Neurobehavioral Disorder Associated With Prenatal Alcohol Exposure Joseph F. Hagan Jr, MD, FAAP, a Tatiana Balachova, PhD,b Jacquelyn Bertrand, PhD,c Ira Chasnoff, MD, FAAP, d Elizabeth Dang, MPH,c Daniel Fernandez-Baca, MA, e Julie Kable, PhD,f Barry Kosofsky, MD, PhD,g Yasmin N. Senturias, MD, FAAP, h Natasha Singh, MPA, c Mark Sloane, DO, i Carol Weitzman, MD, FAAP,j Jennifer Zubler, MD, FAAP,c on behalf of Neurobehavioral Disorder Associated With Prenatal Alcohol Exposure Workgroup, American Academy of Pediatrics

Children and adolescents affected by prenatal exposure to alcohol abstract who have brain damage that is manifested in functional impairments of neurocognition, self-regulation, and adaptive functioning may most appropriately be diagnosed with neurobehavioral disorder associated with Disclaimer: The guidelines/recommendations prenatal exposure. This Special Article outlines clinical implications and in this article are not American Academy of guidelines for pediatric medical home clinicians to identify, diagnose, and Pediatrics policy, and publication herein does not imply endorsement. refer children regarding neurobehavioral disorder associated with prenatal exposure. Emphasis is given to reported or observable behaviors that can be a University of Vermont College of Medicine, Burlington, identified as part of care in pediatric medical homes, differential diagnosis, Vermont; bUniversity of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma; cCenters for Disease Control and and potential comorbidities. In addition, brief guidance is provided on the Prevention, Atlanta, Georgia; dChildren’s Research Triangle, management of affected children in the pediatric medical home. Finally, Chicago, Illinois; eUniversity of Florida, Gainesville, Florida; f g suggestions are given for obtaining prenatal history of in utero exposure to Emory University, Atlanta, Georgia; Weill Cornell Medical College, New York, New York; hUniversity of North Carolina, alcohol for the pediatric patient. Chapel Hill, North Carolina; iWestern Michigan University, Portage, Michigan; and jYale Medical School, New Haven, Connecticut

This report was prepared and written by the Neurobehavioral disorder associated is to better capture the behavioral American Academy of Pediatrics Neurobehavioral with prenatal alcohol exposure and mental health effects of in utero Disorder–Prenatal Alcohol Exposed (ND-PAE) Work (ND-PAE) is a newly proposed mental exposure to alcohol of individuals with Group. Each member of the Work Group contributed health diagnosis associated with the and without the physical dysmorphia to the conceptualization and preparation of this teratogenic effects of in utero exposure associated with prenatal alcohol document; Dr Hagan served as chair of the ND-PAE Work Group, planned the preparation of this report, to alcohol. This behavioral and mental exposure, in contrast to the term and participated in drafting the initial manuscript; health diagnosis is under the umbrella alcohol-related neurodevelopmental Drs Balachova, Chasnoff, Kable, Kosofsky, Senturias, of fetal alcohol spectrum disorders disorder, which applies only to Sloane, Weitzman, and Zubler participated in (FASDs), which also includes fetal individuals with neurobehavioral drafting the initial manuscript and assisted in the alcohol syndrome (FAS), partial FAS effects in the absence of physical multiple conference calls needed to craft the fi nal 3, 4 manuscript; Dr Bertrand participated in drafting (pFAS), and alcohol-related birth dysmorphia effects. This report the initial manuscript and obtained Centers for defects; additional information is outlines the clinical manifestations Disease Control and Prevention approval for available at the American Academy of ND-PAE that are most salient for the the fi nal manuscript; Ms Dang and Ms Singh of Pediatrics (AAP) Web site (http:// pediatric medical home, including participated in drafting the initial manuscript and www. aap. org/ fasd). 1 ND-PAE was identification of children in need of assisted in the multiple conference calls needed to craft the fi nal manuscript; Mr Fernandez-Baca introduced into the Diagnostic and evaluation, diagnosis, comorbid or assisted in research and served as the Work Statistical Manual of Mental Disorders, differential diagnosis, referral, and Group’s technical writer; and all authors approved Fifth Edition (DSM-5) of the American management. Although they do the fi nal manuscript as submitted. Psychiatric Association in 2013 as not represent AAP policy, specific The fi ndings and conclusions of this report are a “Condition for Further Study,” as suggestions are provided for assessment solely those of the authors and do not necessarily well as a specified condition under of maternal use of alcohol during represent the offi cial position of the Centers for “Other Specified Neurodevelopmental pregnancy at routine pediatric visits. Disease Control and Prevention. Disorder” (International Classification of Diseases, Ninth Revision code 315.8, The most recent national data from To cite: Hagan JF, Balachova T, Bertrand J, et al. International Classification of Diseases, the Centers for Disease Control and Neurobehavioral Disorder Associated With Pre- 10th Revision code F88).2 The intent Prevention (CDC) indicate that alcohol natal Alcohol Exposure. Pediatrics. 2016;138(4): e20151553 of this new diagnostic designation consumption during pregnancy is not

