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R E S E A R C H A R T I C L E
Bone Health in Children and
Adolescents With Juvenile
Idiopathic Arthritis and the
Influence of Short-term Physical
Exercise
Eva Sandstedt, PT, MSc; Anders Fasth, MD, PhD; Hans Fors, MD, PhD; Eva Beckung, PT, PhD
Department of Pediatrics, The Queen Silvia Children’s Hospital, Sahlgrenska University Hospital (Ms Sandstedt and Dr
Fors), G¨oteborg, Sweden; Department of Pediatrics, Institute of Clinical Sciences (Dr Fasth) and Department of
Neuroscience and Physiotherapy, Sahlgrenska Academy (Dr Beckung), University of Gothenburg, Gothenburg, Sweden;
Northern ¨Alvsborg Hospital (Dr Fors), Trollh¨attan, Sweden.
Purpose: To study bone mineral density (BMD) in 54 children and adolescents with juvenile idiopathic arthritis
before and after a short-term exercise program. Methods: Fifty-four children, 41 girls and 13 boys, median age
13.9 years, participated in a 12-week exercise program, with 33 children in an exercise group. The program
consisted of one hundred 2-footed jumps with a rope and standardized muscle strength exercise. Both
BMD and bone mineral content were assessed with dual-energy x-ray absorptiometry (DXA) and DXA Laser
Calscan for the heel at the start and after 3 and 6 months. Results: The study group had BMD measurements
within the reference range compared with normative data with Z score at start. Bone mineral density values
in total body, but not Z score, increased significantly (P = .012) in the exercise group. Conclusions: The
study group had BMD measurements within the reference range. Twelve weeks of exercise increases BMD
in children with juvenile idiopathic arthritis. (Pediatr Phys Ther 2012;24:155–162) Key words: 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
INTRODUCTION
Bone health in children and adolescents is of great im-
portance in preventing fractures later in life.1
The preva-
lence of vertebral and hip fractures is increasing in the
0898-5669/110/2402-0155
Pediatric Physical Therapy
Copyright C 2012 Wolters Kluwer Health | Lippincott Williams &
Wilkins and Section on Pediatrics of the American Physical Therapy
Association
Correspondence: Eva Sandstedt, PT, MSc, Department of Pediatrics,
The Queen Silvia Children’s Hospital, Sahlgrenska University, SE-416
85 G¨oteborg, Sweden (eva.sandstedt@vgregion.se).
Grant Support: This study was supported by the Petter Silfverski¨old
Foundation; the Norrbacka Eugenia Foundation; and the Research and
Development Foundation of G¨oteborg and Bohusl¨an.
The authors declare no conflict of interest.
DOI: 10.1097/PEP.0b013e31824cce6e
elderly in Western countries.2
Many chronic diseases, such
as juvenile idiopathic arthritis (JIA), and different treat-
ments 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 en-
hance 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 den-
sity (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 sever-
ity, corticosteroid use, and inactivity in children and
adolescents with JIA.7-10
The pubertal stage and dis-
ease 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
Copyright © 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy
Association. Unauthorized reproduction of this article is prohibited.
Pediatric Physical Therapy Effects of Exercise on Bone in JIA 155
outcome for children and adolescents with JIA has im-
proved during the last 10 to 15 years. In their study, the
medical efficacy of anti-tumor necrosis factor (TNF) ther-
apy was shown to be high for polyarticular JIA and that
long-term methotrexate therapy did not negatively influ-
ence bone composition.
Physical activity and physical exercise improve mus-
cle 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 pre-
dictors of changes in total bone mineral content (BMC).
Several recently published studies demonstrate the effect
of physical activity, disease activity, corticosteroids, espe-
cially 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 chil-
dren with JIA has established that a sedentary lifestyle con-
tributes to secondary impairments in bone health, muscu-
lar fitness, and functional limitations, despite advances in
pharmacologic treatment of inflammatory diseases.13
In a
review study from 2007, 8 randomized intervention stud-
ies 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 lon-
gitudinal 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 crite-
ria alone. According to the International Society for Clin-
ical Densitometry, the diagnosis of osteoporosis in chil-
dren and adolescents (males and females aged 5-19 years)
requires the presence of both a clinically significant frac-
ture 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
Purpose
The aim was to study BMD in a cohort of children and
adolescents with JIA before and after a physical exercise
program.
