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Does Prenatal Maternal Distress Contribute to Sex Differences in Child Psychopathology?

  • Laurel M. Hicks
  • Danielle A. Swales
  • Sarah E. Garcia
  • Camille Driver
  • Elysia Poggi DavisEmail author
Sex and Gender Issues in Behavioral Health (CN Epperson and L Hantsoo, Section Editors)
  • 10 Downloads
Part of the following topical collections:
  1. Topical Collection on Sex and Gender Issues in Behavioral Health

Abstract

Purpose of Review

Prenatal maternal psychological distress is an established risk factor for the development of psychopathology in offspring. The purpose of this review is to evaluate whether sex differences in fetal responses to maternal distress contribute to sex differences in subsequent psychopathology.

Recent Findings

Male and female fetuses respond differently to stress signals. We review recent evidence that demonstrates a sex-specific pattern of association between prenatal maternal distress and pathways associated with risk for psychopathology including offspring hypothalamic pituitary adrenocortical (HPA) axis regulation, brain development, and negative emotionality.

Summary

Prenatal maternal distress exerts sex-specific consequences on the fetus. These differences may contribute to the well-established sex differences in psychopathology and in particular to greater female vulnerability to develop internalizing problems.

Keywords

Prenatal Stress Sex differences Depression Development Psychopathology 

Notes

Funding information

This work supported by the National Institutes of Health [R01 MH 109662; RO1 HD065823; P50MH 096889].

