Adhesive capsulitis, also called frozen shoulder is a clinical syndrome of pain and severely decreased joint motion caused by thickening and contraction of the joint capsule and synovium. The risk factors are female sex, patients aged > 40 years, trauma, diabetes, prolonged immobilization, thyroid disease, stroke, myocardial infarction, and autoimmune disease [19].
Although spontaneous resolution is the rule, years can ensue (mean 18–30 months) before joint mobility returns to normal. Various treatment options exist for AC (e.g., oral anti-inflammatory drugs, intraarticular corticoid injection, physiotherapy, percutaneous capsular distention, surgical release, etc.) depending on the level of clinical impairment, and on an accurate diagnosis. Thus, disease staging and identification of inflammatory changes could have an impact on patient management [20].
The diagnosis of AC might be challenging because it is a diagnosis of exclusion, and it is mainly based on the clinical examination, with the only additional study suggested being the plain shoulder radiograph to rule out other possible causes of a limited ROM such as osteoarthritis, fracture, and chronic shoulder dislocation [13].
Recent studies have shown that Magnetic Resonance Imaging (MRI) can provide reliable imaging indicators of frozen shoulder. Potentially useful MR findings in frozen shoulder include thickening of the CHL, thickening of the joint capsule in the rotator cuff interval, and obliteration of the fat triangle under the coracoid process [4].
The aim of work of the current study was to examine the association between clinical features (stages) and MRI findings in adhesive capsulitis of the shoulder. To elucidate the aim of this study, 70 patients were included. In the present study,there was female predominance (62.9%) with female to male ratio about 1.7:1 which agree with Park et al. [5] who found that among the 103 patients there were 62 women, 41 men. That also, agree with Ewald [6] who stated that women are more often affected than men.
In the current study, the mean age of patients with AC is 44.84 ± 10.65 years ranged between 22 to 62 years which near to the results in the study done by Park et al.[5] who found that mean age, 51.9 years; range, 34–75 years. Also, in the study done by Pag [7] the mean age of the studied cases was 54.1 years ranged between 22 and 78 years.
In this study, the duration of symptoms “months” ranged between 0.08–7 months with mean 0.86 ± 1.36 months but in the study by Park et al. [5] who found that the duration of symptoms at the time of medical record analysis varied from 2 to 24 months (mean, 5.8 months).
As regard to the affected side, there were 35 patients (50.0%) had the right side of shoulder and 35 patients (50.0%) had left side of shoulder affection which near to the results in the study done by Do et al. [8] who found that 28 patients (45.9) had right shoulder affected and 33 patients have left side shoulder affection (54.1).
Although various structural abnormalities have been associated with adhesive capsulitis, only a few studies have examined the association between MRI findings and clinical features [8,9,10,11].
Teixeira et al. [12] reported that edema at the axillary recess is a good diagnostic indicator with excellent reproducibility and high sensitivity. In line with this conclusion, we found that joint capsule edema in the humeral portion of the axillary recess on fat suppressed T2-weighted MR images was present in 44.3% of adhesive capsulitis patients in our study and in the glenoid portion in 38.6% while there were 25 patients (35.7%) were anterior and 21 patients (30.0%) were posterior among extra capsular edema. Teixeira et al. [12] also suggested that a layer of high signal intensity bordering the outer capsular surface of the shoulder joint on fat-suppressed T2-weighted MR images is highly specific for the diagnosis of adhesive capsulitis, consistent with the MRI findings of extracapsular edema in our study.
As regard to stages; there were 17 patients (24.3%) were stage 1, 27 patients (38.6%) were stage 2, 21 patients (30.0%) were stage 3 and 5 patients (7.1%) were stage 4 among Stage while in the study done by Park et al. [5], thirty-eight patients had stage 1 capsulitis; 52 patients, stage 2; and 14 patients, stages 3 and 4.
Although the pathophysiologic mechanism of adhesive capsulitis is controversial, pathologic findings reflect both synovial inflammatory and capsular fibrotic conditions, depending on the clinical stage [13]. The early stages of adhesive capsulitis involve considerable pain with gradually increasing joint stiffness caused by ongoing synovial inflammation and fibrosis. During the later stages, as inflammation decreases, capsular fibrosis reaches its peak [14]. Several studies have shown that gadolinium enhancement of the joint capsule and synovial membrane is common in stage 2 adhesive capsulitis [15, 16].
In the present study, obliteration of subcoracoid fat triangle was detected in 35 patients (50%) moreover, in 17 of 22 patients, Mengiardi et al. [17] found an inflammatory obliteration of the subcoracoid fat triangle with AC, which we also observed in partial or complete form in this investigation. The complete obliteration of this fat triangle was specific to the diagnosis of frozen shoulder or AC.
In our study, the mean capsular thickening of glenoid portion of axillary recess (mm) (5.85 ± 1.28) and the mean thickening of humeral portion of axillary recess (mm) (5.11 ± 1.79) which is near to the results in the study done by Park et al. [5] who found that joint capsule thickness in the axillary recess was 4.06 ± (SD) 1.59 mm in the humeral portion and 4.34 ± 1.46 mm in the glenoid portion. Capsule thickness in the axillary recess has been described as a reliable diagnostic tool of AC when > 4 mm [17, 18].
In this study, joint capsule thickness in the humeral portion of the axillary recess and pain intensity had a positive correlation (p = 0.046. There was a negative correlation between height of the axillary recess and pain intensity (p = 0.033).In the current study, we found statistically significant negative linear correlations between anterior extracapsular edema and ROM on abduction with (p = 0.014. In the present study, we found statistically significant negative linear correlations between anterior extracapsular edema and limited ROM on external rotation (p = 0.001). In our study, there was statistically significant negative linear correlations between joint capsule edema in the humeral portion of the axillary recess and limited ROM on external rotation (p = 0.013 and all of theses results previously mentioned coincide with Park et al. [5].
