Hostname: page-component-8448b6f56d-42gr6 Total loading time: 0 Render date: 2024-04-18T19:59:56.529Z Has data issue: false hasContentIssue false
  • English
  • Français

Prenatal maternal infection, neurodevelopment and adult schizophrenia: a systematic review of population-based studies

Published online by Cambridge University Press:  16 April 2012

G. M. Khandaker ,
J. Zimbron ,
G. Lewis  and
P. B. Jones
G. M. Khandaker*
Affiliation:
Department of Psychiatry, University of Cambridge, UK Cambridgeshire and Peterborough NHS Foundation Trust, Cambridge, UK
J. Zimbron
Affiliation:
Department of Psychiatry, University of Cambridge, UK Cambridgeshire and Peterborough NHS Foundation Trust, Cambridge, UK
G. Lewis
Affiliation:
Academic Unit of Psychiatry, University of Bristol, UK
P. B. Jones
Affiliation:
Department of Psychiatry, University of Cambridge, UK Cambridgeshire and Peterborough NHS Foundation Trust, Cambridge, UK
*
*Address for correspondence: Dr G. M. Khandaker, Department of Psychiatry, University of Cambridge, Box 189, Addenbrooke's Hospital, Cambridge CB2 2QQ, UK. (Email: gmk24@medschl.cam.ac.uk)
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

Disruption of foetal development by prenatal maternal infection is consistent with a neurodevelopmental model of schizophrenia. Whether specific prenatal infections are involved, their timing and the mechanisms of any effect are all unknown. We addressed these questions through a systematic review of population-based studies.

Method

Electronic and manual searches and rigorous quality assessment yielded 21 studies that included an objective assessment of individual-level prenatal maternal infection and standardized psychotic diagnoses in adult offspring. Methodological differences between studies necessitated a descriptive review.

Results

Results for prenatal maternal non-specific bacterial, respiratory or genital and reproductive infection differed between studies, which reported up to a two- to fivefold increased risk of schizophrenia. Evidence for herpes simplex virus type 2 (HSV-2) and Toxoplasma gondii was mixed; some studies reported up to a doubling of schizophrenia risk. Prenatal HSV-1 or cytomegalovirus (CMV) infections were not associated with increased risk. Exposure to influenza or other infections during early pregnancy may be more harmful than later exposure. Increased proinflammatory cytokines during pregnancy were also associated with risk. Prenatal infection was associated with structural and functional brain abnormalities relevant to schizophrenia.

Conclusions

Prenatal exposure to a range of infections and inflammatory responses may be associated with risk of adult schizophrenia. Larger samples, mediation and animal models should be used to investigate whether there is a ‘sensitive period’ during development, and the effects of prenatal infections on neurodevelopment. Inclusion of genetic and immunological information should help to elucidate to what extent genetic vulnerability to schizophrenia may be explained by vulnerability to infection.

