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ELSEVIER Journal of Ort hopaed ic Research Journal of Orthopaedic Research 19 (1001) 206-212 www.elsevier.nl/locate/orthres Dynamic contributions to superior shoulder stability A.M. Halder, K.D. Zhao, S.W. O'Driscoll, B.F. Morrey, K.N. An * h f a j o Clinic, Orthopedic Biamechanic~Lahouatory, ,700 First Street S U', Rochrster, hfN 5590.5, LISA Received 1 November 1999; accepted 24 April 2000 Abstract It has been suggested that superior decentralization of the humeral head is a mechanical factor in the etiology of degenerative rotator cuff tears. This superior decentralization may be caused by muscular imbalance. The objective of this study was to investigate the contribution of individual shoulder muscles to superior stability of the glenohumeral joint. In 10 fresh frozen cadaver shoulders the tendons of the rotator cuff, teres major, latissimus, pectoralis major, deltoid and biceps were prepared. The shoulders were tested in a shoulder-loading device in O", 30°, 60" and 90" of glenohumeral abduction. A constant superior force of 20 N was applied to the humerus. Tensile loads were applied sequentially to the tendons in proportion to their cross-sectional areas and translations of the humeral head relative to the glenoid were recorded with a 3Space'" Fastrak system. Depression of the humeral head was most effectively achieved by the latissimus (5.6 f 2.2 mm) and the teres major (5.1 k 2.0 mm). Further studies should elucidate their possible in vivo role in the frontal plane force couple to counter balance the deltoid. The infraspinatus (4.6 i2.0 mm) and subscapularis (4.7 i 1.9 mm) showed similar effects while the supraspinatus (2.0 & 1.4 mm) was less effective in depression. Therefore, the infraspinatus and subscapularis should be surgically repaired whenever possible. The supraspinatus may be of less importance for superior stability than previously assumed. Published by Elsevier Science Ltd on behalf of Orthopaedic Research Society. Introduction Rotator cuff lesions are among the most common shoulder diseases. However, the origin of rotator cuff degeneration is still unclear. Possible explanations include intrinsic factors such as decreased circulation in the critical area with limited vascularization [29] or changes in collagen synthesis and turnover [30]. Extrinsic factors include increased shear and compressive forces as a result of a narrowed acromio-humeral interval [24,31]. It is probable that a combination of intrinsic and extrinsic factors is present prior to rotator cuff failure [32]. A decrease in acromio-humeral distance may be due to osteophytes on the undersurface of the acromion or hypertrophy of the coracoacromial ligament [ 1,9,22], as well as superior migration of the humeral head [7,34,31,391. Superior decentralization of the humeral head may increase shear and compressive forces on the rotator cuff tendons. This potentially causes fiber dis- *Corresponding author. Tel.: + 1-507-281-2262;fax: + 1-507-284- 5392. E-ma2 address: aii.kainan(a~mayo.edu (K.N. An). ruption on the bursa1 and articular side [21], as well as sclerosis of the acromion and thickening of the coracoacromial ligament [4]. This would further narrow the acromio-humeral interval initiating a vicious cycle eventually leading to rotator cuff rupture. However, superior decentralization of the humeral head may be the cause as well as the result of rotator cuff thinning. Several studies identified static structures contributing to superior stability of the glenohumeral joint. In conjunction with the insertion of the long head of biceps tendon. the glenoid labrum has a stabilizing effect [26]. The size of the rotator cuff interval also seems to be important [ 131. Negative intraarticular pressure has a stabilizing effect in all directions but only at low loads ~141. Few studies have focused on dynamic stabilizers of the glenohumeral joint in the superior-inferior direction [6,11,24,31.34,37]. Their results are controversial and the relative contributions to superior stability of different shoulder muscles are not yet known. However, this would be of tremendous importance in order to address the most effective muscles in conservative treatment of the impingement syndrome as well as postoperative rehabiliation. Furthermore, it would help to direct rotator cuff surgery to the most relevant structures. The objective of this study was to investigate the contribution of 0736-0266/01/$ - see front matter Published by Elsevier Science Ltd on behalf of Orthopaedic Research Society. PII: S 0 7 3 6 - 0 2 6 6 ( 0 0 ) 0 0 0 2 8 - 0 A. hf. Hulder rt al. I Journal of'Orthopaedic Rrsrurch 