was performed.16-18 For example, Ekstrom and Osborn16 introduced external rotation at 0° of shoulder elevation for the selective stretching positions of the subscapularis, whereas Houglum18 used external rotation at the maximum shoulder elevation. Furthermore, Evjenth and Hamberg17 advocated the application of external rotation at 90° of shoulder elevation in the coronal plane. Identifying the shoulder position for the stretching is difficult because the “shoulder” includes 4 mobile joints, the glenohumeral, acromioclavicular, sternoclavicular, and scapulothoracic joints, as well as many muscles. Because the subscapularis muscle connects the scapula and humerus, at least the glenohumeral joint position for the subscapularis stretching should be identified. In addition, the subscapularis muscle consists of muscle fibers oriented in different directions. The stretching position of each muscle fiber group may be different. To overcome the discrepancies of subscapularis stretching position, the glenohumeral joint positions that effectively stretch the subscapularis muscle should be determined quantitatively by directly observing the strain on each muscle fiber group. For this purpose, direct measurement of the muscle strain by using cadaveric glenohumeral joints is useful. Although the measurement of physiologic strain with muscle contraction or tension is impossible in this method, engineering strain can be measured and be compared between various glenohumeral joint positions because the construction of the cadaveric and in vivo glenohumeral joints is the same. The purpose of this study was to determine the appropriate glenohumeral joint position for the effective stretching of the subscapularis muscle by measuring the strain on each subscapularis muscle fiber group at various glenohumeral joint positions. METHODS Preparation of the Specimen In this experiment, we used frozen glenohumeral joints (5 right and 4 left joints) without any evidence of rotator cuff tears or osteoarthritis. These were obtained from 9 fresh cadavers aged 78 to 85 years at death (average age, 80y) after acquiring informed consent prior to death. The cadaveric shoulders were kept in a freezer at ⫺20°C after disarticulating the scapula from Arch Phys Med Rehabil Vol 88, July 2007
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the thorax. The thawing of the specimens at room temperature began 12 hours prior to the experiment. Thawing was confirmed through preconditioned movement of the glenohumeral joint in all directions. We then excised the serratus anterior, latissimus dorsi, rhomboids, and levator scapulae muscles. The distal third of the humerus was exposed. To control the rotational angle of the humerus, an acrylic stick was inserted perpendicular to the shaft, which denoted the longitudinal axis of the forearm at 90° of elbow flexion. Next, the humerus was amputated above the elbow. Throughout the experiment, which was performed at room temperature (22°C), the specimens were kept moist by spraying saline solution every 5 to 10 minutes. In this experiment, we used a wood jig consisting of a wood board and a square timber. The scapula was fixed to the wood jig such that the medial border of the scapula was perpendicular to the ground19 (fig 1). Two threaded anchorsa were inserted into the bony insertions of the infraspinatus and subscapularis tendons such that a compressive force of 11N could be applied to each thread (total, 22N) against the glenoid fossa. In previous cadaveric studies,20,21 this compressive force was used as the minimum force required preventing subluxation of the humeral head on the application of translational loads. Using this system, the humeral head maintained a concentric position against the glenoid fossa during glenohumeral joint motion. Tested Muscles In previous reports, the subscapularis muscle was studied by dividing the muscle into more than 2 fiber groups.2,7,22-24 In this study, we divided the muscle into 3 fiber groups from the upper third to the lower third of the muscle fiber; the groups thus formed were upper, middle, and lower fiber groups. Measurement Devices We recorded the strain on each muscle fiber group using 3 precise displacement sensors, each consisting of a coil sensor and a brass pipeb (fig 2). This instrument was described in a previous study.25 The nonlinearity was .25% of full scale and the range of measurement was 14mm. To accurately reflect the shortening and stretching behavior of the muscle, the sensors with 12-mm-long barbed points were mounted on the center of
Fig 1. Schematic representation of the experimental setup. A shoulder specimen was mounted vertically on a wood jig. Precise displacement sensors (Pulse-Coderb) were attached to the upper, middle, and lower fiber groups of the subscapularis muscle. 3SPACE sensorsc were attached to the acromion and humerus.
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Fig 2. Photograph and diagram of the Pulse Coder. (A) The PulseCoder, which was aligned with the muscle fibers, was used to measure the strain on the muscles by determining the changes in the length between specified points. (B) The 4 fishhook-like barbed points, which were inserted in the middle of the muscle, prevented the sensor from slipping out of the muscle.
each muscle belly oriented parallel to the muscle fiber. The center of each muscle belly was determined by measuring its length and width with a caliper. The fishhook-like barbed points attached to each coil sensor and brass pipe prevented the sensors from slipping out of the muscle. The changes in the length between the points of the coil sensor and the brass pipe enabled the measurement of strain on the muscles by the sensor. A 6-degree-of-freedom electromagnetic tracking devicec was used for the measurement and monitoring of the precise glenohumeral angles. This device enabled the measurement of the 3-dimensional position and orientation of the sensors relative to the absolute coordination generated by the source. One of the 2 sensors was placed on the acromion and the other was placed on the middle portion of the humerus (see fig 1). Within a 750-mm range from the source, the positional accuracy was 0.8-mm root mean square (RMS), and the angular accuracy was 0.5° RMS. Experimental Procedure Neutral position was defined as 30° of external rotation at 0° of elevation in the glenohumeral angle simulating 0° of elevation and neutral rotation of the in vivo shoulder angle, because the scapula internally tilts by 30° relative to the coronal plane in vivo.19 The strain on each muscle fiber during neutral rotation was recorded as 0% strain. The strain on each muscle was measured at the full range of internal rotation and external rotation in 0°, 30°, 60°, and 90° of glenohumeral elevation in the scapular plane (elevation), 60° of glenohumeral elevation in the sagittal plane (flexion), and 60° of glenohumeral elevation in the coronal plane (abduction). In addition, the strain was measured during neutral and external
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STRAIN ON THE SUBSCAPULARIS MUSCLE, Muraki
Fig 3. The arm elevation positions used in this measurement: (A) scapular plane and (B) axial plane. In the globe graph, longitudinal lines represent the angle of the elevation plane and latitudinal lines represent the elevation angles.
