Pectoralis Major Tendon Transfers Above or Underneath the Conjoint Tendon in Subscapularis-Deficient Shoulders: An in Vitro Biomechanical Analysis

Konrad, Gerhard G. MD; Sudkamp, Norbert P. MD; Kreuz, Peter C. MD; Jolly, John T. MS; McMahon, Patrick J. MD; Debski, Richard E. PhD

Journal of Bone & Joint Surgery - American Volume:
doi: 10.2106/JBJS.F.00811
Scientific Articles
Abstract

Background: Different operative techniques for transfer of the pectoralis major tendon have been proposed for the treatment of irreparable ruptures of the subscapularis tendon. The objective of this study was to compare the effects of two techniques of transferring the pectoralis major tendon (above or underneath the conjoint tendon) on glenohumeral kinematics during active abduction in a biomechanical model of a subscapularis-deficient shoulder.

Methods: Six shoulder specimens were tested with a custom dynamic shoulder testing apparatus. After the kinematics of the intact shoulder were recorded, a complete tear of the subscapularis tendon was simulated surgically. A transfer of the clavicular portion of the pectoralis major muscle to the lesser tuberosity was then performed with the transferred tendon placed either above (tendon-transfer 1) or underneath (tendon-transfer 2) the conjoint tendon. For each condition, the maximum abduction angle as well as the external rotation angle and the superoinferior and anteroposterior humeral translations at the maximum abduction angle were recorded.

Results: With the rotator cuff intact, the mean maximum glenohumeral abduction angle (and standard error of the mean) was 86.3° ± 2.1° and the mean amount of external rotation at the maximum abduction angle was 5.5° ± 7.6°. A complete tear of the subscapularis tendon decreased the mean maximum abduction angle to 40.8° ± 2.4° (p < 0.001) and increased the mean external rotation to 91.8° ± 4.8° (p < 0.001). The mean humeral translations in the anterior and superior directions (+3.4 ± 0.5 and +6.3 ± 0.3 mm, respectively) at the maximum abduction angle were also increased (p < 0.01 and p < 0.001) when compared with those in the intact shoulder. Significant differences were found in the mean maximum abduction angle as well as the mean external rotation angle and humeral translations (anterior and superior) at maximum abduction between the tendon-transfer-1 condition (63.2° ± 13.5°, 82.4° ± 6.6°, 4.0 ± 1.8 mm, and 3.3 ± 1.9 mm, respectively) and tendon-transfer-2 condition (89.5° ± 12.3°, 45.7° ± 22.5°, –0.6 ± 2.0 mm, and 0.5 ± 2.3 mm, respectively). The tendon-transfer-2 condition restored glenohumeral kinematics that were closer to those in the intact shoulder than were those resulting from the tendon-transfer-1 condition.

Conclusions: Transfer of the pectoralis major tendon in subscapularis-deficient shoulders partially restored the glenohumeral kinematics of the intact shoulder. One possible explanation for the superior effect of the tendon-transfer-2 condition is that, with a pectoralis major tendon transfer underneath the conjoint tendon, the line of action of the transferred tendon is closer to that of the subscapularis muscle.

Clinical Relevance: From a biomechanical standpoint, it may be preferable to perform a pectoralis major tendon transfer underneath the conjoint tendon in subscapularis-deficient shoulders.

Author Information

1 Department of Orthopaedic and Trauma Surgery, University of Freiburg, Hugstetter Strasse 55, 79106 Freiburg, Germany

2 Musculoskeletal Research Center, Departments of Orthopaedic Surgery and Bioengineering, University of Pittsburgh, 405 Center for Bioengineering, 300 Technology Drive, Pittsburgh, PA 15219. E-mail address for R.E. Debski: genesis1@pitt.edu

Article Outline

Isolated ruptures of the subscapularis tendon are less frequent than tears of the supraspinatus. Loss of subscapularis function leads to anterior shoulder pain as well as to dysfunction due to weakness not only in internal rotation but also in shoulder elevation1,2. Excellent results, with restoration of mobility and strength, can be expected after direct repair of the tendon when feasible3,4. However, the outcome after surgical treatment of chronic lesions is less predictable as a result of fatty degeneration and atrophy of the subscapularis muscle. Therefore, substitution of subscapularis muscle function with a musculotendinous transfer is the recommended treatment for chronic irreparable ruptures of the tendon2,5-8.

