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Pediatric Physical Therapy:
doi: 10.1097/PEP.0b013e318036a25e
Review Article

Can Exercise Influence Low Bone Mineral Density in Children with Juvenile Rheumatoid Arthritis?

Gannotti, Mary E. PT, PhD; Nahorniak, Maureen MBA, PT; Gorton, George E. III BS; Sciascia, Krystal SPT; Sueltenfuss, Megan SPT; Synder, Michelle SPT; Zaniewski, Anna MSPT

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Author Information

University of Hartford (M.E.G., K.S., M.S., M.S, A.Z.), Hartford, Connecticut and Shriners Hospital for Children (M.N., G.E.G.), Springfield, Massachusetts

Address correspondence to: Mary E. Gannotti, PT, PhD, Physical Therapy Department, Dana 410F, 200 Bloomfield Avenue, University of Hartford, West Hartford, CT 06117. Email: gannotti@hartford.edu

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Abstract

Purpose: Low bone mineral density (BMD) is a common secondary condition associated with juvenile idiopathic arthritis (JIA). The purpose of this review was evaluate the literature pertinent to designing an effective, safe weight-bearing exercise program to reduce the risk of low BMD in children with JIA.

Summary of key points: Thirty-seven articles on the risk of low BMD and children with JIA, weight-bearing interventions to improve BMD in healthy children, or safety and efficacy of exercise interventions with children with JIA were critiqued on the basis of their design. Three highly rated studies confirmed the multifactorial nature of low BMD in children with JIA, two highly rated studies support the efficacy of weight-bearing interventions for increasing BMD in children who are healthy, and one moderately rated study demonstrated the safety of low impact exercise by children with JIA.

Statement of conclusions and recommendations for clinical practice: Weight-bearing activities should be included in exercise programs for individuals with JIA, although more research is needed to determine the amount, duration, and frequency of weight-bearing activity needed to reduce the risk for low BMD.

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INTRODUCTION

Children with chronic arthritis are at risk for developing joint deformities and contractures. These impairments, coupled with pain and inflammation, lead to decreased ability to perform activities of daily living and decreased participation in recreational or social activities.1 Secondary effects of chronic arthritis include growth retardation, reduced bone mineral density (BMD), joint deformity, and decreased physical conditioning.2–8 Of these, reduced BMD is a significant problem, increasing the risk for osteoporosis, compression fractures, or fractures in long bones.

Osteoporosis is low bone mass and the structural deterioration of bone tissue leading to bone fragility and increased risk of fracture.9 Low BMD, or osteopenia, is defined by the World Health Organization (WHO) as bone density 1.0 to 2.5 standard deviations below the mean for young white women.10 Osteoporosis is defined by WHO as 2.5 standard deviations or more below the mean. There currently are no accepted definitions for osteoporosis in childhood because the WHO criteria refer to peak bone mass obtained by adults.11 However, z-scores can be used to classify the BMD of children. Using an age- and gender-matched control group, a z-score can be calculated (the BMD of child is subtracted from the mean BMD of control group divided by the standard deviation of control group). For children with a z-score of −2.0 or less, a characterization of “low bone density for chronologic age” is appropriate.11

Osteoporosis in children is rare and usually is associated with an underlying condition.12 Juvenile idiopathic arthritis (JIA) is a condition recognized by the National Institute of Health as placing children at risk for osteoporosis.12 JIA is “arthritis of unknown etiology that begins before the 16th birthday and persists for at least six weeks; and other known conditions are excluded.”13(p. 390) JIA is the most common form of arthritis in children, affecting more than 300,000 U.S. children (or 1:1000),1,14 with incidences reported from two to 20 per 100,000 worldwide.14 The International League of Associations of Rheumatology identifies seven subtypes of JIA, and the features of each condition are listed in the Appendix of this review.*13,15,16

Healthy People 201017 goals include preventing secondary conditions in people with chronic disability that lead to a decreased quality of life. Physical therapists could play an important role in reducing risk for low BMD in children with JIA. Although rheumatologists advocate nutritional supplementation and weight-bearing activities to improve BMD,18 no studies provide clinicians with guidelines for a safe, effective weight-bearing program for children with chronic arthritis to increase BMD.

