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Prenatal alcohol exposure and developmental programming of mental illness

Part of: DOHaD ANZ Conference 2018: Genes, Environment and Evolution

Published online by Cambridge University Press:  20 February 2020

Danielle J. Burgess  and
Karen M. Moritz Open the ORCID record for Karen M. Moritz [Opens in a new window]
Danielle J. Burgess
Affiliation:
School of Biomedical Sciences, The University of Queensland, St Lucia, 4072, QLD, Australia
Karen M. Moritz*
Affiliation:
School of Biomedical Sciences, The University of Queensland, St Lucia, 4072, QLD, Australia Child Health Research Centre, The University of Queensland, South Brisbane, QLD4101, Australia
*
Address for correspondence: Professor Karen Moritz, Child Health Research Centre, The University of Queensland, Graham Street, South Brisbane, QLD4101, Australia. Email: [email protected].
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Abstract

It is well established that high-dose alcohol consumption during pregnancy increases the risk for a plethora of adverse offspring outcomes. These include neurodevelopmental, cognitive and social deficits, as well as psychiatric illnesses, such as depression and anxiety. However, much less evidence is available on the effects of low- and early-dose alcohol exposure on mental health outcomes, regardless of the accumulating evidence that mental health outcomes should be considered in the context of the Developmental Origins of Health and Disease hypothesis. This review will discuss the evidence that indicates low-dose and early prenatal alcohol exposure can increase the risk of mental illness in offspring and discuss the mechanistic pathways that may be involved.

Keywords

Foetal alcohol spectrum disorderprenatal alcoholbehavioural disorders
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 11 , Issue 3 , June 2020 , pp. 211 - 221
Copyright
© The Author(s) 2020. Published by Cambridge University Press and the International Society for Developmental Origins of Health and Disease

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References

Barker, DJ, Osmond, C.Diet and coronary heart disease in England and Wales during and after the second world war. J Epidemiol Community Health. 1986; 40, 37–44.CrossRefGoogle ScholarPubMed
Barker, DJ.Intrauterine programming of adult disease. Mol Med Today. 1995; 1, 418–423.CrossRefGoogle ScholarPubMed
Gluckman, PD, Hanson, MA, Beedle, AS.Early life events and their consequences for later disease: a life history and evolutionary perspective. Am J Hum Biol. 2007; 19, 1–19.CrossRefGoogle ScholarPubMed
McMillen, IC, Robinson, JS.Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev. 2005; 85, 571–633.CrossRefGoogle ScholarPubMed
Dorey, ES, Pantaleon, M, Weir, KA, Moritz, KM.Adverse prenatal environment and kidney development: implications for programing of adult disease. Reproduction, 2014; 147, R189–R198.CrossRefGoogle ScholarPubMed
Gluckman, P, Hanson, M.The developmental origins of health and disease : an oveview. In Developmental Origins of Health and Disease (eds. Gluckman, P, Hanson, M), 2006; 1–5. Cambridge University Press, Cambridge.CrossRefGoogle Scholar
Clifton, VL.Sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta. 2010; 31 Suppl, S33–S39.CrossRefGoogle ScholarPubMed
Sundrani, DP, Roy, SS, Jadhav, AT, Joshi, SR.Sex-specific differences and developmental programming for diseases in later life. Reprod Fertil Dev. 2017; 29, 2085–2099.CrossRefGoogle ScholarPubMed
Warner, MJ, Ozanne, SE.Mechanisms involved in the developmental programming of adulthood disease. Biochem J. 2010; 427, 3333–3470.CrossRefGoogle ScholarPubMed
Langley-Evans, SC.Developmental programming of health and disease. Proc Nutr Soc. 2006; 65, 97–105.CrossRefGoogle ScholarPubMed
O’Donnell, KJ, Meaney, MJ.Fetal origins of mental health: the Developmental Origins of Health and Disease Hypothesis. Am J Psychiatry. 2017; 174, 319–328.CrossRefGoogle ScholarPubMed
Breslau, N, Chilcoat, HD.Psychiatric sequelae of low birth weight at 11 years of age. Biol Psychiatry. 2000; 47, 1005–1011.CrossRefGoogle ScholarPubMed
Wiles, NJ, Peters, TJ, Heron, J, et al.Fetal growth and childhood behavioral problems: results from the ALSPAC cohort. Am J Epidemiol. 2006; 163, 829–837.CrossRefGoogle ScholarPubMed
Sucksdorff, M, Lehtonen, L, Chudal, R, et al.Preterm birth and poor fetal growth as risk factors of attention-deficit/ hyperactivity disorder. Pediatrics. 2015; 136, e599–608.CrossRefGoogle ScholarPubMed
Aizer, A, Currie, J.The intergenerational transmission of inequality: maternal disadvantage and health at birth. Science. 2014; 344, 856–861.CrossRefGoogle ScholarPubMed
