Abstract
Although diagnostic criteria for generalised ligamentous laxity (hypermobility) in children are widely used, they may have limited validity as robust descriptive epidemiology of this condition is lacking. We used a large population-based birth cohort to describe the point prevalence and pattern of hypermobility in children aged 14 years.
We performed a cross-sectional analysis of the Avon Longitudinal Study of Parents and Children (ALSPAC). Hyperrmobility was measured at aged 14 years using the Beighton scoring system. Objective measures of physical activity were collected by accelerometry. Data were collected on other variables including puberty and socio-economic status. Simple prevalence was calculated. Chi-squared tests and logistic regression were used to assess associations between variables and hypermobility.
6022 children were evaluated. Using a cut-off of ≥4, the prevalence of hypermobilty in girls and boys aged 13.8 years was 27.5% and 10.6% respectively. 45% of girls and 29% of boys had hypermobile fingers. There was a suggestion of a positive association between hypermobility in girls and variables including physical activity, body mass index and maternal education. No associations were seen in boys.
We have shown that the prevalence of hypermobility in UK children is high; possibly suggesting that the Beighton cut off is too low or that the score is not appropriate in a developing musculoskeletal system. These results give a platform to evaluate the relationships between the Beighton criteria and key clinical features (including pain), thereby testing the clinical validity of this score in the childhood population.
Keywords: Hypermobility, Children, Epidemiology, Cohort study, Pediatric Rheumatology
Introduction
Joint hypermobility results from ligamentous laxity[1], and may occur in individuals with a primary genetic disorder affecting the connective tissue matrix proteins (conditions such as osteogenesis imperfecta or Marfan syndrome), or other syndromes including Trisomy 21, bony dysplasias or velocardiofacial syndrome. In the majority of instances hypermobility exists as an isolated finding (labelled as generalised joint laxity for the rest of this paper), but may by labelled as ‘Hypermobility Syndrome’ when associated with musculoskeletal symptoms such as pain and ‘clicking joints’, and known genetic causes are absent. However, the extent to which generalised joint laxity is associated with significant clinical sequelae, including joint pain, is unclear, since previous reports linking generalised joint laxity with joint pain in school children suffer from problems with sample size, methods of assessing hypermobility and methods of assessing pain. Despite this, the suggestion from school-based populations is the prevalence of pain among those children with generalised joint laxity ranges from 30% [2] to 55% [3]. An alternative view, namely that generalised joint laxity as generally defined represents part of the normal population variance and that any co-association with joint pain is spurious [4], is also plausible. However, current understanding of the prevalence and descriptive epidemiology of generalised joint laxity in childhood is limited, making it difficult to draw clear conclusions about causal pathways.
The reported prevalence of generalised joint laxity in children aged 6-15 years varies between 8.8%[5] to 64.6%[6]. One explanation for the wide range of these prevalence estimates of childhood generalised joint laxity is that previous studies have been performed on selected populations [5-12]. For example, some studies used preschool children aged 4-7[6], others used children from a single school ranging from aged 5 to 17 with no explanation of recruitment[5,12] and sample sizes of previous studies were generally small, ranging from 364[9] to 2432[5] children, all reflecting the fact that true population-based studies have not previously been undertaken.
Another explanation for these wide estimates of prevalence relates to differences in definitions. All of these studies used the method of examining and scoring for hypermobility developed by Beighton[13]. The Beighton Score was devised in South Africa and based on 1083 Tswana Africans (adults and children), adapting a score previously described by Carter in 1960[14]. The Beighton score has subsequently been used internationally to define generalised joint laxity in all populations and all age groups. Most of the prevalence studies available used different cut-offs ranging from three hypermobile joints or more, to six or more out of nine (both thumbs, both little fingers, both elbows, both knees and the trunk – see Figure 1), and some only assessed the dominant side. The most usual choice of cut-off was four or more hypermobile joints.
Figure 1.
The Beighton score. Permission was obtained from Arthritis Research-UK to use this image, available from the AR-UK website: http://www.arthritisresearchuk.org/arthritis_information/arthritis_types__symptoms/joint_hypermobility.aspx#non
Although there is some information about the descriptive epidemiology of generalised joint laxity, studies were largely performed in selected groups, making it difficult to draw definitive conclusions. For example, generalised joint laxity is thought to be more common in girls compared to boys[5,9,15]. There is also a suggestion that ethnic background can influence hypermobility[16,17], and that generalised joint laxity is more common in ballet-dancers[18], musicians[19], gymnasts[20] and swimmers[21]. Contradictory results from some small studies report that greater degrees of joint laxity is seen in either the dominant[22] or non-dominant limb[23]. There is consistent reporting of lack of association with body weight[8,24,25]. It is also widely believed that younger children are more flexible than adolescents[26], but there is very little literature to support this. For example, one rigorous population-based study from Sweden[15] investigated 1845 children aged 9, 12 or 15 from 48 geographically randomly selected schools, and reported that at all ages girls had a higher degree of generalised joint laxity as assessed by the modified Beighton’s criteria. However, joint laxity in boys decreased with increasing age, whereas girls had the highest degree of general joint laxity at the age of 15 years. Similarly, a study on high-school basket ball players[27] showed that after the onset of puberty, females demonstrated greater joint laxity than males. Conversely, other studies report no decline in generalised joint laxity with age[28].
Therefore, to provide a basis for exploring relationships between generalised joint laxity and clinical sequelae, we aimed to define the prevalence and descriptive epidemiology of this characteristic. We performed a cross sectional analysis of the Avon Longitudinal Study of Parents and Children (ALSPAC), based on Beighton scores collected at the age 14 research clinic.
Methods
Study design
Cross-sectional analysis of a large population-based cohort study.
