Fat distribution in the rotator cuff interval determining the coracohumeral ligament visualization: Magnetic resonance imaging findings

Jinqing Li; Linheng Song; Zhibo Yu; Qing Qiao; Fusuo Li; Yunquan Zhang; Hongguang Zhang; Xiaochuan Lan; Min Huang; Yi Wu; Shaoxiang Zhang

doi:10.4103/2226-8561.182296

ORIGINAL ARTICLE

Year : 2016 | Volume : 2 | Issue : 1 | Page : 34-39

Fat distribution in the rotator cuff interval determining the coracohumeral ligament visualization: Magnetic resonance imaging findings

Jinqing Li¹, Linheng Song¹, Zhibo Yu¹, Qing Qiao¹, Fusuo Li¹, Yunquan Zhang¹, Hongguang Zhang¹, Xiaochuan Lan¹, Min Huang¹, Yi Wu², Shaoxiang Zhang²
¹ Department of Radiology, 324^th Hospital of the PLA, Chongqing 400020, China
² Institute of Digital Medicine, Third Military Medical University, Chongqing 400038, China

Date of Web Publication

11-May-2016

Correspondence Address:
Jinqing Li
Department of Radiology, 324^th Hospital of the PLA, Chongqing 400020
China
Shaoxiang Zhang
Institute of Digital Medicine, Third Military Medical University, Chongqing 400038
China

Source of Support: None, Conflict of Interest: None

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DOI: 10.4103/2226-8561.182296

Abstract

Objective: The purpose of this study was to analyze how fat distribution in the rotator cuff interval (RCI) in normal volunteer shoulders determines the coracohumeral ligament (CHL) visualization, including the CHL visualization rate, type, and thickness, using routine magnetic resonance imaging (MRI). Materials and Methods: This study prospectively analyzed 120 shoulder joints in 60 normal volunteer individuals (30 males and 30 females) using MRI to identify the fat distribution type in the RCI as well as the CHL visualization rate, type, and thickness. Results: The fat in the RCI was visualized in 110 of 120 shoulders (91.7%) while the fat in the RCI was not identifiable in 8.3% of normal volunteer shoulders. The fat distribution in the RCI was classified into five types: Type A (52.5%), Type B (26.7%), Type C (5.8%), Type D (6.7%), and Type E (8.3%). The CHL types included the horizontal type (73.3%), upsloping type (12.5%), downsloping type (5.9%), and unseen type (8.3%) (The CHL was not identifiable in 8.3% of normal volunteer shoulders). No significant difference existed for the fat distribution types in the RCI or the CHL visualization rate, types, or thickness in either different lateral shoulders or different gender shoulders, using a Chi-square test (P > 0.05). In addition, no significant correlation emerged between body mass index (23.4 ± 2.5, n = 110) and the CHL thickness (3.1 ± 1.3 mm) in normal volunteer shoulders, using the Pearson correlation test (n = 110) (r = −0.095, P> 0.05). Conclusion: MRI is a satisfactory method for determining the fat distribution in the RCI and CHL depiction in normal volunteer shoulders. The fat distribution in the RCI determines the CHL visualization, including the CHL visualization rate, type, and thickness.

Keywords: Adhesive capsulitis, coracohumeral ligament, frozen shoulder, magnetic resonance imaging, rotator cuff interval

How to cite this article:
Li J, Song L, Yu Z, Qiao Q, Li F, Zhang Y, Zhang H, Lan X, Huang M, Wu Y, Zhang S. Fat distribution in the rotator cuff interval determining the coracohumeral ligament visualization: Magnetic resonance imaging findings. Digit Med 2016;2:34-9

How to cite this URL:
Li J, Song L, Yu Z, Qiao Q, Li F, Zhang Y, Zhang H, Lan X, Huang M, Wu Y, Zhang S. Fat distribution in the rotator cuff interval determining the coracohumeral ligament visualization: Magnetic resonance imaging findings. Digit Med [serial online] 2016 [cited 2023 Mar 24];2:34-9. Available from: http://www.digitmedicine.com/text.asp?2016/2/1/34/182296

Introduction

The rotator cuff interval (RCI) is a triangular anatomic area in the anterosuperior aspect of the shoulder, which is defined by the coracoid process at its base, superiorly by the anterior margin of the supraspinatus tendon, and inferiorly by the superior margin of the subscapularis tendon. The rotator interval contains the coracohumeral ligament (CHL), the superior glenohumeral ligament, and the long head of the biceps tendon.^{[1],[2],[3],[4],[5],[6],[7],[8],[9]} Rotator interval pathology is implicated in glenohumeral instability, biceps instability,^{[10],[11],[12],[13],[14],[15],[16]} and adhesive capsulitis ^{[17],[18],[19],[20],[21]} all of which remain a challenge to diagnosis and treatment.