Schlotz, W, Phillips, DIW.Fetal origins of mental health: evidence and mechanisms. Brain Behav Immun. 2009; 23, 905–916.CrossRefGoogle Scholar
Räikkönen, K, Pesonen, AK, RoseboomTJ,. TJ,.Eriksson, JG.Early determinants of mental health. Best Pract Res Clin Endocrinol Metab. 2012; 599–611.CrossRefGoogle ScholarPubMed
Costello, EJ, Worthman, C, Erkanli, A, Angold, A.Prediction from low birth weight to female adolescent depression. Arch Gen Psychiatry. 2007; 64, 338–344.CrossRefGoogle ScholarPubMed
Abel, KM, Wicks, S, Susser, ES.Birth weight, schizophrenia, and adult mental disorder. Arch Gen Psychiatry. 2010; 67, 923–930.CrossRefGoogle ScholarPubMed
O’Connor, TG, Heron, J, Golding, J, Beveridge, M, Glover, V.Maternal antenatal anxiety and children’s behavioural/emotional problems at 4 years. Report from the Avon Longitudinal Study of Parents and Children. Br J Psychiatry. 2002; 180, 502–508.CrossRefGoogle ScholarPubMed
Kleinhaus, K, Harlap, S, Perrin, M, et al.Prenatal stress and affective disorders in a population birth cohor. Bipolar Disord. 2013; 15, 92–99.CrossRefGoogle Scholar
Rouse, MH & Goodman, SH.Perinatal depression influences on infant negative affectivity: riming, severity, and co-morbid anxiety. Infant Behav Dev. 2014; 37, 739–751.CrossRefGoogle Scholar
Khashan, AS, Abel, KM, McNamee, R, et al.Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry. 2008; 65, 146–152.CrossRefGoogle ScholarPubMed
O’Connor, TG, Heron, J, Golding, J, et al.Maternal antenatal anxiety and behavioural/emotional problems in children: a test of a programming hypothesis. J Child Psychol Psychiatry. 2003; 44, 1025–1036.CrossRefGoogle ScholarPubMed
Van Os, J, Selten, JP.Prenatal exposure to maternal stress and subsequent schizophrenia. The May 1940 invasion of The Netherlands. Br J Psychiatry. 1998; 172, 324–326.CrossRefGoogle ScholarPubMed
Hentges, RF, Graham, SA, Plamondon, A, Tough, S, Madigan, SA.Developmental cascade from prenatal stress to child internalizing and externalizing problems. J Pediatr Psychol. 2019; [Epub ahead of print].CrossRefGoogle ScholarPubMed
Van den Bergh, BRH, Van den Heuvel, MI, Lahti, M, et al.Prenatal developmental origins of behavior and mental health: the influence of maternal stress in pregnancy. Neurosci Biobehav Rev. 2017; 16, 1–39.Google Scholar
Rodriguez, A, Bohlin, G.Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiatry. 2005; 46, 246–254.CrossRefGoogle ScholarPubMed
Huizink, AC, de Rooij, SR.Prenatal stress and models explaining risk for psychopathology revisited: generic vulnerability and divergent pathways. Dev Psychopathol. 2018; 30, 1041–1062.CrossRefGoogle ScholarPubMed
Diego, MA, Field, T, Hernandez-Reif, M, Al, E. Prepartum, postpartum, and chronic depression effects on newborns. Psychiatry. 2004; 67, 63–80.CrossRefGoogle ScholarPubMed
Van den Bergh, BRH, Dahnke, R, Mennes, M.Prenatal stress and the developing brain: risks for neurodevelopmental disorders. Dev Psychopathol. 2018; 30, 743–762.CrossRefGoogle ScholarPubMed
Bergman, K, Sarkar, P, O’Connor, TG, et al.Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. J Am Acad Child Adolesc Psychiatry. 2007; 46, 1454–1463.CrossRefGoogle ScholarPubMed
Clark, CAC, Espy, KA, Wakschlag, L.Developmental pathways from prenatal tobacco and stress exposure to behavioral disinhibition. Neurotoxicol Teratol. 2016; 53, 64–74.CrossRefGoogle ScholarPubMed
Gutteling, BM, de Weerth, C, Willemsen-Swinkels, SH, et al.The effects of prenatal stress on temperament and problem behavior of 27-month-old toddlers. Eur Child Adolesc Psychiatry. 2005; 14, 41–51.CrossRefGoogle ScholarPubMed
Mennes, M, Stiers, P, Lagae, L, Van den Bergh, B.Long-term cognitive sequelae of antenatal maternal anxiety: involvement of the orbitofrontal cortex. Neurosci Biobehav Rev. 2006; 30, 1078–1086.CrossRefGoogle ScholarPubMed
Laplante, DP, A. Brunet, A, Schmitz, N, et al.Project Ice Storm: prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2-year-old children. J Am Acad Child Adolesc Psychiatry. 2008; 47, 1063–1072.CrossRefGoogle ScholarPubMed
Austin, MP, Hadzi-Pavlovic, D, Leader, L, et al.Maternal trait anxiety, depression and life event stress in pregnancy: relationships with infant temperament. Early Hum Dev. 2005; 82, 183–190.CrossRefGoogle Scholar
Buitelaar, JK, Huizink, AC, Mulder, EJ, et al.Prenatal stress and cognitive development and temperament in infants. Neurobiol Aging. 2003; 24, S53–S60.CrossRefGoogle ScholarPubMed
Goel, N, Bale, TL.Examining the intersection of sex and stress in modelling neuropsychiatric disorders. J Neuroendocrinol. 2009; 21, 415–420.CrossRefGoogle ScholarPubMed
