Juvenile Idiopathic Arthritis

Baydogan SN, Tarakci E, Kasapcopur O: Effect of strengthening versus balanceproprioceptive exercises on lower extremity function in patients with juvenile idiopathic arthritis: a randomized, single-blind clinical trial. Am J Phys Med Rehabil 2015;94:417Y428. Objective: The aim of this study was to investigate the effects of two exercise programs on lower extremity function in patients with juvenile idiopathic arthritis. Design: Thirty patients with juvenile idiopathic arthritis participated in this study. Pain, passive range of motion, muscle strength, balance, and functional abilities were assessed with the Numeric Rating Scale, goniometer, handheld dynamometer, Flamingo Balance Test, Functional Reach Test, 10-meter walking test, 10-stair climbing test, and Childhood Health Assessment Questionnaire. Participants were randomly assigned to the strengthening exercise group (group 1, n = 15) or the proprioceptive-balance exercise group (group 2, n = 15). Results: Intragroup analysis showed statistically significant improvements in all outcome measures except muscle strength in the hip and ankle after strengthening exercises in group 1. However, statistically significant improvements were found in all outcome measures after the proprioceptive-balance exercises in group 2. Intergroup analysis showed statistically significant improvement in all outcome measures in group 2 except for the Numeric Rating Scale, Childhood Health Assessment Questionnaire, and passive range of motion scores and hip extension and knee flexion muscle strengths. Conclusions: This study demonstrates that exercise treatment significantly improves musculoskeletal symptoms in patients with juvenile idiopathic arthritis. However, balance-proprioceptive exercises prove to be effective more than strengthening exercises for improving lower extremity function such as walking, climbing stairs, and balance in patients with juvenile idiopathic arthritis.

Juveni le idiopathic arthritis (JIA) encompasses a complex group of disorders with arthritis as a common feature. 1 Children with JIA are believed to have lower aerobic capacity, anaerobic capacity, and functional ability, which means that they have more difficulty performing daily activities than do healthy children. 2 JIA often results in muscle weakness, poor flexibility, atrophy, pain, and decreased proprioception of the affected joints. 3 Patients with JIA may have abnormal biomechanics, which could place them at increased risk of injury or future articular cartilage damage. Delayed neuromuscular development, muscular weakness, ligamentous laxity, and generalized or localized growth disturbances can all be factors that contribute to musculoskeletal changes. 4 Accordingly, a significant proportion of children with leg arthritis have impaired balance. 5 Medical treatment and rest were recommended in patients with arthritis in the past, but there is evidence today of the benefits of regular exercise for these patients. 6Y8 In the literature, some studies focused on neuromuscular training, aerobic exercises, aquatherapy, and land-based exercises for patients with JIA. According to the results of these studies, exercise interventions result in improved aerobic capacity, muscle strength, and disease activity with a possible beneficial effect on pain, function, and quality of life. 9,10 In addition to specialized neuromuscular training, balance-proprioceptive exercises or strengthening exercises may help to decrease the patient's risk for future injury or disease progression. Therefore, both balanceproprioceptive exercises and strengthening exercises may have an important role in the treatment of children with JIA and lower extremity arthritis.
This study's hypothesis was that proprioceptivebalance exercise increases muscle strength and range of motion (ROM) via promoting daily activities and that it improves lower extremity function in patients with JIA.
The best therapeutic exercise program for children with JIA remains unknown, and studies comparing exercise programs have not been found in the literature. Therefore, the aim of the present study was to investigate the effect of strengthening versus balance-proprioceptive exercises on lower extremity function in patients with JIA.

METHOD Study Design
This study was conducted in the Outpatient Department of Physical Therapy at the Faculty of Health Science, University of Istanbul, Istanbul, Turkey. Participant recruitment started in October 2010, and the final data collection procedure was performed in June 2011. Thirty-six participants were followed up regularly at the Department of Pediatric Rheumatology, Medical Faculty of Cerrahpasa, Istanbul University, Turkey. Thirty-six subjects were eligible to participate in the study, assessed at baseline, and randomly assigned to the strengthening exercise group (group 1) and proprioceptive-balance exercise group (group 2). Six participants were excluded because of an increase in disease activity and out of step with exercises; therefore, a total of 30 participants completed the treatment and attended the last assessment. The randomization was done by using the Microsoft Excel BRAND (USA)[ function. A participant flow diagram is presented in supplemental Figure 1 (http://links.lww.com/PHM/A95). Patients in group 1 (n = 15) and group 2 (n = 15) completed 12-wk exercise programs. All measurements were performed before and after 12 wks. The selector (OK) was aware of the randomization scheme but did not perform any assessments. The assessor (ET) was blind to the groups to which the participants had been allocated and conducted standard procedures in both groups. The physical therapist (SNB) was blind to the assessments but was aware of the nature of this intervention and the physical findings of JIA and treated the participants.