rotations in horizontal abduction, where subscapularis muscle injuries commonly occur7 (fig 3). The glenohumeral elevation angle differs from the shoulder elevation angle. In vivo, the scapula is laterally rotated by 30° during 90° of arm elevation.26 Hence, 60° and 90° of elevations used in this experiment corresponded to 90° and 150° of arm elevation in vivo. Therefore, rotation and abduction at 60° of elevation in this experiment corresponded to the rotation at 90° of elevation and horizontal abduction of the in vivo shoulder angle, respectively. The angle between the plane of the glenoid fossa and the longitudinal axis of the humerus was used to measure the glenohumeral elevation and horizontal abduction. The glenohumeral rotation angle was defined as the angle formed by the rotation of the humerus along the longitudinal axis. We performed the measurements 3 times for each glenohumeral joint position. After the passive motion of the glenohumeral joint had reached the end of the range of motion (ROM), each position was maintained for more than 10 seconds until no increase or decrease of strain values was observed. The measurement order was randomized to eliminate the order effect of joint position. Data Analysis In the first step, the length between the barbed points of the coil sensor and the brass pipe on the sensors at the neutral glenohumeral position was recorded. When the muscles were stretched for 10 seconds, the longitudinal displacement of the sensors in the measurement area of each muscle was recorded. The displacement was defined as the change in length from the neutral position. The strain on each muscle was calculated by the following formula: Strain (%) ⫽ ⌬L (mm) ⁄ L (mm) ⫻ 100 where L is the length between the points at the neutral position and ⌬L is the displacement from the neutral position. We calculated the mean values and standard deviations (SDs) of the ROM and strain at each glenohumeral joint position. Statistical analysis was performed using SPSSd for Windows. One-way repeated-measures analysis of variance (ANOVA) was used to determine the difference of the range of external and internal rotation among their 7 positions and 6 positions, respectively. The differences of the strain among glenohumeral joint positions and muscle fiber groups were determined with mixed design 2-way ANOVA. A post hoc Dunnett multiple comparisons test was conducted to detect the
glenohumeral joint positions that showed significantly greater strain than that observed at the neutral position. If this test detected 2 or more glenohumeral joint positions, a paired t test with a Bonferroni adjustment of ␣ was used to test the significant differences among these positions. For the significant difference among the muscle fiber groups, only a Bonferroni multiple comparisons test was used as a post hoc test. Statistical significance was set at the .05 ␣ level. RESULTS The mean range of each glenohumeral joint motion and SD measured by the electromagnetic device are represented in table 1. In terms of the extent of the mean range of external rotation, the position that obtained the largest mean range was the 60° abduction position, which was followed by 30° and 60° of elevations. Although the difference among the positions was significant (P⬍.001), the position in which the range was the largest was not statistically detected. The mixed design 2-way ANOVA showed that there was a significant interaction between joint position and muscle fiber group, indicating the difference of the strain pattern between the 3 muscle fiber groups (P⬍.001). Upper Fiber Group The mean strain in external rotation at 0° of elevation was the largest, followed by the strain in external rotation at 30° of elevation (fig 4). The mean strain decreased from the neutral position when the glenohumeral joint was elevated by more
Table 1: The Glenohumeral Joint ROM Measured by the Electromagnetic Device Used in This Study External Rotation (deg)
Internal Rotation (deg)
53.6⫾21.8 66.3⫾14.0 63.0⫾26.2 26.1⫾11.9 52.1⫾33.0 70.1⫾32.9
45.2⫾14.3 44.5⫾21.2 31.5⫾21.5 17.7⫾18.8 31.5⫾15.1 19.4⫾18.3
ROM
Neutral Rotation (deg)
External Rotation (deg)
Horizontal abduction
46.1⫾14.6
25.2⫾10.2
ROM
Elevation 0° Elevation 30° Elevation 60° Elevation 90° Flexion 60° Abduction 60°
NOTE. Values are mean range of the glenohumeral joint motion ⫾ SD.
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Fig 4. Strain on the following upper fiber groups of the subscapularis muscle at each glenohumeral joint position. Values are mean ⴞ SD. Abbreviations: Abd, abduction; Elev, elevation; ER, external rotation; Flex, flexion; H. Abd, horizontal abduction; IR, internal rotation.
Fig 6. Strain on the following lower fiber groups of the subscapularis muscle at each glenohumeral joint position. Values are mean ⴞ SD. *Position showed a significantly greater strain than the neutral position (P<.05). Abbreviations: see fig 4.
than 60° despite the direction of the rotation and elevation plane (ie, flexion, abduction). The main effect of glenohumeral joint position was not significant (P⫽.143).
rotation positions. In addition, neutral rotation at horizontal abduction and even internal rotations at 90° of elevation, 60° of flexion, and 60° of abduction showed positive strain.
Middle Fiber Group The middle fiber group showed a similar strain pattern to the upper fiber group except for external rotation in horizontal abduction, which showed positive strain (fig 5). The strains in external rotation at 0° and 30° of elevations remained positive, and the elevation angle that showed the largest mean strain shifted to 30°. Although the main effect of glenohumeral joint position was significant (P⫽.019), no position showed significantly larger strain compared with the neutral position.
Differences in Strain Among the 3 Fiber Groups Except at 0° of elevation, all other external rotation positions showed significantly larger strain on the lower fiber group (13.4% to 26.6%) compared with the upper (P⬍.005) and middle fiber groups (⫺11.5% to 4.2%) (P⬍.005). There were no significant differences between the upper and middle fiber groups in all positions (P range, 0.408⫺1.000).
Lower Fiber Group All external rotations showed positive strain (fig 6). The main effect of glenohumeral joint position was significant (P⬍.001). The strain values in external rotation at 30° (P⬍.001), 60° (P⬍.001), and 90° (P⬍.01) of elevation and 60° of flexion (P⬍.001), 60° of abduction (P⬍.001), and horizontal abduction (P⬍.001) were significantly larger than that at the neutral position. However, external rotation at 0° (P⫽.106) did not show a significant increase in strain. Although external rotation at horizontal abduction showed the greatest mean strain, this was not significantly larger than the other external
Fig 5. Strain on the following middle fiber groups of the subscapularis muscle at each glenohumeral joint position. Values are mean ⴞ SD. Abbreviations: see fig 4.