Study population
ALSPAC is a geographically based UK cohort that recruited pregnant women residing in Avon (South-west England) with an expected date of delivery between April 1st 1991 and December 31st 1992[29]. A total of 14,541 pregnancies were enrolled with 14,062 children born (see www.alspac.bris.ac.uk for more information). Of these births, 13,988 children were alive at 12 months. This study is based on 6022 children who attended the aged 14 research clinic and had hypermobility data collected. Compared to the complete cohort, those taking part in this generalised joint laxity study were more likely to have mothers educated to degree level or higher (17.1% versus 9.4% of mothers of children not included in this analysis, P<0.001). Ethical approval was obtained from the ALSPAC Law and Ethics committee, and the Local Research Ethics Committees. Parental consent and child’s assent was obtained for all measurements made. Funders and study sponsor had no role in study design, collection, analysis or interpretation of data, the writing of this article, nor the decision to submit it for publication. All researchers had full access to the data and were independent from funders and sponsors.
Measurement of generalised joint laxity
See Figure 1. Generalised joint laxity was assessed by trained measurers in the aged 14 research clinic using the modified Beighton nine-point scoring system as already described[13]. Each joint was assessed separately and scored as hypermobile if it exceeded 90° of extension at the little finger metacarlpophalangeal joint, the thumb could be opposed to the wrist, or elbows and knees extended more than 10°. The trunk was considered hypermobile if both palms could be put flat on the floor with the knees straight. Scores were recorded for the individual joints as well as a total out of nine. A cut-off of ≥4 hypermobile joints was used, based on the most common cut-off cited in the literature[6-9]. In addition, a more extreme phenotype was selected with a cut-off of ≥6 hypermobile joints (reported to be the median number in children with any hypermobile joints[4]) to allow simple sensitivity-type analyses to confirm any associations found.
Other measures
Anthropometrics
At the research clinic at aged 14 years, height was measured to the last complete millimetre using a Harpenden stadiometer. Weight was measured to the nearest 50g using a Tanita Body Fat Analyzer (model TBF 305). BMI was calculated as weight (in kilograms) divided by height squared (in metres), and categorised into underweight (<18.5), recommended weight (18.5 to 24.9), overweight (25 to 29.9) or obese (greater than 30) based on standard definitions.
Physical activity
Physical activity was measured objectively using the MTI Actigraph (model WAM 7164, Manufacturing Technology Incorporated [MTI], Fort Walton Beach, FL) when the children were 14 years old for up to 7 days. For the purposes of this study, physical activity was categorised into those children who did 60 minutes or more of moderate and vigorous physical activity (MVPA) per day, or not. This categorisation has been previously described in detail[30], but briefly a cut-point of >3600 counts/minute was used after calibration performed in a subgroup of 260 children in whom these count frequencies were associated with oxygen consumptions of greater than 4 METS (the ratio of the associated metabolic rate for the specific activity divided by the resting metabolic rate).
Socio-economic status
Mothers highest educational qualifications were also assessed at 32 weeks gestation and were coded 1 to 5 where 1 referred to those with no formal qualifications or the lowest level of school educational qualification, 2 as vocational qualifications, 3 as O-levels (generally gained at school by aged 16 years), 4 as A levels (generally gained at school by aged 18 years), and level 5 refers to university degrees. Other measures of socio-economic status such as paternal education, maternal and paternal social class and housing tenure where not used in this analysis as they gave similar results to maternal education alone, as shown in a previous study on this cohort[31].
Others
Age was calculated from date of birth. Gender was obtained from birth notifications. Hand dominance, or handedness was collated from data collected at research clinics the children attended at aged 7, 9 and 11 years as this is considered a stable trait. Puberty was assessed at aged 13 using self-completion Tanner staging based on pubic hair distribution. The mother’s, partner’s and grandparent’s race and ethnic group was recorded by the mother on self-reported questionnaires sent out at approximately 32 weeks gestation, and was categorised as white or non-white.
Statistical analysis
All statistics were carried out by KD using Stata 11. Simple percentages were calculated for the point prevalence and pattern of generalised joint laxity. Chi-squared tests were used to assess associations between binary variables and the presence or absence of generalised joint laxity. Logistic regression was used to assess trend in associations between categorical variables and the presence or absence of generalised joint laxity. To assess strength of association, logistic regression was used to calculate Odds Ratios (ORs) for presence or absence of generalised joint laxity according to each of the variables. Multivariable logistic regression was used to assess independent associations. Interactions between gender and BMI were assessed using the likelihood ratio test.
Results
The prevalence of generalised joint laxity in this population of 6022 children aged 13.8 years was 19.2% based on a cut-off of ≥4 joints. Girls had a higher prevalence than boys (27.5% vs 10.6%, P<0.001). Using a more rigorous cut-off of ≥6, the prevalence was 4.2% (girls 7.0% and boys 1.3%, P<0.001).
The distribution of hypermobile joints in the whole population is shown in Table 1. The fingers were most likely to be hypermobile, followed by the thumbs. Knee, elbow or trunk hypermobility was seen in approximately 9%. However, in girls trunk hypermobility was more prevalent (15%) than elbow (13%) and knee (11%). In boys, thumb hypermobility was more prevalent (15%) than knee (7%), elbow (4%) or trunk. Trunk hypermobility in boys was unusual, with only 50 out of 2961 (1.7%) boys able to put both palms flat on the floor with the knees straight. Limiting our analysis to those children with hypermobility defined as ≥4 joints, 85% had hypermobile fingers (Table 2), 75% thumbs and 29% knees. Gender differences were seen, with 40% of hypermobile girls having a hypermobile trunk, and 31% hypermobile elbows. Conversely 21% of hypermobile boys had hypermobile elbows but only 4% a hypermobile trunk.
Table 1.
