Mental Health Difficulties in Children With Developmental Coordination Disorder Raghu Lingam, Marian J.

Jongmans, Matthew Ellis, Linda P. Hunt, Jean Golding and Alan Emond Pediatrics 2012;129;e882; originally published online March 26, 2012; DOI: 10.1542/peds.2011-1556

The online version of this article, along with updated information and services, is located on the World Wide Web at:
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PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly publication, it has been published continuously since 1948. PEDIATRICS is owned, published, and trademarked by the American Academy of Pediatrics, 141 Northwest Point Boulevard, Elk Grove Village, Illinois, 60007. Copyright 2012 by the American Academy of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.

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Mental Health Difculties in Children With Developmental Coordination Disorder

WHAT S KNOWN ON THIS SUBJECT: Cross-sectional studies have shown an increased risk of mental health difculties in children with developmental coordination disorder. However, there has been limited longitudinal research in this area controlling for confounding factors and assessing the role of potential mediators. WHAT THIS STUDY ADDS: Children with "probable" developmental coordination disorder at 7 years had a signicantly increased risk mental health difculties at 10 years. Protective factors for self-reported depression included high IQ, high self-esteem, good social communication skills, and the absence of bullying.
AUTHORS: Raghu Lingam, MBChB, MSC, MRCPCH,a Marian J. Jongmans, PhD,b Matthew Ellis, MD, PhD,a Linda P. Hunt, PhD,c Jean Golding, PhD,a and Alan Emond, MDa
aCentre for Child and Adolescent Health, School of Social and Community Medicine and cSchool of Clinical Sciences, University of Bristol, Bristol, United Kingdom; and bDepartment of Neonatology, Wilhelmina Childrens Hospital, University Medical Centre Utrecht, and Department of Special Education, Faculty of Social Sciences, Utrecht University, Utrecht, Netherlands

KEY WORDS developmental coordination disorder, DCD, child development, depression, mental health, child behavior, ALSPAC, developmental disabilities ABBREVIATIONS ALSPACAvon Longitudinal Study of Parents and Children ASDautistic spectrum disorder CI95% condence interval DCDdevelopmental coordination disorder DSM IV-TRDiagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Revision EPDSEdinburgh Postnatal Depression Scale MABCMovement Assessment Battery for Children ORodds ratio SDQStrengths and Difculties Questionnaire SMFQShort Mood and Feelings Questionnaire This publication is the work of the authors and Dr Lingam will serve as guarantor for the contents of this article. www.pediatrics.org/cgi/doi/10.1542/peds.2011-1556 doi:10.1542/peds.2011-1556 Accepted for publication Nov 29, 2011 Address correspondence to Raghu Lingam, MBChB, MSC, MRCPCH, Centre for Child and Adolescent Health, School of Social and Community Medicine, Oakeld House, Oakeld Rd, Bristol BS8 2BN, UK. E-mail: raghu.lingam@bristol.ac.uk PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright 2012 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no nancial relationships relevant to this article to disclose. FUNDING: The UK Medical Research Council, the Wellcome Trust, and the University of Bristol currently provide core support for the Avon Longitudinal Study of Parents and Children. Dr Lingam is funded by a Researcher Development Award from the UK National Institute for Health Research. COMPANION PAPER: A companion to this article can be found on page e892, online at www.pediatrics.org/cgi/doi/10.1542/ peds.2011-1237.

abstract
OBJECTIVE: To explore the associations between probable developmental coordination disorder (DCD) dened at age 7 years and mental health difculties at age 9 to 10 years. METHODS: We analyzed of prospectively collected data (N = 6902) from the Avon Longitudinal Study of Parents and Children. "Probable" DCD was dened by using Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Revision criteria as those children below the 15th centile of the Avon Longitudinal Study of Parents and Children Coordination Test, with functional limitations in activities of daily living or handwriting, excluding children with neurologic difculties or an IQ ,70. Mental health was measured by using the child-reported Short Moods and Feelings Questionnaire and the parent-reported Strengths and Difculties Questionnaire. Multiple logistic regression models, with the use of multiple imputation to account for missing data, assessed the associations between probable DCD and mental health difculties. Adjustments were made for environmental confounding factors, and potential mediating factors such as verbal IQ, associated developmental traits, bullying, self-esteem, and friendships. RESULTS: Children with probable DCD (N = 346) had an increased odds of self-reported depression, odds ratio: 2.08 (95% condence interval: 1.363.19) and parent-reported mental health difculties odds ratio: 4.23 (95% condence interval: 3.105.77). The odds of mental health difculties signicantly decreased after accounting for verbal IQ, social communication, bullying, and self-esteem. CONCLUSIONS: Children with probable DCD had an increased risk of mental health difculties that, in part, were mediated through associated developmental difculties, low verbal IQ, poor self-esteem, and bullying. Prevention and treatment of mental health difculties should be a key element of intervention for children with DCD. Pediatrics 2012;129:e882e891

