2 ANATOMY

2.1 The subscapular nerves are anatomical constraints to circumferential release of the subscapularis muscle1

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Ariane Gerber, MD, Stefan Greiner, MD

Investigation performed at the Center for Musculoskeletal Surgery, Charité-Universitätsmedizin, Berlin, Germany

2.1.1 Introduction

Circumferential mobilization of the subscapularis muscle is an important step in reconstructive shoulder procedures, like repair of subscapularis or anterosuperior rotator cuff tears, shoulder arthroplasty, revision instability surgery or open capsular release. The subscapularis muscle is shortened in such pathologies due to chronic rupture of the tendon or longstanding limitation of external rotation. In absence of advanced degenerative muscle changes, circumferential release of adhesions and mobilisation of the subcapularis is considered as an essential surgical step for direct repair.1 The mobilization of the muscle includes release of adhesions at the upper border of the muscle, at the anterior surface between the conjoined tendon and the muscle, and along the scapular neck at the posterior surface of the muscle.2

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The anatomic description of the subscapular nerves has been subject of several cadaveric studies.3-7 Most of them are concentrating on detailled description of the subscapularis innervation without considering their surgical relevance. Checchia et al. and Yung et al. have been the first to describe the surgical anatomy of the subscapular nerves. 6 ,7 In shoulders with an intact subscapularis tendon they reported on the location of the subscapular nerves relative to the glenoid rim and showed that the nerve branches are at risk when the arm is externally rotated.

None of the studies mentioned above has described the position of the subscapular nerves after circumferential release and lateral mobilization of the subscapularis tendon.

It was the first objective of this study to evaluate the influence of subscapularis release and lateral traction on the postion of the subscapularis nerves relative to the coracoid process. And the second purpose was to define surgical guidelines to avoid injury of the neurovascular supply to the subscapularis muscle during release.

2.1.2 Material and Methods

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Fifteen fresh frozen human cadaveric shoulders were thawed at room temperature for dissection. None of the donors had suffered rotator cuff pathology or had had previous injuries or surgical procedures performed on the shoulder joint. The skin was removed circumferentially and the deltopectoral interval identified. To expose the proximal third of the humerus, the deltoid muscle was detached from the clavicle and the anterolateral acromion. The tendon of the pectoralis major was identified and dissected sharply from the humeral shaft. Then the pectoralis major was dissected up to the clavicule and the pectoralis minor tendon was detached from the coracoid. To expose the infaclavicular portion of the brachial plexus, the neurovascular pedicles to the pectoralis major and minor muscles were sectioned. Then the medial border of the conjoined tendon was dissected and the musculocutaenous nerve identified. The conjoined tendon was detached from the coracoid and the musculotendinous unit removed after the musculocutaneous nerve had been sectioned at its entry point into the muscle.

In a next step attention was turned to the posterior part of the plexus. The dissection was performed from lateral to medial identifying and preserving every vascular and neural structures entering the subscapularis muscle. Then the subscapular nerves were dissected from the posterior part of the plexus and it became possible to record the number of branches including their ramifications and to mark the penetration area of each branch into the subscapularis muscle.

The rotator interval was identified and opened to visualize the upper border of the subscapularis and the base of the coracoid. A suture was fixed at the lateral border of the base of the coracoid and tightened inferiorly following the medial border of the scapula . Starting from the same point at the basis of the coracoid a second suture was placed perpendiculary to the first suture.

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With the arm held in neutral position the vertical and horizontal distances between the lateral border of the base of the coracoid and the entry point of the subscapular nerves into the subscapularis muscle were measured using the two sutures as reference axis.

Finally the tendon of the subscapularis was detached from the lesser tuberosity and braided sutures were passed through the edge of the tendon in a modified Mason-Allen stich configuration. Using the sutures the tendon was pulled anteriorly to expose the articular part of the subscapularis muscle. The joint capsule was incised at the level of the labrum from the upper to the lower border of the subscapularis, simulating a circumferencial release. Then the tendon was pulled laterally and the horizontal and vertical distances between the lateral border of the coracoid and subscapular nerves were recorded as described above .

