Skip to main content Accessibility help

We use cookies to distinguish you from other users and to provide you with a better experience on our websites. Close this message to accept cookies or find out how to manage your cookie settings.

Close cookie message
×
Hostname: page-component-848d4c4894-pjpqr Total loading time: 0 Render date: 2024-06-29T00:55:02.777Z Has data issue: false hasContentIssue false

13 - The fetal hypothalamic–pituitary–adrenal axis: relevance to developmental origins of health and disease

Published online by Cambridge University Press:  08 August 2009

By
Deborah M. Sloboda ,
John P. Newnham ,
Timothy J. M. Moss  and
John R. G. Challis
Edited by
Peter Gluckman  and
Mark Hanson
Deborah M. Sloboda
Affiliation:
University of Western Australia
John P. Newnham
Affiliation:
University of Western Australia
Timothy J. M. Moss
Affiliation:
University of Western Australia
John R. G. Challis
Affiliation:
University of Toronto
Peter Gluckman
Affiliation:
University of Auckland
Mark Hanson
Affiliation:
University of Southampton
Get access

Summary

Introduction

A clear relationship exists between intrauterine development and predisposition to postnatal disease. It is now understood that pre- and periconceptional nutritional status, glucocorticoid exposure and immediate postnatal development including catch-up growth may all contribute to these influences of early development on later-life disease. Barker and colleagues have described in detail the potential influence that an adverse intrauterine environment could play in the risk of developing particular diseases later in life (Barker 1994a, 1994b, 1995). It has been proposed that resetting of endocrine axes controlling growth and development could be one pathway for the developmental programming of later health and wellbeing. The fetal hypothalamic–pituitary–adrenal (HPA) axis in particular is highly vulnerable to changes in the intrauterine environment. Fetal HPA axis activity increases with gestation in most species and contributes to increased fetal levels of circulating glucocorticoids (Fowden et al. 1998). Even subtle changes in the intrauterine environment can disrupt the delicate balance of fetal HPA development and glucocorticoid production and can therefore alter long-term HPA activity and function. HPA hyperactivity has been demonstrated in animals after prenatal undernutrition (Lingas et al. 1999), prenatal stress (Takahashi and Kalin 1991) and maternal synthetic glucocorticoid administration (Uno et al. 1990, Sloboda et al. 2000).

Programming of the fetal HPA axis during development appears to play a central role in the link between fetal growth and long-term disease in adulthood. Prenatal programming of HPA axis function may increase the risk of developing cardiovascular and metabolic diseases.

Type
Chapter
Information
Developmental Origins of Health and Disease , pp. 191 - 205
Publisher: Cambridge University Press
Print publication year: 2006

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Amaral, D. G. and Witter, M. P. (1989). The three dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience, 31, 571–91.CrossRefGoogle ScholarPubMed
Andrews, M. H., Kostaki, A., Setiawan, E.et al. (2004). Developmental regulation of 5-HT7 receptor and NGFI-A in the fetal limbic system: influence of glucocorticoid. J. Physiol., 555, 659–70.CrossRefGoogle Scholar
Antonow-Schlorke, I., Schwab, M., Li, C. and Nathanielsz, P. W. (2003). Glucocorticoid exposure at the dose used clinically alters cytoskeletal proteins and presynaptic terminals in the fetal baboon brain. J. Physiol., 547, 117–23.CrossRefGoogle ScholarPubMed
Anyaegbunam, W. I. and Adetona, A. B. (1997). Use of antenatal corticosteroids for fetal maturation in preterm infants. Am. Fam. Physician, 56, 1093–6.Google ScholarPubMed
