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Child Neuropsychology

A Journal on Normal and Abnormal Development in Childhood and


Adolescence

ISSN: 0929-7049 (Print) 1744-4136 (Online) Journal homepage: http://www.tandfonline.com/loi/ncny20

Neuropsychological status of French children with


developmental dyslexia and/or developmental
coordination disorder: Are both necessarily worse
than 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?, Child
Neuropsychology, DOI: 10.1080/09297049.2015.1127339

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

Published online: 04 Jan 2016.

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http://www.tandfonline.com/action/journalInformation?journalCode=ncny20

Download by: [88.177.156.165] Date: 04 January 2016, At: 23:45


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

Neuropsychological status of French children with


developmental dyslexia and/or developmental coordination
disorder: Are both necessarily worse than one?
Maëlle Biotteaua,b, Jean-Michel Albaret c
, Sandrine Lelongd and Yves Chaixa,b,d
a
Inserm, Imagerie Cérébrale et Handicaps Neurologiques UMR 825, Centre Hospitalier Universitaire (CHU)
Purpan, Toulouse, France; bUniversité de Toulouse, UPS, Imagerie Cérébrale et Handicaps Neurologiques
UMR 825, CHU Purpan, Toulouse, France; cUniversité de Toulouse III, UPS, PRISSMH-EA4561, Toulouse,
France; dHôpital des Enfants, CHU de Toulouse, CHU Purpan, Toulouse, France
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ABSTRACT ARTICLE HISTORY


Developmental dyslexia (DD) and developmental coordination Received 17 June 2014
disorder (DCD) co-occur frequently, raising the underlying ques- Accepted 27 November 2015
tion of shared etiological bases. We investigated the cognitive Published online 5 January
profile of children with DD, children with DCD, and children with 2016
the dual association (DD + DCD) to determine the inherent char- KEYWORDS
acteristics of each disorder and explore the possible additional Co-morbidity; Developmental
impact of co-morbidity on intellectual, attentional, and psychoso- dyslexia; Developmental
cial functioning. The participants were 8- to 12-year-olds (20 DD, coordination disorder; WISC-
22 DCD, and 23 DD + DCD). Cognitive abilities were assessed by IV; CBCL
the 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 Child
Behavior Checklist (CBCL). No differences were found between the
three groups on attention testing (CPT-II) or psychosocial charac-
teristics (CBCL), but a higher percentage of DD + DCD children had
pathological scores on psychosocial scales. Significant between-
group differences were observed on Processing Speed Index
scores and the block design and symbol search subtests, where
DD 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 children
with DD only and children with DCD only. In particular, visuo-
spatial disabilities and heterogeneity of intellectual profile seem to
be good markers of DCD. However, it should be noted that despite
these distinct and separate characteristics, a common cognitive
profile (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.

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 Neurologiques


UMR 825, CHU Purpan, Place du Dr Baylac, F-31059 Toulouse Cedex 9, France.
© 2016 Taylor & Francis
2 M. BIOTTEAU ET AL.

ADHD, see Feldman, Blum, Gahman, Shults, & DBPNet Steering Committee, 2014; for
the association between SLI and DD, see Ramus, Marshall, Rosen, & van der Lely,
2013). According to Kaplan, Wilson, Dewey, and Crawford (1998), co-morbidity of
learning disorders is more common than not.
There is an ongoing debate regarding why neurodevelopmental disorders are so
frequently associated. One question is whether they are distinct or overlapping condi-
tions, further leading to the question of shared underlying etiology. Pursuant to
previous research by our team relating to both DD (Démonet, Taylor, & Chaix, 2004)
and DCD (Chaix et al., 2007; de Castelnau, Albaret, Chaix, & Zanone, 2007), we
focused this article on DD and DCD co-occurrence.

Neurodevelopmental disorders
Developmental Dyslexia (DD)
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DD or specific reading disability is a persistent neurodevelopmental disorder that affects a


