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Inattention and impulsivity associated with prenatal alcohol exposure in a prospective cohort study with 11-years-old Brazilian children

European Child & Adolescent Psychiatry volume 25, pages 1327–1335 (2016)Cite this article

Abstract

This paper aimed to examine prenatal alcohol exposure and neuropsychological parameters and its relationship to impulsivity and inattention. Longitudinal prospective case–control cohort study starting with the risk drinking assessment of 449 third-trimester pregnant women, and a follow-up phase with 56 mother–child pairs (28 alcohol-exposed versus 28 non-exposed), with 11–12 years old children. The cohort study was followed up for 11 years. Quantity-frequency structured questions as well as AUDIT and T-ACE questionnaires were used to assess maternal alcohol consumption. A comprehensive set of neuropsychological testing instruments was used, including d2 Test, RCFT, RAVLT, WISC-III, among others. To control low IQ effects and intellectual disability diagnoses, as well differences in school skills biasing the neuropsychological comparison assessment, children with IQ <70 or learning disabilities were excluded of the sample. The two groups showed to be very comparable regarding sex, age, schooling, global IQ, laterality and maternal and social risk factors. Significant statistical differences were found for higher speed processing, total errors, and number of omission errors in the d2 Test. Likewise, there were differences found on RCFT test (lower scores for copy, immediate and delayed recall), and on semantic verbal fluency tests with a lower score. Prenatal alcohol-exposed children seems to be more inattentive and impulsive; they have poorer skills in verbal fluency, visuospatial working memory, and executive processing when compared to non-exposed children who were part of the same cohort sample.

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References

  1. Doerrie N, Foecker M, Freunscht I, Hebebrand J (2014) Fetal alcohol spectrum disorders. Eur Child Adolesc Psychiatry 23:863–875

    Article  Google Scholar 

  2. Jones KL, Smith DW (1973) Recognition of fetal alcohol syndrome in early infancy. Lancet 2:999–1001

    Article  Google Scholar 

  3. Niccols A (2007) Fetal alcohol syndrome and the developing socio-emotional brain. Brain Cogn 65:135–142

    Article  PubMed  Google Scholar 

  4. American Psychiatric Association (2013) Diagnostic and statistical manual of mental disorders: DSM-5. American Psychiatric Association, Washington, D.C

    Book  Google Scholar 

  5. Archibald SL, Fennema-Notestine C, Gamst A et al (2001) Brain dysmorphology in individuals with severe prenatal alcohol exposure. Dev Med Child Neurol 43:148–154

    CAS  Article  PubMed  Google Scholar 

  6. Guerri C, RenauPiqueras J (1997) Alcohol, astroglia, and brain development. Mol Neurobiol 15:65–81

    CAS  Article  PubMed  Google Scholar 

  7. Sulik KK (2014) Fetal alcohol spectrum disorder: pathogenesis and mechanisms. Handb Clin Neurol 125:463–475

    Article  PubMed  Google Scholar 

  8. Mattson SN, Riley EP (1998) A review of the neurobehavioral deficits in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcohol Clin Exp Res 22:279–294

    CAS  Article  PubMed  Google Scholar 

  9. Niclasen J (2015) Prenatal exposure to alcohol and the developing fetus: methodological issues. BJOG 122:770–772

    CAS  Article  PubMed  Google Scholar 

  10. Fabbri CE, Furtado EF, Laprega MR (2007) Alcohol consumption in pregnancy: performance of the Brazilian version of the questionnaire T-ACE. Rev Saude Publica 41:979–984

    Article  PubMed  Google Scholar 

  11. Pinheiro SN, Laprega MR, Furtado EF (2005) Psychiatric morbidity and alcohol use by pregnant women in a public obstetric service. Rev Saude Publica 39:593–598

    Article  PubMed  Google Scholar 

  12. World Health Organization (1993) The ICD-10 classification of mental and behavioural disorders: diagnostic criteria for research. World Health Organization, Geneva

    Google Scholar 

  13. Kish L (1965) Survey sampling. Wiley, New York

    Google Scholar 

  14. Obuchowski NA (1998) Sample size calculations in studies of test accuracy. Stat Methods Med Res 7:371–392

    CAS  Article  PubMed  Google Scholar 

  15. Brickenkamp R, Zillmer E (1998) The d2 test of attention. Hogrefe & Huber, Seattle

    Google Scholar 

  16. Diniz LFM, Cruz MDFD, Torres VDM, Cosenza RM (2000) O teste de aprendizagem auditivo-verbal de Rey: normas para uma população brasileira. Rev Bras Neurol 3:79–83

