29
Views
3
CrossRef citations to date
0
Altmetric
Review

Prenatal glucocorticoid exposure and physiological programming of adult disease

Pages 391-402 | Published online: 10 Jan 2014

References

  • Barker DJP, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischemic heart disease.Lancet2, 577–580 (1989).
  • Barker DJP, Gluckman PD, Godfrey KM, Harding JE, Owens JA, Robinson JS. Fetal nutrition and cardiovascular disease in adult life.Lancet341, 938–941 (1993).
  • Curhan GC, Willett WC, Rimm EB, Spiegelman D, Ascherio AL, Stampfer MJ. Birth weight and adult hypertension, diabetes mellitus, and obesity in US men.Circulation94, 3246–3250 (1996).
  • Leon DA, Koupilova I, Lithell HO et al. Failure to realise growth potential in utero and adult obesity in relation to blood pressure in 50 year old Swedish men.Br. Med. J.312, 401–406 (1996).
  • Forsen T, Eriksson JG, Tuomilehto J, Teramo K, Osmond C, Barker DJP. Mother’s weight in pregnancy and coronary heart disease in a cohort of Finnish men: follow up study.Br. Med. J.315, 837–840 (1997).
  • Yajnik CS, Fall CHD, Vaidya U et al. Fetal growth and glucose and insulin metabolism in four-year- old Indian children.Diab. Med.12, 330–336 (1995).
  • Hales CN, Barker DJP. Type 2 (non-insulin-dependent) diabetes mellitus; the thrifty phenotype hypothesis.Diabetologia35, 595–601 (1992).
  • Weismann A.Essays on Heredity and Kindred Biological Problems. Edward B, Poulton, Selmar S, Arthur ES (Eds). Claredon Press, Oxford, UK (1892).
  • Arai Y, Gorski RA. Critical exposure time for androgenization of the developing hypothalamus in the female rat.Endocrinology82, 1010–1014 (1968).
  • Gustafsson JA, Mode A, Norstedt G, Skett P. Sex steroid-induced changes in hepatic enzymes.Ann. Rev. Physiol.45, 51–60 (1983).
  • Edwards CRW, Benediktsson R, Lindsay R, Seckl JR. Dysfunction of the placental glucocorticoid barrier: a link between the fetal environment and adult hypertension?Lancet341, 355–357 (1993).
  • Yamamoto KR. Steroid receptor regulated transcription of specific genes and gene networks.Ann. Rev. Gen.19, 209–252 (1985).
  • Sheppard KE. Corticosteroid receptors, 11β-hydroxysteroid dehydrogenase, and the heart.Vitam. Horm.66, 77–112 (2003).
  • Howlett TA, Rees LH, Besser GM. Cushing’s syndrome.Clin. Endocrinol. Metab.14, 911–945 (1985).
  • Liggins GC. The role of cortisol in preparing the fetus for birth.Reprod. Fertil. Dev.6, 141–150 (1994).
  • Ballard PL. Glucocorticoids and differentiation. In:Glucocorticoid Hormone Action (Monographs in Endocrinology). Rousseau GG (Ed.). Springer-Verlag, Berlin, 493–497 (1979).
  • Fowden AL. Endocrine regulation of fetal growth.Reprod. Fertil. Dev.7, 351–363 (1995).
  • Cole T, Blendy JA, Monaghan AP et al. Targeted disruption of the glucocorticoid receptor blocks adrenergic chromaffin cell development and severely retards lung maturation.Genes Dev.9, 1608–1621 (1995).
  • NIH Consensus Development Conference. Effect of corticosteroid for fetal maturation on perinatal outcomes.Am. J. Obstetr. Gynecol.173(Suppl.), 253–344 (1995).
  • Ward RM. Pharmacologic enhancement of fetal lung maturation.Clin. Perinatol.21, 523–542 (1994).
  • Reinisch JM, Simon NG, Karwo WG, Gandleman R. Prenatal exposure to prednisone in humans and animals retards intra-uterine growth.Science202, 436–438 (1978).
  • Goland RS, Josak S, Warren WB, Conwell IM, Stark RI, Tropper PJ. Elevated levels of umbilical cord plasma corticotrophin-releasing hormone in growth-retarded fetuses. J.Clin. Endocrinol. Metab.77, 1174–1179 (1993).