sizeable proportion (3–10%) of the school-age population (Démonet et al., 2004; Peterson
& Pennington, 2012). Children with DD have difficulties in learning to read, despite
sociocultural opportunities, scholarly education, adequate conventional instruction and
intelligence, as well as intact sensory abilities (World Health Organization, 1993). In
addition, poor performance on a variety of measures has been reported, including auditory
processing (Tallal, 2004), working memory (Gathercole, Alloway, Willis, & Adams, 2006),
oral language (McArthur, Hogben, Edwards, Heath, & Mengler, 2000) and motor function-
ing (Ramus, Pidgeon, & Frith, 2003).
Various theories have been offered to explain the neurological and cognitive aspects
of DD. Although significant phenotypic variability and co-morbidity have been
recorded, substantial evidence has established the basis of DD. There is widespread
agreement that difficulties with phonological processing, especially problems with
phonological 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 underlined
the 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 affects
2–7% of school-age children, with an additional 5–10% considered as being “at risk” for
the disorder (American Psychiatric Association, 2000; Asonitou, Koutsouki, Kourtessis, &
Charitou, 2012; Lingam, Hunt, Golding, Jongmans, & Emond, 2009). Despite normal
intelligence, children with DCD have significant and long-standing difficulties in daily
activities that require motor coordination (American Psychiatric Association, 2000; Geuze,
2005a). The disorder’s specific manifestations are varied and pervasive, affecting both
gross and fine motor skills (Macnab, Miller, & Polatajko, 2001; Smits-Engelsman,
Niemeijer, & van Galen, 2001). According to Geuze (2005b), the main characteristics
are postural control problems (hypo/hypertonia, poor distal control, static/dynamic
CHILD NEUROPSYCHOLOGY 3

balance), difficulties in motor learning (learning new skills, planning movements, adapting
to change, automatization) and poor sensori-motor coordination (coordination within/
between limbs, sequencing of movement, use of feedback, timing, anticipation, and
strategic 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 frequent
and has been studied for quite a long time (Denckla, 1985; Haslum, 1989). To cite a few
recent examples, Chaix et al. (2007) discerned an unusually high DCD percentage in a
study of 58 children with DD and phonological disorders: 23 (40%) scored below −2
standard deviations (SDs) on the Lincoln-Oseretsky Motor Development Scale (Rogé,
1984), and 10 scored between −1 and −2 SDs. Similarly, Iversen, Berg, Ellertsen, and
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Tønnessen (2005) examined three groups of children: a clinical group with severe DD
and two ordinary school groups (without DD, composed of 5% least able to read and
5% 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 the
Movement 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 other
hand, O’Hare and Khalid (2002) found that 70% of children with DCD had reading
problems (versus 14% of the control group). However, while their frequency is well
documented, the meaning of this co-occurrence remains an intriguing question, with
questions surrounding the reasons for such associations.
According to theoretical approaches, co-occurrence would reflect partially common
etiological bases, as proposed in the cerebellar hypothesis (Nicolson & Fawcett, 2011;
Nicolson, Fawcett, & Dean, 2001). Considering that dyslexics are significantly impaired
on a large range of abilities and cognitive processes known to be dependent on the
cerebellum, such as executive functioning, memory, learning, attention, visuo-spatial
regulation, language and motor skills (Baillieux, De Smet, Paquier, De Deyn, & Mariën,
2008), it has been suggested that cerebellar dysfunction could constitute a common
causal factor in comorbid reading disabilities and motor impairments (Nicolson et al.,
2001). Conversely, even if shared bases actually provide a suitable explanation for DD
and DCD co-occurrence, other studies lean toward the view that both disorders are
largely distinct. For instance, focusing on genetic aspects, Francks et al. (2003) did not
observe the linkage of hand motor skills to any chromosomal regions implicated in DD
and 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 that
addressing the issue of co-morbidity at the cognitive level might be relevant. In this
specific context, few recent investigations (for DD and SLI co-occurrence, see Ramus
et al., 2013; for DD and dyscalculia co-occurrence, see A. J. Wilson et al., 2015) have
4 M. BIOTTEAU ET AL.

attempted to identify the cognitive bases of co-morbidity, especially proposing domains


specific to each learning disorder (core symptoms central to the disorder) and domains
general to all (symptoms likely shared by other disorders). However, and despite highly
frequent co-morbidity, the cognitive bases in the context of DD + DCD comorbidity
have 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 both
disorders provides conflicting information. DD and DCD may not necessarily be associated
with any specific cognitive profile or co-morbidity, and heterogeneity may obscure the
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picture. Children with DCD have been reported to have lower general intelligence test scores
than 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 the
general intelligence quotient (IQ) of children with DCD was 1 SD below the comparison
group on the four WISC-IV indexes. In the American version of WISC-IV (Wechsler, 2003),
21 children aged 6 to 15 years and identified as having motor dysfunction scored very low on
the 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 the
WISC (comprehension, similarities, vocabulary subtests, and more broadly on the Verbal
Comprehension Index [VCI]), and some studies have found a discrepancy between verbal
subtests comprising the VCI and the Perceptual Reasoning Index (PRI) or the Full-Scale
IQ 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 working
memory (Alloway & Archibald, 2008). De Clercq-Quaegebeur et al. (2010), Jeffries and
Everatt (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 have
mentioned 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 has
found high levels of internalizing problems among children identified as having motor
coordination 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 poor
attentional abilities.