METHODS
Ethics
The Regional Ethics Committee approved the study.
Written consent was obtained from the participants and
from their parents.
Subjects
The subjects were recruited in 2004-2007, in a ran-
domized experimental study. Fifty-four children and ado-
lescents 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 ac-
cording to the revised criteria of the International League of
the Associations for Rheumatology.16
Included were chil-
dren with polyarticular onset form or severe oligoartic-
ular onset form, being treated with methotrexate, TNF
blockers, and/or prednisone (12-58 mg), and requiring re-
peated corticosteroid injections in the foot, knee, or hip
(see Table 1).
Procedures
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. An-
swers 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 ex-
ercise group (n = 33) or a control group (n = 21). An ex-
ercise program with pictures, instructions, and a 12-week
diary were given to the exercise group at the first test oc-
casion, 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, struc-
tured, repetitive and purposeful in the sense that im-
provement 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
Copyright © 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy
Association. Unauthorized reproduction of this article is prohibited.
156 Sandstedt et al Pediatric Physical Therapy
TABLE 1
Distribution of Gender, Age, Height, Weight, Body Mass Index, Disease Onset and Type, Medication, and Injections for the Whole Group, the
Experimental Group, the Control Group, and the Dropouts on the First Test Occasion
Survey Study
(n = 54)
Experimental Group
(n = 33)
Control Group
(n = 21)
Dropouts
(n = 6)
Girls, n (%) 41 (74%) 25 (76%) 17 (76%) 4 (67%)
Boys, n (%) 13 (26%) 8 (24%) 5 (24%) 2 (33%)
Age, y 13.9 (8.8-20.6) 13.3 (8.8-19.9) 14.9 (8.8-20.6) 15.2 (11.8-19.6)
Height, cm 157 (128.6-185.8) 153.4 (128.6-175.8) 163.8 (129-185.8) 167.6 (155-185.8)
Weight, kg 50.6 (22.3-82.9) 47.9 (22.3-78) 56 (35.8-82.9) 58.9 (48.8-75.5)
Body mass index 20.2 (12.8-28.9) 20.0 (12.8-28.9) 20.7 (14.4-27.7) 21.1 (16.2-20)
3.4 3.4 3.5 1.7
Disease onset, y 5.8 (1-16.5) 6.1 (1.2-16.5) 4.8 (1-13.4) 9.5 (3-12.1)
Polyarticular onset 31 20 9 2
Oligoarticular onset 17 7 8 2
Entesite/psoriasis arthritis 6 1 3 2
Methotrexate months (r) years 3789 (.1-181) 5.8 2497 (1.2-181) 6.3 1292 (.1-161) 5.1 1292 (.1-161) 5.1
Enbrel/remicade months (r)
years
326 (5-78) 2.3 (n = 12) 272 (5-7) 10.8 (n = 9) 36 (17-19) 3 (n = 2) 5 (5-48) 2.7 (n = 2)
Corticosteroids, mg/wk 5107.2 (n = 19) 12846 (n = 10) 26445 (n = 6) 11781 (n = 3)
Total number of steroid
injections
404 194 131 79
Number of steroid injections in
foot, knee, hip
261 113 98 50
Number of steroid injections in
finger, wrist, shoulder
143 81 33 29
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 ana-
logue 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
Statistical Analyses
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 regres-
sion 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.
RESULTS
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 du-
ration, 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
Copyright © 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy
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Pediatric Physical Therapy Effects of Exercise on Bone in JIA 157
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 corticos-
teroids, 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 in-
creased 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 chil-
dren and adolescents, and compliance with the program
TABLE 2
Distribution, Median, Standard Deviation, and Range for BMI, BMD,
BMC, and Z Score for Total Body, Z Score for L1 Through L4, BMD for
Legs and Area for Legs, and BMD and BMC for Left Heel at Baseline
n Median (SD) Range
BMI, kg/m2 54 19.9 (3.4) 12.8-28.9
BMD, total 54 0.969 (0.11) 0.79-1.25
BMC, total 54 1953.8 (631.3) 776-3463
Z score total 54 − 1.1 (0.83) −2.2 to 1.7
Z score, L1-L4 54 0.400 (1.21) −2.3 to 3.8
BMD, legs 54 0.994 (0.16) 0.72-1.4
Area, legs 54 647.98 (137.26) 352.00-904.00
BMD, heel, 49 0.372 (0.076) 0.201-0.533
BMC, heel 49 0.279 (0.098) 0.148-0.539
Abbreviations: BMC, bone mineral content; BMD, bone mineral den-
sity; BMI, body mass index.