Some studies have shown that the CHL plays an important role in the genesis and development, diagnosis, and treatment of frozen shoulder. Neer et al.^[22] stated that the CHL limited external rotation and was often shortened in frozen shoulder, indicating that it might require a release. Bunker and Anthony ^[23] found that the CHL in 11 of 12 cases studied appeared to be abnormal and had the appearance of a nodular fleshy band that was inextensible and prevented external rotation. Mengiardi et al.^[17] found that patients with frozen shoulder had a significantly thickened CHL using magnetic resonance (MR) arthrography, and the thickened CHL was the most characteristic MR findings in frozen shoulder. Homsi et al.^[24] identified a thickened CHL using ultrasonography examinations.

However, few studies have attempted to determine the rate of CHL visualization in normal volunteers using routine MR imaging (MRI). In addition, some studies have shown that fat distribution in the RCI could affect the CHL visualization.^{[17],[24],[25]} In view of the fact that MRI can demonstrate the CHL and this ligament is thickened in frozen shoulder, the purpose of this study is to analyze fat distribution in the RCI in normal volunteers by determining the CHL visualization including the CHL visualization rate, type, and thickness using routine MRI.

Materials and Methods

Study population

The normal volunteer individuals included 120 shoulder joints in 30 males and 30 females (a mean age of 50.5 years) who underwent MRI. The average body mass index (BMI) was 23.4 ± 2.5. Exclusion criteria included rheumatoid arthritis, previous shoulder surgery, previous trauma, and/or abnormal radiographs. Our institutional review board does not require its approval or informed consent for the review of normal volunteers' images. The normal volunteers' rights are protected by law.

The MRI protocol

MRI was performed using a 1.5-T system (Avanto; Siemens Medical Solutions, Germany). A phased-array surface coil was centered over the glenohumeral joint and strapped in place. The arm position was standardized, with the thumb pointing upward in a neutral position. T1-weighted spin-echo images were obtained in the transverse plane (repetition time/echo time [TR/TE] = 624 ms/11 ms; section thickness, 3 mm; intersection gap, 0.3 mm; field of view (FOV), 18 cm; matrix size, 256 × 256). In the sagittal oblique plane, parallel to the glenohumeral joint (TR/TE = 550 ms/15 ms; section thickness, 3 mm; intersection gap, 0.3 mm; FOV, 18 cm; matrix size, 256 × 256), fat-suppressed proton-density weighted spin-echo images were obtained in the coronal oblique plane, paralleling the long axis of the supraspinatus tendon (TR/TE = 3000 ms/34 ms; section thickness, 3 mm; intersection gap, 0.3 mm; FOV, 18 cm; matrix size, 256 × 256). The same MRI protocol was for both the transverse and sagittal oblique planes. T2-weighted spin-echo images were obtained in the coronal oblique plane (TR/TE = 3700 ms/84 ms; section thickness, 3 mm; intersection gap, 0.3 mm; FOV, 18 cm; matrix size, 256 × 256).

Analysis of the MRI images

A qualitative MRI evaluation of the rotator interval was performed. The fat distribution types in the RCI, and CHL types were analyzed on sagittal T1-weighted spin-echo oblique images through consensus by two staff radiologists with 8 years and 20 years of experience in musculoskeletal radiology, respectively. The fat in the RCI was inspected in two regions (above and below the CHL) on sagittal T1-weighted spin-echo oblique images. The fat in the RCI was above and below the CHL with regard to fat signal intensity or obliteration that was classified as marked fat, mild fat, or none (obliteration of the fat). The fat distribution types in the RCI were classified into Type A (fat distribution was marked above and below the CHL, with the area of fat signal intensity above the CHL roughly equaling the area of fat signal intensity below the CHL), Type B (fat distribution type was marked above the CHL and mild below the CHL, with the area of fat signal intensity above the CHL roughly exceeding the area of fat signal intensity below the CHL), Type C (fat distribution type was mild above the CHL and marked below the CHL, with the area of fat signal intensity below the CHL exceeding the area of fat signal intensity above the CHL), Type D (fat distribution type was mild above the CHL and mild below the CHL), or Type E (fat distribution type was obscuration above and below the CHL).

