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Research ArticlePediatric Rheumatology
Open Access

Bone Health in Adult Men and Women with a History of Juvenile Idiopathic Arthritis

JUDITH THORNTON, STEPHEN R. PYE, TERENCE W. O’NEILL, DAVID RAWLINGS, ROGER M. FRANCIS, DEBORAH P.M. SYMMONS, DARREN M. ASHCROFT and HELEN E. FOSTER
The Journal of Rheumatology August 2011, 38 (8) 1689-1693; DOI: https://doi.org/10.3899/jrheum.101232
JUDITH THORNTON
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STEPHEN R. PYE
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TERENCE W. O’NEILL
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  • For correspondence: terence.o'neill@manchester.ac.uk
DAVID RAWLINGS
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ROGER M. FRANCIS
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DEBORAH P.M. SYMMONS
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DARREN M. ASHCROFT
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HELEN E. FOSTER
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Abstract

Objective. Our aim was to determine areal bone mineral density (BMDa) and disease-related factors linked with BMDa in adults with a history of juvenile idiopathic arthritis (JIA).

Methods. Men and women with a history of JIA attending a young adult rheumatology clinic in Newcastle, UK, underwent dual energy x-ray absorptiometry (DEXA) of the lumbar spine and total hip. Information was obtained about disease duration and subtype, previous treatment including corticosteroid and methotrexate therapy, and large-joint replacement. Subjects completed the modified Health Assessment Questionnaire (HAQ). Blood was taken for assessment of C-reactive protein, erythrocyte sedimentation rate, and rheumatoid factor (RF).

Results. Seventy-one women and 16 men, mean age 28.7 and 31.4 years, and mean disease duration 20.6 and 24.0 years, respectively, were studied. Mean BMDa was 0.982 (Z-score = −0.328; 95% CI −0.657, 0.001) and 1.028 g/cm2 (Z-score = −0.251; 95% CI −1.266, 0.764) in women and men, respectively, at the spine and 0.817 (Z-score = −0.542; 95% CI −0.975, −0.109) and 0.857 g/cm2 (Z-score = −0.176; 95% CI −2.323, 1.971) at the hip. After adjusting for age and sex, increasing HAQ score was associated with both lower spine BMDa and hip BMDa. Compared with patients with oligoarticular disease, those with enthesitis-related arthritis had higher BMDa at the spine, while those with extended oligoarticular and polyarticular RF-negative disease had lower hip BMDa. Oral corticosteroids and the presence of a large-joint replacement were associated with lower BMDa at both the spine and hip.

Conclusion. There was a trend toward low BMDa in women with a history of JIA. These patients may be at risk of the complications of osteoporosis including fragility fractures and should be considered for targeted preventive measures.

Key Indexing Terms:
  • JUVENILE IDIOPATHIC ARTHRITIS
  • AREAL BONE MINERAL DENSITY
  • FRACTURE
  • RISK FACTORS

Juvenile idiopathic arthritis (JIA) is a chronic inflammatory disease of childhood. It is associated with decreased areal bone mineral density (BMDa)1,2,3,4,5,6. Known risk factors for low BMDa and fragility fractures in children with JIA include the inflammatory process7, nutrition8, growth impairment9, reduced physical activity8, and treatment, especially corticosteroids5,10. Children with a mean duration of systemic onset JIA of 10.2 years attending Great Ormond Street Hospital, London, UK, had lumbar spine BMDa assessments that were on average 2 SD lower than expected11. Reduced BMDa is associated with an increased risk of fractures. Data from the UK General Practice Research Database showed that a higher proportion of children with arthritis experienced fractures compared with a control group during a median followup of 3.9 years (6.7% vs 3.3%)12.

JIA can persist into adulthood, but few studies have followed bone health beyond childhood7,13,14,15. An understanding of bone health and factors influencing bone health in adults with a history of JIA is important, as reduced bone mass may lead to an increased risk of fracture in later life. Further, a knowledge of factors influencing bone mass is an important first step in developing strategies to optimize bone.

We examined a series of UK patients with a history of JIA who attended a young adult rheumatology clinic. Our aims were to determine the BMDa in affected individuals and to assess disease-related factors linked with BMDa.

MATERIALS AND METHODS

Patients

Consecutive men and women with a history of JIA attending a young adult rheumatology clinic in Newcastle upon Tyne, UK, between 1996 and 2002, were included in the analysis. All patients were seen by the same rheumatologist and assigned a JIA subtype according to the International League of Associations for Rheumatology classification16. The patient group and the JIA young adult clinic have been described17.

Data collection

Dual energy x-ray absorptiometry (DEXA) of the lumbar spine (L1–L4) and hip was performed as part of routine clinical assessment. All scans were done between 1996 and 2002 on either a Hologic 4500A or Hologic QDR 2000 scanner (Bedford, Massachusetts, USA). Each machine was subject to maintenance and regular quality assurance and testing in accordance with the manufacturer’s recommendations. Results were recorded as BMDa (g/cm2) and as an age-standardized or Z-score (the number of SD an observed measurement is from the mean value for an individual of the same age and sex, calculated using the manufacturer’s normative data).