TABLE 3
P Values for BMD, BMC, Z Score, and Fat for Total Body, Z Score for L1
Through L4, BMD, BMC, Area in Legs, and BMD and BMC for Left Heel
at Baseline and After 12 Weeks’ Exercise and After Another 12 Weeks’
Follow-upa
Exercise-
Control 2-1
Exercise-
Control 3-1
BMD, total .012 .061
BMC, total weight NS NS
Z score total .15 .13
Fat total, %/kg .17 NS
Z score, L1-L4 NS NS
BMD, legs NS .74
BMC, legs NS NS
Area, legs NS NS
BMD, heel, NS NS
BMC, heel NS NS
Abbreviations: BMC, bone mineral content; BMD, bone mineral den-
sity; NS, nonsignificant.
aChanges between test occasions 2-1 and 3-1 with the Fisher permu-
tation test within groups.
was 70% of the expected value. Twenty-eight of 33 partici-
pants 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.
DISCUSSION
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 longitu-
dinal 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 ex-
ercise 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 op-
timally medicated, which could explain the normal BMD.
Girls appeared to have lower Z scores than boys, but no sta-
tistical 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 de-
creased total BMD in patients with the polyarticular onset
form, low weight, and early disease onset treated with cor-
ticosteroids 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
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158 Sandstedt et al Pediatric Physical Therapy
Fig. 1. Distribution of Z scores for the control and the exercise group at baseline, after 3 months, and at 6 months. Z scores for children
are described with respect to standard deviations between +2 and −2.5.
Fig. 2. Physical exercise in leisure time at the second and third test occasions, from baseline to 12 weeks and from 12 to 24 weeks, divided
into categories according to the level of weight-bearing activity: category 1—jogging, football, ball sports; category 2—walking, horse
riding; category 3—swimming, cycling; category 4—physical activity (pt) at school. Abbreviations: Con, control group; Exp, experimental
group; Tot, total.
TABLE 4
Seasonal Effects of Exercise: Regression Analysis With Analysis of Covariance-Dependent Variable BMD1.
Unstandardized
Coefficients
Standardized
Coefficients
95.0% Confidence Interval
for B
Model B SE β t P
Lower
Bound
Upper
Bound
1. (Constant) − 0.015 0.015 .995 − 1.007 .319 − 0.046 0.015
BMD2 1.006 0.015 67.308 .000 0.976 1.036
2. (Constant) − 0.014 0.015 − 0.984 .330 − 0.044 0.015
BMD2 0.981 0.018 .970 53.488 .000 0.944 1.018
BMD3 0.024 0.011 .040 2.187 .034 0.002 0.047
3. (Constant) − 0.009 0.015 − 0.588 .560 − 0.039 0.022
BMD2 0.979 0.018 .969 53.830 .000 0.943 1.016
BMD3 0.024 0.011 .040 2.207 .032 0.002 0.047
Season − 0.002 0.001 − .019 − 1.380 .174 − 0.005 0.001
4. (Constant) − 0.008 0.014 − 0.537 .594 − 0.037 0.021
BMD2 0.971 0.018 .960 54.728 .000 0.935 1.006
BMD3 0.021 0.011 .035 2.017 .050 0.000 0.043
Season − 0.002 0.001 − .019 − 1.437 .158 − 0.005 0.001
Group 0.008 0.003 .034 2.350 .023 0.001 0.014
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 per-
formed 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.
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Pediatric Physical Therapy Effects of Exercise on Bone in JIA 159
Fig. 3. Physical exercise in leisure time, presenting seasonal effects on physical activity level.
