Abstract
Background
The middle glenohumeral ligament (MGHL) is one of the three ligaments that stabilize the anterior capsule of the shoulder. Recent work suggests that it inserts distally into the deep layer of the subscapularis tendon. The role of the MGHL remains debated. The hypothesis of this study was that the MGHL plays a significant functional role in limiting external rotation of the shoulder while allowing a wide range of motion through its distal insertion into the subscapularis rather than directly onto the humerus.
Methods
In a cadaveric study performed on 20 shoulders (10 subjects), the MGHL and the other anterior structures of the shoulder were successively cut according to a standardized protocol. At each stage, the external rotation range of the shoulder was measured with the arm at the side (ER 1) and in 90° abduction (ER 2) using a goniometer. After dissection, the structure of the MGHL and its distal insertion were analyzed.
Results
Cutting the MGHL led to significant increases in ER 1 but not in ER 2. Shoulder range of motion in ER 1 increased on average by 15 ± 5° (P < .001) after cutting the MGHL and by 21 ± 11° (P < .001) after subscapularis peel. The range of motion in ER 2 increased by 3 ± 4° (P = .048) after cutting the MGHL, by 4 ± 6° (P = .02) after subscapularis peel and by 25 ± 8° (P < .001) after cutting the inferior glenohumeral ligament. The MGHL was present in all dissected shoulders. It was leaf-like in 12 cases, cord-like in 6 cases and had a vestigial appearance in 2 cases. The distal insertion was in all cases in the deep layer of the subscapularis in a thickening of the anterior capsule in the superior part of the muscle, except for two cases in which the tendinous part of the subscapularis was also involved.
Conclusion
The MGHL limited shoulder external rotation by a similar amount as the subscapularis muscle. Further studies are required to understand the clinical relevance of these findings, notably for the treatment of shoulder stiffness.
Keywords: Shoulder, Subscapularis, Biomechanics, Middle glenohumeral ligament, External rotation, Dissection
Introduction
The middle glenohumeral ligament (MGHL) stabilizes the anterior part of the shoulder capsule along with the superior and inferior glenohumeral ligaments (SGHL and IGHL). The MGHL is classically described as inserting proximally on the anterosuperior part of the glenoid labrum and distally on the lesser tuberosity.5,12,16,18
Recent in-vivo arthroscopic observations have offered a more precise description of the MGHL’s anatomy and suggest that it inserts distally into the deep layer of the subscapularis tendon, rather than on the humerus.1,4,9
These studies also highlight the variability of its structure and of its distal insertion.1,4,9Although the role of the IGHL is well-established in anterior glenohumeral instability,2,6,14,22 the MGHL’s function remains unclear.2,22 Some studies suggest it contributes to the anterior stability of the shoulder,2,6,14,22 whereas others highlight its role in limiting external rotation.7,10,14,19,22
The hypothesis of this study was that the MGHL plays a significant limiting role in external shoulder rotation while nevertheless allowing a considerable range of motion through the lack of a direct insertion on the humerus. Our main objective was to quantify the effect of the MGHL in external shoulder rotation. The secondary objectives were to describe the distal insertion and the structure of the MGHL.
Material and methods
The study was approved by the local ethics committee (Conseil d’Orientation Scientifique Ramsay Santé, approval number 00010835, 18 November 2021).
Twenty fresh (nonfrozen and nonembalmed) cadaveric shoulders from 10 whole body cadavers were dissected in September and October 2021 by three surgeons (AW, TD, and MB). Shoulders with severe glenohumeral arthritis, scaring suggestive of surgery, a callus consistent with traumatic injury, or a subscapular tear were excluded.
A protocol was established to investigate the role of the MGHL in external shoulder rotation, with the primary aim of evaluating the effect of isolated section of the MGHL on external rotation. The cadavers were taken out of cold storage (3°C) at least 30 minutes before dissection to limit the effect of temperature on joint range of motion. The shoulders were gently mobilized to eliminate any residual cadaveric stiffness.
The subjects were placed in the beach chair position at 45°. A first set of range of motion measurements was performed before dissection. The dissections followed the usual steps of an anterior deltopectoral approach to the glenohumeral joint:
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Step 1: skin incision and dissection of soft tissue through a deltopectoral approach.