Compliance with Ethics Guidelines

Conflict of Interest

The authors declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. 1.
    Bale TL, Epperson CN. Sex differences and stress across the lifespan. Nat Neurosci. 2015;18(10):1413–20.  https://doi.org/10.1038/nn.4112.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Kessler RC, Berglund P, Demler O, Jin R, Koretz D, Merikangas KR, et al. The epidemiology of major depressive disorder: results from the national comorbidity survey replication (ncs-r). JAMA. 2003;289(23):3095–105.  https://doi.org/10.1001/jama.289.23.3095.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Kessler RC, Chiu W, Demler O, Walters EE. Prevalence, severity, and comorbidity of 12-month dsm-iv disorders in the national comorbidity survey replication. Arch Gen Psychiatry. 2005;62(6):617–27.  https://doi.org/10.1001/archpsyc.62.6.617.CrossRefPubMedPubMedCentralGoogle Scholar
  4. 4.
    Eme R. Sex differences in the prevalence and expression of externalizing behavior. In: Beauchaine TP, Hinshaw SP, editors. The Oxford Handbook of Externalizing Spectrum Disorders. New York: Oxford University Press; 2016. p. 239–62.Google Scholar
  5. 5.
    Rutter M, Caspi A, Moffitt TE. Using sex differences in psychopathology to study causal mechanisms: unifying issues and research strategies. J Child Psychol Psychiatry Allied Discip. 2003;44(8):1092–115.  https://doi.org/10.1111/1469-7610.00194.CrossRefGoogle Scholar
  6. 6.
    • Sandman CA, Glynn LM, Davis EP. Is there a viability–vulnerability tradeoff? Sex differences in fetal programming. J Psychosom Res. 2013;75(4):327–35.  https://doi.org/10.1016/j.jpsychores.2013.07.009 This study presents evidence that there is a “viability-vulnerability trade off”. Specifically, under conditions of prenatal exposure to adversity, male fetuses are directly impacted via precipitous declines in their mortality and morbidity. Although females are spared this early hit to their survival, their vulnerability may be revealed later in development. CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Davis EP, Pfaff D. Sexually dimorphic responses to early adversity: implications for affective problems and autism spectrum disorder. Psychoneuroendocrinology. 2014;49:11–25.  https://doi.org/10.1016/j.psyneuen.2014.06.014.CrossRefPubMedGoogle Scholar
  8. 8.
    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.  https://doi.org/10.1016/j.physbeh.2012.02.011.CrossRefPubMedGoogle Scholar
  9. 9.
    Bourgeois J-P, Goldman-Rakic PS, Rakic P. Synaptogenesis in the prefrontal cortex of rhesus monkeys. Cereb Cortex. 1994;4(1):78–96.  https://doi.org/10.1093/cercor/4.1.78.CrossRefPubMedGoogle Scholar
  10. 10.
    Barker DJ. The fetal and infant origins of adult disease. BMJ. 1990;301(6761):1111.CrossRefGoogle Scholar
  11. 11.
    Godfrey KM, Barker DJ. Fetal programming and adult health. Public Health Nutr. 2001;4(2b):611–24.CrossRefGoogle Scholar
  12. 12.
    Dunkel Schetter C, Tanner L. Anxiety, depression and stress in pregnancy: implications for mothers, children, research, and practice. Curr Opin Psychiatry. 2012;25(2):141–8.  https://doi.org/10.1097/YCO.0b013e3283503680.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Van den Bergh BR, Mulder EJ, Mennes M, Glover V. Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. A review. Neurosci Biobehav Rev. 2005;29(2):237–58.  https://doi.org/10.1016/j.neubiorev.2004.10.007.CrossRefPubMedGoogle Scholar
  14. 14.
    Kapoor A, Dunn E, Kostaki A, Andrews MH, Matthews SG. Fetal programming of hypothalamo-pituitary-adrenal function: prenatal stress and glucocorticoids. J Phys. 2006;572(Pt 1):31–44.  https://doi.org/10.1113/jphysiol.2006.105254.CrossRefGoogle Scholar
  15. 15.
    Marcus SM. Depression during pregnancy: rates, risks and consequences—Motherisk update 2008. Can J Clin Pharmacol. 2009;16(1):e15–22.Google Scholar
  16. 16.
