Home LiteratureArticle Details
PMID: 24863382 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Review

Glucocorticoids and fetal programming part 1: Outcomes.

Nature reviews. Endocrinology ·Vol. 10 ·No. 7 ·2014-07-00 ·Pages 391-402

Moisiadis VG, Matthews SG

Abstract

Fetal development is a critical period for shaping the lifelong health of an individual. However, the fetus is susceptible to internal and external stimuli that can lead to adverse long-term health consequences. Glucocorticoids are an important developmental switch, driving changes in gene regulation that are necessary for normal growth and maturation. The fetal hypothalamic-pituitary-adrenal (HPA) axis is particularly susceptible to long-term programming by glucocorticoids; these effects can persist throughout the life of an organism. Dysfunction of the HPA axis as a result of fetal programming has been associated with impaired brain growth, altered behaviour and increased susceptibility to chronic disease (such as metabolic and cardiovascular disease). Moreover, the effects of glucocorticoid-mediated programming are evident in subsequent generations, and transmission of these changes can occur through both maternal and paternal lineages.

MeSH Terms
Adult Animals Behavior, Animal/drug effects Betamethasone/adverse effects Child Dexamethasone/adverse effects Female Fetal Development/drug effects Fetus/drug effects Glucocorticoids/adverse effects,physiology Humans Hypothalamo-Hypophyseal System/drug effects,physiology Male Pituitary-Adrenal System/drug effects,physiology Pregnancy Premature Birth/physiopathology Prenatal Exposure Delayed Effects Stress, Physiological/physiology Stress, Psychological/physiopathology
Chemicals
Glucocorticoids Dexamethasone Betamethasone
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Moisiadis Vasilis G
Department of Physiology, University of Toronto, Medical Sciences Building, 1 King's College Circle, Toronto, ON M5S 1A8, Canada.
Matthews Stephen G
Departments of Obstetrics and Gynaecology, Medicine and Physiology, University of Toronto, Medical Sciences Building, 1 King's College Circle, Toronto, ON M5S 1A8, Canada.
References (157)
157 references, click to expand
  1. Maternal life stress events in pregnancy link to children's school achievement at age 10 years.
    J Pediatr. 2013 Mar;162(3):483-9 PMID: 23084705
  2. Prenatal stress modifies behavior and hypothalamic-pituitary-adrenal function in female guinea pig offspring: effects of timing of prenatal stress and stage of reproductive cycle.
    Endocrinology. 2008 Dec;149(12):6406-15 PMID: 18755800
  3. Global, regional, and national causes of child mortality: an updated systematic analysis for 2010 with time trends since 2000.
    Lancet. 2012 Jun 9;379(9832):2151-61 PMID: 22579125
  4. Effects of prenatal dexamethasone treatment on physical growth, pituitary-adrenal hormones, and performance of motor, motivational, and cognitive tasks in juvenile and adolescent common marmoset monkeys.
    Endocrinology. 2008 Dec;149(12):6343-55 PMID: 18755792
  5. Maternal mood and neuroendocrine programming: effects of time of exposure and sex.
    J Neuroendocrinol. 2012 Jul;24(7):999-1011 PMID: 22385021
  6. Are we prescribing multiple courses of antenatal corticosteroids? A survey of practice in the UK.
    Br J Obstet Gynaecol. 1999 Sep;106(9):977-9 PMID: 10492112
  7. Antenatal betamethasone administration alters stress physiology in healthy neonates.
    Obstet Gynecol. 2009 May;113(5):1082-1088 PMID: 19384124
  8. Prenatal glucocorticoid modifies hypothalamo-pituitary-adrenal regulation in prepubertal guinea pigs.
    Neuroendocrinology. 2001 Mar;73(3):194-202 PMID: 11307038
  9. Use of corticosteroids by Australian obstetricians--a survey of clinical practice.
    Aust N Z J Obstet Gynaecol. 1998 Feb;38(1):1-7 PMID: 9521380
  10. Long-term outcomes after repeat doses of antenatal corticosteroids.
    N Engl J Med. 2007 Sep 20;357(12):1190-8 PMID: 17881751
  11. Glucocorticoids and type 2 diabetes: from physiology to pathology.
    J Nutr Metab. 2012;2012:525093 PMID: 23316348
  12. Differential effect of prenatal stress on the expression of corticotrophin-releasing hormone and its receptors in the hypothalamus and amygdala in male and female rats.
