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Stress
The International Journal on the Biology of Stress
Volume 14, 2011 - Issue 6: The Parental Brain and the Next Generation
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Themed Reviews

Stress, glucocorticoids and liquorice in human pregnancy: Programmers of the offspring brain

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Pages 590-603 | Received 18 Jan 2011, Accepted 04 May 2011, Published online: 29 Aug 2011

References

  • Alastalo H, Räikkönen K, Pesonen A-K, Osmond C, Barker DJ, Kajantie E, Heinonen K, Forsen TJ, Eriksson JG. 2009. Cardiovascular health of Finnish war evacuees 60 years later. Ann Med. 41:66–72.
  • Austin MP, Hadzi-Pavlovic D, Leader L, Saint K, Parker G. 2005. Maternal trait anxiety, depression and life event stress in pregnancy: Relationships with infant temperament. Early Hum Dev. 81:183–190.
  • Barker DJ. 1991. The intrauterine environment and adult cardiovascular disease. Ciba Found Symp. 156:3–10 discussion 10–6.
  • Barker DJ. 1998. In utero programming of chronic disease. Clin Sci (Lond). 95:115–128.
  • Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. 1989. Weight in infancy and death from ischaemic heart disease. Lancet. 2:577–580.
  • Barker DJ, Osmond C, Rodin I, Fall CH, Winter PD. 1995. Low weight gain in infancy and suicide in adult life. Br Med J. 311:1203.
  • Barker DJ, Osmond C, Forsen TJ, Kajantie E, Eriksson JG. 2005. Trajectories of growth among children who have coronary events as adults. N Engl J Med. 353:1802–1809.
  • Belmaker RH, Agam G. 2008. Major depressive disorder. N Engl J Med. 358:55–68.
  • Benediktsson R, Lindsay RS, Noble J, Seckl JR, Edwards CR. 1993. Glucocorticoid exposure in utero: New model for adult hypertension. Lancet. 341:339–341.
  • Benediktsson R, Calder AA, Edwards CR, Seckl JR. 1997. Placental 11 beta-hydroxysteroid dehydrogenase: A key regulator of fetal glucocorticoid exposure. Clin Endocrinol (Oxf). 46:161–166.
  • Bergman K, Sarkar P, O'Connor TG, Modi N, Glover V. 2007. Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. J Am Acad Child Adolesc Psychiatry. 46:1454–1463.
  • Bolt RJ, van Weissenbruch MM, Lafeber HN, Delemarre-van de Waal HA. 2001. Glucocorticoids and lung development in the fetus and preterm infant. Pediatr Pulmonol. 32:76–91.
  • Brand SR, Engel SM, Canfield RL, Yehuda R. 2006. The effect of maternal PTSD following in utero trauma exposure on behavior and temperament in the 9-month-old infant. Ann N Y Acad Sci. 1071:454–458.
  • Brennan PA, Pargas R, Walker EF, Green P, Newport DJ, Stowe Z. 2008. Maternal depression and infant cortisol: Influences of timing, comorbidity and treatment. J Child Psychol Psychiatry. 49:1099–1107.
  • Broekman BF, Chan YH, Chong YS, Quek SC, Fung D, Low YL, Ooi YP, Gluckman PD, Meaney MJ, Wong TY, Saw SM. 2009. The influence of birth size on intelligence in healthy children. Pediatrics. 123:e1011–e1016.
  • Brouwers EPM, van Baar AL, Pop VJM. 2001. Maternal anxiety during pregnancy and subsequent infant development. Inf Behav Dev. 24:95–106.
  • Buss C, Davis EP, Muftuler LT, Head K, Sandman CA. 2009. High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6–9-year-old children. Psychoneuroendocrinology. 35:141–153.
  • Cheung YB. 2002. Early origins and adult correlates of psychosomatic distress. Soc Sci Med. 55:937–948.
  • Clark PM, Hindmarsh PC, Shiell AW, Law CM, Honour JW, Barker DJP. 1996. Size at birth and adrenocortical function in childhood. Clin Endocrinol. 45:721–726.
  • Cornelius MD, Day NL. 2009. Developmental consequences of prenatal tobacco exposure. Curr Opin Neurol. 22:121–125.
  • Dalziel SR, Walker NK, Parag V, Mantell C, Rea HH, Rodgers A, Harding JE. 2005. Cardiovascular risk factors after antenatal exposure to betamethasone: 30-year follow-up of a randomised controlled trial. Lancet. 365:1856–1862.
  • Dave-Sharma S, Wilson RC, Harbison MD, Newfield R, Azar MR, Krozowski ZS, Funder JW, Shackleton CH, Bradlow HL, Wei JQ, Hertecant J, Moran A, Neiberger RE, Balfe JW, Fattah A, Daneman D, Akkurt HI, De Santis C, New MI. 1998. Examination of genotype and phenotype relationships in 14 patients with apparent mineralocorticoid excess. J Clin Endocrinol Metab. 83:2244–2254.
  • Davis EP, Snidman N, Wadhwa PD, Glynn LM, Schetter CD, Sandman CA. 2004. Prenatal maternal anxiety and depression predict negative behavioral reactivity in infancy. Infancy. 6:319–331.