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Step 2: a 1 cm incision in the cranial part of the pectoralis major tendon.
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Step 3: identification of the long head of the biceps tendon in the bicipital groove and extra-articular tenotomy.
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Step 4: subscapularis exposure, opening of the rotator interval, identification and protection of the MGHL, and resection of the rotator interval, including the coracohumeral ligament, up to the glenoid cavity, including the SGHL.
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Step 5: positioning of a double bent Hohmann retractor in the glenohumeral joint to retract the humeral head backward; identification of the MGHL from its medial insertion on the glenoid fossa to its lateral insertion, and sectioning of the MGHL in contact with the glenoid.
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Step 6: subscapularis peel; elevation of the subscapularis (including the anterior capsule) by peeling it away from the lesser tuberosity, starting from the bicipital groove. Identification of the plane between the subscapularis muscle and the IGHL to avoid damaging the latter.
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Step 7: sectioning of the IGHL in contact with the glenoid. IGHL cut in full, from front to back, up to and including the posterior band, under visual control.
Ranges of motion in external rotation were measured manually at each step using a goniometer with the arm at the side (external rotation 1) and in 90° abduction (external rotation 2), at the maximum rotational range without anterior glenohumeral instability (subluxation or dislocation). Measurements were rounded to the nearest 5°. The measurements were performed by two investigators in a blinded manner and the average value was taken.
At the end of each dissection, the MGHL and the distal extremity of the subscapularis were removed by sectioning the subscapularis at the level of the glenoid neck, and the structure of the MGHL and its distal insertion site were analyzed (Fig. 1). The most cranial insertion point was measured with respect to the superior and inferior borders of the subscapularis and the most lateral insertion point was measured with respect to the lesser tuberosity. The structure of the MGHL was described using Collote et al’s classification4 as either leaf-like (if only one border was identifiable), cord-like (if both borders were identifiable), or vestigial.
Figure 1.
Photograph of an anatomical specimen removed at the end of the dissection process: distal subscapularis (SSC) muscle with middle glenohumeral ligament (MGHL).
Statistical analysis
Continuous variables are reported as mean and standard deviation. Univariate analyses were performed with paired t-tests if the data were normally distributed and Wilcoxon signed-rank tests, otherwise. Differences were considered statistically significant at P < .05. All analyses were performed online using EasyMedStat (version 3.13; www.easymedstat.com; EasyMedStat, Levallois-Perret, France).
Results
Eight of the subjects were female and two were male. The mean age at death was 86 years (range, 72-98 years). Rotator cuff tears were observed in ten shoulders: five superior (supraspinatus) tears and five posterosuperior (supra- and infraspinatus) tears. The long head of the biceps tendon was in the bicipital groove in all cases.
External rotation
The main results of the study are summarized in Table I (full sets of measurements in Supplementary Tables S1 and S2). There was no significant difference in terms of initial ER 1 values between shoulders with and without cuff tears (45° vs 49°, respectively). The measured values of ER 1 and ER 2 before dissection and in the first two steps (skin incision and subcutaneous dissection, and partial section of the pectoralis major) were identical in all cases. Increases in ER 1 and ER 2 were observed from steps 3 and 4 onward (Table I).
Table I.
Changes in external rotation with arm at the side (ER 1) and in 90° abduction (ER 2) after each stage of capsular release.
