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Prenatal risk factors for depression: a critical review of the evidence and potential mechanisms

Published online by Cambridge University Press:  20 June 2014

E. C. Braithwaite ,
S. E. Murphy  and
P. G. Ramchandani
E. C. Braithwaite*
Affiliation:
Department of Psychiatry, University of Oxford, Warneford Hospital, Oxford, UK
S. E. Murphy
Affiliation:
Department of Psychiatry, University of Oxford, Warneford Hospital, Oxford, UK
P. G. Ramchandani
Affiliation:
Academic Unit of Child & Adolescent Psychiatry, Imperial College, St Mary’s Campus, London, UK
*
*Address for correspondence: E. Braithwaite, Department of Psychiatry, University of Oxford, Warneford Hospital, Oxford OX3 7JX, UK. (Email Elizabeth.braithwaite@psych.ox.ac.uk)
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Abstract

Exposure to adverse experiences in early life increases the risk of depression during adulthood. Recent findings have highlighted that exposure of a fetus to an adverse intrauterine environment may also have implications for later offspring depression. This review considers the status of the evidence for these associations and the potential mechanisms underlying prenatal developmental risks for later depression, addressing the challenging possibility that environmental predisposition to depression may begin before birth.

Keywords

depressionfetal programmingprenatal adversity
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 5 , Issue 5 , October 2014 , pp. 339 - 350
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2014 

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References

1.Wang, H, Dwyer-Lindgren, L, Lofgren, KT, et al. Age-specific and sex-specific mortality in 187 countries, 1970–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012; 380, 2071–2094.CrossRefGoogle ScholarPubMed
2.Kendler, KS, Gardner, CO, Neale, MC, et al.Genetic risk factors for major depression in men and women: similar or different heritabilities and same or partly distinct genes? Psychol Med. 2001; 31, 605–616.Google Scholar
3.Boyce, P, Parker, G, Barnett, B, et al.Personality as a vulnerability factor to depression. Br J Psychiatry. 1991; 159, 106–114.Google Scholar
4.Bruce, ML. Psychosocial risk factors for depressive disorders in late life. Biol Psychiatry. 2002; 52, 175–184.Google Scholar
5.Kilzieh, N, Rastam, S, Maziak, W, et al.Comorbidity of depression with chronic diseases: a population-based study in Aleppo, Syria. Int J Psychiatry Med. 2008; 38, 169–184.CrossRefGoogle ScholarPubMed
6.Kessler, RC, Magee, WJ. Childhood adversities and adult depression: basic patterns of association in a US national survey. Psychol Med. 1993; 23, 679–690.CrossRefGoogle Scholar
7.Kessler, RC, Davis, CG, Kendler, KS. Childhood adversity and adult psychiatric disorder in the US National Comorbidity Survey. Psychol Med. 1997; 27, 1101–1119.Google Scholar
8.Briere, J, Elliott, DM. Prevalence and psychological sequelae of self-reported childhood physical and sexual abuse in a general population sample of men and women. Child Abuse Negl. 2003; 27, 1205–1222.CrossRefGoogle Scholar
9.Lenze, SN, Xiong, C, Sheline, YI. Childhood adversity predicts earlier onset of major depression but not reduced hippocampal volume. Psychiatry Res. 2008; 162, 39–49.Google Scholar
10.Rudolph, K, Flynn, M. Childhood adversity and youth depression: influence of gender and pubertal status. Dev Psychopathol. 2007; 19, 497–521.Google Scholar