  • Davis EP, Glynn LM, Schetter CD, Hobel C, Chicz-Demet A, Sandman CA. 2007. Prenatal exposure to maternal depression and cortisol influences infant temperament. J Am Acad Child Adolesc Psychiatry. 46:737–746.
  • Dawson G, Ashman SB. 2000. On the origins of a vulnerability to depression: The influence of the early social environment on the development of psychobiological systems related to risk for affective disorder. Mahwah, NJ: Erlbaum.
  • Dawson G, Ashman SB, Hessl D, Spieker S, Frey K, Panagiotides H, Embry L. 2001. Autonomic and brain electrical activity in securely- and insecurely-attached infants of depressed mothers. Inf Behav Dev. 24:135–149.
  • de Bruijn ATCE, van Bakel HJA, van Baar AL. Sex differences in the relation between prenatal maternal emotional complaints and child outcome. Early Hum Dev. 2009a; 85:319–324.
  • de Bruijn ATCE, van Bakel HJA, Wijnen H, Pop VJM, van Baar AL. Prenatal maternal emotional complaints are associated with cortisol responses in toddler and preschool aged girls. Dev Psychobiol. 2009b; 51:553–563.
  • de Vries A, Holmes MC, Heijnis A, Seier JV, Heerden J, Louw J, Wolfe-Coote S, Meaney MJ, Levitt NS, Seckl JR. 2007. Prenatal dexamethasone exposure induces changes in nonhuman primate offspring cardiometabolic and hypothalamic–pituitary–adrenal axis function. J Clin Invest. 117:1058–1067.
  • Diego MA, Field T, Hernandez-Reif M, Cullen C, Schanberg S, Kuhn C. 2004. Prepartum, postpartum, and chronic depression effects on newborns. Psychiatry. 67:63–80.
  • DiPietro JA, Ghera MM, Costigan KA. 2008. Prenatal origins of temperamental reactivity in early infancy. Early Hum Dev. 84:569–575.
  • Doyle LW, Ford GW, Davis NM, Callanan C. 2000. Antenatal corticosteroid therapy and blood pressure at 14 years of age in preterm children. Clin Sci. 98:137–142.
  • Edwards CR, Benediktsson R, Lindsay RS, Seckl JR. 1993. Dysfunction of placental glucocorticoid barrier: Link between fetal environment and adult hypertension?. Lancet. 341:355–357.
  • El Marroun H, Tiemeier H, Steegers EA, Jaddoe VW, Hofman A, Verhulst FC, van den Brink W, Huizink AC. 2009. Intrauterine cannabis exposure affects fetal growth trajectories: The generation R study. J Am Acad Child Adolesc Psychiatry. 48 12: 1173–1181.
  • Entringer S, Kumsta R, Hellhammer DH, Wadhwa PD, Wust S. 2009. Prenatal exposure to maternal psychosocial stress and HPA axis regulation in young adults. Horm Behav. 55:292–298.
  • Eriksson JG, Osmond C, Kajantie E, Forsen TJ, Barker DJ. 2006. Patterns of growth among children who later develop type 2 diabetes or its risk factors. Diabetologia. 49:2853–2858.
  • Eriksson JG, Forsén TJ, Kajantie E, Osmond C, Barker DJ. 2007. Childhood growth and hypertension in later life. Hypertension. 49:1415–1421.
  • Espy KA, Fang H, Johnson C, Stopp C, Wiebe SA, Respass J. 2011. Prenatal tobacco exposure: Developmental outcomes in the neonatal period. Dev Psychol. 47:153–156.
  • Feldt K, Räikkönen K, Eriksson JG, Andersson S, Osmond C, Barker DJ, Phillips DI, Kajantie E. 2007. Cardiovascular reactivity to psychological stressors in late adulthood is predicted by gestational age at birth. J Hum Hypertens. 21:401–410.
  • Field T, Sandberg D, Garcia R, Vega-Lahr N, Goldstein S, Guy L. 1985. Pregnancy problems, postpartum depression, and early mother–infant interactions. Dev Psychol. 21:1152–1156.
  • Fox SE, Levitt P, Nelson CA3rd. 2010. How the timing and quality of early experiences influence the development of brain architecture. Child Dev. 81:28–40.
  • French NP, Hagan R, Evans SF, Godfrey M, Newnham JP. 1999. Repeated antenatal corticosteroids: Size at birth and subsequent development. Am J Obstet Gynecol. 180:114–121.
  • Gale CR, O'Callaghan FJ, Godfrey KM, Law CM, Martyn CN. 2004. Critical periods of brain growth and cognitive function in children. Brain. 127:321–329.
  • Gitau R, Cameron A, Fisk NM, Glover V. 1998. Fetal exposure to maternal cortisol. Lancet. 352:707–708.
  • Glover V, Bergman K, Sarkar P, O'Connor TG. 2009. Association between maternal and amniotic fluid cortisol is moderated by maternal anxiety. Psychoneuroendocrinology. 34:430–435.
