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From the * Department of Radiology, Wright-Patterson Air Force Base, Ohio, the
Department of Radiology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma,
National Musculoskeletal Imaging, Weston, Florida, the
Department of Orthopaedic Surgery & Rehabilitation, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma, the || Department of Radiology, Lackland Air Force Base, Texas, and the ¶ Department of Pathology, University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma
# Address correspondence to Charles B. Pasque, MD, Department of Orthopaedic Surgery and Rehabilitation, University of Oklahoma Health Sciences Center, PO Box 26901, Oklahoma City, OK 73190 (e-mail: charles-pasque{at}ouhsc.edu).
| ABSTRACT |
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Hypothesis: There is no separate identifiable transverse humeral ligament, but rather the fibers covering the intertubercular groove are composed of a sling formed by fibers from the subscapularis and supraspinatus tendons.
Study Design: Descriptive laboratory study.
Methods: A total of 14 shoulder examinations were performed on 7 matched pairs of fresh-frozen cadaveric shoulders. Magnetic resonance imaging scans were performed, followed by gross and microscopic anatomical dissection.
Results: In the location of the transverse humeral ligament, magnetic resonance imaging and gross dissection revealed the continuation of superficial fibers of the subscapularis tendon from the tendon body across the intertubercular groove to attach to the greater tuberosity, whereas deeper fibers of the subscapularis tendon inserted on the lesser tuberosity. Longitudinal fibers of the supraspinatus tendon and the coracohumeral ligament were also noted to travel the length of the groove, deep to the other interdigitating fibers but superficial to the biceps tendon. Histologic studies confirmed these gross dissection patterns of fiber attachment and also revealed the absence of elastin fibers, which are more commonly seen in ligamentous structures and are typically absent from tendinous structures.
Conclusion: There is no identifiable transverse humeral ligament, but rather the fibers covering the intertubercular groove are composed of a sling formed mainly by the fibers of the subscapularis tendon, with contributions from the supraspinatus tendon and the coracohumeral ligament.
Clinical Relevance: According to our findings, dislocations of the long head of the biceps must disrupt at least the deep fibers of the annular sling created mainly by the subscapularis tendon insertion. This finding provides anatomical support for the findings of a positive biceps tendon subluxation or dislocation and subscapularis tear during glenohumeral arthroscopy with a normal-appearing subscapularis during open surgery or subacromial arthroscopy.
Key Words: transverse humeral ligament subscapularis tears biceps tendon dislocation
| INTRODUCTION |
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Meyer9 was the first to challenge the perceived function of the THL. He made 2 key observations based on 286 cadaveric dissections of the shoulder. First, he noted that in those shoulders with biceps tendon dislocation, the tissue described as the THL was actually intact. Second, he noticed that the dislocation of the biceps was consistently medial, either underneath or into the substance of the sub-scapularis tendon. More recently, Slatis and Aalto14 have suggested that the disruption of the coracohumeral ligament is a prerequisite for dislocation of the long head of the biceps tendon. Despite these contentions, anatomical studies continue to identify the THL as a distinct entity, but none of them has isolated the THL as a separate histologic entity and defined it in relationship to the biceps tendon and the rotator cuff interval.1,3
Dislocations of the long head of the biceps tendon have been described since the 17th century,4 but their exact mechanism of injury and their association to the rotator cuff tendon are controversial. For example, many authors report concomitant rotator cuff tendinopathy.2,8,9,14 However, ODonoghue10 and Railhac et al13 suggest that dislocations of the biceps tendon may occur without associated abnormalities in the rotator cuff. A subject of even more debate is the relationship of the biceps tendon dislocation to the subscapularis tendon. Hitchcock and Bechtol,8 De Palma,6 and Slatis and Aalto14 describe the biceps tendon as dislocating over the subscapularis tendon. In contrast, Meyer,9 Petersson,12 Collier and Wynn-Jones,2 and Patte et al11 describe the biceps tendon as dislocating either into or under the subscapularis tendon. Many of the dislocations into the subscapularis tendon have been described as "hidden," secondary to an intact anterior fibrous fascia that gives the impression of normal anatomy. To identify this type of biceps tendon dislocation, it is most often necessary to incise this anterior fibrous fascia, which extends from the subscapularis tendon to the bicipital groove.15
Despite the controversies, no study to date has isolated the anatomical nature of the THL and its relationship to the biceps tendon and the anterosuperior portion of the rotator cuff. The purpose of this study was to identify these relationships utilizing radiographic, gross dissection, and histologic studies.
| MATERIALS AND METHODS |
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The shoulders initially underwent MRI examination. All images were acquired on a Signa 1.5-T scanner (General Electric Medical Systems, Milwaukee, Wis). The MRI protocols used a head coil to image the cadaveric shoulders. Axial T1-weighted images were obtained (repetition time, 400 milliseconds; echo time, 11 milliseconds). The field of view was 14 x 14 cm, and the slice thickness was 3 mm with a 1-mm interslice gap. The matrix size was 512 x 256 with 3 excitations. Axial 3-dimensional spoiled gradient images were also obtained (repetition time, 10 milliseconds; echo time, 2.5 milliseconds) with a flip angle of 20°. The field of view was 18 x 18 cm, and the slice thickness was 2 mm with no interslice gap. The matrix was 256 x 256 with 3 excitations. After radiographic examination, 3 experienced musculoskeletal radiologists read the images (Figures 1
and 2
).
