J Shoulder Elbow Surg (2013) -, 1-7

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The role of pectoralis major and latissimus dorsi muscles in a biomechanical model of massive rotator cuff tear Sean T. Campbell, BSa, Kier J. Ecklund, MDa,b, Eileen H. Chu, MDa, Michelle H. McGarry, MSa, Ranjan Gupta, MDa,b, Thay Q. Lee, PhDa,b,* a b

Orthopaedic Biomechanics Laboratory, VA Healthcare System, Long Beach, CA, USA Department of Orthopaedic Surgery, University of California, Irvine, Irvine, CA, USA Background: Superior migration of the humeral head after massive rotator cuff tear (mRCT) is thought to lead to cuff tear arthropathy. Previous biomechanical studies have demonstrated the ability of the pectoralis major and latissimus dorsi (PM/LD) muscles to resist this migration. This study examined the role of PM/ LD muscles on glenohumeral joint forces and acromiohumeral contact pressures in a mRCT model. Methods: Six cadaveric shoulders were tested using a custom shoulder-testing system. Muscle insertions of the rotator cuff, deltoid, and PM/LD were preserved and used for muscle loading. Specimens were tested in 3 different humeral rotation positions at 0 abduction and 2 rotation positions at 60 abduction. Testing was performed for intact specimens, after supraspinatus removal, and after supraspinatus/infraspinatus/ teres minor removal. PM/LD were loaded or unloaded to determine their effect. Humeral head kinematics, glenohumeral joint forces, and acromiohumeral contact area and pressure were measured. Results: For the mRCT condition at 0 abduction, unloading the PM/LD resulted in superior shift of the humeral head. Acromiohumeral contact pressures were undetectable when the PM/LD were loaded but increased significantly after PM/LD unloading. After mRCT, superior joint forces were increased and compressive forces were decreased compared with intact; loading the PM/LD resolved these abnormal forces in some testing conditions. Conclusion: In mRCT, the PM and LD muscles are effective in improving glenohumeral kinematics and reducing acromiohumeral pressures. Strengthening or neuromuscular training of this musculature, or both, may delay the progression to cuff tear arthropathy. Level of evidence: Basic Science Study, Biomechanics. Ó 2013 Journal of Shoulder and Elbow Surgery Board of Trustees. Keywords: Massive rotator cuff tear; rotator cuff tear arthropathy; latissimus dorsi; pectoralis major; acromiohumeral pressure

Cuff-tear arthropathy (CTA), as originally described by Neer,21 involves subacromial impingement of the humeral Institutional Review Board approval was not required for this basic science study. *Reprint requests: Thay Q. Lee, PhD, Orthopaedic Biomechanics Laboratory, VA Long Beach Healthcare System (09/151), 5901 E 7th St, Long Beach, CA 90822, USA. E-mail address: [email protected] (T.Q. Lee).

head, acetabularization of the acromion, and glenoid erosion after a massive tear of the rotator cuff.4,5,20 These sequelae are thought to be caused by the loss of stabilizing compressive forces across the glenohumeral joint after a massive cuff tear, followed by superior migration of the humeral head in the direction of deltoid pull.4,5,15,19-21 The term massive rotator cuff tear (mRCT) is often defined as a tear involving the detachment of at least 2 cuff

1058-2746/$ - see front matter Ó 2013 Journal of Shoulder and Elbow Surgery Board of Trustees. http://dx.doi.org/10.1016/j.jse.2013.11.030

2 muscle tendons, most commonly the infraspinatus and supraspinatus (SS).9 Radiographic features of CTA include superior migration of the humeral head, narrowing of the glenohumeral joint space, and occasionally, degenerative changes to adjacent bony structures such as the clavicle or coracoid process.5,12,15,20 Clinical symptoms include pain, loss of motion, weakness, and swelling of the affected joint.5,15,20 Treatment of such pathology has traditionally included hemiarthroplasty6,21,26,27; more recently, reverse total shoulder arthroplasty has shown promising clinical and biomechanical results.1,8,14,16,22,25 Previous biomechanical studies have identified the important role of the rotator cuff and shoulder muscles as stabilizers of the glenohumeral joint.2,3,11,18,23,24,28 One biomechanical study by Halder et al11 found that the latissimus dorsi (LD) is the most effective depressor of the humeral head, and others have shown by electromyography (EMG) that activation of the LD and teres major is increased after a mRCT.13 Another biomechanical study demonstrated that tears of the SS and infraspinatus muscles result in superior shift of the humeral head and that loading of the pectoralis major (PM) and LD (PM/LD) muscles plays a role in reducing this elevation.23 Other work has shown that the subscapularis is an important stabilizer and the most powerful of the rotator cuff muscles.17,29 Subscapularis function has been shown to be especially important in shoulders undergoing LD transfer for large cuff tears, where a deficiency results in an uncentered humeral head and poor clinical outcome.10,30 Although previous work has described the importance of the PM/LD muscles in resisting superior migration of the humeral head, no biomechanical studies to date have evaluated the role of these muscles on acromiohumeral contact pressure and glenohumeral joint forces after mRCT, including the degree to which loading of this musculature alters such biomechanical properties. The purpose of this study was to examine the biomechanics of mRCT and the role of the PM/LD muscles in a cadaveric model, including measurement of kinematics, acromiohumeral contact pressures, and glenohumeral joint forces.

