ARTICLES

The Association Between Developmental Coordination

Disorder and Other Developmental Traits
AUTHORS: Raghu Lingam, MBChB, MSc, MRCPCH,a Jean WHAT’S KNOWN ON THIS SUBJECT: Previous clinic-based
Golding, PhD, DSc, FMedSci,a Marian J. Jongmans, PhD,b,c samples have shown an overlap between developmental
Linda P. Hunt, PhD,d Matthew Ellis, MB, ChB, PhD, coordination disorder, ADHD, autism, and dyslexia. However,
MRCPCH,a and Alan Emond, MB, MD, FRCPCHa there has been limited population-based work on the association
aCentre for Child and Adolescent Health, School of Social and
of DCD with other developmental traits that account for potential
Community-Based Medicine, University of Bristol, Bristol, United confounding factors.
Kingdom; bDepartment of Pediatric Psychology, Wilhelmina
Children’s Hospital, Utrecht, Netherlands; cUniversity Medical
Center Utrecht and Department of Special Education, Faculty of WHAT THIS STUDY ADDS: Using data from the ALSPAC (N ⫽ 6902
Social Sciences, Utrecht University, Utrecht, Netherlands; and maximum), these study results show that children with probable
dSchool of Clinical Sciences, University of Bristol, Bristol, United
DCD have an increased risk of difficulties in attention, short-term
Kingdom memory, and academic and social skills, after controlling for
KEY WORDS confounding factors including IQ and other developmental traits.
developmental coordination disorder, DCD, child development,
attention, language development, memory, reading, spelling,
social interaction, ALSPAC, developmental disabilities
ABBREVIATIONS
DCD—developmental coordination disorder
DSM-IV—Diagnostic and Statistical Manual of Mental Disorders abstract
Fourth Edition
ADL—activity of daily living
OBJECTIVE: To explore associations between developmental coordina-
SLI—specific-language impairment tion disorder (DCD) and attention, language, social skills, and aca-
ASD—autism spectrum disorder demic ability in a population-based cohort.
ALSPAC—Avon Longitudinal Study of Parents and Children
DAWBA—Development and Well-being Assessment METHODS: We analyzed data (N ⫽ 6902) from the Avon Longitudinal Study
MABC—Movement Assessment Battery for Children of Parents and Children (ALSPAC). Probable DCD was defined as children
WOLD—Wechsler Objective Language Dimensions below the 15th centile of the ALSPAC Coordination Test aged 7 years with
SCDC—Social and Communication Disorders Checklist
WORD—Wechsler Objective Reading Dimensions functional impairment in activities of daily living or handwriting, excluding
OR—odds ratio children with neurologic difficulties or an IQ of ⬍70. Four developmental
CI—confidence interval domains were assessed by using standardized tests between the ages of
www.pediatrics.org/cgi/doi/10.1542/peds.2009-2789 7.5 and 9 years: attention; language skills (expressive language, compre-
doi:10.1542/peds.2009-2789 hension, short-term memory); social skills (nonverbal skills and social
Accepted for publication Jul 20, 2010 communication); and academic ability (reading and spelling). The worst
Address correspondence to Raghu Lingam, MBChB, MSc, 5% of each trait was used to define impairment. We used multiple logistic
MRCPCH, Centre for Child and Adolescent Health, Department of regression models to assess the association between probable DCD and
Community-Based Medicine, University of Bristol, Bristol BS6
each trait. Our final model controlled for IQ, socioeconomic factors, and
6JS, United Kingdom. E-mail: [email protected]
other developmental traits not in the domain assessed.
PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).
Copyright © 2010 by the American Academy of Pediatrics
RESULTS: A total of 346 (5.0%) children met criteria for probable DCD.
Probable DCD was associated with difficulties in attention (odds ratio
FINANCIAL DISCLOSURE: The authors have indicated they have
no financial relationships relevant to this article to disclose. [OR]: 1.94 [95% confidence interval (CI): 1.17–3.24]), nonword repeti-
tion (OR: 1.83 [95% CI: 1.26 –2.66]), social communication (OR: 1.87 [95%
CI: 1.15–3.04]), reading (OR: 3.35 [95% CI: 2.36 – 4.77]), and spelling (OR:
2.81 [95% CI: 2.03–3.90]).
CONCLUSIONS: Children with probable DCD had an increased risk of
difficulties in attention, social skills, reading, and spelling. These
additional difficulties need to be screened for during assessment
and considered when formulating interventions. Pediatrics 2010;
126:e1109–e1118