  • Rashid S, Lewis GF. The mechanisms of differential glucocorticoid and mineralocorticoid action in the brain and peripheral tissues.Clin. Biochem.38, 401–409 (2005).
  • McCabe L, Marash D, Li A, Matthews SG. Repeated antenatal glucocorticoid treatment decreases hypothalamic corticotropin releasing hormone mRNA but not corticosteroid receptor mRNA expression in the fetal guinea-pig brain.J. Neuroendocrinol.13, 425–431 (2001).
  • Campbell AL, Murphy BEP. The maternal-fetal cortisol gradient during pregnancy and at delivery.J. Clin. Endocrinol. Metab.45, 435–440 (1977).
  • Seckl JR. Glucocorticoids, feto-placental 11β-hydroxysteroid dehydrogenase type 2 and the early life origins of adult disease.Steroids62, 89–94 (1997).
  • Funder JW, Pearce PT, Smith R, Smith AI. Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated.Science242, 583–585 (1988).
  • Brown RW, Chapman KE, Kotelevtsev Y et al. Cloning and production of antisera to human placental 11 β-hydroxysteroid dehydrogenase type 2.Biochem. J.313, 1007–1017 (1996).
  • Stewart PM, Corrie JET, Shackleton CHL, Edwards CRW. Syndrome of apparent mineralocorticoid excess: a defect in the cortisol-cortisone shuttle.J. Clin. Invest.82, 340–349 (1988).
  • Mune T, Rogerson FM, Nikkilä H, Agarwal AK, White PC. Human hypertension caused by mutations in the kidney isozyme of 11β-hydroxysteroid dehydrogenase.Nature Gen.10, 394–399 (1995).
  • Stewart PM, Rogerson FM, Mason JI. Type 2 11β-hydroxysteroid dehydrogenase messenger RNA and activity in human placenta and fetal membranes: its relationship to birth weight and putative role in fetal steroidogenesis.J. Clin. Endocrinol. Metab.80, 885–890 (1995).
  • Alikhani-Koopaei R, Fouladkou F, Frey FJ, Frey BM. Epigenetic regulation of 11 β-hydroxysteroid dehydrogenase type 2 expression.J. Clin. Invest.114, 1146–1157 (2004).
  • Pepe G, Albrecht E. Actions of placental and fetal adrenal steroid hormones in primate pregnancy.Endocrinol. Rev.16, 608–648 (1995).
  • Langley-Evans SC, Phillips PG, Benediktsson R et al. Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat.Placenta17, 169–172 (1996).
  • Langley-Evans, SC. Hypertension induced by fetal exposure to a maternal low-protein diet, in the rat, is prevented by pharmacological blockade of maternal glucocorticoid synthesis.J. Hypertens.15, 537–544 (1997).
  • Sugden MC, Langdown ML, Munns MJ, Holness MJ. Maternal glucocorticoid treatment modulates placental leptin physiology during late pregnancy, and elicits hypertension associated with hyperleptinaemia in the early-growth-retarded adult offspring.Eur. J. Endocrinol.145, 529–539 (2001).
  • Woods LL, Weeks DA. Prenatal programming of adult blood pressure: role of maternal corticosteroids.Am. J. Physiol. Regul. Integr. Comp. Physiol.289, R955–R962 (2005).
  • Benediktsson R, Lindsay R, Noble J, Seckl JR, Edwards CRW. Glucocorticoid exposure in utero: a new model for adult hypertension.Lancet341, 339–341 (1993).
  • Levitt N, Lindsay RS, Holmes MC, Seckl JR. Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring in the rat.Neuroendocrinology64, 412–418 (1996).
  • Lindsay RS, Lindsay RM, Edwards CRW, Seckl JR. Inhibition of 11β-hydroxysteroid dehydrogenase in pregnant rats and the programming of blood pressure in the offspring.Hypertension27, 1200–1204 (1996).
  • Dodic M, May CN, Wintour EM, Coghlan JP. An early prenatal exposure to excess glucocorticoid leads to hypertensive offspring in sheep.Clin. Sci.94, 149–155 (1998).
  • Dodic M, Hantzis V, Duncan J et al. Programming effects of short prenatal exposure to cortisol.FASEB J.16, 1017–1026 (2002).
