Prenatal exposure to polycyclic aromatic hydrocarbons is not associated with behavior problems in preschool and early school-aged children: A prospective multi-cohort study

Erin R. Wallace; Erin Buth; Adam A. Szpiro; Yu Ni; Christine T. Loftus; Erin Masterson; Drew B. Day; Bob Z. Sun; Alexis Sullivan; Emily Barrett; Ruby HN Nguyen; Morgan Robinson; Kurunthachalam Kannan; Alex Mason; Sheela Sathyanarayana; Kaja Z. LeWinn; Nicole R. Bush; Catherine J. Karr

doi:10.1016/j.envres.2022.114759

Prenatal exposure to polycyclic aromatic hydrocarbons is not associated with behavior problems in preschool and early school-aged children: A prospective multi-cohort study

Erin R. Wallace, Erin Buth, Adam A. Szpiro, Yu Ni, Christine T. Loftus, Erin Masterson, Drew B. Day, Bob Z. Sun, Alexis Sullivan, Emily Barrett, Ruby HN Nguyen, Morgan Robinson, Kurunthachalam Kannan, Alex Mason, Sheela Sathyanarayana, Kaja Z. LeWinn, Nicole R. Bush, Catherine J. Karr

Epidemiology

Research output: Contribution to journal › Article › peer-review

5 Scopus citations

Abstract

Background: Epidemiological study findings are inconsistent regarding associations between prenatal polycyclic aromatic hydrocarbon (PAH) exposures and childhood behavior. This study examined associations of prenatal PAH exposure with behavior at age 4-6 years in a large, diverse, multi-region prospective cohort. Secondary aims included examination of PAH mixtures and effect modification by child sex, breastfeeding, and child neighborhood opportunity. Methods: The ECHO PATHWAYS Consortium pooled 1118 mother-child dyads from three prospective pregnancy cohorts in six U.S. cities. Seven PAH metabolites were measured in prenatal urine. Child behavior was assessed at age 4–6 using the Total Problems score from the Child Behavior Checklist (CBCL). Neighborhood opportunity was assessed using the socioeconomic and educational scales of the Child Opportunity Index. Multivariable linear regression was used to estimate associations per 2-fold increase in each PAH metabolite, adjusted for demographic, prenatal, and maternal factors and using interaction terms for effect modifiers. Associations with PAH mixtures were estimated using Weighted Quantile Sum Regression (WQSR). Results: The sample was racially and sociodemographically diverse (38% Black, 49% White, 7% Other; household-adjusted income range $2651-$221,102). In fully adjusted models, each 2-fold increase in 2-hydroxynaphthalene was associated with a lower Total Problems score, contrary to hypotheses (b = -0.80, 95% CI = -1.51, -0.08). Associations were notable in boys (b = -1.10, 95% CI = -2.11, -0.08) and among children breastfed 6+ months (b = -1.31, 95% CI = -2.25, -0.37), although there was no statistically significant evidence for interaction by child sex, breastfeeding, or neighborhood child opportunity. Associations were null for other PAH metabolites; there was no evidence of associations with PAH mixtures from WQSR. Conclusion: In this large, well-characterized, prospective study of mother-child pairs, prenatal PAH exposure was not associated with child behavior problems. Future studies characterizing the magnitude of prenatal PAH exposure and studies in older childhood are needed.

Original language	English (US)
Article number	114759
Journal	Environmental Research
Volume	216
DOIs	https://doi.org/10.1016/j.envres.2022.114759
State	Published - Jan 1 2023