Austin, M. P. and Leader, L. (2000). Maternal stress and obstetric and infant outcomes: epidemiological findings and neuroendocrine mechanisms. Aust. NZ J. Obstet. Gynaecol., 40, 331–7.CrossRefGoogle ScholarPubMed
Bakker, J. M., Schmidt, E. D., Kroes, H.et al. (1995). Effects of short-term dexamethasone treatment during pregnancy on the development of the immune system and the hypothalamo-pituitary adrenal axis in the rat. J. Neuroimmunol., 63, 183–91.CrossRefGoogle ScholarPubMed
Ballard, R. A. and Ballard, P. L. (1996). Antenatal hormone therapy for improving the outcome of the preterm infant. J. Perinatol., 16, 390–6.Google ScholarPubMed
Bamberger, C. M., Schulte, H. M. and Chrousos, G. P. (1996). Molecular determinants of glucocorticoid receptor function and tissue sensitivity to glucocorticoids. Endocr. Rev., 17, 245–60.CrossRefGoogle ScholarPubMed
Barker, D. J. P. (1966). Low intelligence: its relation to length of gestation and rate of foetal growth. Br. J. Prev. Soc. Med., 20, 58–66.Google ScholarPubMed
Barker, D. J. P. (1994a). The fetal origins of adult disease. Fetal Matern. Med. Rev., 6, 71–80.CrossRefGoogle Scholar
Barker, D. J. P. (1994b). Mothers, Babies and Disease in Later Life., London: BMJ Publishing Group.Google Scholar
Barker, D. J. P. (1995). The fetal and infant origins of disease. Eur. J. Clini. Investiga., 25, 457–63.CrossRefGoogle Scholar
Benediktsson, R., Lindsay, R. S., Noble, J. M., Seckl, J. R. and Edwards, C. R. W. (1993). Glucocorticoid exposure in utero: new model for adult hypertension. Lancet, 341, 339–41.CrossRefGoogle ScholarPubMed
Bertram, C. E. and Hanson, M. A. (2002). Prenatal programming of postnatal endocrine responses by glucocorticoids. Reproduction, 124, 459–67.CrossRefGoogle ScholarPubMed
Bloomfield, F. H., Oliver, M. H., Hawkins, P.et al. (2003). A periconceptional nutritional origin for noninfectious preterm birth. Science, 300, 606.CrossRefGoogle ScholarPubMed
Boshier, D. P. and Holloway, H. (1989). Morphometric analyses of adrenal gland growth in fetal and neonatal sheep. I. The adrenal cortex. J. Anat., 167, 1–14.Google ScholarPubMed
Boshier, D. P. and Holloway, H. (1991). Morphometric analyses of adrenal gland growth in fetal and neonatal sheep. III. Volumes of the major organelles within the zona fasciculata steroidogenic cells. J. Anat., 178, 175–87.Google ScholarPubMed
Brooks, A. N. and Challis, J. R. G. (1989). Effects of CRF, AVP and opioid peptides on pituitary–adrenal responses in sheep. Peptides, 10, 1291–3.CrossRefGoogle Scholar
Challis, J. R. G., Lye, S. J. and Welsh, J. (1986). Ovine fetal adrenal maturation at term and during fetal ACTH administration: evidence that the modulating effect of cortisol may involve cAMP. Can. J. Physiol. Pharmacol., 64, 1085–90.CrossRefGoogle ScholarPubMed
Challis, J. R. G., Sloboda, D., Matthews, S. G.et al. (2001). The fetal placental hypothalamic–pituitary–adrenal (HPA) axis, parturition and post natal health. Mol. Cell. Endocrinol., 185, 135–44.CrossRefGoogle ScholarPubMed
Clark, P. M. S., Hindmarsh, P. C., Shiell, A. W., Law, C. M., Honour, J. W. and Barker, D. J. P. (1996). Size at birth and adrenocortical function in childhood. Clin. Endocrinol., 45, 721–6.CrossRefGoogle ScholarPubMed
Clarke, A. S., Wittwer, D. J., Abbott, D. H. and Schneider, M. L. (1994). Long-term effects of prenatal stress on HPA axis activity in juvenile rhesus monkeys. Dev. Psychobiol., 27, 257–69.CrossRefGoogle ScholarPubMed
Cox, D. B., Brubaker, P., Fraser, M., Whittle, W. and Challis, J. R. G. (1999). The effect of maternal dexamethasone during early pregnancy on fetal growth, HPA development and the control of glucose homeostasis. J. Soc. Gynecol. Investig., 6, 110A.Google Scholar
Crowley, P. (2003). Antenatal corticosteroids: current thinking. BJOG, 110 (Suppl. 20), 77–8.Google ScholarPubMed