    Grote NK, Bridge JA, Gavin AR, Melville JL, Iyengar S, Katon WJ. A meta-analysis of depression during pregnancy and the risk of preterm birth, low birth weight, and intrauterine growth restriction. Arch Gen Psychiatry. 2010;67(10):1012–24.  https://doi.org/10.1001/archgenpsychiatry.2010.111.CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Accortt EE, Cheadle AC, Schetter CD. Prenatal depression and adverse birth outcomes: an updated systematic review. Matern Child Health J. 2015;19(6):1306–37.  https://doi.org/10.1007/s10995-014-1637-2.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Austin M-P, Hadzi-Pavlovic D, Leader L, Saint K, Parker G. Maternal trait anxiety, depression and life event stress in pregnancy: relationships with infant temperament. Early Hum Dev. 2005;81(2):183–90.  https://doi.org/10.1016/j.earlhumdev.2004.07.001.CrossRefPubMedGoogle Scholar
  19. 19.
    de Bruijn AT, van Bakel HJ, Wijnen H, Pop VJ, van Baar AL. Prenatal maternal emotional complaints are associated with cortisol responses in toddler and preschool aged girls. Dev Psychobiol. 2009;51(7):553–63.  https://doi.org/10.1002/dev.20393.CrossRefPubMedGoogle Scholar
  20. 20.
    Sandman CA, Buss C, Head K, Davis EP. Fetal exposure to maternal depressive symptoms is associated with cortical thickness in late childhood. Biol Psychiatry. 2015;77(4):324–34.  https://doi.org/10.1016/j.biopsych.2014.06.025.CrossRefPubMedGoogle Scholar
  21. 21.
    Glover V, O'connor TG. Effects of antenatal stress and anxiety: implications for development and psychiatry. Br J Psychiatry J Ment Sci. 2002;180(5):389–91.  https://doi.org/10.1192/bjp.180.5.389.CrossRefGoogle Scholar
  22. 22.
    Essau CA, Sasagawa S, Lewinsohn PM, Rohde P. The impact of pre- and perinatal factors on psychopathology in adulthood. J Affect Disord. 2018;236:52–9.  https://doi.org/10.1016/j.jad.2018.04.088.CrossRefPubMedGoogle Scholar
  23. 23.
    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.  https://doi.org/10.1017/S0954579414000029.CrossRefPubMedGoogle Scholar
  24. 24.
    Luoma I, Tamminen T, Kaukonen P, Laippala P, Puura K, Salmelin R, et al. Longitudinal study of maternal depressive symptoms and child well-being. J Am Acad Child Adolesc Psychiatry. 2001;40(12):1367–74.  https://doi.org/10.1097/00004583-200112000-00006.CrossRefPubMedGoogle Scholar
  25. 25.
    Capron LE, Glover V, Pearson RM, Evans J, O’Connor TG, Stein A, et al. Associations of maternal and paternal antenatal mood with offspring anxiety disorder at age 18 years. J Affect Disord. 2015;187:20–6.  https://doi.org/10.1016/j.jad.2015.08.012.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Ashley JM, Harper BD, Arms-Chavez CJ, LoBello SG. Estimated prevalence of antenatal depression in the US population. Arch Womens Ment Health. 2016;19(2):395–400.  https://doi.org/10.1007/s00737-015-0593-1.CrossRefPubMedGoogle Scholar
  27. 27.
    Dennis C-L, Falah-Hassani K, Shiri R. Prevalence of antenatal and postnatal anxiety: systematic review and meta-analysis. British J Psychiatry. 2017;210(5):315–23.  https://doi.org/10.1192/bjp.bp.116.187179.CrossRefGoogle Scholar
  28. 28.
    Hicks LM, Dayton CJ, Victor BG. Depressive and trauma symptoms in expectant, risk-exposed, mothers and fathers: is mindfulness a buffer? J Affect Disord. 2018;238:179–86.  https://doi.org/10.1016/j.jad.2018.05.044.CrossRefPubMedGoogle Scholar
  29. 29.
    Jallo N, Elswick RK Jr, Kinser P, Masho S, Price SK, Svikis DS. Prevalence and predictors of depressive symptoms in pregnant African American women. Issues Ment Health Nurs. 2015;36(11):860–9.  https://doi.org/10.3109/01612840.2015.1048014.CrossRefPubMedGoogle Scholar
  30. 30.
    Chung TK, Lau TK, Yip AS, Chiu HF, Lee DT. Antepartum depressive symptomatology is associated with adverse obstetric and neonatal outcomes. Psychosom Med. 2001;63(5):830–4.  https://doi.org/10.1097/00006842-200109000-00017.CrossRefGoogle Scholar
  31. 31.
    Da-Silva V, Moraes-Santos A, Carvalho M, Martins M, Teixeira N. Prenatal and postnatal depression among low income Brazilian women. Braz J Med Biol Res. 1998;31(6):799–804.  https://doi.org/10.1590/S0100-879x1998000600012.CrossRefGoogle Scholar
