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Child NeuropsychologyA Journal on Normal and Abnormal Development in Childhood andAdolescence

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Neuropsychological status of French children withdevelopmental dyslexia and/or developmentalcoordination disorder: Are both necessarily worsethan one?

Maëlle Biotteau, Jean-Michel Albaret, Sandrine Lelong & Yves Chaix

To cite this article: Maëlle Biotteau, Jean-Michel Albaret, Sandrine Lelong & Yves Chaix(2016): Neuropsychological status of French children with developmental dyslexia and/or developmental coordination disorder: Are both necessarily worse than one?, ChildNeuropsychology, DOI: 10.1080/09297049.2015.1127339

To link to this article: http://dx.doi.org/10.1080/09297049.2015.1127339

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Neuropsychological status of French children withdevelopmental dyslexia and/or developmental coordinationdisorder: Are both necessarily worse than one?Maëlle Biotteaua,b, Jean-Michel Albaret c, Sandrine Lelongd and Yves Chaixa,b,d

aInserm, Imagerie Cérébrale et Handicaps Neurologiques UMR 825, Centre Hospitalier Universitaire (CHU)Purpan, Toulouse, France; bUniversité de Toulouse, UPS, Imagerie Cérébrale et Handicaps NeurologiquesUMR 825, CHU Purpan, Toulouse, France; cUniversité de Toulouse III, UPS, PRISSMH-EA4561, Toulouse,France; dHôpital des Enfants, CHU de Toulouse, CHU Purpan, Toulouse, France

ABSTRACTDevelopmental dyslexia (DD) and developmental coordinationdisorder (DCD) co-occur frequently, raising the underlying ques-tion of shared etiological bases. We investigated the cognitiveprofile of children with DD, children with DCD, and children withthe dual association (DD + DCD) to determine the inherent char-acteristics of each disorder and explore the possible additionalimpact of co-morbidity on intellectual, attentional, and psychoso-cial functioning. The participants were 8- to 12-year-olds (20 DD,22 DCD, and 23 DD + DCD). Cognitive abilities were assessed bythe Wechsler Intelligence Scale for Children – Fourth Edition(WISC-IV) and the Continuous Performance Test – Second Edition(CPT-II) and behavioral impairments were evaluated by the ChildBehavior Checklist (CBCL). No differences were found between thethree groups on attention testing (CPT-II) or psychosocial charac-teristics (CBCL), but a higher percentage of DD + DCD children hadpathological scores on psychosocial scales. Significant between-group differences were observed on Processing Speed Indexscores and the block design and symbol search subtests, whereDD children fared better than DCD children. No significant differ-ences were evident between the co-morbid vs. the pure groups.Our results clearly show significant differences between childrenwith DD only and children with DCD only. In particular, visuo-spatial disabilities and heterogeneity of intellectual profile seem tobe good markers of DCD. However, it should be noted that despitethese distinct and separate characteristics, a common cognitiveprofile (weaknesses and strengths) is likely shared by both neuro-developmental disorders. Surprisingly, concerning co-morbidity,DD + DCD association is not associated with a decrease in intel-lectual or attentional capacities.

ARTICLE HISTORYReceived 17 June 2014Accepted 27 November 2015Published online 5 January2016

KEYWORDSCo-morbidity; Developmentaldyslexia; Developmentalcoordination disorder; WISC-IV; CBCL

Research has shown that neurodevelopmental disorders, such as developmental dyslexia(DD), developmental coordination disorder (DCD), attention deficit hyperactivity dis-order (ADHD) and specific language impairment (SLI), co-occur frequently (for

CONTACT Maëlle Biotteau maelle.biotteau@inserm.fr Inserm, Imagerie Cérébrale et Handicaps NeurologiquesUMR 825, CHU Purpan, Place du Dr Baylac, F-31059 Toulouse Cedex 9, France.

CHILD NEUROPSYCHOLOGY, 2015http://dx.doi.org/10.1080/09297049.2015.1127339

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ADHD, see Feldman, Blum, Gahman, Shults, & DBPNet Steering Committee, 2014; forthe association between SLI and DD, see Ramus, Marshall, Rosen, & van der Lely,2013). According to Kaplan, Wilson, Dewey, and Crawford (1998), co-morbidity oflearning disorders is more common than not.

There is an ongoing debate regarding why neurodevelopmental disorders are sofrequently associated. One question is whether they are distinct or overlapping condi-tions, further leading to the question of shared underlying etiology. Pursuant toprevious research by our team relating to both DD (Démonet, Taylor, & Chaix, 2004)and DCD (Chaix et al., 2007; de Castelnau, Albaret, Chaix, & Zanone, 2007), wefocused this article on DD and DCD co-occurrence.

Neurodevelopmental disorders

Developmental Dyslexia (DD)

DD or specific reading disability is a persistent neurodevelopmental disorder that affects asizeable proportion (3–10%) of the school-age population (Démonet et al., 2004; Peterson& Pennington, 2012). Children with DD have difficulties in learning to read, despitesociocultural opportunities, scholarly education, adequate conventional instruction andintelligence, as well as intact sensory abilities (World Health Organization, 1993). Inaddition, poor performance on a variety of measures has been reported, including auditoryprocessing (Tallal, 2004), working memory (Gathercole, Alloway, Willis, & Adams, 2006),oral language (McArthur, Hogben, Edwards, Heath, &Mengler, 2000) andmotor function-ing (Ramus, Pidgeon, & Frith, 2003).

Various theories have been offered to explain the neurological and cognitive aspectsof DD. Although significant phenotypic variability and co-morbidity have beenrecorded, substantial evidence has established the basis of DD. There is widespreadagreement that difficulties with phonological processing, especially problems withphonological awareness (Snowling, 2000), may constitute the core impairment in DD.However, the precise nature of that phonological deficit is still being debated (Boada &Pennington, 2006; Ramus & Szenkovits, 2008), and several studies have even underlinedthe existence of DD sub-types (Bosse, Tainturier, & Valdois, 2007; Facoetti et al., 2006).

