School Children With Generalized Joint Hypermobility
WHAT’S KNOWN ON THIS SUBJECT: Diverging results exist for children regarding the relation between GJH and musculoskeletal complaints, as well as relations between GJH and an insufficient motor development and/or a reduced physical activity level. In addition, the prevalence of GJH varies considerable.
WHAT THIS STUDY ADDS: The prevalence of GJH in Danish primary school–aged children at 8 years is described, besides the relation between GJH and BJHS and incidence of musculoskeletal pain and injuries, measured motor competence, in addition to daily level of physical activity.
abstract
OBJECTIVE:Because the criteria used for diagnosing between gener-alized joint hypermobility (GJH) and musculoskeletal complaints, as well as relations between GJH and an insufficient motor development and/or a reduced physical activity level differ, the prevalence of GJH varies considerably. The aim of this study was to survey the prevalence of GJH defined by a Beighton score atⱖ4,ⱖ5, orⱖ6 positive tests of 9 and benign joint hypermobility syndrome (BJHS) in Danish primary school children at 8 years of age. A second aim was to compare chil-dren with and without GJH and BJHS regarding motor competence, self-reported physical activity, and incidence of musculoskeletal pain and injuries.
METHODS:A cross-sectional study of 524 children in the second grade from 10 public schools was performed. A positive response rate was obtained for 416 (79.4%) children, and 411 (78.4%) children were clin-ically examined and tested for motor competence, whereas question-naire response to items comprising musculoskeletal pain and injuries, in addition to daily level and duration of physical activity, corresponded to 377 (71.9%) children.
RESULTS:In total, 29% of the children had GJH4, 19% had GJH5, 10% had GJH6, and 9% had BJHS, with no gender difference. There was no difference in daily level and duration of physical activity and in fre-quency of musculoskeletal pain and injuries between those with and without GJH. Children withⱖGJH5 as well as withⱖGJH6 performed better in the motor competence tests.
CONCLUSION:Motor competence and physical activity are not reduced in primary school children at 8 years of age with GJH or BJHS. It is recommended that a potential negative influence on the musculoskel-etal system over time, as a result of GJH, be investigated by longitudinal studies.Pediatrics2009;124:1380–1387
AUTHORS:Birgit Juul-Kristensen, PhD, PT,a,b
Jens Halkjær Kristensen, DMSc,aBritt Frausing, PT,c
Dorte Vendelboe Jensen, MD,dHenrik Røgind, PhD,eand
Lars Remvig, DMSca
Departments ofaRheumatology andcPhysiotherapy and
Occupational Therapy, Rigshospitalet, University Hospital, Copenhagen, Denmark;bResearch Initiative in Physiotherapy,
University of Southern Denmark, Odense, Denmark;dDepartment
of Rheumatology, Hørsholm Hospital, Hørsholm, Denmark; and
eDepartment of Rheumatology, Frederiksberg Hospital,
Frederiksberg, Denmark
KEY WORDS
joint instability, musculoskeletal system, pain, pediatric rheumatic diseases
ABBREVIATIONS
JHS—joint hypermobility syndrome GJH— general joint hypermobility BJHS— benign joint hypermobility syndrome PAL—physical activity level
MET—metabolic equivalent
TAA3M—time in physical activity above 3 METs
www.pediatrics.org/cgi/doi/10.1542/peds.2009-0294
doi:10.1542/peds.2009-0294
Accepted for publication Jun 9, 2009
Address correspondence to Birgit Juul-Kristensen, PhD, PT, Research Initiative in Physiotherapy, University of Southern Denmark, Campusvej 55, DK-5230 Odense M. E-mail: [email protected]
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright © 2009 by the American Academy of Pediatrics
Musculoskeletal disorders, including joint hypermobility syndrome (JHS), are in general characterized by pain and physical disorders, leading to de-creased quality of life and economic burdens to society. General joint hy-permobility (GJH), which has a strong relation to age, gender, ethnicity, and heredity,1–6is defined from a certain
number of joint mobility tests7and is
part of the diagnostic criteria for be-nign joint hypermobility syndrome (BJHS)8 and for a number of serious
hereditary connective tissue diseases. The criterion for GJH varies but has been suggested to beⱖ4 positive tests of Beighton’s 9 tests for joint hypermo-bility,8 here called ⱖGJH4; however,
for 1 of the hereditary diseases, Ehlers Danlos syndrome, the levelⱖ5 positive Beighton tests (ⱖGJH5) is recom-mended,9and for children at 10 to 12
years of age, the level ofⱖ6 positive Beighton tests (ⱖGJH6) has been used.10Different criteria for different
age groups11and genders12 are
sug-gested, but there is no consensus for GJH.
