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Published in: Social Psychiatry and Psychiatric Epidemiology 3/2012

01-03-2012 | Original Paper

Impact of fetal versus perinatal hypoxia on sex differences in childhood outcomes: developmental timing matters

Authors: Michael Anastario, Carolyn M. Salafia, Garrett Fitzmaurice, Jill M. Goldstein

Published in: Social Psychiatry and Psychiatric Epidemiology | Issue 3/2012

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Abstract

Purpose

To examine how the timing of hypoxic exposure results in specific childhood outcomes and whether there is a differential effect by sex.

Methods

A sample of 10,879 prospectively followed pregnancies was drawn from the Boston and Providence sites (New England, NE) of the National Collaborative Perinatal Project. Based on placental pathology, we developed and validated a measure of probable chronic placental hypoxia (CHP) and contrasted the effects of acute perinatal hypoxia on age 7 emotional, behavioral, and cognitive outcomes.

Results

Perinatal hypoxia had a significant impact on multiple behavioral and cognitive outcomes in boys and girls by age 7, in contrast to probable CHP which had a differential effect on girls and boys such that there was decreased verbal IQ and increased inhibition in females alone.

Conclusions

Findings underscore the importance of considering the timing of obstetric complications and offspring sex in investigations of the impact of fetal and perinatal hypoxia on offspring’s outcomes throughout the life course.
Literature
1.
go back to reference Cannon TD, Yolken R, Buka S, Torrey EF, Goldstein JM, Seidman LJ, Tsuang M, Hadley T, Bearden CE, Rossso J, Dhavale D (2008) Decreased neurotrophic response to birth hypoxia in the etiology of schizophrenia. Biol Psychiatry 64:797–802PubMedCrossRef Cannon TD, Yolken R, Buka S, Torrey EF, Goldstein JM, Seidman LJ, Tsuang M, Hadley T, Bearden CE, Rossso J, Dhavale D (2008) Decreased neurotrophic response to birth hypoxia in the etiology of schizophrenia. Biol Psychiatry 64:797–802PubMedCrossRef
2.
go back to reference Mallen C, Mottram S, Thomas E (2008) Birth factors and common mental health problems in young adults: a population-based study in North Staffordshire. Soc Psychiatry Psychiatr Epidemiol 43:325–330PubMedCrossRef Mallen C, Mottram S, Thomas E (2008) Birth factors and common mental health problems in young adults: a population-based study in North Staffordshire. Soc Psychiatry Psychiatr Epidemiol 43:325–330PubMedCrossRef
3.
go back to reference Cannon TD, van Erp TG, Rosso IM, Huttunen MO, Lonnqvist J, Pirkola T, Salonen O, Valanne L, Poutanen V-P, Standertskjold-Nordenstam CG (2002) Fetal hypoxia and structural brain abnormalities in schizophrenic patients, their siblings, and controls. Arch Gen Psychiatry 59:35–41PubMedCrossRef Cannon TD, van Erp TG, Rosso IM, Huttunen MO, Lonnqvist J, Pirkola T, Salonen O, Valanne L, Poutanen V-P, Standertskjold-Nordenstam CG (2002) Fetal hypoxia and structural brain abnormalities in schizophrenic patients, their siblings, and controls. Arch Gen Psychiatry 59:35–41PubMedCrossRef
4.
go back to reference Buka SL, Lipsitt LP, Tsuang MT (1993) Pregnancy/delivery complications and psychiatric diagnosis: a prospective study. Arch Gen Psychiatry 50:151–156PubMedCrossRef Buka SL, Lipsitt LP, Tsuang MT (1993) Pregnancy/delivery complications and psychiatric diagnosis: a prospective study. Arch Gen Psychiatry 50:151–156PubMedCrossRef
5.
go back to reference Zornberg GL, Buka SL, Tsuang MT (2000) Hypoxic-ischemia-related fetal/neonatal complications and risk of schizophrenia and other nonaffective psychoses: a 19-year longitudinal study. Am J Psychiatry 157:196–202PubMedCrossRef Zornberg GL, Buka SL, Tsuang MT (2000) Hypoxic-ischemia-related fetal/neonatal complications and risk of schizophrenia and other nonaffective psychoses: a 19-year longitudinal study. Am J Psychiatry 157:196–202PubMedCrossRef
6.
go back to reference Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, Schutz G (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23:99–103PubMedCrossRef Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, Schutz G (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23:99–103PubMedCrossRef
7.
go back to reference van Os J, Jones P, Lewis G, Wadsworth M, Murray R (1997) Developmental precursors of affective illness in a general population birth cohort. Arch Gen Psychiatry 54:625–631PubMedCrossRef van Os J, Jones P, Lewis G, Wadsworth M, Murray R (1997) Developmental precursors of affective illness in a general population birth cohort. Arch Gen Psychiatry 54:625–631PubMedCrossRef
8.
go back to reference Goldstein JM, Walder DJ (2002) Sex differences in schizophrenia: the case for developmental origins and etiological implications. In: Sharma T, Harvey P (eds) The early course of schizophrenia. Oxford University Press, UK Goldstein JM, Walder DJ (2002) Sex differences in schizophrenia: the case for developmental origins and etiological implications. In: Sharma T, Harvey P (eds) The early course of schizophrenia. Oxford University Press, UK
9.