Impact of co-occurrence
To date, we are not aware of any study that has assessed the cognitive profiles for
children 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
CHILD NEUROPSYCHOLOGY 5

often limited to ADHD co-morbidity, only evaluated differences between the co-morbid
group and a comparison group, or looked at differences between the co-morbid group
and a group with one of the two disorders (e.g., SLI vs. SLI + DCD, but not DCD vs
SLI + DCD; (Flapper & Schoemaker, 2013). Other studies did not clearly define their
samples, 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 with
ADHD only (Pitcher, Piek, & Barrett, 2002; Pitcher, Piek, & Hay, 2003), especially with
regard to behavioral and social problems or low education level (Rasmussen & Gillberg,
2000). In contrast, other studies suggest that comorbidity is not associated with greater
deficits than a single diagnosis. For example, Loh, Piek, and Barrett (2011) detected
significant group differences between ADHD and co-morbid groups and between
control and co-morbid groups, but not between DCD and co-morbid groups in
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cognitive abilities (assessed by the WISC-IV), highlighting an equivalent degree of


deficit 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 to
one disorder and what belongs to another, (II) take into account not only differences
but 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 difficulty
identifying the impact of multiple impairments.
In the present study, we attempted to address this issue by comparing children with
DD 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. The
aim of our study was twofold. The primary goal was to determine the inherent
characteristics of each disorder. The second goal was to provide a comprehensive
description of the cognitive profile of children with a dual diagnosis to explore the
possible additional impact of co-morbidity. First, we hypothesized that DD and DCD
would demonstrate independent specific deficits (markers specific to DD only and
markers specific to DCD only) as well as a general cognitive profile associated with
both disorders. Secondly, we hypothesized that we would find an additive impairment
of 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 and
11 months, participated in our study. Most of them came from south-western France
and were referred for participation by the Regional Centre for Learning Disabilities
6 M. BIOTTEAU ET AL.

Diagnosis or by external therapists (e.g., speech or psychomotor therapists). They had


normal or corrected-to-normal eyesight, normal hearing, no known psychiatric or
neurological disorders and no history of birth complications. Participants were free
from any medical treatment.
To obtain homogeneous groups, children with intellectual disability, SLI or ADHD
according to Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition,
Text Revision (DSM-IV-TR) criteria were excluded. To reduce heterogeneity and define
more 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 on
their reading skills and motor skills scores. A child was classified as dyslexic only if he
or she met both of the following criteria: first, his or her reading fluency score in
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reading isolated words (word or pseudo-word reading on the ODEDYS-2 (Outils de


dépistage des dyslexies, Second Edition) battery) fell below −1.5 SDs and, second, his or
her reading speed score fell below −1.5 SDs (Alouette reading test) or his or her reading
speed 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 on
reading skills and the Alouette reading test. Children with intermediate results were
excluded. Motor ability was tested with the French version of the Movement
Assessment Battery for Children (M-ABC; Soppelsa & Albaret, 2004), according to
the recommendations of the European Academy for Childhood Disability (Blank,
Smits-Engelsman, Polatajko, & Wilson, 2012). A child was classified as DCD if his or
her Total Impairment Score (TIS) on the M-ABC was below the 5th percentile, and was
considered as have=ing no motor impairment if his or her TIS was above the 15th
percentile.
After the test period, 2 children were excluded because of IQ scores <70. Of the
remaining 65 children (21 girls, 44 boys), 20 had DD (8 girls, 12 boys), 22 had DCD (6
girls, 16 boys) and 23 had both DD and DCD (7 girls, 16 boys).

Measures
Cognitive assessment: WISC-IV
Cognitive 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 6
to 16 years of age and produces an IQ based on the results of four index scores obtained
from ten core subtests: comprehension, similarities, and vocabulary subtests for the
VCI; block design, picture concepts and matrix reasoning for the PRI; coding and
symbol search for the PSI; digit span and letter-number sequencing for the WMI. Raw
scores obtained with the WISC-IV were converted to age-scaled scores using tables in
the 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 have
demonstrated good reliability and validity and are considered good measures of general
intelligence (Sattler, 2008).
CHILD NEUROPSYCHOLOGY 7

