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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
Parent rating of executive function in fetal alcohol
spectrum disorder: A review of the literature and
new data on Aboriginal Canadian children
Jaspreet K. Rai, Maurissa Abecassis, Joseph E. Casey, Lloyd Flaro, Laszlo A.
Erdodi & Robert M. Roth
To cite this article: Jaspreet K. Rai, Maurissa Abecassis, Joseph E. Casey, Lloyd Flaro, Laszlo A.
Erdodi & Robert M. Roth (2016): Parent rating of executive function in fetal alcohol spectrum
disorder: A review of the literature and new data on Aboriginal Canadian children, Child
Neuropsychology, DOI: 10.1080/09297049.2016.1191628
To link to this article: http://dx.doi.org/10.1080/09297049.2016.1191628
Published online: 10 Jun 2016.
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Parent rating of executive function in fetal alcohol spectrum
disorder: A review of the literature and new data on
Aboriginal Canadian children
Jaspreet K. Rai
a
, Maurissa Abecassis
b
, Joseph E. Casey
a
, Lloyd Flaro
c
, Laszlo A. Erdodi
a
and Robert M. Roth
b
a
Department of Psychology, University of Windsor, Ontario, Canada;
b
Neuropsychology Program,
Department of Psychiatry, Geisel School of Medicine at Dartmouth, Lebanon, NH, USA;
c
Private Practice,
Edmonton, Alberta, Canada
ABSTRACT
Aboriginal children in Canada are at high risk of fetal alcohol
spectrum disorder (FASD) but there is little research on the cog-
nitive impact of prenatal alcohol exposure (PAE) in this population.
This paper reviews the literature on parent report of executive
functioning in children with FASD that used the Behavior Rating
Inventory of Executive Function (BRIEF). New data on the BRIEF is
then reported in a sample of 52 Aboriginal Canadian children with
FASD for whom a primary caregiver completed the BRIEF. The
children also completed a battery of neuropsychological tests.
The results reveal mean scores in the impaired range for all
three BRIEF index scores and seven of the eight scales, with the
greatest difficulties found on the Working Memory, Inhibit and
Shift scales. The majority of the children were reported as impaired
on the index scores and scales, with Working Memory being most
commonly impaired scale. On the performance-based tests, Trails
B and Letter Fluency are most often reported as impaired, though
the prevalence of impairment is greater for parent ratings than
test performance. No gender difference is noted for the parent
report, but the boys had slightly slower intellectual functioning
and were more perseverative than the girls on testing. The pre-
sence of psychiatric comorbidity is unrelated to either BRIEF or test
scores. These findings are generally consistent with prior studies
indicating that parents observe considerable executive dysfunc-
tion in children with FASD, and that children with FASD may have
more difficulty with executive functions in everyday life than is
detected by laboratory-based tests alone.
ARTICLE HISTORY
Received 21 December 2015
Accepted 14 May 2016
Published online
10 June 2016
KEYWORDS
Fetal alcohol spectrum
disorders; Neuropsychology;
Executive function;
Cognition;
Neurodevelopment
Fetal alcohol spectrum disorder (FASD) is a non-diagnostic umbrella term widely
adopted to refer to a variety of conditions related to prenatal alcohol exposure (PAE)
(Bertrand, Floyd, & Weber, 2005; Sokol, Delaney-Black, & Nordstrom, 2003). One such
condition is fetal alcohol syndrome (FAS), which involves craniofacial dysmorphology,
growth deficiency, and central nervous system abnormality. Other conditions that do
CONTACT Laszlo A. Erdodi lerdodi@uwindsor.ca Department of Psychology, University of Windsor, Chrysler
Hall South 168 401 Sunset Avenue, Windsor, Ontario N9B 3P4, Canada
CHILD NEUROPSYCHOLOGY, 2016
http://dx.doi.org/10.1080/09297049.2016.1191628
© 2016 Informa UK Limited, trading as Taylor & Francis Group
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not meet the full criteria for FAS but are associated with PAE include partial FAS
(PFAS), alcohol-related neurodevelopmental disorder (ARND), and alcohol-related
birth defects (ARBD).
The prevalence rate of FASD has been reported to be as high as 2–5% in the general
population of the United States (US) and Western Europe (May et al., 2014,2009). In
Canada, prevalence rates in the general population have ranged from 0.1% (Roberts &
Hanson, 2000) to 0.9% (Public Health Agency of Canada, 2003). The rate for children
under the care of the child welfare system, however, has been reported to be consider-
ably higher (Fuchs, Burnside, Marchenski, & Murdy, 2005; Popova, Lange, Burd, &
Rehm, 2014).
The prevalence rate of FASD has generally been reported to be higher for Aboriginal
than non-Aboriginal communities, with rates as high as 10–19% in Canadian samples
(Tough & Jack, 2011). Some have attributed the higher rates of FASD to risk factors
such as poor education, physical and sexual abuse, untreated mental illness, and
poverty, which are often more common in Aboriginal communities (Schröter, 2010).
Others have argued that methodological problems in the epidemiological literature
preclude any firm conclusions with respect to prevalence rates among Aboriginal
Canadians (Pacey, 2009).
FASD and Executive Function
FASD is associated with a variety of cognitive deficits, including in general intellectual
ability, executive function, attention, language, visuospatial skills, verbal and visual
learning and memory, motor function, and social cognition (Davis, Gagnier, Moore,
& Todorow, 2013; Kodituwakku, 2009; Mattson, Crocker, & Nguyen, 2011). Such
deficits are common in relation to PAE, irrespective of whether or not full diagnostic
criteria for FAS are met.
Executive function in particular has been the focus of considerable research in FASD.
This is due in part to the vital role that executive functions play in the self-regulation of
behavior, cognition and emotion (Roth, Isquith, & Gioia, 2005), all of which are com-
monly disrupted in FASD. Furthermore, the neural substrates of executive function, such
as the prefrontal cortex, are vulnerable to the effects of PAE in both animal models (Fabio,
Vivas, & Pautassi, 2015; Mihalick, Crandall, Langlois, Krienke, & Dube, 2001)andin
children with FASD, as revealed by neuroimaging studies (Donald et al., 2015).