  • Glover V, O'Connor TG, O'Donnell K. 2010. Prenatal stress and the programming of the HPA axis. Neurosci Biobehav Rev. 35:17–22.
  • Gluckman PD, Hanson MA, Pinal C. 2005. The developmental origins of adult disease. Matern Child Nutr. 1:130–141.
  • Gluckman PD, Hanson MA, Cooper C, Thornburg KL. 2008. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 359:61–73.
  • Gluckman PD, Hanson MA, Bateson P, Beedle AS, Law CM, Bhutta ZA, Bhutta ZA, Anokhin KV, Bougnères P, Chandak GR, Dasgupta P, Smith GD, Ellison PT, Forrester TE, Gilbert SF, Jablonka E, Kaplan H, Prentice AM, Simpson SJ, Uauy R, West-Eberhard MJ. 2009. Towards a new developmental synthesis: Adaptive developmental plasticity and human disease. Lancet. 373:1654–1657.
  • Grant KA, McMahon C, Austin MP, Reilly N, Leader L, Ali S. 2009. Maternal prenatal anxiety, postnatal caregiving and infants' cortisol responses to the still-face procedure. Dev Psychobiol. 51:625–637.
  • Gunnell D, Rasmussen F, Fouskakis D, Tynelius P, Harrison G. 2003. Patterns of fetal and childhood growth and the development of psychosis in young males: A cohort study. Am J Epidemiol. 158:291–300.
  • Gutteling BM, de Weerth C, Buitelaar JK. 2004. Maternal prenatal stress and 4–6 year old children's salivary cortisol concentrations pre- and post-vaccination. Stress. 7:257–260.
  • Gutteling BM, de Weerth C, Buitelaar JK. 2005. Prenatal stress and children's cortisol reaction to the first day of school. Psychoneuroendocrinology. 30:541–549.
  • Gutteling BM, de Weerth C, Willemsen-Swinkels SH, Huizink AC, Mulder EJ, Visser GH, Buitelaar JK. The effects of prenatal stress on temperament and problem behavior of 27-month-old toddlers. Eur Child Adolesc Psychiatry. 2005b; 14:41–51.
  • Gutteling BM, de Weerth C, Zandbelt N, Mulder EJ, Visser GH, Buitelaar JK. 2006. Does maternal prenatal stress adversely affect the child's learning and memory at age six?. J Abnorm Child Psychol. 34:789–798.
  • Hanson MA, Gluckman PD. 2008. Developmental origins of health and disease: New insights. Basic Clin Pharmacol Toxicol. 102:90–93.
  • Harvison KW, Molfese DL, Woodruff-Borden J, Weigel RA. 2009. Neonatal auditory evoked responses are related to perinatal maternal anxiety. Brain Cogn. 71:369–374.
  • Heinonen K, Räikkönen K, Pesonen AK, Kajantie E, Andersson S, Eriksson JG, Niemelä A, Vartia T, Peltola J, Lano A. 2008. Prenatal and postnatal growth and cognitive abilities at 56 months of age: A longitudinal study of infants born at term. Pediatrics. 121:e1325–e1333.
  • Heinonen K, Räikkönen K, Pesonen AK, Andersson S, Kajantie E, Eriksson JG, Wolke D, Lano A. 2010. Behavioural symptoms of attention deficit/hyperactivity disorder in preterm and term children born small and appropriate for gestational age: A longitudinal study. BMC Pediatr. 15:10–91.
  • Heinonen K, Räikkönen K, Pesonen AK, Andersson S, Kajantie E, Eriksson JG, Wolke D, Lano A. 2011. Longitudinal study of smoking cessation before pregnancy and children's cognitive abilities at 56 months of age. Early Hum Dev. 87 5: 353–359.
  • Hellemans KG, Sliwowska JH, Verma P, Weinberg J. 2010. Prenatal alcohol exposure: Fetal programming and later life vulnerability to stress, depression and anxiety disorders. Neurosci Biobehav Rev. 34:791–807.
  • Henrichs J, Schenk JJ, Schimdt HG, Velders FP, Hofman A, Jaddoe VWV, Verhulst FC, Tiemeier H. 2009. Maternal pre- and postnatal anxiety and infant temperament. The generation R study. Inf Child Dev. 18:556–572.
  • Hernandez-Martinez C, Arija V, Balaguer A, Cavalle P, Canals J. 2008. Do the emotional states of pregnant women affect neonatal behaviour?. Early Hum Dev. 84:745–750.
  • Hernandez-Reif M, Field T, Diego M, Ruddock M. 2006. Greater arousal and less attentiveness to face/voice stimuli by neonates of depressed mothers on the Brazelton Neonatal Behavioral Assessment Scale. Inf Child Dev. 29:594–598.
  • Holmes MC, Abrahamsen CT, French KL, Paterson JM, Mullins JJ, Seckl JR. 2006. The mother or the fetus? 11beta-hydroxysteroid dehydrogenase type 2 null mice provide evidence for direct fetal programming of behavior by endogenous glucocorticoids. J Neurosci. 26:3840–3844.
