Neurobiological plausibility of prenatal nutritional deprivation as a risk factor for schizophrenia

Journal of Nervous and Mental Disease

Volumn 184, Issue 2, 1996, Pages 71-85

  Brown, Alan S ^a   Susser, Ezra S ^a   Butler, Pamela D ^b   Andrews, R Richardson ^c   Kaufmann, Charles A ^a   Gorman, Jack M ^a  

^a NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c CHARING CROSS HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BRAIN DEVELOPMENT; HUMAN; NEUROBIOLOGY; NUTRITIONAL DEFICIENCY; PRENATAL DEVELOPMENT; RISK FACTOR; SCHIZOPHRENIA;

BRAIN; FEMALE; FOLIC ACID DEFICIENCY; HUMANS; INFANT, NEWBORN; IODINE; MATERNAL EXPOSURE; NUTRITION DISORDERS; PREGNANCY; PREGNANCY COMPLICATIONS; PRENATAL EXPOSURE DELAYED EFFECTS; RISK FACTORS; SCHIZOPHRENIA; STRESS, PSYCHOLOGICAL; THYROID HORMONES; ZINC;

EID: 0029985655     PISSN: 00223018     EISSN: None     Source Type: Journal    
DOI: 10.1097/00005053-199602000-00003     Document Type: Article

References (98)

1. Adams W, Kendell RE, Hare EH, Munk-Jorgensen P (1993) Epidemiological evidence that maternal influenza contributes to the aetiology of schizophrenia. Br J Psychiatry 163:522-534.
2. Andreasen NC, Nasrallah HA, Dunn V, Olson SC, Grove WM, Ehrhardt JC, Coffman JA, Crossett JHW (1986) Structural abnormalities in the frontal system in schizophrenia: A magnetic resonance imaging study. Arch Gen Psychiatry 43:136-144.
3. Bedi KS (1991) Effects of undernutrition during early life on granule cell numbers in the rat dentate gyrus. Dev Brain Res 29:267-273.
4. Blanchard JJ, Neale JM (1994) The neuropsychological signature of schizophrenia. Am J Psychiatry 151:40-48.
5. Bradbury TN, Miller GA (1985) Season of birth in schizophrenia: A review of evidence, methodology, and etiology. Psychol Bull 3:569-594.
6. Brenton DP, Jackson MJ, Young A (1981) Two pregnancies in a patient with acrodermatitis enteropathica treated with zinc sulphate. Lancet 2:500.
7. Bronzino JD, Austin-LaFrance RJ, Morgane PF, Galler JR (1991) Effects of prenatal protein malnutrition on kindling-induced alteration in dentate granule cell excitability. I: Synaptic transmission measures. Exp Neurol 112:206-215.
8. 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.
9. Buamah PK, Russell M, Bates G, Milford-Ward A, Skillen AW (1984) Maternal zinc status: A determination of central nervous system malformation. Br J Obstet Gynaecol 91:788-790.
10. Butler PD, Susser ES, Brown AS, Kaufmann CA, Gorman JM (1994) Prenatal nutritional deprivation as a risk factor in schizophrenia: Preclinical evidence. Neuropsychopharmacology 11:227-235.
11. Butterworth RF (1990) Vitamin deficiencies and brain development. In NM van Gelder, RF Butterworth, BD Drujan (Eds), (Mal)Nutrition and the infant brain (pp. 207-224). New York: Wiley-Liss.
12. Campbell LR, Dayton DH, Sohal GS (1986) Neural tube defects: A review of human and animal studies on the etiology of neural tube defects. Teratology 34:171-187.
13. Czeizel AE, Dudas I (1992) Prevention of the first occurrence of neural tube defects by periconceptional vitamin supplementation. N Engl J Med 327:1832-1835.
14. Davis KL, Kahn RS, Ko G, Davidson M (1991) Dopamine in schizophrenia: A review and reconceptualization. Am J Psychiatry 148:1474-1486.
15. Delange FM (1986) Endemic cretinism. In SH Ingbar, LE Braverman (Eds), The thyroid: A fundamental and clinical text (pp. 722-734). Philadelphia: JB Lippincott.
