Advertisement

European Child & Adolescent Psychiatry

, Volume 23, Issue 10, pp 943–956 | Cite as

Mechanisms underlying the effects of prenatal psychosocial stress on child outcomes: beyond the HPA axis

  • Roseriet Beijers
  • Jan K. Buitelaar
  • Carolina de Weerth
Review

Abstract

Accumulating evidence from preclinical and clinical studies indicates that maternal psychosocial stress and anxiety during pregnancy adversely affect child outcomes. However, knowledge on the possible mechanisms underlying these relations is limited. In the present paper, we review the most often proposed mechanism, namely that involving the HPA axis and cortisol, as well as other less well-studied but possibly relevant and complementary mechanisms. We present evidence for a role of the following mechanisms: compromised placental functioning, including the 11β-HSD2 enzyme, increased catecholamines, compromised maternal immune system and intestinal microbiota, and altered health behaviors including eating, sleep, and exercise. The roles of (epi)genetics, the postnatal environment and the fetus are also discussed. We conclude that maternal prenatal psychosocial stress is a complex phenomenon that affects maternal emotions, behavior and physiology in many ways, and may influence the physiology and functioning of the fetus through a network of different pathways. The review concludes with recommendations for future research that helps our understanding of the mechanisms by which maternal prenatal stress exerts its effect on the fetus.

Keywords

Prenatal stress Anxiety Child outcomes Mechanisms HPA axis 

References

  1. 1.
    Huizink AC, Mulder EJ, Buitelaar JK (2004) Prenatal stress and risk for psychopathology: specific effects or induction of general susceptibility? Psychol Bull 130(1):115–142PubMedGoogle Scholar
  2. 2.
    Räikkönen K, Seckl JR, Pesonen AK, Simons A, Van den Bergh BR (2011) Stress, glucocorticoids and liquorice in human pregnancy: programmers of the offspring brain. Stress 14:590–603PubMedGoogle Scholar
  3. 3.
    Seckl JR, Meaney MJ (2004) Glucocorticoid programming. Ann NY Acad Sci 1032:63–84PubMedGoogle Scholar
  4. 4.
    De Weerth C, Buitelaar JK (2005) Physiological stress reactivity in human pregnancy—a review. Neurosci Biobehav Rev 29:295–312PubMedGoogle Scholar
  5. 5.
    Matthews SG, Phillips DI (2012) Transgenerational inheritance of stress pathology. Exp Neurol 233:95–101PubMedGoogle Scholar
  6. 6.
    Bale TL, Baram TZ, Brown AS (2010) Early life programming and neurodevelopmental disorders. Biol Psychiatry 68(4):314–319PubMedPubMedCentralGoogle Scholar
  7. 7.
    Charil A, Laplante DP, Vaillancourt C, King S (2010) Prenatal stress and brain development. Brain Res Rev 65:56–79PubMedGoogle Scholar
  8. 8.
    Glover V (2011) Annual research review: prenatal stress and the origins of psychopathology: an evolutionary perspective. J Child Psychol Psychiatry 52(4):356–367PubMedGoogle Scholar
  9. 9.
    Sandman CA, Davis EP, Buss C, Glynn LM (2011) Exposure to prenatal psychobiological stress exerts programming influences on the mother and her fetus. Neuroendocrinology 95(1):7–21PubMedGoogle Scholar
  10. 10.
    Swanson JD, Wadhwa PM (2008) Developmental origins of child mental health disorders. J Child Psychol Psychiatry 49(10):1009–1019PubMedPubMedCentralGoogle Scholar
  11. 11.
    Talge NM, Neal C, Glover V (2007) Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J Child Psychol Psychiatry 48:245–261PubMedGoogle Scholar
  12. 12.
    Lobel M, Dunkel-Schetter C (1990) Conceptualizing stress to study effects on health: environmental, perceptual, and emotional components. Anx Res 3:213–230Google Scholar
  13. 13.
    Lobel M, Dunkel-Schetter C, Scrimshaw SC (1992) Prenatal maternal stress and prematurity: a prospective study of socioeconomically disadvantaged women. Health Psychol 11:32–40PubMedGoogle Scholar
  14. 14.