go back to reference Brown AS, Susser ES, Lin SP, Neugebauer R, Gorman JM (1995) Increased risk of affective disorders in males after second trimester prenatal exposure to the Dutch Hunger Winter of 1944–45. Br J Psychiatry 166:601–606PubMedCrossRef Brown AS, Susser ES, Lin SP, Neugebauer R, Gorman JM (1995) Increased risk of affective disorders in males after second trimester prenatal exposure to the Dutch Hunger Winter of 1944–45. Br J Psychiatry 166:601–606PubMedCrossRef
10.
go back to reference Brown AS, van Os J, Driessens C, Hoek HW, Susser ES (2000) Further evidence of relation between prenatal famine and major affective disorder. Am J Psychiatry 157:190–195PubMedCrossRef Brown AS, van Os J, Driessens C, Hoek HW, Susser ES (2000) Further evidence of relation between prenatal famine and major affective disorder. Am J Psychiatry 157:190–195PubMedCrossRef
11.
go back to reference Machon RA, Mednick SA, Huttunen MO (1997) Adult major affective disorder after prenatal exposure to an influenza epidemic. Arch Gen Psychiatry 54:322–328PubMedCrossRef Machon RA, Mednick SA, Huttunen MO (1997) Adult major affective disorder after prenatal exposure to an influenza epidemic. Arch Gen Psychiatry 54:322–328PubMedCrossRef
12.
go back to reference Watson JB, Mednick SA, Huttunen M, Wang X (1999) Prenatal teratogens and the development of adult mental illness. Dev Psychopathol 11:457–466PubMedCrossRef Watson JB, Mednick SA, Huttunen M, Wang X (1999) Prenatal teratogens and the development of adult mental illness. Dev Psychopathol 11:457–466PubMedCrossRef
13.
go back to reference Jones PB, Tarrant CJ (1999) Specificity of developmental precursors to schizophrenia and affective disorders. Schizophr Res 39:121–126PubMedCrossRef Jones PB, Tarrant CJ (1999) Specificity of developmental precursors to schizophrenia and affective disorders. Schizophr Res 39:121–126PubMedCrossRef
14.
go back to reference Brown AS, Susser ES, Lin SP, Gorman JM (1995) Affective disorders in Holland after prenatal exposure to the 1957 A2 influenza epidemic. Biol Psychiatry 38:270–273PubMedCrossRef Brown AS, Susser ES, Lin SP, Gorman JM (1995) Affective disorders in Holland after prenatal exposure to the 1957 A2 influenza epidemic. Biol Psychiatry 38:270–273PubMedCrossRef
15.
go back to reference Thompson C, Syddall H, Rodin I, Osmond C, Barker DJ (2001) Birth weight and the risk of depressive disorder in late life. Br J Psychiatry 179:450–455PubMedCrossRef Thompson C, Syddall H, Rodin I, Osmond C, Barker DJ (2001) Birth weight and the risk of depressive disorder in late life. Br J Psychiatry 179:450–455PubMedCrossRef
16.
go back to reference Ley D, Tideman E, Laurin J, Bjerre I, Marsal K (1996) Abnormal fetal aortic velocity waveform and intellectual function at 7 years of age. Ultrasound Obstetr Gynecol 8:160–165CrossRef Ley D, Tideman E, Laurin J, Bjerre I, Marsal K (1996) Abnormal fetal aortic velocity waveform and intellectual function at 7 years of age. Ultrasound Obstetr Gynecol 8:160–165CrossRef
17.
go back to reference Wienerroither H, Steiner H, Tomaselli J, Lobendanz M, Thun-Hohenstein L (2001) Intrauterine blood flow and long-term intellectual, neurologic, and social development. Obstet Gynecol 97:449–453PubMedCrossRef Wienerroither H, Steiner H, Tomaselli J, Lobendanz M, Thun-Hohenstein L (2001) Intrauterine blood flow and long-term intellectual, neurologic, and social development. Obstet Gynecol 97:449–453PubMedCrossRef
18.
go back to reference Goldstein JM, Seidman LJ, Buka SL, Horton NJ, Donatelli JAL, Rieder RO, Tsuang MT (2000) Impact of genetic vulnerability and hypoxia on overall intelligence by age 7 in offspring at high risk for schizophrenia compared with affective psychoses. Schizophr Bull 26:323–334PubMed Goldstein JM, Seidman LJ, Buka SL, Horton NJ, Donatelli JAL, Rieder RO, Tsuang MT (2000) Impact of genetic vulnerability and hypoxia on overall intelligence by age 7 in offspring at high risk for schizophrenia compared with affective psychoses. Schizophr Bull 26:323–334PubMed
19.
go back to reference Li J, Lin JC, Wang H, Peterson JW, Furie BC, Furie B, Booth SL, Volpe JJ, Rosenberg PA (2003) Novel role of vitamin k in preventing oxidative injury to developing oligodendrocytes and neurons. J Neurosci 23:5816–5826PubMed Li J, Lin JC, Wang H, Peterson JW, Furie BC, Furie B, Booth SL, Volpe JJ, Rosenberg PA (2003) Novel role of vitamin k in preventing oxidative injury to developing oligodendrocytes and neurons. J Neurosci 23:5816–5826PubMed
20.