Participants
Thirty-six participants who were followed-up regularly at the Department of Pediatric Rheumatology and diagnosed with JIA in accordance with the International League of Associations for Rheumatology criteria were prospectively evaluated. Inclusion criteria included age range 6 to 18 years, diagnosis with JIA in accordance with International League of Associations for Rheumatology criteria, involvement with inflammation and/or movement restrictions in the knee, and ability to attend regular training. Exclusion criteria included the presence of a neurologic disease, decompensated organ failure, intra-articular steroid injection or surgery in any joint, active synovitis, active arthritis psychiatric disease, and inability to understand and follow the prescribed exercise. This study was approved by the Research Ethics Committee of Istanbul University and conducted in accordance with the Declaration of Helsinki. All participants signed informed consent forms. The

Disclosures:
Financial disclosure statements have been obtained, and no conflicts of interest have been reported by the authors or by any individuals in control of the content of this article.

Editor's Note:
Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal_s Web site (www.ajpmr.com). participants were volunteers who were examined and prescribed physiotherapy by the pediatric rheumatologist who participated in the present study. All participants provided written approval from their physician to participate in the study.

Intervention
All participants were treated by the same physiotherapist, who did not take part in the evaluations. Those assigned to the strengthening exercises group (group 1) completed an exercise program that included bicycle ergometer (not resistant for warming up), lower extremity muscle stretching, and strengthening exercises. Participants assigned to the proprioceptivebalance exercise group (group 2) received the same bicycle ergometer (not resistant for warming up) and lower extremity muscle stretching as in group 1 and additional proprioceptive-balance exercises. All participants completed 36 supervised sessions of their respective program in a 12-wk period.
During the supervised exercise sessions, the therapist began instructing the participants in the home exercise activities so that they would be independent in this program until the end of the supervised therapy period. The content of the home exercise program for groups 1 and 2 was the same with supervised sessions having some modifications for 12 wks. Calisthenic exercises for the lower extremities were practiced instead of the bicycle ergometer in the warm-up session of the exercise program. Participants in both groups performed self-stretching exercises. In group 2, exercises with the balance board and mini trampoline could not be used at home, but other balance exercises were performed repetitively. All exercises for both groups are represented in Table 1. Figures 1, 2, and 3 show some sample exercises.

Outcome Measurements
The participants were evaluated before and after treatment in terms of pain, passive ROM (PROM), muscle strength, balance, functional ability, walking, and stair-climbing performance by the same physiotherapist.
Pain was assessed by using the Numeric Rating Scale (NRS). 11 Participants were asked to verbally rate their level of perceived pain intensity on a numerical scale from 0 (no pain) to 10 (worst pain possible).  PROM of knee flexion and extension was assessed by using a universal goniometer. During the measurements, the Kendall-McCreary criteria were considered. Participants were placed in the prone position with their pelvis in a neutral position at rest and denied compensatory hip and body movements by firmly being secured to the examination table. The knee was passively flexed and extended in this position. The measurement was repeated thrice, and the mean values were recorded. 12 Muscular strength was estimated at maximal isometric force for the muscles of the lower extremities by using a portable handheld dynamometer (Lafayette, LA). Subjects were asked to exert maximum effort and then straighten (for the quadriceps) or curl (the hamstrings) their knees as forcefully as possible. The maximum force realized during a 3-to 5-sec effort was recorded in kilograms. 13 The test was performed thrice with a 30-sec interval between tests, and the mean value was recorded.
Static balance was measured by using the Functional Reach Test (FRT). In the literature, the good reliability and low interexaminer variability of the FRT have been demonstrated in a range of studies. The FRT score correlates with the anteroposterior excursion of the center of pressure. Furthermore, the FRT also shows good reproducibility over time, and it is sensitive to change. At the same time, an abnormally low FRT score is a good predictor of fall risk. 14 The individual is first asked to elevate his/her arm to shoulder height. The position of the metacarpal phalangeal joint is then marked, and the patient is asked to perform a maximum forward reach while maintaining an independent standing posture. The reach is measured from the initial metacarpal phalangeal joint position to the final metacarpal phalangeal joint position, and an individual's score is typically recorded in centimeters.
Postural balance control was evaluated by using the Flamingo Balance Test (FBT). 15 Subjects with their eyes open were instructed to stand on the affected leg on a 1-in-wide, 12-in-high, and 20-in-long bar, while the free leg was flexed at the knee joint and held at the ankle joint close to the buttocks. A 1-min stance was performed, and the number of falls was counted and used as a measure of postural balance.
The Turkish version of the Childhood Health Assessment Questionnaire (CHAQ)Va reliable and valid tool for measuring the functional, physical, and psychosocial assessment of children with JIAVwas used to assess functional ability. 16 In eight activities (dressing/grooming, arising, eating, walking, hygiene, reach, grip, and activities), a number of questions were answered and scored on a scale of 0 to 3, where 0 = able to do with no difficulty, 1 = able to do with some difficulty, 2 = able to do with much difficulty, and 3 = unable to do. The mean of the eight scores identified the CHAQ score (range, 0Y3).
The participants' 10-meter walking test times were evaluated. The test was performed thrice, and the mean value was recorded. The participants' 10-stair climbing test times were evaluated. The tests were performed thrice, and the mean values of all were recorded. 17