  • Moss TJ, Sloboda DM, Gurrin LC Harding R, Challis JR, Newnham JP. Programming effects in sheep of prenatal growth restriction and glucocorticoid exposure.Am. J. Physiol.281, R960–R970 (2001).
  • Wintour EM, Johnson K, Koukoulas I, Moritz K, Tersteeg M, Dodic M. Programming the cardiovascular system, kidney and the brain – a review.Placenta24(Suppl. A), S65–S71 (2003).
  • Tangalakis K, Lumbers ER, Moritz KM, Wintour EM, Moritz KM. Effect of cortisol on blood pressure and vascular reactivity in the ovine fetus.Exp. Physiol.77, 709–717 (1992).
  • Koenen SV, Mecenas CA, Smith GS, Jenkins S, Nathanielsz PW. Effects of maternal betamethasone administration on fetal and maternal blood pressure and heart rate in the baboon at 0.7 of gestation.Am. J. Obstet. Gynecol.186, 812–817 (2002).
  • Kari MA, Hallman M, Eronen M et al. Prenatal dexamethasone treatment in conjunction with rescue therapy of human surfactant: a randomized placebo-controlled multicenter study.Pediatrics93, 730–736 (1994).
  • Matthews SG. Antenatal glucocorticoids and programming of the developing CNS.Pediatr. Res.47, 291–300 (2000).
  • Ortiz LA, Quan A, Weinberg A, Baum M. Effect of prenatal dexamethasone on rat renal development.Kidney Int.59, 1663–1669 (2001).
  • Wintour EM, Moritz KM, Johnson K, Ricardo S, Samuel CS, Dodic M. Reduced nephron number in adult sheep, hypertensive as a result of prenatal glucocorticoid treatment.J. Physiol.549, 929–935 (2003).
  • Zimmermann H, Gardner DS, Jellyman JK, Fowden AL, Giussani DA, Forhead AJ. Effect of dexamethasone on pulmonary and renal angiotensin-converting enzyme concentration in fetal sheep during late gestation.Am. J. Obstet. Gynecol.189, 1467–1471 (2003).
  • Molnar J, Howe DC, Nijland MJM, Nathanielsz PW. Prenatal dexamethasone leads to both endothelial dysfunction and vasodilatory compensation in sheep.J. Physiol.547, 61–66 (2003).
  • Roghair RD, Segar JL, Sharma RV et al. Newborn lamb coronary artery reactivity is programmed by early gestation dexamethasone prior to the onset of systemic hypertension.Am. J. Physiol. Regul. Integr. Comp. Physiol.289, R1169–R1176 (2005).
  • Bian XP, Seidler FJ, Slotkin TA. Fetal dexamethasone exposure interferes with establishment of cardiac noradrenergic innervation and sympathetic activity.Teratology47, 109–117 (1993).
  • Langdown ML, Holness MJ, Sugden MC. Early growth retardation induced by excessive exposure to glucocorticoids in utero selectively increases cardiac GLUT1 protein expression and Akt/protein kinase B activity in adulthood.J. Endocrinol.169, 11–22 (2001).
  • Langdown ML, Holness MJ, Sugden MC. Effects of prenatal glucocorticoid exposure on cardiac calreticulin and calsequestrin protein expression during early development and in adulthood.Biochem. J.371, 61–69 (2003).
  • Lindsay RS, Lindsay RM, Waddell BJ, Seckl JR. Prenatal glucocorticoid exposure leads to offspring hyperglycemia in the rat: studies with 11β-hydroxysteroid dehydrogenase inhibitor carbenoxolone.Diabetologia39, 1299–1305 (1996).
  • Nyirenda MJ, Lindsay RS, Kenyon CJ, Burchell A, Seckl JR. 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 (1998).
  • Nyirenda MJ, Welberg LA, Seckl JR. Programming hyperglycemia in the rat through prenatal exposure to glucocorticoids-fetal effect or maternal influence?J. Endocrinol.170, 653–60 (2001).
  • Lesage J, Del-Favero F, Leonhardt M et al. Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat.J. Endocrinol.181, 291–296 (2004).
  • Avishai-Eliner S, Brunson KL, Sandman CA, Baram TZ. Stressed-out, or in utero?Trends Neurosci.25, 518–524 (2002).