go back to reference Kawata M (1995) Roles of steroid hormones and their receptors in structural organization in the nervous system. Neurosci Res 24:1–46PubMedCrossRef Kawata M (1995) Roles of steroid hormones and their receptors in structural organization in the nervous system. Neurosci Res 24:1–46PubMedCrossRef
21.
go back to reference Tobet SA (2002) Genes controlling hypothalamic development and sexual differentiation. Eur J Neurosci 16:373–376PubMedCrossRef Tobet SA (2002) Genes controlling hypothalamic development and sexual differentiation. Eur J Neurosci 16:373–376PubMedCrossRef
22.
go back to reference Tobet SA, Hanna IK (1997) Ontogeny of sex differences in the mammalian hypothalamus and preoptic area. Cell Mol Neurobiol 17:565–601PubMedCrossRef Tobet SA, Hanna IK (1997) Ontogeny of sex differences in the mammalian hypothalamus and preoptic area. Cell Mol Neurobiol 17:565–601PubMedCrossRef
23.
go back to reference Grimm VE, Frieder B (1985) Differential vulnerability of male and female rats to the timing of various perinatal insults. Int J Neurosci 27:155–164PubMedCrossRef Grimm VE, Frieder B (1985) Differential vulnerability of male and female rats to the timing of various perinatal insults. Int J Neurosci 27:155–164PubMedCrossRef
24.
go back to reference Amato M, Howald H, Muralt GV (1987) Foetal sex distribution of peri-intraventricular haemorrhage in preterm infants. Eur Neurol 27:20PubMedCrossRef Amato M, Howald H, Muralt GV (1987) Foetal sex distribution of peri-intraventricular haemorrhage in preterm infants. Eur Neurol 27:20PubMedCrossRef
25.
go back to reference Rantakallio P, Wendt LV (1985) Prognosis for low-birthweight infants up to the age of 14: a population study. Dev Med Child Neurol 27:655–663PubMedCrossRef Rantakallio P, Wendt LV (1985) Prognosis for low-birthweight infants up to the age of 14: a population study. Dev Med Child Neurol 27:655–663PubMedCrossRef
26.
go back to reference Murray RM, Owen MJ, Goodman R, Lewis SW (1989) A neurodevelopmental perspective on some epiphenomena of schizophrenia. In: Cazullo CL, Invernizzi G, Sacchetti E, Vita A (eds) Plasticity and Morphology of the CNS. MIT Press, Lancaster Murray RM, Owen MJ, Goodman R, Lewis SW (1989) A neurodevelopmental perspective on some epiphenomena of schizophrenia. In: Cazullo CL, Invernizzi G, Sacchetti E, Vita A (eds) Plasticity and Morphology of the CNS. MIT Press, Lancaster
27.
go back to reference Niswander KR, Gordon M (1972) The collaborative perinatal study of the national institute of neurological diseases and stroke: the women and their pregnancies. Government Printing Office, U.S. Department of Health, Education, and Welfare, Washington, DC Niswander KR, Gordon M (1972) The collaborative perinatal study of the national institute of neurological diseases and stroke: the women and their pregnancies. Government Printing Office, U.S. Department of Health, Education, and Welfare, Washington, DC
28.
go back to reference Sebire NJ, Jain V, Talbert DG (2004) Spiral artery associated restricted growth (SPAARG): a computer model of pathophysiology resulting from low intervillous pressure having fetal programming implications. Pathophysiology 11:87–94PubMedCrossRef Sebire NJ, Jain V, Talbert DG (2004) Spiral artery associated restricted growth (SPAARG): a computer model of pathophysiology resulting from low intervillous pressure having fetal programming implications. Pathophysiology 11:87–94PubMedCrossRef
29.
go back to reference Lackman F, Capewell V, Gagnon R, Richardson B (2001) Fetal umbilical cord oxygen values and birth to placental weight ratio in relation to size at birth. Am J Obstet Gynecol 185:674–682PubMedCrossRef Lackman F, Capewell V, Gagnon R, Richardson B (2001) Fetal umbilical cord oxygen values and birth to placental weight ratio in relation to size at birth. Am J Obstet Gynecol 185:674–682PubMedCrossRef
30.
go back to reference Salafia CM, Minior VK, Lopez-Zeno JA, Whittington SS, Pezzullo JC, Vintzileos AM (1995) Relationship between placental histologic features and umbilical cord blood gases in preterm gestations. Am J Obstet Gynecol 173:1058–1064PubMedCrossRef Salafia CM, Minior VK, Lopez-Zeno JA, Whittington SS, Pezzullo JC, Vintzileos AM (1995) Relationship between placental histologic features and umbilical cord blood gases in preterm gestations. Am J Obstet Gynecol 173:1058–1064PubMedCrossRef
31.
go back to reference McDermott M, Gillan JE (1995) Chronic reduction in fetal blood flow is associated with placental infarction. Placenta 16:165–170PubMedCrossRef McDermott M, Gillan JE (1995) Chronic reduction in fetal blood flow is associated with placental infarction. Placenta 16:165–170PubMedCrossRef
32.
