Fetal Alcohol Spectrum Disorders: Diagnostic Considerations for Children with a History of Trauma

  • Prachi E. ShahEmail author
  • Danielle Shapiro
  • Tedi Milgrom
  • H. Eugene Hoyme


Fetal alcohol spectrum disorders (FASDs) is an umbrella term that describes a variety of conditions characterized by a pattern of atypical facial features, growth restriction, structural physical abnormalities, and brain dysfunction resulting from prenatal alcohol exposure. Because the cognitive and behavioral phenotype of children with fetal alcohol spectrum disorders can be nonspecific, and overlap with the phenotype of other neurodevelopmental disorders, and because the majority of individuals with FASDs do not manifest dysmorphic craniofacial features, misdiagnosis and under-diagnosis of FASDs is common. To mitigate the long-term morbidities associated with fetal alcohol spectrum disorders, it is important to maintain a heightened index of suspicion for prenatal alcohol exposure and the possibility of an alcohol-related diagnosis in children at risk, as early diagnosis and recognition of the disabilities associated with FASDs can help optimize future outcomes.


  1. 1.
    Walker SP, Wachs TD, Grantham-McGregor S, et al. Inequality in early childhood: risk and protective factors for early child development. Lancet. 2011;378(9799):1325–38.PubMedCrossRefGoogle Scholar
  2. 2.
    Wachs TD. Known and potential processes underlying developmental trajectories in childhood and adolescence. Dev Psychol. 1996;32(4):796.CrossRefGoogle Scholar
  3. 3.
    Wachs TD. Expanding our view of context: the bio-ecological environment and development. Adv Child Dev. 2003;31:363–409.Google Scholar
  4. 4.
    Molteno CD, Jacobson JL, Carter RC, Jacobson SW. Infant symbolic play as an early indicator of fetal alcohol-related deficit. Infancy. 2010;15(6):586–607.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    May PA, Baete A, Russo J, et al. Prevalence and characteristics of fetal alcohol spectrum disorders. Pediatrics. 2014;134(5):855–66.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Chasnoff IJ, Wells AM, King L. Misdiagnosis and missed diagnoses in foster and Adopted children with prenatal alcohol exposure. Pediatrics. 2015;135(2):264–70.PubMedCrossRefGoogle Scholar
  7. 7.
    Fast DK, Conry J. Fetal alcohol spectrum disorders and the criminal justice system. Dev Disabil Res Rev. 2009;15(3):250–7.PubMedCrossRefGoogle Scholar
  8. 8.
    Hoyme HE, Kalberg WO, Elliott AJ, et al. Updated clinical guidelines for diagnosing fetal alcohol spectrum disorders. Pediatrics. 2016;138(2):e20154256.PubMedPubMedCentralCrossRefGoogle Scholar
  9. 9.
    Jones KL. Recognition of the fetal alcohol syndrome in early infancy. Lancet. 1973;302(7836):999.PubMedCrossRefGoogle Scholar
  10. 10.
    Jones KL, Smith DW. The fetal alcohol syndrome. Teratology. 1975;12(1):1–10.PubMedCrossRefGoogle Scholar
  11. 11.
    Hoyme HE, May PA, Kalberg WO, et al. A practical clinical approach to diagnosis of fetal alcohol spectrum disorders: clarification of the 1996 institute of medicine criteria. Pediatrics. 2005;115(1):39–47.PubMedCrossRefGoogle Scholar
  12. 12.
    Manning MA, Eugene Hoyme H. Fetal alcohol spectrum disorders: a practical clinical approach to diagnosis. Neurosci Biobehav Rev. 2007;31(2):230–8.PubMedCrossRefGoogle Scholar
  13. 13.
    Rojmahamongkol P, Cheema-Hasan A, Weitzman C. Do pediatricians recognize fetal alcohol spectrum disorders in children with developmental and behavioral problems? J Dev Behav Pediatr. 2015;36(3):197–202.PubMedCrossRefGoogle Scholar
  14. 14.
    Elgen I, Bruaroy S, Laegreid LM. Lack of recognition and complexity of foetal alcohol neuroimpairments. Acta Paediatr. 2007;96(2):237–41.PubMedCrossRefGoogle Scholar
  15. 15.
    Gahagan S, Sharpe TT, Brimacombe M, et al. Pediatricians’ knowledge, training, and experience in the care of children with fetal alcohol syndrome. Pediatrics. 2006;118(3):e657–68.PubMedCrossRefGoogle Scholar
  16. 16.
    Lange S, Shield K, Rehm J, Popova S. Prevalence of fetal alcohol spectrum disorders in child care settings: a meta-analysis. Pediatrics. 2013;132(4):e980–95.PubMedCrossRefGoogle Scholar
  17. 17.
    English DJ, Thompson R, White CR. Predicting risk of entry into foster care from early childhood experiences: a survival analysis using LONGSCAN data. Child Abuse Negl. 2015;45(0):57–67.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Pelton LH. The continuing role of material factors in child maltreatment and placement. Child Abuse Negl. 2015;41(0):30–9.PubMedCrossRefGoogle Scholar
  19. 19.
    Chernoff R, Combs-Orme T, Risley-Curtiss C, Heisler A. Assessing the health status of children entering foster care. Pediatrics. 1994;93(4):594–601.PubMedGoogle Scholar
  20. 20.
