Prenatal exposure to polycyclic aromatic hydrocarbons modifies the effects of early life stress on attention and Thought Problems in late childhood

Abstract

Background: Risk for childhood psychopathology is complex and multifactorial, implicating direct and interacting effects of familial and environmental factors. The role of environmental neurotoxicants in psychiatric risk is of growing concern, including polycyclic aromatic hydrocarbons (PAH), common in air pollution. Prenatal PAH exposure is linked to adverse physical, behavioral, and cognitive outcomes as well as increasing psychiatric risk. It is unclear whether environmental exposures, like PAH, magnify the effects of exposure to early life stress (ELS), a critical risk factor for psychopathology. The current work aimed to test potential interactions between prenatal PAH exposure and psychosocial/socioeconomic stress on psychiatric symptoms in school-age children. Methods: Data were from the Columbia Center for Children's Environmental Health Mothers and Newborns longitudinal birth cohort study. Prenatal PAH exposure was ascertained though air monitoring during pregnancy and maternal PAH-DNA adducts at delivery. Mothers reported on ELS (child age 5) and on child psychiatric symptoms across childhood (child age 5, 7, 9, and 11) using the Child Behavior Checklist (CBCL). Results: Significant prenatal airborne PAH 9 ELS interactions (FDR-corrected) predicted CBCL Attention (b = 0.22, t(307) = 3.47, p < .001, p fdr = .003) and Thought Problems Tscores (b = 0.21, t(307) = 3.29, p = .001, p fdr = .004) at age 11 (n = 319). Relative to those with lower exposure, children with higher prenatal PAH exposure exhibited stronger positive associations between ELS and CBCL Attention and Thought Problem T-scores. This interaction was also significant examining convergent ADHD measures (Conners, DuPaul) and examining maternal PAH-DNA adducts (b = 0.29, t(261) = 2.48, p = .01; n = 273). A three-way interaction with assessment wave indicated that the PAH 9 ELS interaction on Attention Problems was stronger later in development (b = 0.03, t(1,601) = 2.19, p = .03; n = 477). Conclusions: Prenatal exposure to PAH, a common neurotoxicant in air pollution, may magnify or sustain the effects of early life psychosocial/socioeconomic stress on psychiatric outcomes later in child development. This work highlights the critical role of air pollution exposure on child mental health.

Impact of Polycyclic Aromatic Hydrocarbon Exposure on Cognitive Function and Neurodegeneration in Humans. A Systematic Review and Meta-Analysis

“…Associations with anxious/ depressed behaviour were found in 3/4 studies(Perera et al 2012;Perera et al 2011;Perera et al 2013) (OR=8.89, 95%CI, 1.7 to 46.51; OR= 8.14, 95%CI, 1.21 to 54.94; OR=1.7, 95%CI, 1.08 to 2.68 respectively) with no association found byPagliaccio et al (2020). 3/5 studies reported negative effect on child attentiveness(Perera et al 2018;Pagliaccio et al 2020;Perera et al 2012) (OR=1.34, 95%, 0.85 to 1.83; OR= 2.02, 95%,…”

“…11 included cohorts from the USA. 6 selected participants from the Columbia Centre for Children's Environmental Health cohort, however each selected different subgroups of the population, and measured different outcomes (Perera et al 2006;Perera et al 2018;Perera et al 2015;Perera et al 2012;Perera et al 2011;Pagliaccio et al 2020). 2 studies selected a subgroup of participants from the National Health and Nutrition Examination Survey 2001-2002 (NHANES) (Best et al 2016), 1 of which included additional participants from the NHANES 2003-2004 cohort (Abid et al 2014).…”

“…did however report an effect on impaired thought problems (OR= 1.95, 95%CI, 1.3 to 2.91) which was contradicted byPerera et al (2013). Only 1/7 studies reported an association between PAH and social problems(Perera et al 2013) (OR= 1.57, 95%CI, 1.00 to 2.48), the remaining 6 reported no effect(Pagliaccio et al 2020;Zhang et al 2019, Perera et al 2008Tang et al 2008;Cao et al 2020).Both Perera et al (2013) andPagliaccio et al (2020) found no effect on rule breaking behaviour or somatic complaints Perera et al (2018). reported no associations with attention deficit hyperactivity disorder (ADHD) index scores, or hyperactive compulsive behaviour nor didPerera et al (2006) with total behavioural problems.…”

“…Studies with measured prenatal PAH exposure on cognitive development.Association between prenatal PAH exposure and neurobehavioral developmentChildren with a high prenatal PAH exposure were found to exhibit externalizing and internalizing behavioural problems (OR= 2.49, 95%CI, 1.57 to 3.95; OR=2.39, 95%CI, 1.51 to 3.79 respectively)(Perera et al 2013) and infants exhibited a decrease in behavioural development (OR= 2, 95%CI, 1.27 to 3.15)(Nie et al 2019). Associations with anxious/ depressed behaviour were found in 3/4 studies(Perera et al 2012;Perera et al 2011;Perera et al 2013) (OR=8.89, 95%CI, 1.7 to 46.51; OR= 8.14, 95%CI, 1.21 to 54.94; OR=1.7, 95%CI, 1.08 to 2.68 respectively) with no association found byPagliaccio et al (2020). 3/5 studies reported negative effect on child attentiveness(Perera et al 2018;Pagliaccio et al 2020;Perera et al 2012) (OR=1.34, 95%, 0.85 to 1.83; OR= 2.02, 95%,…”

“…1.35 to 3.03; OR=3.79, 95%CI, 1.14 to 12.66) whilstPerera et al (2011) andPerera et al (2013) reported no effect Perera et al (2013). report of an effect in both withdrawn/ depressed and aggressive behaviour (OR=2, 95%CI, 1.27 to 3.16; OR=2.29, 95%CI, 1.45 to 3.62 respectively) was contradicted byPagliaccio et al (2020) reporting no effect for either Pagliaccio et al (2020). did however report an effect on impaired thought problems (OR= 1.95, 95%CI, 1.3 to 2.91) which was contradicted byPerera et al (2013).…”