go back to reference Becroft DM, Thompson JM, Mitchell EA (2004) Placental infarcts, intervillous fibrin plaques, and intervillous thrombi: incidences, cooccurrences, and epidemiological associations. Pediatr Dev Pathol 7:26–34PubMedCrossRef Becroft DM, Thompson JM, Mitchell EA (2004) Placental infarcts, intervillous fibrin plaques, and intervillous thrombi: incidences, cooccurrences, and epidemiological associations. Pediatr Dev Pathol 7:26–34PubMedCrossRef
33.
go back to reference Beinder E, Mohaupt MG, Schlembach D, Fischer T, Sterzel RB, Lang N, Baylis C (1999) Nitric oxide synthase activity and Doppler parameters in the fetoplacental and uteroplacental circulation in preeclampsia. Hypertens Pregnancy 18:115–127PubMedCrossRef Beinder E, Mohaupt MG, Schlembach D, Fischer T, Sterzel RB, Lang N, Baylis C (1999) Nitric oxide synthase activity and Doppler parameters in the fetoplacental and uteroplacental circulation in preeclampsia. Hypertens Pregnancy 18:115–127PubMedCrossRef
34.
go back to reference Kumazaki K, Nakayama M, Sumida Y, Ozono K, Mushiake S, Suehara N, Wada Y, Fujimura M (2002) Placental features in preterm infants with periventricular leukomalacia. Pediatrics 109:650–655PubMedCrossRef Kumazaki K, Nakayama M, Sumida Y, Ozono K, Mushiake S, Suehara N, Wada Y, Fujimura M (2002) Placental features in preterm infants with periventricular leukomalacia. Pediatrics 109:650–655PubMedCrossRef
35.
go back to reference Nelson DM, Crouch EC, Curran EM, Farmer DR (1990) Trophoblast interaction with fibrin matrix. Epithelialization of perivillous fibrin deposits as a mechanism for villous repair in the human placenta. Am J Pathol 136:855–865PubMed Nelson DM, Crouch EC, Curran EM, Farmer DR (1990) Trophoblast interaction with fibrin matrix. Epithelialization of perivillous fibrin deposits as a mechanism for villous repair in the human placenta. Am J Pathol 136:855–865PubMed
36.
go back to reference Wyatt SM, Kraus FT, Roh CR, Elchalal U, Nelson DM, Sadovsky Y (2005) The correlation between sampling site and gene expression in the term human placenta. Placenta 26:372–379PubMedCrossRef Wyatt SM, Kraus FT, Roh CR, Elchalal U, Nelson DM, Sadovsky Y (2005) The correlation between sampling site and gene expression in the term human placenta. Placenta 26:372–379PubMedCrossRef
37.
go back to reference Wataba K, Saito T, Takeuchi M, Nakayama M, Suehara N, Kudo R (2004) Changed expression of heat shock proteins in various pathological findings in placentas with intrauterine fetal growth restriction. Med Electron Microsc 37:170–176PubMedCrossRef Wataba K, Saito T, Takeuchi M, Nakayama M, Suehara N, Kudo R (2004) Changed expression of heat shock proteins in various pathological findings in placentas with intrauterine fetal growth restriction. Med Electron Microsc 37:170–176PubMedCrossRef
38.
go back to reference Out HJ, Kooijman CD, Bruinse HW, Derksen RH (1991) Histopathological findings in placentae from patients with intra-uterine fetal death and anti-phospholipid antibodies. Eur J Obstet Gynecol Reprod Biol 41:179–186PubMedCrossRef Out HJ, Kooijman CD, Bruinse HW, Derksen RH (1991) Histopathological findings in placentae from patients with intra-uterine fetal death and anti-phospholipid antibodies. Eur J Obstet Gynecol Reprod Biol 41:179–186PubMedCrossRef
39.
go back to reference Salafia CM, Pezzullo JC, Lopez-Zeno JA, Simmens S, Minior VK, Vintzileos AM (1995) Placental pathologic features of preterm preeclampsia. Am J Obstet Gynecol 173:1097–1105PubMedCrossRef Salafia CM, Pezzullo JC, Lopez-Zeno JA, Simmens S, Minior VK, Vintzileos AM (1995) Placental pathologic features of preterm preeclampsia. Am J Obstet Gynecol 173:1097–1105PubMedCrossRef
40.
go back to reference Mardi K, Sharma J (2003) Histopathological evaluation of placentas in IUGR pregnancies. Indian J Pathol Microbiol 46:551–554PubMed Mardi K, Sharma J (2003) Histopathological evaluation of placentas in IUGR pregnancies. Indian J Pathol Microbiol 46:551–554PubMed
41.
go back to reference Salafia CM, Minior VK, Pezzullo JC, Popek EJ, Rosenkrantz TS, Vintzileos AM (1995) Intrauterine growth restriction in infants of less than thirty-two weeks’ gestation: associated placental pathologic features. Am J Obstet Gynecol 173:1049–1057PubMedCrossRef Salafia CM, Minior VK, Pezzullo JC, Popek EJ, Rosenkrantz TS, Vintzileos AM (1995) Intrauterine growth restriction in infants of less than thirty-two weeks’ gestation: associated placental pathologic features. Am J Obstet Gynecol 173:1049–1057PubMedCrossRef
42.
