Long-term Effects of Prenatal Stress and Glucocorticoid Exposure

Birth Defects Research Part C - Embryo Today: Reviews

Volumn 96, Issue 4, 2012, Pages 315-324

  Painter, Rebecca C ^a   Roseboom, Tessa J ^a   de Rooij, Susanne R ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Glucocorticoid; Long term; Prenatal; Stress

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 2; GLUCOCORTICOID;

AFFECT; ANXIETY; BEHAVIOR; ENVIRONMENTAL STRESS; ENZYME INACTIVATION; FETUS LUNG MATURITY; FETUS OUTCOME; HEAD CIRCUMFERENCE; HUMAN; HYPERTENSION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; INCIDENCE; LIFE EVENT; LOW BIRTH WEIGHT; MATERNAL NUTRITION; MATERNAL STRESS; NONHUMAN; PREGNANCY OUTCOME; PREMATURE LABOR; PRENATAL DRUG EXPOSURE; PRENATAL EXPOSURE; PRENATAL STRESS; PREVALENCE; PRIORITY JOURNAL; PROGENY; PUERPERAL DEPRESSION; REVIEW;

GLUCOCORTICOID; LONG-TERM; PRENATAL; STRESS;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 2; ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; FETAL DEVELOPMENT; FETUS; GLUCOCORTICOIDS; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; PITUITARY-ADRENAL SYSTEM; PLACENTA; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; STRESS, PHYSIOLOGICAL; TIME FACTORS;

EID: 84873820477     PISSN: 1542975X     EISSN: 15429768     Source Type: Journal    
DOI: 10.1002/bdrc.21021     Document Type: Review

References (88)