    Burd L, Cohen C, Shah R, Norris J. A court team model for young children in foster care: the role of prenatal alcohol exposure and fetal alcohol spectrum disorders. J Psychiatry Law. 2011;39(1):179–91.CrossRefGoogle Scholar
  21. 21.
    Herrick KHL, Burd L. The elephant in the cradle: fetal alcohol spectrum disorders. Zero Three. 2011;31(3):44–50.Google Scholar
  22. 22.
    Popova S, Lange S, Burd L, Rehm J. Canadian children and youth in care: the cost of fetal alcohol spectrum disorder. Child Youth Care Forum. 2014;43(1):83–96.PubMedCrossRefGoogle Scholar
  23. 23.
    Kvigne VL, Leonardson GR, Neff-Smith M, Brock E, Borzelleca J, Welty TK. Characteristics of children who have full or incomplete fetal alcohol syndrome. J Pediatr. 2004;145(5):635–40.PubMedCrossRefGoogle Scholar
  24. 24.
    Centers for Disease Control and Prevention. Fetal development chart. Accessed 20 Oct 2017.
  25. 25.
    Pruett D, Waterman EH, Caughey AB. Fetal alcohol exposure: consequences, diagnosis, and treatment. Obstet Gynecol Surv. 2013;68(1):62–9.PubMedCrossRefGoogle Scholar
  26. 26.
    Brien JF, Smith GN. Effects of alcohol (ethanol) on the fetus. J Dev Physiol. 1991;15(1):21–32.PubMedGoogle Scholar
  27. 27.
    Ramanathan R, Wilkemeyer MF, Mittal B, Perides G, Charness ME. Alcohol inhibits cell-cell adhesion mediated by human L1. J Cell Biol. 1996;133(2):381–90.PubMedCrossRefGoogle Scholar
  28. 28.
    Fitzgerald DM, Charness ME, Leite-Morris KA, Chen S. Effects of ethanol and NAP on cerebellar expression of the neural cell adhesion molecule L1. PLoS One. 2011;6(9):e24364.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Dou X, Menkari CE, Shanmugasundararaj S, Miller KW, Charness ME. Two alcohol binding residues interact across a domain interface of the L1 neural cell adhesion molecule and regulate cell adhesion. J Biol Chem. 2011;286(18):16131–9.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Ramachandran V, Perez A, Chen J, Senthil D, Schenker S, Henderson GI. In utero ethanol exposure causes mitochondrial dysfunction, which can result in apoptotic cell death in fetal brain: a potential role for 4-hydroxynonenal. Alcohol Clin Exp Res. 2001;25(6):862–71.PubMedCrossRefGoogle Scholar
  31. 31.
    Ramachandran V, Watts LT, Maffi SK, Chen J, Schenker S, Henderson G. Ethanol-induced oxidative stress precedes mitochondrially mediated apoptotic death of cultured fetal cortical neurons. J Neurosci Res. 2003;74(4):577–88.PubMedCrossRefGoogle Scholar
  32. 32.
    Cohen-Kerem R, Koren G. Antioxidants and fetal protection against ethanol teratogenicity. I. Review of the experimental data and implications to humans. Neurotoxicol Teratol. 2003;25(1):1–9.PubMedCrossRefGoogle Scholar
  33. 33.
    Boyadjieva NI, Sarkar DK. Microglia play a role in ethanol-induced oxidative stress and apoptosis in developing hypothalamic neurons. Alcohol Clin Exp Res. 2013;37(2):252–62.PubMedCrossRefGoogle Scholar
  34. 34.
    Nakatsuji N. Craniofacial malformation in Xenopus laevis tadpoles caused by the exposure of early embryos to ethanol. Teratology. 1983;28(2):299–305.PubMedCrossRefGoogle Scholar
  35. 35.
    Lossie AC, Muir WM, Lo CL, et al. Implications of genomic signatures in the differential vulnerability to fetal alcohol exposure in C57BL/6 and DBA/2 mice. Front Genet. 2014;5:173.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Lussier AA, Weinberg J, Kobor MS. Epigenetics studies of fetal alcohol spectrum disorder: where are we now? Epigenomics. 2017;9(3):291–311.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Balaraman S, Schafer JJ, Tseng AM, et al. Plasma miRNA profiles in pregnant women predict infant outcomes following prenatal alcohol exposure. PLoS One. 2016;11(11):e0165081.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Astley SJSJ. Validation of the fetal alcohol spectrum disorder (FASD) 4-digit diagnostic code. J Popul Ther Clin Pharmacol. 2013;20(3):e416.PubMedGoogle Scholar
  39. 39.
    Chudley AE, Conry J, Cook JL, et al. Fetal alcohol spectrum disorder: Canadian guidelines for diagnosis. CMAJ. 2005;172(5 Suppl):S1–S21.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Bertrand JJ. Guidelines for identifying and referring persons with fetal alcohol syndrome. MMWR Recomm Rep. 2005;54(rr-11):1.PubMedGoogle Scholar
  41. 41.
    Moore ES, Ward RE, Wetherill LF, et al. Unique facial features distinguish fetal alcohol syndrome patients and controls in diverse ethnic populations. Alcohol Clin Exp Res. 2007;31(10):1707–13.PubMedCrossRefGoogle Scholar
  42. 42.