Fig. 4. Distribution of numbers of repetitions of the expected
and performed exercise programs for the exercise group. Abbre-
viations: Hip ext, hip extension; Shouldabd, shoulder abduction;
Shouldflex, shoulder flexion.
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. Chil-
dren with optimal medical treatment and without disease
activity should be given an opportunity to challenge their
physical capacity. The International League of the Asso-
ciations for Rheumatology recommends adequate medi-
cal 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 de-
manding 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 chal-
lenge 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 re-
cently 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 encourage-
ment during growth are of great importance for improve-
ment in a childhood chronic conditions.1,2,6,7,10,13,23–26
CONCLUSIONS
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 im-
proved 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.
ACKNOWLEDGMENTS
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 analyz-
ing the results of the DXL, Helena Johansson and Eva
Andersson for statistical support, and Anne Dohs´e for the
expert assistance.
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pathic 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, ex-
ercise, 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
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20. S¨oderpalm AC, Kullenberg R, Swolin-Eide D. The relationship be-
tween 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
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2008;3(122):728-736.
Copyright © 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy
Association. Unauthorized reproduction of this article is prohibited.
Pediatric Physical Therapy Effects of Exercise on Bone in JIA 161
C L I N I C A L B O T T O M L I N E
Commentary on “Bone Health in Children and Adolescents With Juvenile Idiopathic Arthritis and the
Influence of Short-term Physical Exercise”
How should I apply this information?
Children with juvenile idiopathic arthritis (JIA) who have polyarticular arthritis, growth retardation, reduced
weight-bearing activities, biochemical abnormalities of bone formation, and use steroid medications are at risk
for low bone mineral density (BMD). With advances in medical management, some children with JIA can tolerate
impact exercise.
The authors implemented a 3 times a week/12-week jumping/strengthening program to promote increased BMD
in children with oligoarthritic and polyarticular arthritis. They found that the intervention resulted in increased
total body BMD at the conclusion of the program and at 3-month follow-up as compared with a control group.
Clinicians cannot assume that all children with JIA will be able to tolerate one hundred 2-footed jumps and
a resisted strengthening program. The 5 children who dropped out of the exercise group had a longer disease
duration, severity, and higher medication use. More research is needed on tolerance of children with severe
arthritis and at greatest risk for low BMD for low-impact and resistive exercise programs.
The authors’ report that children in this study did not have decreased BMD, although the tables demonstrate
some children had Z scores below −2.0. It is not clear whether they were in the exercise or control group. Specific
information on the changes in the femoral neck or lumbar spine in the exercise group is not reported. Thus,
interpreting the results is difficult.
What should I be mindful in applying this information?
Therapists need to encourage physical activity (both leisure and structured) and make bone health a priority
for children with JIA. All children should be provided with opportunities and knowledge about how to challenge
their physical capacity and promote bone health throughout life.
Bone mineral density management needs to be a team process—physical activity, calcium intake, growth
hormones, and steroid use all affect BMD. Maximal bone accrual occurs in the presence of growth hormones, for
example, prepuberty, so timing of interventions is critical. In addition, medical management must be optimized
to allow children to participate in structured or leisure activities that are osteogenic.
Exercise and activity interventions may need to be ongoing or episodic to maintain optimal bone health in
children with JIA, given changes in medication, disease state, growth hormones, and natural physical activity.
Maureen T. Nahorniak, PT, MBA, PPI, DPT
Shriners Hospital for Children
Springfield, Massachusetts
Mary E. Gannotti, PT, PhD
University of Hartford
Hartford, Connecticut
The authors declare no conflict of interest.
DOI: 10.1097/PEP.0b013e31824d6de8
Copyright © 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy
Association. Unauthorized reproduction of this article is prohibited.