Decreased aerobic and anaerobic fitness, decreased physical activity and functional abilities, and concern about joint health and the ability to participate in weight-bearing activities have been identified as issues for children with JIA. Exercise recommendations for aerobic and anaerobic exercise include activities that do not load the joints (ie, isometric knee contractions, aquatic therapy).19–22 Encouraging increased physical activity as part of daily routines is also suggested.23 Aerobic fitness in children with JIA is limited,19,22–25 and aerobic conditioning is recommended as soon as the diagnosis is made. Anaerobic conditioning also is needed, as anaerobic fitness has been found to be strongly associated with functional abilities.26

Nonetheless, no studies were located in the literature that examine the safety of a physical exercise regime or weight-bearing activities designed to reduce the risk for low BMD in children with JIA. Additionally, not all children with JIA have low BMD, and certain factors may place children at greater risk.18 More information is needed before physical therapists are able to appropriately prescribe a weight-bearing program for at-risk children with JIA. In fact, a synthesis of the literature pertinent to this topic is necessary before an appropriate exercise program can be designed or prescribed.

The purpose of this review of the literature was to explore the topics of low BMD in children with JIA and exercises to improve BMD in such a way that a research project could be designed to advance knowledge in this area. Because there currently are no published studies on the topic of weight-bearing programs to improve BMD in children with JIA, research on activities designed to promote BMD in healthy children also were considered.

Thus, specific questions guiding the review included: (1) what factors are the most strongly associated with low BMD in children with chronic arthritis? (2) What activities promote the most bone accrual in healthy children? (3) What exercises and physical activities that promote weight-bearing/physical activity have been proven safe and effective for children with JIA?

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METHODS

A systematic review of the literature related to the questions outlined previously was performed. Criteria for considering studies concerning factors associated with reduced BMD in children with JIA (question 1) included case-series and cohort studies of patients with the diagnosis of JIA and with BMD as the outcome variable. Narrative reviews of the literature and expert opinion articles were not included because of the large number of published case-series and cohort studies. For question 2, criteria included randomized controlled trials (RCTs) with children who are healthy as subjects and using weight-bearing programs as an intervention with BMD as an outcome variable. Only RCTs were considered because of the large amount of published literature on the topic. And, finally, to address question 3 concerning the safe use of exercises that promote weight-bearing and physical activity for children with JIA, criteria included articles with children with JIA as subjects and an exercise program as an intervention. Cohort and RCTs were included.

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Identifying Articles

Databases searched included Pub Med, CINHAL, Physiotherapy Evidence Database (PEDro), Cochrane Reviews, and Cochrane DataBase of Effectiveness Trials. Searches were limited to studies published after 1990 and only those published in English or those with an English translation available. The studies’ references were also checked for relevant articles. Because of the broad nature of the searches, it was expected that articles would be identified that did not meet the criteria for content or study design. The first two authors reviewed the articles and eliminated those that did not meet the criteria. When disagreements arose, the third author was consulted, and consensus was reached.

The following search terms were used to identify literature related to JIA and osteoporosis: “juvenile rheumatoid arthritis and osteoporosis,” “juvenile rheumatoid arthritis and bone mineral density,” and “rheumatoid arthritis and osteoporosis.” “Juvenile idiopathic arthritis” and “juvenile chronic arthritis” were substituted for “juvenile rheumatoid arthritis” with no additional articles found. Sixty-six articles were identified and, after review, 28 articles were included for question 1.

Search terms used to find articles in electronic databases to address question 2 included “randomized controlled trial children weight bearing,” “randomized controlled trial children bone mineral density jumping,” and “randomized controlled trial children exercise bone mineral density.” Initially, 32 articles were identified; after removing duplicates and reviewing content, seven articles were selected for inclusion.