The criteria and consequently the prevalence of GJH vary, depending on the study population and the tests and criteria used. This is illustrated by a ⱖGJH4 prevalence at 9.4% among 12-to 13-year-olds,13aⱖGJH5 prevalence
at 14% among 13- to 16-year-old school children,14 compared with a ⱖGJH6
prevalence at 7.8% and 7.4% in 2 child cohorts of 10- to 15-year-olds.10,15
Some studies of adult populations have indicated a relation between GJH and musculoskeletal complaints (eg, arthralgia [knee, back, and pelvis], joint luxations [ankle, knee, and hip], soft tissue rheumatism [tendonitis/ bursitis and fibromyalgia], osteoar-thritis, other types of musculoskeletal disorders).15–18 Other studies did not
find any relation between GJH and musculoskeletal complaints.10,19,20
A possible relationship has been sug-gested between children with BJHS (ⱖGJH4) and a delayed and insufficient motor development, clumsiness, and speech and learning problems21;
how-ever, this was not confirmed in other studies, in part because of methodologic differences between study designs and methods, by using either a Spanish scor-ing system for diagnosscor-ing hypermobility syndromes22 or a questionnaire20
in-stead of physical tests23for motor
com-petence, making data comparison diffi-cult. Furthermore, some studies found that 11- to 13-year-old children with ⱖGJH4 and pain and/or exposure to in-juries had a reduced self-reported phys-ical activity level (PAL).13,24
Poor motor competence and musculo-skeletal joint symptoms may interfere with daily life activities, resulting in a less active lifestyle in primary school– aged children.25,26 This is in contrast
to the recommended duration of a minimum of 60 minutes per day of physical activity (moderate- and high-intensity level) for children to reduce the risk for chronic diseases and disabilities.27–29
The relation between GJH and muscu-loskeletal disorders has often been described in elderly populations, whereas the relation is rarely de-scribed in children, and neither has the relation between GJH and physical tests for motor competence, in addi-tion to physical activity in primary school–aged children been described; therefore the aim of this study was to survey the prevalence of GJH and BJHS in a Danish population of school chil-dren at 8 years age and to compare children with and without GJH and BJHS regarding incidence of musculo-skeletal pain and injuries, motor com-petence, and physical activity.
METHODS
All children in the second grade in a midsize Danish municipality (total
pop-ulation: 46 759), housing 10 public schools including 23 classes, were in-vited to participate through a letter to their parents (Fig 1). Parents of 524 children at 8 years of age were asked, and 416 (79.4%) parents consented to let their child participate. Ninety-eight (18.7%) denied, 9 (1.7%) did not reply, and 1 had moved. A positive response rate was obtained for 416 (79.4%), through consecutive information and written reminders to the parents. A to-tal of 411 (78.4%) children were clini-cally examined and tested for motor competence, and 377 (71.9%) re-sponded to the questionnaire, result-ing in a complete data set of 374 (71.4%) children. Twenty-five (4.8%) of those children represented other eth-nic origins than Caucasian, which left 349 (66.6%) children of Caucasian ori-gin to be analyzed.
The Committee on Biomedical Re-search Ethics for Copenhagen and Frederiksberg, Denmark, approved the experimental protocol (jnr. KF 01-2006-178). Parents of each participating child gave their informed written consent according to the Declaration of Helsinki,30and before the
examina-tion, each child gave oral assent to participation.
Clinical and Motor Competence Tests
The children, performing no stretching or warm-up exercise before the tests, were tested in groups during March to June 2007. Four different examiners and 3 different testers took part in the clinical and motor competence exami-nations, respectively. Examiners and testers all were thoroughly trained be-fore the investigation, and they were mutually blinded to each other’s results.
tested by the same examiners to have a high reproducibility,beingⱖ0.80 and ⱖ0.73.31 Prevalence of positive
Beighton tests and Brighton signs were registered, in addition to the prevalence of GJH, based onⱖGJH4, ⱖGJH5,ⱖGJH6, and BJHS.
Three motor competence tests were included, focusing on the main factors for motor competence, such as agility, static balance, and speed and hand re-action, previously tested to have a good reproducibility, with r between 0.87 and 0.89 and an acceptable face
before being tested.
For testing agility, a quadrant jump test was performed, whereby the child had to jump around in a 4-quadrant square with the legs together, bare-footed on a nonslippery surface. The total number of quadrants reached in 10 seconds was counted but reduced by 0.5 every time 1 of the boundaries of the 4 quadrants was touched. The test was performed twice, and the best re-sult was selected.
For testing the static balance, a stork stand test was performed, whereby the child had to stand on his or her tiptoe on 1 (self-selected) leg, with the other leg flexed so that the lifted foot rested on the side of the standing knee. The total time (in seconds) was registered until the balance was lost and the resting foot touched the ground. This test was performed 3 times, and the best result was selected.
For testing speed and hand reaction, a Nelson hand reaction test was per-formed, whereby the child had to hold a vertical oriented 30-cm-long ruler at 0 cm in the dominant hand, then let the ruler drop and catch it again, as fast as possible. The level (in cm) at which the child caught the ruler was registered, and the test was performed 10 times and the average of the middle 4 tests was used.