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Developmental coordination disorder is maintained with ⬃10 000 children.6 nation: manual dexterity (placing pegs
(DCD) is defined according to the Diag- Mothers of infants in the ALSPAC were task); ball skills (throwing bean bag
nostic and Statistical Manual of Men- broadly representative of the rest of into box); and balance (heel-to-toe
tal Disorders, Fourth Edition (DSM-IV) the United Kingdom at the 1991 census. walking). These motor subtests have
criteria, as a condition marked by a Further details of study recruitment, been shown to have concurrent valid-
severe impairment in the development retention, and data collection have ity with other similar coordination
of motor coordination, which signifi- been described previously.6 tests and represent the 3 domains of
cantly interferes with activities of daily Data have been collected on a variety coordination using principal compo-
living (ADL) and/or academic achieve- of developmental traits by using face- nent analysis of original standardiza-
ment, not caused by a general medical tion data from the MABC.8,10 The 5th
to-face assessments at special clinics,
condition or severe learning impair- centile of a standardized motor coordi-
parental self-completion question-
ment.1 Although there is extensive lit- nation test is generally used to define
naires, and linked education and
erature describing the overlap be- severe motor impairment; children be-
health records. Data on potential ante-
tween DCD and conditions such as tween the 5th and 15th centile are con-
natal and postnatal confounding fac-
attention-deficit/hyperactivity disor- sidered at risk of impairment. We used
tors were collected prospectively from
der, specific-language impairment the 15th centile of the ALSPAC Coordi-
a number of questionnaires.
(SLI), autism spectrum disorder (ASD), nation Test to define children as having
and dyslexia in clinic-based samples, Participating parents provided in-
or being at risk of coordination difficul-
few population-based studies have ad- formed consent for testing sessions,
ties in keeping with the MABC manual
equately controlled for confounding and assent was gained from the chil-
and previous literature.9,11
factors.2–5 dren. Ethical approval for the study
was obtained from the ALSPAC Law and Those children below the 15th centile
The aim of our study was to assess the on motor testing were then said to
Ethics Committee and the local re-
association between children with have functional impairment in motor
search ethics committees.
probable DCD, defined by using criteria skills if, in addition, they either failed
based on the DSM-IV, and difficulties in their National Curriculum Key Stage 1
Measures
attention, language, and short-term writing test or they were below the
memory; social skills; and academic Exposure Variable: Probable DCD 15th centile of a 23-item ADL scale de-
ability (reading and spelling) within a Children with probable DCD were de- rived from parent-completed question-
prospective population-based sample, fined by using the DSM-IV criteria, naires.8 Those children with a known
accounting for known confounding adapted for research by using the 2006 visual deficit or neurologic condition
factors and the colinearity of the devel- Leeds Consensus Statement.1,7,8 Chil- such as cerebral palsy were excluded,
opmental traits themselves. dren were defined as having probable as were children with an IQ of ⬍70.
DCD if they met all 4 DSM-IV criteria for Children with an ASD diagnosis, identi-
PATIENTS AND METHODS DCD: poor motor coordination (crite- fied from linked education and health
Sample rion A), which causes functional im- records, were not excluded as recom-
The Avon Longitudinal Study of Parents pairment in ADL, or academic achieve- mended by the Leeds Consensus State-
and Children (ALSPAC) is a prospective ment (criterion B) not caused by a ment.7 However, secondary analyses
population-based birth cohort study general medical condition or severe excluding these children were per-
designed to investigate the interaction learning difficulties (exclusion criteria formed. The multistage definition used
of environment and genotype on the C and D).1 Full details of the case defi- met DSM-IV criteria for DCD. However,
health and development of children. nition and the numbers of children at because we used the 15th centile,
The study investigators invited all each stage of definition have previ- rather than the more conservative 5th
pregnant women in the geographically ously been described.8 centile, of the motor coordination test,
defined area of Avon, southwest En- Motor skills of children were assessed we described our population as having
gland, with an expected date of deliv- between 7 and 8 years using the AL- probable DCD in keeping with our pre-
ery between April 1, 1991, and Decem- SPAC Coordination Test, which con- vious work.8
ber 31, 1992, to take part. The study sisted of the subtests derived from the After excluding children with an IQ of
contains data on 14 062 live births, of Movement Assessment Battery for ⬍70, data were available for 6902 chil-
which 13 988 were still alive at 12 Children (MABC).9 The subtests were dren who attended motor testing and
months of age; active contact currently selected to test the 3 realms of coordi- who had data from their handwriting

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ARTICLES

test or the ADL scale; of these, 346 chil- formed by trained observers at face- Analysis
dren representing 5% of our eligible to-face research clinics, except the Logistic regression models were used
cohort met criteria for probable DCD. DAWBA and the SCDC, which were to assess the association between the
parent-completed questionnaires. exposure variable probable DCD and
Outcome Variables
each of the 8 developmental traits in
Between the ages of 7 and 9 years, the Possible Confounding or Mediating
turn as outcomes.
children of the ALSPAC were assessed Factors
All tests apart from the comprehen-
by using a number of standardized Potential confounding factors were se-
sion subtests from the WOLD, the read-
tests and subtests that were grouped lected after appraisal of the relevant
ing test of the WORD, and the test of
into 4 major domains of develop- literature.20 Factors were divided into
nonword repetition had a skewed dis-
ment: (1) attention and hyperactivity; child and parental/environmentally re-
tribution even after logarithmic trans-
(2) language skills and short-term lated confounding factors and added
formation. Measures were dichoto-
memory; (3) social skills; and (4) ac- to the model in blocks to assess the
ademic ability. mized by using both the 5th and the
effect on any association between ex-
15th centiles to define significant diffi-
Inattention and hyperactivity were as- posure and outcome.21
culties, as done previously.24,26–28
sessed by using the Development and Child-related confounding factors
Well-being Assessment (DAWBA) at We first looked at the unadjusted asso-
were gender, birth weight (ⱕ2500 and
ciation between probable DCD and
91 months of age.12 The DAWBA is ⬎2500 g), gestation (⬍37 and ⱖ37
a parent-completed, questionnaire- each developmental trait (model 1).
weeks’ gestation), hearing difficulties,
based assessment that includes 18 Adjustment was then made for all child
and cognitive ability (IQ). Children
questions relating to the child’s activ- and parental factors excluding IQ
were defined as having normal hear-
ity and attention. (model 2); model 3 added IQ. For the
ing thresholds if bilateral average air
final model (model 4), adjustment was
Speech and language were tested conduction was ⱖ20 dB on testing. IQ
also made for all the other develop-
by using items from the oral expres- was measured by using alternate
mental traits not in the domain under
sion and language comprehension items of the Wechsler Intelligence
investigation. For example, for the out-
subtests of the Wechsler Objective Lan- Scale for Children III at a mean age of
come variable reading (5th centile),
guage Dimensions (WOLD).13 Short- 8.7 years.22 For language-based out-
the final model adjusted for all child
term memory was assessed by using a comes, performance IQ was con-
and parental factors along with all the
shortened version of the Children’s trolled. For all other outcome mea-
traits outside the academic ability do-
Test of Nonword Repetition.14 Nonword sures, total IQ was controlled. Gender
main (ie, inattention and hyperactivity,
repetition has been shown to be and IQ were tested as potential effect
modifiers. nonverbal skills, social communica-
strongly associated with language de-
tion, expressive language, language
velopment and was therefore grouped Parental and environmental confound- comprehension, and short-term
within this developmental domain.15 ing factors were highest maternal ed- memory).
The domain of social skills included ucational attainment (3 categories),
nonverbal skills and social communi- highest parental social class (non- The number of children in each model
cation. Nonverbal impairment was as- manual [I, II, and III nonmanual], III differed, because not all children at-
sessed by using the faces subtest of manual, and IV and V manual), housing tended the various tests and returned
the Diagnostic Analysis of Nonverbal tenure of the family in pregnancy questionnaires. To deal with the poten-
Accuracy, and social communication (owned or rented), financial difficul- tial bias introduced by these missing
abilities were measured by using the ties in pregnancy (5-point scale de- data, we used multiple imputation by
Social and Communication Disorders rived from maternal report of ability chained equations to impute missing
Checklist (SCDC).16,17 Measures of aca- to afford food, clothing, heating, ac- data in the confounding factors.29,30
demic ability consisted of reading, as- commodation, and items for the in- Further details of the multiple impu-
sessed by using the basic-reading fant), maternal smoking in preg- tation models are reported in Appen-
subtest of the Wechsler Objective nancy (ever or never), and antenatal dix 1.
Reading Dimensions (WORD),18 and depression and anxiety using the Ed- IQ and gender were considered poten-
spelling was assessed by using 15 age- inburgh Postnatal Depression Scale tial effect modifiers and assessed by
appropriate words developed by and Crown–Crisp Experiential Index using likelihood ratio tests. Sensitivity
Nunes and Bryant.19 All tests were per- respectively.23–25 analyses were performed by using the