    Alderdice F, Lynn F, Lobel M (2012) A review and psychometric evaluation of pregnancy-specific stress measures. J Psychosom Obstet Gynaecol 33(2):62–77PubMedGoogle Scholar
  15. 15.
    Huizink AC, Mulder EJ, Robles de Medina PG, Visser G, Buitelaar J (2004) Is pregnancy anxiety a distinctive syndrome? Early Hum Dev 79(2):81–91PubMedGoogle Scholar
  16. 16.
    Tollenaar MS, Beijers R, Jansen J, Riksen-Walraven JM, de Weerth C (2011) Maternal prenatal stress and cortisol reactivity to stressors in human infants. Stress 14(1):53–65PubMedGoogle Scholar
  17. 17.
    Dunkel-Schetter C, Tanner L (2012) Anxiety, depression and stress in pregnancy: implications for mothers, children, research, and practice. Curr Opin Psychiatry 25(2):141–148PubMedGoogle Scholar
  18. 18.
    Field T (2011) Prenatal depression effects on early development: a review. Inf Beh Dev 34:1–14Google Scholar
  19. 19.
    Glover V, O’Connor TG, O’Donnell K (2010) Prenatal stress and the programming of the HPA axis. Neurosci Biobehav Rev 35(1):17–22PubMedGoogle Scholar
  20. 20.
    Pryce CR, Aubert Y, Maier C, Pearce PC, Fuchs E (2011) The developmental impact of prenatal stress, prenatal dexamethasone and postnatal social stress on physiology, behaviour and neuroanatomy of primate offspring: studies in rhesus macaque and common marmoset. Psychopharmacology 214(1):33–53PubMedPubMedCentralGoogle Scholar
  21. 21.
    Weinstock M (2011) Sex-dependent changes induced by prenatal stress in cortical and hippocampal morphology and behaviour in rats: an update. Stress 14(6):604–613PubMedGoogle Scholar
  22. 22.
    Peña CJ, Monk C, Champagne FA (2012) Epigenetic effects of prenatal stress on 11b-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain. PLoS ONE 7:e39791Google Scholar
  23. 23.
    Shapiro GD, Fraser WD, Frasch MG, Séguin JR (2013) Psychosocial stress in pregnancy and preterm birth: associations and mechanisms. J Perinat Med 41(6):631–645PubMedGoogle Scholar
  24. 24.
    Buss C, Davis EP, Muftuler T et al (2010) High pregnancy anxiety during midgestation is associated with decreased gray matter density in 6–9-year-old children. Psychoneuroendocrinology 35:141–153PubMedPubMedCentralGoogle Scholar
  25. 25.
    Mennes M, Stiers P, Lagae L, Van Den Bergh B (2006) Long-term cognitive sequelae of antenatal maternal anxiety: involvement of the orbitofrontal cortex. Neurosci Biobehav Rev 30:1078–1086PubMedGoogle Scholar
  26. 26.
    Entringer S (2013) Impact of stress and stress physiology during pregnancy on child metabolic function and obesity risk. Curr Opin Clin Nutr Metab Care 16(3):320–327PubMedPubMedCentralGoogle Scholar
  27. 27.
    Seckl JR (2008) Glucocorticoids, developmental ‘programming’ and the risk of affective dysfunction. Prog Brain Res 167:17–34PubMedGoogle Scholar
  28. 28.
    Rodriguez A, Bohlin G (2005) Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiatry 46:246–254PubMedGoogle Scholar
  29. 29.
    Van Den Bergh BR, Marcoen A (2004) High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Dev 75:1085–1097PubMedGoogle Scholar
  30. 30.
    Tarabulsy GM, Pearson J, Vaillancourt-Morel MP et al (2014) Meta-analytic findings of the relation between maternal prenatal stress and anxiety and child cognitive outcome. J Dev Behav Pediatr 35(1):38–43PubMedGoogle Scholar
  31. 31.
    Kashan AS, Abel KM, McNamee R et al (2008) Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry 65:146–152Google Scholar
  32. 32.
    Markham JA, Koenig JI (2011) Prenatal stress: role in psychotic and depressive diseases. Psychopharmacology 214(1):89–106PubMedPubMedCentralGoogle Scholar
  33. 33.