Materials and methods Specimen preparation The study used 6 fresh frozen cadaveric shoulders from male donors (average age, 79.3 years; range, 76-85 years) with no evidence of musculoskeletal pathology. Specimens were dissected free of overlying skin and soft tissue while preserving the insertions of the rotator cuff, deltoid, PM, and LD muscles as well as the coracoacromial and coracohumeral ligaments and the long head of the biceps tendon. The glenohumeral joint capsule was also resected to eliminate its effect on joint forces and humeral head kinematics at the various positions tested. A modified Kessler stitch was used to tie No. 5 Ethibond suture (Ethicon, Somerville, NJ, USA) to each muscle insertion. Each

S.T. Campbell et al.

Figure 1 Photograph shows a specimen mounted to the custom testing system after the creation of a supraspinatus lesion.

scapula and corresponding humerus were placed in a custom aluminum testing box and section of polyvinyl chloride pipe, respectively; care was taken to keep the glenoid surface parallel to the top opening of the box and the humerus centered in the pipe with the long axis of the humeral shaft parallel to the side of the pipe. The scapula and humerus were secured within their containers using plaster of Paris. Specimens were kept moist with 0.9% normal saline during all phases of testing.

Biomechanical testing After preparation, specimens were mounted to a custom shouldertesting system (Fig. 1). The testing system allowed the glenohumeral joint to be positioned with 6 degrees of freedom and for muscle loading using LabVIEW (National Instruments, Austin, TX, USA) controlled pneumatic cylinders. The rotator cuff muscles (subscapularis, SS, and infraspinatus/teres minor) were loaded with 40 N, the deltoid was loaded with 80 N or 40 N, and the PM/LD were loaded with 40 N or left unloaded. These parameters were similar to those used in previous work and allowed multiple loading conditions for the deltoid and PM/LD to be tested with reproducible results.23,24 The teres minor and infraspinatus were loaded in a combined fashion due to their similar function and orientation. Glenohumeral joint forces in the anterior-posterior, superiorinferior, and medial-lateral directions were measured using a multiaxis load cell (Assurance Technologies, Garner, NC, USA). Joint force was normalized by calculating force as a percentage of the resultant. Humeral kinematics were measured using a Microscribe 3DLX system (Revware Inc, Raleigh, NC, USA) by digitizing 3 constant points on the humerus and scapula under each testing condition, followed by digitization of the humeral head and glenoid geometry. Acromiohumeral contact pressure and area were measured using a Tekscan 4000 (Tekscan Inc, South Boston, MA, USA) pressure measurement system inserted between the acromion and the superior aspect of the humeral head. All data were recorded twice to ensure repeatability. Testing was carried out in the following positions: 0 abduction-60 external rotation, 0 abduction-0 external rotation, 0 abduction-30 internal rotation, 60 abduction-90 external rotation, and 60 abduction-30 external rotation. These were

Pectoralis and latissimus in cuff tear

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Figure 2 Histogram demonstrates the effect of pectoralis (PM)/latissimus dorsi (LD) unloading on humeral head apex position for the massive rotator cuff tear condition with 80 N and 40 N deltoid loads. P values are shown overlying the corresponding data; all shifts displayed are significant. The error bars represent standard error of the mean. ER, external rotation; IR, internal rotation. meant to represent a range of functional anatomic positions at the waist and overhead level. This was repeated for (1) intact specimens, (2) after removal of the SS muscle (SS tear), (3) and after removal of the SS/infraspinatus/teres minor muscles (mRCT).

Data analysis A repeated measures analysis of variance was used for statistical analysis to compare the 3 cuff conditions: intact, SS tear, and mRCT. A paired Student t test was used to evaluate the differences between biomechanical data collected under different muscleloading conditions.

