Article Text
Abstract
Objective To compare the longitudinal trajectories of cardiorespiratory fitness (CRF) in children with probable developmental coordination disorder (DCD) with those of typically developing children.
Setting School-based study, conducted in a large region of Ontario, Canada. 75 out of a possible 92 schools (83%) consented to participate.
Participants A cohort of children, enrolled in grade 4 (mean 9 years 11 months; SD 0.05) at baseline (n=2278) were followed twice-yearly over a 2-year period.
Measures The short form of the Bruininks–Oseretsky test of motor proficiency was used to identify children with probable DCD and the Leger shuttle run to measure maximal oxygen uptake (VO2max).
Results Mixed-effects modelling was used to estimate the change over time in predicted VO2max for both children with probable DCD and typically developing children. For all children, VO2max declined over time. Children (boys and girls) with probable DCD not only had lower VO2max at baseline compared with typically developing children, VO2max declined among these children at a much steeper rate.
Conclusion Although previous research has found children with DCD to have poor CRF compared with typically developing children, most of this work has relied on cross-sectional designs to examine group differences. The results of this study confirm that differences in CRF between children with and without probable DCD persist over time, highlighting the concern that DCD is a risk factor for poor cardiovascular health in children.
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For activities lasting more than a few minutes, energy for movement is produced through aerobic mechanisms.1 The efficiency with which the cardiopulmonary system collects and transports oxygen and its uptake by muscle tissue is typically referred to as cardiorespiratory fitness (CRF).2 The most widely accepted measure of CRF is maximal oxygen uptake (VO2max): the volume of oxygen that can be consumed by the body in a given time. Higher levels of CRF have been associated with numerous health benefits, whereas poor fitness is an independent risk factor for a variety of negative health outcomes, including premature mortality.3,–,6 In childhood and adolescence, poor CRF is associated with hypercholesterolaemia and body fatness.7 Poor CRF (<20th percentile) in young adulthood (ages 18–30 years) predicts the emergence of cardiovascular disease (CVD) 15 years later.8 As CVD pathology begins to emerge in childhood,9 poor fitness among children is a cause for concern.
As CVD is the leading cause of death for both men and women in the developed world, and given the association between CRF and cardiovascular health, it is important to identify groups of children who may be at particular risk of poor CRF. Children with developmental coordination disorder (DCD) are one such group. DCD is a neurodevelopmental condition that affects between 5% and 6% of school-aged children.10 Children with DCD present with a range of coordination difficulties, including fine and gross motor problems,11 12 all of which significantly interfere with normal daily activities such as self-care (eg, dressing, brushing teeth, combing hair), recreational activities (eg, sports and non-organised play) and academic performance skills such as handwriting.12 The diagnosis of DCD requires motor coordination abilities well below the level expected for the child's age and intelligence level. These deficits must substantially interfere with activities of daily living and/or academic achievement. DCD is a diagnosis of exclusion, and can only be made when other physical health problems (eg, cerebral palsy or muscular dystrophy) have been ruled out. A consensus framework for operationalising these criteria is available,13 and has begun to be used to identify cases of DCD in the research literature.14
Possibly as a result of their coordination difficulties, many children with DCD are less physically active than children without the condition.15,–,17 Although genetic factors play a significant role in determining CRF,18 it is also influenced by physical activity, especially activity that is aerobic in nature.1 2 For most children, physical fitness is developed by everyday activities such as walking, running, climbing and jumping.19 As children with DCD are much more likely to be sedentary than their typically developing peers, it has been hypothesised that children with the disorder may also have poorer CRF,20 and indeed several recent studies support this view.19 21,–,26
However, existing data are limited in several respects. First, many existing studies are based on small samples of children with motor coordination difficulties, and these samples are often samples of convenience.19 21,–,26 Perhaps most importantly, only one study to date has attempted to examine the association between motor coordination problems and physical fitness over time in the same group of children.24 It is not known whether differences in CRF between children with and without DCD remain constant or change over time. Characterising the trajectories of children with suspected DCD with respect to CRF will provide important data on the long-term risk of CVD associated with this condition.
