Prenatal infectious and nutritional factors and risk of adult schizophrenia

Expert Review of Neurotherapeutics

Volumn 7, Issue 7, 2007, Pages 797-805

  Penner, Justin D ^c   Brown, Alan S ^a,b  

^a New York State Psychiatric Institute ^*  (United States)

^b Columbia University ^*  (United States)

^c NEW YORK STATE PSYCHIATRIC INSTITUTE   (United States)

Author keywords

Epidemiology; Gene environment interaction; Infection; Nutrition; Pregnancy complications; Prenatal risk factors; Schizophrenia

Indexed keywords

CYTOKINE; HOMOCYSTEINE;

BRAIN MALFORMATION; DISEASE PREDISPOSITION; ENVIRONMENTAL EXPOSURE; GENE INTERACTION; GENITAL TRACT INFECTION; HUMAN; INFLUENZA; INTRAUTERINE INFECTION; MATERNAL NUTRITION; NUTRITION; PATHOGENESIS; REVIEW; RISK FACTOR; RUBELLA; SCHIZOPHRENIA; TOXOPLASMOSIS;

ADULT; FEMALE; FETAL DISEASES; HUMANS; INFECTION; NUTRITION DISORDERS; PREGNANCY; RISK FACTORS; SCHIZOPHRENIA;

EID: 34447133469     PISSN: 14737175     EISSN: 17448360     Source Type: Journal    
DOI: 10.1586/14737175.7.7.797     Document Type: Review

References (83)

