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

Social Psychiatry and Psychiatric Epidemiology

Volumn 47, Issue 3, 2012, Pages 455-464

  Anastario, Michael ^a,b   Salafia, Carolyn M ^c   Fitzmaurice, Garrett ^d,e   Goldstein, Jill M ^a,e  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b Cicatelli Inc   (United States)

^c NEW YORK UNIVERSITY   (United States)

^d MCLEAN HOSPITAL   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Fetal hypoxia; Fetal programming; Inhibition; Sex differences

Indexed keywords

ARTICLE; CHILD; COGNITIVE DEFECT; FEMALE; FETUS HYPOXIA; HUMAN; MALE; OUTCOME ASSESSMENT; PERINATAL CARE; PREGNANCY; PREGNANCY COMPLICATION; PROSPECTIVE STUDY; PSYCHOLOGICAL ASPECT; SEX DIFFERENCE; UNITED STATES;

BOSTON; CHILD; COGNITION DISORDERS; FEMALE; FETAL HYPOXIA; HUMANS; MALE; OUTCOME ASSESSMENT (HEALTH CARE); PERINATAL CARE; PREGNANCY; PREGNANCY COMPLICATIONS; PROSPECTIVE STUDIES; RHODE ISLAND; SEX FACTORS;

EID: 84862640381     PISSN: 09337954     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00127-011-0353-0     Document Type: Article

References (85)