    J Neuroendocrinol. 2011 Apr;23(4):320-8 PMID: 21306450
  13. Persistence of cytosine methylation of DNA following fertilisation in the mouse.
    PLoS One. 2012;7(1):e30687 PMID: 22292019
  14. The bed nucleus of stria terminalis and the amygdala as targets of antenatal glucocorticoids: implications for fear and anxiety responses.
    Psychopharmacology (Berl). 2012 Apr;220(3):443-53 PMID: 21935638
  15. A new view on hypocortisolism.
    Psychoneuroendocrinology. 2005 Nov;30(10):1010-6 PMID: 15950390
  16. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease.
    BMJ. 1989 Mar 4;298(6673):564-7 PMID: 2495113
  17. Antenatal and early postnatal dexamethasone treatment decreases cortisol secretion in preterm infants.
    Horm Res. 2000;53(4):170-6 PMID: 11044800
  18. Repeated maternal glucocorticoid treatment affects activity and hippocampal NMDA receptor expression in juvenile guinea pigs.
    J Physiol. 2007 Jan 1;578(Pt 1):249-57 PMID: 17068098
  19. Treatment of asthma during pregnancy and perinatal outcomes.
    Curr Opin Allergy Clin Immunol. 2005 Jun;5(3):229-33 PMID: 15864080
  20. Repeated betamethasone treatment of pregnant sheep programs persistent reductions in circulating IGF-I and IGF-binding proteins in progeny.
    Am J Physiol Endocrinol Metab. 2008 Jul;295(1):E170-8 PMID: 18492775
  21. Maternal glucocorticoid secretion mediates long-term effects of prenatal stress.
    J Neurosci. 1996 Jun 15;16(12):3943-9 PMID: 8656288
  22. Effects of antenatal glucocorticoid therapy on hippocampal histology of preterm infants.
    PLoS One. 2012;7(3):e33369 PMID: 22457757
  23. Neural regulation of endocrine and autonomic stress responses.
    Nat Rev Neurosci. 2009 Jun;10(6):397-409 PMID: 19469025
  24. Developmental programming of obesity and metabolic dysfunction: role of prenatal stress and stress biology.
    Nestle Nutr Inst Workshop Ser. 2013;74:107-20 PMID: 23887109
  25. Effect of corticosteroids for fetal maturation on perinatal outcomes. NIH Consensus Development Panel on the Effect of Corticosteroids for Fetal Maturation on Perinatal Outcomes.
    JAMA. 1995 Feb 1;273(5):413-8 PMID: 7823388
  26. Australasian randomised trial to evaluate the role of maternal intramuscular dexamethasone versus betamethasone prior to preterm birth to increase survival free of childhood neurosensory disability (A*STEROID): study protocol.
    BMC Pregnancy Childbirth. 2013 May 03;13:104 PMID: 23642125
  27. Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: possible implications for behaviour.
    Neuroscience. 2001;104(1):71-9 PMID: 11311532
  28. Anxiety induced by prenatal stress is associated with suppression of hippocampal genes involved in synaptic function.
    J Neurochem. 2007 May;101(4):1018-30 PMID: 17254015
  29. Prenatal treatment with glucocorticoids sensitizes the hpa axis response to stress among full-term infants.
    Dev Psychobiol. 2011 Mar;53(2):175-83 PMID: 21298632
  30. Fetal glucocorticoid exposure is associated with preadolescent brain development.
    Biol Psychiatry. 2013 Nov 1;74(9):647-55 PMID: 23611262
  31. Effect of prenatal betamethasone administration on maternal and fetal corticosteroid-binding globulin concentrations.
    Am J Obstet Gynecol. 1999 Dec;181(6):1546-51 PMID: 10601941
  32. Intrauterine exposure to dexamethasone impairs proliferation but not neuronal differentiation in the dentate gyrus of newborn common marmoset monkeys.