    May PA, Fiorentino D, Coriale G, et al. Prevalence of children with severe fetal alcohol spectrum disorders in communities near Rome, Italy: new estimated rates are higher than previous estimates. Int J Environ Res Public Health. 2011;8(6):2331–51.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Autti-Rämö I, Fagerlund Å, Ervalahti N, Loimu L, Korkman M, Hoyme HE. Fetal alcohol spectrum disorders in Finland: clinical delineation of 77 older children and adolescents. Am J Med Genet A. 2006;140((2):137–43.CrossRefGoogle Scholar
  44. 44.
    May PA, Blankenship J, Marais AS, et al. Approaching the prevalence of the full spectrum of fetal alcohol Spectrum disorders in a South African population-based study. Alcohol Clin Exp Res. 2013;37(5):818–30.PubMedCrossRefGoogle Scholar
  45. 45.
    O’Connor MJ, Rotheram-Borus MJ, Tomlinson M, Bill C, LeRoux IM, Stewart IM. Screening for fetal alcohol spectrum disorders by nonmedical community workers. J Popul Ther Clin Pharmacol. 2014;21(3):e442.PubMedPubMedCentralGoogle Scholar
  46. 46.
    Jones KL, Robinson LK, Bakhireva LN, et al. Accuracy of the diagnosis of physical features of fetal alcohol syndrome by pediatricians after specialized training. Pediatrics. 2006;118(6):e1734–8.PubMedCrossRefGoogle Scholar
  47. 47.
    Caputo C, Wood E, Jabbour L. Impact of fetal alcohol exposure on body systems: a systematic review. Birth Defects Res C Embryo Today. 2016;108(2):174–80.PubMedCrossRefGoogle Scholar
  48. 48.
    Warren KR, Foudin LL. Alcohol-related birth defects—the past, present, and future. Alcohol Res Health. 2001;25(3):153–8.PubMedGoogle Scholar
  49. 49.
    Makelarski JA, Romitti PA, Sun L, et al. Periconceptional maternal alcohol consumption and neural tube defects. Birth Defects Res A Clin Mol Teratol. 2013;97(3):152–60.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Jacobson SW, Chiodo LM, Sokol RJ, Jacobson JL. Validity of maternal report of prenatal alcohol, cocaine, and smoking in relation to neurobehavioral outcome. Pediatrics. 2002;109(5):815–25.PubMedCrossRefGoogle Scholar
  51. 51.
    Czeizel AEA. Smoking and alcohol drinking during pregnancy. The reliability of retrospective maternal self-reported information. Cent Eur J Public Health. 2005;12(4):179.Google Scholar
  52. 52.
    Lange S, Shield K, Koren G, Rehm J, Popova S. A comparison of the prevalence of prenatal alcohol exposure obtained via maternal self-reports versus meconium testing: a systematic literature review and meta-analysis. BMC Pregnancy Childbirth. 2014;14:127.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Knudsen AK, Skogen JC, Ystrom E, Sivertsen B, Tell GS, Torgersen L. Maternal pre-pregnancy risk drinking and toddler behavior problems: the Norwegian mother and child cohort study. Eur Child Adolesc Psychiatry. 2014;23(10):901–11.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    May PA, Blankenship J, Marais A-S, et al. Maternal alcohol consumption producing fetal alcohol spectrum disorders (FASD): quantity, frequency, and timing of drinking. Drug Alcohol Depend. 2013;133(2):502–12.PubMedCrossRefGoogle Scholar
  55. 55.
    Chiodo LM, Delaney-Black V, Sokol RJ, Janisse J, Pardo Y, Hannigan JH. Increased cut-point of the TACER-3 screen reduces false positives without losing sensitivity in predicting risk alcohol drinking in pregnancy. Alcohol Clin Exp Res. 2014;38(5):1401–8.PubMedCrossRefGoogle Scholar
  56. 56.
    Sobell LC, Sobell MB, Leo GI, Cancilla A. Reliability of a timeline method: assessing normal drinkers’ reports of recent drinking and a comparative evaluation across several populations. Br J Addict. 1988;83(4):393–402.PubMedCrossRefGoogle Scholar
  57. 57.
    Sobell LC, Agrawal S, Annis H, et al. Cross-cultural evaluation of two drinking assessment instruments: alcohol timeline followback and inventory of drinking situations. Subst Use Misuse. 2001;36(3):313–31.PubMedCrossRefGoogle Scholar
  58. 58.
    Jones KL, Hoyme HE, Robinson LK, et al. Fetal alcohol spectrum disorders: extending the range of structural defects. Am J Med Genet A. 2010;152A(11):2731–5.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 59.
    Thomason ME, Marusak HA. Toward understanding the impact of trauma on the early developing human brain. Neuroscience. 2017;342:55–67.PubMedCrossRefGoogle Scholar
  60. 60.
    Mattson SN, Riley EP. The quest for a neurobehavioral profile of heavy prenatal alcohol exposure. Alcohol Res Health. 2011;34(1):51–5.PubMedPubMedCentralGoogle Scholar
  61. 61.
    Mattson SN, Roesch SC, Fagerlund Å, et al. Toward a neurobehavioral profile of fetal alcohol spectrum disorders. Alcohol Clin Exp Res. 2010;34(9):1640–50.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Mattson SN, Roesch SC, Glass L, et al. Further development of a neurobehavioral profile of fetal alcohol spectrum disorders. Alcohol Clin Exp Res. 2013;37(3):517–28.PubMedCrossRefGoogle Scholar
  63. 63.
