Prenatal Infection and Schizophrenia: A Review of Epidemiologic and Translational Studies

Brown, Alan S.; Derkits, Elena J.

doi:10.1176/appi.ajp.2009.09030361

Cited by 1,269Tryptophan and brain disordersSchizophrenia research and treatmentMaternal Mental Health During Pregnancy and Postpartum

Prenatal Infection and Schizophrenia: A Review of Epidemiologic and Translational Studies

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Brown, Alan S., Derkits, Elena J.·2010·American Journal of Psychiatry

DOI 10.1176/appi.ajp.2009.09030361PMC PMC3652286

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Abstract

An emerging literature from epidemiologic, clinical, and preclinical investigations has provided evidence that gestational exposure to infection contributes to the etiology of schizophrenia. In recent years, these studies have moved from ecologic designs, which ascertain infection based on epidemics in populations, to investigations that have capitalized on reliable biomarkers in individual pregnancies. These studies have documented specific candidate infections that appear to be associated with an elevated risk of schizophrenia. Animal models of maternal immune activation inspired by this work have revealed intriguing findings indicating behavioral, neurochemical, and neurophysiologic abnormalities consistent with observations in schizophrenia. In parallel studies in humans and animals, investigators are working to uncover the cellular and molecular mechanisms by which in utero exposure to infection contributes to schizophrenia risk. In this review, the authors discuss and critically evaluate the epidemiologic literature on in utero exposure to infection and schizophrenia, summarize emerging animal models of maternal immune activation, and discuss putative unique and common mechanisms by which in utero exposure to infection alters neurodevelopment, potentially increasing susceptibility to schizophrenia. The promise of this work for facilitating the identification of susceptibility loci in genetic studies of schizophrenia is illustrated by examples of interaction between in utero exposure to infection and genetic variants. The authors then elaborate on possible implications of this work, including the use of preventive measures for reducing the incidence of schizophrenia. Finally, they discuss new approaches aimed at addressing current challenges in this area of research.

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Maternal inflammation may represent a pathway by which infectious and other insults may give rise to neurodevelopmental disorders.
“it has been proposed that maternal inflammation may represent a pathway by which infectious and other insults may give rise to neurodevelopmental disorders8, 10.”
From Elevated maternal C-reactive protein and autism in a national birth cohort (2014) · cites this paper as [10]
Multiple animal models of prenatal infection have found evidence of diverse neurobehavioral abnormalities, whether through direct exposure of pregnant mice or rodents to influenza virus, or through non-infectious activation of the maternal immune system.
“Multiple animal models of prenatal infection have found evidence of diverse neurobehavioral abnormalities, whether through direct exposure of pregnant mice or rodents to influenza virus, or through non-infectious activation of the maternal immune system (e.g., using RNA poly(I:C) to stimulate an antiviral inflammatory response or lipopolysaccharide to stimulate a bacterial inflammatory response) (”
From Maternal hospitalization with infection during pregnancy and risk of autism spectrum disorders (2015) · cites this paper as Brown and Derkits, 2010
Epidemiological data showed significantly increased risk of developing schizophrenia after prenatal microbial infection.
“Epidemiological data showed significantly increased risk of developing schizophrenia after prenatal microbial infection [169].”
From The Role of Microbiota-Gut-Brain Axis in Neuropsychiatric and Neurological Disorders (2021) · cites this paper as [169]

