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The Journal of Bone and Joint Surgery 80:474-80 (1998)
© 1998 The Journal of Bone and Joint Surgery, Inc.

A Dynamic Analysis of Glenohumeral Motion after Simulated Capsulolabral Injury. A Cadaver Model*

M. APRELEVA, M.S.{dagger}, C. T. HASSELMAN, M.D.{dagger}, R. E. DEBSKI, PH.D.{dagger}, F. H. FU, M.D.{dagger}, S. L-Y. WOO, PH.D.{dagger} and J. J. P. WARNER, M.D.{ddagger}, PITTSBURGH, PENNSYLVANIA

Investigation performed at the Musculoskeletal Research Center, University of Pittsburgh Medical Center, Pittsburgh


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
We used a dynamic shoulder-testing apparatus and nine fresh-frozen, entire upper extremities from cadavera to evaluate the effects of varying degrees of capsulolabral injury on the kinematics of the glenohumeral joint during abduction in the scapular plane and external rotation. Joint kinematics were recorded with use of a six-degrees-of-freedom magnetic tracking device before and after the creation of each capsulolabral lesion in a progressive manner. Dislocation did not occur after simulation of a large Bankart lesion or even after sectioning of the anterior aspect of the joint capsule. However, division of the entire joint capsule (that is, both the anterior aspect and the posterior aspect) resulted in a significant increase (p < 0.05) in posterior translation during abduction in the scapular plane, and two of the nine shoulders dislocated posteriorly. External rotation of the abducted extremity produced no increase in anterior or posterior translation. CLINICAL RELEVANCE: We concluded that dynamic stability can be maintained by the rotator-cuff muscles even when the anterior aspect of the capsule is divided and the anterior portion of the labrum is separated. Thus, anterior glenohumeral instability is a complex phenomenon that may include a combination of muscle imbalance and capsulolabral injury. Our findings suggest that the importance of the active stabilizers of the glenohumeral joint should be considered when capsulolabral injuries and defects are reconstructed and when rehabilitation regimens are formulated.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
The glenohumeral joint has the widest range of motion of any of the joints in the body, but little inherent stability is provided by its articular surface. Stability of the glenohumeral joint is maintained by static restraints, including the capsule, ligaments, and labrum, as well as by dynamic restraints, including the rotator-cuff muscles7,14,24,26,32. The rotator-cuff muscles maintain stability by compressing the humeral head, which is convex, into the glenoid fossa, which is concave, during glenohumeral motion13. Subluxation or dislocation of the humeral head is thought to result from either capsulolabral separation of the inferior glenohumeral ligament or direct capsular rupture, or both1,2,37. The optimum method of stabilizing the joint operatively and recreating the delicate balance between mobility and stability after a capsulolabral injury continues to be a controversial topic in sports medicine22,30.

Our previous studies of tears of the rotator cuff in a cadaver model have shown that a large tear that includes rupture of the capsule does not lead to instability of the shoulder as long as the appropriate muscles act to provide forces that prevent instability36. Furthermore, patients who have adhesive capsulitis may have complete rupture of the capsule after closed manipulation or arthroscopic capsular release, yet few of these patients have instability after such treatment40. This may be due to residual stiffness that remains after the procedure; such stiffness causes greater static tension in the rotator-cuff muscles, which, in turn, compresses the humeral head into the glenoid. Therefore, the relative importance and interaction of these static and dynamic stabilizers must be defined further.

Most previous studies of stability of the shoulder have involved cutting of the ligaments or have included other biomechanical analyses of the passive restraints around the glenohumeral joint27,29,35. As instability is manifested by subluxation of the humeral head out of the glenoid fossa during active motion, muscle action must be incorporated into any experimental design that models glenohumeral instability.