11.Schilling, EA, Aseltine, RH Jr, Gore, S. Adverse childhood experiences and mental health in young adults: a longitudinal survey. BMC Public Health. 2007; 7, 30.Google Scholar
12.O’Connor, TG, Heron, J, Glover, V. Antenatal anxiety predicts child behavioral/emotional problems independently of postnatal depression. J Am Acad Child Adolesc Psychiatry. 2002; 41, 1470–1477.Google Scholar
13.Van den Bergh, BR, Mulder, EJ, Mennes, M, et al. Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. A review. Neurosci Biobehav Rev. 2005; 29, 237–258.Google Scholar
14.Talge, NM, Neal, C, Glover, V. Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? J Child Psychol Psychiatry. 2007; 48, 245–261.CrossRefGoogle ScholarPubMed
15.Van den Bergh, BRH, Van Calster, B, Smits, T, et al.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. 2007; 33, 536–545.Google Scholar
16.Barker, DJ, Winter, PD, Osmond, C, et al.Weight in infancy and death from ischaemic heart disease. Lancet. 1989; 2, 577–580.Google Scholar
17.Barker, DJ. Fetal origins of cardiovascular disease Ann Med. 1999; 31(Suppl. 1), 3–6.Google Scholar
18.Glover, V. Annual research review: prenatal stress and the origins of psychopathology: an evolutionary perspective. J Child Psychol Psychiatry. 2011; 52, 356–367.Google Scholar
19.Jaddoe, VWV, Troe, E.-J.W.M., Hofman, A, et al.Active and passive maternal smoking during pregnancy and the risks of low birthweight and preterm birth: the Generation R Study. Paediatr Perinat Epidemiol. 2008; 22, 162–171.Google Scholar
20.Misra, DP, Nguyen, RH. Environmental tobacco smoke and low birth weight: a hazard in the workplace? Environ Health Perspect. 1999; 107(Suppl. 6), 897–904.CrossRefGoogle ScholarPubMed
21.Lieberman, E, Gremy, I, Lang, JM, et al.Low birthweight at term and the timing of fetal exposure to maternal smoking. Am J Public Health. 1994; 84, 1127–1131.Google Scholar
22.Newton, RW, Hunt, LP. Psychosocial stress in pregnancy and its relation to low birth weight. Br Med J. 1984; 288, 1191–1194.CrossRefGoogle ScholarPubMed
23.Brown, SJ, Yelland, JS, Sutherland, GA, et al.Stressful life events, social health issues and low birthweight in an Australian population-based birth cohort: challenges and opportunities in antenatal care. BMC Public Health. 2011; 11, 196.Google Scholar
24.Bhagwanani, SG, Seagraves, K, Dierker, LJ, et al.Relationship between prenatal anxiety and perinatal outcome in nulliparous women: a prospective study. JAMA. 1997; 89, 93–98.Google Scholar
25.Barker, DJ. The developmental origins of adult disease. J Am Coll Nutr. 2004; 23(6), 588S–595S.Google Scholar
26.Huxley, R, Owen, CG, Whincup, PH, et al.Is birth weight a risk factor for ischemic heart disease in later life? Am J Clin Nutr. 2007; 85, 1244–1250.CrossRefGoogle ScholarPubMed
27.Barker, DJ, Bagby, SP, Hanson, MA. Mechanisms of disease: in utero programming in the pathogenesis of hypertension. Nat Clin Pract Nephrol. 2006; 2, 700–707.Google Scholar
28.Whincup, PH, Kaye, SJ, Owen, CG, et al.Birth weight and risk of type 2 diabetes: a systematic review. JAMA. 2008; 300, 2886–2897.Google Scholar
29.Thompson, C, Syddall, H, Rodin, I, et al.Birth weight and the risk of depressive disorder in late life. Br J Psychiatry. 2001; 179, 450–455.CrossRefGoogle ScholarPubMed
30.Bellingham-Young, DA, Adamson-Macedo, EN. Foetal origins theory: links with adult depression and general self-efficacy. Neuro Endocrinol Lett. 2003; 24, 412–416.Google Scholar
31.Gale, C, Martyn, C. Birth weight and later risk of depression in a national birth cohort. Br J Psychiatry. 2004; 184, 28–33.Google Scholar