1. Aghajafari F, Murphy K, Matthews S, et al. 2002. Repeated doses of antenatal corticosteroids in animals: a systematic review. Am J Obstet Gynecol 186:843-849.
2. Bennett HA, Einarson A, Taddio A, et al. 2004. Prevalence of depression during pregnancy: systematic review. Obstet Gynecol 103:698-709.
3. Bergman K, Sarkar P, O'Connor TG, et al. 2007. Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. J Am Acad Child Adolesc Psychiatry 46:1454-1463.
4. Bermudez-Millan A, Damio G, Cruz J, et al. 2011. Stress and the social determinants of maternal health among Puerto Rican women: a CBPR approach. J Health Care Poor Underserved 22:1315-1330.
5. Boomsma CM, Macklon NS. 2008. Does glucocorticoid therapy in the peri-implantation period have an impact on IVF outcomes? Curr Opin Obstet Gynecol 20:249-256.
6. Brand SR, Engel SM, Canfield RL, Yehuda R. 2006. The effect of maternal PTSD following in utero trauma exposure on behavior and temperament in the 9-month-old infant. Ann N Y Acad Sci 1071:454-458.
7. Braun T, Li S, Sloboda DM, et al. 2009. Effects of maternal dexamethasone treatment in early pregnancy on pituitary-adrenal axis in fetal sheep. Endocrinology 150:5466-5477.
8. Brown AS, Susser ES, Lin SP, et al. 1995. Increased risk of affective disorders in males after second trimester prenatal exposure to the Dutch hunger winter of 1944-45. Br J Psychiatry 166:601-606.
9. Buss C, Davis EP, Muftuler LT, et al. 2010. High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children. Psychoneuroendocrinology 35:141-153.
10. Choe HK, Son GH, Chung S, et al. 2011. Maternal stress retards fetal development in mice with transcriptome-wide impact on gene expression profiles of the limb. Stress 14:194-204.
11. Clifton VL, Davies M, Moore V, et al. 2012. Developmental perturbation induced by maternal asthma during pregnancy: the short- and long-term impacts on offspring. J Pregnancy 2012:741613.
12. Clifton VL, Engel P, Smith R, et al. 2009. Maternal and neonatal outcomes of pregnancies complicated by asthma in an Australian population. Aust N Z J Obstet Gynaecol 49:619-626.
13. Crowther CA, McKinlay CJ, Middleton P, Harding JE. 2011. Repeat doses of prenatal corticosteroids for women at risk of preterm birth for improving neonatal health outcomes. Cochrane Database Syst Rev CD003935.
14. Dalziel SR, Walker NK, Parag V, et al. 2005. Cardiovascular risk factors after antenatal exposure to betamethasone: 30-year follow-up of a randomised controlled trial. Lancet 365:1856-1862.
15. de Bruijn AT, van Bakel HJ, van Baar AL. 2009. Sex differences in the relation between prenatal maternal emotional complaints and child outcome. Early Hum Dev 85:319-324.
16. de Rooij SR, Wouters H, Yonker JE, et al. 2010. Prenatal undernutrition and cognitive function in late adulthood. Proc Natl Acad Sci USA 107:16881-16886.
17. de Vries VA, 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.
18. Dessens AB, Haas HS, Koppe JG. 2000. Twenty-year follow-up of antenatal corticosteroid treatment. Pediatrics 105:E77.
19. Dickinson H, Walker DW, Wintour EM, Moritz K. 2007. Maternal dexamethasone treatment at midgestation reduces nephron number and alters renal gene expression in the fetal spiny mouse. Am J Physiol Regul Integr Comp Physiol 292:R453-R461.
20. DiPietro JA, Novak MF, Costigan KA, et al. 2006. Maternal psychological distress during pregnancy in relation to child development at age two. Child Dev 77:573-587.
21. Dodic M, Abouantoun T, O'Connor A, et al. 2002. Programming effects of short prenatal exposure to dexamethasone in sheep. Hypertension 40:729-734.
22. Doyle LW, Ford GW, Davis NM, Callanan C. 2000a. Antenatal corticosteroid therapy and blood pressure at 14 years of age in preterm children. Clin Sci (Lond) 98:137-142.
23. Doyle LW, Ford GW, Rickards AL, et al. 2000b. Antenatal corticosteroids and outcome at 14 years of age in children with birth weight less than 1501 grams. Pediatrics 106:E2.
24. Drake AJ, Raubenheimer PJ, Kerrigan D, et al. 2010. Prenatal dexamethasone programs expression of genes in liver and adipose tissue and increased hepatic lipid accumulation but not obesity on a high-fat diet. Endocrinology 151:1581-1587.
25. Entringer S, Buss C, Swanson JM, et al. 2012. Fetal programming of body composition, obesity, and metabolic function: the role of intrauterine stress and stress biology. J Nutr Metab 2012:632548.
26. Entringer S, Epel ES, Kumsta R, et al. 2011. Stress exposure in intrauterine life is associated with shorter telomere length in young adulthood. Proc Natl Acad Sci USA 108:E513-E518.
27. Entringer S, Kumsta R, Hellhammer DH, et al. 2009. Prenatal exposure to maternal psychosocial stress and HPA axis regulation in young adults. Horm Behav 55:292-298.
28. Evans J, Xu K, Heron J, et al. 2009. Emotional symptoms in children: the effect of maternal depression, life events, and COMT genotype. Am J Med Genet B Neuropsychiatr Genet 150B:209-218.