Keywords

Cytokinesinfectionneurodevelopmentpregnancyschizophrenia
Type
Review Article
Information
Psychological Medicine , Volume 43 , Issue 2 , February 2013 , pp. 239 - 257
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Albert, LJ, Inman, RD (1999). Molecular mimicry and autoimmunity. New England Journal of Medicine 341, 2068–2074.CrossRefGoogle ScholarPubMed
Babulas, V, Factor-Litvak, P, Goetz, R, Schaefer, CA, Brown, AS (2006). Prenatal exposure to maternal genital and reproductive infections and adult schizophrenia. American Journal of Psychiatry 163, 927–929.CrossRefGoogle ScholarPubMed
Barker, DJ, Gluckman, PD, Godfrey, KM, Harding, JE, Owens, JA, Robinson, JS (1993). Fetal nutrition and cardiovascular disease in adult life. Lancet 341, 938–941.CrossRefGoogle ScholarPubMed
Bocchio Chiavetto, L, Boin, F, Zanardini, R, Popoli, M, Michelato, A, Bignotti, S, Tura, GB, Gennarelli, M (2002). Association between promoter polymorphic haplotypes of interleukin-10 gene and schizophrenia. Biological Psychiatry 51, 480–484.CrossRefGoogle ScholarPubMed
Bradley, AJ, Dinan, TG (2010). A systematic review of hypothalamic-pituitary-adrenal axis function in schizophrenia: implications for mortality. Journal of Psychopharmacology 24, 91–118.CrossRefGoogle ScholarPubMed
Brown, AS, Begg, MD, Gravenstein, S, Schaefer, CA, Wyatt, RJ, Bresnahan, M, Babulas, VP, Susser, ES (2004 a). Serologic evidence of prenatal influenza in the etiology of schizophrenia. Archives of General Psychiatry 61, 774–780.CrossRefGoogle ScholarPubMed
Brown, AS, Cohen, P, Harkavy-Friedman, J, Babulas, V, Malaspina, D, Gorman, JM, Susser, ES (2001). A.E. Bennett Research Award. Prenatal rubella, premorbid abnormalities, and adult schizophrenia. Biological Psychiatry 49, 473–486.CrossRefGoogle ScholarPubMed
Brown, AS, Deicken, RF, Vinogradov, S, Kremen, WS, Poole, JH, Penner, JD, Kochetkova, A, Kern, D, Schaefer, CA (2009 a). Prenatal infection and cavum septum pellucidum in adult schizophrenia. Schizophrenia Research 108, 285–287.CrossRefGoogle ScholarPubMed
Brown, AS, Derkits, EJ (2010). Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. American Journal of Psychiatry 167, 261–280.CrossRefGoogle ScholarPubMed
Brown, AS, Hooton, J, Schaefer, CA, Zhang, H, Petkova, E, Babulas, V, Perrin, M, Gorman, JM, Susser, ES (2004 b). Elevated maternal interleukin-8 levels and risk of schizophrenia in adult offspring. American Journal of Psychiatry 161, 889–895.CrossRefGoogle ScholarPubMed
Brown, AS, Schaefer, CA, Quesenberry, Jr. CP, Liu, L, Babulas, VP, Susser, ES (2005). Maternal exposure to toxoplasmosis and risk of schizophrenia in adult offspring. American Journal of Psychiatry 162, 767–773.CrossRefGoogle ScholarPubMed
Brown, AS, Schaefer, CA, Quesenberry, Jr. CP, Shen, L, Susser, ES (2006). No evidence of relation between maternal exposure to herpes simplex virus type 2 and risk of schizophrenia? American Journal of Psychiatry 163, 2178–2180.CrossRefGoogle ScholarPubMed
Brown, AS, Schaefer, CA, Wyatt, RJ, Goetz, R, Begg, MD, Gorman, JM, Susser, ES (2000). Maternal exposure to respiratory infections and adult schizophrenia spectrum disorders: a prospective birth cohort study. Schizophrenia Bulletin 26, 287–195.CrossRefGoogle ScholarPubMed
Brown, AS, Vinogradov, S, Kremen, WS, Poole, JH, Bao, Y, Kern, D, McKeague, IW (2011). Association of maternal genital and reproductive infections with verbal memory and motor deficits in adult schizophrenia. Psychiatry Research 188, 179–186.CrossRefGoogle ScholarPubMed
Brown, AS, Vinogradov, S, Kremen, WS, Poole, JH, Deicken, RF, Penner, JD, McKeague, IW, Kochetkova, A, Kern, D, Schaefer, CA (2009 b). Prenatal exposure to maternal infection and executive dysfunction in adult schizophrenia. American Journal of Psychiatry 166, 683–690.CrossRefGoogle ScholarPubMed