  • Huizink AC, de Medina PG, Mulder EJ, Visser GH, Buitelaar JK. 2002. Psychological measures of prenatal stress as predictors of infant temperament. J Am Acad Child Adolesc Psychiatry. 41:1078–1085.
  • Huizink AC, Robles de Medina P, Mulder EJ, Visser GH, Buitelaar JK. 2003. Stress during pregnancy is associated with developmental outcome in infancy. J Child Psychol Psychiatry. 44:810–818.
  • Huizink AC, Bartels M, Rose RJ, Pulkkinen L, Eriksson CJ, Kaprio J. 2008. Chernobyl exposure as stressor during pregnancy and hormone levels in adolescent offspring. J Epidemiol Community Health. 62:e5.
  • IJzerman R, Stehouwer CD, de Geus EJ, van Weissenbruch MM, Delemarre-van de Waal HA, Boomsma DI. 2003. Low birth weight is associated with increased sympathetic activity: Dependence on genetic factors. Circulation. 108:566–571.
  • Isbrucker RA, Burdock GA. 2006. Risk and safety assessment on the consumption of Licorice root (Glycyrrhiza sp.), its extract and powder as a food ingredient, with emphasis on the pharmacology and toxicology of glycyrrhizin. Regul Toxicol Pharmacol. 46:167–192.
  • Jones A, Godfrey KM, Wood P, Osmond C, Goulden P, Phillips DI. 2006. Fetal growth and the adrenocortical response to psychological stress. J Clin Endocrinol Metab. 91:1868–1871.
  • Jones A, Beda A, Ward AM, Osmond C, Phillips DI, Moore VM, Simpson DM. 2007. Size at birth and autonomic function during psychological stress. Hypertension. 49:548–555.
  • Kajantie E. 2008. Early-life events. Effects on aging. Hormones (Athens). 7:101–113.
  • Kajantie E, Räikkönen K. 2010. Early life predictors of the physiological stress response later in life. Neurosci Biobehav Rev. 35:23–32.
  • Kajantie E, Feldt K, Räikkönen K, Phillips DI, Osmond C, Heinonen K, Pesonen AK, Andersson S, Barker DJ, Eriksson JG. 2007. Body size at birth predicts hypothalamic–pituitary–adrenal axis response to psychosocial stress at age 60 to 70 years. J Clin Endocrinol Metab. 92:4094–4100.
  • Khashan AS, Abel KM, McNamee R, Pedersen MG, Webb RT, Baker PN, Kenny LC, Mortensen PB. Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Arch Gen Psychiatry. 2008a; 65:146–152.
  • Khashan AS, McNamee R, Abel KM, Pedersen MG, Webb RT, Kenny LC, Mortensen PB, Baker PN. Reduced infant birthweight consequent upon maternal exposure to severe life events. Psychosom Med. 2008b; 70:688–694.
  • Kinney DK, Miller AM, Crowley DJ, Huang E, Gerber E. 2008. Autism prevalence following prenatal exposure to hurricanes and tropical storms in Louisiana. J Autism Dev Disord. 38:481–488.
  • Knorr U, Vinberg M, Kessing LV, Wetterslev J. 2010. Salivary cortisol in depressed patients versus control persons: A systematic review and meta-analysis. Psychoneuroendocrinology. 35:1275–1286.
  • Lahti J, Räikkönen K, Kajantie E, Heinonen K, Pesonen AK, Järvenpää AL, Strandberg T. 2006. Small body size at birth and behavioural symptoms of ADHD in children aged five to six years. J Child Psychol Psychiatry. 47:1167–1174.
  • Lahti J, Räikkönen K, Sovio U, Miettunen J, Hartikainen AL, Pouta A, Taanila A, Joukamaa M, Järvelin MR, Veijola J. 2009. Early-life origins of schizotypal traits in adulthood. Br J Psychiatry. 195:132–137.
  • Lahti J, Räikkönen K, Pesonen AK, Heinonen K, Kajantie E, Forsén T, Osmond C, Barker DJ, Eriksson JG. Prenatal growth, postnatal growth, and trait anxiety in late adulthood—the Helsinki Birth Cohort Study. Acta Psychiatr Scand. 2010a; 121:227–235.
  • Lahti M, Räikkönen K, Wahlbeck K, Heinonen K, Forsen T, Kajantie E, Pesonen AK, Osmond C, Barker DJ, Eriksson JG. Prenatal origins of hospitalization for personality disorders: The Helsinki birth cohort study. Psychiatry Res. 2010b; 179:226–230.
  • Langley-Evans SC, Phillips GJ, Benediktsson R, Gardner DS, Edwards CR, Jackson AA, Seckl JR. 1996. Protein intake in pregnancy, placental glucocorticoid metabolism and the programming of hypertension in the rat. Placenta. 17:169–172.
  • Laplante DP, Barr RG, Brunet A, Galbaud du Fort G, Meaney ML, Saucier JF, Zelazo PR, King S. 2004. Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatr Res. 56:400–410.
  • Laplante DP, Brunet A, Schmitz N, Ciampi A, King S. 2008. Project Ice Storm: Prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2-year-old children. J Am Acad Child Adolesc Psychiatry. 47:1063–1072.
