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Background: Adverse in-utero and perinatal conditions might contribute to an increased suicide risk throughout the lifespan; however, existing evidence is sparse and contradictory. We aimed to investigate in-utero and perinatal exposures associated with suicide, suicide attempt, and suicidal ideation. Methods: We did a systematic review and meta-analysis and searched MEDLINE, Embase, and PsycINFO from inception to Jan 24, 2019, for population-based prospective studies that investigated the association between in-utero and perinatal factors and suicide, suicide attempt, and suicidal ideation. Only papers published in English in peer-reviewed journals were considered. Two researchers independently extracted formal information (eg, country, year, duration of follow-up) and number of cases and non-cases exposed and non-exposed to each risk factor. We calculated pooled odds ratios (ORs) with 95% CIs using random-effects models and used meta-regression to investigate heterogeneity. This study was registered with PROSPERO, number CRD42018091205. Findings: We identified 42 eligible studies; they had a low risk of bias (median quality score 9/9 [IQR 8–9]). Family or parental characteristics, such as high birth order (eg, for fourth-born or later-born vs first-born, pooled OR 1·51 [95% CIs 1·21–1·88]), teenage mothers (1·80 [1·52–2·14]), single mothers (1·57 [1·31–1·89]); indices of socioeconomic position, such as low maternal (1·36 [1·28–1·46]) and paternal (1·38 [1·27–1·51]) education; and fetal growth (eg, low birthweight 1·30 [1·09–1·55] and small for gestational age 1·18 [1·00–1·40]) were associated with higher suicide risk. Father's age, low gestational age, obstetric characteristics (eg, caesarean section), and condition or exposure during pregnancy (eg, maternal smoking or hypertensive disease) were not associated with higher suicide risk. Similar patterns of associations were observed for suicide attempt and suicidal ideation; however, these results were based on a lower number of studies. In meta-regression, differences in length of follow-up explained most between-study heterogeneity (inital I 2 ranged from 0 to 79·5). Interpretation: These findings suggest that prenatal and perinatal characteristics are associated with increased suicide risk during the life course, supporting the developmental origin of health and diseases hypothesis for suicide. The low number of studies for some risk factors, especially for suicide attempt and ideation, leaves gaps in knowledge that need to be addressed. The mechanisms underlying the reported associations and their causal nature still remain unclear. Funding: Horizon 2020 (EU).