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DISCUSSION In this cadaveric study, except 0° and 30° of elevations, no external rotations showed positive strains on the upper and middle fiber groups of the subscapularis, whereas all external rotations produced positive strain on the lower fiber group. The subscapularis is the primary internal rotator of the glenohumeral joint.27,28 For physiologic motion, it is believed that glenohumeral internal rotation shortens the muscle and external rotation lengthens it under active muscle contractions. However, this seemed to be different from the muscle behavior of the upper and middle fiber groups in the cadaveric glenohumeral joint. The subscapularis is a wide and flat multipennate muscle that extends from the medial border of the scapula to the lesser tuberosity of the humerus. Its upper fiber group is inferolaterally oriented from the medial border of the scapula, whereas its lower fiber group is superolaterally oriented. These anatomic features may explain the manner in which the stretching behavior of each fiber group changed as the elevation angle in the glenohumeral joint increased. This study clarified that the external rotation at 30°, 60°, and 90° of elevation and flexion, abduction, and horizontal abduction significantly stretched the lower fiber group. On the other hand, only a small amount of positive strain on the upper and middle fiber groups was observed in external rotation with 0° and 30° of elevation. For in vivo stretching positions of the subscapularis muscle, Evjenth and Hamberg17 advocated only external rotation at 90° of shoulder abduction. Houglum,18 in her textbook, described the external rotation at maximum shoulder elevation as the stretching position. Ekstrom and Osborn16 introduced external rotation at 0° of shoulder elevation as a position that tests the length of the subscapularis
STRAIN ON THE SUBSCAPULARIS MUSCLE, Muraki
muscle. Our findings suggest that these stretching positions may stretch different muscle fiber groups of the subscapularis. In external rotation at 30° of glenohumeral elevation, significantly large muscle strain on the lower fiber group and positive muscle strain on the upper and middle fiber groups were observed simultaneously. For patients with limited glenohumeral motion, for example, periarthritis of the shoulder, external rotation at greater than 60° of glenohumeral abduction is supposed to be inadequate as a stretching position for the subscapularis muscle. Instead, external rotation at 30° of glenohumeral elevation is considered to be the possible stretching position. External rotation at horizontal abduction showed small or negative strain on the upper and middle fiber groups. Based on clinical reports, the upper part of the subscapularis tendon is frequently torn by forcible external rotation at horizontal abduction.7-10 The small muscle strain on the upper and middle fiber groups in this study may explain the observation that the upper two thirds of the muscle is vulnerable to forcible external rotation at horizontal abduction. Another possible reason for the very small amount of muscle strain on the upper and middle fiber groups in external rotation is the difference in function between the upper two-thirds group and the lower fiber group.22,23 Because the subscapularis muscle has been reported to stabilize the humeral head during the glenohumeral joint motion29 and restrain excessive external rotation in horizontal extension,30,31 the upper and middle fiber groups may play an important role on the former function and lower fiber group may play the latter function. Study Limitations There are a few limitations of this study. First, because the shoulder specimens were harvested from aged cadavers, the ROM and mechanical properties of the specimens might differ from those of specimens from younger people in whom recurrent shoulder dislocation or subscapularis tendon tear tend to occur. Second, in the present study, we measured only the glenohumeral joint in vitro, whereas the shoulder positions were usually determined based on the in vivo scapular positions in the coronal and horizontal planes in the thorax. Our findings may be slightly different from the in vivo studies because we did not consider the scapular position in the sagittal plane. CONCLUSIONS The stretching position of each fiber group of the subscapularis differs depending on the glenohumeral joint positions. External rotation at 30° to 60° of glenohumeral elevation including abduction, flexion, and horizontal abduction can stretch the lower fiber group of the subscapularis muscle. These findings may be applied to the stretching of the subscapularis muscle in order to improve its flexibility and reduce muscle damage. Acknowledgments: We thank Tomoya Miyasaka, PhD, for his technical assistance. This study is part of the doctoral thesis submitted to the Graduate School of Health Sciences. References 1. Decker MJ, Tokish JM, Ellis HB, Torry MR, Hawkins RJ. Subscapularis muscle activity during selected rehabilitation exercises. Am J Sports Med 2003;31:126-34. 2. Glousman R, Jobe F, Tibone J, Moynes D, Antonelli D, Perry J. Dynamic electromyographic analysis of the throwing shoulder with glenohumeral instability. J Bone Joint Surg Am 1988;70: 220-6.