We used an established biomechanical model to analyze a combination of these static and dynamic factors (Fig. 1)9,23,36. The objective of the present study was to quantitatively evaluate glenohumeral kinematics during abduction in the scapular plane followed by external rotation with increasing degrees of injury to the labrum, capsule, and anterior aspect of the glenoid rim. We hypothesized that, even in the presence of a Bankart lesion or capsular disruption, the dynamic restraints (the rotator-cuff muscles) would be able to maintain so-called ball-and-socket kinematics in our model. We further hypothesized that this would be the case even when the joint was placed in the potentially unstable positions at the extremes of external rotation.



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  		Fig. 1. Drawing of the dynamic shoulder-testing apparatus (left). A = scapular mount, B = cable-pulley system, C = load-cell, D = hydraulic cylinder, and E = linear variable differential transducer.

 


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 

Preparation of Specimens
Nine fresh-frozen, entire upper extremities were obtained from human cadavera (average age at the time of death, seventy years; range, fifty-nine to eighty years) and were frozen at -20 degrees Celsius. The specimens were thawed at room temperature for twenty-four hours before dissection and testing. None of the specimens had evidence of joint disease or of previous operative repair. The skin and subcutaneous tissues proximal to the glenohumeral joint were removed in order to expose the tendons of the subscapularis, supraspinatus, infraspinatus, and teres minor muscles. A lateral skin incision was made over the deltoid to expose the tendon of the middle portion of that muscle. A small arthrotomy incision was made through the rotator interval in a transverse orientation and parallel to the biceps tendon. This incision vented the joint capsule and allowed access to the anterior-inferior aspect of the capsulolabral complex so that a simulated Bankart lesion could be created during the experiment. All joints distal to the glenohumeral joint were rigidly fixed in extension with use of Kirschner wires. The scapula was fixed in a block with epoxy, with the plane of the scapula oriented vertically, to allow for rigid mounting to the dynamic testing apparatus (Fig. 1). The scapula was mounted on the apparatus so that the glenoid was facing upward approximately 10 degrees from the vertical orientation. This anatomical position of the scapula was verified by examination of an anteroposterior radiograph of the joint that was made before testing. The specimens were kept moist by irrigation with saline solution during preparation and testing.

Testing Apparatus and Simulation of Motions
Clinical research and experimental studies have shown that the muscles of the rotator cuff and the middle portion of the deltoid work in concert to achieve full glenohumeral abduction8,17,19,21,34. Therefore, we simulated the actions of these muscles to achieve abduction and external rotation. As the infraspinatus and the teres minor have similar direction and function at the glenohumeral joint, these muscles were combined to form one infraspinatus-teres minor muscle-tendon unit.

Previous work in our laboratory has shown that the dynamic testing apparatus produces highly repeatable six-degrees-of-freedom motion of the glenohumeral joint9,23,36. The apparatus consists of six servo-actuated hydraulic cylinders that apply force to each muscle-tendon unit through a tendon clamp-cable-pulley system (Fig. 1). Each cylinder is controlled independently by a computer with use of custom-designed software. A load-cell (model 3397; Lebow Products, Troy, Michigan) with an accuracy of ±0.5 newton and a linear variable differential transducer (model 853-029; Moog, East Aurora, New York) with an accuracy of ±0.1 millimeter are attached to each hydraulic cylinder to provide feedback on force and position, respectively; this feedback is used to monitor tendon excursions and to measure the forces that are applied to each muscle. A six-degrees-of-freedom magnetic tracking device (The Bird; Ascension Technologies, Burlington, Vermont) is rigidly mounted on the humeral shaft with screws to record the motion of the glenohumeral joint during abduction and external rotation. This tracking device has an accuracy of ±0.8 millimeter of translation and ±0.8 degree of rotation under our testing conditions9,23,36. The muscle force vectors chosen for the infraspinatus-teres minor, subscapularis, and supraspinatus were based on the findings of previous anatomical and magnetic resonance imaging studies of the shoulder performed in our laboratory. The angle theta ({theta}) for each of these muscle forces in the scapular plane, as measured in relation to the horizontal axis, was 51 degrees for the infraspinatus-teres minor, 58 degrees for the subscapularis, and 8 degrees for the supraspinatus. The force that was applied to the middle portion of the deltoid muscle was directed to a point approximately five millimeters dorsal to the anterolateral corner of the acromion (Fig. 1, inset). Before testing, an anteroposterior radiograph of the experimental setup was used to verify the orientation of the muscle force vectors; the orientation was determined by examining the direction of the cable representing each muscle as seen on the radiograph. The forces that were applied by each cylinder and the humeral rotations and translations in the anterior-posterior, superior-inferior, and medial-lateral directions were recorded during each test.