Questionnaire
An electronic- or paper-based ques-tionnaire with 75 items on health and physical activity was forwarded to the parents, depending on their choice. Most of the questionnaires were an-swered by the children and their par-ents together, whereas a small part of the questionnaires, 55 (14.6%), mostly from those who were bilingual, was filled out at the school during the
Positive to participate (n = 416, 79.4%)
No replies (n = 9, 1.7%) Moved to another geographic area (n = 1)
Answers to questionnaire (n = 377, 71.9%) (electronic version: n = 322; paper version: n = 55)
Clinical examination and motor competence tests (n = 411, 78.4%)
Complete data set (n = 374, 71.4%)
Excluded due to poor physical and cooperative abilities (n = 2)
Caucasian ethnicity (n = 349, 66.6%)
Excluded due to non-Caucasian ethnicity (n = 25, 4.8%) Absent from school on examination (n = 4) Denied participation (n = 1)
No questionnaire replies (n = 39, 7.4%)
Declined to let child participate at school (n = 3)
FIGURE 1
Flow diagram of recruitment and inclusion procedures.
TABLE 1 Brighton Tests and Criteria for BJHS and Beighton Tests and Criteria for GJH
Brighton Criteria8 Beighton Tests6,9,31
Major criteria 1. First right finger, apposition
1. Beighton scoreⱖ4 (currently or historically) 2. First left finger, apposition
2. Arthralgiaⱖ4 joints for⬎3 mo 3. Fifth right finger, dorsiflexion
Minor criteria 4. Fifth left finger, dorsiflexion
1. Skin signs 5. Right elbow, extension
2. Eye signs 6. Left elbow, extension
3. Marfanoid habitus 7. Right knee, extension
4. Beighton score⬍4 8. Left knee, extension
5. Arthralgia⬍4 joints 9. Forward bending
6. Dislocation/subluxation 7. Soft tissue
8. Varicose veins, hernia, prolapse 9. A first-degree relative
Diagnosis: BJHS (2 major, 1 major⫹2 minor, 4 minor, or 2 minor⫹1 first-degree relative)
follow-up round by the children to-gether with 1 of the researchers.
The items included on musculoskeletal health, pain (pain inⱖ4 joints for⬎3 months), and injuries (dislocation/ subluxation in⬎1 joint or in 1 joint⬎1 time) were those equal to the historical signs used for BJHS8 and previously
tested to have a high reproducibility.31
PAL was measured using a standard-ized questionnaire, originally based on standards and questionnaires for adults34,35but adjusted to meet
school-children’s pattern of activity and en-ergy expenditure per kilogram.36
Fur-thermore, when tested on children, it has revealed a high validity compared with a computerized motion sensor and calculated metabolic equivalents (METs; with 1 MET being equal to the resting metabolic rate during quiet sit-ting). Questions included physical ac-tivities on an average day and week in school; breaks; leisure time; during transportation to/from school and to/ from sports; and the duration of TV watching, computer use, homework performance, leisure time reading, and sleep during average weekdays and weekends. Weekly and daily METs were calculated by summing up dura-tion, frequency, and relevant MET level per week in school and leisure time for all physical activities.36METs per hour
were calculated, in addition to daily du-ration (in minutes) of time in physical activity above 3 METs (TAA3M), which equals a moderate to high intensity level.28,29
Data Analysis and Statistics
Differences in prevalence of (1) Beigh-ton tests and BrighBeigh-ton signs with re-spect to gender and (2) musculoskele-tal pain (arthralgia) and injuries (dislocation/subluxation) with respect to ⱖGJH4/⬍GJH4, ⱖGJH5/⬍GJH5, ⱖGJH6/⬍GJH6, and BJHS/non-BJHS were tested with a2test. Differences
in motor competence and PAL for each
of the 4 GJH groups were tested in a general linear regression model. De-pendent factors were motor compe-tence tests and parameters on PAL (1 at a time), fixed factors were the 4 GJH groups (1 at a time) and gender, and covariates were age and calculated BMI (weight in kg/height in m2). The
correlation between Beighton scores and motor competence and PAL, re-spectively, was tested by Spearman’s correlation coefficient. Selected signif-icance level in all analyses wasPⱕ.05. SPSS 15.0 (SPSS Inc, Chicago, IL) was used for the calculations.
RESULTS
The cohort consisted of 46% (160) girls and 54% (189) boys (mean age: 8.40 years; SD: 0.52 years), with no differ-ence between boys and girls in demo-graphic variables. In all, 101 (29%) of the children fulfilled the criteria for ⱖGJH4, 65 (19%) forⱖGJH5, and 33 (10%) forⱖGJH6 (Table 2). A total of 31 (9%) fulfilled the criteria for BJHS, the 2 dominant criteria being GJH, either as a major or a minor criterion, and the presence of a hypermobile first-degree relative (Table 3). Among those with BJHS, 6 (19%) met theⱖGJH5 cri-teria for GJH and 11 (35%) reported musculoskeletal pain.