2.1.3 Results

In all shoulders an upper, middle and inferior subscapular nerve branches could be identified. The nerve branches arose from the posterior cord of the brachial plexus in all shoulders with one exception. For this specimen, the inferior subscapular branch arose directly from the axillary nerve.

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Figures 2a and 2b show the distribution of the subscapular nerve branches for all specimens and their relative position according to the lateral border of the coracoid before and after release of the subscapularis.

Figure 2a: Distribution of the nerve entry points before release of the subscapularis with the arm in neutral rotation. Red points: upper subscapular nerve branches; green points middle subscapular nerve branches; blue points lower subscapular nerve branches. Star:base of the coracoid process.

Figure 2b: Distribution of the nerve entry points after release of the subscapularis and lateral traction on the tendon. Red points: upper subscapular nerve branches; green points middle subscapular nerve branches; blue points lower subscapular nerve branches. Star:base of the coracoid process.

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Table I below gives an overview of the measured distances for each group of nerve branches.

The mean horizontal distance between the lateral border of the coracoid and the most lateral ramification of the upper subscapular nerve group was 40.1 mm ± SD 9.2 mm (ranging from 25 mm to 55 mm) with the arm in neutral rotation. When the subscapularis was pulled laterally after release, the mean distance between the most lateral nerve branch and the lateral border of the coracoid process was 25.1 mm ±SD 9.0mm (ranging from 5 mm to 40 mm). This was significantly shorter than before the release (p<0.0001).

TABLE I: Overview of the mean horizontal and vertical distances between the lateral border of the coracoid and the entry point of the subscapularis nerve branches into the suscapularis muscle

HORIZONTAL DISTANCE

VERTICAL DISTANCE§

Neutral rotation, subscapularis intact

Neutral rotation, subscapularis detached, released and pulled laterally

 

 

Mean±SD (mm)

Range (mm)

Mean±SD (mm)

Range (mm)

P value*

Mean±SD (mm)

Range (mm)

Upper subscapularis branch

40.1±9.2

25-55

25.1±9.0

5-40

<0.0001

10.6±5.0

2-25

Middle subscapularis branch

45.3±7.7

40-60

29.9±5.6

20-40

<0.0001

26.0±7.8

15-45

Lower subscapularis branch

45.2±10.9

35-80

30.0±6.5

15-45

<0.0001

46.3±8.6

34-62

* Determined with the Student t-test for paired correlated groups
§ No difference could be measured for the vertical distance before and after release with lateral mobilization of the subscapularis muscle

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The mean horizontal distance between the lateral border of the coracoid and the most lateral ramification of the middle subscapular nerve group was 45.3 mm ± SD 7.7mm (ranging from 40 mm to 60 mm) with the arm in neutral rotation. When the subscapularis was released and pulled laterally this distance decreased to 29.9 mm ±SD 5.6mm (ranging from 20 mm to 40 mm) and this was significantly shorter than prior the release (p<0.0001).

The mean horizontal distance between the lateral border of the coracoid and the most lateral ramification of the lower subscapular nerve group was 45.2 mm ±SD 10.9 mm (range from 35 mm to 80 mm) with the arm in neutral rotation When the subscapularis was pulled leaterally this distance was 30.0 mm ±SD 6.5 (ranging from 15 mm to 45 mm) and this was again significantly shorter than prior the release (p>0.0001).

No difference could be measured before and after release with lateral mobilization of the subscapularis muscle. The mean vertical distance between the lateral border of the coracoid and the entry point of the most lateral ramification of the subscapular nerve branches was 10.5 mm ± SD 5.0 mm (range from 2 mm to 25 mm) for the upper subscapular nerve branch, 26.0 mm ± SD7.8 mm (range 15 mm to 45 mm) for the middle branch, and 46,3 mm ± SD 8.6 mm (range from 34 mm to 62 mm) for the lower branch.

2.1.4 Discussion

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Although the descriptive anatomy of the subscpular nerve branches was registrated during dissection, the main purpose of this study was to define surgical guidelines to avoid iatrogenic denervation of the subscpularis muscle during mobilization of the musculotendinous unit.