A transfer of the clavicular portion of the pectoralis major muscle has been proposed for the treatment of irreparable ruptures of the subscapularis tendon2,5. Although pain relief is usually achieved with this transfer, recovery of strength does not reliably occur2,9. In addition, improvements in the active range of motion have been small2,9, and there have been differences in the range of motion between patients with satisfactory and unsatisfactory results2. Since the pectoralis major muscle originates anterior to the chest, the line of action of the pectoralis transfer is directed more anteriorly than is the subscapularis force vector. In order to improve the line of action of the transfer, a technique in which the superior part of the pectoralis major is rerouted underneath the conjoint tendon has been described5. Theoretically, this tendon transfer would result in a line of action more closely resembling that of the subscapularis. In these investigations, the range of motion (active flexion, abduction, and functional external and internal rotation) was the primary outcome measure2,5,8.

The objective of the present study was to compare the effects of two techniques of transferring the pectoralis major tendon (above or beneath the conjoint tendon) on glenohumeral kinematics during active abduction in a biomechanical model of a subscapularis-deficient shoulder. We hypothesized that a transfer of the clavicular portion of the pectoralis major muscle to the lesser tuberosity underneath the conjoint tendon would restore glenohumeral kinematics that were closer to those of the intact shoulder than were those produced by a tendon transfer above the conjoint tendon.

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Materials and Methods

Testing Apparatus

In this study, we employed a custom dynamic shoulder testing apparatus to simulate active glenohumeral abduction in the scapular plane. Previous work in our laboratory had shown that this apparatus produces highly repeatable six-degrees-of-freedom motion of the glenohumeral joint10,11. The testing system consists of a rigid frame, which supports a six-degrees-of-freedom scapular mount on which cadaveric upper extremities can be fixed to replicate the anatomical position of the scapula relative to the axial skeleton. Servo-actuated hydraulic cylinders, attached to the frame, applied forces to the rotator cuff and middle deltoid tendons through a clamp-cable-pulley system. Each cylinder was controlled independently with use of programs written with LabVIEW 6i software (National Instruments, Austin, Texas). The position and orientation of the humerus with respect to the scapula were measured with a magnetic tracking device (Flock of Birds; Ascension Technology, Burlington, Vermont) that was rigidly mounted on the shaft of the humerus. This device has an accuracy of ±0.8° in rotation and ±0.8 mm in translation in our testing environment10,11. Custom data-acquisition software was developed to continuously monitor the position and orientation of the humerus in real time.

Glenohumeral joint motion was described by humeral rotations about the axes of the fixed scapular coordinate system10. The medial-lateral and anterior-posterior axes of the scapula were established by digitizing the surfaces of the scapular block with use of a second sensor of the magnetic tracking device. The superior-inferior axis was the cross product of these two axes. The superior-inferior axis of the humerus was defined by digitizing points along the humeral shaft, the anterior-posterior axis was defined by the same vector as was used to define the scapular anterior-posterior axis of the scapula, and the medial-lateral axis was the cross product of these two vectors. Glenohumeral rotation was quantified with use of an Euler angle sequence, z-x-z, measuring three rotations of the humerus about axes fixed to the scapula. Internal-external rotation was defined as rotation of the humerus about the superior-inferior axis (z-axis) with the humerus at 0° of abduction in the scapular plane, abduction in the scapular plane was defined as rotation of the humerus about the scapular anterior-posterior axis (x-axis), and horizontal abduction was defined as rotation of the humerus about the superior-inferior axis (z-axis). The kinematic and kinetic coordinate systems were aligned with use of a transformation from the coordinate system of the sensor to the scapular coordinate system.

