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Objective. To compare the aerobic and anaerobic exercise capacity of children with juvenile idiopathic arthritis (JIA)
with healthy controls, to determine if there were differences based on disease onset type, and to examine the relationship
between aerobic and anaerobic exercise capacity in children with JIA.
Methods. Sixty-two patients with JIA (mean ⴞ SD age 11.9 ⴞ 2.2 years, range 6.7–15.9) participated in this study. Aerobic
exercise capacity was measured using a cardiopulmonary exercise test. Anaerobic exercise capacity was measured using
the Wingate Anaerobic Exercise Test (WAnT).
Results. All patients were able to perform the cardiopulmonary exercise test and WAnT without adverse events. On
average, the maximal oxygen uptake (VO2peak) and VO2peak/kg were 69.8% and 74.8%, respectively, of that predicted
compared with healthy controls. Mean ⴞ SD power was 66.7% ⴞ 37.2% of that predicted compared with healthy children.
Mean ⴞ SD peak power was 65.5% ⴞ 43.1% of that predicted compared with healthy children. There were significant
differences between subgroups of JIA; the oligoarticular-onset group values did not significantly differ from healthy
control values; the polyarticular rheumatoid factor positive– onset subgroup had the greatest impairment in both aerobic
and anaerobic exercise capacity. The correlations of mean power and peak power with VO2peak were r ⴝ 0.884 and r ⴝ
0.697, respectively (P < 0.05).
Conclusion. This study demonstrates that both the aerobic and anaerobic exercise capacity in children with JIA are
significantly decreased. The WAnT might be a valuable adjunct to other assessment tools in the followup of patients with
JIA.
KEY WORDS. Exercise tolerance; Aerobic fitness; Cardiovascular deconditioning; Physical fitness.
891
892 van Brussel et al
Fisher et al (18) found that children with JIA could im- American College of Sports Medicine guidelines (23). The
prove muscle strength significantly after an exercise train- sum of the 7 skin folds was used as an index for subcuta-
ing program, without increase in disease signs and symp- neous fat according to methods described by Pollack et al
toms. (24).
The current evidence base for anaerobic exercise capac-
ity is small and is derived from findings in small cohorts. Joint status. Joint status was assessed by the number of
In the current study, we aimed to increase the evidence tender and swollen joints. Tenderness and swelling were
basis for both aerobic and anaerobic exercise capacity and scored for the following joints: temporomandibular, ster-
their interrelationship. We therefore studied 1) the aerobic noclavicular, shoulder, elbow, wrist, metacarpophalangeal
and anaerobic exercise capacity of a large cohort of pa- and fingers, knee, ankle, metatarsophalangeal, and toes.
tients with JIA and compared these with healthy controls, Joint mobility was scored on the Pediatric Escola Paulista
2) if there were differences in aerobic and anaerobic exer- de Medicina Range of Motion Scale (pEPMROM) (25). The
cise capacity in children with JIA based on disease onset pEPMROM measures mobility in children with JIA based
type, and 3) the relationship among aerobic and anaerobic on the evaluation of joint range of motion. Ten joint move-
exercise capacity in children with JIA. ments (cervical spine [rotation], shoulder [abduction],
wrist [flexion and extension], thumb [flexion metacarpo-
PATIENTS AND METHODS phalangeal], hip [internal and external rotation], knee [ex-
tension], and ankle [dorsiflexion and plantar flexion]) were
examined using a goniometer and were classified on a
Patients. Sixty-two patients with JIA participated in
4-point Likert scale ranging from 0 to 3 (0 ⫽ no limitation
this study. The patients were recruited from the pediatric
and 3 ⫽ severe limitation). The final score was calculated
rheumatology outpatient clinic of the Wilhelmina Chil-
as the sum of the joint score of each movement divided by
dren’s Hospital and were diagnosed with JIA according to
10, providing a final range of scores for joint movement
the International League of Associations for Rheumatology
from 0 to 3.