    Howerton CL, Bale TL (2012) Prenatal programing: at the intersection of maternal stress and immune activation. Horm Behav 62(3):237–242PubMedPubMedCentralGoogle Scholar
  34. 34.
    Entringer S, Kumsta R, Nelson EL, Hellhammer DH, Wadhwa PD, Wust S (2008) Influence of prenatal psychosocial stress on cytokine production in adult women. Dev Psychobiol 50(6):579–587Google Scholar
  35. 35.
    Lupien SJ, 2009, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10(6):434–445Google Scholar
  36. 36.
    Huizink AC (2012) Prenatal substance use, prenatal stress and offspring behavioural outcomes: considerations for future studies. Nord J Psychiatry 66(2):115–122PubMedGoogle Scholar
  37. 37.
    Gitau R, Cameron A, Fisk NM, Glover V (1998) Fetal exposure to maternal cortisol. Lancet 352(9129):707–708PubMedGoogle Scholar
  38. 38.
    Majzoub JA, Karalis KP (1999) Placental corticotropin-releasing hormone: function and regulation. Am J Obstet Gynecol 180:S242–S246PubMedGoogle Scholar
  39. 39.
    Wadhwa PD, Garite TJ, Porto M et al (2004) Placental corticotropin-releasing hormone (CRH), spontaneous preterm birth, and fetal growth restriction: a prospective investigation. Am J Obstet Gynecol 191:1063–1069PubMedGoogle Scholar
  40. 40.
    Nyirenda MJ, Lindsay RS, Kenyon CJ et al (1998) Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J Clin Invest 101:2174–2181PubMedPubMedCentralGoogle Scholar
  41. 41.
    De Blasio MJ, Dodic M, Jefferies AJ et al (2007) Maternal exposure to dexamethasone or cortisol in early pregnancy differentially alters insulin secretion and glucose homeostasis in adult male sheep offspring. Am J Physiol Endocrinol Metab 293:E75–E82PubMedGoogle Scholar
  42. 42.
    De Vries A, Holmes MC, Heijnis A et al (2007) Prenatal dexamethasone exposure induces changes in nonhuman primate offspring cardiometabolic and hypothalamic–pituitary–adrenal axis function. J Clin Invest 117:1058–1067PubMedPubMedCentralGoogle Scholar
  43. 43.
    De Weerth C, Buitelaar JK, Beijers R (2013) Infant cortisol and behavioural habituation to weekly maternal separations: links with maternal prenatal cortisol and psychosocial stress. Psychoneuroendocrinology 38(12):2863–2874PubMedGoogle Scholar
  44. 44.
    Beijers R, Jansen J, Riksen-Walraven M, de Weerth C (2010) Maternal prenatal anxiety and stress predict infant illnesses and health complaints. Pediatrics 126(2):e401–e409PubMedGoogle Scholar
  45. 45.
    Speirs HJ, Seckl JR, Brown RW (2004) Ontogeny of glucocorticoid receptor and 11beta-dydroxysteroid dehydrogenase type-1 gene expression identifies potential critical periods of glucocorticoid susceptibility during development. J Endocrinol 181(1):105–116PubMedGoogle Scholar
  46. 46.
    Mueller BR, Bale TL (2008) Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 28(36):9055–9065PubMedPubMedCentralGoogle Scholar
  47. 47.
    Brunton PJ, Russell JA (2011) Neuroendocrine control of maternal stress responses and fetal programming by stress in pregnancy. Prog Neuropsychopharmacol Biol Psychiatry 35(5):1178–1191PubMedGoogle Scholar
  48. 48.
    Hartikainen-Sorri AL, Kirkinen P, Sorri M, Anttonen H, Tuimala R (1991) No effect of experimental noise exposure on human pregnancy. Obstet Gynecol 77(4):611–615PubMedGoogle Scholar
  49. 49.
    Schulte HM, Weisner D, Allolia B (1990) The corticotrophin releasing hormone test in late pregnancy—a lack of adrenocorticotropin and cortisol response. Clin Endocrinol 33(1):99–106Google Scholar
  50. 50.