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3. Jobe FW, Tibone JE, Perry J, Moynes D. An EMG analysis of the shoulder in throwing and pitching. A preliminary report. Am J Sports Med 1983;11:3-5. 4. Cleeman E, Brunelli M, Gothelf T, Hayes P, Flatow EL. Releases of subscapularis contracture: an anatomic and clinical study. J Shoulder Elbow Surg 2003;12:231-6. 5. Ogilvie-Harris DJ, Biggs DJ, Fitsialos DP, MacKay M. The resistant frozen shoulder. Manipulation versus arthroscopic release. Clin Orthop Relat Res 1995;Oct(319):238-48. 6. Pearsall AW, Osbahr DC, Speer KP. An arthroscopic technique for treating patients with frozen shoulder. Arthroscopy 1999;15: 2-11. 7. Deutsch A, Altchek DW, Veltri DM, Potter HG, Warren RF. Traumatic tears of the subscapularis tendon. Clinical diagnosis, magnetic resonance imaging findings, and operative treatment. Am J Sports Med 1997;25:13-22. 8. Edwards TB, Walch G, Sirveaux F, et al. Repair of tears of the subscapularis. J Bone Joint Surg Am 2005;87:725-30. 9. Gerber C, Krushell RJ. Isolated rupture of the tendon of the subscapularis muscle. Clinical features in 16 cases. J Bone Joint Surg Br 1991;73:389-94. 10. Gerber C, Hersche O, Farron A. Isolated rupture of the subscapularis tendon. J Bone Joint Surg Am 1996;78:1015-23. 11. Yoshikawa GI, Hori K, Kaneko H, Matsusue Y, Murakami M. Acute subscapularis tendon rupture caused by throwing: a case report. J Shoulder Elbow Surg 2005;14:218-20. 12. Moseley HF, Overgaard B. The anterior capsular mechanism in recurrent anterior dislocation of the shoulder: morphological and clinical studies with special reference to the glenoid labrum and the glenohumeral ligaments. J Bone Joint Surg Br 1962;48: 913-27. 13. Yanagisawa O, Niitsu M, Takahashi H, Itai Y. Magnetic resonance imaging of the rotator cuff muscles after baseball pitching. J Sports Med Phys Fitness 2003;43:493-9. 14. Bohannon RW, Larkin PA. Passive ankle dorsiflexion increases in patients after a regimen of tilt table-wedge board standing. A clinical report. Phys Ther 1985;65:1676-8. 15. American College of Sports Medicine. The recommended quantity and quality of exercise for developing and maintaining cardiorespiratory and muscular fitness and flexibility in healthy adults. Med Sci Sports Exerc 1998;30:975-91. 16. Ekstrom RA, Osborn RW. Muscle length testing and electromyographic data for manual strength testing and exercise for the shoulder. In: Donatelli RA, editor. Physical therapy of the shoulder. 4th ed. St. Louis: Churchill Livingstone; 2004. p 440-1. 17. Evjenth O, Hamberg J. Muscle stretching in manual therapy: a clinical manual. Vol 1: the extremities. Alfta: Alfta Rehab Forlag; 1984. 18. Houglum PA. Therapeutic exercise for athletic injuries. Champaign: Human Kinetics; 2001. 19. Culham E, Peat M. Functional anatomy of shoulder complex. J Orthop Sports Phys Ther 1993;18:342-50. 20. Tibone JE, McMahon PJ, Shrader TA, Sandusky MD, Lee TQ. Glenohumeral joint translation after arthroscopic, nonablative, thermal capsuloplasty with a laser. Am J Sports Med 1998;26: 495-8. 21. Warner JJ, Deng XH, Warren RF, Torzilli PA. Static capsuloligamentous restraints to superior-inferior translation of the glenohumeral joint. Am Sports Med 1992;20:675-85. 22. Kadaba MP, Cole A, Wootten ME, et al. Intramuscular wire electromyography of the subscapularis. J Orthop Res 1992;10: 394-7. 23. Kato K. Innervation of the scapular muscles and its morphological significance in man. Anat Anz 1989;168:155-68. Arch Phys Med Rehabil Vol 88, July 2007
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24. Suenaga N, Minami A, Fujisawa H. Electromyographic analysis of internal rotational motion of the shoulder in various arm positions. J Shoulder Elbow Surg 2003;12:501-5. 25. Muraki T, Aoki M, Uchiyama E, Murakami G, Miyamoto S. The effect of arm position on stretching of the supraspinatus, infraspinatus, and posterior portion of deltoid muscles: a cadaveric study. Clin Biomech (Bristol, Avon) 2006;21:474-80. 26. Poppen NK, Walker PS. Normal and abnormal motion of the shoulder. J Bone Joint Surg Am 1976;58:195-201. 27. Inman VT, Saunders JB, Abbott LC. Observations of the function of the shoulder joint. J Bone Joint Surg Am 1944;26:1-30. 28. Kuechle DK, Newman SR, Itoi E, Niebur GL, Morrey BF, An KN. The relevance of the moment arm of shoulder muscles with respect to axial rotation of the glenohumeral joint in four positions. Clin Biomech (Bristol, Avon) 2000;15:322-9. 29. Lee SB, Kim KJ, O’Driscoll SW, Morrey BF, An KN. Dynamic glenohumeral stability provided by the rotator cuff muscles in the mid-range and end-range of motion. J Bone Joint Surg Am 2000; 82:849-57.
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30. Glousman R, Jobe F, Tibone J, Moynes D, Antonelli D, Perry J. Dynamic electromyographic analysis of the throwing shoulder with glenohumeral instability. J Bone Joint Surg Am 1988;70: 220-6. 31. Kuhn JE, Huston LJ, Soslowsky LJ, Shyr Y, Blasier RB. External rotation of the glenohumeral joint: ligament restraints and muscle effects in the neutral and abducted positions. J Shoulder Elbow Surg 2005;14(1 Suppl S):39S-48S. Suppliers a. Fastin RC; DePuy Mitek Inc, 3-2 Toyo 6-chome, Koto-ku, Tokyo 135-0016, Japan. b. Pulse-Coder; LEVEX Corp, 102 Gshonouchiminami-cho, Shomokyo-ku 7, Kyoto 600-8864, Japan. c. 3SPACE FASTRAK; Polhemus Inc, 40 Hercules Dr, Colchester, VT 05446. d. Version 11.5J; SPSS Japan Inc, 10F Ebisu Prime Square Tower 1-1-39 Hiroo, Shibuya-ku Tokyo 150-0021, Japan.