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 and
fine 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 eight
items. Each subscale produces a separate score for manual dexterity, ball skills
(aiming and catching) and balance, and the three subscales generate an overall
score (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-related
percentile scores. Children who score below the 5th percentile are considered as
having DCD. The M-ABC has acceptable validity and reliability (Henderson &
Sugden, 1992), and French norms are valid for the French population (Soppelsa &
Albaret, 2004).
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Reading speed skills (Alouette) and reading strategies and phonological skills
(ODEDYS)
Reading disorders were evaluated with the Alouette French reading test (revised
version; Lefavrais, 2005). Alouette assesses the level of lexical decoding and consists
of text to be read aloud. To score the test, the examiner counts the number of words
read and the number of errors in a given time period, which yields reading age and
two 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 20
non-words (pseudo-words) are presented for reading aloud. Both accuracy and
speed are considered. This test subdivides the reading profile of participants (e.g.,
phonological, surface, or mixed DD). The reliability and validity of these two tests
are 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 overall
psychosocial 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 and
lists 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 presence
and degree of each of 113 child behaviors, which are summed to yield (I) competence
and adaptive scale scores, (II) eight syndrome scale scores, (III) six DSM-oriented scale
scores, and (IV) broad-band scale scores (including internalizing and externalizing total
scores). High scores mean higher levels of behavioral problems. It is well standardized
and 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 sustained
attention and impulsivity. During 14 minutes, respondents are told to click the space
bar when they are presented with any letter except “X”, which they must refrain from
8 M. BIOTTEAU ET AL.

clicking. The unique CPT paradigm is a test structure consisting of six blocks and three
sub-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 the
different ISIs varies between blocks. We recorded the following four main scores:
omissions (number of non-responses to the target), commissions (number of responses
to non-target stimuli), hit reaction time and perseverations. Each child’s scores were
compared with standard scores (in percentiles) for age, group and gender of the child
being tested. Test and test-retest reliability coefficients are highly satisfactory for most
measures (Conners & Staff, 2000).

Procedure
Children were recruited by advertisement via the Centre for Learning Disabilities
Diagnosis or speech/psychomotor therapists and specialized parent associations.
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Parents were contacted by telephone, and a leaflet describing the study characteristics,
a recruitment letter, a consent form, the CBCL and a demographic/health screening
questionnaire were sent to them. All parents and children gave their written informed
consent or assent before participating in the study, which was approved by the local
ethics committee (CPP Southwest, France).
Participants were tested separately in specially prepared, quiet rooms in the INSERM
unit (France). They were subjected to the same complete neuropsychological evaluation
during a half-day session, including an assessment of intellectual abilities (WISC-IV;
Wechsler, 2003), reading skills (Alouette test and ODEDYS-2 battery; Jacquier-Roux
et al., 2005, Lefavrais, 2005), motor skills (M-ABC; Henderson & Sugden, 1992), oral
skills (Échelle de Vocabulaire en Images Peabody, the French version of the Peabody
Picture Vocabulary Test – Revised; Dunn, Theriault-Whalen, & Dunn, 1993; Épreuve
Verbale d’Aptitudes Cognitives; Flessas & Lussier, 2003; Épreuve de Compréhension
Syntaxico-Sémantique; Lecocq, 1996), attention capacities (CPT-II; Conners & Staff,
2000) and child behavior (CBCL; Achenbach & Rescorla, 2001). These tests were given
in a specific order as part of a neuropsychological battery designed to avoid fatigue and
boredom. In addition, all children underwent a medical examination to exclude ADHD
and other neurological and psychiatric diseases.

Statistical analyses
All statistical analyses were performed with IBM SPSS 21.0.0.0. Chi2 tests comparing
DD, DCD and DD + DCD by gender, sex and National Statistics Socio-economic
Classification (NS-SEC).
Descriptive statistics of the dependent variables were tabulated and examined. For
cognitive variables, three categories of scores were considered in the analyses: (i) index
scores (the VCI, PRI, WMI and PSI), which resulted in an FSIQ Score, (ii) subtest
scores (similarities, vocabulary, comprehension, block design, picture concepts, matrix
reasoning, digit span, letter-number sequence, coding, and symbol search), and (iii)
differences between indexes commonly used to test the homogeneity of cognitive
profiles (Wilkinson, 1993). For psychosocial aspects, the six DSM-oriented scores and
five broad-band scale scores (including internalizing and externalizing total scores)
CHILD NEUROPSYCHOLOGY 9

were considered in the analyses. For attention variables, omission, commission, hit
reaction time and perseveration scores were taken into account.
Analyses of variance (ANOVAs) were used to investigate group differences for
psychometric measures of cognitive, attention and psychosocial adjustment. Tukey
post hoc tests compared means for the different groups. For all tests, a probability
level of p = .05 was considered to be statistically significant (Huberty & Morris, 1989).
Correlations between motor and significant group differences on the WISC-IV were
sought 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
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General characteristics of the study population


Demographic 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 that
could influence cognitive ability (socioeconomic status, parental educational level and
vocabulary level) were similar across groups. As expected, DD groups with and without
DCD 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 DD
group on all subtests of the M-ABC (p < .001).