1. Eaton WW. Evidence for universality and uniformity of schizophrenia around the world: assessment and implications. In: Search for the Causes of Schizophrenia (IV). Gattaz WF, Hafner H (Eds). Springer-Verlag, Berlin, Germany 21-33 (1999).
2. McGuffin P, Owen MJ, Farmer AE. Genetic basis of schizophrenia. Lancet 346(8976), 678-682 (1995).
3. Davis JO, Phelps JA, Bracha HS. Prenatal development of monozygotic twins and concordance for schizophrenia. Schizophr. Bull. 21(3), 357-366 (1995).
4. Bradbury TN, Miller GA. Season of birth in schizophrenia: a review of evidence, methodology, and etiology. Psychol. Bull. 98(3), 569-594 (1985).
5. Mortensen PB, Pedersen CB, Westergaard T et al. Effects of family history and place and season of birth on the risk of schizophrenia. N. Engl. J. Med. 340(8), 603-608 (1999).
6. Pedersen CB, Mortensen PB. Evidence of a dose-response relationship between urbanicity during upbringing and schizophrenia risk. Arch. Gen. Psychiatry 58 (11), 1039-1046 (2001).
7. Van Os J, Pedersen CB, Mortensen PB. Confirmation of synergy between urbanicity and familial liability in the causation of psychosis. Am. J. Psychiatry 161(12), 2312-2314 (2004).
8. Krabbendam L, van Os J. Schizophrenia and urbanicity: a major environmental influence - conditional on genetic risk. Schizophr. Bull. 31(4), 795-799 (2005).
9. Cantor-Graae E, Selten JP. Schizophrenia and migration: a meta-analysis and review. Am. J. Psychiatry 162(1), 12-24 (2005).
10. Selten JP, Veen N, Feller W et al. Incidence of psychotic disorders in immigrant groups to The Netherlands. Br. J. Psychiatry 178, 367-372 (2001).
11. Brown AS. New perspectives on the neurodevelopmental hypothesis of schizophrenia. Psychiatr. Ann. 29(3), 128-130 (1999).
12. Brown AS, Cohen P, Greenwald S, Susser E. Nonaffective psychosis after prenatal exposure to rubella. Am. J. Psychiatry 157(3), 438-443 (2000).
13. Brown AS, Cohen P, Harkavy-Friedman J et al. A.E. Bennett Research Award. Prenatal rubella, premorbid abnormalities, and adult schizophrenia. Biol. Psychiatry 49(6), 473-486 (2001).
14. Chess S, Korn S, Fernandez P. Psychiatric Disorders of Children with Congenital Rubella. Brunner/Mazel, NY, USA (1971).
15. Chess S. Follow-up report on autism in congenital rubella. J. Autism Child Schizophr. 7(1), 69-81 (1977).
16. Nurnberger JI Jr, Blehar MC, Kaufmann CA et al. Diagnostic interview for genetic studies. Rationale, unique features, and training. NIMH Genetics Initiative. Arch. Gen. Psychiatry 51(11), 849-859 (1994).
17. Eaton WW. Epidemiology of schizophrenia. Epidemiol. Rev. 7, 105-126 (1985).
18. Kendler KS, MacLean CJ, O'Neill FA et al. Evidence for a schizophrenia vulnerability locus on chromosome 8p in the Irish Study of High-Density Schizophrenia Families. Am. J. Psychiatry 153(12), 1534-1540 (1996).
19. Brown AS. Serologic studies of prenatal infection and schizophrenia. In: Neuropsychiatric Disorders and Infection. Fatemi SH (Ed.). Martin Dunitz-Taylor & Francis Group, London, UK 43-50 (2005).
20. Brown AS. Prenatal infection and adult schizophrenia: a review and synthesis. Int. J. Ment. Health 29, 22-37 (2001).
21. Brown AS, Begg MD, Gravenstein S et al. Serologic evidence for prenatal influenza in the etiology of schizophrenia. Arch. Gen. Psychiatry 61, 774-780 (2004).
22. van den Berg BJ. The California Child Health and Development Studies: twenty years of research. World Health Stat. Q. 32(4), 269-286 (1979).
23. van den Berg BJ. The California Child Health and Development Studies. In: Handbook of Longitudinal Research. Mednick SA, Harway M, Finello K (Eds). Praeger, NY, USA 166-179 (1984).
24. Susser ES, Schaefer CA, Brown AS, Begg MD, Wyatt RJ. The design of the Prenatal Determinants of Schizophrenia Study. Schizophr. Bull. 26(2), 257-273 (2000).
25. Remington JS, McLeod R, Thulliez P, Desmonts G. Toxoplasmosis. In: Infectious Diseases of the Fetus & Newborn Infant. Remington JS, Klein JO (Eds). WB Saunders Co., PA, USA 205-346 (2001).
26. Dukes C, Luft B, Durack D. Toxoplasmosis. In: Infections of the Central Nervous System. Scheld WM, Whitley RJ, Durack DT (Eds). Lippincott-Raven, PA, USA, 785-806 (1997).
27. Brown AS, Schaefer CA, Quesenberry CP Jr, Liu L, Babulas VP, Susser ES. Maternal exposure to toxoplasmosis and risk of schizophrenia in adult offspring. Am. J. Psychiatry 162 (4), 767-773 (2005).
28. Corey L, Whitley RJ, Stone EF, Mohan K. Difference between herpes simplex virus type 1 and type 2 neonatal encephalitis in neurological outcome. Lancet 1(8575-8576), 1-4 (1988).
29. Ingall D, Sanchez PJ. Syphilis. In: Infectious Diseases of the Fetus & Newborn Infant. Remington JS, Klein JO (Eds). WB Saunders Co., PA, USA 652 (1995).