The CHL type included the upsloping type (the origination of CHL from the posterior aspect of the coracoid process was lower than the insertion of CHL in the RCI), downsloping type (the origination of CHL from the posterior aspect of the coracoid process was higher than the insertion of CHL in the RCI), horizontal type (the origination of CHL from the posterior aspect of the coracoid process was parallel to the insertion of CHL in the RCI), and unseen type (the distinct fatty tissue surrounding the CHL had disappeared, and the CHL could not be measured), according to the insertion of the CHL in the RCI. The thickness of the CHL was measured at its widest portion within the rotator interval on sagittal T1-weighted spin-echo oblique images by a fellow in musculoskeletal radiology who was blinded to the use of CHL thickness. Rotator cuff tendons were also evaluated using MRI.

Statistical analysis

Statistical analysis was completed using the SPSS software program SPSS version 13.0 for Windows (SPSS, Inc., Chicago, IL, USA). A Chi-square test was used to analyze the data for the fat distribution type, the rate of CHL visualization, and CHL type. An independent t-test was used to analyze the maximum thickness of CHL for different lateral shoulders and different gender shoulders. The results of the CHL thickness analysis were then expressed as a mean ± standard deviation for each group. The Pearson correlation test was used to analyze the correlation measures between CHL thickness and BMI. Two-tailed hypothesis tests were used, and local statistical significance was assumed to be P < 0.05 for all parameters.

Results

The sagittal oblique T1-weighted image demonstrated that the CHL appeared a flat, homogeneous, hypointense band. However, the CHL from some shoulders could not be measured on the sagittal oblique images because of the complete obliteration surrounding the CHL [Figure 1] and [Figure 2].

Figure 1: (a-e) Sagittal oblique T1-weighted image (repetition time/echo time = 550 ms/15 ms) shows fat distribution types in the rotator cuff interval in normal volunteer shoulders. (a). Type A the fat distribution was marked above and below the coracohumeral ligament, with the area of fat signal intensity above the coracohumeral ligament (#) roughly equaling the area of fat stranding below the coracohumeral ligament (*). #: An area of fat signal intensity above the coracohumeral ligament. *: An area of fat signal intensity below the coracohumeral ligament. (b) Type B the fat distribution type was marked above the coracohumeral ligament and mild below the coracohumeral ligament, with the area of fat signal intensity above the coracohumeral ligament roughly exceeding the area of fat signal intensity below the coracohumeral ligament. (c) Type C the fat distribution type was mild above the coracohumeral ligament and marked below the coracohumeral ligament, with the area of fat signal intensity below the coracohumeral ligament exceeding the area of fat signal intensity above the coracohumeral ligament. (d) Type D the fat distribution type was mild above and below the coracohumeral ligament. (e) Type E the fat distribution type was obscured above and below the coracohumeral ligament. AP = Acromion process, CP = Coracoid process, HH = Humeral head, SST = Supraspinatus tendon, CHL = Coracohumeral ligament

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Figure 2: (a-d) Sagittal oblique T1-weighted image (repetition time/echo time = 550 ms/15 ms) shows the coracohumeral ligament types in normal volunteer shoulders. (a) The upsloping type according the insertion of the coracohumeral ligament in the rotator cuff interval (the origination of coracohumeral ligament from the posterior aspect of the coracoid process was lower than the insertion of coracohumeral ligament in the rotator cuff interval). A normal coracohumeral ligament showed a flat, homogeneous, low-signal intensity band (arrows). (b) The horizontal type (the origination of coracohumeral ligament from the posterior aspect of the coracoid process was parallel to the insertion of coracohumeral ligament in the rotator cuff interval). (c) The down sloping type (the origination of coracohumeral ligament from the posterior aspect of the coracoid process was higher than the insertion of coracohumeral ligament in the rotator cuff interval). (d) The unseen type (the distinct fatty tissue surrounding the coracohumeral ligament disappeared, and the coracohumeral ligament cannot be measured)

