Skip to main content
Top
Published in: Current Psychiatry Reports 2/2015

01-02-2015 | Women's Mental Health (D Rubinow, Section Editor)

Prenatal Programming of Mental Illness: Current Understanding of Relationship and Mechanisms

Authors: Deborah R. Kim, Tracy L. Bale, C. Neill Epperson

Published in: Current Psychiatry Reports | Issue 2/2015

Login to get access

Abstract

The British epidemiologist Dr. David J. Barker documented the relationship between infant birth weight and later onset of hypertension, coronary heart disease, insulin resistance, and type II diabetes. A stressful in utero environment can cause long-term consequences for offspring through prenatal programming. Prenatal programming most commonly occurs through epigenetic mechanisms and can be dependent on the type and timing of exposure as well as the sex of the fetus. In this review, we highlight the most recent evidence that prenatal programming is implicated in the development of psychiatric disorders in offspring exposed to maternal stress during pregnancy. Methodological differences between studies contribute to unavoidable heterogeneity in study findings. Current data suggest that fetal exposure to maternal hypothalamic-pituitary-adrenal axis dysregulation, excessive glucocorticoids, and inflammation with resulting epigenetic changes at both the placental and fetal levels are important areas of continued investigation.
Literature
2.
go back to reference Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989;2(8663):577–80.PubMedCrossRef Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989;2(8663):577–80.PubMedCrossRef
5.
6.
go back to reference Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992;35(7):595–601.PubMedCrossRef Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992;35(7):595–601.PubMedCrossRef
7.
go back to reference Gluckman PD, Hanson MA. Maternal constraint of fetal growth and its consequences. Semin Fetal Neonatal Med. 2004;9(5):419–25.PubMedCrossRef Gluckman PD, Hanson MA. Maternal constraint of fetal growth and its consequences. Semin Fetal Neonatal Med. 2004;9(5):419–25.PubMedCrossRef
9.•
go back to reference Bale TL, Baram TZ, Brown AS, Goldstein JM, Insel TR, McCarthy MM, et al. Early life programming and neurodevelopmental disorders. Biol Psychiatry. 2010;68(4):314–9. This review summarizes findings from a workshop on Early Life Programming and Neurodevelopmental Disorders held at the University of Pennsylvania in 2009 and reviews the programming effects of nutrition as well as the importance of fetal sex in the outcome of prenatal programming.PubMedCentralPubMedCrossRef Bale TL, Baram TZ, Brown AS, Goldstein JM, Insel TR, McCarthy MM, et al. Early life programming and neurodevelopmental disorders. Biol Psychiatry. 2010;68(4):314–9. This review summarizes findings from a workshop on Early Life Programming and Neurodevelopmental Disorders held at the University of Pennsylvania in 2009 and reviews the programming effects of nutrition as well as the importance of fetal sex in the outcome of prenatal programming.PubMedCentralPubMedCrossRef
10.
go back to reference Lewis AJ, Galbally M, Gannon T, Symeonides C. Early life programming as a target for prevention of child and adolescent mental disorders. BMC Med. 2014;12:33.PubMedCentralPubMedCrossRef Lewis AJ, Galbally M, Gannon T, Symeonides C. Early life programming as a target for prevention of child and adolescent mental disorders. BMC Med. 2014;12:33.PubMedCentralPubMedCrossRef
11.
go back to reference Daskalakis NP, Bagot RC, Parker KJ, Vinkers CH, de Kloet ER. The three-hit concept of vulnerability and resilience: toward understanding adaptation to early-life adversity outcome. Psychoneuroendocrinology. 2013;38(9):1858–73.PubMedCentralPubMedCrossRef Daskalakis NP, Bagot RC, Parker KJ, Vinkers CH, de Kloet ER. The three-hit concept of vulnerability and resilience: toward understanding adaptation to early-life adversity outcome. Psychoneuroendocrinology. 2013;38(9):1858–73.PubMedCentralPubMedCrossRef
12.
go back to reference Hansen D, Lou HC, Olsen J. Serious life events and congenital malformations: a national study with complete follow-up. Lancet. 2000;356(9233):875–80.PubMedCrossRef Hansen D, Lou HC, Olsen J. Serious life events and congenital malformations: a national study with complete follow-up. Lancet. 2000;356(9233):875–80.PubMedCrossRef
13.
go back to reference Zhu JL, Olsen J, Sorensen HT, Li J, Nohr EA, Obel C, et al. Prenatal maternal bereavement and congenital heart defects in offspring: a registry-based study. Pediatrics. 2013;131(4):e1225–30.PubMedCrossRef Zhu JL, Olsen J, Sorensen HT, Li J, Nohr EA, Obel C, et al. Prenatal maternal bereavement and congenital heart defects in offspring: a registry-based study. Pediatrics. 2013;131(4):e1225–30.PubMedCrossRef
14.
