Bone health in children and adolescents is of great importance in preventing fractures later in life.1 The prevalence of vertebral and hip fractures is increasing in the elderly in Western countries.2 Many chronic diseases, such as juvenile idiopathic arthritis (JIA), and different treatments of diseases affect the development of optimal peak bone mass, which is achieved during late adolescence and early adult life.3–8 Exercise during growth appears to enhance the building of a strong skeleton owing to a high peak bone mass and large bone size.5,6,9–11
Many researchers have shown that children with rheumatic diseases have decreased bone mineral density (BMD), potentially reduced peak bone mass, and an increased fracture risk, both as children and as adults.7–10 Reduced BMD is associated with disease severity, corticosteroid use, and inactivity in children and adolescents with JIA.7–10 The pubertal stage and disease activity also significantly influence early changes in BMD.6–9,11 Growth retardation and osteoporosis are primarily consequences of oral treatment with corticosteroids.9,11,12 Murray and Lovell11 showed that the outcome for children and adolescents with JIA has improved during the last 10 to 15 years. In their study, the medical efficacy of anti-tumor necrosis factor (TNF) therapy was shown to be high for polyarticular JIA and that long-term methotrexate therapy did not negatively influence bone composition.
Physical activity and physical exercise improve muscle strength and bone density in children with JIA.10,12,13 Jumping has been found to improve hip and lumbar spine bone mass in prepubertal children.12–16 Lien et al6 showed that weight-bearing activities for boys are independent predictors of changes in total bone mineral content (BMC). Several recently published studies demonstrate the effect of physical activity, disease activity, corticosteroids, especially before puberty, nutrition, sun exposure, vitamin D, growth, and smoking on the quality of BMD in children with JIA.5,7,10,12,13 Current knowledge on bone health in children with JIA has established that a sedentary lifestyle contributes to secondary impairments in bone health, muscular fitness, and functional limitations, despite advances in pharmacologic treatment of inflammatory diseases.13 In a review study from 2007, 8 randomized intervention studies showed beneficial effects from weight-bearing exercise for 8 to 16 weeks, 2 and 3 times a week. In most studies the children had been jumping with a rope.12 Burnham et al17 pointed out, in a study from 2009, the importance of longitudinal studies over 12 months, to see changes in BMD and BMC. They also referred to the connection between muscle strength and weight-bearing physical activity and the influence on bone health.
The World Health Organization defines bone health in adults as normal if BMD measured by dual-energy x-ray absorptiometry (DXA) is less than −1 SD, osteopenic between 1 and 2.5 SDs, and osteoporotic if more than 2.5 SD.3,4,14 In children, the diagnosis of osteoporosis should not be made on the basis of densitometric criteria alone. According to the International Society for Clinical Densitometry, the diagnosis of osteoporosis in children and adolescents (males and females aged 5–19 years) requires the presence of both a clinically significant fracture history and low BMD or BMC defined as a Z score of −2.0 or less adjusted for age, gender, and body size. The term osteopenia should not be used in children and adolescents. The definition of osteoporosis in children has been proposed by the International Society for Clinical Densitometry.15
The aim was to study BMD in a cohort of children and adolescents with JIA before and after a physical exercise program.
The Regional Ethics Committee approved the study. Written consent was obtained from the participants and from their parents.
The subjects were recruited in 2004–2007, in a randomized experimental study. Fifty-four children and adolescents with JIA, aged 9 to 21 years (median = 13.9; range = 8.8–21.6), 40 (74%) girls and 14 (26%) boys, consented to participate in the study.
The children and the adolescents were diagnosed according to the revised criteria of the International League of the Associations for Rheumatology.16 Included were children with polyarticular onset form or severe oligoarticular onset form, being treated with methotrexate, TNF blockers, and/or prednisone (12–58 mg), and requiring repeated corticosteroid injections in the foot, knee, or hip (see Table 1).
Letters were sent out to 90 children with JIA, with the polyarthritis onset form or the oligoarthritis onset form, and who were medically treated with methotrexate. Answers from 64 families were received. Randomization was performed by lot and was completed when 54 participants accepted the random assignment. At the first test occasion, all 54 completed the tests.
The participants were randomized into a physical exercise group (n = 33) or a control group (n = 21). An exercise program with pictures, instructions, and a 12-week diary were given to the exercise group at the first test occasion, along with performance instructions. The program consisted of 100 two-footed jumps with a rope, muscle strength core exercises and muscle strength exercises with a load (0.5–2 kg) for the arms and shoulders, and 10 × 3 repetitions 3 times a week for 12 weeks. The number of repetitions performed was documented. Physical exercise in leisure time outside the program was documented in both groups in two 12-week activity diaries. The physical exercise was quantified as 1 point for each activity occasion that was planned and lasted for at least 20 minutes.
