The Association Between Developmental Coordination Disorder and Other Developmental Traits

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The Association Between Developmental Coordination

Disorder and Other Developmental Traits

WHAT’S KNOWN ON THIS SUBJECT: Previous clinic-based samples have shown an overlap between developmental coordination disorder, ADHD, autism, and dyslexia. However, there has been limited population-based work on the association of DCD with other developmental traits that account for potential confounding factors.

WHAT THIS STUDY ADDS: Using data from the ALSPAC (N⫽6902 maximum), these study results show that children with probable DCD have an increased risk of difﬁculties in attention, short-term memory, and academic and social skills, after controlling for confounding factors including IQ and other developmental traits.

abstract

OBJECTIVE:To explore associations between developmental coordina-tion disorder (DCD) and attencoordina-tion, language, social skills, and aca-demic ability in a population-based cohort.

METHODS:We analyzed data (N⫽6902) from the Avon Longitudinal Study of Parents and Children (ALSPAC). Probable DCD was defined as children below the 15th centile of the ALSPAC Coordination Test aged 7 years with functional impairment in activities of daily living or handwriting, excluding children with neurologic difficulties or an IQ of⬍70. Four developmental domains were assessed by using standardized tests between the ages of 7.5 and 9 years: attention; language skills (expressive language, compre-hension, short-term memory); social skills (nonverbal skills and social communication); and academic ability (reading and spelling). The worst 5% of each trait was used to define impairment. We used multiple logistic regression models to assess the association between probable DCD and each trait. Our final model controlled for IQ, socioeconomic factors, and other developmental traits not in the domain assessed.

RESULTS:A total of 346 (5.0%) children met criteria for probable DCD. Probable DCD was associated with difﬁculties in attention (odds ratio [OR]: 1.94 [95% conﬁdence interval (CI): 1.17–3.24]), nonword repeti-tion (OR: 1.83 [95% CI: 1.26 –2.66]), social communicarepeti-tion (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

AUTHORS:Raghu Lingam, MBChB, MSc, MRCPCH,a_Jean

Golding, PhD, DSc, FMedSci,a_{Marian J. Jongmans, PhD,}b,c

Linda P. Hunt, PhD,d_{Matthew Ellis, MB, ChB, PhD,}

MRCPCH,a_{and Alan Emond, MB, MD, FRCPCH}a

a_{Centre for Child and Adolescent Health, School of Social and}

Community-Based Medicine, University of Bristol, Bristol, United Kingdom;b_{Department of Pediatric Psychology, Wilhelmina}

Children’s Hospital, Utrecht, Netherlands;c_{University Medical}

Center Utrecht and Department of Special Education, Faculty of Social Sciences, Utrecht University, Utrecht, Netherlands; and

d_{School of Clinical Sciences, University of Bristol, Bristol, United}

Kingdom

KEY WORDS

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 Fourth Edition

ADL—activity of daily living SLI—speciﬁc-language impairment ASD—autism spectrum disorder

ALSPAC—Avon Longitudinal Study of Parents and Children DAWBA—Development and Well-being Assessment MABC—Movement Assessment Battery for Children WOLD—Wechsler Objective Language Dimensions SCDC—Social and Communication Disorders Checklist WORD—Wechsler Objective Reading Dimensions OR—odds ratio

CI—conﬁdence interval

www.pediatrics.org/cgi/doi/10.1542/peds.2009-2789

doi:10.1542/peds.2009-2789

Accepted for publication Jul 20, 2010

Address correspondence to Raghu Lingam, MBChB, MSc, MRCPCH, Centre for Child and Adolescent Health, Department of Community-Based Medicine, University of Bristol, Bristol BS6 6JS, United Kingdom. E-mail: [email protected]

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

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Developmental coordination disorder (DCD) is deﬁned according to the Diag-nostic and Statistical Manual of Men-tal Disorders, Fourth Edition(DSM-IV) criteria, as a condition marked by a severe impairment in the development of motor coordination, which signiﬁ-cantly interferes with activities of daily living (ADL) and/or academic achieve-ment, not caused by a general medical condition or severe learning impair-ment.1_{Although there is extensive}

lit-erature describing the overlap be-tween DCD and conditions such as

attention-deﬁcit/hyperactivity

disor-der, speciﬁc-language impairment

(SLI), autism spectrum disorder (ASD), and dyslexia in clinic-based samples, few population-based studies have ad-equately controlled for confounding factors.2–5

The aim of our study was to assess the association between children with probable DCD, deﬁned by using criteria based on the DSM-IV, and difﬁculties in attention, language, and short-term memory; social skills; and academic ability (reading and spelling) within a prospective population-based sample, accounting for known confounding factors and the colinearity of the devel-opmental traits themselves.