Assessment of behavioral and attention skills


Between-group variations were not significant on the CBCL. All children had mean
scores slightly above the normal range on internalizing symptoms (social problems,
anxiety/depression, somatic complaints and social withdrawal). DCD children (with or
without DD) presented more internalizing and externalizing symptoms than DD
children (delinquent behaviors, aggressive behaviors); the percentage of DCD children
with scores below the 15th percentile was almost twice as high for internalizing and
externalizing symptoms than that of DD children. The co-morbid group had more
children with pathological scores on the CBCL (almost twice those of the other two
groups for total problems, social withdrawal and anxiety/depression). Between-group
variations were also not significant on the CPT-II. The three groups did not differ but
all children had mean scores within, or slightly above, the normal range for the
attention test.

Assessment of cognitive abilities


Looking at index scores from the WISC-IV, the DD, DCD and DD + DCD groups had
mean scores within, or slightly above, the normal range for the VCI, similarities and
vocabulary subtests. On the other hand, all groups had mean scores within or slightly
below the normal range for the PSI, symbol search and coding subtests. For the three
groups, symbol search and coding were the lowest scores. ANOVAs revealed that the
PSI, F(2, 62) = 4.1, p = .02, symbol search, F(2, 62) = 4.6, p = .01, and block design
scores, F(2, 62) = 4.7, p = .01, differed across groups. Post hoc group comparisons with
10 M. BIOTTEAU ET AL.