16. Economides DL, Ferguson J, MacKenzie IZ, Darley J, Ware II, Holmes-Siedle, MH (1992) Folate and vitamin B12 concentrations in maternal and fetal blood, and amniotic fluid in second trimester pregnancies complicated by neural tube defects. Br J Obstet Gynaecol 99:23-25.
17. Elwood JM, Elwood JH (Eds) (1980) Epidemiology of anencephalus and spina bifida (pp. 159-166). New York: Oxford University Press.
18. Elwood M, Elwood H, Little J (1992) Classification, anatomy, and embryology. In JM Elwood, J Little, JH Elwood (Eds), Epidemiology and control of neural tube defects (pp. 10-36). Oxford: Oxford University Press.
19. Elwood M, Little J (1992) Secular trends. In JM Elwood, J Little, JH Elwood (Eds), Epidemiology and control of neural tube defects (pp. 168-194). Oxford: Oxford University Press.
20. Farde L, Wiesel FA, Stone-Elander S, Halldin C, Nordstrom AL, Hall H, Sedvall G (1990) D2 dopamine receptors in neuroleptic-naive schizophrenic patients: A positron emission tomography study with C11-raclopride. Arch Gen Psychiatry 47: 213-219.
21. Flynn A, Miller SI, Martier SS, Golden NL, Sokol RJ, Del Villano BC (1981) Zinc status of pregnant alcoholic women: A determinant of fetal outcome. Lancet 1:572-574.
22. Gardiki-Kouidou P, Seller MJ (1988) Amniotic fluid folate, vitamin B12 and transcobalamins in neural tube defects. Clin Genet 33:441-448.
23. Golub MS, Gershwin ME, Vijayan VK (1983) Passive avoidance performance of mice fed marginally or severely zinc-deficient diets during post embryonic brain development. Physiol Behav 30:409-413.
24. Goodman A (1994) Retinoid dysregulation as a cause of schizophrenia? Am J Psychiatry 151:452-453.
25. Goodman R (1988) Are complications of pregnancy and birth causes of schizophrenia? Dev Med Child Neurol 30:391-395.
26. Gould E, Westlind-Danielsson A, Frankfurt M, McEwen BS (1990) Sex differences and thyroid hormone sensitivity of hippocampal pyramidal cells. J Neurosci 10:996-1003.
27. Gould E, Woolley CS, McEwen BS (1991) The hippocampal formation: Morphological changes induced by thyroid, gonadal, and adrenal hormones. Psychoneuroendocrinology 16:67-84.
28. Hall JG, Friedman JM, Kenna BA, Popkin J, Jawanda M, Arnold W (1988) Clinical, genetic, and epidemiological factors in neural tube defects. Am J Hum Genet 43:827-837.
29. Hambidge KM, Neider KH, Walravens PA (1975) Zinc acrodermatitis enteropathica and congenital malformation. Lancet 1: 577-578.
30. Hare EH, Moran PAP (1979) Raised parental age in psychiatric patients: Evidence for the constitutional hypothesis. Br J Psychiatry 134:169-177.
31. Hetzel BS (1987) An overview of the prevention and control of iodine deficiency disorders. In BS Hetzel, JT Dunn, JB Stanbury (Eds), The prevention and control of iodine deficiency disorders (pp. 7-31). Amsterdam: Elsevier.
32. Hinks LJ, Ogilvy-Stuart A, Hambidge KM, Walker V (1989) Maternal zinc and selenium status in pregnancies with a neural tube defect or elevated plasma alpha-fetoprotein. Br J Obstet Gynaecol 96:61-66.
33. Huether G (1990) Malnutrition and developing synaptic transmitter systems: Lasting effects, functional implications. In NM van Gelder; RS Butterworth, BD Drujan (Eds), (Mal)Nutrition and the infant brain (pp. 141-156). New York: Wiley-Liss.
34. Hurley LS (1981) Teratogenic aspects of manganese, zinc, and copper nutrition. Physiol Rev 61:249-288.
35. Huttenen M, Niskanen P (1978) Prenatal loss of father and psychiatric disorders. Arch Gen Psychiatry 35:429-431.
36. Jacobsen B, Kinney DK (1980) Perinatal complications in adopted and non-adopted schizophrenics and their controls. Acta Psychiatr Scand 62(suppl 285):337-346.