    Brain Pathol. 2006 Jul;16(3):209-17 PMID: 16911478
  33. Neonatal adrenal function after repeat dose prenatal corticosteroids: a randomized controlled trial.
    Am J Obstet Gynecol. 2006 Mar;194(3):861-7 PMID: 16522426
  34. Repeated antenatal corticosteroids: effects on cerebral palsy and childhood behavior.
    Am J Obstet Gynecol. 2004 Mar;190(3):588-95 PMID: 15041985
  35. Neonatal respiratory distress syndrome after repeat exposure to antenatal corticosteroids: a randomised controlled trial.
    Lancet. 2006 Jun 10;367(9526):1913-9 PMID: 16765760
  36. Psychological distress and salivary cortisol covary within persons during pregnancy.
    Psychoneuroendocrinology. 2012 Feb;37(2):270-9 PMID: 21752548
  37. Transgenerational effects of prenatal nutrient restriction on cardiovascular and hypothalamic-pituitary-adrenal function.
    J Physiol. 2008 Apr 15;586(8):2217-29 PMID: 18292131
  38. Effect of betamethasone in vivo on placental corticotropin-releasing hormone in human pregnancy.
    Am J Obstet Gynecol. 1998 Apr;178(4):770-8 PMID: 9579442
  39. Concurrent levels of maternal salivary cortisol are unrelated to self-reported psychological measures in low-risk pregnant women.
    Arch Womens Ment Health. 2013 Apr;16(2):101-8 PMID: 23269500
  40. 11β-hydroxysteroid dehydrogenases: intracellular gate-keepers of tissue glucocorticoid action.
    Physiol Rev. 2013 Jul;93(3):1139-206 PMID: 23899562
  41. Cardiovascular risk factors after antenatal exposure to betamethasone: 30-year follow-up of a randomised controlled trial.
    Lancet. 2005 May 28-Jun 3;365(9474):1856-62 PMID: 15924982
  42. National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications.
    Lancet. 2012 Jun 9;379(9832):2162-72 PMID: 22682464
  43. Autonomous adrenocorticotropin reaction to stress stimuli in human fetus.
    Early Hum Dev. 2012 Apr;88(4):197-201 PMID: 21925813
  44. Antenatal glucocorticoids reset the level of baseline and hypoxemia-induced pituitary-adrenal activity in the sheep fetus during late gestation.
    Am J Physiol Endocrinol Metab. 2004 Feb;286(2):E311-9 PMID: 14559720
  45. Prenatal betamethasone exposure results in pituitary-adrenal hyporesponsiveness in adult sheep.
    Am J Physiol Endocrinol Metab. 2007 Jan;292(1):E61-70 PMID: 16882931
  46. Short periods of prenatal stress affect growth, behaviour and hypothalamo-pituitary-adrenal axis activity in male guinea pig offspring.
    J Physiol. 2005 Aug 1;566(Pt 3):967-77 PMID: 15932885
  47. 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. 2010 Apr;151(4):1581-7 PMID: 20133452
  48. Retinal maturation is delayed by repeated, but not single, maternal injections of betamethasone in sheep.
    Eye (Lond). 2000 Feb;14 ( Pt 1):93-8 PMID: 10755109
  49. Prenatal Maternal Stress Associated with ADHD and Autistic Traits in early Childhood.
    Front Psychol. 2011 Jan 19;1:223 PMID: 21833278
  50. Glucocorticoid exposure of sheep at 0.7 to 0.75 gestation augments late-gestation fetal stress responses.
    Am J Obstet Gynecol. 2012 Mar;206(3):253.e16-22 PMID: 22192534
  51. Swimming exercise ameliorates depression-like behaviors induced by prenatal exposure to glucocorticoids in rats.
    Neurosci Lett. 2012 Aug 30;524(2):119-23 PMID: 22813978
  52. Differential effects of maternal betamethasone and cortisol on lung maturation and growth in fetal sheep.
    Am J Obstet Gynecol. 2003 Jan;188(1):22-8 PMID: 12548191
  53. Transgenerational effects of prenatal synthetic glucocorticoids on hypothalamic-pituitary-adrenal function.
    Endocrinology. 2012 Jul;153(7):3295-307 PMID: 22564976
  54. The effects of prenatal stress on learning in adult offspring is dependent on the timing of the stressor.
    Behav Brain Res. 2009 Jan 30;197(1):144-9 PMID: 18786572
  55. Stress and the brain: from adaptation to disease.
    Nat Rev Neurosci. 2005 Jun;6(6):463-75 PMID: 15891777
  56. Glucocorticoid levels in maternal and cord serum after prenatal betamethasone therapy to prevent respiratory distress syndrome.