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Caspi, A., Sugden, K., Moffitt, T. E., Taylor, A., Craig, I. W., Harrington, H., McClay, J., Mill, J., Martin, J., Braithwaite, A., et al. (2003) · Science · doi:10.1126/science.1083968 · Cited by 8,120 · see citing works
Common polygenic variation contributes to risk of schizophrenia and bipolar disorder
The International Schizophrenia Consortium (2009) · Nature · doi:10.1038/nature08185 · Cited by 4,821 · see citing works
Infectious Diseases of the Fetus and Newborn Infant
Remington, J. S., & Klein, J. O. (1984) · The Pediatric Infectious Disease Journal · doi:10.1097/00006454-198401000-00024 · Cited by 2,473 · see citing works
Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence
Harrison, P. J., & Weinberger, D. R. (2005) · Molecular Psychiatry · doi:10.1038/sj.mp.4001558 · Cited by 2,020 · see citing works
Common variants conferring risk of schizophrenia
†Genetic Risk and Outcome in Psychosis (GROUP), Stefansson, H., Ophoff, R. A., Steinberg, S., Andreassen, O. A., Cichon, S., Rujescu, D., Werge, T., Pietiläinen, O. P. H., Mors, O., et al. (2009) · Nature · doi:10.1038/nature08186 · Cited by 1,677 · see citing works
Maternal Immune Activation Alters Fetal Brain Development through Interleukin-6
Smith, S. E. P., Li, J., Garbett, K., Mirnics, K., & Patterson, P. H. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2178-07.2007 · Cited by 1,605 · see citing works
Moderation of the effect of adolescent-onset cannabis use on adult psychosis by a functional polymorphism in the catechol-O-methyltransferase gene: Longitudinal evidence of a gene X environment interaction
Caspi, A., Moffitt, T. E., Cannon, M., McClay, J., Murray, R., Harrington, H., Taylor, A., Arseneault, L., Williams, B., Braithwaite, A., et al. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.01.026 · Cited by 1,409 · see citing works
Herpes simplex virus infections
Whitley, R. J., & Roizman, B. (2001) · The Lancet · doi:10.1016/s0140-6736(00)04638-9 · Cited by 1,365 · see citing works
Adult Schizophrenia Following Prenatal Exposure to an Influenza Epidemic
Mednick, S. A. (1988) · Archives of General Psychiatry · doi:10.1001/archpsyc.1988.01800260109013 · Cited by 1,198 · see citing works
Common variants on chromosome 6p22.1 are associated with schizophrenia
Shi, J., Levinson, D. F., Duan, J., Sanders, A. R., Zheng, Y., Pe’er, I., Dudbridge, F., Holmans, P., Whittemore, A. S., Mowry, B. J., et al. (2009) · Nature · doi:10.1038/nature08192 · Cited by 1,154 · see citing works
Obstetric Complications and Schizophrenia: Historical and Meta-Analytic Review
Cannon, M. D., Jones, P. B., & Murray, R. M. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.7.1080 · Cited by 1,138 · see citing works
Identification of loci associated with schizophrenia by genome-wide association and follow-up
Molecular Genetics of Schizophrenia Collaboration, O'Donovan, M. C., Craddock, N., Norton, N., Williams, H., Peirce, T., Moskvina, V., Nikolov, I., Hamshere, M., Carroll, L., et al. (2008) · Nature Genetics · doi:10.1038/ng.201 · Cited by 1,070 · see citing works
Serologic Evidence of Prenatal Influenza in the Etiology of Schizophrenia
Brown, A. S., Begg, M. D., Gravenstein, S., Schaefer, C. A., Wyatt, R. J., Bresnahan, M. A., Babulas, V. P., & Susser, E. (2004) · Archives of General Psychiatry · doi:10.1001/archpsyc.61.8.774 · Cited by 1,048 · see citing works
Self-citation
Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring
Shi, L., Fatemi, S. H., Sidwell, R. W., & Patterson, P. H. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-01-00297.2003 · Cited by 1,025 · see citing works
Axonal Neuregulin-1 Regulates Myelin Sheath Thickness
Michailov, G. V., Sereda, M. W., Brinkmann, B. G., Fischer, T. M., Haug, B., Birchmeier, C., Role, L. W., Lai, C., Schwab, M. H., & Nave, K. (2004) · Science · doi:10.1126/science.1095862 · Cited by 940 · see citing works
Maternal Intrauterine Infection, Cytokines, and Brain Damage in the Preterm Newborn
Dammann, O., & Leviton, A. (1997) · Pediatric Research · doi:10.1203/00006450-199707000-00001 · Cited by 886 · see citing works
Synaptic plasticity and dysconnection in schizophrenia
Stephan, K. E., Baldeweg, T., & Friston, K. J. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.005 · Cited by 841 · see citing works
White Matter Changes in Schizophrenia: Evidence for Myelin-Related Dysfunction