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Previous longitudinal research has found an increased risk of anxiety and depression in teenagers with severe functional motor coordination difculties, especially in association with attention decit hyperactivity disorder.13 However, these studies did not use standardized tools for the measurements of motor coordination or mental health difculties, and in the case of the Goteborg cohort, did not control for potential confounding factors.4 Recent work has highlighted the need for robust epidemiological analyses to assess not only the risk of mental health difculties in children with developmental coordination disorder (DCD), but also to consider factors that may mediate this relationship.59 Our objective was, rst, to assess the associations between children with probable DCD (dened by using criteria based on the Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition, Text Revision [DSM IV-TR]10) at age 7 years and parent and child reported mental health difculties at age 9 or 10 years, accounting for known confounding factors. Second, we aimed to explore the effect of associated developmental difculties, and social factors, specically bullying, self-esteem, and friendships as potential mediating factors in this relationship.

6902 children who attended a research clinic for motor testing at 7 years, and who had data from a school-based handwriting test or an Activities of Daily Living scale. Children with an IQ ,70 were excluded. Children who attended motor coordination testing at 7 years were more likely to have white mothers who were educated to a higher level and come from a higher social class.12 Data on a variety of parent- and childrelated confounding factors and developmental traits were collected by parent self-completion questionnaires, from face-to-face assessments at special clinics, and linked education and health records. Ethical approval for the study was obtained from the ALSPAC Law and Ethics Committee and the Local Research Ethics Committees. Measures Exposure Variable: Probable DCD Children with probable DCD were dened by the use of the DSM IV-TR criteria, adapted for research by using the 2006 Leeds Consensus Statement, which have been described previously.10,12,13 Children were dened as having probable DCD if they met all 4 DSM IV-TR criteria for DCD: poor motor coordination (criterion A), which causes functional limitations in activities of daily living or academic achievement (criterion B), not caused by a general medical condition nor severe learning difculties (exclusion criteria C and D).10,12 Motor skills of children were assessed between 7 and 8 years by using the ALSPAC Coordination Test, which consisted of 3 subtests derived from the Movement Assessment Battery for Children (MABC).14 The subtests were selected to test the 3 realms of coordination: 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 validity with other similar coordination tests and represent the 3 domains of coordination by using principal component analysis of original standardization data from the MABC.12,15 We used the 15th centile of the ALSPAC Coordination Test to dene children as having or being at risk for coordination difculties in keeping with the MABC manual and previous literature.14,16,17 Those children scoring below the 15th centile on motor testing were then considered to have functional limitations in motor skills if, in addition, they either failed their National Curriculum Key Stage 1 writing test (a standardized assessment undertaken by all children in state education in England at aged 7), or they scored below the 15th centile on a 23-item activity of daily living scale derived from parent-completed questionnaires.12 Those children with a known visual decit or neurologic condition such as cerebral palsy were excluded, as were children with an IQ ,70. The multistage denition used met DSM IV-TR criteria for DCD. However, as we used the 15th centile, rather than the more conservative fth centile of the motor coordination test, we described our population as having "probable" DCD in keeping with our previous work.18,19 Outcome Variables: Measures of Mental Health and Child Behavior The primary outcome was depressive symptoms reported at the age of 10 years, by using the child-completed 13item Short Mood and Feelings Questionnaire (SMFQ), which has been shown to have high levels of reliability and validity.20,21 The assumed latent trait underlying the SMFQ is depression.21,22 Parents were asked to complete the Strengths and Difculties Questionnaire (SDQ) for their child at 9.5 years.23,24 The SDQ is a standardized screening questionnaire used extensively in mental
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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.11 The study invited all pregnant women in the geographically dened area of Avon, southwest England, with an expected date of delivery between April 1, 1991 and December 31, 1992 to take part. The study contains data on 14 062 live births. Our sample consisted of