Dean, F. and Matthews, S. G. (1999). Maternal dexamethasone treatment in late gestation alters glucocorticoid and mineralocorticoid receptor mRNA in the fetal guinea pig brain. Brain Res., 846, 253–9.CrossRefGoogle ScholarPubMed
Kloet, E. R., Vreugdenhil, E., Oitzl, M. S. and Joels, M. (1998). Brain corticosteroids receptor balance in health and disease. Endocr. Rev., 19, 269–301.Google ScholarPubMed
Dinan, T. G. (1996). Serotonin and the regulation of hypothalamic–pituitary–adrenal axis function. Life Sci., 58, 1683–94.CrossRefGoogle ScholarPubMed
Dobbing, J. and Sands, J. (1979). Comparative aspects of the brain growth spurt. Early Hum. Dev., 3, 79–83.CrossRefGoogle ScholarPubMed
Dodic, M. and Wintour, E. M. (1994). Effects of prolonged (48 h) infusion of cortisol on blood pressure, renal function and fetal fluids in the immature ovine foetus. Clin. Exp. Pharmacol. Physiol., 21, 971–80.CrossRefGoogle ScholarPubMed
Dunlop, S. A., Archer, M. A., Quinlivan, J. A., Beazley, L. D. and Newnham, J. P. (1997). Repeated prenatal corticosteroids delay myelination in the ovine central nervous system. J. Matern. Fetal Med., 6, 309–13.Google ScholarPubMed
Durand, P. (1979). ACTH receptor levels in lamb adrenals at late gestation and early neonatal stages. Biol. Reprod., 20, 837–45.CrossRefGoogle ScholarPubMed
Durand, P., Bosc, M. J. and Locatelli, A. (1980). Adrenal maturation of the sheep fetus during late pregnancy. Reprod. Nutr. Dev., 20, 339–47.CrossRefGoogle ScholarPubMed
Durand, P., Locatelli, A., Cathiard, A. M., Dazord, A. and Saez, J. M. (1981). ACTH induction of the maturation of ACTH-sensitive adenylate cyclase system in the ovine fetal adrenal. J. Steroid Biochem., 15, 445–8.CrossRefGoogle ScholarPubMed
Edwards, C. R. W., Benediktsson, R., Lindsay, R. S. and Seckl, J. R. (1993). Dysfunction of placental glucocorticoid barrier: link between fetal environment and adult hypertension?Lancet, 341, 355–7.CrossRefGoogle ScholarPubMed
Feldman, S. and Conforti, N. (1980). Participation of the dorsal hippocampus in the glucocorticoid feedback effect on adrenocortical activity. Neuroendocrinology, 30, 52–5.CrossRefGoogle ScholarPubMed
Fernald, L. C. and Grantham-McGregor, S. M. (2002). Growth retardation is associated with changes in the stress response system and behavior in school-aged Jamaican children. J. Nutr., 132, 3674–9.CrossRefGoogle ScholarPubMed
Field, T., Diego, M., Hernandez-Reif, M.et al. (2003). Pregnancy anxiety and comorbid depression and anger: effects on the fetus and neonate. Depress. Anxiety, 17, 140–51.CrossRefGoogle ScholarPubMed
Fowden, A. L. and Forhead, A. J. (2004). Endocrine mechanisms of intrauterine programming. Reproduction, 127, 515–26.CrossRefGoogle ScholarPubMed
Fowden, A. L., Li, J. and Forhead, A. J. (1998). Glucocorticoids and the preparation for life after birth: are there long-term consequences of the life insurance?Proc. Nutr. Soc., 57, 113–22.CrossRefGoogle ScholarPubMed
Fraser, M., Braems, G. and Challis, J. R. G. (2001a). Developmental regulation of corticotrophin receptor gene expression in the adrenal gland of the ovine fetus and newborn lamb: effects of hypoxia during late pregnancy. J. Endocrinol., 169, 1–10.CrossRefGoogle Scholar
Fraser, M., Oliver, M. H., Harding, J. E., Gluckman, P. D. and Challis, J. R. G. (2001b). Alterations in ovine fetal adrenal corticotropin receptor and steroidogenic enzyme mRNA expresssion following maternal undernutrition in late pregnancy. J. Soc. Gynecol. Investig., 6, 116A.Google Scholar
French, N. P., Evans, S. F., Godfrey, K. M. and Newnham, J. P. (1999). Repeated antenatal corticosteroids: size at birth and subsequent development. Am. J. Obstet. Gynecol., 180, 114–21.CrossRefGoogle ScholarPubMed