Developmental Coordination Disorder (DCD)

DCD or specific developmental disorder of motor function is a persistent disorder(Cousins & Smyth, 2003; Missiuna, Moll, King, Stewart, & MacDonald, 2008) that affects2–7% of school-age children, with an additional 5–10% considered as being “at risk” forthe disorder (American Psychiatric Association, 2000; Asonitou, Koutsouki, Kourtessis, &Charitou, 2012; Lingam, Hunt, Golding, Jongmans, & Emond, 2009). Despite normalintelligence, children with DCD have significant and long-standing difficulties in dailyactivities that require motor coordination (American Psychiatric Association, 2000; Geuze,2005a). The disorder’s specific manifestations are varied and pervasive, affecting bothgross and fine motor skills (Macnab, Miller, & Polatajko, 2001; Smits-Engelsman,Niemeijer, & van Galen, 2001). According to Geuze (2005b), the main characteristicsare postural control problems (hypo/hypertonia, poor distal control, static/dynamic

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balance), difficulties in motor learning (learning new skills, planning movements, adaptingto change, automatization) and poor sensori-motor coordination (coordination within/between limbs, sequencing of movement, use of feedback, timing, anticipation, andstrategic planning). Several studies have cited poor social integration (Chen & Cohn,2003) and problems in everyday and academic activities (Geuze, 2005a).

DD and DCD co-occurrence

Although DD and DCD do not co-occur systematically, their association is frequentand has been studied for quite a long time (Denckla, 1985; Haslum, 1989). To cite a fewrecent examples, Chaix et al. (2007) discerned an unusually high DCD percentage in astudy of 58 children with DD and phonological disorders: 23 (40%) scored below −2standard deviations (SDs) on the Lincoln-Oseretsky Motor Development Scale (Rogé,1984), and 10 scored between −1 and −2 SDs. Similarly, Iversen, Berg, Ellertsen, andTønnessen (2005) examined three groups of children: a clinical group with severe DDand two ordinary school groups (without DD, composed of 5% least able to read and5% most able to read) aged 10 to 11 years. A total of 60% of the clinical group and 53%of the poor readers obtained pathological scores (below the 5th percentile) on theMovement Assessment Battery for Children (Henderson & Sugden, 1992) vs. 13.6%of the best readers group. Thus, motor disorders can affect 59% (Ramus et al., 2003)and even up to 80% (Nicolson & Fawcett, 1999) of subjects with DD. On the otherhand, O’Hare and Khalid (2002) found that 70% of children with DCD had readingproblems (versus 14% of the control group). However, while their frequency is welldocumented, the meaning of this co-occurrence remains an intriguing question, withquestions surrounding the reasons for such associations.

According to theoretical approaches, co-occurrence would reflect partially commonetiological bases, as proposed in the cerebellar hypothesis (Nicolson & Fawcett, 2011;Nicolson, Fawcett, & Dean, 2001). Considering that dyslexics are significantly impairedon a large range of abilities and cognitive processes known to be dependent on thecerebellum, such as executive functioning, memory, learning, attention, visuo-spatialregulation, language and motor skills (Baillieux, De Smet, Paquier, De Deyn, & Mariën,2008), it has been suggested that cerebellar dysfunction could constitute a commoncausal factor in comorbid reading disabilities and motor impairments (Nicolson et al.,2001). Conversely, even if shared bases actually provide a suitable explanation for DDand DCD co-occurrence, other studies lean toward the view that both disorders arelargely distinct. For instance, focusing on genetic aspects, Francks et al. (2003) did notobserve the linkage of hand motor skills to any chromosomal regions implicated in DDand concluded that DD and DCD are separate disorders.

Cognitive profiles

These previous studies (Francks et al., 2003; Nicolson et al., 2001; Nicolson & Fawcett,2011) were focused at the anatomical or genetic explanatory levels, and we think thataddressing the issue of co-morbidity at the cognitive level might be relevant. In thisspecific context, few recent investigations (for DD and SLI co-occurrence, see Ramuset al., 2013; for DD and dyscalculia co-occurrence, see A. J. Wilson et al., 2015) have

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attempted to identify the cognitive bases of co-morbidity, especially proposing domainsspecific to each learning disorder (core symptoms central to the disorder) and domainsgeneral to all (symptoms likely shared by other disorders). However, and despite highlyfrequent co-morbidity, the cognitive bases in the context of DD + DCD comorbidityhave not yet been explored.

Cognitive profiles of DD and DCD

Children with developmental disorders often present certain neuropsychological and cogni-tive characteristics (Démonet et al., 2004; Vellutino, Fletcher, Snowling, & Scanlon, 2004).However, previous studies based on the Wechsler Intelligence Scale for Children (WISC)have failed to identify consistent profiles of DD and DCD, and the literature on bothdisorders provides conflicting information. DD and DCD may not necessarily be associatedwith any specific cognitive profile or co-morbidity, and heterogeneity may obscure thepicture. Children with DCD have been reported to have lower general intelligence test scoresthan their peers, with performances deviating by 1 to 2 SDs from the norm on all measures(Alloway & Temple, 2007). For example, Kastner and Petermann (2010) found that thegeneral intelligence quotient (IQ) of children with DCD was 1 SD below the comparisongroup on the fourWISC-IV indexes. In the American version ofWISC-IV (Wechsler, 2003),21 children aged 6 to 15 years and identified as having motor dysfunction scored very low onthe Processing Speed Index (PSI) and coding, symbol search and block design subtests.

DD is also associated with certain cognitive characteristics. Compared to typically-developing children, those with DD seem to perform poorly on all verbal measures of theWISC (comprehension, similarities, vocabulary subtests, and more broadly on the VerbalComprehension Index [VCI]), and some studies have found a discrepancy between verbalsubtests comprising the VCI and the Perceptual Reasoning Index (PRI) or the Full-ScaleIQ Score (FSIQ; Wechsler, 2005). However, this finding is not consistent (Vellutino et al.,2004). Children with DD have also often been identified as having a poor workingmemory (Alloway & Archibald, 2008). De Clercq-Quaegebeur et al. (2010), Jeffries andEveratt (2004) and Wechsler (2005) found relative weakness on the digit span subtest and,more broadly, on the Working Memory Index (WMI). In addition, some studies havementioned a weakness in the coding and symbol search subtests (Catts, Gillispie, Leonard,Kail, & Miller, 2002; De Clercq-Quaegebeur et al., 2010; Thomson, 2003).