Downloaded from www.aappublications.org/news by guest on September 27, 2021 PEDIATRICS Volume 138 , number 4 , October 2016 :e 20151553 SPECIAL ARTICLE TABLE 1 DSM-5 Proposed Criteria for Neurobehavioral Disorder Associated With Prenatal Alcohol Exposure A. More than minimal exposure to alcohol during gestation, including prior to pregnancy recognition. Confi rmation of gestational exposure to alcohol may be obtained from maternal self-report of alcohol use in pregnancy, medical or other records, or clinical observation. B. Impaired neurocognitive functioning as manifested by one or more of the following: 1. Impairment in global intellectual performance (i.e., IQ of 70 or below, or a standard score of 70 or below on a comprehensive developmental assessment). 2. Impairment in executive functioning (e.g., poor planning and organization; infl exibility: diffi culty with behavioral inhibition). 3. Impairment in learning (e.g., lower academic achievement than expected for intellectual level; specifi c learning disability). 4. Memory impairment (e.g., problems remembering information learned recently; repeatedly making the same mistakes; diffi culty remembering lengthy verbal instructions). 5. Impairment in visual–spatial reasoning (e.g., disorganized or poorly planned drawings or constructions; problems differentiating left from right). C. Impaired self-regulation as manifested by one or more of the following: 1. Impairment in mood or behavioral regulation (e.g., mood lability; negative affect or irritability; frequent behavioral outbursts). 2. Attention defi cit (e.g., diffi culty shifting attention; diffi culty sustaining mental effort). 3. Impairment in impulse control (e.g., diffi culty waiting turn; diffi culty complying with rules). D. Impairment in adaptive functioning as manifested by two or more of the following, one of which must be (1) or (2): 1. Communication defi cit (e.g., delayed acquisition of language; diffi culty understanding spoken language). 2. Impairment in social communication and interaction (e.g., overly friendly with strangers; diffi culty reading social cues; diffi culty understanding social consequences). 3. Impairment in daily living skills (e.g., delayed toileting, feeding, or bathing; diffi culty managing daily schedule). 4. Impairment in motor skills (e.g., poor fi ne motor development; delayed attainment of gross motor milestones or ongoing defi cits in gross motor function; defi cits in coordination and balance). E. Onset of the disorder (symptoms in Criteria B, C, and D) occurs in childhood. F. The disturbance causes clinically signifi cant distress or impairment in social, academic, occupational, or other important areas of functioning. G. The disorder is not better explained by the direct physiologic effects associated with postnatal use of a substance (e.g., a medication, alcohol or other drugs), a general medical condition (e.g., traumatic brain injury, delirium, dementia), another known teratogen (e.g., fetal hydantoin syndrome), a genetic condition (e.g., Williams syndrome, Down syndrome, Cornelia de Lange syndrome), or environmental neglect. Reprinted with permission of the American Psychiatric Association. a rare event, with 10.2% of pregnant exposure to alcohol exhibit physical factors (eg, genetic or teratogenic women reporting that they consumed features.15 In 2011, under the auspices syndrome). Although these broad alcohol in the past 30 days and 3.1% of the Interagency Coordinating domains overlap with other disorders reporting binge drinking in the past Committee on Fetal Alcohol Spectrum of childhood, specific deficits within 30 days.5 Furthermore, approximately Disorders, the National Institute on them are indicative of ND-PAE. As half of pregnancies are unplanned, Alcohol Abuse and Alcoholism and with any developmental condition, and a woman might not know she the CDC convened a panel of experts impairments in these domains present is pregnant until the sixth week of to evaluate the research on FASDs not differently as a child matures. To gestation or beyond, a period when associated with the typical physical aid identification of patients with she might still be consuming alcohol features. (Information on these ND-PAE across development, age- and causing damage. 6 Thus, many proceedings can be found at http:// specific traits in the framework for pregnancies are alcohol-exposed and www.niaaa. nih. gov/ about- niaaa/ our- the continuous and comprehensive represent a population of children work/ICCFASD/ proceedings/ 2011.) developmental screening included in at risk for FASDs, especially ND-PAE. In their consensus statement, 3 major The Bright Futures Guidelines, fourth Recent studies including active, areas of impairment were identified: edition, are presented in Fig 1A, Fig expert clinical assessment of school- neurocognition, self-regulation, and 1B, and Fig1C. 16 aged children report estimates that adaptive functioning. These areas of ~2% to 5% of children in the United deficit, along with evidence of in utero Impairment in Neurocognition States have an FASD. 7 – 10 Review of exposure to alcohol, formed the basis medical records indicates that most of the ND-PAE diagnostic criteria.3, 13 Criteria for neurocognitive of these children are not identified or impairment include evidence of 1 11 of the following: global impairment, diagnosed. CLINICAL FEATURES OF ND-PAE executive dysfunction, deficits in Criteria for ND-PAE are based on Diagnosis of ND-PAE is appropriate learning, memory problems, or extensive brain imaging and animal if a child presents with impairment trouble with visual–spatial reasoning. model studies of adverse effects of in neurocognition, impaired self- These criteria may be assessed prenatal alcohol exposure despite the regulation, 2 impairments of adaptive by standardized testing, clinical absence of physical features functioning, and a history of more observation, or, more often, clinical (ie, dysmorphia and growth than minimal exposure to alcohol in history. To ensure the integrity of restriction).3, 12 – 14 In fact, only ~25% utero (Table 1), as long as the disorder the diagnostic criteria for ND-PAE, of children affected by in utero is not better explained by other findings based on clinical observation