Table showing the point prevalence of hypermobility at each of the nine sites used in the modified Beighton’s criteria, based on the full population (n=6022) at aged 13.8 years (number of males = 2961, females=3061)
| Beighton site | Male (%) |
Female (%) |
All (%) | |
|---|---|---|---|---|
| Fingers | Left | 29.9 | 46.6 | 38.4 |
| Right | 28.5 | 43.0 | 35.9 | |
| Thumbs | Left | 16.4 | 34.2 | 25.4 |
| Right | 14.0 | 30.0 | 22.1 | |
| Elbows | Left | 4.8 | 13.1 | 9.0 |
| Right | 4.4 | 12.4 | 8.5 | |
| Knees | Left | 7.8 | 11.2 | 9.6 |
| Right | 7.1 | 11.0 | 9.1 | |
| Trunk | ~ | 1.7 | 15.1 | 8.5 |
Table 2.
Proportion of those children with hypermobility defined as ≥4 hypermobile joints (n=1156) who are hypermobile at each of the nine sites, hypermobile at fingers and thumbs, or hypermobile at fingers, thumbs and elbows.
| Beighton score >=4 | Males (%) n=314 |
Females (%) n=842 |
All (%) n=1156 |
|---|---|---|---|
| a. Fingers | 84.7 | 85.4 | 85.2 |
| b. Thumbs | 75.2 | 74.7 | 74.8 |
| c. Elbows | 20.7 | 31.0 | 28.2 |
| d. Knees | 28.7 | 28.6 | 28.6 |
| e. Trunk | 4.1 | 25.8 | 19.9 |
| Hands (a + b) | 66.6 | 65.9 | 66.1 |
| Upperlimbs (a + b + c) | 4.5 | 12.5 | 10.3 |
The basic descriptives and potential confounding variables of generalised joint laxity in this cohort are shown in Table 3. There was no age difference between those with and without generalised joint laxity (results not shown). No associations were seen for boys (Table 4). There was evidence of an interaction between BMI and gender (P<0.001), and so assessment of associations was carried out separately for boys and girls. In girls (Table 5), there was a positive association between BMI and presence of generalised joint laxity when using ≥4 as the definition, both unadjusted and after adjustment for all other variables (handedness, puberty, physical activity, ethnicity and maternal education): obese children were 2.7 times more likely to be hypermobile (OR 2.70, 95%CI 1.24 to 5.88) compared to underweight children. There was a suggestion of a similar direction of association when using a definition of ≥6, but only from underweight, through normal weight to overweight. Obesity was not associated with hypermobility of ≥6 joints, although this was based on only 69 girls. No other associations were seen using ≥4 as the definition of generalised joint laxity.
Table 3.
Basic descriptives of children with and without generalised joint laxity using different cut-offs of ≥4 and ≥6 hypermobile joints. Results are shown separately for boys and girls. P values for difference between those with and without generalised joint laxity were calculated using Ch-squared. Results in bold in shaded boxes are have P values <0.05
| Beighton score ≥4 | Beighton score ≥6 | Beighton score ≥4 | Beighton score ≥6 | ||||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
| No | Yes | No | Yes | No | Yes | No | Yes | ||||||
| n (%) | n (%) | P value |
n (%) | n (%) | P value |
n (%) | n (%) | P value |
n (%) | n (%) | P value |
||
| BOYS | GIRLS | ||||||||||||
| Handedness (n=2961) | 0.74 | 0.25 | Handedness (n=3061) | 0.91 | 0.76 | ||||||||
| Left | 372 (89.9) | 42 (10.1) | 411 (99.3) | 3 (0.7) | Left | 227 (72.8) | 85 (27.2) | 289 (92.6) | 23 (7.4) | ||||
| Right | 2275 (89.3) | 272 (10.7) | 2511 (98.6) | 36 (1.4) | Right | 1992 (72.5) | 757 (27.5) | 2559 (93.1) | 190 (6.9) | ||||
|
| |||||||||||||
| BMI (n=2961) | 0.53 | 0.96 | BMI (n=3061) | 0.01 | 0.87 | ||||||||
| Underweight | 1038 (89.9) | 116 (10.1) | 1141 (98.9) | 13 (1.1) | Underweight | 649 (74.6) | 221 (25.4) | 808 (92.9) | 62 (7.1) | ||||
| Ideal | 1363 (88.2) | 82 (11.8) | 1520 (98.4) | 25 (1.6) | Ideal | 1335 (72.5) | 507 (27.5) | 1716 (92.7) | 126 (7.3) | ||||
| Overweight | 206 (94.1) | 13 (5.9) | 219 (100.0) | 0 (0) | Overweight | 192 (68.6) | 88 (31.4) | 259 (92.5) | 21 (7.5) | ||||
| Obese | 40 (93.0) | 3 (7.0) | 42 (97.7) | 1 (2.3) | Obese | 43 (62.3) | 26 (37.7) | 65 (94.2) | 4 (5.8) | ||||
|
| |||||||||||||
| Tanner stage (n=1855) | 0.31 | 0.96 | Tanner stage (n=2163) | 0.34 | 0.55 | ||||||||
| I (pre-pubertal) | 207 (90.4) | 22 (9.6) | 226 (98.7) | 3 (1.3) | I (pre-pubertal) | 80 (72.7) | 30 (27.3) | 103 (93.6) | 7 (6.4) | ||||
| II | 389 (91.3) | 37 (8.7) | 420 (98.6) | 6 (1.4) | II | 183 (74.7) | 62 (25.3) | 224 (91.4) | 21 (8.6) | ||||
| III | 460 (89.7) | 53 (10.3) | 508 (99.0) | 5 (1.0) | III | 372 (76.2) | 116 (23.8) | 461 (94.5) | 27 (5.5) | ||||
| IV | 522 (89.1) | 64 (10.9) | 577 (98.5) | 9 (1.5) | IV | 605 (70.5) | 253 (29.5) | 788 (91.8) | 70 (8.2) | ||||
| V (post-pubertal) | 90 (89.1) | 11 (10.9) | 100 (99.0) | 1 (1.0) | V (post-pubertal) | 339 (73.4) | 123 (26.6) | 438 (94.8) | 24 (5.2) | ||||