Bosquet Enlow, M, Devick, KL, Brunst, KJ, et al.Maternal lifetime trauma exposure, prenatal cortisol, and infant negative affectivity. Infancy. 2011; 22, 492–513.CrossRefGoogle Scholar
Rothenberger, SE, Resch, F, Doszpod, N, Moehler, E.Prenatal stress and infant affective reactivity at five months of age. Early Hum Dev. 2011; 87, 129–136.CrossRefGoogle ScholarPubMed
Brown, AS, Deicken, RF, Vinogradov, S, et al.Prenatal infection and cavum septum pellucidum in adult schizophrenia. Schizophr Res. 2009; 108, 285–287.CrossRefGoogle ScholarPubMed
Bale, TL.Neuroendocrine and immune influences on the cns: it’s a matter of sex. Neuron. 2009; 64, 13–16.CrossRefGoogle Scholar
Buka, SL, Tsuang, MT, Torrey, EF, Klebanoff, MA, Bernstein, DYR.Maternal infections and subsequent psychosis among offspring. M Arch Gen Psychiatry. 2001; 58, 1032–1037.CrossRefGoogle ScholarPubMed
Brown, AS, Vinogradov, S, Kremen, WS, et al.Prenatal exposure to maternal infection and executive dysfunction in adult schizophrenia. Am J Psychiatry. 2009; 166, 683–690.CrossRefGoogle ScholarPubMed
Van Os, J, Jones, P, Lewis, G, Wadsworth, M, Murray, R.Developmental precursors of affective illness in a general population birth cohort. Arch Gen Psychiatry. 1997; 54, 625–632.CrossRefGoogle Scholar
Van Os, J, Jones, PB.Early risk factors and adult person–environment relationships in affective disorder. Psychol Med. 1999; 29, 1055–1067.CrossRefGoogle ScholarPubMed
Machón, RA, Mednick, SA, Huttunen, MO.Adult major affective disorder after prenatal exposure to an influenza epidemic. Arch Gen Psychiatry. 1997; 54, 322–329.CrossRefGoogle Scholar
Cannon, TD, Van Erp, TG, Russo, IM, et al.Fetal hypoxia and structural brain abnormalities in schizophrenic patients, their siblings, and controls. Arch Gen Psychiatry. 2002; 59, 35–41.CrossRefGoogle ScholarPubMed
Zornberg, GL.Hypoxic-ischemia-related fetal/neonatal complications and risk of schizophrenia and other nonaffective psychoses: a 19-year longitudinal study. Am J Psychiatry. 2000; 157, 196–202.CrossRefGoogle ScholarPubMed
Brown, AS.Further evidence of relation between prenatal famine and major affective disorder. Am J Psychiatry. 2000; 157, 190–195.CrossRefGoogle ScholarPubMed
Brown, AS, Susser, ES, Lin, SP, Neugebauer, R, Gorman, JM.Increased risk of affective disorders in males after second trimester prenatal exposure to the Dutch hunger winter of 1944-45. Br J Psychiatry. 1995; 166, 601–606.CrossRefGoogle ScholarPubMed
Xu, MQ, Sun, WS, Liu, BX, et al.Prenatal malnutrition and adult schizophrenia: further evidence from the 1959-1961 Chinese Famine. Schizophr Bull. 2009; 35, 568–576.CrossRefGoogle ScholarPubMed
Brown, AS, Susser, ES.Prenatal nutritional deficiency and risk of adult schizophrenia. Schizophr Bull. 2008; 34, 1054–1063.CrossRefGoogle ScholarPubMed
Hoek, HW, Brown, AS, Susser, E.The Dutch famine and schizophrenia spectrum disorders. Soc Psychiatr Epidemiol. 1988; 33, 373–379.CrossRefGoogle Scholar
Davis, EP, Snidman, N, Wadhwa, PD, et al.Prenatal maternal anxiety and depression predict negative behavioral reactivity in infancy. Infancy. 2004; 6, 319–331.CrossRefGoogle Scholar
Sohr-Preston, SL, Scaramella, LV.Implications of timing of maternal depressive symptoms for early cognitive and language development. Clin Child Fam Psychol Rev. 2006; 9, 65–83.CrossRefGoogle ScholarPubMed
Plant, DT, Pariante, CM, Sharp, D, Pawlby, S.Maternal depression during pregnancy and offspring depression in adulthood: role of child maltreatment. Br J Psychiatry. 2015; 207, 213–220.10.1192/bjp.bp.114.156620CrossRefGoogle ScholarPubMed
Luoma, I, Tamminen, T, Kaukonen, P, et al.Longitudinal study of maternal depressive symptoms and child well-being. J Am Acad Child Adolesc Psychiatry. 2001; 40, 1367–1374.CrossRefGoogle ScholarPubMed
Godleski, SA, Eiden, RD, Schuetze, P, Colder, CR, Huestis, MA.Tobacco exposure and maternal psychopathology: impact on toddler problem behavior. Neurotoxicol Teratol. 2016; 57, 87–94.CrossRefGoogle ScholarPubMed
Scott, JG, Matuschla, L, Niemela, S, et al.Evidence of a causal relationship between smoking tobacco and schizophrenia spectrum disorders. Front Psychiatry. 2018; 9, 607–616.CrossRefGoogle ScholarPubMed
Keyes, KM, Davey Smith, G, Susser, E.Associations of prenatal maternal smoking with offspring hyperactivity: causal or confounded? Psychol Med. 2014; 44, 857–867.CrossRefGoogle ScholarPubMed
Rodriguez, A.Maternal pre-pregnancy obesity and risk for inattention and negative emotionality in children. J Child Psychol Psychiatry. 2010; 51, 134–143.CrossRefGoogle ScholarPubMed