    Riley EP, McGee CL, Sowell ER. Teratogenic effects of alcohol: a decade of brain imaging. Am J Med Genet C Semin Med Genet. 2004;127c(1):35–41.PubMedCrossRefGoogle Scholar
  64. 64.
    Norman AL, Crocker N, Mattson SN, Riley EP. Neuroimaging and fetal alcohol spectrum disorders. Dev Disabil Res Rev. 2009;15(3):209–17.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Fryer SL, Schweinsburg BC, Bjorkquist OA, et al. Characterization of white matter microstructure in fetal alcohol spectrum disorders. Alcohol Clin Exp Res. 2009;33(3):514–21.PubMedCrossRefGoogle Scholar
  66. 66.
    Guerri C. Neuroanatomical and neurophysiological mechanisms involved in central nervous system dysfunctions induced by prenatal alcohol exposure. Alcohol Clin Exp Res. 1998;22(2):304–12.PubMedCrossRefGoogle Scholar
  67. 67.
    Roebuck TM, Mattson SN, Riley EP. A review of the neuroanatomical findings in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol Clin Exp Res. 1998;22(2):339–44.PubMedCrossRefGoogle Scholar
  68. 68.
    Mattson SN, Schoenfeld AM, Riley EP. Teratogenic effects of alcohol on brain and behavior. Alcohol Res Health. 2001;25(3):185–91.PubMedGoogle Scholar
  69. 69.
    Niccols A. Fetal alcohol syndrome and the developing socio-emotional brain. Brain Cogn. 2007;65(1):135–42.PubMedCrossRefGoogle Scholar
  70. 70.
    Lebel C, Mattson SN, Riley EP, et al. A longitudinal study of the long-term consequences of drinking during pregnancy: heavy in utero alcohol exposure disrupts the normal processes of brain development. J Neurosci. 2012;32(44):15243–51.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Rajaprakash M, Chakravarty MM, Lerch JP, Rovet J. Cortical morphology in children with alcohol-related neurodevelopmental disorder. Brain Behav. 2014;4(1):41–50.PubMedCrossRefGoogle Scholar
  72. 72.
    Donald KA, Fouche JP, Roos A, et al. Alcohol exposure in utero is associated with decreased gray matter volume in neonates. Metab Brain Dis. 2016;31(1):81–91.PubMedCrossRefGoogle Scholar
  73. 73.
    Sowell ER, Johnson A, Kan E, et al. Mapping white matter integrity and neurobehavioral correlates in children with fetal alcohol spectrum disorders. J Neurosci. 2008;28(6):1313–9.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Kodituwakku PW, Kalberg W, May PA. The effects of prenatal alcohol exposure on executive functioning. Alcohol Res Health. 2001;25(3):192–8.PubMedGoogle Scholar
  75. 75.
    Gautam P, Nunez SC, Narr KL, et al. Developmental trajectories for visuo-spatial attention are altered by prenatal alcohol exposure: a longitudinal FMRI study. Cereb Cortex. 2015;25(12):4761–71.PubMedCrossRefGoogle Scholar
  76. 76.
    Kodali VN, Jacobson JL, Lindinger NM, et al. Differential recruitment of brain regions during response inhibition in children prenatally exposed to alcohol. Alcohol Clin Exp Res. 2017;41(2):334–44.PubMedPubMedCentralCrossRefGoogle Scholar
  77. 77.
    Wozniak JR, Muetzel RL. What does diffusion tensor imaging reveal about the brain and cognition in fetal alcohol spectrum disorders? Neuropsychol Rev. 2011;21(2):133–47.PubMedCrossRefGoogle Scholar
  78. 78.
    Wozniak JR, Mueller BA, Muetzel RL, et al. Inter-hemispheric functional connectivity disruption in children with prenatal alcohol exposure. Alcohol Clin Exp Res. 2011;35(5):849–61.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Coles CD, Goldstein FC, Lynch ME, et al. Memory and brain volume in adults prenatally exposed to alcohol. Brain Cogn. 2011;75(1):67–77.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Willoughby KA, Sheard ED, Nash K, Rovet J. Effects of prenatal alcohol exposure on hippocampal volume, verbal learning, and verbal and spatial recall in late childhood. J Int Neuropsychol Soc. 2008;14(6):1022–33.PubMedCrossRefGoogle Scholar
  81. 81.
    Willford J, Day R, Aizenstein H, Day N. Caudate asymmetry: a neurobiological marker of moderate prenatal alcohol exposure in young adults. Neurotoxicol Teratol. 2010;32(6):589–94.PubMedPubMedCentralCrossRefGoogle Scholar
  82. 82.
    Khoury JE, Milligan K, Girard TA. Executive functioning in children and adolescents prenatally exposed to alcohol: a meta-analytic review. Neuropsychol Rev. 2015;25(2):149–70.PubMedCrossRefGoogle Scholar
  83. 83.
    Gerhold MM, Jacobson SW, Jacobson JL, Molteno CD, Meintjes EM, Andrew CM. An ERP study of response inhibition in the auditory domain in children with fetal alcohol spectrum disorders. Alcohol Clin Exp Res. 2017;41(1):96–106.PubMedCrossRefGoogle Scholar
  84. 84.
