Prenatal exposure to polycyclic aromatic hydrocarbons and executive functions at school age: Results from a combined cohort study
Executive functions develop rapidly in childhood, enabling problem-solving, focused attention, and planning. Exposures to environmental toxicants in pregnancy may impair healthy executive function development in children. There is increasing concern regarding polycyclic aromatic hydrocarbons (PAHs)...
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creator | Ni, Yu Szpiro, Adam A. Loftus, Christine T. Workman, Tomomi Sullivan, Alexis Wallace, Erin R. Riederer, Anne M. Day, Drew B. Murphy, Laura E. Nguyen, Ruby H.N. Sathyanarayana, Sheela Barrett, Emily S. Zhao, Qi Enquobahrie, Daniel A. Simpson, Christopher Ahmad, Shaikh I. Arizaga, Jessica A. Collett, Brent R. Derefinko, Karen J. Kannan, Kurunthachalam Bush, Nicole R. LeWinn, Kaja Z. Karr, Catherine J. |
description | Executive functions develop rapidly in childhood, enabling problem-solving, focused attention, and planning. Exposures to environmental toxicants in pregnancy may impair healthy executive function development in children. There is increasing concern regarding polycyclic aromatic hydrocarbons (PAHs) given their ability to transfer across the placenta and the fetal blood-brain barrier, yet evidence from epidemiological studies is limited.
We examined associations between prenatal PAH exposure and executive functions in 814 children of non-smoking mothers from two U.S. cohorts in the ECHO-PATHWAYS Consortium. Seven mono-hydroxylated PAH metabolites were measured in mid-pregnancy urine and analyzed individually and as mixtures. Three executive function domains were measured at age 8–9: cognitive flexibility, working memory, and inhibitory control. A composite score quantifying overall performance was further calculated. We fitted linear regressions adjusted for socio-demographics, maternal health behaviors, and psychological measures, and examined modification by child sex and stressful life events in pregnancy. Bayesian kernel machine regression was performed to estimate the interactive and overall effects of the PAH mixture.
The results from primary analysis of linear regressions were generally null, and no modification by child sex or maternal stress was indicated. Mixture analyses suggested several pairwise interactions between individual PAH metabolites in varied directions on working memory, particularly interactions between 2/3/9-FLUO and other PAH metabolites, but no overall or individual effects were evident.
We conducted a novel exploration of PAH-executive functions association in a large, combined sample from two cohorts. Although findings were predominantly null, the study carries important implications for future research and contributes to evolving science regarding developmental origins of diseases.
•The PAH-executive functions associations were predominantly null.•Evidence suggested pairwise interactions between PAH metabolites on working memory.•Results did not support the “double jeopardy” of PAHs and maternal stress on executive functions. |
doi_str_mv | 10.1016/j.ijheh.2024.114407 |
format | Article |
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We examined associations between prenatal PAH exposure and executive functions in 814 children of non-smoking mothers from two U.S. cohorts in the ECHO-PATHWAYS Consortium. Seven mono-hydroxylated PAH metabolites were measured in mid-pregnancy urine and analyzed individually and as mixtures. Three executive function domains were measured at age 8–9: cognitive flexibility, working memory, and inhibitory control. A composite score quantifying overall performance was further calculated. We fitted linear regressions adjusted for socio-demographics, maternal health behaviors, and psychological measures, and examined modification by child sex and stressful life events in pregnancy. Bayesian kernel machine regression was performed to estimate the interactive and overall effects of the PAH mixture.
The results from primary analysis of linear regressions were generally null, and no modification by child sex or maternal stress was indicated. Mixture analyses suggested several pairwise interactions between individual PAH metabolites in varied directions on working memory, particularly interactions between 2/3/9-FLUO and other PAH metabolites, but no overall or individual effects were evident.
We conducted a novel exploration of PAH-executive functions association in a large, combined sample from two cohorts. Although findings were predominantly null, the study carries important implications for future research and contributes to evolving science regarding developmental origins of diseases.