  • Levitt NS, Lambert EV, Woods D, Hales CN, Andrew R, Seckl JR. 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. 85:4611–4618.
  • Li J, Vestergaard M, Obel C, Christensen J, Precht DH, Lu M, Olsen J. A nationwide study on the risk of autism after prenatal stress exposure to maternal bereavement. Pediatrics. 2009a; 123:1102–1107.
  • Li J, Vestergaard M, Obel C, Precht DH, Christensen J, Lu M, Olsen J. Prenatal stress and cerebral palsy: A nationwide cohort study in Denmark. Psychosom Med. 2009b; 71:615–618.
  • Lindsay RS, Lindsay RM, Edwards CR, Seckl JR. Inhibition of 11-beta-hydroxysteroid dehydrogenase in pregnant rats and the programming of blood pressure in the offspring. Hypertension. 1996a; 27:1200–1204.
  • Lindsay RS, Lindsay RM, Waddell BJ, Seckl JR. Prenatal glucocorticoid exposure leads to offspring hyperglycaemia in the rat: Studies with the 11 beta-hydroxysteroid dehydrogenase inhibitor carbenoxolone. Diabetologia. 1996b; 39:1299–1305.
  • Lou HC, Hansen D, Nordentoft M, Pryds O, Jensen F, Nim J, Hemmingsen R. 1994. Prenatal stressors of human life affect fetal brain development. Dev Med Child Neurol. 36:826–832.
  • Lucassen PJ, Bosch OJ, Jousma E, Kromer SA, Andrew R, Seckl JR, Neumann ID. 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.
  • MacArthur BA, Howie RN, Dezoete JA, Elkins J. 1982. School progress and cognitive development of 6-year-old children whose mothers were treated antenatally with betamethasone. Pediatrics. 70:99–105.
  • Mairesse J, Lesage J, Breton C, Breant B, Hahn T, Darnaudery M, Dickson SL, 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 Endocrinol Metab. 292:E1526–E1533.
  • Martin RP, Noyes J, Wisenbaker J, Huttunen M. 1999. Prediction of early childhood negative emotionality and inhibition from maternal distress during pregnancy. Merrill-Palmer Q. 45:370–391.
  • McGrath JM, Records K, Rice M. 2008. Maternal depression and infant temperament characteristics. Infant Behav Dev. 31:71–80.
  • Meaney MJ. 2010. Epigenetics and the biological definition of gene × environment interactions. Child Dev. 81:41–79.
  • Mennes M. 2008. Longitudinal study on the effects of maternal anxiety during pregnancy: Neuropsychological and neurophysiological examination of cognitive control in the adolescent offspring. Leuven: Katholieke Universiteit Leuven.
  • Mennes M, Stiers P, Lagae L, Van den Bergh BR. 2006. Long-term cognitive sequelae of antenatal maternal anxiety: Involvement of the orbitofrontal cortex. Neurosci Biobehav Rev. 30:1078–1086.
  • Mennes M, Van den Bergh BR, Lagae L, Stiers P. 2009. Developmental brain alterations in 17 year old boys are related to antenatal maternal anxiety. Clin Neurophysiol. 120:1116–1122.
  • Niederhofer H, Reiter A. 2004. Prenatal maternal stress, prenatal fetal movements and perinatal temperament factors influence behavior and school marks at the age of 6 years. Fetal Diagn Ther. 19:160–162.
  • Obel C. 2003. Epidemiological studies of stress during pregnancy and fetal brain development. Denmark: University of Aarhus.
  • Oberlander TF, Weinberg J, Papsdorf M, Grunau R, Misri S, Devlin AM. 2008. Prenatal exposure to maternal depression, neonatal methylation of human glucocorticoid receptor gene (NR3C1) and infant cortisol stress responses. Epigenetics. 3:97–106.
  • O'Connor TG, Heron J, Golding J, Beveridge M, Glover V. 2002. Maternal antenatal anxiety and children's behavioural/emotional problems at 4 years. Report from the Avon Longitudinal Study of Parents and Children. Br J Psychiatry. 180:502–508.
  • O'Connor TG, Heron J, Golding J, Glover V. 2003. Maternal antenatal anxiety and behavioural/emotional problems in children: A test of a programming hypothesis. J Child Psychol Psychiatry. 44:1025–1036.
  • O'Connor TG, 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.
  • O'Keane V, Lightman S, Marsh M, Pawlby S, Papadopoulos AS, Taylor A, Moore R, Patrick K. 2011. Increased pituitary–adrenal activation and shortened gestation in a sample of depressed pregnant women: A pilot study. J Affect Disord. 130:300–305.
  • O'Regan D, Welberg LL, Holmes MC, Seckl JR. 2001. Glucocorticoid programming of pituitary–adrenal function: Mechanisms and physiological consequences. Semin Neonatol. 6:319–329.
  • Pesonen AK, Räikkönen K, Strandberg TE, Järvenpää AL. 2005. Continuity of maternal stress from the pre- to the postnatal period: Associations with infant's positive, negative and overall temperamental reactivity. Inf Behav Devel. 28:36–47.
