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- PATIENTS AND METHODS
Among inflammatory rheumatic diseases, the spondylarthropathies form a prominent subgroup (1). The characteristic clinical features of ankylosing spondylitis (AS) have been well documented over the years with efforts to clinically classify the condition among the other spondylarthropathies (2). Shoulder involvement as part of the spectrum of joint disease in AS has been described (3, 4), as has shoulder pain as a first clinical presentation in AS patients in whom a diagnosis had not been made (5, 6). Reported prevalence based on clinical assessment has varied from 7% to 33%, although these studies were neither controlled nor conducted using standardized and validated clinical assessment instruments (3, 4, 7, 8). A prevalence of 11.7% for shoulder pain has been reported in 1 community-based survey (9).
The cause of shoulder pain in AS patients has, on clinical grounds, been presumed to be due to synovitis, bursitis, or structural joint damage; however, no studies have systematically examined the etiology of shoulder pain in a controlled format. Several cross-sectional plain radiographic surveys have described joint space narrowing, erosion, and bony proliferation in the acromioclavicular joint, the glenohumeral joint, and around the rotator cuff insertion (3, 4, 10). Limitations of these studies include the lack of controls and systematic evaluation together with the limited sensitivity of plain radiographic assessment. In one study, radiographs were reported as normal in 23% of patients with restricted shoulder movement (4).
Since the term enthesopathy was first used, there has been increasing evidence in support of enthesitis being a prominent feature of AS (11, 12). Enthesitis has been demonstrated in various peripheral locations including the Achilles tendon, pes anserinus, greater trochanter, ischial tuberosities, and the knee (13–16), but it has not yet been formally evaluated in the shoulder. Limited success has been achieved in demonstrating enthesitis in patients with seronegative arthropathy using high-definition ultrasound and scintigraphy. One study reported abnormal echogenicity in 46% of patients with symptomatic plantar fasciitis and spondylarthropathy (17) and bone scintigraphy identified 94% of lesions in a group of patients with heel enthesitis secondary to Reiter's syndrome; specificity was not examined (18).
These techniques, however, do not reveal abnormalities in the bone marrow adjacent to an enthesis. The advent of fat suppression sequences in magnetic resonance imaging (MRI) has allowed study of bone marrow changes in AS at various sites, with most attention being paid to the spine and the lower limbs (12, 19–22). McGonagle et al have demonstrated the value of fat suppression sequences in imaging of the knee in patients presenting to an early arthritis clinic (12). They were able to locate separate regions of entheseal and nonentheseal bone marrow edema (BME) in addition to synovitis. The presence of entheseal edema within the knee allowed differentiation of those patients who ultimately developed AS versus rheumatoid arthritis.
Despite the common occurrence of shoulder pain in AS, its etiologic basis remains to be defined. The humeral tuberosities, acromial insertion of the rotator cuff, and clavicular insertion of the deltoid muscle represent entheses that could be inflamed, but also include sites where pathology is commonly observed in the general population. The purpose of this study was therefore to examine the prevalence and characteristics of clinically defined shoulder disease in patients with AS compared with age- and sex-matched controls; furthermore, we aim to determine the sensitivity and specificity of MRI-defined lesions in the shoulders of AS patients compared with otherwise normal individuals with nonspecific shoulder pain presenting for MRI examination.
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- PATIENTS AND METHODS
This work represents the first systematic, controlled evaluation by clinical exam and MRI of shoulder disorders in patients with AS. It shows that symptomatic disease is comparatively common when compared with other peripheral sites of involvement. Furthermore, the frequency of abnormal radiologic findings may represent a conservative estimate because MRI examination demonstrated lesions in the acromioclavicular joint of almost all AS patients. This is despite the absence of supporting clinical findings and despite the fact that AS patients with asymptomatic shoulders were not scanned.
The greater tuberosity was included in the first index that was developed to score enthesitis (28), but the comparative frequency of involvement has been addressed in only one study that attempted to develop a more simplified version of this index (29). In this latter study, the process of data reduction based on the frequency of involvement led to a more concise index that primarily included entheses located in the axial skeleton with only the Achilles tendon enthesis being included as a peripheral site. Achilles tendon involvement was much less common in our prospective cohort (data not shown), suggesting either referral bias or potential differences in disease phenotype as possible explanations. Yet another recent approach to scoring enthesitis does not even include the shoulder in the scoring system (30). In addition, a recent comprehensive evaluation of peripheral entheses by ultrasound in 164 patients with spondylarthropathy also did not evaluate the shoulder (31).