PATIENTS AND METHODS

Sample

The Avon Longitudinal Study of Parents and Children (ALSPAC) is a prospective population-based birth cohort study designed to investigate the interaction of environment and genotype on the health and development of children. The study investigators invited all pregnant women in the geographically deﬁned area of Avon, southwest En-gland, with an expected date of deliv-ery between April 1, 1991, and Decem-ber 31, 1992, to take part. The study contains data on 14 062 live births, of which 13 988 were still alive at 12 months of age; active contact currently

is maintained with⬃10 000 children.6

Mothers of infants in the ALSPAC were broadly representative of the rest of the United Kingdom at the 1991 census. Further details of study recruitment, retention, and data collection have been described previously.6

Data have been collected on a variety of developmental traits by using face-to-face assessments at special clinics,

parental self-completion

question-naires, and linked education and health records. Data on potential ante-natal and postante-natal confounding fac-tors were collected prospectively from a number of questionnaires.

Participating parents provided in-formed consent for testing sessions, and assent was gained from the chil-dren. Ethical approval for the study was obtained from the ALSPAC Law and Ethics Committee and the local re-search ethics committees.

Measures

Exposure Variable: Probable DCD

Children with probable DCD were de-ﬁned by using the DSM-IV criteria, adapted for research by using the 2006 Leeds Consensus Statement.1,7,8

Chil-dren were deﬁned as having probable DCD if they met all 4 DSM-IV criteria for DCD: poor motor coordination (crite-rion A), which causes functional im-pairment in ADL, or academic achieve-ment (criterion B) not caused by a general medical condition or severe learning difﬁculties (exclusion criteria C and D).1_{Full details of the case}

deﬁ-nition and the numbers of children at each stage of deﬁnition have previ-ously been described.8

Motor skills of children were assessed between 7 and 8 years using the AL-SPAC Coordination Test, which con-sisted of the subtests derived from the Movement Assessment Battery for

Children (MABC).9 _{The subtests were}

selected to test the 3 realms of

coordi-nation: manual dexterity (placing pegs task); ball skills (throwing bean bag into box); and balance (heel-to-toe walking). These motor subtests have been shown to have concurrent valid-ity with other similar coordination tests and represent the 3 domains of coordination using principal compo-nent analysis of original

standardiza-tion data from the MABC.8,10 _{The 5th}

centile of a standardized motor coordi-nation test is generally used to define severe motor impairment; children be-tween the 5th and 15th centile are con-sidered at risk of impairment. We used the 15th centile of the ALSPAC Coordi-nation Test to define children as having or being at risk of coordination difficul-ties in keeping with the MABC manual and previous literature.9,11

Those children below the 15th centile on motor testing were then said to have functional impairment in motor skills if, in addition, they either failed their National Curriculum Key Stage 1 writing test or they were below the 15th centile of a 23-item ADL scale de-rived from parent-completed

question-naires.8 _{Those children with a known}

visual deﬁcit or neurologic condition such as cerebral palsy were excluded,

as were children with an IQ of ⬍70.

Children with an ASD diagnosis, identi-ﬁed from linked education and health records, were not excluded as recom-mended by the Leeds Consensus

State-ment.7 _{However, secondary analyses}

excluding these children were per-formed. The multistage deﬁnition used met DSM-IV criteria for DCD. However, because we used the 15th centile, rather than the more conservative 5th centile, of the motor coordination test, we described our population as having probable DCD in keeping with our pre-vious work.8

After excluding children with an IQ of

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test or the ADL scale; of these, 346 chil-dren representing 5% of our eligible cohort met criteria for probable DCD.