|
| |||||||||||||
| Physical activity (n=1944) | 0.67 | 0.63 | Physical activity (n=2257) | 0.44 | 0.02 | ||||||||
| <60 minutes mod/vig | 1645 (89.4) | 196 (10.6) | 1814 (92.4) | 27 (7.6) | <60 minutes mod/vig | 1625 (73.4) | 588 (26.6) | 2066 (93.4) | 147 (6.6) | ||||
| <60 minutes mod/vig | 135 (88.2) | 18 (11.8) | 150 (90.0) | 3 (10.0) | <60 minutes mod/vig | 30 (68.2) | 14 (31.8) | 37 (84.1) | 7 (15.9) | ||||
|
| |||||||||||||
| Ethnicity (n=2699) | 0.5 | Ethnicity (n=2782) | 0.33 | 0.24 | |||||||||
| White | 2323 (89.5) | 273 (10.5) | 2560 (98.6) | 36 (1.4) | 0.20 | White | 1937 (72.3) | 742 (27.7) | 2495 (93.1) | 184 (6.9) | |||
| Non-white | 90 (87.4) | 13 (12.6) | 100 (97.1) | 3 (2.9) | Non-white | 79 (76.7) | 24 (23.3) | 99 (96.1) | 4 (3.9) | ||||
|
| |||||||||||||
| Maternal education (n=2747) | 0.37 | 0.92 | Maternal education (n=2812) | 0.63 | 0.01 | ||||||||
| 1 (low) | 302 (91.2) | 29 (8.8) | 328 (99.1) | 3 (0.9) | 1 (low) | 259 (73.2) | 95 (26.8) | 343 (96.9) | 11 (3.1) | ||||
| 2 | 213 (89.1) | 26 (10.9) | 233 (97.5) | 6 (2.5) | 2 | 164 (77.7) | 47 (22.3) | 203 (96.2) | 8 (3.8) | ||||
| 3 | 861 (88.4) | 113 (11.6) | 957 (98.3) | 17 (1.7) | 3 | 694 (70.5) | 291 (29.5) | 906 (92.0) | 79 (8.0) | ||||
| 4 | 680 (90.9) | 68 (9.1) | 744 (99.5) | 4 (0.5) | 4 | 571 (73.4) | 207 (26.6) | 725 (93.2) | 53 (6.8) | ||||
| 5 (high) | 403 (87.6) | 57 (12.4) | 451 (98.0) | 9 (2.0) | 5 (high) | 355 (72.0) | 138 (28.0) | 453 (91.9) | 40 (8.1) | ||||
Abbreviations: BMI body mass index; mod/vig moderate and/or vigorous physical activity
Table 4.
Odds ratios for presence of generalised joint laxity (defined as either ≥4 or ≥6 hypermobile joints) in boys, according to variables of interest. Results are shown unadjusted, and then adjusted for all other variables in the table. Because of small numbers, some analyses could not be performed (indicated by -). Results in bold in shaded boxes are have P values of <0.05
| Beighton score ≥4 | Beighton score ≥6 | |||
|---|---|---|---|---|
| Unadjusted ORs | Adjusted for all other variables in the table |
Unadjusted ORs | Adjusted for all other variables in the table |
|
| OR (95%CI) | OR (95%CI) | OR (95%CI) | OR (95%CI) | |
| Handedness | ||||
| Left | 1.0 | 1.0 | 1.0 | 1.0 |
| Right | 1.06 (0.75, 1.49) | 1.22 (0.69, 2.16) | 1.96 (0.60, 6.41) | 3.17 (0.42, 24.06) |
|
| ||||
| BMI | ||||
| Underweight | 1.0 | 1.0 | 1.0 | 1.0 |
| Ideal | 1.20 (0.93, 1.53) | 1.31 (0.88, 1.95) | 1.44 (0.74, 2.83) | 1.87 (0.70, 5.04) |
| Overweight | 0.57 (0.31, 1.02) | 0.36 (0.11, 1.18) | - | - |
| Obese | 0.67 (0.20, 2.20) | 1.57 (0.18, 13.33) | 2.09 (0.27, 16.4) | - |
| OR Test for trend | OR Test for trend | OR Test for trend | OR Test for trend | |
| 0.95 (0.79, 1.13) P=0.531 | 0.97 (0.72, 1.32) P=0.864 | 1.01 (0.63, 1.63) P=0.965 | 1.07 (0.52, 2.18) P=0.872 | |
|
| ||||
| Tanner stage | ||||
| I (pre-pubertal) | 1.0 | 1.0 | 1.0 | 1.0 |
| II | 0.90 (0.51, 1.56) | 0.94 (0.49, 1.79) | 1.08 (0.27, 4.34) | 0.92 (0.21, 3.94) |
| III | 1.08 (0.64, 1.83) | 0.73 (0.39, 1.40) | 0.74 (0.18, 3.13) | 0.51 (0.11, 2.32) |
| IV | 1.15 (0.69, 1.92) | 0.85 (0.46, 1.58) | 1.18 (0.32, 4.38) | 0.79 (0.20, 3.20) |
| V (post-pubertal) | 1.15 (0.54, 2.47) | 0.76 (0.28, 2.07) | 0.75 (0.08, 7.33) | 0.69 (0.07, 7.05) |
| OR Test for trend | OR Test for trend | OR Test for trend | OR Test for trend | |
| 1.07 (0.94, 1.23) P=0.312 | 0.96 (0.81, 1.14) P=0.654 | 1.01 (0.70, 1.45) P=0.965 | 0.94 (0.63, 1.41) P=0.774 | |
|
| ||||
| Physical activity | ||||
| <60 minutes mod/vig | 1.0 | 1.0 | 1.0 | 1.0 |
| >60 minutes mod/vig | 1.12 (0.67, 1.87) | 1.73 (0.93, 3.19) | 1.34 (0.40, 4.48) | 1.48 (0.33, 6.59) |
|
| ||||
| Ethnicity | ||||
| White | 1.0 | 1.0 | 1.0 | 1.0 |
| Non-white | 1.23 (0.68, 2.23) | 0.40 (0.05, 2.93) | 2.13 (0.64, 7.05) | - |
|
| ||||
| Maternal education | ||||
| 1 (low) | 1.0 | 1.0 | 1.0 | 1.0 |
| 2 | 1.25 (0.72, 2.18) | 0.97 (0.37, 2.52) | 2.77 (0.69, 11.2) | - |
| 3 | 1.34 (0.88, 2.06) | 1.21 (0.58, 2.51) | 1.91 (0.56, 6.57) | - |
| 4 | 1.02 (0.65, 1.62) | 0.73 (0.33, 1.58) | 0.58 (0.13, 2.60) | - |
| 5 (high) | 1.45 (0.90, 2.32) | 1.31 (0.61, 2.82) | 2.15 (0.58, 8.00) | - |
| OR Test for trend | OR Test for trend | OR Test for trend | OR Test for trend | |
| 1.04 (0.94, 1.15) P=0.433 | 1.02 (0.87, 1.20) P=0.778 | 0.98 (0.75, 1.28) P=0.889 | 1.30 (0.86, 1.98) P=0.219 | |
Abbreviations: BMI body mass index; mod/vig moderate and/or vigorous physical activity
Table 5.
Odds ratios for presence of generalised joint laxity (defined as either ≥4 or ≥6 hypermobile joints) in girls, according to variables of interest. Results are shown unadjusted, and then adjusted for all other variables in the table. Results in bold in shaded boxes are have P values of <0.05