Both DD and DCD are also associated with adjustment problems. Research hasfound high levels of internalizing problems among children identified as having motorcoordination problems (Emck, Bosscher, Beek, & Doreleijers, 2009; Green, Baird, &Sugden, 2006) with a high prevalence of internalizing disorders in children with DD(Maughan, Rowe, Loeber, & Stouthamer-Loeber, 2003). These children also have poorattentional abilities.

Impact of co-occurrence

To date, we are not aware of any study that has assessed the cognitive profiles forchildren with co-morbid DD and DCD. More broadly, despite high rates of co-occurrence among neurodevelopmental disorders, few studies have examined the influ-ence of co-morbidity on cognitive abilities. The studies that have been performed were

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often limited to ADHD co-morbidity, only evaluated differences between the co-morbidgroup and a comparison group, or looked at differences between the co-morbid groupand a group with one of the two disorders (e.g., SLI vs. SLI + DCD, but not DCD vsSLI + DCD; (Flapper & Schoemaker, 2013). Other studies did not clearly define theirsamples, or formally assess for DD (Jongmans, Smits-Engelsman, & Schoemaker, 2003),or did not exclude or test for other developmental disorders.

Some studies have suggested that comorbidity leads to greater deficits, where chil-dren with both DCD and ADHD showed significant deficits compared to children withADHD only (Pitcher, Piek, & Barrett, 2002; Pitcher, Piek, & Hay, 2003), especially withregard to behavioral and social problems or low education level (Rasmussen & Gillberg,2000). In contrast, other studies suggest that comorbidity is not associated with greaterdeficits than a single diagnosis. For example, Loh, Piek, and Barrett (2011) detectedsignificant group differences between ADHD and co-morbid groups and betweencontrol and co-morbid groups, but not between DCD and co-morbid groups incognitive abilities (assessed by the WISC-IV), highlighting an equivalent degree ofdeficit for DCD only and DCD + ADHD.

Objectives

Given the co-occurrence of neurodevelopmental disorders, it seems essential to take co-morbidity into account in order to (I) draw clear boundaries between what belongs toone disorder and what belongs to another, (II) take into account not only differencesbut also, and even more so, commonalities between disorders that co-occur frequently,and (III) provide an overview of children who have these disorders. Despite consider-able progress in understanding these conditions, the underlying causes and conse-quences of co-morbidity remain poorly understood, and there is still difficultyidentifying the impact of multiple impairments.

In the present study, we attempted to address this issue by comparing children withDD only to those with DCD only and those with DD + DCD on a broad battery of tests,including measures of intellectual ability, attention, and psychosocial adjustment. Theaim of our study was twofold. The primary goal was to determine the inherentcharacteristics of each disorder. The second goal was to provide a comprehensivedescription of the cognitive profile of children with a dual diagnosis to explore thepossible additional impact of co-morbidity. First, we hypothesized that DD and DCDwould demonstrate independent specific deficits (markers specific to DD only andmarkers specific to DCD only) as well as a general cognitive profile associated withboth disorders. Secondly, we hypothesized that we would find an additive impairmentof cognitive abilities and psychosocial adjustment in the DD + DCD group.

Method

Participants

A total of 67 children (23 girls, 44 boys), aged 7 years and 8 months to 12 years and11 months, participated in our study. Most of them came from south-western Franceand were referred for participation by the Regional Centre for Learning Disabilities

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Diagnosis or by external therapists (e.g., speech or psychomotor therapists). They hadnormal or corrected-to-normal eyesight, normal hearing, no known psychiatric orneurological disorders and no history of birth complications. Participants were freefrom any medical treatment.

To obtain homogeneous groups, children with intellectual disability, SLI or ADHDaccording to Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition,Text Revision (DSM-IV-TR) criteria were excluded. To reduce heterogeneity and definemore homogeneous groups of participants with DD, children presenting surface dys-lexia as defined by a specific disorder in learning to read without difficulty on meta-phonological tests and/or exclusive impairment of the addressing reading route(reading irregular words) were also excluded.

Children were placed into one of three groups (DD, DCD, or DD + DCD) based ontheir reading skills and motor skills scores. A child was classified as dyslexic only if heor she met both of the following criteria: first, his or her reading fluency score inreading isolated words (word or pseudo-word reading on the ODEDYS-2 (Outils dedépistage des dyslexies, Second Edition) battery) fell below −1.5 SDs and, second, his orher reading speed score fell below −1.5 SDs (Alouette reading test) or his or her readingspeed score below −1 SDs was associated with a reading accuracy score below −1.5 SDs.A child was classified as reading normally if the score was equal to or above +0.5 SDs onreading skills and the Alouette reading test. Children with intermediate results wereexcluded. Motor ability was tested with the French version of the MovementAssessment Battery for Children (M-ABC; Soppelsa & Albaret, 2004), according tothe recommendations of the European Academy for Childhood Disability (Blank,Smits-Engelsman, Polatajko, & Wilson, 2012). A child was classified as DCD if his orher Total Impairment Score (TIS) on the M-ABC was below the 5th percentile, and wasconsidered as have=ing no motor impairment if his or her TIS was above the 15thpercentile.

After the test period, 2 children were excluded because of IQ scores <70. Of theremaining 65 children (21 girls, 44 boys), 20 had DD (8 girls, 12 boys), 22 had DCD (6girls, 16 boys) and 23 had both DD and DCD (7 girls, 16 boys).

