Current Opinion in Psychiatry:
NEURODEVELOPMENTAL AND NEUROCOGNITIVE DISORDERS: Edited by James C. Harris and Perminder Sachdev
Foetal alcohol spectrum disorder: identifying the neurobehavioural phenotype and effective interventions
Koren, Gideona; Zelner, Irenea; Nash, Kellyb; Koren, Gala
aMotherisk Program, Division of Clinical Pharmacology-Toxicology, Department of Pediatrics
bDepartment of Psychiatry, The Hospital for Sick Children, Toronto, Ontario, Canada
Correspondence to Gideon Koren, MD, FRCPC, Motherisk Program, Hospital for Sick Children, 555 University Ave, Toronto, ON M5G 1X8, Canada. Tel: +1 416 813 5781; e-mail: firstname.lastname@example.org
Purpose of review: Since the first description of the foetal damage of alcohol in 1967, numerous studies have outlined different aspects of neurodevelopmental dysfunction, adversely affecting the lives of children worldwide. Although the cause of the syndrome is sorted out, the pathogenesis of brain damage is far from being clear. In contrast to children exhibiting the full facial dysmorphology, who are relatively easy to diagnose, in those presenting only with alcohol-related neurodevelopmental damage diagnosis is much more challenging due to poor specificity of the brain dysfunction. Hence, identifying the neurodevelopmental phenotype of foetal alcohol spectrum disorder (FASD) is a major challenge.
Recent findings: Recently, a behavioural phenotype of FASD has been described and validated using items from the Child Behaviour Checklist. This tool has high sensitivity and specificity in separating children with FASD from those with ADHD and from healthy controls. In parallel, a number of intervention studies show promise in improving the abilities of children and adolescents with the syndrome to cope with daily tasks and improve their quality of life.
Summary: The neurobehavioural screening test can facilitate screening for FASD and is an official screening tool in the FASD toolkit of the Public Health Agency of Canada. Promising new interventions may attenuate the long-term outcome of these children.
Alcohol is a human teratogen with marked effects on the developing brain. The various presentations arising from prenatal alcohol exposure, such as the full-blown foetal alcohol syndrome (FAS) and alcohol-related neurodevelopmental disorder (ARND), are defined collectively as foetal alcohol spectrum disorder (FASD). FASD is characterized by a wide range of deficiencies, including reduced intelligence quotient (IQ) [1,2], cognitive and learning disabilities and severe behaviour problems [3,4]. Attention problems are prevalent, with approximately 70% of children with FASD having a clinically diagnosed attention disorder, with attention deficit/hyperactivity disorder (ADHD) being three to nine times higher in children with FASD than in the general population [5–8]. Of importance, children with FASD are characterized by oppositional defiant/conduct disorder (ODD/CD) being the next most common to ADHD [8–10], including deficits in moral development, lack of social judgement and failure to learn from experience . A large proportion of individuals with FASD require extensive mental health services throughout their lifetime. Currently, the majority of children with FASD fail to receive a diagnosis because skilled professionals and adequate mental health services are often lacking, especially if children reside in rural and remote areas, which represents an important public health concern. Hence, children with FASD are often diagnosed with, and treated for, a comorbid disorder rather than for FASD itself, with the effects of the alcohol-related disorder being overlooked and not addressed. To be able to differentially diagnose children on the FASD spectrum from those with other psychiatric disturbances of childhood, appropriate tools have to be developed.