Initially, a five-newton force was applied to each of the four muscles in order to center the humeral head before testing and to compensate for the absence of the vacuum effect of negative intra-articular pressure in the vented joint15. The position of the upper extremity at this time was defined as the initial position (0 degrees of abduction and 0 degrees of internal-external rotation).

Equal forces then were applied to each muscle at a rate of twenty newtons per second23,36. Our data-acquisition system monitors the change in the abduction angle of the upper extremity in real time. The magnitude of the forces was increased until the extremity achieved an abduction angle of approximately 90 degrees, which was defined as the full abduction position. The force that was necessary in order to achieve full abduction or external rotation varied because of differences in the weights of the specimens. Therefore, force was applied at a constant rate to maintain consistency among the specimens. Once the extremity was in full abduction, it was externally rotated in this position. External rotation was achieved by increasing the force on the infraspinatus-teres minor to 160 per cent of that required to achieve abduction (a 60 per cent increase) while simultaneously decreasing the force on the subscapularis to 40 per cent of that required to achieve abduction (a 60 per cent decrease). These changes in force were made on the basis of pilot studies, which showed that additional equal changes in force did not have a noticeable effect on the amount of external rotation achieved. Forces applied to the supraspinatus and the middle portion of the deltoid were not altered during testing in external rotation.

Once the forces that were needed for abduction and external rotation had been determined, the specimen was cycled through the full range of motion twenty-five times in order to minimize the viscoelastic effects of the soft tissues43. Six simulated conditions then were examined sequentially for each specimen. These included (1) the normal condition, in which the only defect was the incision that had been made in the rotator interval during the preparation of the specimen (Fig. 2); (2) a small anterior-inferior Bankart lesion, characterized by detachment of the glenoid labrum from the glenoid, with the incision extending from the superior and middle glenohumeral ligaments to the anterior band of the inferior glenohumeral ligament down to the six o'clock position; (3) a large anterior-inferior Bankart lesion, with stripping of the labrum and periosteum to a point approximately two centimeters proximal to the glenoid to simulate a labral tear with periosteal stripping (Fig. 3); (4) a partial capsular defect, with the cut made at the mid-portion of the capsule to include the middle glenohumeral ligament and the anterior band of the inferior glenohumeral ligament; (5) a full capsular defect, with the incision advanced posteriorly to include the posterior aspect of the capsule and the posterior band of the inferior glenohumeral ligament (Fig. 4); and (6) an osseous defect of the glenoid, made by removal of a 1.5-centimeter-long by 0.5-centimeter-wide piece of the anterior-inferior aspect of the glenoid rim with use of rongeurs.



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  		Fig. 2. Drawing and photograph showing the lateral and superior views of the glenohumeral joint in the normal testing condition. The capsule is vented through the rotator interval, and the glenohumeral ligaments are left intact. SGHL = superior glenohumeral ligament, MGHL = middle glenohumeral ligament, IGHLC = inferior glenohumeral ligament complex, A = anterior, and P = posterior. (Reproduced, with modification, from: Warner, J. J. P., and Caborn, D. N. M.: Overview of shoulder instability. Crit. Rev. Phys. Rehab. and Med., 4: 150, 1992. Reprinted with permission.)