Measures

Cognitive assessment: WISC-IVCognitive abilities were assessed with the French-language version of the WISC-IV(Wechsler, 2005). The WISC-IV is a psychometric measure of intelligence in children 6to 16 years of age and produces an IQ based on the results of four index scores obtainedfrom ten core subtests: comprehension, similarities, and vocabulary subtests for theVCI; block design, picture concepts and matrix reasoning for the PRI; coding andsymbol search for the PSI; digit span and letter-number sequencing for the WMI. Rawscores obtained with the WISC-IV were converted to age-scaled scores using tables inthe WISC-IV administration and scoring manual (standard scores for subtest: M = 10,SD = 3; standard scores for index: M = 100, SD = 15). All subtests and indexes havedemonstrated good reliability and validity and are considered good measures of generalintelligence (Sattler, 2008).

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Motor assessment: the Movement Assessment Battery for Children (M-ABC;Henderson & Sugden, 1992).Motor abilities were assessed with the French version of the M-ABC (Soppelsa &Albaret, 2004), an internationally-accepted test that provides indications of gross andfine motor functioning in children aged 4 to 12 years. Depending on their perfor-mance, children obtain scores that range from 0 (success) to 5 (failure) on eightitems. Each subscale produces a separate score for manual dexterity, ball skills(aiming and catching) and balance, and the three subscales generate an overallscore (TIS), which can vary from 0 to 40. Higher scores mean poorer performance.The TIS is an overall measure of motor ability and can be transformed to age-relatedpercentile scores. Children who score below the 5th percentile are considered ashaving DCD. The M-ABC has acceptable validity and reliability (Henderson &Sugden, 1992), and French norms are valid for the French population (Soppelsa &Albaret, 2004).

Reading speed skills (Alouette) and reading strategies and phonological skills(ODEDYS)Reading disorders were evaluated with the Alouette French reading test (revisedversion; Lefavrais, 2005). Alouette assesses the level of lexical decoding and consistsof text to be read aloud. To score the test, the examiner counts the number of wordsread and the number of errors in a given time period, which yields reading age andtwo indices of accuracy and speed when reading a text. Word recognition proce-dures are measured by the ODEDYS-2 test (Jacquier-Roux, Valdois, Zorman,Lequette, & Pouget, 2005). A series of 20 regular words, 20 irregular words and 20non-words (pseudo-words) are presented for reading aloud. Both accuracy andspeed are considered. This test subdivides the reading profile of participants (e.g.,phonological, surface, or mixed DD). The reliability and validity of these two testsare highly satisfactory for most measures (Jacquier-Roux et al., 2005; Lefavrais,2005).

Measures of psychosocial adjustment: child Behavior checklist (CBCL)The parent form of the CBCL (Achenbach & Rescorla, 2001) served to assess overallpsychosocial adjustment. It is a parent-report measure of youth emotional and beha-vioral problems in both clinical and research settings for children aged 6 to 18 years andlists internalizing and externalizing symptoms that parents rate as not true (0), some-what or sometimes true (1), or very true or often true (2). Parents indicate the presenceand degree of each of 113 child behaviors, which are summed to yield (I) competenceand adaptive scale scores, (II) eight syndrome scale scores, (III) six DSM-oriented scalescores, and (IV) broad-band scale scores (including internalizing and externalizing totalscores). High scores mean higher levels of behavioral problems. It is well standardizedand has adequate validity and reliability (Achenbach & Rescorla, 2001).

Measures of attention: the Continuous Performance Test (CPT-II)The CPT-II (Conners & Staff, 2000) is a computerized test that measures sustainedattention and impulsivity. During 14 minutes, respondents are told to click the spacebar when they are presented with any letter except “X”, which they must refrain from

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clicking. The unique CPT paradigm is a test structure consisting of six blocks and threesub-blocks, each containing 20 trials (letter presentations). Inter-stimulus intervals(ISIs) are 1, 2 and 4 s with a display time of 250 ms. The presentation order of thedifferent ISIs varies between blocks. We recorded the following four main scores:omissions (number of non-responses to the target), commissions (number of responsesto non-target stimuli), hit reaction time and perseverations. Each child’s scores werecompared with standard scores (in percentiles) for age, group and gender of the childbeing tested. Test and test-retest reliability coefficients are highly satisfactory for mostmeasures (Conners & Staff, 2000).

Procedure

Children were recruited by advertisement via the Centre for Learning DisabilitiesDiagnosis or speech/psychomotor therapists and specialized parent associations.Parents were contacted by telephone, and a leaflet describing the study characteristics,a recruitment letter, a consent form, the CBCL and a demographic/health screeningquestionnaire were sent to them. All parents and children gave their written informedconsent or assent before participating in the study, which was approved by the localethics committee (CPP Southwest, France).

Participants were tested separately in specially prepared, quiet rooms in the INSERMunit (France). They were subjected to the same complete neuropsychological evaluationduring a half-day session, including an assessment of intellectual abilities (WISC-IV;Wechsler, 2003), reading skills (Alouette test and ODEDYS-2 battery; Jacquier-Rouxet al., 2005, Lefavrais, 2005), motor skills (M-ABC; Henderson & Sugden, 1992), oralskills (Échelle de Vocabulaire en Images Peabody, the French version of the PeabodyPicture Vocabulary Test – Revised; Dunn, Theriault-Whalen, & Dunn, 1993; ÉpreuveVerbale d’Aptitudes Cognitives; Flessas & Lussier, 2003; Épreuve de CompréhensionSyntaxico-Sémantique; Lecocq, 1996), attention capacities (CPT-II; Conners & Staff,2000) and child behavior (CBCL; Achenbach & Rescorla, 2001). These tests were givenin a specific order as part of a neuropsychological battery designed to avoid fatigue andboredom. In addition, all children underwent a medical examination to exclude ADHDand other neurological and psychiatric diseases.

Statistical analyses

All statistical analyses were performed with IBM SPSS 21.0.0.0. Chi2 tests comparingDD, DCD and DD + DCD by gender, sex and National Statistics Socio-economicClassification (NS-SEC).