Bibliographical note

Funding Information:
In this large, diverse, and well-characterized multi-site prospective study of mother-child pairs participating in the ECHO-PATHWAYS consortium, we examined associations of prenatal PAH exposure measured in individual OH-PAH metabolites as well as OH-PAH mixtures and child behavior at age 4 to 6 years. We did not see evidence to support our hypothesis that prenatal OH-PAH exposure was associated with higher Total Problems scores. Most associations were null. After adjustment, 2-NAP was associated with lower Total Problems scores in our main analyses and some sensitivity and secondary analyses. The magnitudes of these effect sizes were small (e.g. most estimates reflect an approximately 1-point difference in raw behavior score), were not in the hypothesized direction, and were not robust to expanded adjustment or alternative methods of adjustment for specific gravity. There was also no evidence from WQS regression of PAH mixtures on behavior scores nor evidence for effect modification by child sex, breastfeeding, neighborhood social and economic or educational opportunity.ECHO PATHWAYS is funded by NIH (UG3/UH3OD023271, P30ES007033). The Conditions Affecting Neurocognitive Development and Learning in Early Childhood (CANDLE) study was funded by the Urban Child Institute. The TIDES study was funded by NIH R01ES016863 and National Institute of Environmental Health Sciences (NIEHS) Intramural Funding (ZIA10331): Reproductive outcomes and oxidative stress in TIDES (ROOST). Dr. Kannan analyzed OH-PAH metabolites in TIDES with support from the New York University ECHO Cohort Center (UG3/UH3OD023305 (PI: Leonardo Trasande)). Research including Global Alliance to Prevent Prematurity and Stillbirth (GAPPS) participants was conducted using specimens and data collected and stored on behalf of the GAPPS Repository. We are grateful for the participation of families enrolled in the CANDLE, TIDES, and GAPPS cohort, as well as the dedication of CANDLE, TIDES, and GAPPS research staff and investigators. This manuscript has been reviewed by PATHWAYS for scientific content and consistency of data interpretation with previous PATHWAYS publications.

Funding Information:
ECHO PATHWAYS is funded by NIH ( UG3/UH3OD023271 , P30ES007033 ). The Conditions Affecting Neurocognitive Development and Learning in Early Childhood (CANDLE) study was funded by the Urban Child Institute. The TIDES study was funded by NIH R01ES016863 and National Institute of Environmental Health Sciences ( NIEHS ) Intramural Funding ( ZIA10331 ): Reproductive outcomes and oxidative stress in TIDES (ROOST). Dr. Kannan analyzed OH-PAH metabolites in TIDES with support from the New York University ECHO Cohort Center ( UG3/UH3OD023305 (PI: Leonardo Trasande)). Research including Global Alliance to Prevent Prematurity and Stillbirth (GAPPS) participants was conducted using specimens and data collected and stored on behalf of the GAPPS Repository. We are grateful for the participation of families enrolled in the CANDLE, TIDES, and GAPPS cohort, as well as the dedication of CANDLE, TIDES, and GAPPS research staff and investigators. This manuscript has been reviewed by PATHWAYS for scientific content and consistency of data interpretation with previous PATHWAYS publications.

Publisher Copyright:
© 2022 The Authors

Keywords

Behavioral development
Neurodevelopment
Polycyclic aromatic hydrocarbons
Prenatal

PubMed: MeSH publication types

Journal Article
Research Support, N.I.H., Intramural
Research Support, N.I.H., Extramural

Access

10.1016/j.envres.2022.114759

OpenUrl availability

Full text

Cite this

Wallace, E. R., Buth, E., Szpiro, A. A., Ni, Y., Loftus, C. T., Masterson, E., Day, D. B., Sun, B. Z., Sullivan, A., Barrett, E., Nguyen, R. HN., Robinson, M., Kannan, K., Mason, A., Sathyanarayana, S., LeWinn, K. Z., Bush, N. R., & Karr, C. J. (2023). Prenatal exposure to polycyclic aromatic hydrocarbons is not associated with behavior problems in preschool and early school-aged children: A prospective multi-cohort study. Environmental Research, 216, Article 114759. https://doi.org/10.1016/j.envres.2022.114759

