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The Association Between Prenatal Stress and Externalizing Symptoms in Childhood: Evidence From the Avon Longitudinal Study of Parents and Children

      Abstract

      Background

      It has been suggested that prenatal maternal stress may increase the risk of childhood externalizing disorders, yet no large cohort study has investigated this association across a large range of acute stressors. Our objective was to estimate the association between prenatal stressful events and risk of offspring conduct disorder and hyperactivity.

      Methods

      We used data from 10,184 mother–offspring pairs from the United Kingdom–based Avon Longitudinal Study of Parents and Children. Mothers self-reported 42 prenatal stressful life events at 18 weeks’ gestation. Symptoms of conduct disorder and hyperactivity in their offspring were measured at 6, 9, 11, 13, and 16 years of age using the Strengths and Difficulties Questionnaire. The primary outcome was membership in high-symptom trajectories of 1) conduct disorder and 2) hyperactivity throughout childhood, identified using latent class growth modeling. Multinomial logistic regression models estimated the association between prenatal stress and both conduct disorder and hyperactivity, after adjusting for sex, parental education, low birth weight, preterm birth, parental social class, maternal smoking and drinking, maternal mental health, offspring stressful life events, and offspring depressive and anxious symptoms.

      Results

      Those exposed to the highest quartile of prenatal stress were more likely to belong to the high symptom trajectory for hyperactivity (B = 0.46, p < .05) and conduct disorder (B = 0.88, p < .01), respectively. Prenatal stress further demonstrated a positive, dose–response relationship with symptoms of externalizing disorders at independent time points.

      Conclusions

      The findings suggest that prenatal stressful events may be an independent risk factor for offspring externalizing symptoms, regardless of maternal mental health and offspring internalizing.