32.Alati, R, Lawlor, DA, Mamun, AA, 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, 575–582.Google Scholar
33.Costello, EJ, Worthman, C, Erkanli, A, et al.Prediction from low birth weight to female adolescent depression: a test of competing hypotheses. Arch Gen Psychiatry. 2007; 64, 338–344.CrossRefGoogle ScholarPubMed
34.Mallen, C, Mottram, S, Thomas, E. Birth factors and common mental health problems in young adults: a population-based study in North Staffordshire. Soc Psychiatry Psychiatr Epidemiol. 2008; 43, 325–330.Google Scholar
35.Gudmundsson, P, Andersson, S, Gustafson, D, et al.Depression in Swedish women: relationship to factors at birth. Eur J Epidemiol. 2011; 26, 55–60.Google Scholar
36.Osler, M, Nordentoft, M, Andersen, AM. Birth dimensions and risk of depression in adulthood: cohort study of Danish men born in 1953. Br J Psychiatry. 2005; 186 400–403.Google Scholar
37.Raikkonen, K, Pesonen, AK, Kajantie, E, et al.Length of gestation and depressive symptoms at age 60 years. Br J Psychiatry. 2007; 190, 469–474.Google Scholar
38.Inskip, HM, Dunn, N, Godfrey, KM, et al.Is birth weight associated with risk of depressive symptoms in young women? Evidence from the Southampton Women's Survey. Am J Epidemiol. 2008; 167, 164–168.CrossRefGoogle ScholarPubMed
39.Vasiliadis, HM, Gilman, SE, Buka, SL. Fetal growth restriction and the development of major depression. Acta Psychiatr Scand. 2008; 117, 306–312.Google Scholar
40.Wojcik, W, Lee, W, Colman, I, et al.Foetal origins of depression? A systematic review and meta-analysis of low birth weight and later depression. Psychol Med. 2012; 43, 1–12.Google Scholar
41.Haavind, S, Bergin, I, Brubakk, AM. Mental health, school and leisure time of adolescents born “small for gestational age”. Tidsskr Nor Laegeforen. 2007; 127, 1933–1937.Google Scholar
42.Smith, CA. The effect of wartime starvation in Holland upon pregnancy and its product. Am J Obstet Gynecol. 1947; 53, 599–608.Google Scholar
43.Stein, AD, Ravelli, AC, Lumey, LH. Famine, third-trimester pregnancy weight gain, and intrauterine growth: the Dutch Famine Birth Cohort Study. Hum Biol. 1995; 67, 135–150.Google Scholar
44.Stein, AD, Kahn, HS, Rundle, A, et al. Anthropometric measures in middle age after exposure to famine during gestation: evidence from the Dutch famine. Am J Clin Nutr. 2007; 85, 869–876.Google Scholar
45.Stein, AD, Zybert, PA, van der Pal-de Bruin, K, et al.Exposure to famine during gestation, size at birth, and blood pressure at age 59 y: evidence from the Dutch Famine. Eur J Epidemiol. 2006; 21, 759–765.Google Scholar
46.Painter, RC, de Rooij, SR, Bossuyt, PM, et al.Early onset of coronary artery disease after prenatal exposure to the Dutch famine. Am J Clin Nutr. 2006; 84 322–327, quiz 466–327.Google Scholar
47.Roseboom, T, de Rooij, S, Painter, R. The Dutch famine and its long-term consequences for adult health. Early Hum Dev. 2006; 82 485–491.Google Scholar
48.Brown, AS, van Os, J, Driessens, C, et al.Further evidence of relation between prenatal famine and major affective disorder. Am J Psychiatry. 2000; 157, 190–195.Google Scholar
49.Stein, AD, Pierik, FH, Verrips, GH, et al.Maternal exposure to the Dutch famine before conception and during pregnancy: quality of life and depressive symptoms in adult offspring. Epidemiology. 2009; 20, 909–915.Google Scholar
50.Monk, C, Georgieff, MK, Osterholm, EA. Research review: maternal prenatal distress and poor nutrition–mutually influencing risk factors affecting infant neurocognitive development. J Child Psychol Psychiatry. 2013; 54, 115–130.Google Scholar