go back to reference Schuurmans C, Kurrasch DM. Neurodevelopmental consequences of maternal distress: what do we really know? Clin Genet. 2013;83(2):108–17.PubMedCrossRef Schuurmans C, Kurrasch DM. Neurodevelopmental consequences of maternal distress: what do we really know? Clin Genet. 2013;83(2):108–17.PubMedCrossRef
16.
go back to reference O’Donnell K, O’Connor TG, Glover V. Prenatal stress and neurodevelopment of the child: focus on the HPA axis and role of the placenta. Dev Neurosci. 2009;31(4):285–92.PubMedCrossRef O’Donnell K, O’Connor TG, Glover V. Prenatal stress and neurodevelopment of the child: focus on the HPA axis and role of the placenta. Dev Neurosci. 2009;31(4):285–92.PubMedCrossRef
17.
go back to reference Buka SL, Tsuang MT, Torrey EF, Klebanoff MA, Bernstein D, Yolken RH. Maternal infections and subsequent psychosis among offspring. Arch Gen Psychiatry. 2001;58(11):1032–7.PubMedCrossRef Buka SL, Tsuang MT, Torrey EF, Klebanoff MA, Bernstein D, Yolken RH. Maternal infections and subsequent psychosis among offspring. Arch Gen Psychiatry. 2001;58(11):1032–7.PubMedCrossRef
18.
19.
go back to reference Brown AS, Vinogradov S, Kremen WS, Poole JH, Deicken RF, Penner JD, et al. Prenatal exposure to maternal infection and executive dysfunction in adult schizophrenia. Am J Psychiatry. 2009;166(6):683–90.PubMedCentralPubMedCrossRef Brown AS, Vinogradov S, Kremen WS, Poole JH, Deicken RF, Penner JD, et al. Prenatal exposure to maternal infection and executive dysfunction in adult schizophrenia. Am J Psychiatry. 2009;166(6):683–90.PubMedCentralPubMedCrossRef
20.
go back to reference O’Donnell KJ, Bugge Jensen A, Freeman L, Khalife N, O’Connor TG, Glover V. Maternal prenatal anxiety and downregulation of placental 11β-HSD2. Psychoneuroendocrinology. 2012;37(6):818–26.PubMedCrossRef O’Donnell KJ, Bugge Jensen A, Freeman L, Khalife N, O’Connor TG, Glover V. Maternal prenatal anxiety and downregulation of placental 11β-HSD2. Psychoneuroendocrinology. 2012;37(6):818–26.PubMedCrossRef
21.
go back to reference Howerton CL, Morgan CP, Fischer DB, Bale TL. O-GlcNAc transferase (OGT) as a placental biomarker of maternal stress and reprogramming of CNS gene transcription in development. Proc Natl Acad Sci U S A. 2013;110(13):5169–74.PubMedCentralPubMedCrossRef Howerton CL, Morgan CP, Fischer DB, Bale TL. O-GlcNAc transferase (OGT) as a placental biomarker of maternal stress and reprogramming of CNS gene transcription in development. Proc Natl Acad Sci U S A. 2013;110(13):5169–74.PubMedCentralPubMedCrossRef
22.
go back to reference Susser E, Lin SP, Brown AS, Lumey LH, Erlenmeyer-Kimling L. No relation between risk of schizophrenia and prenatal exposure to influenza in Holland. Am J Psychiatry. 1994;151(6):922–4.PubMedCrossRef Susser E, Lin SP, Brown AS, Lumey LH, Erlenmeyer-Kimling L. No relation between risk of schizophrenia and prenatal exposure to influenza in Holland. Am J Psychiatry. 1994;151(6):922–4.PubMedCrossRef
23.
go back to reference Susser E, Neugebauer R, Hoek HW, Brown AS, Lin S, Labovitz D, et al. Schizophrenia after prenatal famine. Further evidence. Arch Gen Psychiatry. 1996;53(1):25–31.PubMedCrossRef Susser E, Neugebauer R, Hoek HW, Brown AS, Lin S, Labovitz D, et al. Schizophrenia after prenatal famine. Further evidence. Arch Gen Psychiatry. 1996;53(1):25–31.PubMedCrossRef
24.
go back to reference Susser E, St Clair D, He L. Latent effects of prenatal malnutrition on adult health: the example of schizophrenia. Ann N Y Acad Sci. 2008;1136:185–92.PubMedCrossRef Susser E, St Clair D, He L. Latent effects of prenatal malnutrition on adult health: the example of schizophrenia. Ann N Y Acad Sci. 2008;1136:185–92.PubMedCrossRef
25.
go back to reference Meyer U, Feldon J. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Prog Neurobiol. 2010;90(3):285–326.PubMedCrossRef Meyer U, Feldon J. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Prog Neurobiol. 2010;90(3):285–326.PubMedCrossRef
26.
go back to reference Matrisciano F, Tueting P, Dalal I, Kadriu B, Grayson DR, Davis JM, et al. Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice. Neuropharmacology. 2013;68:184–94.PubMedCentralPubMedCrossRef Matrisciano F, Tueting P, Dalal I, Kadriu B, Grayson DR, Davis JM, et al. Epigenetic modifications of GABAergic interneurons are associated with the schizophrenia-like phenotype induced by prenatal stress in mice. Neuropharmacology. 2013;68:184–94.PubMedCentralPubMedCrossRef
27.•
go back to reference Bock J, Rether K, Groger N, Xie L, Braun K. Perinatal programming of emotional brain circuits: an integrative view from systems to molecules. Front Neurosci. 2014;8:11. Reviews animal models showing that early life stress causes neuronal damage in the prefrontal and limbic brain regions as well data showing that in some cases, early life stress promotes resilience.PubMedCentralPubMedCrossRef Bock J, Rether K, Groger N, Xie L, Braun K. Perinatal programming of emotional brain circuits: an integrative view from systems to molecules. Front Neurosci. 2014;8:11. Reviews animal models showing that early life stress causes neuronal damage in the prefrontal and limbic brain regions as well data showing that in some cases, early life stress promotes resilience.PubMedCentralPubMedCrossRef