The position of the susbcapular nerve branches relative to selected anatomical landmarks has been described previously.3-7 However only few of the points used as reference for measurements are easy to identify when performing a deltopectoral approach.

In their studies Checcia et al. and Yung et al. proposed the use of the glenoid rim as reference to localize the subscapular nerves. 6 ,7 Although the rim can be palpated through the subscapularis muscle during release at its anterior surface, direct visualization is not possible. This renders the intraoperative localisation of the nerves difficult.

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In the present study the basis of the coracoid process was used as a reference to localize the subscapular nerve branches. As the release of the coracohumeral ligament is required when the subscapularis tendon is mobilized, the lateral border of the base of the coracoid can be seen easily.

The influence of the position of the arm has been shown to influence the relative localisation of the subscapular nerves. 6 ,7. In general, circumferential subscapularis release is required when the tendon is torn and retracted. Thus the influence of the rotation of the arm is only of theoretical value only. During subscapularis repair, dissection of adhesions at the anterior surface of the subscapularis is usually performed after sutures have been passed through the tendon and the muscle-tendon unit is pulled laterally. Although tissue quality in fresh frozen cadavers is inferior to well vascularised and innervated muscle, the design of the present study gave a better basis to simulate the conditions in vivo.

The present data have shown that all superior nerve branches were located within a range 2.5 cm vertical distance below the base of the coracoid process. Within this vertical distance, there was a 95% probability to find upper subscapular nerve branches beyond a 2 cm distance medially (horizontal disctance) from the lateral border of the base of the coracoid process before release of the subscapularis tendon and with the arm held in neutral rotation. After circumferential release and with lateral traction on the tendon, the average distance between the superior nerve branches and the lateral border of the base is decreased significantly from 4.0 to 2.5 cm (p<0.0001). Accordingly there was a 95 % chance to find a nerve branche 0.5 cm medially from the lateral border of the base of the coracoid.

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The middle nerve branches were located between 1.5 cm and 4.5 cm below the base of the coracoid process. Although they entered the muscle more medially than the superior branches, the probability to find a middle branch 2 cm medially from the lateral border of the coracoid process was 95% when the muscle was pulled laterally. Based on this analysis, there is a risk of nerve injury within the „safe harbor“ defined by Yung et al. 7

Based on the present study, the risk to injure the lower subscapular nerves seems to be relatively low. One reason is that the nerve branches entered the muscle more medially (average distance 4.5 cm before and 3 cm after release) than the upper and middle nerve branches. Furthermore the inferior nerve branches were found within a distance between 3.5 cm and 6 cm, which corresponds to the lower border of the glenoid. As the axillary nerve is usually localised and protected at this level during surgery, it is unlikely to injure the lower subscapular nerve branches when releasing the anterior surface of the subscapularis.

In conclusion, their is a high risk for denervation of the upper part of the subscapularis muscle when release is performed underneath the conjoined tendon beyond the coracoid base and within a distance reaching from the base of the coracoid base to the axillary nerve. This is especially true when the subscapularis tendon is pulled laterally.

2.1.5 References

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1. Gerber C, Hersche O, Farron A. Isolated rupture of the subscapularis tendon. J Bone Joint Surg Am 1996 ;78:1015 -23.

2. Cleeman E, Brunelli M, Gothelf T, Hayes P, Flatow EL. Releases of subscapularis contracture: an anatomic and clinical study. J Shoulder Elbow Surg 2003 ;12:231 -6.

3. Kerr A. The brachial plexus of the nerves in man. Am J Anat 1918 ;1:285 -395.

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4. Kato K. Innervation of the scapular muscles and its morphological significance in man. Anat Anz 1989 ;168:155 -68.

5. McCann P, Cordasco FA, Ticker JB, Kadaba MP, Wootten ME, April EW, Bigliani L. An anatomic study of the subscapular nerves: A guide for electromyographic analysis of the subscapularis muscle. J Shoulder Elbow Surg 1994 ;3:94 -9.

6. Checchia SL, Doneaux P, Martins MG, Meireles FS. Subscapularis muscle enervation: the effect of arm position. J Shoulder Elbow Surg 1996 ;5:214 -8.