Investigations of children with FASD using performance-based tests have reported
deficits in several aspects of executive function (Connor, Sampson, Bookstein, Barr, &
Streissguth, 2000; Fuglestad et al., 2014). Recent meta-analyses examining studies that
have compared children with FASD and typically-developing (TD) children have
provided further support for the presence of executive dysfunction in the disorder.
One such analysis yielded medium effect sizes for working memory and inhibition, and
a large effect size for set shifting (Khoury, Milligan, & Girard, 2015). Another reported
the largest effect sizes for planning, fluency, and set shifting, along with a moderate to
large effect for working memory and a smaller effect for inhibition (Kingdon, Cardoso,
& McGrath, 2015).
A complementary approach to investigating executive function in FASD has
involved the use of rating scales completed by parents, and to a much lesser extent
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by teachers. The use of such rating scales permits a clinician to gauge the integrity of
executive functions as manifested in the “real world”, allowing for a more ecologically
valid assessment of these cognitive abilities than provided by performance-based mea-
sures alone (Isquith, Roth, & Gioia, 2013).
The Behavior Rating Inventory of Executive Function (BRIEF; Gioia, Isquith, Guy, &
Kenworthy, 2000) has been employed in several studies of children with FASD. It has
been shown to have good psychometric properties and has been used extensively in the
pediatric literature with children having the study of a wide variety of disorders (Roth,
Isquith, & Gioia, 2014). The BRIEF was designed to assess executive functioning in the
everyday lives of children over the prior six months. It yields two main index scores,
each of which is composed of several scales. The Behavior Regulation Index (BRI)
reflects an individual’s ability to regulate his or her behavior and emotional responses,
and includes scales assessing the ability to inhibit thoughts and actions (Inhibit),
flexibly shift problem-solving strategies and adjust to changes in his or her environment
(Shift), and regulate his or her emotions (Emotional Control). The Metacognition Index
(MI) reflects the individual’s ability to actively solve problems by evaluating the ability
to get started on tasks without external prompting (Initiate), hold and manipulate
information in mind in order to complete tasks (Working Memory), plan and organize
problem-solving approaches (Plan/Organize), monitor his or her own performance on
tasks for accuracy, monitor the effect of his or her behavior on others (Monitor), and
maintain an organized environment such as maintaining an orderly room and being
able to readily find materials needed for schoolwork (Organization of Materials). The
BRIEF also yields an overall index score, the Global Executive Composite (GEC),
reflecting overall executive functioning. Higher t-scores (mean of 50, standard deviation
[SD] of 10) indicate worse executive functioning, and a t-score of 65 or higher is
considered to be clinically significant (Gioia et al., 2000).
Only one published study to date has evaluated executive functions on performance-
based tests in Aboriginal children with FASD, but it does not report findings specifically
for that subset of their mixed ethnicity sample (Rasmussen et al., 2010). Similarly, only
two studies of the BRIEF in FASD have included Aboriginal children in mixed ethnicity
samples, but neither have reported scores for the Aboriginal subsample (Rasmussen
et al., 2010; Rasmussen, Horne, & Witol, 2006).
In the present paper, we first review the literature on the BRIEF in children with
FASD in order to determine whether they differ from TD children and the prevalence
of clinically significant executive dysfunction as assessed by the BRIEF (Table 1), and
then report new data on parent report BRIEF index and scale scores for a sample of
Aboriginal Canadian children with FASD.
Literature Review
BRIEF Parent Report in FASD: Index Scores
Mean BRIEF index t-scores for children with FASD have been consistently found to be
in the clinical range relative to the standardization sample. This has been found for nine
studies that reported on the GEC (Astley et al., 2009; Gross, Deling, Wozniak, & Boys,
2015; Knuiman, Rijk, Hoksbergen, & van Baar, 2015; McGee, Fryer, Bjorkquist,
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Mattson, & Riley, 2008; Nash et al., 2015; Rasmussen et al., 2006; Rasmussen, McAuley,
& Andrew, 2007; Stevens et al., 2013; Wozniak et al., 2013), all six studies that included
the BRI (Astley et al., 2009; McGee et al., 2008; Nash et al., 2015; Rasmussen et al., 2007;
Schonfeld, Paley, Frankel, & O’Connor, 2006; Stevens et al., 2013), and all five studies
that used the MI (Astley et al., 2009; McGee et al., 2008; Rasmussen et al., 2007;
Schonfeld et al., 2006; Stevens et al., 2013). One study reported higher GEC in children
with FASD than TD children, but did not provide scores (Gautam et al., 2015). Studies
that have compared children with FASD and TD children recruited for the same study
have also found poorer executive functions in the FASD group on the GEC (McGee
et al., 2008; Wozniak et al., 2013), the BRI (McGee et al., 2008), and the MI (McGee
et al., 2008).
It is also informative to know the prevalence of everyday executive dysfunction in
FASD given the heterogeneity of cognitive functioning among these children (Davis
et al., 2013; Mattson et al., 2013). To date, only three studies have reported the
Table 1. Studies Reporting Parent Report BRIEF t-scores in Children with FASD.