  • Pesonen AK, Räikkönen K, Kajantie E, Heinonen K, Strandberg TE, Järvenpää AL. 2006. Fetal programming of temperamental negative affectivity among children born healthy at term. Dev Psychobiol. 48:633–643.
  • Pesonen AK, Räikkönen K, Heinonen K, Kajantie E, Forsen T, Eriksson JG. 2007. Depressive symptoms in adults separated from their parents as children: A natural experiment during World War II. Am J Epidemiol. 166:1126–1133.
  • Pesonen AK, Räikkönen K, Heinonen K, Andersson S, Hovi P, Järvenpää AL, Eriksson JG, Kajantie E. Personality of young adults born prematurely: The Helsinki study of very low birth weight adults. J Child Psychol Psychiatry. 2008a; 49:609–617.
  • Pesonen AK, Räikkönen K, Heinonen K, Kajantie E, Forsen T, Eriksson JG. Reproductive traits following a parent-child separation trauma during childhood: A natural experiment during World War II. Am J Hum Biol. 2008b; 20:345–351.
  • Pesonen AK, Räikkönen K, Matthews K, Heinonen K, Paavonen JE, Lahti J, Komsi N, Lemola S, Järvenpää AL, Kajantie E, Strandberg T. 2009. Prenatal origins of poor sleep in children. Sleep. 32:1086–1092.
  • Pesonen AK, Räikkönen K, Feldt K, Heinonen K, Osmond C, Phillips DI, Barker DJ, Eriksson JG, Kajantie E. 2010. Childhood separation experience predicts HPA axis hormonal responses in late adulthood: A natural experiment of World War II. Psychoneuroendocrinology. 35:758–767.
  • Pesonen AK, Räikkönen K, Kajantie E, Heinonen K, Osmond C, Barker DJ, Forsén T, Eriksson JG. 2011. Intergenerational social mobility following early life stress. Ann Med. 43 4: 320–328.
  • Phillips DI, Jones A. 2006. Fetal programming of autonomic and HPA function: Do people who were small babies have enhanced stress responses?. J Physiol. 572:45–50.
  • Phillips DI, Fall CHD, Whorwood CB, Seckl JR, Wood PJ, Barker DJP, . 1998. Elevated plasma cortisol concentrations: A link between low birth weight and the insulin resistance syndrome?. J Clin Endocrinol Metab. 83:757–760.
  • Phillips DI, Walker BR, Reynolds RM, Flanagan DE, Wood PJ, Osmond C, Barker DJ, Whorwood CB. 2000. Low birth weight predicts elevated plasma cortisol concentrations in adults from 3 populations. Hypertension. 35:1301–1306.
  • Ponirakis A, Susman EJ, Stifter CA. 1998. Negative emotionality and cortisol during adolescent pregnancy and its effects on infant health and autonomic nervous system reactivity. Dev Psychobiol. 33:163–174.
  • Räikkönen K, Pesonen AK. 2009. Early life origins of psychological development and mental health. Scand J Psychol. 50:583–591.
  • Räikkönen K, Pesonen AK, Kajantie E, Heinonen K, Forsen T, Phillips DI, Osmond C, Barker DJ, Eriksson JG. 2007. Length of gestation and depressive symptoms at age 60 years. Br J Psychiatry. 190:469–474.
  • Räikkönen K, Pesonen A-K, Heinonen K, Lahti J, Kajantie E, Forsen T, Osmond C, Barker DJ, Eriksson JG. Infant growth and hostility in adult life. Psychosom Med. 2008a; 70:306–313.
  • Räikkönen K, Pesonen AK, Heinonen K, Kajantie E, Hovi P, Järvenpää AL, Eriksson JG, Andersson S. Depression in young adults with very low birth weight: The Helsinki study of very low-birth-weight adults. Arch Gen Psychiatry. 2008b; 65:290–296.
  • Räikkönen K, Forsén T, Henriksson M, Kajantie E, Laaksonen I, Leskinen JT, Laaksonen I, Osmond C, Barker DJ, Eriksson JG. Growth trajectories and intellectual abilities in young adulthood: The Helsinki Birth Cohort Study. Am J Epidemiol. 2009a; 15:447–455.
  • Räikkönen K, Pesonen AK, Heinonen K, Lahti J, Komsi N, Eriksson JG, Seckl JR, Järvenpää AL, Strandberg TE. Maternal licorice consumption and detrimental cognitive and psychiatric outcomes in children. Am J Epidemiol. 2009b; 170:1137–1146.
  • Räikkönen K, Lahti M, Heinonen K, Pesonen AK, Wahlbeck K, Kajantie E, Osmond C, Barker DJP, Eriksson JG. 2011. Risk of severe mental disorders in adults separated temporarily from their parents in childhood: The Helsinki birth cohort study. J Psychiatr Res. 45:332–338.
  • Räikkönen K, Matthews KA, Pesonen AK, Pyhälä R, Paavonen EJ, Feldt K, Jones A, Phillips DI, Seckl JR, Heinonen K, Lahti J, Komsi N, Järvenpää AL, Eriksson JG, Strandberg TE, Kajantie E. Poor sleep and altered hypothalamic–pituitary–adrenocortical and sympatho–adrenal–medullary system activity in children. J Clin Endocrinol Metab. 2010b; 95:2254–2261.