There was no difference between gen-ders in the prevalence of criteria for
GJH and BJHS, but girls had a higher prevalence than boys in a few tests (first right finger apposition,P⫽.039; forward bending, P ⫽ .005; disloca-tion/subluxation, P ⫽ .038; Tables 2 and 3). There was no difference be-tween children with and without GJH (no matter the cutoff level) regarding musculoskeletal pain and injuries (ⱖGJH4,P⫽.510,P⫽.720; ⱖGJH5, P⫽.912,P⫽.875;ⱖGJH6,P⫽.424, P⫽.254). The frequency of musculo-skeletal pain and injuries did not cor-relate with the level of GJH.
Static balance seemed to be better in children with ⱖGJH5 (P ⫽ .04) and ⱖGJH6 (nonsignificant), and so were the speed and reaction tests (ⱖGJH5, P⫽.007;ⱖGJH6P⫽.05; Table 4), with a significant gender and age effect. There was a significant negative corre-lation between the Beighton score and the speed and reaction test (P⫽.006, rs⫽ ⫺0.147; ie, the higher the
Beigh-ton score, the better the perfor-mance). There was no correlation be-tween the various parameters and the agility test, except for a negative corre-lation to BMI. The BJHS group did not perform worse than the non-BJHS group in any of the motor competence tests.
There was no significant effect of any of the GJH groups in the parameters of
TABLE 2 Prevalence of Positive Beighton Scores, GJH With a Beighton Score ofⱖ4,ⱖ5, andⱖ6 Positive Tests of 9, Analyzed for Boys and Girls and for the Total Group (Caucasian Ethnicity)
Beighton Scores (1–9) Boys (n⫽189),n(%) Girls (n⫽160),n(%) Total (n⫽349),n(%)
1. First finger apposition, right 46 (24.3)a 55 (34.4)a 101 (28.9)
2. First finger apposition, left 50 (26.5) 55 (34.4) 105 (30.1)
3. Fifth finger dorsiflexion, right 87 (46.0) 60 (37.5) 147 (42.1)
4. Fifth finger dorsiflexion, left 80 (42.3) 58 (36.3) 138 (39.5)
5. Elbow extension, right 66 (34.9) 55 (34.4) 121 (34.7)
6. Elbow extension, left 68 (36.0) 56 (35.0) 124 (35.5)
7. Knee extension, right 28 (14.8) 26 (16.3) 54 (15.5)
8. Knee extension, left 25 (13.2) 25 (15.6) 50 (14.3)
9. Forward bending 6 (3.2)a 17 (10.6)a 23 (6.6)
ⱖGJH4 48 (25.4) 53 (33.1) 101 (28.9)
ⱖGJH5 31 (16.4) 34 (21.3) 65 (18.6)
ⱖGJH6 18 (9.5) 15 (9.4) 33 (9.5)
aSignificant difference between genders.
PAL (Table 4), and there was no corre-lation between number of positive Beighton tests and PAL. The recom-mended PAL of a minimum 60 minutes above 3 METs per day was not passed by 34.9% of the children (data not shown).
DISCUSSION
The 10% prevalence of ⱖGJH6 is in agreement with a Finnish study of chil-dren at the same age10but lower than
results from similar-aged children in a Swedish study, in which the preva-lence was 16% for boys and 22% for girls.12In contrast to both studies, we
did not find gender differences in many of the tests. The Swedish study, having a total prevalence of ⱖGJH4 equal to 42%, ofⱖGJH5 to 23%, and of ⱖGJH6 to 18%, suggested the same GJH cutoff point for both genders at the age of 8 years but a higher cutoff
level for girls at 12 years of age, be-cause the divergence in Beighton scores between genders by that age became clearer.12
The prevalence of musculoskeletal pain and injuries among hypermobile children at 8 years of age, no matter the cutoff level, is supported by other cross-sectional studies of children.10,37
Characteristics as chronic fatigue syn-drome have also rarely been found be-low the age of 10 to 12 years, although GJH was found at an earlier age38;
how-ever, a 4-year follow-up study found ⱖGJH6 to be an independent predictor for pain recurrence,15,39 indicating
musculoskeletal pain to develop over time and possibly after 12 to 14 years of age, when havingⱖGJH5 orⱖGJH6 as a child. This means that pain and/or injuries had not yet become a problem in the 8-year-old children in our study.
competence tests, which is in contrast to many previous studies showing significant neuromuscular and motor development dysfunctions,21,24,40
ex-plained by a poor proprioception seen in adults as well as in children (8 –15 years) with BJHS and GJH5,41–44but this
issue has not been studied well in chil-dren. Generally, in those studies, highly selected populations (patients who were referred from pediatric and rheumatology clinics), presumably with several other comorbidities, have been examined, besides the use of dif-ferent methods for testing motor com-petence21,45; however, we do not know
whether a poor motor competence and/or musculoskeletal pain will de-velop in the children with GJH in this study, when the physical demands dur-ing the years of growth are increas-ing.46,47 The relative small number of
children withⱖGJH6 may be the rea-son that static balance was not in-creased also inⱖGJH6 versus⬍GJH6.