| Beighton score ≥4 | Beighton score ≥6 | |||
|---|---|---|---|---|
| Unadjusted ORs | Adjusted for all other variables in the table |
Unadjusted ORs | Adjusted for all other variables in the table |
|
| OR (95%CI) | OR (95%CI) | OR (95%CI) | OR (95%CI) | |
| Handedness | ||||
| Left | 1.0 | 1.0 | 1.0 | 1.0 |
| Right | 1.02 (0.78, 1.32) | 0.94 (0.64, 1.40) | 0.93 (0.60, 1.46) | 0.77 (0.41, 1.46) |
|
| ||||
| BMI | ||||
| Underweight | 1.0 | 1.0 | 1.0 | 1.0 |
| Ideal | 1.12 (0.93, 1.34) | 1.36 (1.03, 1.80) | 0.96 (0.70, 1.32) | 1.38 (0.85, 2.25) |
| Overweight | 1.35 (1.01, 1.81) | 2.13 (1.37, 3.30) | 1.06 (0.63, 1.77) | 1.74 (0.81, 3.73) |
| Obese | 1.78 (1.07, 2.96) | 2.70 (1.24, 5.88) | 0.80 (0.28, 2.27) | 0.81 (0.10, 6.37) |
| OR Test for trend | OR Test for trend | OR Test for trend | OR Test for trend | |
| 1.17 (1.04, 1.32), P=0.009 | 1.39 (1.17, 1.67), P<0.001 | 0.98 (0.80, 1.21) P=0.869 | 1.18 (0.88, 1.63) P=0.256 | |
|
| ||||
| Tanner stage | ||||
| I (pre-pubertal) | 1.0 | 1.0 | 1.0 | 1.0 |
| II | 0.90 (0.54, 1.51) | 1.05 (0.55, 1.99) | 1.38 (0.57, 3.35) | 1.90 (0.52, 6.89) |
| III | 0.83 (0.52, 1.33) | 1.08 (0.60, 1.95) | 0.86 (0.37, 2.03) | 1.52 (0.44, 5.24) |
| IV | 1.12 (0.72, 1.74) | 1.20 (0.68, 2.12) | 1.31 (0.59, 2.92) | 1.90 (0.57, 6.34) |
| V (post-pubertal) | 0.97 (0.61, 1.54) | 0.93 (0.51, 1.70) | 0.81 (0.34, 1.92) | 1.09 (0.30, 3.93) |
| OR Test for trend | OR Test for trend | OR Test for trend | OR Test for trend | |
| 1.04 (0.96, 1.14), P=0.343 | 0.99 (0.89, 1.11) P=0.923 | 0.96 (0.82, 1.11) P=0.549 | 0.97 (0.81, 1.18) P=0.779 | |
|
| ||||
| Physical activity | ||||
| <60 minutes mod/vig | 1.0 | 1.0 | 1.0 | 1.0 |
| >60 minutes mod/vig | 1.29 (0.68, 2.45) | 1.29 (0.57, 2.92) | 2.66 (1.17, 6.07) | 2.87 (1.04, 7.91) |
|
| ||||
| Ethnicity | ||||
| White | 1.0 | 1.0 | 1.0 | 1.0 |
| Non-white | 0.79 (0.50, 1.26) | 0.90 (0.48, 1.66) | 0.55 (0.20, 1.51) | 0.48 (0.12, 3.02) |
|
| ||||
| Maternal education | ||||
| 1 (low) | 1.0 | 1.0 | 1.0 | 1.0 |
| 2 | 0.78 (0.52, 1.16) | 0.78 (0.40, 1.49) | 1.32 (0.51, 3.40) | 0.83 (0.19, 3.57) |
| 3 | 1.14 (0.86, 1.50) | 1.65 (1.05, 2.57) | 2.92 (1.50, 5.71) | 2.24 (0.86, 5.84) |
| 4 | 0.98 (0.74, 1.31) | 1.37 (0.87, 2.16) | 2.45 (1.23, 4.87) | 1.82 (0.68, 4.88) |
| 5 (high) | 1.05 (0.77, 1.43) | 1.36 (0.84, 2.12) | 2.96 (1.46, 6.00) | 3.13 (1.18, 8.36) |
| 5 (high) | 1.05 (0.77, 1.43) | 1.36 (0.84, 2.12) | 2.96 (1.46, 6.00) | 3.13 (1.18, 8.36) |
| OR Test for trend | OR Test for trend | OR Test for trend | OR Test for trend | |
| 1.02 (0.95, 1.09), P=0.678 | 1.07 (0.97, 1.18) P=0.189 | 1.21 (1.06, 1.38) P=0.004 | 1.30 (1.08, 1.57) P=0.006 | |
Abbreviations: BMI body mass index; mod/vig moderate and/or vigorous physical activity
When using ≥6 as the definition of generalised joint laxity, a strong positive association was seen between physical activity and generalised joint laxity, with those girls who do more than 60 minutes of moderate or vigorous activity per day almost 3 times more likely to be hypermobile, after adjustment for all other variables (OR 2.87, 95%CI 1.04 to 7.91). A similar direction of association was seen when generalised joint laxity was defined as ≥4 joints. A positive association was also seen with increasing maternal education (OR for presence of generalised joint laxity in girls with mothers educated to degree level of 3.13, 95%CI 1.18 to 8.36 compared to mothers with no formal education). There was a suggestion of a similar association in those with generalised joint laxity defined as ≥4 once adjusted for all other variables. No independent associations were seen in boys (Table 4).
Discussion
In this first population-based cohort study from the UK, the prevalence of generalised joint laxity in girls and boys aged 13.8 years was 27.5% and 10.6% respectively when using the commonly used cut-off of four or more hypermobile joints from the modified Beighton nine-point scoring system. This provides the first population-based point prevalence data for 14 year old children from the UK, and fits in well with the rest of the literature, being approximately mid-range in terms of other estimates. Girls were more likely to be hypermobile at the fingers, thumbs and trunk, whereas boys were most often hypermobile at the fingers, thumbs and knees. The fact that over 40% of girls showed hyper-extensibility at the little finger leads to the conclusion that this may be normal in a teenage population. Similarly, over 30% of girls also scored positively for thumb apposition.