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7. Yung SW, Lazarus MD, Harryman DT, 2nd. Practical guidelines to safe surgery about the subscapularis. J Shoulder Elbow Surg 1996 ;5:467 -70.

2.2 Selective reconstruction of the lower subscapularis with the teres major. Anatomical basis for a new tendon transfer2

Ariane Gerber, MD

Investigation performed performed at the Center for Musculoskeletal Surgery, Charité-Universitätsmedizin, Berlin

2.2.1 Introduction

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There is no optimal tendon transfer procedure for treatment of irreparable subscapularis tears.

The idea to reconstruct the lower part of the subscapularis muscle with a teres major transfer is based on the following considerations. In his analysis of segmental innervation of the scapular muscles, Kato postulates that formation of the subscapularis muscle out of the cervical myotmes derives from 3 components of the muscle mass.1 The larger portion, which is supplied by the superior and middle subscapular nerves forms the thoracal subscapularis muscle. The component supplied by the lower subscapular nerve, divides into a cranial and caudal portion. The cranial portion forms the lower or axillary subscapularis muscle, whereas the caudal portion becomes the teres major. Finally the third part of the subscapularis is formed by the mass is supplied by the axillary nerve. Most of the third part of the mass shifts on the dorsal side of the scapula and become the teres minor and the deltoideus muscles. Electromyographic analysis could confirm that the subscapularis muscle is composed by two functional units 2, the thoracal and the axillary parts. Based on the fact that the teres major and the axillary subscapularis belongs to the same functional unit and knowing that the pectoralis major transfer does not reproduce the force vector of the subscapularis optimally, the teres major turns out to be an attractive alternative for subscapularis reconstruction.

The objective of this study was to evaluate the surgical anatomy of the teres major and its potential value as a transfer for reconstruction of the lower portion of the subscapularis muscle.

2.2.2 Material and Methods

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Sixteen fresh frozen human cadaveric shoulders without pathology or previous surgical intervention were selected for dissection and thawed at room temperature. The skin was removed circumferentially and the deltopectoral interval identified. The deltoid was detached from the clavicle, the anterolateral acromion and it was partially detached from its humeral insertion to expose the proximal third of the humerus. The tendon of the pectoralis major was identified and dissected sharply from the humerus. Then the pectoralis major and pectoralis minor mucles were dissected carefully from the underlying structures to expose the infaclavicular portion of the brachial plexus. Care was taken not to injure the underlying neurovascular structures. Only the neurovascular pedicles to the pectoralis major and minor muscles were sectioned to facilitate exposure. The medial border of the conjoined tendon was dissected and the musculocutaenous nerve identified. Then the conjoined tendon was detached from the coracoid and the musculotendinous unit removed after the musculocutaneous nerve had been sectioned.

Attention was then turned to the humeral insertion of the latissimus dorsi muscle. The interval between the latissimus tendon and the teres major tendon was dissected. The width of the latissimus dorsi tendon at its insertion was measured. Furthermore the pattern of overlap between the latissimus tendon and the underlying teres major tendon was described. The latissimus dorsi tendon was detached from the humeral shaft, and sutures were passed through the tendon to retracted the muscle-tendon unit medially. After the width of the exposed teres major tendon was measured, it was sharply detached from the bone and tagged with three sutures using a modified Mason-Allen stitch.3

The next steps of dissection were directed to the identification of the neurovascular supply to the teres major. Whereas the muscle was pulled laterally, the dissection was carried on medially, identifying and preserving every vascular and neural structures entering the muscle. The entry point of each identified pedicle into the muscle was marked and the vascular anatomy was classified according to Mathes and Nahai.4. The distance between each pedicle and the lateral edge of the tendon was measured. To describe their topographic relationship within the brachial plexus, the pedicles were dissected and followed proximally.

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Before the teres major was transferred to the lesser tuberosity, all adhesions between the latissimus dorsi and the teres major were released to optimize the availble excursion of the muscle. The axillary nerve was identified and marked with a loop. Using a transosseous fixation technique, the teres major was fixed to the lesser tuberosity. After the latissimus dorsi was sawed back to the humeral shaft , the arm was moved at the end range of all physiologic postions and the relationsship between the axillary nerve and the upper border of the transferred teres major was recorded.