Age (years)
Study Participants (% female) MSD BRIEF Indices and Scales
Astley et al. (2009) FAS/PFAS, n= 20 (50.0) 12.7 2.4 GEC, BRI, MI
SE/AE, n= 24 (33.3) 12.2 2.0
ND/AE, n= 21 (47.6) 12.4 2.3
TD, n= 16 (50.0) 12.4 2.7
Gautam et al. (2015) PAE, n= 75 (38.6) 12.3 2.6 GEC
TD, n= 64 (51.6) 12.3 2.5
Gross et al. (2015) FASD, n= 551 (42.5) 10.0 N/A GEC, Shift, Initiate, WM
Knuiman et al. (2015) FASD, n= 37 (46.0) 11.0 2.9 GEC, Inhibit, Shift, EC,
Initiate, WM, P/O, Monitor,
OM
Suspected FASD, n= 25 (56.0) 11.4 2.4
TD, n= 59 (46.0) 10.5 2.7
McGee et al. (2008) PAE, n= 28 (54.2) 15.2 1.5 GEC, BRI, MI, Inhibit, Shift, EC,
Initiate, WM, P/O, Monitor,
OM
TD, n= 15 (46.7) 15.4 1.6
Nash et al. (2015) FASD, n= 25 (48.0) 10.3 N/A GEC, BRI, Inhibit, Shift, EC
Nguyen et al. (2014)
*
FASD with ADHD, n= 73 (36.7) 12.6 2.6 Inhibit,Shift, EC, Initiate, WM,
P/O, Monitor, OMFASD without ADHD, n= 35 (55.6) 12.9 2.8
ADHD, n= 87 (25.6) 11.5 2.7
TD, n= 151 (44.6) 12.4 2.5
Rasmussen et al. (2006) FASD, n= 31 (N/A) 10.0 N/A GEC, Inhibit, Shift, EC,
Initiate, WM, P/O, Monitor,
OM
Rasmussen et al. (2007) FASD, n= 64 (42.2) 8.0 N/A GEC, BRI, MI, Inhibit, Shift, EC,
Initiate, WM, P/O, Monitor,
OM
Schonfeld et al. (2006) FASD, n= 98 (48.0)* 8.6 1.5 GEC, BRI, MI, Inhibit, Shift, EC,
Initiate, WM, P/O, Monitor,
OM
FAS, n= 10 (N/A) N/A N/A
PFAS, n= 45 (N/A) N/A N/A
ARND, n= 43 (N/A) N/A N/A
Stevens et al. (2013) FASD, n= 110 (N/A) N/A N/A GEC, BRI, MI
PAE, n= 49 (N/A) N/A N/A
Wozniak et al. (2013) FASD, n= 24 (46.0) 14.3 2.2 GEC
TD, n= 31 (45.0) 13.7 2.3
Note. *Gender distribution and mean age was reported only for the overall sample of children with FASD. Sample sizes
are also reported for the three subgroups. ADHD = attention-deficit/hyperactivity disorder; ARND = alcohol-related
neurodevelopmental disorder; BRI = Behavioral Regulation Index; EC = Emotional Control; FAS = fetal alcohol
syndrome; GEC = General Executive Composite; MI = Metacognition Index; N/A = not available; ND/
AE = neurobehavioral disorder/alcohol exposed; OM = Organization of Materials; PAE = prenatal alcohol exposure;
PFAS = partial fetal alcohol syndrome; P/O = Plan/Organize; SE/AE = static encephalopathy/alcohol exposed;
TD = typically-developing; WM = Working Memory.
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percentage of children within a sample with FASD who obtained BRIEF index scores in
the clinical range. Of a sample of 64 children, Rasmussen et al. (2007) reported that
86.5%, 83.9%, and 84.5% scored in the clinical range on the GEC, BRI, and MI,
respectively. Using a higher cutoffof two SDs from the standardization sample mean,
Astley et al. (2009) observed impairment for 76.2–85.0% of the sample for the GEC,
71.4–80.0% for the BRI, and 76.2–90.0% for the MI. Most recently, Knuiman et al.
(2015) reported a lower prevalence of clinical-range GEC scores in FASD than prior
studies. They found rates of 46% for children with FASD, 24% for those with suspected
FASD, and 12% for those without FASD. These latter findings must be interpreted with
caution, however, as classification into groups was based solely on a questionnaire
completed by parents asking whether or not their child had been diagnosed with or was
suspected of having FASD.
Three studies examined whether the subtype of FASD is related to BRIEF scores.
One reported no differences for the BRI and the MI between children with diagnoses of
FAS, PFAS, or ARND (Schonfeld et al., 2006). Another found comparable index scores
for children classified as FAS/PFAS, static encephalopathy/alcohol-exposed or neuro-
behavioral disorder/alcohol-exposed (Astley et al., 2009). In contrast, the three BRIEF
index scores were reported to be more impaired and more likely to be in the clinical
range for a group of children with FASD than children with PAE (i.e., not meeting
criteria for FASD), although the mean t-scores for both groups were in the clinical
range, with the exception of the MI for the PAE group, which was just below the cutoff
(t= 64.9; Stevens et al., 2013).
Together, these studies indicate that children with FASD typically score within the
clinical range on all three BRIEF index scores. This holds true regardless of whether the
children are compared to the published normative sample or to TD children recruited
for the same study. Furthermore, although the literature is relatively sparse and some-
what inconsistent at this time, the extent of executive dysfunction as reflected by BRIEF
index scores is generally comparable across most FASD subtypes.
BRIEF Parent Report in FASD: Scale Scores
Three studies reported scores for all BRIEF scales within a sample of children with
FASD. In the first such study, Rasmussen et al. (2006) observed that nearly all scales
were in the clinical range, with the greatest difficulty experienced for Working Memory
and Plan/Organize, and the least for Organization of Materials. No ethnic difference
was found on the BRIEF between Aboriginal and non-Aboriginal children, although
separate scores for these subgroups are not provided. In a follow-up study (with
participants of unspecified ethnicity), all scales were in the clinical range, with the
highest scores obtained for Initiate, Working Memory and Inhibit, and the lowest
scores for Plan/Organize and again for Organization of Materials (Rasmussen et al.,
2007). Impairment was most common for Initiate (79.4%), Working Memory (78.1%),
and Inhibit (75.0%), while even the scale with the lowest percentage—Plan/Organize—
identified almost 59.6% of the sample as impaired. McGee et al. (2008) found worse
scores on all BRIEF scales in adolescents with PAE as compared to TD children, with
the largest effects seen for Initiate, Plan/Organize and Monitor, and the smallest for
Organization of Materials. In contrast, Knuiman et al. (2015) only observed worse
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scores in their FASD group compared to their TD group for the Inhibit, Emotional
Control, and Organization of Materials scales, with Inhibit the only one in the clinical
range.
Two studies only examined a few of the BRIEF scales. Gross et al. (2015) observed
mean t-scores in the clinical range for the three scales they examined (Initiate, Shift,
and Working Memory) in their large sample of children with FASD, with Working
Memory having the highest score. In a study of a self-regulation intervention for
children with FASD, pre-treatment BRIEF scores were in the clinical range for the
three scales evaluated—Inhibit, Shift, and Emotional Control (Nash et al., 2015).