Wallace, ER, Buth, E, Szpiro, AA, Ni, Y, Loftus, CT, Masterson, E, Day, DB, Sun, BZ, Sullivan, A, Barrett, E, Nguyen, RHN, Robinson, M, Kannan, K, Mason, A, Sathyanarayana, S, LeWinn, KZ, Bush, NR & Karr, CJ 2023, 'Prenatal exposure to polycyclic aromatic hydrocarbons is not associated with behavior problems in preschool and early school-aged children: A prospective multi-cohort study', Environmental Research, vol. 216, 114759. https://doi.org/10.1016/j.envres.2022.114759

@article{dd62f4ea62014c2f9381239bb5f8efcf,

title = "Prenatal exposure to polycyclic aromatic hydrocarbons is not associated with behavior problems in preschool and early school-aged children: A prospective multi-cohort study",

abstract = "Background: Epidemiological study findings are inconsistent regarding associations between prenatal polycyclic aromatic hydrocarbon (PAH) exposures and childhood behavior. This study examined associations of prenatal PAH exposure with behavior at age 4-6 years in a large, diverse, multi-region prospective cohort. Secondary aims included examination of PAH mixtures and effect modification by child sex, breastfeeding, and child neighborhood opportunity. Methods: The ECHO PATHWAYS Consortium pooled 1118 mother-child dyads from three prospective pregnancy cohorts in six U.S. cities. Seven PAH metabolites were measured in prenatal urine. Child behavior was assessed at age 4–6 using the Total Problems score from the Child Behavior Checklist (CBCL). Neighborhood opportunity was assessed using the socioeconomic and educational scales of the Child Opportunity Index. Multivariable linear regression was used to estimate associations per 2-fold increase in each PAH metabolite, adjusted for demographic, prenatal, and maternal factors and using interaction terms for effect modifiers. Associations with PAH mixtures were estimated using Weighted Quantile Sum Regression (WQSR). Results: The sample was racially and sociodemographically diverse (38% Black, 49% White, 7% Other; household-adjusted income range $2651-$221,102). In fully adjusted models, each 2-fold increase in 2-hydroxynaphthalene was associated with a lower Total Problems score, contrary to hypotheses (b = -0.80, 95% CI = -1.51, -0.08). Associations were notable in boys (b = -1.10, 95% CI = -2.11, -0.08) and among children breastfed 6+ months (b = -1.31, 95% CI = -2.25, -0.37), although there was no statistically significant evidence for interaction by child sex, breastfeeding, or neighborhood child opportunity. Associations were null for other PAH metabolites; there was no evidence of associations with PAH mixtures from WQSR. Conclusion: In this large, well-characterized, prospective study of mother-child pairs, prenatal PAH exposure was not associated with child behavior problems. Future studies characterizing the magnitude of prenatal PAH exposure and studies in older childhood are needed.",

keywords = "Behavioral development, Neurodevelopment, Polycyclic aromatic hydrocarbons, Prenatal",

author = "Wallace, {Erin R.} and Erin Buth and Szpiro, {Adam A.} and Yu Ni and Loftus, {Christine T.} and Erin Masterson and Day, {Drew B.} and Sun, {Bob Z.} and Alexis Sullivan and Emily Barrett and Nguyen, {Ruby HN} and Morgan Robinson and Kurunthachalam Kannan and Alex Mason and Sheela Sathyanarayana and LeWinn, {Kaja Z.} and Bush, {Nicole R.} and Karr, {Catherine J.}",