      Keywords

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      References

        • Barker D.J.
        The fetal and infant origins of adult disease.
        BMJ. 1990; 301: 1111
        • Reynolds L.P.
        • Borowicz P.P.
        • Caton J.S.
        • Vonnahme K.A.
        • Luther J.S.
        • Hammer C.J.
        • et al.
        Developmental programming: The concept, large animal models, and the key role of uteroplacental vascular development.
        J Anim Sci. 2010; 88: E61-E72
        • Glover V.
        • O’Connor T.G.
        • O’Donnell K.
        Prenatal stress and the programming of the HPA axis.
        Neurosci Biobehav Rev. 2010; 35: 17-22
        • Mick E.
        • Biederman J.
        • Prince J.
        • Fischer M.J.
        • Faraone S.V.
        Impact of low birth weight on attention-deficit hyperactivity disorder.
        J Dev Behav Pediatr. 2002; 23: 16-22
        • Botting N.
        • Powls A.
        • Cooke R.W.I.
        • Marlow N.
        Attention deficit hyperactivity disorders and other psychiatric outcomes in very low birthweight children at 12 years.
        J Child Psychol Psychiatry. 1997; 38: 931-941
        • Class Q.A.
        • Rickert M.E.
        • Larsson H.
        • Lichtenstein P.
        • D’Onofrio B.M.
        Fetal growth and psychiatric and socioeconomic problems: Population-based sibling comparison.
        Br J Psychiatry. 2014; 205: 355-361
        • Glover V.
        Maternal depression, anxiety and stress during pregnancy and child outcome; What needs to be done.
        Best Pract Res Clin Obstet Gynaecol. 2014; 28: 25-35
        • Morley-Fletcher S.
        • Rea M.
        • Maccari S.
        • Laviola G.
        Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats.
        Eur J Neurosci. 2003; 18: 3367-3374
        • Maccari S.
        • Piazza P.V.
        • Kabbaj M.
        • Barbazanges A.
        • Simon H.
        • Le Moal M.
        Adoption reverses the long-term impairment in glucocorticoid feedback induced by prenatal stress.
        J Neurosci. 1995; 15: 110-116
        • Clarke A.S.
        • Wittwer D.J.
        • Abbott D.H.
        • Schneider M.L.
        Long-term effects of prenatal stress on HPA axis activity in juvenile rhesus monkeys.
        Dev Psychobiol. 1994; 27: 257-269
        • Van Den Bergh B.R.H.
        • Mulder E.J.H.
        • Mennes M.
        • Glover V.
        Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: Links and possible mechanisms. A review.
        Neurosci Biobehav Rev. 2005; 29: 237-258
        • Korhonen M.
        • Luoma I.
        • Salmelin R.
        • Tamminen T.
        Maternal depressive symptoms: Associations with adolescents’ internalizing and externalizing problems and social competence.
        Nord J Psychiatry. 2014; 68: 323-332
        • Van Batenburg-Eddes T.
        • Brion M.J.
        • Henrichs J.
        • Jaddoe V.W.V.
        • Hofman A.
        • Verhulst F.C.
        • et al.
        Parental depressive and anxiety symptoms during pregnancy and attention problems in children: A cross-cohort consistency study.
        J Child Psychol Psychiatry. 2013; 54: 591-600
        • Lahti M.
        • Savolainen K.
        • Tuovinen S.
        • Pesonen A.K.
        • Lahti J.
        • Heinonen K.
        • et al.
        Maternal depressive symptoms during and after pregnancy and psychiatric problems in children.
        J Am Acad Child Adolesc Psychiatry. 2017; 56: 30-39.e7
        • Farmer E.M.Z.
        • Compton S.N.
        • Burns B.J.
        • Robertson E.
        Review of the evidence base for treatment of childhood psychopathology: Externalizing disorders.
        J Consult Clin Psychol. 1998; 70: 1267-1302
        • Liu J.
        Childhood externalizing behavior: Theory and implications.
        J Child Adolesc Psychiatr Nurs. 2004; 17: 93-103
        • Barker E.D.
        • Maughan B.
        Differentiating early-onset persistent versus childhood-limited conduct problem youth.
        Am J Psychiatry. 2009; 166: 900-908
        • Van den Bergh B.R.H.
        • Marcoen A.
        High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8-and 9-year-olds.
        Child Dev. 2004; 75: 1085-1097
        • O’Donnell K.J.
        • Glover V.
        • Barker E.D.
        • O’Connor T.G.
        The persisting effect of maternal mood in pregnancy on childhood psychopathology.
        Dev Psychopathol. 2014; 26: 393-403
        • O’Connor T.G.
        • Heron J.
        • Golding J.
        • Glover V.
        Maternal antenatal anxiety and behavioural/emotional problems in children: A test of a programming hypothesis.
        J Child Psychol Psychiatry. 2003; 44: 1025-1036
        • Martini J.
        • Knappe S.
        • Beesdo-Baum K.
        • Lieb R.
        • Wittchen H.U.
        Anxiety disorders before birth and self-perceived distress during pregnancy: Associations with maternal depression and obstetric, neonatal and early childhood outcomes.
        Early Hum Dev. 2010; 86: 305-310
        • Grizenko N.
        • Shayan Y.R.
        • Polotskaia A.
        • Ter-Stepanian M.