The different types of exercises in the self-reported activity diaries were categorized into 3 groups according to the level of weight-bearing exercise; (1) jogging and ball sports, (2) walking, gymnastics and horse riding, and (3) cycling and swimming (see Table 3). Physical exercise was defined as:
“A subset of physical activity that is planned, structured, repetitive and purposeful in the sense that improvement or maintenance of physical fitness is the objective.”
Physical activity was defined as:
“Any bodily movement produced by skeletal muscles that result in energy expenditure.”18
The 54 participants were evaluated 3 times: at the start, after 3 months, and after 6 months. Bone measurements, with BMD and BMC, were assessed with DXA for the total body, lumbar spine L1 through L4, arms, and legs. Dual-energy x-ray absorptiometry was performed using a Lunar Prodigy device (fan beam), pediatric mode, with software version 10 (GE Lunar, Madison, Wisconsin). Age- and gender-specific Z score were calculated.19 Bone mineral density of the calcaneus was also measured with DXA Laser Calscan (DXL),19 which is a combination of DXA and laser and measures the width of the heel. The length of the left foot was measured with a foot ruler to the nearest 0.1 cm. For the heel measures, the apparent BMD (mg/cm3) was calculated by dividing the BMD by the calcaneal height.20
Standing height without shoes was measured to the nearest 0.1 cm, using a wall-mounted ruler (stat meter). Weight to the nearest 0.1 kg was measured using an analogue weight scale. Dual-energy x-ray absorptiometry was performed by the same investigator for all the participants. The calculation of BMD and BMC Z score in the foot was analyzed by the same investigator. Pubertal stage was not evaluated.
Information on the onset of JIA, disease duration, and medical treatment was obtained from medical records. Bone mineral density values were compared with a healthy age- and gender-matched reference group.20
The analyses were completed according to “intention to treat.”
The Fisher permutation test was used for differences between groups. The Fisher test for pair comparison was used for comparisons of differences within groups and for the whole group. Correlations were evaluated with the Pitman test.21–23 Two-tailed P values were used. SPSS (version 15.0) was used to analyze correlation and regression analysis. Alpha levels of .05 or less were regarded as evidence of statistically significant findings. Correlation and regression analyses were conducted in children with the polyarticular onset form in terms of disease duration, corticosteroid use, and age in BMD for total body, lumber spine L1 through L4, legs, and heels. Multiple regression analysis, analysis of covariance, was used for presenting seasonal effects on physical activity level at the second and third test occasions.
Forty-eight children participated fully in the exercise study: 28 children in the exercise program and 20 children in the control group. After the first assessments at baseline (n = 54), there were 6 dropouts. The dropouts, 5 from the exercise group and 1 from the control group, were more heavily medicated and/or had long disease duration.
Anthropometric data, JIA disease onset, type and duration, and medical treatment at baseline for the exercise group, the control group, and for the dropouts are listed in Table 1.
Total BMD, total BMC, Z score of the total body, and Z score for the lumbar spine L1 through L4, BMD, BMC, and the area for the legs, and BMD and BMC for the left heel at baseline for the whole group are shown in Table 2. The assessment with the DXL was performed for 49 children on the first test occasion, 20 children in the control group, and 29 children in the experimental group. There were 20 invalid measurements from a total of 151 test occasions due to failure of the software (see Table 2).
At the start of the study, BMD and BMC measurements did not show any significant difference in this group of children and adolescents with JIA compared with reference values.19 Bone mineral density values in total body, but not Z score increased significantly (P = .012) in the exercise group compared with the control group (P = .061) after 3 months (Table 3).
Z scores for the exercise group and for the control group at the start, at 3 months, and at 6 months are shown in Figure 1. Nineteen children treated with oral corticosteroids, 1.25 to 3.75 mL/mg across 3 to 24 weeks, had normal Z score values at baseline.
The amount of physical exercise in leisure time increased between the second and third test occasions for the exercise group, the control group, and the whole group in all categories (Figure 2). There was increased activity in all 3 different physical exercise categories.
Seasonal effects on physical activity level and the effect on BMD values at the second and third test occasions are shown in Table 4 and Figure 3. No correlation for seasonal effects between groups was found.
The exercise program was well accepted by the children and adolescents, and compliance with the program was 70% of the expected value. Twenty-eight of 33 participants in the exercise group completed the exercise program in full (Figure 4).
Regression analysis with the Z score as the dependent variable and disease duration, age, and polyarticular onset as independent variables was calculated, but no statistically significant correlation was found. No change was found in BMC values for the participants in the study.
Multiple regression analysis, with the Z score as the dependent variable, analysis of covariance, was used for analyzing seasonal effects on physical activity level and the their effect on BMD values at the second and third test occasions. No correlation for seasonal effects between groups was found.
