2017 Parent Rating of Executive Function in Fetal Alcohol Spectrum Disorder PDF

CHILD NEUROPSYCHOLOGY, 2017 VOL. 23, NO. 6, 713–732 https://doi.org/10.1080/09297049.2016.1191628 Parent rating of executive function in fetal alcohol spectrum disorder: A review of the literature and new data on Aboriginal Canadian children Jaspreet K. Raia, Maurissa Abecassisb, Joseph E. Caseya, Lloyd Flaroc, Laszlo A. Erdodia and Robert M. Rothb a Department of Psychology, University of Windsor, Ontario, Canada; bNeuropsychology Program, Department of Psychiatry, Geisel School of Medicine at Dartmouth, Lebanon, NH, USA; cPrivate Practice, Edmonton, Alberta, Canada ABSTRACT ARTICLE HISTORY Aboriginal children in Canada are at high risk of fetal alcohol Received 21 December 2015 spectrum disorder (FASD) but there is little research on the cog- Accepted 14 May 2016 nitive impact of prenatal alcohol exposure (PAE) in this population. Published online 10 June 2016 This paper reviews the literature on parent report of executive functioning in children with FASD that used the Behavior Rating KEYWORDS Inventory of Executive Function (BRIEF). New data on the BRIEF is Fetal alcohol spectrum then reported in a sample of 52 Aboriginal Canadian children with disorders; Neuropsychology; FASD for whom a primary caregiver completed the BRIEF. The Executive function; children also completed a battery of neuropsychological tests. Cognition; The results reveal mean scores in the impaired range for all Neurodevelopment 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. 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 [email protected] Department of Psychology, University of Windsor, Chrysler Hall South 168 401 Sunset Avenue, Windsor, Ontario N9B 3P4, Canada © 2016 Informa UK Limited, trading as Taylor & Francis Group 714 J. K. RAI ET AL. 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) and in 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 CHILD NEUROPSYCHOLOGY 715 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, 716 J. K. RAI ET AL. Table 1. Studies Reporting Parent Report BRIEF t-scores in Children with FASD. Age (years) Study Participants (% female) M SD 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, Suspected FASD, n = 25 (56.0) 11.4 2.4 Initiate, WM, P/O, Monitor, TD, n = 59 (46.0) 10.5 2.7 OM McGee et al. (2008) PAE, n = 28 (54.2) 15.2 1.5 GEC, BRI, MI, Inhibit, Shift, EC, TD, n = 15 (46.7) 15.4 1.6 Initiate, WM, P/O, Monitor, OM 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, FASD without ADHD, n = 35 (55.6) 12.9 2.8 P/O, Monitor, OM 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, FAS, n = 10 (N/A) N/A N/A Initiate, WM, P/O, Monitor, PFAS, n = 45 (N/A) N/A N/A OM 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. 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 CHILD NEUROPSYCHOLOGY 717 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 cutoﬀ of 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 718 J. K. RAI ET AL. 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 CHILD NEUROPSYCHOLOGY 719 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 720 J. K. RAI ET AL. 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, and often), 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 CHILD NEUROPSYCHOLOGY 721 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) is a 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 722 J. K. RAI ET AL. 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’s d. 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. CHILD NEUROPSYCHOLOGY 723 Table 2. Descriptive Statistics for BRIEF Parent Report and Performance-Based Tests in Aboriginal Canadian Children with FASD. Test M SD Range 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 cutoﬀ for impairment is t ≥ 65. Many BRIEF and neuropsychological test scores had a bimodal distribution (Table 2). For most BRIEF scales, a ﬁrst peak was observed around the cutoﬀ for 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 724 J. K. RAI ET AL. 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 cutoﬀ for impairment is t ≥ 65. 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 CHILD NEUROPSYCHOLOGY 725 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 726 J. K. RAI ET AL. 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-speciﬁc eﬀect. 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, while BRIEF scores in the present FASD sample are typically in the impaired range, a bimodal distribution is observed for most scores, with one peak close to the clinical cutoﬀ of 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; Schonfeld et al., 2006). Unfortunately, CHILD NEUROPSYCHOLOGY 727 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 a suﬃcient subset of any given diagnosis to identify potentially more speciﬁc eﬀects. 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 728 J. K. RAI ET AL. 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. References Astley, S. J. (2004). Diagnostic guide for fetal alcohol spectrum disorders: The 4-digit diagnostic code (3rd ed.). Seattle, WA: University of Washington Publication Sevrices. Astley, S. J., Olson, H. C., Kerns, K., Brooks, A., Aylward, E. H., Coggins, T. E.,... Richards, T. (2009). 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