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 years
Mean (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) <.001
M-ABC Ball Skills 0.8 (1.4) 6.0 (2.4) 7.0 (3.7) <.001
M-ABC Balance 0.9 (1.4) 7.7 (4.6) 7.7 (4.4) <.001
M-ABC Total Score 4.4 (3.6) 26.4 (6.0) 25.3 (6.3) <.001
Reading Speed (Alouette)
CM (Z score) −2.8 (1.4) 0.4 (0.4) −2.4 (1.0) <.001
CTL (Z score) −1.5 (0.7) 0.0 (0.7) −1.4 (0.6) <.001
Reading Strategies (ODEDYS)
IWR Accuracy (Z score) −1.2 (1.3) 0.8 (0.7) −1.1 (1.3) <.001
IWR Time (Z score) −2.0 (1.9) 0.2 (0.9) −2.1 (2.2) <.001
RWR Accuracy (Z score) −2.3 (2.1) 0.3 (0.7) −1.7 (1.8) <.001
RWR Time (Z score) −2.3 (2.3) 0.0 (0.9) −1.6 (1.4) <.001
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PWR Accuracy (Z score) −2.6 (1.1) 0.3 (0.8) −2.7 (1.1) <.001
PWR Time (Z score) −2.6 (2.4) −0.4 (0.8) −1.9 (1.7) <.001
CPT-II (Percentiles)
Omission 55.9 (26.2) 54.1 (27.0) 52.6 (22.2) .91
Comission 70.2 (26.0) 64.8 (26.9) 67.7 (27.5) .81
Hit Reaction Time 56.4 (26.8) 53.5 (27.3) 60.6 (26.1) .67
Perseveration 53.2 (22.1) 56.0 (23.2) 59.7 (24.5) .66
CBCL (Z score)
Total Problems 0.8 (1.3) 1.0 (1.3) 1.2 (1.6) .76
Internalizing 1.2 (1.7) 1.4 (1.4) 1.4 (1.7) .79
Externalizing −0.1 (0.9) 0.0 (1.1) 0.3 (1.3) .43
Social Withdrawal 0.7 (1.7) 0.8 (1.0) 1.5 (1.8) .21
Somatic Complaints 0.9 (2.0) 1.7 (1.8) 0.8 (1.4) .21
Anxiety/Depression 1.1 (1.5) 1.2 (1.5) 1.2 (1.4) .96
Social Problems 1.3 (2.2) 1.1 (1.7) 1.0 (1.5) .83
Thought Problems 0.5 (1.5) 0.6 (1.9) 1.1 (1.9) .45
Attention Problems 1.7 (1.5) 1.8 (1.4) 1.8 (1.7) .99
Delinquent Behaviors 0.1 (1.0) 1.1 (1.1) 0.2 (1.0) .91
Aggressive Behaviors −0.2 (0.9) 0.3 (1.1) 0.3 (1.4) .42
WISC-IV
Block Design 11.6 (3.6)* 8.5 (3.2)* 9.2 (3.3) .01
Similarities 13.0 (3.5) 13.8 (3.8) 12.2 (4.3) .39
Digit Span 10.4 (3.3) 10.4 (3.5) 9.4 (2.8) .52
Picture Concepts 10.6 (2.0) 9.9 (2.6) 10.4 (2.2) .59
Coding 7.8 (2.8) 6.0 (2.4) 7.1 (2.8) .12
Vocabulary 12.8 (3.3) 12.7 (3.1) 11.9 (3.9) .68
Letter-Number Sequence 10.6 (2.3) 10.3 (3.2) 9.7 (3.1) .55
Matrix Reasoning 10.3 (1.7) 9.1 (1.9) 10.1 (3.0) .19
Comprehension 11.7 (3.7) 11.3 (4.1) 10.9 (3.4) .79
Symbol Search 9.9 (3.1)* 7.4 (2.7)* 8.3 (2.4) .01
VCI 114.7 (18.3) 117.2 (20.5) 109.9 (21.7) .48
PRI 105.3 (13.4)* 95.0 (12.3)* 98.5 (15.3) .06
WMI 103.6 (14.4) 102.1 (18.3) 97.9 (15.9) .50
PSI 93.7 (13.8)* 82.4 (11.4)* 86.3 (13.7) .02
TIQ 107.4 (14.0) 100.2 (16.6) 98.7 (16.9) .18
TIQ_VCI −7.4 (10.4)* −17.0 (9.6)* −11.3 (12.3) .02
TIQ_PRI 2.1 (11.2) 5.2 (10.3) 0.2 (9.3) .26
TIQ_WMI 3.8 (18.6) −1.9 (12.8) 0.7 (13.6) .48
TIQ_PSI 13.7 (10.0) 17.9 (14.1) 12.4 (15.9) .38
VCI_PRI 9.4 (17.3)* 22.2 (16.6)* 11.4 (17.2) .04
PRI_WMI 1.8 (21.5) −7.1 (17.7) 0.6 (16.6) .24
VCI_PSI 21.0 (16.1) 34.8 (20.7) 23.7 (24.9) .08
PSI_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 Battery
for 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 Intelligence
Scale for Children – Fourth Edition; WMI = Working Memory Index. Values in parentheses are percentage.
CHILD NEUROPSYCHOLOGY 11

the Tukey test showed that the DCD group scores were significantly weaker than the
DD scores, with very robust effect sizes (d ≥ 0.8). The same trend was observed for PRI
scores, F(2, 62) = 3.0, p = .06. No difference was found for the gap between the highest
index (VCI) and the lowest index (PSI). However, this difference was not clinically
meaningful since all groups had very large discrepancies (34 for DCD, 21 for DD and
23 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 showed
that discrepancies in the DCD group were significantly greater than those in the DD
group.

Correlations between neuropsychological results and motor skills


Coding, block design, symbol search, PSI and PRI were significantly and negatively
correlated with the four motor factors of the M-ABC on all motor skills (negative
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correlations 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 with
manual 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 negatively
correlated 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 with
manual dexterity (r = −.35, p = .004), ball skills (r = −.30, p = .015) and the total M-ABC
score (r = −.35, p = .004); the PRI was significantly and negatively correlated with
manual dexterity (r = −.31, p = .013), balance (r = −.28, p = .025) and total M-ABC
score (r = −.30, p = .014; see Table 2).

Discussion
In this paper, we attempted to compare isolated disorders (DD and DCD only) and
their co-occurrence (DD + DCD) in order to (i) explore differences and commonalities
between both disorders, (ii) clarify the contribution of each independent disorder to the
observed 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 characteristics
revealed specificities that differentiated DD and DCD, even though there were also
common features with general cognitive and psychosocial dysfunction. Conversely,
concerning possible additive effects in the co-morbid group, our results did not confirm
our hypothesis: we did not find any cumulative impact on cognitive abilities associated
with a dual diagnosis and, even more so, co-morbidity seemed to balance the children’s
deficits.