note = "Funding Information: In this large, diverse, and well-characterized multi-site prospective study of mother-child pairs participating in the ECHO-PATHWAYS consortium, we examined associations of prenatal PAH exposure measured in individual OH-PAH metabolites as well as OH-PAH mixtures and child behavior at age 4 to 6 years. We did not see evidence to support our hypothesis that prenatal OH-PAH exposure was associated with higher Total Problems scores. Most associations were null. After adjustment, 2-NAP was associated with lower Total Problems scores in our main analyses and some sensitivity and secondary analyses. The magnitudes of these effect sizes were small (e.g. most estimates reflect an approximately 1-point difference in raw behavior score), were not in the hypothesized direction, and were not robust to expanded adjustment or alternative methods of adjustment for specific gravity. There was also no evidence from WQS regression of PAH mixtures on behavior scores nor evidence for effect modification by child sex, breastfeeding, neighborhood social and economic or educational opportunity.ECHO PATHWAYS is funded by NIH (UG3/UH3OD023271, P30ES007033). The Conditions Affecting Neurocognitive Development and Learning in Early Childhood (CANDLE) study was funded by the Urban Child Institute. The TIDES study was funded by NIH R01ES016863 and National Institute of Environmental Health Sciences (NIEHS) Intramural Funding (ZIA10331): Reproductive outcomes and oxidative stress in TIDES (ROOST). Dr. Kannan analyzed OH-PAH metabolites in TIDES with support from the New York University ECHO Cohort Center (UG3/UH3OD023305 (PI: Leonardo Trasande)). Research including Global Alliance to Prevent Prematurity and Stillbirth (GAPPS) participants was conducted using specimens and data collected and stored on behalf of the GAPPS Repository. We are grateful for the participation of families enrolled in the CANDLE, TIDES, and GAPPS cohort, as well as the dedication of CANDLE, TIDES, and GAPPS research staff and investigators. This manuscript has been reviewed by PATHWAYS for scientific content and consistency of data interpretation with previous PATHWAYS publications. Funding Information: ECHO PATHWAYS is funded by NIH ( UG3/UH3OD023271 , P30ES007033 ). The Conditions Affecting Neurocognitive Development and Learning in Early Childhood (CANDLE) study was funded by the Urban Child Institute. The TIDES study was funded by NIH R01ES016863 and National Institute of Environmental Health Sciences ( NIEHS ) Intramural Funding ( ZIA10331 ): Reproductive outcomes and oxidative stress in TIDES (ROOST). Dr. Kannan analyzed OH-PAH metabolites in TIDES with support from the New York University ECHO Cohort Center ( UG3/UH3OD023305 (PI: Leonardo Trasande)). Research including Global Alliance to Prevent Prematurity and Stillbirth (GAPPS) participants was conducted using specimens and data collected and stored on behalf of the GAPPS Repository. We are grateful for the participation of families enrolled in the CANDLE, TIDES, and GAPPS cohort, as well as the dedication of CANDLE, TIDES, and GAPPS research staff and investigators. This manuscript has been reviewed by PATHWAYS for scientific content and consistency of data interpretation with previous PATHWAYS publications. Publisher Copyright: {\textcopyright} 2022 The Authors",

year = "2023",

month = jan,

day = "1",

doi = "10.1016/j.envres.2022.114759",

language = "English (US)",

volume = "216",

journal = "Environmental Research",

issn = "0013-9351",

publisher = "Academic Press Inc.",

}

TY - JOUR

T1 - Prenatal exposure to polycyclic aromatic hydrocarbons is not associated with behavior problems in preschool and early school-aged children

T2 - A prospective multi-cohort study

AU - Wallace, Erin R.

AU - Buth, Erin

AU - Szpiro, Adam A.

AU - Ni, Yu

AU - Loftus, Christine T.

AU - Masterson, Erin

AU - Day, Drew B.

AU - Sun, Bob Z.

AU - Sullivan, Alexis

AU - Barrett, Emily

AU - Nguyen, Ruby HN

AU - Robinson, Morgan

AU - Kannan, Kurunthachalam

AU - Mason, Alex

AU - Sathyanarayana, Sheela

AU - LeWinn, Kaja Z.

AU - Bush, Nicole R.

AU - Karr, Catherine J.

