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

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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.

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References

  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):115–142

    PubMed  Google Scholar 

  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 14:590–603

    PubMed  Google Scholar 

  3. Seckl JR, Meaney MJ (2004) Glucocorticoid programming. Ann NY Acad Sci 1032:63–84

    PubMed  CAS  Google Scholar 

  4. De Weerth C, Buitelaar JK (2005) Physiological stress reactivity in human pregnancy—a review. Neurosci Biobehav Rev 29:295–312

    PubMed  Google Scholar 

  5. Matthews SG, Phillips DI (2012) Transgenerational inheritance of stress pathology. Exp Neurol 233:95–101

    PubMed  Google Scholar 

  6. Bale TL, Baram TZ, Brown AS (2010) Early life programming and neurodevelopmental disorders. Biol Psychiatry 68(4):314–319

    PubMed  PubMed Central  Google Scholar 

  7. Charil A, Laplante DP, Vaillancourt C, King S (2010) Prenatal stress and brain development. Brain Res Rev 65:56–79

    PubMed  Google Scholar 

  8. Glover V (2011) Annual research review: prenatal stress and the origins of psychopathology: an evolutionary perspective. J Child Psychol Psychiatry 52(4):356–367

    PubMed  Google Scholar 

  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):7–21

    PubMed  Google Scholar 

  10. Swanson JD, Wadhwa PM (2008) Developmental origins of child mental health disorders. J Child Psychol Psychiatry 49(10):1009–1019

    PubMed  PubMed Central  Google Scholar 

  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 48:245–261

    PubMed  Google Scholar 

  12. Lobel M, Dunkel-Schetter C (1990) Conceptualizing stress to study effects on health: environmental, perceptual, and emotional components. Anx Res 3:213–230

    Google Scholar 

  13. Lobel M, Dunkel-Schetter C, Scrimshaw SC (1992) Prenatal maternal stress and prematurity: a prospective study of socioeconomically disadvantaged women. Health Psychol 11:32–40

    PubMed  CAS  Google Scholar 

  14. Alderdice F, Lynn F, Lobel M (2012) A review and psychometric evaluation of pregnancy-specific stress measures. J Psychosom Obstet Gynaecol 33(2):62–77

    PubMed  Google Scholar 

  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):81–91

    PubMed  Google Scholar 

  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):53–65

    PubMed  CAS  Google Scholar 

  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):141–148

    PubMed  Google Scholar 

  18. Field T (2011) Prenatal depression effects on early development: a review. Inf Beh Dev 34:1–14

    Google Scholar 

  19. Glover V, O’Connor TG, O’Donnell K (2010) Prenatal stress and the programming of the HPA axis. Neurosci Biobehav Rev 35(1):17–22

    PubMed  CAS  Google Scholar 

  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):33–53

    PubMed  CAS  PubMed Central  Google Scholar 

  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):604–613

    PubMed  CAS  Google Scholar 

  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:e39791

    Google Scholar 

  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):631–645

    PubMed  Google Scholar 

  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 35:141–153

    PubMed  PubMed Central  Google Scholar 

  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 30:1078–1086

    PubMed  Google Scholar 

  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):320–327

    PubMed  PubMed Central  Google Scholar 

  27. Seckl JR (2008) Glucocorticoids, developmental ‘programming’ and the risk of affective dysfunction. Prog Brain Res 167:17–34

    PubMed  CAS  Google Scholar 

  28. Rodriguez A, Bohlin G (2005) Are maternal smoking and stress during pregnancy related to ADHD symptoms in children? J Child Psychol Psychiatry 46:246–254

    PubMed  Google Scholar 

  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 75:1085–1097

    PubMed  Google Scholar 

  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):38–43

    PubMed  Google Scholar 

  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 65:146–152

    Google Scholar 

  32. Markham JA, Koenig JI (2011) Prenatal stress: role in psychotic and depressive diseases. Psychopharmacology 214(1):89–106

    PubMed  CAS  PubMed Central  Google Scholar 

  33. Howerton CL, Bale TL (2012) Prenatal programing: at the intersection of maternal stress and immune activation. Horm Behav 62(3):237–242