    NICHD (2011) Scientific vision workshop on pregnancy and pregnancy outcomes. Retrieved on March 7th from http://www.nichd.nih.gov/vision/vision_themes/pregnancy/Documents/Vision_Pregnancy_WP_042811.pdf
  51. 51.
    Drake AJ, Tang JI, Nyirenda MJ (2007) Mechanisms underlying the role of glucocorticoids in the early life programming of adult disease. Clin Sci 113(5):219–232PubMedGoogle Scholar
  52. 52.
    Mairesse J, Lesage J, Breton C et al (2007) Maternal stress alters endocrine function of the feto-placental unit in rats. Am J Physiol Endocrinol Metab 292(6):E1526–E1533PubMedGoogle Scholar
  53. 53.
    Welberg LA, Thrivikraman KV, Plotsky PM (2005) Chronic maternal stress inhibits the capacity to up-regulate placental 11beta-hydroxysteriod dehydrogenase type 2 activity. J Endocrinol 186(3):R7–R12PubMedGoogle Scholar
  54. 54.
    O’Donnell Bugge Jensen, Freeman L, Khalife N, O’Connor TG, Glover V (2012) Maternal prenatal anxiety and downregulation of placental 11β-HSD2. Psychoneuroendocrinology 37(6):818–826PubMedGoogle Scholar
  55. 55.
    Myatt L (2006) Placental adaptive responses and fetal programming. J Physiol 572:25–30PubMedPubMedCentralGoogle Scholar
  56. 56.
    Zijlmans M, de Weerth C, Riksen-Walraven JMA (submitted). A systematic review on the association between prenatal maternal cortisol and child outcomesGoogle Scholar
  57. 57.
    Sapolsky RM, Romero LM, Munck AU (2000) How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. Endocr Rev 21(1):55–89PubMedGoogle Scholar
  58. 58.
    Wroble-Diglan MC, Dietz LJ, Pienkosky TV (2009) Prediction of infant temperament from catecholamine and self-report measures of maternal stress during pregnancy. J Reprod Infant Psychol 27:374–389Google Scholar
  59. 59.
    Petraglia F, Hatch M, Lapinski R et al (2001) Lack of effect of psychosocial stress on maternal corticotropin-releasing factor and catecholamine levels at 28 weeks gestation. J Soc Gynecol Invest 8:83–88Google Scholar
  60. 60.
    Vähä-Eskeli KK, Erkkola RU, Scheinin M, Seppänen A (1992) Effects of short-term thermal stress on plasma catecholamine concentrations and plasma renin activity in pregnant and nonpregnant women. Am J Obstet Gynecol 167:785–789PubMedGoogle Scholar
  61. 61.
    Gu W, Jones CT (1986) The effect of elevation of maternal plasma catecholamines on the fetus and placenta of the pregnant sheep. J Dev Physiol 8(3):173–186PubMedGoogle Scholar
  62. 62.
    Chen CH, Klein DC, Robinson JC (1974) Catechol-O-methyltransferase in rat placenta, human placenta and choriocarcinoma grown in culture. J Reprod Fertil 39(2):407–410PubMedGoogle Scholar
  63. 63.
    Morgan CD, Sandler M, Panigel M (1972) Placental transfer of catecholamines in vitro and in vivo. Am J Obstet Gynecol 112:1068–1075PubMedGoogle Scholar
  64. 64.
    Saarikoski S (1974) Fate of noradrenaline in the human fetoplacental unit. Acta Physiol Scand 421:1–82Google Scholar
  65. 65.
    Sodha RJ, Proegler M, Schneider H (1984) Transfer and metabolism of norepinephrine studied from maternal-to-fetal and fetal-to-maternal sides in the in vitro perfused human placental lobe. Am J Obstet Gynecol 148:474–481PubMedGoogle Scholar
  66. 66.
    Merlot E, Couret D, Otten W (2008) Prenatal stress, fetal imprinting and immunity. Brain Behav Immun 22(1):42–51PubMedGoogle Scholar
  67. 67.
    Giannakoulopoulos X, Teixeira J, Fisk N, Glover V (1999) Human fetal and maternal noradrenaline responses to invasive procedures. Pediatr Res 45:494–499PubMedGoogle Scholar
  68. 68.