2.2.3 Results

2.2.3.1 Vascular supply

In 14 specimens the vascular supply to the teres major was based on one main pedicle (Type I according to Mathes and Nahai). In two specimens there were one main pedicle plus one minor pedicle (Type II according to Mathes and Nahai).

The main pedicle entered the muscle at its anterosuperior surface at an average distance of 68 mm ± SD 6 mm (range, from 55 mm to 80 mm) from the lateral edge of the tendon.

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The main vessel to the teres major was a branch of the thoracodorsal artery in 11 shoulders. (Fig.1) In 4 specimens the vessel arose from the circumflex scapular artery and in one case the vessel was a branch of the subscapular artery. The main pedicle was more than 2 mm in diameter in all cadavers.

Considering the secondary pedicles, they were located between the main vessel and the humeral insertion of the tendon at 30mm and 50 mm respectively. One of these minor pedicles arose from the thoracodorsal artery and was less than 1mm in diameter. The other was a branch of the subscapular artery and was also less than 1 mm in diameter.

Figure 1: Anterior view of a right shoulder showing the neurovascular pedicle(1) to the teres major(*). The main artery is emerging from the thoracodorsal artery(2) and the innervation comes from the lower subscapular nerve(4). The latissimus dorsi tendon(5) has been detached from the humerus. Thoracodorsal nerve(3).

2.2.3.2 Neural supply

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The nerve supply of the teres major was a branch of the lower subscapular nerve in 15 cases. In one case , innervation was coming directly from the posterior cord. The nerves entered the muscle with the main vascular pedicle in all shoulders. (Fig.1)

2.2.3.3 Description of the latissimus dorsi and teres major tendons

The latissimus tendon showed an average width of 34 mm ± SD 10 mm (range, from 20 mm to 52 mm). The average length of this tendon was 75 mm ± SD 11 mm (range, from 60 mm to 90 mm).

For the teres major tha average width of the tendon was 44 mm ± SD 10 mm (range, from 33 mm to 70 mm) and the average length 31 mm ± SD 7 mm (range, from 15 mm to 40 mm). Tendinous tissue was only found at the ventral surface of the muscle, whereas the posterior surface was muscular and inserting directly to the bone.

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The latissimus dorsi tendon always inserted more laterally on the humeral shaft than the teres major. Between both insertions a bursa was found in all specimens, clearly separating both tendons. More medially the tendons became adherent to each other especially at their inferior edges where the latissimus muscle tendon unit is spinning around the teres major.

Furthermore the relationsship between the latissimus tendon and the teres major tendon at their humeral insertion could be divided in three patterns:

Type I: the latissimus covers the complete teres major tendon

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Type II: the superior edge of the latissimus dorsi tendon inserts at the same level as the superior edge of the teres major, whereas the lower edge inserts more cranially.

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Type III: the superior and lower edges of the latissimus tendon insert more cranially than the superior and lower edges of the teres major.

Configuration I was found in three, configuration II in nine (Fig.2) and configuration III in four specimens.

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Figure 2: Type II pattern where the superior edge of the latissimus dorsi tendon(1) inserts at the same level as the superior edge of the teres major(2), whereas the lower edge inserts more cranially. The lower picture shows the complete teres major insertion(2) after detachment of the latissimus dorsi tendon(1).

2.2.3.4 Transfer of the teres major to the lesser tuberosity

The teres major muscle-tendon unit could be transferred to the lesser tuberosity easily still allowing 30° external rotation of the arm in all cadavers. However this was only possible after complete release of the adhesions between the teres major and the latissimus dorsi. Whereas the dissection plane was well defined superiorly, the muscles where adherent inferiorly. At this level, the radial nerve was approximatively 2 cm from the insertion of the lower insertion of the teres major.(Fig.3) In the transferred position and regardless of the position of the arm, there was no traction either on the vascular pedicle nor on the axillary nerve.

Figure 3: Note the proximity of the radial nerve(1) to the lower border of the teres major tendon(3), when the latissimus dorsi is retracted medially(2). Subscapularis(4), axillary nerve and circumflex vessels(5).

