Indirect MR Arthrographic Findings of Adhesive Capsulitis

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1 Musculoskeletal Imaging Original Research Song et al. MR Arthrography of Adhesive Capsulitis Musculoskeletal Imaging Original Research Kyoung Doo Song 1 Jong Won Kwon Young Cheol Yoon Sang-Hee Choi Song KD, Kwon JW, Yoon YC, Choi SH Keywords: adhesive capsulitis, arthrography, MRI, shoulder, sports medicine DOI: /AJR Received November 8, 2010; accepted after revision May 18, All authors: Department of Radiology and Center for Imaging Science, Samsung Medical Center, Sungkyunkwan University School of Medicine, 50, Ilwon-Dong, Kangnam-Ku, Seoul , Korea. Address correspondence to J. W. Kwon (jwjwkwon@gmail.com). WEB This is a Web exclusive article. AJR 2011; 197:W1105 W X/11/1976 W1105 American Roentgen Ray Society Indirect MR Arthrographic Findings of Adhesive Capsulitis OBJECTIVE. The objective of our study was to compare the indirect MR arthrographic findings of patients with adhesive capsulitis and patients without adhesive capsulitis. MATERIALS AND METHODS. Indirect MR arthrograms of 35 patients (21 women, 14 men; mean age, 50.1 years) diagnosed with adhesive capsulitis clinically were compared with indirect MR arthrograms of 45 patients (23 women, 22 men; mean age, 48.9 years) without adhesive capsulitis. Joint capsule thickness in the axillary recess and the thicknesses of the enhancing portion of the axillary recess and the rotator interval were, respectively, evaluated on coronal T2-weighted images and coronal and sagittal fat-suppressed enhanced T1-weighted images by two radiologists independently. Reliability was studied using the intraclass correlation coefficient (ICC). Receiver operating characteristic (ROC) curves were compared. RESULTS. Patients with adhesive capsulitis had significantly thickened joint capsules in the axillary recess and a thickened enhancing portion in the axillary recess and in the rotator interval. The difference in the thicknesses of the enhancing portion in the axillary recess and in the rotator interval were significantly greater than the difference in joint capsule thicknesses in the axillary recess between the adhesive capsulitis group and the control group (p < 0.001). Interobserver reliability was good for all three indexes (ICC 0.80). The area under the ROC curve for the thickness of the joint capsule in the axillary recess and the thicknesses of the enhancing portion of the axillary recess and the rotator interval were 0.797, 0.861, and 0.847, respectively. CONCLUSION. An abundance of enhancing tissue in the rotator interval and thickening and enhancement of the axillary recess are signs suggestive of adhesive capsulitis on indirect MR arthrography. A dhesive capsulitis, or frozen shoulder, is a disabling and sometimes severely painful condition that is commonly managed in the primary care setting [1 5]. This clinical entity is characterized by gradual worsening of pain and loss of active and passive glenohumeral movement. The term frozen shoulder was first introduced by Codman in 1934 [6]. In 1945, Naviesar [7] coined the term adhesive capsulitis in recognition of the pathologic changes in the capsule. Today, the two terms are commonly interchangeable. Although the cause of adhesive capsulitis remains unclear, abnormalities in the synovium and joint capsule have been reported in several histologic studies. Arthroscopy shows small joint capacity with the loss of the axillary fold and a tight anterior capsule, synovial changes in the glenohumeral joint such as villous hypertrophy, fibrinous reaction, increased vascularity, and thickening of the synovium [8, 9]. These results suggest that adhesive capsulitis is associated with inflammatory or degenerative change of the glenohumeral joint capsule with subsequent reactive capsular fibrosis. Adhesive capsulitis is essentially a clinical diagnosis [1]. There are few laboratory tests or radiologic markers specific for frozen shoulder. Arthrography has been the advocated imaging test of choice to assess for adhesive capsulitis. It shows characteristic findings, such as limited shoulder joint capacity and a small or nonexistent dependent axillary fold [1]. However, arthrography is invasive and cannot explore changes in the synovial and capsular membranes [10]. Therefore, in most institutions, this modality is not used routinely to diagnose adhesive W1105