    Broadbent E, Koschwanez HE (2012) The psychology of wound healing. Curr Opin Psychiatry 25(2):135–140PubMedGoogle Scholar
  69. 69.
    Hasan KM, Rahman MS, Arif KM, Sobhani ME (2012) Psychological stress and aging: role of glucocorticoids (GCs). Age 34(6):1421–1433PubMedPubMedCentralGoogle Scholar
  70. 70.
    Kristenson M, Eriksen HR, Sluiter JK, Starke D, Ursin H (2004) Psychobiological mechanisms of socioeconomic differences in health. Soc Sci Med 58(8):1511–1522PubMedGoogle Scholar
  71. 71.
    Bernstein CN (2012) Why and where to look in the environment with regard to the etiology of inflammatory bowel disease. Dig Dis 3:28–32Google Scholar
  72. 72.
    Konturek PC, Brzozowski T, Konturek SJ (2011) Stress and the gut: pathophysiology, clinical consequences, diagnostic approach and treatment options. J Physiol Pharmacol 62(6):591–599PubMedGoogle Scholar
  73. 73.
    Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308(5722):648–652PubMedGoogle Scholar
  74. 74.
    Goldenberg RL, Culhane JF, Iams JD, Romero R (2008) Epidemiology and causes of preterm birth. The Lancet 371(9606):75–84Google Scholar
  75. 75.
    Coussons-Read ME, Okun ML, Schmitt MP, Giese S (2005) Prenatal stress alters cytokine levels in a manner that may endanger human pregnancy. Psychosom Med 67:625–631PubMedGoogle Scholar
  76. 76.
    Coussons-Read ME, Okun ML, Nettles CD (2007) Psychosocial stress increases inflammatory markers and alters cytokine production across pregnancy. Brain Behav Immun 21:343–350PubMedGoogle Scholar
  77. 77.
    Cryan JF, Dinan TG (2013) Unraveling the longstanding scars of early neurodevelopmental stress. Biol Psychiatry 74(11):788–789PubMedGoogle Scholar
  78. 78.
    Coe CL, Crispen HR (2000) Social stress in pregnant squirrel monkeys (Saimiri boliviensis peruviensis) differentially affects placental transfer of maternal antibody to male and female infants. Health Psychol 19(6):554–559PubMedGoogle Scholar
  79. 79.
    Entringer S, Kumsta R, Nelson EL, Hellhammer DH, Wadhwa PD, Wüst S (2008) Influence of prenatal psychosocial stress on cytokine production in adult women. Dev Psychobiol 50(6):579–587PubMedPubMedCentralGoogle Scholar
  80. 80.
    De Weerth C, Fuentes S, de Vos WM (2013) Crying in infants: On the possible role of intestinal microbiota in the development of colic. Gut Microbes 4:416–421PubMedPubMedCentralGoogle Scholar
  81. 81.
    Matamoros S, Gras-Leguen C, Le Vacon F, Potel G, de La Cochetiere MF (2013) Development of intestinal microbiota in infants and its impact on health. Trends Microbiol 21(4):167–173PubMedGoogle Scholar
  82. 82.
    Purchiaroni F, Tortora A, Gabrielli M et al (2013) The role of intestinal microbiota and the immune system. Eur Rev Med Pharmacol Sci. 17(3):323–333PubMedGoogle Scholar
  83. 83.
    Chen X, D’Souza R, Hong ST (2013) The role of gut microbiota in the gut-brain axis: current challenges and perspectives. Protein Cell 4(6):403–414PubMedGoogle Scholar
  84. 84.
    Foster JA, McVey Neufeld KA (2013) Gut-brain axis: how the microbiota influences anxiety and depression. Trends Neurosci 36(5):305–312PubMedGoogle Scholar
  85. 85.
    Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, Bienenstock J, Cryan JF (2011) Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci USA 108:16050–16055PubMedPubMedCentralGoogle Scholar
  86. 86.
    Jiménez E, Fernández L, Marín ML et al (2005) Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol 51(4):270–274PubMedGoogle Scholar
  87. 87.