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complete case data set and by remov- TABLE 1 Characteristics of Those Children With Probable DCD Compared to Controls
ing those children with a known ASD Control Probable Significance, P
diagnosis. All statistical analyses used Subjects DCD

Stata 9.2 (Stata Corp, College Station, N 6556 max 346 max
Child factors
TX). Gender, n (%)
Boys 3255 (49.7) 217 (62.7) ⬍.001a
RESULTS Girls 3301 (50.4) 129 (37.3)
Gestation, n (%)
The characteristics of the 346 children ⱖ37 wk 6005 (95.0) 302 (91.8) .01a
with probable DCD compared with our ⬍37 wk 316 (5.0) 27 (8.2)
n 6321 329
6556 normally developing control sub- Birth weight, n (%)
jects are listed in Table 1. As reported ⬎2500 g 5956 (95.2) 294 (90.7) ⬍.001a
previously, children with probable DCD ⱕ2500 g 301 (4.8) 30 (9.3)
n 6257 324
were more likely to be male, have a
Ethnicity, n (%)
lower birth weight, and come from a White 6237 (95.7) 324 (93.6) .07a
more deprived social background8 (Ta- Nonwhite 280 (4.3) 22 (6.4)
ble 1, characteristics of those children n 6517 346
IQ, mean (SD) 105.67 (15.4) 93.90 (16.4) ⬍.001b
with probable DCD compared with con- n 5375 244
trol subjects). Hearing, n (%)
Normal 5606 (92.4) 278 (89.4) .05a
Of a maximum of 6902 children, the Either side not reaching thresholds 459 (7.6) 33 (10.6)
number of children who completed de- n 6065 311
velopmental outcome tests ranged Parental and environmental factors, n (%)
Highest maternal or paternal social class
from 5204 to 6791 (mean: 5863), of I, II, and III nonmanual 4982 (85.5) 222 (76.3) ⬍.001a
which an average of 270 children had IIIM 606 (10.4) 46 (15.8)
probable DCD. In the complete case IV and V 238 (4.1) 23 (7.9)
n 5826 291
analysis, the total number of children
Housing tenure at 8 wk gestation, n (%)
in the final analysis was additionally Owned 5077 (84.9) 238 (76.3) ⬍.001a
reduced when confounding factors Rented 900 (15.1) 74 (23.7)
were added (illustrated in Fig 1). This n 5977 312
Maternal education highest qualification, n (%)
was not the case when multiple impu- A-level/degree 2569 (42.2) 121 (39.0) .001a
tation was used, because missing data O level 2210 (36.3) 94 (30.3)
were accounted for in the confounding CSE/vocational 1313 (21.6) 95 (30.7)
n 6092 310
factors. Further details on the number Maternal age at delivery, n (%)
of children in each model are presented ⬍21 y 198 (3.1) 12 (3.7) .60a
in Appendix 1 (including Table 6). ⱖ 21 y 6123 (96.9) 317 (96.4)
n 6321 329
The odds ratios (ORs) of having signif- Ever smoked in pregnancy, n (%)
icant difficulties (5th centile) in each Never 4995 (80.0) 246 (75.7) .06a
Ever 1247 (20.0) 79 (24.3)
developmental trait for children with
n 6242 325
probable DCD compared with control Antenatal depression at 32 wk gestation using
subjects are presented in Tables 2 and the Edinburgh Postnatal Depression
3, for the complete case set and multi- Scale, n (%)
Not depressed 5166 (87.3) 243 (82.4) .01a
ple imputation data sets, respectively. EPDS ⱕ 12
Children with probable DCD had signif- Depressed 752 (12.7) 52 (17.6)
icantly increased odds of having diffi- n 5918 295
EPDS ⱖ13
culties in all the developmental do- Antenatal anxiety using the Crown Crisp
mains investigated in the unadjusted Experimental Index 32 wk gestation, n (%)
model (model 1) and after controlling Anxiety score ⱕ 9 5101 (88.5) 240 (83.9) .02a
Anxiety score ⱖ10 660 (11.5) 46 (16.1)
for child and parental factors (model n 5761 286
2). The addition of IQ decreased the a ␹2 test.
ORs, but there still was a significantly b Student’s t test.
increased odds of having difficulties in