  32. 32.
    Vohr BR, Davis EP, Wanke CA, Krebs NF. Neurodevelopment: the impact of nutrition and inflammation during preconception and pregnancy in low-resource settings. Pediatrics. 2017;139(Supplement 1):S38–49.  https://doi.org/10.1542/peds.2016-2828F.CrossRefPubMedGoogle Scholar
  33. 33.
    Buss C, Davis EP, Shahbaba B, Pruessner JC, Head K, Sandman CA. Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems. Proc Natl Acad Sci. 2012;109(20):201201295–E1319.  https://doi.org/10.1073/pnas.1201295109.CrossRefGoogle Scholar
  34. 34.
    • Carpenter T, Grecian S, Reynolds R. Sex differences in early-life programming of the hypothalamic–pituitary–adrenal axis in humans suggest increased vulnerability in females: a systematic review. J Dev Orig Health Dis. 2017;8(2):244–55.  https://doi.org/10.1017/S204017441600074X This systematic review reports that exposure to adversity during the prenatal period exerts stronger consequences on the HPA axis for girls as compared to boys. Sex-specific consequences of prenatal adversity on the HPA axis may contribute to sex differences in vulnerability to subsequent disease. CrossRefPubMedGoogle Scholar
  35. 35.
    Trivers R, Willard DE. Natural selection of parental ability to vary the sex ratio of offspring. Science. 1973;179(4068):90–2.  https://doi.org/10.1126/science.179.4068.90.CrossRefPubMedGoogle Scholar
  36. 36.
    Trivers R. Parental investment and sexual selection. In: Gruyter AD, editor. Sexual selection & the descent of man. New York: Aldine Publishing Company; 1972. p. 136–79.Google Scholar
  37. 37.
    Petraglia F, Florio P, Gallo R, Simoncini T, Saviozzi M, Di Blasio AM, et al. Human placenta and fetal membranes express human urocortin mRNA and peptide. J Clin Endocrinol Metab. 1996;81(10):3807–10.  https://doi.org/10.1210/jcem.81.10.8855842.CrossRefPubMedGoogle Scholar
  38. 38.
    DiPietro JA, Costigan KA, Kivlighan KT, Chen P, Laudenslager ML. Maternal salivary cortisol differs by fetal sex during the second half of pregnancy. Psychoneuroendocrinology. 2011;36(4):588–91.  https://doi.org/10.1016/j.psyneuen.2010.09.005.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Giesbrecht GF, Campbell T, Letourneau N, Team AS. Sexually dimorphic adaptations in basal maternal stress physiology during pregnancy and implications for fetal development. Psychoneuroendocrinology. 2015;56:168–78.  https://doi.org/10.1016/j.psyneuen.2015.03.013.CrossRefPubMedGoogle Scholar
  40. 40.
    Edwards CR, Benediktsson R, Lindsay RS, Seckl JR. Dysfunction of placental glucocorticoid barrier: link between fetal environment and adult hypertension? Lancet. 1993;341(8841):355–7.CrossRefGoogle Scholar
  41. 41.
    Gitau R, Cameron A, Fisk NM, Glover V. Fetal exposure to maternal cortisol. Lancet. 1998;352(9129):707–8.  https://doi.org/10.1016/S0140-6736(05)60824-0.CrossRefPubMedGoogle Scholar
  42. 42.
    • Clifton VL. Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta. 2010;31:S33–S9.  https://doi.org/10.1016/j.placenta.2009.11.010 This paper proposes that sexually dimorphic responses of the placenta to prenatal signals of adversity contribute to sex differences in fetal growth as well as to morbidity and mortality. This author suggests that male and female fetuses employ different placental responses to adversity and that these differences contribute to neonatal outcomes and survival. CrossRefPubMedGoogle Scholar
  43. 43.
    Mina TH, Räikkönen K, Riley SC, Norman JE, Reynolds RM. Maternal distress associates with placental genes regulating fetal glucocorticoid exposure and IGF2: role of obesity and sex. J Psychoneuroendocrinology. 2015;59:112–22.  https://doi.org/10.1016/j.psyneuen.2015.05.004.CrossRefGoogle Scholar
  44. 44.
    Osei-Kumah A, Smith R, Jurisica I, Caniggia I, Clifton V. Sex-specific differences in placental global gene expression in pregnancies complicated by asthma. Placenta. 2011;32(8):570–8.  https://doi.org/10.1016/j.placenta.2011.05.005.CrossRefPubMedGoogle Scholar