ORIGINAL ARTICLE
A Cadaveric Study of Strain on the Subscapularis Muscle Takayuki Muraki, PT, PhD, Mitsuhiro Aoki, MD, PhD, Eiichi Uchiyama, MD, PhD, Hiroshi Takasaki, PT, MS, Gen Murakami, MD, PhD, Shigenori Miyamoto, PT, PhD ABSTRACT. Muraki T, Aoki M, Uchiyama E, Takasaki H, Murakami G, Miyamoto S. A cadaveric study of strain on the subscapularis muscle. Arch Phys Med Rehabil 2007;88:941-6. Objectives: To measure the strain on 3 fiber groups of the subscapularis muscle at various glenohumeral joint positions and to determine the appropriate shoulder position for subscapularis muscle stretching. Design: Repeated-measures design. Setting: Biomechanics laboratory. Specimens: Nine frozen-thawed glenohumeral joints obtained from 9 fresh cadavers. Interventions: Not applicable. Main Outcome Measure: The strain on the upper, middle, and lower fiber groups of the subscapularis were measured by precise displacement sensors during 14 different glenohumeral joint positions. Results: The glenohumeral joint position that showed the largest strain varied among the 3 fiber groups. Although no position showed significantly large strain on the upper and middle fiber groups, external rotation at 30°, 60°, and 90° of elevation, abduction, flexion, and horizontal abduction revealed significantly greater strain on the lower fiber groups (P⬍.005). Additionally, except for external rotation at 0° of elevation, the strain on the lower fiber group was significantly greater than that on the upper and middle fiber groups in external rotation (P⬍.005). Conclusions: The stretching position of each fiber group of the subscapularis differs depending on the glenohumeral joint position. External rotation at 30° to 60° of glenohumeral elevation, abduction, flexion, and horizontal abduction can significantly stretch the lower fiber group of the subscapularis muscle. Key Words: Cadaver; Muscles; Rehabilitation; Sprains and strains. © 2007 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation UNCTIONS OF THE SUBSCAPULARIS muscle, such as flexibility and strength, are essential for the normal shoulF der motion required for daily activities and for the high per-
formance necessitated by overhead sports.1-3 The flexibility of the muscle could be reduced due to muscle contracture.4-6 Moreover, the subscapularis muscle strength has been reported
From the Doctoral Course of Physical Therapy, Graduate School of Health Sciences, Sapporo Medical University, Sapporo, Japan (Muraki, Takasaki); and Departments of Physical Therapy (Aoki, Miyamoto) and Anatomy (Uchiyama, Murakami), Sapporo Medical University School of Health Sciences, Sapporo, Japan. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to Takayuki Muraki, PT, PhD, Doctoral Course of Physical Therapy, Graduate School of Health Sciences, Sapporo Medical University, South-1, West-17, Chuo-ku, Sapporo, Japan, e-mail: [email protected]. 0003-9993/07/8807-11250$32.00/0 doi:10.1016/j.apmr.2007.04.003
to be compromised by subscapularis tendon tear7-11 and muscle damage due to repetitive overload.12,13 In rehabilitation, muscle stretching is an important technique for restoring the flexibility of shortened musculotendinous units.14 This technique is also frequently used as part of both warming-up and cooling-down procedures in order to prevent muscle injury while participating in sports-related activities.15 If it is applied effectively, muscle injury occurring during strenuous activities may be avoided. Generally, the most effective shoulder position for stretching the subscapularis muscle is considered to be unclear. Although, based on the anatomic characteristics of the subscapularis muscle, some authors have reported the use of shoulder external rotation for the selective stretching positions of the subscapularis muscle; other authors have reported the use of other shoulder elevation angles at which the external rotation was performed.16-18 For example, Ekstrom and Osborn16 introduced external rotation at 0° of shoulder elevation for the selective stretching positions of the subscapularis, whereas Houglum18 used external rotation at the maximum shoulder elevation. Furthermore, Evjenth and Hamberg17 advocated the application of external rotation at 90° of shoulder elevation in the coronal plane. Identifying the shoulder position for the stretching is difficult because the “shoulder” includes 4 mobile joints, the glenohumeral, acromioclavicular, sternoclavicular, and scapulothoracic joints, as well as many muscles. Because the subscapularis muscle connects the scapula and humerus, at least the glenohumeral joint position for the subscapularis stretching should be identified. In addition, the subscapularis muscle consists of muscle fibers oriented in different directions. The stretching position of each muscle fiber group may be different. To overcome the discrepancies of subscapularis stretching position, the glenohumeral joint positions that effectively stretch the subscapularis muscle should be determined quantitatively by directly observing the strain on each muscle fiber group. For this purpose, direct measurement of the muscle strain by using cadaveric glenohumeral joints is useful. Although the measurement of physiologic strain with muscle contraction or tension is impossible in this method, engineering strain can be measured and be compared between various glenohumeral joint positions because the construction of the cadaveric and in vivo glenohumeral joints is the same. The purpose of this study was to determine the appropriate glenohumeral joint position for the effective stretching of the subscapularis muscle by measuring the strain on each subscapularis muscle fiber group at various glenohumeral joint positions. METHODS Preparation of the Specimen In this experiment, we used frozen glenohumeral joints (5 right and 4 left joints) without any evidence of rotator cuff tears or osteoarthritis. These were obtained from 9 fresh cadavers aged 78 to 85 years at death (average age, 80y) after acquiring informed consent prior to death. The cadaveric shoulders were kept in a freezer at ⫺20°C after disarticulating the scapula from Arch Phys Med Rehabil Vol 88, July 2007
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the thorax. The thawing of the specimens at room temperature began 12 hours prior to the experiment. Thawing was confirmed through preconditioned movement of the glenohumeral joint in all directions. We then excised the serratus anterior, latissimus dorsi, rhomboids, and levator scapulae muscles. The distal third of the humerus was exposed. To control the rotational angle of the humerus, an acrylic stick was inserted perpendicular to the shaft, which denoted the longitudinal axis of the forearm at 90° of elbow flexion. Next, the humerus was amputated above the elbow. Throughout the experiment, which was performed at room temperature (22°C), the specimens were kept moist by spraying saline solution every 5 to 10 minutes. In this experiment, we used a wood jig consisting of a wood board and a square timber. The scapula was fixed to the wood jig such that the medial border of the scapula was perpendicular to the ground19 (fig 1). Two threaded anchorsa were inserted into the bony insertions of the infraspinatus and subscapularis tendons such that a compressive force of 11N could be applied to each thread (total, 22N) against the glenoid fossa. In previous cadaveric studies,20,21 this compressive force was used as the minimum force required preventing subluxation of the humeral head on the application of translational loads. Using this system, the humeral head maintained a concentric position against the glenoid fossa during glenohumeral joint motion. Tested Muscles In previous reports, the subscapularis muscle was studied by dividing the muscle into more than 2 fiber groups.2,7,22-24 In this study, we divided the muscle into 3 fiber groups from the upper third to the lower third of the muscle fiber; the groups thus formed were upper, middle, and lower fiber groups. Measurement Devices We recorded the strain on each muscle fiber group using 3 precise displacement sensors, each consisting of a coil sensor and a brass pipeb (fig 2). This instrument was described in a previous study.25 The nonlinearity was .25% of full scale and the range of measurement was 14mm. To accurately reflect the shortening and stretching behavior of the muscle, the sensors with 12-mm-long barbed points were mounted on the center of
Fig 1. Schematic representation of the experimental setup. A shoulder specimen was mounted vertically on a wood jig. Precise displacement sensors (Pulse-Coderb) were attached to the upper, middle, and lower fiber groups of the subscapularis muscle. 3SPACE sensorsc were attached to the acromion and humerus.