    PubMed  PubMed Central  Google Scholar 

  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):579–587

  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):434–445

  36. Huizink AC (2012) Prenatal substance use, prenatal stress and offspring behavioural outcomes: considerations for future studies. Nord J Psychiatry 66(2):115–122

    PubMed  Google Scholar 

  37. Gitau R, Cameron A, Fisk NM, Glover V (1998) Fetal exposure to maternal cortisol. Lancet 352(9129):707–708

    PubMed  CAS  Google Scholar 

  38. Majzoub JA, Karalis KP (1999) Placental corticotropin-releasing hormone: function and regulation. Am J Obstet Gynecol 180:S242–S246

    PubMed  CAS  Google Scholar 

  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 191:1063–1069

    PubMed  CAS  Google Scholar 

  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 101:2174–2181

    PubMed  CAS  PubMed Central  Google Scholar 

  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–E82

    PubMed  Google Scholar 

  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 117:1058–1067

    PubMed  PubMed Central  Google Scholar 

  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):2863–2874

    PubMed  Google Scholar 

  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–e409

    PubMed  Google Scholar 

  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):105–116

    PubMed  CAS  Google Scholar 

  46. Mueller BR, Bale TL (2008) Sex-specific programming of offspring emotionality after stress early in pregnancy. J Neurosci 28(36):9055–9065

    PubMed  CAS  PubMed Central  Google Scholar 

  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):1178–1191

    PubMed  CAS  Google Scholar 

  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):611–615

    PubMed  CAS  Google Scholar 

  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):99–106

    CAS  Google Scholar 

  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. 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):219–232

    PubMed  CAS  Google Scholar 

  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–E1533

    PubMed  CAS  Google Scholar 

  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–R12

    PubMed  CAS  Google Scholar 

  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):818–826

    PubMed  Google Scholar 

  55. Myatt L (2006) Placental adaptive responses and fetal programming. J Physiol 572:25–30

    PubMed  CAS  PubMed Central  Google Scholar 

  56. Zijlmans M, de Weerth C, Riksen-Walraven JMA (submitted). A systematic review on the association between prenatal maternal cortisol and child outcomes

  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):55–89

    PubMed  CAS  Google Scholar 

  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 27:374–389

    Google Scholar 

  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 8:83–88

    CAS  Google Scholar 

  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 167:785–789

    PubMed  Google Scholar 

  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):173–186

    PubMed  CAS  Google Scholar 

  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):407–410

    PubMed  CAS  Google Scholar 

  63. Morgan CD, Sandler M, Panigel M (1972) Placental transfer of catecholamines in vitro and in vivo. Am J Obstet Gynecol 112:1068–1075

    PubMed  CAS  Google Scholar 

  64. Saarikoski S (1974) Fate of noradrenaline in the human fetoplacental unit. Acta Physiol Scand 421:1–82

    CAS  Google Scholar 

  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 148:474–481

    PubMed  CAS  Google Scholar 

  66. Merlot E, Couret D, Otten W (2008) Prenatal stress, fetal imprinting and immunity. Brain Behav Immun 22(1):42–51

    PubMed  CAS  Google Scholar 

  67. Giannakoulopoulos X, Teixeira J, Fisk N, Glover V (1999) Human fetal and maternal noradrenaline responses to invasive procedures. Pediatr Res 45:494–499

    PubMed  CAS  Google Scholar 

  68. Broadbent E, Koschwanez HE (2012) The psychology of wound healing. Curr Opin Psychiatry 25(2):135–140

    PubMed  Google Scholar 

  69. Hasan KM, Rahman MS, Arif KM, Sobhani ME (2012) Psychological stress and aging: role of glucocorticoids (GCs). Age 34(6):1421–1433

    PubMed  CAS  PubMed Central  Google Scholar 

  70. Kristenson M, Eriksen HR, Sluiter JK, Starke D, Ursin H (2004) Psychobiological mechanisms of socioeconomic differences in health. Soc Sci Med 58(8):1511–1522

    PubMed  CAS  Google Scholar 

  71. Bernstein CN (2012) Why and where to look in the environment with regard to the etiology of inflammatory bowel disease. Dig Dis 3:28–32