  45. 45.
    St-Pierre J, Laplante DP, Elgbeili G, Dawson PA, Kildea S, King S, et al. Natural disaster-related prenatal maternal stress is associated with alterations in placental glucocorticoid system: the QF2011 Queensland flood study. Psychoneuroendocrinology. 2018;94:38–48.  https://doi.org/10.1016/j.psyneuen.2018.04.027.CrossRefPubMedGoogle Scholar
  46. 46.
    Seth S, Lewis AJ, Saffery R, Lappas M, Galbally M. Maternal prenatal mental health and placental 11β-HSD2 gene expression: initial findings from the mercy pregnancy and emotional wellbeing study. Int J Mol Sci. 2015;16(11):27482–96.  https://doi.org/10.3390/ijms161126034.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    O’Donnell KJ, Jensen AB, Freeman L, Khalife N, O’Connor TG, Glover V. Maternal prenatal anxiety and downregulation of placental 11β-HSD2. Psychoneuroendocrinology. 2012;37(6):818–26.  https://doi.org/10.1016/j.psyneuen.2011.09.014.CrossRefPubMedGoogle Scholar
  48. 48.
    Conradt E, Adkins DE, Crowell SE, Monk C, Kobor MS. An epigenetic pathway approach to investigating associations between prenatal exposure to maternal mood disorder and newborn neurobehavior. Dev Psychopathol. 2018;30(3):881–90.  https://doi.org/10.1017/S0954579418000688.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    DiPietro JA, Voegtline KM. The gestational foundation of sex differences in development and vulnerability. J Neurosci. 2017;342:4–20.  https://doi.org/10.1016/j.neuroscience.2015.07.068.CrossRefGoogle Scholar
  50. 50.
    Doyle C, Werner E, Feng T, Lee S, Altemus M, Isler JR, et al. Pregnancy distress gets under fetal skin: maternal ambulatory assessment & sex differences in prenatal development. Dev Psychobiol. 2015;57(5):607–25.  https://doi.org/10.1002/dev.21317.CrossRefPubMedPubMedCentralGoogle Scholar
  51. 51.
    Glynn LM, Sandman CA. Sex moderates associations between prenatal glucocorticoid exposure and human fetal neurological development. Dev Sci. 2012;15(5):601–10.  https://doi.org/10.1111/j.1467-7687.2012.01159.x.CrossRefPubMedGoogle Scholar
  52. 52.
    Quesada AA, Tristao RM, Pratesi R, Wolf OT. Hyper-responsiveness to acute stress, emotional problems and poorer memory in former preterm children. Stress. 2014;17(5):389–99.  https://doi.org/10.3109/10253890.2014.949667.CrossRefPubMedGoogle Scholar
  53. 53.
    Alexander N, Rosenlöcher F, Stalder T, Linke J, Distler W, Morgner J, et al. Impact of antenatal synthetic glucocorticoid exposure on endocrine stress reactivity in term-born children. J Clin Endocrinol Metab. 2012;97(10):3538–44.  https://doi.org/10.1210/jc.2012-1970.CrossRefPubMedGoogle Scholar
  54. 54.
    Ping EY, Laplante DP, Elgbeili G, Hillerer KM, Brunet A, O’Hara MW, et al. Prenatal maternal stress predicts stress reactivity at 2½ years of age: the Iowa flood study. Psychoneuroendocrinology. 2015;56:62–78.  https://doi.org/10.1016/j.psyneuen.2015.02.015.CrossRefGoogle Scholar
  55. 55.
    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.  https://doi.org/10.1038/sj.npp.1301450.CrossRefPubMedGoogle Scholar
  56. 56.
    Stonawski V, Frey S, Golub Y, Rohleder N, Kriebel J, Goecke TW, et al. Associations of prenatal depressive symptoms with DNA methylation of HPA axis-related genes and diurnal cortisol profiles in primary school-aged children. Dev Psychopathol. 2018:1–13.  https://doi.org/10.1017/S0954579418000056.
  57. 57.
    Adam EK, Quinn ME, Tavernier R, McQuillan MT, Dahlke KA, Gilbert KE. Diurnal cortisol slopes and mental and physical health outcomes: a systematic review and meta-analysis. J Psychoneuroendocrinology. 2017;83:25–41.  https://doi.org/10.1016/j.psyneuen.2017.05.018.CrossRefGoogle Scholar
  58. 58.
    Roozendaal B, Barsegyan A, Lee S. Adrenal stress hormones, amygdala activation, and memory for emotionally arousing experiences. Prog Brain Res. 2007;167:79–97.  https://doi.org/10.1016/S0079-6123(07)67006-X.CrossRefGoogle Scholar
  59. 59.