A perfect motor competence in GJH may also be 1 of the reasons for being selected into elite sports, such as bal-let, dancing, gymnastics, and swim-ming with especially high demands of flexibility.48–50In fact, in these sports,
an increased prevalence of hypermo-bility has been found in most of the joints, indicating a general hypermobil-ity, rather than a training/stretching ef-fect only in the trained joints. A nega-tive consequence among individuals
Brighton Criteria (1–10) Boys
(n⫽189),n(%)
Girls (n⫽160),n(%)
Total (n⫽349),n(%)
Major
1.ⱖGJH4 48 (25.4) 53 (33.1) 101 (28.9)
2. Arthralgia inⱖ4 joints for⬎3 mo 1 (0.5) 5 (3.1) 6 (1.7)
Minor
3. Skin signs 17 (9.0) 10 (6.3) 27 (7.7)
4. Eye signs 19 (10.1) 21 (13.1) 40 (11.5)
5. Marfanoid habitus 11 (5.8) 10 (6.3) 21 (6.0)
6. Beighton score between 1 and 3 99 (52.4) 70 (43.8) 169 (48.4)
7. Arthralgia in 1–3 joints 16 (8.5) 12 (7.5) 28 (8.0)
8. Dislocation/subluxation 3 (1.6)a 9 (5.7)a 12 (3.4)
9. Soft tissue rheumatism 0 (0.0) 0 (0.0) 0 (0.0)
10. Varicose veins, hernia, prolapse 3 (1.6) 2 (1.3) 5 (1.4)
Prevalence of a first-degree relative 60 (31.7) 43 (26.9) 103 (29.5)
BJHS 17 (9.0) 14 (8.8) 31 (8.9)
aSignificant difference between genders.
TABLE 4 Motor Competence and Self-reported PAL Within the GJH Groups of Children, for Caucasian Ethnicity
Parameter 4 GJH Groups Covering All Children (n⫽349), Mean (SD)
⬍GJH4 ⱖGJH4 ⬍GJH5 ⱖGJH5 ⬍GJH6 ⱖGJH6 Non-BJHS BJHS
Motor competence
Agility, No. of quadrants 18.9 (3.2)b; 19.5 (3.9) 18.9 (3.2)b; 19.8 (4.2) 19.0 (3.3)b; 19.8 (4.1) 19.0 (3.3)b; 19.5 (3.8)
Static balance, s 4.8 (2.9)c4.9 (2.8) 4.7 (2.8)a,c5.4 (3.2)a 4.7 (2.8)c5.5 (3.3) 4.9 (2.9)c4.3 (2.0)
Speed and reaction, cm 25.6 (5.3)c,d 24.9 (5.7) 25.8 (5.7)a,c,d 23.8 (3.6)a 25.6 (5.6)a,c,d 23.6 (4.1)a 25.3 (5.4)c,d 25.9 (6.1)
PAL
Total METs/d 37.51 (1.51) 37.58 (1.73) 37.50 (1.49) 37.67 (1.89) 37.49 (1.49) 37.92 (2.21) 37.50 (1.49) 37.92 (2.23)
PAL, METs/h 1.56 (0.06) 1.57 (0.07) 1.56 (0.06) 1.57 (0.08) 1.56 (0.06) 1.58 (0.09) 1.56 (0.06) 1.58 (0.09)
TAA3M/d, h 1.32 (0.59) 1.29 (0.62) 1.32 (0.59) 1.27 (0.65) 1.31 (0.59) 1.32 (0.67) 1.30 (0.60) 1.40 (0.62)
aSignificant difference as a result of GJH group.
with GJH in elite sports, though, was a higher frequency of injuries developed over time.18,51
Presence of GJH and BJHS did not in-fluence PAL (mean number of METs per hour) negatively at the age of 8 years, which is supported by a Finish cross-sectional study of 10- to 12-year-old children with ⱖGJH6.10 In contrast,
other studies found that 12-year-old children withⱖGJH4 were less active in sport activities than ⬍GJH437 and
that maximum exercise capacity was decreased in children with symptom-atic ⱖGJH5, because of decondition-ing24; however, this was attributable to
a highly selected population with strict inclusion criteria for children with ⱖGJH5, such as exercise-induced pain and exercise intolerance. An additional reason for the difference may be the age.
Although a large part of this popula-tion, as much as one third, did not pass the internationally recommended TAA3M, as also found in other studies of children,52 TAA3M was not
influ-enced by the presence of ⱖGJH4, ⱖGJH5,ⱖGJH6, or BJHS.
The weakness of this study is the cross-sectional nature of the study, which makes it difficult to evaluate the effect of GJH and BJHS in relation to a possible development of musculoskel-etal complaints, reduced motor com-petence, and/or physical activity. The strength of this study is the relatively high positive response rate, 79.4%, and the combination of clinical measures
of joint hypermobility, motor compe-tence, and physical activity. This co-hort, which is selected from a suburb of 1 of the midsize Danish municipali-ties, is assumed to be representative of a normal Danish child population. The clinical and motor competence tests were conducted with reproduc-ible methods and with examiners who were mutually blinded to each other’s test results,31,32 reducing the risk for
bias. Furthermore, the motor compe-tence tests have shown an acceptable face validity32 and the questions on
physical activity a high validity in chil-dren in relation to calculated energy expenditure.36The BJHS criteria have
never been tested for validity, and re-producibility has been measured only in adults, making the prevalence of BJHS in children to be interpreted with caution. The same may be argued for the prevalence of hypermobility in the first-degree relative (parents and siblings), because this information is self-reported.