French, , , N. P., Hagan, R., Evans, S. F., Mullan, A. and Newnham, J. P. (2004). Repeated antenatal corticosteroids: effects on cerebral palsy and childhood behaviour. Am. J. Obstet. Gynecol., 190, 588–95.CrossRefGoogle Scholar
Gale, C. R., Walton, S. and Martyn, C. N. (2003). Foetal and postnatal head growth and risk of cognitive decline in old ageBrain, 126, 2273–8.CrossRefGoogle ScholarPubMed
Glickman, J. A. and Challis, J. R. G. (1980). The changing response pattern of sheep fetal adrenal cells throughout the course of gestation. Endocrinology, 106, 1371–6.CrossRefGoogle ScholarPubMed
Glover, V., Connor, T. G., Heron, J. and Golding, J. (2004). Antenatal maternal anxiety is linked with atypical handedness in the child. Early Hum. Dev., 79, 107–18.CrossRefGoogle ScholarPubMed
Goland, R. S., Jozak, S., Warren, W. B., Conwell, I. M., Stark, R. I. and Tropper, P. J. (1993). Elevated levels of umbilical cord plasma corticotropin-releasing hormone in growth retarded fetuses. J. Clin. Endocrinol. Metab., 77, 1174–9.Google ScholarPubMed
Habib, M. and Galaburda, A. M. (1986). [Biological determinants of cerebral dominance]. Rev. Neurol. (Paris), 142, 869–94.Google Scholar
Haussmann, M. F., Carroll, J. A., Weesner, G. D., Daniels, M. J., Matteri, R. L. and Lay, D. C. Jr. (2000). Administration of ACTH to restrained, pregnant sows alters their pigs' hypothalamic–pituitary–adrenal (HPA) axis. J. Anim. Sci., 78, 2399–411.CrossRefGoogle ScholarPubMed
Hawkins, P., Steyn, C., McGarrigle, H. H. G.et al. (1999). Effect of maternal nutrient restiction in early gestation on development of the hypothalamic pituitary adrenal axis in fetal sheep at 0.8–0.9 of gestation. J. Endocrinol., 163, 553–61.CrossRefGoogle Scholar
Hawkins, P., Steyn, C., McGarrigle, H. H. G.et al. (2000). Effect of maternal nutrient restriction in early gestation on hypothalamic pituitary adrenal axis responses during acute hypoxemia in late gesation fetal sheep. Exp. Physiol., 85, 85–96.CrossRefGoogle Scholar
Hawkins, P., Hanson, M. A. and Matthews, S. G. (2001). Maternal undernutrition in early gestation alters molecular regulation of the hypothalamic–pituitary–adrenal axis in the ovine fetus. J. Neuroendocrinol., 13, 855–61.CrossRefGoogle ScholarPubMed
Herrick, K., Phillips, D. I., Haselden, S., Shiell, A. W., Campbell-Brown, M. and Godfrey, K. M. (2003). Maternal consumption of a high-meat, low-carbohydrate diet in late pregnancy: relation to adult cortisol concentrations in the offspring. J. Clin. Endocrinol. Metab., 88, 3554–60.CrossRefGoogle ScholarPubMed
Holmes, M. C., French, , K. L. and Seckl, J. R. (1997). Dysregulation of diurnal rhythms of serotonin 5-HT2C and corticosteroid receptor gene expression in the hippocampus with food restriction and glucocorticoids. J. Neurosci., 17, 4056–65.CrossRefGoogle ScholarPubMed
Huang, W. L., Beazley, L. D., Quinlivan, J. A., Evans, S., Newnham, J. and Dunlop, S. A. (1999). Effect of corticosteroids on brain growth in fetal sheepObstet. Gynecol., 94, 213–18.Google ScholarPubMed
Jacobson, L. and Sapolsky, R. M. (1991). The role of the hippocampus in feedback regulation of the hypothalamic–pituitary–adrenocortical axis. Endocr. Rev., 12, 118–34.CrossRefGoogle ScholarPubMed
Jacobson, L., Zurakowski, D. and Majzoub, J. A. (1997). Protein malnutrition increases plasma adrenocorticotropin and anterior pituitary proopiomelanocortin messenger ribonucleic acid in the rat. Endocrinology, 138, 1048–57.CrossRefGoogle ScholarPubMed
Kajantie, E., Dunkel, L., Turpeinen, U.et al. (2003). Placental 11β-hydroxysteroid dehydrogenase-2 and fetal cortisol/cortisone shuttle in small preterm infants. J. Clin. Endocrinol. Metab., 88, 493–500.CrossRefGoogle Scholar
Kari, M. A., Hallman, M., Eronen, M.et al. (1994). Prenatal dexamethasone treatment in conjunction with rescue therapy of human surfactant: a randomized placebo-controlled multicenter study. Pediatrics, 93, 730–6.Google ScholarPubMed