It is interesting that the lumbar spine was considerably less hypermobile, particularly in boys. This may be explained by the fact that the majority of lumbar flexion is a combination of hamstring extension as well as actual vertebral flexion[32], and short hamstrings have been associated with reduced lumbar flexion in men[33]. It is possible that short hamstrings may have contributed to a perceived reduction in lumbar flexion, and explain the low prevalence of lumbar hypermobility we have seen in boys.
Our study has also presented the first population-based basic descriptives and associations between potential confounding variables of generalised joint laxity in adolescents. No associations were found in boys, possibly because of small numbers. However, we have shown a positive association between generalised joint laxity and habitual levels of physical activity, BMI and maternal education in girls. We found that girls who did more than 60 minutes of moderate to vigorous physical activity per day were almost three times more likely to have generalised joint laxity than those who were not active. We are unable to provide evidence that certain sports are associated with generalised joint laxity because our method of assessing activity was by accelerometry data which does not distinguish between activity types. Nonetheless, as children who do gymnastics or ballet, for example, are likely to be generally more active than children who do not[34], our study supports the results from previous papers that have reported that those children who have a higher range of joint movement may be involved in certain sports or music[18-21].
We also report a positive association between generalised joint laxity and maternal education, with mothers educated to degree level approximately three times as likely to have hypermobile children compared to mothers with no formal qualification. However, this is in direct contrast to a previous study from Mumbai, India[35] that reported that moderate and severe malnutrition were associated with generalised joint laxity, suggesting lower socio-economic factors may be important. Conversely, our study suggests that in the UK, lifestyle choices of families with mothers educated to degree level are associated with generalised joint laxity in the children. For example, ballet dancing or gymnastics may either maintain the presence of hypermobility, or perhaps promote hypermobility through forced hyperextension.
We also found an independent positive association between generalised joint laxity in girls and BMI when using a definition of ≥4, and a suggestion of a similar association when using a definition of ≥6. This is in direct contrast to previous literature that found no evidence that joint hypermobility is associated with BMI[8,24,25]. However, these previous studies were much smaller and therefore had less power than our study to assess this relationship clearly.
In our study, there was little evidence for laterality of hypermobility, consistent with one previous small study but contrary to another [22,23]. In addition there was no evidence of an association with ethnicity, although ALSPAC has only a small proportion (3.7%) of non-whites. Interestingly we also showed no association with either age or puberty. This agrees with the largest of the previous studies[15], but contradicts the generally held belief that generalised joint laxity lessens with aging and growth during childhood. Although the small age range of our study might have explained the null association with age, we had sufficient numbers of children in each stage of puberty so were well placed to observe a relationship between maturational status and joint hypermobility had one been present. Further limitations of our study include loss of a large proportion of the original ALSPAC cohort that may have introduced bias, for example, with a preferential dropout of children from families of lower socio-economic status. In common with all observational studies we cannot exclude confounding and chance, and we are only reporting associations without commenting on temporal relationships or causality.
In conclusion, using the standard cut-off of ≥4 hypermobile joints, 1560 of our 6022 school-children would currently receive a diagnosis of generalised joint laxity. This suggests that a Beighton score of 4 is too low a cut-off, if we wish to use it to identify children with a pathological entity. Increasing the threshold for diagnosing this condition, for example by raising the Beighton score cut-off, should result in a smaller proportion of children being diagnosed in whom risk factors and pathological sequelae may be easier to detect. We have shown stronger evidence of associations with physical activity and maternal education based on a Beighton score cut-off of ≥ 6 compared with ≥ 4.