Davis, K. L., Stewart, D. G., Friedman, J. I., Buchsbaum, M., Harvey, P. D., Hof, P. R., Buxbaum, J., & Haroutunian, V. (2003) · Archives of General Psychiatry · doi:10.1001/archpsyc.60.5.443 · Cited by 793 · see citing works
Immune involvement in schizophrenia and autism: Etiology, pathology and animal models
Patterson, P. H. (2009) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.12.016 · Cited by 766 · see citing works
Advancing Paternal Age and the Risk of Schizophrenia
Malaspina, D., Harlap, S., Fennig, S., Heiman, D., Nahon, D., Feldman, D., & Susser, E. S. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.4.361 · Cited by 562 · see citing works
A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development
Kamiya, A., Kubo, K., Tomoda, T., Takaki, M., Youn, R., Ozeki, Y., Sawamura, N., Park, U., Kudo, C., Okawa, M., et al. (2005) · Nature Cell Biology · doi:10.1038/ncb1328 · Cited by 531 · see citing works
Behavioral phenotypes of Disc1 missense mutations in mice
Clapcote, S. J., Lipina, T. V., Millar, J. K., Mackie, S., Christie, S., Ogawa, F., Lerch, J. P., Trimble, K., Uchiyama, M., Sakuraba, Y., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.04.015 · Cited by 526 · see citing works
Maternal Infections and Subsequent Psychosis Among Offspring
Buka, S. L. (2001) · Archives of General Psychiatry · doi:10.1001/archpsyc.58.11.1032 · Cited by 512 · see citing works
Variation in DISC1 affects hippocampal structure and function and increases risk for schizophrenia
Callicott, J. H., Straub, R. E., Pezawas, L., Egan, M. F., Mattay, V. S., Hariri, A. R., Verchinski, B. A., Meyer‐Lindenberg, A., Balkissoon, R., Kolachana, B. S., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0500515102 · Cited by 512 · see citing works
Maternal Exposure to Toxoplasmosis and Risk of Schizophrenia in Adult Offspring
Brown, A. S., Schaefer, C. A., Quesenberry, C. P., Liu, L., Babulas, V. P., & Susser, E. (2005) · American Journal of Psychiatry · doi:10.1176/appi.ajp.162.4.767 · Cited by 490 · see citing works
Self-citation
Elevated Maternal Interleukin-8 Levels and Risk of Schizophrenia in Adult Offspring
Brown, A. S., Hooton, J. W. L., Schaefer, C. A., Zhang, H., Petkova, E., Babulas, V. P., Perrin, M. A., Gorman, J. M., & Susser, E. (2004) · American Journal of Psychiatry · doi:10.1176/appi.ajp.161.5.889 · Cited by 484 · see citing works
Self-citation
Converging Evidence of NMDA Receptor Hypofunction in the Pathophysiology of Schizophrenia
Coyle, J. T., Tsai, G. E., & GOFF, D. C. (2003) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1300.020 · Cited by 443 · see citing works
Tangential Neuronal Migration Controls Axon Guidance: A Role for Neuregulin-1 in Thalamocortical Axon Navigation
López‐Bendito, G., Cautinat, A., Sánchez‐Alcañiz, J. A., Bielle, F., Flames, N., Garratt, A. N., Talmage, D. A., Role, L. W., Charnay, P., Marín, Ó., et al. (2006) · Cell · doi:10.1016/j.cell.2006.01.042 · Cited by 367 · see citing works
Inducible expression of mutant human DISC1 in mice is associated with brain and behavioral abnormalities reminiscent of schizophrenia
Pletnikov, M. V., Ayhan, Y., Nikolskaia, O. V., Xu, Y., Ovanesov, M. V., Huang, H., Mori, S., Moran, T. H., & Ross, C. A. (2007) · Molecular Psychiatry · doi:10.1038/sj.mp.4002079 · Cited by 339 · see citing works
Immune signalling in neural development, synaptic plasticity and disease
Boulanger, L. M., & Shatz, C. J. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1428 · Cited by 334 · see citing works
Exposure to Influenza Epidemics During Gestation and Adult Schizophrenia
Barr, C. E. (1990) · Archives of General Psychiatry · doi:10.1001/archpsyc.1990.01810210077012 · Cited by 329 · see citing works
Maternal Cytokine Levels during Pregnancy and Adult Psychosis
Buka, S. L., Tsuang, M. T., Torrey, E. F., Klebanoff, M. A., Wagner, R., & Yolken, R. H. (2001) · Brain Behavior and Immunity · doi:10.1006/brbi.2001.0644 · Cited by 316 · see citing works
Cysteine-Rich Domain Isoforms of the Neuregulin-1 Gene Are Required for Maintenance of Peripheral Synapses
Wolpowitz, D., Mason, T. B. A., Dietrich, P., Mendelsohn, M. M., Talmage, D. A., & Role, L. W. (2000) · Neuron · doi:10.1016/s0896-6273(00)80873-9 · Cited by 313 · see citing works
Prenatal rubella, premorbid abnormalities, and adult schizophrenia