Methods
Sample and procedure
The population sampled for this project included all children enrolled in grade 4 during the 2004–5 school year in a public school board located in southern Ontario, Canada. In year one (2004–5) of the study, ethics approval was obtained from the District School Board of the region and from Brock University. Permission from 75 of 92 possible schools (83%), and informed consent from the parents of 2278 of 2378 children (95.4%) within these schools was also obtained. We established testing and training protocols, developed a cadre of trained assistants, and completed baseline testing in the autumn of 2004. Formal data collection began in the spring of 2005 (children in grade 4), with complete re-assessments carried out in each of the autumn of 2005, spring and autumn of 2006 and spring of 2007. We have data, therefore, on a cohort of children as they move from the end of grade 4 through to the end of grade 6 (five time points over 3 years). A total of 2470 students (including those who entered participating schools after baseline) gave consent over the course of the data collection. Of these, 2083 completed motor coordination testing. Baseline sample characteristics are presented in table 1.
A detailed description of the data collection procedures is provided in previous publications.27 28 In brief, motor proficiency and CRF assessments were conducted by trained research assistants in the gymnasium of the school, when possible, and in other locations (eg, library) when a school lacked this facility. Two separate teams of research assistants conducted the motor and fitness testing, on separate occasions, during regular school hours. Reasonable steps, given that all testing was conducted under field conditions, were taken to ensure privacy during motor proficiency testing. All research assistants attended training sessions before being allowed to test children. A research coordinator and individual members of the core research team randomly observed testing during the in-school phase of the project to ensure data quality.
Motor proficiency assessments were made on a single occasion for each child; testing took place over three waves. The origins of DCD, although at present not fully understood, probably begin during fetal development.29,–,32 This means that children with DCD are born with the condition, even though the condition is usually not detectable until early childhood (ages 4–6 years).33 34 It is therefore unlikely that a child would develop DCD later in childhood or adolescence. It is more likely that the condition would have been present from early life, but not identified.35 Further, previous research has demonstrated that DCD persists well into adolescence and early adulthood.36 37 Given our understanding of the disorder, any child identified with significant motor coordination problems, characteristic of DCD, at any point over our assessment period would have had, and continue to have, a compromised motor coordination system over the entire time period. For these reasons, it was deemed sufficient to assess motoric competence at a single point in time. The 75 schools that agreed to participate were randomly divided into three groups. In autumn 2005, the first group of children (n=688) were screened for coordination difficulties and 36 children with probable DCD were identified. In the spring of 2006, the second group (n=723) was screened and 39 more children with probable DCD were identified. In the spring of 2007, the final group of 25 schools were tested (n=672), and a further 36 children with probable DCD were identified.
Measures
Cardiorespiratory fitness
CRF was determined using the Léger 20-m shuttle run test.38 39 The test involves running back and forth between two lines set 20 m apart in synchrony with a sound signal.40 This test is a well-established field measure of VO2max in children,41 and has been validated against Bruce protocol treadmill stress tests with good results (r=0.72, p<0.01).42 Subjects performed the test in groups of up to 15. The test was terminated when a child could not maintain the required running pace for two consecutive signals. The maximum speed (km·h−1) attained during the final stage of the test was used to calculate the metabolic equivalent using the equation:
Case identification for DCD
The Bruininks–Oseretsky test of motor proficiency (BOTMP) is the most commonly used standardised test for the identification of DCD in North America.44 In this study, motor coordination was evaluated using the short form of this measure (BOTMP-SF). The short form uses selected items from the full instrument to assess motor proficiency (including static and dynamic balance, reaction time, bilateral coordination, etc) and has been validated against the full scale with correlations between 0.90 and 0.91 for children between the ages of 8 and 14 years.45 The BOTMP-SF was administered individually to each consenting child in each school's gymnasium. Children who scored at or below the fifth percentile (based on population-derived norms) on the BOTMP-SF were classified as probable DCD for all analyses. We describe cases as probable DCD because our method of case identification is a field test administered by trained researchers, not a diagnostic protocol administered by a physician. Moreover, our method does not include all of the criteria stipulated in the Diagnostic and Statistical Manual of Mental Disorders, version IV.46 In this study, the BOTMP-SF is used for criterion A, and all children and adolescents with known learning disabilities or physical health problems were excluded from the analyses (criteria C and D). Criterion B (limitations in activities of daily living) is the only aspect of diagnosis not measured. However, as Visser11 notes, most studies do not take into account the exclusion criteria in the Diagnostic and Statistical Manual of Mental Disorders, version IV.