 


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  		Fig. 3. Drawing and photograph showing the lateral and superior views of the glenohumeral joint after the creation of a large Bankart lesion. The labrum and periosteum are stripped to a point approximately two centimeters proximal to the glenoid to simulate a labral tear and capsular stretch. SGHL = superior glenohumeral ligament, MGHL = middle glenohumeral ligament, IGHLC = inferior glenohumeral ligament complex, A = anterior, and P = posterior. (Reproduced, with modification, from: Warner, J. J. P., and Caborn, D. N. M.: Overview of shoulder instability. Crit. Rev. Phys. Rehab. and Med., 4: 150, 1992. Reprinted with permission.)

 


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  		Fig. 4 Drawing and photograph showing the lateral and superior views of the glenohumeral joint after sectioning of the entire capsule. The capsule is sectioned to include the middle glenohumeral ligament and the anterior and posterior bands of the inferior glenohumeral ligament. SGHL = superior glenohumeral ligament. (Reproduced, with modification, from: Warner, J. J. P., and Caborn, D. N. M.: Overview of shoulder instability. Crit. Rev. Phys. Rehab. and Med., 4: 150, 1992. Reprinted with permission.)

 
Full abduction followed by external rotation of the abducted extremity was simulated under each condition according to the testing protocol. The test was repeated three times under each condition, and humeral translations were plotted on the computer screen and were compared to ensure the reproducibility and quality of the data. At the completion of testing, each specimen was disarticulated at the glenohumeral joint to confirm the absence of joint disease, osteoarthrosis, and any evidence of previous operations or injuries. Gross examination of the rotator-cuff tendons revealed no evidence of accidental laceration during cutting of the capsule.

Description of Joint Motion
A system of Euler angles was chosen to describe motion of the glenohumeral joint (Fig. 5). Each rotation occurs about one of the axes of the fixed reference system defined by the scapular anatomy. The reference system is located at the geometric center of the humeral head when the upper extremity is in the neutral position (0 degrees of abduction and 0 degrees of rotation). The three axes of the reference coordinate system are directed anteriorly, superiorly, and laterally with respect to the scapular plane. The following sequence of Euler angles was used to describe the rotation angles of the moving humerus: rotation about the superior axis defined internal-external rotation of the humerus in the adducted position, rotation about the anterior axis defined abduction in the scapular plane, and rotation about the lateral axis defined internal-external rotation of the humerus in the abducted position. Humeral rotations were calculated with use of the data supplied by the magnetic tracking device regarding the initial and final orientation of the humerus9. The tracking device also provided the data on position and orientation that were needed to calculate humeral translations; these data were displayed after each test to allow for verification that abduction and external rotation were within the normal range of motion. Humeral translations during external rotation were calculated relative to the position of the humerus in full abduction (the initial position for external rotation); that is, translations in the anterior-posterior, superior-inferior, and medial-lateral directions were considered to be zero at the beginning of the external rotation. We assessed the joint physically throughout the experiment and considered it to be dislocated when the humeral head was completely out of the glenoid socket. The joint was considered to be subluxated when the translations for any testing condition exceeded two standard errors from the mean translation for the normal condition during abduction or external rotation.



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  		Fig. 5 Drawing depicting the coordinate system and the sequence of rotations used to describe humeral orientation.

 

Statistical Analysis
A one-factor analysis of variance was performed, with significance set at p < 0.05, to evaluate the effect of each simulated injury on glenohumeral translations in the anterior-posterior and superior-inferior directions during abduction in the scapular plane and external rotation. The Tukey honest significant-difference test was used for post hoc analysis.