        • Joober R.
        Relation of maternal stress during pregnancy to symptom severity and response to treatment in children with ADHD.
        J Psychiatry Neurosci. 2008; 33: 10-16
        • Li J.
        • Olsen J.
        • Vestergaard M.
        • Obel C.
        Attention-deficit/hyperactivity disorder in the offspring following prenatal maternal bereavement: A nationwide follow-up study in Denmark.
        Eur Child Adolesc Psychiatry. 2010; 19: 747-753
        • Class Q.A.
        • Abel K.M.
        • Khashan A.S.
        • Rickert M.E.
        • Dalman C.
        • Larsson H.
        • et al.
        Offspring psychopathology following preconception, prenatal and postnatal maternal bereavement stress.
        Psychol Med. 2014; 44: 71-84
        • Grizenko N.
        • Fortier M.E.
        • Zadorozny C.
        • Thakur G.
        • Schmitz N.
        • Duval R.
        • Joober R.
        Maternal stress during pregnancy, ADHD symptomatology in children and genotype: Gene-environment interaction.
        J Can Acad Child Adolesc Psychiatry. 2012; 21: 9-15
        • Robinson M.
        • Mattes E.
        • Oddy W.H.
        • Pennell C.E.
        • van Eekelen A.
        • McLean N.J.
        • et al.
        Prenatal stress and risk of behavioral morbidity from age 2 to 14 years: The influence of the number, type, and timing of stressful life events.
        Dev Psychopathol. 2011; 23: 507-520
        • Ronald A.
        • Pennell C.E.
        • Whitehouse A.J.O.
        Prenatal maternal stress associated with ADHD and autistic traits in early childhood.
        Front Psychol. 2010; 1: 223
        • Naicker K.
        • Wickham M.
        • Colman I.
        Timing of first exposure to maternal depression and adolescent emotional disorder in a national canadian cohort.
        PLoS One. 2012; 7: 17-19
        • Wickham M.E.
        • Senthilselvan A.
        • Wild C.
        • Hoglund W.L.
        • Colman I.
        Maternal depressive symptoms during childhood and risky adolescent health behaviors.
        Pediatrics. 2015; 135: 59-67
        • Talge N.M.
        • Neal C.
        • Glover V.
        Antenatal maternal stress and long-term effects on child neurodevelopment: How and why?.
        J Child Psychol Psychiatry. 2007; 48: 245-261
        • Chronis-Tuscano A.
        • Molina B.S.G.
        • Pelham W.E.
        • Applegate B.
        • Dahlke A.
        • Overmyer M.
        • Lahey B.B.
        Very early predictors of adolescent depression and suicide attempts in children with attention-deficit/hyperactivity disorder.
        Arch Gen Psychiatry. 2010; 67: 1044-1051
        • Latimer K.
        • Wilson P.
        • Kemp J.
        • Thompson L.
        • Sim F.
        • Gillberg C.
        • et al.
        Disruptive behaviour disorders: A systematic review of environmental antenatal and early years risk factors.
        Child Care Health Dev. 2012; 38: 611-628
        • Odgers C.L.
        • Caspi A.
        • Broadbent J.M.
        • Dickson N.
        • Hancox R.J.
        • Harrington H.
        • et al.
        Prediction of differential adult health burden by conduct problem subtypes in males.
        Arch Gen Psychiatry. 2007; 64: 476-484
        • Odgers C.L.
        • Moffitt T.E.
        • Broadbent J.M.
        • Dickson N.
        • Hancox R.J.
        • Harrington H.
        • et al.
        Female and male antisocial trajectories: From childhood origins to adult outcomes.
        Dev Psychopathol. 2008; 20: 673-716
        • Moffitt T.E.
        • Arseneault L.
        • Jaffee S.R.
        • Kim-Cohen J.
        • Koenen K.C.
        • Odgers C.L.
        • et al.
        Research review: DSM-V conduct disorder: Research needs for an evidence base.
        J Child Psychol Psychiatry. 2008; 49: 3-33
        • Nagin D.
        • Tremblay R.E.
        Trajectories of boys’ physical aggression, opposition, and hyperactivity on the path to physically violent and nonviolent juvenile delinquency.
        Child Dev. 1999; 70: 1181-1196
        • Boyd A.
        • Golding J.
        • Macleod J.
        • Lawlor D.A.
        • Fraser A.
        • Henderson J.
        • et al.
        Cohort profile: The “children of the 90s”—The index offspring of the Avon Longitudinal Study of Parents and Children.
        Int J Epidemiol. 2013; 42: 111-127
        • Goodman R.
        • Ford T.
        • Richards H.
        • Gatward R.
        • Meltzer H.
        The Development and Well-Being Assessment: Description and initial validation of an integrated assessment of child and adolescent psychopathology.
        J Child Psychol Psychiatry. 2000; 41: 644-655
        • Goodman R.
        The Strengths and Difficulties Questionnaire: A research note.
        J Child Psychol Psychiatry. 1997; 38: 581-586
        • He J.P.
        • Burstein M.
        • Schmitz A.
        • Merikangas K.R.
        The Strengths and Difficulties Questionnaire (SDQ): The factor structure and scale validation in U.S. adolescents.
        J Abnorm Child Psychol. 2013; 41: 583-595
        • Evans J.
        • Heron J.
        • Patel R.R.