    J Clin Invest. 1975 Dec;56(6):1548-54 PMID: 1202085
  57. Maternal pregnancy-specific anxiety is associated with child executive function at 6-9 years age.
    Stress. 2011 Nov;14(6):665-76 PMID: 21995526
  58. Glucocorticoids and the preparation for life after birth: are there long-term consequences of the life insurance?
    Proc Nutr Soc. 1998 Feb;57(1):113-22 PMID: 9571716
  59. Impact of antenatal synthetic glucocorticoid exposure on endocrine stress reactivity in term-born children.
    J Clin Endocrinol Metab. 2012 Oct;97(10):3538-44 PMID: 22869608
  60. Corticosterone mediates some but not other behavioural changes induced by prenatal stress in rats.
    J Neuroendocrinol. 2011 Feb;23(2):118-28 PMID: 21108672
  61. Growth in utero and blood pressure levels in the next generation.
    J Hypertens. 2000 Jul;18(7):843-6 PMID: 10930180
  62. Sex-specific alterations in placental 11beta-hydroxysteroid dehydrogenase 2 activity and early postnatal clinical course following antenatal betamethasone.
    Am J Physiol Regul Integr Comp Physiol. 2009 Aug;297(2):R510-4 PMID: 19535674
  63. Multiple courses of antenatal corticosteroids for preterm birth study: outcomes in children at 5 years of age (MACS-5).
    JAMA Pediatr. 2013 Dec;167(12):1102-10 PMID: 24126948
  64. Repeated antenatal glucocorticoid treatment decreases hypothalamic corticotropin releasing hormone mRNA but not corticosteroid receptor mRNA expression in the fetal guinea-pig brain.
    J Neuroendocrinol. 2001 May;13(5):425-31 PMID: 11328452
  65. Early determinants of cardiovascular disease.
    Best Pract Res Clin Endocrinol Metab. 2012 Oct;26(5):581-97 PMID: 22980042
  66. Prenatal maternal mood is associated with altered diurnal cortisol in adolescence.
    Psychoneuroendocrinology. 2013 Sep;38(9):1630-8 PMID: 23433748
  67. Twenty-year follow-up of antenatal corticosteroid treatment.
    Pediatrics. 2000 Jun;105(6):E77 PMID: 10835090
  68. Acute stress and hippocampal histone H3 lysine 9 trimethylation, a retrotransposon silencing response.
    Proc Natl Acad Sci U S A. 2012 Oct 23;109(43):17657-62 PMID: 23043114
  69. Repeat doses of prenatal corticosteroids for women at risk of preterm birth for improving neonatal health outcomes.
    Cochrane Database Syst Rev. 2011 Jun 15;(6):CD003935 PMID: 21678343
  70. Predictors of neonatal hypothalamic-pituitary-adrenal axis activity at delivery.
    Clin Endocrinol (Oxf). 2011 Jul;75(1):90-5 PMID: 21521269
  71. Influence of early stress on social abilities and serotonergic functions across generations in mice.
    PLoS One. 2011;6(7):e21842 PMID: 21799751
  72. Prenatal dexamethasone exposure induces changes in nonhuman primate offspring cardiometabolic and hypothalamic-pituitary-adrenal axis function.
    J Clin Invest. 2007 Apr;117(4):1058-67 PMID: 17380204
  73. Treating fetal thyroid and adrenal disorders through the mother.
    Nat Clin Pract Endocrinol Metab. 2008 Dec;4(12):675-82 PMID: 18981991
  74. Antenatal glucocorticoids and programming of the developing CNS.
    Pediatr Res. 2000 Mar;47(3):291-300 PMID: 10709726
  75. Prenatal stress induces long term stress vulnerability, compromising stress response systems in the brain and impairing extinction of conditioned fear after adult stress.
    Neuroscience. 2011 Sep 29;192:438-51 PMID: 21723377
  76. Adult glucocorticoid exposure leads to transcriptional and DNA methylation changes in nuclear steroid receptors in the hippocampus and kidney of mouse male offspring.