Two studies have examined parent report BRIEF in children with FASD and
comorbid attention-deficit/hyperactivity disorder (ADHD), with ADHD being highly
prevalent among those with FASD (Mattson et al., 2011). Rasmussen et al. (2010) found
that children with FASD with and without comorbid ADHD do not differ on an
executive function composite score that includes the BRIEF and a performance-based
test; the results for the BRIEF itself are not reported. Nguyen et al. (2014) compared
children with FASD with and without comorbid ADHD, children with ADHD only,
and TD children. Their results revealed that the FASD without ADHD group had
higher t-scores for all BRIEF scales relative to the TD group, although none of the
scores were clinically elevated. In contrast, children with FASD and comorbid ADHD
had higher scores than the other groups on almost all scales, with the highest scores
obtained for Inhibit and Working Memory.
These findings indicate that children with FASD have difficulty with multiple aspects
of executive functions, as assessed by the individual scales of the BRIEF parent report,
with comorbid ADHD being associated with an exacerbating of executive dysfunction
in at least one study. However, no clear profile of scale elevations has emerged across
studies. This may be due in part to there being relatively few investigations reporting
scores for all eight scales. Nonetheless, the available research indicates that the most
pronounced impairment tends to be seen for Working Memory, while Organization of
Materials typically has the lowest score, though in some studies is still within the clinical
range.
Relationship between BRIEF Scores and Performance-Based Tests
A small number of studies of children with FASD have investigated the relationship
between scores on the parent report BRIEF and scores on performance-based tests of
executive function. These have revealed low or non-significant correlations (Gross et al.,
2015; Nguyen et al., 2014). Interestingly, in one study impairment was observed in
80–90% of the sample for the BRIEF index scores but only 34% on the Trail Making
Test (TMT), the latter being the performance-based test with the highest percentage of
impaired scores (Astley et al., 2009).
No association to modest relationships between parent ratings on the BRIEF and
neuropsychological test performance is common in the literature on a number of
disorders (McAuley, Chen, Goos, Schachar, & Crosbie, 2010; Parrish et al., 2007;
Toplak, Bucciarelli, Jain, & Tannock, 2008). The reason for such a discrepancy is
unclear, but it has been hypothesized to be related to performance-based tests assessing
executive functions over a short time frame in a typically highly structured setting, in
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contrast to the integrated, multidimensional, and priority-based decision-making that is
frequently needed in real-world situations (Goldberg & Podell, 2000; Isquith et al.,
2013).
Summary of BRIEF Studies
Overall, the current literature on the parent report BRIEF indicates considerable
executive dysfunction in the everyday lives of children with FASD. This is reflected in
both the more general measures of functioning (the GEC, BRI, and MI) and several of
the individual scales, with the Working Memory scale being the most commonly
impaired across studies. However, few studies have examined whether ratings of
executive function are impacted by factors such as gender or the presence of psychiatric
conditions that are highly comorbid with FASD, such as ADHD and depression (Fryer,
McGee, Matt, Riley, & Mattson, 2007).
The Present Investigation
In the present investigation, we sought to replicate a prior study that used the parent
report BRIEF in a sample of Aboriginal Canadian children but that does not provide
scores for the Aboriginal subset of participants and only states that there are no
ethnicity effects in the data (Rasmussen et al., 2006). We hypothesized that our
Aboriginal children with FASD would have a high prevalence of executive dysfunction
both on the BRIEF and on performance-based tests, but that rates would be higher for
the former given the findings of Astley et al. (2009). Furthermore, since generally low to
modest correlations are seen between the BRIEF and performance-based test scores in
FASD (Gross et al., 2015) and other populations (Lovstad et al., 2012; McAuley et al.,
2010), we expected to observe a similar limited relationship in our sample. We also
evaluated whether there are gender differences on the BRIEF in Aboriginal children
with FASD. Based on the work of Rasmussen et al. (2006), we expected that girls would
be reported to have worse executive functions than boys, especially for the BRI and the
Inhibit scale, although these authors did not report on whether there were gender
effects within their Aboriginal subsample specifically. Finally, we evaluated whether the
presence of psychiatric comorbidity is associated with greater impairment on the
BRIEF.
Method
Participants
The sample included a consecutive series of Aboriginal children with FASD referred for
neuropsychological assessment. The term “Aboriginal”refers to those people who are
First Nations as characterized within the constitution of Canada. All children were
referred to a child neuropsychologist in private practice in Edmonton, Alberta, Canada
by psychiatrists, pediatricians, neurologists, or social workers. The presence of FASD
was primarily established by medical specialists (pediatricians, psychiatrists, pediatric
neurologists) in clinics specializing in the evaluation of FASD prior to referral for
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neuropsychological assessment, or in some cases confirmed upon further evaluation by
a neuropsychologist. This was based on medical history and evaluation, including
information about growth factors, facial morphology, central nervous system dysfunc-
tion, and an admission of alcohol use during pregnancy. The specific subtype of FASD,
based on the four-digit coding system (Astley, 2004), was available for only a small
subset of the patients, as reports provided by the FASD clinics generally concluded “this
child meets the diagnostic criteria for FASD”without reference to a specific four-digit
code.
Seven performance validity tests (PVTs) were used to determine the credibility of the
test performance: Word Memory Test standard cutoff(Green, 2003), Medical Symptom
Validity Test standard cutoff(Green, 2004), Non-Verbal Medical Symptom Validity
Test standard cutoff(Green, 2008), TMT B/A ratio < 1.50 (Iverson, Lange, Green, &
Franzen, 2002), Wisconsin Card Sorting Test (WCST) Failure to Maintain Set > 3
(Greve, Heinly, Bianchini, & Love, 2009), Conners’Continuous Performance Test –
Second Edition (CPT-II) omissions and perseverations t-scores > 100 (Conners, 2004).
The majority of the sample (65.4%) passed all PVTs, and 34.6% failed one.
The final sample for analyses consisted of 52 children aged 9–16 years (mean = 13.2,
SD = 2.7). There were 23 girls (44.2%) and 29 boys (55.8%). The presence of comorbid
diagnoses was established from clinical evaluation and collateral sources of information.
Half of the children in the sample had at least one comorbid diagnosis. These included
ADHD (n= 12), conduct disorder (n= 2), nonverbal learning disability (n= 1),
language impairment (n= 2), mood disorder (n= 1), anxiety disorder (n= 1), post-
traumatic stress disorder (n= 1), reactive attachment disorder (n= 1), personality
disorder (n= 4), and pica (n= 1).