Outcome Variables

Between the ages of 7 and 9 years, the children of the ALSPAC were assessed by using a number of standardized tests and subtests that were grouped into 4 major domains of develop-ment: (1) attention and hyperactivity; (2) language skills and short-term memory; (3) social skills; and (4) ac-ademic ability.

Inattention and hyperactivity were as-sessed by using the Development and Well-being Assessment (DAWBA) at

91 months of age.12 _{The DAWBA is}

a parent-completed,

questionnaire-based assessment that includes 18 questions relating to the child’s activ-ity and attention.

Speech and language were tested by using items from the oral expres-sion and language comprehenexpres-sion subtests of the Wechsler Objective

Lan-guage Dimensions (WOLD).13

Short-term memory was assessed by using a shortened version of the Children’s Test of Nonword Repetition.14_Nonword

repetition has been shown to be strongly associated with language de-velopment and was therefore grouped within this developmental domain.15

The domain of social skills included nonverbal skills and social communi-cation. Nonverbal impairment was as-sessed by using the faces subtest of the Diagnostic Analysis of Nonverbal Accuracy, and social communication abilities were measured by using the Social and Communication Disorders Checklist (SCDC).16,17_{Measures of}

aca-demic ability consisted of reading, as-sessed by using the basic-reading subtest of the Wechsler Objective

Reading Dimensions (WORD),18 _and

spelling was assessed by using 15

age-appropriate words developed by

Nunes and Bryant.19_{All tests were}

per-formed by trained observers at face-to-face research clinics, except the DAWBA and the SCDC, which were parent-completed questionnaires.

Possible Confounding or Mediating Factors

Potential confounding factors were se-lected after appraisal of the relevant literature.20_{Factors were divided into}

child and parental/environmentally re-lated confounding factors and added to the model in blocks to assess the effect on any association between

ex-posure and outcome.21

Child-related confounding factors

were gender, birth weight (ⱕ2500 and

⬎2500 g), gestation (⬍37 and ⱖ37

weeks’ gestation), hearing difﬁculties, and cognitive ability (IQ). Children were deﬁned as having normal hear-ing thresholds if bilateral average air

conduction wasⱖ20 dB on testing. IQ

was measured by using alternate items of the Wechsler Intelligence Scale for Children III at a mean age of

8.7 years.22 _{For language-based}

out-comes, performance IQ was con-trolled. For all other outcome mea-sures, total IQ was controlled. Gender and IQ were tested as potential effect modiﬁers.

Parental and environmental confound-ing factors were highest maternal ed-ucational attainment (3 categories), highest parental social class (non-manual [I, II, and III non(non-manual], III manual, and IV and V manual), housing tenure of the family in pregnancy (owned or rented), ﬁnancial difﬁcul-ties in pregnancy (5-point scale de-rived from maternal report of ability to afford food, clothing, heating, ac-commodation, and items for the in-fant), maternal smoking in preg-nancy (ever or never), and antenatal depression and anxiety using the Ed-inburgh Postnatal Depression Scale and Crown–Crisp Experiential Index respectively.23–25

Analysis

Logistic regression models were used to assess the association between the exposure variable probable DCD and each of the 8 developmental traits in turn as outcomes.

All tests apart from the comprehen-sion subtests from the WOLD, the read-ing test of the WORD, and the test of nonword repetition had a skewed dis-tribution even after logarithmic trans-formation. Measures were dichoto-mized by using both the 5th and the 15th centiles to define significant diffi-culties, as done previously.24,26–28

We first looked at the unadjusted asso-ciation between probable DCD and each developmental trait (model 1). Adjustment was then made for all child and parental factors excluding IQ (model 2); model 3 added IQ. For the final model (model 4), adjustment was also made for all the other develop-mental traits not in the domain under investigation. For example, for the out-come variable reading (5th centile), the final model adjusted for all child and parental factors along with all the traits outside the academic ability do-main (ie, inattention and hyperactivity, nonverbal skills, social communica-tion, expressive language, language

comprehension, and short-term

memory).

The number of children in each model differed, because not all children at-tended the various tests and returned questionnaires. To deal with the poten-tial bias introduced by these missing data, we used multiple imputation by chained equations to impute missing data in the confounding factors.29,30

Further details of the multiple impu-tation models are reported in Appen-dix 1.