19 (2001) 206-212 different muscles to superior gelnohumeral stability. These contributions may be relevant to our understanding of the etiology and prevention of rotator cuff degeneration. Materials and methods Ten fresh frozen cadaver shoulders without rotator cuff tears or radiological evidence of glenohumeral osteoarthritis were used in the study. During dissection, preparation and testing the specimens were moistened using physiologic saline solution to prevent dehydration. All soft tissues superficial to the muscles were removed except rotator cuff muscles, teres major, latissimus, deltoid and pectoralis major muscles and their respective tendons. All muscles, except the deltoid, were elevated from the bone and resected at the musculotendinous junction. The deltoid was preserved. Their tendons were carefully separated from surrounding soft tissue to ensure unrestricted movement. Nylon strings were sutured to each margin of the flat tendons to allow even loading. Fiberglass rods were cemented into the medullary canals of the proximal humeri to control position in the frontal plane. Thinner rods were fixed in drill holes perpendicular to the humeral shaft in the neutral position employing the bicipital groove as a landmark to control rotation. The scapulae were mounted onto a Plexiglas plate. The shoulder-testing device (Fig. 1) was made of non-metal materials to avoid interference with the electromagnetic tracking device. A hinged Plexiglas are attached to the humerus allowed control of the degree of abduction. Through variable-position pulleys, strings from the tendons were connected to pneumatic actuators (Airpot Corporation, Norwalk, Connecticut, USA). A commercially-available computer controlled by Labview'" software (National Instruments Corporation 1994, Austin, Texas, USA) drove electro-pneumatic valves (Proportion-Air 1997, McCordsville, Indiana, USA) to load the pneumatic actuators. Custom-made load cells on each cylinder verified the applied loads. A 3Space'" Fastrak system (Polhemus 1993, Col- 207 Chester, Vermont, USA) measured the three-dimensional positions and orientations of sensors attached to the specimen in relation to the source of electromagnetic waves. The glenohumeral joint was positioned according to laser-pointers which were located superiorly and laterally and whose beam intersected at the center of rotation of the hinged arc. The scapulae were aligned and rigidly mounted in the shoulder-testing device so that the medial margin of the scapula was in line with the vertical axis of the device, and the humeral head was in the center of the pivoting arc. Nylon loops were sutured to the tendons and were connected to the pneumatic actuators by strings that were guided by pulleys. The positions of the pulleys were carefully adjusted so that the strings imitated muscle lines of action by running through the centroids of each muscle [16]. Finally, 3Space'" sensors were attached to the proximal humerus close to the head and to the spine of the scapula. The source of the electromagnetic waves was rigidly mounted in line with the vertical axis of the shoulder-testing device. To selectively investigate the stabilizing function of the tested muscles only translations of the humeral head relative to the glenoid were allowed while the humerus was kept in a fixed degree of abduction in the scapular plane. As tightness of the ligaments in the extremes of motion kept in the muscles from generating vertical translations [13,38] the humerus was locked in neutral rotation. The experiment started in the hanging arm position and was performed in 30", 60". and 90" of glenohumeral abduction (Fig. 2). The joints were confirmed to be vented prior to testing. Of the muscles tested, the pectoralis major and the latissimus did not originate from the scapula. Therefore, adjusting the pulleys according to the scapular tilt [28] changed their lines of action. The potentials of different muscles to reverse superior translation of the humeral head were measured. Superior translation of the humeral head was accomplished by application of a constant superior force of 20 N. The depressor effects of the supraspinatus, infraspinatus, teres minor, teres major, latissimus, superior and inferior part of the subscapularis, pectoralis major, and long head of biceps were tested. The tendons were loaded sequentially in random order in line of muscle action and proportional to their respectivc physiologic cross-sectional Pulley Actuator Weight Actuator Control System Fig. 1. Shoulder testing device. A hinged Plexiglas arc attached to the humerus allowed control of abduction and rotation. Strings from the tendons were