    Jiménez E, Marín ML, Martín R et al (2008) Is meconium from healthy newborns actually sterile? Res Microbiol 159:187–193PubMedGoogle Scholar
  88. 88.
    De Weerth C, Fuentes S, Puylaert Ph, de Vos WM (2013) Intestinal microbiota of Infants with colic: development and specific signatures. Pediatrics 131(2):e550–e558PubMedGoogle Scholar
  89. 89.
    Grönlund MM, Grześkowiak Ł, Isolauri E, Salminen S (2011) Influence of mother’s intestinal microbiota on gut colonization in the infant. Gut Microbes 2(4):227–233PubMedGoogle Scholar
  90. 90.
    Collado MC, Cernada M, Baüerl C, Vento M, Pérez-Martínez G (2012) Microbial ecology and host-microbiota interactions during early life stages. Gut Microbes 3:352–365PubMedPubMedCentralGoogle Scholar
  91. 91.
    Bailey MT, Lubach GR, Coe CL (2004) Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr 38:414–421PubMedGoogle Scholar
  92. 92.
    Pärtty A, Kalliomäki M, Endo A, Salminen S, Isolauri E (2012) Compositional development of bifidobacterium and Lactobacillus microbiota is linked with crying and fussing in early infancy. PLoS ONE 7(3):e32495PubMedPubMedCentralGoogle Scholar
  93. 93.
    Chomitz VR, Cheung LW, Lieberman E (1995) The role of lifestyle in preventing low birth weight. Future Child 5(1):121–138PubMedGoogle Scholar
  94. 94.
    Lobel M, Cannella DL, Graham JE, DeVincent C, Schneider J, Meyer BA (2008) Pregnancy-specific stress, prenatal health behaviors, and birth outcomes. Health Psychol 27(5):604–615PubMedGoogle Scholar
  95. 95.
    Teegarden SL, Bale TL (2008) Effects of stress on dietary preference and intake are dependent on access and stress sensitivity. Physiol Behav 18:713–723Google Scholar
  96. 96.
    Hurley KM, Caulfield LE, Sacco LM, Costigan KA, DiPietro JA (2005) Psychosocial influences in dietary patterns during pregnancy. J Am Diet Assoc 105(6):963–966PubMedGoogle Scholar
  97. 97.
    Georgieff MK (2007) Nutrition and the developing brain: nutrient priorities and measurement. Am J Clin Nutr 85:614S–620SPubMedGoogle Scholar
  98. 98.
    Monk C, Georgieff MK, Osterholm EA (2013) Research review: maternal prenatal distress and poor nutrition—mutually influencing risk factors affecting infant neurocognitive development. J Child Psychol Psychiatry 54(2):115–130PubMedPubMedCentralGoogle Scholar
  99. 99.
    Pien GW, Schwab RJ (2004) Sleep disorders during pregnancy. Sleep 27:1405–1417PubMedGoogle Scholar
  100. 100.
    Facco FL, Liu CS, Cabello AA, Kick A, Grobman WA, Zee PC (2012) Sleep-disordered breathing: a risk factor for adverse pregnancy outcomes? Am J Perinatol 29:277–282PubMedGoogle Scholar
  101. 101.
    Okun ML, Kline CE, Roberts JM, Wettlaufer B, Glover K, Hall M (2013) Prevalence of sleep deficiency in early gestation and its associations with stress and depressive symtoms. J Womens Health 22:1028–1037Google Scholar
  102. 102.
    Okun ML, Schetter CD, Glynn LM (2011) Poor sleep quality is associated with preterm birth. Sleep 34:1493–1498PubMedPubMedCentralGoogle Scholar
  103. 103.
    Okun ML, Roberts JM, Marsland AL, Hall M (2009) How disturbed sleep may be a risk factor for adverse pregnancy outcomes. Obstet Gynecol Surv 64(4):273–280Google Scholar
  104. 104.
    Mor G (2008) Inflammation and pregnancy: the role of toll-like receptors in trophoblast-immune interaction. Ann NY Acad Sci 1127:121–128Google Scholar
  105. 105.
    Fluhr H, Krenzer S, Stein GM et al (2007) Interferon-gamma and tumor necrosis factor-alpha sensitize primarily resistant human endometrial stromal cells to Fas- mediated apoptosis. J Cell Sci 120:4126–4133PubMedGoogle Scholar
  106. 106.