Results Humeral head position When the PM/LD were unloaded in the SS tear condition, a significant superior shift of the humeral head occurred when 80 N deltoid loads were applied (P < .05), but not with 40 N deltoid loads. When the PM/LD were unloaded in the mRCT condition, a significant superior shift of the humeral head occurred under all testing conditions at 0 abduction (Fig. 2). In all but 1 of the 12 conditions tested at 0 abduction, creation of a mRCT resulted in a significant superior shift of the humeral head compared with the intact condition (P < .05).

Acromiohumeral contact pressure and area For the SS tear condition, acromiohumeral contact pressure and area were not measurable under most of the conditions. For the mRCT condition at 0 abduction, no acromiohumeral contact pressure or area were recorded at any rotation position when PM/LD were loaded. When PM/LD were unloaded, significantly increased mean and peak acromiohumeral contact pressure and decreased contact area were observed with 80 N deltoid loads (Fig. 3, A-C).

Glenohumeral joint forces Superior glenohumeral joint forces increased significantly from the PM/LD loaded to PM/LD unloaded state under all conditions tested (Table I). Compressive forces decreased from the PM/LD loaded to the PM/LD unloaded state under 80 N deltoid loads but not under 40 N deltoid loads (Table II). No difference in superior glenohumeral joint forces was observed after creation of the SS tear at 0 abduction compared with intact. Creation of a mRCT significantly increased superior glenohumeral joint forces compared with intact under all but 1 testing condition at 0 abduction. At 60 abduction, creation of the SS lesion resulted in significantly different superior forces compared with intact in 4 of the 8 conditions tested, which increased to 6 of 8 after creation of the mRCT lesion (Table I). Creation of an SS tear alone did not significantly alter compressive forces, but mRCT resulted in significantly decreased force compared with intact in 15 of the 20 conditions tested (Table II).

Discussion This biomechanical study evaluated the role of the PM/LD muscles on humeral head translation, glenohumeral joint forces, and acromiohumeral contact pressure in the setting of a mRCT. After the creation of a mRCT, we found significant superior shifts of the humeral head, increased superior and decreased compressive glenohumeral joint forces, and elevated acromiohumeral pressures, especially at 0 glenohumeral abduction. When the PM/LD were loaded after injury, the humerus did not exert pressure against the acromion at these positions. A recent study by Hawkes et al13 used EMG to evaluate shoulder muscle activation after mRCT. EMG results from 13 shoulder muscles during arm elevation were compared in 13 healthy volunteers and 11 patients with a mRCT involving at least 2 tendons. The authors found increased

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Figure 3 Histogram shows (A) mean acromiohumeral contact pressure, (B) peak acromiohumeral contact pressure, and (C) acromiohumeral contact area with 80 N deltoid loads and unloaded pectoralis major/latissimus dorsi at different shoulder positions in the intact condition and after creation of a massive rotator cuff tear (mRCT) by removal of the supraspinatus/infraspinatus/teres minor muscles. P values are shown overlying the data, with boldface values representing a significant change. The error bars represent standard error of the mean. ER, external rotation; IR, internal rotation.

signal amplitude in multiple shoulder muscles, including the LD, in patients with mRCT and also identified a correlation between deltoid and LD activation. They went on to suggest

increased activation of the LD results from an attempt to stabilize the humeral head and limit superior translation.13 Although the current study did not isolate the PM from

Pectoralis and latissimus in cuff tear Table I

Superior glenohumeral joint forcesdpercentage of resultant)