As part of routine clinical practice at the time, all clinic attendees completed a modified Health Assessment Questionnaire (HAQ) and had blood taken for erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), and rheumatoid factor (RF) estimation. Height and weight were recorded at the time of the scan. Clinical records were reviewed within 6 months of the DEXA scan date and often involved retrieval of case notes from many years previously. Information was obtained about disease subtype, disease duration, and current and previous treatment with oral corticosteroids (ever/never). In addition, data were recorded on duration of treatment (months), treatment with methotrexate (yes/no), and large-joint replacement (hip or knee, yes/no). Because this was an audit of clinical practice, all data were anonymous and informed consent was not required.

Analysis

Body mass index was calculated [weight (kg)/height (m)2]. The associations between putative disease-related risk factors and BMDa at both the spine and hip were examined using linear regression, with adjustments made for age and sex. The results were expressed as ß coefficients and 95% CI. Analysis was undertaken using STATA version 9.2 (http://stata.com).

RESULTS

Subjects

Of the 130 patients with a history of JIA who attended the young adult rheumatology clinic, 98 had bone densitometry done of the spine and hip. Eleven of them (3 men and 8 women) were excluded from our study because of missing DEXA data. That left 87 patients for our analysis. The characteristics of these patients are summarized in Table 1. There were 71 women and 16 men; mean age at scan was 28.7 (SD 10.1) and 31.4 (SD 13.8) years, respectively, and mean disease duration was 20.6 (SD 11.0) and 24.0 (SD 13.6) years, respectively. Fifty-one percent of the patients had ever received oral corticosteroids and 29% had taken methotrexate. Some patients had a history of polyarticular RF-negative disease (26%); 21% had polyarticular RF-positive disease, 17% oligoarticular disease, 14% systemic disease, 9% extended oligoarticular disease, 6% psoriasis, 5% enthesitis-related disease, and 2% other. One in 4 had had either hip or knee arthroplasty. The mean ESR at the time of assessment was 23 mm/h, and CRP was 19.2 mg/l.

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Table 1.

Demographic and disease-related characteristics. All data are mean (SD) or n (%).

Bone mineral density

Mean (95% CI) BMDa was 0.982 (0.947, 1.018) and 1.028 (0.910, 1.146) g/cm2 in women and men, respectively, at the lumbar spine and 0.817 (0.761, 0.874) and 0.857 (0.665, 1.050) g/cm2 at the hip (Table 2). In women, the mean Z-score at the spine was −0.328, and at the hip, −0.542, a value significantly lower than would be expected in a normal population (p < 0.02). In men, mean Z-scores were −0.251 at the spine and −0.176 at the hip. Increasing age was significantly associated with BMDa at the spine. BMDa was lower in women compared to men at both spine and hip, although CI embraced unity. After adjusting for age and sex, increasing weight and height were associated with a higher BMDa at both the spine and hip (Table 3). Increasing physical disability (HAQ score) was associated with both a lower spine and hip BMDa. Compared with oligoarticular disease, those with enthesitis-related arthritis had a higher lumbar spine BMDa, while those with extended oligoarticular disease and polyarticular RF-negative disease had lower hip BMDa. Treatment with oral corticosteroids was associated with a lower lumbar spine and hip BMDa, as was having a large-joint arthroplasty (hip or knee).

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Table 2.

Areal bone mineral density (BMDa) and Z-score at the lumbar spine and total hip. Data are mean (95% CI).

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Table 3.

Influence of disease-related factors on areal bone mineral density (BMDa) at the lumbar spine and total hip. Results are expressed as ß-coefficient (95% CI) adjusted for age and sex.

DISCUSSION

In our study, there was a trend toward a low BMDa, particularly at the hip, in women with a history of JIA. BMDa was reduced particularly among patients with more severe disease as determined by disease subtype and level of function.

Ours is the first UK study to examine the effect of disease-related factors on bone health in adults with a history of JIA. It was a retrospective review of clinical practice at the time and accordingly, as with many such clinical outcome studies reliant on retrospective case note analysis, there are a number of limitations to consider. While all patients attending the clinic were offered a bone density scan, about 25% did not subsequently keep the appointment. It is possible that these patients may have differed with respect to bone mass levels from those who had a scan. Their omission may have resulted in an overestimate or underestimate of bone mass levels in the group, and the data need to be interpreted with some caution. It should not have influenced, however, the analysis of disease factors influencing bone mass that was based on an internal analysis of responders. The data concerning disease characteristics, including treatment, were obtained from clinical records and therefore subject to recording errors. Because little information on dose or duration of corticosteroid treatment was available, the analysis of corticosteroid use was restricted to comparison of patients who had ever received or never received corticosteroids. Recording was incomplete for other risk factors for osteoporosis, for example, smoking and drinking habits. The DEXA scans were performed as part of routine clinical practice and on a separate date (invariably within 6 months of the clinical notes reviews and clinic assessment). Finally, the subjects included in the analysis were those who were attending an adult continuity rheumatology clinic and who were therefore likely to have had more severe disease; results should be extrapolated beyond this group with caution.