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In 7 shoulders, a humeral osteotomy was performed at the inferior edge of the subscapularis tendon. The entire greater tuberosity, lesser tuberosity, bicipital groove, and rotator cuff insertions were then excised en masse.
The long head of the biceps tendon was transected at its origin on the supraglenoid tubercle and distally at the musculotendinous junction. This dissection technique allowed the biceps tendon to maintain its position in the bicipital groove. The specimens were subsequently placed in 10% neutral buffered formalin.
The humeral head and associated soft tissue were then cut axially with a band saw into 3- to 4-mm-thick sections. These sections were decalcified overnight in a 1:1 mixture of 10% neutral buffered formalin and 10% hydrochloric acid. The softened tissue was submitted for routine tissue processing (dehydration with alcohol followed by clearing with xylene and embedding in paraffin). Five-µm sections were cut from the block and stained with Harris hematoxylin and eosin-Y or Masson trichrome and Verhoeff stain for elastin fibers. Elastin is typically absent from tendinous structures and more commonly seen in ligamentous structures.
In the other 7 shoulders, the common rotator cuff tendinous insertion was carefully dissected free from the underlying humeral tuberosities. Of those specimens, 5 were sectioned transversely at multiple levels along the bicipital groove. The remaining 2 specimens were coronally sectioned from superficial to deep in the rotator interval tissue that overlies the bicipital groove. Again, this tissue was placed in 10% neutral buffered formalin and subsequently processed for hematoxylin and eosin or Masson trichrome staining and Verhoeff stain for elastin fibers. The principal authors and a pathologist examined all histologic slides.
| RESULTS |
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Gross Dissection
Of 14 cadaveric shoulders, 13 showed no obvious rotator lesions after dissection of the superficial muscle layers. A single specimen revealed a large crescent-shaped tear in the anterior portion of the supraspinatus tendon near the insertion of the tendon on the greater tuberosity. The remaining 13 specimens revealed no evidence of gross rotator cuff abnormalities. The biceps tendons were clearly visible coursing over the humeral head and within the bicipital groove. No medial or superficial dislocation of the biceps tendon was identified within the shoulders examined. One specimen demonstrated a complete rupture of the biceps tendon. The tendon was absent from the supraglenoid tubercular attachment proximal to the distal portion of the bicipital groove. The remaining tendon was adherent to the anterior portion of the proximal humerus in this location, an appearance consistent with autotenodesis.
Dissection under loupe magnification and removal of loose areolar tissue revealed the continuation of superficial fibers from the subscapularis tendon extending over the lesser tuberosity to the greater tuberosity at the level of the intertubercular groove. This finding was corroborated by the axially sectioned humeral head specimens that showed the subscapularis tendon attachment to the humeral head (Figure 3
).
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In those specimens with intact osseous structures, transverse sectioning at the level of the intertubercular groove revealed a separation of the fibers of the subscapularis tendon at the medial edge of the bicipital groove. The deep subscapularis fibers inserted onto the lesser tuberosity and formed a fibrous floor in the bicipital groove. Superficial fibers of the subscapularis tendon extended superficially over the biceps tendon body across the groove and inserted onto the greater tuberosity. We did not find a separate anatomical structure traversing the bicipital groove in any anatomical specimen.
A characteristic shape of the fibroosseous bicipital groove was noted consistently in each of the 14 shoulders. The groove appeared teardrop shaped, with the apex directed medially into the substance of the subscapularis tendon. The biceps tendon was covered by the fibrous tissue from the overlying subscapularis tendon and from the anterior portion of the supraspinatus tendon (Figure 4
). The deep fibers were consistently thicker in appearance on both MRI and histologic sections, but this finding was not specifically quantified. Regarding the vertical length of the subscapularis tendon, 100% of the subscapularis tendon insertion was involved in the covering of the bicipital groove.
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In 10 of the 12 axially cut specimens, the collagen fibers that were continuous with the subscapularis tendon split into 2 groups of fibers just before reaching the lesser tuberosity. The most superficial collagen fibers continued over the biceps tendon as it passed through the intertubercular groove and terminated onto the greater tuberosity. The deeper fibers of the subscapularis tendon passed medial to the long head of the biceps tendon and terminated some of the fibers onto the lesser tuberosity. A thin layer of this insertional footprint of fibers continued around the biceps tendon and covered the floor of the bicipital groove. These fibers then inserted onto the lateral border of the bicipital groove (Figure 4
).
The specimens that were cut coronally showed an abundant amount of interdigitation between the superficial layers of the subscapularis tendon and contributions of the supraspinatus tendon and the coracohumeral ligament within the rotator interval and proximal bicipital groove.