connected to pneumatic actuators through pulleys that were variable in position. A commerically-available computer drove electropneumatic valves to load the pneumatic actuators. Custom-made load cells on each cylinder verified the applied loads. A 3Space'" Fastrak system attached to the specimen measured the three-dimensional positions and orientation of sensors in relation to the source of electromagnetic waves. A.M. Hulder et ul. I Journul of Orthopurdic Rescurch 19 (2001) 206-212 3-Space Sensor Humerus 3-Space Sensor Scapula Pulley String 3-Space Sensor Ninged Arc Pulley Weight Actuator Fig. 2. Testing of the infraspinatus muscle in the hanging arm position. The humertls was locked in neutral rotation. A constant superior force of 20 N was applied to the humerus, and the tendon was loaded in line of muscle action proportional to its cross-sectional area by computer-controlled pneumatic actuators. Positional measurements were taken by a 3Space'" Fastrak system. areas (reported hy Veeger [36]). This was based on the assumption that the maximum generated muscle force is proportional to its cross-sectional area [35].To ensure identical starting positions for all muscles, the humerus was reset between each test according to position values provided by the 3Space'" Fastrak system. After testing, the glenohumeral joint was disarticulated. and the bony landmarks were digitized to determine their positions relative to Ihe sensors. From the digitization data, the center of the humeral head, defined as the geometric center of its convexity, and the center of the glenoid, defined as the intersection of its vertical and horizontal axes, were calculated. Translations caused by each muscle were calculated by comparing the positions of the center of the humeral head before and after muscle loading. Results are reported as translation values in millimeters for each joint position and as an average of all positions. Summary statistics are reported as means ( M . D . ) .Translational distances were lirst analyzed using two-factor analysis of variance with repeated measures o n both [actors (muscle and arm position). However, because significant interactions between muscle and arm positions were identified, separate one-way repeated measures ANOVAs were run for each arm position. Significant effects were then, further analyzed using the Studeiit-Newman Keuls multiple comparison procedure. All statistical tests were two-sided, with the threshold of significance set at c( = 0.05. All analysis were performed using SAS version 6.17 (SAS Institute, Cary, NC) on a Sun Ultra IT computer (Sun Microsystems, Palo Alto, CA). Results Generally the largest translations were generated by the tested muscles in 30" and 60" of glenohumeral abduction (Fig. 3). In the hanging arm position, the translations were smaller because the superior joint capsule limited inferior translations [13]. In 90" of glenohumeral abduction the smallest translations oc- curred because of the progressive tightness of the inferior glenohumeral ligament complex [25]. The latissimus was the most effective depressor (average: 5.6 i2.2 mm) which was significant (Table 1) in the hanging arm position (5.5 i 1.0 mm). At 30" ( 7 . 6 f 3 . 0 mm), 60" (5.6+ 1.8 mm) and 90" (3.6%2.0 mm) of glenohumeral abduction, it was still significantly ( P < 0.05) more effective than all muscles tested, except the teres major, the infraspinatus and the subscapularis. In these positions, it had the most inferiorly directed line of action, and its large cross-sectional area was capable of generating high muscle force. With increasing abduction, the line of action of the latissimus became perpendicular to the glenoid due to scapular tilt and thus, became a compressor more than a depressor of the humeral head. The teres major was the second most effective depressor (average: 5.1 f 2.0 mm). Its inferiorly directed line of action was constant in relation to the glenohumeral joint because it originated from the scapula and it had a large cross-sectional area. It was significantly less effective than the latissimus in the hanging arm position (3.9 i 1.2 mm), but not significantly diffcrent from the latissimus in 30" (6.9 i 1.7 mm), 60" (5.5 & 1.8 mm) and 90" (4.2 f 2.0 mm) of glenohumeral abduction. The depressor effects of the infraspinatus (average: 4.6 f 3.0 mm) and subscapularis (average: 4.7 1.9 mm) were comparable as their lines of action were similar. Both were significantly ( P < 0.05) more effective than * A.M. Halder et al. I Journal of Orthopuedic Research 19 (2001i 206-212 209 Humeral Head Depressor Effects hanging arm position -g 30 degrees abduction R 60 degrees abduction 90 degrees