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Association Between Prenatal Exposure to Bacterial Infection and Risk of Schizophrenia

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Association Between Prenatal Exposure to Bacterial Infection and Risk of Schizophrenia Schizophrenia Bulletin vol. 35 no. 3 pp. 631–637, 2009 doi:10.1093/schbul/sbn121 Advance Access publication on October 1, 2008 Association Between Prenatal Exposure to Bacterial Infection and Risk of Schizophrenia Holger J. Sørensen2,3, Erik L. Mortensen1,2,4, June ciation between risk of schizophrenia and prenatal expo- M. Reinisch2,5, and Sarnoff A. Mednick6 sure to bacterial infections might be mediated through 2Danish Epidemiology Science Center, Institute of Preventive transplacental passage of maternally produced cytokines Medicine, Copenhagen University Hospital; 3Department of in response to bacterial infections. Psychiatry, Amager Hospital, Copenhagen University Hospital, Denmark; 4Department of Environmental Health, Institute of Key words: schizophrenia/bacterial infections/viral Public Health, University of Copenhagen, Øster Farimagsgade 5, infections/prenatal infections PO Box 2099, DK-1014 Copenhagen K, Denmark; 5The Kinsey Institute for Research in Sex, Gender, and Reproduction, Indiana University, Bloomington, IN; 6Social Science Research Center, University of Southern California Introduction The hypothesis that viral infection during pregnancy may Recent research suggests that prenatal exposure to nonvi- increase the risk of adult schizophrenia received much at- ral infection may be associated with increased risk of tention after the demonstration that people who were ex- schizophrenia, and we hypothesized an association between posed to the 1957 type A2 influenza in Helsinki were at maternal bacterial infection during pregnancy and elevated elevated risk of being admitted with schizophrenia.1 This offspring risk of schizophrenia. Data on maternal infec- association was replicated in several studies,2–7 and tions from the Copenhagen Perinatal Cohort were linked although not all studies point in the same direction,8–10 it with the Danish National Psychiatric Register. Offspring seems plausible that viruses play a role in the etiology of cases of narrowly defined schizophrenia (International chronic diseasessuchasschizophreniaduetotheirpotential Classification of Diseases, Eighth Revision [ICD-8]) and for neurotropism and latency.11 Recent studies have also more broadly defined schizophrenia (ICD-8 and ICD-10) explored the risk of schizophrenia associated with child- were identified before the ages of 32–34 and 45–47 years, hood infections,12,13 and the largest of these investigations respectively. The effect of prenatal exposure to bacterial has found associations between serious viral central infections was adjusted for prenatal exposure to analgesics nervous system infections during childhood and later and parental social status. In a risk set of 7941 individuals, schizophrenia.14 85 cases (1.1%) of ICD-8 schizophrenia were identified by Less is known about the possible relationship between the age of 32–34 years and 153 cases (1.9%) of more early-life exposure to other infectious agents than viruses broadly defined schizophrenia by the age of 45–47 years. and risk of schizophrenia. Recently, studies have First-trimester exposure conferred an elevated risk of addressed the possible associations of in utero or perina- ICD-8 schizophrenia (odds ratio 2.53; 95% confidence tal exposure to Toxoplasma gondii, a protozoan parasite, interval [CI] 1.07–5.96) and also of broadly defined schizo- and the development of schizophrenia; one study in- phrenia (odds ratio 2.14; 95% CI 1.06–4.31). Second- cluded maternal sera drawn before birth15 and one trimester exposure also conferred a significantly elevated used sera from infants.16 Both studies found associations risk of schizophrenia but only in unadjusted analyses. These between risk of schizophrenia (or schizophrenia spectrum findings suggest a relationship between maternal bacterial disorder) and increased levels of immunoglobulin infection in pregnancy and offspring risk of schizophrenia, G (IgG) antibodies to T gondii. Increased risk of schizo- and this effect was somewhat stronger for ICD-8 schizo- phrenia has also been linked with respiratory infections17 phrenia with earlier onset. Post hoc analyses showed and periconceptual maternal genital infections.18 that upper respiratory tract and gonococcal infections It is important to further examine prospective were associated with elevated risk of the disease. An asso- relationships between early exposures to viral and nonvi- ral infectious agents and risk of schizophrenia. The 1To whom correspondence should be addressed; tel: þ45-3532- Copenhagen Perinatal Cohort contains data on maternal 7839, fax: þ45-3532-7748, e-mail: [email protected]. viral and bacterial infection during pregnancy. The use of Ó The Author 2008. Published by Oxford University Press on behalf of the Maryland Psychiatric Research Center. All rights reserved. For permissions, please email: [email protected]. 