The children were usually raised on reserves until placed with Caucasian or
Aboriginal families (equally) in homes outside the reserve. All of the children were
either adopted or placed in foster homes. The children were typically exposed to the
English language from birth, and most attended either regular or specialized school
programs. Informed consent was obtained from a parent or other legal guardian for the
use of the child’s demographics, diagnostic information, and neuropsychological test
data for the purpose of research. The study was approved by the University of Windsor
Ethics Review Board.
Procedure
Behavior Rating Inventory of Executive Function (BRIEF)
A caregiver completed the BRIEF (Gioia et al., 2000), an 86-item rating scale for
children and adolescents aged 5–18 years. Items are rated on a three-point scale
(with the responses never,sometimes,andoften), with higher scores reflecting greater
difficulty with executive function. The BRIEF yields an overall score, the GEC,
composed of two index scores: the Behavioral Regulation Index (BRI) and
Metacognition Index (MI). The BRI is comprised of three clinical scales (Inhibit,
Shift, and Emotional Control) and the MI is comprised of four clinical scales
(Working Memory, Plan/Organize, Organization of Materials, and Monitor). Raw
scores are converted to t-scores relative to the large normative sample (n= 1419). A
t-score of 65 or higher is considered impaired (Gioia et al., 2000). The measure has
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good psychometric properties, including internal consistency and test-retest reliabil-
ity, and there is a wealth of evidence for its usefulness for assessing executive
functioning in a variety of populations (for a review, see Roth et al., 2014). All
BRIEF profiles met the published criteria for response validity.
Performance-Based Tests
Children with FASD were administered a battery of neuropsychological tests.
Intellectual functioning was assessed using the Full Scale IQ (FSIQ) from the
Wechsler Intelligence Scale for Children –Third Edition (WISC-III; Wechsler, 1991)
or WISC –Fourth Edition (WISC-IV; Wechsler, 2003). Executive functions were
assessed using the following measures.
Wisconsin Card Sorting Test (WCST) Total Perseverative Errors. The WCST (Heaton,
Chelune, Talley, Kay, & Curtis, 1993) measures concept formation and set shifting. The
child is asked to match key cards from a deck, one by one, to one of four key cards. The
cards can be matched based on one or more of three principles, and the child uses
feedback from the examiner to determine which of these principles is correct at any
given time. Once the child demonstrates an understanding of the operating matching
criterion by obtaining ten consecutive correct scores, the criterion is changed without
warning to the child. The test is discontinued when the child successfully completes six
categories (ten consecutive correct matches per category) or when all 128 cards have
been sorted.
Trail Making Test (TMT) Time to Complete Part A and Part B. The TMT (Reitan &
Wolfson, 1985)is a timed paper-and-pencil test consisting of two parts. The children’s
version of the TMT is used for children aged 9 to 14 years, while the adult version is
used for individuals aged 15 years and over. In Part A (TMT-A), participants are
presented with numbered circles scattered around the page and asked to connect
them in numerical order as quickly as possible. The children’s version consists of 15
circles, while the adult version consists of 25 circles. Part B (TMT-B), which is
considered a measure of set shifting, requires participants to connect encircled numbers
and letters in alternating order as quickly as possible (i.e., 1-A-2-B-3-C. . .).
Controlled Oral Word Association Test (COWAT) Total Correct. The Controlled Oral
Word Association Test (COWAT; Spreen & Benton, 1977) is a task of phonemic verbal
fluency in which children are asked to orally generate as many words as they can that
begin with a specific letter (“F”,“A”, and “S”in this study) in 60-second trials. Children
are not permitted to use proper nouns (i.e., the names of people or places).
Conners’Continuous Performance Test –Second Edition (CPT-II) Errors of Omission,
Errors of Commission, and Mean Hit Reaction Time. The CPT-II (Conners, 2004)i
sa
test in which letters are presented on a computer screen, one at a time, over a period of
approximately 14 minutes. Participants are instructed to respond by pressing the
spacebar when a letter appears on the screen, but to withhold their responses when
presented with the letter X (target). Errors of omission reflect a failure to respond to
non-target stimuli, while errors of commission occur when the participant responds to
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an “X”stimulus, reflecting impulsivity. A fast mean hit reaction time can also reflect
impulsivity, especially in the context of elevated errors of commission.
Statistical Analysis
To facilitate comparison with the BRIEF, neuropsychological test scores were converted
to t-scores using appropriate normative data, with higher scores reflecting worse
performance. The exception is the FSIQ, for which the standardized scale score is
employed.
Descriptive statistics (mean, SD, range and skew) were computed for the variables of
interests. The percentage of children with scores in the clinical range (t≥65) was
computed. BRIEF scores for boys and girls, as well as subsets of participants with and
without a psychiatric comorbidity, were compared using independent sample t-tests.
Effect size was computed using Cohen’sd. Pearson correlation coefficients were com-
puted between the BRIEF and performance-based measure scores. All analyses used
p< .05 two-tailed significance tests to determine significance.
Results
Outlier Analysis
While all BRIEF scores had a skew within ±1.0, while most were within ±0.50, some of
the cognitive tests had excessive skew in the impaired direction (TMT-A: 2.89; TMT-B:
1.92; CPT-II Errors of Omission: 1.26). Outliers on these scales were replaced with the
t-score corresponding to a z-score of +2.0, computed using the standard raw-to-z
transformation formula. This procedure reduces the undue influence of extreme scores
while still preserving their relative standing within the sample (Field, 2005).
Transformed scores were used in subsequent analyses.
The BRIEF and Neuropsychological Test Performance
Table 2 presents the BRIEF and neuropsychological test results. All of the mean BRIEF
scale and index scores were in the impaired range, with the exception of Organization of
Materials. Among the scales, Working Memory and Inhibit had the highest mean t-scores.
A majority of the children were rated as being in the impaired range on the indices and
scales. Among the scales, the percentage impaired ranged from a low of 55.8% for
Organization of Materials to a high of 82.7% for Working Memory, with about 70% of
children being impaired on most scales. For both the MI and the GEC, over 80% of
children fell into the impaired range, while 73.1% were impaired on the BRI.