Two different disorders


The DD and DCD results are clearly associated with inter-group variations occurring
only between the DD and DCD groups, suggesting that DD and DCD are distinct and
separate disorders with unique characteristics. They are twofold. Firstly, we found that
12 M. BIOTTEAU ET AL.

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 −.162
PSI −.018 .118 −.098 −.004
Block Design −.039 −.233 −.024 −.133
Coding −.142 .155 −.182 −.115
Symbol Search .094 .056 .033 .106
DCD (n = 22)
PRI −.116 −.055 −.218 −.242
PSI .221 −.263 −.019 −.024
Block Design .090 .052 −.011 .052
Coding .399 −.329 −.070 −.013
Symbol Search −.027 −.128 .082 .000
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DD + DCD (n = 23)
PRI −.171 .236 −.081 −.016
PSI −.431* −.174 .057 −.307
Block Design −.052 .270 −.020 .115
Coding −.437* −.249 .008 −.389
Symbol Search −.378 −.053 −.107 −.321
Note.
*p <.05; **p <.01.

comparisons commonly used to test the homogeneity of cognitive profiles (VCI-PRI


and VCI-FSIQ; Wilkinson, 1993) showed greater discrepancies in the DCD than in the
DD group. Thus, if heterogeneity is an essential component of the three profiles, it is
more pronounced in the case of children with DCD. Secondly, children with DCD only
were significantly weaker than children with DD only in the block design and symbol
search subtests. In both subtests, the DD group produced results in the average range
while the DCD group scored more than 2 SDs below average. Both subtests give a good
measure of visuo-spatial abilities. The block design subtest is especially considered to be
the 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 also
assesses visuo-perceptual and visuo-spatial abilities, visuo-motor coordination, visual
scanning, cognitive flexibility and attention (Sattler, 2008; Wechsler, 2003). Besides, in
the literature based on the Cattell–Horn–Carroll theory, Keith, Fine, Taub, Reynolds,
and Kranzler (2006) established a connection between both subtests with a common
visual processing factor (Gv). In agreement with previous studies that showed visuo-
spatial impairment in DCD (P. H. Wilson & McKenzie, 1998) but efficient visuo-spatial
abilities in DD (Bonifacci & Snowling, 2008; De Clercq-Quaegebeur et al., 2010), our
results suggest that, unlike DD, DCD involves a deficit in visuo-spatial abilities when a
motor component is required. Effectively, between-group differences were encountered
in visuo-spatial tasks, but only when a motor response was expected (differences on
block design and symbol search but not on matrix reasoning or picture concept
subtests). It should be noted that the coding subtest, which involves visuo-spatial and
motor abilities (such as block design and symbol search), cannot be considered, since all
groups failed it uniformly. Our correlation analysis supports this finding, as it reveals
CHILD NEUROPSYCHOLOGY 13

that all five measures on the WISC-IV involving visuo-spatial and motor abilities were
significantly 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 most
striking results were the substantial similarity between disorders, illustrated by the
failure to find significant differences between groups on the majority of measures.
The children seemed to perform similarly in most of the items tested, sharing a
common profile in terms of weaknesses and strengths. Firstly, there was a high
incidence of emotional and behavioral disturbance. Specifically, the percentage of
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pathological scores reached 30–40% in social skills and emotional disturbance (anxiety
or depression). In accordance with previous studies (Emck et al., 2009), our results
highlight psychological difficulties as a common feature in neurodevelopmental dis-
orders. Secondly, since a previous study found a link between DD, DCD and attention
problems (Chaix et al., 2007), we assessed the attentional functions of children as part
of the cognitive profile. Once again, we did not observe any significant between-group
differences, but attentional problems were common. Thus, although none of the
children was affected by ADHD (one of our exclusion criteria), each of the three groups
presented behaviors typical of inattention. Finally, the children’s intellectual profiles
presented 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 PSI
scores were within a low average range, and the VCI scores were slightly above the
normal range. Variations in performances and differences among the four indexes were
considerable in all three groups. The gap between the best index (VCI) and the lowest
index (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 the
cognitive profiles of learning disorders. Similarly, the three groups uniformly failed in
coding and symbol search, their two lowest subtests. They scored more than 2 SDs
below 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 is
particularly interesting as far as the coding subtest is concerned, because it is the only
subtest 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 or
the other of these disorders, but appear to be common to the three groups. A. J. Wilson
et al. (2015) showed a similar trend for DD–dyscalculia co-morbidity. Indeed, in their
study, besides demonstrating that dyscalculia and DD are clearly associated with
separate specific cognitive deficits, these authors mainly provide evidence of “domain
general bridge symptoms” common to both disorders. Such striking similarities
between disorders that co-occur frequently (as in DD–dyscalculia for A. J. Wilson
14 M. BIOTTEAU ET AL.

et al., 2015 or as in DD–DCD co-morbidity in the present study) can be explained by a


common model linked to specific learning disorders. Common failure in the coding
subtest, 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 seems
to be neither DD- nor DCD- nor co-morbid-dependent but linked to a broader, more
integrative understanding of neurodevelopmental disorders.