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complete case data set and by remov-ing those children with a known ASD diagnosis. All statistical analyses used Stata 9.2 (Stata Corp, College Station, TX).

RESULTS

The characteristics of the 346 children with probable DCD compared with our 6556 normally developing control sub-jects are listed in Table 1. As reported previously, children with probable DCD were more likely to be male, have a lower birth weight, and come from a more deprived social background8

(Ta-ble 1, characteristics of those children with probable DCD compared with con-trol subjects).

Of a maximum of 6902 children, the number of children who completed de-velopmental outcome tests ranged from 5204 to 6791 (mean: 5863), of which an average of 270 children had probable DCD. In the complete case analysis, the total number of children in the ﬁnal analysis was additionally reduced when confounding factors were added (illustrated in Fig 1). This was not the case when multiple impu-tation was used, because missing data were accounted for in the confounding factors. Further details on the number of children in each model are presented in Appendix 1 (including Table 6).

The odds ratios (ORs) of having signif-icant difficulties (5th centile) in each developmental trait for children with probable DCD compared with control subjects are presented in Tables 2 and 3, for the complete case set and multi-ple imputation data sets, respectively. Children with probable DCD had signif-icantly increased odds of having diffi-culties in all the developmental do-mains investigated in the unadjusted model (model 1) and after controlling for child and parental factors (model 2). The addition of IQ decreased the ORs, but there still was a significantly increased odds of having difficulties in

TABLE 1 Characteristics of Those Children With Probable DCD Compared to Controls

Control Subjects

Probable DCD

Signiﬁcance,P

N 6556 max 346 max

Child factors Gender,n(%)

Boys 3255 (49.7) 217 (62.7) ⬍.001a

Girls 3301 (50.4) 129 (37.3)

Gestation,n(%)

ⱖ37 wk 6005 (95.0) 302 (91.8) .01a

⬍37 wk 316 (5.0) 27 (8.2)

n 6321 329

Birth weight,n(%)

⬎2500 g 5956 (95.2) 294 (90.7) ⬍.001a

ⱕ2500 g 301 (4.8) 30 (9.3)

n 6257 324

Ethnicity,n(%)

White 6237 (95.7) 324 (93.6) .07a

Nonwhite 280 (4.3) 22 (6.4)

n 6517 346

IQ, mean (SD) 105.67 (15.4) 93.90 (16.4) ⬍.001b

n 5375 244

Hearing,n(%)

Normal 5606 (92.4) 278 (89.4) .05a

Either side not reaching thresholds 459 (7.6) 33 (10.6)

n 6065 311

Parental and environmental factors,n(%) Highest maternal or paternal social class

I, II, and III nonmanual 4982 (85.5) 222 (76.3) ⬍.001a

IIIM 606 (10.4) 46 (15.8)

IV and V 238 (4.1) 23 (7.9)

n 5826 291

Housing tenure at 8 wk gestation,n(%)

Owned 5077 (84.9) 238 (76.3) ⬍.001a

Rented 900 (15.1) 74 (23.7)

n 5977 312

Maternal education highest qualiﬁcation,n(%)

A-level/degree 2569 (42.2) 121 (39.0) .001a

O level 2210 (36.3) 94 (30.3)

CSE/vocational 1313 (21.6) 95 (30.7)

n 6092 310

Maternal age at delivery,n(%)

⬍21 y 198 (3.1) 12 (3.7) .60a

ⱖ21 y 6123 (96.9) 317 (96.4)

n 6321 329

Ever smoked in pregnancy,n(%)

Never 4995 (80.0) 246 (75.7) .06a

Ever 1247 (20.0) 79 (24.3)

n 6242 325

Antenatal depression at 32 wk gestation using the Edinburgh Postnatal Depression Scale,n(%)

Not depressed 5166 (87.3) 243 (82.4) .01a

EPDSⱕ12

Depressed 752 (12.7) 52 (17.6)

n 5918 295

EPDSⱖ13

Antenatal anxiety using the Crown Crisp Experimental Index 32 wk gestation,n(%)

Anxiety scoreⱕ9 5101 (88.5) 240 (83.9) .02a

Anxiety scoreⱖ10 660 (11.5) 46 (16.1)

n 5761 286

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each domain for those children in the probable-DCD group. Model 4, when using both the multiple imputation and complete case data sets, showed a persistent strong association between probable DCD and difﬁculties in inat-tention/hyperactivity, nonword repeti-tion, reading, and spelling after adjust-ment for the other traits outside the domain under investigation and an in-creased risk of difﬁculties in nonver-bal skills and social communication only in the multiple-imputation model. The differences seen between the com-plete case and imputed data sets can be attributed to potential bias intro-duced by missing data, because model 4 of the complete case data

set had ⬎2000 fewer children than

the unadjusted imputed model for each analysis.