Brown, A. S., Cohen, P., Harkavy‐Friedman, J., Babulas, V. P., Malaspina, D., Gorman, J., & Susser, E. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01068-x · Cited by 298 · see citing works
Self-citation
Maternal Exposure to Respiratory Infections and Adult Schizophrenia Spectrum Disorders: A Prospective Birth Cohort Study
Brown, A. S., Schaefer, C. A., Wyatt, R. J., Goetz, R. R., Begg, M. D., Gorman, J. M., & Susser, E. (2000) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a033453 · Cited by 273 · see citing works
Self-citation
Toxoplasma gondii as a Risk Factor for Early-Onset Schizophrenia: Analysis of Filter Paper Blood Samples Obtained at Birth
Mortensen, P. B., Nørgaard‐Pedersen, B., Waltoft, B. L., Sørensen, T. L., HOUGAARD, D. M., Torrey, E. F., & Yolken, R. H. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.05.024 · Cited by 269 · see citing works
A mutation in mouse <i>Disc1</i> that models a schizophrenia risk allele leads to specific alterations in neuronal architecture and cognition
Kvajo, M., McKellar, H., Arguello, P. A., Drew, L. J., Moore, H., MacDermott, A. B., Karayiorgou, M., & Gogos, J. A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802615105 · Cited by 268 · see citing works
Defective corticogenesis and reduction in Reelin immunoreactivity in cortex and hippocampus of prenatally infected neonatal mice
Fatemi, S. H., Emamian, E. S., Kist, D. A., Sidwell, R. W., Nakajima, K., Akhter, P., Shier, A. C., Sheikh, S. A., & Bailey, K. W. (1999) · Molecular Psychiatry · doi:10.1038/sj.mp.4000520 · Cited by 261 · see citing works
Association Between Prenatal Exposure to Bacterial Infection and Risk of Schizophrenia
Sørensen, H. J., Mortensen, E. L., Reinisch, J. M., & Mednick, S. A. (2008) · Schizophrenia Bulletin · doi:10.1093/schbul/sbn121 · Cited by 261 · see citing works
Schizophrenia-Related Neural and Behavioral Phenotypes in Transgenic Mice Expressing TruncatedDisc1
Shen, S., Lang, B., Nakamoto, C., Zhang, F., Pu, J., Kuan, S. L., Chatzi, C. A., He, S., Mackie, I., Brandon, N. J., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3299-08.2008 · Cited by 250 · see citing works
Schizophrenia Following Pre-natal Exposure to Influenza Epidemics Between 1939 and 1960
Sham, P. C., O’Callaghan, E., Takei, N., Murray, G. K., Hare, E. H., & Murray, R. M. (1992) · The British Journal of Psychiatry · doi:10.1192/bjp.160.4.461 · Cited by 250 · see citing works
Maternal Exposure to Herpes Simplex Virus and Risk of Psychosis Among Adult Offspring
Buka, S. L., Cannon, T. D., Torrey, E. F., & Yolken, R. H. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2007.09.022 · Cited by 233 · see citing works
Prenatal Exposure to Maternal Genital and Reproductive Infections and Adult Schizophrenia
Babulas, V. P., Factor-Litvak, P. R., Goetz, R. R., Schaefer, C. A., & Brown, A. S. (2006) · American Journal of Psychiatry · doi:10.1176/ajp.2006.163.5.927 · Cited by 233 · see citing works
Self-citation
NMDA Agonists and Antagonists as Probes of Glutamatergic Dysfunction and Pharmacotherapies in Neuropsychiatric Disorders
Krystal, J. H., D’Souza, C., Petrakis, I. L., Belger, A., Berman, R., Charney, D. S., Abi‐Saab, W., & Madonick, S. H. (1999) · Harvard Review of Psychiatry · doi:10.3109/hrp.7.3.125 · Cited by 232 · see citing works
Phenotypic characterization of spatial cognition and social behavior in mice with ‘knockout’ of the schizophrenia risk gene neuregulin 1
O’Tuathaigh, C. M. P., Babovic, D., O’Sullivan, G. J., Clifford, J. J., Tighe, O., Croke, D. T., Harvey, R. P., & Waddington, J. L. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.03.051 · Cited by 230 · see citing works
Neural development of the neuregulin receptor ErbB4 in the cerebral cortex and the hippocampus: preferential expression by interneurons tangentially migrating from the ganglionic eminences
Yau, H.-J. (2003) · Cerebral Cortex · doi:10.1093/cercor/13.3.252 · Cited by 225 · see citing works
Schizophrenic Birth Seasonality in Relation to the Incidence of Infectious Diseases and Temperature Extremes
Watson, C. G. (1984) · Archives of General Psychiatry · doi:10.1001/archpsyc.1984.01790120089011 · Cited by 220 · see citing works
Nonaffective Psychosis After Prenatal Exposure to Rubella
Brown, A. S., Cohen, P., Greenwald, S., & Susser, E. (2000) · American Journal of Psychiatry · doi:10.1176/appi.ajp.157.3.438 · Cited by 219 · see citing works