go back to reference Salafia CM, Vogel CA, Bantham KF, Vintzileos AM, Pezzullo JC, Silberman L (1992) Preterm delivery: correlations of fetal growth. Am J Perinatol 9:190–193PubMedCrossRef Salafia CM, Vogel CA, Bantham KF, Vintzileos AM, Pezzullo JC, Silberman L (1992) Preterm delivery: correlations of fetal growth. Am J Perinatol 9:190–193PubMedCrossRef
43.
go back to reference Salafia CM, Vintzileos AM, Silberman L, Bantham KF, Vogel CA (1992) Placental pathology of idiopathic intrauterine growth retardation at term. Am J Perinatol 9:179–184PubMedCrossRef Salafia CM, Vintzileos AM, Silberman L, Bantham KF, Vogel CA (1992) Placental pathology of idiopathic intrauterine growth retardation at term. Am J Perinatol 9:179–184PubMedCrossRef
44.
go back to reference Salafia CM, Lopez-Zeno JA, Sherer DM, Whittington SS, Minior VK, Vintzileos AM (1995) Histologic evidence of old intrauterine bleeding is more frequent in prematurity. Am J Obstet Gynecol 173:1065–1070PubMedCrossRef Salafia CM, Lopez-Zeno JA, Sherer DM, Whittington SS, Minior VK, Vintzileos AM (1995) Histologic evidence of old intrauterine bleeding is more frequent in prematurity. Am J Obstet Gynecol 173:1065–1070PubMedCrossRef
45.
go back to reference Redline RW, Pappin A (1995) Fetal thrombotic vasculopathy: the clinical significance of extensive avascular villi. Hum Pathol 26:80–85PubMedCrossRef Redline RW, Pappin A (1995) Fetal thrombotic vasculopathy: the clinical significance of extensive avascular villi. Hum Pathol 26:80–85PubMedCrossRef
46.
go back to reference Bjoro K Jr (1983) Vascular anomalies of the umbilical cord. II. Perinatal and pediatric implications. Early Hum Dev 8:279–287PubMedCrossRef Bjoro K Jr (1983) Vascular anomalies of the umbilical cord. II. Perinatal and pediatric implications. Early Hum Dev 8:279–287PubMedCrossRef
47.
go back to reference Dudiak CM, Salomon CG, Posniak HV, Olson MC, Flisak ME (1995) Sonography of the umbilical cord. Radiographics 15:1035–1050PubMed Dudiak CM, Salomon CG, Posniak HV, Olson MC, Flisak ME (1995) Sonography of the umbilical cord. Radiographics 15:1035–1050PubMed
48.
go back to reference Liu BN (1991) Pathological analysis of 76 placentae in fetal distress. Zhonghua Fu Chan Ke Za Zhi 26(3):144–148, 187 Liu BN (1991) Pathological analysis of 76 placentae in fetal distress. Zhonghua Fu Chan Ke Za Zhi 26(3):144–148, 187
49.
go back to reference Gaffney G, Squier MV, Johnson A, Flavell V, Sellers S (1994) Clinical associations of prenatal ischaemic white matter injury. Arch Dis Child Fetal Neonatal Ed 70:F101–F106PubMedCrossRef Gaffney G, Squier MV, Johnson A, Flavell V, Sellers S (1994) Clinical associations of prenatal ischaemic white matter injury. Arch Dis Child Fetal Neonatal Ed 70:F101–F106PubMedCrossRef
50.
51.
go back to reference Amir H, Weintraub A, Aricha-Tamir B, Apel-Sarid L, Holcberg G, Sheiner E (2009) A piece in the puzzle of intrauterine fetal death: Pathological findings in placentas from term and preterm intrauterine fetal death pregnancies. J Matern Fetal Neonatal Med 22:759–764PubMedCrossRef Amir H, Weintraub A, Aricha-Tamir B, Apel-Sarid L, Holcberg G, Sheiner E (2009) A piece in the puzzle of intrauterine fetal death: Pathological findings in placentas from term and preterm intrauterine fetal death pregnancies. J Matern Fetal Neonatal Med 22:759–764PubMedCrossRef
52.
go back to reference Kramer MS, Kahn SR, Rozen R, Evans R, Platt RW, Chen MF, Goulet L, Séguin L, Dassa C, Lydon J, McNamara H, Dahhou M, Genest J (2009) Vasculopathic and thrombophilic risk factors for spontaneous preterm birth. Int J Epidemiol 38:715–723PubMedCrossRef Kramer MS, Kahn SR, Rozen R, Evans R, Platt RW, Chen MF, Goulet L, Séguin L, Dassa C, Lydon J, McNamara H, Dahhou M, Genest J (2009) Vasculopathic and thrombophilic risk factors for spontaneous preterm birth. Int J Epidemiol 38:715–723PubMedCrossRef
53.
