Clinical features of adult-onset ankylosing spondylitis in Korean patients: patients with peripheral joint disease (PJD) have less severe spinal disease course than those without PJD

H. J. Baek, K. C. Shin1, Y. J. Lee2, S. W. Kang3, E. B. Lee1, C. D. Yoo1 and Y. W. Song1

Division of Rheumatology, Department of Internal Medicine, Gachon Medical School, Gil Medical Center, Inchon, 1 Division of Rheumatology, Department of Internal Medicine, Seoul National University College of Medicine, Seoul, 2 Division of Rheumatology, Department of Internal Medicine, Seoul National University Bundang Hospital, Seongnam, Gyeonggi Province and 3 Division of Rheumatology, Department of Internal Medicine, Chungnam National University College of Medicine, Daejeon, South Korea.

Correspondence to: Y. W. Song, Department of Internal Medicine, Seoul National University Hospital, 28 Yungon-dong, Chongno-gu, Seoul 110-744, Korea. E-mail: ysong{at}snu.ac.kr


    Abstract
 Top
 Abstract
 Introduction
 Patient and methods
 Results
 Discussion
 References
 
Objective. We investigated the clinical features of Korean patients with adult-onset ankylosing spondylitis (AAS) and examined the differences between AAS patients with and without peripheral joint disease (PJD).

Methods. We studied 67 consecutive patients with primary AAS who visited the rheumatology clinic of a tertiary referral hospital. All patients experienced joint symptoms after the age of 15 and fulfilled the modified New York criteria for ankylosing spondylitis. Hips and shoulders were not considered as peripheral joints.

Results. The male-to-female ratio was 8.6:1.0. Mean age at disease onset was 22.3 ± 5.5 (mean ± S.D.) yr and disease duration was 10.8 ± 8.0 yr. Spinal symptoms were the first manifestations in 80.6% of patients. During the disease course, hip, shoulder and peripheral joint involvement were found in about 60% of patients. In patients with PJD, the most commonly affected joints were the knees and ankles. The pattern of PJD, in most cases, was asymmetrical and mono/oligoarticular. AAS patients with PJD had fewer spinal symptoms than those without PJD as a presenting feature (71.8 vs 92.9%, P = 0.035). The modified Schober test showed greater increments in patients with PJD (4.9 ± 2.4 vs 3.0 ± 2.4 cm, P = 0.002). Forced vital capacity was better in patients with PJD (79.0 ± 11.4 vs 70.8 ± 15.5% of predicted value, P = 0.016). Totally ankylosed sacroiliitis, spinal squaring and syndesmophytes on radiographs were less common in the patients with PJD than in those without PJD (33.3 vs 64.2%, P = 0.012; 20.5 vs 67.9%, P = 0.000; and 38.5 vs 71.4%, P = 0.008, respectively).

Conclusion. Peripheral joints as well as shoulder and hip joints were more frequently involved during the disease course in Korean AAS patients compared with earlier reports in Caucasians. The general joint involvement pattern of PJD was similar to patterns reported previously. Our data suggest that, clinically and radiographically, AAS patients with PJD have a less severe spinal disease course than those without PJD.

KEY WORDS: Ankylosing spondylitis, Adult-onset ankylosing spondylitis, Peripheral arthritis


    Introduction
 Top
 Abstract
 Introduction
 Patient and methods
 Results
 Discussion
 References
 
Ankylosing spondylitis (AS) is a chronic, systemic inflammatory rheumatic disorder of the axial skeleton which affects the sacroiliac joints and the spine. Involvement of the peripheral joints, other than the hips and shoulders, is known to be infrequent in primary AS [1]. Moreover, peripheral arthritis has been suggested to be a predictor of disease progression [2] and loss of function [3].

AS occurs worldwide, but some researchers have remarked that ethnic or geographic differences exist in terms of the prevalence and clinical expression of the disease [4, 5]. For example, the prevalence of AS varies from 0 to 1.8% and is highest in persons of northern European heritage and lowest in sub-Saharan Africa [6]. It has also been reported that juvenile onset in AS is relatively more common in non-Caucasians, such as Koreans, native Americans and Mexican mestizos, and in many other developing countries than in Caucasians [5, 7].

The documented clinical features of AS have been largely derived from studies on Caucasian patients, and studies on non-Caucasians are relatively scarce. Previously we assessed the frequency of juvenile-onset in Korean AS patients, and differentiated the clinical characteristics of juvenile-onset and adult-onset AS (AAS) [7]. The present study was conducted upon AAS patients enrolled in the previous study to investigate the clinical features of AAS, and the differences between AAS patients with and without peripheral joint disease (PJD).