| Dissection | PM incision | LHB section | RI and SGHL section | MGHL section | SSC section | IGHL section |
|---|---|---|---|---|---|---|
| 1 | 70° | 70° | 70° | 85° | 100° | 100° |
| 2 | 40° | 40° | 40° | 50° | 80° | 80° |
| 3 | 45° | 45° | 45° | 70° | 90° | 90° |
| 4 | 45° | 50° | 50° | 60° | 90° | 90° |
| 5 | 40° | 50° | 50° | 75° | 90° | 90° |
| 6 | 45° | 45° | 60° | 75° | 90° | 90° |
| 7 | 45° | 45° | 65° | 80° | 90° | 90° |
| 8 | 60° | 60° | 60° | 80° | 90° | 90° |
| 9 | 30° | 30° | 35° | 50° | 85° | 85° |
| 10 | 30° | 30° | 35° | 45° | 90° | 90° |
| 11 | 50° | 50° | 50° | 60° | 75° | 75° |
| 12 | 50° | 50° | 55° | 65° | 80° | 80° |
| 13 | 40° | 40° | 60° | 70° | 90° | 90° |
| 14 | 40° | 40° | 40° | 50° | 70° | 70° |
| 15 | 50° | 50° | 50° | 70° | 80° | 80° |
| 16 | 50° | 50° | 50° | 65° | 80° | 80° |
| 17 | 40° | 40° | 40° | 50° | 85° | 85° |
| 18 | 40° | 40° | 40° | 50° | 85° | 85° |
| 19 | 60° | 60° | 60° | 80° | 90° | 90° |
| 20 | 60° | 60° | 65° | 80° | 90° | 90° |
| Mean ± SD | 47 ± 10° | 47 ± 10° | 51 ± 11° | 66 ± 13° | 86 ± 7° | 86 ± 7° |
ER, external rotation; PM, pectoralis major; LHB, long head of biceps; RI, rotator interval; SGHL, superior glenohumeral ligament; MGHL, middle glenohumeral ligament; SSC, subscapularis; IGHL, inferior glenohumeral ligament.
Results are reported as mean ± standard deviation (SD).
The range of motion in ER 1 (with the arm at the side) increased in 7/20 shoulders, by 4° ± 7° on average (P = .02) after rotator cuff interval and SGHL section and in all shoulders by 15 ± 5° (P < .001), after MGHL section (Fig. 2; Table I). After subscapularis peel, the range of motion in ER 1 increased in all shoulders and by 21 ± 11° on average (P < .001). Inferior gleno-humeral ligament section had no effect on ER 1 (Table I).
Figure 2.
Box plot of the increase in external rotation range of the shoulder with the arm at the side after section of the middleMGHL and of the SSC, in degrees (°). The difference between the two mean values is of borderline significance (paired t-test, P = .07). MGHL, middle glenohumeral ligament; SSC, subscapularis.
The range of motion in ER 2 (arm in 90° abduction) did not increase after rotator cuff interval and SGHL section, increased in 5/20 shoulders, by 3 ± 4° on average (P = .02), after MGHL section, increased in 7/20 shoulders, by 4 ± 6° on average (P = .01), after subscapularis peel, and increased in all shoulders, by 25 ± 8° on average (P < .001), after IGHL section (Table I). Anterior dislocation or subluxation was systematically observed after subscapularis peel in maximal ER 1, and anteroinferior dislocation was observed in all cases after IGHL section in maximal ER 2. The instability was due to cam impingement of the greater tuberosity with the superior rim of the glenoid.
Anatomical description
The MGHL was present in all shoulders. Its structure was classified as leaf-like in 12 cases, cord-like in 6 cases, and vestigial in 2 cases. A clear distal insertion into the deep layer of the subscapularis in a horizontal thickening of the capsule was observed in all cases. The insertion site was in the upper third or half of the subscapularis muscle, without involving the tendon, in 18/20 cases, and involved the subscapularis muscle and tendon in 2/20 cases.
Discussion
In this group of 10 fresh cadavers, sectioning the MGHL increased the external rotation range of the shoulder with the arm at the side by 15° on average, but there was no clinically significant increase in the external rotation range with the arm in 90° abduction. This supports the hypothesis that the MGHL limits external shoulder rotation, particularly when the arm is placed at the side. In this position, the two main anatomical structures that limit external rotation, are the MGHL and the subscapularis. In 90° abduction, external rotation is only limited by the IGHL.
The effects of MGHL section on shoulder instability and external rotation range have previously been investigated by Turkel et al.22 The smaller increases observed by these authors (+5° on average with the arm at the side, +8° on average in 45° abduction, and +1° on average in 90° abduction) can be explained by their sectioning of the subscapularis muscle before measurements at an unspecified level, the subscapularis, and the MGHL interacting closely as described above. They interpreted the increases as being mainly due to the section of the IGHL, and described the MGHL as being mostly taut with the arm at the side and in 45° abduction. In their cadaveric biomechanical study, Kuhn et al were the first to specifically assess the involvement of the anterior glenohumeral ligaments in limiting external rotation.10 They found that external rotation (ER 1 and ER 2) was mainly limited by the IGHL, with only limited involvement of the SGHL and MGHL (evaluated together). While our results suggest likewise that ER 2 is mainly limited by the IGHL (ER 2 increased by 25° on average after IGHL section), they also indicate, in disagreement with Kuhn et al,10 that the MGHL significantly limits external rotation with the arm at the side while the IGHL does not. Our results are in keeping with those reported by Ferrari,7 O’Connell et al14 and Terry et al19 that the MGHL limits external shoulder rotation with the arm at the side and in moderate abduction (mainly up to 45°).7,14,19 More generally in the literature,7,10,14,19,22 while all authors do not agree on the level of involvement of the MGHL, the general consensus is that it limits external rotation with the arm at the side and at low abduction angles.