28.•
go back to reference Class QA, Khashan AS, Lichtenstein P, Langstrom N, D’Onofrio BM. Maternal stress and infant mortality: the importance of the preconception period. Psychol Sci. 2013;24(7):1309–16. A study with a total of 20,651 offspring which evaluated preconception and prenatal stress (defined as death of a first-degree relative of the mother) on infant mortality. The results suggested that the period immediately before conception may be a sensitive developmental period with ramifications for infant mortality risk.PubMedCentralPubMedCrossRef Class QA, Khashan AS, Lichtenstein P, Langstrom N, D’Onofrio BM. Maternal stress and infant mortality: the importance of the preconception period. Psychol Sci. 2013;24(7):1309–16. A study with a total of 20,651 offspring which evaluated preconception and prenatal stress (defined as death of a first-degree relative of the mother) on infant mortality. The results suggested that the period immediately before conception may be a sensitive developmental period with ramifications for infant mortality risk.PubMedCentralPubMedCrossRef
29.
go back to reference O’Connor TG, Heron J, Glover V, Alspac Study Team. Antenatal anxiety predicts child behavioral/emotional problems independently of postnatal depression. J Am Acad Child Adolesc Psychiatry. 2002;41(12):1470–7.PubMedCrossRef O’Connor TG, Heron J, Glover V, Alspac Study Team. Antenatal anxiety predicts child behavioral/emotional problems independently of postnatal depression. J Am Acad Child Adolesc Psychiatry. 2002;41(12):1470–7.PubMedCrossRef
30.
go back to reference Huizink AC, Robles de Medina PG, Mulder EJ, Visser GH, Buitelaar JK. Stress during pregnancy is associated with developmental outcome in infancy. J Child Psychol Psychiatry. 2003;44(6):810–8.PubMedCrossRef Huizink AC, Robles de Medina PG, Mulder EJ, Visser GH, Buitelaar JK. Stress during pregnancy is associated with developmental outcome in infancy. J Child Psychol Psychiatry. 2003;44(6):810–8.PubMedCrossRef
31.
go back to reference Bale TL. Sex differences in prenatal epigenetic programming of stress pathways. Stress. 2011;14(4):348–56.PubMed Bale TL. Sex differences in prenatal epigenetic programming of stress pathways. Stress. 2011;14(4):348–56.PubMed
32.
go back to reference Mueller BR, Bale TL. Early prenatal stress impact on coping strategies and learning performance is sex dependent. Physiol Behav. 2007;91(1):55–65.PubMedCrossRef Mueller BR, Bale TL. Early prenatal stress impact on coping strategies and learning performance is sex dependent. Physiol Behav. 2007;91(1):55–65.PubMedCrossRef
33.
34.
go back to reference Zucchi FC, Yao Y, Ward ID, Ilnytskyy Y, Olson DM, Benzies K, et al. Maternal stress induces epigenetic signatures of psychiatric and neurological diseases in the offspring. PLoS One. 2013;8(2):e56967.PubMedCentralPubMedCrossRef Zucchi FC, Yao Y, Ward ID, Ilnytskyy Y, Olson DM, Benzies K, et al. Maternal stress induces epigenetic signatures of psychiatric and neurological diseases in the offspring. PLoS One. 2013;8(2):e56967.PubMedCentralPubMedCrossRef
35.
go back to reference Bronson SL, Bale TL. Prenatal stress-induced increases in placental inflammation and offspring hyperactivity are male-specific and ameliorated by maternal antiinflammatory treatment. Endocrinology. 2014;155(7):2635–46.PubMedCrossRef Bronson SL, Bale TL. Prenatal stress-induced increases in placental inflammation and offspring hyperactivity are male-specific and ameliorated by maternal antiinflammatory treatment. Endocrinology. 2014;155(7):2635–46.PubMedCrossRef
36.
go back to reference Garcia-Caceres C, Lagunas N, Calmarza-Font I, Azcoitia I, Diz-Chaves Y, Garcia-Segura LM, et al. Gender differences in the long-term effects of chronic prenatal stress on the HPA axis and hypothalamic structure in rats. Psychoneuroendocrinology. 2010;35(10):1525–35.PubMedCrossRef Garcia-Caceres C, Lagunas N, Calmarza-Font I, Azcoitia I, Diz-Chaves Y, Garcia-Segura LM, et al. Gender differences in the long-term effects of chronic prenatal stress on the HPA axis and hypothalamic structure in rats. Psychoneuroendocrinology. 2010;35(10):1525–35.PubMedCrossRef
37.
go back to reference Spauwen J, Krabbendam L, Lieb R, Wittchen HU, van Os J. Early maternal stress and health behaviours and offspring expression of psychosis in adolescence. Acta Psychiatr Scand. 2004;110(5):356–64.PubMedCrossRef Spauwen J, Krabbendam L, Lieb R, Wittchen HU, van Os J. Early maternal stress and health behaviours and offspring expression of psychosis in adolescence. Acta Psychiatr Scand. 2004;110(5):356–64.PubMedCrossRef
38.
go back to reference Rodriguez A, Bohlin G. Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiatry. 2005;46(3):246–54.PubMedCrossRef Rodriguez A, Bohlin G. Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiatry. 2005;46(3):246–54.PubMedCrossRef