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health research with young people, which has been validated in a survey of .10 000 British 5- to 15-year-olds and their parents.25,26 Within this validation dataset, SDQ scores above the 10th centile from parental report were associated with a 15-fold increased odds of the young person having an independently diagnosed psychiatric disorder.27 The test consists of 20 questions arranged to create 4 difculty subscales (measuring emotional symptoms, conduct, hyperactivity and inattention, and peer relationship difculties). Responses were scored by using a 3-point Likert scale; each of the 4 difculty subscales were summed and prorated, in keeping with the authors instructions, to give a total difculty score out of 40.24,28 In addition, the SDQ also provides 5 questions that measure prosocial behavior. Confounding Factors Potential confounding factors were selected after appraisal of the relevant literature and additional univariable analyses against both the exposure (probable DCD) and primary outcome (child-reported depression).29,30 Child-related confounding factors selected were: gender, age when the SDQ or SMFQ were performed, and extremely stressful events in the childs life, taken from parent report at age 7.5 years. Parent and environmental confounding factors were highest maternal educational attainment (3 categories), highest parent social class (3 categories), housing tenure of the family in pregnancy (owned or rented), nancial difculties in pregnancy (with the use of a 5-point scale derived from maternal report of ability to afford food, clothing, heating, accommodation, and items for the baby), and family income at age 8 years. Measures of parent mental health shown in univariable analysis to be associated with both probable DCD and child-reported depression at 10 years were antenatal depression and
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anxiety. Antenatal depression was measured by using the Edinburgh Postnatal Depression Scale (EPDS) at 32 weeks gestation by using a binary cutoff of $13 as used previously.31,32 Maternal anxiety was measured at 32 weeks gestation by using the anxiety items from the Crown-Crisp Index, a validated self-rating inventory.33 Maternal depression at 9 years was taken from maternal self-report. Mediating Factors IQ was measured at age 7 by using a short version of Wechsler Intelligence Scale for Children III.34,35 Verbal IQ was considered to be a potential mediating factor in keeping with recent research, which assessed the association between IQ and later psychosis and depression.36,37 We have previously shown a strong association between probable DCD and difculties in attention and hyperactivity, short-term memory, nonverbal skills, social communication, and academic ability, measured by using validated tests and subtest within ALSPAC, between 7.5 and 9 years.18 Inattention and hyperactivity were assessed by using the Development and Well-Being Assessment38; short-term memory was assessed by using a shortened version of the Childrens Test of Nonword Repetition39; nonverbal skills were assessed by using the Faces subtest of the Diagnostic Analysis of Nonverbal Accuracy; and social communication was measured by the Social and

Communication Disorders Checklist.40,41 Measures of academic ability consisted of reading, assessed by using the Basic Reading subtest of the Wechsler Objective Reading Dimensions42 and spelling, assessed by using 15 age-appropriate words developed by Nunes et al.43 All test results were dichotomized by using the fth centile to dene signicant difculties.18 Univariable analysis showed all of these factors to be associated with child- reported depression at 10 years (Table 1). Details of these tests have been reported previously.18 Bullying was assessed by using a modied version of the Bullying and Friendship Schedule.44 A child was classied as an overt victim if they had been bullied frequently (several times a month) or very frequently (several times a week). Peer relationships and peer support were assessed by using 5 questions from the Cambridge Hormones and Moods project Friendship questionnaire.45 Finally, self-esteem was measured by using a 12-item shortened form of Harters Self Perception Prole for Children comprising the global selfworth and scholastic competence subscales.46 All 3 of these measures were completed by the child and have been reported in ALSPAC.47 Analysis Logistic regression models were used to assess the associations between the exposure variable, probable DCD, and the indicators of mental health. The SMFQ was dichotomized in line with the

TABLE 1 ORs of Child-Reported Depression (SMFQ) at 10 y in Children With Developmental

Difculties, Dened as the Fifth Centile of Each Trait in Turn
Associated Developmental Difculties as Fifth Centilea Inattention or hyperactivity, N = 5913 (n = 338) Short-term memory, N = 6308 (n = 362) Nonverbal skills, N = 5817 (n = 336) Social communication, N = 5884 (n = 337) Reading, N = 6422 (n = 371) Spelling, N = 6353 (n = 356)
a

Odds of Low Mood at 10 y by Using SMF Q and a Binary Cutoff of 11 OR (95% CI) 3.49 (2.484.90) 2.17 (1.592.96) 1.58 (1.042.38) 3.79 (2.765.22) 3.73 (2.685.18) 2.38 (1.743.25)

P ,.001 ,.001 .03 ,.001 ,.001 ,.001

N is the number for analysis (n is the total number children $11 y in the SMFQ).