Alternatively, it would seem reasonable to exclude digits from definitions of generalised joint laxity, since hypermobility of the little finger is essentially normal given this is present in over 40% of girls.
Finally, there may be a need to devise a new, more specific assessment tool to evaluate joint laxity in the developing musculoskeletal system; identifying those children at risk of symptoms such as pain and pathology such as connective tissue disease and, as importantly, reassuring those who do not need further medical intervention.
Acknowledgements
We are extremely grateful to all the families who took part in this study, the midwives for their help in recruiting them, and the whole ALSPAC team, which includes interviewers, computer and laboratory technicians, clerical workers, research scientists, volunteers, managers, receptionists and nurses. The UK Medical Research Council (Grant ref 74882), the Wellcome Trust (Grant ref 076467) and the University of Bristol provide core support for ALSPAC. This publication is the work of the authors and Emma Clark will serve as guarantor for the contents of this paper. This hypermobility research was specifically funded by Arthritis Research-UK (Grant ref 18185). The collection of objective physical activity data was specifically funded by grants from the US National Heart, Lung and Blood Institute (R01HL071248-01A1).
Financial statement: None of the authors received financial support or other benefits from commercial sources for the work reported on in the manuscript.
Footnotes
Contributor statement All authors contributed to study development, eventual design and monitored data collection. In addition, JC drafted and revised the paper. EC trained the ALSPAC measurers, wrote the statistical analysis plan and revised the draft paper. She is guarantor. KD and AS wrote the statistical analysis plan, cleaned and analysed the data, and revised the draft paper. CR developed the methods for measurement, treatment and reduction of the physical activity data. SP and JT revised the draft paper.
Conflict of interest No disclosures
REFERENCES
- 1.Bird HA. Joint hypermobility in children. Rheumatology. 2005;44:703–704. doi: 10.1093/rheumatology/keh639. [DOI] [PubMed] [Google Scholar]
- 2.El-Garf AK, Mahmoud GA, Mahgoub EH. Hypermobility among Egyptian children: Prevalence and features. Journal of Rheumatology. 1998;25(5):1003–1005. [PubMed] [Google Scholar]
- 3.Qvindesland A, Jonsson H. Articular hypermobility in Icelandic 12-year olds. Rhematology. 1999;38(10):1014–1016. doi: 10.1093/rheumatology/38.10.1014. [DOI] [PubMed] [Google Scholar]
- 4.Leone V, Tornese G, Zerial M, Locatelli C, Ciambra R, Bensa M, Pocecco M. Joint hypermobility and its relationship to musculoskeletal pain in schoolchildren: a cross-sectional study. Archives of Disease in Childhood. 2009;94:627–632. doi: 10.1136/adc.2008.150839. [DOI] [PubMed] [Google Scholar]
- 5.Vougiouka O, Moustaki M, Tsanaktsi M. Benign hypermobility syndrome in Greek schoolchildren. European Journal of Pediatrics. 2000;159(8):628. doi: 10.1007/pl00008391. [DOI] [PubMed] [Google Scholar]
- 6.Lamari NM, Chueire AG, Cordeiro JA. Analysis of joint mobility patterns among preschool children. Sao Paulo Medical Journal. 2005;123(3):119–123. doi: 10.1590/S1516-31802005000300006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Subramanyan V, Janaki KY. Joint hypermobility in South Indian children. Indian Journal of Pediatrics. 1996;33:771–772. [PubMed] [Google Scholar]
- 8.Seckin U, Tur BS, Yilmaz O, Yagci I, Bodur H, Arasil T. The prevalence of joint hypermobility among high school students. Rheumatology International. 2005;25:260–263. doi: 10.1007/s00296-003-0434-9. [DOI] [PubMed] [Google Scholar]
- 9.Gyldenkerne B, Iverson K, Roegind H, Fastrup D, Hall K, Remvig L. Prevalence of general hypermobility in 12-13 year old school children and impact of an intervention against injury and pain incidence. Advances in Physiotherapy. 2007;9:10–15. [Google Scholar]
- 10.Cheng JC, Chan PS, Hui PW. Joint laxity in children. Journal of Pediatric Orthopaedics. 1991;11(6):752–756. doi: 10.1097/01241398-199111000-00010. [DOI] [PubMed] [Google Scholar]
- 11.Forleo LHA, Hilario MO, Peixoto AL, Naspitz C, Goldenberg J. Articular hypermobility in school children in Sao Paulo, Brazil. Journal of Rheumatology. 1993;20(5):916–917. [PubMed] [Google Scholar]
- 12.Gedalia A, Person DA, Brewer EJ, Giannini EH. Hypermobility of the joints in juvenile episodic arthritis/arthralgia. Journal of Pediatrics. 1985;107(6):873–876. doi: 10.1016/s0022-3476(85)80178-5. [DOI] [PubMed] [Google Scholar]
- 13.Beighton P, Solomon L, Soskolne CL. Articular mobility in an African population. Annals of Rheumatic Diseases. 1973;32:413–418. doi: 10.1136/ard.32.5.413. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Carter CO, Wilkinson J. Persistent joint laxity and congenital dislocation of the hip. Journal of Bone and Joint Surgery - British Volume. 1964;46:40–45. [PubMed] [Google Scholar]