Downloaded from www.aappublications.org/news by guest on September 27, 2021 2 HAGAN et al FIGURE 1A ND-PAE Age-Dependent Symptom Diagnosis Guidelines: Neurocognitive Domain. (continued)

Downloaded from www.aappublications.org/news by guest on September 27, 2021 PEDIATRICS Volume 138 , number 4 , October 2016 3 FIGURE 1B ND-PAE Age-Dependent Symptom Diagnosis Guidelines: Self-Regulation Domain. (continued) or history are best if based on For global deficits, comprehensive referral for testing or coordination specific examples of impairment and standardized testing results are the with school psychologists. However, documented in the medical record. gold standard. This might require for diagnosis it is important to

Downloaded from www.aappublications.org/news by guest on September 27, 2021 4 HAGAN et al FIGURE 1C ND-PAE Age-Dependent Symptom Diagnosis Guidelines: Adaptive Domains.

Downloaded from www.aappublications.org/news by guest on September 27, 2021 PEDIATRICS Volume 138 , number 4 , October 2016 5 recognize that not all affected particular difficulty shifting attention, level (eg, poor writing skills) or gross children perform in the range resulting in behavior problems. Poor motor level (eg, poor coordination or of intellectual disability. Clinical impulse control is an additional balance). 7, 38 research has found that 86% of impairment. 28, 29 These difficulties individuals with any of the FASDs in all areas of self-regulation are In Utero Exposure to Alcohol have an IQ in the low average or particularly challenging for the entire borderline ranges. 17 The important family of a child with ND-PAE. The point is that the child under sleep problems and mood lability Unlike FAS, which can be diagnosed consideration is functioning below with frequent behavior outbursts, when information about history what would be expected relative to typically caused by frustration with of prenatal alcohol exposure is his or her peers. task shifting, are often the presenting unavailable, diagnosing other complaints to a pediatrician. 30 – 32 conditions along the continuum Even if global delay or impairment of FASDs, including ND-PAE, is not present, specific deficits can requires a confirmed history of in indicate neurocognitive impairment Adaptive Functioning utero exposure. There are clear consistent with ND-PAE. Impairment and strong research human and Adaptive functioning is the ability in executive function often presents animal data documenting adverse to acquire daily skills for personal as poor planning skills, inflexibility, neurodevelopmental outcomes from and social sufficiency. Impairment or difficulty with behavior moderate to heavy levels of prenatal in adaptive functioning can inhibition.18 Impaired learning or exposure to alcohol 36 and adverse occur in communication, social specific learning disabilities often reproductive (eg, prematurity) communication and interaction, daily manifest in the areas of math, effects from even very low living skills, or motor skills for very visual–spatial reasoning, or abstract exposure levels. 39 Linking adverse young children. Adaptive functioning academic material. Finally, memory neurodevelopmental outcomes to is an area of special concern of problems might be seen as problems in utero exposure at these lower children with ND-PAE because remembering recently learned levels remains a challenge but can these impairments are pervasive materials or repeatedly making the be revealed with more sensitive across domains and situations as same mistake. 19 These particular testing. 40 Despite clear evidence for children age. 3 Therefore, meeting types of learning and memory the association between prenatal this criterion requires impairment problems often lead caregivers and exposure to alcohol and the wide across 2 domains of adaptive educators to mistakenly assume the profile of strengths and weaknesses functioning. Although most language child is being defiant or willfully that might be observed across milestones (eg, babbling, first disobeying rather than having children with ND-PAE, the specificity words, and syntax) are acquired on genuine difficulty, the “can’t vs won’t” of the profile is not yet known. schedule, 33 individuals with ND-PAE error.2, 20, 21 Therefore, the criterion of more might exhibit communication than minimal gestational exposure is problems such as difficulty in Self-Regulation required for the ND-PAE diagnosis. understanding figurative language More than minimal exposure is Impaired self-regulation might (eg, understanding idioms, jokes, or defined as maternal consumption include difficulty regulating mood sarcasm) and social communication of ≥13 drinks per month during or behavior, attention deficits, or conventions (eg, how to effectively pregnancy (ie, any 30-day period of poor impulse control. Early signs enter a conversation). 30, 34 Socially, pregnancy). The “More than minimal” of mood and behavior regulation they can be overly friendly with criterion is not intended to denote problems might include sleep strangers, be at high risk of bullying, a threshold for safe consumption problems or severe reactions to have difficulty learning social rules of alcohol during pregnancy. It discomfort for infants and extended through experience (eg, how to join is simply an acknowledgment of tantrums for toddlers. 22 – 25 For a group on the playground), or be ongoing controversy about low levels older children, increased incidence highly susceptible to manipulation of exposure and an attempt make of externalizing behaviors and by others.35 Because of attention sure the diagnosis was not overused severe reactions to stress are most and memory problems, a child with because the base rate of drinking common.3, 26, 27 However, increased ND-PAE might initially learn daily any alcohol among women of levels of anxiety and depression skills such as hygiene or house rules, childbearing years is relatively high. 5 have been documented. 27 Attention yet maintaining those skills and problems are often associated organizing daily activities present a Suggestions for obtaining a prenatal with prenatal alcohol exposure. challenge. 36, 37 Finally, motor skills history of alcohol exposure are Children with ND-PAE can have can be impaired at the fine motor presented in the Appendix.