Self-citation
Evidence for an Interaction Between Familial Liability and Prenatal Exposure to Infection in the Causation of Schizophrenia
Clarke, M. C., Tanskanen, A. J., HUTTUNEN, M. O., Whittaker, J. C., & Cannon, M. D. (2009) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2009.08010031 · Cited by 216 · see citing works
Regulation of NMDA Receptors by Neuregulin Signaling in Prefrontal Cortex
Gu, Z., Jiang, Q., Fu, A. K. Y., Ip, N. Y., & Yan, Z. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1086-05.2005 · Cited by 213 · see citing works
Exposure to infection and brain development: cytokines in the pathogenesis of schizophrenia
GILMORE, J., & FREDRIKJARSKOG, L. (1997) · Schizophrenia Research · doi:10.1016/s0920-9964(96)00123-5 · Cited by 209 · see citing works
Development of hippocampal mossy fiber synaptic outputs by new neurons in the adult brain
Faulkner, R. L., Jang, M., Liu, X.-B., Duan, X., Sailor, K. A., Kim, J. Y., Ge, S., Jones, E. G., Ming, G., Song, H., et al. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0806658105 · Cited by 208 · see citing works
Association Between Prenatal Exposure to Poliovirus Infection and Adult Schizophrenia
Suvisaari, J., Haukka, J. K., Tanskanen, A. J., Hovi, T., & Lönnqvist, J. K. (1999) · American Journal of Psychiatry · doi:10.1176/ajp.156.7.1100 · Cited by 192 · see citing works
Molecular genetic studies of schizophrenia
Riley, B., & Kendler, K. S. (2006) · European Journal of Human Genetics · doi:10.1038/sj.ejhg.5201571 · Cited by 190 · see citing works
Type III Neuregulin-1 Is Required for Normal Sensorimotor Gating, Memory-Related Behaviors, and Corticostriatal Circuit Components
Chen, Y.-J. J., Johnson, M. A., Lieberman, M. D., Goodchild, R. E., Schobel, S., Lewandowski, N., Rosoklija, G., Liu, R.-C., Gingrich, J. A., Small, S., et al. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1815-08.2008 · Cited by 188 · see citing works
Association between −G308A tumor necrosis factor alpha gene polymorphism and schizophrenia
Boin, F., Zanardini, R., Pioli, R., Altamura, C. A., Maes, M. H. J., & Gennarelli, M. (2000) · Molecular Psychiatry · doi:10.1038/sj.mp.4000815 · Cited by 179 · see citing works
Maternal Influenza in the Etiology of Schizophrenia
Kendell, R. E. (1989) · Archives of General Psychiatry · doi:10.1001/archpsyc.1989.01810100020004 · Cited by 174 · see citing works
Prenatal Influenza Infections and Adult Schizophrenia
Mednick, S. A., HUTTUNEN, M. O., & Machón, R. A. (1994) · Schizophrenia Bulletin · doi:10.1093/schbul/20.2.263 · Cited by 169 · see citing works
Cytokine production in chorioamnionitis
Saji, F., Samejima, Y., Kamiura, S., Sawai, K., Shimoya, K., & Kimura, T. (2000) · Journal of Reproductive Immunology · doi:10.1016/s0165-0378(00)00064-4 · Cited by 162 · see citing works
Decline in the Incidence of Schizophrenia in Finnish Cohorts Born From 1954 to 1965
Suvisaari, J., Haukka, J. K., Tanskanen, A. J., & Lönnqvist, J. K. (1999) · Archives of General Psychiatry · doi:10.1001/archpsyc.56.8.733 · Cited by 148 · see citing works
Amniotic fluid concentrations of Interleukin‐1β, Interleukin‐6 and TNF‐α in chorioamnionitis before 32 weeks of gestation: histological associations and neonatal outcome
Baud, O., Émilie, D., Pelletier, E., Lacaze‐Masmonteil, T., Zupan, V., Fernandez, H., Dehan, M., Frydman, R., & Ville, Y. G. (1999) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1999.tb08088.x · Cited by 146 · see citing works
Season of Birth in Schizophrenia
O’Callaghan, E., Gibson, T., Colohan, H. A., Walshe, D. G., Buckley, P., Larkin, C., & Waddington, J. L. (1991) · The British Journal of Psychiatry · doi:10.1192/bjp.158.6.764 · Cited by 138 · see citing works
Prenatal exposure to influenza as a risk factor for adult schizophrenia
Limosin, F., Rouillon, F., Payan, C., Cohen, J., & Strub, N. (2003) · Acta Psychiatrica Scandinavica · doi:10.1034/j.1600-0447.2003.00052.x · Cited by 137 · see citing works
Cytokine effects on cortical neuron MAP-2 immunoreactivity: implications for schizophrenia
Marx, C. E., Jarskog, L. F., Lauder, J. M., Lieberman, J. A., & Gilmore, J. H. (2001) · Biological Psychiatry · doi:10.1016/s0006-3223(01)01209-4 · Cited by 134 · see citing works
Exposure to Prenatal and Childhood Infections and the Risk of Schizophrenia