37. Jablensky A, Sartorious N, Ernberg G, Anker M, Korten A, Cooper JE, Day R, Bertelsen A (1992) Schizophrenia: manifestations, incidence, and course in different cultures. A World Health Organization Study. Psychol Med Monogr Suppl 20.
38. Jordan TC, Cane SE, Howells KF (1981) Deficits in spatial memory performance induced by early undernutrition. Dev Psychobiol 14:317-325.
39. Jordan TC, Clark GA (1983) Early undernutrition impairs hippocampal long-term potentiation in adult rats. Behav Neurosci 97:319-322.
40. Jordan, TC, Howells KF, McNaughton N, Heatlie PL (1982) Effects of early undernutrition on hippocampal development and function. Res Exp Med 180:201-207.
41. Kawamoto JC, Halas ES (1984) Lasting morphological effects of mild perinatal zinc deficiency in the adult hippocampal formation. In CJ Frederickson, GA Howell, EF Kasarski (Eds), The neurobiology of zinc, Part B. Deficiency, toxicity and pathology (pp. 33-48). New York: AR Liss.
42. Keen CL, Hurley LS (1989) Zinc and reproduction: Effects of deficiency on foetal and postnatal development. In CF Mills (Ed), Zinc in human biology (pp. 183-220). Dorchester: Springer Verlag.
43. Kirke PN, Molloy AM, Daly LE, Burke H, Weir DG, Scott JM (1993) Maternal plasma folate and vitamin B12 are independent risk factors for neural tube defects. Q J Med 86:703-708.
44. Laurence KM, James N, Miller MH, Tennant GB, Campbell H (1981) Double-blind randomised controlled trial of folate treatment before conception to prevent recurrence of neural-tube defects. Br Med J 282:1509-1511.
45. Lazebnik N, Kuhnert BR, Huhnert PM, Thompson KI (1988) Zinc status, pregnancy complications, and labor abnormalities. Br J Obstet Gynecol 158:161-166.
46. Leck I (1972) The etiology of human malformations: Insights from epidemiology. Teratology 5:303-314.
47. Leck I (1977) Correlations of malformation frequency with environmental and genetic attributes in man. In JC Wilson, PC Fraser (Eds), Handbook of teratology (Vol 3, pp. 243-324). New York: Plenum.
48. Leck I (1984) The geographical distribution of neural tube defects and oral clefts. Br Med Bull 40:390-395.
49. Leck I (1974) Causation of neural tube defects: Clues from epidemiology. Br Med Bull 30:158-163.
50. Leck I (1983) Fetal malformations. In SL Barron, AM Thomson (Eds), Obstetrical epidemiology. London: Academic Press.
51. Lewis PD, Patel AJ, Balazs R (1979) Effect of undernutrition on cell generation in the rat hippocampus. Brain Res 168:186-189.
52. Lewis SW, Murray RM (1987) Obstetric complications, neurodevelopmental deviance and risk of schizophrenia. J Psychiatr Res 21:413-421.
53. Little J, Elwood M (1992a) Geographical variation. In JM Elwood, J Little, JH Elwood (Eds), Epidemiology and control of neural tube defects (pp. 96-145). Oxford: Oxford University Press.
54. Little J, Elwood M (1992b) Seasonal variation. In JM Elwood J Little, JH Elwood (Eds), Epidemiology and control of neural tube defects (pp. 195-246). Oxford: Oxford University Press.
55. Little J, Elwood M (1992c) Ethnic origin and migration. In JM Elwood, J Little, JH Elwood (Eds), Epidemiology and control of neural tube defects (pp. 146-167). Oxford: Oxford University Press.
56. Machon RA, Mednick SA, Schulsinger F (1983) The interaction of seasonality, place of birth, genetic risk and subsequent schizophrenia in a high risk sample. Br J Psychiatry 143:383-388.
57. Man E, Jones WS, Holden RH, Mellits ED (1971) Throid function in human pregnancy. Retardation of progeny aged 7 years; relationships to maternal age and maternal thyroid function. Am J Obstet Gynecol 111:905-916.
58. Man E, Serunian SA (1976) Thyroid function in human pregnancy: Development or retardation of 7-year-old progeny of hypothyroxinemic women. Am J Obstet Gynecol 125:949-957.