162 Sandstedt et al Pediatric Physical Therapy

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Bone health in_children_and_adolescents_with.7

  • 1. R E S E A R C H A R T I C L E Bone Health in Children and Adolescents With Juvenile Idiopathic Arthritis and the Influence of Short-term Physical Exercise Eva Sandstedt, PT, MSc; Anders Fasth, MD, PhD; Hans Fors, MD, PhD; Eva Beckung, PT, PhD Department of Pediatrics, The Queen Silvia Children’s Hospital, Sahlgrenska University Hospital (Ms Sandstedt and Dr Fors), G¨oteborg, Sweden; Department of Pediatrics, Institute of Clinical Sciences (Dr Fasth) and Department of Neuroscience and Physiotherapy, Sahlgrenska Academy (Dr Beckung), University of Gothenburg, Gothenburg, Sweden; Northern ¨Alvsborg Hospital (Dr Fors), Trollh¨attan, Sweden. Purpose: To study bone mineral density (BMD) in 54 children and adolescents with juvenile idiopathic arthritis before and after a short-term exercise program. Methods: Fifty-four children, 41 girls and 13 boys, median age 13.9 years, participated in a 12-week exercise program, with 33 children in an exercise group. The program consisted of one hundred 2-footed jumps with a rope and standardized muscle strength exercise. Both BMD and bone mineral content were assessed with dual-energy x-ray absorptiometry (DXA) and DXA Laser Calscan for the heel at the start and after 3 and 6 months. Results: The study group had BMD measurements within the reference range compared with normative data with Z score at start. Bone mineral density values in total body, but not Z score, increased significantly (P = .012) in the exercise group. Conclusions: The study group had BMD measurements within the reference range. Twelve weeks of exercise increases BMD in children with juvenile idiopathic arthritis. (Pediatr Phys Ther 2012;24:155–162) Key words: 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 INTRODUCTION Bone health in children and adolescents is of great im- portance in preventing fractures later in life.1 The preva- lence of vertebral and hip fractures is increasing in the 0898-5669/110/2402-0155 Pediatric Physical Therapy Copyright C 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and Section on Pediatrics of the American Physical Therapy Association Correspondence: Eva Sandstedt, PT, MSc, Department of Pediatrics, The Queen Silvia Children’s Hospital, Sahlgrenska University, SE-416 85 G¨oteborg, Sweden (eva.sandstedt@vgregion.se). Grant Support: This study was supported by the Petter Silfverski¨old Foundation; the Norrbacka Eugenia Foundation; and the Research and Development Foundation of G¨oteborg and Bohusl¨an. The authors declare no conflict of interest. DOI: 10.1097/PEP.0b013e31824cce6e elderly in Western countries.2 Many chronic diseases, such as juvenile idiopathic arthritis (JIA), and different treat- ments 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 en- hance 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 den- sity (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 sever- ity, corticosteroid use, and inactivity in children and adolescents with JIA.7-10 The pubertal stage and dis- ease 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 Copyright © 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy Association. Unauthorized reproduction of this article is prohibited. Pediatric Physical Therapy Effects of Exercise on Bone in JIA 155
  • 2. outcome for children and adolescents with JIA has im- proved during the last 10 to 15 years. In their study, the medical efficacy of anti-tumor necrosis factor (TNF) ther- apy was shown to be high for polyarticular JIA and that long-term methotrexate therapy did not negatively influ- ence bone composition. Physical activity and physical exercise improve mus- cle 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 pre- dictors of changes in total bone mineral content (BMC). Several recently published studies demonstrate the effect of physical activity, disease activity, corticosteroids, espe- cially 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 chil- dren with JIA has established that a sedentary lifestyle con- tributes to secondary impairments in bone health, muscu- lar fitness, and functional limitations, despite advances in pharmacologic treatment of inflammatory diseases.13 In a review study from 2007, 8 randomized intervention stud- ies 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 lon- gitudinal 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 crite- ria alone. According to the International Society for Clin- ical Densitometry, the diagnosis of osteoporosis in chil- dren and adolescents (males and females aged 5-19 