IDENTIFYING THE BEHAVIOURAL PHENOTYPE OF FOETAL ALCOHOL SPECTRUM DISORDER
The greatest challenge in developing a method to screen and identify the behavioural characteristics of FASD is the wide and nonspecific range of deficits exhibited by the children. As part of the effort to characterize a neurobehavioural phenotype of FASD, we have developed and validated a 10-item screening tool based on items from a standardized behaviour problems questionnaire known as the Child Behaviour Checklist (CBCL) developed by Achenbach and Rescolora . The full CBCL tool includes 113 items filled by caretakers or teachers who know the child. Out of these items, factor analysis revealed a combination of 10 items that accurately separated children with FASD from the two comparison groups . We compared children with FASD (n = 30) with children with ADHD (n = 30) and with typically developing children (n = 30) . This neurobehavioural test has been shown to be 86% sensitive and 82% specific for FASD. Because 70% children with FASD also exhibit ADHD, we also defined a behavioural phenotype for those 30% who do not have symptoms of hyperactivity and attention deficit. Table 1 presents the full neurobehavioural screening test (NST) in details with two exemplary cases to allow readers to learn how to apply this tool. The NST, validated for children aged 6–13 years, can be completed by health or social workers interviewing the primary caretaker of the child. The NST has been endorsed by the Public Health Agency of Canada as a screening test for FASD as part of the agency-sponsored FASD Screening Toolkit .
Some of the items in the NST reflect features of ODD/CD. We could not be certain whether these items reflected comorbidity with ODD/CD, or represented distinct features of FASD. To address these outstanding issues, we replicated our 2006 original article using a larger and different sample of children with FASD, children with ADHD and controls, and sought to further determine the specificity of our screening tool by also comparing the FASD group with children with ODD/CD.
The sample included 220 children aged 6–18 years, 56 with an FASD, 50 with ADHD, 60 with ODD/CD and 53 typically developing normal control children [14▪▪]. This study, using a different sample of children, corroborated the results of our previous findings. Examination of individual item scores revealed that children with FASD differed from healthy controls in behaviours reflecting immaturity, argumentativeness, inattention and general disobedience. Children with ADHD were less likely than those with FASD to have behaviour problems and act young; in contrast, children with ODD/CD were less likely than FASD to act young but were more cruel and disobedient at home. These findings indicate that the NST is highly discriminative between FASD and healthy controls groups and that certain combinations of items differentiate children with FASD from unexposed children with ADHD and ODD/CD. This consistency, across different samples of children with FASD, further validates this screening method. We found that children with FASD exhibited poor attention and behaviour suggestive of ADHD, but, unlike ADHD, they displayed a greater lack of guilt after misbehaving, cruelty, tendency to act young for their age and likelihood to steal. The latter finding supports previous and current research indicating poor social and moral development in children with FASD [10,15–17,18▪,19▪].
The results show that children with FASD are significantly more likely than ODD/CD to act young, while being somewhat less disobedient at home and cruel. This finding suggests that children with FASD may have a distinct profile of behaviour problems from that seen in ODD/CD. Our finding of greater immaturity in children with FASD than ODD/CD (as well as ADHD) is consistent with reports of arrested social development in this population .
It is critical to highlight the fact that the NST is intended for screening purposes only and is not a diagnostic tool. A number of limitations impede our having a full understanding of how prenatal alcohol exposure affects development, as is characteristic of most clinic-based research. In our studies, we could not adequately control for maternal smoking and drug use, depression and other mental illnesses common among alcohol-dependent women, as well as maternal history of abuse and neglect. Several methodological limitations are also specific to the current study. As data were collected retrospectively, certain background information was not available, and further studies are being conducted now to adequately fill these gaps.
In 2013, Mattson et al. [21▪] tried to characterize a neurobehavioural profile of FASD [12,19▪]. They compared several groups of children on a large neuropsychological test battery. The tests included in this battery were the Cambridge Neuropsychological Test Automated Battery (CANTAB: Delayed Matching to Sample, Intra-Extra Dimensional Shift, Choice Reaction Time, Simple Reaction Time, Spatial Working Memory subtests) (Cambridge Cognition Limited, 2006) and the Delis-Kaplan Executive Function System (D-KEFS: Colorword Interference, Trail Making, 20 Questions, Tower, Verbal Fluency Switching, Design Fluency subtests). Full-scale IQ (FSIQ) scores were obtained using the Wechsler Intelligence Scale for Children, fourth edition (WISC-IV; Wechsler, 2004).