Downloaded from www.aappublications.org/news by guest on September 27, 2021 6 HAGAN et al The primary care pediatrician needs (ie, intellectual disability), sleep and practice 48, 49 or forgetting how to to be aware that there is no known abnormalities, reactive attachment tie his or her shoes, despite previous level of alcohol use during pregnancy disorder, anxiety, posttraumatic mastery, and having to relearn that that has been established as safe. stress disorder, oppositional skill entirely. This is different from The US surgeon general still advises defiant disorder, language disorder, regression of emerging skills seen in that women who are pregnant, or learning disability, depression, some children with autism. 33 are considering pregnancy, should bipolar disorder, some features of Finally, children with intellectual abstain from consuming alcohol. 41 autism, and specific phobias. 45, 47 disability without prenatal alcohol Primary care pediatricians will want Other conditions such as enuresis, exposure tend to have lowered to provide this important health encopresis, and eating disorders may functioning across all neurocognitive message to their adolescent patients be present depending on the age of domains. In contrast, individuals and mothers-to-be and obtain the child. 32 with ND-PAE tend to have specific information on prenatal exposure to difficulty with nonverbal aspects alcohol for all patients. FASDs of cognition such as visual–motor The diagnosis of ND-PAE skills, learning and memory for encompasses the behavioral, recently learned skills, and executive DIFFERENTIAL AND COMORBID developmental, and mental health functioning, resulting in behavioral DIAGNOSES aspects of FASDs. Other diagnoses problems. 3, 49 Cognitive impairment along the spectrum, such as FAS coupled with behavioral problems As would be expected, symptoms or pFAS, focus on structural should prompt clinicians to consider associated with the diagnostic and neurophysiological central a diagnosis of ND-PAE. criteria of ND-PAE may be observed nervous system abnormalities (eg, in children with other disabilities. microcephaly or neurologic soft Attention Problems The diagnosis must be applied with signs). Physical features such as facial care and based on all available Current research demonstrates dysmorphia or growth restrictions information, especially prenatal differences in manifestations of (either prenatal or postnatal) are exposure history. It is important attention-deficit/hyperactivity required for FAS and pFAS. Thus, for to keep in mind that the specific disorder (ADHD) and FASDs. children with both physical findings constellation of impairments and Behaviorally, children with FASDs and behavioral findings consistent unique manifestations of the criteria have higher rates of social behavioral with ND-PAE, it is appropriate that a are most relevant for recognition problems resulting from difficulties comorbid diagnosis of FAS or pFAS and diagnosis rather that the general in social cognition and emotional also be used. 3 symptom domains. Specifying processing.50 They might also be co-occurring disorders can provide more likely to have problems dealing Intellectual Disability the most complete picture of the with overstimulation than children child’s strengths and weaknesses As mentioned, a majority of children with simple ADHD. 51 In contrast, to determine treatment or referral with any of the FASDs score in the children with ADHD due to etiology course.42 – 45 Differential diagnoses low range of normative intellectual not attributable to alcohol have of ND-PAE can be particularly functioning. 15 The history of more difficulty with focus and sustained challenging because the disorder than minimal in utero exposure attention. 52 Medication for symptoms does not always present the same to alcohol will be a major decision of ADHD can result in unexpected way in all children because of point between children with ND-PAE outcomes in children with a history differences in timing and amount comorbid with intellectual disability of prenatal alcohol exposure. 53, 54 of prenatal alcohol exposure and and children with intellectual Stimulant medications are often difference in genetic predispositions disability due to another etiology. ineffective for children with prenatal or postnatal environment.33, 46 Table However, deficits specific to ND-PAE alcohol exposure. 27, 33 Care should 2 presents key differences between are recognized. For example, even be given to investigate whether in ND-PAE and several neurobehavioral with repeated experience and an IQ utero exposure to alcohol contributes conditions. The severity of within normal limits, the memory to attention problems for any child presentation and the constellation and learning impairments of a child because treatment and management of characteristics vary greatly from with ND-PAE may mean that he or plans could differ. 2 child to child. 3, 33, 42 – 45 In a sample she has difficulty with previously of children with FASDs, comorbid learned skills, such as finding his Early Trauma mental health conditions included (in or her locker at school on a routine Children who experience early descending order) mental retardation basis despite repeated instructions trauma (including physical events,