N1 - Funding Information: In this large, diverse, and well-characterized multi-site prospective study of mother-child pairs participating in the ECHO-PATHWAYS consortium, we examined associations of prenatal PAH exposure measured in individual OH-PAH metabolites as well as OH-PAH mixtures and child behavior at age 4 to 6 years. We did not see evidence to support our hypothesis that prenatal OH-PAH exposure was associated with higher Total Problems scores. Most associations were null. After adjustment, 2-NAP was associated with lower Total Problems scores in our main analyses and some sensitivity and secondary analyses. The magnitudes of these effect sizes were small (e.g. most estimates reflect an approximately 1-point difference in raw behavior score), were not in the hypothesized direction, and were not robust to expanded adjustment or alternative methods of adjustment for specific gravity. There was also no evidence from WQS regression of PAH mixtures on behavior scores nor evidence for effect modification by child sex, breastfeeding, neighborhood social and economic or educational opportunity.ECHO PATHWAYS is funded by NIH (UG3/UH3OD023271, P30ES007033). The Conditions Affecting Neurocognitive Development and Learning in Early Childhood (CANDLE) study was funded by the Urban Child Institute. The TIDES study was funded by NIH R01ES016863 and National Institute of Environmental Health Sciences (NIEHS) Intramural Funding (ZIA10331): Reproductive outcomes and oxidative stress in TIDES (ROOST). Dr. Kannan analyzed OH-PAH metabolites in TIDES with support from the New York University ECHO Cohort Center (UG3/UH3OD023305 (PI: Leonardo Trasande)). Research including Global Alliance to Prevent Prematurity and Stillbirth (GAPPS) participants was conducted using specimens and data collected and stored on behalf of the GAPPS Repository. We are grateful for the participation of families enrolled in the CANDLE, TIDES, and GAPPS cohort, as well as the dedication of CANDLE, TIDES, and GAPPS research staff and investigators. This manuscript has been reviewed by PATHWAYS for scientific content and consistency of data interpretation with previous PATHWAYS publications. Funding Information: ECHO PATHWAYS is funded by NIH ( UG3/UH3OD023271 , P30ES007033 ). The Conditions Affecting Neurocognitive Development and Learning in Early Childhood (CANDLE) study was funded by the Urban Child Institute. The TIDES study was funded by NIH R01ES016863 and National Institute of Environmental Health Sciences ( NIEHS ) Intramural Funding ( ZIA10331 ): Reproductive outcomes and oxidative stress in TIDES (ROOST). Dr. Kannan analyzed OH-PAH metabolites in TIDES with support from the New York University ECHO Cohort Center ( UG3/UH3OD023305 (PI: Leonardo Trasande)). Research including Global Alliance to Prevent Prematurity and Stillbirth (GAPPS) participants was conducted using specimens and data collected and stored on behalf of the GAPPS Repository. We are grateful for the participation of families enrolled in the CANDLE, TIDES, and GAPPS cohort, as well as the dedication of CANDLE, TIDES, and GAPPS research staff and investigators. This manuscript has been reviewed by PATHWAYS for scientific content and consistency of data interpretation with previous PATHWAYS publications. Publisher Copyright: © 2022 The Authors