Descriptive statistics of the dependent variables were tabulated and examined. Forcognitive variables, three categories of scores were considered in the analyses: (i) indexscores (the VCI, PRI, WMI and PSI), which resulted in an FSIQ Score, (ii) subtestscores (similarities, vocabulary, comprehension, block design, picture concepts, matrixreasoning, digit span, letter-number sequence, coding, and symbol search), and (iii)differences between indexes commonly used to test the homogeneity of cognitiveprofiles (Wilkinson, 1993). For psychosocial aspects, the six DSM-oriented scores andfive broad-band scale scores (including internalizing and externalizing total scores)

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were considered in the analyses. For attention variables, omission, commission, hitreaction time and perseveration scores were taken into account.

Analyses of variance (ANOVAs) were used to investigate group differences forpsychometric measures of cognitive, attention and psychosocial adjustment. Tukeypost hoc tests compared means for the different groups. For all tests, a probabilitylevel of p = .05 was considered to be statistically significant (Huberty & Morris, 1989).Correlations between motor and significant group differences on the WISC-IV weresought and reported following the recommendations of Huberty and Morris (1989).Finally, magnitudes of the effects were determined through size calculations(Cohen’s d).

Results

Demographic, clinical and neuropsychological results

General characteristics of the study populationDemographic and clinical data are reported in Table 1. The groups were homogeneous,with no differences for age, F(2, 62) = 0.6, or gender, Chi2 = 0.8, df = 2. Factors thatcould influence cognitive ability (socioeconomic status, parental educational level andvocabulary level) were similar across groups. As expected, DD groups with and withoutDCD differed significantly from the DCD group on all subtests of the reading tests(p < .001), and DCD groups with and without DD differed significantly from the DDgroup on all subtests of the M-ABC (p < .001).

Assessment of behavioral and attention skillsBetween-group variations were not significant on the CBCL. All children had meanscores slightly above the normal range on internalizing symptoms (social problems,anxiety/depression, somatic complaints and social withdrawal). DCD children (with orwithout DD) presented more internalizing and externalizing symptoms than DDchildren (delinquent behaviors, aggressive behaviors); the percentage of DCD childrenwith scores below the 15th percentile was almost twice as high for internalizing andexternalizing symptoms than that of DD children. The co-morbid group had morechildren with pathological scores on the CBCL (almost twice those of the other twogroups for total problems, social withdrawal and anxiety/depression). Between-groupvariations were also not significant on the CPT-II. The three groups did not differ butall children had mean scores within, or slightly above, the normal range for theattention test.

Assessment of cognitive abilitiesLooking at index scores from the WISC-IV, the DD, DCD and DD + DCD groups hadmean scores within, or slightly above, the normal range for the VCI, similarities andvocabulary subtests. On the other hand, all groups had mean scores within or slightlybelow the normal range for the PSI, symbol search and coding subtests. For the threegroups, symbol search and coding were the lowest scores. ANOVAs revealed that thePSI, F(2, 62) = 4.1, p = .02, symbol search, F(2, 62) = 4.6, p = .01, and block designscores, F(2, 62) = 4.7, p = .01, differed across groups. Post hoc group comparisons with

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Table 1. Demographic and Clinical Characteristics of the DD, DCD, and DD + DCD groups.DD (n = 20) DCD (n = 22) DD + DCD (n = 23) p-value

Gender (percentage)Male 12 (60%) 16 (73%) 16 (70%)Female 8 (40%) 6 (27%) 7 (30%)Age in yearsMean (SD) 10.2 (1.3) 9.7 (1.6) 9.9 (1.2)M-ABC (Standard Score)M-ABC Manual Dexterity 2.8 (2.7) 12.8 (2.6) 10.7 (3.6) <.001M-ABC Ball Skills 0.8 (1.4) 6.0 (2.4) 7.0 (3.7) <.001M-ABC Balance 0.9 (1.4) 7.7 (4.6) 7.7 (4.4) <.001M-ABC Total Score 4.4 (3.6) 26.4 (6.0) 25.3 (6.3) <.001Reading Speed (Alouette)CM (Z score) −2.8 (1.4) 0.4 (0.4) −2.4 (1.0) <.001CTL (Z score) −1.5 (0.7) 0.0 (0.7) −1.4 (0.6) <.001Reading Strategies (ODEDYS)IWR Accuracy (Z score) −1.2 (1.3) 0.8 (0.7) −1.1 (1.3) <.001IWR Time (Z score) −2.0 (1.9) 0.2 (0.9) −2.1 (2.2) <.001RWR Accuracy (Z score) −2.3 (2.1) 0.3 (0.7) −1.7 (1.8) <.001RWR Time (Z score) −2.3 (2.3) 0.0 (0.9) −1.6 (1.4) <.001PWR Accuracy (Z score) −2.6 (1.1) 0.3 (0.8) −2.7 (1.1) <.001PWR Time (Z score) −2.6 (2.4) −0.4 (0.8) −1.9 (1.7) <.001CPT-II (Percentiles)Omission 55.9 (26.2) 54.1 (27.0) 52.6 (22.2) .91Comission 70.2 (26.0) 64.8 (26.9) 67.7 (27.5) .81Hit Reaction Time 56.4 (26.8) 53.5 (27.3) 60.6 (26.1) .67Perseveration 53.2 (22.1) 56.0 (23.2) 59.7 (24.5) .66CBCL (Z score)Total Problems 0.8 (1.3) 1.0 (1.3) 1.2 (1.6) .76Internalizing 1.2 (1.7) 1.4 (1.4) 1.4 (1.7) .79Externalizing −0.1 (0.9) 0.0 (1.1) 0.3 (1.3) .43Social Withdrawal 0.7 (1.7) 0.8 (1.0) 1.5 (1.8) .21Somatic Complaints 0.9 (2.0) 1.7 (1.8) 0.8 (1.4) .21Anxiety/Depression 1.1 (1.5) 1.2 (1.5) 1.2 (1.4) .96Social Problems 1.3 (2.2) 1.1 (1.7) 1.0 (1.5) .83Thought Problems 0.5 (1.5) 0.6 (1.9) 1.1 (1.9) .45Attention Problems 1.7 (1.5) 1.8 (1.4) 1.8 (1.7) .99Delinquent Behaviors 0.1 (1.0) 1.1 (1.1) 0.2 (1.0) .91Aggressive Behaviors −0.2 (0.9) 0.3 (1.1) 0.3 (1.4) .42WISC-IVBlock Design 11.6 (3.6)* 8.5 (3.2)* 9.2 (3.3) .01Similarities 13.0 (3.5) 13.8 (3.8) 12.2 (4.3) .39Digit Span 10.4 (3.3) 10.4 (3.5) 9.4 (2.8) .52Picture Concepts 10.6 (2.0) 9.9 (2.6) 10.4 (2.2) .59Coding 7.8 (2.8) 6.0 (2.4) 7.1 (2.8) .12Vocabulary 12.8 (3.3) 12.7 (3.1) 11.9 (3.9) .68Letter-Number Sequence 10.6 (2.3) 10.3 (3.2) 9.7 (3.1) .55Matrix Reasoning 10.3 (1.7) 9.1 (1.9) 10.1 (3.0) .19Comprehension 11.7 (3.7) 11.3 (4.1) 10.9 (3.4) .79Symbol Search 9.9 (3.1)* 7.4 (2.7)* 8.3 (2.4) .01VCI 114.7 (18.3) 117.2 (20.5) 109.9 (21.7) .48PRI 105.3 (13.4)* 95.0 (12.3)* 98.5 (15.3) .06WMI 103.6 (14.4) 102.1 (18.3) 97.9 (15.9) .50PSI 93.7 (13.8)* 82.4 (11.4)* 86.3 (13.7) .02TIQ 107.4 (14.0) 100.2 (16.6) 98.7 (16.9) .18TIQ_VCI −7.4 (10.4)* −17.0 (9.6)* −11.3 (12.3) .02TIQ_PRI 2.1 (11.2) 5.2 (10.3) 0.2 (9.3) .26TIQ_WMI 3.8 (18.6) −1.9 (12.8) 0.7 (13.6) .48TIQ_PSI 13.7 (10.0) 17.9 (14.1) 12.4 (15.9) .38VCI_PRI 9.4 (17.3)* 22.2 (16.6)* 11.4 (17.2) .04PRI_WMI 1.8 (21.5) −7.1 (17.7) 0.6 (16.6) .24VCI_PSI 21.0 (16.1) 34.8 (20.7) 23.7 (24.9) .08PSI_WMI −9.9 (20.8) −19.7 (20.0) −11.7 (16.8) .21