Variable 

5

80 N deltoid

40 N deltoid

40 N PM/LD

PM/LD unloaded

40 N PM/LD

PM/LD unloaded

11.9  2.8 13.1  3.3 19.0  4.0y,z

39.6 ± 3.4 44.7 ± 3.6 64.7 ± 6.7y,z

4.7  2.3 6.8  4.1 0.8  5.6

13.3 ± 3.2 18.3 ± 5.2 32.1 ± 6.5y,z

12.7  2.6 15.4  3.7 29.6  4.2y,z

39.1 ± 2.8 42.0 ± 2.4 71.8 ± 5.8y,z

4.7  2.0 3.5  4.6 12.0  7.3y,z

11.8 ± 2.8 16.7 ± 5.2 41.4 ± 5.6y,z

13.0  2.0 14.4  3.1 26.3  4.7y,z

31.4 ± 2.6 39.6 ± 3.2 68.8 ± 8.6y,z

3.2  2.1 5.8  2.7 22.2  7.2y,z

8.4 ± 2.0 12.4 ± 5.8 44.3 ± 5.1y,z

7.4  1.8 7.0  2.1 9.4  2.1

22.6 ± 2.2 26.0 ± 2.1y 37.2 ± 2.4y,z

3.4  1.8 7.5  1.9y 7.0  2.1y

9.8 ± 2.4 8.7 ± 2.5 18.3 ± 2.9y,z

9.2  1.6 8.8  2.1 16.4  2.6y,z

22.4 ± 2.0 26.3 ± 2.1y 43.1 ± 3.0y,z

1.4  1.7 4.9  2.1y 0.2  3.0z

9.2 ± 2.3 9.1 ± 3.0 27.6 ± 4.3y,z



0 Abduction, 60 ER Intact SS tear mRCT 0 Abduction, 0 rotation Intact SS tear mRCT 0 Abduction, 30 IR Intact SS tear mRCT 60 Abduction, 90 ER Intact SS tear mRCT 60 Abduction, 30 ER Intact SS tear mRCT

ER, external rotation; IR, internal rotation; mRCT, massive rotator cuff tear; PM/LD, pectoralis major/latissimus dorsi; SS, supraspinatus. ) Data are expressed as the mean percentage (%) of resultant  standard error of the mean. The boldface data represent a significant difference (P < .05) between the PM/LD loaded and unloaded conditions under equivalent deltoid loads. y Significantly different (P < .05) from intact under same loading conditions. z Significantly different (P < .05) from SS tear under same loading conditions.

the LD when muscle loading was tested, we did demonstrate that combined loading of the PM/LD decreases superior humeral head translation and acromiohumeral pressure. Previous biomechanical work has addressed the contribution of individual muscles to shoulder stability in the setting of superior decentralization of the humerus. One cadaveric model that used intact specimens under constant superior force found the LD was the most effective depressor of the humerus, especially with the arm hanging. With shoulder abduction, the LD maintained a role in depression initially but became increasingly important in glenohumeral compression.11 Our findings demonstrated the capacity of the LD, in combination with the PM, for depression of the humeral head after superior migration. The compressive effect of the PM/LD was also observed: PM/LD loading after mRCT restored compressive glenohumeral joint forces to the intact state in many testing conditions at neutral or externally rotated shoulder positions. Another recent biomechanical study evaluated the progression of rotator cuff injuries and the involvement of the PM/LD. Using a cadaveric model, the authors sequentially created and tested 4 different stages of rotator cuff injury, beginning with a partial SS tear and culminating with tear of the entire SS and infraspinatus.23 Tear of the entire SS significantly altered glenohumeral rotational range of motion and abduction capacity, whereas progression to a tear involving half of the infraspinatus resulted in a shift of the

humeral head. The authors also demonstrated restoration of humeral head kinematics with PM/LD loading and suggested the use of rehabilitation in nonoperative management of patients with RCTs. In the current study, we identified superior shift of the humeral head with SS lesions alone at some testing positions, but found that combined SS and infraspinatus tears resulted in superior translation during all but 1 testing condition at 0 abduction. SS tears alone also had minimal effect on glenohumeral joint forces and acromiohumeral contact pressures, but combined tears resulted in decreased glenohumeral joint forces and increased acromiohumeral contact pressures, which had previously not been measured and only assumed secondary to superior migration. The change in glenohumeral joint forces was similar regardless of arm position in the PM/LD unloaded conditions. Acromiohumeral contact pressures were most often elevated in neutral or internal rotation; this is consistent with radiographic studies demonstrating movement of the greater tuberosity directly beneath the acromion with internal rotation.7 We also demonstrated that loading the PM/LD resulted in improved glenohumeral kinematics and resolution of the increased acromiohumeral pressures seen after mRCT, suggesting that rehabilitation of the PM/LD in patients with mRCT may help decrease pressure and slow the progression to CTA. We acknowledge several limitations of this study. The cadaveric nature of the RCT model means that physiologic factors, such as neuromuscular coordination and shoulder

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S.T. Campbell et al. Table II

Compressive glenohumeral joint forcesdpercentage of resultant)