631 H. J. Sørensen et al. these baseline data and access to psychiatric outcome old. The 1- to 8-point social status scale was based on data enabled us to examine associations between mater- breadwinner’s occupation, breadwinner’s education, nal viral and bacterial infection during pregnancy and type of income, and quality of housing.20 Parental offspring risk of schizophrenia. We hypothesized a rela- social status was categorized in 3 groups: low (status tionship between maternal viral infection and offspring categories 1–4), high (categories 5–8), and missing schizophrenia but possibly also between maternal bacte- data (the missing data rate for parental social status rial infection and schizophrenia in the offspring. was 20.7%). Findings from this cohort indicate a relatively strong relationship between the second-trimester exposure Methods to analgesics and risk of schizophrenia.22 Consequently, The methods of the data collection in the Copenhagen prenatal exposure to analgesics was considered a poten- Perinatal Cohort are described in detail elsewhere.19–21 tial confounder of a relationship between maternal Briefly, the cohort comprises 9125 individuals delivered infection during pregnancy and offspring risk of by 8949 women between September 1, 1959, and December schizophrenia. 31, 1961 at Rigshospitalet in Copenhagen. The mothers were mainly residents in Copenhagen, but some were ad- Psychiatric Follow-up mitted with obstetrical indications or due to their status Written approval to conduct a registry-based psychiatric 19 as single mothers. follow-up was obtained from the regional scientific and The study sample of the present analyses comprised ethics committee. The Danish Psychiatric Central Re- 7941 individuals, 4030 males and 3911 females. Included search Register has been computerized since April 1, were all cohort members with data on prenatal exposure 1969.23 It contains data on all admissions to Danish psy- to infection and personal identification number (required chiatric inpatient facilities. The period of follow-up was for checking in the Danish Psychiatric Central Research from April 1, 1969, until May 7, 2007. The diagnostic sys- Register). tem in use when the Danish Psychiatric Central Research Register was computerized was the International Classi- Prenatal Infection fication of Diseases, Eighth Revision (ICD-8). In ICD-8, When the perinatal cohort was established, Aage Villum- schizophrenia is defined by prototypic descriptions of sen was responsible for collecting information on the symptoms, such as bizarre delusions, delusions of con- mother’s background and the course of pregnancy.19 trol, abnormal affect, autism, hallucinations, and disor- He interviewed all mothers 5 days after delivery and ganized thinking. In 1994, the more operational ICD-10 about 67% of the mothers at their first visit to the ante- criteria were implemented (the ICD-9 classification was natal clinic (these mothers received a form for recording never implemented in Denmark). The cohort and their all illness, including common colds, during the remaining parents were followed in the Danish Psychiatric Central part of pregnancy). For all mothers, data collection was Research Register to identify all admissions with a diag- completed 5 days after delivery and included information nosis of schizophrenia (ICD-8 code 295 or ICD-10 code about infections during different periods of pregnancy. F20). Cohort members were categorized as cases if they A bacterial infection was coded as present if a medical had been admitted with schizophrenia according to ICD- diagnosis had been made and medical treatment insti- 8 (narrow definition) or ICD-8 and/or ICD-10 (broad tuted, for instance, by a general practitioner, a gynaecol- definition). ogist/obstetrician, or acute treatment at a hospital (a diagnosis of a bacterial infection did not necessarily Data Analysis include paraclinical verification). The following catego- Binary variables were used to indicate the presence or ab- ries of bacterial infection were recorded: sinusitis, tonsil- sence of bacterial or viral infection in each trimester of litis, pneumonia, cystitis, pyelonephritis, bacterial pregnancy and to indicate any analgesics exposure during venereal infection, and any other bacterial infection. pregnancy. As described, social status was coded into A viral infection was judged to be present if (1) a medical 3 categories (high, low, and missing) with low social sta- diagnosis had been made (commonly by the general prac- tus as the reference category. titioner) or (2) if symptoms consistent with minor respi- We examined the effect of prenatal exposure to infec- ratory
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