    Patient and methods
 Top
 Abstract
 Introduction
 Patient and methods
 Results
 Discussion
 References
 
We studied 67 consecutive AAS patients who visited or were referred to the Rheumatology Clinic at Seoul National University Hospital (a tertiary referral centre) between March 1997 and August 1998. All patients had experienced joint symptoms after the age of 15, fulfilled the modified New York criteria for AS [8], and had no history of psoriasis, inflammatory bowel disease or infection associated with arthritic symptoms. This study was approved by Seoul National University Hospital Ethics Committee and informed consent was obtained from all patients.

We obtained information about articular symptoms at disease onset and during the disease course, and the histories of extraskeletal manifestations via medical records and interview. Joint symptoms were defined as pain, swelling, or limitations of joint motion. In regard to the spine, symptoms were defined as pain or stiffness of the neck, upper back, lower back or buttock which was relieved by exercise. Enthesopathy was defined as a history of focal pain at entheses. The functional classes of all patients were assessed according to the American College of Rheumatology criteria [9].

We performed complete joint and enthesis examinations and physical measurements in all patients at study entry. Current joint involvement was defined to be present when a joint showed swelling, tenderness, or limited motion on physical examination. Tragus-to-wall distance and chest expansion at the level of the fourth rib anteriorly were measured. Lumbar spinal mobility was assessed by Macrae's modification of Schober's test [10]. At the examination, joint radiographs, and laboratory evaluations, including complete blood cell count, Westergren erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), HLA-B27, rheumatoid factor (RF), antinuclear antibody (ANA), urinalysis, electrocardiography, and pulmonary function test were performed in all patients. Cervical, thoracic, lumbar spine and pelvis radiographs were taken of all patients. Radiographs of other joints were taken where there was joint involvement by history or current joint examination. We compared the clinical, laboratory and radiographic features of patients with and without PJD. PJD was defined when a patient had peripheral joint symptoms at some time during the disease course, as confirmed by careful history taking or a joint examination. Hips and shoulders were not considered as peripheral joints. Radiographs were read by a musculoskeletal radiologist, who had clinical information on the patients but did not know whether the patients had PJD. Differences in the results were analysed using Student's t-test, the {chi}2 test or Fisher's exact test. Significance levels of all tests were set at P = 0.05 without Bonferroni adjustment.


    Results
 Top
 Abstract
 Introduction
 Patient and methods
 Results
 Discussion
 References
 
The male-to-female ratio was 8.6:1.0 (Table 1). Mean age at disease onset was 22.3 ± 5.5 (mean ± S.D.) yr, and disease and spinal symptom durations were 10.8 ± 8.0 and 9.9 ± 8.0 yr, respectively. PJD was detected in 58.2% of the patients (n = 39) and uveitis in 28.4%. No significant difference was found between the patients with or without PJD in terms of sex ratio, age at disease onset, duration of disease or spinal symptoms, frequency of uveitis, or functional class. The percentages of patients who had taken NSAIDs, sulphasalazine and prednisolone at study entry were 73.1, 32.8 and 6.0% respectively. Medication was not different for those with or without PJD (data not shown), except that sulphasalazine was more frequently used in the former (43.6 vs 17.9%, P<0.05; {chi}2 test).


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TABLE 1. Characteristics of AAS patients with PJD vs those without PJD

 
Spinal symptoms were the first manifestations in 80.6% of patients (Table 2). Shoulder involvement was rare as a presenting symptom (4.5%). Hips and peripheral joints were sometimes involved at disease onset (22.4 and 20.9%, respectively). However, during the disease course, hip, shoulder and peripheral joint involvement were found in about 60% of patients. Although enthesopathy was rarely detected as a presenting feature (1.5%), it usually happened during the disease course (82.1%). Patients with PJD had less common spinal involvement at presentation than those without (71.8 vs 92.9%, P = 0.03515; {chi}2 test). Shoulder involvement was more frequent in patients with PJD than those without PJD during the disease course and by current (i.e. the last) joint examination (76.9 vs 35.7%, P = 0.00156 and 43.6 vs 10.7%, P = 0.00373 respectively; {chi}2 test).


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TABLE 2. Joint involvement of patients with AAS with PJD vs those without PJD

 
In the patients with PJD, the lower limb joints, especially knees and ankles, were the most commonly affected (Table 3). Knee joint disease was revealed in 30.8% of the patients at disease onset, in 92.3% during the disease course, and in 20.5% on current joint examination. Ankles were involved in 7.7, 38.5 and 12.8% respectively. The pattern of PJD, in most cases, was asymmetrical and mono/oligoarticular at disease onset (64.3 and 100% respectively) and by current joint examination (93.7 and 93.8% respectively).


