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Cited by 640Birth, Development, and HealthStress Responses and CortisolPrenatal Substance Exposure Effects

Prenatal stress, glucocorticoids and the programming of adult disease

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Cottrell, Elizabeth C.·2009·Frontiers in Behavioral Neuroscience
DOI 10.3389/neuro.08.019.2009PMC PMC2759372
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Abstract

Numerous clinical studies associate an adverse prenatal environment with the development of cardio-metabolic disorders and neuroendocrine dysfunction, as well as an increased risk of psychiatric diseases in later life. Experimentally, prenatal exposure to stress or excess glucocorticoids in a variety of animal models can malprogram offspring physiology, resulting in a reduction in birth weight and subsequently increasing the likelihood of disorders of cardiovascular function, glucose homeostasis, hypothalamic-pituitary-adrenal (HPA) axis activity and anxiety-related behaviours in adulthood. During fetal development, placental 11beta-hydroxysteroid dehydrogenase type 2 (11beta-HSD2) provides a barrier to maternal glucocorticoids. Reduced placental 11beta-HSD2 in human pregnancy correlates with lower birth weight and higher blood pressure in later life. Similarly, in animal models, inhibition or knockout of placental 11beta-HSD2 lowers offspring birth weight, in part by reducing glucose delivery to the developing fetus in late gestation. Molecular mechanisms thought to underlie the programming effects of early life stress and glucocorticoids include epigenetic changes in target chromatin, notably affecting tissue-specific expression of the intracellular glucocorticoid receptor (GR). As such, excess glucocorticoids in early life can permanently alter tissue glucocorticoid signalling, effects which may have short-term adaptive benefits but increase the risk of later disease.

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  • Maternal stress, anxiety and depression during pregnancy increase fetal exposure to glucocorticoids.

    “Maternal stress, anxiety and depression during pregnancy have been shown to increase fetal exposure to glucocorticoids [117].”

    From Developmental programming of offspring adipose tissue biology and obesity risk (2021) · cites this paper as [117]

    The ‘Placental 11β-hydroxysteroid dehydrogenase type 2’ section reports that maternal stress reduces a placental barrier to maternal glucocorticoids, providing a mechanism for increased fetal exposure. But the paper describes increased passage as a proposed mechanism, not a demonstrated effect of maternal stress, anxiety and depression collectively. Its epidemiology section links pregnancy anxiety to cortisol in offspring at age 10, not to measured fetal exposure, and does not establish the claimed effect for depression. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Increased glucocorticoid exposure, either by stress or exogenous treatment, can lead to long-lasting effects in offspring.

    “While glucocorticoid treatment is necessary for survival, increased glucocorticoid exposure, either by stress or by exogenous treatment, can lead to long-lasting effects in offspring (Figure 2) [7,94].”

    From Stress and the HPA Axis: Balancing Homeostasis and Fertility. (2017) · cites this paper as [94]

  • Excess glucocorticoids likely represent a signaling pathway by which poor environmental conditions are signaled from the mother to the fetus, triggering changes in offspring growth and permanently affecting tissue and organ function.

    “Given their essential actions during fetal growth and development, excess glucocorticoids likely represent a signaling pathway by which poor environmental conditions are signaled from the mother to the fetus, triggering changes in offspring growth and permanently affecting tissue and organ function [94].”

    From Stress and the HPA Axis: Balancing Homeostasis and Fertility. (2017) · cites this paper as [94]

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Research works printed but not linked: 64

