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Prenatal Maternal Stress and Risk of Neurodevelopmental Disorders in the Ofspring: a Systematic Review and Meta‑Analysis

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Prenatal Maternal Stress and Risk of Neurodevelopmental Disorders in the Ofspring: a Systematic Review and Meta‑Analysis Social Psychiatry and Psychiatric Epidemiology (2019) 54:1299–1309 https://doi.org/10.1007/s00127-019-01745-3 REVIEW Prenatal maternal stress and risk of neurodevelopmental disorders in the ofspring: a systematic review and meta‑analysis Nicla Manzari1,2 · Karen Matvienko‑Sikar3 · Franco Baldoni1 · Gerard W. O’Keefe4,6 · Ali S. Khashan2,3,5 Received: 6 March 2019 / Accepted: 24 June 2019 / Published online: 20 July 2019 © Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract Purpose Exposure to prenatal stress has been reported to afect the risk of adverse neurodevelopmental outcomes in the ofspring; however, there is currently no clear consensus. The aim of this systematic review and meta-analysis was to examine the existing literature on the association between prenatal stress and autism spectrum disorder (ASD) and attention-defcit hyperactivity disorder (ADHD) in the ofspring. Methods Based on a registered protocol, we searched several electronic databases for articles in accordance with a detailed search strategy. We performed this study following the Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA). Results Prenatal stress was signifcantly associated with an increased risk of both ASD (pooled OR 1.64 [95% CI 1.15–2.34]; I2 = 90%; 15 articles) and ADHD (pooled OR 1.72 [95% CI 1.27–2.34]; I2 = 85%; 12 articles). Conclusions This study suggests that prenatal stress may be associated with ASD and ADHD; however, several limitations in the reviewed literature should be noted including signifcant heterogeneity and there is a need for carefully controlled future studies in this area. Keywords Autism spectrum disorder · Attention-defcit/hyperactivity disorder · Prenatal maternal stress · Pregnancy · Mental health Introduction Gerard W. O’Keefe and Ali S. Khashan contributed equally. Electronic supplementary material The online version of this Prenatal maternal stress is a low or negative state of well- article (https ://doi.org/10.1007/s0012 7-019-01745 -3) contains being in pregnancy [1]. “Stress” in this context includes neg- supplementary material, which is available to authorized users. ative life events, anxiety and depressive symptoms. Feelings * Gerard W. O’Keefe of stress, anxiety and depression are distinct though highly [email protected] correlated constructs, all belonging to the domain of nega- * Ali S. Khashan tive emotions. The prevalence of depression, anxiety, and [email protected] stress in pregnancy has been estimated at 12%, 28% and 31%, respectively [2]. These have been suggested to infu- 1 Department of Psychology, University of Bologna, Bologna, ence neurobehavioural outcomes in exposed ofspring [3, 4]. Italy Autism spectrum disorder (ASD) and attention-defcit/ 2 The Irish Centre for Fetal and Neonatal Translational hyperactivity disorder (ADHD) are two of the most com- Research (INFANT), University College Cork, Cork, Ireland mon neurodevelopmental disorders. ASD has a prevalence 3 School of Public Health, University College Cork, Cork, of 1.7% [5] and is characterised by social defcits, impaired Ireland communication, and stereotyped and repetitive behaviours 4 Department of Anatomy and Neuroscience and Cork [6, 7]. ADHD has a prevalence of 5.3% that is character- Neuroscience Centre, University College Cork, Cork, Ireland ised by inattention, hyperactivity and impulsivity behaviour 5 University College Cork, Room 4.11, Western Gateway [8]. While genetics is crucial in their aetiology [9, 10], a Building, Western Road, Cork, Ireland population-based Swedish study has estimated the environ- 6 University College Cork, Room 4.119, Western Gateway mental variance for ASD at 17% [11]. In addition, ADHD Building, Western Road, Cork, Ireland Vol.:(0123456789)1 3 1300 Social Psychiatry and Psychiatric Epidemiology (2019) 54:1299–1309 heritability has been reported at 70–80%, suggesting that principles of the Boolean logic (AND, OR, or NOT) were environmental exposures may also play a role [12, 13]. used to combine search terms related to the exposure (pre- There is a growing literature examining the associa- natal stress) and the outcomes (ASD and ADHD) and using tion between prenatal maternal stress and risk of ASD and Medical Subject Headings as follows: (Prenatal OR Ante- ADHD in the ofspring [14–16]. For example, large popu- natal OR Pregnant) AND (Stress) OR (Distress) OR (Anxi- lation-based studies have reported signifcant associations ety) OR (Bereavement) AND (Ofspring OR Child) AND between prenatal exposure to bereavement and increased risk (Autism spectrum disorder) OR (Attention-defcit/hyperac- of ASD [15, 17] and ADHD [18]. Others have reported that tivity disorder). The detailed search strategy is presented in antenatal depressive symptoms were related to an increased the supplementary Appendix 1. The literature search was risk of ADHD [19]. Moreover, some studies have also not limited to humans although only human studies were attempted to understand the infuence of gestational age of included in the review and there was no language restriction. exposure [20, 21]. For example, two population-based Dan- The authors hand checked the bibliographies of the included ish studies reported an increased risk of ASD and ADHD studies for further potentially eligible studies. in children following maternal exposure to bereavement in the third trimester [15, 18]. Therefore, evaluating the tim- Study selection ing of the prenatal stressor is important, because trimester- specifc associations may increase the probability of a causal Two investigators (NM and GWOK) independently screened association [22]. However, there are inconsistencies in the the titles and abstracts for all articles to identify potentially literature, with some studies fnding no association between eligible studies. Titles and abstracts obtained from each prenatal maternal stress and ASD and ADHD risk [23, 24]. database were stored and managed in Endnote Reference Moreover for those studies that have reported an association, Manager X8© and duplicates were excluded using the End- there is no clear consensus on the critical gestational period note function “remove duplicates”. The two investigators [17, 25, 26]. independently examined the full texts of potentially relevant Therefore, the aim of this systematic review and meta- articles. analysis was to examine the association between prenatal maternal stress and ASD or ADHD risk in the ofspring Data extraction using available data from the published literature. Two investigators (NM and FB) extracted data using a stand- ardised data extraction form. Extracted data included author, Methods year of publication, study design, study outcome, exposure (exposure type, timing and duration), offspring gender, Protocol and search strategy data sources, sample size, defnition of the outcome used, exclusion criteria, crude and adjusted estimates (if reported, The study protocol was registered on PROSPERO including the RR, OR, HR and 95% CI). Authors of three (CDR42018084222) and subsequently published [27]. The studies [29–31] were contacted for further data, with a reply prenatal stress exposure was defned as a psychological or obtained only from one [31]. environmental stress such as stressful life events, maternal bereavement, anxiety or depressive symptoms, traumatic Bias and quality assessment events and natural disasters. The outcome measures are ASD or ADHD that could be, for example, based on medical Included studies were critically appraised by two investi- records or parent reporting. In accordance with the Preferred gators independently (NM and KMS) using the Cochrane Reporting Items for Systematic reviews and Meta-Analysis collaboration’s tool for observational studies [32], which (PRISMA) [28], a systematic literature search in PubMed, considers six domains: selection bias, exposure, outcome PsycINFO, Web of Science, EMBASE and SCOPUS was measurement, statistical analysis, study attrition and con- conducted by the frst author (NM) from inception until founding. Each study was classifed as having a high, mod- March 24th, 2018. erate, low, minimal or not reported risk of bias for each Observational studies (cohort studies and case–con- domain. Then, each study was rated as having high, mod- trol studies) evaluating the association between prenatal erate or low risk of bias, according to the total of the six maternal stress and the risk of ASD or ADHD at any time domains. For example, those with all six domains rated as before or during pregnancy or in any particular trimester minimal or low were classifed as low-risk bias studies. were considered for inclusion. Cross-sectional study design Disagreements regarding study eligibility, data extraction was included in the search strategy for completeness and or risk of bias assessment were resolved by discussion with to ensure all relevant cohort studies are identified. The another investigator (ASK). 1 3 Social Psychiatry and Psychiatric Epidemiology (2019) 54:1299–1309 1301 Statistical analysis which 22 studies were considered potentially relevant and the full text was obtained (Fig. 1a). Following reviewing All statistical analyses were performed using Review Man- the full text of the 22 articles, nine were excluded because ager software (Cochrane Collaboration Software, RevMan they did not meet the inclusion criteria (reasons for exclu- 5.3). Random-efects models using the generic inverse vari- sion are reported in Fig. 1a), resulting in 13 eligible studies. ance method were performed to calculate the
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