2.2.4 Discussion

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Several studies have analysed the anatomy of the teres major for its use as a tendon transfer for reconstruction of the posterior rotator cuff.5-7 The descriptions are based on a dorsal approach to the shoulder. In the present study the surgical anatomy of the teres major for its use as a transfer for the subscapularis muscle was analysed and was based on a deltopectoral approach.

Furthermore in the present description, the teres major was found to be vascularized by one main pedicle located at an average distance of 7 cm from the lateral insertion of the tendon. This confirms the data published by Wang et al. .5 However it could not be confirmed that the main pedicle of the teres major arises from the circumflex scapular artery. In the present description the artery to the teres major was a branch of the thoracodorsal artery as mentioned by Roswell et al.8

The innervation of the teres major by the inferior subscapular nerve was a constant finding in Kato´s and Wang´s studies1,5 in the same way than in the present report.

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As described earlier5, and confirmed here the tendon of the teres major is relatively short and the tendinous portion of the insertion is only found at the anterior surface of the muscle. When haveresting the tendon for transfer it is essential to preserve the integrity of the tendon to allow secure repair to the lesser tuberosity. Therefore subtile dissection of the latissimus tendon is required.

The present study has shown that the latissimus dorsi most frequently covers the upper edge of the teres major tendon. This renders dissection challenging. At the lower edge there is usually a visible overlap of both tendons which facilitates their separtion. Therefore dissection in a caudocranial direction is recommended .

In all specimens it was technically possible to transfer the teres major to the lesser tuberosity. However dissection of adhesions around the muscle is required to obtain enough excursion. On the superior border of the teres major, dissection is critical due to the proximity of the axillary nerve and posterior circumflex vessels. Furthermore, preparation deeper than 5 cm medially from the lateral edge of the tendon may lead to injury of the main neurovascular pedicle of the muscle. Preparation at the inferior edge of the tendon should be performed after the radial nerve has been identified and protected with a retractor.

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Although the proximalization of the tendon theoretically leads to a narrowing of the quandrangular space, this study suggests that this does not impair the axillary nerve.

On the basis of this anatomical study, the teres major seems to be a reliable and safe muscle for selective reconstruction of the axillary subscapularis.

2.2.5 References

1. Kato K. Innervation of the scapular muscles and its morphological significance in man. Anat Anz 1989 ;168:155 -68.

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2. Kadaba MP, Cole A, Wootten ME, McCann P, Reid M, Mulford G, April E, Bigliani L. Intramuscular wire electromyography of the subscapularis. J Orthop Res 1992 ;10:394 -7.

3. Gerber C, Schneeberger AG, Perren SM, Nyffeler RW. Experimental rotator cuff repair. A preliminary study. J Bone Joint Surg Am 1999 ;81:1281 -90.

4. Mathes SJ, Nahai F. Classification of the vascular anatomy of muscles: experimental and clinical correlation. Plast Reconstr Surg 1981 ;67:177 -87.

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5. Wang AA, Strauch RJ, Flatow EL, Bigliani LU, Rosenwasser MP. The teres major muscle: an anatomic study of its use as a tendon transfer. J Shoulder Elbow Surg 1999 ;8:334 -8.

6. Schoierer O, Herzberg G, Berthonnaud E, Dimnet J, Aswad R, Morin A. Anatomical basis of latissimus dorsi and teres major transfers in rotator cuff tear surgery with particular reference to the neurovascular pedicles. Surg Radiol Anat 2001 ;23:75 -80.

7. Celli L, Rovesta C, Marongiu MC, Manzieri S. Transplantation of teres major muscle for infraspinatus muscle in irreparable rotator cuff tears. J Shoulder Elbow Surg 1998 ;7:485 -90.

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8. Rowsell AR, Davies DM, Eisenberg N, Taylor GI. The anatomy of the subscapular-thoracodorsal arterial system: study of 100 cadaver dissections. Br J Plast Surg 1984 ;37:574 -6.


Footnotes and Endnotes

1  Submitted to J. Shoulder Elbow Surg.

2  Submitted for publication to Surg Rad Anat



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