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test authors guidelines by using a cutoff of 11 or more to dene depression.48,49 The 10th centile of the SDQ score measured in the cohort was used to dene mental health difculties, in line with the standardization literature.27,50,51 The 10th centile was used to dene difculties in each of the SDQ subscales in turn. Multiple Imputation by Chained Equations was used to impute missing data in the confounding factors.52 Analysis of an imputed dataset reduces the potential bias introduced by missing data and was thus chosen as the denitive analysis to meet our study aims.52,53 The unadjusted associations between probable DCD and the binary SMFQ and the SDQ scores were rst analyzed. Adjustment was then made for all child and parent confounding factors (model 1). Potential mediating factors were

then added to the model, starting with verbal IQ (model 2) and subsequently adding developmental traits (model 3). Our nal model assessed the role of bullying, friendship, and self-esteem in this association by adding these factors to the previous factors (model 4). Because hyperactivity was one of the subscales making up the SDQ, inattention and activity were not controlled for when considering total SDQ and the hyperactivity SDQ subscale as outcome variables. A variable focused model of resilience was used to consider the factors that decreased the risk of psychological morbidity in young people with probable DCD compared with normally developing controls.54,55 Further details of the multiple imputation models and missing data are

reported in Appendix 1. Gender was considered as a potential effect modier for the SMFQ and total SDQ score in model 3 and assessed by using the likelihood ratio test. All statistical analyses used Stata version 10.1.

RESULTS
Of our total sample of 6902 children, 346 children (5.0%) met criteria for probable DCD. The children with probable DCD were more likely to be male, come from a more deprived social background, and have been subject to more stressful life events (Table 2). Data for both DCD status and SMFQ were available for 5475 children, whereas 5499 children had data on both DCD status and SDQ. Of the 346 children dened as having probable DCD at 7 years, 235 attended for testing at 10

TABLE 2 Characteristics of Children With Probable DCD Compared With Controls

Controls N = 6556 max Child factors Gender: males, N (%) Gestation ,37 wk, N (%) Birth weight #2500g, N (%) Verbal IQ, mean IQ (SD) Stressful life event for child: Yes, N (%) Parental and environmental factors Highest parental social class: IV, V, N (%) Average weekly income at 8 y ,200 per week, N (%) Housing tenure at 8 wk gestation: rented, N (%) Maternal education highest qualication: certicate of secondary education/vocational, N (%) Maternal age at delivery years ,21, N (%) Ever smoked in pregnancy: ever, N (%) Maternal Parity: 3 or more, N (%) Maternal alcohol in pregnancy (18 wk gestation): .1 glass/wk, N (%) Maternal antenatal depression at 32 wk EPDS $13: depressed, N (%) Maternal antenatal anxiety at 32 wk (Crown Crisp Experimental index 15th centile cutoff): anxious, N (%) Maternal depression 8 wk postdelivery EPDS $13: depressed, N (%) Maternal reported depression in the last 3 y from age 9: yes often, N (%) Friendship difculties at 8 y, median (interquartile range) Bullying child is an overt victim at 8 y: yes, N (%) Global self-esteem at 8 y: median (interquartile range) Scholastic competence at 8 y: median (interquartile range)
x 2 test. b Student t test. c Wilcoxon Mann-Whitney test.
a

Probable DCD N = 346 max 217 (62.7) n = 346 27 (8.2) n = 329 30 (9.3) n = 324 98.52 (17.6) n = 247 46 (18.0) n = 256 23 (7.9) n = 291 33 (15.0) n = 220 74 (23.7) n = 312 95 (30.7) n = 310 12 (3.7) n = 329 79 (24.3) n = 325 20 (6.27) n = 319 47 (14.7) n = 320 52 (17.6) n = 295 46 (16.1) n = 286 28 (9.4) n = 297 38(15.8) n = 240 4 (2 to 6) 93 (39.91) n = 233 19 (1621) 16 (1419)

3255 (49.7) n = 6556 316 (5.0) n = 6321 301 (4.8) n = 6257 108.50 (15.9) n = 5390 666 (12.3) n = 5414 238 (4.1) n = 5826 469 (9.9) n = 4751 900 (15.1) n = 5977 1313 (21.6) n = 6092 198 (3.1) n = 6321 1247 (20.0) n = 6242 264 (4.32) n = 6109 944 (15.3) n = 6167 752 (12.7) n = 5918 660 (11.5) n = 5761 489 (8.3) n = 5912 689 (13.2) n = 5218 3 (2 to 5) 1726 (33.12) n = 5211 20 (1722) 17 (1520)

,.001a .01a ,.001a Mean difference 9.98 (7.9412.00) ,.001b .007a ,.001a .01a ,.001a .001a .60a .06a .31a .44a .01a .02a .5a .001a z = 23.348, ,.001,c
N = 5459

.03a z = 3.148, .002,c

N = 5291

z = 4.036, #.001,c
N = 5301

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years for the SMFQ and 245 had available data for the parent-completed SDQ at 9 years.