Westergaard, T., Mortensen, P. B., Pedersen, C. B., Wohlfahrt, J., & Melbye, M. (1999) · Archives of General Psychiatry · doi:10.1001/archpsyc.56.11.993 · Cited by 133 · see citing works
Neuregulin-1 immunoglobulin-like domain mutant mice: clozapine sensitivity and impaired latent inhibition
Rimer, M., Barrett, D. W., Maldonado, M. A., Vock, V. M., & Gonzalez-Lima, F. (2005) · Neuroreport · doi:10.1097/00001756-200502280-00014 · Cited by 120 · see citing works
Schizophrenia following in utero exposure to the 1957 influenza epidemics in Japan
Kunugi, H., Nanko, S., Takei, N., Saito, K., Hayashi, N., & Kazamatsuri, H. (1995) · American Journal of Psychiatry · doi:10.1176/ajp.152.3.450 · Cited by 119 · see citing works
Prenatal Exposure to the 1957 Influenza Epidemic and Adult Schizophrenia: A Follow-Up Study
Cannon, M. D., Cotter, D., Coffey, V. P., Sham, P. C., Takei, N., Larkin, C., Murray, R. M., & O’Callaghan, E. (1996) · The British Journal of Psychiatry · doi:10.1192/bjp.168.3.368 · Cited by 116 · see citing works
The Relationship of Schizophrenic Births to 16 Infectious Diseases
O’Callaghan, E., Sham, P. C., Takei, N., Murray, G. K., Glover, G. R., Hare, E. H., & Murray, R. M. (1994) · The British Journal of Psychiatry · doi:10.1192/bjp.165.3.353 · Cited by 110 · see citing works
Relationship between in utero exposure to influenza epidemics and risk of schizophrenia in Denmark
Takei, N., Mortensen, P. B., Kl˦ning, U., Murray, R. M., Sham, P. C., O’Callaghan, E., & Munk‐Jørgensen, P. (1996) · Biological Psychiatry · doi:10.1016/0006-3223(95)00592-7 · Cited by 105 · see citing works
Influenza
Kilbourne, E. D. (1987) · Springer eBooks · doi:10.1007/978-1-4684-5239-6 · Cited by 105 · see citing works
The Design of the Prenatal Determinants of Schizophrenia Study
Susser, E., Schaefer, C. A., Brown, A. S., Begg, M. D., & Wyatt, R. J. (2000) · Schizophrenia Bulletin · doi:10.1093/oxfordjournals.schbul.a033451 · Cited by 104 · see citing works
Self-citation
Psychiatric Epidemiology
Susser, E., Schwartz, S., Morabia, A., & Bromet, E. J. (2006) · doi:10.1093/acprof:oso/9780195101812.001.0001 · Cited by 99 · see citing works
Influenza epidemics and incidence of schizophrenia, affective disorders and mental retardation in Western Australia: no evidence of a major effect
Morgan, V. A., Castle, D. J., Page, A. C., Fazio, S., Gurrin, L. C., Burton, P. R., Montgomery, P., & Jablensky, A. V. (1997) · Schizophrenia Research · doi:10.1016/s0920-9964(97)00033-9 · Cited by 98 · see citing works
Prenatal exposure to influenza and the development of schizophrenia: is the effect confined to females?
Takei, N., Sham, P. C., O’Callaghan, E., Murray, G. K., Glover, G. R., & Murray, R. M. (1994) · American Journal of Psychiatry · doi:10.1176/ajp.151.1.117 · Cited by 94 · see citing works
Phenotypic characterization of cognition and social behavior in mice with heterozygous versus homozygous deletion of catechol-O-methyltransferase
Babovic, D., O’Tuathaigh, C. M. P., O'Connor, A. M., O'Sullivan, G. J., Tighe, O., Croke, D. T., Karayiorgou, M., Gogos, J. A., Cotter, D., & Waddington, J. L. (2008) · Neuroscience · doi:10.1016/j.neuroscience.2008.07.006 · Cited by 90 · see citing works
Disrupted-in-schizophrenia 1 and neuregulin 1 are required for the specification of oligodendrocytes and neurones in the zebrafish brain
Wood, J. D., Bonath, F., Kumar, S., Ross, C. A., & Cunliffe, V. T. (2008) · Human Molecular Genetics · doi:10.1093/hmg/ddn361 · Cited by 90 · see citing works
Schizophrenia and influenza
Crow, T. J. (1991) · The Lancet · doi:10.1016/0140-6736(91)90109-3 · Cited by 90 · see citing works
No relation between risk of schizophrenia and prenatal exposure to influenza in Holland
Susser, E., Lin, S. P., Brown, A. S., Lumey, L. H., & Erlenmeyer‐Kimling, L. (1994) · American Journal of Psychiatry · doi:10.1176/ajp.151.6.922 · Cited by 90 · see citing works
Self-citation
Disruption to social dyadic interactions but not emotional/anxiety-related behaviour in mice with heterozygous ‘knockout’ of the schizophrenia risk gene neuregulin-1
O’Tuathaigh, C. M. P., O'Connor, A.-M., O'Sullivan, G. J., Lai, D., Harvey, R. P., Croke, D. T., & Waddington, J. L. (2007) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2007.09.018 · Cited by 88 · see citing works
ERP abnormalities during semantic processing in schizophrenia☆