Search terms to address question 3 included “juvenile rheumatoid arthritis and exercise programs,” “juvenile rheumatoid arthritis and weight-bearing programs,” and “juvenile rheumatoid arthritis and physical therapy guidelines.” “Juvenile idiopathic arthritis” and “juvenile chronic arthritis” were substituted for “juvenile rheumatoid arthritis” with no additional articles found. Initially, 13 articles were identified, after removing duplicates and reviewing content, two articles were selected.

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Analysis of Articles

The articles selected for each of the aforementioned topics were read and analyzed by the authors for both content and level of evidence. All authors participated in content analysis, and the two lead authors performed ratings for level of evidence. Content analysis consisted of individual analysis and group discussion of the details of each study. Descriptive details of each study—study design, number of participants, intervention type and duration, outcome measures were identified as described by Dumholdt.27 These content areas are similar to those in outlined in the APTA’s Hooked on Evidence Database data extraction form. Results were recorded and collated into tables. Additional analysis included: identifying the important variables across the studies, making descriptive comparisons across the studies when possible and, finally, specifying problems that need further research.27

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Levels of Evidence

Levels of evidence were determined by using the Oxford Center for Evidence-based Medicine Levels of Evidence criteria (CEBM)28 as outlined in Table 1. Studies concerned with factors associated with low BMD and JIA were evaluated using the symptom prevalence criteria of the CEBM and studies concerned with exercise and BMD or JIA were evaluated using the therapy/prevention criteria of the CEBM. All intervention studies were also rated according to the PEDro Scale for RCTs, non-RCTs, and Case Series.29,30 The two lead authors worked together to achieve consensus on both the CEBM rating scale and the PEDro Scale.

Table 1
Table 1
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Sample Size

The CEBM rating scale was modified slightly to indicate those studies with either notably large or small samples. All studies with a sample size larger than 100 were denoted with a “>,” and all studies with a sample size less than 20 were denoted with a “<.”

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BMD Measurement

The manner in which BMD was measured also was evaluated. Dual-energy x-ray absorptiometry (DEXA) is considered the most accurate method to measure BMD and provides minimal exposure to radiation.31 All studies that did not measure BMD at the hip and spine with DEXA were denoted with a “−.” Additional forms of measurements of BMD include the following technologies: peripheral DEXA, single-energy x-ray absorptiometry, dual photon absorptiometry, quantitative ultrasound, quantitative computed tomography, and peripheral quantitative computed tomography.31

Low accuracy in measuring BMD in children has been cited as a problem. DEXA allows the researcher to calculate two measures, the bone mineral content (BMC) and BMD. BMD is measured by first determining BMC, which is the total amount of minerals in the selected bone in grams.32 BMD then is calculated using the measured amount of minerals in the bones in grams (or BMC) divided by the area of the bone (g/cm2). Actually, this is a measurement of areal BMD.32 Small bone size can result in erroneous classification of low BMD, and skeletal growth can confound measuring changes in BMD as bones change in both area and volume.32–34 Attempts have been made to calculate a volumetric BMD, which is bone density divided by the approximated volume of the bone area measured.32 This measure may provide a more accurate representation of bone density in children.35 Hence, measurements of bone density can be reported as BMC, BMD volume, or areal BMD. Variation among the studies existed in the quantification of bone density, and this was noted.

Another important consideration is the body site for which the bone density is calculated; the total body, femoral neck, lumbar spine, and tibial shaft are sites that are reported most frequently. Individuals with JIA may have small stature, which may confound interpreting values for total body BMC. In addition, individuals with JIA may have prosthetic joints, necessitating the use specific body sites, eg, lumbar spine, for the calculation of BMD.