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ARTICLES

6902 children were 7 and 8 y when each domain for those children in the
attending the Focus@7 and completing the
ADL questionnaire or handwriting test probable-DCD group. Model 4, when
(IQ < 70 excluded)
using both the multiple imputation and
complete case data sets, showed a
1256 children missing from persistent strong association between
the DAWBA
probable DCD and difficulties in inat-
tention/hyperactivity, nonword repeti-
5646 children also tion, reading, and spelling after adjust-
had results for the
DAWBA
ment for the other traits outside the
domain under investigation and an in-
2241 children had at least
1 missing factor from the
creased risk of difficulties in nonver-
confounding factors in bal skills and social communication
model 4
only in the multiple-imputation model.
The differences seen between the com-
3405 children had data from
plete case and imputed data sets can
exposure, outcome, and all be attributed to potential bias intro-
potential confounding factors
duced by missing data, because
FIGURE 1 model 4 of the complete case data
Number of children in the final analysis for inattention and hyperactivity symptoms measured by set had ⬎2000 fewer children than
using the DAWBA. the unadjusted imputed model for
each analysis.

TABLE 2 ORs (95% CIs) of Significant Difficulties in Developmental Traits (Using the 5th Centile Cutoff) for Children With Probable DCD Compared With
Control Subjects by Using the Complete Case Data Set
Model 1, P Model 2, OR P Model 3, OR P Model 4, OR P
Unadjusted OR (95% CI) (95% CI) (95% CI)
(95% CI)
Inattention or hyperactivity (n ⫽ 5646 max) 4.40 (3.07–6.30) ⬍.001 5.22 (3.41–7.97) ⬍.001 4.07 (2.45–6.73) ⬍.001 2.73 (1.34–5.59) .006
Expressive language (n ⫽ 5624 max) 3.18 (2.22–4.57) ⬍.001 2.74 (1.74–4.33) ⬍.001 1.83 (1.13–2.97) .013 1.09 (0.56–2.14) .790
Language comprehension (n ⫽ 5648 max) 2.43 (1.62–3.64) ⬍.001 1.95 (1.14–3.31) .014 1.50 (0.86–2.60) .153 0.83 (0.39–1.79) .636
Nonword repetition (n ⫽ 5637 max) 3.68 (2.68–5.07) ⬍.001 2.78 (1.81–4.27) ⬍.001 2.37 (1.53–3.66) ⬍.001 1.83 (1.06–3.16) .031
Nonverbal skills (n ⫽ 5204 max) 3.22 (2.18–4.76) ⬍.001 2.93 (1.77–4.84) ⬍.001 1.89 (1.11–3.23) .020 1.40 (0.73–2.68) .313
Social and communication (n ⫽ 5635 max) 4.24 (3.01–6.0) ⬍.001 4.33 (2.84–6.59) ⬍.001 3.29 (1.98–5.48) ⬍.001 1.74 (0.89–3.40) .105
Reading (n ⫽ 6791 max) 10.12 (7.77–13.19) ⬍.001 7.56 (5.24–10.91) ⬍.001 4.04 (2.43–6.70) ⬍.001 4.13 (2.25–7.59) ⬍.001
Spelling (n ⫽ 6702 max) 6.91 (5.36–8.93) ⬍.001 4.97 (3.52–7.02) ⬍.001 2.65 (1.70–4.13) ⬍.001 2.18 (1.28–3.74) .004
Model 2 controlled for child factors (gender, age at which test was performed, birth weight, gestation, and hearing) and parental factors (maternal education, housing tenure in pregnancy,
highest parental social class, financial difficulties score, antenatal maternal smoking, antenatal depression, and antenatal anxiety). Model 3 controlled for all the confounding factors in
model 2 ⫹ total IQ or performance IQ for language based skills (ie, WOLD, nonword repetition). Model 4 controlled for all confounding factors as in model 3 ⫹ all other developmental traits
not in that developmental domain being tested.