Sample Size
A total of 30 participants were needed to detect a statistically significant difference between groups 1 and 2 at the 10% level with a power of 90% within the trial. A 4% (change of 0.13 with a total score of 3) 420 Baydogan et al.  reduction in CHAQ was estimated by using data from a study by Dempster et al. 18 for JIA participants.

Statistical Analysis
The data were evaluated by using the Statistical Package for the Social Sciences (SPSS) 17.0 program for Windows and descriptive statistics analysis (frequency, mean, and standard deviation). A power analysis was performed to determine the sample size at the beginning of the study. Sample size was calculated by using the Raosoft System. Before the statistical analysis, all variables were determined to be nonnormally distributed (P G 0.05) by using the Shapiro-Wilks test, and the Mann-Whitney U test was used to determine the effect of exercise program. Intergroup comparison was made by using the Wilcoxon's signed-rank test. Bonferroni's correction was applied (P G 0.05/n; where n = number of comparisons) when multiple comparisons were made and P G 0.025 was considered statistically significant. Table 2 displays the patients' demographics. There were no statistically significant differences (P 9 0.05) in age, weight, height, body mass index, sex, unilateral/bilateral involvement, affected side, or JIA subtype between the two groups.

RESULTS
The mean age was 9.27 years (range, 6Y18 years; SD, 1.43 years) in group 1 and 10 years (range, 6Y17 years; SD, 3.66 years) in group 2. Intergroup analysis indicated no significant differences in almost all demographic and clinical variables. Comparison of the results of the first assessment NRS, PROM, muscle strength of the lower extremities, FRT, FBT, CHAQ scores of the upper and lower extremities, 10-meter walking test time, and 10-stair climbing test times revealed no statistically significant intergroup differences (P 9 0.05).
Intragroup and intergroup comparisons of the changes in outcome measures after treatment are shown in Table 3. The intragroup analysis showed statistically significant improvements (P G 0.001) in all outcome measures except for muscle strength in the hip and ankle after strengthening exercises in group 1. In contrast, statistically significant improvements (P G 0.001) were found in all outcome measures after the proprioceptive-balance exercises in group 2. The intergroup analysis showed statistically significant improvements in all outcome