    • Wen D, Poh J, Ni S, Chong Y, Chen H, Kwek K, et al. Influences of prenatal and postnatal maternal depression on amygdala volume and microstructure in young children. Transl Psychiatry. 2017;7(4):e1103.  https://doi.org/10.1038/tp.2017.74 In this large prospective cohort prenatal maternal depressive symptoms predict enlarged amygdala volume in girls, but not boys after covarying postnatal maternal depressive symptoms. Postnatal depressive symptoms, did not predict amygdala volume, but were associated with microstructure of the right amygdala only in girls. CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    Soe NN, Wen DJ, Poh JS, Chong YS, Broekman BF, Chen H, et al. Perinatal maternal depressive symptoms alter amygdala functional connectivity in girls. Hum Brain Mapp. 2018;39(2):680–90.  https://doi.org/10.1002/hbm.23873.CrossRefPubMedGoogle Scholar
  61. 61.
    • Graham AM, Rasmussen JM, Entringer S, Ben Ward E, Rudolph MD, Gilmore JH, et al. Maternal cortisol concentrations during pregnancy and sex specific associations with neonatal amygdala connectivity and emerging internalizing behaviors. Biol Psychiatry. 2018.  https://doi.org/10.1016/j.biopsych.2018.06.023 In this recent longitudinal study, that elevated maternal cortisol predicts neonatal functional connectivity in the amygdala and higher internalizing symptoms in 2 year-old girls, but not boys. Functional connectivity of the amygdala mediated the association between prenatal maternal stress and child internalizing problems in girls.
  62. 62.
    Dean DC III, Planalp EM, Wooten W, et al. Association of prenatal maternal depression and anxiety symptoms with infant white matter microstructure. JAMA Pediatr. 2018;172(10):973–81.  https://doi.org/10.1001/jamapediatrics.2018.2132.CrossRefPubMedGoogle Scholar
  63. 63.
    Kim D-J, Davis EP, Sandman CA, Sporns O, O'Donnell BF, Buss C, et al. Prenatal maternal cortisol has sex-specific associations with child brain network properties. Cereb Cortex. 2016;27(11):5230–41.  https://doi.org/10.1093/cercor/bhw303.CrossRefPubMedCentralGoogle Scholar
  64. 64.
    • Sandman CA, Curran MM, Davis EP, Glynn LM, Head K, Baram TZ. Cortical thinning and neuropsychiatric outcomes in children exposed to prenatal adversity: a role for placental CRH? Am J Psychiatr. 2018;175(5):471–9.  https://doi.org/10.1176/appi.ajp.2017.16121433 Results of this prospective and longitudinal study revealed that elevated prenatal placental CRH concentrations predicted cortical thinning in childhood. The impact of placental CRH on cortical thinness is stronger among girls as compared to boys. These sex specific consequences of placental CRH on the developing brain may contribute to greater female vulnerability to internalizing psychopathology. CrossRefPubMedGoogle Scholar
  65. 65.
    Madigan S, Oatley H, Racine N, Fearon RMP, Schumacher L, Akbari E, et al. A meta-analysis of maternal prenatal depression and anxiety on child socioemotional development. J Am Acad Child Adolesc Psychiatry. 2018;57(9):645–57 e8.  https://doi.org/10.1016/j.jaac.2018.06.012.CrossRefPubMedGoogle Scholar
  66. 66.
    Korja R, Nolvi S, Grant KA, McMahon C. The relations between maternal prenatal anxiety or stress and child’s early negative reactivity or self-regulation: a systematic review. Child Psychiatry Hum Dev. 2017;48(6):851–69.  https://doi.org/10.1007/s10578-017-0709-0.CrossRefPubMedGoogle Scholar
  67. 67.
    Compas BE, Connor-Smith J, Jaser SS. Temperament, stress reactivity, and coping: implications for depression in childhood and adolescence. J Clin Child Adolesc Psychol. 2004;33(1):21–31.  https://doi.org/10.1207/S15374424JCCP33013.CrossRefPubMedGoogle Scholar
  68. 68.
    Nigg JT. Temperament and developmental psychopathology. J Child Psychol Psychiatry. 2006;47(3–4):395–422.  https://doi.org/10.1111/j.1469-7610.2006.01612.x.CrossRefPubMedGoogle Scholar
  69. 69.
    Braithwaite EC, Pickles A, Sharp H, Glover V, O'Donnell KJ, Tibu F, et al. Maternal prenatal cortisol predicts infant negative emotionality in a sex-dependent manner. Physiol Behav. 2017;175:31–6.  https://doi.org/10.1016/j.physbeh.2017.03.017.CrossRefPubMedPubMedCentralGoogle Scholar
