Association between prenatal maternal anxiety and/or stress and offspring's cognitive functioning: A meta-analysis.
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ABSTRACT:
SUBMITTER: Delagneau G
PROVIDER: S-EPMC10952806 | biostudies-literature | 2023 May
REPOSITORIES: biostudies-literature
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Association between prenatal maternal anxiety and/or stress and offspring's cognitive functioning: A meta-analysis.
Delagneau Garance G Twilhaar E Sabrina ES Testa Renee R van Veen Sarit S Anderson Peter P
Child development 20221229 3
This meta-analysis examined the relationship between prenatal maternal stress and/or anxiety and the outcomes of children aged 3 months to 9 years. Of the 8754 studies published before June 2021 that were synthesized, 17 conducted in Western countries were included in the meta-analysis (N<sub>total</sub> = 23,307; M<sub>males</sub> 54%; M<sub>ethnicity</sub> White 77%, Pacific 15%, African American/Black 10%, Middle Eastern 7%, Eastern 8%). Effect sizes ranged from -0.41 to 0.15. A weak negativ ...[more]
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Project description:Maternal exposure to stress during pregnancy is associated with an increased risk of psychiatric disorders in the offspring in later life. The mechanisms through which the effects of maternal stress are transmitted to the fetus are unclear, however the placenta, as the interface between mother and fetus, is likely to play a key role. Using a rat model, we investigated a role for placental oxidative stress in conveying the effects of maternal social stress to the fetus and the potential for treatment using a nanoparticle-bound antioxidant to prevent adverse outcomes in the offspring. Maternal psychosocial stress increased circulating corticosterone in the mother, but not in the fetuses. Maternal stress also induced oxidative stress in the placenta, but not in the fetal brain. Blocking oxidative stress using an antioxidant prevented the prenatal stress-induced anxiety phenotype in the male offspring, and prevented sex-specific neurobiological changes, specifically a reduction in dendrite lengths in the hippocampus, as well as reductions in the number of parvalbumin-positive neurons and GABA receptor subunits in the hippocampus and basolateral amygdala of the male offspring. Importantly, many of these effects were mimicked in neuronal cultures by application of placental-conditioned medium or fetal plasma from stressed pregnancies, indicating molecules released from the placenta may mediate the effects of prenatal stress on the fetal brain. Indeed, both placenta-conditioned medium and fetal plasma contained differentially abundant microRNAs following maternal stress, and their predicted targets were enriched for genes relevant to nervous system development and psychiatric disorders. The results highlight placental oxidative stress as a key mediator in transmitting the maternal social stress effects on the offspring's brain and behavior, and offer a potential intervention to prevent stress-induced fetal programming of affective disorders.
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Project description:Prenatal maternal stress exposure has been associated with neonatal differential DNA methylation. However, the available evidence in humans is largely based on candidate gene methylation studies, where only a few CpG sites were evaluated. The aim of this study was to examine the association between prenatal exposure to maternal stress and offspring genome-wide cord blood methylation using different methods. First, we conducted a meta-analysis and follow-up pathway analyses. Second, we used novel region discovery methods [i.e., differentially methylated regions (DMRs) analyses]. To this end, we used data from two independent population-based studies, the Generation R Study (n = 912) and the Avon Longitudinal Study of Parents and Children (ALSPAC, n = 828), to (i) measure genome-wide DNA methylation in cord blood and (ii) extract a prenatal maternal stress composite. The meta-analysis (ntotal = 1,740) revealed no epigenome-wide (meta P <1.00e-07) associations of prenatal maternal stress exposure with neonatal differential DNA methylation. Follow-up analyses of the top hits derived from our epigenome-wide meta-analysis (meta P <1.00e-04) indicated an over-representation of the methyltransferase activity pathway. We identified no Bonferroni-corrected (P <1.00e-06) DMRs associated with prenatal maternal stress exposure. Combining data from two independent population-based samples in an epigenome-wide meta-analysis, the current study indicates that there are no large effects of prenatal maternal stress exposure on neonatal DNA methylation. Such replication efforts are essential in the search for robust associations, whether derived from candidate gene methylation or epigenome-wide studies.
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Project description:ImportanceThere is widespread interest in associations between maternal perinatal depression and anxiety and offspring development; however, to date, there has been no systematic, meta-analytic review on the long-term developmental outcomes spanning infancy through adolescence.ObjectiveTo provide a comprehensive systematic review and meta-analysis of the extant literature on associations between maternal perinatal depression and anxiety and social-emotional, cognitive, language, motor, and adaptability outcomes in offspring during the first 18 years of life.Data sourcesSix databases were searched (CINAHL Complete, Cochrane Library, Embase, Informit, MEDLINE Complete, and PsycInfo) for all extant studies reporting associations between perinatal maternal mental health problems and offspring development to March 1, 2020.Study selectionStudies were included if they were published in English; had a human sample, quantitative data, a longitudinal design, and measures of perinatal depression and/or anxiety and social-emotional, cognitive, language, motor, and/or adaptability development in offspring; and investigated an association between perinatal depression or anxiety and childhood development.Data extraction and synthesisOf 27 212 articles identified, 191 were eligible for meta-analysis. Data were extracted by multiple independent observers and pooled using a fixed- or a random-effects model. A series of meta-regressions were also conducted. Data were analyzed from January 1, 2019, to March 15, 2020.Main outcomes and measuresPrimary outcomes included social-emotional, cognitive, language, motor, and adaptability development in offspring during the first 18 years of life.ResultsAfter screening, 191 unique studies were eligible for meta-analysis, with a combined sample of 195 751 unique mother-child dyads. Maternal perinatal depression and anxiety were associated with poorer offspring social-emotional (antenatal period, r = 0.21 [95% CI, 0.16-0.27]; postnatal period, r = 0.24 [95% CI, 0.19-0.28]), cognitive (antenatal period, r = -0.12 [95% CI, -0.19 to -0.05]; postnatal period, r = -0.25 [95% CI, -0.39 to -0.09]), language (antenatal period, r = -0.11 [95% CI, -0.20 to 0.02]; postnatal period, r = -0.22 [95% CI, -0.40 to 0.03]), motor (antenatal period, r = -0.07 [95% CI, -0.18 to 0.03]; postnatal period, r = -0.07 [95% CI, -0.16 to 0.03]), and adaptive behavior (antenatal period, r = -0.26 [95% CI, -0.39 to -0.12]) development. Findings extended beyond infancy, into childhood and adolescence. Meta-regressions confirmed the robustness of the results.Conclusions and relevanceEvidence suggests that perinatal depression and anxiety in mothers are adversely associated with offspring development and therefore are important targets for prevention and early intervention to support mothers transitioning into parenthood and the health and well-being of next-generation offspring.
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