TABLE 3 ORs (95% CIs) of Significant Difficulties in Developmental Traits (Using the 5th Centile Cutoff) for Children With Probable DCD Compared With
Control Subjects by Using the Multiple-Imputation Data Set
Model 1, P Model 2, OR P Model 3, OR P Model 4, OR P
Unadjusted OR (95% CI) (95% CI) (95% CI)
(95% CI)
Inattention or hyperactivity (n ⫽ 5646) 4.40 (3.07–6.30) ⬍.001 4.04 (2.78–5.86) ⬍.001 3.18 (2.16–4.69) ⬍.001 1.94 (1.17–3.24) .011
Expressive language (n ⫽ 5624) 3.18 (2.22–4.57) ⬍.001 2.94 (2.02–4.27) ⬍.001 2.02 (1.37–2.98) ⬍.001 1.36 (0.88–2.09) .165
Language comprehension (n ⫽ 5648) 2.43 (1.62–3.64) ⬍.001 2.27 (1.49–3.44) ⬍.001 1.84 (1.20–2.82) .005 1.31 (0.82–2.08) .254
Nonword repetition (n ⫽ 5637) 3.68 (2.68–5.07) ⬍.001 3.46 (2.49–4.82) ⬍.001 2.84 (2.03–3.98) ⬍.001 1.83 (1.26–2.66) .002
Nonverbal skills (n ⫽ 5204) 3.22 (2.18–4.76) ⬍.001 3.08 (2.06–4.60) ⬍.001 2.03 (1.34–3.09) .001 1.58 (1.01–2.48) .044
Social and Communication (n ⫽ 5635) 4.24(3.01–6.0) ⬍.001 3.85 (2.70–5.50) ⬍.001 3.31 (2.29–4.79) ⬍.001 1.87 (1.15–3.04) .012
Reading (n ⫽ 6791) 10.12 (7.77–13.19 ⬍.001 8.71 (6.54–11.61) ⬍.001 4.61 (3.32–6.39) ⬍.001 3.35 (2.36–4.77) ⬍.001
Spelling (n ⫽ 6702) 6.91 (5.36–8.93) ⬍.001 5.88 (4.47–7.72) ⬍.001 3.44 (2.53–4.68) ⬍.001 2.81 (2.03–3.90) ⬍.001
Model 2 controlled for child factors (gender, age at which test was performed, birth weight, gestation, and hearing) and parental factors (maternal education, housing tenure in pregnancy,
highest parental social class, financial difficulties score, antenatal maternal smoking, antenatal depression, and antenatal anxiety). Model 3 controlled for all the confounding factors in
model 2 ⫹ total IQ or performance IQ for language based skills (ie, WOLD, nonword repetition). Model 4 controlled for all confounding factors as in model 3 ⫹ all other developmental traits
not in that developmental domain being tested.

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TABLE 4 Gender-Specific ORs (95% CIs) of Reading Difficulty (5th Centile) in the Complete Case and DISCUSSION
Multiple-Imputation Analyses
Complete Case Analysis Model 3 P Model 4 P
Using a large, prospective cohort study,
Probable DCD
we have shown that, after accounting for
Boys 2.84 (1.58–5.11) ⬍.001 2.67 (1.32–5.42) .006 potential confounding factors, children
Girls 11.73 (4.67–29.49) ⬍.001 15.25 (5.19–44.79) ⬍.001 with probable DCD have an increased
Multiple-imputation analysis
probable DCD
risk of other common developmental dif-
Boys 3.35 (2.26–4.97) ⬍.001 2.25 (1.45–3.49) ⬍.001 ficulties. Our findings build on the exist-
Girls 9.62 (5.48–16.87) ⬍.001 7.45 (4.07–13.62) ⬍.001 ing evidence based on selected samples.
Model 3 controlled for child factors (gender, age at which test was performed, birth weight, and gestation hearing) and Previous longitudinal work used
parental factors (maternal education, housing tenure in pregnancy, highest parental social class, financial difficulties
score, antenatal maternal smoking, antenatal depression, and antenatal anxiety) ⫹IQ (total) or IQ performance controlled teacher-completed questionnaires to
for language-based skills (WOLD, nonword repetition) as a continuous variable. Model 4 ⫹ other developmental traits not screen children for attention, speech
in that developmental domain.
and language, and motor difficulties,
which makes the results of these studies
The association between probable DCD creased risk of reading difficulties, but difficult to interpret in terms of comor-
and the test of nonword repetition pre- girls had a higher risk than boys (Table bidity across developmental domains.31–33
sented in Tables 2 and 3 did not control 4). Kaplan et al34 and Dewey et al35 showed
for expressive language or compre- significant overlap between DCD,
Of the original 346 children with prob-
hension. An additional analysis con- attention-deficit/hyperactivity disorder,
able DCD, 19 were on the autistic spec-
trolling for these variables in the and learning difficulties in a sample re-
trum as compared with 15 control chil-
multiple-imputation model 4 did not cruited from clinics, special schools, and
dren. Results of sensitivity analysis
weaken the association of probable resource classrooms. We, in contrast,
excluding these children showed simi-
DCD and nonword repetition (OR: used a population-based sample without
lar results to those obtained with
1.76 [95% confidence interval (CI): the use of an initial screening question-
these children included (Table 5). The
1.21–2.58]). naire, which reduced potential referral
OR for difficulties with nonverbal skills
None of the likelihood ratio tests for an and social communication decreased bias.36 The prospective nature of data
interaction effect between IQ and prob- after exclusion of those children with collection in the ALSPAC allowed for
able DCD were significant at the 5% ASD, from 1.58 (95% CI: 1.01–2.48) to appropriate controlling of potential
level. Results of further exploratory 1.52 (95% CI: 0.96 –2.43) for nonverbal confounding factors, which previous
analysis suggested a significant inter- skills and from 1.87 (95% CI: 1.15–3.04) population-based studies have not
active effect between gender and prob- to 1.62 (95% CI: 0.95–2.75) for social done.5,37,38 We also attempted to minimize
able DCD for reading difficulties (5th communication skills. For comparison, the potential bias of missing data by
centile cutoff) in model 3 (Pinteraction ⫽ the ORs of having difficulties in each using multiple imputation by chained
.01) and model 4 (P ⫽ .01). Strata- trait at the 15th centile are presented equations.30
specific odds according to gender in Appendices 2 and 3; these showed Our case definition of probable DCD
showed that both genders had an in- similar results. used a multistep approach that incor-