  70. 70.
    Sharp H, Hill J, Hellier J, Pickles A. Maternal antenatal anxiety, postnatal stroking and emotional problems in children: outcomes predicted from pre-and postnatal programming hypotheses. Psychol Med. 2015;45(2):269–83.  https://doi.org/10.1017/S0033291714001342.CrossRefPubMedGoogle Scholar
  71. 71.
    Swales DA, Winiarski DA, Smith AK, Stowe ZN, Newport DJ, Brennan PA. Maternal depression and cortisol in pregnancy predict offspring emotional reactivity in the preschool period. Dev Psychobiol. 2018;60(5):557–66.  https://doi.org/10.1002/dev.21631.CrossRefPubMedGoogle Scholar
  72. 72.
    Soe NN, Wen DJ, Poh JS, Li Y, Broekman BFP, Chen H, et al. Pre- and post-natal maternal depressive symptoms in relation with infant frontal function, connectivity, and behaviors. PLoS One. 2016;11(4):e0152991.  https://doi.org/10.1371/journal.pone.0152991.CrossRefPubMedPubMedCentralGoogle Scholar
  73. 73.
    Glynn LM, Howland MA, Sandman CA, Davis EP, Phelan M, Baram TZ, et al. Prenatal maternal mood patterns predict child temperament and adolescent mental health. J Affect Disord. 2018;228:83–90.  https://doi.org/10.1016/j.jad.2017.11.065.CrossRefPubMedGoogle Scholar
  74. 74.
    Hill J, Pickles A, Wright N, Quinn JP, Murgatroyd C, Sharp H. Maternal depression and child behaviours: sex-dependent mediation by glucocorticoid receptor gene methylation in a longitudinal study from pregnancy to age 5 years. bioRxiv. 2017:187351.  https://doi.org/10.1101/187351.
  75. 75.
    Davis EP, Sandman CA. Prenatal psychobiological predictors of anxiety risk in preadolescent children. Psychoneuroendocrinology. 2012;37(8):1224–33.  https://doi.org/10.1016/j.psyneuen.2011.12.016.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    • Quarini C, Pearson RM, Stein A, Ramchandani PG, Lewis G, Evans J. Are female children more vulnerable to the long-term effects of maternal depression during pregnancy? J Affect Disord. 2016;189:329–35.  https://doi.org/10.1016/j.jad.2015.09.039 This longitudinal study finds that girls of prenatally depressed mothers were at higher risk for depression diagnosis at 18 years of age, compared to boys. This finding remained even after covarying effects of postnatal maternal depression as well as other confounds. CrossRefPubMedPubMedCentralGoogle Scholar
  77. 77.
    Hay DF, Pawlby S, Waters CS, Perra O, Sharp D. Mothers’ antenatal depression and their children’s antisocial outcomes. Child Dev. 2010;81(1):149–65.  https://doi.org/10.1111/j.1467-8624.2009.01386.x.CrossRefPubMedGoogle Scholar
  78. 78.
    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.  https://doi.org/10.1111/j.1467-8624.2004.00727.xC.CrossRefPubMedGoogle Scholar
  79. 79.
    Barker ED, Oliver BR, Viding E, Salekin RT, Maughan B. The impact of prenatal maternal risk, fearless temperament and early parenting on adolescent callous-unemotional traits: a 14-year longitudinal investigation. J Child Psychol Psychiatry. 2011;52(8):878–88.  https://doi.org/10.1111/j.1469-7610.2011.02397.x.CrossRefPubMedGoogle Scholar
  80. 80.
    Plant DT, Pariante CM, Sharp D, Pawlby S. Maternal depression during pregnancy and offspring depression in adulthood: role of child maltreatment. Br J Psychiatry. 2015;207(3):213–20.  https://doi.org/10.1192/bjp.bp.114.156620.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    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.  https://doi.org/10.1001/jamapsychiatry.2013.2163.CrossRefPubMedPubMedCentralGoogle Scholar
  82. 82.
    Kim DR, Bale TL, Epperson CN. Prenatal programming of mental illness: current understanding of relationship and mechanisms. Curr Psychiatry Rep. 2015;17(2):5.  https://doi.org/10.1007/s11920-014-0546-9.CrossRefPubMedPubMedCentralGoogle Scholar
  83. 83.
    Laplante DP, Hart KJ, O'Hara MW, Brunet A, King S. Prenatal maternal stress is associated with toddler cognitive functioning: the Iowa flood study. Early Hum Dev. 2018;116:84–92.  https://doi.org/10.1016/j.earlhumdev.2017.11.012.CrossRefPubMedGoogle Scholar