Koehl, M., Barbazanges, A., Moal, M. and Maccari, S. (1997). Prenatal stress induces a phase advance of circadian corticosterone rhythm in adult rats which is prevented by postnatal stress. Brain Res., 759, 317–20.CrossRefGoogle ScholarPubMed
Kofman, O. (2002). The role of prenatal stress in the etiology of developmental behavioural disorders. Neurosci. Biobehav. Rev., 26, 457–70.CrossRefGoogle ScholarPubMed
Kupfermann, I. (1991). Hypothalamus and limbic system: peptidergic neurons, homeostasis, and emotional behavior. In Principles of Neural Science (ed. Kandel, E. R., Schwartz, J. H. and Jessell, T. M.). New York, NY: Elsevier, pp. 735–49.Google Scholar
Langley-Evans, S. C., Gardner, D. S. and Jackson, A. A. (1996a). Maternal protein restriction influences the programming of the rat hypothalamic–pituitary–adrenal axis. J. Nutr., 126, 1578–85.CrossRefGoogle Scholar
Langley-Evans, S. C., Phillips, G. J., Benediktsson, R.et al. (1996b). Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat. Placenta, 17, 169–72.CrossRefGoogle Scholar
Laplante, P., Diorio, J. and Meaney, M. J. (2002). Serotonin regulates hippocampal glucocorticoid receptor expression via a 5-HT7 receptor. Brain Res. Dev. Brain Res., 139, 199–203.CrossRefGoogle Scholar
Lemaire, V., Koehl, M., LeMoal, M. and Abrous, D. N. (2000). Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl. Acad. Sci. USA, 97, 11032–7.CrossRefGoogle ScholarPubMed
Leon, D. A. (2001). Commentary. Getting to grips with fetal programming: aspects of a rapidly evolving agenda. Int. J. Epidemiol., 30, 96–8.CrossRefGoogle ScholarPubMed
Levidiotis, M. L., Oldfield, B. J. and Wintour, E. M. (1987). Corticotropin-releasing factor and arginine vasopressin fibre projections to the median eminence of fetal sheep. Neuroendocrinology, 46, 453–6.CrossRefGoogle ScholarPubMed
Levitt, N. S., Lindsay, R. S., Holmes, M. C. and 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, 412–19.CrossRefGoogle ScholarPubMed
Levitt, N. S., Lambert, E. V., Woods, D., Hales, C. N., Andrew, R. and Seckl, J. R. (2000). Impaired glucose tolerance and elevated blood pressure in low birth weight, nonobese, young south african adults: early programming of cortisol axis. J. Clin. Endocrinol. Metab., 85, 4611–18.Google ScholarPubMed
Liakos, P., Chambaz, E. M., Feige, J. J. and Defaye, G. (1998). Expression of ACTH receptors (MC2-R and MC5-R) in the glomerulosa and the fasciculata-reticularis zones of bovine adrenal cortex. Endocr. Res., 24, 427–32.CrossRefGoogle ScholarPubMed
Liggins, G. C. (1969). Premature delivery of fetal lambs infused with glucocorticoids. J. Endocrinol., 45, 515–23.CrossRefGoogle ScholarPubMed
Liggins, G. C. (1994). The role of cortisol in preparing the fetus for birth. Reprod., Fertil. Dev., 6, 141–50.CrossRefGoogle ScholarPubMed
Liggins, G. C. and Howie, R. N. (1972). A controlled trial of antepartum glucocorticoid treatment for prevention of the respiratory distress syndrome in premature infants. Pediatrics, 50, 515–25.Google ScholarPubMed
Liggins, G. C. and Kennedy, P. C. (1968). Effects of electrocoagulation of the fetal lamb hypophysis on growth and development. J. Endocrinol., 40, 371–81.CrossRefGoogle ScholarPubMed
Lindsay, R. S., Lindsay, R. M., Waddell, B. J. and Seckl, J. R. (1996). Prenatal glucocorticoid exposure leads to offspring hyperglycaemia in the rat: studies with the 11β-hydroxysteroid dehydrogenase inhibitor carbenoxolone. Diabetologia, 39, 1299–305.CrossRefGoogle Scholar
Lingas, R., Dean, F. and Matthews, S. G. (1999). Maternal nutient restriction (48h) modifies brain corticosteorid receptor expression and endocrine function in the fetal guinea pig. Brain Res., 846, 236–42.CrossRefGoogle Scholar