Van Lieshout, RJ, Robinson, M, Boyle, MH.Maternal pre-pregnancy body mass index and internalizing and externalizing problems in offspring. Can J Psychiatry. 2013; 58, 151–159.CrossRefGoogle ScholarPubMed
Buss Entringer, S, Davis, EP, et al.Impaired executive function mediates the association between maternal pre-pregnancy body mass index and child adhd symptoms. PLoS One. 2012; 7, e37758–e37766.CrossRefGoogle Scholar
Krakowiak, P, Walker, CK, Bremer, AA, et al.Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders. Pediatrics. 2012; 129, e1121–1128.CrossRefGoogle ScholarPubMed
Reynolds, LC, Inder, TE, Neil, JJ, et al.Maternal obesity and increased risk for autism and developmental delay among very preterm infants. J Perinatol. 2014; 34, 688–692.CrossRefGoogle ScholarPubMed
Moss, BG, Chugani, DC.Increased risk of very low birth weight, rapid postnatal growth, and autism in underweight and obese mothers. Am J Hea Promot. 2014; 28, 181–188.CrossRefGoogle ScholarPubMed
Dodds, L, Fell, DB, Shea, S, et al.The role of prenatal, obstetric and neonatal factors in the development of autism. J Autism Dev Disord. 2011; 41, 891–902.CrossRefGoogle ScholarPubMed
Contu, L & Hawkes, CA.A review of the impact of maternal obesity on the cognitive function and mental health of the offspring. Int J Mol Sci. 2017; 18, 1–11.Google ScholarPubMed
Bilder, DA, Bakian, AV, Viskochil, J, et al.Maternal prenatal weight gain and autism spectrum disorders. Pediatrics. 2013; 132, e1276–1283.CrossRefGoogle ScholarPubMed
Hinkle, SN, Schieve, LA, Stein, AD, et al.Associations between maternal prepregnancy body mass index and child neurodevelopment at 2 years of age. Int J Obes (Lond). 2012; 36, 1312–1319.CrossRefGoogle ScholarPubMed
Tanda, R, Salsberry, PJ, Reagan, PB, Fang, MZ.The impact of prepregnancy obesity on children’s cognitive test scores. Matern Child Health J. 2013; 17, 222–229.CrossRefGoogle ScholarPubMed
Neggers, YH, Goldenberg, RL, Ramey, SL, Cliver, SP.Maternal prepregnancy body mass index and psychomotor development in children. Acta Obstet Gynecol Scand. 2003; 82, 235–240.CrossRefGoogle ScholarPubMed
Jones, PB, Rantakallio, P, Hartikainen, AL, Isohanni, M, Sipila, P.Schizophrenia as a long-term outcome of pregnancy, delivery, and perinatal complications: a 28-year follow-up of the 1966 north finland general population birth cohort. Am J Psychiatry. 1998; 155, 355–364.CrossRefGoogle ScholarPubMed
Colman, I, Ataullahjan, A, Naicker, K, Van Lieshout, RJ.Birth weight, stress, and symptoms of depression in adolescence: evidence of fetal programming in a national canadian cohort. Can J Psychiatry. 2012; 57, 422–428.CrossRefGoogle Scholar
Rodriguez, A, Miettunen, J, Henriksen, TB, et al.Maternal adiposity prior to pregnancy is associated with ADHD symptoms in offspring: evidence from three prospective pregnancy cohorts. Int J Obes. 2008; 32, 550–557.CrossRefGoogle ScholarPubMed
Chen, Q, Sjolander, A, Langstrom, N.et al.Maternal pre-pregnancy body mass index and offspring attention deficit hyperactivity disorder: a population-based cohort study using a sibling-comparison design. Int Epidemiol. 2014; 43, 83–90.CrossRefGoogle ScholarPubMed
Kawai, M, Minabe, T, Takagai, S, et al.Poor maternal care and high maternal body mass index in pregnancy as a risk factor for schizophrenia in offspring. Acta Psychiatr Scand. 2004; 110, 257–263CrossRefGoogle ScholarPubMed
Nomura, Y, Marks, DJ, Grossman, B, et al.Exposure to Gestational Diabetes Mellitus and low socioeconomic status. Arch Pediatr Adolesc Med. 2012; 166, 337–343.Google ScholarPubMed
Yamada, L, Chong, S.Epigenetic studies in Developmental Origins of Health and Disease: pitfalls and key considerations for study design and interpretation. J Dev Orig Health Dis. 2016; 8, 30–43.CrossRefGoogle ScholarPubMed
Popova, S, Lange, S, Shield, K, et al.Comorbidity of fetal alcohol spectrum disorder: a systematic review and meta-analysis. Lancet. 2016; 387, 978–987.CrossRefGoogle ScholarPubMed
Bower, C, Elliott, E.Report to the Australian Government Department of Health: “Australian guide to the diagnosis of Fetal Alcohol Spectrum Disorder (FASD)”. (2016).Google Scholar
May, PA, Chambers, CD, Kalberg, WO.Prevalence of fetal alcohol spectrum disorders in 4 us communities. JAMA. 2018; 319, 474–482.CrossRefGoogle ScholarPubMed
Shelton, D, Reid, N, Till, H, Butel, F, Moritz, K.Responding to fetal alcohol spectrum disorder in Australia. J Paediatr Child Health. 2018; 54, 1121–1126.CrossRefGoogle ScholarPubMed
Fitzpatrick, JP, Latimer, J, Olson, HS, et al.Prevalence and profile of neurodevelopment and fetal alcohol spectrum disorder (FASD) amongst Australian Aboriginal children living in remote communities. Res Dev Disabil. 2017; 65, 114–126.CrossRefGoogle ScholarPubMed