TABLE 5 ORs (95% CIs) of Significant Difficulties in Developmental Traits (Using the 5th Centile Cutoff) for Children With Probable DCD Excluding Those
Children on the Autistic Spectrum, Compared With Control Subjects by Using the Multiple-Imputation Analysis Data Set
Model 1, P Model 2, OR P Model 3, OR P Model 4, OR P
Unadjusted OR (95% CI) (95% CI) (95% CI)
(95% CI)
Inattention or hyperactivity (n ⫽ 5646) 3.71 (2.50–5.52) ⬍.001 3.44 (2.28–5.18) ⬍.001 2.80 (1.83–4.29) ⬍.001 1.96 (1.14–3.36) .015
Expressive language (n ⫽ 5624) 3.06 (2.11–4.45) ⬍.001 2.83 (1.92–4.17) ⬍.001 1.98 (1.33–2.96) .001 1.37 (0.88–2.12) .159
Language comprehension (n ⫽ 5648) 2.39 (1.57–3.63) ⬍.001 2.22 (1.44–3.42) ⬍.001 1.80 (1.16–2.80) ⬍.001 1.36 (0.85–2.19) .200
Nonword repetition (n ⫽ 5637) 3.44 (2.47–4.80) ⬍.001 3.22 (2.29–4.53) ⬍.001 2.66 (1.88–3.78) ⬍.001 1.78 (1.21–2.61) .003
Nonverbal skills (n ⫽ 5204) 2.96 (1.96–4.46) ⬍.001 2.83 (1.85–4.31) ⬍.001 1.90 (1.22–2.94) ⬍.001 1.52 (0.96–2.43) .077
Social and communication (n ⫽ 5635) 3.30 (2.24–4.87) ⬍.001 2.99 (2.00–4.46) ⬍.001 2.62 (1.73–3.96) ⬍.001 1.62 (0.95–2.75) .075
Reading (n ⫽ 6791) 9.62 (7.32–12.65) ⬍.001 8.23 (6.12–11.06) ⬍.001 4.38 (3.13–6.13) ⬍.001 3.49 (2.39–5.08) ⬍.001
Spelling (n ⫽ 6702) 6.53 (5.02–8.49) ⬍.001 5.59 (4.22–7.41) ⬍.001 3.30 (2.42–4.50) ⬍.001 2.77 (1.99–3.85) ⬍.001
Model 2 controlled for child factors (gender, age at which test was performed, birth weight, gestation, and hearing) and parental factors (maternal education, housing tenure in pregnancy,
highest parental social class, financial difficulties score, antenatal maternal smoking, antenatal depression, and antenatal anxiety). Model 3 controlled for all the confounding factors in
model 2 ⫹ total IQ or performance IQ for language based skills (ie, WOLD, nonword repetition). Model 4 controlled for all confounding factors as in model 3 ⫹ all other developmental traits
not in that developmental domain.

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porated both poor motor coordination sociation between probable DCD and In summary, the complex difficulties
and impairment in ADL or handwriting. reading (which was especially appar- experienced by children with DCD can
We considered handwriting as a ent in girls) has potential implications best be understood by using a dynamic
marker of academic ability, as recom- for educational interventions, and ad- neuroconstructivist approach in
mended in the Leeds Consensus State- ditional research is needed in this which genetic, neurologic, and envi-
ment, as opposed to reading and spell- area by using more comprehensive ronmental factors interact multidirec-
ing, which were defined as outcome reading tests. tionally.49 Future work in the field of
variables in our analysis.7 Children did The neurobiology of DCD is complex, genetic epidemiology may help us un-
not have a medical examination as and different mechanisms have been derstand the neurobiology of this com-
part of their ALSPAC assessment, but proposed to explain the motor deficit mon developmental condition.
we linked ALSPAC-unique identifiers seen in DCD and the association with For clinicians, although it is desirable
with clinical records and IQ tests to ex- other developmental difficulties. The to diagnose and accurately classify de-
clude those children with known neu- overlap between DCD and attention- velopmental conditions in which the
rologic, chromosomal, and severe vi- deficit/hyperactivity disorder has been major impairment is in 1 domain, our
sual difficulties or an IQ of ⬍70. We supported by results of a recent twin results show that many children’s dif-
were able to consider the independent study that pointed to a potential ficulties do not fit into discrete diag-
association between motor function- shared genetic etiology.42 Fawcett and nostic categories. What is needed to
ing and each developmental trait, in Nicholson43 demonstrated impaired inform appropriate interventions is a
turn, after controlling for difficulties motor control in children with dyslexia careful documentation of the child’s
outside that domain of interest, effec- and highlighted the potential role of strengths and difficulties and an accu-
tively excluding (controlling for) chil- lobules VI and VIIB in the neocerebel- rate formulation of the individuals’
dren with attention difficulties and so- lum to explain these difficulties in complex multidimensional needs.
cial communication difficulties when adults.44 We documented a strong as-
sociation between probable DCD and CONCLUSIONS
considering reading skills and vice
versa. reading skills as well as with other de- We have shown that children with
velopmental difficulties that are hard probable DCD have an increased risk
In 1966, Clements39 proposed the term to explain by a localized deficit in the of wide-ranging difficulties outside the
minimal brain dysfunction in refer- cerebellum. motor domain. This has important clin-
ence to children of normal intelligence
There is increasing evidence for a ical implications for the assessment
who display “various combinations of and management of children with DCD,
shared genetic etiology of develop-
impairment in perception, conceptual- especially relating to their educational
mental conditions, with specific inter-
ization, language, memory, attention, needs. These associations need to be
est in the role of downstream gene tar-
or motor function.”40 The minimal- explored in greater depth to under-
gets to which proteins bind. In the case
brain-dysfunction concept has been stand their biological basis, the impli-
of the FOXP2 protein, these down-
criticized as being overinclusive; many stream genes have a wide array of cations for intervention, and the long-
studies have identified clusters of functions including neural growth, term outcomes for children with DCD.
symptoms but no overarching syn- synaptic plasticity, and neurotrans-
drome.40 In 1982, Gillberg et al31 de- mission.45 Others have hypothesized APPENDIX 1: REPORTING OF
scribed the overlap between attention, that children with DCD and MISSING DATA MODEL
motor, and perceptual deficits. The attention-deficit/hyperactivity disorder The number of children in the
ALSPAC data support the strong non- share a genetically determined distur- significant-difficulties group, taken as
causal association between probable bance in the dopamine pathway.46,47 the 5th centile, of each developmental
DCD and inattention proposed by Gill- Dopamine is thought to be the key neu- trait who had data on their DCD status
berg et al but also provide evidence for rotransmitter in many developmental varied from 266 (4.7% inattention and
a broader association, because chil- pathways, including motor planning, hyperactivity) to 501(7.5% spelling),
dren with probable DCD showed in- working memory, cognitive flexibility, with a mean of 346 (5.9%), where the
creased risk of significant problems language, reasoning, and sequencing; denominator is the number of children
with reading, spelling, social, and non- however, to date, no study has directly in the unadjusted model. The number
verbal skills, irrespective of hyperac- examined specific neurotransmitters of children in the multiple-imputation
tivity and inattention.41 The strong as- in children with DCD.48 data sets did not vary after addition of