30. Babulas V, Factor-Litvak P, Goetz R, Schaefer CA, Brown AS. Prenatal exposure to maternal genital and reproductive infections and adult schizophrenia. Am. J. Psychiatry 163(5), 927-929 (2006).
31. Weizman R, Bessler H. Cytokines: stress and immunity. In: Cytokines: Stress and Immunity. Plotnikoff NP, Faith RE, Murgo AJ, Good RA (Eds). CRC Press, FL, USA 1-15 (1999).
32. Shimoya K, Matsuzaki N, Taniguchi T, Okada T, Saji F, Murata Y. Interleukin-8 level in maternal serum as a marker for screening of histological chorioamnionitis at term. Int. J. Gynaecol. Obstet. 57(2), 153-159 (1997).
33. Gilmore JH, Jarskog LF. Exposure to infection and brain development: cytokines in the pathogenesis of schizophrenia. Schizophr. Res. 24(3), 365-367 (1997).
34. Brown AS, Hooton J, Schaefer CA et al. Elevated maternal interleukin-8 levels and risk of schizophrenia in adult offspring. Am. J. Psychiatry 161(5), 889-895 (2004).
35. Harker LA, Ross R, Slichter SJ, Scott CR. Homocystine-induced arteriosclerosis: the role of endothelial cell injury and platelet response in its genesis. J. Clin. Invest. 58(3), 731-741 (1976).
36. Nelen WL, Bulten J, Steegers EA, Blom HJ, Hanselaar AG, Eskes TK. Maternal homocysteine and chorionic vascularization in recurrent early pregnancy loss. Hum. Reprod. 15(4), 954-960 (2000).
37. Holmes VA. Changes in haemostasis during normal pregnancy: does homocysteine play a role in maintaining homeostasis? Proc. Nutr. Soc. 62(2), 479-493 (2003).
38. Starkebaum G, Harlan JM. Endothelial-cell injury due to copper-catalyzed hydrogen-peroxide generation from homocysteine. J. Clin. Invest. 77(4), 1370-1376 (1986).
39. Parnetti L, Bottiglieri T, Lowenthal D. Role of homocysteine in age-related vascular and non-vascular diseases. Aging. Clin. Exp. Res. 9(4), 241-257 (1997).
40. di Simone N, Riccardi P, Maggiano N et al. Effect of folic acid on homocysteine-induced trophoblast apoptosis. Mol. Hum. Reprod. 10(9), 665-669 (2004).
41. Murphy MM, Scott JM, Arija V, Molloy AM, Fernandez-Ballart JD. Maternal homocysteine before conception and throughout pregnancy predicts fetal homocysteine and birth weight. Clin. Chem. 50(8), 1406-1412 (2004).
42. Baschat AA. Fetal responses to placental insufficiency: an update. BJOG 111 (10), 1031-1041 (2004).
43. Lipton SA, Kim WK, Choi YB et al. Neurotoxicity associated with dual actions of homocysteine at the N-methyl-D-aspartate receptor. Proc. Natl Acad. Sci. USA 94(11), 5923-5928 (1997).
44. Coyle JT, Tsai GC. NMDA receptor function, neuroplasticity, and the pathophysiology of schizophrenia. Disorders of synaptic plasticity and schizophrenia. Int. Rev. Neurobiol. 59, 491-515 (2004).
45. Javitt DC, Steinschneider M, Schroeder CE, Arezzo JC. Role of cortical N-methyl-D-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. Proc. Natl Acad. Sci. USA. 93(21), 11962-11967 (1996).
46. Brown AS, Bottiglieri T, Schaefer CA et al. Elevated prenatal homocysteine levels as a risk factor for schizophrenia. Arch. Gen. Psychiatry 64(1), 31-39 (2007).
47. Whitley RJ, Stagno S. Perinatal infections. In: Infections of the Central Nervous System. Scheld WM, Whitley RJ, Durack DT (Eds). Lippincott-Raven, PA, USA 223-253 (1997).
48. Boue JG, Boue A. Effects of rubella virus infection on the division of human cells. Am. J. Dis. Child. 118(1), 45-48 (1969).
49. Rorke LB. Nervous system lesions in the congenital rubella syndrome. Arch. Otolaryngol. 98(4), 249-251 (1973).
50. Kemper TL, Lecours AR, Gates MJ, Yakovlev PI. Retardation of the myelo- and cytoarchitectonic maturation of the brain in the congenital rubella syndrome. Res. Publ. Assoc. Res. Nerv. Ment. Dis. 51, 23-62 (1973).
51. Townsend JJ. Rubella virus disease. In: Handbook of Neurovirology. McKendall RR, Stropp WG (Eds). Marcel Dekker, NY, USA 603-611 (1994).
52. Frenkel JK, Nelson BM, Ariasstella J. Immunosuppression and toxoplasmic encephalitis - clinical and experimental aspects. Hum. Path. 6(1), 97-111 (1975).
53. DeLisi LE. Is there a viral or immune dysfunction etiology to schizophrenia? Re-evaluation a decade later. Schizophr. Res. 22(1), 1-4 (1996).
54. Wright P, Takei N, Murray RM, Sham PC. Seasonality, prenatal influenza exposure, and schizophrenia. In: Prenatal Exposures in Schizophrenia. Susser ES, Brown AS, Gorman JM (Eds). American Psychiatric Press, Inc., DC, USA 89-112 (1999).
55. Atta-ur-Rahman, Harvey K, Siddiqui RA. Interleukin-8: an autocrine inflammatory mediator. Curr. Pharm. Des. 5(4), 241-253 (1999).
56. Mukaida N. The roles of cytokine receptors in diseases. Rinsho Byori 48(5), 409-415 (2000).
57. Detmers PA, Lo SK, Olsen-Egbert E, Walz A, Baggiolini M, Cohn ZA. Neutrophil activating protein 1/interleukin-8 stimulates the binding activity of the leukocyte adhesion receptor CD11b/CD18 on human neutrophils. J. Exp. Med. 171(4), 1155-1162 (1990).