Jones, K, Smith, D.Recognition of the fetal alcohol syndrome in early infancy. Lancet. 1973; 302, 999–1001.CrossRefGoogle ScholarPubMed
Jones, KL, Smith, DW, Ulleland, CN, Streissguth, P.Pattern of malformation in offspring of chronic alcoholic mothers. Lancet. 1973; 1, 1267–1271.CrossRefGoogle ScholarPubMed
Jones, KL, Smith, DW, Hanson, JW.The Fetal Alcohol Syndrome: clincal delineation. Ann N Y Acad Sci. 1976; 273, 130–137.CrossRefGoogle Scholar
Riley, E, Infante, MA, Warren, K.Fetal Alcohol Spectrum Disorders: an overview. Neuropsychol Rev. 2011; 21, 73–80.CrossRefGoogle ScholarPubMed
Streissguth, A, Barr, H, Kogan, J. Understanding the occurrence of secondary disabilities in clients with Fetal Alcohol Syndrome (FAS) and Fetal Alcohol Effects (FAE): Final report: University of Washington School of Medicine, Department of Psychiatry and Behavioral Sciences, Fetal Alcohol and Drug Unit, 1996.Google Scholar
Ipsiroglu, OS, Wind, K, Hung, YA, Berger, M, et al.Prenatal alcohol exposure and sleep-wake behaviors: exploratory and naturalistic observations in the clinical setting and in an animal model. Sleep Med. 2018; 54, 101–112.CrossRefGoogle ScholarPubMed
O’Connor, MJ, Shah, B, Whaley, S, et al.Psychiatric illness in a clinical sample of children with prenatal alcohol exposure. Am J Drug Alcohol Abuse. 2002; 28, 743–754.CrossRefGoogle Scholar
Niclasen, J, Andersen, AMN, Strandberg-Larsen, K, Teasdale, TW.Is alcohol binge drinking in early and late pregnancy associated with behavioural and emotional development at age 7 years? Eur Child Adolesc Psychiatry. 2014; 23, 1175–1180.CrossRefGoogle ScholarPubMed
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, 711–718.CrossRefGoogle ScholarPubMed
Schonfeld, AM, Paley, B, Frankel, F, O’Connor, MJ.Executive functioning predicts social skills following prenatal alcohol exposure. Child Neuropsychol. 2006; 12, 439–452.CrossRefGoogle ScholarPubMed
Bailey, BN, Delaney-Black, V, Convington, CY, et al.Prenatal exposure to binge drinking and cognitive and behavioral outcomes at age 7 years. Am J Obstet Gynecol. 2004; 191, 1037–1043.CrossRefGoogle ScholarPubMed
Jacobson, JL, Jacobson, SW, Sokol, RJ, Ager, JW.Relation of maternal age and pattern of pregnancy drinking to functionally significant cognitive deficit in infancy. Alcohol Clin Exp Res. 1998; 22, 345–51.CrossRefGoogle ScholarPubMed
Streissguth, AP, Barr, HM, Sampson, PD.Moderate prenatal alcohol exposure: effects on child IQ and learning problems at age 7 1/2 years. Alcohol Clin Exp Res. 1990; 14, 662–669.CrossRefGoogle ScholarPubMed
Barr, HM, Bookstein, FL, O’Malley, KD, et al.Binge drinking during pregnancy as a predictor of psychiatric disorders on the structured clinical interview for dsm-iv in young adult offspring. Am J Psychiatry. 2006; 163, 1061–1065.CrossRefGoogle ScholarPubMed
Sayal, K, Heron, J, Golding, J, et al.Binge pattern of alcohol consumption during pregnancy and childhood mental health outcomes: longitudinal population-based study. Pediatrics. 2009; 123, e289–e296.CrossRefGoogle ScholarPubMed
Sayal, K, Heron, J, Golding, J, Emond, A.Prenatal alcohol exposure and gender differences in childhood mental health problems: a longitudinal population-based study. Pediatrics. 2007; 119, e426–e434.CrossRefGoogle ScholarPubMed
O’Connor, MJ, Kasari, C.Prenatal alcohol exposure and depressive features in children. Alcohol Clin Exp Res. 2000; 24, 1084–1092.CrossRefGoogle ScholarPubMed
Niclasen, J, Nybo Andersen, AM, Teasdale, TW, Strandberg-Larsen, K.Prenatal exposure to alcohol, and gender differences on child mental health at age seven years. J Epidemiol Community Health. 2014; 68, 224–232.CrossRefGoogle ScholarPubMed
Alvik, A, Torgersen, AM, Aalen, OO, Lindemann, R.Binge alcohol exposure once a week in early pregnancy predicts temperament and sleeping problems in the infant. Early Hum Dev. 2011; 87, 827–833.CrossRefGoogle ScholarPubMed
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, 1954–1962.CrossRefGoogle ScholarPubMed
Nulman, I, Rovet, J, Kennedy, D, et al.Binge alcohol consumption by non-alcohol dependent women during pregnancy affects child behaviour, but not general intellectual functioning; a prospective controlled study. Arch Women’s Ment Heal. 2004; 7, 173–81.Google Scholar
Goldschmidt, L, Richardson, G A, De Genna, N M, Day, Cornelius MDNL. Prenatal alcohol exposure and offspring alcohol use and misuse at 22 years of age: a prospective longitudinal study. Neurotoxicol Teratol. 2019; 71, 1–5.CrossRefGoogle Scholar
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, 1171–1178.CrossRefGoogle ScholarPubMed