39.
go back to reference Costello EJ, Worthman C, Erkanli A, Angold A. Prediction from low birth weight to female adolescent depression: a test of competing hypotheses. Arch Gen Psychiatry. 2007;64(3):338–44.PubMedCrossRef Costello EJ, Worthman C, Erkanli A, Angold A. Prediction from low birth weight to female adolescent depression: a test of competing hypotheses. Arch Gen Psychiatry. 2007;64(3):338–44.PubMedCrossRef
40.
go back to reference Grizenko N, Fortier ME, Zadorozny C, Thakur G, Schmitz N, Duval R, et al. Maternal stress during pregnancy, ADHD symptomatology in children and genotype: gene-environment interaction. J Can Acad Child Adolesc Psychiatry. 2012;21(1):9–15.PubMedCentralPubMed Grizenko N, Fortier ME, Zadorozny C, Thakur G, Schmitz N, Duval R, et al. Maternal stress during pregnancy, ADHD symptomatology in children and genotype: gene-environment interaction. J Can Acad Child Adolesc Psychiatry. 2012;21(1):9–15.PubMedCentralPubMed
41.
go back to reference Glover V, Hill J. Sex differences in the programming effects of prenatal stress on psychopathology and stress responses: an evolutionary perspective. Physiol Behav. 2012;106(5):736–40.PubMedCrossRef Glover V, Hill J. Sex differences in the programming effects of prenatal stress on psychopathology and stress responses: an evolutionary perspective. Physiol Behav. 2012;106(5):736–40.PubMedCrossRef
42.
go back to reference Van den Bergh BR, Van Calster B, Smits T, Van Huffel S, Lagae L. Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: a prospective study on the fetal origins of depressed mood. Neuropsychopharmacology. 2008;33(3):536–45.PubMedCrossRef Van den Bergh BR, Van Calster B, Smits T, Van Huffel S, Lagae L. Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: a prospective study on the fetal origins of depressed mood. Neuropsychopharmacology. 2008;33(3):536–45.PubMedCrossRef
43.
go back to reference McGrath J, Saha S, Welham J, El Saadi O, MacCauley C, Chant D. A systematic review of the incidence of schizophrenia: the distribution of rates and the influence of sex, urbanicity, migrant status and methodology. BMC Med. 2004;2:13.PubMedCentralPubMedCrossRef McGrath J, Saha S, Welham J, El Saadi O, MacCauley C, Chant D. A systematic review of the incidence of schizophrenia: the distribution of rates and the influence of sex, urbanicity, migrant status and methodology. BMC Med. 2004;2:13.PubMedCentralPubMedCrossRef
45.
go back to reference Goldstein JM, Seidman LJ, O’Brien LM, Horton NJ, Kennedy DN, Makris N, et al. Impact of normal sexual dimorphisms on sex differences in structural brain abnormalities in schizophrenia assessed by magnetic resonance imaging. Arch Gen Psychiatry. 2002;59(2):154–64.PubMedCrossRef Goldstein JM, Seidman LJ, O’Brien LM, Horton NJ, Kennedy DN, Makris N, et al. Impact of normal sexual dimorphisms on sex differences in structural brain abnormalities in schizophrenia assessed by magnetic resonance imaging. Arch Gen Psychiatry. 2002;59(2):154–64.PubMedCrossRef
46.
go back to reference Khashan AS, Abel KM, McNamee R, Pedersen MG, Webb RT, Baker PN, et al. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry. 2008;65(2):146–52.PubMedCrossRef Khashan AS, Abel KM, McNamee R, Pedersen MG, Webb RT, Baker PN, et al. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry. 2008;65(2):146–52.PubMedCrossRef
47.
go back to reference Class QA, Abel KM, Khashan AS, Rickert ME, Dalman C, Larsson H, et al. Offspring psychopathology following preconception, prenatal and postnatal maternal bereavement stress. Psychol Med. 2014;44(1):71–84.PubMedCrossRef Class QA, Abel KM, Khashan AS, Rickert ME, Dalman C, Larsson H, et al. Offspring psychopathology following preconception, prenatal and postnatal maternal bereavement stress. Psychol Med. 2014;44(1):71–84.PubMedCrossRef
48.
go back to reference Dorrington S, Zammit S, Asher L, Evans J, Heron J, Lewis G. Perinatal maternal life events and psychotic experiences in children at twelve years in a birth cohort study. Schizophr Res. 2014;152(1):158–63.PubMedCentralPubMedCrossRef Dorrington S, Zammit S, Asher L, Evans J, Heron J, Lewis G. Perinatal maternal life events and psychotic experiences in children at twelve years in a birth cohort study. Schizophr Res. 2014;152(1):158–63.PubMedCentralPubMedCrossRef
49.
go back to reference Huttunen MO, Niskanen P. Prenatal loss of father and psychiatric disorders. Arch Gen Psychiatry. 1978;35(4):429–31.PubMedCrossRef Huttunen MO, Niskanen P. Prenatal loss of father and psychiatric disorders. Arch Gen Psychiatry. 1978;35(4):429–31.PubMedCrossRef
50.
go back to reference Myhrman A, Rantakallio P, Isohanni M, Jones P, Partanen U. Unwantedness of a pregnancy and schizophrenia in the child. Br J Psychiatry. 1996;169(5):637–40.PubMedCrossRef Myhrman A, Rantakallio P, Isohanni M, Jones P, Partanen U. Unwantedness of a pregnancy and schizophrenia in the child. Br J Psychiatry. 1996;169(5):637–40.PubMedCrossRef