51.Micali, N, Stahl, D, Treasure, J, et al.Childhood psychopathology in children of women with eating disorders: understanding risk mechanisms. J Child Psycholo Psychiatry. 2014; 55, 124–134.Google Scholar
52.Micali, N, De Stavola, B, Ploubidis, GB, et al.The effects of maternal eating disorders on offspring childhood and early adolescent psychiatric disorders. Int J Eat Disord. 2013.Google Scholar
53.O’Connor, TG, Heron, J, Golding, J, et al.Maternal antenatal anxiety and children's behavioural/emotional problems at 4 years. Report from the Avon Longitudinal Study of Parents and Children. Br J Psychiatry. 2002; 180, 502–508.Google Scholar
54.Field, T. Prenatal depression effects on early development: a review. Infant Behav Dev. 2011; 34, 1–14.Google Scholar
55.Pawlby, S, Hay, D, Sharp, D, et al. Antenatal depression and offspring psychopathology: the influence of childhood maltreatment. Br J Psychiatry. 2011; 199, 106–112.Google Scholar
56.Pearson, RM, Evans, J, Koundali, D, et al. Maternal depression during pregnancy and the postnatal period: risks and possible mechanisms for offspring depression at 18 years. JAMA Psychiatry. 2013; 70, 1312–1319.Google Scholar
57.Hellemans, KGC, Sliwowska, JH, Verma, P, et al. Prenatal alcohol exposure: fetal programming and later life vulnerability to stress, depression and anxiety disorders. Neurosci Biobehav Rev. 2010; 34, 791–807.Google Scholar
58.Mattson, SN, Crocker, N, Nguyen, TT. Fetal alcohol spectrum disorders: neuropsychological and behavioral features. Neuropsychol Rev. 2011; 21, 81–101.CrossRefGoogle ScholarPubMed
59.Famy, C, Streissguth, AP, Unis, AS. Mental illness in adults with fetal alcohol syndrome or fetal alcohol effects. Am J Psychiatry. 1998; 155, 552–554.Google Scholar
60.O’Connor, MJ, Kasari, C. Prenatal alcohol exposure and depressive features in children. Alcohol Clin Exp Res. 2000; 24, 1084–1092.Google Scholar
61.O’Connor, MJ, Paley, B. The relationship of prenatal alcohol exposure and the postnatal environment to child depressive symptoms. J Pediatr Psychol. 2006; 31, 50–64.Google Scholar
62.Barr, HM, Bookstein, FL, O’Malley, KD, et al.Binge drinking during pregnancy as a predictor of psychiatric disorders on the Structured Clinical Interview for DSM-IV in young adult offspring. Am J Psychiatry. 2006; 163, 1061–1065.Google Scholar
63.Liu, T, Gatsonis, CA, Baylin, A, et al. Maternal smoking during pregnancy and anger temperament among adult offspring. J Psychiatr Res. 2011; 45, 1648–1654.Google Scholar
64.Cornelius, MD, De Genna, NM, Leech, SL, et al.Effects of prenatal cigarette smoke exposure on neurobehavioral outcomes in 10-year-old children of adolescent mothers. Neurotoxicol Teratol. 2011; 33, 137–144.Google Scholar
65.Fergusson, DM, Woodward, LJ, Horwood, LJ. Maternal smoking during pregnancy and psychiatric adjustment in late adolescence. Arch Gen Psychiatry. 1998; 55, 721–727.Google Scholar
66.Menezes, AM, Murray, J, Laszlo, M, et al.Happiness and depression in adolescence after maternal smoking during pregnancy: birth cohort study. PLoS One. 2013; 8, e80370.Google Scholar
67.Goldschmidt, L, Richardson, GA, Cornelius, MD, et al.Prenatal marijuana and alcohol exposure and academic achievement at age 10. Neurotoxicol Teratol. 2004; 26, 521–532.Google Scholar
68.Gray, KA, Day, NL, Leech, S, et al.Prenatal marijuana exposure: effect on child depressive symptoms at ten years of age. Neurotoxicol Teratol. 2005; 27, 439–448.Google Scholar