Richter, L, Richter, DM.Exposure to parental tobacco and alcohol use: effects on children’s health and development. Am J Orthopsychiarty. 2001; 71, 182–203.CrossRefGoogle ScholarPubMed
Kelly, Y, Sacker, A, Gray, R, et al.Light drinking in pregnancy, a risk for behavioural problems and cognitive deficits at 3 years of age? Int J Epidemiol. 2009; 38, 129–140.CrossRefGoogle ScholarPubMed
Larkby, CA, Goldschmidt, L, Hanusa, BH, Day, NL.Prenatal alcohol exposure is associated with conduct disorder in adolescence: findings from a birth cohort. J Am Acad Child Adolesc Psychiatry 2011; 50, 262–271.CrossRefGoogle ScholarPubMed
Stockard, CR, Craig, DM.An experimental study of the influence of alcohol on the germ cells and the developing embryos of mammals. Archiv für Entwicklungsmechanik der Organismen. 1912; 35, 569–584.CrossRefGoogle Scholar
Stockard, CR.The influence of alcohol and other anaesthetics on embryonic development. Am J Anat. 1910; 10, 369–392.CrossRefGoogle Scholar
Brocardo, PS, Boehme, F, Patten, A, et al.Anxiety- and depression-like behaviors are accompanied by an increase in oxidative stress in a rat model of fetal alcohol spectrum disorders: protective effects of voluntary physical exercise. Neuropharmacology. 2012; 62, 1607–1618.CrossRefGoogle Scholar
Wieczorek, L, Fish, EW, O’Leary-Moore, SK, Parnell, SE, Sulik, KK.Hypothalamic-pituitary-adrenal axis and behavioral dysfunction following early binge-like prenatal alcohol exposure in mice. Alcohol. 2015; 49, 207–217.CrossRefGoogle ScholarPubMed
Weinberg, J.Effects of ethanol and maternal nutritional status on fetal development. Alcohol Clin Exp Res. 1985; 9, 49–55.CrossRefGoogle ScholarPubMed
Hellemans, KGC, Sliwowska, JH, Verma, P, Weinberg, J.Prenatal alcohol exposure: fetal programming and later life vulnerability to stress, depression and anxiety disorders. Neurosci Biobehav Rev. 2010; 34, 791–807.CrossRefGoogle Scholar
Weinberg, J, Sliwowska, JH, Lan, N, Hellemans, KGC.Prenatal Alcohol Exposure: foetal programming, the Hypothalamic-Pituitary-Adrenal Axis and sex differences in outcome. J Neuroendocrinol. 2008; 20, 470–488.CrossRefGoogle ScholarPubMed
Brancato, A, Castelli, V, Cavallaro, A, Lavanco, A, et al.Pre-conceptional and peri-gestational maternal binge alcohol drinking produces inheritance of mood disturbances and alcohol vulnerability in the adolescent offspring. Front Psychiatry. 2018; 9, 150–163.CrossRefGoogle ScholarPubMed
Hellemans, KGC, Verma, P, Yoon, E, et al.Prenatal alcohol exposure and chronic mild stress differentially alter depressive- and anxiety-like behaviors in male and female offspring. Alcohol Clin Exp Res. 2010; 34, 633–645.CrossRefGoogle ScholarPubMed
Holman, PJ, Ellis, L, Morgan, E, Weinberg, J.Prenatal alcohol exposure disrupts male adolescent social behavior and oxytocin receptor binding in rodents. Horm Behav. 2018; 105, 115–127.CrossRefGoogle ScholarPubMed
Holman, PJ, Baglot, SL, Morgan, E, Weinberg, J.Effects of prenatal alcohol exposure on social competence: asymmetry in play partner preference among heterogeneous triads of male and female rats. Dev Psychobiol. 2019; 61, 513–524.CrossRefGoogle ScholarPubMed
Mooney, SM, Varlinskaya, EI.Acute prenatal exposure to ethanol and social behavior: effects of age, sex, and timing of exposure. Behav Brain Res. 2011; 216, 358–364.CrossRefGoogle ScholarPubMed
Lucia, D, Burgess, DJ, Cullen, CL, et al.Periconceptional maternal alcohol consumption leads to behavioural changes in adult and aged offspring and alters the expression of hippocampal genes associated with learning and memory and regulators of the epigenome. Behav Brain Res. 2019; 362, 249–257.CrossRefGoogle ScholarPubMed
Cullen, CL, Burne, THJ, Lavidis, NA, Moritz, KM.Low dose prenatal ethanol exposure induces anxiety-like behaviour and alters dendritic morphology in the basolateral amygdala of rat offspring. PLoS One. 2013; 8, e54924–e54936.CrossRefGoogle ScholarPubMed
Hamilton, DA, Akers, KG, Rice, JP, et al.Prenatal exposure to moderate levels of ethanol alters social behavior in adult rats: relationship to structural plasticity and immediate early gene expression in frontal cortex. Behah Brain Res. 2010; 207, 290–304.CrossRefGoogle ScholarPubMed
Catlin, MC, Abdollah, S, Brien, JF.Dose-dependent effects of prenatal alcohol exposure in the guinea pig. Alcohol. 1993; 10, 109–115.CrossRefGoogle ScholarPubMed
Shea, KM, Hewitt, AJ, Olmstead, MC, Brien, JF, Reynolds, JN.Maternal ethanol consumption by pregnant guinea pigs causes neurobehavioral deficits and increases ethanol preference in offspring. Behav Pharmacol. 2012; 23, 105–112CrossRefGoogle ScholarPubMed