They included 185 healthy controls, 74 children with ADHD and 209 children heavily exposed to alcohol in pregnancy (both diagnosed and undiagnosed with FASD). The healthy children differed from the alcohol-exposed children with high statistical power. However, classification accuracy was moderate across the groups, which is not surprising in light of the numerous tests included in the analysis, and the fact that not all children exposed to heavy alcohol were diagnosed with FASD.
In summary, the NST has allowed a set of behavioural characteristics to be identified that distinguish children with FASD from children with two commonly associated childhood disorders, namely ADHD and ODD/CD, as well as from healthy controls; clinicians and researchers working with children with FASD have long struggled to identify a behavioural phenotype characteristic of FASD. After the NST is further validated on a larger and more diverse sample, it may allow clinicians to employ this behavioural phenotype to diagnose FASD in cases with unclear maternal drinking history and lack of the pathognomonic facial features of FASD.
PROTECTIVE FACTORS AND INTERVENTION STUDIES IN FOETAL ALCOHOL SPECTRUM DISORDER
Although the primary alcohol-induced damage is thought to be, for the most part, permanent, studies have shown that factors such as early diagnosis (specifically before the age of 6), living in a stable and nurturing home, never having experienced violence, having been found eligible for developmental disability services and having basic needs met are protective in that they are associated with a decreased risk of developing secondary disabilities such as disrupted school experience, unemployment, institutionalization and trouble with the law . Early diagnosis is associated with improved life outcomes in FASD-affected individuals, likely because it permits early intervention and access to specialized support and resources, all of which may help affected individuals lead more productive lives and lessen the impact that FASD has on the individual and society. Of interest, Streissguth et al. noted that individuals who did not meet the criteria for a FAS diagnosis or those with an IQ greater than 70 were at a higher risk for delinquency, alcohol and drug problems, and school problems. This may be due to the fact that these individuals were less likely to be identified and qualify for services. Because the younger the age at which an affected child is identified, the lower the frequency of secondary disabilities , early diagnosis is of paramount importance for managing FASD in our society and reducing the tremendous economic burden associated with it.
In a systematic review of animal studies that examined interventions for the detrimental effects of prenatal alcohol exposure, Sussman and Koren  reported that, in rodents, postnatal environmental enrichment, postnatal handling, exercise and therapeutic motor training may attenuate and ameliorate ethanol-induced abnormalities and deficits such as learning, motor function and planning. For example, one study  showed that motor and spatial impairments in rat pups exposed to ethanol can be ameliorated by providing them with various objects to manipulate and play with and housing them with other pups. Another study  showed that providing ethanol-exposed rat pups with opportunities for voluntary exercise improved spatial memory (performance on Morris water maze test). In another series of studies, it was shown that postnatal choline supplementation attenuated the severity of ethanol-induced learning deficits and behavioural changes such as hyperactivity in rats prenatally exposed to ethanol [26–28]. These findings are encouraging and require further research in humans to determine whether such interventions could improve neurological performance and reduce the severity of foetal alcohol effects.
In humans, a number of interventions have been shown to improve outcomes in FASD-affected individuals, as well as provide the necessary supports to aid the development of necessary skills that will help the child become an independent adult. In terms of pharmacotherapy, Snyder et al. found that stimulants (methylphenidate, pemoline or dexedrine) improved hyperactivity but not attention compared with placebo in a group of 12 children (6–16 years of age) with FAS and ADHD. In a retrospective study in which data were extracted from the medical records of 27 children with FASD who had been referred to an ADHD medication service, stimulants were found to improve hyperactivity/impulsivity and opposition/defiance but were not as effective at improving inattention . The authors speculated that these findings suggest that inattention may be less responsive to ADHD medication.