Our data are consistent with previous studies that reported that BMDa was low in adults with JIA7,13,14,15. A cohort of 32 adults with JIA was followed retrospectively for a mean of 27.1 years; a greater proportion were osteopenic at the femoral neck than would have been expected14. In a case–control study, 65 adult patients (mean age 32.2 years) with a history of JIA were compared with healthy control subjects matched for age, sex, height, and weight. BMDa at the hip and lumbar spine were significantly lower in both men and women with JIA compared with matched healthy control subjects13. Subsequent linear regression with group (JIA or control) as the only predictor confirmed that JIA was strongly associated with hip or spine BMDa (p < 0.001), explaining about 20% of the variation in outcome13. Haugen, et al followed 229 adults with JIA7. The mean followup since diagnosis was 15.6 years in women and 14.9 years in men. Men and women with persistent JIA had significantly reduced BMDa at the femoral neck, total body, and radius and lumbar spine compared with healthy subjects7. In 26 young women with JIA, BMDa (measured using dual photon absorptiometry) was lower than expected in 23% of patients15.

There is some evidence in the literature that disease activity is associated with reduced bone mass in adults with JIA. Zak, et al noted that active disease and spine erosions at baseline were associated with significantly reduced spine BMDa at followup13. In contrast, French, et al, found no association with disease activity as measured by joint count14. Haugen, et al differentiated subjects with active disease and those in remission7. Men and women with persistent disease activity had reduced BMDa, while men in remission had BMDa similar to controls and women had a similar BMDa to controls at the spine, although BMDa was significantly reduced at the femoral neck and total body7. Our study included patients with active disease and also those in remission; who are only seen infrequently. Overall, there was no association with current disease activity as assessed by ESR and CRP at the time of our study.

Previous studies suggested a greater degree of bone loss among those with functional impairment. Thus, higher Steinbrocker functional class in adolescence was associated with reduced adult BMDa at the femoral neck or lumbar spine14 and hip13. Our data support these findings, demonstrating lower bone mass in those with higher HAQ scores. Our data are consistent also with previous studies that suggest that polyarticular disease is associated with a greater degree of bone loss than other disease subtypes13,14. We found also that those with extended oligoarticular disease had reduced bone mass at the hip13. The higher spine bone mass in those with enthesitis-related disease may perhaps reflect the presence of abnormal bone formation related to spondylitis.

Longterm oral corticosteroid treatment is known to be associated with low BMDa and fractures in patients with chronic diseases18,19. Some studies support an association between corticosteroid therapy and bone mass in JIA. Haugen, et al found duration of corticosteroid treatment was associated with low BMDa7 and comparing T-scores, while Zak, et al found corticosteroid treatment for > 1 year was associated with reduced BMDa13. In contrast, French, et al found no association of reduced BMDa with corticosteroid treatment, although the number of patients treated with corticosteroids was low14. We found that those with a history of corticosteroid therapy had lower bone mass than those without, although there was no apparent association with duration of therapy. It is possible this may have been due to a lack of accurate recording of therapy in the medical record. Evidence of an association, however, does not imply causality and it is possible that the apparent association may have been confounded by disease severity.

Our results suggest that there is a reduction in bone mass in adults with a history of JIA and they are therefore likely to be at increased risk of fracture in later life. A metaanalysis of 11 prospective cohort studies (90,000 patient-years and 2000 fractures of any type) demonstrated that the risk of fracture in otherwise healthy adults appears to double for each 1 SD decrease in BMDa20. Thus, measures to optimize bone health in patients with JIA need to be considered, including modification of reversible risk factors and also optimizing function. In those with severe disease or those on longterm corticosteroids, bone densitometry should be considered an important component of routine clinical practice.

BMDa is reduced in some adults with JIA, particularly among those with more severe disease. These patients are at risk of the complications of osteoporosis in the future, including fragility fractures, and should be considered for preventive therapy.

Acknowledgment

The authors thank Dr. Namita Kumar and Dr. Sarah Bartram, who were involved in the data collection.

Footnotes

  • Support from the UK Department of Health through its Health Technology Assessment Programme and Arthritis Research UK.

  • Full Release Article. For details see Reprints/Permissions at jrheum.org

  • Accepted for publication April 4, 2011.

Free online via JRheum Full Release option

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Bone Health in Adult Men and Women with a History of Juvenile Idiopathic Arthritis
JUDITH THORNTON, STEPHEN R. PYE, TERENCE W. O’NEILL, DAVID RAWLINGS, ROGER M. FRANCIS, DEBORAH P.M. SYMMONS, DARREN M. ASHCROFT, HELEN E. FOSTER
The Journal of Rheumatology Aug 2011, 38 (8) 1689-1693; DOI: 10.3899/jrheum.101232

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Bone Health in Adult Men and Women with a History of Juvenile Idiopathic Arthritis
JUDITH THORNTON, STEPHEN R. PYE, TERENCE W. O’NEILL, DAVID RAWLINGS, ROGER M. FRANCIS, DEBORAH P.M. SYMMONS, DARREN M. ASHCROFT, HELEN E. FOSTER
The Journal of Rheumatology Aug 2011, 38 (8) 1689-1693; DOI: 10.3899/jrheum.101232
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