Lu, F. and Challis, J. R. G. (1994). Regulation of ovine fetal pituitary function by corticotrophin-releasing hormone, arginine vasopressin and cortisol in vitro. J. Endocrinol., 143, 199–208.CrossRefGoogle ScholarPubMed
Lunblad, J. R. and Roberts, J. L. (1988). Regulation of proopiomelanocortin gene expression in pituitary. Endocr. Rev., 9, 135–58.CrossRefGoogle Scholar
Mandell, A. J., Chapman, L. F., Rand, R. W. and Walter, R. D. (1963). Plasma corticosteroids: changes in concentration after stimulation of hippocampus and amygdala. Science, 139, 1212.CrossRefGoogle ScholarPubMed
Matthews, S. G. (2001). Antenatal glucocorticoids and the developing brain: mechanisms of action. Semin. Neonatol., 6, 309–17.CrossRefGoogle ScholarPubMed
Matthews, S. G. and Challis, J. R. G. (1995). Levels of proopiomelanocortin and prolactin mRNA in the fetal sheep pituitary following hypoxemia and glucocorticoid treatment in late gestation. J. Endocrinol., 147, 139–46.CrossRefGoogle ScholarPubMed
Matthews, S. G., Owen, D., Kalabis, G.et al. (2004). Fetal glucocorticoid exposure and hypothalamo–pituitary–adrenal (HPA) function after brith. Endocr. res., 30, 827–36.CrossRefGoogle Scholar
McCormick, C. M., Smythe, J. W., Sharma, S. and Meaney, M. (1995). Sex specific effects of prenatal stress on hypothalamic-pituitary adrenal responses to stress and brain gluccocorticoid receptors density in rats. Dev. Brain Res., 84, 55–61.CrossRefGoogle Scholar
McDonald, T. J., Hoffman, G. E. and Nathaneilsz, P. W. (1992). Hypothalamic paraventricular nuclear lesions delay corticotroph maturation in the fetal sheep anterior pituitary. Endocrinology, 131, 1101–6.CrossRefGoogle ScholarPubMed
McLaughlin, K. J. and Crowther, C. A. (2003). Repeat prenatal corticosteroids: who still recommends their use and why?Aust. NZ J. Obstet. Gynaecol., 43, 199–202.CrossRefGoogle Scholar
McMullen, S., Osgerby, J. C., Thurston, L. M.et al. (2004). Alterations in placental 11 beta-hydroxysteroid dehydrogenase (11 betaHSD) activities and fetal cortisol: cortisone ratios induced by nutritional restriction prior to conception and at defined stages of gestation in ewes. Reproduction, 127, 717–25.CrossRefGoogle ScholarPubMed
Meaney, M., Sapolsky, R. M. and McEwen, B. S. (1985). The development of the glucocorticoid receptor system in the rat limbic brain. I. Ontogeny and autoregulation. Dev. Brain Res., 18, 159–164.CrossRefGoogle Scholar
Modi, N., Lewis, H., Al-Naqeeb, N., Ajayi-Obe, M., Dore, C. J. and Rutherford, M. (2001). The effects of repeated antenatal glucocorticoid therapy on the developing brain. Pediatr. Res., 50, 581–5.CrossRefGoogle ScholarPubMed
Moss, T. J. M., Doherty, D., Nitsos, I., Sloboda, D. M., Harding, R. and Newnham, J. P. (2005). Effects into adulthood of single or repeated antenatal corticosteroids in sheep. Am. J. Obstet. Gynecol., 192, 146–52.CrossRefGoogle ScholarPubMed
Mulchahey, J. J., DiBlasio, A. M., Martin, M. C., Blumenfeld, Z. and Jaffe, R. B. (1987). Hormone production and peptide regulation of the human fetal pituitary gland. Endocr. Rev., 8, 406–425.CrossRefGoogle ScholarPubMed
Muneoka, K., Mikuni, M., Ogawa, T.et al. (1997). Prenatal dexamethasone exposure alters brain monoamine metabolism and adrenocortical response in rat offspring. Am. J. Physiol., 273, R1669–75.Google ScholarPubMed
Newnham, J. P., Evans, S. F., Godfrey, M., Huang, W., Ikegami, M. and Jobe, A. (1999). Maternal, but not fetal, administration of corticosteroids restricts fetal growth. J. Matern. Fetal Med., 8, 81–7.Google Scholar
NIH (1995). 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, 273, 413–18.CrossRef
NIH (2001). Antenatal corticosteroids revisited: repeat courses. National Institutes of Health Consensus Development Conference Statement, August 17–18, 2000. Obstet. Gynecol., 98, 144–50.