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Specimen Preparation

Six fresh-frozen full upper extremities were obtained from human cadavers and stored at –20°C before testing. The mean age (and standard error of the mean) of the donors at the time of death was 57 ± 1.9 years (range, fifty-two to sixty-one years), and all donors were male. Our protocol for use of human cadaveric tissue was deemed exempt by the institutional review board. No specimen had a history of trauma, degenerative joint disease, or prior surgery involving the glenohumeral joint. After each specimen was thawed at room temperature, the skin and subcutaneous tissue proximal to the glenohumeral joint were removed to expose the muscular envelope around the scapula. The clavicle and the coracohumeral, coracoclavicular, and acromioclavicular ligaments were preserved. Remnants of the scalene, pectoralis minor, teres major, and trapezius muscles were discarded, and the pectoralis major and rotator cuff muscles were exposed. Muscle fibers were bluntly dissected off their tendons, and the muscle bellies were removed. The glenohumeral joint was vented to the atmosphere through the subscapularis muscle recess during this dissection to standardize testing conditions. The individual tendons were wrapped in saline solution-soaked gauze to prevent desiccation. A longitudinal skin incision was then made over the deltoid tuberosity of the humerus to expose the broad deltoid insertion. This tendon was carefully separated from the muscle fibers; most of the muscle belly covering the glenohumeral joint was thus left intact. Gross observation of the rotator cuff and deltoid tendons confirmed that the specimens had no pathological changes in the rotator cuff or the deltoid.

Specially designed sinusoidal clamps were firmly secured to each of the rotator cuff tendons, the pectoralis major tendon, and the middle deltoid tendon. The infraspinatus and teres minor tendons were modeled as one musculotendinous unit because the two muscles have a similar line of action and function similarly as external rotators of the shoulder. To eliminate the effect of motion on the inertial properties of the upper extremity, all joints distal to the glenohumeral joint were immobilized with use of threaded pins. The scapula was potted in a rectangular epoxy putty block and fixed to the testing apparatus. The glenoid has a slight upward tilt of about 5° with respect to the medial border of the scapula, and the resting position of the scapula is defined by the medial border being rotated about 3° to 5° superior in the frontal plane12; thus, in this study, the glenoid faced upward 10° from the vertical. This position was confirmed on an anteroposterior radiograph.

Once the scapula was fixed to the apparatus, cables from the hydraulic cylinders were attached to the tendon clamps through a system of pulleys, which could be adjusted to approximate the line of action of each muscle. Muscle force vectors for the rotator cuff and middle deltoid were based on prior anatomic and magnetic resonance imaging studies of the shoulder11,13. Muscle force vectors for the pectoralis major tendon transfer were based on a geometric model of the shoulder14. Throughout the testing protocol, specimens were kept moist with physiologic saline solution.

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Experimental Protocol

Prior to each test, 5 N of force was applied to each tendon to center the humeral head on the glenoid. The position of the humerus with 5 N applied to the rotator cuff and middle deltoid tendons was defined as the reference position for joint translation. The position of maximum abduction was then achieved by applying equal forces to the rotator cuff and middle deltoid tendons at a constant rate of 20 N/s until the upper extremity reached approximately 90° of abduction in the scapular plane10,11. This position was designated as maximum abduction. The specimens were cycled through the range of maximum abduction twenty-five times in order to minimize the effect of soft-tissue viscoelasticity on glenohumeral motion.

Four testing conditions were examined to assess the effects of two techniques for transfer of the pectoralis major tendon on glenohumeral kinematics in subscapularis-deficient shoulders: (1) the intact shoulder condition, with equal force applied to the rotator cuff and middle deltoid tendons; (2) the subscapularis tear condition, consisting of a complete subscapularis tendon tear, with 100% force applied to the supraspinatus, infraspinatus/teres minor, and middle deltoid tendons, (3) the tendon-transfer-1 condition, consisting of a complete subscapularis tendon tear, a tendon transfer above the conjoint tendon, 30% force applied to the transferred pectoralis major tendon, and 100% force applied to the supraspinatus, infraspinatus/teres minor, and middle deltoid tendons; and (4) the tendon-transfer-2 condition, consisting of a complete subscapularis tendon tear, a tendon transfer underneath the conjoint tendon, 30% force applied to the transferred pectoralis major tendon, and 100% force applied to the supraspinatus, infraspinatus/teres minor, and middle deltoid tendons.