go back to reference Kramer MS, Chen MF, Roy I, Dassa C, Lamoureux J, Kahn SR, McNamara H, Platt RW (2006) Montreal Prematurity Study Group. Intra- and interobserver agreement and statistical clustering of placental histopathologic features relevant to preterm birth. Am J Obstet Gynecol 195:1674–1679PubMedCrossRef Kramer MS, Chen MF, Roy I, Dassa C, Lamoureux J, Kahn SR, McNamara H, Platt RW (2006) Montreal Prematurity Study Group. Intra- and interobserver agreement and statistical clustering of placental histopathologic features relevant to preterm birth. Am J Obstet Gynecol 195:1674–1679PubMedCrossRef
54.
go back to reference Salafia CM, Pezzullo JC, Ghidini A, Lopez-Zeno JA, Whittington SS (1998) Clinical correlations of patterns of placental pathology in preterm pre-eclampsia. Placenta 19:67–72PubMedCrossRef Salafia CM, Pezzullo JC, Ghidini A, Lopez-Zeno JA, Whittington SS (1998) Clinical correlations of patterns of placental pathology in preterm pre-eclampsia. Placenta 19:67–72PubMedCrossRef
55.
go back to reference Beebe LA, Cowan LD, Altshuler G (1996) The epidemiology of placental features: associations with gestational age and neonatal outcome. Obstet Gynecol 87:771–778PubMedCrossRef Beebe LA, Cowan LD, Altshuler G (1996) The epidemiology of placental features: associations with gestational age and neonatal outcome. Obstet Gynecol 87:771–778PubMedCrossRef
57.
go back to reference Langston C, Kaplan CG, Macpherson T, Manci E, Peevy K, Clark B, Murtagh C, Cox S, Glenn G (1997) Practice guideline for examination of the placenta: developed by the placental pathology practice guideline development task force of the college of American pathologists. Arch Pathol Lab Med 121:449–476PubMed Langston C, Kaplan CG, Macpherson T, Manci E, Peevy K, Clark B, Murtagh C, Cox S, Glenn G (1997) Practice guideline for examination of the placenta: developed by the placental pathology practice guideline development task force of the college of American pathologists. Arch Pathol Lab Med 121:449–476PubMed
58.
go back to reference Sherer DM (2002) A review of amniotic fluid dynamics and the enigma of isolated oligohydramnios. Am J Perinatol 19:253–266PubMedCrossRef Sherer DM (2002) A review of amniotic fluid dynamics and the enigma of isolated oligohydramnios. Am J Perinatol 19:253–266PubMedCrossRef
59.
go back to reference Robbins S, Cotran R (2005) Robbins and Cotran pathologic basis of disease, 7th edn. Elsevier Saunders, Philadelphia Robbins S, Cotran R (2005) Robbins and Cotran pathologic basis of disease, 7th edn. Elsevier Saunders, Philadelphia
60.
go back to reference Done DJ, Johnstone EC, Frith CD, Golding J, Shepherd PM, Crow TJ (1991) Complications of pregnancy and delivery in relation to psychosis in adult life: data from the British perinatal mortality survey sample. Br Med J 302:1576–1580CrossRef Done DJ, Johnstone EC, Frith CD, Golding J, Shepherd PM, Crow TJ (1991) Complications of pregnancy and delivery in relation to psychosis in adult life: data from the British perinatal mortality survey sample. Br Med J 302:1576–1580CrossRef
61.
go back to reference Kubzansky LD, Martin LT, Buka SL (2004) Early manifestations of personality and adult emotional functioning. Emotion 4:364–377PubMedCrossRef Kubzansky LD, Martin LT, Buka SL (2004) Early manifestations of personality and adult emotional functioning. Emotion 4:364–377PubMedCrossRef
62.
go back to reference Rothbart MK, Bates JE (1998) Temperament. In: Damon W, Eisenberg N (eds) Handbook of child psychology, vol 3, 5th edn. Wiley, New York, pp 105–176 Rothbart MK, Bates JE (1998) Temperament. In: Damon W, Eisenberg N (eds) Handbook of child psychology, vol 3, 5th edn. Wiley, New York, pp 105–176
63.
go back to reference Seidman LJ, Buka SL, Goldstein JM, Horton NJ, Rieder RO, Tsuang MT (2000) The relationship of obstetrical complications to cognitive functioning at age 7 in the New England cohorts of the National Collaborative Perinatal Project. Schizophr Bull 26:309–321PubMed Seidman LJ, Buka SL, Goldstein JM, Horton NJ, Rieder RO, Tsuang MT (2000) The relationship of obstetrical complications to cognitive functioning at age 7 in the New England cohorts of the National Collaborative Perinatal Project. Schizophr Bull 26:309–321PubMed
64.
go back to reference Collaer ML, Hines M (1995) Human behavioral sex differences: a role for gonadal hormones during early development? Psychol Bull 118:55–107PubMedCrossRef Collaer ML, Hines M (1995) Human behavioral sex differences: a role for gonadal hormones during early development? Psychol Bull 118:55–107PubMedCrossRef
65.