Downloaded from www.aappublications.org/news by guest on September 27, 2021 PEDIATRICS Volume 138 , number 4 , October 2016 7 Key Differential From ND-PAE delayed or intellectually impaired in ND-PAE. Early developmental problems in ND-PAE are often detected motor functioning or quality of cits may functioning. The cognitive defi rst year of not be detectable in the fi life on measures of early childhood development. cits, and those with regulation defi intellectual disability may not. below IQ or declining with age. is often greater in children with ND-PAE than those with ADHD. declines in adaptive skills with age. conditions of high arousal, but those with ADHD often improve. Not applicable. • Overall development or IQ is often not • Children with ND-PAE have behavioral • Children with ND-PAE have adaptive skills • The extent of neurocognitive impairment • Children with ND-PAE also demonstrate • Children with ND-PAE deteriorate under Adaptive Functioning below that of their overall IQs, and often there are declines in their skills as they grow older relative to their peers. This decline may result in the standard scores being lower as they age. They often have impairments in the pragmatic communication skills, are socially disinhibited, and have poor motor skills or coordination, with the cit in young latter being a greater defi rather than older children. cient range and are the low or defi generally stable over the lifetime relative to peers and consistent with their levels of intellectual functioning. in untreated individuals with ADHD but with appropriate supports and medication may be age appropriate. Adaptive functioning skills often fall Adaptive functioning skills are also in cits are often present Adaptive skill defi Behavioral Regulation the form of poor mood or behavioral cits, and regulation skills, attention defi poor impulse control. They are best characterized by arousal dysfunction involving slower gating of incoming stimulation and reduced capacity to inhibit attending to distracting stimuli. cation of They respond to simplifi sensory input (fewer distracters and slower presentation). depending on the nature of disorder causing the developmental delays or intellectual disability and the extent of the brain damage. with sustaining attention and being impulsive or hyperactive. The disorder may be seen as being chronically underaroused, and individuals respond to stimulant medications and increases in arousal (exercise and movement or increasing arousal level of learning material). Self-regulation impairments may take Behavioral regulation skills are variable, ADHD is characterized by problems Neurocognitive intellectually defi cient range for some intellectually defi cits in executive but not most. Defi functioning skills, learning, memory, and visual spatial reasoning are common. nition have impairments in by defi multiple domains of functioning (eg, cognitive and motor functioning). limits, but often individuals with ADHD culties and may be have learning diffi academic underachievers. defi cient range by defi nition. This cient range by defi defi often involves IQ score <70 on most standardized tests. Other cognitive skills general consistent with overall IQ. Intellectual skills may be in the Children with global developmental delay Overall IQ is typically within normal Intellectual skills are in the intellectually Differential Diagnosis for ND-PAE to as alcohol-related neurodevelopmental disorder intellectual disability ND-PAE (formerly referred Global developmental delay or ADHD TABLE 2

Downloaded from www.aappublications.org/news by guest on September 27, 2021 8 HAGAN et al Key Differential From ND-PAE being socially withdrawn, and children with ND-PAE are more likely to be socially disinhibited. and emotional reciprocity, whereas in ND-PAE, the problem is socially inappropriate behavior that relates to their lack of cause-and-effect reasoning, slow and ineffective processing of what people say during conversation, and lack of visual–spatial skills that govern their ability to put body at an appropriate distance from another. stereotypies that are odd or very repetitive, which are not as common or may not be seen at all in some children with ND PAE. quicker recovery of function in cognitive skills if placed into a stable, nurturing environment. symptoms. forming positive relationships with caregivers. is typically not as great but may be in extreme abusive cases. • Children with ASD are characterized by cant lack of social • In ASD, there is signifi • Children with ASD generally have • Young children with PTSD demonstrate • Children with PTSD may have more anxiety culties • Children with PTSD may have diffi • The extent of the cognitive impairment Adaptive Functioning typically they have relative defi cits in typically they have relative defi the social and communication skills as compared with their independent living skills. cognitive functioning skills. Some may cits associated with cues have defi associated with the traumatic event. associated with environmental deprivation, but when removed from the adverse environment and placed in a positive, nurturing environment, young children often demonstrate dramatic gains in developmental functioning. Older children may have cits. more persistent adaptive defi The length of exposure to trauma and environmental deprivation typically relate to the extent of impairment. Adaptive skills are often defi cient, but Adaptive skills are often defi Adaptive skills are often below their cits may be For many, these defi Behavioral Regulation reducing sensory input during instruction. dysfunction. They may have sleep problems, be anxious, and easily culty startle. They often have diffi focusing on tasks and sustaining cits mental effort. Often these defi are the result of anxiety or intrusive thoughts. Easily overaroused and benefi t from Easily overaroused and benefi Children with PTSD often have arousal Neurocognitive in the severely intellectually defi cient in the severely intellectually defi range and others functioning within normal limits or gifted. normal limits. For many, there may be cits associated with environmental defi deprivation, but when removed from the adverse environment, young children often demonstrate dramatic gains in developmental functioning. Older children may have cits, more persistent cognitive defi particularly in the area of memory functioning. The length of exposure to trauma and environmental deprivation typically relates to the extent of impairment. Intellectual skills vary, with some being Continued ASD Early trauma exposure or PTSD Intellectual skills would typically be within TABLE 2

Downloaded from www.aappublications.org/news by guest on September 27, 2021 PEDIATRICS Volume 138 , number 4 , October 2016 9 psychological events, and abuse or neglect) often display serious behavioral problems, receiving a mental health diagnosis of conduct disorder, oppositional defiant disorder, anxiety, or depression. Because of overlap between these other behavioral disorders and ND-PAE, at a general level Key Differential From ND-PAE (especially for the self-regulation do not have the same magnitude of cognitive impairment. component) it is important for a • Children with bipolar disorder typically clinician to consider these as both differential and comorbid diagnoses. Until additional data are available about the validity and reliability of all childhood behavior disorders, including ND-PAE, this will continue to be a tricky diagnostic issue. Furthermore, for some children