51.
go back to reference Sacker A, Done DJ, Crow TJ, Golding J. Antecedents of schizophrenia and affective illness. Obstetric complications. Br J Psychiatry. 1995;166(6):734–41.PubMedCrossRef Sacker A, Done DJ, Crow TJ, Golding J. Antecedents of schizophrenia and affective illness. Obstetric complications. Br J Psychiatry. 1995;166(6):734–41.PubMedCrossRef
52.
go back to reference Selten JP, van der Graaf Y, van Duursen R, Gispen-de Wied CC, Kahn RS. Psychotic illness after prenatal exposure to the 1953 Dutch flood disaster. Schizophr Res. 1999;35(3):243–5.PubMedCrossRef Selten JP, van der Graaf Y, van Duursen R, Gispen-de Wied CC, Kahn RS. Psychotic illness after prenatal exposure to the 1953 Dutch flood disaster. Schizophr Res. 1999;35(3):243–5.PubMedCrossRef
53.
go back to reference Selten JP, Cantor-Graae E, Nahon D, Levav I, Aleman A, Kahn RS. No relationship between risk of schizophrenia and prenatal exposure to stress during the Six-Day War or Yom Kippur War in Israel. Schizophr Res. 2003;63(1–2):131–5.PubMedCrossRef Selten JP, Cantor-Graae E, Nahon D, Levav I, Aleman A, Kahn RS. No relationship between risk of schizophrenia and prenatal exposure to stress during the Six-Day War or Yom Kippur War in Israel. Schizophr Res. 2003;63(1–2):131–5.PubMedCrossRef
54.
go back to reference Cannon TD, Rosso IM, Hollister JM, Bearden CE, Sanchez LE, Hadley T. A prospective cohort study of genetic and perinatal influences in the etiology of schizophrenia. Schizophr Bull. 2000;26(2):351–66.PubMedCrossRef Cannon TD, Rosso IM, Hollister JM, Bearden CE, Sanchez LE, Hadley T. A prospective cohort study of genetic and perinatal influences in the etiology of schizophrenia. Schizophr Bull. 2000;26(2):351–66.PubMedCrossRef
55.
go back to reference Zornberg GL, Buka SL, Tsuang MT. Hypoxic-ischemia-related fetal/neonatal complications and risk of schizophrenia and other nonaffective psychoses: a 19-year longitudinal study. Am J Psychiatry. 2000;157(2):196–202.PubMedCrossRef Zornberg GL, Buka SL, Tsuang MT. Hypoxic-ischemia-related fetal/neonatal complications and risk of schizophrenia and other nonaffective psychoses: a 19-year longitudinal study. Am J Psychiatry. 2000;157(2):196–202.PubMedCrossRef
56.
go back to reference Zornberg GL, Buka SL, Tsuang MT. The problem of obstetrical complications and schizophrenia. Schizophr Bull. 2000;26(2):249–56.PubMedCrossRef Zornberg GL, Buka SL, Tsuang MT. The problem of obstetrical complications and schizophrenia. Schizophr Bull. 2000;26(2):249–56.PubMedCrossRef
57.
58.
go back to reference Holloway T, Moreno JL, Umali A, Rayannavar V, Hodes GE, Russo SJ, et al. Prenatal stress induces schizophrenia-like alterations of serotonin 2A and metabotropic glutamate 2 receptors in the adult offspring: role of maternal immune system. J Neurosci. 2013;33(3):1088–98.PubMedCentralPubMedCrossRef Holloway T, Moreno JL, Umali A, Rayannavar V, Hodes GE, Russo SJ, et al. Prenatal stress induces schizophrenia-like alterations of serotonin 2A and metabotropic glutamate 2 receptors in the adult offspring: role of maternal immune system. J Neurosci. 2013;33(3):1088–98.PubMedCentralPubMedCrossRef
59.
go back to reference Baron-Cohen S, Scott FJ, Allison C, Williams J, Bolton P, Matthews FE, et al. Prevalence of autism-spectrum conditions: UK school-based population study. Br J Psychiatry. 2009;194(6):500–9.PubMedCrossRef Baron-Cohen S, Scott FJ, Allison C, Williams J, Bolton P, Matthews FE, et al. Prevalence of autism-spectrum conditions: UK school-based population study. Br J Psychiatry. 2009;194(6):500–9.PubMedCrossRef
60.
go back to reference Depino AM. Peripheral and central inflammation in autism spectrum disorders. Mol Cell Neurosci. 2013;53:69–76.PubMedCrossRef Depino AM. Peripheral and central inflammation in autism spectrum disorders. Mol Cell Neurosci. 2013;53:69–76.PubMedCrossRef
61.
go back to reference Ciaranello AL, Ciaranello RD. The neurobiology of infantile autism. Annu Rev Neurosci. 1995;18:101–28.PubMedCrossRef Ciaranello AL, Ciaranello RD. The neurobiology of infantile autism. Annu Rev Neurosci. 1995;18:101–28.PubMedCrossRef
62.
go back to reference Singh VK, Jensen RL. Elevated levels of measles antibodies in children with autism. Pediatr Neurol. 2003;28(4):292–4.PubMedCrossRef Singh VK, Jensen RL. Elevated levels of measles antibodies in children with autism. Pediatr Neurol. 2003;28(4):292–4.PubMedCrossRef
63.
go back to reference Atladottir HO, Thorsen P, Ostergaard L, Schendel DE, Lemcke S, Abdallah M, et al. Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord. 2010;40(12):1423–30.PubMedCrossRef Atladottir HO, Thorsen P, Ostergaard L, Schendel DE, Lemcke S, Abdallah M, et al. Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord. 2010;40(12):1423–30.PubMedCrossRef
64.