6902 children were 7 and 8 y when attending the Focus@7 and completing the ADL questionnaire or handwriting test (IQ < 70 excluded)

5646 children also had results for the DAWBA

2241 children had at least 1 missing factor from the confounding factors in model 4

3405 children had data from exposure, outcome, and all potential confounding factors

1256 children missing from the DAWBA

FIGURE 1

Number of children in the ﬁnal analysis for inattention and hyperactivity symptoms measured by using the DAWBA.

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, Unadjusted OR

(95% CI)

P Model 2, OR (95% CI)

P

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

(95% CI)

P

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

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The association between probable DCD and the test of nonword repetition pre-sented in Tables 2 and 3 did not control for expressive language or compre-hension. An additional analysis con-trolling for these variables in the multiple-imputation model 4 did not weaken the association of probable DCD and nonword repetition (OR: 1.76 [95% conﬁdence interval (CI): 1.21–2.58]).

None of the likelihood ratio tests for an interaction effect between IQ and prob-able DCD were significant at the 5% level. Results of further exploratory analysis suggested a significant inter-active effect between gender and prob-able DCD for reading difficulties (5th centile cutoff) in model 3 (P_interaction⫽

.01) and model 4 (P ⫽ .01).

Strata-speciﬁc odds according to gender showed that both genders had an

in-creased risk of reading difﬁculties, but girls had a higher risk than boys (Table 4).

Of the original 346 children with prob-able DCD, 19 were on the autistic spec-trum as compared with 15 control chil-dren. Results of sensitivity analysis excluding these children showed simi-lar results to those obtained with these children included (Table 5). The OR for difﬁculties with nonverbal skills and social communication decreased after exclusion of those children with ASD, from 1.58 (95% CI: 1.01–2.48) to 1.52 (95% CI: 0.96 –2.43) for nonverbal skills and from 1.87 (95% CI: 1.15–3.04) to 1.62 (95% CI: 0.95–2.75) for social communication skills. For comparison, the ORs of having difﬁculties in each trait at the 15th centile are presented in Appendices 2 and 3; these showed similar results.

DISCUSSION

Using a large, prospective cohort study, we have shown that, after accounting for potential confounding factors, children with probable DCD have an increased risk of other common developmental dif-ﬁculties. Our ﬁndings build on the exist-ing evidence based on selected samples.

Previous longitudinal work used

teacher-completed questionnaires to screen children for attention, speech and language, and motor difﬁculties, which makes the results of these studies difﬁcult to interpret in terms of comor-bidity across developmental domains.31–33

Kaplan et al34_{and Dewey et al}35_showed

signiﬁcant overlap between DCD,

attention-deﬁcit/hyperactivity disorder, and learning difﬁculties in a sample re-cruited from clinics, special schools, and resource classrooms. We, in contrast, used a population-based sample without the use of an initial screening question-naire, which reduced potential referral bias.36 _{The prospective nature of data}

collection in the ALSPAC allowed for appropriate controlling of potential confounding factors, which previous

population-based studies have not

done.5,37,38_{We also attempted to minimize}

the potential bias of missing data by using multiple imputation by chained equations.30

Our case definition of probable DCD used a multistep approach that incor-TABLE 4 Gender-Specific ORs (95% CIs) of Reading Difficulty (5th Centile) in the Complete Case and

Multiple-Imputation Analyses

Complete Case Analysis Model 3 P Model 4 P

Probable DCD

Boys 2.84 (1.58–5.11) ⬍.001 2.67 (1.32–5.42) .006

Girls 11.73 (4.67–29.49) ⬍.001 15.25 (5.19–44.79) ⬍.001 Multiple-imputation analysis

probable DCD

Boys 3.35 (2.26–4.97) ⬍.001 2.25 (1.45–3.49) ⬍.001

Girls 9.62 (5.48–16.87) ⬍.001 7.45 (4.07–13.62) ⬍.001

Model 3 controlled for child factors (gender, age at which test was performed, birth weight, and gestation 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)⫹IQ (total) or IQ performance controlled for language-based skills (WOLD, nonword repetition) as a continuous variable. Model 4⫹other developmental traits not

in that developmental domain.