  • Räikkönen K, Seckl JR, Heinonen K, Pyhälä R, Feldt K, Jones A, Pesonen AK, Phillips DI, Lahti J, Järvenpää AL, Eriksson JG, Matthews KA, Strandberg TE, Kajantie E. Maternal prenatal licorice consumption alters hypothalamic–pituitary–adrenocortical axis function in children. Psychoneuroendocrinology. 2010c; 35:1587–1593.
  • Reynolds RM, Walker BR, Syddall HE, Andrew R, Wood PJ, Whorwood CB, Phillips DI. 2001. Altered control of cortisol secretion in adult men with low birth weight and cardiovascular risk factors. J Clin Endocrinol Metab. 86:245–250.
  • Reynolds RM, Godfrey KM, Barker M, Osmond C, Phillips DI. 2007. Stress responsiveness in adult life: Influence of mother's diet in late pregnancy. J Clin Endocrinol Metab. 92:2208–2210.
  • Rieger M, Pirke KM, Buske-Kirschbaum A, Wurmser H, Papousek M, Hellhammer DH. 2004. Influence of stress during pregnancy on HPA activity and neonatal behavior. Ann N Y Acad Sci. 1032:228–230.
  • Rodriguez A. 2010. Maternal pre-pregnancy obesity and risk for inattention and negative emotionality in children. J Child Psychol Psychiatry. 51:134–143.
  • Rodriguez A, Bohlin G. 2005. Are maternal smoking and stress during pregnancy related to ADHD symptoms in children?. J Child Psychol Psychiatry. 46:246–254.
  • Roelofs K, van Peer J, Berretty E, Jong P, Spinhoven P, Elzinga BM. 2009. Hypothalamus–pituitary–adrenal axis hyperresponsiveness is associated with increased social avoidance behavior in social phobia. Biol Psychiatry. 65:336–343.
  • Rogerson FM, Kayes KM, White PC. 1997. Variation in placental type 2 11beta-hydroxysteroid dehydrogenase activity is not related to birth weight or placental weight. Mol Cell Endocrinol. 128:103–109.
  • Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP. 2001. Effects of prenatal exposure to the Dutch famine on adult disease in later life: An overview. Mol Cell Endocrinol. 185:93–98.
  • Sarkar P, Bergman K, O'Connor TG, Glover V. 2008. Maternal antenatal anxiety and amniotic fluid cortisol and testosterone: Possible implications for foetal programming. J Neuroendocrinol. 20:489–496.
  • Schlotz W, Jones A, Godfrey KM, Phillips DI. 2008. Effortful control mediates associations of fetal growth with hyperactivity and behavioural problems in 7- to 9-year-old children. J Child Psychol Psychiatry. 49:1228–1236.
  • Schmidt LA, Miskovic V, Boyle MH, Saigal S. 2008. Shyness and timidity in young adults who were born at extremely low birth weight. Pediatrics. 122:e181–e187.
  • Seckl JR. 2001. Glucocorticoid programming of the fetus; adult phenotypes and molecular mechanisms. Mol Cell Endocrinol. 185:61–71.
  • Seckl JR. 2008. Glucocorticoids, developmental “programming” and the risk of affective dysfunction. Prog Brain Res. 167:17–34.
  • Seckl JR, Meaney MJGlucocorticoid programmingBiobehavioral stress response: Protective and damaging effects. New York: Annals of the New York Academy of Sciences2004a63–84 Vol. 1032.
  • Seckl JR, Meaney MJ. Glucocorticoid programming. Ann N Y Acad Sci. 2004b; 1032:63–84.
  • Seckl JR, Meaney MJ. 2006. Glucocorticoid “programming” and PTSD risk. Ann N Y Acad Sci. 1071:351–378.
  • Seckl JR, Holmes MC. 2007. Mechanisms of disease: Glucocorticoids, their placental metabolism and fetal “programming” of adult pathophysiology. Nat Clin Pract Endocrinol Metab. 3:479–488.
  • Shenkin SD, Starr JM, Deary IJ. 2004. Birth weight and cognitive ability in childhood: A systematic review. Psychol Bull. 130:989–1013.
  • Sloboda DM, Challis JR, Moss TJ, Newnham JP. 2005. Synthetic glucocorticoids: Antenatal administration and long-term implications. Curr Pharm Des. 11:1459–1472.
  • Speirs HJ, Seckl JR, Brown RW. 2004. Ontogeny of glucocorticoid receptor and 11beta-hydroxysteroid dehydrogenase type-1 gene expression identifies potential critical periods of glucocorticoid susceptibility during development. J Endocrinol. 181:105–116.
  • Stewart PM, Whorwood CB, Mason JI. 1995. Type 2 11 beta-hydroxysteroid dehydrogenase in foetal and adult life. J Steroid Biochem Mol Biol. 55:465–471.
  • Strandberg TE, Järvenpää AL, Vanhanen H, McKeigue PM. 2001. Birth outcome in relation to licorice consumption during pregnancy. Am J Epidemiol. 153:1085–1088.