Bond, NW, Di Giusto, EL.Effects of prenatal alcohol consumption open-field behaviour and alcohol preference. Psychopharmacologia. 1976; 46, 163–165.CrossRefGoogle ScholarPubMed
Meyer, LS, Riley, EP.Social play in juvenile rats prenatally exposed to alcohol. Teratology. 1986; 34, 1–7.CrossRefGoogle Scholar
Olson, HC, Feldman, JJ, Streissguth, AP, Sampson, PD, Bookstein, FL.Neuropsychological deficits in adolescents with Fetal Alcohol Syndrome: clinical findings. Alcohol Clin Exp Res. 1998; 22, 1998–2012.Google ScholarPubMed
Pittenger, C, Duman, RS. Stress, depression and neuroplasticity: a convergence of mechanisms. Neuropsychopharmacology. 2008; 33, 88–109.CrossRefGoogle Scholar
Clarren, SK, Alvord, EC, Sumi, SM, Streissguth, AP, Smith, DW.Brain malformations related to prenatal exposure to ethanol. J Pediatr. 1978; 92, 64–67.CrossRefGoogle ScholarPubMed
Autti-Rämö, I, Autti, T, Korkman, M, et al.MRI findings in children with school problems who had been exposed prenatally to alcohol. Dev Med Child Neurol. 2002; 44, 98–106.CrossRefGoogle Scholar
Clarren, SK.Neuropathology in fetal alcohol syndrome. In: West, JR ed. Alcohol and Brain Development. New York, NY: Oxford University Press. 1986; 158–166.Google Scholar
Ramsay, DS, Bendersky, MI, Lewis, M.Effect of prenatal alcohol and cigarette exposure on two- and six-month-old infants’ adrenocortical reactivity to stress. J Pediatr Psychol. 1996; 21, 833–840.CrossRefGoogle ScholarPubMed
Ouellet-Morin, I, Dionne, G, Lupien, SJ, et al.Prenatal alcohol exposure and cortisol activity in 19-month-old toddlers: an investigation of the moderating effects of sex and testosterone. Psychopharmacology (Berl). 2011; 214, 297–307.CrossRefGoogle ScholarPubMed
Jacobson, SW, Bihun, JT, Chiodo, LM.Effects of prenatal alcohol and cocaine exposure on infant cortisol levels. Dev Psychopathol. 1999; 11, 195–208.CrossRefGoogle ScholarPubMed
Haley, DW, Handmaker, NS, Lowe, J.Infant stress reactivity and prenatal alcohol exposure. Alcohol Clin Exp Res. 2006; 30, 2055–2064CrossRefGoogle ScholarPubMed
Bonthius, DJ, West, JR.Acute and long-term neuronal deficits in the rat olfactory bulb following alcohol exposure during the brain growth spurt. Neurotoxicol Teratol. 1991; 13, 611–619.CrossRefGoogle ScholarPubMed
Goodlett, CR, Eilers, AT.Alcohol-induced Purkinje cell loss with a single binge exposure in neonatal rats: a stereological study of temporal windows of vulnerability. Alcohol Clin Exp Res. 1997; 21, 738–744.Google ScholarPubMed
Ikonomidou, C, Bittigau, P, Ishimaru, MJ, et al.Ethanol-induced apoptotic neurodegeneration and fetal alcohol syndrome. Science. 2000; 287, 1056–1060.CrossRefGoogle ScholarPubMed
Cartwright, MM, Smith, SM.Stage-dependent effects of ethanol on cranial neural crest cell development: partial basis for the phenotypic variations observed in fetal alcohol syndrome. Alcohol Clin Exp Res. 1995; 19, 1454–1462.CrossRefGoogle ScholarPubMed
Gabriel, KI, Yu, W, Ellis, L, Weinberg, J.Postnatal handling does not attenuate Hypothalamic-Pituitary-Adrenal hyperresponsiveness after prenatal ethanol exposure. Alcohol Clin Exp Res. 2000; 24, 1566–1574.CrossRefGoogle Scholar
Glavas, M, Ellis, L, Yu, WK, Weinberg, J.Effects of prenatal ethanol exposure on basal limbic-hypothalamic-pituitary-adrenal regulation: role of corticosterone. Alcohol Clin Exp Res. 2007; 31, 1598–1610.CrossRefGoogle ScholarPubMed
Burgess, D. J.et al.Periconceptional ethanol exposure alters the stress axis in adult female but not male rat offspring. Stress. 2019; 1–11. doi:10.1080/10253890.2018.1563068Google Scholar
Kakihana, R, Butte, JC, Moore, JA.Endocrine effects of maternal alcoholization: plasma and brain testosterone, dihydrotestosterone, estradiol, and corticosterone. Alcohol Clin Exp Res. 1980; 4, 57–61.CrossRefGoogle ScholarPubMed
Aird, F, Halasz, I, Redei, E.Ontogeny of hypothalamic corticotropin-releasing factor and anterior pituitary pro-opiomelanocortin expression in male and female offspring of alcohol-exposed and adrenalectomized dams. Alcohol Clin Exp Res. 1997; 21, 1560–1566.CrossRefGoogle ScholarPubMed
Lam, VYY, Raineki, C, Ellis, L, Yu, W, Weinberg, J.Interactive effects of prenatal alcohol exposure and chronic stress in adulthood on anxiety-like behavior and central stress-related receptor mRNA expression: sex- and time-dependent effects. Psychoneuroendocrinology. 2018; 97, 8–19.CrossRefGoogle ScholarPubMed
Dorey, ES, Cullen, CL, Lucia, D, et al.The impact of periconceptional alcohol exposure on fat preference and gene expression in the mesolimbic reward pathway in adult rat offspring. J Dev Orig Health Dis. 2018; 9, 223–231.CrossRefGoogle ScholarPubMed