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

(95% CI)

P

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

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porated both poor motor coordination and impairment in ADL or handwriting.

We considered handwriting as a

marker of academic ability, as recom-mended in the Leeds Consensus State-ment, as opposed to reading and spell-ing, which were deﬁned as outcome

variables in our analysis.7_{Children did}

not have a medical examination as part of their ALSPAC assessment, but we linked ALSPAC-unique identiﬁers with clinical records and IQ tests to

ex-clude those children with known neu-rologic, chromosomal, and severe

vi-sual difﬁculties or an IQ of ⬍70. We

were able to consider the independent

association between motor function-ing and each developmental trait, in turn, after controlling for difﬁculties outside that domain of interest, effec-tively excluding (controlling for)

chil-dren with attention difﬁculties and so-cial communication difﬁculties when considering reading skills and vice versa.

In 1966, Clements39_{proposed the term}

minimal brain dysfunction in refer-ence to children of normal intelligrefer-ence

who display “various combinations of impairment in perception, conceptual-ization, language, memory, attention,

or motor function.”40 _The

minimal-brain-dysfunction concept has been

criticized as being overinclusive; many studies have identiﬁed clusters of symptoms but no overarching syn-drome.40 _{In 1982, Gillberg et al}31

de-scribed the overlap between attention, motor, and perceptual deﬁcits. The ALSPAC data support the strong non-causal association between probable DCD and inattention proposed by

Gill-berg et al but also provide evidence for a broader association, because chil-dren with probable DCD showed in-creased risk of signiﬁcant problems

with reading, spelling, social, and non-verbal skills, irrespective of hyperac-tivity and inattention.41_{The strong}

as-sociation between probable DCD and reading (which was especially appar-ent in girls) has potappar-ential implications for educational interventions, and ad-ditional research is needed in this area by using more comprehensive reading tests.

The neurobiology of DCD is complex, and different mechanisms have been proposed to explain the motor deficit seen in DCD and the association with other developmental difficulties. The overlap between DCD and attention-deficit/hyperactivity disorder has been supported by results of a recent twin study that pointed to a potential shared genetic etiology.42_{Fawcett and}

Nicholson43 _{demonstrated impaired}

motor control in children with dyslexia and highlighted the potential role of lobules VI and VIIB in the neocerebel-lum to explain these difﬁculties in

adults.44_{We documented a strong}

as-sociation between probable DCD and reading skills as well as with other de-velopmental difﬁculties that are hard to explain by a localized deﬁcit in the cerebellum.

There is increasing evidence for a shared genetic etiology of develop-mental conditions, with speciﬁc inter-est in the role of downstream gene tar-gets to which proteins bind. In the case of the FOXP2 protein, these down-stream genes have a wide array of functions including neural growth, synaptic plasticity, and

neurotrans-mission.45 _{Others have hypothesized}

that children with DCD and

attention-deﬁcit/hyperactivity disorder share a genetically determined

distur-bance in the dopamine pathway.46,47

Dopamine is thought to be the key neu-rotransmitter in many developmental pathways, including motor planning, working memory, cognitive ﬂexibility, language, reasoning, and sequencing; however, to date, no study has directly examined speciﬁc neurotransmitters in children with DCD.48

In summary, the complex difﬁculties experienced by children with DCD can best be understood by using a dynamic

neuroconstructivist approach in

which genetic, neurologic, and envi-ronmental factors interact multidirec-tionally.49 _{Future work in the ﬁeld of}

genetic epidemiology may help us un-derstand the neurobiology of this com-mon developmental condition.

For clinicians, although it is desirable to diagnose and accurately classify de-velopmental conditions in which the major impairment is in 1 domain, our results show that many children’s dif-ficulties do not fit into discrete diag-nostic categories. What is needed to inform appropriate interventions is a careful documentation of the child’s strengths and difficulties and an accu-rate formulation of the individuals’ complex multidimensional needs.