2 Song et al. capsulitis. On the other hand, MRI is a noninvasive modality. It can identify changes in the synovium and the joint capsule and can exclude other causes of shoulder pain that mimic adhesive capsulitis such as rotator cuff tear, tendinitis, osteoarthritis, subacromial impingement, and occult fracture [10 12]. In several studies, investigators reported unenhanced MRI, contrast-enhanced MRI, or direct MR arthrography imaging findings suggestive of adhesive capsulitis and assessed the usefulness of these modalities in diagnosing the condition [10, 11, 13 15]. To our knowledge, no study has investigated the indirect MR arthrographic findings of adhesive capsulitis and the usefulness of indirect MR arthrography in diagnosing adhesive capsulitis. The purpose of this study was to compare the indirect MR arthrographic findings of patients with adhesive capsulitis and patients without adhesive capsulitis. Materials and Methods Patients and Control Subjects Between January 2008 and December 2009, 194 patients underwent indirect MR arthrography at our institution; of those patients, 80 were enrolled in the study. Thirty-five patients (21 women, 14 men; mean age, 50.1 years) were clinically diagnosed with adhesive capsulitis on the basis of the following criteria [16 20]: painful stiff shoulder for at least 4 weeks, severe shoulder pain that interfered with successful performance of activities of daily living or work activities, nocturnal pain, painful restriction of both active and passive elevation to less than 100, 50% restriction of external rotation, normal radiologic appearance, and A no secondary causes. The control group consisted of 45 subjects (23 women, 22 men; mean age, 48.9 years) with shoulder discomfort who underwent indirect MR arthrography for evaluation. However, they did not have limited range of motion in the shoulder joint in all directions. Of the 114 excluded patients, 27 had a clinical history and clinical evidence of rotator cuff tear. Twenty-eight had calcium deposition on radiography suggestive of calcific tendinitis. Five had bony abnormalities, such as fracture of the clavicle, fracture of the greater tuberosity of the humerus, and bony Bankart lesion. One had a history of shoulder surgery. The remaining 53 patients were excluded because they did not meet the criteria for limited range of motion. MRI Protocol MRI was performed using a 3-T whole-body MR imager (Gyroscan Intera Achieva, Philips Healthcare) with a dedicated receive-only shoulder coil. Indirect MR arthrography was initiated after IV injection of gadobutrol (Gadovist, Schering; 0.1 mmol/kg body weight) into an antecubital vein. Immediately after the injection of contrast material, patients were instructed to move their shoulder for 15 minutes. Patients were positioned for imaging with the humerus in a neutral position and the thumb pointing upward [21]. Indirect MR arthrography was performed using the following imaging sequences: Fat-suppressed T1-weighted turbo spin-echo sequences were performed in the axial and coronal oblique planes (TR range/te range, /18 24; section thickness, 3 mm; FOV, 15 cm; matrix size, ), parallel to the long axis of the supraspinatus tendon and in the sagittal oblique plane Fig. 1 Indirect MR arthrography of 50-year-old man with adhesive capsulitis. A, Oblique coronal T2-weighted image shows thickened joint capsule in axillary recess (arrows). B, Oblique coronal gadolinium chelate enhanced T1-weighted image shows enhancing portion of axillary recess (arrows). C, Oblique sagittal gadolinium chelate enhanced T1-weighted image shows enhancing portion of rotator interval (arrows). B ( /20 24; section thickness, 3 mm; FOV, 15 cm; matrix size, ), and perpendicular to the long axis of the supraspinatus tendon ( /18 24; section thickness, 4 mm; FOV, 15 cm; matrix size, ). T2-weighted turbo spinecho sequences were performed in the axial plane (TR range/te, /80; section thickness, 3 mm; FOV, 15 cm; matrix size, ; echo-train length [ETL], 16), the coronal oblique plane ( /80; section thickness, 3 mm; FOV, 15 cm; matrix size, ; ETL, 16), and the sagittal oblique plane ( /80; section thickness, 4 mm; FOV, 15 cm; matrix size, ; ETL, 16). Analysis of MR Images Analysis was performed by a musculoskeletal radiologist with 5 years of experience in the interpretation of shoulder MRI and by a radiology resident; both were blinded to the diagnoses. A PACS (Centricity 2.0, GE Healthcare) was used. The thickness of the joint