(ILAR) criteria (19). Thirty-six patients had polyarticular-
onset JIA (29 rheumatoid factor negative and 7 rheumatoid
Functional ability. The Childhood Health Assessment
factor positive), 11 patients had oligoarticular-onset JIA, 8
patients were classified as having extended oligoarticular- Questionnaire (C-HAQ) was adapted by Sing et al (26)
onset JIA, and 7 patients were classified as having system- from the Stanford Health Assessment Questionnaire for
ic-onset JIA. Fifteen patients in the cohort were off medi- use in patients ages 1–19 years, and measures functional
cation. Of the remaining patients, 41 patients were status. A Dutch version was translated and validated (27).
receiving nonsteroidal antiinflammatory drugs, 28 were The C-HAQ is a pediatric multidimensional questionnaire,
receiving disease-modifying antirheumatic drugs, 6 were which measures the child’s ability in performing functions
receiving corticosteroids, and 7 were receiving biologic included in 8 areas (dressing and grooming, arising, eating,
agents (biologic response modifiers). Disease onset and walking, hygiene, reach, grip, and activities) for a total
duration were assessed by retrospective analysis of pa- item number of 30. Respondents are directed to note only
tients’ files. During the tests, 35 patients had active dis- those difficulties caused by arthritis. Each question is
ease, 12 patients were in clinical remission and taking scored from 0 to 3 (0 ⫽ able to do with no difficulty, 1 ⫽
medication, and 15 patients were in clinical remission and able to do with some difficulty, 2 ⫽ able to do with much
off medication, according to criteria developed by Ruperto difficulty, 3 ⫽ unable to do). The question with the highest
and Martini (20). All tests and measurements of the pa- score within each domain determined the score for that
tients were performed on the same day, with enough rest- domain. Whenever aids or assistance were required, the
ing time between the aerobic and anaerobic exercise tests. score for that domain was increased to a minimum of 2.
Informed consent was obtained from the parents and/or The mean of the scores on the 8 domains provided the
from the children if they were ⬎12 years of age. The C-HAQ disability scale (range 0 –3, with 0 denoting no
Medical Ethics Committee of the University Medical Cen- disability and 3 denoting severe disability). The C-HAQ
ter Utrecht approved all study procedures. also incorporates a double-anchored, horizontal, 10-cm
visual analog scale for the assessment of the child’s overall
Anthropometry. The children’s body mass and height well-being and a visual analog scale for the assessment of
were determined using an electronic scale and a stadiom- the intensity of the child’s pain.
eter, respectively. Body mass index (BMI) was calculated
as body mass (kg)/height (m2). The BMI of the included Cardiopulmonary exercise test. The maximal oxygen
children was compared with reference values of healthy uptake (VO2peak) attained during a graded exercise test to
Dutch children (21) and with international cutoff points volitional exhaustion is considered the single best indica-
for BMI for overweight and obese children (22). Subcuta- tor of aerobic physical fitness. Cardiopulmonary exercise
neous adiposity was determined from skinfold measure- test was performed on an electronically braked cycle er-
ments using Harpenden skinfold calipers (British Indica- gometer (Lode examiner; Lode BV, Groningen, The Neth-
tions, St. Albans, Hertfordshire, UK). Measurements were erlands). The seat height was adjusted to the patient’s
obtained in triplicate at 7 sites (at the right side of the comfort. Cycling started at a workload of 0W and the
body): triceps, biceps, subscapular, suprailiac, mid-ab- workload was increased by 20W every minute until the
dominal, medial calf, and thigh in accordance with the patient stopped due to volitional exhaustion, despite
Exercise Capacity in Children With JIA 893
* Values are the mean ⫾ SD (range) unless otherwise indicated. BMI ⫽ body mass index; ⌺7SF ⫽ sum of 7 skinfold measurements; pEPMROM ⫽
Pediatric Escola Paulista de Medicina Range of Motion Scale; C-HAQ ⫽ Childhood Health Assessment Questionnaire.