1. 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 64:797-802
2. 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 43:325-330
3. 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 59:35-41
4. Buka SL, Lipsitt LP, Tsuang MT (1993) Pregnancy/delivery complications and psychiatric diagnosis: a prospective study. Arch Gen Psychiatry 50:151-156
5. Zornberg GL, Buka SL, Tsuang MT (2000) Hypoxic-ischemiarelated fetal/neonatal complications and risk of schizophrenia and other nonaffective psychoses: a 19-year longitudinal study. Am J Psychiatry 157:196-202
6. 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 23:99-103
7. 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 54:625-631
8. 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. 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 166:601-606
10. 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 157:190-195
11. Machon RA, Mednick SA, Huttunen MO (1997) Adult major affective disorder after prenatal exposure to an influenza epidemic. Arch Gen Psychiatry 54:322-328
12. Watson JB, Mednick SA, Huttunen M, Wang X (1999) Prenatal teratogens and the development of adult mental illness. Dev Psychopathol 11:457-466
13. Jones PB, Tarrant CJ (1999) Specificity of developmental precursors to schizophrenia and affective disorders. Schizophr Res 39:121-126
14. Brown AS, Susser ES, Lin SP, Gorman JM (1995) Affective disorders in Holland after prenatal exposure to the 1957 A2 influenza epidemic. Biol Psychiatry 38:270-273
15. 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 179:450-455
16. 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 8:160-165
17. 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 97:449-453
18. 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 26:323-334
19. 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 23:5816-5826
20. Kawata M (1995) Roles of steroid hormones and their receptors in structural organization in the nervous system. Neurosci Res 24:1-46
21. Tobet SA (2002) Genes controlling hypothalamic development and sexual differentiation. Eur J Neurosci 16:373-376
22. Tobet SA, Hanna IK (1997) Ontogeny of sex differences in the mammalian hypothalamus and preoptic area. Cell Mol Neurobiol 17:565-601
23. Grimm VE, Frieder B (1985) Differential vulnerability of male and female rats to the timing of various perinatal insults. Int J Neurosci 27:155-164
24. Amato M, Howald H, Muralt GV (1987) Foetal sex distribution of peri-intraventricular haemorrhage in preterm infants. Eur Neurol 27:20
25. Rantakallio P, Wendt LV (1985) Prognosis for low-birthweight infants up to the age of 14: a population study. Dev Med Child Neurol 27:655-663
26. 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. 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. 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 11:87-94
29. 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 185:674-682
30. 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 173:1058-1064
31. McDermott M, Gillan JE (1995) Chronic reduction in fetal blood flow is associated with placental infarction. Placenta 16:165-170
32. Becroft DM, Thompson JM, Mitchell EA (2004) Placental infarcts, intervillous fibrin plaques, and intervillous thrombi: incidences, cooccurrences, and epidemiological associations. Pediatr Dev Pathol 7:26-34
33. 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 18:115-127
34. 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 109:650-655
35. 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 136:855-865
36. 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 26:372-379
37. 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 37:170-176
38. Out HJ, Kooijman CD, Bruinse HW, Derksen RH (1991) Histopathological findings in placentae from patients with intrauterine fetal death and anti-phospholipid antibodies. Eur J Obstet Gynecol Reprod Biol 41:179-186
39. Salafia CM, Pezzullo JC, Lopez-Zeno JA, Simmens S, Minior VK, Vintzileos AM (1995) Placental pathologic features of preterm preeclampsia. Am J Obstet Gynecol 173:1097-1105
40. Mardi K, Sharma J (2003) Histopathological evaluation of placentas in IUGR pregnancies. Indian J PatholMicrobiol 46:551-554
41. 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 173:1049-1057
42. Salafia CM, Vogel CA, Bantham KF, Vintzileos AM, Pezzullo JC, Silberman L (1992) Preterm delivery: correlations of fetal growth. Am J Perinatol 9:190-193
43. Salafia CM, Vintzileos AM, Silberman L, Bantham KF, Vogel CA (1992) Placental pathology of idiopathic intrauterine growth retardation at term. Am J Perinatol 9:179-184
44. 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 173:1065-1070
45. Redline RW, Pappin A (1995) Fetal thrombotic vasculopathy: the clinical significance of extensive avascular villi. Hum Pathol 26:80-85
46. Bjoro K Jr (1983) Vascular anomalies of the umbilical cord. II. Perinatal and pediatric implications. Early Hum Dev 8:279-287
47. Dudiak CM, Salomon CG, Posniak HV, Olson MC, Flisak ME (1995) Sonography of the umbilical cord. Radiographics 15:1035-1050
48. Liu BN (1991) Pathological analysis of 76 placentae in fetal distress. Zhonghua Fu Chan Ke Za Zhi 26(3):144-148, 187
49. 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-F106
50. Brace RA (1997) Physiology of amniotic fluid volume regulation. Clin Obstet Gynecol 40:280-289
51. 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 22:759-764
52. 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 38:715-723
53. 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 195:1674-1679
54. Salafia CM, Pezzullo JC, Ghidini A, Lopez-Zeno JA, Whittington SS (1998) Clinical correlations of patterns of placental pathology in preterm pre-eclampsia. Placenta 19:67-72
55. Beebe LA, Cowan LD, Altshuler G (1996) The epidemiology of placental features: associations with gestational age and neonatal outcome. Obstet Gynecol 87:771-778
56. Kaplan CG (2007) Fetal and maternal vascular lesions. Semin Diagn Pathol 24:14-22
57. 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 121:449-476
58. Sherer DM (2002) A review of amniotic fluid dynamics and the enigma of isolated oligohydramnios. Am J Perinatol 19:253-266
59. Robbins S, Cotran R (2005) Robbins and Cotran pathologic basis of disease, 7th edn. Elsevier Saunders, Philadelphia
60. 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 302:1576-1580
61. Kubzansky LD, Martin LT, Buka SL (2004) Early manifestations of personality and adult emotional functioning. Emotion 4:364-377
62. 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. 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 26:309-321
64. Collaer ML, Hines M (1995) Human behavioral sex differences: a role for gonadal hormones during early development? Psychol Bull 118:55-107
65. 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. Corah NL, Anthony EJ, Painter P, Stern JA, Thurston DL (1965) Effects of perinatal anoxia after seven years. Psychol Monogr 79(suppl 3):1-34
67. Maneru C, Junque C, Botet F, Tallada M, Guardia J (2001) Neuropsychological long-term sequelae of perinatal asphyxia. Brain Inj 15:1029-1039
68. Maneru C, Junque C (2002) Cognitive deficit in perinatal asphyxia. Revista de Neurologia 34:1171-1177
69. Perlman JM (2006) Intervention strategies for neonatal hypoxicischemic cerebral injury. Clin Ther 28:1353-1365
70. 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 90:295-301
71. 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 11:490-497
72. Schwartz CE, Wright CI, Shin LM, Kagan J, Rauch SL (2003) Inhibited and uninhibited infants "grown up": adult Amygdalar response to novelty. Science 300:1952-1953
73. 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 1:2-16
74. 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 289:3095-3105
75. Kendler K, GAtz M, Gardner C, Pedersen N (2006) A Swedish National twin study of lifetime major depression. Am J Psychiatry 163:109-114
76. Schwartz CE, Snidman N, Kagan J (1999) Adolescent social anxiety as an outcome of inhibited temperament in childhood. J Am Acad Child Adolesc Psychiatry 38:1008-1015
77. 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 44:489-494
78. Goldstein JM, Cherkerzian S, Buka SL, Fitzmaurice G, Susser E, Hornig M, Gillman MW, Factor-Litvak P, Sloan R (2011) Sexspecific impact of maternal-fetal inflammatory risk factors on depression and cardiovascular risk 40 Years Later. J Dev Orig Health Dis (under review)
79. Bale TL, Vale WW (2003) Increased depression-like behaviors in corticotropin-releasing factor receptor-2-deficient mice: sexually dichotomous responses. J Neurosci 23:5295-5301
80. McCormick CM, Smythe JW, Sharma S, Meaney MJ (1995) Sexspecific effects of prenatal stress on hypothalamic-pituitaryadrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Res Dev Brain Res 84:55-61
81. 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 22:193-199
82. Funayama CA, de Moura-Ribeiro MV, Goncalves AL (1997) Hypoxic-ischemic encephalopathy in newborn infants. Acute period and outcome. Arquivos de Neuro-Psiquiatria 55:771-779
83. Robertson C, Finer N (1985) Term infants with hypoxic-ischemic encephalopathy: outcome at 3.5 years. Dev Med Child Neurol 27:473-484
84. Robertson CM, Finer NN, Grace MG (1989) School performance of survivors of neonatal encephalopathy associated with birth asphyxia at term. J Pediatr 114:753-760
85. 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