- 15.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 Paediatrica. 2004;93:1202–1206. doi: 10.1080/08035250410023971. [DOI] [PubMed] [Google Scholar]
- 16.Grahame R, Hakim AJ. Joint hypermobility syndrome is highly prevalent in general rheumatology clinics, its occurrence and clinical presentation being gender, age and race-related. Annals of Rheumatic Diseases. 2006;65(suppl 2):263. [Google Scholar]
- 17.Remvig L, Jensen DV. Generalised joint hypermobility and BJHS II: Epidemiology and clinical criteria. Ugeskrift for Laeger. 2005;167(47):4449–4454. [PubMed] [Google Scholar]
- 18.Briggs J, McCormack M, Hakim AJ, Grahame R. Injury and joint hypermobility syndrome in ballet dancers - a 5-year follow-up. Rhematology. 2009;48(12):1613–1614. doi: 10.1093/rheumatology/kep175. [DOI] [PubMed] [Google Scholar]
- 19.Grahame R. Joint hypermobility and the performing musician. N Engl J Med. 1993;329:1120–1121. doi: 10.1056/NEJM199310073291512. [DOI] [PubMed] [Google Scholar]
- 20.Gannon LM, Bird HA. The quantification of joint laxity in dancers and gymnasts. Journal of Sports Sciences. 1999;17(9):743–750. doi: 10.1080/026404199365605. [DOI] [PubMed] [Google Scholar]
- 21.Jansson A, Saartok T, Werner S, Renstrom P. Evaluation of general joint laxity, shoulder laxity and mobility in competitive swimmers during growth and in normal controls. Scandinavian Journal of Medicine & Science in Sports. 2005;15:169–176. doi: 10.1111/j.1600-0838.2004.00417.x. [DOI] [PubMed] [Google Scholar]
- 22.Lin HC, Lai WH, Shih YF, Chang CM, Lo CY, Hsu HC. Physiological anterior laxity in healthy young females: the effect of knee hyperextension and dominance. Knee Surgery, Sports Traumatology, Arthroscopy. 2009;17(9):1083–1088. doi: 10.1007/s00167-009-0818-9. [DOI] [PubMed] [Google Scholar]
- 23.Verhoeven JJ, Tuinman M, van Dongen PW. Joint hypermobility in African non-pregnant nulliparous women. European Journal of Obstetrics and Gynaecological Reproductive Biology. 1999;82(1):69–72. doi: 10.1016/s0301-2115(98)00182-1. [DOI] [PubMed] [Google Scholar]
- 24.Kannus P, Jarvinen M. Age, overweight, sex and knee instability: their relationship to the post-traumatic OA of the knee joint. Injury. 1988;19(2):105–108. doi: 10.1016/0020-1383(88)90084-8. [DOI] [PubMed] [Google Scholar]
- 25.Englebert RH, Bank RA, Sakkers RJ, Helders PJ, Beemer FA, Uiterwaal CS. Pediatric generalised joint hypermobility with and without musculoskeletal complaints: A localised or systemic disorder. Pediatrics. 2003;111(3):e248–e254. doi: 10.1542/peds.111.3.e248. [DOI] [PubMed] [Google Scholar]
- 26.Beighton P, Grahame R, Bird HA. Hypermobility of Joints. Springer-Verlag; London: 1999. [Google Scholar]
- 27.Quatman CE, Ford KR, Myer GD, Paterno MV, Hewett TE. The effects of gender and pubertal status on generalized joint laxity in young athletes. Journal of Science and Medicine in Sport. 2008;11:257–263. doi: 10.1016/j.jsams.2007.05.005. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Rikken-Bultman DG, Wellink L, van Dongen PW. Hypermobility in two Dutch school populations. European Journal of Obstetrics and Gynaecological Reproductive Biology. 1997;73:189–192. doi: 10.1016/s0301-2115(97)02745-0. [DOI] [PubMed] [Google Scholar]
- 29.Golding J, Pembrey M, Jones R. ALSPAC - The Avon Longitudinal Study of Parents and Children 1. Study methodology. Paediatric and Perinatal Epidemiology. 2001;15:74–87. doi: 10.1046/j.1365-3016.2001.00325.x. [DOI] [PubMed] [Google Scholar]
- 30.Mattocks C, Leary S, Ness AR, Deere K, Saunders J, Tilling K, Kirkby J, Blair SN, Riddoch C. Calibration of an accelerometer during free-living activities in children. International Journal of Pediatric Obesity. 2007;2:218–226. doi: 10.1080/17477160701408809. [DOI] [PubMed] [Google Scholar]
- 31.Clark EM, Ness AR, Tobias JH, the ALSPAC Study Team Social position affects bone mass in childhood through opposing actions on height and weight. Journal of Bone and Mineral Research. 2005;20(12):2082–2089. doi: 10.1359/JBMR.050808. [DOI] [PubMed] [Google Scholar]
- 32.Corben T, Lewis JS, Petty NJ. Contribution of lumbar spine and hip movements during the palsm to floor test in individuals with diagnosed hypermobility syndrome. Physiotherapy Theory and Practice. 2008;24(1):1–12. doi: 10.1080/09593980701686708. [DOI] [PubMed] [Google Scholar]
- 33.Gajdosik RL, Albert CR, Mitman JJ. Influence of hamstring length on the standing position and flexion range of motion of the pelvic angle, lumbar angle and thoracic angle. Journal of Orthopaedic and Sports Physical Therapy. 1994;20(4):213–219. doi: 10.2519/jospt.1994.20.4.213. [DOI] [PubMed] [Google Scholar]
- 34.Epstein Y, Keren G, Udassin R, Shapiro Y. Way of life as a determinant of physical fitness. European Journal of Applied Physiology and Occupational Physiology. 1981;47(1):1–5. doi: 10.1007/BF00422477. [DOI] [PubMed] [Google Scholar]
- 35.Hasija RP, Khubchandani RP, Shenoi S. Joint hypermobility in Indian children. Clinical and Experimental Rheumatology. 2008;26(1):146–150. [PubMed] [Google Scholar]