strong verbal encouragement. Patients breathed through a was compared with age-, weight-, and sex-matched refer-
mouth piece that was connected to a calibrated metabolic ence values obtained from 50 healthy Dutch children and
cart (Oxycon Champion; Jaeger, Viasys, Bilthoven, The adolescents as has been reported previously (30). The sub-
Netherlands). Expired gas was passed through a flow jects were recruited from family members of staff at our
meter, oxygen analyzer, and carbon dioxide analyzer. The hospital or were living in the neighborhood of our hospi-
flow meter and gas analyzer were connected to a computer, tal. All controls were tested following the same protocol as
which calculated breath-by-breath minute ventilation, ox- the patients.
ygen consumption, carbon dioxide production, and respi-
ratory exchange ratio from conventional equations. Heart Statistical analysis. Statistical analyses were performed
rate was measured continuously during the maximal exer- using the statistical Package for the Social Sciences for
cise test with a 3 lead electrocardiogram. Windows (version 12.0; SPSS, Chicago, IL). Variables were
expressed as the mean ⫾ SD and range; statistical compar-
Wingate Anaerobic Exercise Test. The Wingate Anaer- isons between measurements were made using the Stu-
obic Test (WAnT), as described by Bar-Or (28), was per- dent’s t-test. The data were also expressed as the percent-
formed on a calibrated electromagnetic braked cycle er- age of impairment compared with reference values,
gometer (Lode Examiner; Lode BV). The ergometer was because of the large ranges in age. Spearman’s correlations
upgraded and calibrated by the manufacturer to a maxi- were used to calculate possible correlations between the
mum resistance of 800W instead of the standard 400W. aerobic and anaerobic capacity. The level of statistical
External resistance was controlled, the power output was significance was set at P less than 0.05.
measured, and mean power and peak power were calcu-
lated from the exercise results using the Lode Wingate
software package (Lode BV, Groningen, The Netherlands). RESULTS
The seat height was adjusted to patients’ leg length (com-
fortable cycling height). The external load (torque; in Nm) Fifteen boys and 47 girls were included in this study. The
was determined by body weight (at 0.53 ⫻ body weight mean ⫾ SD age of the patients was 11.9 ⫾ 2.2 years with a
and 0.55 ⫻ body weight for girls and boys, respectively, range of 6.7–15.9 years. Mean ⫾ SD age at disease onset
⬍14 years of age and 0.67 ⫻ body weight and 0.7 ⫻ body and duration were 6.6 ⫾ 3.6 years (range 0.5–15.3 years)
weight for older girls and boys, respectively) according to and 4.7 ⫾ 3.2 years (range 0.4 –11.8 years), respectively.
the user manual. The patients’ feet were placed in the The anthropometric values are shown in Table 1. The
Velcro toe straps and the exercise protocol was explained. mean body mass of the patients was 44.5 ⫾ 14.4 kg (range
The patients were instructed to exercise for 1 minute with 22.2– 81.0 kg), the mean height was 1.53 ⫾ 0.14 meters
the cycle ergometer with an external load of 15W at 50 – 60 (range 1.24 –1.83 meters), and mean BMI was 18.7 ⫾ 3.7
revolutions per minute. Thereafter the sprint protocol kg/m2 (range 13.2–28.2 kg/m2). The mean sum of the 7
started. The patients were instructed to cycle as fast as skinfold measurements was 103.2 ⫾ 46.5 mm (range
possible for 30 seconds. Power output during the WAnT 41.33–240.3 mm). The sum of the 7 skinfold measure-
was corrected for the inertia of the mass of the flywheel ments of the children with JIA was significantly higher
(23.11 kg/m2). Measured variables were mean power and (P ⬍ 0.0001) compared with healthy controls. The anthro-
peak power. Mean power represents the average power pometric parameters of the patients indicated that none of
output over the 30-second sprint. Peak power is the high- the patients were obese and 10 patients were overweight,
est recorded power output achieved during the 30-second although mean BMI and weight values did not differ from
sprint and represents the explosive characteristics of a reference values. The results of joint status, joint mobility,
person’s muscle power. Recent data indicated that the and functional ability are shown in Table 1. The patients
WAnT could be reliably assessed in children with JIA (29). had a mean ⫾ SD of 3.0 ⫾ 4.6 tender and swollen joints
The anaerobic exercise capacity of the patients with JIA (range 0.0 –24.0) and a mean pEPMROM score of 0.3 ⫾ 0.3
894 van Brussel et al
Table 2. Aerobic and anaerobic exercise capacity of patients with JIA and controls*
* Values are the mean ⫾ SD unless otherwise indicated. JIA ⫽ juvenile idiopathic arthritis; VO2peak ⫽ maximal oxygen uptake; VO2peak/kg ⫽ maximal
oxygen uptaken corrected for body mass.