abduction 10.0 I 8.0 v 2 6.0 3 B 5 4.0 G ru 0 E .3 2.0 m v1 2 0.0 -2.0 muscle Fig. 3. Translation values of the tested muscles in millimeters in hanging arm position, at 30", at 60" and at 90" of glenohumeral abduction. The graphs depict the inferior translations of the humeral head relative to the glenoid effected by the tested muscles counteracting a constant superior force of 20 N. Table 1 The multiple comparisons test results using the Studen-NewmanKeuls procedure" Muscle Hanging arm 30" 60" 90" Latissimus A A A A Long head of biceps B BC BC B Teres major B AB A A Infraspinatus BC AB AB A C AB AB A Subscapularis Subscapularis inferior C BC ABC A Pectoralis major E B D D Subscapularis superior DE C C B Teres minor DE D D B Supraspinat us E D D B "Within each position, muscles with letters in common were not found to be significantly different ( P > 0.05) in terms of their mean translational distance. Examination of this table shows the interaction between muscle and position. the supraspinatus throughout all positions. The separately tested inferior portion of the subscapularis generated significantly ( P < 0.05) larger inferior translations than the superior portion in the hanging arm position and at 90" of glenohumeral abduction. Probably due to its smaller cross-sectional area, the teres minor was significantly ( P < 0.05) less effective in depression (average: 2.3 f 1.2 mm) than the inferior portion of the subscapularis. The long head of biceps was comparable in depression (average: 4.0 It 2.1 mm) to the infraspinatus and subscapularis in 30" (6.0 f 1.9 mm) and 60" (4.3 f 1.8 mm) of glenohumeral abduction but was less effective than both in 90" of glenohumeral abduction (1.7 f 1.0 mm). The supraspinatus was an ineffective depressor (average: 2.0 f 1.4 mm), as its line of action is almost perpendicular to the glenoid, and its cross-sectional area is of medium size. It caused a significantly ( P < 0.05) smaller depression than that of the subscapularis and the infraspinatus. Depending on the glenohumeral abduction angle, the pectoralis major either partially reversed or exacerbated the humeral head superior translation as its line of action moved from inferior to superior with respect to the glenoid. Depression of the humeral head in the hanging arm position ( 3 . 4 f 0 . 7 mm) and 30" of glenohumeral abduction (2.6 f 2.2 mm) changed to superior humeral head translation in 60" of glenohumeral abduction (-0.5 f 0.9 mm) and 90" of gelnohumeral abduction (-0.7 f 0.5 mm). Discussion In preliminary experiments we were unable to identify static constraints that would stabilize the glenohumeral joint in the superior direction in the mid-range of motion. However, in the extremes of rotation, adduction and abduction, the glenohumeral and coracohumeral ligaments locked the humeral head in the center of the glenoid. As the pathomechanism of superior decentralization of the humeral head is still unknown, the 210 A . M . Huldrr et a/. I Journul of Orthopardie Rrsrurch 19 (20011 206-212 purpose of this study was to investigate the contribution of different muscles to superior stability of the gleno h umeral joint . The latissimus and the teres major were most capable of reversing superior translations of the humeral head. Traditionally, the latissimus is described as a mover of the shoulder joint causing adduction, extension, and internal rotation [I 51 without any apparent stabilizing function. However, the extent to which the latissimus is necessary for shoulder function is unclear, as some investigators reported permanent deterioration of shouldcr function following surgical removal of the latissimus [S] while some found only minor changes [2]. The rotator cuff muscles surrounding the glenohumeral joint act through force couples and serve as its primary stabilizers. The horizontal plane force couple consists of the subscapularis anteriorly and the infraspinatus posteriorly [3]. In the frontal plane, the deltoid has the largest elevator moment arm that needs to be counterbalanced inferiorly. The inferior rotator cuff muscles have substantially smaller depressor moment arms and may not be sufficient to counterbalance maximum deltoid activity. The latissimus dorsi, the teres major and the pectoralis major have depressor moment arms of the same dimension as the deltoid [19]. Consequently, these muscles may contribute to the inferior part of the frontal plane force couple. Electromyographic studies that have documented activity in the latissimus during abduction movements lend support to this idea [18]. These findings suggest the usefulness of strengthening and coordination excercises for the latissimus and the