  1. Anway M. D. Cupp A. S. Uzumcu M. Skinner M. K. (2005). Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308, 1466– 1469 10.1126/science.1108190 15933200 PMC11423801 · DOI · Paper page
  2. Avishai-Eliner S. Brunson K. L. Sandman C. A. Baram T. Z. (2002). Stressed-out, or in (utero)? Trends Neurosci. 25, 518– 524 10.1016/S0166-2236(02)02241-5 12220880 PMC2930786 · DOI
  3. Avishai-Eliner S. Eghbal-Ahmadi M. Tabachnik E. Brunson K. L. Baram T. Z. (2001). Down-regulation of hypothalamic corticotropin-releasing hormone messenger ribonucleic acid (mRNA) precedes early-life experience-induced changes in hippocampal glucocorticoid receptor mRNA. Endocrinology 142, 89– 97 10.1210/en.142.1.89 11145570 PMC3100725 · DOI
  4. Berkowitz G. S. Wolff M. S. Janevic T. M. Holzman I. R. Yehuda R. Landrigan P. J. (2003). The World Trade Center disaster and intrauterine growth restriction. JAMA 290, 595– 596 10.1001/jama.290.5.595-b 12902358 · DOI
  5. Bertram C. Trowern A. R. Copin N. Jackson A. A. Whorwood C. B. (2001). The maternal diet during pregnancy programs altered expression of the glucocorticoid receptor and type 2 11beta-hydroxysteroid dehydrogenase: potential molecular mechanisms underlying the programming of hypertension in utero. Endocrinology 142, 2841– 2853 10.1210/en.142.7.2841 11416003 · DOI
  6. Chisaka H. Johnstone J. F. Premyslova M. Manduch Z. Challis J. R. (2005). Effect of pro-inflammatory cytokines on expression and activity of 11beta-hydroxysteroid dehydrogenase type 2 in cultured human term placental trophoblast and human choriocarcinoma JEG-3 cells. J. Soc. Gynecol. Investig. 12, 303– 309 10.1016/j.jsgi.2005.02.003 15979541 · DOI
  7. Clifton V. L. Murphy V. E. (2004). Maternal asthma as a model for examining fetal sex-specific effects on maternal physiology and placental mechanisms that regulate human fetal growth. Placenta 25(Suppl. A), S45– S52 10.1016/j.placenta.2004.01.004 15033307 · DOI
  8. Cole T. J. Blendy J. A. Monaghan A. P. Krieglstein K. Schmid W. Aguzzi A. Fantuzzi G. Hummler E. Unsicker K. Schutz G. (1995). Targeted disruption of the glucocorticoid receptor gene blocks adrenergic chromaffin cell development and severely retards lung maturation. Genes Dev. 9, 1608– 1621 10.1101/gad.9.13.1608 7628695 · DOI · Paper page
  9. Dave-Sharma S. Wilson R. C. Harbison M. D. Newfield R. Azar M. R. Krozowski Z. S. Funder J. W. Shackleton C. H. Bradlow H. L. Wei J. Q. Hertecant J. Moran A. Neiberger R. E. Balfe J. W. Fattah A. Daneman D. Akkurt H. I. De Santis C. New M. I. (1998). Examination of genotype and phenotype relationships in 14 patients with apparent mineralocorticoid excess. J. Clin. Endocrinol. Metab. 83, 2244– 2254 10.1210/jc.83.7.2244 9661590 · DOI
  10. de Vries A. Holmes M. C. Heijnis A. Seier J. V. Heerden J. Louw J. Wolfe-Coote S. Meaney M. J. Levitt N. S. Seckl J. R. (2007). Prenatal dexamethasone exposure induces changes in nonhuman primate offspring cardiometabolic and hypothalamic-pituitary-adrenal axis function. J. Clin. Invest. 117, 1058– 1067 10.1172/JCI30982 17380204 PMC1821070 · DOI
  11. Diaz R. Brown R. W. Seckl J. R. (1998). Distinct ontogeny of glucocorticoid and mineralocorticoid receptor and 11beta-hydroxysteroid dehydrogenase types I and II mRNAs in the fetal rat brain suggest a complex control of glucocorticoid actions. J. Neurosci. 18, 2570– 2580 9502816 PMC6793118
  12. Doyle L. W. Ford G. W. Davis N. M. Callanan C. (2000). Antenatal corticosteroid therapy and blood pressure at 14 years of age in preterm children. Clin. Sci. 98, 137– 142 10.1042/CS19990211 10657267 · DOI
  13. Drake A. J. Walker B. R. Seckl J. R. (2005). Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R34– R38 10.1152/ajpregu.00106.2004 15178540 · DOI
  14. Edwards C. R. Benediktsson R. Lindsay R. S. Seckl J. R. (1993). Dysfunction of placental glucocorticoid barrier: link between fetal environment and adult hypertension? Lancet 341, 355– 357 10.1016/0140-6736(93)90148-A 8094124 · DOI
  15. Fenoglio K. A. Brunson K. L. Avishai-Eliner S. Stone B. A. Kapadia B. J. Baram T. Z. (2005). Enduring, handling-evoked enhancement of hippocampal memory function and glucocorticoid receptor expression involves activation of the corticotropin-releasing factor type 1 receptor. Endocrinology 146, 4090– 4096 10.1210/en.2004-1285 15932935 PMC3100718 · DOI · Paper page