Buka, SL, Cannon, TD, Torrey, EF, Yolken, RH (2008). Maternal exposure to herpes simplex virus and risk of psychosis among adult offspring. Biological Psychiatry 63, 809–815.CrossRefGoogle ScholarPubMed
Buka, SL, Tsuang, MT, Torrey, EF, Klebanoff, MA, Bernstein, D, Yolken, RH (2001 a). Maternal infections and subsequent psychosis among offspring. Archives of General Psychiatry 58, 1032–1037.CrossRefGoogle ScholarPubMed
Buka, SL, Tsuang, MT, Torrey, EF, Klebanoff, MA, Wagner, RL, Yolken, RH (2001 b). Maternal cytokine levels during pregnancy and adult psychosis. Brain Behaviour and Immunity 15, 411–420.CrossRefGoogle ScholarPubMed
Bushe, C, Holt, R (2004). Prevalence of diabetes and impaired glucose tolerance in patients with schizophrenia. British Journal of Psychiatry 184 (Suppl. 47), S67–S71.CrossRefGoogle Scholar
Cannon, M, Jones, PB, Murray, RM (2002). Obstetric complications and schizophrenia: historical and meta-analytic review. American Journal of Psychiatry 159, 1080–1092.CrossRefGoogle ScholarPubMed
Clarke, MC, Tanskanen, A, Huttunen, M, Whittaker, JC, Cannon, M (2009). Evidence for an interaction between familial liability and prenatal exposure to infection in the causation of schizophrenia. American Journal of Psychiatry 166, 1025–1030.CrossRefGoogle ScholarPubMed
Curkendall, SM, Mo, J, Glasser, DB, Rose Stang, M, Jones, JK (2004). Cardiovascular disease in patients with schizophrenia in Saskatchewan, Canada. Journal of Clinical Psychiatry 65, 715–720.CrossRefGoogle ScholarPubMed
Dalmau, J, Lancaster, E, Martinez-Hernandez, E, Rosenfeld, MR, Balice-Gordon, R (2011). Clinical experience and laboratory investigations in patients with anti-NMDAR encephalitis. Lancet Neurology 10, 63–74.CrossRefGoogle ScholarPubMed
Dalton, P, Deacon, R, Blamire, A, Pike, M, McKinlay, I, Stein, J, Styles, P, Vincent, A (2003). Maternal neuronal antibodies associated with autism and a language disorder. Annals of Neurology 53, 533–537.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Edwards, MJ (1968). Congenital malformations in the rat following induced hyperthermia during gestation. Teratology 1, 173–177.CrossRefGoogle ScholarPubMed
Ellman, LM, Deicken, RF, Vinogradov, S, Kremen, WS, Poole, JH, Kern, DM, Tsai, WY, Schaefer, CA, Brown, AS (2010). Structural brain alterations in schizophrenia following fetal exposure to the inflammatory cytokine interleukin-8. Schizophrenia Research 121, 46–54.CrossRefGoogle Scholar
Ellman, LM, Yolken, RH, Buka, SL, Torrey, EF, Cannon, TD (2009). Cognitive functioning prior to the onset of psychosis: the role of fetal exposure to serologically determined influenza infection. Biological Psychiatry 65, 1040–1047.CrossRefGoogle Scholar
Garver, DL, Tamas, RL, Holcomb, JA (2003). Elevated interleukin-6 in the cerebrospinal fluid of a previously delineated schizophrenia subtype. Neuropsychopharmacology 28, 1515–1520.CrossRefGoogle ScholarPubMed
Golding, J, Pembrey, M, Jones, R (2001). ALSPAC – the Avon Longitudinal Study of Parents and Children. I. Study methodology. Paediatric and Perinatal Epidemiology 15, 74–87.CrossRefGoogle ScholarPubMed
Gottesman, II, Shields, J (1982). Schizophrenia: The Epigenetic Puzzle. Cambridge University Press: New York.Google Scholar
Gunawardana, L, Zammit, S, Lewis, G, Gunnell, D, Hollis, C, Wolke, D, Harrison, G (2011). Examining the association between maternal analgesic use during pregnancy and risk of psychotic symptoms during adolescence. Schizophrenia Research 126, 220–225.CrossRefGoogle ScholarPubMed