DISCUSSION
This study is a randomized trial of neuromuscular exercise that compared the effects of two different exercise programs on lower extremity function in patients with JIA. The findings herein showed that exercise treatment provides significant improvements in pain, ROM, muscular strength, static balance, postural balance control, and functional ability in patients with JIA. The balance-proprioceptive exercise program was more effective for lower extremity function than strengthening exercise program in these patients.
Patients with JIA may experience significant disability owing to muscular weakness, joint pain, contracture, and reduced mobility. 19Y22 Therefore, treatment goals are pain relief, eliminating active disease, normalizing physical function, normal growth and development, and improving quality of life. Physiotherapy and occupational therapy are integral parts of the therapeutic concept in children and adolescents with JIA. Therapeutic goals of physiotherapy are relaxation and pain relief, preservation or rehabilitation of the physiologic range of joint movement, preventing contractures, stretching and activating muscles, increasing muscle force, and training physiologic movements. 23 The therapeutic effects of a physiotherapy program, including JIA exercise, have also been recently investigated.
There are few studies in the literature about exercise treatment in patients with JIA. Many of these studies focus on the issues of land-based exercise, aquatic therapy, fitness, and aerobic exercise in patients with JIA. 9,20Y29 At the same time, few studies include strength training or neuromuscular exercises in patients with JIA. 8,20,24,28 In this study, a statistically significant reduction in all pain scores was observed in both groups after treatment. However, this reduction did not differ between the two groups except for pain scores during exercise. Similar to this study, many studies have indicated that exercise decreases pain in patients with JIA. 27Y29 In a study by Epps et al., 27 patients were assigned randomly to a combined hydrotherapy and land-based exercise group or a land-based physiotherapy exerciseYonly group. They reported that pain scores decreased in both groups. In the other studies, Sing-Grewal et al. 8 and Klepper 26 indicated that pain scores decreased after aerobic exercise programs in patients with JIA.
Bacon et al. 28 indicated that ROM of the lower extremity increased in patients with JIA after an aquatic exercise program. Similarly, statistically significantly improved ROM at the knee joint in both groups was noted in this study. Although the intergroup differences were not statistically significant, this improvement in the proprioceptivebalance exercise group was higher than that in the strengthening exercises group. This suggests that this result has been related to treatment in both groups involved in the same type of stretching exercises. In addition, this improvement of ROM in both groups may lead to increased independent participation in functional and daily living activities involving the lower extremities in children.
Klepper, 26 after the combined exercise program in JIA, found improved muscle strength. Improvements in almost all muscle strengths of the lower extremities were achieved in both groups, but greater improvement was found in almost all areas of muscle strength in the proprioceptive-balance exercise group. A greater increase in knee extension in the proprioceptive-balance exercise group is the most important indication according to results of the muscle strength assessment after treatment. This finding suggests that balance-proprioceptive exercise by weight bearing may increase knee extension muscle strength as well as proprioceptive sense. These increases may encourage patients to become more active in daily life.
In this study, improved balance parameters were obtained in both groups, but more improvements were found in the proprioceptive-balance exercise group. Greater improvements in balance parameters in the proprioceptive-balance exercise group are very important. Therefore, proprioceptive-balance exercise should be included in the treatment of children with JIA. In the literature, only one case study indicated improved postural stability and balance after exercise treatment in patients with JIA. 24 There are very limited data on this subject.
Significant improvement was observed in the CHAQ scores as well as 10-meter walking test and 10-stair climbing test durations in both groups after treatment in the present study. Improvement of these outcomes may be associated with improved ROM, muscle strength, pain scores, and participation in activities of daily living. Similarly to the results of this study, some exercise studies in the literature indicated that functional abilities increased in patients with JIA. 8,20,23 In particular, Dempster et al. 18 showed that a minimal clinically important improvement is represented by a median change of j0, 13 in the CHAQ. In this study, significant improvement was found in both groups; however, no difference was found between groups. The CHAQ is not sensitive enough to determine the efficacy of rehabilitation because it assesses whether the children do an activity rather than how well they do it. Although the CHAQ can prove the efficacy of the rehabilitation, some other assessment scales should be used as well.
In the literature, no exercise studies have focused on lower extremity function and proprioception in patients with JIA. This study is the first to investigate the effects of balance-proprioceptive exercise in patients with JIA. The other strengths of this study are its careful experimental design, two randomized groups, and use of valid outcome measures. However, this study had some limitations. First, the 12-wk exercise program was difficult for the participants to perform because they were in school. Second, the proprioception test did not objectively assess the knee joint. Although there are isokinetic systems for the objective assessment of proprioception, their use in children is difficult. Finally, long-term results were not collected here.
In conclusion, similar outcomes should be possible with both exercise programs, although the proprioceptive-balance exercise program results were better because those exercises were performed in a more enjoyable mood and with higher motivation. Physiotherapists may consider suggesting well-designed proprioceptive-balance exercises for patients with JIA according to their preferences and convenience. Therefore, this study should be helpful to professionals in this field. However, further research is needed to establish the mechanisms underlying the effects of the proprioceptive-balance exercises on lower extremity function and objectively assess proprioception improvements. Thi s is an adult learning experience and there is no requirement for obtaining a certain score. The objective is to have each participant learn from the total experience of studying the article, taking the exam, and being able to immediately receive feedback with the correct answers. For complete information, please see BInstructions for Obtaining Continuing Medical Education Credit[ at the front of this issue. Every question must be completed on the exam answering sheet to be eligible for CME credit. Leaving any item unanswered will make void the participant's response. This CME activity must be completed and postmarked by December 31, 2016. The documentation received will be compiled throughout the calendar year, and once a year in January, participants will receive a certificate indicating CME credits earned for the prior year of work. This CME activity was planned and produced in accordance with the ACCME Essentials.  3. This educational activity must be completed and postmarked by December 31, 2016. AAP Members may complete and submit this CME Answering Sheet and the following Standardized CME Activity Evaluation page and Certification page online through the membersonly section of the AAP web page at www.physiatry.org.

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