Adams, J., Faux, S. F., Nestor, P. G., Shenton, M. E., Marcy, B., Smith, S. T., & McCarley, R. W. (1993) · Schizophrenia Research · doi:10.1016/0920-9964(93)90059-r · Cited by 81 · see citing works
No Evidence of Relation Between Maternal Exposure to Herpes Simplex Virus Type 2 and Risk of Schizophrenia?
Brown, A. S., Schaefer, C. A., Quesenberry, C. P., Shen, L., & Susser, E. (2006) · American Journal of Psychiatry · doi:10.1176/ajp.2006.163.12.2178 · Cited by 76 · see citing works
Self-citation
Heterozygous neuregulin 1 mice display greater baseline and Δ9-tetrahydrocannabinol-induced c-Fos expression
Boucher, A. A., Hunt, G. E., Karl, T., Micheau, J., McGregor, I. S., & Arnold, J. C. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.08.020 · Cited by 72 · see citing works
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O’Donovan, M. C., Norton, N., Williams, H. J., Peirce, T., Moskvina, V., Nikolov, I., Hamshere, M. L., Carroll, L. S., Georgieva, L., Dwyer, S., et al. (2008) · Molecular Psychiatry · doi:10.1038/mp.2008.108 · Cited by 72 · see citing works
Schizophrenia and the influenza epidemics of 1957 in Japan
Izumoto, Y., Inoue, S., & Yasuda, N. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(98)00359-x · Cited by 69 · see citing works
Evidence Against Maternal Influenza as a Risk Factor for Schizophrenia
Selten, J., & Slaets, J. P. J. (1994) · The British Journal of Psychiatry · doi:10.1192/bjp.164.5.674 · Cited by 65 · see citing works
Stalking the Schizovirus
Torrey, Ε. F. (1988) · Schizophrenia Bulletin · doi:10.1093/schbul/14.2.223 · Cited by 62 · see citing works
Does Influenza Cause Schizophrenia? A Five Year Review
McGrath, J. J., & Castle, D. J. (1995) · Australian & New Zealand Journal of Psychiatry · doi:10.3109/00048679509075888 · Cited by 55 · see citing works
Serologic evidence for prenatal influenza in the etiology of schizophrenia
Brown, A. S., Begg, M. D., Gravenstein, S., Schaefer, C. A., Wyatt, R. J., Bresnahan, M. A., Babulas, V. P., & Susser, E. (2003) · Schizophrenia Research · doi:10.1016/s0920-9964(03)80098-1 · Cited by 53 · see citing works
Self-citation
Schizophrenia and prenatal exposure to the 1957 A2 influenza epidemic in Croatia
Erlenmeyer‐Kimling, L., Folnegović, Z., Hrabak-Žerjavić, V., Borcić, B., Folnegović-Šmalc, V., & Susser, E. (1994) · American Journal of Psychiatry · doi:10.1176/ajp.151.10.1496 · Cited by 52 · see citing works
Enlargement of the lateral ventricles in mutant DISC1 transgenic mice
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Does prenatal influenza divert susceptible females from later affective psychosis to schizophrenia?
Takei, N., O’Callaghan, E., Sham, P. C., Glover, G. R., & Murray, R. M. (1993) · Acta Psychiatrica Scandinavica · doi:10.1111/j.1600-0447.1993.tb03468.x · Cited by 49 · see citing works
No relationship between schizophrenic birth and influenza epidemics in Japan
Mino, Y., Oshima, I., Tsuda, T., & Okagami, K. (2000) · Journal of Psychiatric Research · doi:10.1016/s0022-3956(00)00003-0 · Cited by 43 · see citing works
Prenatal exposure to influenza and schizophrenia in surinamese and Dutch Antillean immigrants to The Netherlands
Selten, J., Slaets, J. P. J., & Kahn, R. S. (1998) · Schizophrenia Research · doi:10.1016/s0920-9964(97)00105-9 · Cited by 40 · see citing works
Maternal exposure to influenza and paranoid schizophrenia
Grech, A., Takei, N., & Murray, R. M. (1997) · Schizophrenia Research · doi:10.1016/s0920-9964(97)00056-x · Cited by 24 · see citing works
No significant association between prenatal exposure topoliovirus epidemics and psychosis
Cahill, M., Chant, D. C., Welham, J., & McGrath, J. J. (2002) · Australian & New Zealand Journal of Psychiatry · doi:10.1046/j.1440-1614.2001.01006.x · Cited by 15 · see citing works
Schizophrenia risk for women from in utero exposure to influenza
Takei, N., Murray, R. M., Sham, P. C., & O’Callaghan, E. (1995) · American Journal of Psychiatry · doi:10.1176/ajp.152.1.150b · Cited by 12 · see citing works
The Direct Embryotoxicity of Immunoglobulin G Fractions From Patients With Systemic Lupus Erythematosus
Nadler, D., Klein, N. W., Aramli, L. A., Chambers, B. J., MAVES, M., & Wener, M. H. (1995) · American Journal of Reproductive Immunology · doi:10.1111/j.1600-0897.1995.tb00963.x · Cited by 11 · see citing works
Cytokines
Weizman, R., & Bessler, H. (1998) · CRC Press eBooks · doi:10.1201/9781420048193.ch1 · Cited by 10 · see citing works