Bone mineral density in this cohort of children and adolescents with JIA was normal compared with a healthy age- and gender-matched reference group.18 This finding differs from several other studies.5–10 Our results, however, show that a well-designed exercise program limited to a short period of time can improve BMD. This is notable, as bone remodeling and bone formation are long processes; a complete cycle takes about 3 to 6 months.6–9 Ganotti et al12 and Klepper13 reported that in children, aged 8 to 15 years with polyarticular disease onset, BMD increased 8 to 12 months after a weight-bearing exercise program No calculation of the Z score was reported in those studies. Burnham et al17 also point out the importance of longitudinal studies over 12 months to see changes in BMD and BMC. In this study, the children performed both jumping and muscle strength training and there was a significant effect on bone health. The effect of muscle strength will be presented in another paper. We also included physical activity in leisure time.
In our study, BMD increased significantly in the exercise group after 3 months. Follow-up after 1 year would have been preferable to give a more valid outcome, as change in DXA values takes time.5,7–9
The children and adolescents in our study were optimally medicated, which could explain the normal BMD. Girls appeared to have lower Z scores than boys, but no statistical significance was found. Total body BMC and BMD values were lower in the polyarticular disease onset form than in the oligoarticular disease form.7–10,14,15 Our study did not confirm the results of other studies that showed decreased total BMD in patients with the polyarticular onset form, low weight, and early disease onset treated with corticosteroids orally or as injections.7–9,11 One reason could be that our patients had DXA measurements within the reference range and the group was heterogeneous and of different ages. Heterogeneity arises from the range of years of disease, the range in age, weight, and height for the group.
The values of P ≤ .05 were considered evidence of statistically significant findings. The clinically meaningful change in BMD and BMC was difficult to approximate, as there were no such studies published at the time of the start of our study. We had no knowledge of the status of bone health in the study group. We had knowledge about the lack of bone health in children with JIA in general and especially in those with the polyarthritis onset form.7
The correlation between BMD measurements performed with DXA for the total body, spine, and hip was examined to explore the diagnostic capacity of laser DXL of the calcaneus.20 Significant correlations were found at all sites in a study of 112 children with Duchenne or Becker muscular dystrophy, JIA, and chronic kidney diseases and in healthy boys.19 In our study, we did not observe any differences in calcaneus values between the groups using this newly validated method.
Not only did the children in our study complete the fairly heavy exercise program but they also changed their behavior and improved their physical activity in leisure time during the 12-week follow-up. It is time to reconsider the content of activity and exercise in this group. Children with optimal medical treatment and without disease activity should be given an opportunity to challenge their physical capacity. The International League of the Associations for Rheumatology recommends adequate medical treatment plus physical activity and physical exercise according to the international guidelines.16 It is always necessary to achieve a balance when deciding on how demanding an exercise program should be. We do not think our model was too demanding, as a similar design has been used in recent publications.10,12,13
The special exercise program was designed to challenge the children to reach an expected higher level of performance and achieve changes in BMD. It was based on knowledge of increased fracture risk, clinical knowledge of performance, disabilities, and the outcome of chronic JIA; and the physical exercise program correlated well with recently published studies. In our study, there was a higher level of weight-bearing exercise and muscle strengthening in the program.5,11,13,18
Enhancing physical exercise, support, and encouragement during growth are of great importance for improvement in a childhood chronic conditions.1,2,6,7,10,13,23–26
The children and adolescents with JIA in this cohort had normal BMD compared with a healthy age- and gender-matched reference group. The children completed a fairly heavy exercise program with a high level of weight-bearing exercise consisting of both jumping and muscle strength training, and they also changed their behavior and improved their physical activity in leisure time during the 12-week follow-up. Our results demonstrate that 12 weeks of exercise increases BMD in children with JIA.
The authors thank all participating children and their parents who made this study possible. They also thank Diana Swolin-Eide for her expert assistance and analyzing the results of the DXL, Helena Johansson and Eva Andersson for statistical support, and Anne Dohsé for the expert assistance.
1. Karlsson MK, Nordqvist A, Karlsson O. Physical activity, muscle function, falls and fractures. Food Nutr Res. 2008;52. doi:10.3402/fnr.V52i0.1920.
2. Karlsson MK, Nordkvist A, Karlsson O. Physical activity increases bone mass during growth. Food Nutr Res. 2008;52. doi:10.3402/fnr.v52i0.1871.
3. World Health Organization. Assessment of Fracture Risk and Its Application to Screening for Postmenopausal Osteoporosis technical report series]. Geneva, Switzerland: World Health Organization; 1994.
4. Moorthy LN, Peterson MGE, Harrison MJ, Onel KB, Lehman TJA. Physical function assessment tools in pediatric rheumatology. Pediatr Rheumatol Online J. 2008;6:9.