The remaining 2 cases fit into indeterminate patterns. The true anatomy of these samples could not be accurately assessed because of poor orientation of the tissue or the lack of the full anatomical structure present on the slide. The slides in this category were either dissected off the humerus or previously injured. The architecture could not be determined because of the formation of adhesions and scar tissue that caused distortion of the fibrous tissue in the region of interest.
All of the cases had slides stained with an elastin stain (Verhoeff method for elastin fibers). Verhoeff staining consistently showed the absence of elastin fibers, which are more commonly seen in ligamentous structures and are typically absent in tendinous structures (Figure 5
).
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| DISCUSSION |
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The most remarkable finding of this study was the lack of an identifiable structure that could be defined as the THL as it has been depicted in previous anatomical descriptions. Neither cadaveric MRI or histologic sectioning revealed a distinct structure that inserted onto both borders of the intertubercular groove, covering the biceps tendon. Rather, superficial collagen fibers from the subscapularis tendon continued over the biceps tendon and inserted onto the greater tuberosity, whereas deep fibers from the subscapularis tendon inserted onto the lesser tuberosity just medial to the long head of the biceps tendon. Fibers originating from the subscapularis tendon also were seen to be present along the floor of the intertubercular groove and inserting onto the lateral rim of the inter-tubercular groove and greater tuberosity, thereby creating a sling of tissue around the biceps tendon. In addition, there were fibers found proximally within the rotator cuff interval that originated from the superficial fibers of the supraspinatus tendon. These fibers interdigitated with the superficial fibers of the subscapularis tendon and the coracohumeral ligament to help form the roof of the proximal intertubercular groove. This anatomical relationship has been previously described by Clark and Harryman,1 in their discussion of the distinct morphologic zones at the tendinous insertion of the rotator cuff tendons. Interestingly, we found a histologic pattern in the subscapularis tendon insertion onto the greater tuberosity that looks very similar to their histologic findings of the supraspinatus tendon insertion onto the greater tuberosity.
The true benefit of this study is that it gives anatomical support to clinical observations that have been made throughout the literature regarding the THL and its association to biceps tendon subluxation or dislocation. Meyer9 was the first to question the THLs purported role as securing the biceps tendon in the bicipital groove.(p498) Slatis and Aalto14 provided further evidence that the coracohumeral ligament and the superior glenohumeral ligament may be more important stabilizers of the biceps tendon.
The key to Meyers observation was that he noted dislocations of the biceps tendon occurring either underneath or into the substance of the subscapularis muscle.9 Many subsequent studies have confirmed this observation.2,11,12,15 Walch et al15 commented that in the large majority of biceps dislocations, "intact anterior fibrous fascia was observed extending from the subscapularis tendon to the bicipital groove giving the impression of normal anatomy."15 Our study provides an anatomical explanation for this pattern of dislocation by describing the anatomical nature of the biceps sling. Our results show that fibers from the subscapularis tendon divide and form an annular sling around the biceps tendon. The biceps tendon lies within a groove that is teardrop shaped, with its apex directed medially. Furthermore, gross dissection of the subscapularis tendon insertion off the lesser tuberosity is performed more easily when compared with dissection off the greater tuberosity insertion. In biceps dislocation, the deep fibers from the subscapularis tendon would tend to avulse more easily, allowing for dislocation of the biceps tendon into the joint. This anatomical description helps support the common arthroscopic findings of a positive biceps tendon subluxation or dislocation during the glenohumeral arthoscopic examination, in association with a normal-appearing subscapularis tendon during the subacromial arthroscopic examination.
The association of biceps tendon dislocation with rotator cuff injury is not new to the orthopaedic literature. Walch et al15 reported that in their cohort of patients, "subluxation of the biceps tendon [was] always associated with a minor lesion of the subscapularis and in most cases with rupture of the supraspinatus tendon."(p108) This association, however, is not universally accepted. For example, ODonoghue10 and Railhac et al13 contended that there could be isolated dislocations of the biceps tendon without concomitant lesions of the rotator cuff. Our findings challenge this contention and support the notion that to subluxate or dislocate the long head of the biceps tendon, there must be injury to what we refer to as "the biceps sling" annular fibers, which originate from the subscapularis tendon and receive contributions from the supraspinatus tendon.
Our anatomical study provides substantial support for the integral relationship between the biceps and subscapularis tendons. It also supports the findings that with biceps tendon lesions, a high index of suspicion should be raised for a concomitant subscapularis tendon tear and injury to the rotator cuff interval. By understanding this association, earlier diagnosis and treatment may be accomplished.
| FOOTNOTES |
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| REFERENCES |
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This article has been cited by other articles:
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D. Maier, M. Jaeger, N. P. Suedkamp, and W. Koestler Stabilization of the Long Head of the Biceps Tendon in the Context of Early Repair of Traumatic Subscapularis Tendon Tears J. Bone Joint Surg. Am., August 1, 2007; 89(8): 1763 - 1769. [Abstract] [Full Text] [PDF] |
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