Anatomically speaking, we observed in all cases that the MGHL inserted distally on the articular side of the subscapularis rather than directly onto the lesser tuberosity,15 merging almost perpendicularly with the horizontal fibers of the anterior capsule that define the fasciculus obliquus. Our results therefore differ from other macroscopic studies that report an insertion onto the humerus5,18 but are in keeping with those that suggest that the distal insertion is into the deep layer of the subscapularis.1,4 A histological study would be beneficial to confirm this relationship. We chose not to report the measured distances of the MGHL’s insertion points from the lateral borders of the subscapularis, as these measurements were imprecise and poorly reproducible.
The role of the MGHL in external shoulder rotation is clinically relevant information. External rotation is limited in frozen shoulder, in particular in cases of capsulitis with substantial anterior fibrosis involving the rotator interval and neighboring tissues.21 MGHL involvement in this pathology may limit external rotation. Hagiwara et al found that arthroscopic sectioning of the MGHL in cases of adhesive capsulitis was associated with statistically significant increases of +3° in ER 1 and +2° in ER 2.8 Meanwhile, Tipton et al have suggested arthroscopic sectioning of the MGHL to increase postoperative mobility in patients at risk of limited external rotation.20
On the other hand, given the MGHL’s distal insertion into the subscapularis, the limiting role of the MGHL in ER 1 must surely be intimately linked to the integrity of the subscapularis muscle. In massive, retracted subscapularis tears, the shoulder is clinically observed to be in excessive external rotation; a consequence of it no longer being restricted in this regard by the subscapularis and MGHL. In this situation, the MGHL loses its limiting effect on external rotation because its distal insertion is carried away by the retracted subscapularis. This mechanism is evidenced arthroscopically by the invisible MGHL sign and nonobservation of the MGHL being indicative of a retracted subscapularis tear.3,13 The fact the ER 1 increases further after subscapularis peel (step 6) supports these clinical observations. The MGHL only restricts ER 1 if the subscapularis muscle and tendon are intact.
Anatomical and clinical observations provide a better understanding of the MGHL’s functions. The first is its restriction of external shoulder rotation with the arm at the side, as demonstrated biomechanically by the present study and clinically by excessive external rotation and capsulitis-type stiffness. The second role, was supported by phylogenetic arguments,11,17 may be as a secondary stabilizer in cases of anterior instability.
The strengths of this study lie in the precise analysis of the successive anatomical structures involved in controlling external shoulder rotation. The study is limited by its small size and cadaveric nature, while the old age and gender imbalance of the subjects means the findings need to be confirmed in the general population. Some subjects with superior and/or posterior rotator cuff tears were included because these tendons (supra and infraspinatus) are not directly involved in external rotation. Finally, since subscapularis peel involved sectioning the anterior capsule, the effects of these two structures could not be evaluated independently. However, our results do provide useful information on the effects of not repairing the subscapularis or the anterior capsule in total shoulder arthroplasty.
Conclusion
The MGHL limits external shoulder rotation with the arm at the side. In these 20 cadaveric shoulders, sectioning the MGHL led to a significant mean increase of 15° in external rotation range with the arm at the side but had no clinically significant effect on external rotation with the arm in 90° abduction. These observations support MGHL section, as proposed by some authors in the treatment of frozen shoulder, to improve mobility, particularly in external rotation.
Disclaimers
Funding: No funding was disclosed by the authors.
Conflicts of interest: The authors, their immediate families, and any research foundation 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.
Footnotes
This study was approved by Conseil d’Orientation Scientifique Ramsay Santé; study number: IRB00010835.
Supplementary data to this article can be found online at https://doi.org/10.1016/j.jseint.2022.10.013.
Supplementary data
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