go back to reference Zerbo O, Qian Y, Yoshida C, Grether JK, Van de Water J, Croen LA. Maternal infection during pregnancy and autism spectrum disorders. J Autism Dev Disord. 2013 Dec 24. Zerbo O, Qian Y, Yoshida C, Grether JK, Van de Water J, Croen LA. Maternal infection during pregnancy and autism spectrum disorders. J Autism Dev Disord. 2013 Dec 24.
65.
go back to reference Atladottir HO, Thorsen P, Schendel DE, Ostergaard L, Lemcke S, Parner ET. Association of hospitalization for infection in childhood with diagnosis of autism spectrum disorders: a Danish cohort study. Arch Pediatr Adolesc Med. 2010;164(5):470–7.PubMed Atladottir HO, Thorsen P, Schendel DE, Ostergaard L, Lemcke S, Parner ET. Association of hospitalization for infection in childhood with diagnosis of autism spectrum disorders: a Danish cohort study. Arch Pediatr Adolesc Med. 2010;164(5):470–7.PubMed
66.
go back to reference Crawley JN. Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol. 2007;17(4):448–59.PubMedCrossRef Crawley JN. Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol. 2007;17(4):448–59.PubMedCrossRef
67.
go back to reference Malkova NV, Yu CZ, Hsiao EY, Moore MJ, Patterson PH. Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism. Brain Behav Immun. 2012;26(4):607–16.PubMedCentralPubMedCrossRef Malkova NV, Yu CZ, Hsiao EY, Moore MJ, Patterson PH. Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism. Brain Behav Immun. 2012;26(4):607–16.PubMedCentralPubMedCrossRef
68.
go back to reference Flegal KM, Carroll MD, Kit BK, Ogden CL. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA. 2012;307(5):491–7.PubMedCrossRef Flegal KM, Carroll MD, Kit BK, Ogden CL. Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999-2010. JAMA. 2012;307(5):491–7.PubMedCrossRef
69.
go back to reference Krakowiak P, Walker CK, Bremer AA, Baker AS, Ozonoff S, Hansen RL, et al. Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders. Pediatrics. 2012;129(5):e1121–8.PubMedCentralPubMedCrossRef Krakowiak P, Walker CK, Bremer AA, Baker AS, Ozonoff S, Hansen RL, et al. Maternal metabolic conditions and risk for autism and other neurodevelopmental disorders. Pediatrics. 2012;129(5):e1121–8.PubMedCentralPubMedCrossRef
70.
go back to reference Reynolds LC, Inder TE, Neil JJ, Pineda RG, Rogers CE. Maternal obesity and increased risk for autism and developmental delay among very preterm infants. J Perinatol. 2014;34:688–92.PubMedCrossRef Reynolds LC, Inder TE, Neil JJ, Pineda RG, Rogers CE. Maternal obesity and increased risk for autism and developmental delay among very preterm infants. J Perinatol. 2014;34:688–92.PubMedCrossRef
71.
go back to reference Dodds L, Fell DB, Shea S, Armson BA, Allen AC, Bryson S. The role of prenatal, obstetric and neonatal factors in the development of autism. J Autism Dev Disord. 2011;41(7):891–902.PubMedCrossRef Dodds L, Fell DB, Shea S, Armson BA, Allen AC, Bryson S. The role of prenatal, obstetric and neonatal factors in the development of autism. J Autism Dev Disord. 2011;41(7):891–902.PubMedCrossRef
72.
go back to reference Sullivan EL, Nousen EK, Chamlou KA. Maternal high fat diet consumption during the perinatal period programs offspring behavior. Physiol Behav. 2014;123:236–42.PubMedCrossRef Sullivan EL, Nousen EK, Chamlou KA. Maternal high fat diet consumption during the perinatal period programs offspring behavior. Physiol Behav. 2014;123:236–42.PubMedCrossRef
73.
go back to reference Ashwood P, Kwong C, Hansen R, Hertz-Picciotto I, Croen L, Krakowiak P, et al. Brief report: plasma leptin levels are elevated in autism: association with early onset phenotype? J Autism Dev Disord. 2008;38(1):169–75.PubMedCrossRef Ashwood P, Kwong C, Hansen R, Hertz-Picciotto I, Croen L, Krakowiak P, et al. Brief report: plasma leptin levels are elevated in autism: association with early onset phenotype? J Autism Dev Disord. 2008;38(1):169–75.PubMedCrossRef
76.
go back to reference Froehlich-Santino W, Londono Tobon A, Cleveland S, Torres A, Phillips J, Cohen B, et al. Prenatal and perinatal risk factors in a twin study of autism spectrum disorders. J Psychiatr Res. 2014;54:100–8.PubMedCrossRef Froehlich-Santino W, Londono Tobon A, Cleveland S, Torres A, Phillips J, Cohen B, et al. Prenatal and perinatal risk factors in a twin study of autism spectrum disorders. J Psychiatr Res. 2014;54:100–8.PubMedCrossRef
77.
go back to reference Zimmerman AW, Connors SL. Neuroscience. Could autism be treated prenatally? Science. 2014;343(6171):620–1.PubMedCrossRef Zimmerman AW, Connors SL. Neuroscience. Could autism be treated prenatally? Science. 2014;343(6171):620–1.PubMedCrossRef
78.
go back to reference Gaynes BN, Christian R, Saavedra LM, Wines R, Jonas DE, Viswanathan M, et al. Attention-deficit/hyperactivity disorder: identifying high priority future research needs. J Psychiatr Pract. 2014;20(2):104–17.PubMedCrossRef Gaynes BN, Christian R, Saavedra LM, Wines R, Jonas DE, Viswanathan M, et al. Attention-deficit/hyperactivity disorder: identifying high priority future research needs. J Psychiatr Pract. 2014;20(2):104–17.PubMedCrossRef