Adaptive Functioning a history of early trauma, abuse, neglect, or parental loss will be the

be present but often are the result of the mood disturbance interfering with learning age-appropriate adaptive skills or being able to carry out the skills. only presenting problem because Adaptive skill defi cits may or not Adaptive skill defi children with prenatal exposure to alcohol are at higher risk for these negative events. Therefore, it is particularly important to obtain prenatal exposure history in these situations. 18, 55 Such early trauma has been shown to drastically worsen the effects of prenatal alcohol exposure and must be taken Behavioral Regulation into account. 55

periods of depression and mania. During episodes of depression, the at and he or child’s affect may be fl she may lack interest in his or her preferred activities. During episodes of mania, the child may be extremely or culty organizing active and have diffi regulating his or her thought patterns. Often children do not have the full pattern of cycling in the early stages of the disorder and may only become cant easily irritated or have signifi mood lability. Other Conditions The disorder is characterized by cyclic Children with diagnoses of conduct disorder, oppositional defiant disorder, or even posttraumatic stress disorder (PTSD) are often aggressive without appropriate provocation, whereas children with ND-PAE might have behavioral

Neurocognitive outbursts caused by situational frustrations they experience when interacting with others or by

normal limits. their own neurodevelopmental Intellectual skills typically are within limitations. 35 Furthermore, children with other early trauma diagnoses might have inappropriate social interactions but tend to withdraw from others as self-protection, whereas children with ND-PAE are more likely to be overly friendly, Continued seeking out companionship and social acceptance, although often in 35,56 Bipolar disorder TABLE 2 ASD, autism spectrum disorder. an inappropriate manner.

Downloaded from www.aappublications.org/news by guest on September 27, 2021 10 HAGAN et al Foster Care and Adoption can experience a host of physical Behavioral, Mental Health, and conditions and secondary disabilities Academic Referrals A special issue regarding ND-PAE and including mental health problems, early trauma is that among children in By definition ND-PAE is a behavioral or disrupted school experiences, the child welfare system and children mental health diagnosis, and therefore trouble with the law, incarceration adopted internationally. Researchers such patients will benefit from referral or confinement, inappropriate sexual have found disproportionately to specialties that can address these behavior, alcohol or drug problems, high rates of children with FASDs, needs.3, 73, 74 In addition, academic dependent living, and problems with including diagnoses without physical problems are a natural sequela of these employment. 17 In 1 study, only 8% of features such as ND-PAE, in these primary disabilities. An overview of people diagnosed with FAS or a related populations. 57 – 60 Because these interventions developed specifically condition did not have problems with children also often experience early for these children found that effective independent living or employment. trauma, separation, and poor early interventions include explicit teaching Even if this finding encompasses caregiving, they are at elevated risk techniques, repetitive presentation, some amount of ascertainment bias for a comorbid diagnosis of reactive and caregiver instructions about because it is a clinical sample, the attachment disorder or PTSD after specific strengths and weaknesses number of individuals with FASDs who abandonment.61 – 64 Obtaining associated with prenatal alcohol do not achieve independent living is information about, and documenting, exposure.73, 75, 76 As with many aspects striking and cause for concern.15 Early possible prenatal exposures for all of ND-PAE, additional systematic diagnosis and treatment of children who have a current or history of research is needed to develop new with FASDs, including ND-PAE, can involvement with the child welfare intervention strategies and to get reduce the risk of additional disabilities system is prudent clinical practice. a clearer picture of the long-term and adverse lifelong consequences. Such information can inform effectiveness of available This protective effect of early diagnosis assessments and evaluation at older programs. 24, 73, 74, 77, 78 However, has been demonstrated in a number ages. a sample of currently available of studies.15, 24,35, 68 In addition, referral evidence-based and evidence- Finally, although prenatal alcohol to other specialist may be warranted informed interventions are exposure does occur in various (eg, genetics, neurology, cardiology, described in the online Supplemental contexts and varying levels, the nephrology). Information. presence of ongoing alcohol or substance abuse in the home confers Medications It is important to remember that all additional risk. Families with substance aspects of the ND-PAE diagnosis (ie, abuse problems are more likely to The evidence base for pharmacologic neurocognition, self-regulation, and suffer from multiple forms of trauma, treatment in this population is adaptive behavior) are developmental antisocial behavior, financial instability, limited, 53, 69, 70 with no medications processes, and the type of specialty and poverty.18 These factors can lead indicated specifically for ND-PAE. needed might change across to additional comorbid conditions in a Studies on human and animal models development. For younger children, child with ND-PAE. are inconclusive at this time, and allied health referrals, such as more data are needed for proper physical or occupational therapies, REFERRAL AND MANAGEMENT guidance. However, findings from might be most appropriate. Early small pilot studies suggest that intervention might focus on general Although providing appropriate ADHD stimulant medication can developmental skills for the infant or diagnoses (including comorbidities) improve hyperactive symptoms but preschooler. Occupational therapy is can make a positive impact by giving not attention and impulsivity. 71, 72 often recommended for fine motor families and clinicians a framework And another small study found that impairments, sensory integration for understanding a child’s behavior, neuroleptics can be more beneficial problems, and emerging self-regulation it is only a starting point. Ongoing than psychostimulants for improving problems.79 For older school-age care is the major role of the pediatric social skills. 56 A poor or adverse children, several evidence-based medical home. 65 Although specific clinical response to stimulants (ie, interventions targeting specific skills and targeted early interventions have ineffective clinical response or and adapted for children with FASDs been shown to be most effective, significant side effects) can occur, are available and can be recommended more general special education and clinicians should plan to adjust to school-age children. Several of these and support services also improve medications as necessary. Such interventions are described in the outcomes. 15, 17, 55, 66, 67 medication failure also might be an online Supplemental Information. 73 Individuals with FASDs, including indicator to consider a diagnosis More information on such interventions children without physical stigmata, under the umbrella of FASDs. is available at the National Organization