On the neuropsychological measures, the mean FSIQ fell into the low average range,
with scores ranging from the borderline to average range. Mean scores on letter fluency
and TMT-B were in the impaired range, with the majority of children scoring in the
impaired range (66.8% and 78%, respectively). In contrast, perseverative errors on the
WCST, TMT-A and CPT-II variables were not in the impaired range, with only around
one quarter of the children obtaining scores within the impaired range on these
measures.
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Many BRIEF and neuropsychological test scores had a bimodal distribution
(Table 2). For most BRIEF scales, a first peak was observed around the cutofffor
impairment, while a second peak reflected more severe impairment. A similar trend was
observed for FSIQ and TMT-B. For FAS, TMT-A and CPT-II a first peak was well
within the normal range, while a second peak was in the impaired range.
Effect of Psychiatric Comorbidity and Gender
Table 3 presents the BRIEF and performance-based test scores for children with and
without psychiatric comorbidities. No effect of comorbidity was observed for either the
BRIEF or the performance-based tests. Gender differences on mean BRIEF t-scores
were also examined. No gender effect is observed for the BRIEF. On performance-based
tests, a lower FSIQ was found for boys (M= 79.9, SD = 7.7) than girls (M= 84.6,
SD = 9.3), t(50) = 2.0, p= .05, d= .55. Similarly, boys (M= 55.3, SD = 10.2) were more
perseverative than girls (M= 48.3, SD = 9.2) on the WCST, t(50) = 2.51, p< .05, d= .72.
No other significant gender differences are observed.
Correlation between the BRIEF and Neuropsychological Test Performance
Table 4 presents the correlations between the BRIEF and the neuropsychological test
scores. Few significant correlations are observed. A greater number of perseverative
errors on the WCST is associated with better scores on the MI and Organization of
Materials. Slower reaction time on the CPT-II is associated with better Organization of
Table 2. Descriptive Statistics for BRIEF Parent Report and Performance-Based Tests in Aboriginal
Canadian Children with FASD.
Test MSDRange Skew % Impaired Peaks
BRIEF: Inhibit 73.6 14.8 41–103 −0.26 73.1 75 & 85
BRIEF: Shift 72.4 12.7 40–94 −0.34 75.0 65 & 85
BRIEF: Emotional Control 70.3 15.6 38–123 0.30 69.2 -
BRIEF: Initiate 68.8 12.3 43–93 −0.25 69.2 55 & 70
BRIEF: Working Memory 74.0 11.1 45–93 −0.28 82.7 70 & 80
BRIEF: Plan/Organize 72.1 10.7 53–103 0.50 75.0 -
BRIEF: Monitor 70.2 8.4 47–86 −0.56 76.9 65 & 75
BRIEF: Organization of Materials 63.6 10.1 34–98 −0.14 55.8 -
BRIEF: BRI 74.4 13.6 44–109 −0.27 73.1 -
BRIEF: MI 73.6 9.4 54–92 −0.23 80.8 75 & 85
BRIEF: GEC 75.0 11.4 38–101 −0.53 86.5 75 & 90
FSIQ 82.0 8.7 70–102 0.35 38.5 72 & 90
WCST Perseverative Errors 52.2 10.3 27–72 −0.37 12.2 -
TMT-A* 59.4 15.1 36–107 1.04 26.9 50 & 65
TMT-B* 78.0 28.8 35–160 1.09 63.3 -
COWAT 66.8 13.8 37–97 −0.15 58.3 55 & 75
CPT-II Errors of Omission* 55.3 12.4 41–83 1.13 20.0 45 & 80
CPT-II Errors of Commission 52.0 10.9 23–72 −0.50 8.0 40 & 65
CPT-II Mean Hit Reaction Time 47.5 10.3 20–80 0.25 8.0 -
Note. *Outliers transformed by converting original value to raw score corresponding to z= 2.0.
BRI = Behavioral Regulation Index; COWAT = Controlled Oral Word Association Test; CPT-II = Conners’Continuous
Performance Test –Second Edition; FSIQ = Full Scale IQ (standard score); GEC = Global Executive Composite; MI =
Metacognition Index; TMT-A = Trail Making Test, Part A; TMT-B = Trail Making Test, Part B; WCST = Wisconsin Card
Sorting Test. The Peaks column represents peaks in score distribution. Except for FSIQ, all scores on performance
measures are converted to t-scores, with higher scores reflecting more severe impairment. The cutofffor impairment
is t≥65.
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Materials. None of the other neuropsychological measures correlate with any BRIEF
index or scale score.
Discussion
In the present study, the parent report BRIEF results indicate significant executive
dysfunction in the everyday lives of Aboriginal children with FASD. All three index
scores (the GEC, BRI and MI) are in the clinical range at the group level in this FASD
sample, with 73–86% of the children having scores in the clinical range (t≥65). All
Table 3. Independent t-tests Comparing Parent Report BRIEF t-scores in Children with FASD with and
without Psychiatric Comorbidity.
Present (n= 28) Absent (n= 24)
Test M SD M SD p
BRIEF: Inhibit 73.0 14.2 74.3 15.7 .76
BRIEF: Shift 70.9 13.5 74.2 11.8 .35
BRIEF: Emotional Control 68.4 15.6 72.6 15.7 .34
BRIEF: Initiate 67.1 11.6 70.8 12.9 .28
BRIEF: Working Memory 72.4 10.1 76.0 12.2 .25
BRIEF: Plan/Organize 70.8 10.4 73.7 11.1 .34
BRIEF: Monitor 69.3 9.4 71.3 7.2 .38
BRIEF: Organization/Materials 62.6 8.2 64.8 11.9 .46
BRIEF: BRI 72.4 13.7 76.7 13.4 .26
BRIEF: MI 72.7 9.6 74.6 9.4 .47
BRIEF: GEC 74.3 10.3 75.8 12.7 .63
FSIQ 81.1 8.1 83.0 9.3 .43
WCST Perseverative errors 53.0 10.7 51.1 9.9 .51
TMT-A 59.8 14.8 59.0 15.8 .86
TMT-B 76.6 24.6 79.7 33.3 .71
COWAT 66.5 12.3 67.2 15.6 .87
CPT-II Omissions 56.7 13.4 53.7 11.3 .40
CPT-II Commissions 53.0 11.4 50.8 10.5 .48
CPT-II Hit Reaction Time 46.1 12.4 49.0 7.4 .33
Note. BRI = Behavioral Regulation Index; COWAT = Controlled Oral Word Association Test; CPT-II = Conners’Continuous
Performance Test –Second Edition; FSIQ = Full Scale IQ (standard score); GEC = Global Executive Composite; MI =
Metacognition Index; TMT-A = Trail Making Test, Part A; TMT-B = Trail Making Test, Part B; WCST = Wisconsin Card
Sorting Test.