    Biol Reprod. 2014 Feb 27;90(2):43 PMID: 24451982
  77. Maternal cortisol over the course of pregnancy and subsequent child amygdala and hippocampus volumes and affective problems.
    Proc Natl Acad Sci U S A. 2012 May 15;109(20):E1312-9 PMID: 22529357
  78. Antenatal glucocorticoid exposure enhances the inhibition of adrenal steroidogenesis by leptin in a sex-specific fashion.
    Am J Physiol Endocrinol Metab. 2013 Jun 15;304(12):E1404-11 PMID: 23632631
  79. Antenatal exposure to betamethasone: psychological functioning and health related quality of life 31 years after inclusion in randomised controlled trial.
    BMJ. 2005 Sep 24;331(7518):665 PMID: 16143712
  80. Prenatal stress and children's cortisol reaction to the first day of school.
    Psychoneuroendocrinology. 2005 Jul;30(6):541-9 PMID: 15808923
  81. Antenatal glucocorticoids modulate the amplitude of pulsatile cortisol secretion in premature neonates.
    Pediatr Res. 1998 Dec;44(6):876-81 PMID: 9853921
  82. Infantile experience and resistance to physiological stress.
    Science. 1957 Aug 30;126(3270):405 PMID: 13467220
  83. Antenatal dexamethasone treatment in midgestation reduces system A-mediated transport in the late-gestation murine placenta.
    Endocrinology. 2011 Sep;152(9):3561-70 PMID: 21733830
  84. Expression of glucocorticoid receptor, mineralocorticoid receptor, and 11beta-hydroxysteroid dehydrogenase 1 and 2 in the fetal and postnatal ovine hippocampus: ontogeny and effects of prenatal glucocorticoid exposure.
    J Endocrinol. 2008 May;197(2):213-20 PMID: 18434351
  85. Glucocorticoid hormone resistance during primate evolution: receptor-mediated mechanisms.
    Proc Natl Acad Sci U S A. 1982 Mar;79(6):2036-40 PMID: 6952251
  86. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys.
    Biol Psychiatry. 2003 Nov 15;54(10):1025-34 PMID: 14625144
  87. Elevated maternal cortisol levels during pregnancy are associated with reduced childhood IQ.
    Int J Epidemiol. 2009 Dec;38(6):1700-10 PMID: 19423658
  88. Glucocorticoids, prenatal stress and the programming of disease.
    Horm Behav. 2011 Mar;59(3):279-89 PMID: 20591431
  89. Single course of antenatal steroids did not alter cortisol in preterm infants up to 18 months.
    Acta Paediatr. 2012 Jun;101(6):604-8 PMID: 22313364
  90. Testosterone is involved in mediating the effects of prenatal stress in male guinea pig offspring.
    J Physiol. 2011 Feb 1;589(Pt 3):755-66 PMID: 21173081
  91. Transgenerational effects of prenatal exposure to the Dutch famine on neonatal adiposity and health in later life.
    BJOG. 2008 Sep;115(10):1243-9 PMID: 18715409
  92. The association between the acute psychobiological stress response in second trimester pregnant women, amniotic fluid glucocorticoids, and neonatal birth outcome.
    Dev Psychobiol. 2014 May;56(4):734-47 PMID: 23775363
  93. Prenatal psychobiological predictors of anxiety risk in preadolescent children.
    Psychoneuroendocrinology. 2012 Aug;37(8):1224-33 PMID: 22265195
  94. Maternal glucocorticoid treatment programs HPA regulation in adult offspring: sex-specific effects.
    Am J Physiol Endocrinol Metab. 2001 May;280(5):E729-39 PMID: 11287355
  95. Sex-specific effects of prenatal stress on neuronal development in the medial prefrontal cortex and the hippocampus.
    Neuroreport. 2012 May 9;23(7):430-5 PMID: 22426025
  96. Molecular regulation of the hypothalamic-pituitary-adrenal axis in adult male guinea pigs after prenatal stress at different stages of gestation.