58. Huber AR, Kunkel SL, Todd RF III, Weiss SJ. Regulation of transendothelial neutrophil migration by endogenous interleukin-8. Science 254(5028), 99-102 (1991).
59. Brown AS, Susser E. Plausibility of prenatal rubella, influenza, and other viral infections as risk factors for schizophrenia. In: Prenatal Exposures in Schizophrenia. Susser ES, Brown AS, Gorman JM (Eds). American Psychiatric Press, Inc., DC, USA 113-131 (1999).
60. Koenig JI, Kirkpatrick B, Lee P. Glucocorticoid hormones and early brain development in schizophrenia. Neuropsychopharmacology 27(2), 309-318 (2002).
61. Brown AS, Susser ES, Butler PD, Richardson AR, Kaufmann CA, Gorman JM. Neurobiological plausibility of prenatal nutritional deprivation as a risk factor for schizophrenia. J. Nerv. Ment. Dis. 184(2), 71-85 (1996).
62. Graham I. Homocysteine Metabolism: From Basic Science to Clinical Medicine. Kluwer Academic Publishers, MA, USA (1997).
63. Lewis CA, Pancharuniti N, Sauberlich HE. Plasma folate adequacy as determined by homocysteine level. Ann. NY Acad. Sci. 669, 360-362 (1992).
64. Goff DC, Coyle JT. The emerging role of glutamate in the pathophysiology and treatment of schizophrenia. Am. J. Psychiatry 158(9), 1367-1377 (2001).
65. McGrath J. Hypothesis: is low prenatal vitamin D a risk-modifying factor for schizophrenia? Schizophr. Res. 40(3), 173-177 (1999).
66. McGrath J, Eyles D, Mowry B et al. Low maternal vitamin D as a risk factor for schizophrenia: a pilot study using banked sera. Schizophr. Res. 63(1-2), 73-78 (2003).
67. MacKay-Sim A, Feron F, Eyles D, Burne T, McGrath J. Schizophrenia, vitamin D, and brain development. Int. Rev. Neurobiol. 59, 351-380 (2004).
68. Anton ES, Marchionni MA, Lee KF, Rakic P. Role of GGF/neuregulin signaling in interactions between migrating neurons and radial glia in the developing cerebral cortex. Development 124(18), 3501-3510 (1997).
69. Kamiya A, Kubo K, Tomoda T et al. A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development. Nat. Cell Biol. 7(12), 1167-1178 (2005).
70. Lencz T, Morgan TV, Athanasiou M et al. Converging evidence for a pseudoautosomal cytokine receptor gene locus in schizophrenia. Mol. Psychiatry 12(6), 572-580 (2007).
71. Tan EC, Chong SA, Lim LC et al. Genetic analysis of the thermolabile methylenetetrahydrofolate reductase variant in schizophrenia and mood disorders. Psychiatr. Genet. 14(4), 227-231 (2004).
72. Virgos C, Martorell L, Simo JM et al. Plasma homocysteine and the methylenetetrahydrofolate reductase C677T gene variant: lack of association with schizophrenia. Neuroreport 10(10), 2035-2038 (1999).
73. Shi L, Fatemi SH, Sidwell RW, Patterson PH. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J. Neurosci. 23(1), 297-302 (2003).
74. Fatemi SH, Emamian ES, Kist D et al. Defective corticogenesis and reduction in reelin immunoreactivity in cortex and hippocampus of prenatally infected neonatal mice. Mol. Psychiatry 4(2), 145-154 (1999).
75. Zuckerman L, Rehavi M, Nachman R, Weiner I. Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: a novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology 28(10), 1778-1789 (2003).
76. Centers for Disease Control and Prevention. CDC Recommendations Regarding Selected Conditions Affecting Women's Health, 49 No. RR-2. Centers for Disease Control and Prevention, GA, USA 57-75 (2000).
77. Amminger GP, Berger GE, Schafer MF et al. Omega-3 fatty acids supplementation in children withautism: a double-blind randomized, placebo-controlled pilot study. Biol. Psychiatry 61(4), 551-553 (2007).
78. Brown AS, Schaefer CA, Wyatt RJ et al. Maternal exposure to respiratory infections and adult schizophrenia spectrum disorders: a prospective birth cohort study. Schizophr. Bull. 26(2), 287-295 (2000).
79. Mortensen PB, Norgaard-Pedersen B, Waltoft BL et al. Toxoplasma gondii as a risk factor for early-onset schizophrenia: analysis of filter paper blood samples obtained at birth. Biol. Psychiatry 61(5), 688-693 (2007).
80. Buka SL, Tsuang MT, Torrey EF, Klebanoff MA, Bernstein D, Yolken RH. Maternal infections and subsequent psychosis among offspring. Arch. Gen. Psychiatry 58(11), 1032-1037 (2001).
81. Susser E, Neugebauer R, Hoek HW et al. Schizophrenia after prenatal famine. Further evidence. Arch. Gen. Psychiatry 53(1), 25-31 (1996).
82. St Clair D, Xu M, Wang P et al. Rates of adult schizophrenia following prenatal exposure to the Chinese famine of 1959-1961. JAMA 294(5), 557-562 (2005).
83. Schaefer CA, Brown AS, Wyatt RJ et al. Maternal prepregnant body mass and risk of schizophrenia in adult offspring. Schizophr. Bull. 26(2), 275-286 (2000).