59. Martinot JL, Paillere-Martinot ML, Loc'h C, Hardy P, Poirier MF, Mazoyer B, Beaufils B, Maziere B, Allaire JF, Syrota A (1991) The estimated density of D2 striatal receptors in schizophrenia. Br J Psychiatry 158:346-350.
60. Martinot JL, Peron-Magnan P, Huret JD, Mazoyer B, Baron JC, Boulenger JP, Loc'h C, Maziere B, Caillard V, Loo H, Syrota A (1990) Striatal D2 dopaminergic receptors assessed with positron emission tomography and (76-Br) bromspiperone in untreated schizophrenic patients. Am J Psychiatry 147:44-50.
61. McNeil TF, Kaij L (1978) Obstetric factors in the development of schizophrenia: Complications in the birth of preschizophrenics and in reproduction by schizophrenic parents. In LC Wynne, RL Cromwell, S Matthysse (Eds), The nature of schizophrenia (pp. 401-429). New York: John Wiley.
62. Mednick SA, Machon RA, Huttenen MO, Bonett D (1988) Adult schizophrenia following prenatal exposure to an influenza epidemic. Arch Gen Psychiatry 45:189-192.
63. Meltzer HY (1989) Clinical studies on the mechanism of action of clozapine: The dopamine-serotonin hypothesis of schizophrenia. Psychopharmacology 99:S18-S27.
64. Mills JL, McPartlin JM, Kirke PN, Lee YJ, Conley MR, Weir DG, Scott JM (1995) Homocysteine metabolism in pregnancies complicated by neural-tube defects. Lancet 345:149-151.
65. Mills JL, Rhoads GG, Leigh Simpson J, Cunningham GC, Conley MR, Lassman MR, Walden ME, Depp OR, Hoffman JH, the NICHHD Neural Tube Defects Study Group (1989) The absence of a relation between the periconceptional use of vitamins and neural tube defects. N Engl J Med 321:430-435.
66. Molloy AM, Kirke P, Hillary I, Weir DG, Scott JM (1985) Maternal serum folate and vitamin B12 concentrations in pregnancies associated with neural tube defects. Arch Dis Child 60:660-665.
67. MRC Vitamin Research Study Group (1991) Prevention of neural tube defects: Results of the Medical Research Council Vitamin Study. Lancet 338:131-137.
68. Mukherjee S, Schnurr DB, Reddy R (1989) Family history of type 2 diabetes in schizophrenic patients. Lancet V334;495.
69. O'Callaghan E, Sham P, Takei N, Glover G, Murray RM (1991) Schizophrenia after prenatal exposure to 1957 A2 influenza epidemic. Lancet 337:1248-1250.
70. Pasamanick B, Rogers ME, Lilienfeld AM (1956) Pregnancy experience and the development of behavior disorder in children. Am J Psychiatry 112:613-618.
71. Pharaoh P, Delange F, Fierro-Benitez R, Stanbury JB (1980) Endemic cretinism. In JB Stanbury, BS Hetzel (Eds), Endemic goiter and endemic cretinism (pp. 395-421). New York: Wiley-Liss.
72. Pharoah POD, Connolly KJ (1991) Relationship between maternal thyroxine levels during pregnancy and memory function in childhood. Early Hum Dev 25:43-51.
73. Pulver AE, Liang KY, Brown GH, Wolyniec P, McGrath J, Adler L, Tam D, Carpenter WT, Childs B (1992) Risk factors in schizophrenia: Season of birth, gender, and familial risk. Br J Psychiatry 160:65-71.
74. Rakic P (1988) Defects of neuronal migration and the pathogenesis of cortical malformations. In GJ Boer, MGP Feenstra, M Mirmiran, DF Swaab, F Van Haaren (Eds), Progress in brain research (Vol 73, pp. 15-37). Amsterdam: Elsevier Science Publishers B.V.
75. Richardson Andrews RC (1990a) Unification of the findings in schizophrenia by reference to the effects of gestational zinc deficiency. Med Hypotheses 31:141-153.
76. Richardson Andrews RC (1990b) Obstetric complications and schizophrenia (Letter). Lancet V336:122-123.
77. Richardson Andrews RC (1992) An update of the zinc deficiency theory of schizophrenia. Identification of the sex determining system as the site of action of reproductive zinc deficiency. Med Hypotheses 38:284-291.