  84. 84.
    Davis EP, Stout SA, Molet J, Vegetabile B, Glynn LM, Sandman CA, et al. Exposure to unpredictable maternal sensory signals influences cognitive development across species. Proc Natl Acad Sci. 2017;114(39):10390–5.  https://doi.org/10.1073/pnas.1703444114.CrossRefPubMedGoogle Scholar
  85. 85.
    Laplante DP, Brunet A, Schmitz N, Ciampi A, King S. Project ice storm: prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2-year-old children. J Am Acad Child Adolesc Psychiatry. 2008;47(9):1063–72.  https://doi.org/10.1097/CHI.0b013e31817eec80.CrossRefPubMedGoogle Scholar
  86. 86.
    Glynn L, Wadhwa PD, Dunkel Schetter C, Sandman CA. When stress happens matters: the effects of earthquake timing on stress responsivity in pregnancy. Am J Obstet Gynecol. 2001;184:637–42.  https://doi.org/10.1067/mob.2001.111066.CrossRefPubMedGoogle Scholar
  87. 87.
    Davis EP, Hankin BL, Swales DA, Hoffman MC. An experimental test of the fetal programming hypothesis: can we reduce child ontogenetic vulnerability to psychopathology by decreasing maternal depression? Dev Psychopathol. 2018;30(3):787–806.  https://doi.org/10.1017/S0954579418000470.CrossRefPubMedGoogle Scholar
  88. 88.
    Glasheen C, Richardson GA, Kim KH, Larkby CA, Swartz HA, Day NL. Exposure to maternal pre-and postnatal depression and anxiety symptoms: risk for major depression, anxiety disorders, and conduct disorder in adolescent offspring. Dev Psychopathol. 2013;25(4pt1):1045–63.  https://doi.org/10.1017/S0954579413000369.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Eichler A, Walz L, Grunitz J, Grimm J, Van Doren J, Raabe E, et al. Children of prenatally depressed mothers: externalizing and internalizing symptoms are accompanied by reductions in specific social-emotional competencies. J Child Fam Stud. 2017;26(11):3135–44.  https://doi.org/10.1007/s10826-017-0819-0.CrossRefGoogle Scholar
  90. 90.
    Howland MA, Sandman CA, Glynn LM, Crippen C, Davis EP. Fetal exposure to placental corticotropin-releasing hormone is associated with child self-reported internalizing symptoms. Psychoneuroendocrinology. 2016;67:10–7.  https://doi.org/10.1016/j.psyneuen.2016.01.023.CrossRefPubMedPubMedCentralGoogle Scholar
  91. 91.
    Gluckman PD, Hanson MA. Living with the past: evolution, development, and patterns of disease. Science. 2004;305(5691):1733–6.  https://doi.org/10.1126/science.1095292.CrossRefPubMedGoogle Scholar
  92. 92.
    Sandman CA, Davis EP, Glynn LM. Prescient human fetuses thrive. Psychol Sci. 2012;23(1):93–100.  https://doi.org/10.1177/0956797611422073.CrossRefPubMedGoogle Scholar
  93. 93.
    Schechter JC, Brennan PA, Smith AK, Stowe ZN, Newport DJ, Johnson KC. Maternal prenatal psychological distress and preschool cognitive functioning: the protective role of positive parental engagement. J Abnorm Child Psychol. 2017;45(2):249–60.  https://doi.org/10.1007/s10802-016-0161-9.CrossRefPubMedPubMedCentralGoogle Scholar
  94. 94.
    Bergman K, Sarkar P, Glover V, O'Connor TG. Maternal prenatal cortisol and infant cognitive development: moderation by infant–mother attachment. Biol Psychiatry. 2010;67(11):1026–32.  https://doi.org/10.1016/j.biopsych.2010.01.002.CrossRefPubMedPubMedCentralGoogle Scholar
  95. 95.
    Bergman K, Sarkar P, Glover V, O'Connor TG. Quality of child-parent attachment moderates the impact of antenatal stress on child fearfulness. J Child Psychol Psychiatry Allied Discip. 2008;49(10):1089–98.  https://doi.org/10.1111/j.1469-7610.2008.01987.x.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Laurel M. Hicks
    • 1
  • Danielle A. Swales
    • 1
  • Sarah E. Garcia
    • 1
  • Camille Driver
    • 1
  • Elysia Poggi Davis
    • 1
    • 2
    Email author
  1. 1.Department of PsychologyUniversity of DenverDenverUSA
  2. 2.Department of Psychiatry and Human BehaviorUniversity of California IrvineOrangeUSA

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