    Google Scholar 

  17. Rey A (2010) Figuras Complexas de Rey-teste de cópia e de reprodução de memória de Figuras Geométricas Complexas. Casa do Psicólogo, São Paulo

    Google Scholar 

  18. Heaton RK, Chelune GJ, Talley JL, Kay GG, Curtiss G (2004) Teste Wisconsin de classificação de cartas. Casa do Psicólogo, São Paulo

    Google Scholar 

  19. Brucki SMD, Malheiros SMF, Okamoto IH, Bertolucci PHF (1997) Normative data: category verbal fluency. Arq Neuropsiquiatr 55:56–61

    CAS  Article  PubMed  Google Scholar 

  20. Fernandes Malloy-Diniz L, Bentes RC, Figueiredo PM et al (2007) Standardisation of a battery of tests to evaluate language comprehension, verbal fluency and naming skills in 7–10 years old Brazilian children: preliminary findings. Rev Neurol 44:275–280

    PubMed  Google Scholar 

  21. Prifitera A, Saklofske DH (1998) WISC-III clinical use and interpretation: scientist–practitioner perspectives. Academic Press, San Diego

  22. Wechsler D (2002) Escala de inteligência Wechsler para crianças. Casa do Psicólogo, São Paulo

    Google Scholar 

  23. Stein LM (1994) TDE teste de desempenho escolar. Casa do Psicólogo, São Paulo

    Google Scholar 

  24. Streissguth AP, Sampson PD, Barr HM et al (1986) Studying alcohol teratogenesis from the perspective of the fetal alcohol syndrome: methodological and statistical issues. Ann N Y Acad Sci 477:63–86

    CAS  Article  PubMed  Google Scholar 

  25. Esper LH, Furtado EF (2014) Identifying maternal risk factors associated with fetal alcohol spectrum disorders: a systematic review. Eur Child Adolesc Psychiatry 23:877–889

    Article  PubMed  Google Scholar 

  26. Vaurio L, Riley ER, Mattson SN (2008) Differences in executive functioning in children with heavy prenatal alcohol exposure or attention-deficit/hyperactivity disorder. J Int Neuropsychol Soc 14:119–129

    Article  PubMed  PubMed Central  Google Scholar 

  27. Quattlebaum JL, O’Connor MJ (2013) Higher functioning children with prenatal alcohol exposure: is there a specific neurocognitive profile? Child Neuropsychol 19:561–578

    Article  PubMed  Google Scholar 

  28. Sampson PD, Streissguth AP, Bookstein FL, Barr HM (2000) On categorizations in analyses of alcohol teratogenesis. Environ Health Perspect 108:421–428

    Article  PubMed  PubMed Central  Google Scholar 

  29. Burden MJ, Andrew C, Saint-Amour D et al (2009) The effects of fetal alcohol syndrome on response execution and inhibition: an event-related potential study. Alcohol Exp Res 33:1994–2004

    Article  Google Scholar 

  30. Coles CD, Brown RT, Smith IE et al (1991) Effects of prenatal alcohol exposure at school age: I-physical and cognitive development. Neurotoxicol Teratol 13:357–367

    CAS  Article  PubMed  Google Scholar 

  31. Mirsky AF, Anthony BJ, Duncan CC et al (1991) Analysis of the elements of attention: a neuropsychological approach. Neuropsychol Rev 2:109–145

    CAS  Article  PubMed  Google Scholar 

  32. Jacobson SW, Jacobson JL, Sokol RJ (1994) Effects of fetal alcohol exposure on infant reaction-time. Alcohol Exp Res 18:1125–1132

    CAS  Article  Google Scholar 

  33. Patton JH, Stanford MS, Barratt ES (1995) Factor structure of the Barratt Impulsiveness Scale. J Clin Psychol 51:768–774

    CAS  Article  PubMed  Google Scholar 

  34. Mattson SN, Calarco KE, Lang AR (2006) Focused and shifting attention in children with heavy prenatal alcohol exposure. Neuropsychology 20:361–369