•The PAH-executive functions associations were predominantly null.•Evidence suggested pairwise interactions between PAH metabolites on working memory.•Results did not support the “double jeopardy” of PAHs and maternal stress on executive functions.</description><identifier>ISSN: 1438-4639</identifier><identifier>ISSN: 1618-131X</identifier><identifier>EISSN: 1618-131X</identifier><identifier>DOI: 10.1016/j.ijheh.2024.114407</identifier><identifier>PMID: 38879913</identifier><language>eng</language><publisher>Germany: Elsevier GmbH</publisher><subject>Adult ; Child ; Cohort Studies ; Environmental Pollutants - urine ; Executive Function - drug effects ; Executive functions ; Female ; Humans ; Male ; Maternal Exposure ; Maternal psychosocial stress ; Memory, Short-Term - drug effects ; Mixture analysis ; Polycyclic aromatic hydrocarbons ; Polycyclic Aromatic Hydrocarbons - urine ; Pregnancy ; Prenatal Exposure Delayed Effects</subject><ispartof>International journal of hygiene and environmental health, 2024-07, Vol.260, p.114407, Article 114407</ispartof><rights>2024 The Authors</rights><rights>Copyright © 2024 The Authors. Published by Elsevier GmbH.. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c354t-bd17bc789352b90e8c68ca3f2324b9a9770b29fe77ca7f38fbbc54a01d6d387c3</cites><orcidid>0000-0003-1399-6583 ; 0000-0002-8245-7279 ; 0000-0003-0217-9975 ; 0000-0001-8753-0220 ; 0000-0001-5662-278X ; 0000-0002-0729-4326 ; 0000-0003-1024-8184 ; 0000-0001-6552-898X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1438463924000889$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38879913$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ni, Yu</creatorcontrib><creatorcontrib>Szpiro, Adam A.</creatorcontrib><creatorcontrib>Loftus, Christine T.</creatorcontrib><creatorcontrib>Workman, Tomomi</creatorcontrib><creatorcontrib>Sullivan, Alexis</creatorcontrib><creatorcontrib>Wallace, Erin R.</creatorcontrib><creatorcontrib>Riederer, Anne M.</creatorcontrib><creatorcontrib>Day, Drew B.</creatorcontrib><creatorcontrib>Murphy, Laura E.</creatorcontrib><creatorcontrib>Nguyen, Ruby H.N.</creatorcontrib><creatorcontrib>Sathyanarayana, Sheela</creatorcontrib><creatorcontrib>Barrett, Emily S.</creatorcontrib><creatorcontrib>Zhao, Qi</creatorcontrib><creatorcontrib>Enquobahrie, Daniel A.</creatorcontrib><creatorcontrib>Simpson, Christopher</creatorcontrib><creatorcontrib>Ahmad, Shaikh I.</creatorcontrib><creatorcontrib>Arizaga, Jessica A.</creatorcontrib><creatorcontrib>Collett, Brent R.</creatorcontrib><creatorcontrib>Derefinko, Karen J.</creatorcontrib><creatorcontrib>Kannan, Kurunthachalam</creatorcontrib><creatorcontrib>Bush, Nicole R.</creatorcontrib><creatorcontrib>LeWinn, Kaja Z.</creatorcontrib><creatorcontrib>Karr, Catherine J.</creatorcontrib><title>Prenatal exposure to polycyclic aromatic hydrocarbons and executive functions at school age: Results from a combined cohort study</title><title>International journal of hygiene and environmental health</title><addtitle>Int J Hyg Environ Health</addtitle><description>Executive functions develop rapidly in childhood, enabling problem-solving, focused attention, and planning. Exposures to environmental toxicants in pregnancy may impair healthy executive function development in children. There is increasing concern regarding polycyclic aromatic hydrocarbons (PAHs) given their ability to transfer across the placenta and the fetal blood-brain barrier, yet evidence from epidemiological studies is limited.
We examined associations between prenatal PAH exposure and executive functions in 814 children of non-smoking mothers from two U.S. cohorts in the ECHO-PATHWAYS Consortium. Seven mono-hydroxylated PAH metabolites were measured in mid-pregnancy urine and analyzed individually and as mixtures. Three executive function domains were measured at age 8–9: cognitive flexibility, working memory, and inhibitory control. A composite score quantifying overall performance was further calculated. We fitted linear regressions adjusted for socio-demographics, maternal health behaviors, and psychological measures, and examined modification by child sex and stressful life events in pregnancy. Bayesian kernel machine regression was performed to estimate the interactive and overall effects of the PAH mixture.