  • Strandberg TE, Andersson S, Järvenpää AL, McKeigue PM. 2002. Preterm birth and licorice consumption during pregnancy. Am J Epidemiol. 156:803–805.
  • Strang-Karlsson S, Räikkönen K, Kajantie E, Andersson S, Hovi P, Heinonen K, Pesonen AK, Järvenpää AL, Eriksson JG, Paavonen EJ. Sleep quality in young adults with very low birth weight—the Helsinki study of very low birth weight adults. J Pediatr Psychol. 2008a; 33:387–395.
  • Strang-Karlsson S, Räikkönen K, Pesonen AK, Kajantie E, Paavonen EJ, Lahti J, Hovi P, Heinonen K, Järvenpää AL, Eriksson JG, Andersson S. Very low birth weight and behavioral symptoms of attention deficit hyperactivity disorder in young adulthood: The Helsinki study of very-low-birth-weight adults. Am J Psychiatry. 2008b; 165:1345–1353.
  • Trautman PD, Meyer-Bahlburg HFL, Postelnek J, New MI. 1995. Effects of early prenatal dexamethasone on the cognitive and behavioral development of young children: Results of a pilot study. Psychoneuroendocrinology. 20:439–449.
  • Tuovinen S, Räikkönen K, Kajantie E, Pesonen AK, Heinonen K, Osmond C, Barker DJ, Eriksson JG. 2010. Depressive symptoms in adulthood and intrauterine exposure to pre-eclampsia: The Helsinki Birth Cohort Study. Br J Obstet Gynaecol. 117:1236–1242.
  • Tuovinen SH, Räikkönen K, Kajantie E, Lehtinen J, Henriksson M, Pesonen AK, Heinonen K, Osmond C, Barker D, Eriksson JG. Hypertensive disorders in pregnancy and intellectual abilities in the offspring in young adulthood: The Helsinki birth cohort study. Ann Med. 2011 Apr 15. [Epub ahead of print].
  • Van den Bergh BR. 1990. The influence of maternal emotions during pregnancy on fetal and neonatal behavior, Win, 1990. J Prenatal Perinatal Psychol Health. 5:119–130.
  • Van den Bergh BR. 1992. Maternal emotions during pregnancy and fetal and neonatal behavior. Oxford University Press: Oxford, UK.
  • Van den Bergh BR, Marcoen A. 2004. High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8- and 9-year-olds. Child Dev. 75:1085–1097.
  • Van den Bergh BR, Mennes M, Oosterlaan J, Stevens V, Stiers P, Marcoen A, Lagae L. High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds. Neurosci Biobehav Rev. 2005a; 29:259–269.
  • Van den Bergh BR, Mulder EJ, Mennes M, Glover V. Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: Links and possible mechanisms. A review. Neurosci Biobehav Rev. 2005b; 29:237–258.
  • Van den Bergh BR, 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.
  • van der Wal MF, van Eijsden M, Bonsel GJ. 2007. Stress and emotional problems during pregnancy and excessive infant crying. J Dev Behav Pediatr. 28:431–437.
  • Van den Bergh BR, Van Calster B, Smits T, Van Huffel S, Lagae L. 2008. Antenatal maternal anxiety is related to HPA-axis dysregulation and self-reported depressive symptoms in adolescence: A prospective study on the fetal origins of depressed mood. Neuropsychopharmacology. 33:536–545.
  • Vaughn B, Bradley C, Joffe L, Seifer R, Barglow P. 1987. Maternal characteristics measured prenatally are predictive of ratings of temperamental “difficulty” on the Carey Infant Temperament Questionnaire. Dev Psychol. 23:152–161.
  • Wahlbeck K, Forsen T, Osmond C, Barker DJ, Eriksson JG. 2001. Association of schizophrenia with low maternal body mass index, small size at birth, and thinness during childhood. Arch Gen Psychiatry. 58:48–52.
  • Warner MJ, Ozanne SE. Mechanisms involved in the developmental programming of adulthood disease. Biochem J. 2010427.
  • Welberg LA, Seckl JR, Holmes MC. 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.
  • Wisborg K, Barklin A, Hedegaard M, Henriksen TB. 2008. Psychological stress during pregnancy and stillbirth: Prospective study. BJOG: Int J Obstet Gynaecol. 115:882–885.
  • Wust S, Entringer S, Federenko IS, Schlotz W, Hellhammer DH. 2005. Birth weight is associated with salivary cortisol responses to psychosocial stress in adult life. Psychoneuroendocrinology. 30:591–598.
  • Yeh TF, Lin YJ, Lin HC, Huang CC, Hsieh WS, Lin CH, Tsai CH. 2004. Outcomes at school age after postnatal dexamethasone therapy for lung disease of prematurity. N Engl J Med. 350:1304–1313.
  • Yehuda R, Engel SM, Brand SR, Seckl J, Marcus SM, Berkowitz GS. 2005. Transgenerational effects of posttraumatic stress disorder in babies of mothers exposed to the World Trade Center attacks during pregnancy. J Clin Endocrinol Metab. 90:4115–4118.

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