CONCLUSIONS

We have shown that children with probable DCD have an increased risk of wide-ranging difﬁculties outside the motor domain. This has important clin-ical implications for the assessment and management of children with DCD, especially relating to their educational needs. These associations need to be explored in greater depth to under-stand their biological basis, the impli-cations for intervention, and the long-term outcomes for children with DCD.

APPENDIX 1: REPORTING OF MISSING DATA MODEL

The number of children in the

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confounding factors and was equal to number of children in the unadjusted complete case analysis.

Multiple-imputation models were used to create data sets to allow for missing data only in the confounding factors. Multiple imputation by chained equa-tions was performed by using the “ICE” command in Stata 9.2. Twenty sepa-rate, stacked data sets were created for the ﬁnal analysis, which used the MIM command in Stata.

The imputation was done twice, once for model 3 and again for model 4, for each of the outcome variables. For model 3, variables included in the mul-tiple imputation model included all those variables in the ﬁnal regression model (model 3) plus variables that predicted missingness in the con-founders. Within the ALSPAC, we know that socioeconomic factors affect loss to follow-up. It has been shown that children from lower socioeconomic groups were less likely to attend for assessment than children from more afﬂuent, well-educated families.8

Variables that predicted missingness in the confounding factors were as-sessed by using logistic regression. The following factors were selected for exploration if they were associated

with missingness: family income; age of the mother (binary older or younger than 21 years); use of hot water in the household; index of crowding (ordered categorical variable); parity (3 catego-ries: ﬁrst infant, second child, or ⱖ3 children); ever used drugs; maternal special-needs schooling; temperature of the house in winter; postnatal de-pression; or anxiety.

Of these factors, family income, age of the mother, use of hot water in the household, crowding, and parity were associated with being missing in the

data set (P ⬍ .01); these variables

were included in the ﬁnal multiple-imputation model.

In addition, for the multiple-imputation model 4, all the developmental traits were added to create the imputed data set. Binary variables and categorical variables used logistic, ordinal, and multinomial regression, as appropri-ate, speciﬁed in the ICE command. IQ was normally distributed and incorpo-rated using linear regression in the imputation model. A signiﬁcant inter-active effect between gender and prob-able DCD was found for reading in model 3 (P_interaction⫽.01) and model 4 (P_interaction ⫽.01). An interaction term,

gender ⫻probable DCD, was

incorpo-rated into the imputation model for this outcome. Strata-speciﬁc odds according to gender are presented in Table 4.

The wealth of prospectively collected data in the ALSPAC allows the analysis to not only account for confounding factors but also account for factors that help to explain missingness, thus supporting the “missing-at-random” assumption.

ACKNOWLEDGMENTS

The United Kingdom Medical Research Council, the Wellcome Trust, and the

University of Bristol currently provide core support for the ALSPAC. Dr Lingam is funded by a Personal Award

Scheme Researcher Development

Award from the National Institute for Health Research. This publication is the work of the authors, and Dr Lingam will serve as guarantor for the con-tents of this article.

We are grateful to all the families who took part in this study, the mid-wives for their help in recruiting them, and the whole ALSPAC team, which includes interviewers,

com-puter and laboratory technicians, clerical workers, research scien-tists, volunteers, managers, recep-tionists and nurses.

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 With Signiﬁcant Difﬁculties (5th Centile Outcome) Who

Had Data on DCD Status

No. of children With Probable DCD in Unadjusted Analysis or in the Multiple-Imputation

Analysis Data Set (N⫽346 max)

No. of Children in the Unadjusted Complete Case

Analysis

No. of Children in the Adjusted Complete Case Analysis Model 2

Inattention and hyperactivity symptoms

266 (4.7) 255 5646 4448 3882 3405

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

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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

(95% CI)

P

Any severe inattention or hyperactivity symptoms (n⫽5665 max)

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

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

(95% CI)

P

Any severe inattention or hyperactivity symptoms (n⫽5665)

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

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⫹

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DOI: 10.1542/peds.2009-2789 originally published online October 18, 2010;

2010;126;e1109

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The Association Between Developmental Coordination Disorder and Other Developmental Traits