go back to reference Buka S, Seidman L, Goldstein J, Zornberg G, Donatelli J, Denny L, Tsuang M (1999) Impacts of perinatal hypoxia and genetic vulnerability on schizophrenia: the New England longitudinal studies of schizophrenia. Psychiatr Ann 29:151–156 Buka S, Seidman L, Goldstein J, Zornberg G, Donatelli J, Denny L, Tsuang M (1999) Impacts of perinatal hypoxia and genetic vulnerability on schizophrenia: the New England longitudinal studies of schizophrenia. Psychiatr Ann 29:151–156
66.
go back to reference Corah NL, Anthony EJ, Painter P, Stern JA, Thurston DL (1965) Effects of perinatal anoxia after seven years. Psychol Monogr 79(suppl 3):1–34PubMedCrossRef Corah NL, Anthony EJ, Painter P, Stern JA, Thurston DL (1965) Effects of perinatal anoxia after seven years. Psychol Monogr 79(suppl 3):1–34PubMedCrossRef
67.
go back to reference Maneru C, Junque C, Botet F, Tallada M, Guardia J (2001) Neuropsychological long-term sequelae of perinatal asphyxia. Brain Inj 15:1029–1039PubMedCrossRef Maneru C, Junque C, Botet F, Tallada M, Guardia J (2001) Neuropsychological long-term sequelae of perinatal asphyxia. Brain Inj 15:1029–1039PubMedCrossRef
68.
go back to reference Maneru C, Junque C (2002) Cognitive deficit in perinatal asphyxia. Revista de Neurologia 34:1171–1177PubMed Maneru C, Junque C (2002) Cognitive deficit in perinatal asphyxia. Revista de Neurologia 34:1171–1177PubMed
69.
go back to reference Perlman JM (2006) Intervention strategies for neonatal hypoxic-ischemic cerebral injury. Clin Ther 28:1353–1365PubMedCrossRef Perlman JM (2006) Intervention strategies for neonatal hypoxic-ischemic cerebral injury. Clin Ther 28:1353–1365PubMedCrossRef
70.
go back to reference Walder DJ, Seidman LJ, Makris N, Tsuang MT, Kennedy DN, Goldstein JM (2007) Neuroanatomic substrates of sex differences in language dysfunction in schizophrenia: a pilot study. Schizophr Res 90:295–301PubMedCrossRef Walder DJ, Seidman LJ, Makris N, Tsuang MT, Kennedy DN, Goldstein JM (2007) Neuroanatomic substrates of sex differences in language dysfunction in schizophrenia: a pilot study. Schizophr Res 90:295–301PubMedCrossRef
71.
go back to reference Goldstein JM, Seidman LJ, Horton NJ, Makris N, Kennedy DN, Caviness VS Jr, Faraone SV, Tsuang MT (2001) Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cereb Cortex 11:490–497PubMedCrossRef Goldstein JM, Seidman LJ, Horton NJ, Makris N, Kennedy DN, Caviness VS Jr, Faraone SV, Tsuang MT (2001) Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cereb Cortex 11:490–497PubMedCrossRef
72.
go back to reference Schwartz CE, Wright CI, Shin LM, Kagan J, Rauch SL (2003) Inhibited and uninhibited infants “grown up”: adult Amygdalar response to novelty. Science 300:1952–1953PubMedCrossRef Schwartz CE, Wright CI, Shin LM, Kagan J, Rauch SL (2003) Inhibited and uninhibited infants “grown up”: adult Amygdalar response to novelty. Science 300:1952–1953PubMedCrossRef
73.
go back to reference Rosenbaum JF, Biederman J, Bolduc-Murphy EA, Faraone SV, Chaloff J, Hirshfeld DR, Kagan J (1993) Behavioral inhibition in childhood: a risk factor for anxiety disorders. Harv Rev Psychiatry 1:2–16PubMedCrossRef Rosenbaum JF, Biederman J, Bolduc-Murphy EA, Faraone SV, Chaloff J, Hirshfeld DR, Kagan J (1993) Behavioral inhibition in childhood: a risk factor for anxiety disorders. Harv Rev Psychiatry 1:2–16PubMedCrossRef
74.
go back to reference Kessler RC, Berglund P, Demler O, Jin R, Koretz D, Merikangas KR, Rush AJ, Walters EE, Wang PS (2003) The epidemiology of major depressive disorder: results from the National Comorbidity Survey Replication (NCS-R). J Am Med Assoc 289:3095–3105CrossRef Kessler RC, Berglund P, Demler O, Jin R, Koretz D, Merikangas KR, Rush AJ, Walters EE, Wang PS (2003) The epidemiology of major depressive disorder: results from the National Comorbidity Survey Replication (NCS-R). J Am Med Assoc 289:3095–3105CrossRef
75.
go back to reference Kendler K, GAtz M, Gardner C, Pedersen N (2006) A Swedish National twin study of lifetime major depression. Am J Psychiatry 163:109–114PubMedCrossRef Kendler K, GAtz M, Gardner C, Pedersen N (2006) A Swedish National twin study of lifetime major depression. Am J Psychiatry 163:109–114PubMedCrossRef
76.