    J Physiol. 2008 Sep 1;586(17):4317-26 PMID: 18635650
  97. Prenatal cortisol exposure predicts infant cortisol response to acute stress.
    Dev Psychobiol. 2013 Mar;55(2):145-55 PMID: 22315044
  98. Overexposure to antenatal corticosteroids: a global concern.
    J Obstet Gynaecol Can. 2007 Nov;29(11):879 PMID: 18062040
  99. Morning cortisol levels and cognitive abilities in people with type 2 diabetes: the Edinburgh type 2 diabetes study.
    Diabetes Care. 2010 Apr;33(4):714-20 PMID: 20097784
  100. Effects of repeated prenatal glucocorticoid exposure on long-term potentiation in the juvenile guinea-pig hippocampus.
    J Physiol. 2007 Jun 15;581(Pt 3):1033-42 PMID: 17412773
  101. Brief undernutrition in late-gestation sheep programs the hypothalamic-pituitary-adrenal axis in adult offspring.
    Endocrinology. 2003 Jul;144(7):2933-40 PMID: 12810548
  102. Effects of early- and late-gestational maternal stress and synthetic glucocorticoid on development of the fetal hypothalamus-pituitary-adrenal axis in sheep.
    Stress. 2013 Jan;16(1):122-9 PMID: 22512268
  103. The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission.
    Nat Rev Neurosci. 2011 Nov 30;13(1):22-37 PMID: 22127301
  104. Effects of intrauterine exposure to synthetic glucocorticoids on fetal, newborn, and infant hypothalamic-pituitary-adrenal axis function in humans: a systematic review.
    Endocr Rev. 2009 Dec;30(7):753-89 PMID: 19837868
  105. The effect of prenatal betamethasone administration on postnatal ovine hypothalamic-pituitary-adrenal function.
    J Endocrinol. 2002 Jan;172(1):71-81 PMID: 11786375
  106. Repeated prenatal corticosteroids delay myelination in the ovine central nervous system.
    J Matern Fetal Med. 1997 Nov-Dec;6(6):309-13 PMID: 9438210
  107. Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: sex-specific effects.
    J Neuroendocrinol. 2010 Apr;22(4):258-71 PMID: 20136688
  108. Glucocorticoid exposure at the dose used clinically alters cytoskeletal proteins and presynaptic terminals in the fetal baboon brain.
    J Physiol. 2003 Feb 15;547(Pt 1):117-23 PMID: 12562943
  109. Glucocorticoids and sex-dependent development of brain glucocorticoid and mineralocorticoid receptors.
    Endocrinology. 2003 Jul;144(7):2775-84 PMID: 12810530
  110. Direct and dam-mediated effects of prenatal dexamethasone on emotionality, cognition and HPA axis in adult Wistar rats.
    Horm Behav. 2009 Oct;56(4):364-75 PMID: 19616002
  111. Inhibition of fetal adrenal adrenocorticotropin receptor messenger ribonucleic acid expression by betamethasone administration to the baboon fetus in late gestation.
    Endocrinology. 1997 Jul;138(7):2705-12 PMID: 9202207
  112. Antenatal glucocorticoid administration increases corticotrophin-releasing hormone in maternal plasma.
    Br J Obstet Gynaecol. 1998 May;105(5):556-61 PMID: 9637127
  113. Prenatal maternal stress programs infant stress regulation.
    J Child Psychol Psychiatry. 2011 Feb;52(2):119-29 PMID: 20854366
  114. Perinatal dexamethasone-induced alterations in apoptosis within the hippocampus and paraventricular nucleus of the hypothalamus are influenced by age and sex.
    J Neurosci Res. 2012 Jul;90(7):1403-12 PMID: 22388926
  115. Pancreatic islets and their roles in metabolic programming.
    Nutrition. 2014 Apr;30(4):373-9 PMID: 24206821
  116. Ontogeny of hippocampal corticosteroid receptors: effects of antenatal glucocorticoids in human and mouse.
    J Comp Neurol. 2006 Dec 20;499(6):924-32 PMID: 17072842
  117. The effects of repeated antenatal glucocorticoid therapy on the developing brain.
    Pediatr Res. 2001 Nov;50(5):581-5 PMID: 11641451
  118. Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats.
    Am J Physiol Regul Integr Comp Physiol. 2005 Jan;288(1):R34-8 PMID: 15178540
  119. Exaggerated sympathetic mediated responses to behavioral or pharmacological challenges following antenatal betamethasone exposure.