  16. Goland R. S. Jozak S. Warren W. B. Conwell I. M. Stark R. I. Tropper P. J. (1993). Elevated levels of umbilical cord plasma corticotropin-releasing hormone in growth-retarded fetuses. J. Clin. Endocrinol. Metab. 77, 1174– 1179 10.1210/jc.77.5.1174 8077309 · DOI
  17. Hales C. N. Barker D. J. (1992). Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia 35, 595– 601 10.1007/BF00400248 1644236 · DOI
  18. Hales C. N. Desai M. Ozanne S. E. Crowther N. J. (1996). Fishing in the stream of diabetes: from measuring insulin to the control of fetal organogenesis. Biochem. Soc. Trans. 24, 341– 350 8736760
  19. Hardy D. B. Yang K. (2002). The expression of 11 beta-hydroxysteroid dehydrogenase type 2 is induced during trophoblast differentiation: effects of hypoxia. J. Clin. Endocrinol. Metab. 87, 3696– 3701 10.1210/jc.87.8.3696 12161498 · DOI
  20. Heim C. Nemeroff C. B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 49, 1023– 1039 10.1016/S0006-3223(01)01157-X 11430844 · DOI · Paper page
  21. Herman J. P. Patel P. D. Akil H. Watson S. J. (1989). Localization and regulation of glucocorticoid and mineralocorticoid receptor messenger RNAs in the hippocampal formation of the rat. Mol. Endocrinol. 3, 1886– 1894 10.1210/mend-3-11-1886 2558306 · DOI
  22. Homan A. Guan H. Hardy D. B. Gratton R. J. Yang K. (2006). Hypoxia blocks 11beta-hydroxysteroid dehydrogenase type 2 induction in human trophoblast cells during differentiation by a time-dependent mechanism that involves both translation and transcription. Placenta 27, 832– 840 10.1016/j.placenta.2005.09.006 16271275 · DOI
  23. Jansson N. Pettersson J. Haafiz A. Ericsson A. Palmberg I. Tranberg M. Ganapathy V. Powell T. L. Jansson T. (2006). Down-regulation of placental transport of amino acids precedes the development of intrauterine growth restriction in rats fed a low protein diet. J. Physiol. 576, 935– 946 16916910 PMC1892642
  24. Kapoor A. Kostaki A. Janus C. Matthews S. G. (2009). The effects of prenatal stress on learning in adult offspring is dependent on the timing of the stressor. Behav. Brain Res. 197, 144– 149 10.1016/j.bbr.2008.08.018 18786572 · DOI
  25. Kapoor A. Petropoulos S. Matthews S. G. (2008). Fetal programming of hypothalamic-pituitary-adrenal (HPA) axis function and behavior by synthetic glucocorticoids. Brain Res. Rev. 57, 586– 595 10.1016/j.brainresrev.2007.06.013 17716742 · DOI
  26. King B. R. Smith R. Nicholson R. C. (2001). The regulation of human corticotrophin-releasing hormone gene expression in the placenta. Peptides 22, 795– 801 10.1016/S0196-9781(01)00393-X 11337093 · DOI
  27. Kotelevtsev Y. Brown R. W. Fleming S. Kenyon C. Edwards C. R. Seckl J. R. Mullins J. J. (1999). Hypertension in mice lacking 11beta-hydroxysteroid dehydrogenase type 2. J. Clin. Invest. 103, 683– 689 10.1172/JCI4445 10074485 PMC408118 · DOI
  28. Langley-Evans S. C. (1997a). Hypertension induced by foetal exposure to a maternal low-protein diet, in the rat, is prevented by pharmacological blockade of maternal glucocorticoid synthesis. J. Hypertens. 15, 537– 544 10.1097/00004872-199715050-00010 9170007 · DOI
  29. Langley-Evans S. C. (1997b). Maternal carbenoxolone treatment lowers birthweight and induces hypertension in the offspring of rats fed a protein-replete diet. Clin. Sci. 93, 423– 429 9486087
  30. Langley-Evans S. C. Phillips G. J. Benediktsson R. Gardner D. S. Edwards C. R. Jackson A. A. Seckl J. R. (1996). Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat. Placenta 17, 169– 172 10.1016/S0143-4004(96)80010-5 8730887 · DOI
  31. Lesage J. Blondeau B. Grino M. Breant B. Dupouy J. P. (2001). Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth retardation, and disturbs the hypothalamo–pituitary adrenal axis in the newborn rat. Endocrinology 142, 1692– 1702 10.1210/en.142.5.1692 11316731 · DOI
  32. Levitt N. S. Lindsay R. S. Holmes M. C. Seckl J. R. (1996). Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring in the rat. Neuroendocrinology 64, 412– 418 10.1159/000127146 8990073 · DOI
  33. Lindsay R. S. Lindsay R. M. Waddell B. J. Seckl J. R. (1996). Prenatal glucocorticoid exposure leads to offspring hyperglycaemia in the rat: studies with the 11 beta-hydroxysteroid dehydrogenase inhibitor carbenoxolone. Diabetologia 39, 1299– 1305 10.1007/s001250050573 8932995 · DOI