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A comparison of the fat distribution type in the RCI in different lateral shoulders and different gender shoulders is given in [Table 1]. The fat in the RCI was visualized in 110 of 120 shoulders (91.7%) in normal volunteer individuals while 10 of 120 shoulders (8.3%) were not visualized. The Type A fat distribution in the RCI was visualized in 63 of 120 shoulders (52.5%) in normal volunteer individuals while Type B accounted for 26.7%, Type C accounted for 5.8%, Type D accounted for 6.7%, and Type E accounted for 8.3% [Figure 1] and [Figure 2]. When the fat distribution type in the RCI for the female shoulders was compared with that for the male shoulders, no significant difference emerged based on the χ² test (P > 0.05). Furthermore, the fat distribution type in the RCI for the right shoulders compared with that for the left shoulders showed no significant difference based on the χ² test (P > 0.05).

Table 1: Comparison of the fat distribution type in the rotator cuff interval for different lateral shoulders and different gender shoulders

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[Table 2] summarizes the comparison of the CHL type in the RCI in different lateral shoulders and different gender shoulders. The CHL was visualized in 110 of 120 shoulders in normal volunteer individuals (91.7%) while 10 of 120 shoulders (8.3%) were not visualized. The horizontal type of CHL was visualized in 88 of 120 shoulders in normal volunteer individuals (73.3%), while the upsloping type accounted for 12.5%, down sloping type accounted for 5.9%, and unseen type accounted for 8.3% [Figure 1] and [Figure 2]. When the CHL type in the RCI for the female shoulders was compared with that for the male shoulders, no significant difference was evident based on the χ² test (P > 0.05). When the CHL type in the RCI for the right shoulders was compared with that for the left shoulders, no significant difference emerged based on the χ² test (P > 0.05).

Table 2: Comparison of the coracohumeral ligament types in different lateral shoulders and different gender shoulders

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The CHL thickness (3.0 ± 1.1 mm) in female shoulders (n = 57) was not significantly lower than that thickness (3.1 ± 1.5 mm) in male shoulders (n = 53) according to an independent t-test (P > 0.05). In addition, the CHL thickness (3.2 ± 1.3 mm) in right shoulders (n = 55) was not significantly greater than that (3.0 ± 1.1 mm) in left shoulders (n = 55). No significant correlation existed between BMI (23.4 ± 2.5, n = 110) and CHL thickness (3.0 ± 1.3 mm) in volunteer shoulders (n = 110) (r = −0.095, P = 0.491). The subacromial-subdeltoid bursa was visualized in 8 of 120 shoulders in normal volunteer shoulders (6.7%), as seen in the sagittal oblique fat-suppressed, proton-density weighted, spin-echo images of the shoulders. The subscapularis bursa was visualized in 48 of 120 shoulders (40%), as seen in the sagittal oblique fat-suppressed, proton-density weighted, spin-echo images of the shoulders. None of the normal volunteer shoulders had subcoracoid bursa effusions. No high-signal intensity soft tissue was evident in the RCI, and no thickened axillary recess or rotator cuff tear was seen on the sagittal oblique, coronal oblique, or transverse fat-suppressed, proton-density weighted, and spin-echo images in normal volunteer shoulders.

Discussion

The CHL is always well-identified in the mid portion of the RCI and is visualized on all planes, but sagittal images are the most useful for analysis of this structure.^[5],[6] The CHL appears to be a flat, homogeneous, low-signal intensity linear band surrounded by hyper-signal intensity fat tissue in T1-weighted spin-echo images. In addition, T1 weighted images were sensitive for fat. Hence, In the current study, the thickest portion of the CHL was measured on sagittal, T1-weighted, spin-echo oblique images.