years) requires the presence of both a clinically significant frac- ture 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 Purpose The aim was to study BMD in a cohort of children and adolescents with JIA before and after a physical exercise program. METHODS Ethics The Regional Ethics Committee approved the study. Written consent was obtained from the participants and from their parents. Subjects The subjects were recruited in 2004-2007, in a ran- domized experimental study. Fifty-four children and ado- lescents 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 ac- cording to the revised criteria of the International League of the Associations for Rheumatology.16 Included were chil- dren with polyarticular onset form or severe oligoartic- ular onset form, being treated with methotrexate, TNF blockers, and/or prednisone (12-58 mg), and requiring re- peated corticosteroid injections in the foot, knee, or hip (see Table 1). Procedures 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. An- swers 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 ex- ercise group (n = 33) or a control group (n = 21). An ex- ercise program with pictures, instructions, and a 12-week diary were given to the exercise group at the first test oc- casion, 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, struc- tured, repetitive and purposeful in the sense that im- provement 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 Copyright © 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy Association. Unauthorized reproduction of this article is prohibited. 156 Sandstedt et al Pediatric Physical Therapy
  • 3. TABLE 1 Distribution of Gender, Age, Height, Weight, Body Mass Index, Disease Onset and Type, Medication, and Injections for the Whole Group, the Experimental Group, the Control Group, and the Dropouts on the First Test Occasion Survey Study (n = 54) Experimental Group (n = 33) Control Group (n = 21) Dropouts (n = 6) Girls, n (%) 41 (74%) 25 (76%) 17 (76%) 4 (67%) Boys, n (%) 13 (26%) 8 (24%) 5 (24%) 2 (33%) Age, y 13.9 (8.8-20.6) 13.3 (8.8-19.9) 14.9 (8.8-20.6) 15.2 (11.8-19.6) Height, cm 157 (128.6-185.8) 153.4 (128.6-175.8) 163.8 (129-185.8) 167.6 (155-185.8) Weight, kg 50.6 (22.3-82.9) 47.9 (22.3-78) 56 (35.8-82.9) 58.9 (48.8-75.5) Body mass index 20.2 (12.8-28.9) 20.0 (12.8-28.9) 20.7 (14.4-27.7) 21.1 (16.2-20) 3.4 3.4 3.5 1.7 Disease onset, y 5.8 (1-16.5) 6.1 (1.2-16.5) 4.8 (1-13.4) 9.5 (3-12.1) Polyarticular onset 31 20 9 2 Oligoarticular onset 17 7 8 2 Entesite/psoriasis arthritis 6 1 3 2 Methotrexate months (r) years 3789 (.1-181) 5.8 2497 (1.2-181) 6.3 1292 (.1-161) 5.1 1292 (.1-161) 5.1 Enbrel/remicade months (r) years 326 (5-78) 2.3 (n = 12) 272 (5-7) 10.8 (n = 9) 36 (17-19) 3 (n = 2) 5 (5-48) 2.7 (n = 2) Corticosteroids, mg/wk 5107.2 (n = 19) 12846 (n = 10) 26445 (n = 6) 11781 (n = 3) Total number of steroid injections 404 194 131 79 Number of steroid injections in foot, knee, hip 261 113 98 50 Number of steroid injections in finger, wrist, shoulder 143 81 33 29 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 ana- logue 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 Statistical Analyses 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 regres- sion 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. RESULTS 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 du- ration, 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 Copyright © 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy Association. Unauthorized reproduction of this article is prohibited. Pediatric Physical Therapy Effects of Exercise on Bone in JIA 157
  • 4. 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 corticos- teroids, 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 in- creased 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 chil- dren and adolescents, and compliance with the program TABLE 2 Distribution, Median, Standard Deviation, and Range for BMI, BMD, BMC, and Z Score for Total Body, Z Score for L1 Through L4, BMD for Legs and Area for Legs, and BMD and BMC for Left Heel at Baseline n Median (SD) Range BMI, kg/m2 54 19.9 (3.4) 12.8-28.9 BMD, total 54 0.969 (0.11) 0.79-1.25 BMC, total 54 1953.8 (631.3) 776-3463 Z score total 54 − 1.1 (0.83) −2.2 to 1.7 Z score, L1-L4 54 0.400 (1.21) −2.3 to 3.8 BMD, legs 54 0.994 (0.16) 0.72-1.4 Area, legs 54 647.98 (137.26) 352.00-904.00 BMD, heel, 49 0.372 (0.076) 0.201-0.533 BMC, heel 49 0.279 (0.098) 0.148-0.539 Abbreviations: BMC, bone mineral content; BMD, bone mineral den- sity; BMI, body mass index. TABLE 3 P Values for BMD, BMC, Z Score, and Fat for Total Body, Z Score for L1 Through L4, BMD, BMC, Area in Legs, and BMD