  34. Lucassen P. J. Bosch O. J. Jousma E. Kromer S. A. Andrew R. Seckl J. R. Neumann I. D. (2009). Prenatal stress reduces postnatal neurogenesis in rats selectively bred for high, but not low, anxiety: possible key role of placental 11beta-hydroxysteroid dehydrogenase type 2. Eur. J. Neurosci. 29, 97– 103 10.1111/j.1460-9568.2008.06543.x 19032587 · DOI
  35. Mairesse J. Lesage J. Breton C. Breant B. Hahn T. Darnaudery M. Dickson S. L. Seckl J. Blondeau B. Vieau D. Maccari S. Viltart O. (2007). Maternal stress alters endocrine function of the feto-placental unit in rats. Am. J. Physiol. 292, E1526– E1533 17264224
  36. Matthews S. G. Owen D. Banjanin S. Andrews M. H. (2002). Glucocorticoids, hypothalamo–pituitary–adrenal (HPA) development, and life after birth. Endocr. Res. 28, 709– 718 10.1081/ERC-120016991 12530687 · DOI
  37. McCormick J. A. Lyons V. Jacobson M. D. Noble J. Diorio J. Nyirenda M. Weaver S. Ester W. Yau J. L. Meaney M. J. Seckl J. R. Chapman K. E. (2000). 5’-Heterogeneity of glucocorticoid receptor messenger RNA is tissue specific: differential regulation of variant transcripts by early-life events. Mol. Endocrinol. 14, 506– 517 10.1210/me.14.4.506 10770488 · DOI
  38. Meaney M. J. Aitken D. H. Viau V. Sharma S. Sarrieau A. (1989). Neonatal handling alters adrenocortical negative feedback sensitivity and hippocampal type II glucocorticoid receptor binding in the rat. Neuroendocrinology 50, 597– 604 10.1159/000125287 2558328 · DOI
  39. Michailidou Z. Carter R. N. Marshall E. Sutherland H. G. Brownstein D. G. Owen E. Cockett K. Kelly V. Ramage L. Al-Dujaili E. A. Ross M. Maraki I. Newton K. Holmes M. C. Seckl J. R. Morton N. M. Kenyon C. J. Chapman K. E. (2008). Glucocorticoid receptor haploinsufficiency causes hypertension and attenuates hypothalamic–pituitary–adrenal axis and blood pressure adaptions to high-fat diet. FASEB J 22, 3896– 3907 10.1096/fj.08-111914 18697839 PMC2749453 · DOI
  40. Mueller B. R. Bale T. L. (2008). Sex-specific programming of offspring emotionality after stress early in pregnancy. J. Neurosci. 28, 9055– 9065 10.1523/JNEUROSCI.1424-08.2008 18768700 PMC2731562 · DOI · Paper page
  41. Munck A. Naray-Fejes-Toth A. (1994). Glucocorticoids and stress: permissive and suppressive actions. Ann. N. Y. Acad. Sci. 746, 115– 130; discussion 131– 113 7825870
  42. Murphy V. E. Zakar T. Smith R. Giles W. B. Gibson P. G. Clifton V. L. (2002). Reduced 11beta-hydroxysteroid dehydrogenase type 2 activity is associated with decreased birth weight centile in pregnancies complicated by asthma. J. Clin. Endocrinol. Metab. 87, 1660– 1668 10.1210/jc.87.4.1660 11932298 · DOI
  43. Nyirenda M. J. Lindsay R. S. Kenyon C. J. Burchell A. Seckl J. R. (1998). Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J. Clin. Invest. 101, 2174– 2181 10.1172/JCI1567 9593773 PMC508805 · DOI
  44. O'Connor T. G. Ben-Shlomo Y. Heron J. Golding J. Adams D. Glover V. (2005). Prenatal anxiety predicts individual differences in cortisol in pre-adolescent children. Biol. Psychiatry 58, 211– 217 10.1016/j.biopsych.2005.03.032 16084841 · DOI
  45. Ozanne S. E. Smith G. D. Tikerpae J. Hales C. N. (1996). Altered regulation of hepatic glucose output in the male offspring of protein-malnourished rat dams. Am. J. Physiol. 270, E559– 564 8928759
  46. Pepin M. C. Pothier F. Barden N. (1992). Impaired type II glucocorticoid-receptor function in mice bearing antisense RNA transgene. Nature 355, 725– 728 10.1038/355725a0 1741058 · DOI
  47. Reichardt H. M. Umland T. Bauer A. Kretz O. Schutz G. (2000). Mice with an increased glucocorticoid receptor gene dosage show enhanced resistance to stress and endotoxic shock. Mol. Cell. Biol. 20, 9009– 9017 10.1128/MCB.20.23.9009-9017.2000 11073999 PMC86554 · DOI
  48. Roberts D. Dalziel S. (2006). Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth. Cochrane Database Syst. Rev. 3, CD004454 16856047
  49. Rondo P. H. Ferreira R. F. Nogueira F. Ribeiro M. C. Lobert H. Artes R. (2003). Maternal psychological stress and distress as predictors of low birth weight, prematurity and intrauterine growth retardation. Eur. J. Clin. Nutr. 57, 266– 272 10.1038/sj.ejcn.1601526 12571658 · DOI