The current study indicated that fat distribution in the RCI determined the CHL visualization. In this study, the fat in the RCI was visualized in 110 of 120 shoulders (91.7%), whereas the fat in the RCI was not visualized in 8.3% of normal volunteer shoulders. The rate of CHL visualization (91.7%) was also the same as the rate of fat visualization in the RCI and was similar to Neer et al.'s findings (93.7%, 59/63) and Wu et al.'s findings (93.75%, 30/32),^[26] although higher than Chung et al.'s report in which the CHL was seen by MRI in only 60% of specimens ^[2] and Homsi et al.'s results indicating that 76.0% (92/121) of the CHL was visualized in the asymptomatic group using Ultrasound.^[24] Neer et al. reported that the CHL was not visualized in 4 out of 63 (6.7%) anatomic specimens of the shoulder because the CHL was absent or vestigial. However, Homsi et al. did not explain the why 24.0% (29/121) of the CHL was not visualized in the asymptomatic group, using Ultrasound.^[24] The CHL measurement with MRI depended on the hyper-intensity fat surrounding the CHL in the RCI distinguishing from the hypo-intensity CHL. We cannot explain the reasons that the fat surrounding the CHL in the RCI disappeared in a percentage of normal volunteer shoulders (8.3%). In our study, we found that fat-suppressed, proton density weighted, spin-echo images did not show high-signal intensity soft tissue in the RCI in normal volunteer shoulders. We suspected that the fat surrounding the CHL in the RCI might be absent in a percentage of normal shoulders (8.3%). What a percentage of the fat surrounding the CHL in the RCI being absent in normal shoulders needed to be further confirmed in the future study.

In the current study, the fat distribution in the RCI was classified into 5 types, and Type A (fat distribution was marked above and below the CHL, with the area of fat signal intensity above the CHL roughly equaling the area of fat signal intensity below the CHL) was the main fat distribution type, accounting for 52.5%. The horizontal type was the main CHL types (73.3%). No significant difference occurred in different fat distribution types in the RCI, CHL types in different lateral shoulders and different gender shoulders. The correlation between RCI fat type and CHL type was not clear and needed to be further investigated in the future. However, our study suspects that the complete obliteration of the subcoracoid fat triangle is specific for the diagnosis of frozen shoulder, as Mengiardi et al. reported.^[17] After all, Type E of fat distribution type in the RCI (obscuration above and below the CHL) accounted for 8.3%, which was similar to the result of report that two was not be identified for healthy individuals (6.25%, 2/32).^[26] The complete obliteration of the subcoracoid fat triangle is not specific, but useful for the diagnosis of frozen shoulder.

Previous studies have proposed that a thickened CHL was one of the most characteristic manifestations of frozen shoulder. The thickness of the CHL is a useful criterion for diagnosing frozen shoulder, including Mengiardi et al.'s result (CHL thickness of 4.1 mm vs. 2.7 mm in controls) and Homsi et al.'s results (showing 3 mm of adhesive capsulitis, 1.34 mm in asymptomatic shoulders and 1.39 mm in painful shoulders).^[17],[24] In our study, the thickness of CHL was 3.0 ± 1.3 mm in volunteer shoulders, which supported the CHL reference baseline value for diagnosing frozen shoulder. The CHL was not significantly thicker in men (3.1 ± 1.5 mm) than in women (3.0 ± 1.1 mm), which was contrary to Wu et al. report that 2.2 mm in men was significantly thicker than 2.0 mm in women.^[26] Of course, shoulder MR arthrography may improve the rate of CHL visualization of the shoulder as indicated in Mengiardi et al.'s report. In the future study, shoulder MR arthrography might be useful to evaluate the CHL visualization. To sum up, our study indicated that MRI was a quite satisfactory method for depicting the CHL because the higher MRI visualization rate of the fat distribution (91.7%) in the RCI determined the subsequent higher CHL visualization in normal volunteer shoulders. In the future study, we will provide an evaluation of the imaging classification of the CHL in a clinical cohort of patients with rotator cuff pathology, with and without adhesive capsulitis.

We acknowledge several limitations for our study. First, our study lacked MR arthrography for normal volunteer shoulders. Second, our study was done with just one institute and was based on a small sample factors that might cause a certain selection bias in terms of normal volunteer shoulders. Third, our study lacked data for different ages and different occupations of normal volunteer shoulders. Finally, our study lacked inter- and intra-observer correlation to CHL measurement.

Conclusion

MRI is a satisfactory method for determining the fat distribution type in the RCI and CHL depiction in normal volunteer shoulders. The fat distribution in the RCI determines the CHL visualization, including the CHL visualization rate, type, and thickness.

Financial support and sponsorship

This project was supported by the Natural Science Foundation of Chongqing, China (No. cstc2014jcyjA10011) and National Natural Science Foundation of China (No. 81301300).

Conflicts of interest

There are no conflicts of interest.

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