capsule in the axillary recess and the thicknesses of the enhancing portion of the axillary recess and the rotator interval were independently measured by the two radiologists. The subacromial bursa, acromioclavicular joint, and glenohumeral joint effusion were evaluated by consensus of the two radiologists. Joint capsule thickness and the thickness of the enhancing portion of the axillary recess were measured at the widest portion of the humeral and glenoid aspects of the axillary recess on oblique coronal T2-weighted (Fig. 1A) and oblique coronal fat-suppressed enhanced T1-weighted (Fig. 1B) images, respectively [10]. In the rotator interval, the thickness of the enhancing portion was measured by the widest portion of the capsule and the synovium between the superior aspect of C W1106

3 MR Arthrography of Adhesive Capsulitis the subscapularis tendon and the anterior aspect of the supraspinatus tendon perpendicular to the adjacent humeral head cortex on oblique sagittal fat-suppressed enhanced T1-weighted images [10] (Fig. 1C). The images were also evaluated for evidence of subacromial bursitis and osteoarthritis of the acromioclavicular joint. The criteria for these entities were the presence of a fluid collection and enhancement in the subacromial bursa and acromioclavicular joint on oblique coronal T2-weighted images and oblique coronal fat-suppressed enhanced T1-weighted images. The glenohumeral joint effusion was evaluated. It was scored on oblique coronal T2-weighted images using a modified MRI classification scheme developed by Schweitzer et al. [22] as follows by consensus of the two radiologists: 0, no joint fluid; 1, mild loculated fluid signal; or 2, extensive fluid signal [23]. Statistical Analysis Interobserver reliability was assessed using the intraclass correlation coefficient (ICC) (3,1 method) under the mixed-effects model. In an analysis using a mixed model, raters corresponded to fixed effect and subjects corresponded to random effect. The ICC (3,1 method) was determined as follows: Each subject was measured by a rater involved in the study who then selected the two-way mixed-effects model. Reliability was calculated from a single measurement. The two-tailed Student t test was used to compare the mean thickness of the joint capsule in the axillary recess and the mean thicknesses of the enhancing portion of the axillary recess and the rotator interval between the adhesive capsulitis group and control group. Subacromial bursitis, osteoarthritis of the acromioclavicular joint, and glenohumeral joint effusion were compared using a chi-square test. A p value of < 0.05 indicated a statistically significant difference. In addition, to determine the diagnostic performance of joint capsule thickness in the axillary recess and the thicknesses of the enhancing portion of the axillary recess and the rotator interval for the diagnosis of adhesive capsulitis, receiver operating characteristic (ROC) curves were constructed and the area under the ROC curve (AUC) was calculated. The constructed ROC curves were compared, and p values were constructed using the methodology of DeLong et al. [24], which is a nonparametric approach using generalized U statistics, to compare the areas under three correlated ROC curves in the prediction of adhesive capsulitis. To calculate the corresponding sensitivity, specificity, positive predictive value, and negative predictive value, the variables were dichotomized at the most optimal cutoff point determined by maximizing the Youden index (defined as sensitivity plus specificity minus 1). TABLE 1: Joint Capsule Thickness in the Axillary Recess and Enhancing Portion of the Axillary Recess and the Rotator Interval in Patients With Adhesive Capsulitis and Control Group Mean Thickness ± SD (mm) Intraclass Correlation Structure Adhesive Capsulitis Control Group p Coefficient (95% CI) Axillary recess Joint capsule 5.9 ± ± 1.7 < ( ) Enhancing portion 6.5 ± ± 3.0 < ( ) Rotator interval Enhancing portion 8.3 ± ± 3.6 < ( ) Results The patient group had a significantly thicker joint capsule in the axillary recess and significantly thicker enhancing portion of the axillary recess and the rotator interval than the control group (p < 0.001) (Table 1 and Figs. 1 and 2). The differences in the thicknesses of the enhancing portion in the axillary recess and in the rotator interval were significantly greater than the difference in joint capsule thickness in the