(range 0.0 –1.3), indicating that the cohort had almost no that 95% of all patients (n ⫽ 59) had an impaired aerobic
limitation due to active synovitis. The mean ⫾ SD C-HAQ exercise capacity and 94% (n ⫽ 58) had an impaired
score of the patients was 0.7 ⫾ 0.7 (range 0.0 –2.5), indi- anaerobic capacity. The outcomes of the aerobic and an-
cating mild-to-moderate disability (31). aerobic capacity for the different subtypes in this study are
The results of aerobic and anaerobic exercise tests are shown in Table 3 as additional findings. Table 4 shows
depicted in Table 2. All children were able to complete the that there were significant correlations between the im-
aerobic and anaerobic exercise test without adverse ef- pairments of the mean power, peak power, and VO2peak.
fects, such as dizziness, fainting, or even vomiting. VO2peak
was on average 77.1% ⫾ 30.6% and 67.6% ⫾ 20.8% of that
predicted for boys and girls, respectively. VO2peak/kg was DISCUSSION
on average 73.6% ⫾ 13.4% and 75.1% ⫾ 17.6% of that
predicted for boys and girls, respectively. The anaerobic The goal of this study was to compare the aerobic and
capacity was ⬍67% of that predicted for both peak power anaerobic exercise capacity of children with JIA with that
and mean power compared with the healthy controls. of age-, weight-, and sex-matched healthy controls; to de-
Mean power was on average 79.4% ⫾ 52.7% and 62.5% ⫾ termine if there were differences in aerobic and anaerobic
30.3% of that predicted for boys and girls, respectively. exercise capacity in children with JIA based on disease
Peak power was on average 75.5% ⫾ 55.0% and 62.3% ⫾ onset type; and to examine the relationship among aerobic
38.7% of that predicted for boys and girls, respectively. and anaerobic exercise capacity in children with JIA. The
The differences between boys and girls were statistically results show a significantly decreased aerobic as well as
significant for VO2peak (P ⫽ 0.023) and for VO2peak/kg (P ⫽ anaerobic capacity in children with JIA compared with
0.009). healthy controls. The decreased aerobic capacity is in line
The children in remission (off medication) also had with earlier findings by our group (5) and by others (4,13)
lower aerobic and anaerobic exercise capacity than con- and has been discussed extensively. In the current study,
trols. The VO2peak and VO2peak/kg were 69.8% (P ⬍ 0.0001) anaerobic capacity was expressed by means of peak power
and 74.8% (P ⬍ 0.0001) of that predicted, respectively. and mean power, which demonstrated that most of the
The mean power and peak power were 60.4% (P ⬍ 0.0001) children with JIA had a significantly lower anaerobic ca-
and 49.3% (P ⬍ 0.0001) of that predicted, respectively. pacity compared with healthy children. Our study is the
There was no difference in aerobic and anaerobic exercise first to assess anaerobic exercise capacity in a large cohort
capacity between the children in remission and the chil- of children with JIA compared with a healthy control
dren receiving medication. It is noteworthy to mention group. Lower anaerobic capacity was also found in the
Table 3. Outcome values (% of predicted) of aerobic and anaerobic capacity for the different subgroups of JIA*
Polyarticular RF negative 64.4 ⫾ 29.5† 64.7 ⫾ 41.5† 65.2 ⫾ 19.9† 70.2 ⫾ 14.8†
Polyarticular RF positive 52.5 ⫾ 38.2† 48.4 ⫾ 41.1† 52.8 ⫾ 22.3† 62.5 ⫾ 8.4†
Oligoarticular 94.8 ⫾ 55.3 94.4 ⫾ 57.8 89.3 ⫾ 32.6 78.8 ⫾ 16.9†
Oligoarticular extended 57.2 ⫾ 23.4† 52.7 ⫾ 26.1† 68.3 ⫾ 14.6† 75.7 ⫾ 21.1†
Systemic 64.7 ⫾ 27.9† 65.2 ⫾ 30.7† 64.5 ⫾ 19.7† 60.3 ⫾ 1.8†
* Values are the mean ⫾ SD. RF ⫽ rheumatoid factor; see Table 2 for additional definitions.