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 

Abduction
The specimens weighed a mean (and standard deviation) of 33.3 ± 6.3 newtons, and the mean force that was applied to all muscles in order to achieve full abduction was 130.0 ± 19.0 newtons. The mean maximum angle of glenohumeral abduction that was achieved under the normal condition was 86.4 ± 8.3 degrees. This angle was calculated for each of the testing conditions and no significant differences were found. The initial position of the upper extremity did not change after each cut was made. Creation of a large Bankart lesion increased the passive laxity of the joint on manual assessment but did not result in dislocation of the joint. After sectioning of the anterior-inferior aspect of the capsule, the humeral head could be anteriorly dislocated easily with a drawer test when simulated muscle forces were absent; however, when simulated muscle forces were applied by the testing device, no noticeable humeral translations were noted in the anterior, superior, or inferior direction. The mean maximum translation in the posterior direction was 2.0 ± 0.8 millimeters under the normal condition and 2.9 ± 0.8 millimeters after the creation of a large Bankart lesion (Fig. 6). There were no significant differences among the translations that were observed in association with the first four testing conditions (the normal condition through partial sectioning of the capsule). However, sectioning of the entire capsule led to significantly larger posterior humeral translations compared with those observed under the first four conditions (p < 0.05 for all comparisons). During the late phases of abduction, the posterior translation that was associated with complete sectioning of the capsule (5.3 ± 1.7 millimeters) was almost twofold greater than that associated with the normal condition (Fig. 6). This increased translation was considered to be subluxation of the humeral head as it was more than two standard errors from the mean for the normal condition. The translations of the humeral head after the creation of an osseous defect of the glenoid were not significantly different from those after sectioning of the entire capsule. Two of the nine specimens dislocated in the posterior direction after sectioning of the entire capsule.



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  		Fig. 6 Graph of the humeral translations (mean and standard error of the mean) during glenohumeral abduction. The translations of the humeral head after the creation of an osseous defect of the glenoid were not significantly different from those after sectioning of the entire capsule and therefore are not shown.

 

External Rotation
The mean maximum angle of external rotation with the upper extremity in full abduction was 78.2 ± 24.3 degrees under the normal condition. This angle was determined for each of the testing conditions and no significant differences were found. Because of the complexity of glenohumeral motion and the simplifications made in our model, the strong eccentric force that was applied to the infraspinatus-teres minor during external rotation moved the upper extremity outside of the scapular plane to an extreme and potentially unstable position (49.1 ± 24.3 degrees of horizontal humeral extension).

The position of the glenohumeral joint in full abduction was defined as the initial position for external rotation; that is, humeral translations in the anterior-posterior, superior-inferior, and medial-lateral directions were considered to be zero at the beginning of external rotation and were calculated accordingly. The mean maximum translation in the anterior-posterior direction was 1.1 ± 0.5 millimeters under the normal condition, 1.0 ± 0.7 millimeter after the creation of a large Bankart lesion, 2.1 ± 0.7 millimeters after sectioning of the entire capsule, and 2.3 ± 2.1 millimeters after the creation of an osseous defect of the glenoid. There were no significant differences among any of these translations. Similarly, the glenohumeral translations in the superior-inferior direction were small, and no significant differences were found among any of the testing conditions.


   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
The optimum treatment for anterior instability of the shoulder after traumatic dislocation remains a subject of debate. Although clinical studies have shown a direct relationship between traumatic anterior instability of the shoulder and capsulolabral injury, the findings of electromyographic and histological studies have suggested that a more complicated lesion exists14,20,25,26,41. Using the dynamic testing apparatus, we found that glenohumeral translations during active abduction and external rotation were minimally affected by disruption of the anterior-inferior portion of the capsulolabral complex. Small translations of the humeral head occurred in all three directions, and the joint maintained ball-and-socket kinematics during these motions. These findings agree with those of previous studies3,16,28. The two specimens that dislocated posteriorly were examined grossly, a superior-inferior radiograph of the scapula and glenoid was made, and retroversion was measured with use of techniques that have been described previously38. The glenoid retroversions for these two specimens were 14 and 18 degrees, which are outside of the normal range of glenoid version as reported by Saha32,33 and others6,10. This finding may explain why these specimens dislocated posteriorly, and it is in agreement with the work of Brewer et al.6 and Hurley et al.18, who suggested that excessive retroversion of the glenoid can be a major contributing factor to posterior instability.