    Am J Physiol Endocrinol Metab. 2011 Jun;300(6):E979-85 PMID: 21386063
  120. Multigenerational effects of fetal dexamethasone exposure on the hypothalamic-pituitary-adrenal axis of first- and second-generation female offspring.
    Am J Obstet Gynecol. 2013 Mar;208(3):217.e1-8 PMID: 23220271
  121. Glucocorticoids and fetal programming part 2: Mechanisms.
    Nat Rev Endocrinol. 2014 Jul;10(7):403-11 PMID: 24863383
  122. Reproductive outcomes in women prenatally exposed to undernutrition: a review of findings from the Dutch famine birth cohort.
    Proc Nutr Soc. 1998 Feb;57(1):129-35 PMID: 9571718
  123. Glucocorticoid excess and the developmental origins of disease: two decades of testing the hypothesis--2012 Curt Richter Award Winner.
    Psychoneuroendocrinology. 2013 Jan;38(1):1-11 PMID: 22998948
  124. Fetal programming of hypothalamic-pituitary-adrenal (HPA) axis function and behavior by synthetic glucocorticoids.
    Brain Res Rev. 2008 Mar;57(2):586-95 PMID: 17716742
  125. Respiratory compliance in preterm infants after a single rescue course of antenatal steroids: a randomized controlled trial.
    Am J Obstet Gynecol. 2010 Jun;202(6):544.e1-9 PMID: 20227053
  126. Intergenerational influences affecting birth outcome. I. Birthweight for gestational age in the children of the 1958 British birth cohort.
    Paediatr Perinat Epidemiol. 1998 Jul;12 Suppl 1:45-60 PMID: 9690273
  127. Child health, developmental plasticity, and epigenetic programming.
    Endocr Rev. 2011 Apr;32(2):159-224 PMID: 20971919
  128. Multiple courses of antenatal corticosteroids for preterm birth (MACS): a randomised controlled trial.
    Lancet. 2008 Dec 20;372(9656):2143-51 PMID: 19101390
  129. Placental programming of chronic diseases, cancer and lifespan: a review.
    Placenta. 2013 Oct;34(10):841-5 PMID: 23916422
  130. Effects of prenatal dexamethasone treatment on postnatal physical, endocrine, and social development in the common marmoset monkey.
    Endocrinology. 2007 Apr;148(4):1813-22 PMID: 17218413
  131. Challenges of lupus pregnancies.
    Rheumatology (Oxford). 2008 Jun;47 Suppl 3:iii9-12 PMID: 18504287
  132. Antenatal corticosteroids revisited: repeat courses - National Institutes of Health Consensus Development Conference Statement, August 17-18, 2000.
    Obstet Gynecol. 2001 Jul;98(1):144-50 PMID: 11430973
  133. Neurotoxicity of glucocorticoids in the primate brain.
    Horm Behav. 1994 Dec;28(4):336-48 PMID: 7729802
  134. Effects of prenatal betamethasone exposure on regulation of stress physiology in healthy premature infants.
    Psychoneuroendocrinology. 2004 Sep;29(8):1028-36 PMID: 15219654
  135. Prenatal synthetic glucocorticoid exposure alters hypothalamic-pituitary-adrenal regulation and pregnancy outcomes in mature female guinea pigs.
    J Physiol. 2010 Mar 1;588(Pt 5):887-99 PMID: 20064858
  136. Prenatal corticosteroid exposure affects hippocampal plasticity and reduces lifespan.
    Dev Neurobiol. 2008 Feb 1;68(2):237-46 PMID: 18000831
  137. Effect of varied gestational stress on acquisition of spatial memory, hippocampal LTP and synaptic proteins in juvenile male rats.
    Behav Brain Res. 2007 Apr 16;179(1):126-32 PMID: 17320196
  138. Early-life glucocorticoid exposure: the hypothalamic-pituitary-adrenal axis, placental function, and long-term disease risk.