The maximum abduction angle as well as the external rotation angle and humeral translations at maximum abduction were recorded for each condition. The muscle forces for the intact shoulder condition were based on values previously utilized in our research center that resulted in abduction in the scapular plane10,11. A complete disruption of the subscapularis tendonwas then surgically simulated by incising the full thickness of the tendon at its insertion into the proximal part of the humerus. For the subscapularis tear condition, no force was applied to the subscapularis tendon. A transfer of the clavicular portion of the pectoralis major tendon to the lesser tuberosity was then performed. The superior 3 cm of the pectoralis major tendon was released from its insertion on the crest of the greater tubercle of the humerus and transferred to the lesser tuberosity. To achieve stable fixation, the transferred tendon was attached to the lesser tuberosity with two 3.5-mm standard cortical screws and washers (Synthes, West Chester, Pennsylvania). The course of the transferred tendon was simulated above (tendon-transfer 1; Fig. 1) or underneath (tendon-transfer 2; Fig. 2) the conjoint tendon according to the operative techniques described in the literature2,5. Both tendon transfer techniques were performed sequentially on each specimen in a random order. To ensure that the screw fixation was not compromised after the first test sequence, it was verified with the use of a torque screwdriver; no loosening of screw fixation during the testing was found. The force applied to the transferred pectoralis major tendon was based on values for physiologic cross-sectional area that are frequently used for muscle force predictions and finite element modeling15,16. Physiologic cross-sectional area is directly proportional to muscle force and may be used to predict the maximal muscle force17,18. Since the cross-sectional area of the clavicular portion of the pectoralis major is approximately 30% of the cross-sectional area of the subscapularis muscle, 30% of the standard subscapularis force was applied to the transferred pectoralis major tendon. After completion of the testing protocol, the specimens were disarticulated at the glenohumeral joint and the absence of osteoarthritis, prior surgical intervention, and osseous deformities was confirmed by gross observations.

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Statistical Analysis

A two-factor repeated-measures analysis of variance was utilized to assess the maximum glenohumeral abduction as well as the external rotation angle and humeral translations at maximum abduction. The two factors that were evaluated were the testing condition and the glenohumeral abduction angle. Multiple contrasts were performed to evaluate the effects of each testing condition at specific angles of glenohumeral abduction. The mean and standard error of the mean were determined for the weight of the specimen, the applied force, and the maximum glenohumeral abduction as well as the external rotation angle and humeral translations at maximum abduction. Significance was set at p < 0.05.

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Results

The weight of the specimens averaged 38 ± 3 N (range, 32 to 50 N), and the force that was applied to the rotator cuff and middle deltoid tendons to achieve maximum abduction averaged 118 ± 10 N. With the shoulder intact, the maximum abduction angle averaged 86.3° ± 2.1° and the amount of external rotation at the maximum abduction angle averaged 5.5° ± 7.6° (Fig. 3). The translation of the humerus at the maximum abduction angle averaged –3.0 ± 1.2 mm in the posterior direction and 0.2 ± 0.2 mm in the superior direction in the intact shoulder (Fig. 4).

A complete tear of the subscapularis tendon resulted in decreased abduction (40.8° ± 2.4°) and increased external rotation (91.8° ± 4.8°) compared with the values for the intact shoulder. Humeral translation occurred in the anterior (3.4 ± 0.5 mm) and superior (6.3 ± 0.3 mm) directions at the maximum abduction angle. The complete tear resulted in significant differences in abduction (p < 0.001), external rotation (p < 0.001), anterior translation (p < 0.01), and superior translation (p < 0.001) compared with the values for the intact shoulder.