Downloaded from www.aappublications.org/news by guest on September 27, 2021 PEDIATRICS Volume 138 , number 4 , October 2016 11 on Fetal Alcohol Syndrome (www. language, the value of routines, Although additional taxometric NOFAS.org). and the need to relearn some skills research on ND-PAE is needed, an and obtain repeated instruction extensive scientific literature already Older children with ND-PAE might is a practical technique. provides support for its constellation need more traditional mental Furthermore, such instruction provides of symptoms and criteria. Several health services and can begin to reassurance and support.64, 73 efforts are under way to obtain benefit from modified insight- It often helps to explain to parents appropriate taxometric data, with based therapies. 27, 80 Referral to a that structural brain abnormalities results forthcoming (J. Kable, PhD, psychiatrist or psychologist can be and the resulting neurobehavioral personal communication, 2015); appropriate. Referral for substance manifestations their child has (eg, our understanding may require abuse evaluation or treatment also problems with poor problem solving modification once tested in a sizable might be warranted. 15, 27 For the and executive dysfunction) might cohort of children with developmental medical home provider, however, it is make him or her less responsive to disabilities. Children and adolescents most effective to provide background pharmacotherapy than other children with ND-PAE can reach their full information on the strengths and with a developmental disability. The potential with proper identification, weaknesses of a child with ND-PAE in pediatric medical home is an ideal diagnosis, and treatment if clinicians addition to child specific symptoms setting to provide such education and families work as a team, especially when making such a referral. and reassurance that the child’s toward early identification, treatment, primary care pediatrician will be and family support. 24, 73 Diagnosis Of special note for this population available to work with the family to and care of the patient with ND-PAE is that many affected children and address problems as they arise.65 It provides the child, family, and pediatric adolescents do not qualify for special is especially helpful for the clinician clinician with a lens through which education under standard criteria, to explain that the vulnerabilities of to help that child reach his or her 17,81 yet they still need services. a child with ND-PAE might not be developmental potential. Specific This gap must be addressed at the readily recognizable by others. For points to consider are presented in individual patient or student level. example, the child’s good structural Table 3. Psychoeducational testing (by school language skills and friendly nature can Clinical and research evidence personnel or private psychologists) give a false impression of competence, clearly indicates that children might be required for diagnostic and forgetting previously learned affected by ND-PAE and their confirmation and treatment planning. material might give a false impression families face substantial challenges. Creative solutions and closely of a defiant or oppositional disorder.74 Although these recommendations engaging with the family, school, and Additionally, the medical home do not represent AAP policy, early community by the pediatric medical provider caring for the child with recognition in the medical home home can facilitate meaningful ND-PAE can help explain how the needs can capitalize on neural plasticity, results (see the AAP FASD Toolkit at of the child change across development 82,83 early intervention, and ongoing www. aap. org/ fasd). and provide anticipatory care. support systems to maximize Family Support the developmental potential of Parental education about ND-PAE, SUMMARY AND PEDIATRIC MEDICAL these children. Thus the pediatric and even about FASDs in general, is HOME PRACTICE SUGGESTIONS medical home plays a central role particularly effective. 84 For parents in maximizing the developmental The value of the medical home starts there might be fears about stigma outcomes of children with ND-PAE. at the identification and diagnostic or the legal implications of the stage and continues through treatment child’s diagnosis. It is important that planning and ongoing care. Although ACKNOWLEDGMENTS clinicians ask the difficult questions to barriers to diagnosis and treatment The authors thank Rachel Daskalov screen for prenatal alcohol exposure remain,85 the AAP endorses the and Joshua Benke for their assistance when they suspect a child might have identification, diagnosis, referral, with preparation and submission of been prenatally exposed to alcohol. and management of all children and this article. Caregivers appreciate information adolescents with FASDs, including about how the behavioral difficulties ND-PAE. The brain damage that is they experienced with their child were caused by prenatal alcohol exposure APPENDIX: SUGGESTED SCREENING directly related to their child’s exposure is permanent and irreversible, FOR PRENATAL EXPOSURE TO ALCOHOL to alcohol in utero. 17, 73, 84 Instruction resulting in impaired neurocognitive Maternal self-report remains the on the use of explicit explanations functioning regardless of IQ; however, major approach for identifying that avoid idioms or other figurative interventions can improve function. alcohol consumption during