69.Leech, SL, Larkby, CA, Day, R, et al. Predictors and correlates of high levels of depression and anxiety symptoms among children at age 10. J Am Acad Child Adolesc Psychiatry. 2006; 45, 223–230.Google Scholar
70.Weinstock, M. Alterations induced by gestational stress in brain morphology and behaviour of the offspring. Prog Neurobiol. 2001; 65, 427–451.Google Scholar
71.Abe, H, Hidaka, N, Kawagoe, C, et al. Prenatal psychological stress causes higher emotionality, depression-like behavior, and elevated activity in the hypothalamo-pituitary-adrenal axis. Neurosci Res. 2007; 59, 145–151.Google Scholar
72.Trezza, V, Campolongo, P, Cassano, T, et al. Effects of perinatal exposure to delta-9-tetrahydrocannabinol on the emotional reactivity of the offspring: a longitudinal behavioral study in Wistar rats. Psychopharmacology. 2008; 198, 529–537.Google Scholar
73.O’Shea, M, McGregor, IS, Mallet, PE. Repeated cannabinoid exposure during perinatal, adolescent or early adult ages produces similar longlasting deficits in object recognition and reduced social interaction in rats. J Psychopharmacol. 2006; 20, 611–621.Google Scholar
74.Levinson, DF. The genetics of depression: a review. Biol Psychiatry. 2006; 60, 84–92.Google Scholar
75.Sullivan, PF, Neale, MC, Kendler, KS. Genetic epidemiology of major depression: review and meta-analysis. Am J Psychiatry. 2000; 157, 1552–1562.Google Scholar
76.Caspi, A, Sugden, K, Moffitt, TE, et al.Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science. 2003; 301, 386–389.Google Scholar
77.Ribeiro, L, Busnello, JV, Cantor, RM, et al.The brain-derived neurotrophic factor rs6265 (Val66Met) polymorphism and depression in Mexican-Americans. Neuroreport. 2007; 18, 1291–1293.Google Scholar
78.Hek, K, Demirkan, A, Lahti, J, et al. A genome-wide association study of depressive symptoms. Biol Psychiatry. 2013; 73, 667–678.Google Scholar
79.Lewis, CM, Ng, MY, Butler, AW, et al.Genome-wide association study of major recurrent depression in the U.K. population. Am J Psychiatry. 2010; 167, 949–957.Google Scholar
80.Wray, NR, Pergadia, ML, Blackwood, DH, et al.Genome-wide association study of major depressive disorder: new results, meta-analysis, and lessons learned. Mol Psychiatry. 2012; 17, 36–48.Google Scholar
81.Major Depressive Disorder Working Group of the Psychiatric GWAS Consortium, Ripke, S, Wray, NR, et al.A mega-analysis of genome-wide association studies for major depressive disorder. Mol Psychiatry. 2013; 18, 497–511.Google ScholarPubMed
82.Rice, F, Harold, GT, Boivin, J, et al. The links between prenatal stress and offspring development and psychopathology: disentangling environmental and inherited influences. Psychol Med. 2010; 40, 335–345.Google Scholar
83.Leigh, B, Milgrom, J. Risk factors for antenatal depression, postnatal depression and parenting stress. BMC Psychiatry. 2008; 8, 24.Google Scholar
84.Champagne, FA, Meaney, MJ. Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model Biol Psychiatry. 2006; 59, 1227–1235.Google Scholar
85.Lewis, SJ, Relton, C, Zammit, S, et al. Approaches for strengthening causal inference regarding prenatal risk factors for childhood behavioural and psychiatric disorders. J Child Psychol Psychiatry. 2013; 54, 1095–1108.Google Scholar
86.Owens, M, Herbert, J, Jones, PB, et al.Elevated morning cortisol is a stratified population-level biomarker for major depression in boys only with high depressive symptoms. Proc Natl Acad Sci U S Am. 2014; 111, 3638–3643.Google Scholar