    Google Scholar 

  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):591–599

    PubMed  CAS  Google Scholar 

  73. Sapolsky RM (2005) The influence of social hierarchy on primate health. Science 308(5722):648–652

    PubMed  CAS  Google Scholar 

  74. Goldenberg RL, Culhane JF, Iams JD, Romero R (2008) Epidemiology and causes of preterm birth. The Lancet 371(9606):75–84

    Google Scholar 

  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 67:625–631

    PubMed  CAS  Google Scholar 

  76. Coussons-Read ME, Okun ML, Nettles CD (2007) Psychosocial stress increases inflammatory markers and alters cytokine production across pregnancy. Brain Behav Immun 21:343–350

    PubMed  CAS  Google Scholar 

  77. Cryan JF, Dinan TG (2013) Unraveling the longstanding scars of early neurodevelopmental stress. Biol Psychiatry 74(11):788–789

    PubMed  Google Scholar 

  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):554–559

    PubMed  CAS  Google Scholar 

  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):579–587

    PubMed  CAS  PubMed Central  Google Scholar 

  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 4:416–421

    PubMed  PubMed Central  Google Scholar 

  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):167–173

    PubMed  CAS  Google Scholar 

  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):323–333

    PubMed  CAS  Google Scholar 

  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):403–414

    PubMed  Google Scholar 

  84. Foster JA, McVey Neufeld KA (2013) Gut-brain axis: how the microbiota influences anxiety and depression. Trends Neurosci 36(5):305–312

    PubMed  CAS  Google Scholar 

  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 108:16050–16055

    PubMed  CAS  PubMed Central  Google Scholar 

  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):270–274

    PubMed  Google Scholar 

  87. Jiménez E, Marín ML, Martín R et al (2008) Is meconium from healthy newborns actually sterile? Res Microbiol 159:187–193

    PubMed  Google Scholar 

  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–e558

    PubMed  Google Scholar 

  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):227–233

    PubMed  Google Scholar 

  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 3:352–365

    PubMed  PubMed Central  Google Scholar 

  91. Bailey MT, Lubach GR, Coe CL (2004) Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr 38:414–421

    PubMed  Google Scholar 

  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):e32495

    PubMed  PubMed Central  Google Scholar 

  93. Chomitz VR, Cheung LW, Lieberman E (1995) The role of lifestyle in preventing low birth weight. Future Child 5(1):121–138

    PubMed  CAS  Google Scholar 

  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):604–615

    PubMed  Google Scholar 

  95. Teegarden SL, Bale TL (2008) Effects of stress on dietary preference and intake are dependent on access and stress sensitivity. Physiol Behav 18:713–723

    Google Scholar 

  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):963–966

    PubMed  Google Scholar 

  97. Georgieff MK (2007) Nutrition and the developing brain: nutrient priorities and measurement. Am J Clin Nutr 85:614S–620S

    PubMed  CAS  Google Scholar 

  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):115–130

    PubMed  PubMed Central  Google Scholar 

  99. Pien GW, Schwab RJ (2004) Sleep disorders during pregnancy. Sleep 27:1405–1417

    PubMed  Google Scholar 

  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 29:277–282

    PubMed  Google Scholar 

  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 22:1028–1037

    Google Scholar 

  102. Okun ML, Schetter CD, Glynn LM (2011) Poor sleep quality is associated with preterm birth. Sleep 34:1493–1498

    PubMed  PubMed Central  Google Scholar 

  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):273–280

  104. Mor G (2008) Inflammation and pregnancy: the role of toll-like receptors in trophoblast-immune interaction. Ann NY Acad Sci 1127:121–128

  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 120:4126–4133

    PubMed  CAS  Google Scholar 

  106. Salamonsen LA, Hannan NJ, Dimitriadis E (2007) Cytokines and chemokines during human embryo implantation: roles in implantation and early placentation. Seminin Reprod Med 25:437–444

    CAS  Google Scholar 

  107. Omisade A, Buxton OM, Rusak B (2010) Impact of acute sleep restriction on cortisol and leptin levels in young women. Physiol Behav 99:651–656