Follow-up tests on small subsets of children revealed good agreement between the BOTMP-SF and a clinician-administered movement-ABC (n=24; positive predictive value of 88% at the 15th percentile of the movement-ABC, 62% at the fifth percentile) and acceptable stability in re-testing after an interval averaging approximately 1 year (n=77; r=0.70, p<0.001). A more detailed description of these procedures is provided in a previous publication.27
Statistical analysis
We used repeated measures analysis of variance to test overall bivariate differences by gender and probable DCD status while taking into account the correlation of measures within children. To examine the independent effects of our predictor variables on CRF, we used mixed effects modelling.47 Mixed effects modelling, also known as multilevel modelling, is a statistical approach appropriate to the analysis of nested observations and to the examination of variables that may be influential at different levels of nesting. Our models take into account the nesting of observations within children (ie, repeated measures) and the nesting of children within schools. We include random intercepts at the school and student levels, as well as a random slope for time. Analysis of the data revealed possible seasonal effects, so we chose to use an unstructured covariance matrix. In order to test whether trajectories of CRF over time differed between children with probable DCD and typically developing children, we fit a model that examined the main effects of probable DCD and time and the interaction between the two, adjusting for gender and age at baseline. We also tested for a three-way interaction between probable DCD, time and gender, given that boys have, on average, higher CRF than girls,1 2 and that previous work has shown boys with probable DCD to be at greater risk of poor CRF than both typically developing children and girls with probable DCD.19 All analyses were conducted using SAS version 9.1
Results
Descriptive statistics, including mean VO2max scores for both genders, and for children with and without probable DCD are provided in table 1. Simple repeated measures analysis of variance indicated an overall gender difference, with VO2max scores for girls significantly lower than those for boys (F=144.96, df=12 423, p<0.001). This difference was also present within the subgroup of children without probable DCD (F=134.68, df=11 966, p<0.001), but not in the much smaller group scoring in the probable DCD range on our measure of motor coordination (F=0.63, df=1108, p=0.43).
The results of the multivariate, mixed effects analysis are presented in table 2. While overall CRF levels are lower in girls than boys, and lower for children with probable DCD, we found no evidence that the trajectories of CRF in children with probable DCD and those without differed by gender. In other words, we did not find a significant three-way interaction between probable DCD status, time and gender. We did, however, find a significant interaction between probable DCD status and time, suggesting the there is a difference in trajectories of CRF between children with and without the disorder. Moreover, we also tested for non-linear trajectories and found that the addition of a term representing time-squared significantly improved the fit of the model. The significant effect for the interaction of time-squared with probable DCD status further suggests that the difference in trajectories between groups is not strictly linear.
In order to aid the interpretation of this interaction, we used the equation in table 2 to calculate predicted values of VO2max for both groups, the results of which are depicted graphically in figure 1. We plot predicted values for both boys and girls, although these values differ only in their intercepts. For all children, VO2max declines over time. However, as can be seen, children with probable DCD not only have lower VO2max at baseline compared with typically developing children, VO2max declines among these children at a much greater rate, with reductions over the course of the study of approximately 2% for boys and girls without probable DCD and 4% for those with. For typically developing children, VO2max remains relatively stable until approximately 15 months from baseline; from there the decline accelerates until the final observation period. The difference between groups then shows some sign of narrowing over this particular developmental period.
Discussion
The purpose of the present study was to examine trajectories of CRF—measured here as predicted VO2max—in children with and without DCD. Although previous work has found differences in CRF between these groups, data have been almost exclusively cross-sectional, with CRF assessed at a single point in time.21,–,23 25 26 Only one study in the published literature to date has examined CRF over time in these populations.24 However, this study was based on a very small sample of children with low (n=19) and high (n=19) motor competence, so the findings must be interpreted with caution. Ours is the first study available in the published literature to examine CRF differences related to probable DCD longitudinally in a large cohort of children.
Our results are consistent with previous cross-sectional studies, in that we found, at baseline, substantial differences in CRF between children with probable DCD and those without.21,–,26 Moreover, we found these differences persisted over the study period. However, unlike previous research, we did not find that these differences increased.24 Rather, our results show a narrowing of group differences, attributable to a more rapid decline in CRF in typically developing children during the final 9 months of the study. The discrepancy is probably due to the differences in the developmental period examined between studies, with our study following an older cohort of children, and possibly due to sample size differences, as our study followed a much larger group of children with coordination problems. Unlike previous work, we also did not find any evidence of a gender interaction between probable DCD, gender and CRF.21 Although girls with probable DCD have the lowest levels of CRF throughout the study, both genders with probable DCD show a similar rate of decline in CRF over time.