The results from primary analysis of linear regressions were generally null, and no modification by child sex or maternal stress was indicated. Mixture analyses suggested several pairwise interactions between individual PAH metabolites in varied directions on working memory, particularly interactions between 2/3/9-FLUO and other PAH metabolites, but no overall or individual effects were evident.
We conducted a novel exploration of PAH-executive functions association in a large, combined sample from two cohorts. Although findings were predominantly null, the study carries important implications for future research and contributes to evolving science regarding developmental origins of diseases.
•The PAH-executive functions associations were predominantly null.•Evidence suggested pairwise interactions between PAH metabolites on working memory.•Results did not support the “double jeopardy” of PAHs and maternal stress on executive functions.</description><subject>Adult</subject><subject>Child</subject><subject>Cohort Studies</subject><subject>Environmental Pollutants - urine</subject><subject>Executive Function - drug effects</subject><subject>Executive functions</subject><subject>Female</subject><subject>Humans</subject><subject>Male</subject><subject>Maternal Exposure</subject><subject>Maternal psychosocial stress</subject><subject>Memory, Short-Term - drug effects</subject><subject>Mixture analysis</subject><subject>Polycyclic aromatic hydrocarbons</subject><subject>Polycyclic Aromatic Hydrocarbons - urine</subject><subject>Pregnancy</subject><subject>Prenatal Exposure Delayed Effects</subject><issn>1438-4639</issn><issn>1618-131X</issn><issn>1618-131X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kE2L1TAUhoMozjj6CwTJ0k2vSdPbJIILGfyCAUUU3IXk5NTm0jbXJB2mS_-5mbmjSxchL-F5zyEPIc8523HG-1eHXTiMOO5a1nY7zruOyQfknPdcNVzwHw9r7oRqul7oM_Ik5wNjLWdKPyZnQimpNRfn5PeXhIstdqJ4c4x5TUhLpMc4bbDBFIDaFGdbahg3nyLY5OKSqV18LSCsJVwjHdYFSrh7LzTDGONE7U98Tb9iXqeS6VCHUEshzi4s6GsYY6poWf32lDwa7JTx2f19Qb6_f_ft8mNz9fnDp8u3Vw2IfVca57l0IJUW-9Zphgp6BVYMrWg7p62WkrlWDyglWDkINTgH-84y7nsvlARxQV6e5h5T_LViLmYOGXCa7IJxzUawXnPZ1lNRcUIhxZwTDuaYwmzTZjgzt-7Nwdy5N7fuzcl9bb24X7C6Gf2_zl_ZFXhzArB-8zpgMhkCLoA-JIRifAz_XfAHKkOZaw</recordid><startdate>202407</startdate><enddate>202407</enddate><creator>Ni, Yu</creator><creator>Szpiro, Adam A.</creator><creator>Loftus, Christine T.</creator><creator>Workman, Tomomi</creator><creator>Sullivan, Alexis</creator><creator>Wallace, Erin R.</creator><creator>Riederer, Anne M.</creator><creator>Day, Drew B.</creator><creator>Murphy, Laura E.</creator><creator>Nguyen, Ruby H.N.</creator><creator>Sathyanarayana, Sheela</creator><creator>Barrett, Emily S.</creator><creator>Zhao, Qi</creator><creator>Enquobahrie, Daniel A.</creator><creator>Simpson, Christopher</creator><creator>Ahmad, Shaikh I.</creator><creator>Arizaga, Jessica A.</creator><creator>Collett, Brent R.</creator><creator>Derefinko, Karen J.</creator><creator>Kannan, Kurunthachalam</creator><creator>Bush, Nicole R.</creator><creator>LeWinn, Kaja Z.</creator><creator>Karr, Catherine J.