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Fig 2. Photograph and diagram of the Pulse Coder. (A) The PulseCoder, which was aligned with the muscle fibers, was used to measure the strain on the muscles by determining the changes in the length between specified points. (B) The 4 fishhook-like barbed points, which were inserted in the middle of the muscle, prevented the sensor from slipping out of the muscle.
each muscle belly oriented parallel to the muscle fiber. The center of each muscle belly was determined by measuring its length and width with a caliper. The fishhook-like barbed points attached to each coil sensor and brass pipe prevented the sensors from slipping out of the muscle. The changes in the length between the points of the coil sensor and the brass pipe enabled the measurement of strain on the muscles by the sensor. A 6-degree-of-freedom electromagnetic tracking devicec was used for the measurement and monitoring of the precise glenohumeral angles. This device enabled the measurement of the 3-dimensional position and orientation of the sensors relative to the absolute coordination generated by the source. One of the 2 sensors was placed on the acromion and the other was placed on the middle portion of the humerus (see fig 1). Within a 750-mm range from the source, the positional accuracy was 0.8-mm root mean square (RMS), and the angular accuracy was 0.5° RMS. Experimental Procedure Neutral position was defined as 30° of external rotation at 0° of elevation in the glenohumeral angle simulating 0° of elevation and neutral rotation of the in vivo shoulder angle, because the scapula internally tilts by 30° relative to the coronal plane in vivo.19 The strain on each muscle fiber during neutral rotation was recorded as 0% strain. The strain on each muscle was measured at the full range of internal rotation and external rotation in 0°, 30°, 60°, and 90° of glenohumeral elevation in the scapular plane (elevation), 60° of glenohumeral elevation in the sagittal plane (flexion), and 60° of glenohumeral elevation in the coronal plane (abduction). In addition, the strain was measured during neutral and external
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Fig 3. The arm elevation positions used in this measurement: (A) scapular plane and (B) axial plane. In the globe graph, longitudinal lines represent the angle of the elevation plane and latitudinal lines represent the elevation angles.
rotations in horizontal abduction, where subscapularis muscle injuries commonly occur7 (fig 3). The glenohumeral elevation angle differs from the shoulder elevation angle. In vivo, the scapula is laterally rotated by 30° during 90° of arm elevation.26 Hence, 60° and 90° of elevations used in this experiment corresponded to 90° and 150° of arm elevation in vivo. Therefore, rotation and abduction at 60° of elevation in this experiment corresponded to the rotation at 90° of elevation and horizontal abduction of the in vivo shoulder angle, respectively. The angle between the plane of the glenoid fossa and the longitudinal axis of the humerus was used to measure the glenohumeral elevation and horizontal abduction. The glenohumeral rotation angle was defined as the angle formed by the rotation of the humerus along the longitudinal axis. We performed the measurements 3 times for each glenohumeral joint position. After the passive motion of the glenohumeral joint had reached the end of the range of motion (ROM), each position was maintained for more than 10 seconds until no increase or decrease of strain values was observed. The measurement order was randomized to eliminate the order effect of joint position. Data Analysis In the first step, the length between the barbed points of the coil sensor and the brass pipe on the sensors at the neutral glenohumeral position was recorded. When the muscles were stretched for 10 seconds, the longitudinal displacement of the sensors in the measurement area of each muscle was recorded. The displacement was defined as the change in length from the neutral position. The strain on each muscle was calculated by the following formula: Strain (%) ⫽ ⌬L (mm) ⁄ L (mm) ⫻ 100 where L is the length between the points at the neutral position and ⌬L is the displacement from the neutral position. We calculated the mean values and standard deviations (SDs) of the ROM and strain at each glenohumeral joint position. Statistical analysis was performed using SPSSd for Windows. One-way repeated-measures analysis of variance (ANOVA) was used to determine the difference of the range of external and internal rotation among their 7 positions and 6 positions, respectively. The differences of the strain among glenohumeral joint positions and muscle fiber groups were determined with mixed design 2-way ANOVA. A post hoc Dunnett multiple comparisons test was conducted to detect the
glenohumeral joint positions that showed significantly greater strain than that observed at the neutral position. If this test detected 2 or more glenohumeral joint positions, a paired t test with a Bonferroni adjustment of ␣ was used to test the significant differences among these positions. For the significant difference among the muscle fiber groups, only a Bonferroni multiple comparisons test was used as a post hoc test. Statistical significance was set at the .05 ␣ level. RESULTS The mean range of each glenohumeral joint motion and SD measured by the electromagnetic device are represented in table 1. In terms of the extent of the mean range of external rotation, the position that obtained the largest mean range was the 60° abduction position, which was followed by 30° and 60° of elevations. Although the difference among the positions was significant (P⬍.001), the position in which the range was the largest was not statistically detected. The mixed design 2-way ANOVA showed that there was a significant interaction between joint position and muscle fiber group, indicating the difference of the strain pattern between the 3 muscle fiber groups (P⬍.001). Upper Fiber Group The mean strain in external rotation at 0° of elevation was the largest, followed by the strain in external rotation at 30° of elevation (fig 4). The mean strain decreased from the neutral position when the glenohumeral joint was elevated by more
Table 1: The Glenohumeral Joint ROM Measured by the Electromagnetic Device Used in This Study External Rotation (deg)
Internal Rotation (deg)
53.6⫾21.8 66.3⫾14.0 63.0⫾26.2 26.1⫾11.9 52.1⫾33.0 70.1⫾32.9
45.2⫾14.3 44.5⫾21.2 31.5⫾21.5 17.7⫾18.8 31.5⫾15.1 19.4⫾18.3
ROM
Neutral Rotation (deg)
External Rotation (deg)
Horizontal abduction
46.1⫾14.6
25.2⫾10.2
ROM
Elevation 0° Elevation 30° Elevation 60° Elevation 90° Flexion 60° Abduction 60°
NOTE. Values are mean range of the glenohumeral joint motion ⫾ SD.
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Fig 4. Strain on the following upper fiber groups of the subscapularis muscle at each glenohumeral joint position. Values are mean ⴞ SD. Abbreviations: Abd, abduction; Elev, elevation; ER, external rotation; Flex, flexion; H. Abd, horizontal abduction; IR, internal rotation.
Fig 6. Strain on the following lower fiber groups of the subscapularis muscle at each glenohumeral joint position. Values are mean ⴞ SD. *Position showed a significantly greater strain than the neutral position (P<.05). Abbreviations: see fig 4.
than 60° despite the direction of the rotation and elevation plane (ie, flexion, abduction). The main effect of glenohumeral joint position was not significant (P⫽.143).
rotation positions. In addition, neutral rotation at horizontal abduction and even internal rotations at 90° of elevation, 60° of flexion, and 60° of abduction showed positive strain.