Hurme, M, Haanpaa, M, Nurmikko, T, Wang, XY, Virta, M, Pessi, T, Kilpinen, S, Hulkkonen, J, Helminen, M (2003). IL-10 gene polymorphism and herpesvirus infections. Journal of Medical Virology 70 (Suppl. 1), S48–S50.CrossRefGoogle ScholarPubMed
Janeway, CA, Travers, P, Walport, M, Shlomchik, MJ (2001). Immunobiology: The Immune System in Health and Disease. Garland Science: New York.Google Scholar
Johnstone, JF, Bocking, AD, Unlugedik, E, Challis, JR (2005). The effects of chorioamnionitis and betamethasone on 11beta hydroxysteroid dehydrogenase types 1 and 2 and the glucocorticoid receptor in preterm human placenta. Journal of the Society for Gynecologic Investigation 12, 238–245.CrossRefGoogle ScholarPubMed
Jones, P, Rodgers, B, Murray, R, Marmot, M (1994). Child development risk factors for adult schizophrenia in the British 1946 birth cohort. Lancet 344, 1398–1402.CrossRefGoogle ScholarPubMed
Khandaker, GM, Barnett, JH, White, IR, Jones, PB (2011). A quantitative meta-analysis of population-based studies of premorbid intelligence and schizophrenia. Schizophrenia Research 132, 220–227.CrossRefGoogle ScholarPubMed
Lencz, T, Morgan, TV, Athanasiou, M, Dain, B, Reed, CR, Kane, JM, Kucherlapati, R, Malhotra, AK (2007). Converging evidence for a pseudoautosomal cytokine receptor gene locus in schizophrenia. Molecular Psychiatry 12, 572–580.CrossRefGoogle ScholarPubMed
Magnus, P, Irgens, LM, Haug, K, Nystad, W, Skjaerven, R, Stoltenberg, C (2006). Cohort profile: the Norwegian Mother and Child Cohort Study (MoBa). International Journal of Epidemiology 35, 1146–1150.CrossRefGoogle ScholarPubMed
Mednick, SA, Machon, RA, Huttunen, MO, Bonett, D (1988). Adult schizophrenia following prenatal exposure to an influenza epidemic. Archives of General Psychiatry 45, 189–192.CrossRefGoogle Scholar
Menninger, KA (1994). Influenza and schizophrenia. An analysis of post-influenzal ‘dementia precox,’ as of 1918, and five years later further studies of the psychiatric aspects of influenza. 1926. American Journal of Psychiatry 151, 182–187.Google ScholarPubMed
Meyer, U, Feldon, J (2009). Prenatal exposure to infection: a primary mechanism for abnormal dopaminergic development in schizophrenia. Psychopharmacology (Berlin) 206, 587–602.CrossRefGoogle ScholarPubMed
Meyer, U, Feldon, J (2010). Epidemiology-driven neurodevelopmental animal models of schizophrenia. Progress in Neurobiology 90, 285–326.CrossRefGoogle ScholarPubMed
Meyer, U, Feldon, J, Yee, BK (2009). A review of the fetal brain cytokine imbalance hypothesis of schizophrenia. Schizophrenia Bulletin 35, 959–972.CrossRefGoogle ScholarPubMed
Milunsky, A, Ulcickas, M, Rothman, KJ, Willett, W, Jick, SS, Jick, H (1992). Maternal heat exposure and neural tube defects. Journal of the American Medical Association 268, 882–885.CrossRefGoogle ScholarPubMed
Mortensen, PB, Norgaard-Pedersen, B, Waltoft, BL, Sorensen, TL, Hougaard, D, Torrey, EF, Yolken, RH (2007). Toxoplasma gondii as a risk factor for early-onset schizophrenia: analysis of filter paper blood samples obtained at birth. Biological Psychiatry 61, 688–693.CrossRefGoogle ScholarPubMed
Mortensen, PB, Pedersen, CB, Hougaard, DM, Norgaard-Petersen, B, Mors, O, Borglum, AD, Yolken, RH (2010). A Danish National Birth Cohort study of maternal HSV-2 antibodies as a risk factor for schizophrenia in their offspring. Schizophrenia Research 122, 257–263.CrossRefGoogle ScholarPubMed
Murray, RM, Lewis, SW (1987). Is schizophrenia a neurodevelopmental disorder? British Medical Journa (Clinical Research Edition) 295, 681–682.CrossRefGoogle ScholarPubMed
Nielsen, PR, Laursen, TM, Mortensen, PB (2011). Association between parental hospital-treated infection and the risk of schizophrenia in adolescence and early adulthood. Schizophrenia Bulletin. Published online 20 October 2011. doi:10.1093/schbul/sbr149.Google ScholarPubMed