† Significantly different (P ⬍ 0.05) from reference values.
Exercise Capacity in Children With JIA 895
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9. Golebiowska M, Brozik H, Bujnowski T. Aerobic and anaero-
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study in which children showed similar impairment in Coutts KD, Turner SP, et al. Physical fitness and its relation-
anaerobic and aerobic performance. Despite our finding of ship to other indices of health status in children with chronic
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other more commonly used assessment tools, such as the 12. Klepper SE, Darbee J, Effgen SK, Singsen BH. Physical fitness
C-HAQ, the Juvenile Arthritis Functional Assessment levels in children with polyarticular juvenile rheumatoid ar-
Scale, hand-held myometry, and aerobic exercise tests. thritis. Arthritis Care Res 1992;5:93–100.
13. Takken T, Hemel A, van der Net J, Helders PJ. Aerobic fitness
In conclusion, we found that both aerobic and anaerobic
in children with juvenile idiopathic arthritis: a systematic
exercise capacity were significantly decreased in a large review. J Rheumatol 2002;29:2643–7.
cohort of patients with JIA under 16 years of age. More- 14. Feldman BM, Wright FV, Bar-Or O, Dent P. Rigorous fitness
over, distinct differences were observed between sexes training and testing for children with polyarticular arthritis: a
and disease subgroups. A moderate to large relationship pilot study [abstract]. Arthritis Rheum 2000;43 Suppl 9:S120.
15. Takken T, van der Net J, Helders PJ. Relationship between
was found between aerobic and anaerobic capacity mea- functional ability and physical fitness in juvenile idiopathic
sures. arthritis patients. Scand J Rheumatol 2003;32:174 – 8.
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strength and function in females with juvenile rheumatoid
ACKNOWLEDGMENT arthritis. J Rheumatol 1998;25:1399 – 405.
We are grateful to Harriët Wittink, PhD, MSc, PT, for the 17. Wessel J, Kaup C, Fan J, Ehalt R, Ellsworth J, Speer C, et al.
Isometric strength measurements in children with arthritis:
revision and correction of the final manuscript. reliability and relation to function. Arthritis Care Res 1999;
12:238 – 46.
18. Fisher NM, Venkatraman JT, O’Neil KM. Effects of resistance
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Dr. Takken had full access to all of the data in the study and tis Rheum 1999;42 Suppl 9:S396.
takes responsibility for the integrity of the data and the accuracy 19. Hofer M, Southwood TR. Classification of childhood arthritis.
of the data analysis. Best Pract Res Clin Rheumatol 2002;16:379 –96.
Study design. Takken, van Brussel, Lelieveld, van der Net, Engel- 20. Ruperto N, Martini A. International research networks in
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Analysis and interpretation of data. Takken, van Brussel, Le- 21. Gerver W, de Bruin R. Paediatric morphometrics: a reference
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