The odds ratios (OR) of having signicant difculties according to the SMFQ score, total SDQ score, and SDQ subtest scores with the use of the multiple imputed data set are presented in Table 3. For comparison, the same analyses with the use of a nonimputed data set with all available data are presented (Table 4).

Cross-tabulation showed that 28 children with probable DCD (11.9%) reported symptoms of depression (SMFQ) compared with 279 of 5240 controls (5.3%), equating to an unadjusted OR of 2.41 (95% condence interval [CI] 1.593.63). Model 1 showed a twofold increased odds of child-reported symptoms of depression for children with probable DCD compared with controls, after controlling for confounding factors. The addition of verbal IQ (model 2) and associated developmental traits (model 3) to the original model decreased the OR of depression in children with probable DCD from 2.08 (1.363.19) to 1.29 (0.812.06), with a signicantly better tting model. The nal addition of markers of bullying, friendship, and self-esteem (model 4) further decreased the association between probable DCD and childreported depression.

Similar cross-tabulation for the total SDQ showed that 71 (23.0%) children with probable DCD were at risk for mental health and behavioral difculties (SDQ) compared with 423 of 5254 (8.1%) controls (unadjusted OR 4.66; 95% CI 3.486.25). Children with probable DCD had increased odds of hyperactivity and inattention, emotional problems, peer relationship difculties, and fewer prosocial skills compared with their peers after adjustment for confounding factors. The addition of verbal IQ (model 2), developmental traits (model 3), bullying, friendship,
P
(95% CI) (95% CI)

LINGAM et al Model 1a OR P .001 ,.001 ,.001 ,.001 .025 ,.001 ,.001 1.67(1.082.59) 3.62(2.644.98) 2.90(2.064.10) 2.37 (1.743.23) 1.47(0.97 2.22) 3.64(2.625.06) 2.58(1.783.73) 2.08(1.363.19) 4.23(3.105.77) 3.51(2.514.90) 2.53(1.863.44) 1.59(1.062.40) 3.85(2.795.31) 2.49(1.733.58) Model 2b OR P .022 ,.001 ,.001 ,.001 .07 ,.001 ,.001 Model 3c OR
(95% CI)

TABLE 3 OR (95% CI) of Signicant Mental Health Difculties by Using the SDQ at 9 y and SMFQ at 10 y for Children With Probable DCD Compared With Controls by Using Multiple Imputation Data
P 1.29(0.812.06) 2.91(2.004.22) 2.24(1.513.33) 1.97(1.412.76) 1.00(0.611.63) 2.61(1.803.79) 2.17(1.453.26) .282 ,.001 ,.001 ,.001 .99 ,.001 ,.001 Model 4d OR
(95% CI)

OR of: 2.41(1.593.63) 4.66(3.486.25) 4.10(2.995.63) 2.54(1.893.41) 1.94(1.312.87) 4.31(3.165.87) 2.70(1.893.85) ,.001 ,.001 .001 ,.001 ,.001 ,.001 ,.001

Unadjusted OR (95%CI)

P 1.19(0.741.92) 2.80(1.914.09) 2.17(1.453.24) 1.91(1.362.68) 0.95(0.581.57) 2.45(1.673.58) 2.13(1.413.21) .476 ,.001 ,.001 ,.001 .838 ,.001 ,.001

SMFQ at 10 y (with binary cutoff of 11 to dene depression), n = 5475 Total SDQ difculty score at 9 y (with a 10th centile cutoff), n = 5499 SDQ hyperactivity subscale, n = 5516 SDQ emotional subscale, n = 5509 SDQ conduct subscale, n = 5514 SDQ peer subscale, n = 5511 SDQ prosocial subscale, n = 5521

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a Model 1 controlled for child factors: gender, stressful life event, age when SDQ/SMFQ performed; and parental factors: highest maternal or paternal social class, housing tenure during pregnancy, nancial difculties measured at 32 wk gestation, highest maternal educational qualication, family income at 8 y of age, maternal antenatal anxiety and depression at 32 wk gestation, and maternal depression at 9 y. b Model 2 plus verbal IQ measured at 8 y as a continuous variable. c Model 3 plus difculties in attention and hyperactivity, short-term memory, nonverbal skills, social communication, and academic ability assessed between 7.5 and 9 y were also controlled for as binary variables by using the fth centile of each trait (note: difculties in attention and hyperactivity not controlled for in SDQ analysis). d Model 4 plus being subject to overt bullying, low self-esteem, and friendship difculties measured at 8 y.