87.Bhagwagar, Z, Hafizi, S, Cowen, PJ. Increased salivary cortisol after waking in depression. Psychopharmacology (Berl). 2005; 182, 54–57.Google Scholar
88.Mannie, ZN, Harmer, CJ, Cowen, PJ. Increased waking salivary cortisol levels in young people at familial risk of depression. Am J Psychiatry. 2007; 164, 617–621.CrossRefGoogle ScholarPubMed
89.Portella, MJ, Harmer, CJ, Flint, J, et al.Enhanced early morning salivary cortisol in neuroticism. Am J Psychiatry. 2005; 162, 807–809.Google Scholar
90.Bhagwagar, Z, Hafizi, S, Cowen, PJ. Increase in concentration of waking salivary cortisol in recovered patients with depression. Am J Psychiatry. 2003; 160, 1890–1891.Google Scholar
91.Carnegie, R, Araya, R, Ben-Shlomo, Y, et al.Cortisol awakening response and subsequent depression: prospective longitudinal study. Br J Psychiatry. 2014; 204, 137–143.Google Scholar
92.Strickland, P, Morriss, R, Wearden, A, et al.A comparison of salivary cortisol in chronic fatigue syndrome, community depression and healthy controls. J Affect Disord. 1998; 47, 191–194.Google Scholar
93.Vreeburg, SA, Hoogendijk, WG, van Pelt, J, et al. Major depressive disorder and hypothalamic-pituitary-adrenal axis activity: results from a large cohort study. Arch Gen Psychiatry. 2009; 66, 617–626.Google Scholar
94.Doane, LD, Mineka, S, Zinbarg, RE, et al. Are flatter diurnal cortisol rhythms associated with major depression and anxiety disorders in late adolescence? The role of life stress and daily negative emotion. Dev Psychopathol. 2013; 25, 629–642.Google Scholar
95.Davis, EP, Glynn, LM, Waffarn, F, et al. Prenatal maternal stress programs infant stress regulation. J Child Psychol Psychiatry. 2011; 52, 119–129.Google Scholar
96.Brennan, PA, Pargas, R, Walker, EF, et al. Maternal depression and infant cortisol: influences of timing, comorbidity and treatment. J Child Psychol Psychiatry. 2008; 49, 1099–1107.Google Scholar
97.O’Connor, TG, Ben-Shlomo, Y, Heron, J, et al.Prenatal anxiety predicts individual differences in cortisol in pre-adolescent children. Biol Psychiatry. 2005; 58, 211–217.Google Scholar
98.Maccari, S, Darnaudery, M, Morley-Fletcher, S, et al. Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev. 2003; 27, 119–127.Google Scholar
99.Witzmann, SR, Turner, JD, Meriaux, SB, et al.Epigenetic regulation of the glucocorticoid receptor promoter 1(7) in adult rats. Epigenetics. 2012; 7, 1290–1301.Google Scholar
100.Liu, D, Diorio, J, Tannenbaum, B, et al.Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science. 1997; 277, 1659–1662.Google Scholar
101.Weaver, IC, Cervoni, N, Champagne, FA, et al.Epigenetic programming by maternal behavior Nat Neurosci. 2004; 7, 847–854.CrossRefGoogle ScholarPubMed
102.McGowan, PO, Sasaki, A, D'Alessio, AC, et al. Epigenetic regulation of the glucocorticoid receptor in human brain associates with childhood abuse. Nat Neurosci. 2009; 12, 342–348.Google Scholar
103.Oberlander, TF, Weinberg, J, Papsdorf, M, et al. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics. 2008; 3, 97–106.Google Scholar
104.Mairesse, J, Lesage, J, Breton, C, et al. Maternal stress alters endocrine function of the feto-placental unit in rats. Am J Physiol Endocrinol Metab. 2007; 292, E1526–E1533.Google Scholar
105.Glover, V, Bergman, K, Sarkar, P, et al. Association between maternal and amniotic fluid cortisol is moderated by maternal anxiety. Psychoneuroendocrinology. 2009; 34, 430–435.Google Scholar
106.O’Donnell, KJ, Bugge Jensen, A, Freeman, L, et al. Maternal prenatal anxiety and downregulation of placental 11beta-HSD2. Psychoneuroendocrinology. 2012; 37, 818–826.Google Scholar