5. Boot AM, de Ridder MA, Pols HA, Krenning EP, de Muinck Keizer-Schrama SM. Bone mineral density in children and adolescents: relation to puberty, calcium intake and physical activity. J Clin Endocrinol Metab. 1997;82(1):57–62.
6. Lien G, Selvaag A M, Flatö B, et al. A two-year prospective controlled study of bone mass and bone turnover in children with early juvenile idiopathic arthritis
7. Kelly A, Rouster-Stevens KA, Klein-Gitelman MS. Bone health in pediatric rheumatic disease. Curr Opin Pediatr. 2005;17:703–708.
8. Gough AK, et al. Generalised bone loss in patients with early rheumatoid arthritis
. Lancet 1994;3444:23–27.
9. Von Scheven E. Pediatric bone density
and fracture. Bone health in pediatric rheumatic disease. Curr Osteoporos Rep. 2007;5(3):128–134.
10. Stagi S, Masi L, Capannini S, et al. Cross-sectional and longitudinal evaluation of bone mass in children and young adults with juvenile idiopathic arthritis
: the role of bone mass determinants in a large cohort of patients. J Rheumatol. 2010;37(9):1935–1943.
11. Murray KJ, Lovell D J. Advanced therapy for juvenile arthritis
. Best Pract Res Clin Rheumatol. 2002;16(3):361–378.
12. Ganotti ME, Nahorniak M, Gorton GE, et al. Can exercise
influence low bone mineral density in children with juvenile rheumatoid arthritis
? Pediatr Phys Ther. 2007;2(19):128–139.
13. Klepper SE. Exercise
in pediatric rheumatic diseases. Curr Opin Rheumatol. 2008;20(5):619–624.
14. Rahlston SH. What determines peak bone mass and bone loss in rheumatoid arthritis
? Clin Rheumatol (Baillières). 1997;3(11):479–494.
15. Bianch ML, Bains S, Bishop NJ, et al. Official position of the International Society for Clinical Densitometry (ISCD) on DXA evaluation in children and adolescents. Pediatr Nephrol. 2010;25(1):37–47.
16. Berntson L et al; Nordic Study Group. Incidence of juvenile idiopathic arthritis
in the Nordic countries. A population based study with special reference to the validity of the ILAR and EULAR criteria. J Rheumatol. 2003;30(10):2275–2282.
17. Burnham JM, Shults J, Dubner SE, Sembhi H, Zemel BS, Leonard MB. Bone density
, structure, and strength in juvenile idiopathic arthritis
: importance of disease severity and muscle deficits. Arhritis Rheum. 2008;58(8):2518–2527.
18. Caspersen CJ, Powell KE, Christenson GM. Physical activity, exercise
, and physical fitness: definitions and distinctions for health-related research. Public Health Rep. 1985;100(2):126–131.
19. Karlberg J, Kwan CW, Albertsson-Wikland K. Reference values for change in body mass index from birth to 18 years of age. Acta Paediatr. 2003;92(6):648–652.
20. Söderpalm AC, Kullenberg R, Swolin-Eide D. The relationship between dual energy x-ray absorptiometry and DXA with laser (DXL) measurements in children. J Clin Densitom. 2008;(4):555–560.
21. Bradley JW. Statistical Tests 68–86. London, England: Prentice-Hall; 1968:215 and 256.
22. Good P. Permutation Tests: A Practical Giude to Resampling Methods for Testing Hypotheses, 2nd ed. New York: Springer-Verlag; 2000.
23. Mantel N. Chi-square tests one degree of freedom; extensions of the Mantel-Haenszel procedure. J Am Stat Assoc. 1963;58:690–700.
24. Hind K, Burrows M. Weight-bearing exercise
and bone mineral accrual in children and adolescents: a review of controlled trials. Bone. 2007;40(1):14–27.
25. Jürimäe T, Hurbo T, Jurimäe J. Relationship between legs and bone mineral density, anthropometry and jumping height in pre pubertal children. Coll Antropol. 2008;32(1):61–66.
26. Fuchs RK, Bauer JJ, Snow CM. Jumping improves hip and lumbar spine bone mass in prepubescent children: a randomised controlled trial. J Bone Miner Res. 2000;16:148–156.
27. Sardinha LB, Baptista F, Ekelund U. Objectively measured physical activity and bone strength in 9-year-old boys and girls. Pediatrics. 2008;3(122):728–736.
Keywords:© 2012 Lippincott Williams & Wilkins, Inc.
adolescent; arthritis; biological markers/analysis; bone density; child; child development; exercise; female; humans; male; juvenile rheumatoid/physiopathology; motor activity; physical therapy modalities; randomized control trial; strength training; weight-bearing