    Roos LE, Beauchamp KG, Pears KC, Fisher PA, Berkman ET, Capaldi D. Effects of prenatal substance exposure on neurocognitive correlates of inhibitory control success and failure. Appl Neuropsychol Child. 2017;6(4):269–80.PubMedCrossRefGoogle Scholar
  85. 85.
    du Plooy CP, Malcolm-Smith S, Adnams CM, Stein DJ, Donald KA. The effects of prenatal alcohol exposure on episodic memory functioning: a systematic review. Arch Clin Neuropsychol. 2016;31(7):710–26.CrossRefGoogle Scholar
  86. 86.
    Fryer SL, Mattson SN, Jernigan TL, Archibald SL, Jones KL, Riley EP. Caudate volume predicts neurocognitive performance in youth with heavy prenatal alcohol exposure. Alcohol Clin Exp Res. 2012;36(11):1932–41.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Donald KA, Eastman E, Howells FM, et al. Neuroimaging effects of prenatal alcohol exposure on the developing human brain: a magnetic resonance imaging review. Acta Neuropsychiatr. 2015;27(5):251–69.PubMedCrossRefGoogle Scholar
  88. 88.
    Meintjes EM, Narr KL, van der Kouwe AJ, et al. A tensor-based morphometry analysis of regional differences in brain volume in relation to prenatal alcohol exposure. NeuroImage Clin. 2014;5:152–60.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Luo J. Effects of ethanol on the cerebellum: advances and prospects. Cerebellum. 2015;14(4):383–5.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Valenzuela CF, Lindquist B, Zamudio-Bulcock PA. A review of synaptic plasticity at Purkinje neurons with a focus on ethanol-induced cerebellar dysfunction. Int Rev Neurobiol. 2010;91:339–72.PubMedCrossRefGoogle Scholar
  91. 91.
    Jacobson SW, Jacobson JL, Molteno CD, et al. Heavy prenatal alcohol exposure is related to smaller corpus callosum in newborn MRI scans. Alcohol Clin Exp Res. 2017;41(5):965–75.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Wozniak JR, Muetzel RL, Mueller BA, et al. Microstructural corpus callosum anomalies in children with prenatal alcohol exposure: an extension of previous diffusion tensor imaging findings. Alcohol Clin Exp Res. 2009;33(10):1825–35.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Dodge NC, Jacobson JL, Molteno CD, et al. Prenatal alcohol exposure and interhemispheric transfer of tactile information: Detroit and Cape Town findings. Alcohol Clin Exp Res. 2009;33(9):1628–37.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Kable JA, O’Connor MJ, Olson HC, et al. Neurobehavioral disorder associated with prenatal alcohol exposure (ND-PAE): proposed DSM-5 diagnosis. Child Psychiatry Hum Dev. 2016;47(2):335–46.PubMedCrossRefGoogle Scholar
  95. 95.
    Doyle LR, Mattson SN. Neurobehavioral disorder associated with prenatal alcohol exposure (ND-PAE): review of evidence and guidelines for assessment. Curr Dev Disord Rep. 2015;2(3):175–86.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Hagan JF, Balachova T, Bertrand J, et al. Neurobehavioral disorder associated with prenatal alcohol exposure. Pediatrics. 2016;138(4):e20151553.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Kable JA, Mukherjee RA. Neurodevelopmental disorder associated with prenatal exposure to alcohol (ND-PAE): a proposed diagnostic method of capturing the neurocognitive phenotype of FASD. Eur J Med Genet. 2017;60(1):49–54.PubMedCrossRefGoogle Scholar
  98. 98.
    Coles CD, Smith IE, Falek A. Prenatal alcohol exposure and infant behavior: immediate effects and implications for later development. Adv Alcohol Subst Abuse. 1987;6(4):87–104.PubMedCrossRefGoogle Scholar
  99. 99.
    Jacobson JL, Jacobson SW, Sokol RJ, Martier SS, Ager JW, Kaplan-Estrin MG. Teratogenic effects of alcohol on infant development. Alcohol Clin Exp Res. 1993;17(1):174–83.PubMedCrossRefGoogle Scholar
  100. 100.
    Jacobson SW, Jacobson JL, Sokol RJ. Effects of fetal alcohol exposure on infant reaction time. Alcohol Clin Exp Res. 1994;18(5):1125–32.PubMedCrossRefGoogle Scholar
  101. 101.
    Coles CD, Kable JA, Drews-Botsch C, Falek A. Early identification of risk for effects of prenatal alcohol exposure. J Stud Alcohol. 2000;61(4):607–16.PubMedCrossRefGoogle Scholar
  102. 102.
    Molteno CD, Jacobson JL, Carter RC, Dodge NC, Jacobson SW. Infant emotional withdrawal: a precursor of affective and cognitive disturbance in fetal alcohol spectrum disorders. Alcohol Clin Exp Res. 2014;38(2):479–88.PubMedCrossRefGoogle Scholar
  103. 103.
    Streissguth AP, Sampson PD, Barr HM. Neurobehavioral dose-response effects of prenatal alcohol exposure in humans from infancy to adulthood. Ann N Y Acad Sci. 1989;562(1):145–58.PubMedCrossRefGoogle Scholar
  104. 104.
    Kalberg WO, Provost B, Tollison SJ, et al. Comparison of motor delays in young children with fetal alcohol syndrome to those with prenatal alcohol exposure and with no prenatal alcohol exposure. Alcohol Clin Exp Res. 2006;30(12):2037–45.PubMedCrossRefGoogle Scholar
  105. 105.