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TABLE 3. Peripheral joint involvement in patients with AAS (n = 39)

 
In terms of spinal mobility measurements, the tragus-to-wall distance, chest expansion and modified Schober index were 12.9 ± 6.4, 3.3 ± 1.8 and 4.1 ± 2.5 cm respectively (Table 4). Comparing patients with and without PJD, the former had better spinal mobility results than the latter. The patients with PJD had more increment than those without PJD in the modified Schober test (4.9 ± 2.4 vs 3.0 ± 2.4 cm, P = 0.00231; Student's t-test). Tragus-to-wall distance tended to be shorter and chest expansion greater in patients with PJD (11.6 ± 3.6 vs 14.7 ± 8.8 cm; P = 0.09 and 3.6 ± 1.8 vs 2.8 ± 1.6 cm, P = 0.06 respectively; Student's t-test).


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TABLE 4. Spinal mobility measurements of patients with AAS with PJD vs those without PJD

 
All patients showed radiographic sacroiliitis (Table 5). Sacroiliitis grade 4 (total ankylosis) [8] was less common in the patients with PJD (33.3 vs 64.2%, P = 0.0122; {chi}2 test), and radiographic abnormalities of the spine seemed to be less prevalent in those with PJD (69.2 vs 96.4%), but this was not statistically significant. However, patients with PJD showed significantly less common squaring and syndesmophytes (20.5 vs 67.9%, P = 0.0001 and 38.5 vs 71.4%, P = 0.00771 respectively; {chi}2 test). Frequencies of radiographic abnormalities of hip, shoulder or enthesis were similar in the two groups.


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TABLE 5. Radiographic abnormalities of patients with AAS with PJD vs those without PJD

 
Our data suggest that AAS patients with PJD have a clinically and radiographically less severe spinal disease course than those without PJD. Therefore, we performed an additional comparison between the patients with current PJD on examination (n = 16) and those without PJD during the disease course (Table 6). There were no significant differences between the patients with current PJD and without PJD in terms of sex ratio, age at disease onset, disease duration and duration of spinal symptoms (data not shown). However, the modified Schober test showed a greater increment (4.6 ± 2.3 vs 3.0 ± 2.4 cm, P = 0.0359; Student's t test) and squaring was less frequent (25.0 vs 67.9%, P = 0.00618; {chi}2 test) in the patients with current PJD than in those without PJD. Proportions of advanced sacroiliitis (grade 4) and syndesmophytes tended to be decreased in those with current PJD compared with those without PJD (43.8 vs 64.2%, P = 0.18587 and 43.8 vs 71.4%, P = 0.06970 respectively, {chi}2 test).


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TABLE 6. Comparison between patients with AAS with current PJD vs those without PJD during the disease course

 
Anaemia, leucocytosis, elevated Westergren ESR (>20 mm/h) and CRP (>0.5 mg/dl) were observed in 35.8, 10.4, 67.7 and 64.2% of AAS patients respectively. Laboratory studies, except ESR and forced vital capacity (FVC), were not significantly different between the two groups (Table 7). ESR was higher in those with PJD (45.9 ± 34.2 vs 26.5 ± 20.0 mm/h; P = 0.0047, Student's t-test), as was FVC (79.0 ± 11.4 vs 70.8 ± 15.5% of predicted value; P = 0.01632; Student's t-test).


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TABLE 7. Laboratory characteristics of patients with AAS with PJD vs those without PJD

 

    Discussion
 Top
 Abstract
 Introduction
 Patient and methods
 Results
 Discussion
 References
 
AS is more common in men than in women. The male:female ratio has been reported recently to be about 2:1 to 3:1 [11, 12], but in our series it was found to be higher (8.6:1.0). The ratio varies by geographical location, and like ours, some studies of non-Caucasians have revealed a remarkable male predominance (7:1 to 16:1) in AS [13–18]. Moreover, ethnic factors may have influenced male predominance in the present study. However, it may be more associated with the referral bias. Since in AS men tend to have a more severe disease course and/or more spinal involvement than women [19–25], men might have been recruited more often than women in the present study, which was conducted at a tertiary referral hospital.

AS usually begins in late adolescence or early adulthood; onset after 45 yr is very uncommon. Chronic back pain is a presenting symptom in approximately 75% of AAS patients. Hips and shoulders are the most frequently involved extraspinal joints in AS. Involvement of peripheral joints other than hips and shoulders is infrequent in primary AS [1]. Hips and shoulders are involved at presentation in up to 15% of patients and at some stage of disease in up to 35% [19]. Peripheral joint involvement is a presenting feature in only 10–20% of patients and occurs during the disease course in 30–40% [26–28]. Age at disease onset and the frequencies of presenting joint symptoms in our series are comparable to those in earlier reports. However, during the disease course the frequencies of extraspinal joint involvements were higher (shoulder, 59.7%; hip, 59.7%; peripheral joints, 58.2%) than in previous studies. Recent studies have reported that peripheral joint involvement is relatively more frequent (61–100%) in some areas [4, 17, 18, 29–31], or among patients with juvenile onset AS [5, 7, 16]. Our study revealed that Korean patients with primary AAS also have a higher frequency of extraspinal joint involvement.