29. Forest MG, Betuel H, David M. 1989. Prenatal treatment in congenital adrenal hyperplasia due to 21-hydroxylase deficiency: up-date 88 of the French multicentric study. Endocr Res 15:277-301.
30. Franzek EJ, Sprangers N, Janssens AC, et al. 2008. Prenatal exposure to the 1944-45 Dutch 'hunger winter' and addiction later in life. Addiction 103:433-438.
31. Grant KA, McMahon C, Austin MP. 2008. Maternal anxiety during the transition to parenthood: a prospective study. J Affect Disord 108:101-111.
32. Gutteling BM, de WC, Buitelaar JK. 2004. Maternal prenatal stress and 4-6 year old children's salivary cortisol concentrations pre- and post-vaccination. Stress 7:257-260.
33. Gutteling BM, de WC, Buitelaar JK. 2005a. Prenatal stress and children's cortisol reaction to the first day of school. Psychoneuroendocrinology 30:541-549.
34. Gutteling BM, de WC, Willemsen-Swinkels SH, et al. 2005b. The effects of prenatal stress on temperament and problem behavior of 27-month-old toddlers. Eur Child Adolesc Psychiatry 14:41-51.
35. Gutteling BM, de WC, Willemsen-Swinkels SH, et al. 2005c. The effects of prenatal stress on temperament and problem behavior of 27-month-old toddlers. Eur Child Adolesc Psychiatry 14:41-51.
36. Gutteling BM, de WC, Zandbelt N, et al. 2006. Does maternal prenatal stress adversely affect the child's learning and memory at age six? J Abnorm Child Psychol 34:789-798.
37. Harris A, Seckl J. 2011. Glucocorticoids, prenatal stress and the programming of disease. Horm Behav 59:279-289.
38. Hirvikoski T, Nordenstrom A, Lindholm T, et al. 2008. Long-term follow-up of prenatally treated children at risk for congenital adrenal hyperplasia: does dexamethasone cause behavioral problems? Eur J Endocrinol 159:309-316.
39. Hougaard KS, Andersen MB, Kjaer SL, et al. 2005. Prenatal stress may increase vulnerability to life events: comparison with the effects of prenatal dexamethasone. Brain Res Dev Brain Res 159:55-63.
40. Huizink AC, Dick DM, Sihvola E, et al. 2007. Chernobyl exposure as stressor during pregnancy and behavior in adolescent offspring. Acta Psychiatr Scand 116:438-446.
41. Ikegami M, Jobe AH, Newnham J, et al. 1997. Repetitive prenatal glucocorticoids improve lung function and decrease growth in preterm lambs. Am J Respir Crit Care Med 156:178-184.
42. Jewell D, Young G. 2003. Interventions for nausea and vomiting in early pregnancy. Cochrane Database Syst Rev CD000145.
43. Khashan 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.
44. Khashan AS, Wicks S, Dalman C, et al. 2012. Prenatal stress and risk of asthma hospitalization in the offspring: a Swedish population-based study. Psychosom Med 74:635-641.
45. King S, Laplante DP. 2005. The effects of prenatal maternal stress on children's cognitive development: project ice storm. Stress 8:35-45.
46. Kinney DK, Miller AM, Crowley DJ, et al. 2008. Autism prevalence following prenatal exposure to hurricanes and tropical storms in Louisiana. J Autism Dev Disord 38:481-488.
47. Kwong WY, Wild AE, Roberts P, et al. 2000. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development 127:4195-4202.
48. Laplante DP, Brunet A, Schmitz N, et al. 2008. Project ice storm: prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2-year-old children. J Am Acad Child Adolesc Psychiatry 47:1063-1072.
49. Li J, Olsen J, Vestergaard M, Obel C. 2010a. Attention-deficit/hyperactivity disorder in the offspring following prenatal maternal bereavement: a nationwide follow-up study in Denmark. Eur Child Adolesc Psychiatry 19:747-753.
50. Li J, Olsen J, Vestergaard M, et al. 2010b. Prenatal stress exposure related to maternal bereavement and risk of childhood overweight. PLoS One 5:e11896.
51. Li J, Vestergaard M, Obel C, et al. 2012. Antenatal maternal bereavement and childhood cancer in the offspring: a population-based cohort study in 6 million children. Br J Cancer 107:544-548.
52. Liggins GC. 1969. Premature delivery of foetal lambs infused with glucocorticoids. J Endocrinol 45:515-523.
53. Liggins GC, Howie RN. 1972. A controlled trial of antepartum glucocorticoid treatment for prevention of the respiratory distress syndrome in premature infants. Pediatrics 50:515-525.
54. Littleton HL, Bye K, Buck K, Amacker A. 2010. Psychosocial stress during pregnancy and perinatal outcomes: a meta-analytic review. J Psychosom Obstet Gynaecol 31:219-228.
55. Loomans EM, van der Stelt O, van EM, et al. 2012. High levels of antenatal maternal anxiety are associated with altered cognitive control in five-year-old children. Dev Psychobiol 54:441-450.
56. Mennes M, Van den Bergh B, Lagae L, Stiers P. 2009. Developmental brain alterations in 17 year old boys are related to antenatal maternal anxiety. Clin Neurophysiol 120:1116-1122.
57. Moss TJ, Doherty DA, Nitsos I, et al. 2005. Effects into adulthood of single or repeated antenatal corticosteroids in sheep. Am J Obstet Gynecol 192:146-152.