Variable

80 N Deltoid



40 N Deltoid

40 N PM/LD

PM/LD unloaded

40 N PM/LD

PM/LD unloaded

98.9  0.4 98.7  0.4 97.5  0.6y,z

91.3 ± 1.3 88.8 ± 1.8 72.8 ± 6.1y,z

99.7  0.2 99.3  0.3 99.0  0.4

98.7  0.4 97.5  1.0 92.9  2.3y,z

98.8  0.3 98.1  0.4 94.9  1.2y,z

91.2 ± 1.0 90.0 ± 2.2 66.4 ± 6.5y,z

99.6  0.2 99.2  0.3 97.8  1.3

98.8  0.3 97.5  0.9 89.9  2.5y,z

98.5  0.2 98.0  0.3 95.3  1.2y,z

93.8 ± 0.7 90.2 ± 1.2 66.3 ± 8.0y,z

99.6  0.2 99.4  0.2 95.7  1.3y,z

99.0  0.3 97.7  0.7 88.3  2.6y,z

99.6  0.1 99.6  0.2 99.3  0.2z

97.1 ± 0.4 96.3 ± 0.5 92.4 ± 0.9y,z

99.8  0.1 99.6  0.2 99.5  0.1

99.2  0.2 99.3  0.1 97.9  0.5y,z

99.3  0.2 99.3  0.2 98.4  0.4y,z

97.0 ± 0.5 96.0 ± 0.5 89.7 ± 1.4y,z

99.8  0.1 99.6  0.1 99.7  0.1

99.2  0.2 99.1  0.3 95.4  1.3y,z



0 Abduction, 60 ER Intact SS tear mRCT 0 Abduction, 0 rotation Intact SS tear mRCT 0 Abduction, 30 IR Intact SS tear mRCT 60 Abduction, 90 ER Intact SS tear mRCT 60 Abduction, 30 ER Intact SS tear mRCT

ER, external rotation; IR, internal rotation; mRCT, massive rotator cuff tear; PM/LD, pectoralis major/latissimus dorsi; SS, supraspinatus. ) Data are expressed as mean percentage of resultant (%)  standard error of the mean. The boldface data represent a significant difference (P < .05) between the PM/LD loaded and unloaded conditions under equivalent deltoid loads. y Significantly different (P < .05) from intact under same loading conditions. z Significantly different (P < .05) from SS tear under same loading conditions.

pain, that may play a role in glenohumeral biomechanics after mRCT in patients could not be studied. In addition, the testing system was not capable of reproducing scapulothoracic motion, meaning that the movement permitted by our system represented a simplified version of true in vivo scapular motion. Also, although resection of the capsule allowed for isolated evaluation of the cuff muscles and the PM/ LD at the various positions tested, it also represented a simplification of the in vivo state. However, testing was not performed in certain positions (maximum internal or external rotation) at which the lack of a capsule might dramatically alter joint biomechanics from the in vivo state. Our study did not attempt to evaluate deficiency of the subscapularis or the effect of PM/LD loading in the absence of subscapularis function because we chose to focus on loading/unloading of the humerothoracic musculature. Previous biomechanical work by Werner et al30 evaluated the effect of subscapularis loading on cadaveric specimens that underwent LD transfer after the creation of a mRCT. That study showed significantly altered humeral head translation and rotation when the subscapularis was not loaded, especially in the neutral and abducted/externally rotated positions.30 Clinical studies have corroborated this conclusion, including a study by Gerber et al10 that demonstrated no clinical improvement after tendon transfer in patients with a subscapularis deficiency. Future studies evaluating the role of the subscapularis in massive cuff tears

and its contribution to the prevention of CTA are indicated, especially given its previously demonstrated importance in the setting of LD transfer. Another limitation of our study is that loading of the PM/LD was done in combined fashion; controlling the load of these muscles individually in future studies may provide valuable information regarding their individual role in the prevention of CTA. Future work could also include an evaluation of the teres major because it has a similar orientation and function. Finally, RCTs in this study were created in a controlled environment with surgical tools. This is not the mechanism of injury causing RCTs in patients, and these laboratorygenerated lesions may not have been completely accurate representations of patient pathology.

Conclusion In this biomechanical model, SS tears alone produced superior translation of the humeral head at some shoulder positions. When a massive tear was created, this superior translation increased, and increases in superior glenohumeral joint forces and acromiohumeral pressures were also observed. Loading of the PM and LD muscles resulted in improved glenohumeral kinematics and joint forces and decreased acromiohumeral

Pectoralis and latissimus in cuff tear pressures. These findings may lend weight to previous literature suggesting that treatment focusing on rehabilitation of this musculature may decrease acromiohumeral contact pressures in patients with mRCTs and may help in delaying the progression to CTA.

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Disclaimer

15.

Funding was provided by Veterans Affairs Rehabilitation Research and Development Merit Review. The funding source did not play a role in the investigation. The authors, their immediate families, and any research foundations with which they are affiliated have not received any financial payments or other benefits from any commercial entity related to the subject of this article.

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The role of pectoralis major and latissimus dorsi muscles in a biomechanical model of massive rotator cuff tear.

Superior migration of the humeral head after massive rotator cuff tear (mRCT) is thought to lead to cuff tear arthropathy. Previous biomechanical stud...
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