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Research works printed but not linked: 4

[2]Martin RP Dombrowski SC Prenatal infections Prenatal Exposures: Psychological and Educational Consequences for Children New York Springer 2008 57 86
[49]Dukes CS Luft BJ Durack DT Scheld WM Whitley RJ Scheld WM Whitley RJ Durack DT Toxoplasmosis Infections of the Central Nervous System Philadelphia Lippincott-Raven 1997 785 806
[51]Weizman R Bessler H Plotnikoff NP Faith RE Murgo AJ Good RA Cytokines: stress and immunity: an overview Cytokines: Stress and Immunity Boca Raton, Fla CRC Press 1999 1 15
[94]Rothman KJ Modern Epidemiology 3 Philadelphia Lippincott Williams & Wilkins 2008

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Gardiner, E. J., Beveridge, N. J., Wu, J. Q., Carr, V. J., Scott, R. J., Tooney, P. A., & Cairns, M. J. (2011) · Molecular Psychiatry · doi:10.1038/mp.2011.78 · Cited by 232 · see citing works
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Miller, B. J., & Goldsmith, D. R. (2016) · Neuropsychopharmacology · doi:10.1038/npp.2016.211 · Cited by 182 · see citing works

Authors: Brown, A. S., & Derkits, E. J.
Affiliations: New York State Psychiatric Institute (US)
ORCID: Brown, Alan S.
Venue: American Journal of Psychiatry
Publisher: American Psychiatric Association Publishing
Published: 2010-03-01
Volume: 167
Issue: 3
Pages: 261-280
ISSN: 0002-953X (ISSN-L)
1535-7228
DOI: 10.1176/appi.ajp.2009.09030361
PMC: PMC3652286
OpenAlex: W2040789766
Cited by: 1,269
References: 99
Citations by year: 2026: 33 · 2025: 47 · 2024: 73 · 2023: 68 · 2022: 74 · 2021: 78 · 2020: 90 · 2019: 79 · 2018: 84 · 2017: 68 · 2016: 90 · 2015: 89 · 2014: 87 · 2013: 89 · 2012: 98
FWCI: 34.35
Type: journal article
Language: en
Open access: green
europepmc.org
Locations: American Journal of Psychiatry (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Mental Health (K02MH065422, R01MH082052, R01MH060249, 1R01MH-082052-01A1)
Eunice Kennedy Shriver National Institute of Child Health and Human Development (N01-HD13334, N010HD-6-3258)
Topics: Life Sciences › Neuroscience › Biological Psychiatry › Tryptophan and brain disorders
Health Sciences › Medicine › Psychiatry and Mental health › Schizophrenia research and treatment
Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Maternal Mental Health During Pregnancy and Postpartum
Keywords: prenatal infection, schizophrenia, maternal immune activation, intrauterine infection, brain development, animal models, genetic susceptibility loci, gene-environment interaction, infection biomarkers, schizophrenia prevention, etiology of schizophrenia
MeSH terms: Animals, Cross-Sectional Studies, Female, Herpes Genitalis, Humans, Infant, Newborn, Influenza, Human, Pregnancy, Pregnancy Complications, Infectious, Prenatal Exposure Delayed Effects, Pyelonephritis, Risk Factors, Schizophrenia, Social Environment, Toxoplasmosis, Congenital, Cohort Studies, Causality, Cytokines, Genetic Predisposition to Disease, Epigenesis, Genetic, Mice, Rats, Genome-Wide Association Study

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Prenatal Infection and Schizophrenia: A Review of Epidemiologic and Translational Studies

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