Middle Fiber Group The middle fiber group showed a similar strain pattern to the upper fiber group except for external rotation in horizontal abduction, which showed positive strain (fig 5). The strains in external rotation at 0° and 30° of elevations remained positive, and the elevation angle that showed the largest mean strain shifted to 30°. Although the main effect of glenohumeral joint position was significant (P⫽.019), no position showed significantly larger strain compared with the neutral position.
Differences in Strain Among the 3 Fiber Groups Except at 0° of elevation, all other external rotation positions showed significantly larger strain on the lower fiber group (13.4% to 26.6%) compared with the upper (P⬍.005) and middle fiber groups (⫺11.5% to 4.2%) (P⬍.005). There were no significant differences between the upper and middle fiber groups in all positions (P range, 0.408⫺1.000).
Lower Fiber Group All external rotations showed positive strain (fig 6). The main effect of glenohumeral joint position was significant (P⬍.001). The strain values in external rotation at 30° (P⬍.001), 60° (P⬍.001), and 90° (P⬍.01) of elevation and 60° of flexion (P⬍.001), 60° of abduction (P⬍.001), and horizontal abduction (P⬍.001) were significantly larger than that at the neutral position. However, external rotation at 0° (P⫽.106) did not show a significant increase in strain. Although external rotation at horizontal abduction showed the greatest mean strain, this was not significantly larger than the other external
Fig 5. Strain on the following middle fiber groups of the subscapularis muscle at each glenohumeral joint position. Values are mean ⴞ SD. Abbreviations: see fig 4.
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DISCUSSION In this cadaveric study, except 0° and 30° of elevations, no external rotations showed positive strains on the upper and middle fiber groups of the subscapularis, whereas all external rotations produced positive strain on the lower fiber group. The subscapularis is the primary internal rotator of the glenohumeral joint.27,28 For physiologic motion, it is believed that glenohumeral internal rotation shortens the muscle and external rotation lengthens it under active muscle contractions. However, this seemed to be different from the muscle behavior of the upper and middle fiber groups in the cadaveric glenohumeral joint. The subscapularis is a wide and flat multipennate muscle that extends from the medial border of the scapula to the lesser tuberosity of the humerus. Its upper fiber group is inferolaterally oriented from the medial border of the scapula, whereas its lower fiber group is superolaterally oriented. These anatomic features may explain the manner in which the stretching behavior of each fiber group changed as the elevation angle in the glenohumeral joint increased. This study clarified that the external rotation at 30°, 60°, and 90° of elevation and flexion, abduction, and horizontal abduction significantly stretched the lower fiber group. On the other hand, only a small amount of positive strain on the upper and middle fiber groups was observed in external rotation with 0° and 30° of elevation. For in vivo stretching positions of the subscapularis muscle, Evjenth and Hamberg17 advocated only external rotation at 90° of shoulder abduction. Houglum,18 in her textbook, described the external rotation at maximum shoulder elevation as the stretching position. Ekstrom and Osborn16 introduced external rotation at 0° of shoulder elevation as a position that tests the length of the subscapularis
STRAIN ON THE SUBSCAPULARIS MUSCLE, Muraki
muscle. Our findings suggest that these stretching positions may stretch different muscle fiber groups of the subscapularis. In external rotation at 30° of glenohumeral elevation, significantly large muscle strain on the lower fiber group and positive muscle strain on the upper and middle fiber groups were observed simultaneously. For patients with limited glenohumeral motion, for example, periarthritis of the shoulder, external rotation at greater than 60° of glenohumeral abduction is supposed to be inadequate as a stretching position for the subscapularis muscle. Instead, external rotation at 30° of glenohumeral elevation is considered to be the possible stretching position. External rotation at horizontal abduction showed small or negative strain on the upper and middle fiber groups. Based on clinical reports, the upper part of the subscapularis tendon is frequently torn by forcible external rotation at horizontal abduction.7-10 The small muscle strain on the upper and middle fiber groups in this study may explain the observation that the upper two thirds of the muscle is vulnerable to forcible external rotation at horizontal abduction. Another possible reason for the very small amount of muscle strain on the upper and middle fiber groups in external rotation is the difference in function between the upper two-thirds group and the lower fiber group.22,23 Because the subscapularis muscle has been reported to stabilize the humeral head during the glenohumeral joint motion29 and restrain excessive external rotation in horizontal extension,30,31 the upper and middle fiber groups may play an important role on the former function and lower fiber group may play the latter function. Study Limitations There are a few limitations of this study. First, because the shoulder specimens were harvested from aged cadavers, the ROM and mechanical properties of the specimens might differ from those of specimens from younger people in whom recurrent shoulder dislocation or subscapularis tendon tear tend to occur. Second, in the present study, we measured only the glenohumeral joint in vitro, whereas the shoulder positions were usually determined based on the in vivo scapular positions in the coronal and horizontal planes in the thorax. Our findings may be slightly different from the in vivo studies because we did not consider the scapular position in the sagittal plane. CONCLUSIONS The stretching position of each fiber group of the subscapularis differs depending on the glenohumeral joint positions. External rotation at 30° to 60° of glenohumeral elevation including abduction, flexion, and horizontal abduction can stretch the lower fiber group of the subscapularis muscle. These findings may be applied to the stretching of the subscapularis muscle in order to improve its flexibility and reduce muscle damage. Acknowledgments: We thank Tomoya Miyasaka, PhD, for his technical assistance. This study is part of the doctoral thesis submitted to the Graduate School of Health Sciences. References 1. Decker MJ, Tokish JM, Ellis HB, Torry MR, Hawkins RJ. Subscapularis muscle activity during selected rehabilitation exercises. Am J Sports Med 2003;31:126-34. 2. Glousman R, Jobe F, Tibone J, Moynes D, Antonelli D, Perry J. Dynamic electromyographic analysis of the throwing shoulder with glenohumeral instability. J Bone Joint Surg Am 1988;70: 220-6.