TABLE 4 OR (95% CI) of Signicant Mental Health Difculties by Using the SDQ at 9 y and SMFQ at 10 y for Children With Probable DCD Compared With Controls Using All Available Data
P ,.001 .001 .035 .05 ,.001 5.74 (3.848.56), n = 3533 ,.001 5.22 (3.368.12), n = 3258 ,.001 6.50 (3.7911.14), n = 2862 ,.001 2.64 (1.504.64), n = 3314 1.96 (1.053.68), n = 3144 1.98 (1.003.93), n = 2768 Model 1a OR (95%CI) P P P Model 2b OR (95%CI) Model 3c OR (95%CI) Model 4d OR (95%CI) 2.20 (1.034.71), n = 2509 6.08 (3.3411.08), n = 2580 P .042

OR of:

Unadjusted OR (95%CI)

2.41 (1.593.63), n = 5475

PEDIATRICS Volume 129, Number 4, April 2012 ,.001 ,.001 ,.001 .001 ,.001 ,.001 3.27 (2.204.84), n = 3537 1.57 (0.882.78), n = 3537 4.21 (2.776.41), n = 3535 2.64 (1.654.22), n = 3540 ,.001 .125 ,.001 ,.001 3.13 (2.034.82), n = 3263 1.48 (0.792.75), n = 3262 3.75 (2.346.02), n = 3261 2.25 (1.313.85), n = 3266 ,.001 .22 ,.001 .003 3.22 (1.985.22), n = 2865 1.38 (0.672.86), n = 2866 2.77 (1.574.92), n = 2863 2.09 (1.103.96), n = 2868 3.87 (2.505.99), n = 3541 ,.001 3.20 (1.955.25), n = 3267 ,.001 2.52 (1.364.68), n = 2869 .003 ,.001 .381 ,.001 .024 3.33 (1.706.52), n = 2586 2.33 (1.344.06), n = 2583 1.37 (0.603.10), n = 2585 2.88 (1.535.40), n = 2582 2.33 (1.154.72), n = 2586 ,.001 .003 .452 .001 .019

4.66 (3.486.25), n = 5499

SMFQ at 10 y(with binary cutoff of 11 to dene depression) Total SDQ difculty score at 9 y (with a 10th centile cutoff) SDQ hyperactivity subscale SDQ emotional subscale SDQ conduct subscale SDQ peer subscale SDQ prosocial subscale

4.10 (2.995.63), n = 5516

2.54 (1.893.41), n = 5509 1.94 (1.312.87), n = 5514 4.31 (3.165.87), n = 5511 2.70 (1.893.85), n = 5521

a Model 1 controlled for child factors: gender, stressful life event, age when SDQ/SMFQ performed; and parental factors: highest maternal or paternal social class, housing tenure during pregnancy, nancial difculties measured at 32 wk gestation, highest maternal educational qualication, family income at 8 y of age, maternal antenatal anxiety and depression at 32 wk gestation, and maternal depression at 9 y. b Model 2 plus verbal IQ measured at 8 y as a continuous variable. c Model 3 plus difculties in attention and hyperactivity, short-term memory, nonverbal skills, social communication, and academic ability assessed between 7.5 and 9 y were also controlled for as binary variables by using the fth centile of each trait (note: difculties in attention and hyperactivity not controlled for in SDQ analysis). d Model 4 plus being subject to overt bullying, low self-esteem, and friendship difculties measured at 8 y.

DISCUSSION

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Interpretation of these models is that for each of the main outcome variables, SMFQ, and total SDQ, decreased verbal IQ, poor social communication (5th centile), being an overt victim, and lower global self-esteem and scholastic competence all signicantly increased the risk of mental health difculties in children with probable DCD (P , .05). These factors can thus be thought of as potential mediating factors in this relationship.56,57

There was no interaction detected for gender in either the model by using the SMFQ or total SDQ. Sensitivity analyses excluding children with a clinical diagnosis of ASD (n = 29 for the SDQ analysis and n = 19 in the SMFQ analysis) were similar, and are presented in Appendix Table 5.

This study has shown that children with probable DCD, dened by using the DSM IV-TR criteria at 7 years, have a 2-fold increased risk of self-reported depression and a 4-fold increased risk of parent-reported mental health and behavioral difculties at 9 or 10 years by the use of prospectively collected data from a large United Kingdom birth cohort, accounting for important confounding factors. The unique aspect of this study is the longitudinal nature of the dataset that has allowed us to consider potential mediating factors in this relationship.