The peripheral joints most commonly involved in AS are those of the lower limbs, particularly the knees and ankles, with an oligoarticular and asymmetrical pattern [26]. In our patients, similarly, the most commonly involved peripheral joints were the knees and ankles at disease onset, during the disease course and on current physical examination. Mono/oligoarticular and asymmetrical involvement also predominated at disease onset (100 and 64.3%) and on current examination (93.8 and 93.7%) (data not shown).

Early involvement of peripheral joints, including the hips and shoulders, was reported to be a poor prognostic sign of spinal mobility [2]. However, in our study patients with PJD showed better results in the modified Schober test than those without PJD. Pulmonary function tests also revealed a smaller FVC reduction in patients with PJD. Reduced FVC is caused by restriction of chest wall movement due to the fusion of costovertebral joints [32]. On radiographs, totally ankylosed sacroiliitis (grade 4), spinal squaring and syndesmophytes were observed less frequently in those with PJD. These results suggest that, clinically and radiographically, AAS patients with PJD have a less severe spinal disease course than those without. Taking sulphasalazine was more prevalent in the former group. However, spinal disease in those with PJD would not be influenced by sulphasalazine since it was found to have no significant effect in ameliorating the axial disease associated with AS and spondyloarthropathies [33, 34].

In our study, PJD was defined as having peripheral joint disease at some time during the disease course, not current peripheral joint involvement confirmed by joint examination. Such a definition would be relevant in classifying PJD in AS because PJD is usually transient and rarely persistent in patients with AS [1]. However, it could be less clear that PJD group was classified based mainly on history and medical records. Therefore, we performed an additional comparison of the patients with current PJD on examination, the smaller but more clearly defined group. The difference mentioned above was still evident. In addition, decreased FVC was significantly less frequent in those with current PJD than in those without PJD (37.5 vs 71.4%, P = 0.02767; {chi}2 test) (data not shown). Statistical non-significance in regard to advanced sacroiliitis and syndesmophytes could have occurred because the sample size of patients with current PJD was too small. Some authors have reported that female sex [19, 20, 22–25] and juvenile onset [7] are associated with less severe spinal disease course in AS patients. According to our data, PJD may also indicate a relatively less severe spinal disease course in patients with primary AAS.

Clinical and radiographic differences are known to exist in spondyloarthropathies [35]. Peripheral arthropathy is more common in patients with reactive and psoriatic arthritis than in those with primary AS. On the contrary, sacroiliitis and radiographic spinal changes, such as squaring and syndesmophytes, are observed less frequently in reactive and psoriatic arthritis than in primary AS. Therefore, AS with PJD in our series could be regarded as having features intermediate between those of primary AS with predominant axial disease and reactive or psoriatic arthritis.

Elevated ESR or CRP is common in patients with active AS (up to 70%). These variables are not clearly correlated with clinical disease activity and may be related more to peripheral arthropathy than axial disease in AS [20, 36, 37]. ESR was higher in patients with PJD in the present study. Anterior uveitis is the most common extraskeletal feature in AS patients, and occurs in 20–30% of patients at some time during the disease course [38]. We found a similar frequency of uveitis in AAS patients (28.4%). HLA-B27 is known to be positive in over 90% of Caucasian AS patients, in 50% of black AS patients [39, 40] and in 83.3% of Korean AS patients [41]. HLA-B27 positivity was very high in our patients (98.5%).

Some limitations of the present study should be considered. The study might contain an inevitable referral bias since our patients with current AAS were collected, classified and analysed retrospectively in a single tertiary hospital. It is also likely that there are recall biases with respect to symptoms at onset and during the disease course, since our data relied to a large extent on patient memory. Our series also included some prevalent cases referred from other hospitals or being followed at our clinic. Thus, our data could be less representative than data collected at diagnosis, although this condition does not significantly influence comparisons between those with and without PJD.

Our study describes clinical features of AAS in Korean patients. Peripheral joints, shoulders and hips were found to be more frequently involved during the disease course than has been reported for Caucasians. However, the general joint involvement pattern of PJD was similar to those reported previously. Patients with PJD showed better results in the modified Schober test and FVC, and had a reduced frequency of advanced radiographic sacroiliitis, spinal squaring and syndesmophytes than those without PJD. These data suggest that, clinically and radiographically, AAS patients with PJD have a less severe spinal disease course than those without.


    Acknowledgments
 
This study was supported by a grant from Seoul National University and KISTEP.

The authors have declared no conflicts of interest.


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 Abstract
 Introduction
 Patient and methods
 Results
 Discussion
 References
 

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Submitted 2 March 2004; revised version accepted 13 July 2004.



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