axillary recess between the adhesive capsulitis group and the control group (p < 0.001). Interobserver reliability, as measured by the ICC, was good (Table 1). The AUCs for joint capsule thickness in the axillary recess and for the thicknesses of the enhancing portion of the axillary recess and of the rotator interval were 0.797, 0.861, and 0.847, respectively (Fig. 3). However, the AUC between these thicknesses was not significantly different (p = 0.189). The optimal cutoff values of joint capsule thickness in the axillary recess and the thicknesses of the enhancing portion of the axillary recess and of Fig. 2 Indirect MR arthrography of 21-year-old man without adhesive capsulitis who presented with shoulder pain but did not show restricted range of motion. There is no visible enhancing portion in axillary recess on oblique coronal gadolinium chelate enhanced T1-weighted image. the rotator interval were 4.8, 3, and 4.6 mm, respectively. The corresponding sensitivity and specificity for the diagnosis of adhesive capsulitis were 69% and 78%, 91% and 78%, and 89% and 80%, respectively. Five patients with adhesive capsulitis (14%) and seven control subjects (16%) had subacromial bursitis (p = 1.0). Three patients with adhesive capsulitis (9%) and seven control subjects (16%) had osteoarthritis of the acromioclavicular joint (p = 0.5). No glenohumeral joint effusion was observed in 29 of 35 patients with adhesive capsulitis (83%) and mild loculated fluid signal in six (17%). No glenohumeral joint effusion was observed in 41 of the 45 control subjects (91%), mild loculated fluid signal in three (7%), and extensive fluid signal in one (2%). There was no statistical difference between the two groups in the amount of glenohumeral joint effusion (p = 0.223). Discussion Although the results of many studies have suggested that synovial inflammation with subsequent reactive capsular fibrosis is the underlying pathologic process of adhesive capsulitis based on arthroscopic and pathologic findings and biochemical studies [8, 25 28], the exact cause of adhesive capsulitis remains unclear. Furthermore, there are few laboratory tests or radiologic markers specific for frozen shoulder, so the diagnosis is essentially clinical [1]. However, many studies using various imaging modalities have been performed to determine findings specific for adhesive capsulitis. One of the modalities is MRI. Emig et al. [14] reported imaging findings suggestive of adhesive capsulitis using unenhanced MR images. Several groups of researchers have performed studies with enhanced MR images [10, 13, 29, 30], and Mengiardi et al. [31] and Lee et al. [15] used direct MR arthrography. However, to our knowledge, no study on the imaging findings of adhesive capsulitis has been performed using indirect MR arthrography. W1107

4 Song et al. Sensitivity Specificity Indirect MR arthrography is based on the concept that IV injected contrast material diffuses into the joint space over time, so direct arthrography like images can be obtained [32]. Several advantages of indirect MR arthrography are that intraarticular injection is not needed and the timing of MRI after contrast injection does not have to be exact. In addition, both the joint space and extraarticular vascularized structures will be enhanced on indirect MR arthrography [33]. Hyperemia related to the pathologic process will cause enhancement of extraarticular structures more quickly and intensely. Therefore, the presence and extent of enhancement can be used to detect the pathologic processes. In addition, indirect MR arthrography of the shoulder includes the process of active joint movement after IV gadolinium injection. This process may increase blood supply to the inflamed tissue in the joint. As a result, indirect MR arthrography may increase enhancement in the inflamed tissue in the joint compared with conventional enhanced MR images. There has been disagreement about the usefulness of joint capsule thickness measurements in the axillary recess for the diagnosis of adhesive capsulitis. Emig et al. [14] reported that capsular thickening of more than 4 mm in the axillary recess was a useful criterion for the diagnosis of adhesive capsulitis. On the other hand, there was no significant thickening of the joint capsule in the axillary recess in adhesive capsulitis patients according to Mengiardi et al. [31]. In our Fig. 3 Receiver operating characteristic curve and area under curve (AUC) for diagnosis of adhesive capsulitis using joint capsule thickness in axillary recess evaluated on coronal T2- weighted images (thick black line; AUC = 0.797), thickness of enhancing portion in axillary recess on coronal fatsuppressed enhanced T1-weighted images (thin black line; AUC = 0.861), and thickness of enhancing portion of the rotator interval on sagittal fat-suppressed enhanced T1-weighted images (dashed line; AUC = 0.847). study, joint capsule thickness in the axillary recess was statistically different between the patient group and the control group. However, the mean thickness of the joint capsule in the axillary recess on coronal T2-weighted images was 4.2 ± 1.7 mm in the control group and 5.9 ± 1.7 mm in patients with adhesive capsulitis. The difference between the groups is not substantial. On the other hand, the mean thicknesses of the enhancing portion in the axillary recess and in the rotator interval were, respectively, 2.1 ± 3.0 mm and 3.0 ± 3.6 mm in the control group and 6.5 ± 2.5 mm and 8.3 ± 3.4 mm in the adhesive capsulitis group. The differences in the thicknesses of the enhancing portion in the axillary recess and in the rotator interval were significantly greater than the difference in joint capsule thickness in the axillary recess between the adhesive capsulitis group and the control group. These results may be explained by the possible pathologic process of adhesive capsulitis, such as inflammation and fibrosis, which were mentioned at the beginning of this discussion. Joint capsule inflammation may cause hyperemia in the surrounding soft tissue, which can be enhanced. In other words, enhancement can reflect abnormalities of the joint capsule as well as secondary change of the surrounding soft tissue. On the other hand, joint capsule thickness reflects only joint capsule abnormalities. For this reason, the differences in the thicknesses of the enhancing portion may be greater than the difference of joint capsule thickness between the adhesive capsulitis group and control group. Our study has several potential limitations. We used a set of clinical and radiographic criteria as the reference standard for the diagnosis of adhesive capsulitis. In previous studies, arthrographic or arthroscopic findings were treated as the gold standard for the diagnosis of adhesive capsulitis. However, diagnostic criteria for adhesive capsulitis have not been fully established in arthrography and arthroscopy. In addition, these modalities are invasive. Adhesive capsulitis is usually managed with medical and physical therapies [3 5]. Surgical treatment is applied only to severe cases. Therefore, if arthroscopy findings are treated as the gold standard, selection bias may be increased. The criteria that we used are not a gold standard for the diagnosis of adhesive capsulitis. However, the criteria based on the patient s history, physical examination findings, and radiographic findings are a second-best method considering real clinical situations. Nevertheless, our criteria might not be exactly the same as the criteria used at other institutions. Therefore, our results might not be generalized to populations of patients in other practices using different criteria. Another limitation of our study was that the control group was not age- and sex-matched with the adhesive capsulitis group. There was no significant difference in the mean age. However, subjects in the control group tended to be men. It remains unclear whether matching the control group to the patient group would have had any impact on the results. A final limitation of our study was the exclusion criteria. We excluded patients who had limited shoulder joint motion but did not fulfill the inclusion criteria (i.e., painful restriction of both active and passive elevation to less than 100 and 50% restriction of external rotation). Patients with early-stage adhesive capsulitis may have been excluded. As a result, patients with relatively severe adhesive capsulitis were included in our study and the difference in the thicknesses between the patient and control groups could be exaggerated. In conclusion, an abundance of enhancing tissue in the rotator interval and thickening and enhancement of the axillary recess are signs suggestive of adhesive capsulitis on indirect MR arthrography. References 1. Dias R, Cutts S, Massoud S. Frozen shoulder. BMJ 2005; 331: W1108

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