Both the tendon-transfer-1 (p < 0.01) and the tendon-transfer-2 (p < 0.001) condition significantly increased the maximum abduction angle compared with that associated with the subscapularis tear condition (Fig. 3). Only the tendon-transfer-2 condition resulted in a significant decrease in the amount of external rotation (p < 0.01). A significant difference in superior humeral translation was found between the subscapularis tear condition and the tendon-transfer-1 (p < 0.05) and tendon-transfer-2 (p < 0.01) conditions (Fig. 4). Only the tendon-transfer-2 condition was associated with a significant difference in anterior humeral translation compared with the anterior translation associated with the subscapularis tear condition (p < 0.05).

Comparison of the tendon-transfer-1 and tendon-transfer-2 conditions demonstrated a significant difference in all parameters, including maximum abduction (63.2° ± 13.5° compared with 89.5° ± 12.3°; p < 0.01) as well as external rotation (82.4° ± 6.6° compared with 45.7° ± 22.5°; p < 0.01) and anterior (4.0 ± 1.8 mm compared with –0.6 ± 2.0 mm; p < 0.05) and superior (3.3 ± 1.9 mm compared with 0.5 ± 2.3 mm; p < 0.05) humeral translation at maximum abduction. A transfer of the pectoralis major tendon underneath the conjoint tendon (the tendon-transfer-2 condition) restored glenohumeral kinematics (the maximum abduction angle as well as the external rotation angle and the humeral translations at maximum abduction) that were closer to those of the intact shoulder than were the glenohumeral kinematics resulting from the transfer above the conjoint tendon (tendon-transfer-1 condition) (Figs. 3 and 4). Significant differences were found between the tendon-transfer-1 condition and the intact shoulder condition in terms of the maximum abduction angle (p < 0.01) and the amount of external rotation (p < 0.001) and anterior and superior humeral translation (p < 0.05) at maximum abduction. The amount of external rotation at maximum abduction was the only parameter that was found to be significantly different between the intact-shoulder and tendon-transfer-2 conditions (p < 0.01).

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Discussion

In this study, we examined the effects of two techniques for transfer of the pectoralis major tendon on glenohumeral kinematics during active abduction of subscapularis-deficient shoulders. A transfer of the clavicular portion of the pectoralis major muscle to the lesser tuberosity underneath the conjoint tendon was hypothesized to restore glenohumeral kinematics that were closer to those of the intact shoulder than were those produced by a tendon transfer above the conjoint tendon. The results of the study support our hypothesis.

A simulated tear of the subscapularis tendon resulted in decreased abduction, increased external rotation, and increased humeral translations compared with the values for the intact shoulder condition. This effect on glenohumeral kinematics may be caused by the imbalance between the anterior and posterior rotator cuff muscles. In accordance with the results of our study, Halder et al.19 demonstrated that the infraspinatus and subscapularis muscles provide superior glenohumeral stability by depressing the humeral head. Other biomechanical studies have also shown that disruption of the transverse force couple leads to increased translations of the humerus20,21. An evaluation of the anterior stabilizing factors of the glenohumeral joint demonstrated that the subscapularis provided the greatest amount of stabilization in external rotation22 and prevented anterior subluxation in the lower range of abduction23. The anterior humeral translation, with respect to the glenoid, in our model may have been due to the loss of muscle tension after the simulated tear of the subscapularis tendon. In another biomechanical study, the subscapularis muscle consistently tightened during both external rotation and abduction of the glenohumeral joint, preventing anterior displacement24. That study showed that cutting the subscapularis tendon increased external rotation of the joint with the arm at 0° and 45° of abduction24. These results correspond well to the increased external rotation and increased anterior humeral translation that occurred in our study.

Partial or complete ruptures of the subscapularis muscle in association with anterior dislocation of the glenohumeral joint have been described in the clinical setting25-27. Several authors have noted that the subscapularis acts as an active and passive stabilizer of the glenohumeral joint, and a subscapularis tear has been associated with pain, increased external rotation, and recurrent anterior subluxation or dislocation of the shoulder3,26,28. Furthermore, magnetic resonance imaging has demonstrated a reduction in the distance between the humeral head and the coracoid process, accompanied by anterior translation of the humeral head compared with the position on the contralateral side, in patients with a lesion of the subscapularis and supraspinatus tendons5. This translation appears to be caused by an imbalance between the anterior and posterior muscles5,29. These findings are similar to the effects on glenohumeral kinematics observed in our biomechanical model, in which the simulated tear of the subscapularis tendon resulted in increased anterior and superior humeral translation.