PY - 2023/1/1

Y1 - 2023/1/1

N2 - Background: Epidemiological study findings are inconsistent regarding associations between prenatal polycyclic aromatic hydrocarbon (PAH) exposures and childhood behavior. This study examined associations of prenatal PAH exposure with behavior at age 4-6 years in a large, diverse, multi-region prospective cohort. Secondary aims included examination of PAH mixtures and effect modification by child sex, breastfeeding, and child neighborhood opportunity. Methods: The ECHO PATHWAYS Consortium pooled 1118 mother-child dyads from three prospective pregnancy cohorts in six U.S. cities. Seven PAH metabolites were measured in prenatal urine. Child behavior was assessed at age 4–6 using the Total Problems score from the Child Behavior Checklist (CBCL). Neighborhood opportunity was assessed using the socioeconomic and educational scales of the Child Opportunity Index. Multivariable linear regression was used to estimate associations per 2-fold increase in each PAH metabolite, adjusted for demographic, prenatal, and maternal factors and using interaction terms for effect modifiers. Associations with PAH mixtures were estimated using Weighted Quantile Sum Regression (WQSR). Results: The sample was racially and sociodemographically diverse (38% Black, 49% White, 7% Other; household-adjusted income range $2651-$221,102). In fully adjusted models, each 2-fold increase in 2-hydroxynaphthalene was associated with a lower Total Problems score, contrary to hypotheses (b = -0.80, 95% CI = -1.51, -0.08). Associations were notable in boys (b = -1.10, 95% CI = -2.11, -0.08) and among children breastfed 6+ months (b = -1.31, 95% CI = -2.25, -0.37), although there was no statistically significant evidence for interaction by child sex, breastfeeding, or neighborhood child opportunity. Associations were null for other PAH metabolites; there was no evidence of associations with PAH mixtures from WQSR. Conclusion: In this large, well-characterized, prospective study of mother-child pairs, prenatal PAH exposure was not associated with child behavior problems. Future studies characterizing the magnitude of prenatal PAH exposure and studies in older childhood are needed.

AB - Background: Epidemiological study findings are inconsistent regarding associations between prenatal polycyclic aromatic hydrocarbon (PAH) exposures and childhood behavior. This study examined associations of prenatal PAH exposure with behavior at age 4-6 years in a large, diverse, multi-region prospective cohort. Secondary aims included examination of PAH mixtures and effect modification by child sex, breastfeeding, and child neighborhood opportunity. Methods: The ECHO PATHWAYS Consortium pooled 1118 mother-child dyads from three prospective pregnancy cohorts in six U.S. cities. Seven PAH metabolites were measured in prenatal urine. Child behavior was assessed at age 4–6 using the Total Problems score from the Child Behavior Checklist (CBCL). Neighborhood opportunity was assessed using the socioeconomic and educational scales of the Child Opportunity Index. Multivariable linear regression was used to estimate associations per 2-fold increase in each PAH metabolite, adjusted for demographic, prenatal, and maternal factors and using interaction terms for effect modifiers. Associations with PAH mixtures were estimated using Weighted Quantile Sum Regression (WQSR). Results: The sample was racially and sociodemographically diverse (38% Black, 49% White, 7% Other; household-adjusted income range $2651-$221,102). In fully adjusted models, each 2-fold increase in 2-hydroxynaphthalene was associated with a lower Total Problems score, contrary to hypotheses (b = -0.80, 95% CI = -1.51, -0.08). Associations were notable in boys (b = -1.10, 95% CI = -2.11, -0.08) and among children breastfed 6+ months (b = -1.31, 95% CI = -2.25, -0.37), although there was no statistically significant evidence for interaction by child sex, breastfeeding, or neighborhood child opportunity. Associations were null for other PAH metabolites; there was no evidence of associations with PAH mixtures from WQSR. Conclusion: In this large, well-characterized, prospective study of mother-child pairs, prenatal PAH exposure was not associated with child behavior problems. Future studies characterizing the magnitude of prenatal PAH exposure and studies in older childhood are needed.

KW - Behavioral development

KW - Neurodevelopment

KW - Polycyclic aromatic hydrocarbons

KW - Prenatal

UR - http://www.scopus.com/inward/record.url?scp=85141964918&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85141964918&partnerID=8YFLogxK

U2 - 10.1016/j.envres.2022.114759

DO - 10.1016/j.envres.2022.114759

M3 - Article

C2 - 36370819

AN - SCOPUS:85141964918

SN - 0013-9351

VL - 216

JO - Environmental Research

JF - Environmental Research

M1 - 114759

ER -

Prenatal exposure to polycyclic aromatic hydrocarbons is not associated with behavior problems in preschool and early school-aged children: A prospective multi-cohort study

Abstract

Bibliographical note

Keywords

PubMed: MeSH publication types

Access

OpenUrl availability

Other files and links

Fingerprint

Cite this