Prenatal exposure to air pollution and childhood internalizing problems: roles of shyness and anterior cingulate cortex activity

Abstract

Background
Prenatal exposure to air pollution increases the risk for psychiatric disorders characterized by internalizing problems. In this study, we examined the roles of shyness and anterior cingulate cortex (ACC) activity in the association between prenatal exposure to polycyclic aromatic hydrocarbons (PAH) and children's internalizing problems at 7–9 years old.

Methods
Participants include 53 children (31 girls, 22 boys). Personal air monitoring was conducted over 48 continuous hours during the third trimester of pregnancy to measure 8 PAHs. Mothers reported children's shyness (Emotionality Activity Sociability Temperament Survey) at age 5 and internalizing problems (Child Behavior Checklist) at ages 7–9. ACC activity was measured by fMRI during the Simon Spatial Incompatibility task at ages 7–9.

Results
Shyness mediated the association between prenatal PAH exposure and internalizing problems. Higher prenatal PAH exposure predicted increased shyness, which in turn predicted greater internalizing problems. Moreover, left ACC activity during the Simon task moderated the association between prenatal PAH exposure and internalizing problems. Prenatal PAH exposure predicted increased risk for internalizing problems only when children showed heightened left ACC activity during the resolution of cognitive conflict.

Conclusions
Our study innovatively synthesizes the fields of developmental psychology and environmental health science to offer new insights into the risk factors for anxiety disorders. Facilitating the development of healthy reactive and regulatory processes may improve the developmental outcomes for children highly exposed to air pollution.

Full text

Prenatal exposure to air pollution and childhood
internalizing problems: roles of shyness and anterior
cingulate cortex activity
Ran Liu,
1,2,3
David Pagliaccio,
1,2
Julie B. Herbstman,
4,5
Nathan A. Fox,
6,7
and
Amy E. Margolis
1,2
1
Division of Child and Adolescent Psychiatry, New York State Psychiatric Institute, New York, NY, USA;
2
Department
of Psychiatry, Vagelos College of Physicians and Surgeons, Columbia University, New York, NY, USA;
3
Faculty of
Psychology, Beijing Normal University, Beijing, China;
4
Department of Environmental Health Sciences, Mailman
School of Public Health, Columbia University, New York, NY, USA;
5
Columbia Center for Children’s Environmental
Health, Mailman School of Public Health, Columbia University, New York, NY, USA;
6
Neuroscience and Cognitive
Science Program, University of Maryland, College Park, MD, USA;
7
Department of Human Development and
Quantitative Methodology, University of Maryland, College Park, MD, USA
Background: Prenatal exposure to air pollution increases the risk for psychiatric disorders characterized by
internalizing problems. In this study, we examined the roles of shyness and anterior cingulate cortex (ACC) activity in
the association between prenatal exposure to polycyclic aromatic hydrocarbons (PAH) and children’s internalizing
problems at 7–9 years old. Methods: Participants include 53 children (31 girls, 22 boys). Personal air monitoring was
conducted over 48 continuous hours during the third trimester of pregnancy to measure 8 PAHs. Mothers reported
children’s shyness (Emotionality Activity Sociability Temperament Survey) at age 5 and internalizing problems (Child
Behavior Checklist) at ages 7–9. ACC activity was measured by fMRI during the Simon Spatial Incompatibility task at
ages 7–9. Results: Shyness mediated the association between prenatal PAH exposure and internalizing problems.
Higher prenatal PAH exposure predicted increased shyness, which in turn predicted greater internalizing problems.
Moreover, left ACC activity during the Simon task moderated the association between prenatal PAH exposure and
internalizing problems. Prenatal PAH exposure predicted increased risk for internalizing problems only when
children showed heightened left ACC activity during the resolution of cognitive conflict. Conclusions: Our study
innovatively synthesizes the fields of developmental psychology and environmental health science to offer new
insights into the risk factors for anxiety disorders. Facilitating the development of healthy reactive and regulatory
processes may improve the developmental outcomes for children highly exposed to air pollution. Keywords: Air
pollution; polycyclic aromatic hydrocarbons; prenatal; internalizing problems; shyness; anterior cingulate cortex.
Introduction
Polycyclic aromatic hydrocarbons (PAHs) are air
pollutants generated by the incomplete combustion
of fossil fuel, tobacco, and other organic material
(Bostr€
om et al., 2002). PAH enters the human body
mainly through food consumption, air inhalation,
dust ingestion, and dermal contact (Zhang et
al., 2021) and can cross the placenta and fetal
blood–brain barrier (Drwal, Rak, & Gregoraszc-
zuk, 2019). Critically, the fetal brain is extremely
vulnerable to PAH exposure because it is undergoing
rapid development, particularly in the third trimes-
ter of pregnancy (Andescavage et al., 2017). Human
epidemiologic studies have linked prenatal exposure
to PAH with dimensions of psychiatric symptoms
(Volk et al., 2021) including internalizing problems,
attention problems, and ADHD (Genkinger et
al., 2015; Perera et al., 2011,2012, Perera et
al., 2014). Little is understood, however, about the
biological and cognitive pathways that link prenatal
exposure to PAH with psychiatric problems.
Shyness is a key risk factor for the onset of
internalizing problems (Liu, Calkins, & Bell, 2021;
Poole, Hassan, & Schmidt, 2021) and refers to
heightened wariness and anxiety when faced with
novel people and situations (Rubin, Coplan, &
Bowker, 2009). Other risk markers for internalizing
problems that share conceptual similarities with
shyness include behavioral inhibition, social wari-
ness, and fear (Buss et al., 2013; Fox et al., 2021).
Animal models document the effects of gestational
exposure to PAH on animal behaviors that are
analogous to human risk markers of behavioral
inhibition (Margolis et al., 2022). For example,
gestational exposure to PAH increases fearful behav-
iors in zebrafish (Gao et al., 2017). In rodent models,
prenatal PAH-exposed offspring spent more time
immobile and less time exploring the inner area of
the open field, reflecting avoidant behaviors (Miller et
al., 2016). Consistent with these findings from
animal models, we recently showed that prenatal
exposure to PAH was associated with lowered infant
approach behaviors as measured by decreased
surgency (Liu et al., 2022). Such evidence linking
gestational PAH with fear and avoidance behaviors
suggests that prenatal PAH exposure may be
Conflict of interest statement: No conflicts declared.
Ó2023 Association for Child and Adolescent Mental Health.
Journal of Child Psychology and Psychiatry 64:7 (2023), pp 1037–1044 doi:10.1111/jcpp.13768