  50. Schneider M. L. Moore C. F. Kraemer G. W. Roberts A. D. DeJesus O. T. (2002). The impact of prenatal stress, fetal alcohol exposure, or both on development: perspectives from a primate model. Psychoneuroendocrinology 27, 285– 298 10.1016/S0306-4530(01)00050-6 11750784 · DOI
  51. Smythe J. W. Rowe W. B. Meaney M. J. (1994). Neonatal handling alters serotonin (5-HT) turnover and 5-HT2 receptor binding in selected brain regions: relationship to the handling effect on glucocorticoid receptor expression. Brain Res. 80, 183– 189 10.1016/0165-3806(94)90103-1 7525113 · DOI · Paper page
  52. Stewart P. M. Rogerson F. M. Mason J. I. (1995). Type 2 11 beta-hydroxysteroid dehydrogenase messenger ribonucleic acid and activity in human placenta and fetal membranes: its relationship to birth weight and putative role in fetal adrenal steroidogenesis. J. Clin. Endocrinol. Metab. 80, 885– 890 10.1210/jc.80.3.885 7883847 · DOI
  53. Stocker C. O'Dowd J. Morton N. M. Wargent E. Sennitt M. V. Hislop D. Glund S. Seckl J. R. Arch J. R. Cawthorne M. A. (2004). Modulation of susceptibility to weight gain and insulin resistance in low birthweight rats by treatment of their mothers with leptin during pregnancy and lactation. Int. J. Obes. Relat. Metab. Disord. 28, 129– 136 10.1038/sj.ijo.0802476 14557827 · DOI
  54. Turner J. D. Muller C. P. (2005). Structure of the glucocorticoid receptor (NR3C1) gene 5’ untranslated region: identification, and tissue distribution of multiple new human exon 1. J. Mol. Endocrinol. 35, 283– 292 10.1677/jme.1.01822 16216909 · DOI · Paper page
  55. van den Bergh B. R. Mennes M. Stevens V. van der Meere J. Borger N. Stiers P. Marcoen A. Lagae L. (2006). ADHD deficit as measured in adolescent boys with a continuous performance task is related to antenatal maternal anxiety. Pediatr. Res. 59, 78– 82 10.1203/01.pdr.0000191143.75673.52 16327007 · DOI
  56. van Os J. Selten J. P. (1998). Prenatal exposure to maternal stress and subsequent schizophrenia. The May 1940 invasion of The Netherlands. Br. J. Psychiatry 172, 324– 326 10.1192/bjp.172.4.324 9715334 · DOI
  57. Weaver I. C. Cervoni N. Champagne F. A. D'Alessio A. C. Sharma S. Seckl J. R. Dymov S. Szyf M. Meaney M. J. (2004). Epigenetic programming by maternal behavior. Nat. Neurosci. 7, 847– 854 10.1038/nn1276 15220929 · DOI · Paper page
  58. Weaver I. C. D'Alessio A. C. Brown S. E. Hellstrom I. C. Dymov S. Sharma S. Szyf M. Meaney M. J. (2007). The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: altering epigenetic marks by immediate-early genes. J. Neurosci. 27, 1756– 1768 10.1523/JNEUROSCI.4164-06.2007 17301183 PMC2951014 · DOI · Paper page
  59. Wei Q. Lu X. Y. Liu L. Schafer G. Shieh K. R. Burke S. Robinson T. E. Watson S. J. Seasholtz A. F. Akil H. (2004). Glucocorticoid receptor overexpression in forebrain: a mouse model of increased emotional lability. Proc. Natl. Acad. Sci. U.S.A. 101, 11851– 11856 10.1073/pnas.0402208101 15280545 PMC511063 · DOI
  60. Welberg L. A. Seckl J. R. Holmes M. C. (2000). Inhibition of 11beta-hydroxysteroid dehydrogenase, the foeto-placental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behaviour in the offspring. Eur. J. Neurosci. 12, 1047– 1054 10.1046/j.1460-9568.2000.00958.x 10762336 · DOI
  61. Whincup P. H. Kaye S. J. Owen C. G. Huxley R. Cook D. G. Anazawa S. Barrett-Connor E. Bhargava S. K. Birgisdottir B. E. Carlsson S. de Rooij S. R. Dyck R. F. Eriksson J. G. Falkner B. Fall C. Forsen T. Grill V. Gudnason V. Hulman S. Hypponen E. Jeffreys M. Lawlor D. A. Leon D. A. Minami J. Mishra G. Osmond C. Power C. Rich-Edwards J. W. Roseboom T. J. Sachdev H. S. Syddall H. Thorsdottir I. Vanhala M. Wadsworth M. Yarbrough D. E. (2008). Birth weight and risk of type 2 diabetes: a systematic review. JAMA 300, 2886– 2897 10.1001/jama.2008.886 19109117 · DOI
  62. Williams M. T. Hennessy M. B. Davis H. N. (1995). CRF administered to pregnant rats alters offspring behavior and morphology. Pharmacol. Biochem. Behav. 52, 161– 167 10.1016/0091-3057(95)00082-8 7501659 · DOI
  63. Williams M. T. Hennessy M. B. Davis H. N. (1998). Stress during pregnancy alters rat offspring morphology and ultrasonic vocalizations. Physiol. Behav. 63, 337– 343 10.1016/S0031-9384(97)00428-9 9469724 · DOI
  64. Yehuda R. (2002). Post-traumatic stress disorder. N. Engl. J. Med. 346, 108– 114 10.1056/NEJMra012941 11784878 · DOI · Paper page