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TABLE 6 Number of Children in the Unadjusted Model Compared With the Complete Case Analysis Logistic Regression Models 2, 3, and 4
No. (%) of Children No. of children With Probable No. of Children No. of Children No. of Children No. of Children
With Significant DCD in Unadjusted Analysis in the in the Adjusted in the Adjusted in the Adjusted
Difficulties (5th or in the Multiple-Imputation Unadjusted Complete Case Complete Case Complete Case
Centile Outcome) Who Analysis Data Set (N ⫽ 346 Complete Case Analysis Model 2 Analysis Model 3 Analysis Model 4
Had Data on DCD max) Analysis
Status
Inattention and hyperactivity 266 (4.7) 255 5646 4448 3882 3405
symptoms
Expressive language 334 (5.9) 250 5624 4351 4306 3441
Language comprehension 302 (5.4) 253 5648 4362 4315 3449
Nonword repetition 429 (7.6) 250 5637 4359 4313 3448
Nonverbal skills 275 (5.3) 233 5204 4032 3986 3460
Social and communication 306 (5.4) 253 5635 4445 3882 3715
Reading 353 (5.2) 342 6791 5096 4291 3455
Spelling 501 (7.5) 323 6702 5043 4264 3431

confounding factors and was equal to with missingness: family income; age rated into the imputation model for this
number of children in the unadjusted of the mother (binary older or younger outcome. Strata-specific odds according
complete case analysis. than 21 years); use of hot water in the to gender are presented in Table 4.
Multiple-imputation models were used household; index of crowding (ordered The wealth of prospectively collected
to create data sets to allow for missing categorical variable); parity (3 catego- data in the ALSPAC allows the analysis to
data only in the confounding factors. ries: first infant, second child, or ⱖ3 not only account for confounding factors
Multiple imputation by chained equa- children); ever used drugs; maternal but also account for factors that help to
tions was performed by using the “ICE” special-needs schooling; temperature explain missingness, thus supporting
command in Stata 9.2. Twenty sepa- of the house in winter; postnatal de-
the “missing-at-random” assumption.
rate, stacked data sets were created pression; or anxiety.
for the final analysis, which used the Of these factors, family income, age of
MIM command in Stata. ACKNOWLEDGMENTS
the mother, use of hot water in the
The United Kingdom Medical Research
The imputation was done twice, once household, crowding, and parity were
Council, the Wellcome Trust, and the
for model 3 and again for model 4, for associated with being missing in the
University of Bristol currently provide
each of the outcome variables. For data set (P ⬍ .01); these variables
were included in the final multiple- core support for the ALSPAC. Dr
model 3, variables included in the mul-
imputation model. Lingam is funded by a Personal Award
tiple imputation model included all
Scheme Researcher Development
those variables in the final regression In addition, for the multiple-imputation
Award from the National Institute for
model (model 3) plus variables that model 4, all the developmental traits
predicted missingness in the con- Health Research. This publication is
were added to create the imputed data
founders. Within the ALSPAC, we know the work of the authors, and Dr Lingam
set. Binary variables and categorical
that socioeconomic factors affect loss will serve as guarantor for the con-
variables used logistic, ordinal, and
to follow-up. It has been shown that tents of this article.
multinomial regression, as appropri-
children from lower socioeconomic ate, specified in the ICE command. IQ We are grateful to all the families
groups were less likely to attend for was normally distributed and incorpo- who took part in this study, the mid-
assessment than children from more rated using linear regression in the wives for their help in recruiting
affluent, well-educated families.8 imputation model. A significant inter- them, and the whole ALSPAC team,
Variables that predicted missingness active effect between gender and prob- which includes interviewers, com-
in the confounding factors were as- able DCD was found for reading in puter and laboratory technicians,
sessed by using logistic regression. model 3 (Pinteraction ⫽ .01) and model 4 clerical workers, research scien-
The following factors were selected for (Pinteraction ⫽.01). An interaction term, tists, volunteers, managers, recep-
exploration if they were associated gender ⫻ probable DCD, was incorpo- tionists and nurses.