Note. *p <.001. CBCL = Child Behavior Checklist; CM = reading speed index; CPT-II = Continuous Performance Test –Second Edition; CTL = reading accuracy index; IWR = irregular words reading; M-ABC = Movement Assessment Batteryfor Children; PRI = Perceptual Reasoning Index; PSI = Processing Speed Index; PWR = pseudo-words reading;RWR = regular words reading; TIQ = Total IQ; VCI = Verbal Comprehension Index; WISC-IV = Wechsler IntelligenceScale for Children – Fourth Edition; WMI = Working Memory Index. Values in parentheses are percentage.

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the Tukey test showed that the DCD group scores were significantly weaker than theDD scores, with very robust effect sizes (d ≥ 0.8). The same trend was observed for PRIscores, F(2, 62) = 3.0, p = .06. No difference was found for the gap between the highestindex (VCI) and the lowest index (PSI). However, this difference was not clinicallymeaningful since all groups had very large discrepancies (34 for DCD, 21 for DD and23 for DD + DCD). The two gaps, VCI-PRI, F(2, 62) = 3.5, p = .04, IQ-VCI, F(2,62) = 4.2, p = .02, differed across groups. For both, post hoc group comparisons showedthat discrepancies in the DCD group were significantly greater than those in the DDgroup.

Correlations between neuropsychological results and motor skills

Coding, block design, symbol search, PSI and PRI were significantly and negativelycorrelated with the four motor factors of the M-ABC on all motor skills (negativecorrelations were due to the fact that, unlike other tests, the M-ABC measures degrada-tion). For all groups, block design was significantly and negatively correlated withmanual dexterity (r = −.30, p = .014) and total M-ABC score (r = −.30, p = .016);coding was significantly and negatively correlated with manual dexterity (r = −.26,p = .035) and total M-ABC scores (r = −.27, p = .027); symbol search was negativelycorrelated with manual dexterity (r = −.35, p = .004), total M-ABC score (r = −.34,p = .006) and ball skills (r = −.25, p = .047); the PSI was negatively correlated withmanual dexterity (r = −.35, p = .004), ball skills (r = −.30, p = .015) and the total M-ABCscore (r = −.35, p = .004); the PRI was significantly and negatively correlated withmanual dexterity (r = −.31, p = .013), balance (r = −.28, p = .025) and total M-ABCscore (r = −.30, p = .014; see Table 2).

Discussion

In this paper, we attempted to compare isolated disorders (DD and DCD only) andtheir co-occurrence (DD + DCD) in order to (i) explore differences and commonalitiesbetween both disorders, (ii) clarify the contribution of each independent disorder to theobserved deficits, and (iii) determine the impact of co-occurrence on the cognitive,behavioral and attention profiles of children with DD and/or DCD. Our results con-firmed our first hypothesis: a review of the cognitive and psychosocial characteristicsrevealed specificities that differentiated DD and DCD, even though there were alsocommon features with general cognitive and psychosocial dysfunction. Conversely,concerning possible additive effects in the co-morbid group, our results did not confirmour hypothesis: we did not find any cumulative impact on cognitive abilities associatedwith a dual diagnosis and, even more so, co-morbidity seemed to balance the children’sdeficits.