The agility and static balance tests may have been too advanced for children at this age, which was also confirmed by the significant age effect32; however,
these motor competence tests were reproducible, simple, and quick to use in a large population and required no advanced instruments. Besides, they were valid and comparable with data from other studies of the same-aged children.33
This questionnaire was valid36;
how-ever, level and type of physical activity
are known to vary during seasons, and because we performed 2 rounds with 3 months in between, we cannot exclude this possibility of bias. Furthermore, self-reported PAL for children may es-pecially be underreported, because much child activity is impulsive and un-organized and may be difficult to re-member for children53–55; however,
this potential bias is assumed to influ-ence all groups equally.
CONCLUSIONS
GJH did not affect PAL, musculoskeletal pain, and injuries negatively, and chil-dren with BJHS did not perform worse than those without BJHS. Children with ⱖGJH5 as well as those with ⱖGJH6 performed even better in physical tests for motor competence, showing no negative effects of GJH on the mus-culoskeletal system by the age of 8 years. It is recommended that poten-tial negative influence of daily life ac-tivities on the musculoskeletal system be investigated in individuals with GJH in future longitudinal studies.
ACKNOWLEDGMENTS
This study was supported by the National Research Fund for Health and Disease, the Research Founda-tion of the Danish Physiotherapy As-sociation, the National Health Ser-vice Research Fund for Promotion of Research in Physiotherapy, Britta Holle’s Foundation, and sawmill owner Jeppe Juhl and his wife Ovita Juhl’s Foundation.
REFERENCES
1. Child AH. Joint hypermobility syndrome:
inher-ited disorder of collagen synthesis.J Rheuma-tol.1986;13(2):239 –243
2. Hakim AJ, Cherkas LF, Grahame R, Spector TD, MacGregor AJ. The genetic epidemiology of
joint hypermobility: a population study of fe-male twins. Arthritis Rheum.2004;50(8):
2640 –2644
3. Remvig L, Jensen DV, Ward RC. Epidemiology of
general joint hypermobility and basis for the
proposed criteria for benign joint
hypermobil-ity syndrome: review of the literature.J Rheu-matol.2007;34(4):804 – 809
4. Schalkwijk J, Zweers MC, Steijlen PM, et al. A recessive form of the Ehlers-Danlos syndrome
caused by tenascin-X deficiency.N Engl J Med. 2001;345(16):1167–1175
5. Zweers MC, Kucharekova M, Schalkwijk J. Tenascin-X: a candidate gene for benign joint
hypermobility syndrome and hypermobility
type Ehlers-Danlos syndrome?Ann Rheum Dis.
2005;64(3):504 –505
6. Beighton P, Solomon L, Soskolne CL. Articular
mobility in an African population.Ann Rheum Dis.1973;32(5):413– 418
7. Remvig L, Jensen DV, Ward RC. Are diagnostic criteria for general joint hypermobility and
be-nign joint hypermobility syndrome based on re-producible and valid tests? A review of the
liter-ature.J Rheumatol.2007;34(4):798–803
J Rheumatol.2000;27(7):1777–1779
9. Beighton P, De Paepe A, Steinmann B, Tsi-pouras P, Wenstrup RJ. Ehlers-Danlos syndromes: revised nosology, Villefranche, 1997. Ehlers-Danlos National Foundation (USA) and Ehlers-Danlos Support Group (UK). Am J Med Genet.1998;77(1):31–37
10. Mikkelsson M, Salminen JJ, Kautiainen H. Joint hypermobility is not a contributing factor to musculoskeletal pain in pre-adolescents. J Rheumatol.1996;23(11):1963–1967
11. Que´rol JR, Duran J, Subiros R, Pifferer J, Go-mez J. Articular laxity as a factor in locomotor apparatus changes (new 1971 study) [in French].Rhumatologie.1972;24(5):179 –191
12. Jansson A, Saartok T, Werner S, Renstrom P. General joint laxity in 1845 Swedish school children of different ages: age- and gender-specific distributions.Acta Paediatr.2004; 93(9):1202–1206