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


The absence of significant group differences in all neuropsychological abilities between
co-morbid children and those with only one disorder suggests that the co-morbid
condition does not add to the severity of each deficit. Previous studies have reached
the 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 to
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that in the DCD + ADHD groups. However, in our study, children with co-morbidity
seemed to take a middle course that softened the deficit profile by considering the
weaknesses and strengths of both groups of disorders. This is particularly striking in the
visuo-spatial component, in which DCD children are impaired but DD + DCD children
are only marginally affected. This compensatory or protective effect has already been
mentioned in other studies which have emphasized that co-morbidity might balance a
child’s deficits. For instance, coexisting anxiety disorders might lower the level of
impulsivity for children with ADHD (Newcorn et al., 2001). In particular, according
to these authors, the symptoms might vary according to the types of co-morbid
association; some pathologies appear to aggravate the symptoms while others tend to
reduce them. Focusing on a group of ADHD subjects, they thus showed that the
association with oppositional defiant disorder or conduct disorder increased impulsivity
but 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 even
indicated 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 hypothesis
requires confirmation in future research, and may be of significant importance to the
field.
The second major point of interest is the impact of co-morbidity on psychosocial
adjustment. Indeed, even if no significant difference was found between children with
only one disorder and those with a dual diagnosis, the percentage of children with
pathological 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 of
disorders (and might even help to reduce their effects in some cases), dual association
seems to create an accumulation of psychosocial disorders. Greater impairment in
everyday functioning has already been seen in previous studies (Crawford, Kaplan, &
CHILD NEUROPSYCHOLOGY 15

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

Conclusion and limitations


Our study tried to present a comprehensive psychological and cognitive analysis of the
skills of children with DD, DCD, and DD + DCD. Three key results have the potential
to be added to the literature. Firstly, this study provides evidence concerning the
differences between DD and DCD. Specific characteristics, especially visuo-spatial
disabilities in tasks requiring a motor response and high heterogeneity of the cognitive
profile, may be good markers of DCD. As expected, the results also suggest a common
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cognitive profile (weaknesses and strengths) related to both disorders. However, that
shared model may be attributable to neurodevelopmental disorders as a whole, as
common failure in the coding subtest (the only one requiring learning) seems to
provide. This trend (the presence of general “bridge symptoms” common to both
disorders despite a cognitive profile specific to each disorder) was previously found in
other studies of co-morbidity (DD–dyscalculia), so it would be interesting to explore
the hypothesis further in future studies, including a wider range of neurodevelopmental
disorders.
Secondly, concerning co-morbidity, the DD + DCD association does not cause a
decrease in intellectual or attentional capacities. Moreover, the DD + DCD association
appears to improve some abilities, as children with co-morbidity seem to acquire the
weaknesses and strengths of both disorders, which tends to soften their overall cognitive
profile. Our results, and those of previous studies, suggest that it would be useful to take
co-morbidity into account, both in research and clinical practice. Children’s symptoms
could indeed vary according to types of co-morbidity, and some associations could
aggravate the disorders while others could reduce them. Even if our hypothesis must be
improved and reinforced by future investigations, our results encourage us to conclude
that studies on children with DD and DCD (and more generally children with neuro-
developmental disorders) should pay careful attention to co-morbidity when they
review the competencies of these children.
Thirdly, despite the positive neuropsychological results in co-morbid children, the
psychosocial incidence for them seems to be more severe. Dual association seems to
create an accumulation of psychosocial disorders. This particular feature indicates that
efforts are needed in the psychological care of children with co-morbid associations
and, more broadly, in learning disorders. From a therapeutic point of view, it seems
important to explain to children and parents that the overlap of several disorders is not
necessarily negative.
Although our work adds to the literature on the co-morbidity of developmental
disorders, its limitations need to be acknowledged. First of all, although we used
well-standardized tests, the absence of a control group should be taken into account
when analyzing our results. Secondly, our design and data analysis strategy was
exploratory in nature, so the overall impact was certainly more modest. The large
16 M. BIOTTEAU ET AL.

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

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

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