    Article  PubMed  PubMed Central  Google Scholar 

  35. Mattson SN, Goodman AM, Caine C et al (1999) Executive functioning in children with heavy prenatal alcohol exposure. Alcohol Exp Res 23:1808–1815

    CAS  Article  Google Scholar 

  36. Kodituwakku PW, Handmaker NS, Cutler SK et al (1995) Specific impairments in self-regulation in children exposed to alcohol prenatally. Alcohol Exp Res 19:1558–1564

    CAS  Article  Google Scholar 

  37. Nanson JL, Hiscock M (1990) Attention deficits in children exposed to alcohol prenatally. Alcohol Clin Exp Res 14:656–661

    CAS  Article  PubMed  Google Scholar 

  38. Pei J, Job J, Kully-Martens K, Rasmussen C (2011) Executive function and memory in children with fetal alcohol spectrum disorder. Child Neuropsychol 17:290–309

    Article  PubMed  Google Scholar 

  39. Aragon AS, Coriale G, Fiorentino D et al (2008) Neuropsychological characteristics of Italian children with fetal alcohol spectrum disorders. Alcohol Exp Res 32:1909–1919

    Google Scholar 

  40. Mattson SN, Roesch SC, Fagerlund A et al (2010) Toward a neurobehavioral profile of fetal alcohol spectrum disorders. Alcohol Exp Res 34:1640–1650

    Article  Google Scholar 

  41. Schonfeld AM, Mattson SN, Lang AR et al (2001) Verbal and nonverbal fluency in children with heavy prenatal alcohol exposure. J Stud Alcohol 62:239–246

    CAS  Article  PubMed  Google Scholar 

  42. Kodituwakku P, Coriale G, Fiorentino D et al (2006) Neurobehavioral characteristics of children with fetal alcohol spectrum disorders in communities from Italy: preliminary results. Alcohol Clin Exp Res 30:1551–1561

    Article  PubMed  Google Scholar 

  43. Kodituwakku PW, Adnams CM, Hay A et al (2006) Letter and category fluency in children with fetal alcohol syndrome from a community in South Africa. J Stud Alcohol 67:502–509

    Article  PubMed  Google Scholar 

  44. Rasmussen C, Bisanz J (2009) Executive functioning in children with fetal alcohol spectrum disorders: profiles and age-related differences. Child Neuropsychol 15:201–215

    Article  PubMed  Google Scholar 

  45. Brocki KC, Bohlin G (2004) Executive functions in children aged 6–13: a dimensional and developmental study. Dev Neuropsychol 26:571–593

    Article  PubMed  Google Scholar 

  46. Korkman M, Kemp SL, Kirk U (2001) Effects of age on neurocognitive measures of children ages 5–12: a cross-sectional study on 800 children from the United States. Dev Neuropsychol 20:331–354

    CAS  Article  PubMed  Google Scholar 

  47. Baldo JV, Schwartz S, Wilkins D, Dronkers NF (2006) Role of frontal versus temporal cortex in verbal fluency as revealed by voxel-based lesion symptom mapping. J Int Neuropsychol Soc 12:896–900

    Article  PubMed  Google Scholar 

  48. Birn RM, Kenworthy L, Case L et al (2010) Neural systems supporting lexical search guided by letter and semantic category cues: a self-paced overt response fMRI study of verbal fluency. Neuroimage 49:1099–1107

    Article  PubMed  Google Scholar 

  49. Davidson PSR, Gao FQ, Mason WP et al (2008) Verbal fluency, trail making, and Wisconsin card sorting test performance following right frontal lobe tumor resection. J Clin Exp Neuropsychol 30:18–32

    Article  PubMed  Google Scholar 

  50. Grogan A, Green DW, Ali N et al (2009) Structural correlates of semantic and phonemic fluency ability in first and second languages. Cereb Cortex 19:2690–2698

    Article  PubMed  PubMed Central  Google Scholar 

  51. Sowell ER, Lu LH, O’Hare ED et al (2007) Functional magnetic resonance imaging of verbal learning in children with heavy prenatal alcohol exposure. NeuroReport 18:635–639

    Article  PubMed  Google Scholar 

  52. Coles CD, Platzman KA, RaskindHood CL et al (1997) A comparison of children affected by prenatal alcohol exposure and attention deficit, hyperactivity disorder. Alcohol Clin Exp Res 21:150–161