Previous cross-sectional studies (varying in size from n = 40 to n = 270) have also found children with poor motor coordination to have an increased risk of mental health difculties.8,5861 This is supported by longitudinal work from the United States, United Kingdom, and

and self-esteem (model 4) decreased the odds of parent-reported total SDQ difculties by 34%. However, children with probable DCD still had signicantly increased odds of difculties: OR 2.80 (95% CI 1.914.09).

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Sweden, showing that children with poor motor coordination, dened by nonstandardized clinical examination or parental report, have an increased risk of anxiety and depression as young adults.14,62 More recent work with a smaller cohort of children (n = 50) showed that early motor development was a strong predictor of parentreported anxiety and depression at 6 to 12 years.63 A major limitation of the current study, as with all large cohort studies, is attrition bias. To minimize this bias, we used multiple imputation by chained equations, an increasingly used statistical technique to account for missing data.52 Another limitation, because of the size of the sample tested, was the use of subtests for measures such as self-esteem and friendship. The effect of therapeutic interventions in the study population was not measured. Decreased verbal IQ, poor social communication (,5th centile), being bullied, and lower global self-esteem and scholastic competence all signicantly increased the risk of mental health difculties in children with probable DCD (P , .05). Within a resilience framework, factors such as having a high IQ and high self-esteem can therefore be thought of as factors that engender resilience in this population of children. The odds of self-reported depression were attenuated after the addition of confounding and mediating factors; in contrast, there was still a strong association between probable DCD and parent-reported child mental

health dif culties (SDQ) even after these factors were added to the model. The differences seen between the parent and child-reported measures of mental health may relate to the differences between the parent s and childs perception of the young persons wellbeing,64,65 or may reect the fact that the SDQ and the SMFQ are measuring different components of mental health. Jensen et al66 in a study of 1285 parentchild dyads found high rates of discrepancy between parents and children in terms of diagnosis of mental disorders, but discrepant cases were still considered to reect clinically meaningful impairment. The complex interaction between environmental and genetic components in the lives of children with DCD has been highlighted by recent twin studies.6,7 Morruzi et al6 found an increased risk of anxiety and behavioral problems in children with coordination difculties, although they questioned the causal relationship of these ndings. Piek et al,7 with the use of data from an Australian cohort, showed that twin children with poor motor coordination difculties had an increased risk of depressive symptoms compared with their non-DCD co-twin. Because the cotwin had decreased depression scores but similar home environment and genetic characteristics, the authors stated that this observed difference may be due to the unique environment of a child with motor difculties in school and home. Skinner and Piek8 showed decreased levels of self-worth

in children with DCD compared with controls matched on age, gender, and verbal IQ. This was mirrored by the ndings of Poulson et al,9 who found decreased levels of life satisfaction and self-esteem in children with DCD mediated through self-concept of physical ability, appearance, and peer and parental relationships. In summary, this work adds robust epidemiological data to the growing evidence that children with DCD have an increased risk of mental health difculties. The work also demonstrates the importance of high IQ, high global selfesteem, scholastic competence, good social communication skills, and the absence of bullying as protective factors in the associations between DCD, depression, and behavioral difculties.56

CONCLUSIONS
Children with DCD need to be screened for mental health difculties. Interventions focusing on increasing selfesteem, tackling bullying, and enhancing social interaction may alleviate some of the risk of depression and behavioral difculties in children with DCD.

ACKNOWLEDGMENTS We are extremely grateful to all the families who took part in this study, the midwives for their help in recruiting them, and the whole ALSPAC team, which includes interviewers, computer and laboratory technicians, clerical workers, research scientists, volunteers, managers, receptionists and nurses.

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APPENDIX 1: DETAILS OF MISSING DATA AND MULTIPLE IMPUTATION USED

Missing data are a problem in all longitudinal birth cohort studies, especially when data relating to confounding factors are collected at different time points and from different sources (eg, in this case, different parental reported questionnaires and face-to-face assessments). Of those children with probable DCD, 5499 had data for the total SDQ score, and 5475 had data from the SMFQ at 10 years. The model for the SDQ and SMFQ analyses were the same. Taking the SDQ analysis, of the 5499 children with both SDQ and DCD variables, 2580 had no missing data in the confounding factors. In total, 1961 children (69% of those with missing data) had missing data in between 1 and 4 confounding factors with 1002 children (34%) having a single missing value from the nal model. Multiple imputation models were used to create data sets to allow for missing data only in the confounding factors. Multiple imputation by using chained equations was employed with the use of the ICE command in STATA version