13. Gyldenkerne B, Iversen K, Roegind H, Fastrup D, Hall K, Remvig L. Prevalence of general hy-permobility in 12–13-year-old school children and impact of an intervention against injury and pain incidence.Adv Physiother.2006; PrEview(November):1– 6
14. Harreby M, Nygaard B, Jessen T, et al. Risk factors for low back pain in a cohort of 1389 Danish school children: an epidemiologic study.Eur Spine J.1999;8(6):444 – 450
15. El-Metwally A, Salminen JJ, Auvinen A, Kautiainen H, Mikkelsson M. Prognosis of non-specific musculoskeletal pain in preadolescents: a prospective 4-year follow-up study till ado-lescence.Pain.2004;110(3):550 –559
16. Acasuso Díaz M, Collantes Estevez E, Sanchez Guijo P. Joint hyperlaxity and musculoliga-mentous lesions: study of a population of ho-mogeneous age, sex and physical exertion. Br J Rheumatol.1993;32(2):120 –122
17. Hudson N, Fitzcharles MA, Cohen M, Starr MR, Esdaile JM. The association of soft-tissue rheu-matism and hypermobility.Br J Rheumatol. 1998;37(4):382–386
18. Smith R, Damodaran AK, Swaminathan S, Campbell R, Barnsley L. Hypermobility and sports injuries in junior netball players.Br J Sports Med.2005;39(9):628 – 631
19. Bridges AJ, Smith E, Reid J. Joint hypermobility in adults referred to rheumatology clinics. Ann Rheum Dis.1992;51(6):793–796
20. Ruperto N, Malattia C, Bartoli M, et al. Func-tional ability and physical and psychosocial well-being of hypermobile schoolchildren.Clin Exp Rheumatol.2004;22(4):495– 498
21. Adib N, Davies K, Grahame R, Woo P, Murray KJ. Joint hypermobility syndrome in childhood: a
22. Bulbena A, Duro JC, Porta M, Faus S, Vallescar
R, Martin-Santos R. Clinical assessment of hy-permobility of joints: assembling criteria. J Rheumatol.1992;19(1):115–122
23. Engelbert RH, Kooijmans FT, van Riet AM, Feitsma TM, Uiterwaal CS, Helders PJ. The re-lationship between generalized joint
hyper-mobility and motor development.Pediatr Phys Ther.2005;17(4):258 –263
24. Engelbert RH, van Bergen M, Henneken T, Helders PJ, Takken T. Exercise tolerance in children and adolescents with
musculoskele-tal pain in joint hypermobility and joint hypo-mobility syndrome.Pediatrics.2006;118(3). Available at: www.pediatrics.org/cgi/content/ full/118/3/e690
25. Ekelund U, Sardinha LB, Anderssen SA, et al. Associations between objectively assessed
physical activity and indicators of body fat-ness in 9- to 10-y-old European children: a population-based study from 4 distinct re-gions in Europe (the European Youth Heart Study).Am J Clin Nutr.2004;80(3):584 –590
26. Reed JA, Metzker A, Phillips DA. Relationships between physical activity and motor skills in
middle school children.Percept Mot Skills. 2004;99(2):483– 494
27. Andersen LB, Harro M, Sardinha LB, et al. Phys-ical activity and clustered cardiovascular risk in children: a cross-sectional study (The Euro-pean Youth Heart Study). Lancet.2006;
368(9532):299 –304
28. Norden. Physical activity. In: Nordic Council of Ministers, ed.Nordic Nutrition Recommenda-tion, NNR 2204: Integrating Nutrition and Phys-ical Activity. 4th ed. Copenhagen, Denmark: Nordic Council of Ministers; 2004:139 –151
29. Strong WB, Malina RM, Blimkie CJ, et al. Evi-dence based physical activity for school-age youth.J Pediatr.2005;146(6):732–737
30. Vollmann J, Winau R. Informed consent in hu-man experimentation before the Nuremberg code.BMJ.1996;313(7070):1445–1449
31. Juul-Kristensen B, Rogind H, Jensen DV, Rem-vig L. Inter-examiner reproducibility of tests and criteria for generalized joint hypermobil-ity and benign joint hypermobilhypermobil-ity syndrome. Rheumatology (Oxford). 2007;46(12): 1835–1841
32. Johnson L, Nelson B.Practical Measurements
for Evaluation in Physical Education. New York, NY: Macmillan; 1986
33. Gofin R, Donchin M, Schulrof B. Motor ability: protective or risk for school injuries?Accid Anal Prev.2004;36(1):43– 48