This study also demonstrates the major MRI findings in the shoulder of a group of AS patients with shoulder pain compared with a control group of symptomatic patients not known to have any inflammatory arthropathy. Intense entheseal BME, particularly in the acromion and in association with erosion at the greater tuberosity, was the most specific finding in AS shoulders. Greater tuberosity edema was evident in controls, where it was usually mild and almost always associated with cuff tear. In the AS group, 5 patients demonstrated intense humeral BME, 3 of which had no associated cuff tear and 2 had only a small tear. Entheseal BME at the acromial or clavicular origin of the deltoid was present in 10 shoulders in the AS group compared with 1 control shoulder with a deltoid muscle injury. The presence of entheseal BME, particularly intense BME in the absence of significant injury, appears to be a finding specifically associated with AS. It was interesting to note that in one of our patients, acromial entheseal BME at the posterior deltoid origin was only well demonstrated on the sagittal fat suppressed image. The coronal image made confident assessment for edema at the posterior aspect of the acromion difficult due to partial volume averaging at this location. In view of this observation, we feel a sagittal fat suppressed image is essential in the assessment of acromial edema.
A previous study had examined the shoulder of 26 consecutive AS patients attending an in-patient physiotherapy program using plain radiography (4). Radiologic changes were common but usually minor, being evident in 31% of patients, the acromioclavicular joint being most commonly involved. Severe radiologic changes in the glenohumeral joints were noted in 9 (17.3%) shoulders, these being cystic changes, proliferation, and enthesopathy. Features suggesting rotator cuff degeneration were common and included cystic changes in the humeral head, erosion at the rotator cuff insertion, bony proliferation, and enthesopathy. A significant limitation of this latter study (4) was the absence of a control group. Our present study showed an even lower prevalence of glenohumeral lesions that was no different from that observed in controls. In addition, the lack of sensitivity is highlighted by the absence of radiologic changes in 26% of patients that had restricted shoulder movement. One additional study examined 52 AS patients and noted plain radiographic abnormalities in 29 shoulders, especially narrowing of the acromioclavicular joint (3). As highlighted in our report, acromioclavicular joint arthropathy is also commonly observed in other causes of shoulder pain. Sclerosis of the greater tuberosity and cystic changes in the humeral head were again noted, although as for the previous study, there was no control group.
McGonagle et al have demonstrated the presence of entheseal BME in sites around the knee joint and differentiated this from the findings in patients with rheumatoid arthritis (11). In their AS population, 6 (60%) of the 10 knee examinations demonstrated entheseal BME at an entheseal site. This is in concordance with our own findings in which 70.6% of the examinations in AS patients demonstrated entheseal BME (53% intense) either at the humeral tuberosity, acromial enthesis, or clavicular enthesis. However, they demonstrated perientheseal edema in all 10 knee examinations in their AS group, which was seen less commonly in our group. It is unclear whether this difference is due to image interpretation or a real variation in the course of the disease in the shoulder and the knee. This group has also shown that BME is common in patients with mechanical enthesopathy, namely, plantar fasciitis (32). However, this was more pronounced in spondylarthropathy patients with concomitant plantar fasciitis who were HLA–B27 positive. This concurs with our results demonstrating the specificity of intense entheseal edema for AS.
The variable sensitivity and specificity of clinical examination techniques has been previously noted (33, 34). One limitation of our study was the absence of a subacromial lidocaine injection test, although this may not discern the presence of symptoms arising from entheseal bone edema. As a consequence, it was unclear from this study whether the presence of entheseal BME and enthesitis was the predominant cause of pain in the AS patients in whom it was observed. A further limitation was that MRI examination was not performed on the control group that was also evaluated clinically (control cohort A).
Our data clearly show that primary glenohumeral joint involvement is not a feature of AS. This concurs with the careful pathologic examination by Romanus and Yden (35). Previous reports of narrowing of this joint likely reflect the elevation of the humeral head in relation to the glenoid, indicating rotator cuff disease associated with impingement and secondary osteoarthritis of the glenohumeral joint.
Early detection of AS is now becoming more important with the promise of disease-modifying therapy (30, 36). BME, rotator cuff tear, and entheseal inflammation can be examined by the single modality of MRI. As MRI examination becomes more widespread, the need to recognize features that may indicate the presence of AS becomes more important.
Our results lead us to conclude that in the absence of a significant rotator cuff injury, the presence of entheseal BME and, in particular, intense entheseal BME or erosive change with adjacent BME strongly suggests the presence of AS. The comparatively high frequency of rotator cuff enthesopathy also emphasizes the importance of recording this site both in routine clinical evaluation and in instruments for scoring enthesitis in clinical research. These findings will need to be further validated in other types of spondylarthropathy.