Ramadoss, J, Lunde, ER, Piña, KB, Chen, WA, Cudd, TA.All three trimester binge alcohol exposure causes fetal Cerebellar Purkinje cell loss in the presence of maternal hypercapnea, acidemia, and normoxemia: ovine model. Alcohol Clin Exp Res. 2007; 31, 1252–1258.CrossRefGoogle ScholarPubMed
Washburn, SE, Ramadoss, J, Chen, WA, Cudd, TA.Effects of all three trimester moderate binge alcohol exposure on the foetal hippocampal formation and olfactory bulb. Brain Inj. 2015; 29, 104–109.CrossRefGoogle ScholarPubMed
Cudd, TA, Chen, WA, West, JR.Fetal and maternal sheep hypothalamus pituitary adrenal axis responses to chronic binge ethanol exposure during the third trimester equivalent. Alcohol Clin Exp Res. 2001; 25, 1065–1071CrossRefGoogle ScholarPubMed
Liu, Y, Balaraman, Y, Wang, G, Nephew, KP, Zhou, FC.Alcohol exposure alters DNA methylation profiles in mouse embryos at early neurulation. Epigenetics. 2009; 4, 500–511.CrossRefGoogle ScholarPubMed
Haycock, PC, Ramsay, M.Exposure of mouse embryos to ethanol during preimplantation development: effect on dna methylation in the h19 imprinting control region. Biol Reprod. 2009; 81, 618–627.CrossRefGoogle ScholarPubMed
Kalisch-Smith, JI, Steane, SE, Simmons, DG, et al.Periconceptional alcohol exposure causes female-specific perturbations to trophoblast differentiation and placental formation in the rat. Development. 2019; 146, [Epub ahead of print].CrossRefGoogle ScholarPubMed
Chen, Y, Ozturk, NC, Zhou, FC.DNA methylation program in developing hippocampus and its alteration by alcohol. PLoS One 2013; 8, e60503–e605514.CrossRefGoogle Scholar
Otero, NKH, Thomas, JD, Saski, CA, Xia, X, Kelly, SJ.Choline supplementation and dna methylation in the hippocampus and prefrontal cortex of rats exposed to alcohol during development. Alcohol Clin Exp Res. 2012; 36, 1701–1709.CrossRefGoogle ScholarPubMed
Gangisetty, O, Bekdash, R, Maglakelidze, G, Sarkar, DK.Fetal alcohol exposure alters proopiomelanocortin gene expression and hypothalamic-pituitary-adrenal axis function via increasing MeCP2 expression in the hypothalamus. PLoS One. 2014; 9, e113228–e11337.CrossRefGoogle ScholarPubMed
Ngai, YF, Sulistyoningrum, DC, O’Neill, R, et al.Prenatal alcohol exposure alters methyl metabolism and programs serotonin transporter and glucocorticoid receptor expression in brain. Am J Physiol – Regul Integr Comp Physiol. 2015; 309, R613–R622.CrossRefGoogle ScholarPubMed
Hill, SY, Lowers, L, Locke-Wellman, J, Shen, SA.Maternal smoking and drinking during pregnancy and the risk for child and adolescent psychiatric disorders. J Stud Alcohol. 2000; 61, 661–668.CrossRefGoogle ScholarPubMed
Abel, EL.An update on incidence of FAS: FAS is not an equal opportunity birth defect. Neurotoxicol Teratol. 1195; 17, 437–443.CrossRefGoogle Scholar
Skagerstróm, J, Chang, G, Nilsen, P.Predictors of drinking during pregnancy: a systematic review. J Women’s Heal. 2011; 20, 901–913.CrossRefGoogle ScholarPubMed
O’Leary, CM, Nassar, N, Zubrick, SR, et al.Evidence of a complex association between dose, pattern and timing of prenatal alcohol exposure and child behaviour problems. Addiction. 2010; 105, 74–86.CrossRefGoogle ScholarPubMed
Milton, AL & Holmes, EA.Of mice and mental health: facilitating dialogue and seeing further. Philos Trans R Soc B Biol Sci. 2018; 373, 20170022–20170028.CrossRefGoogle Scholar
National Health and Medical Research Council. Australian guidelines to reduce health risks from drinking alcohol. Canberra National Health and Medical Research Council. (2009).Google Scholar
Tan, CH, Denny, CH, Cheal, N, Sniezek, EJ, Kanny, D.Alcohol use and binge drinking among women of childbearing age--United States, 2011/2013. Morb Mortal Wkly Rep. 2015; 64, 1042–1046.CrossRefGoogle ScholarPubMed
Payne, J, Elliott, E, D’Antoine, H, et al.Health professionals’ knowledge, practice and opinions about fetal alcohol syndrome and alcohol consumption in pregnancy. Aust NZ J Public Health. 2005; 29, 558–564.CrossRefGoogle ScholarPubMed
Colvin, L, Payne, J, Parsons, D, Kurinczuk, JJ, Bower, C.Alcohol consumption during pregnancy in nonindigenous west Australian women. Alcohol Clin Exp Res. 2007; 31, 276–84.CrossRefGoogle ScholarPubMed
Finer, LB, Zolna, MR.Declines in unintended pregnancy in the United States, 2008-2011. N Engl J Med. 2016; 374, 843–852.CrossRefGoogle ScholarPubMed
Hutchinson, D, Youssef, GJ, McCormack, C, et al.Prenatal alcohol exposure and infant gross motor development: a prospective cohort study. BMC Pediatr. 2019; 19, 149–163.CrossRefGoogle ScholarPubMed
Muggli, E, O’Leary, C, Donath, S, et al.“Did you ever drink more?” A detailed description of pregnant women’s drinking patterns. BMC Public Health. 2016; 16, 683–696.CrossRefGoogle ScholarPubMed