Table 4. Correlations between BRIEF Parent Report and Performance-Based Test Scores.
BRIEF Scale FSIQ WCST TMT-A TMT-B FAS OMI COM HRT
Inhibit −.08 −.22 .05 .03 −.18 −.07 .19 −.16
Shift −.27 −.10 .25 .15 .13 .00 .06 −.11
Emotional Control −.12 −.17 .09 .05 .04 −.21 .05 −.02
Initiate −.17 −.06 .27 .26 .19 −.06 −.28 −.19
Working Memory −.24 −.11 .21 .26 .20 −.03 .05 −.16
Plan/Organize .02 −.17 .09 −.20 .11 −.17 .00 −.08
Monitor −.14 −.19 .25 .01 .09 −.19 .03 −.11
Organization of Materials .00 −.31* .19 .00 −.04 .06 −.02 −.35*
BRI −.12 −.15 .17 .10 .00 −.11 .09 −.10
MI −.20 −.34* .23 .05 .17 −.11 −.06 −.24
GEC −.21 −.26 .24 .09 .12 −.12 −.04 −.15
Note.*p <.05. BRI = Behavioral Regulation Index; COM = CPT-II errors of commission; COWAT = Controlled Oral Word
Association Test; CPT-II = Conners’Continuous Performance Test –Second Edition; FAS = letter fluency FSIQ = Full
Scale IQ (standard score); GEC = Global Executive Composite; HRT = CPT-II mean hit reaction time; MI =
Metacognition Index; OMI = CPT-II errors of omission; TMT-A = Trail Making Test, Part A; TMT-B = Trail Making
Test, Part B; WCST = Wisconsin Card Sorting Test. Except for FSIQ, all scores on performance measures are converted
to t-scores, with higher scores reflecting more severe impairment. The cutofffor impairment is t≥65.
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prior studies reporting BRIEF index scores have found that they are significantly worse
in children with FASD relative to either the measure’s standardization sample or a
study-specific sample of TD children. Only three studies to date have reported the
percentage of children with FASD in their samples who are in the clinical range on the
BRIEF (Knuiman et al., 2015), two of which also observed very high rates, ranging from
71.4% to 90% (Astley et al., 2009; Rasmussen et al., 2007), and one reporting a rate of
46% for the GEC, though diagnostic grouping in that study was solely based on a
questionnaire completed by parents (Knuiman et al., 2015). The present findings are
consistent with the few studies that have reported impairment, as reflected by both the
BRI and MI t-scores (Astley et al., 2009; McGee et al., 2008; Rasmussen et al., 2007;
Stevens et al., 2013).
Mean scores for seven of the eight BRIEF scales were also in the clinical range in our
sample. The greatest difficulty was endorsed for Working Memory, followed by Inhibit,
Shift and Plan/Organize, with all but Organization of Materials within a range of about
five t-scores. Prior studies of non-Aboriginal samples have most commonly found the
greatest impairment on Working Memory, typically followed closely by Initiate, Inhibit
or Plan/Organize. Both in the present sample and in prior research, Organization of
Materials generally shows the least impairment, with studies differing with respect to
whether the score is in the clinical range or not. Together, these findings indicate
widespread disruption of executive functions in children with FASD, at least as reported
by their parents. This is largely consistent with recent meta-analyses of performance-
based tests indicating that children with FASD are impaired in several aspects of their
executive function, including working memory, inhibition, planning, set shifting and
fluency (Khoury et al., 2015; Kingdon et al., 2015).
This study has found that the presence of psychiatric comorbidity in children with
FASD did not have an impact on the BRIEF results. This contrasts with some prior
work which found that comorbidities such as ADHD are associated with worse execu-
tive function on the parent report BRIEF (Nguyen et al., 2014), although not on
performance-based executive function measures (Glass et al., 2013; Nguyen et al.,
2014). The reason for the present results is unclear, and there is not a sufficiently
large subset of children with a specific comorbidity such as ADHD to permit subgroup
analyses. Thus, the possibility that the present findings are due, at least in part, to the
presence or lack thereof of specific comorbid diagnoses among this FASD sample
cannot be ruled out. Additional studies evaluating the impact of prevalent comorbid-
ities in FASD on ratings of executive functioning, in both Aboriginal and non-
Aboriginal samples, are needed to clarify this issue.
A sizeable subset of this sample of Aboriginal children with FASD was impaired on
performance-based tests of executive function, most prominently on Trails B (63.3%)
and letter fluency (58.3%). Rates of impairment on the other cognitive measures
(excluding FSIQ) range from a low of 8.0% (CPT-II errors of commission and mean
hit reaction time) to a high of 26.9% (Trails A). Overall, the children have much higher
rates of executive dysfunction as assessed by the BRIEF than by performance-based
tests. Not surprisingly, almost no significant relationships are observed between parent
report of executive functioning and test performance. This is consistent with prior
research on children with FASD (Gross et al., 2015), as well as a broader literature
showing generally none to at best modest correlations in a variety of pediatric patient
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samples (Lovstad et al., 2012; McAuley et al., 2010). This discrepancy may indicate that
rating scales and performance-based tests tap different aspects of executive functions, or
that children with FASD may be unable to adequately engage their execute abilities in
their everyday lives. The possibility that elevated parental ratings may at least partly
reflect a negative bias, such as due to parental frustration with respect to behavior,
cannot be completely ruled out. However, while there is inherent subjectivity in parent
report of cognitive functioning, recent neuroimaging studies showing associations
between the GEC and brain integrity on magnetic resonance imaging scans in children
with FASD lends support to the validity of the BRIEF as tapping into cognitive
dysfunction in this population (Gautam et al., 2015; Wozniak et al., 2013). It is also
possible that the ability to identify a significant relationship between the BRIEF and
performance-based tests in this study has been impacted by the selection of measures.