    Salamonsen LA, Hannan NJ, Dimitriadis E (2007) Cytokines and chemokines during human embryo implantation: roles in implantation and early placentation. Seminin Reprod Med 25:437–444Google Scholar
  107. 107.
    Omisade A, Buxton OM, Rusak B (2010) Impact of acute sleep restriction on cortisol and leptin levels in young women. Physiol Behav 99:651–656PubMedGoogle Scholar
  108. 108.
    Field T (2012) Prenatal exercise research. Infant Behav Dev 35:397–407PubMedGoogle Scholar
  109. 109.
    Field T (2009) Complementary and alternative therapies research. American Psychological Association, Washington, DCGoogle Scholar
  110. 110.
    Borodulin K, Evenson KR, Monda K, Wen F, Herring AH, Dole N (2010) Physical activity and sleep among pregnant women. Peadiatr Perinatal Epidemiol 24:45–52Google Scholar
  111. 111.
    Struder HK, Hollmann W, Platen P, Wostmann R, Ferrauti A, Weber K (1997) Effects of exercise intensity on free trypophan to branched-chain amino acids ratio and plasma prolactin during endurance exercise. Can J Appl Physiol 22:280–291PubMedGoogle Scholar
  112. 112.
    Claesson IM, Klein S, Sydsjo G, Josefsson A (2014) Physical activity and psychological well-being in obese pregnant and postpartum women attending a weight-gain restriction programme. Midwifery 30:11–16PubMedGoogle Scholar
  113. 113.
    Barker DJ (2001) A new model for the origins of chronic disease. Med Health Care Philos 4(1):31–35PubMedGoogle Scholar
  114. 114.
    Gauthier TW, Drews-Botsch C, Falek A, Coles C, Brown LA (2005) Maternal alcohol abuse and neonatal infection. Alcohol Clin Exp Res 29(6):1035–1043PubMedGoogle Scholar
  115. 115.
    Ng SP, Zelikoff JT (2006) Smoking during pregnancy: subsequent effects on offspring immune competence and disease vulnerability in later life. Reprod Toxicol 23(3):428–437PubMedGoogle Scholar
  116. 116.
    Noakes PS, Holt PG, Prescott SL (2003) Maternal smoking in pregnancy alters neonatal cytokine responses. Allergy 58(10):1053–1058PubMedGoogle Scholar
  117. 117.
    Weissgerber TL, Wolfe LA, Davies GA, Mottola MF (2006) Exercise in the prevention and treatment of maternal-fetal disease: a review of the literature. Appl Physiol Nutr Metab 31(6):661–674PubMedGoogle Scholar
  118. 118.
    Saraceno L, Munafó M, Heron J, Craddock N, van den Bree MB (2009) Genetic and non-genetic influences on the development of co-occurring alcohol problem use and internalizing symptomatology in adolescence: a review. Addiction 7:1100–1121Google Scholar
  119. 119.
    Homberg JR, Lesch KP (2011) Looking on the bright side of serotonin transporter gene variation. Biol Psychiatry 69(6):513–519PubMedGoogle Scholar
  120. 120.
    Rice F, Harold GT, Boivin J, van den Bree M, Hay DF, Thapar A (2010) The links between prenatal stress and offspring development and psychopathology: disentangling environmental and inherited influences. Psychol Med 2:335–345Google Scholar
  121. 121.
    Meaney MJ (2010) Epigenetics and the biological definition of gene × environment interactions. Child Dev 81(1):41–79PubMedGoogle Scholar
  122. 122.
    Szyf M, Weaver I, Meaney M (2007) Maternal care, the epigenome and phenotypic differences in behavior. Reprod Toxicol 24(1):9–19PubMedGoogle Scholar
  123. 123.
    Appleton AA, Armstrong DA, Lesseur C, Lee J, Padbury JF, Lester BM, Marsit CJ (2013) Patterning in placental 11-B hydroxysteroid dehydrogenase methylation according to prenatal socioeconomic adversity. PLoS ONE 8(9):e74691PubMedPubMedCentralGoogle Scholar
  124. 124.