    Lucas BR, Latimer J, Pinto RZ, et al. Gross motor deficits in children prenatally exposed to alcohol: a meta-analysis. Pediatrics. 2014;134(1):e192–209.PubMedCrossRefGoogle Scholar
  106. 106.
    McGee CL, Bjorkquist OA, Riley EP, Mattson SN. Impaired language performance in young children with heavy prenatal alcohol exposure. Neurotoxicol Teratol. 2009;31(2):71–5.PubMedCrossRefGoogle Scholar
  107. 107.
    Cone-Wesson B. Prenatal alcohol and cocaine exposure: influences on cognition, speech, language, and hearing. J Commun Disord. 2005;38(4):279–302.PubMedCrossRefGoogle Scholar
  108. 108.
    Stephen JM, Kodituwakku PW, Kodituwakku EL, et al. Delays in auditory processing identified in preschool children with FASD. Alcohol Clin Exp Res. 2012;36(10):1720–7.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Fuglestad AJ, Whitley ML, Carlson SM, et al. Executive functioning deficits in preschool children with fetal alcohol spectrum disorders. Child Neuropsychol. 2015;21(6):716–31.PubMedCrossRefGoogle Scholar
  110. 110.
    D’Onofrio BM, Van Hulle CA, Waldman ID, Rodgers JL, Rathouz PJ, Lahey BB. Causal inferences regarding prenatal alcohol exposure and childhood externalizing problems. Arch Gen Psychiatry. 2007;64(11):1296–304.PubMedCrossRefGoogle Scholar
  111. 111.
    Alvik A, Aalen OO, Lindemann R. Early fetal binge alcohol exposure predicts high behavioral symptom scores in 5.5-year-old children. Alcohol Clin Exp Res. 2013;37(11):1954–62.PubMedCrossRefGoogle Scholar
  112. 112.
    Rasmussen C, Becker M, McLennan J, Urichuk L, Andrew G. An evaluation of social skills in children with and without prenatal alcohol exposure. Child Care Health Dev. 2011;37(5):711–8.PubMedCrossRefGoogle Scholar
  113. 113.
    Chen ML, Olson HC, Picciano JF, Starr JR, Owens J. Sleep problems in children with fetal alcohol spectrum disorders. J Clin Sleep Med. 2012;8(4):421–9.PubMedPubMedCentralGoogle Scholar
  114. 114.
    Carr JL, Agnihotri S, Keightley M. Sensory processing and adaptive behavior deficits of children across the fetal alcohol spectrum disorder continuum. Alcohol Clin Exp Res. 2010;34(6):1022–32.PubMedCrossRefGoogle Scholar
  115. 115.
    Lenroot RK, Giedd JN. Brain development in children and adolescents: insights from anatomical magnetic resonance imaging. Neurosci Biobehav Rev. 2006;30(6):718–29.PubMedCrossRefGoogle Scholar
  116. 116.
    Roussotte FF, Sulik KK, Mattson SN, et al. Regional brain volume reductions relate to facial dysmorphology and neurocognitive function in fetal alcohol spectrum disorders. Hum Brain Mapp. 2012;33(4):920–37.PubMedCrossRefGoogle Scholar
  117. 117.
    Gautam P, Lebel C, Narr KL, et al. Volume changes and brain-behavior relationships in white matter and subcortical gray matter in children with prenatal alcohol exposure. Hum Brain Mapp. 2015;36(6):2318–29.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    O’Leary CM, Taylor C, Zubrick SR, Kurinczuk JJ, Bower C. Prenatal alcohol exposure and educational achievement in children aged 8-9 years. Pediatrics. 2013;132(2):e468–75.PubMedCrossRefGoogle Scholar
  119. 119.
    Carter RC, Jacobson JL, Molteno CD, Dodge NC, Meintjes EM, Jacobson SW. Fetal alcohol growth restriction and cognitive impairment. Pediatrics. 2016;138(2):e20160775.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Lewis CE, Thomas KG, Molteno CD, et al. Prospective memory impairment in children with prenatal alcohol exposure. Alcohol Clin Exp Res. 2016;40(5):969–78.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Tsang TW, Lucas BR, Carmichael Olson H, Pinto RZ, Elliott EJ. Prenatal alcohol exposure, FASD, and child behavior: a meta-analysis. Pediatrics. 2016;137(3):e20152542.PubMedCrossRefGoogle Scholar
  122. 122.
    Glass L, Graham DM, Deweese BN, Jones KL, Riley EP, Mattson SN. Correspondence of parent report and laboratory measures of inattention and hyperactivity in children with heavy prenatal alcohol exposure. Neurotoxicol Teratol. 2014;42:43–50.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Kully-Martens K, Denys K, Treit S, Tamana S, Rasmussen C. A review of social skills deficits in individuals with fetal alcohol spectrum disorders and prenatal alcohol exposure: profiles, mechanisms, and interventions. Alcohol Clin Exp Res. 2012;36(4):568–76.PubMedCrossRefGoogle Scholar
  124. 124.
    Keil V, Paley B, Frankel F, O’Connor MJ. Impact of a social skills intervention on the hostile attributions of children with prenatal alcohol exposure. Alcohol Clin Exp Res. 2010;34(2):231–41.PubMedCrossRefGoogle Scholar
  125. 125.