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3. Jobe FW, Tibone JE, Perry J, Moynes D. An EMG analysis of the shoulder in throwing and pitching. A preliminary report. Am J Sports Med 1983;11:3-5. 4. Cleeman E, Brunelli M, Gothelf T, Hayes P, Flatow EL. Releases of subscapularis contracture: an anatomic and clinical study. J Shoulder Elbow Surg 2003;12:231-6. 5. Ogilvie-Harris DJ, Biggs DJ, Fitsialos DP, MacKay M. The resistant frozen shoulder. Manipulation versus arthroscopic release. Clin Orthop Relat Res 1995;Oct(319):238-48. 6. Pearsall AW, Osbahr DC, Speer KP. An arthroscopic technique for treating patients with frozen shoulder. Arthroscopy 1999;15: 2-11. 7. Deutsch A, Altchek DW, Veltri DM, Potter HG, Warren RF. Traumatic tears of the subscapularis tendon. Clinical diagnosis, magnetic resonance imaging findings, and operative treatment. Am J Sports Med 1997;25:13-22. 8. Edwards TB, Walch G, Sirveaux F, et al. Repair of tears of the subscapularis. J Bone Joint Surg Am 2005;87:725-30. 9. Gerber C, Krushell RJ. Isolated rupture of the tendon of the subscapularis muscle. Clinical features in 16 cases. J Bone Joint Surg Br 1991;73:389-94. 10. Gerber C, Hersche O, Farron A. Isolated rupture of the subscapularis tendon. J Bone Joint Surg Am 1996;78:1015-23. 11. Yoshikawa GI, Hori K, Kaneko H, Matsusue Y, Murakami M. Acute subscapularis tendon rupture caused by throwing: a case report. J Shoulder Elbow Surg 2005;14:218-20. 12. Moseley HF, Overgaard B. The anterior capsular mechanism in recurrent anterior dislocation of the shoulder: morphological and clinical studies with special reference to the glenoid labrum and the glenohumeral ligaments. J Bone Joint Surg Br 1962;48: 913-27. 13. Yanagisawa O, Niitsu M, Takahashi H, Itai Y. Magnetic resonance imaging of the rotator cuff muscles after baseball pitching. J Sports Med Phys Fitness 2003;43:493-9. 14. Bohannon RW, Larkin PA. Passive ankle dorsiflexion increases in patients after a regimen of tilt table-wedge board standing. A clinical report. Phys Ther 1985;65:1676-8. 15. American College of Sports Medicine. The recommended quantity and quality of exercise for developing and maintaining cardiorespiratory and muscular fitness and flexibility in healthy adults. Med Sci Sports Exerc 1998;30:975-91. 16. Ekstrom RA, Osborn RW. Muscle length testing and electromyographic data for manual strength testing and exercise for the shoulder. In: Donatelli RA, editor. Physical therapy of the shoulder. 4th ed. St. Louis: Churchill Livingstone; 2004. p 440-1. 17. Evjenth O, Hamberg J. Muscle stretching in manual therapy: a clinical manual. Vol 1: the extremities. Alfta: Alfta Rehab Forlag; 1984. 18. Houglum PA. Therapeutic exercise for athletic injuries. Champaign: Human Kinetics; 2001. 19. Culham E, Peat M. Functional anatomy of shoulder complex. J Orthop Sports Phys Ther 1993;18:342-50. 20. Tibone JE, McMahon PJ, Shrader TA, Sandusky MD, Lee TQ. Glenohumeral joint translation after arthroscopic, nonablative, thermal capsuloplasty with a laser. Am J Sports Med 1998;26: 495-8. 21. Warner JJ, Deng XH, Warren RF, Torzilli PA. Static capsuloligamentous restraints to superior-inferior translation of the glenohumeral joint. Am Sports Med 1992;20:675-85. 22. Kadaba MP, Cole A, Wootten ME, et al. Intramuscular wire electromyography of the subscapularis. J Orthop Res 1992;10: 394-7. 23. Kato K. Innervation of the scapular muscles and its morphological significance in man. Anat Anz 1989;168:155-68. Arch Phys Med Rehabil Vol 88, July 2007
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24. Suenaga N, Minami A, Fujisawa H. Electromyographic analysis of internal rotational motion of the shoulder in various arm positions. J Shoulder Elbow Surg 2003;12:501-5. 25. Muraki T, Aoki M, Uchiyama E, Murakami G, Miyamoto S. The effect of arm position on stretching of the supraspinatus, infraspinatus, and posterior portion of deltoid muscles: a cadaveric study. Clin Biomech (Bristol, Avon) 2006;21:474-80. 26. Poppen NK, Walker PS. Normal and abnormal motion of the shoulder. J Bone Joint Surg Am 1976;58:195-201. 27. Inman VT, Saunders JB, Abbott LC. Observations of the function of the shoulder joint. J Bone Joint Surg Am 1944;26:1-30. 28. Kuechle DK, Newman SR, Itoi E, Niebur GL, Morrey BF, An KN. The relevance of the moment arm of shoulder muscles with respect to axial rotation of the glenohumeral joint in four positions. Clin Biomech (Bristol, Avon) 2000;15:322-9. 29. Lee SB, Kim KJ, O’Driscoll SW, Morrey BF, An KN. Dynamic glenohumeral stability provided by the rotator cuff muscles in the mid-range and end-range of motion. J Bone Joint Surg Am 2000; 82:849-57.
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30. Glousman R, Jobe F, Tibone J, Moynes D, Antonelli D, Perry J. Dynamic electromyographic analysis of the throwing shoulder with glenohumeral instability. J Bone Joint Surg Am 1988;70: 220-6. 31. Kuhn JE, Huston LJ, Soslowsky LJ, Shyr Y, Blasier RB. External rotation of the glenohumeral joint: ligament restraints and muscle effects in the neutral and abducted positions. J Shoulder Elbow Surg 2005;14(1 Suppl S):39S-48S. Suppliers a. Fastin RC; DePuy Mitek Inc, 3-2 Toyo 6-chome, Koto-ku, Tokyo 135-0016, Japan. b. Pulse-Coder; LEVEX Corp, 102 Gshonouchiminami-cho, Shomokyo-ku 7, Kyoto 600-8864, Japan. c. 3SPACE FASTRAK; Polhemus Inc, 40 Hercules Dr, Colchester, VT 05446. d. Version 11.5J; SPSS Japan Inc, 10F Ebisu Prime Square Tower 1-1-39 Hiroo, Shibuya-ku Tokyo 150-0021, Japan.