Norman, L. J., Lye, S. J., Wlodek, M. E. and Challis, J. R. G. (1985). Changes in pituitary responses to synthetic ovine corticotrophin releasing factor in fetal sheep. Can. J. Physiol. Pharmacol., 63, 1398–403.CrossRefGoogle ScholarPubMed
Connor, T. G., Heron, J., Golding, J. and Glover, V. (2003). Maternal antenatal anxiety and behavioural/emotional problems in children: a test of a programming hypothesis. J. Child Psychol. and Psychiatry., 44, 1025–36.CrossRefGoogle Scholar
Owen, D. and Matthews, S. G. (2003). Glucocorticoids and sex-dependent development of brain glucocorticoid and mineralocorticoid receptors. Endocrinology, 144, 2775–84.CrossRefGoogle ScholarPubMed
Page, R. B. (1988). The anatomy of the hypothalamo-hypophyseal complex. In The Physiology of Reproduction (ed. Knobil, E. and Neill, J. D.). New York, NY: Raven Press pp. 1161–233.Google Scholar
Pasamanick, B. and Lilienfeld, A. M. (1955). Association of maternal and fetal factors with development of mental deficiency. 1. Abnormalities in the prenatal and paranatal periods. J Am Med Assoc, 159, 155–60.CrossRefGoogle ScholarPubMed
Perry, R. A., Robinson, P. M. and Ryan, G. B. (1982). Ultrastructure of the pars intermedia of the developing sheep hypophysisCell Tissue Res., 224, 369–81.CrossRefGoogle ScholarPubMed
Perry, R. A., Mulvogue, H. M., McMillen, I. C. and Robinson, P. M. (1985). Immunohistochemical localization of ACTH in the adult and fetal sheep pituitary. J. Dev. Physiol., 7, 397–404.Google ScholarPubMed
Phillips, D. I. (2001). Fetal growth and programming of the hypothalamic–pituitary–adrenal axis. Clin. Exp. Pharmacol. Physiol., 28, 967–70.CrossRefGoogle ScholarPubMed
Quinlivan, J. A., Dunlop, S. A., Newnham, J., Evans, S. F. and Beazley, L. D. (1999). Repeated, but not single, maternal administration of corticosteroids delays myelination in the brain of fetal sheep. Prenat. Neonatal Med., 4, 47–55.Google Scholar
Reperant, E. N. and Durand, P. (1997). The development of the ovine fetal adrenal gland and its regulation. Reprod. Nutr. Dev. 37, 81–95.CrossRefGoogle Scholar
Reul, J. M. H. M. and Kloet, E. R. (1985). Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology, 117, 2505–11.CrossRefGoogle ScholarPubMed
Reynolds, R. M., Walker, B. R., Syddall, H. E.et al. (2001a). Altered control of cortisol secretion in adult men with low birth weight and cardiovascular risk factors. J. Clin. Endocrinol. Metab., 86, 245–50.Google Scholar
Reynolds, R. M., Walker, B. R., Syddall, H. E.et al. (2001b). Elevated plasma cortisol in glucose-intolerant men: differences in responses to glucose and habituation to venepuncture. J. Clin. Endocrinol. Metab., 86, 1149–53.CrossRefGoogle Scholar
Richards, M., Hardy, R., Kuh, D. and Wadsworth, M. E. J. (2001). Birth weight and cognitive function in the British 1946 birth cohort: longitudinal population based study. BMJ, 322, 199–203.CrossRefGoogle ScholarPubMed
Roussel, S., Hemsworth, P. H., Boissy, A. and Duvaux-Ponter, C. (2004). Effects of repeated stress during pregnancy in ewes on the behavioural and physiological responses to stressful events and birth weight of their offspring. Appl. Anim. Behav. Sci., 85, 259–76.CrossRefGoogle Scholar
Rubin, R. T., Mandell, A. J. and Crandall, P. H. (1966). Corticosteroid responses to limbic stimulation in man: localization of stimulus site. Science, 153, 767–8.CrossRefGoogle Scholar
Sebaai, N., Lesage, J., Breton, C., Vieau, D. and Deloof, S. (2004). Perinatal food deprivation induces marked alterations of the hypothalamo–pituitary–adrenal axis in 8-month-old male rats both under basal conditions and after a dehydration period. Neuroendocrinology, 79, 163–73.CrossRefGoogle ScholarPubMed
Setiawan, E., Owen, D., McCabe, L., Kostaki, A., Andrews, M. H. and Matthews, S. G. (2004). Glucocorticoids do not alter developmental expression of hippocampal or pituitary steroid receptor coactivator-1 and -2 in the late gestation fetal guinea pig. Endocrinology, 145, 3796–803.CrossRefGoogle ScholarPubMed
Sloboda, D. M., Newnham, J. and Challis, J. R. G. (2000). Effects of repeated maternal betamethasone administration on growth and hypothalamic–pituitary–adrenal function of the ovine fetus at term. J. Endocrinol., 165, 79–91.CrossRefGoogle ScholarPubMed
Sloboda, D. M., Moss, T. J., Gurrin, L. C., Newnham, J. and Challis, J. R. G. (2002). The effect of prenatal betamethasone administration on postnatal ovine hypothalamic–pituitary–adrenal function. J. Endocrinol., 172, 71–81.CrossRefGoogle ScholarPubMed