Two different disorders

The DD and DCD results are clearly associated with inter-group variations occurringonly between the DD and DCD groups, suggesting that DD and DCD are distinct andseparate disorders with unique characteristics. They are twofold. Firstly, we found that

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comparisons commonly used to test the homogeneity of cognitive profiles (VCI-PRIand VCI-FSIQ; Wilkinson, 1993) showed greater discrepancies in the DCD than in theDD group. Thus, if heterogeneity is an essential component of the three profiles, it ismore pronounced in the case of children with DCD. Secondly, children with DCD onlywere significantly weaker than children with DD only in the block design and symbolsearch subtests. In both subtests, the DD group produced results in the average rangewhile the DCD group scored more than 2 SDs below average. Both subtests give a goodmeasure of visuo-spatial abilities. The block design subtest is especially considered to bethe most complete measure of visuo-spatial processing in the WISC-IV (Wechsler,2003). As for the symbol search subtest, although it measures processing speed, it alsoassesses visuo-perceptual and visuo-spatial abilities, visuo-motor coordination, visualscanning, cognitive flexibility and attention (Sattler, 2008; Wechsler, 2003). Besides, inthe literature based on the Cattell–Horn–Carroll theory, Keith, Fine, Taub, Reynolds,and Kranzler (2006) established a connection between both subtests with a commonvisual processing factor (Gv). In agreement with previous studies that showed visuo-spatial impairment in DCD (P. H. Wilson & McKenzie, 1998) but efficient visuo-spatialabilities in DD (Bonifacci & Snowling, 2008; De Clercq-Quaegebeur et al., 2010), ourresults suggest that, unlike DD, DCD involves a deficit in visuo-spatial abilities when amotor component is required. Effectively, between-group differences were encounteredin visuo-spatial tasks, but only when a motor response was expected (differences onblock design and symbol search but not on matrix reasoning or picture conceptsubtests). It should be noted that the coding subtest, which involves visuo-spatial andmotor abilities (such as block design and symbol search), cannot be considered, since allgroups failed it uniformly. Our correlation analysis supports this finding, as it reveals

Table 2. Correlations between WISC-IV Subtests and Indexes, and M-ABC Factors.Manual Dexterity Ball Skills Balance Total M-ABC

Total sample (n = 65)PRI −.308* −.128 −.277* −.304*PSI −.352** −.300* −.202 −.349**Block Design −.303* −.170 −.238 −.298*Coding −.262* −.252* −.163 −.274*Symbol Search −.353** −.247* −.213 −.337**DD (n = 20)PRI −.036 −.187 −.153 −.162PSI −.018 .118 −.098 −.004Block Design −.039 −.233 −.024 −.133Coding −.142 .155 −.182 −.115Symbol Search .094 .056 .033 .106DCD (n = 22)PRI −.116 −.055 −.218 −.242PSI .221 −.263 −.019 −.024Block Design .090 .052 −.011 .052Coding .399 −.329 −.070 −.013Symbol Search −.027 −.128 .082 .000DD + DCD (n = 23)PRI −.171 .236 −.081 −.016PSI −.431* −.174 .057 −.307Block Design −.052 .270 −.020 .115Coding −.437* −.249 .008 −.389Symbol Search −.378 −.053 −.107 −.321

Note.*p <.05; **p <.01.

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that all five measures on the WISC-IV involving visuo-spatial and motor abilities weresignificantly related to manual dexterity and total M-ABC scores. Hence, our results,which are consistent with the large meta-analysis of P. H. Wilson and McKenzie (1998),suggest that deficits in visuo-spatial processing, when tasks require a motor response,may be a good marker of DCD.

A shared profile

Despite some differences and considering the broad test battery conducted, the moststriking results were the substantial similarity between disorders, illustrated by thefailure to find significant differences between groups on the majority of measures.The children seemed to perform similarly in most of the items tested, sharing acommon profile in terms of weaknesses and strengths. Firstly, there was a highincidence of emotional and behavioral disturbance. Specifically, the percentage ofpathological scores reached 30–40% in social skills and emotional disturbance (anxietyor depression). In accordance with previous studies (Emck et al., 2009), our resultshighlight psychological difficulties as a common feature in neurodevelopmental dis-orders. Secondly, since a previous study found a link between DD, DCD and attentionproblems (Chaix et al., 2007), we assessed the attentional functions of children as partof the cognitive profile. Once again, we did not observe any significant between-groupdifferences, but attentional problems were common. Thus, although none of thechildren was affected by ADHD (one of our exclusion criteria), each of the three groupspresented behaviors typical of inattention. Finally, the children’s intellectual profilespresented similar characteristics, especially in terms of their weaknesses and strengths.In the three groups, the PRI and WMI scores were within the average range, the PSIscores were within a low average range, and the VCI scores were slightly above thenormal range. Variations in performances and differences among the four indexes wereconsiderable in all three groups. The gap between the best index (VCI) and the lowestindex (PSI) highlighted the strong and marked heterogeneity of all groups (21 for DD,34 for DCD, and 23 for DD + DCD). This discrepancy appears to be inherent to thecognitive profiles of learning disorders. Similarly, the three groups uniformly failed incoding and symbol search, their two lowest subtests. They scored more than 2 SDsbelow the average, which confirmed the findings of previous studies on DD and DCD(Catts et al., 2002; Sattler, 2008; Thomson, 2003; Wechsler, 2003). This result isparticularly interesting as far as the coding subtest is concerned, because it is the onlysubtest that requires learning.

Altogether, our results indicate a shared profile between DD and DCD children.Deficits in processing speed, severe weakness on subtests involving learning, discre-pancy between indexes, heterogeneity of profiles, attentional impairments and social,emotional and behavioral difficulties do not seem to be exclusive indicators of one orthe other of these disorders, but appear to be common to the three groups. A. J. Wilsonet al. (2015) showed a similar trend for DD–dyscalculia co-morbidity. Indeed, in theirstudy, besides demonstrating that dyscalculia and DD are clearly associated withseparate specific cognitive deficits, these authors mainly provide evidence of “domaingeneral bridge symptoms” common to both disorders. Such striking similaritiesbetween disorders that co-occur frequently (as in DD–dyscalculia for A. J. Wilson

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et al., 2015 or as in DD–DCD co-morbidity in the present study) can be explained by acommon model linked to specific learning disorders. Common failure in the codingsubtest, which is the only one that requires learning, tends to strengthen this inter-pretation. Hence, the outlined common portrait that we attempted to show here seemsto be neither DD- nor DCD- nor co-morbid-dependent but linked to a broader, moreintegrative understanding of neurodevelopmental disorders.