    CAS  Article  PubMed  Google Scholar 

  53. McGee CL, Schonfeld AM, Roebuck-Spencer TM et al (2008) Children with heavy prenatal alcohol exposure demonstrate deficits on multiple measures of concept formation. Alcohol Clin Exp Res 32:1388–1397

    Article  PubMed  PubMed Central  Google Scholar 

  54. Olson HC, Feldman JJ, Streissguth AP et al (1998) Neuropsychological deficits in adolescents with fetal alcohol syndrome: clinical findings. Alcohol Clin Exp Res 22:1998–2012

    CAS  PubMed  Google Scholar 

  55. Chasnoff IJ, Wells AM, Telford E et al (2010) Neurodevelopmental functioning in children with FAS, pFAS, and ARND. J Dev Behav Pediatr 31:192–201

    Article  PubMed  Google Scholar 

  56. Crocker N, Vaurio L, Riley EP, Mattson SN (2011) Comparison of verbal learning and memory in children with heavy prenatal alcohol exposure or attention-deficit/hyperactivity disorder. Alcohol Clin Exp Res 35:1114–1121

    Article  PubMed  PubMed Central  Google Scholar 

  57. Mattson SN, Roebuck TM (2002) Acquisition and retention of verbal and nonverbal information in children with heavy prenatal alcohol exposure. Alcohol Clin Exp Res 26:875–882

    CAS  Article  PubMed  Google Scholar 

  58. Vaurio L, Riley EP, Mattson SN (2011) Neuropsychological comparison of children with heavy prenatal alcohol exposure and an IQ-matched comparison group. J Int Neuropsychol Soc 17:463–473

    Article  PubMed  PubMed Central  Google Scholar 

  59. Willoughby KA, Sheard ED, Nash K, Rovet J (2008) Effects of prenatal alcohol exposure on hippocampal volume, verbal learning, and verbal and spatial recall in late childhood. J Int Neuropsychol Soc 14:1022–1033

    Article  PubMed  Google Scholar 

  60. Lewis CE, Thomas KGF, Dodge NC et al (2015) Verbal learning and memory impairment in children with fetal alcohol spectrum disorders. Alcohol Clin Exp Res 39:724–732

    Article  PubMed  Google Scholar 

  61. Richardson GA, Ryan C, Willford J et al (2002) Prenatal alcohol and marijuana exposure: effects on neuropsychological outcomes at 10 years. Neurotoxicol Teratol 24:309–320

    CAS  Article  PubMed  Google Scholar 

  62. Strauss E, Sherman EM, Spreen O (2006) A compendium of neuropsychological tests: administration, norms, and commentary. Oxford University Press, New York

    Google Scholar 

  63. Coles CD, Lynch ME, Kable JA et al (2010) Verbal and nonverbal memory in adults prenatally exposed to alcohol. Alcohol Clin Exp Res 34:897–906

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

CAPES Foundation (Brazilian Coordination for the Improvement of Higher Education Personnel, Ministry of Education) provided a PhD Grant for Sarah Teófilo de Sá Roriz.

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Authors and Affiliations

  1. Child and Adolescent Psychiatry, Department of Neurosciences and Behavior, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, Brazil

    Erikson Felipe Furtado

  2. Mental Health Graduate Program, Department of Neurosciences and Behavior, Ribeirão Preto Medical School, University of São Paulo, Ribeirão Preto, Brazil

    Sarah Teófilo de Sá Roriz

  3. Hospital das Clínicas da Faculdade de Medicina de Ribeirão Preto da Universidade de São Paulo Divisão de Psiquiatria, 3º andar, PAI-PAD, Sala 333. Avenida dos Bandeirantes, 3900, Monte Alegre, Ribeirão Preto, SP, 14049-400, Brazil

    Erikson Felipe Furtado

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  1. Erikson Felipe Furtado
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Correspondence to Erikson Felipe Furtado.

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Furtado, E.F., Roriz, S.T.d. Inattention and impulsivity associated with prenatal alcohol exposure in a prospective cohort study with 11-years-old Brazilian children. Eur Child Adolesc Psychiatry 25, 1327–1335 (2016). https://doi.org/10.1007/s00787-016-0857-y

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  • DOI: https://doi.org/10.1007/s00787-016-0857-y

Keywords

  • Fetal alcohol spectrum disorders
  • Prenatal alcohol exposure
  • Neuropsychological assessment
  • Prospective cohort study
  • Inattention
  • Impulsivity