In our in vitro study, anterior and superior stability of the glenohumeral joint was restored to values closer to those for the intact shoulder when the pectoralis major tendon was routed underneath, rather than above, the conjoint tendon. When the pectoralis major tendon is transferred underneath the conjoint tendon, its line of action might be closer to that of the subscapularis muscle5. This difference may be a reason for the superior effect of this tendon transfer in terms of restoration of abduction and internal rotation strength. The transferred muscle at least partially balances the effects of the external rotators to restore the force couple in the transverse plane5,29. Passing the tendon underneath the conjoint tendon also interposes muscle between the coracoid process and the humeral head and increases passive muscle tension.

The limitations of our study relate to the experimental model used to simulate muscle function and to examine the kinematics of the glenohumeral joint. The dynamic shoulder testing apparatus simplifies complex muscle behavior as a single line of action from the centroid of the muscle to the tendon insertion10,11. Other muscles that may contribute to shoulder movement as well as the motion of the sternoclavicular, acromioclavicular, and scapulothoracic joints are not included in the model. Our model also does not account for the rotation of the scapula that occurs during abduction of the upper extremity in vivo. However, it has been shown that scapulothoracic motion is minimal in the first 30° to 45° of scapular plane abduction30. Poppen and Walker30 reported a 4:1 glenohumeral-scapulothoracic motion ratio during the first 25° of arm motion; the average overall ratio was 2:1. The loading conditions simulated by the dynamic shoulder testing apparatus approximate the mechanics of active glenohumeral abduction, and the preservation of the joint capsule and the long head of the biceps tendon allows passive force transmission through these structures. The use of full upper extremities correctly approximates the inertial properties of active abduction. Because the anatomic insertions of the simulated muscles are preserved, the effect of changing muscle moment arms during abduction is also included in the model. Finally, only six specimens were tested in this study; however, a significant difference in all parameters (abduction, external rotation, and anterior and superior humeral translation) was found when the tendon-transfer-1 and tendon-transfer-2 conditions were compared.

The clinical problems associated with transfers of the pectoralis major tendon are the recovery of strength and only small improvements in the range of motion. In this study, we only evaluated glenohumeral joint kinematics following these surgical procedures. Biomechanical as well as in vivo studies have shown a correlation between glenohumeral joint kinematics and muscle strength11,21,31,32. In addition, studies in which the range of motion was measured as part of the clinical assessment before and after transfer of the pectoralis major demonstrated increased abduction and decreased external rotation, findings similar to the results of our biomechanical study2,5.

Transfer of the pectoralis major tendon in subscapularis-deficient shoulders partially restores normal glenohumeral kinematics. In our biomechanical model, a transfer underneath the conjoint tendon restored glenohumeral kinematics (the maximum abduction angle as well as the external rotation angle and humeral translations at maximum abduction) that were closer to those in the intact shoulder than were the kinematics produced by a transfer above the conjoint tendon. Therefore, from a biomechanical standpoint, it may be preferable to transfer the pectoralis major tendon underneath the conjoint tendon in subscapularis-deficient shoulders. A prospective, randomized clinical study is necessary to assess if there is any difference between the two tendon transfer techniques with regard to the functional outcome of operative treatment of subscapularis-deficient shoulders. ▪

NOTE: The support of the German Society for Trauma Surgery is gratefully acknowledged.

Disclosure: The authors did not receive any outside funding or grants in support of their research for or preparation of this work. Neither they nor a member of their immediate families received payments or other benefits or a commitment or agreement to provide such benefits from a commercial entity. No commercial entity paid or directed, or agreed to pay or direct, any benefits to any research fund, foundation, division, center, clinical practice, or other charitable or nonprofit organization with which the authors, or a member of their immediate families, are affiliated or associated.

Investigation performed at the University of Pittsburgh, Pittsburgh, Pennsylvania

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