teres major in the treatment of rotator cuff disease. They also suggest avoiding surgical removal of the latissimus dorsi. Whereas the humeral head depressing function of the latissimus dimnished at higher degrees of abduction, thc teres major had a constant effect due to its scapular origin. The pectoralis major was the most variable causing depression of the humeral head initially and then elevation as the humerus was abducted. Although the pectoralis major affected translations in vitro, an in vivo stabilizing function is improbable according to electromyographic studies [ 181. Further studies should elucidate its in vivo function. In our study, the infraspinatus and the subscapularis showed similar depressor effects, although the effects were smaller than the latissimus and the teres major. We confirmed the findings of earlier cadaver experiments that found that the whole rotator cuff [31], specifically the infraspinatus, teres minor, and subscapularis muscles provide dynamic superior stability [5,27,3 11. Furthermore, we tested the superior and inferior portions of the subscapularis separately because of their separate innervation [17]. We found the inferior part to be a more effective depressor because of its more inferiorly directed line of action. NovC-Josserand identified the infraspin- atus as a major active depressor of the humeral head [24], and it seems important to surgically repair it whenever possible to restore the horizontal and frontal plane force couples. Traditionally, the supraspinatus has been considered to be important for superior stability and a complete closure of rotator cuff defects involving the supraspinatus has been advocated [33].Indeed, the supraspinatus is an important mover of the glenohumeral joint especially since it participates in the initiation of abduction [10,34] and in rotation of the joint [12]. Although some investigators reported a stabilizing effect in the anterior and inferior directions [33], others found little contribution of the supraspinatus to superior stability [31,341. Our study showed that the supraspinatus had a minor superior stabilizing effect. It is assumed that the long head of biceps tendon acts as a primary depressor of the humeral head [37].In our study it showed a considerable depression effect despite its medium cross-sectional area. However, the long head of biceps is minimally activated in shoulder movements, indicating that it primarily serves as an elbow mover [40]. It appears that the long head of the biceps tendon is primarily a passive superior stabilizer in the glenohumeral joint [24,26]. The limitations of our study relate to the use of cadaveric specimens. We strived for the highest accuracy possible using computer-controlled pneumatic actuators and low-friction pulleys for muscle loading. Nevertheless, loading was based on the assumption that maximum muscle force is proportional to its cross-sectional area (which was derived from the literature [36]). In each position, the muscle loading was done sequentially and at a force proportional to the cross-sectional area of the muscle. This method neglected muscle interactions and dependence of muscle activity on joint position. However, the study was designed to show potential effects of single muscles in certain joint positions and not to replicate the exact in vivo situation precisely. Further in vivo studies should elucidate their role. Strings, representing lines of muscle action, were adjusted according to the centroids of the tested muscles (as derived from the literature). Changing lines of muscle action accordingly simulated scapular inclination relevant for thoracohumeral muscles. Although strings are merely an approximation of the vaired lines of action of a muscle, they are a legitimate biomechanical model of muscle forces. In our model, the effect of negative intraarticular pressure was excluded as the joint capsules were vented. This permits simulation of the clinical situation in which a tear of the rotator cuff prevents negative intraarticular pressure. The applied constant forces d o not occur naturally but represent the shear force component generated by muscles or gravity. The clinical effect of contraction of any given muscle might also differ from the effect demonstrated by A.M. Halder et al. I Journul of Orthopaedic Research 19 (20011 ,706-212 isolated contraction of the muscle. Finally, we only looked at whether an individual muscle could reverse the superior translation. In vivo, their importance to glenohumeral stability would also be derived from their contributions to concavity-compression at the joint. 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