34. Ainsworth BE, Haskell WL, Whitt MC, et al.
Com-pendium of physical activities: an update of
35. Craig CL, Marshall AL, Sjostrom M, et al. Inter-national physical activity questionnaire: 12-country reliability and validity.Med Sci Sports Exerc.2003;35(8):1381–1395
36. Anderssen SA, Solberg M.Development of Methods for Measuring Physical Activity: De-velopment and Validation of a Questionnaire for Children[in Norwegian]. Oslo, Norway: NIH, Institute of Sports Sciences; 2005:2–20
37. Qvindesland A, Jonsson H. Articular hypermo-bility in Icelandic 12-year-olds.Rheumatology (Oxford).1999;38(10):1014 –1016
38. Barron DF, Cohen BA, Geraghty MT, Violand R, Rowe PC. Joint hypermobility is more common in children with chronic fatigue syndrome than in healthy controls.J Pediatr.2002; 141(3):421– 425
39. El-Metwally A, Salminen JJ, Auvinen A, Kauti-ainen H, Mikkelsson M. Lower limb pain in a preadolescent population: prognosis and risk factors for chronicity—a prospective 1- and 4-year follow-up study. Pediatrics.2005; 116(3):673– 681
40. Kirby A, Davies R. Developmental coordination disorder and joint hypermobility syndrome: overlapping disorders? Implications for re-search and clinical practice.Child Care Health Dev.2007;33(5):513–519
41. Mallik AK, Ferrell WR, McDonald AG, Sturrock RD. Impaired proprioceptive acuity at the proximal interphalangeal joint in patients with the hypermobility syndrome.Br J Rheumatol. 1994;33(7):631– 637
42. Hall MG, Ferrell WR, Sturrock RD, Hamblen DL, Baxendale RH. The effect of the hypermobility syndrome on knee joint proprioception.Br J Rheumatol.1995;34(2):121–125
43. Fatoye F, Palmer S, Macmillan F, Rowe P, van der Linden M. Proprioception and muscle torque deficits in children with hypermobility syndrome. Rheumatology (Oxford).2009; 48(2):152–157
44. Fatoye FA, Palmer ST, Macmillan F, Rowe PJ, van der Linden ML. Repeatability of joint pro-prioception and muscle torque assessment in healthy children and in children diagnosed with hypermobility syndrome. Musculoskele-tal Care.2008;6(2):108 –123
45. Engelbert RH, Bank RA, Sakkers RJ, Helders PJ, Beemer FA, Uiterwaal CS. Pediatric general-ized joint hypermobility with and without mus-culoskeletal complaints: a localized or sys-temic disorder? Pediatrics.2003;111(3). Available at: www.pediatrics.org/cgi/content/ full/111/3/e248
46. Bird HA. Joint hypermobility in children. Rheu-matology (Oxford).2005;44(6):703–704
in childhood.Rheumatology (Oxford).2001; 40(5):489 – 491
48. Gannon LM, Bird HA. The quantification of joint laxity in dancers and gymnasts.J Sports Sci. 1999;17(9):743–750
49. Grahame R, Jenkins JM. Joint hypermobility: as-set or liability? A study of joint mobility in ballet dancers.Ann Rheum Dis.1972;31(2):109–111
50. McCormack M, Briggs J, Hakim A, Gra-hame R. Joint laxity and the benign joint hypermobility syndrome in student and
professional ballet dancers.J Rheumatol. 2004;31(1):173–178
51. Klemp P, Stevens JE, Isaacs S. A hypermobility study in ballet dancers.J Rheumatol.1984; 11(5):692– 696
52. Wedderkopp N, Froberg K, Hansen HS, Andersen LB. Secular trends in physical fitness and obesity in Danish 9-year-old girls and boys: Odense School Child Study and Danish substudy of the
European Youth Heart Study.Scand J Med Sci Sports.2004;14(3):150–155
53. Pate RR, Freedson PS, Sallis JF, et al. Compli-ance with physical activity guidelines: preva-lence in a population of children and youth. Ann Epidemiol.2002;12(5):303–308
54. Sirard JR, Pate RR. Physical activity assess-ment in children and adolescents.Sports Med. 2001;31(6):439 – 454
55. Welk GJ, Corbin CB, Dale D. Measurement is-sues in the assessment of physical activity in
children.Res Q Exerc Sport.2000;71(2 suppl): S59 –S73
DOI: 10.1542/peds.2009-0294 originally published online October 12, 2009;
2009;124;1380
Pediatrics
Jensen, Henrik Røgind and Lars Remvig
Birgit Juul-Kristensen, Jens Halkjær Kristensen, Britt Frausing, Dorte Vendelboe
Services
Updated Information &
http://pediatrics.aappublications.org/content/124/5/1380 including high resolution figures, can be found at:
References
http://pediatrics.aappublications.org/content/124/5/1380#BIBL This article cites 49 articles, 11 of which you can access for free at:
Subspecialty Collections
skeletal_disorders_sub
http://www.aappublications.org/cgi/collection/rheumatology:musculo
Rheumatology/Musculoskeletal Disorders
following collection(s):
This article, along with others on similar topics, appears in the
Permissions & Licensing
http://www.aappublications.org/site/misc/Permissions.xhtml in its entirety can be found online at:
Information about reproducing this article in parts (figures, tables) or
Reprints
DOI: 10.1542/peds.2009-0294 originally published online October 12, 2009;
2009;124;1380
Pediatrics
Jensen, Henrik Røgind and Lars Remvig
Birgit Juul-Kristensen, Jens Halkjær Kristensen, Britt Frausing, Dorte Vendelboe
Generalized Joint Hypermobility
Motor Competence and Physical Activity in 8-Year-Old School Children With
http://pediatrics.aappublications.org/content/124/5/1380
located on the World Wide Web at:
The online version of this article, along with updated information and services, is
by the American Academy of Pediatrics. All rights reserved. Print ISSN: 1073-0397.