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APPENDIX 2 ORs (95% CIs) of Significant Difficulties in Developmental Traits (Using the 15th Centile Cutoff) for Children With Probable DCD Compared
With Control Subjects by Using the Complete Case Data Set
Model 1, P Model 2, OR P Model 3, OR P Model 4, OR P
Unadjusted OR (95% CI) (95% CI) (95% CI)
(95% CI)
Any severe inattention or hyperactivity 3.37 (2.57–4.43) ⬍.001 3.01 (2.16–4.18) ⬍.001 2.27 (1.54–3.34) ⬍.001 1.68 (1.05–2.69) .030
symptoms (n ⫽ 5665 max)
Expressive language (n ⫽ 5624 max) 2.96 (2.22–3.93) ⬍.001 2.91 (2.04–4.16) ⬍.001 2.08 (1.43–3.02) ⬍.001 1.38 (0.87–2.17) .167
Language comprehension (n ⫽ 5648 max) 2.33 (1.72–3.15) ⬍.001 1.95 (1.33–2.88) .001 1.56 (1.05–2.33) .028 1.43 (0.90–2.26) .130
Short-term memory (n ⫽ 5637 max) 2.87 (2.18–3.78) ⬍.001 2.33 (1.63–3.32) ⬍.001 1.96 (1.37–2.82)a ⬍.001 1.54 (1.0–2.35) .048
Nonverbal skills (n ⫽ 5204 max) 2.86 (2.14–3.83) ⬍.001 2.68 (1.86–3.86) ⬍.001 2.07 (1.42–3.03) ⬍.001 1.79 (1.17–2.75) .008
Social communication skills (n ⫽ 5635 max) 2.82 (2.11–3.77) ⬍.001 2.74 (1.93–3.89) ⬍.001 2.12 (1.41–3.20) ⬍.001 1.49 (0.91–2.44) .111
Reading (n ⫽ 6791 max) 6.41 (5.13–8.02) ⬍.001 4.75 (3.57–6.33) ⬍.001 2.59 (1.79–3.75) ⬍.001 1.96 (1.26–3.04) .003
Spelling (n ⫽ 6702 max) 6.31 (5.01–7.94) ⬍.001 4.74 (3.53–6.38) ⬍.001 2.37 (1.62–3.46) ⬍.001 2.16 (1.39–3.34) .001
a Interaction term probable DCD and IQ (P ⫽ .03).
Model 2 controlled for child factors (gender, age when test performed, birth weight, gestation and hearing) and parental factors (maternal education, housing tenure in pregnancy, highest
parental social class, financial difficulties score, antenatal maternal smoking, antenatal depression and antenatal anxiety). Model 3 controlled for all the confounding factors in model 2 ⫹
total IQ or performance IQ for language based skills (ie, WOLD, nonword repetition). Model 4 controlled for all confounding factors as in model 3 ⫹ all other developmental traits not in that
developmental domain being tested.

APPENDIX 3 ORs (95% CIs) of Significant Difficulties in Developmental Traits (Using the 15th Centile Cutoff) for Children With Probable DCD Compared
With Control Subjects by Using the Multiple-Imputation Data Set
Model 1, P Model 2, OR P Model 3, OR P Model 4, OR P
Unadjusted OR (95% CI) (95% CI) (95% CI)
(95% CI)
Any severe inattention or hyperactivity 3.37 (2.57–4.43) ⬍.001 3.09 (2.33–4.09) ⬍.001 2.72 (2.04–3.62) ⬍.001 1.88 (1.34–2.63) ⬍.001
symptoms (n ⫽ 5665)
Expressive language (n ⫽ 5624) 2.96 (2.22–3.93) ⬍.001 2.70 (2.00–3.64) ⬍.001 1.92 (1.41–2.62) ⬍.001 1.26 (0.90–1.76) .17
Language comprehension (n ⫽ 5648) 2.33 (1.72–3.15) ⬍.001 2.19 (1.60–2.99) ⬍.001 1.76 (1.28–2.42) .001 1.36 (0.97–1.90) .07
Short-term memory (n ⫽ 5637) 2.87 (2.18–3.78) ⬍.001 2.70 (2.03–3.59) ⬍.001 2.24 (1.68–2.30) ⬍.001 1.43 (1.04–1.95) .026
Nonverbal skills (n ⫽ 5204) 2.86 (2.14–3.83) ⬍.001 2.72 (2.02–3.66) ⬍.001 2.10 (1.55–2.86) ⬍.001 1.85 (1.34–2.54) ⬍.001
Social communication skills (n ⫽ 5635) 2.82 (2.11–3.77) ⬍.001 2.64 (1.96–3.56) ⬍.001 2.34 (1.72–3.18) ⬍.001 1.38 (0.96–1.97) .081
Reading (n ⫽ 6791) 6.41 (5.13–8.02) ⬍.001 5.74 (4.53–7.27) ⬍.001 3.60 (2.76–4.71) ⬍.001 2.93 (2.19–3.90) ⬍.001
Spelling (n ⫽ 6702) 6.31 (5.01–7.94) ⬍.001 5.51 (4.31–7.04) ⬍.001 3.50 (2.67–4.59) ⬍.001 2.85 (2.14–3.81) ⬍.001
Model 2 controlled for child factors (gender, age when test performed, birth weight, gestation and hearing) and parental factors (maternal education, housing tenure in pregnancy, highest
parental social class, financial difficulties score, antenatal maternal smoking, antenatal depression and antenatal anxiety). Model 3 controlled for all the confounding factors in model 2 ⫹
total IQ or performance IQ for language based skills (ie, WOLD, nonword repetition). Model 4 controlled for all confounding factors as in model 3 ⫹ all other developmental traits not in that
developmental domain being tested.

e1118 LINGAM et al
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The Association Between Developmental Coordination Disorder and Other
Developmental Traits
Raghu Lingam, Jean Golding, Marian J. Jongmans, Linda P. Hunt, Matthew Ellis and
Alan Emond
Pediatrics originally published online October 18, 2010;

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The Association Between Developmental Coordination Disorder and Other
Developmental Traits
Raghu Lingam, Jean Golding, Marian J. Jongmans, Linda P. Hunt, Matthew Ellis and
Alan Emond
Pediatrics originally published online October 18, 2010;

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