Other concerns with measuring BMD in children are underestimation of bone density as the result of small bone size in relation to the scanning area and the lack of normative data for BMD or BMC for children.34 Modifications can be made to DEXA scanning procedures to decrease the pixel sizes to accommodate small bones; the use of controls matched for age and gender assist with interpreting BMC, areal BMD, or volumetric BMD values.33

To allow for comparison across studies of jumping programs to increase BMD, effect sizes were determined. BMC changes at the femoral neck and lumbar spine were the most commonly reported outcome variables; hence, effect sizes were calculated with these values. The differences between the mean change scores of the control and intervention groups divided by an average of their standard deviations yielded effect size of each study.36

All authors worked together to synthesize the articles. The first author performed a written summary of the synthesis. The second two authors performed a validity check on the final summation and synthesis. Narrative validity analysis of the studies, along with identification of common findings across the studies are presented in the text.27

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Factors Associated with Low BMD and Children with JIA

Twenty-eight studies37–65 used either cohort, case control, or cross-sectional research study designs to evaluate factors associated with decreased bone mineral density in children (Table 2). The two highest-ranked prospective cohort studies37,38 identified disease subtype (children with polyarticular arthritis are at greater risk than those with oligioarthritis), growth retardation, use of steroid treatments, weight-bearing activities, and changes in the biochemical process of bone formation as risk factors for low BMD in children with JIA. The three highest-ranked retrospective cohort studies43–45 and one highly rated ecological study61 identified disease duration and severity, subtype of JIA (children with polyarticular arthritis are at greater risk), use of steroids, growth retardation, physical activity, and calcium intake are associated with low BMD in children with JIA. Other highly rated studies,49,50,52,53 but with sample sizes less than 100, identified low vitamin D and calcium intake and receptor polymorphisms of vitamin D and calcium as contributing factors. Tobacco use during adolescence was identified in only one study of adults with a history of JIA,46 which may be because other studies focused on children and adolescents, and tobacco use may not have been identified as a potential risk factor. In isolation or as part of a multivariate solution, all factors except tobacco use were confirmed by multiple studies of varying size and experimental rigor.

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Weight-Bearing Programs that Produce an Increase in BMD in Healthy Children

A summary of the seven randomized controlled trials33,66–71 of weight-bearing activities for children can be found in Table 3. Important variables identified from these studies include frequency and duration of the activity, ground reaction force (GRF) created during the activity, and age at the time of activity. Bone changes resulting from high-impact activity may be promoted by high levels of growth hormones. Growth hormone levels increase abruptly during prepubescent years. All intervention studies occurred with prepubescent children, and one showed greater bone accrual in prepubescent girls as compared with pubescent girls.69 Only two studies directly measured the GRF produced by each participant at both the beginning and the end of the intervention period.33,66 Other studies either estimated the GRF based on published exercise protocols or by testing a small sample of participants. The greatest effect size on BMC was found in the study by Fuchs et al.33 The intervention in this study had the greatest GRF (eight times body weight), and occurred for more than six months. Fuchs et al72 demonstrated the gains in hip bone mass achieved by study participants were maintained for up to 14 months after the jumping program ceased. The study with the highest PEDro Scale score included randomization of monozygotic twins and an intervention that produced a force of approximately three and one half to five times body weight with a small treatment effect after nine months.68

Table 3
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Exercise Programs for Children with JIA

A summary of the two articles selected for review can be found in Table 4, which included a prospective cohort study and a RCT.21,73 Although Takken et al21 did not find any significant differences between the control group and the intervention group that received aquatic therapy, no increases were observed in disease signs and symptoms of children exercising in the pool, which supports the safety of aquatic therapy, but not its efficacy in improving physical fitness, weight-bearing exercise, activity, or participation. Klepper73 documents the improved health of children with polyarticular JIA who participated in a low-impact exercise program for 60 minutes three times a week (including stepping on and off a four-inch box) for eight weeks. This supports the safety of low-impact weight-bearing activities of short duration for children with polyarticular JIA with similar levels of severity.