and BMC for Left Heel at Baseline and After 12 Weeks’ Exercise and After Another 12 Weeks’ Follow-upa Exercise- Control 2-1 Exercise- Control 3-1 BMD, total .012 .061 BMC, total weight NS NS Z score total .15 .13 Fat total, %/kg .17 NS Z score, L1-L4 NS NS BMD, legs NS .74 BMC, legs NS NS Area, legs NS NS BMD, heel, NS NS BMC, heel NS NS Abbreviations: BMC, bone mineral content; BMD, bone mineral den- sity; NS, nonsignificant. aChanges between test occasions 2-1 and 3-1 with the Fisher permu- tation test within groups. was 70% of the expected value. Twenty-eight of 33 partici- pants 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. DISCUSSION 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 longitu- dinal 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 ex- ercise 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 op- timally medicated, which could explain the normal BMD. Girls appeared to have lower Z scores than boys, but no sta- tistical 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 de- creased total BMD in patients with the polyarticular onset form, low weight, and early disease onset treated with cor- ticosteroids 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 Copyright © 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy Association. Unauthorized reproduction of this article is prohibited. 158 Sandstedt et al Pediatric Physical Therapy
  • 5. Fig. 1. Distribution of Z scores for the control and the exercise group at baseline, after 3 months, and at 6 months. Z scores for children are described with respect to standard deviations between +2 and −2.5. Fig. 2. Physical exercise in leisure time at the second and third test occasions, from baseline to 12 weeks and from 12 to 24 weeks, divided into categories according to the level of weight-bearing activity: category 1—jogging, football, ball sports; category 2—walking, horse riding; category 3—swimming, cycling; category 4—physical activity (pt) at school. Abbreviations: Con, control group; Exp, experimental group; Tot, total. TABLE 4 Seasonal Effects of Exercise: Regression Analysis With Analysis of Covariance-Dependent Variable BMD1. Unstandardized Coefficients Standardized Coefficients 95.0% Confidence Interval for B Model B SE β t P Lower Bound Upper Bound 1. (Constant) − 0.015 0.015 .995 − 1.007 .319 − 0.046 0.015 BMD2 1.006 0.015 67.308 .000 0.976 1.036 2. (Constant) − 0.014 0.015 − 0.984 .330 − 0.044 0.015 BMD2 0.981 0.018 .970 53.488 .000 0.944 1.018 BMD3 0.024 0.011 .040 2.187 .034 0.002 0.047 3. (Constant) − 0.009 0.015 − 0.588 .560 − 0.039 0.022 BMD2 0.979 0.018 .969 53.830 .000 0.943 1.016 BMD3 0.024 0.011 .040 2.207 .032 0.002 0.047 Season − 0.002 0.001 − .019 − 1.380 .174 − 0.005 0.001 4. (Constant) − 0.008 0.014 − 0.537 .594 − 0.037 0.021 BMD2 0.971 0.018 .960 54.728 .000 0.935 1.006 BMD3 0.021 0.011 .035 2.017 .050 0.000 0.043 Season − 0.002 0.001 − .019 − 1.437 .158 − 0.005 0.001 Group 0.008 0.003 .034 2.350 .023 0.001 0.014 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 per- formed 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. Copyright © 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy Association. Unauthorized reproduction of this article is prohibited. Pediatric Physical Therapy Effects of Exercise on Bone in JIA 159
  • 6. Fig. 3. Physical exercise in leisure time, presenting seasonal effects on physical activity level. Fig. 4. Distribution of numbers of repetitions of the expected and performed exercise programs for the exercise group. Abbre- viations: Hip ext, hip extension; Shouldabd, shoulder abduction; Shouldflex, shoulder flexion. 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. Chil- dren with optimal medical treatment and without disease activity should be given an opportunity to challenge their physical capacity. The International League of the Asso- ciations for Rheumatology recommends adequate medi- cal 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 de- manding 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 chal- lenge 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 re- cently 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 encourage- ment during growth are of great importance for improve- ment in a childhood chronic conditions.1,2,6,7,10,13,23–26 CONCLUSIONS 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 im- proved 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. ACKNOWLEDGMENTS 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 analyz- ing the results of the DXL, Helena Johansson and Eva Andersson for statistical support, and Anne Dohs´e for the expert assistance. REFERENCES 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 Appli- cation 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 En- docrinol Metab. 1997;82(1):57-62. 6. Lien G, Selvaag A M, Flat¨o B, et al. A two-year prospective controlled study of bone mass and bone turnover in children with early juvenile idiopathic arthritis. Arthritis Rheum. 2005;52(3):833-840. Copyright © 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy Association. Unauthorized reproduction of this article is prohibited. 160 Sandstedt et al Pediatric Physical Therapy