  • Consoli A, Nurjhan N. Contribution of gluconeogenesis to overall glucose output in diabetic and nondiabetic men.Ann. Med.22, 191–195 (1990).
  • Valera A, Pujol A, Pelegrin M, Bosch F. Transgenic mice overexpressing phosphoenolpyruvate carboxykinase develop non-insulin-dependent diabetes.Proc. Natl Acad. Sci. USA91, 9151–9154 (1994).
  • Xanthopoulos KG, Mirkovitch J. Gene regulation in rodent hepatocyte during development, differentiation and disease.Eur. J. Biochem.216, 353–360 (1993).
  • Cleasby ME, Kelly PA, Walker BR, Seckl JR. Programming of rat muscle and fat metabolism by in utero overexposure to glucocorticoids.Endocrinology144, 999–1007 (2003).
  • Nyirenda MJ, Dean S, Lyons V, Chapman KE, Seckl JR. Prenatal programming of hepatocyte nuclear factor (HNF)4α in the rat: a key mechanism in the ‘foetal origins of hyperglycaemia’?Diabetologia (2006) (In Press).
  • Fowden AL, Forhead AJ. Endocrine mechanisms of intrauterine programming.Reproduction127, 515–526 (2004).
  • Drake AJ, Walker BR. The intergenerational effects of fetal programming: non-genomic mechanisms for the inheritance of low birth weight and cardiovascular risk.J. Endocrinol.180, 1–16 (2004).
  • Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring.J. Nutr.135, 1382–1386 (2005).
  • Blondeau B, Lesage J, Czernichow P, Dupouy JP, Breant B. Glucocorticoids impair fetal β-cell development in rats.Am. J. Physiol. Endocrinol. Metab.281, E592–E599 (2001).
  • Garofano A, Czernichow P, Breant B. β-cell mass and proliferation following late fetal and early postnatal malnutrition in the rat.Diabetologia41, 1114–1120 (1998).
  • Blondeau B, Lesage J, Czernichow P, Dupouy JP, Breant B. Glucocorticoids impair fetal β-cell development in rats.Am. J. Physiol.281, E592–E599 (2001).
  • Gesina E, Tronche F, Herrera P et al. Dissecting the role of glucocorticoids on pancreas development.Diabetes53, 2322–2329 (2004).
  • Dahlgren J, Nilsson C, Jennische E et al. Prenatal cytokine exposure results in obesity and gender-specific programming.Am. J. Physiol.281, E326–E334 (2001).
  • Whorwood CB, Firth KM, Budge H, Symonds ME. Maternal undernutrition during early to midgestation programs tissue-specific alterations in the expression of the glucocorticoid receptor, 11 β-hydroxysteroid dehydrogenase isoforms, and type 1 angiotensin II receptor in neonatal sheep.Endocrinology142, 2854–2864 (2001).
  • Bispham J, Gopalakrishnan GS, Dandrea J et al. Maternal endocrine adaptation throughout pregnancy to nutritional manipulation: consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development.Endocrinology144, 3575–3585 (2003).
  • Gnanalingham MG, Mostyn A, Symonds ME, Stephenson T. Ontogeny and nutritional programming of adiposity in sheep: potential role of glucocorticoid action and uncoupling protein-2.Am. J. Physiol. Regul. Integr. Comp. Physiol.289, R1407–R1415 (2005).
  • Gould E, Cameron HA. Regulation of neuronal birth, migration and death in the rat dentate gyrus.Dev. Neurosci.18, 22–35 (1996).
  • Bakker JM, van Bel F, Heijnen CJ. Neonatal glucocorticoids and the developing brain: short-term treatment with life-long consequences?Trends Neurosci.24, 649–653 (2001).
  • Meaney MJ, Aitken DH, van Berkel C, Bhatnagar S, Sapolsky RM. Effect of neonatal handling on age-related impairments associated with the hippocampus.Science239, 766–768 (1988).
  • Brown RW, Diaz R, Robson AC et al. The ontogeny of 11β-hydroxysteroid dehydrogenase type 2 and mineralocorticoid receptor gene expression reveal intricate control of glucocorticoid action in development.Endocrinology137, 794–797 (1996).