    PubMed  CAS  Google Scholar 

  108. Field T (2012) Prenatal exercise research. Infant Behav Dev 35:397–407

    PubMed  Google Scholar 

  109. Field T (2009) Complementary and alternative therapies research. American Psychological Association, Washington, DC

    Google Scholar 

  110. Borodulin K, Evenson KR, Monda K, Wen F, Herring AH, Dole N (2010) Physical activity and sleep among pregnant women. Peadiatr Perinatal Epidemiol 24:45–52

    Google Scholar 

  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 22:280–291

    PubMed  CAS  Google Scholar 

  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 30:11–16

    PubMed  Google Scholar 

  113. Barker DJ (2001) A new model for the origins of chronic disease. Med Health Care Philos 4(1):31–35

    PubMed  CAS  Google Scholar 

  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):1035–1043

    PubMed  Google Scholar 

  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):428–437

    PubMed  Google Scholar 

  116. Noakes PS, Holt PG, Prescott SL (2003) Maternal smoking in pregnancy alters neonatal cytokine responses. Allergy 58(10):1053–1058

    PubMed  CAS  Google Scholar 

  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):661–674

    PubMed  Google Scholar 

  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 7:1100–1121

    Google Scholar 

  119. Homberg JR, Lesch KP (2011) Looking on the bright side of serotonin transporter gene variation. Biol Psychiatry 69(6):513–519

    PubMed  CAS  Google Scholar 

  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 2:335–345

    Google Scholar 

  121. Meaney MJ (2010) Epigenetics and the biological definition of gene × environment interactions. Child Dev 81(1):41–79

    PubMed  Google Scholar 

  122. Szyf M, Weaver I, Meaney M (2007) Maternal care, the epigenome and phenotypic differences in behavior. Reprod Toxicol 24(1):9–19

    PubMed  CAS  Google Scholar 

  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):e74691

    PubMed  CAS  PubMed Central  Google Scholar 

  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 96:249–260

    PubMed  CAS  Google Scholar 

  125. Monk C, Spicer J, Champagne FA (2012) Linking prenatal maternal adversity to developmental outcomes in infants: the role of epigenetic pathways. Dev Psychopathol 24:1361–1376

    PubMed  PubMed Central  Google Scholar 

  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 38:1843–1849

    Google Scholar 

  127. Paulson JF, Dauber S, Leiferman JA (2006) Individual and combined effects of postpartum depression in mothers and fathers on parenting behavior. Pediatrics 118:659–668

    PubMed  Google Scholar 

  128. Francis DD, Diorio J, Plotsky PM, Meaney MJ (2002) Environmental enrichment reverses the effects of maternal separation on stress reactivity. J Neurosci 22:7840–7843

    PubMed  CAS  Google Scholar 

  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 18:3367–3374

    PubMed  Google Scholar 

  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 54:591–600

    PubMed  PubMed Central  Google Scholar 

  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 17:271–301

    PubMed  Google Scholar 

  132. Pike IL (2005) Maternal stress and fetal responses: evolutionary perspectives on preterm delivery. Am J Hum Biol 17:55–65

    PubMed  Google Scholar 

  133. DiPietro JA, Costigan KA, Gurewitsch ED (2003) Fetal response to induced maternal stress. Early Human Dev 74:125–138

    Google Scholar 

  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 23:488–500

    CAS  Google Scholar 

  135. Clifton VL (2010) Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta 31:S33–S39

    PubMed  Google Scholar 

  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 95:7–21

    PubMed  Google Scholar 

  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):736–740

    PubMed  CAS  Google Scholar 

  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:e86204

    Google Scholar 

  139. Palmer AC (2011) Nutritionally mediated programming of the developing immune system. Adv Nutr 2(5):377–395

    PubMed  CAS  PubMed Central  Google Scholar 

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Correspondence to Jan K. Buitelaar.

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Beijers, R., Buitelaar, J.K. & de Weerth, C. Mechanisms underlying the effects of prenatal psychosocial stress on child outcomes: beyond the HPA axis. Eur Child Adolesc Psychiatry 23, 943–956 (2014). https://doi.org/10.1007/s00787-014-0566-3

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