In particular, tests designed to place great demands on working memory were not
included, though prior studies have not observed a relationship between the BRIEF
Working Memory and tests of working memory (e.g., the WISC-IV Working Memory
Index and Digit Span Backwards) in children with FASD (Gross et al., 2015; Nguyen
et al., 2014). Nevertheless, given that few studies have examined this relationship, future
studies should therefore consider including tests of working memory.
Poorer parent rated executive function is not associated with lower intellectual
functioning in the present sample of Aboriginal children with FASD, restricted to
those with an FSIQ of at least 70. This is consistent with research indicating that the
level of intellectual functioning is associated with executive functioning but does not
fully account for impairment on either the BRIEF (Nguyen et al., 2014) or performance-
based tests of executive functioning (Burden, Jacobson, Sokol, & Jacobson, 2005;
Rasmussen, 2005) in FASD. Nonetheless, the presence of both lower intellectual
functioning and impaired executive functions on the BRIEF has been associated with
more behavioral problems, as rated by teachers in children with FASD (Schonfeld et al.,
2006). Thus, children with FASD with both a low IQ and executive dysfunction may be
at risk for worse outcomes than children with the disorder who have only one or
neither of these difficulties.
No gender differences are observed on the BRIEF in the present sample, in contrast
with a prior study where girls had worse overall scores than boys (Rasmussen et al.,
2006). The reason for this discrepancy is unclear, but may be a sample-specificeffect.
The present finding of minimal sex differences on the BRIEF is, however, consistent
with results of a recent meta-analysis indicating that gender is not consistently related
to executive functioning in FASD (Kingdon et al., 2015).
Interestingly,whileBRIEFscoresinthepresentFASDsamplearetypicallyinthe
impaired range, a bimodal distribution is observed for most scores, with one peak
close to the clinical cutoffof t≥65 and another 1.0 to 2.0 SDs higher. This suggests
the presence of subsets of children with FASD with milder and more severe execu-
tive dysfunction, at least as reflected by parent ratings. The present findings suggest
that gender and the presence of psychiatric comorbidity in general cannot account
for these subsets, although intellectual functioning might play a role. It is possible
that the present sample is composed of a mix of FASD subtypes, with subtype
differences on the BRIEF having been reported in one study (Stevens et al., 2013)
but not in others (Astley et al., 2009;Schonfeldetal.,2006). Unfortunately,
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information on the specific subtype of FASD was not available for the participants in
this study. Further research is needed to determine whether there are characteristics
(e.g., FASD subtype, biological, psychosocial, specific comorbidities) which differ-
entiate these subsets of children and which could help inform interventions to
ameliorate their difficulties with executive functions.
The present study should be interpreted in the context of its limitations. It is possible
that BRIEF scores in this sample are artificially elevated, since central nervous system
dysfunction is one of the criteria employed to identify the presence of FASD. However,
this is unlikely to account for these findings, given that the mean scores are comparable
to those reported in other studies of parent report BRIEF. Although a minimal effect is
observed on the BRIEF scores for having a comorbid psychiatric diagnosis, there is not
asufficient subset of any given diagnosis to identify potentially more specificeffects. In
particular, previous research has found that children with PAE and comorbid ADHD
are reported has having worse executive functions on the BRIEF than children with
PAE but without ADHD in some studies (Nguyen et al., 2014), but not in others
(Rasmussen et al., 2010). As symptoms of ADHD are highly prevalent in Aboriginal
Canadian children (Baydala, Sherman, Rasmussen, Wikman, & Janzen, 2006), further
evaluation of BRIEF scores in subsamples of these children with FASD both with and
without ADHD is important.
This study focuses on parent report of executive functioning. At least one study has
found that problems on the BRIEF in children with FASD are reported to be more
severe by teachers than parents (Rasmussen et al., 2006). It is unclear whether this
discrepancy is due to such factors as different contextual demands placed on the
children’s executive functions (school versus home), rater expectations (e.g., greater
self-regulation expected in the classroom), some combination of these and/or other
factors. Thus, studies comparing parent and teacher reports on the BRIEF in Aboriginal
children with FASD are needed.
The BRIEF scores in this study are examined relative to the standardization sample
(Gioia et al., 2000), consistent with many other studies using the measure in FASD. No
effect of ethnicity on BRIEF scores was observed in a study that included a small
subsample of Aboriginal Canadians (Rasmussen et al., 2006), and there is evidence that
BRIEF parent report scores are unrelated to geographic location in TD children (Roth,
Erdodi, McCulloch, & Isquith, 2015). Nonetheless, the lack of Aboriginal TD and non-
Aboriginal FASD control groups precludes the determination of whether ethnic back-
ground and/or environmental factors impact on executive functions in Aboriginals with
FASD (e.g., cohort effects, sociocultural differences).
All of the children in the present study were either adopted or in foster care.
Problems with executive function have been reported in adopted children on perfor-
mance-based tests (Colvert et al., 2008; Hostinar, Stellern, Schaefer, Carlson, & Gunnar,
2012) and parent ratings on the BRIEF (Merz & McCall, 2011; Merz, McCall, & Groza,
2013). Although the precise reason for these findings remains unclear, early psychoso-
cial deprivation, lower quality of physical/social care in institutions, and genetic influ-
ences have all been suggested as playing a role (Hostinar et al., 2012; Leve et al., 2013;
Merz & McCall, 2011). Further research evaluating the extent to which such factors
may contribute to executive dysfunction in adopted/foster care children with FASD will
therefore be helpful not only with respect to informing our understanding of the
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etiology and maintenance of executive dysfunction in this population but also in terms
of identifying possible preventative and intervention strategies.
In summary, the present study indicates that Aboriginal Canadian children with
FASD show significant executive dysfunction, as reflected by both parent report and
performance-based tests. Such dysfunction may contribute to the problems that chil-
dren with the disorder experience in school, home life, and interpersonal relations.
Thus, interventions targeted at ameliorating executive dysfunction in these children
appears warranted, and may yield broad benefits for their functioning.
Disclosure statement
No potential conflict of interest was reported by the authors.
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