In a recent systematic review of school-based interventions, Peadon et al. evaluated and discussed interventions designed to improve the developmental outcomes of individuals with FASD, reduce secondary disabilities and improve the lives of families of individuals affected by FASD. As a diagnosis of FASD in and of itself does not provide enough information on the appropriate treatment that must be provided, a careful assessment of each individual is essential . Different interventions must be specifically designed to target deficits such as memory, information processing, academic skills, social skills, attention, motor skills and executive functioning, as well as to address various behavioural and mental health issues. It is important to note that the majority of individuals with FASD do not have low IQ and thus may not qualify for many support services. As they nevertheless have impaired mental functioning that has a significant impact on social and academic functioning , individual in-depth assessments are important for identifying the specific deficits and providing these individuals with critical services that would otherwise be unavailable to them .
Numerous human studies have been carried out in recent years on the effectiveness of interventions focusing on math skills, behavioural regulation, peer relations and social communication, executive function, compliance, learning readiness and challenging behaviour of clinical concern in individuals affected by FASD (Table 2) [31,33–39,40▪,41,42▪]. Many of these were randomized controlled trials. Interventions and treatment typically focus on adapting the FASD-affected children to their environment by addressing their neurodevelopmental issues. The common technique used in these interventions is teaching by explicit instruction rather than relying on observational learning [31,33]. Interventions to support emotional and behavioural regulation focus on modifying the environment and providing structure and consistency through daily routines and rules. For example, minimizing visual and auditory distractions in classrooms and use of clearly organized material can aid learning in children with FASD . Researchers have also suggested that, to be effective, interventions must not only aim to address the range of deficits exhibited by individuals with FASD but also focus on educating, training and providing resources and services to their caregivers . In addition, biological parents of these children may be dealing with ongoing substance abuse problems and stigmatization, which must be addressed, as it could have a very detrimental effect on the child and intervention efforts.
Overall, there is increasing evidence in the literature that, although incurable, FASD can be managed, and individuals with prenatal alcohol exposure can lead productive lives if they can be identified and referred to intervention and support programmes. Unfortunately, conditions that fall under the FASD umbrella are vastly underdiagnosed and many individuals affected by in-utero alcohol exposure never receive specialized support and interventions that have been shown to be beneficial. For this reason, screening tools that may identify individuals at risk for FASD such that they can be referred for further assessments and diagnostic clinic need to be developed.
A MODEL CLASSROOM FOR FOETAL ALCOHOL SPECTRUM DISORDER
Children spend a large part of their lives in school, and for children afflicted by FASD the school is the most challenging arena, both in terms of academic difficulties and in terms of adverse behaviour. Typically, these children experience disruptive school attendance, under-achievement and inability to stay in regular, or even special, education programmes . Their low cognitive abilities, attention and hyperactive tendencies, coupled with maladaptive behaviour, make the school experience a nightmare for them and for their families.
In 2012, we commenced a pilot school programme for Grade 2–3 children diagnosed by us with FASD. In collaboration with the Toronto District School Board, nine children were enrolled in two classes, attended by a teacher and educational assistant in each class, aiming to address the specific educational needs of each student, and supported clinically by the Motherisk Program at The Hospital for Sick Children. At the end of the 2012–2013 academic year, all nine families asked to continue in the programme for the subsequent year, and many noted that this was the best year of their children's lives. Although analysis of the progress of the children in different domains by comparing pre and post measurements is still ongoing, quite a few of the children have shown marked progress, above what was expected of them.
The newly described neurobehavioural screening test can facilitate screening for FASD and is an official screening tool in the FASD toolkit of the Public Health Agency of Canada. Although the primary brain damage of FASD appears to be irreversible, promising new interventions can attenuate the long-term outcome of these children.
This work has been supported by grants from (1) the Public Health Agency of Canada through the Canadian Association for Pediatric Health Centres; (2) the Research Leadership for Better Pharmacotherapy during Pregnancy and Lactation; and (3) Shoppers Drug Mart.
Conflicts of interest
There are no conflicts of interest.
REFERENCES AND RECOMMENDED READING
Papers of particular interest, published within the annual period of review, have been highlighted as:
▪ of special interest
▪▪ of outstanding interest
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child behaviour checklist; foetal alcohol spectrum disorder; foetal alcohol spectrum disorder neurobehavioural phenotype; intervention studies; school for foetal alcohol spectrum disorder children
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