    Endocr Rev. 2013 Dec;34(6):885-916 PMID: 23970762
  139. Multiple courses of betamethasone to enhance fetal lung maturation do not suppress neonatal adrenal response.
    Am J Obstet Gynecol. 1999 Jun;180(6 Pt 1):1349-53 PMID: 10368470
  140. Maternal and fetal hypothalamic-pituitary-adrenal axes during pregnancy and postpartum.
    Ann N Y Acad Sci. 2003 Nov;997:136-49 PMID: 14644820
  141. Pharmacokinetics and pharmacodynamics of systemically administered glucocorticoids.
    Clin Pharmacokinet. 2005;44(1):61-98 PMID: 15634032
  142. Intergenerational influences affecting birth outcome. II. Preterm delivery and gestational age in the children of the 1958 British birth cohort.
    Paediatr Perinat Epidemiol. 1998 Jul;12 Suppl 1:61-75 PMID: 9690274
  143. Low serum cortisol predicts early death after acute myocardial infarction.
    Crit Care Med. 2010 Mar;38(3):973-5 PMID: 20081532
  144. High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6-9-year-old children.
    Psychoneuroendocrinology. 2010 Jan;35(1):141-53 PMID: 19674845
  145. Behavioural, educational and respiratory outcomes of antenatal betamethasone for term caesarean section (ASTECS trial).
    Arch Dis Child Fetal Neonatal Ed. 2013 May;98(3):F195-200 PMID: 23424017
  146. Early prenatal stress epigenetically programs dysmasculinization in second-generation offspring via the paternal lineage.
    J Neurosci. 2011 Aug 17;31(33):11748-55 PMID: 21849535
  147. Prenatal dexamethasone exposure affects anxiety-like behaviour and neuroendocrine systems in an age-dependent manner.
    Neurosci Res. 2008 Apr;60(4):364-71 PMID: 18243386
  148. Intergenerational transmission of programmed effects: public health consequences.
    Trends Endocrinol Metab. 2010 Apr;21(4):206-13 PMID: 20005734
  149. Impact of a 'rescue course' of antenatal corticosteroids: a multicenter randomized placebo-controlled trial.
    Am J Obstet Gynecol. 2009 Mar;200(3):248.e1-9 PMID: 19254583
  150. Maternal prenatal stress and cortisol reactivity to stressors in human infants.
    Stress. 2011 Jan;14(1):53-65 PMID: 20666659
  151. Outcomes at 2 years of age after repeat doses of antenatal corticosteroids.
    N Engl J Med. 2007 Sep 20;357(12):1179-89 PMID: 17881750
  152. Prenatal betamethasone exposure has sex specific effects in reversal learning and attention in juvenile baboons.
    Am J Obstet Gynecol. 2011 Jun;204(6):545.e1-10 PMID: 21411054
  153. Psychobiological effects of prenatal glucocorticoid exposure in 10-year-old-children.
    Front Psychiatry. 2012 Dec 10;3:104 PMID: 23233841
  154. Paternal stress exposure alters sperm microRNA content and reprograms offspring HPA stress axis regulation.
    J Neurosci. 2013 May 22;33(21):9003-12 PMID: 23699511
  155. Growth-restricted preterm newborns are predisposed to functional adrenal hyperandrogenism in adult life.
    Eur J Endocrinol. 2010 Oct;163(4):681-9 PMID: 20682633
  156. Prenatal glucocorticoid exposure alters hypothalamic-pituitary-adrenal function in juvenile guinea pigs.
    J Neuroendocrinol. 2007 Mar;19(3):172-80 PMID: 17280590
  157. Childhood trauma and risk for PTSD: relationship to intergenerational effects of trauma, parental PTSD, and cortisol excretion.
    Dev Psychopathol. 2001 Summer;13(3):733-53 PMID: 11523857
Article Info
Journal
Nature reviews. Endocrinology
Abbr.
Nat Rev Endocrinol
ISSN
1759-5037
DOI
10.1038/nrendo.2014.73
Published
2014-07-00
Epub
2014-00-27
Pages
391-402
Language
English
Region
England
NLM ID
101500078
Subset
IM
Grants
Canadian Institutes of Health Research · 126166 · Canada
External Links
PubMed source DOI: 10.1038/nrendo.2014.73 View journal details
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]

Copyright © 2026.Genelibs Jinan Honghui Biotechnology Co., Ltd. 鲁ICP备20007159号-2