10.1. Twenty separate stacked data sets were created for the nal analysis, which used the MIM command in STATA. Variables included in the multiple imputation model included all those variables in the nal regression model plus variables that predicted missingness in the confounders. Within 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 afuent, well-educated families.12 Variables that predicted missingness in the confounding factors were assessed by using logistic regression. The following factors were selected to explore if they were associated with missingness: maternal age, marital status, parity, ethnicity, use of a car, family income, use of hot water in the household, index of crowding (ordered categorical variable), ever used drugs, maternal alcohol usage in pregnancy (ever, never), temperature of the house in winter, postnatal depression or anxiety, and maternal anxiety at 9 years. We also assessed other factors that may add to our knowledge of the confounding factors themselves; these included the childs birth weight and gestational age,

friendship score at 10 years, the oral expression and language comprehension subtests of the Wechsler Objective Language Dimensions67 and the performance IQ measured by using alternate items of the Wechsler Intelligence Scale for Children III at a mean age of 8.7 years.34 Of these factors, friendship at 10 years, maternal anxiety at 9 years, and temperature of the house in winter all predicted missingness in the model with a P value of ,.05. These variables, along with all variables from the nal logistic regression model, model 4 were included in the nal multiple imputation model. Binary variables and categorical variables used logistic, ordinal and multinomial regression as appropriate, specied in the ICE command. IQ was normally distributed and incorporated by using linear regression in the imputation model. The wealth of prospectively collected data in ALSPAC allows the analysis to not only account for confounding factors, but also to account for factors that help to explain missingness, thus supporting the missing at random assumption.

APPENDIX TABLE 5 OR (95% CI) of Signicant Difculties in Mental Health Difculties by Using the SDQ (Total Score and Subscale Scores) at 9 y and
SMFQ at 10 y (by Using the 10th Centile Cutoff) for Children With Probable DCD Compared With Controls by Using Multiple Imputation Data
OR of: Unadjusted OR (95%CI) P Model 1a OR
(95% CI)

Model 2b OR
(95% CI)

Model 3c OR
(95% CI)

Model 4d OR
(95% CI)

SMFQ at 10 y (with binary cutoff 2.27 (1.473.51) ,.001 1.96 (1.263.07) .003 1.59 (1.012.52) .047 1.34 (0.832.17) .233 1.22 (0.752.00) .426 of 11 to dene depression), n = 5456 3.88 (2.825.32) ,.001 3.44 (2.454.81) ,.001 2.96 (2.104.19) ,.001 2.60 (1.753.85) ,.001 2.47 (1.653.69) ,.001 Total SDQ score at 9 y (with a 10th centile cutoff), n = 5470
a Model 1 controlled for child factors: gender, stressful life event, age when outcome test performed; and parental factors: highest maternal or paternal social class, housing tenure during pregnancy, nancial difculties measured at 32 wk gestation, highest maternal educational qualication, family income at 8 y of age, maternal antenatal anxiety and depression at 32 wk gestation, and maternal depression at 9 y. b Model 2 plus verbal IQ measured at 8 y as a continuous variable. c Model 3 plus difculties in attention and hyperactivity, short-term memory, nonverbal skills, social communication, and academic ability assessed between 7.5 and 9 y were also controlled for as binary variables by using the fth centile of each trait (note: difculties in attention and hyperactivity not controlled for in SDQ analysis). d Model 4 plus being subject to overt bullying, self-esteem, and friendship difculties measured at 8 y.

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Mental Health Difficulties in Children With Developmental Coordination Disorder Raghu Lingam, Marian J. Jongmans, Matthew Ellis, Linda P. Hunt, Jean Golding and Alan Emond Pediatrics 2012;129;e882; originally published online March 26, 2012; DOI: 10.1542/peds.2011-1556
Updated Information & Services References including high resolution figures, can be found at: http://pediatrics.aappublications.org/content/129/4/e882.full.h tml This article cites 55 articles, 11 of which can be accessed free at: http://pediatrics.aappublications.org/content/129/4/e882.full.h tml#ref-list-1 This article, along with others on similar topics, appears in the following collection(s): Development/Behavioral Issues http://pediatrics.aappublications.org/cgi/collection/developme nt:behavioral_issues_sub Information about reproducing this article in parts (figures, tables) or in its entirety can be found online at: http://pediatrics.aappublications.org/site/misc/Permissions.xh tml Information about ordering reprints can be found online: http://pediatrics.aappublications.org/site/misc/reprints.xhtml

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