Table 4
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Summary and Implications for Researchers and Clinicians

Currently, we found no evidence that directly supports a safe, effective weight-bearing program for children with JIA to reduce the risk of low BMD. This review was limited by the lack of literature directly related to the issue of reducing the risk of low BMD in children with JIA via a weight-bearing program, literature that used three different classification systems of JIA, and heterogeneity among studies in quantifying bone density. Yet, foundational information does exist, and can guide clinicians and researchers who work with children with JIA. For children with JIA who are at greater risk for low BMD, prescribing an exercise regime to increase physical activity and weight bearing activities is indicated.

Nonetheless, more information is needed about the influence of exercise on bone mass in children with JIA. The primary question that needs to be addressed by researchers is: what intensity and duration of physical activity and weight-bearing forces are necessary to reduce the risk for low BMD in children with JIA? An immediate concern of clinicians is the compression forces generated by weight bearing and the potential for increasing joint pain and swelling. The goal is to prescribe an exercise program that provides enough GRF to improve BMD, but that does not aggravate the joints of children with JIA. Klepper73 demonstrated that children with polyarticular JIA can participate in a low impact exercise program three times a week for eight weeks without injury or disease exacerbation. One question to be addressed by clinicians and researchers is whether this program provides enough GRF to address the risk for low BMD in children with JIA.

High impact exercise (eg, jumping off a 61-cm box) provided the largest treatment effect and the bone accrued was sustained over time.33,72 Studies that used weight-bearing sports or lower impact jumping, such as step aerobics, tuck jumps, hopping, skipping, still had a impact on bone accrual, but showed a smaller effect size.69–71 Participation in high-impact exercise does not seem feasible for children with JIA. However, participation in weight-bearing activities, such as jumping rope, skipping, step aerobics, and tuck jumps, does seem reasonable. Another avenue of investigation would be a replication of the interventions by Bradney et al,70 Heinonen et al,69 or McKay et al71 with children with JIA. Replication of interventions shown to have a small effect size would necessitate a large sample size for statistical power. Obtaining a large sample of prepubescent children with JIA may be difficult.

Turner and Robling74 suggest that because maximal bone accrual occurs when there are repeated sessions of mechanical loading followed by rest; there is a relationship of potential bone accrual (or osteogenic potential), intensity, and frequency of bone loading. They propose the osteogenic potential of an activity is given by the intensity* ln [frequency + 1].74 Theoretically, the intensity of an activity can be decreased and frequency increased to obtain the same osteogenic potential because a less-intense weight-bearing activity with a high osteogenic potential may be most appropriate for children with JIA. Another potential avenue of investigation is to evaluate the proposition of Turner and Robling.74 The osteogenic potential of the intervention used by Fuchs et al33 could be calculated and replicated with a less intense (less than eight times body weight), but more frequent (more than three times a week) program, to evaluate if the same treatment effect is produced.

Although the assumption is widely held that high-intensity weight-bearing forces are contraindicated for children with JIA, the success of the low-impact exercise program designed by Klepper73 provides evidence that low-intensity long-duration forces are tolerable. Likewise, Westby et al75 performed a randomized controlled trial with adult women with rheumatoid arthritis and a weight-bearing program to maintain BMD, and all women were able to tolerate the program and maintained BMD. On the other hand, Ward et al76 describe a randomized controlled pilot study of the impact of six months of standing for 10 minutes on an active or placebo vibrating plate on the tibial BMD of children with disabilities. There was a mean increase in tibial bone density in children who stood on the active plates and a decrease in those who stood on the placebo plates.