    Kerns KA, Siklos S, Baker L, Muller U. Emotion recognition in children with fetal alcohol spectrum disorders. Child Neuropsychol. 2016;22(3):255–75.PubMedCrossRefGoogle Scholar
  126. 126.
    Casey BJ, Getz S, Galvan A. The adolescent brain. Dev Rev. 2008;28(1):62–77.PubMedPubMedCentralCrossRefGoogle Scholar
  127. 127.
    Migliorini R, Moore EM, Glass L, et al. Anterior cingulate cortex surface area relates to behavioral inhibition in adolescents with and without heavy prenatal alcohol exposure. Behav Brain Res. 2015;292:26–35.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Day NL, Helsel A, Sonon K, Goldschmidt L. The association between prenatal alcohol exposure and behavior at 22 years of age. Alcohol Clin Exp Res. 2013;37(7):1171–8.PubMedCrossRefGoogle Scholar
  129. 129.
    Moore EM, Riley EP. What happens when children with Fetal alcohol Spectrum disorders become adults? Curr Dev Disord Rep. 2015;2(3):219–27.PubMedPubMedCentralCrossRefGoogle Scholar
  130. 130.
    Lindinger NM, Malcolm-Smith S, Dodge NC, et al. Theory of mind in children with fetal alcohol spectrum disorders. Alcohol Clin Exp Res. 2016;40(2):367–76.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Stevens SA, Clairman H, Nash K, Rovet J. Social perception in children with fetal alcohol spectrum disorder. Child Neuropsychol. 2017;23(8):980–93.PubMedCrossRefGoogle Scholar
  132. 132.
    Mattson SN, Riley EP. A review of the neurobehavioral deficits in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol Clin Exp Res. 1998;22(2):279.CrossRefPubMedGoogle Scholar
  133. 133.
    Coles CD. Discriminating the effects of prenatal alcohol exposure from other behavioral and learning disorders. Alcohol Res Health. 2011;34(1):42.PubMedPubMedCentralGoogle Scholar
  134. 134.
    Graham DM, Crocker N, Deweese BN, et al. Prenatal alcohol exposure, ADHD, and sluggish cognitive tempo. Alcohol Clin Exp Res. 2013;37(Suppl 1):E338–46.PubMedCrossRefGoogle Scholar
  135. 135.
    Stevens SA, Nash K, Koren G, Rovet J. Autism characteristics in children with fetal alcohol spectrum disorders. Child Neuropsychol. 2013;19(6):579–87.PubMedCrossRefGoogle Scholar
  136. 136.
    Bishop S, Gahagan S, Lord C. Re-examining the core features of autism: a comparison of autism spectrum disorder and fetal alcohol spectrum disorder. J Child Psychol Psychiatry. 2007;48(11):1111–21.PubMedCrossRefGoogle Scholar
  137. 137.
    Miller LC, Chan W, Litvinova A, Rubin A, Tirella L, Cermak S. Medical diagnoses and growth of children residing in Russian orphanages. Acta paediatr. 2007;96(12):1765–9.PubMedCrossRefGoogle Scholar
  138. 138.
    Miller LC, Chan W, Litvinova A, et al. Fetal alcohol spectrum disorders in children residing in Russian orphanages: a phenotypic survey. Alcohol Clin Exp Res. 2006;30(3):531–8.PubMedCrossRefGoogle Scholar
  139. 139.
    Chisholm K, Carter MC, Ames EW, Morison SJ. Attachment security and indiscriminately friendly behavior in children adopted from Romanian orphanages. Dev Psychopathol. 2009;7(2):283–94.CrossRefGoogle Scholar
  140. 140.
    Rutter M, Colvert E, Kreppner J, et al. Early adolescent outcomes for institutionally-deprived and non-deprived adoptees. I: disinhibited attachment. J Child Psychol Psychiatry. 2007;48(1):17–30.PubMedCrossRefGoogle Scholar
  141. 141.
    Smyke AT, Zeanah CH, Gleason MM, et al. A randomized controlled trial comparing foster care and institutional care for children with signs of reactive attachment disorder. Am J Psychiatr. 2012;169(5):508–14.PubMedCrossRefGoogle Scholar
  142. 142.
    Zeanah CH, Smyke AT, Koga SF, Carlson E, The Bucharest Early Intervention Project Core Group. Attachment in institutionalized and community children in Romania. Child Dev. 2005;76(5):1015–28.PubMedCrossRefGoogle Scholar
  143. 143.
    van der Kolk BA, Roth S, Pelcovitz D, Sunday S, Spinazzola J. Disorders of extreme stress: the empirical foundation of a complex adaptation to trauma. J Trauma Stress. 2005;18(5):389–99.PubMedCrossRefGoogle Scholar
  144. 144.
    Ackerman PT, Newton JE, McPherson WB, Jones JG, Dykman RA. Prevalence of post traumatic stress disorder and other psychiatric diagnoses in three groups of abused children (sexual, physical, and both). Child Abuse Negl. 1998;22(8):759–74.PubMedCrossRefGoogle Scholar
  145. 145.
    Kable JA, Coles CD. Evidence supporting the internal validity of the proposed ND-PAE disorder. Child Psychiatry Hum Dev. 2018;49(2):163–75.PubMedCrossRefGoogle Scholar
  146. 146.
    Rutter M, Andersen-Wood L, Beckett C, et al. Quasi-autistic patterns following severe early global privation. J Child Psychol Psychiatry Allied Discip. 1999;40(4):537.CrossRefGoogle Scholar
  147. 147.