  • Stewart PM, Murry BA, Mason JI. Type 2 11β-hydroxysteroid dehydrogenase in human fetal tissues.J. Clin. Endocrinol. Metab.78, 1529–1532 (1994).
  • Matthews SG. Early programming of the hypothalamo–pituitary–adrenal axis. TrendsEndocrinol. Metab.13, 373–380 (2002).
  • Welberg LA, Seckl JR. Prenatal stress, glucocorticoids and the programming of the brain.J. Neuroendocrinol.13, 113–128 (2001).
  • Slotkin TA, Zhang J, McCook EC, Seidler FJ. Glucocorticoid administration alters nuclear transcription factors in fetal rat brain: implications for the use of antenatal steroids.Brain Res. Dev. Brain. Res.111, 11–24 (1998).
  • Takahashi LK. Prenatal stress: consequences of glucocorticoids on hippocampal development and function.Int. J. Dev. Neurosci.16, 199–207 (1998).
  • De Kloet ER, Vreugdenhil E, Oitzl MS, Joels M. Brain corticosteroid receptor balance in health and disease.Endocrinol. Rev.19, 269–301 (1998).
  • Beggs JM, Brown TH, Byrne JH et al. Learning and memory: basic mechanisms. In:Fundamental Neuroscience. Zigmond MJ, Bloom FE, Landis SC, Roberts JL, Squire LR (Eds). Academic Press, CA, USA 1411–1454 (1999).
  • Huang WL, Harper CG, Evans SF, Newnham JP, Dunlop SA. Repeated prenatal corticosteroid administration delays astrocyte and capillary tight junction maturation in fetal sheep.Int. J. Dev. Neurosci.19, 487–493 (2001).
  • Uno H, Lohmiller L, Thieme C et al. Brain damage induced by prenatal exposure to dexamethasone in fetal rhesus macaques. I. hippocampus.Dev. Brain Res.53, 157–167 (1990).
  • Sheline YI, Wang PW, Gado MH, Csernansky JG, Vannier MW. Hippocampal atrophy in recurrent major depression.Proc. Natl Acad. Sci. USA93, 3908–3913 (1996).
  • Uno H, Eisele S, Sakai A et al. Neurotoxicity of glucocorticoids in the primate brain.Horm. Behav.28, 336–348 (1994).
  • Jacobson L, Sapolsky R. The role of the hippocampus in feedback regulation of the hypothalamic–pituitary–adrenocortical axis.Endocrinol. Rev.12, 118–134 (1991).
  • Herman JP, Prewitt CM, Cullinan WE. Neuronal circuit regulation of the hypothalamo–pituitary–adrenocortical stress axis.Crit. Rev. Neurobiol.10, 371–394 (1996).
  • Dean F, Matthews SG. Maternal dexamethasone treatment in late gestation alters glucocorticoid and mineralocorticoid receptor mRNA in the fetal guinea pig brain.Brain Res.846, 253–259 (1999).
  • McCormick CM, Smythe JW, Sharma S, Meaney MJ. Sex-specific effects of prenatal stress on hypothalamic–pituitary–adrenal responses to stress and brain glucocorticoid receptor density in adult rats.Dev. Brain Res.84, 55–61 (1995).
  • Bertram C, Trowern AR, Copin N, Jackson AA, Whorwood CB. The maternal diet during pregnancy programs altered expression of the glucocorticoid receptor and type 2 11β-hydroxysteroid dehydrogenase: Potential molecular mechanisms underlying the programming of hypertension in utero.Endocrinology142, 2841–2853 (2001).
  • Koehl M, Lemaire V, Mayo W et al. Individual vulnerability to substance abuse and affective disorders: role of early environmental influences.Neurotox. Res.4, 281–296 (2002).
  • French NP, Hagan R, Evans SF, Mullan A, Newnham JP. Repeated antenatal corticosteroids: effects on cerebral palsy and childhood behaviour.Am. J. Obstet. Gynecol.190, 588–595 (2004).
  • O’Connor TG, Heron J, Golding J, Glover V. Maternal anteanatal anxiety and behavioural problems in children: a test of a programming hypothesis.J. Child Psychol. Psych.44, 1025–1036 (2003).
  • Velisek L. Prenatal corticosteroid impact on hippocampus: implications for postnatal outcomes.Epilepsy Behav.7, 57–67 (2005).