The findings of a number of basic-science studies have suggested that the glenohumeral capsule and ligaments are not the primary stabilizers of the shoulder but work in combination with the dynamic stabilizing effect of the rotator-cuff muscles5,11,12,20,41. Electromyographic studies have shown that abnormal activation of the rotator cuff can allow substantial anterior and posterior translations to occur with activation of the deltoid20. Furthermore, abnormal muscle activity has been demonstrated in the shoulders of individuals who have instability11,31. Structural analysis of the inferior glenohumeral, superior glenohumeral, and coracohumeral ligaments has demonstrated that these static capsular structures are relatively weak compared with the ligamentous components of the knee joint4,5. Anatomical studies have suggested that the capsuloligamentous structures are relatively lax during most rotations of the glenohumeral joint and therefore do not restrain motion until the joint reaches the extremes of motion or starts to subluxate12,14,41,42. Finally, recent experimental work has suggested that the glenohumeral capsule and ligaments may function to provide proprioceptive feedback that helps to coordinate muscle activity about the shoulder39.

In the present study, the humeral head could be manually dislocated anteriorly after disruption of the anterior-inferior aspect of the capsulolabral complex when no muscle forces were applied. However, during active abduction and external rotation with the rotator-cuff muscles in action, no noticeable glenohumeral translations were seen and the glenohumeral joint behaved as a ball-and-socket joint. This behavior was observed despite the fact that during external rotation the upper extremity was located in an extreme and vulnerable position outside of the scapular plane, where the glenohumeral ligaments are thought to play a critical role in maintaining stability of the joint. Thus, our hypothesis that the dynamic restraints could maintain the ball-and-socket kinematics of the glenohumeral joint was supported until the point of complete disruption of the capsulolabral complex. Sectioning of the entire capsule (that is, both the anterior aspect and the posterior aspect) led to a significant increase (p < 0.05) in posterior translation during abduction, and the glenohumeral joint no longer behaved as a ball-and-socket joint. Our results, together with evidence from other studies, imply that the active glenohumeral restraints (the rotator-cuff muscles) may play a primary role in maintaining stability of the shoulder. These muscles can keep the joint stable during active glenohumeral motion tested with minimum static effect of the labrum, capsule, and anterior portion of the glenoid rim.

We concluded that instability of the glenohumeral joint is a result of a more complex mechanism than simply an injury to static structures, such as a Bankart lesion or a rupture of the capsule. Momentary imbalance of the rotator-cuff forces across the joint or disruption of proprioceptive feedback may occur as a dynamic effect of a capsular injury. More than twenty-five muscles and four joints are involved in overall motion of the shoulder. With the exception of the deltoid, the muscles that were used to achieve abduction and external rotation in our experiments were the rotator-cuff muscles. Other muscles acting across the glenohumeral joint, such as the biceps, pectoralis major, and teres major, were not simulated because of the current limitations of the experimental apparatus.

In our experiment, the scapula was rigidly mounted on the testing apparatus, thereby eliminating scapulothoracic motion as a component in glenohumeral stability. We also could not assess other factors that may affect glenohumeral motion, such as abnormal proprioception and pain. Nevertheless, our findings suggest that the importance of the active stabilizers of the glenohumeral joint should be considered when reconstructing capsulolabral injuries and defects as well as when formulating rehabilitation regimens.


   Footnotes
 
*No benefits in any form have been received or will be received from a commercial party related directly or indirectly to the subject of this article. Funds were received in total or partial support of the research or clinical study presented in this article. The funding source was Orthopaedic Research and Education Foundation Grant 94-031.

{dagger}Musculoskeletal Research Center, University of Pittsburgh Medical Center, P.O. Box 71199, Pittsburgh, Pennsylvania 15213.

{ddagger}Department of Orthopaedic Surgery, Massachusetts General Hospital, Gray Building, Room 624, 55 Fruit Street, Boston, Massachusetts 02114-2617.


   References
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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