    Rutter M, Kreppner J, Croft C, et al. Early adolescent outcomes of institutionally deprived and non-deprived adoptees. III. Quasi-autism. J Child Psychol Psychiatry. 2007;48(12):1200–7.PubMedCrossRefGoogle Scholar
  148. 148.
    Brown NN, Burd L, Grant T, Edwards W, Adler R, Streissguth A. Prenatal alcohol exposure: an assessment strategy for the legal context. Int J Law Psychiatry. 2015;42-43:144–8.PubMedCrossRefGoogle Scholar
  149. 149.
    Mutch RC, Jones HM, Bower C, Watkins RE. Fetal alcohol spectrum disorders: using knowledge, attitudes and practice of justice professionals to support their educational needs. J Popul Ther Clin Pharmacol. 2016;23(1):e77–89.PubMedGoogle Scholar
  150. 150.
    Fisher PA, Beauchamp KG, Roos LE, Noll LK, Flannery J, Delker BC. The neurobiology of intervention and prevention in early adversity. Annu Rev Clin Psychol. 2016;12:331–57.PubMedCrossRefGoogle Scholar
  151. 151.
    Abrams SE. Interventions that protect. Public Health Nurs. 2010;27(3):201–2.PubMedCrossRefGoogle Scholar
  152. 152.
    Currie BA, Hoy J, Legge L, Temple VK, Tahir M. Adults with fetal alcohol Spectrum disorder: factors associated with positive outcomes and contact with the criminal justice system. J Popul Ther Clin Pharmacol. 2016;23(1):e37–52.PubMedGoogle Scholar
  153. 153.
    Clarke-McMullen DM. Evaluation of a successful fetal alcohol spectrum disorder coalition in Ontario, Canada. Public Health Nurs. 2010;27(3):240–7.PubMedCrossRefGoogle Scholar
  154. 154.
    Paley B, O’Connor MJ, Frankel F, Marquardt R. Predictors of stress in parents of children with fetal alcohol spectrum disorders. J Dev Behav Pediatr. 2006;27(5):396–404.PubMedCrossRefGoogle Scholar
  155. 155.
    May PA. A multiple-level, comprehensive approach to the prevention of fetal alcohol syndrome (FAS) and other alcohol-related birth defects (ARBD). Int J Addict. 1995;30(12):1549.PubMedCrossRefGoogle Scholar
  156. 156.
    Smith IEI. Multilevel intervention for prevention of fetal alcohol syndrome and effects of prenatal alcohol exposure. Recent Dev Alcohol. 1991;9:165.PubMedGoogle Scholar
  157. 157.
    Olson HC, Oti R, Gelo J, Beck S. “Family matters:” Fetal alcohol spectrum disorders and the family. Dev Disabil Res Rev. 2009;15(3):235–49.PubMedCrossRefGoogle Scholar
  158. 158.
    Salmon JJ. Fetal alcohol spectrum disorder: New Zealand birth mothers’ experiences. Can J Clin Pharmacol. 2008;15(2):e191.PubMedGoogle Scholar
  159. 159.
    Zarnegar Z, Hambrick EP, Perry BD, Azen SP, Peterson C. Clinical improvements in adopted children with fetal alcohol spectrum disorders through neurodevelopmentally informed clinical intervention: a pilot study. Clin Child Psychol Psychiatry. 2016;21(4):551–67.PubMedCrossRefGoogle Scholar
  160. 160.
    Paley B, O’Connor MJ. Intervention for individuals with fetal alcohol spectrum disorders: treatment approaches and case management. Dev Disabil Res Rev. 2009;15(3):258–67.PubMedCrossRefGoogle Scholar
  161. 161.
    O’Connor MJ, Sigman M, Kasari C. Attachment behavior of infants exposed prenatally to alcohol: mediating effects of infant affect and mother-infant interaction. Dev Psychopathol. 1992;4(02):243–56.CrossRefGoogle Scholar
  162. 162.
    Pei J, Baugh L, Andrew G, Rasmussen C. Intervention recommendations and subsequent access to services following clinical assessment for fetal alcohol spectrum disorders. Res Dev Disabil. 2017;60:176–86.PubMedCrossRefGoogle Scholar
  163. 163.
    Bertrand J. Interventions for children with fetal alcohol spectrum disorders (FASDs): overview of findings for five innovative research projects. Res Dev Disabil. 2009;30(5):986–1006.PubMedCrossRefGoogle Scholar
  164. 164.
    Fagerlund A, Autti-Ramo I, Hoyme HE, Mattson SN, Korkman M. Risk factors for behavioural problems in foetal alcohol spectrum disorders. Acta Paediatr. 2011;100(11):1481–8.PubMedPubMedCentralCrossRefGoogle Scholar
  165. 165.
    Hoyme HE, Hoyme DB, Elliott AJ, et al. A South African mixed race lip/philtrum guide for diagnosis of fetal alcohol spectrum disorders. Am J Med Genet A. 2015;0(4):752–5.PubMedCentralCrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  • Prachi E. Shah
    • 1
    Email author
  • Danielle Shapiro
    • 1
  • Tedi Milgrom
    • 1
  • H. Eugene Hoyme
    • 2
  1. 1.University of MichiganAnn ArborUSA
  2. 2.University of ArizonaTucsonUSA

Personalised recommendations