79.
go back to reference 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(10):747–53.PubMedCrossRef 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(10):747–53.PubMedCrossRef
80.
go back to reference Lee CY, Chang YY, Lung FW. The marriage-related risk factors during maternal pregnancy in children with attention-deficit hyperactivity disorder. Child Care Health Dev. 2006;32(2):205–11.PubMedCrossRef Lee CY, Chang YY, Lung FW. The marriage-related risk factors during maternal pregnancy in children with attention-deficit hyperactivity disorder. Child Care Health Dev. 2006;32(2):205–11.PubMedCrossRef
81.
go back to reference Van den Bergh BR, 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(4):1085–97.PubMedCrossRef Van den Bergh BR, 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(4):1085–97.PubMedCrossRef
82.
go back to reference Martini J, Knappe S, Beesdo-Baum K, Lieb R, Wittchen HU. 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(5):305–10.PubMedCrossRef Martini J, Knappe S, Beesdo-Baum K, Lieb R, Wittchen HU. 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(5):305–10.PubMedCrossRef
83.
go back to reference French NP, Hagan R, Evans SF, Mullan A, Newnham JP. Repeated antenatal corticosteroids: effects on cerebral palsy and childhood behavior. Am J Obstet Gynecol. 2004;190(3):588–95.PubMedCrossRef French NP, Hagan R, Evans SF, Mullan A, Newnham JP. Repeated antenatal corticosteroids: effects on cerebral palsy and childhood behavior. Am J Obstet Gynecol. 2004;190(3):588–95.PubMedCrossRef
85.
go back to reference Fisher D, Baird J, Payne L, Lucas P, Kleijnen J, Roberts H, et al. Are infant size and growth related to burden of disease in adulthood? A systematic review of literature. Int J Epidemiol. 2006;35(5):1196–210.PubMedCrossRef Fisher D, Baird J, Payne L, Lucas P, Kleijnen J, Roberts H, et al. Are infant size and growth related to burden of disease in adulthood? A systematic review of literature. Int J Epidemiol. 2006;35(5):1196–210.PubMedCrossRef
86.
go back to reference Vasiliadis HM, Gilman SE, Buka SL. Fetal growth restriction and the development of major depression. Acta Psychiatr Scand. 2008;117(4):306–12.PubMedCrossRef Vasiliadis HM, Gilman SE, Buka SL. Fetal growth restriction and the development of major depression. Acta Psychiatr Scand. 2008;117(4):306–12.PubMedCrossRef
87.
go back to reference Alati R, Lawlor DA, Mamun AA, Williams GM, Najman JM, O’Callaghan M, et al. Is there a fetal origin of depression? Evidence from the mater university study of pregnancy and its outcomes. Am J Epidemiol. 2007;165(5):575–82.PubMedCrossRef Alati R, Lawlor DA, Mamun AA, Williams GM, Najman JM, O’Callaghan M, et al. Is there a fetal origin of depression? Evidence from the mater university study of pregnancy and its outcomes. Am J Epidemiol. 2007;165(5):575–82.PubMedCrossRef
88.
go back to reference Goodman SH, Gotlib IH. Risk for psychopathology in the children of depressed mothers: a developmental model for understanding mechanisms of transmission. Psychol Rev. 1999;106(3):458–90.PubMedCrossRef Goodman SH, Gotlib IH. Risk for psychopathology in the children of depressed mothers: a developmental model for understanding mechanisms of transmission. Psychol Rev. 1999;106(3):458–90.PubMedCrossRef
89.
go back to reference Weinstock M. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun. 2005;19(4):296–308.PubMedCrossRef Weinstock M. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun. 2005;19(4):296–308.PubMedCrossRef
90.
go back to reference Pearson RM, Evans J, Kounali D, Lewis G, Heron J, Ramchandani PG, et al. Maternal depression during pregnancy and the postnatal period: risks and possible mechanisms for offspring depression at age 18 years. JAMA Psychiatry. 2013;70(12):1312–9.PubMedCentralPubMedCrossRef Pearson RM, Evans J, Kounali D, Lewis G, Heron J, Ramchandani PG, et al. Maternal depression during pregnancy and the postnatal period: risks and possible mechanisms for offspring depression at age 18 years. JAMA Psychiatry. 2013;70(12):1312–9.PubMedCentralPubMedCrossRef
91.
go back to reference Betts KS, Williams GM, Najman JM, Alati R. The relationship between maternal depressive, anxious, and stress symptoms during pregnancy and adult offspring behavioral and emotional problems. Depress Anxiety. 2014 Apr 30. Betts KS, Williams GM, Najman JM, Alati R. The relationship between maternal depressive, anxious, and stress symptoms during pregnancy and adult offspring behavioral and emotional problems. Depress Anxiety. 2014 Apr 30.
92.
go back to reference Darnaudery M, Maccari S. Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev. 2008;57(2):571–85.PubMedCrossRef Darnaudery M, Maccari S. Epigenetic programming of the stress response in male and female rats by prenatal restraint stress. Brain Res Rev. 2008;57(2):571–85.PubMedCrossRef