        • Wiles N.
        Depressive symptoms during pregnancy and low birth weight at term: Longitudinal study.
        Br J Psychiatry. 2007; 191: 84-85
        • Gibson J.
        • McKenzie-McHarg K.
        • Shakespeare J.
        • Price J.
        • Gray R.
        A systematic review of studies validating the Edinburgh Postnatal Depression Scale in antepartum and postpartum women.
        Acta Psychiatr Scand. 2009; 119: 350-364
        • Cox J.L.
        • Holden J.M.
        • Sagovsky R.
        Detection of postnatal depression. Development of the 10-item Edinburgh Postnatal Depression Scale.
        Br J Psychiatry. 1987; 150: 782-786
        • O’Connor T.G.
        • Heron J.
        • Glover V.
        • Team A.S.
        Antenatal anxiety predicts child behavioral/emotional problems independently of postnatal depression.
        J Am Acad Child Adolesc Psychiatry. 2002; 41: 1470-1477
        • Nagin D.S.
        Analyzing developmental trajectories: A semiparametric, group-based approach.
        Psychol Methods. 1999; 4: 139-157
        • Pursell G.R.
        • Laursen B.
        • Rubin K.H.
        • Booth-LaForce C.
        • Rose-Krasnor L.
        Gender differences in patterns of association between prosocial behavior, personality, and externalizing problems.
        J Res Pers. 2008; 42: 472-481
        • Glasheen C.
        • Richardson G.A.
        • Kim K.H.
        • Larkby C.A.
        • Swartz H.A.
        • Day N.L.
        Exposure to maternal pre- and postnatal depression and anxiety symptoms: Risk for major depression, anxiety disorders, and conduct disorder in adolescent offspring.
        Dev Psychopathol. 2013; 25: 1045-1063
        • Sarkar P.
        • Bergman K.
        • O’Connor T.G.
        • Glover V.
        Maternal antenatal anxiety and amniotic fluid cortisol and testosterone: Possible implications for foetal programming.
        J Neuroendocrinol. 2008; 20: 489-496
        • Gitau R.
        • Adams D.
        • Fisk N.M.
        • Glover V.
        Fetal plasma testosterone correlates positively with cortisol.
        Arch Dis Child Fetal Neonatal Ed. 2005; 90: F166-F169
        • Zahn-Waxler C.
        • Shirtcliff E.A.
        • Marceau K.
        Disorders of childhood and adolescence: gender and psychopathology.
        Annu Rev Clin Psychol. 2008; 4: 275-303
        • Knickmeyer R.
        • Baron-Cohen S.
        • Raggatt P.
        • Taylor K.
        • Hackett G.
        Fetal testosterone and empathy.
        Horm Behav. 2006; 49: 282-292
        • Knickmeyer R.
        • Baron-Cohen S.
        • Raggatt P.
        • Taylor K.
        Foetal testosterone, social relationships, and restricted interests in children.
        J Child Psychol Psychiatry. 2005; 46: 198-210
        • Scerbo A.S.
        • Kolko D.J.
        Salivary testosterone and cortisol in disruptive children: Relationship to aggressive, hyperactive, and internalizing behaviors.
        J Am Acad Child Adolesc Psychiatry. 1994; 33: 1174-1184
        • Lou H.C.
        • Rosa P.
        • Pryds O.
        • Cumming P.
        • Gjedde A.
        ADHD: Increased dopamine receptor availability linked to attention deficit and low neonatal cerebral blood flow.
        Dev Med Child Neurol. 2004; 46: 179-183
        • Betts K.S.
        • Williams G.M.
        • Najman J.M.
        • Alati R.
        The relationship between maternal depressive, anxious, and stress symptoms during pregnancy and adult offspring behavioral and emotional problems.
        Depress Anxiety. 2015; 32: 82-90
        • Rice F.
        • Harold G.T.
        • Boivin J.
        • van den Bree M.
        • Hay D.F.
        • Thapar A.
        The links between prenatal stress and offspring development and psychopathology: Disentangling environmental and inherited influences.
        Psychol Med. 2010; 40: 335-345
        • Khashan A.S.
        • Abel K.M.
        • McNamee R.
        • Pedersen M.G.
        • Webb R.T.
        • Baker P.N.
        • et al.
        Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events.
        Arch Gen Psychiatry. 2008; 65: 146-152
        • Bergman K.
        • Sarkar P.
        • Glover V.
        • O’Connor T.G.
        Maternal prenatal cortisol and infant cognitive development: Moderation by infant-mother attachment.
        Biol Psychiatry. 2010; 67: 1026-1032

      Linked Article

      • The Intergenerational Impact of Prenatal Stress: Time to Focus on Prevention?
        Biological PsychiatryVol. 83Issue 2
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          One of the greatest achievements of the 20th century is decreasing maternal and infant mortality and morbidity. The physical care of pregnant women in the developed world has hugely improved; however, the same has not been true for mental health care and psychosocial well-being (1). In this issue of Biological Psychiatry, MacKinnon et al. (2) use data from the Avon Longitudinal Study of Parents and Children birth cohort to document the independent effect of prenatal stress on offspring hyperactivity.
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