    Paternain L, Batlle MA, De la Garza AL et al (2012) Transcriptomic and epigenetic changes in the hypothalamus are involved in an increased susceptibility to a high-fat-sucrose diet in prenatally stressed female rats. Neuroendocrinology 96:249–260PubMedGoogle Scholar
  125. 125.
    Monk C, Spicer J, Champagne FA (2012) Linking prenatal maternal adversity to developmental outcomes in infants: the role of epigenetic pathways. Dev Psychopathol 24:1361–1376PubMedPubMedCentralGoogle Scholar
  126. 126.
    Reynolds RM, Labad J, Buss C, Ghaemmaghami P, Raikkonen K (2014) Transmitting biological effects of stress in utero: implications for mother and offspring. Psychoneuroendocrinology 38:1843–1849Google Scholar
  127. 127.
    Paulson JF, Dauber S, Leiferman JA (2006) Individual and combined effects of postpartum depression in mothers and fathers on parenting behavior. Pediatrics 118:659–668PubMedGoogle Scholar
  128. 128.
    Francis DD, Diorio J, Plotsky PM, Meaney MJ (2002) Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci 22:7840–7843PubMedGoogle Scholar
  129. 129.
    Morley-Fletcher S, Rea M, Maccari S, Laviola G (2003) Environmental enrichment during adolescence reverses the effects of prenatal stress on play behaviour and HPA axis reactivity in rats. Eur J Neurosci 18:3367–3374PubMedGoogle Scholar
  130. 130.
    Van Batenburg-Eddes T, Brion MJ, Henrichs J et al (2013) Parental depressive and anxiety symptoms during pregnancy and attention problems in children: a cross-cohort consistency study. J Child Psychol Psychiatry 54:591–600PubMedPubMedCentralGoogle Scholar
  131. 131.
    Boyce WT, Ellis BJ (2005) Biological sensitivity to context: i. An evolutionary-developmental theory of the origins and functions of stress reactivity. Dev Psychopathol 17:271–301PubMedGoogle Scholar
  132. 132.
    Pike IL (2005) Maternal stress and fetal responses: evolutionary perspectives on preterm delivery. Am J Hum Biol 17:55–65PubMedGoogle Scholar
  133. 133.
    DiPietro JA, Costigan KA, Gurewitsch ED (2003) Fetal response to induced maternal stress. Early Human Dev 74:125–138Google Scholar
  134. 134.
    Fink NS, Urech C, Berger CT (2010) Maternal laboratory stress influences fetal neurobehavior: cortisol does not provide all answers. J Mat Fet Neo Med 23:488–500Google Scholar
  135. 135.
    Clifton VL (2010) Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta 31:S33–S39PubMedGoogle Scholar
  136. 136.
    Sandman CA, Davis EP, Buss C, Glynn LM (2012) Exposure to prenatal psychobiological stress exerts programming influences on the mother and her fetus. Neuroendocrinology 95:7–21PubMedGoogle Scholar
  137. 137.
    Glover V, Hill J (2012) Sex differences in the programming effects of prenatal stress on psychopathology and stress responses: an evolutionary perspective. Physiol Behav 106(5):736–740PubMedGoogle Scholar
  138. 138.
    Moeller J, Lieb R, Meyer AH, Loetscher KQ, Krastel B, Meinlschmidt G (2014) Improving ambulatory saliva-sampling compliance in pregnant women: a randomized controlled study. PLoS ONE 22:e86204Google Scholar
  139. 139.
    Palmer AC (2011) Nutritionally mediated programming of the developing immune system. Adv Nutr 2(5):377–395PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Roseriet Beijers
    • 1
  • Jan K. Buitelaar
    • 2
    • 3
  • Carolina de Weerth
    • 1
  1. 1.Department of Developmental Psychology, Behavioral Science InstituteRadboud University NijmegenNijmegenThe Netherlands
  2. 2.Department of Cognitive NeuroscienceRadboud University Medical Centre, Donders Institute for Brain, Cognition and BehaviorNijmegenThe Netherlands
  3. 3.Karakter Child and Adolescent Psychiatry University CentreNijmegenThe Netherlands

Personalised recommendations