go back to reference Schwartz CE, Snidman N, Kagan J (1999) Adolescent social anxiety as an outcome of inhibited temperament in childhood. J Am Acad Child Adolesc Psychiatry 38:1008–1015PubMedCrossRef Schwartz CE, Snidman N, Kagan J (1999) Adolescent social anxiety as an outcome of inhibited temperament in childhood. J Am Acad Child Adolesc Psychiatry 38:1008–1015PubMedCrossRef
77.
go back to reference Mallen CD, Mottram S, Thomas E (2009) Is childhood pain associated with future mental health problems? A population based study of young adults in North Staffordshire. Soc Psychiatry Psychiatr Epidemiol 44:489–494PubMedCrossRef Mallen CD, Mottram S, Thomas E (2009) Is childhood pain associated with future mental health problems? A population based study of young adults in North Staffordshire. Soc Psychiatry Psychiatr Epidemiol 44:489–494PubMedCrossRef
78.
go back to reference Goldstein JM, Cherkerzian S, Buka SL, Fitzmaurice G, Susser E, Hornig M, Gillman MW, Factor-Litvak P, Sloan R (2011) Sex-specific impact of maternal-fetal inflammatory risk factors on depression and cardiovascular risk 40 Years Later. J Dev Orig Health Dis (under review) Goldstein JM, Cherkerzian S, Buka SL, Fitzmaurice G, Susser E, Hornig M, Gillman MW, Factor-Litvak P, Sloan R (2011) Sex-specific impact of maternal-fetal inflammatory risk factors on depression and cardiovascular risk 40 Years Later. J Dev Orig Health Dis (under review)
79.
go back to reference Bale TL, Vale WW (2003) Increased depression-like behaviors in corticotropin-releasing factor receptor-2-deficient mice: sexually dichotomous responses. J Neurosci 23:5295–5301PubMed Bale TL, Vale WW (2003) Increased depression-like behaviors in corticotropin-releasing factor receptor-2-deficient mice: sexually dichotomous responses. J Neurosci 23:5295–5301PubMed
80.
go back to reference McCormick CM, Smythe JW, Sharma S, Meaney MJ (1995) Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Res Dev Brain Res 84:55–61PubMedCrossRef McCormick CM, Smythe JW, Sharma S, Meaney MJ (1995) Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Res Dev Brain Res 84:55–61PubMedCrossRef
81.
go back to reference Bale TL, Picetti R, Contarino A, Koob GF, Vale WW, Lee KF (2002) Mice deficient for both corticotropin-releasing factor receptor 1 (CRFR1) and CRFR2 have an impaired stress response and display sexually dichotomous anxiety-like behavior. J Neurosci 22:193–199PubMed Bale TL, Picetti R, Contarino A, Koob GF, Vale WW, Lee KF (2002) Mice deficient for both corticotropin-releasing factor receptor 1 (CRFR1) and CRFR2 have an impaired stress response and display sexually dichotomous anxiety-like behavior. J Neurosci 22:193–199PubMed
82.
go back to reference Funayama CA, de Moura-Ribeiro MV, Goncalves AL (1997) Hypoxic-ischemic encephalopathy in newborn infants. Acute period and outcome. Arquivos de Neuro-Psiquiatria 55:771–779PubMedCrossRef Funayama CA, de Moura-Ribeiro MV, Goncalves AL (1997) Hypoxic-ischemic encephalopathy in newborn infants. Acute period and outcome. Arquivos de Neuro-Psiquiatria 55:771–779PubMedCrossRef
83.
go back to reference Robertson C, Finer N (1985) Term infants with hypoxic-ischemic encephalopathy: outcome at 3.5 years. Dev Med Child Neurol 27:473–484PubMedCrossRef Robertson C, Finer N (1985) Term infants with hypoxic-ischemic encephalopathy: outcome at 3.5 years. Dev Med Child Neurol 27:473–484PubMedCrossRef
84.
go back to reference Robertson CM, Finer NN, Grace MG (1989) School performance of survivors of neonatal encephalopathy associated with birth asphyxia at term. J Pediatr 114:753–760PubMedCrossRef Robertson CM, Finer NN, Grace MG (1989) School performance of survivors of neonatal encephalopathy associated with birth asphyxia at term. J Pediatr 114:753–760PubMedCrossRef
85.
go back to reference Robertson CM, Grace MG (1992) Validation of prediction of kindergarten-age school-readiness scores of nondisabled survivors of moderate neonatal encephalopathy in term infants. Can J Public Health Revue (Canadienne de Sante Publique) 83(Suppl 2):S51–S57 Robertson CM, Grace MG (1992) Validation of prediction of kindergarten-age school-readiness scores of nondisabled survivors of moderate neonatal encephalopathy in term infants. Can J Public Health Revue (Canadienne de Sante Publique) 83(Suppl 2):S51–S57
Metadata
Title
Impact of fetal versus perinatal hypoxia on sex differences in childhood outcomes: developmental timing matters
Authors
Michael Anastario
Carolyn M. Salafia
Garrett Fitzmaurice
Jill M. Goldstein
Publication date
01-03-2012
Publisher
Springer-Verlag
Published in
Social Psychiatry and Psychiatric Epidemiology / Issue 3/2012
Print ISSN: 0933-7954
Electronic ISSN: 1433-9285
DOI
https://doi.org/10.1007/s00127-011-0353-0

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