93.
go back to reference Blakeley PM, Capron LE, Jensen AB, O’Donnell KJ, Glover V. Maternal prenatal symptoms of depression and down regulation of placental monoamine oxidase A expression. J Psychosom Res. 2013;75(4):341–5.PubMedCrossRef Blakeley PM, Capron LE, Jensen AB, O’Donnell KJ, Glover V. Maternal prenatal symptoms of depression and down regulation of placental monoamine oxidase A expression. J Psychosom Res. 2013;75(4):341–5.PubMedCrossRef
94.•
go back to reference O’Donnell KJ, Glover V, Barker ED, O’Connor TG. The persisting effect of maternal mood in pregnancy on childhood psychopathology. Dev Psychopathol. 2014;26(2):393–403. Most recent data from the Avon Longitudinal Study of Parents and Children cohort, a prospective, longitudinal study of a large community sample (n = 7944). Severe prenatal anxiety was associated with a twofold increase in the risk of a childhood mental disorder (12.31 versus 6.83 %) compared to low-anxiety mothers. The effects did not decrease as the child aged into adolescence.PubMedCrossRef O’Donnell KJ, Glover V, Barker ED, O’Connor TG. The persisting effect of maternal mood in pregnancy on childhood psychopathology. Dev Psychopathol. 2014;26(2):393–403. Most recent data from the Avon Longitudinal Study of Parents and Children cohort, a prospective, longitudinal study of a large community sample (n = 7944). Severe prenatal anxiety was associated with a twofold increase in the risk of a childhood mental disorder (12.31 versus 6.83 %) compared to low-anxiety mothers. The effects did not decrease as the child aged into adolescence.PubMedCrossRef
95.
go back to reference O’Donnell KJ, Glover V, Jenkins J, Browne D, Ben-Shlomo Y, Golding J, et al. Prenatal maternal mood is associated with altered diurnal cortisol in adolescence. Psychoneuroendocrinology. 2013;38(9):1630–8.PubMedCentralPubMedCrossRef O’Donnell KJ, Glover V, Jenkins J, Browne D, Ben-Shlomo Y, Golding J, et al. Prenatal maternal mood is associated with altered diurnal cortisol in adolescence. Psychoneuroendocrinology. 2013;38(9):1630–8.PubMedCentralPubMedCrossRef
96.
go back to reference Walker AK, Nakamura T, Byrne RJ, Naicker S, Tynan RJ, Hunter M, et al. Neonatal lipopolysaccharide and adult stress exposure predisposes rats to anxiety-like behaviour and blunted corticosterone responses: implications for the double-hit hypothesis. Psychoneuroendocrinology. 2009;34(10):1515–25.PubMedCrossRef Walker AK, Nakamura T, Byrne RJ, Naicker S, Tynan RJ, Hunter M, et al. Neonatal lipopolysaccharide and adult stress exposure predisposes rats to anxiety-like behaviour and blunted corticosterone responses: implications for the double-hit hypothesis. Psychoneuroendocrinology. 2009;34(10):1515–25.PubMedCrossRef
97.
go back to reference Sominsky L, Fuller EA, Bondarenko E, Ong LK, Averell L, Nalivaiko E, et al. Functional programming of the autonomic nervous system by early life immune exposure: implications for anxiety. PLoS One. 2013;8(3):e57700.PubMedCentralPubMedCrossRef Sominsky L, Fuller EA, Bondarenko E, Ong LK, Averell L, Nalivaiko E, et al. Functional programming of the autonomic nervous system by early life immune exposure: implications for anxiety. PLoS One. 2013;8(3):e57700.PubMedCentralPubMedCrossRef
98.
go back to reference Walker AK, Nakamura T, Hodgson DM. Neonatal lipopolysaccharide exposure alters central cytokine responses to stress in adulthood in Wistar rats. Stress. 2010;13(6):506–15.PubMed Walker AK, Nakamura T, Hodgson DM. Neonatal lipopolysaccharide exposure alters central cytokine responses to stress in adulthood in Wistar rats. Stress. 2010;13(6):506–15.PubMed
99.
go back to reference Sasaki A, de Vega WC, St-Cyr S, Pan P, McGowan PO. Perinatal high fat diet alters glucocorticoid signaling and anxiety behavior in adulthood. Neuroscience. 2013;240:1–12.PubMedCrossRef Sasaki A, de Vega WC, St-Cyr S, Pan P, McGowan PO. Perinatal high fat diet alters glucocorticoid signaling and anxiety behavior in adulthood. Neuroscience. 2013;240:1–12.PubMedCrossRef
Metadata
Title
Prenatal Programming of Mental Illness: Current Understanding of Relationship and Mechanisms
Authors
Deborah R. Kim
Tracy L. Bale
C. Neill Epperson
Publication date
01-02-2015
Publisher
Springer US
Published in
Current Psychiatry Reports / Issue 2/2015
Print ISSN: 1523-3812
Electronic ISSN: 1535-1645
DOI
https://doi.org/10.1007/s11920-014-0546-9

Other articles of this Issue 2/2015

Current Psychiatry Reports 2/2015 Go to the issue

Military Mental Health (CH Warner, Section Editor)

Current Directions in Military Health-care Provider Resilience

Anxiety Disorders (A Pelissolo, Section Editor)

Anxiety and Substance Use Disorders: Co-occurrence and Clinical Issues

Geriatric Disorders (W McDonald, Section Editor)

Late-Life Psychosis: Diagnosis and Treatment

Personality Disorders (C Schmahl, Section Editor)

Obsessive–Compulsive Personality Disorder: a Current Review