A low-intensity, daily jumping program could provide a simple, low technology, cost effective measure to minimize the risk of low BMD in prepubescent children with JIA. Pilot or preliminary studies need to be done to establish a safe, effective program. As a result of the multifactorial nature of BMD, any intervention study would require careful planning and coordination between multiple team members: rheumatologist, bone physiologist, dietician, exercise physiologist, and physical therapist. Because of the impact of medication on bone physiology, it would be ideal if medication during the intervention time was stabilized. This may be possible for only short durations, e.g., six months. Although BMD would be the outcome variable, standardized validated measurement of other intervening variables such as daily physical activity, physical fitness, daily intake of calcium and vitamin D, disease severity and duration, body size, bone resorption, and medication intake would need to occur. Ongoing consultation with a rheumatologist would be necessary to insure that the children are not in a constant active disease state and to ensure ongoing disease management. Random assignment of study participants would need to occur in blocks by disease subtype, e.g., oligioarthritis or polyarthritis. Intervention and control groups should have similar characteristics in age and gender. Finally, the relationship of sample size and attrition as it relates to the intervention effect size would need to be carefully considered as the population of children with JIA is relatively small in most geographic regions.

Using exercise to address the risk of low BMD in children with JIA is within the scope of practice for pediatric physical therapists. Clinicians should be aware of the factors that place children with JIA at increased risk for low BMD. Low-impact exercise has been shown to be safe with children with JIA73 and should be incorporated into a daily exercise regime. In the conjunction with proper medical management of disease activity, designing exercise programs that promote weight bearing in prepubescent years may be a way to reduce the risk of low BMD in children with JIA.

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APPENDIX
Seven Subtypes of Juvenile Idiopathic Arthritis as Classified by the International League of Associations for Rheumatology77
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Systemic Arthritis.

Arthritis in one or more joints preceded by fever of at least of two weeks’ duration, and daily for three days, and accompanied by one or more of the following: a rash, enlarged lymph nodes, hepato- or spleno-megaly, and/or serositis.

Exclusions: a, b, c, d.

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Oligioarthritis.

Arthritis affecting one to four joints during the first six months of the disease. Two subtypes are recognized: extended and persistent.

Exclusions: a, b, c, d, e.

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Polyarthritis (Rheumatoid Factor Negative).

Arthritis affecting five or more joints during the first six months, with a negative rheumatoid factor test.

Exclusions: a, b, c, e.

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Polyarthritis (Rheumatoid Factor Positive).

Arthritis affecting five more joints during the first six months, with two or more tests in the first six months positive for rheumatoid factor.

Exclusions: a, b, c, e.

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Psoriatic Arthritis.

Arthritis and psoriasis and at least two of the following: dactylitis, nail pitting or detached/loose nails, or psoriasis in a first-degree relative.

Exclusions: b, c, d, e.

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Enthesitis-Related Arthritis.

Arthritis and enthesitis, or arthritis or enthesitis with two or more or the following: sacroiliac or lumbosacral pain/inflammation, presence of human leukocyte antigen (HLA-B27), onset in arthritis in a male over six years of age, acute anterior uveitis, and history of inflammatory bowel disease, Reiter’s disease, or conditions listed above in a first degree relative.

Exclusions: a, d, e.

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Undifferentiated Arthritis.

Arthritis that does not meet the criteria for the aforementioned categories or meets criteria for two or more categories.

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Exclusions.

The categories are mutually exclusive. The list of possible exclusions is as follows:

a. Psoriasis or a history of psoriasis in the patient or first degree relative.

b. Arthritis in an HLA-B27 positive male beginning after the sixth birthday.

c. Ankylosing spondylitis, enthesitis related arthritis, sacroilitis with inflammatory bowel disease, Reiter’s syndrome, or acute anterior uveitis, or a history of one of these disorders in a first degree relative.

d. The presence of IgM rheumatoid factor on at least two occasions at least three months apart.

e. The presence of systemic JIA in the patient.

Cited Here...

* Three classification systems exist for chronic childhood arthritis issued by the following authorities: the American College of Rheumatology,15 the European League Against Rheumatism,16 and the International League of Associations for Rheumatology (ILAR).13 In this work, the ILAR classification scheme is used when discussing the subtypes of JIA because it is more specific and detailed than the other two classification systems. Cited Here...

Keywords:

adolescent; bone mineral density; child; exercise; juvenile idiopathic arthritis; physical therapy; review literature; weight bearing

© 2007 Lippincott Williams & Wilkins, Inc.

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