Olsen, J, Melbye, M, Olsen, SF, Sorensen, TI, Aaby, P, Andersen, AM, Taxbol, D, Hansen, KD, Juhl, M, Schow, TB, Sorensen, HT, Andresen, J, Mortensen, EL, Olesen, AW, Sondergaard, C (2001). The Danish National Birth Cohort – its background, structure and aim. Scandinavian Journal of Public Health 29, 300–307.CrossRefGoogle ScholarPubMed
Owen, D, Andrews, MH, Matthews, SG (2005). Maternal adversity, glucocorticoids and programming of neuroendocrine function and behaviour. Neuroscience and Biobehavioural Reviews 29, 209–26.CrossRefGoogle ScholarPubMed
Parthasarathi, UD, Harrower, T, Tempest, M, Hodges, JR, Walsh, C, McKenna, PJ, Fletcher, PC (2006). Psychiatric presentation of voltage-gated potassium channel antibody-associated encephalopathy. Case report. British Journal of Psychiatry 189, 182–183.CrossRefGoogle ScholarPubMed
Remington, JS, Klein, JO, Wilson, GB, Baker, CJ (2006). Infectious Diseases of the Fetus and Newborn Infant. Elsevier Saunders: Philadelphia.Google Scholar
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. Journal of Clinical Endocrinology and Metabolism 86, 245–250.Google ScholarPubMed
Seckl, JR, Holmes, MC (2007). Mechanisms of disease: glucocorticoids, their placental metabolism and fetal ‘programming’ of adult pathophysiology. Nature Clinical Practice. Endocrinology and Metabolism 3, 479–488.CrossRefGoogle ScholarPubMed
Selten, JP, Frissen, A, Lensvelt-Mulders, G, Morgan, VA (2010). Schizophrenia and 1957 pandemic of influenza: meta-analysis. Schizophrenia Bulletin 36, 219–228.CrossRefGoogle ScholarPubMed
Shi, J, Levinson, DF, Duan, J, Sanders, AR, Zheng, Y, Pe'er, I, Dudbridge, F, Holmans, PA, Whittemore, AS, Mowry, BJ, Olincy, A, Amin, F, Cloninger, CR, Silverman, JM, Buccola, NG, Byerley, WF, Black, DW, Crowe, RR, Oksenberg, JR, Mirel, DB, Kendler, KS, Freedman, R, Gejman, PV (2009). Common variants on chromosome 6p22.1 are associated with schizophrenia. Nature 460, 753–757.CrossRefGoogle ScholarPubMed
Shi, L, Fatemi, SH, Sidwell, RW, Patterson, PH (2003). Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. Journal of Neuroscience 23, 297–302.CrossRefGoogle ScholarPubMed
Short, SJ, Lubach, GR, Karasin, AI, Olsen, CW, Styner, M, Knickmeyer, RC, Gilmore, JH, Coe, CL (2010). Maternal influenza infection during pregnancy impacts postnatal brain development in the rhesus monkey. Biological Psychiatry 67, 965–973.CrossRefGoogle ScholarPubMed
Smith, SE, Li, J, Garbett, K, Mirnics, K, Patterson, PH (2007). Maternal immune activation alters fetal brain development through interleukin-6. Journal of Neuroscience 27, 10695–10702.CrossRefGoogle ScholarPubMed
Sorensen, HJ, Mortensen, EL, Reinisch, JM, Mednick, SA (2009). Association between prenatal exposure to bacterial infection and risk of schizophrenia. Schizophrenia Bulletin 35, 631–637.CrossRefGoogle ScholarPubMed
Stefansson, H, Ophoff, RA, Steinberg, S, Andreassen, OA, Cichon, S, Rujescu, D, Werge, T, Pietilainen, OP, Mors, O, Mortensen, PB, Sigurdsson, E, Gustafsson, O, Nyegaard, M, Tuulio-Henriksson, A, Ingason, A, Hansen, T, Suvisaari, J, Lonnqvist, J, Paunio, T, Borglum, AD, Hartmann, A, Fink-Jensen, A, Nordentoft, M, Hougaard, D, Norgaard-Pedersen, B, Bottcher, Y, Olesen, J, Breuer, R, Moller, HJ, Giegling, I, Rasmussen, HB, Timm, S, Mattheisen, M, Bitter, I, Rethelyi, JM, Magnusdottir, BB, Sigmundsson, T, Olason, P, Masson, G, Gulcher, JR, Haraldsson, M, Fossdal, R, Thorgeirsson, TE, Thorsteinsdottir, U, Ruggeri, M, Tosato, S, Franke, B, Strengman, E, Kiemeney, LA, Melle, I, Djurovic, S, Abramova, L, Kaleda, V, Sanjuan, J, de Frutos, R, Bramon, E, Vassos, E, Fraser, G, Ettinger, U, Picchioni, M, Walker, N, Toulopoulou, T, Need, AC, Ge, D, Yoon, JL, Shianna, KV, Freimer, NB, Cantor, RM, Murray, R, Kong, A, Golimbet, V, Carracedo, A, Arango, C, Costas, J, Jonsson, EG, Terenius, L, Agartz, I, Petursson, H, Nothen, MM, Rietschel, M, Matthews, PM, Muglia, P, Peltonen, L, St Clair, D, Goldstein, DB, Stefansson, K, Collier, DA (2009). Common variants conferring risk of schizophrenia. Nature 460, 744–747.CrossRefGoogle ScholarPubMed