What is the status of DD and DCD co-morbidity?

The absence of significant group differences in all neuropsychological abilities betweenco-morbid children and those with only one disorder suggests that the co-morbidcondition does not add to the severity of each deficit. Previous studies have reachedthe same conclusion. For example, overall WISC-IV findings in the study by Loh et al.(2011) provide evidence that the degree of severity of deficits in DCD was similar tothat in the DCD + ADHD groups. However, in our study, children with co-morbidityseemed to take a middle course that softened the deficit profile by considering theweaknesses and strengths of both groups of disorders. This is particularly striking in thevisuo-spatial component, in which DCD children are impaired but DD + DCD childrenare only marginally affected. This compensatory or protective effect has already beenmentioned in other studies which have emphasized that co-morbidity might balance achild’s deficits. For instance, coexisting anxiety disorders might lower the level ofimpulsivity for children with ADHD (Newcorn et al., 2001). In particular, accordingto these authors, the symptoms might vary according to the types of co-morbidassociation; some pathologies appear to aggravate the symptoms while others tend toreduce them. Focusing on a group of ADHD subjects, they thus showed that theassociation with oppositional defiant disorder or conduct disorder increased impulsivitybut reduced inattention, while the association with anxiety disorders increased inatten-tion but reduced impulsivity. In the special case of DD and DCD association, co-morbidity may have a protective effect, especially on the visuo-spatial component.Indeed, visuo-spatial abilities have been shown to be efficient in DD (Bonifacci &Snowling, 2008; De Clercq-Quaegebeur et al., 2010), and several studies have evenindicated that DD is positively associated with superior visuo-spatial abilities(Brunswick, Martin, & Marzano, 2010; Chakravarty, 2009). It is therefore quite con-ceivable that DD + DCD children turn this strength to their advantage. This hypothesisrequires confirmation in future research, and may be of significant importance to thefield.

The second major point of interest is the impact of co-morbidity on psychosocialadjustment. Indeed, even if no significant difference was found between children withonly one disorder and those with a dual diagnosis, the percentage of children withpathological scores in internalizing and externalizing symptoms was much higher(almost twice as high) in the DD + DCD group than in the other two groups.Psychological, emotional and social harms therefore appear to be increased in the co-morbid group. Hence, even if co-morbidity does not seem to amplify the severity ofdisorders (and might even help to reduce their effects in some cases), dual associationseems to create an accumulation of psychosocial disorders. Greater impairment ineveryday functioning has already been seen in previous studies (Crawford, Kaplan, &

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Dewey, 2006) and is not surprising, given that a plurality of disorders leads to anaccumulation of problems and, by extension, to the accumulation of psychologicalconsequences. Furthermore, as pointed out by Kaplan, Dewey, Crawford, and Wilson(2001), assigning a dual diagnosis or multiple diagnoses tends to exaggerate a child’sfeeling of being deficient.

Conclusion and limitations

Our study tried to present a comprehensive psychological and cognitive analysis of theskills of children with DD, DCD, and DD + DCD. Three key results have the potentialto be added to the literature. Firstly, this study provides evidence concerning thedifferences between DD and DCD. Specific characteristics, especially visuo-spatialdisabilities in tasks requiring a motor response and high heterogeneity of the cognitiveprofile, may be good markers of DCD. As expected, the results also suggest a commoncognitive profile (weaknesses and strengths) related to both disorders. However, thatshared model may be attributable to neurodevelopmental disorders as a whole, ascommon failure in the coding subtest (the only one requiring learning) seems toprovide. This trend (the presence of general “bridge symptoms” common to bothdisorders despite a cognitive profile specific to each disorder) was previously found inother studies of co-morbidity (DD–dyscalculia), so it would be interesting to explorethe hypothesis further in future studies, including a wider range of neurodevelopmentaldisorders.

Secondly, concerning co-morbidity, the DD + DCD association does not cause adecrease in intellectual or attentional capacities. Moreover, the DD + DCD associationappears to improve some abilities, as children with co-morbidity seem to acquire theweaknesses and strengths of both disorders, which tends to soften their overall cognitiveprofile. Our results, and those of previous studies, suggest that it would be useful to takeco-morbidity into account, both in research and clinical practice. Children’s symptomscould indeed vary according to types of co-morbidity, and some associations couldaggravate the disorders while others could reduce them. Even if our hypothesis must beimproved and reinforced by future investigations, our results encourage us to concludethat studies on children with DD and DCD (and more generally children with neuro-developmental disorders) should pay careful attention to co-morbidity when theyreview the competencies of these children.

Thirdly, despite the positive neuropsychological results in co-morbid children, thepsychosocial incidence for them seems to be more severe. Dual association seems tocreate an accumulation of psychosocial disorders. This particular feature indicates thatefforts are needed in the psychological care of children with co-morbid associationsand, more broadly, in learning disorders. From a therapeutic point of view, it seemsimportant to explain to children and parents that the overlap of several disorders is notnecessarily negative.

Although our work adds to the literature on the co-morbidity of developmentaldisorders, its limitations need to be acknowledged. First of all, although we usedwell-standardized tests, the absence of a control group should be taken into accountwhen analyzing our results. Secondly, our design and data analysis strategy wasexploratory in nature, so the overall impact was certainly more modest. The large

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number of tests increased the probability of error and should be taken into con-sideration. However, it should be noted that we assessed highly homogeneousgroups (without evidence of intellectual disability, SLI, ADHD or surface DD) andthat our results appear to be quite consistent and in line with those of previousstudies.

Disclosure statement

No potential conflict of interest was reported by the authors.

Funding

This work was supported by the Toulouse University Hospital [grant number 1015502 N°ID-RCB 2010-A00909-30].

ORCID

Jean-Michel Albaret http://orcid.org/0000-0002-0432-4681

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