With regard to typically developing children, our VO2max results are remarkably close to previous research on children in this age range. Rowland et al48 reported that average peak oxygen uptake in typically developing 12-year-old boys was 47.0 (±5.8) ml/kg per min. Results from treadmill testing showed that between 7 and 16 years of age, typically developing boys oxygen uptake ranged from approximately 45 to 50 ml/kg per min, with higher average oxygen uptake scores in younger boys and lower values in older children. For typically developing girls in the same age range, values ranged from 35 to 45 ml/kg per min, with a similar pattern of decline with age.2 It is true, however, that the average oxygen uptake scores for both boys and girls with probable DCD still fall within the normal range (albeit at the low end), our interest was in group differences over time. The trends observed here suggest that children with probable DCD, barring an intervention to alter the course, are more likely to fall into the low fitness range at a much faster rate than unaffected children.
Our results show that the difference in VO2max between children with and without probable DCD is substantial, and that it tends to increase over time. Although it is not certain that this divergence persists into adulthood, studies in the general population have shown that childhood fitness levels and obesity are moderately to strongly correlated with adult health outcomes.8 9 The trajectory of children with apparent motor coordination problems may thus place them at heightened risk of inactivity-related health conditions later in life. This adds to existing evidence suggesting that interventions intended to improve physical fitness may be appropriate for children with DCD.
As with any study, there are several limitations that need to be considered when evaluating the results. First, our study is limited to the examination of group differences. Although a difference in levels of physical activity is, as mentioned, the likeliest mediator, we did not examine specific mechanisms that might underlie the relationship between probable DCD and poor CRF. Second, although steps were taken to ensure significant motor coordination difficulties were present for our probable DCD group, and that any child with known neurological and/or physical conditions that might explain the motor difficulties were excluded from the study, not all diagnostic criteria were considered in our case identification protocols. In particular, we did not evaluate criteria B, which considers the impairment due to coordination in terms of activities of daily living and/or scholastic achievement. Future work will need to address this limitation.
Our measure of CRF is also based on a field measure, in which test performance (stage completed) is used to predict VO2max. Until recently, most of the available data on CRF differences between children with and without DCD has used this indirect method.21 23,–,26 A prominent concern with tests such as the shuttle run is the perceived predisposition of children to terminate before maximal effort because of low motivation.1 2 Unlike a laboratory setting, where children are tested one-on-one and maximal effort is easier to monitor (eg, through heart rate), field-based settings where groups of children are tested simultaneously lead to much greater reliance on the internal motivation of the child to perform to exhaustion. This is of particular concern in relation to children with DCD, in which motivation to perform any physical task is apt already to be low, given their abilities, and/or previous negative experiences with such tasks.49 The concern, therefore, is that we may be underestimating VO2max in these children, thereby inflating group differences between children with coordination difficulties and typically developing children. A small body of work has begun to examine VO2max in children with DCD using standard, laboratory-based cycle ergometer50 51 and treadmill19 protocols. The results of that work show similar deficits in VO2max in children with DCD, suggesting robustness to the effect that does not appear limited to field testing only.
Finally, a closely related concern is whether children with DCD can perform the shuttle run adequately in the first place, given their coordination difficulties. Although the shuttle run test was designed to require minimal physical or motoric skill to complete,49 it does demand pacing and rapid turning, which could pose problems for some children with DCD. At the same time, laboratory-based protocols, which require the subject to cycle or run on a moving belt, could also be problematical for some children with DCD. That we get similar results with all of these methodologies, as noted above, provides some assurance that the findings are not merely an artifact of any particular test. At the same time, matching a test to the motoric capabilities of a child with DCD before testing may be a useful protocol to adopt in future studies with this population.
Notwithstanding these concerns, the results presented here are the first data comparing the longitudinal trajectories of aerobic fitness between children with probable DCD to typically developing children using a large sample of children. Given the troubling pattern of decline, it is clear that poor motor coordination is an important factor influencing CRF in childhood.
References
Footnotes
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Funding This study was funded by the Canadian Institutes of Health Research.
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Competing interests None.
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Patient consent Obtained from the parents.
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Ethics approval Ethics approval was obtained from the District School Board of the region and from Brock University.
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Provenance and peer review Not commissioned; externally peer reviewed.