Susser, E (1999). Life course cohort studies of schizophrenia. Psychiatric Annals 29, 161–165.CrossRefGoogle Scholar
Susser, E, Buka, S, Schaefer, CA, Andrews, H, Cirillo, PM, Factor-Litvak, P, Gillman, M, Goldstein, JM, Ivey Henry, P, Lumey, LH, McKeague, IW, Michels, KB, Terry, MB, Cohn, BA; for the EDAH Team (2011). The Early Determinants of Adult Health Study. Journal of Developmental Origins of Health and Disease 2, 311–321.CrossRefGoogle ScholarPubMed
Susser, ES, Schaefer, CA, Brown, AS, Begg, MD, Wyatt, RJ (2000). The design of the Prenatal Determinants of Schizophrenia Study. Schizophrenia Bulletin 26, 257–273.CrossRefGoogle ScholarPubMed
van dan Berg, BJ, Christianson, RE, Oeschsli, FW (1988). The California Child Health and Development Studies of the School of Public Health, University of California, Berkeley. Pediatric and Perinatal Epidemiology 2, 265–282.CrossRefGoogle Scholar
Vincent, A, Deacon, R, Dalton, P, Salmond, C, Blamire, AM, Pendlebury, S, Johansen-Berg, H, Rajogopalan, B, Styles, P, Stein, J (2002). Maternal antibody-mediated dyslexia? Evidence for a pathogenic serum factor in a mother of two dyslexic children shown by transfer to mice using behavioural studies and magnetic resonance spectroscopy. Journal of Neuroimmunology 130, 243–247.CrossRefGoogle Scholar
von Elm, E, Altman, DG, Egger, M, Pocock, SJ, Gøtzsche, PC, Vandenbroucke, JP; STROBE Initiative (2007). The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 370, 1453–1457.CrossRefGoogle ScholarPubMed
Weinberger, DR (1987). Implications of normal brain development for the pathogenesis of schizophrenia. Archives of General Psychiatry 44, 660–669.CrossRefGoogle ScholarPubMed
Weinstock, M (2008). The long-term behavioural consequences of prenatal stress. Neuroscience and Biobehavioural Reviews 32, 1073–1086.CrossRefGoogle ScholarPubMed
Wright, P, Murray, RM (1993). Schizophrenia: prenatal influenza and autoimmunity. Annals of Medicine 25, 497–502.CrossRefGoogle ScholarPubMed
Wright, P, Takei, N, Murray, RM, Sham, P (1999). Seasonality, prenatal influenza exposure, and schizophrenia. In Prenatal Exposures in Schizophrenia (ed. Susser, E, Brown, A. S. and Gorman, J. M.), pp. 89–112. American Psychiatric Press: Washington DC.Google Scholar
Xiao, J, Buka, SL, Cannon, TD, Suzuki, Y, Viscidi, RP, Torrey, EF, Yolken, RH (2009). Serological pattern consistent with infection with type I Toxoplasma gondii in mothers and risk of psychosis among adult offspring. Microbes and Infection 11, 1011–1018.CrossRefGoogle ScholarPubMed
Yolken, RH, Torrey, EF (2008). Are some cases of psychosis caused by microbial agents? A review of the evidence. Molecular Psychiatry 13, 470–479.CrossRefGoogle ScholarPubMed
Zammit, S, Lewis, G, Dalman, C, Allebeck, P (2010). Examining interactions between risk factors for psychosis. British Journal of Psychiatry 197, 207–211.CrossRefGoogle ScholarPubMed
Zandi, MS, Irani, SR, Lang, B, Waters, P, Jones, PB, McKenna, P, Coles, AJ, Vincent, A, Lennox, BR (2011). Disease-relevant autoantibodies in first episode schizophrenia. Journal of Neurology 258, 686–688.CrossRefGoogle ScholarPubMed
Supplementary material: File

Khandaker supplementary material

Appendix

Download Khandaker supplementary material(File)
File 94.7 KB