That means, patients with limited ROM on external rotation and abduction had anterior extracapsular edema and joint capsule edema in the humeral portion of the axillary recess on fat-suppressed T2-weighted MR images. In the present study, there were no significant correlations between obliteration of the subcoracoid fat triangle, effusion in the long head biceps tendon sheath, joint capsule thickness in the humeral portion of the axillary recess, width of the axillary recess, or degree of external rotation during MRI (p > 0.05) which also are in agreement with Park et al. [5].
In this study, no statistically significant association between absence and presence of limitation of ROM “external-rotation” according to capsular thickening of glenoid portion of axillary recess (mm), capsular thickening of humeral portion of axillary recess (mm) which is disagree with Ahn et al. [10] who found a significant negative correlation between the limitation of external rotation and axillary joint capsule thickness.
In the current study, effusion in the long head biceps tendon sheath was not significantly correlated with pain intensity, limitation of ROM on external rotation and ROM on abduction which agree with Park et al. [5] who stated that effusion in the long head biceps tendon sheath was not accompanied by fluid in the shoulder joint capsule and was not significantly correlated with clinical features.
In the present study, There is no statistically significant association between absence and presence of limitation of ROM “external-rotation” according to capsular thickening of glenoid portion of axillary recess (mm) and capsular thickening of humeral portion of axillary recess (mm) which agree with Lee et al. [11] who reported no significant correlation between joint capsule thickness in the axillary recess with either limitation of ROM on external rotation or abduction.
But that disagree with Ahn et al. [10] who found that joint capsule thickness in the axillary recess significantly correlated with ROM on external rotation in patients with adhesive capsulitis, but this finding was not associated with abduction ROM or pain intensity. This discrepancy may be related to differences in measurement methods.
In our study, thicknesses of the joint capsule in the humeral and glenoid portions of the axillary recess were measured separately and analyzed, whereas in previous studies, joint capsule thickness was measured in only one location. In addition, one of the previous studies was conducted with direct MR arthrography Lee et al. [11].
Regarding to capsular edema of humeral portion of axillary recess, the results showed 31 patients out of 70 having capsular edema of humeral portion of axillary recess, 9 patients (52.9%) belong to stage 1; 17 patients (63%) belong to stage 2 and 5 patients (19.2%) belong to stage 3 + 4 while in the study done by Park et al. [5]. Joint capsule edema in the humeral portion of the axillary recess was found in 97% of patients with stage 1 capsulitis, in 83% with stage 2, and in 64% with stages 3 and 4.
In the study done by Chellathurai et al. [19], edema on the humeral aspect was present in 100% of the patients in stage I adhesive capsulitis, 88.5% in stage II capsulitis, 5% in stage III capsulitis, and 0% in stage IV. Mild edema was present in 14.3% in stage III and 7.7% in stage IV. The distribution of edema in the different clinical stages was significant (P 0.001).
In the current study, joint capsule edema in the humeral portion of the axillary recess was more common in patients with stage 2 and that of glenoid portion is more common in stage 1, also there was a statistically significant difference between stage group according to capsular thickening of humeral portion of axillary recess (mm) which is in agreement with Sofka et al. [8] who found that joint capsule thickness in the axillary recess correlates with clinical stage and that joint capsule edema in the axillary recess is common in stage 2.
In the study done by Chellathurai et al. [19] the incidence of edema was more common in stages I and II which progressively decreases in stages III and IV.
In our study, 29 patients out of 70 having obliteration of subcoracoid fat triangle, 2 patients (11.8%) belong to stage 1; 16 patients (59.3%) belong to stage 2 and 11 patients (42.3%) belong to stage 3 + 4, as there was a statistically significant relation. Ahn et al. [10], Lee et al. [11] reported no association between obliteration of the subcoracoid fat triangle and clinical impairment. Park et al. [5] confirmed this lack of association, obliteration of the subcoracoid fat triangle was seen more frequently during the early (stages 1 and 2) than later (stages 3 and 4) stages of adhesive capsulitis. Obliteration of the subcoracoid fat triangle may thus be related to inflammation, which is frequently extensive during the early stages of adhesive capsulitis.
Chellathurai et al. [19] stated that obliteration of the fat in the subcoracoid triangle was present in 44.4% in stage I, 46.2% in stage II, 90.5% in stage III, and 84.6% in stage IV. This distribution was significant (P 0.005).
As regard to effusion of long head biceps tendon sheath, the results showed 48 patients out of 70 having effusion of biceps tendon sheath, 15 patients (88.2%) belong to stage 1; 20 patients (74.1%) belong to stage 2 and 13 patients (50%) belong to stage 3 + 4, as there was a statistically significant negative relation with p-value (p = 0.022) while in the study done by Chellathurai et al. [19] effusion around the long head biceps tendon was found in 100% in stage I, 96.2% in stage II, 81% in stage III, and 61.5% in stage IV. The highest incidence was found in stage I, than in stage II, then decreases in stages III and IV. This distribution was statistically significant (P 0.016).
Study limitations
Our study was limited by that the most of patients had a limitation of ROM on external rotation, so we could not measure the degree of external rotation during the MRI scan. The clinical information was not sufficient to correlate between the clinical features and MRI findings.
The relatively long period of the lockdown for COVID-19 pandemic with its negative impact on the flow of cases.
We did not use the arthroscopy as a gold standard for this study except for examination the pathophysiology of AC.