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Authors
Cottrell, E. C.
Affiliations
The Queen's Medical Research Institute (GB)
Corresponding author
Cottrell, Elizabeth C.
ORCID
Cottrell, Elizabeth C.
Venue
Frontiers in Behavioral Neuroscience
Publisher
Frontiers Media SA
Published
2009
Volume
3
Pages
19-19
ISSN
1662-5153 (ISSN-L)
DOI
10.3389/neuro.08.019.2009
PMC
PMC2759372
OpenAlex
W2126602202
Cited by
640
References
18
Citations by year
2026: 20 · 2025: 26 · 2024: 24 · 2023: 26 · 2022: 39 · 2021: 44 · 2020: 34 · 2019: 42 · 2018: 52 · 2017: 50 · 2016: 55 · 2015: 42 · 2014: 49 · 2013: 29 · 2012: 44
FWCI
31.14
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Frontiers in Behavioral Neuroscience (publishedVersion, cc-by)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • Research Explorer (The University of Manchester) (publishedVersion)
  • Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Topics
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Birth, Development, and Health
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
  • Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
Keywords
prenatal stress, glucocorticoids, developmental programming, fetal origins of adult disease, birth weight, hypothalamic-pituitary-adrenal axis, glucose homeostasis, cardiovascular function, anxiety, epigenetic modifications, glucocorticoid receptor, glucocorticoid signaling, neuroendocrine dysfunction, cardiometabolic disease

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