107.Jensen Pena, C, Monk, C, Champagne, FA. Epigenetic effects of prenatal stress on 11beta-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain. PLoS One. 2012; 7, e39791.Google Scholar
108.Monk, C, Myers, MM, Sloan, RP, et al. Effects of women's stress-elicited physiological activity and chronic anxiety on fetal heart rate. J Dev Behav Pediatr. 2003; 24, 32–38.Google Scholar
109.Giannakoulopoulos, X, Teixeira, J, Fisk, N, et al. Human fetal and maternal noradrenaline responses to invasive procedures. Pediatr Res. 1999; 45(Pt 1), 494–499.Google Scholar
110.Teixeira, JM, Fisk, NM, Glover, V. Association between maternal anxiety in pregnancy and increased uterine artery resistance index: cohort based study. BMJ. 1999; 318, 153–157.Google Scholar
111.Stevens, AD, Lumbers, ER. Effects of intravenous infusions of noradrenaline into the pregnant ewe on uterine blood flow, fetal renal function, and lung liquid flow. Can J Physiol pharmacol. 1995; 73, 202–208.Google Scholar
112.Shnider, SM, Wright, RG, Levinson, G, et al. Uterine blood flow and plasma norepinephrine changes during maternal stress in the pregnant ewe. Anesthesiology. 1979; 50, 524–527.Google Scholar
113.Coe, CL, Lubach, GR, Karaszewski, JW, et al. Prenatal endocrine activation alters postnatal cellular immunity in infant monkeys. Brain Behav Immun. 1996; 10, 221–234.CrossRefGoogle ScholarPubMed
114.Kay, G, Tarcic, N, Poltyrev, T, et al. Prenatal stress depresses immune function in rats. Physiol Behav. 1998; 63, 397–402.Google Scholar
115.Coe, CL, Kramer, M, Kirschbaum, C, et al. Prenatal stress diminishes the cytokine response of leukocytes to endotoxin stimulation in juvenile rhesus monkeys. J Clin Endocrinol Metab. 2002; 87, 675–681.Google Scholar
116.Merlot, E, Couret, D, Otten, W. Prenatal stress, fetal imprinting and immunity. Brain Behav Immun. 2008; 22, 42–51.Google Scholar
117.Couret, D, Jamin, A, Kuntz-Simon, G, et al. Maternal stress during late gestation has moderate but long-lasting effects on the immune system of the piglets. Vet Immunol Immunopathol. 2009; 131, 17–24.Google Scholar
118.Diz-Chaves, Y, Astiz, M, Bellini, MJ, et al. Prenatal stress increases the expression of proinflammatory cytokines and exacerbates the inflammatory response to LPS in the hippocampal formation of adult male mice. Brain Behav Immun. 2013; 28, 196–206.Google Scholar
119.Lefevre, F, Moreau, D, Semon, E, et al. Maternal depression related to infant's wheezing. Pediatr Allergy Immunol. 2011; 22, 608–613.Google Scholar
120.Khashan, AS, Wicks, S, Dalman, C, et al. Prenatal stress and risk of asthma hospitalization in the offspring: a Swedish population-based study. Psychosom Med. 2012; 74, 635–641.Google Scholar
121.Nielsen, NM, Hansen, AV, Simonsen, J, et al. Prenatal stress and risk of infectious diseases in offspring. Am J Epidemiol. 2011; 173, 990–997.Google Scholar
122.Duijts, L, Bakker-Jonges, LE, Labout, JA, et al. Perinatal stress influences lymphocyte subset counts in neonates. The generation R study Pediatr Res. 2008; 63, 292–298.Google Scholar
123.Wright, RJ, Visness, CM, Calatroni, A, et al. Prenatal maternal stress and cord blood innate and adaptive cytokine responses in an inner-city cohort. Am J Respir Crit Care Med. 2010; 182, 25–33.Google Scholar
124.O’Connor, TG, Winter, MA, Hunn, J, et al. Prenatal maternal anxiety predicts reduced adaptive immunity in infants. Brain, Behaviour, and Immunity. 2013; 32, 21–28.Google Scholar