58. Moss TJ, Sloboda DM, Gurrin LC, et al. 2001. Programming effects in sheep of prenatal growth restriction and glucocorticoid exposure. Am J Physiol Regul Integr Comp Physiol 281:R960-R970.
59. Murphy VE, Gibson P, Talbot PI, Clifton VL. 2005. Severe asthma exacerbations during pregnancy. Obstet Gynecol 106:1046-1054.
60. Murphy KE, Hannah ME, Willan AR, et al. 2008. Multiple courses of antenatal corticosteroids for preterm birth (MACS): a randomised controlled trial. Lancet 372:2143-2151.
61. Neugebauer R, Hoek HW, Susser E. 1999. Prenatal exposure to wartime famine and development of antisocial personality disorder in early adulthood. JAMA 282:455-462.
62. Niederhofer H, Reiter A. 2004. Prenatal maternal stress, prenatal fetal movements and perinatal temperament factors influence behavior and school marks at the age of 6 years. Fetal Diagn Ther 19:160-162.
63. 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. JClin Invest 101:2174-2181.
64. O'Connor TG, Ben-Shlomo Y, Heron J, et al. 2005. Prenatal anxiety predicts individual differences in cortisol in pre-adolescent children. Biol Psychiatry 58:211-217.
65. O'Connor TG, Caprariello P, Blackmore ER, et al. 2007. Prenatal mood disturbance predicts sleep problems in infancy and toddlerhood. Early Hum Dev 83:451-458.
66. O'Connor TG, Heron J, Golding J, et al. 2002. Maternal antenatal anxiety and children's behavioral/emotional problems at 4 years. Report from the Avon Longitudinal Study of Parents and Children. Br J Psychiatry 180:502-508.
67. O'Donnell KJ, Bugge JA, Freeman L, et al. 2012. Maternal prenatal anxiety and downregulation of placental 11beta-HSD2. Psychoneuroendocrinology 37:818-826.
68. Phillips DI, Barker DJ, Fall CH, et al. 1998. Elevated plasma cortisol concentrations: a link between low birth weight and the insulin resistance syndrome? J Clin Endocrinol Metab 83:757-760.
69. Powell H, McCaffery K, Murphy VE, et al. 2011. Psychosocial outcomes are related to asthma control and quality of life in pregnant women with asthma. J Asthma 48:1032-1040.
70. Raikkonen K, Pesonen AK, Heinonen K, et al. 2009. Maternal licorice consumption and detrimental cognitive and psychiatric outcomes in children. Am J Epidemiol 170:1137-1146.
71. Raikkonen K, Seckl JR, Heinonen K, et al. 2010. Maternal prenatal licorice consumption alters hypothalamic-pituitary-adrenocortical axis function in children. Psychoneuroendocrinology 35:1587-1593.
72. Roberts D, Dalziel S. 2006. Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth. Cochrane Database Syst Rev CD004454.
73. Roseboom T, de RS, Painter R. 2006. The Dutch famine and its long-term consequences for adult health. Early Hum Dev 82:485-491.
74. Schreier NK, Moltchanova EV, Blomstedt PA, et al. 2011. Prenatal exposure to wartime stress: long-term effect on coronary heart disease in later life. Ann Med 43:555-561.
75. Smith JW, Seckl JR, Evans AT, et al. 2004. Gestational stress induces post-partum depression-like behavior and alters maternal care in rats. Psychoneuroendocrinology 29:227-244.
76. Susser E, Neugebauer R, Hoek HW, et al. 1996. Schizophrenia after prenatal famine. Further evidence. Arch Gen Psychiatry 53:25-31.
77. The Royal College of Obstetricians and Gynaecologists. The Investigation and Treatment of Couples with Recurrent First- and Second-Trimester Miscarriage, Green Top Guideline No 17. 2011. [Online Source].
78. van Abeelen AF, Veenendaal MV, Painter RC, et al. 2012. Survival effects of prenatal famine exposure. Am J Clin Nutr 95:179-183.
79. 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.
80. Van den Bergh BR, Mennes M, Oosterlaan J, et al. 2005. High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds. Neurosci Biobehav Rev 29:259-269.
81. Van den Bergh BR, Mennes M, Stevens V, et al. 2006. ADHD deficit as measured in adolescent boys with a continuous performance task is related to antenatal maternal anxiety. Pediatr Res 59:78-82.
82. Van den Bergh BR, Van CB, Smits T, et al. 2008. 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 33:536-545.
83. van Dijk AE, van EM, Stronks K, et al. 2012a. Prenatal stress and balance of the child's cardiac autonomic nervous system at age 5-6 years. PLoS One 7:e30413.
84. van Dijk AE, van EM, Stronks K, et al. 2012b. The association between prenatal psychosocial stress and blood pressure in the child at age 5-7 years. PLoS One 7:e43548.
85. Vedhara K, Metcalfe C, Brant H, et al. 2012. Maternal mood and neuroendocrine programming: effects of time of exposure and sex. J Neuroendocrinol 24:999-1011.
86. Veenendaal MV, van Abeelen AF, Painter RC, et al. 2011. Consequences of hyperemesis gravidarum for offspring: a systematic review and meta-analysis. BJOG 118:1302-1313.
87. Warkany J, Kalter H. 1962. Maternal impressions and congenital malformations. Plast Reconstr Surg Transplant Bull 30:628-637.
88. Welberg LA, Seckl JR. 2001. Prenatal stress, glucocorticoids and the programming of the brain. J Neuroendocrinol 13:113-128.