78. Richardson Andrews RC (1992b) Diabetes and schizophrenia: Genes or zinc deficiency? Lancet V340:1160.
79. Robins LN, Mills JL (1993) Effects of in utero exposure to street drugs. Am J Public Health 83(suppl):8-32.
80. Rosso PR (1990) Prenatal nutrition and brain growth. In NM van Gelder, RF Butterworth, BD Drujan (Eds), (Mal)Nutrition and the infant brain (pp. 25-40). New York: Wiley-Liss.
81. Saykin AJ, Shtasel DL, Gur RE, Kester DB, Mozley LH, Stafiniak P, Gur RC (1994) Neuropsychological deficits in neuroleptic naive patients with first episode schizophrenia. Arch Gen Psychiatry 51:124-131.
82. Schorah CJ, Smithells RW, Scott J (1980) Vitamin B12 and anencephaly. Lancet 1:880.
83. Scott JM, Weir DG, Molloy A, McPartlin J, Daly L, Kirke P (1994) Folic acid metabolism and mechanisms of neural tube defects (pp. 180-191). West Sussex, England: John Wiley and Sons.
84. Smithells RW, Seller MJ, Harris R (1983) Further experience of vitamin supplementation for prevention of neural tube defect recurrences. Lancet 1:1027-1031.
85. Smithells RW, Sheppard S, Schorah CJ (1976) Vitamin deficiencies and neural tube defects. Arch Dis Child 51:944-950.
86. Stein Z, Susser M, Saenger G, Marolla F (1975) Famine and human development: The Dutch hunger winter of 1944-45 (pp. 119-148). New York: Oxford University Press.
87. Streissguth AP, Aase JM, Clarren SK, Randels SP, LaDu, RA, Smith DF (1991) Fetal alcohol syndrome in adolescents and adults. JAMA 265:1961-1967.
88. Susser ES, Lin SP (1992) Schizophrenia after prenatal exposure to the Dutch hunger winter of 1944-45. Arch Gen Psychiatry 49:983-988.
89. Susser E, Neugebauer R, Hoek HW, Brown AS, Lin S, Labovitz D, Gorman JM (in press) Schizophrenia after prenatal famine: Further evidence. Arch Gen Psychiatry.
90. Tune LE, Wong DF, Pearlson G, Strauss M, Young T, Shaya EK, Dannals RF, Wilson AA, Ravert HT, Sapp J, Cooper T, Chase GA, Wagner HN (1993) Dopamine D2 receptor density estimates in schizophrenia: A positron emission tomography study with 11-C-N-methylspiperone. Psychiatry Res 49:219-237.
91. Waddington JL (1993a) Schizophrenia: Developmental neuroscience and pathobiology. Lancet 341:531-536.
92. Waddington JL (1993b) Neurodynamics of abnormalities in cerebral metabolism and structure in schizophrenia. Schizophr Bull 19:55-69.
93. Watson Duff EM, Cooper ES (1994) Neural tube defects in Jamaica following Hurricane Gilbert. Am J Public Health 84: 473-475.
94. Whitley RJ, Stagno S (1991) Perinatal viral infections. In WM Scheid, RJ Whitley, DT Durack (Eds), Infections of the central nervous system. New York: Raven.
95. Wiggins RC, Fuller G, Enna SJ (1984) Undernutrition and the development of brain neurotransmitter systems. Life Sci 35: 2085-2094.
96. Wong DF, Wagner HN Jr, Tune LE, Dannals RF, Pearlson GD, Links JM, Tamminga CA, Broussolle EP, Ravert HT, Wilson AA, Toung TJK, Malat J, Williams JA, O'Tuama LA, Snyder SH, Duhar MJ, Gjedde A (1986) Positron emission tomography reveals elevated D2 receptors in drug-naive schizophrenics. Science 234:1558-1563.
97. World Health Organization (1990) Report to the 43rd world health assembly. Geneva, Switzerland.
98. Yates JRW, Ferguson-Smith MA, Shenkin A, Guzman-Rodriguez R, White M, Clark BJ (1987) Is disordered folate metabolism the basis for the genetic predisposition to neural tube defects. Clin Genet 31:279-287.