  • 7. 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 rheuma- toid 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 influ- ence 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 (Bailli`eres). 1997;3(11):479- 494. 15. Bianch ML, Bains S, Bishop NJ, et al. Official position of the Interna- tional 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 idio- pathic 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, ex- ercise, 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. S¨oderpalm AC, Kullenberg R, Swolin-Eide D. The relationship be- tween 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 ac- crual in children and adolescents: a review of controlled trials. Bone. 2007;40(1):14-27. 25. J¨urim¨ae T, Hurbo T, Jurim¨ae 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. Copyright © 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy Association. Unauthorized reproduction of this article is prohibited. Pediatric Physical Therapy Effects of Exercise on Bone in JIA 161
  • 8. C L I N I C A L B O T T O M L I N E Commentary on “Bone Health in Children and Adolescents With Juvenile Idiopathic Arthritis and the Influence of Short-term Physical Exercise” How should I apply this information? Children with juvenile idiopathic arthritis (JIA) who have polyarticular arthritis, growth retardation, reduced weight-bearing activities, biochemical abnormalities of bone formation, and use steroid medications are at risk for low bone mineral density (BMD). With advances in medical management, some children with JIA can tolerate impact exercise. The authors implemented a 3 times a week/12-week jumping/strengthening program to promote increased BMD in children with oligoarthritic and polyarticular arthritis. They found that the intervention resulted in increased total body BMD at the conclusion of the program and at 3-month follow-up as compared with a control group. Clinicians cannot assume that all children with JIA will be able to tolerate one hundred 2-footed jumps and a resisted strengthening program. The 5 children who dropped out of the exercise group had a longer disease duration, severity, and higher medication use. More research is needed on tolerance of children with severe arthritis and at greatest risk for low BMD for low-impact and resistive exercise programs. The authors’ report that children in this study did not have decreased BMD, although the tables demonstrate some children had Z scores below −2.0. It is not clear whether they were in the exercise or control group. Specific information on the changes in the femoral neck or lumbar spine in the exercise group is not reported. Thus, interpreting the results is difficult. What should I be mindful in applying this information? Therapists need to encourage physical activity (both leisure and structured) and make bone health a priority for children with JIA. All children should be provided with opportunities and knowledge about how to challenge their physical capacity and promote bone health throughout life. Bone mineral density management needs to be a team process—physical activity, calcium intake, growth hormones, and steroid use all affect BMD. Maximal bone accrual occurs in the presence of growth hormones, for example, prepuberty, so timing of interventions is critical. In addition, medical management must be optimized to allow children to participate in structured or leisure activities that are osteogenic. Exercise and activity interventions may need to be ongoing or episodic to maintain optimal bone health in children with JIA, given changes in medication, disease state, growth hormones, and natural physical activity. Maureen T. Nahorniak, PT, MBA, PPI, DPT Shriners Hospital for Children Springfield, Massachusetts Mary E. Gannotti, PT, PhD University of Hartford Hartford, Connecticut The authors declare no conflict of interest. DOI: 10.1097/PEP.0b013e31824d6de8 Copyright © 2012 Wolters Kluwer Health | Lippincott Williams & Wilkins and the Section on Pediatrics of the American Physical Therapy Association. Unauthorized reproduction of this article is prohibited. 162 Sandstedt et al Pediatric Physical Therapy