Sloboda, D. M., Moss, T., Nitsos, I., Doherty, D. A., Challis, J. R. G. and Newnham, J. P. (2003). Antenatal glucocorticoid treatment in sheep results in adrenal suppression in adulthood. J. Soc. Gynecol. Investig., 10, 233A.Google Scholar
Stathis, S. L., Callaghan, M., Harvey, J. and Rogers, Y. (1999). Head circumference in ELBW babies is associated with learning difficulties and cognition but not ADHD in the school-aged child. Dev. Med. Child Neurol., 41, 375–80.CrossRefGoogle Scholar
Stewart, P. M., Rogerson, F. M. and Mason, J. I. (1995). Type 2 11β 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, 885–90.Google ScholarPubMed
Swanson, L. W. and Sawchenko, P. E. (1983). Hypothalamic integration: organization of the paraventricular and supraoptic nuclei. Ann. Rev. Neurosci., 6, 269–324.CrossRefGoogle ScholarPubMed
Swanson, L. W. and Simmons, D. M. (1989). Differential steroid hormone and neural influences on peptide mRNA levels in CRH cells of the paraventricular nucleus: a hybridization histochemical study in the rat. J. Comp. Neurol., 285, 413–35.CrossRefGoogle ScholarPubMed
Takahashi, L. K. (1998). Prenatal stress: consequences of glucocorticoids on hippocampal development and function. Internat. J. Neurosci., 16, 199–207.Google ScholarPubMed
Takahashi, L. K. and Kalin, N. H. (1991). Early developmental and temporal characteristics of stress-induced secretion of pituitary adrenal hormones in prenatally stressed rat pups. Brain Res., 558, 75–8.CrossRefGoogle ScholarPubMed
Tonolo, G., Fraser, G., Connell, J. M. and Kenyon, C. J. (1988). Chronic low dose infusions of dexamethasone in rats: effects on blood pressure, body weight and plasma atrial natriuretic peptide. J. Hypertens., 6, 25–31.CrossRefGoogle ScholarPubMed
Toth, M. (2003). 5-HT1A receptor knockout mouse as a genetic model of anxiety. Eur. J. Pharmacol., 463, 177–84.CrossRefGoogle ScholarPubMed
Uno, H., Lohmiller, L., Thieme, C.et al. (1990). Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques. I. Hippocampus. Dev. Brain Res., 53, 157–67.CrossRefGoogle ScholarPubMed
Uno, H., Eisele, S., Sakai, A.et al. (1994). Neurotoxicity of glucocorticoids in the primate brain. Horm. Behav., 28, 336–48.CrossRefGoogle ScholarPubMed
Vallee, M., Mayo, W., Maccari, S., Moal, M. and Simon, H. (1996). Long-term effects of prenatal stress and handling on metabolic parameters: relationship to corticosterone secretion response. Brain Res., 712, 287–92.CrossRefGoogle ScholarPubMed
Bergh, B. R. and Marcoen, A. (2004). High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-oldsChild Dev., 75, 1085–97.CrossRefGoogle ScholarPubMed
Vazquez, D. M., Oers, H., Levine, S. and Akil, H. (1996). Regulation of glucocorticoid and mineralocorticoid receptor mRNAs in the hippocampus of the maternally deprived infant rat. Brain Res., 761, 79–90.CrossRefGoogle Scholar
Wang, J. J., Valego, N. K., Su, Y., Smith, J. and Rose, J. C. (2004). Developmental aspects of ovine adrenal adrenocorticotropic hormone receptor expression. J. Soc. Gynecol. Investig., 11, 27–35.CrossRefGoogle ScholarPubMed
Weaver, I. C., Cervoni, N., Champagne, F. A.et al. (2004). Epigenetic programming by maternal behavior. Nat. Neurosci., 7, 847–54.CrossRefGoogle ScholarPubMed
Webb, P. D. (1980). Development of the adrenal cortex in the fetal sheep: an ultrastructural study. J. Dev. Physiol., 2, 161–81.Google ScholarPubMed
Weinstock, M. (1996). Does prenatal stress impair coping and regulation of hypothalamic–pituitary–adrenal axis?Neurosci. Biobehav. Rev., 21, 1–10.CrossRefGoogle Scholar
Weinstock, M., Matlina, E., Maor, G. I., Rosen, H. and McEwen, B. S. (1992). Prenatal stress selectively alters the reactivity of the hypothalamic–pituitary–adrenal system in the female ratBrain Res., 595, 195–200.CrossRefGoogle ScholarPubMed
Welberg, L. A. M. and Seckl, J. R. (2001). Prenatal stress, glucocorticoids and the programming of the brain. J. Neuroendocrinol., 13, 113–28.CrossRefGoogle Scholar
Welberg, L. A. M., Seckl, J. R. and Holmes, M. C. (2000). Inhibition of 11β-hydroxysteroid dehydrogenase, the fetal–placental barrier to maternal glucocorticoids, permanenetly programs amygdala GRmRNA expression and anxiety-like behaviour in the offspring. Eur. J. Neurosci., 12, 1047–54.CrossRefGoogle Scholar
Wintour, E. M., Brown, E. H., Denton, D. A.et al. (1975). The ontogeny and regulation of corticosteroid secretion by the ovine foetal adrenal. Acta Endocrinol., 79, 301–16.Google ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×