  • Feldman S, Weidenfeld J. The excitatory effects of the amygdala on hypothalamo–pituitary–adrenocortical responses are mediated by hypothalamic norepinephrine, serotonin, and CRF-41.Brain. Res. Bull.45, 389–393 (1998).
  • Tronche F, Kellendonk C, Kretz O et al. Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety.Nature Gen.23, 99–103 (1999).
  • Diaz R, Ögren SO, Blum M, Fuxe K. Prenatal corticosterone increases spontaneous and d-amphetamine induced locomotor activity and brain dopamine metabolism in prepubertal male and female rats.Neuroscience66, 467–473 (1995).
  • Emgard M, Paradisi M, Pirondi S, Fernandez M, Giardino L, Calza L. Prenatal glucocorticoid exposure affects learning and vulnerability of cholinergic neurons.Neurobiol. Aging (2006) (In Press).
  • Koenig JI, Kirkpatrick B, Lee P. Glucocorticoid hormones and early brain development in schizophrenia.Neuropsychopharmacology27, 309–318 (2002).
  • Bremne JD, Vermetten E. Stress and development: behavioural and biological consequences.Dev. Psychopathol.13, 473–489 (2001).
  • Heim C, Nemeroff CB. The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies.Biol. Psych.49, 1023–1039 (2001).
  • Plotsky PM, Meaney MJ. Early, postnatal experience alters hypothalamic corticotropin-releasing factor (CRF) mRNA, median eminence CRF content and stress-induced release in adult rats.Mol. Brain Res.18, 195–200 (1993).
  • Weaver IC, Cervoni N, Champagne FA et al. Epigenetic programming by maternal behaviour.Nature Neurosci.7, 847–854 (2004).
  • Rayburn W. Glucocorticoid therapy for rheumatic diseases: maternal, fetal, and breast feeding considerations.Am. J. Reprod. Immunol.28, 138–140 (1992).
  • Kattner E, Metze B, Waiss E, Obladen M. Accelerated lung maturation following maternal steroid treatment in infants born before 30 weeks gestation.J. Perinat. Med.20, 449–457 (1992).
  • Speiser PW, New MI. Prenatal diagnosis and management of congenital adrenal hyperplasia.Clin. Perinatol.21, 631–645 (1994).
  • Aghajafari F, Murphy K, Willan A et al. Multiple courses of antenatal corticosteroids: a systematic review and meta-analysis.Am. J. Obstet. Gynecol.185, 1073–1080 (2001).
  • Dessens AB, Haas HS, JG Koppe. Twenty-year follow-up of antenatal corticosteroid treatment.Pediatrics105, E77 (2000).
  • Doyle LW, Ford GW, Davis NM, Callanan C. Antenatal corticosteroid therapy and blood pressure at 14 years of age in preterm children.Clin. Sci.98, 137–142 (2000).
  • Dalziel SR, Walker NK, Parag V et al. Cardiovascular risk factors after antenatal exposure to betamethasone: 30-year follow-up of a randomised controlled trial.Lancet365, 1856–1862 (2005).
  • Clark PM, Hindmarsh PC, Shiell AW, Law CM, Honour JW, Barker DJP. Size at birth and adrenocortical function in childhood.Clin. Endocrinol.45, 721–726 (1996).
  • Trautman PD, Meyer-Bahlburg HFL, Postelnek J, New MI. Effects of early prenatal dexamethasone on the cognitive and behavioural development of young children: results of a pilot study.Psychoneuroendocrinology20, 439–449 (1995).
  • Lajic S, Wedell A, Bui TH, Ritzen EM, Holst M. Long-term somatic follow-up of prenatally treated children with congenital adrenal hyperplasia. J.Clin. Endocrinol. Metab.83, 3872–3880 (1998).
  • Levitt NS, Lambert EV, Woods D, Hales NC, Andrew R, Seckl JR. Impaired glucose tolerance and elevated blood pressure in low birth weight, non obese, young south african adults: early programming of cortisol axis.J. Clin. Endocrinol. Metab.85, 4611–4618 (2000).
  • Reynolds RM, Walker BR, Syddall HE et al. Altered control of cortisol secretion in adult men with low birth weight and cardiovascular risk factors.J. Clin. Endocrinol. Metab.86, 245–250 (2001).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.