Downloaded from www.aappublications.org/news by guest on September 27, 2021 12 HAGAN et al TABLE 3 ND-PAE Points for the Pediatric Medical Home a single visit or might have emerged Universally screen for prenatal alcohol exposure, prenatally, in the newborn period, at the time of at the time of screening. For example, adoption, and for new patients; the diagnosis should be considered throughout childhood (especially executive function deficits often do at developmental transitions). not become apparent until school Document the presence and, if possible, the amount of prenatal alcohol exposure in the child’s medical age, but documentation of prenatal chart. Perform frequent developmental screening with early referral to developmental specialist if concerns exposure to alcohol would put those are identifi ed. deficits in the proper context. Identify comorbid diagnoses to effectively manage ND-PAE or, if appropriate, identify as a comorbid diagnosis. One concern expressed by some Treat ND-PAE as a chronic condition in a medical home. clinicians is that obtaining exposure Educate women about the risks of alcohol use during pregnancy and advise them to avoid alcohol information will trigger scrutiny by consumption while pregnant or when conception is possible. child welfare agencies. The Child Abuse Prevention and Treatment Act pregnancy, even though women suggested in the newest edition of does not require clinicians to report might be reluctant to reveal Bright Futures16 : to Child Protective Services if a child prenatal alcohol use. 86 More has been prenatally exposed to • “How often do you drink beer, accurate reports about alcohol alcohol. Referral to Child Protective wine or liquor in your household?” use are elicited when screening Services is required if the child (Continue for any response other is conducted in a nonjudgmental has been diagnosed with an FASD than “never”) and nonconfrontational manner, in the period between birth and 3 87,88 respecting confidentiality. • “In the 3 months before you knew years. The intent of this referral is Use of alcohol by a mother during you were pregnant, how many to develop safe care and possible pregnancy should be assessed, times did you have 4 or more treatment plans if needed, not to 93,94 avoiding questions that require drinks in a day?” initiate punitive actions. “yes/no” answers (eg, “Do you drink alcohol?”). Because of the • “During the pregnancy, how many Although discussing prenatal alcohol stigma associated with alcohol use times did you have 4 or more exposure with patients might be during pregnancy, asking patients drinks in a day?” a challenge, and some providers about prepregnancy drinking can express discomfort about discussing improve accuracy of the screening. If positive responses are given to any alcohol use with their patients, it Questions about alcohol use can be of the above questions, the clinician is an important component of both imbedded in a general conversation can follow up to determine frequency prenatal and postnatal care and is 95 about health behaviors during and extent of consumption by asking, necessary for diagnosing FASDs. pregnancy (eg, smoking, diet, current • “During the pregnancy, on average, ABBREVIATIONS medications). Furthermore, single how many days per week did you binge drinking questions have been have a drink?” AAP: American Academy of shown to be effective at identifying Pediatrics women at risk for alcohol use during • “During the pregnancy, on a typical ADHD: attention-deficit/ pregnancy and are consistent with day when you had an alcoholic hyperactivity disorder current CDC and National Institute beverage, how many drinks did CDC: Centers for Disease Control on Alcohol Abuse and Alcoholism you have?” and Prevention recommendations. 89– 91 DSM-5: Diagnostic and Statistical Any affirmative answer indicates Manual of Mental Based on international work that maternal at-risk drinking; a brief Disorders, Fifth Edition involved minimal questioning and intervention or referral is indicated. FAS: fetal alcohol syndrome clinical experience, the ND-PAE The Bright Futures Guidelines (4th FASDs: fetal alcohol spectrum workgroup suggests beginning ed) suggests that these questions disorders screening with an introductory be asked at the prenatal visit, at ND-PAE: neurobehavioral statement, such as “I ask all an initial postnatal well visit, for disorder associated patients standard health questions all new patients, based on clinical with prenatal alcohol to understand factors that may suspicion, and if a caregiver describes exposure affect health of their child and their cognitive or behavioral concerns pFAS: partial fetal alcohol health.” 89, 92 To approach the topic consistent with ND-PAE criteria. 16 syndrome of alcohol and quickly determine Documentation of findings is very PTSD: posttraumatic stress whether prenatal exposure occurred, important because not all criteria for disorder the following sets of questions are a ND-PAE diagnosis might present in

Downloaded from www.aappublications.org/news by guest on September 27, 2021 PEDIATRICS Volume 138 , number 4 , October 2016 13 DOI: 10.1542/peds.2015-1553 Accepted for publication Jul 22, 2016 Address correspondence to Joseph F. Hagan Jr, MD, FAAP, 128 Lakeside Ave, Suite 115, Burlington, VT 05401-4936. E-mail: [email protected] PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright © 2016 by the American Academy of Pediatrics FINANCIAL DISCLOSURE: The authors have indicated they have no fi nancial relationships relevant to this article to disclose. FUNDING: Supported by Cooperative Agreement 5U58DD000587, funded by the Centers for Disease Control and Prevention. POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential confl icts of interest to disclose. COMPANION PAPER: A companion to this article can be found online at www. pediatrics. org/ cgi/ doi/ 10. 1542/peds. 2016-1999.

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