</creator><general>Elsevier GmbH</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-1399-6583</orcidid><orcidid>https://orcid.org/0000-0002-8245-7279</orcidid><orcidid>https://orcid.org/0000-0003-0217-9975</orcidid><orcidid>https://orcid.org/0000-0001-8753-0220</orcidid><orcidid>https://orcid.org/0000-0001-5662-278X</orcidid><orcidid>https://orcid.org/0000-0002-0729-4326</orcidid><orcidid>https://orcid.org/0000-0003-1024-8184</orcidid><orcidid>https://orcid.org/0000-0001-6552-898X</orcidid></search><sort><creationdate>202407</creationdate><title>Prenatal exposure to polycyclic aromatic hydrocarbons and executive functions at school age: Results from a combined cohort study</title><author>Ni, Yu ; Szpiro, Adam A. ; Loftus, Christine T. ; Workman, Tomomi ; Sullivan, Alexis ; Wallace, Erin R. ; Riederer, Anne M. ; Day, Drew B. ; Murphy, Laura E. ; Nguyen, Ruby H.N. ; Sathyanarayana, Sheela ; Barrett, Emily S. ; Zhao, Qi ; Enquobahrie, Daniel A. ; Simpson, Christopher ; Ahmad, Shaikh I. ; Arizaga, Jessica A. ; Collett, Brent R. ; Derefinko, Karen J. ; Kannan, Kurunthachalam ; Bush, Nicole R. ; LeWinn, Kaja Z. ; Karr, Catherine J.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c354t-bd17bc789352b90e8c68ca3f2324b9a9770b29fe77ca7f38fbbc54a01d6d387c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Adult</topic><topic>Child</topic><topic>Cohort Studies</topic><topic>Environmental Pollutants - urine</topic><topic>Executive Function - drug effects</topic><topic>Executive functions</topic><topic>Female</topic><topic>Humans</topic><topic>Male</topic><topic>Maternal Exposure</topic><topic>Maternal psychosocial stress</topic><topic>Memory, Short-Term - drug effects</topic><topic>Mixture analysis</topic><topic>Polycyclic aromatic hydrocarbons</topic><topic>Polycyclic Aromatic Hydrocarbons - urine</topic><topic>Pregnancy</topic><topic>Prenatal Exposure Delayed Effects</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ni, Yu</creatorcontrib><creatorcontrib>Szpiro, Adam A.</creatorcontrib><creatorcontrib>Loftus, Christine T.</creatorcontrib><creatorcontrib>Workman, Tomomi</creatorcontrib><creatorcontrib>Sullivan, Alexis</creatorcontrib><creatorcontrib>Wallace, Erin R.</creatorcontrib><creatorcontrib>Riederer, Anne M.</creatorcontrib><creatorcontrib>Day, Drew B.</creatorcontrib><creatorcontrib>Murphy, Laura E.</creatorcontrib><creatorcontrib>Nguyen, Ruby H.N.</creatorcontrib><creatorcontrib>Sathyanarayana, Sheela</creatorcontrib><creatorcontrib>Barrett, Emily S.</creatorcontrib><creatorcontrib>Zhao, Qi</creatorcontrib><creatorcontrib>Enquobahrie, Daniel A.</creatorcontrib><creatorcontrib>Simpson, Christopher</creatorcontrib><creatorcontrib>Ahmad, Shaikh I.</creatorcontrib><creatorcontrib>Arizaga, Jessica A.</creatorcontrib><creatorcontrib>Collett, Brent R.</creatorcontrib><creatorcontrib>Derefinko, Karen J.</creatorcontrib><creatorcontrib>Kannan, Kurunthachalam</creatorcontrib><creatorcontrib>Bush, Nicole R.</creatorcontrib><creatorcontrib>LeWinn, Kaja Z.</creatorcontrib><creatorcontrib>Karr, Catherine J.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>International journal of hygiene and environmental health</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ni, Yu</au><au>Szpiro, Adam A.</au><au>Loftus, Christine T.</au><au>Workman, Tomomi</au><au>Sullivan, Alexis</au><au>Wallace, Erin R.</au><au>Riederer, Anne M.</au><au>Day, Drew B.</au><au>Murphy, Laura E.</au><au>Nguyen, Ruby H.N.</au><au>Sathyanarayana, Sheela</au><au>Barrett, Emily S.</au><au>Zhao, Qi</au><au>Enquobahrie, Daniel A.</au><au>Simpson, Christopher</au><au>Ahmad, Shaikh I.</au><au>Arizaga, Jessica A.</au><au>Collett, Brent R.</au><au>Derefinko, Karen J.</au><au>Kannan, Kurunthachalam</au><au>Bush, Nicole R.</au><au>LeWinn, Kaja Z.</au><au>Karr, Catherine J.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Prenatal exposure to polycyclic aromatic hydrocarbons and executive functions at school age: Results from a combined cohort study</atitle><jtitle>International journal of hygiene and environmental health</jtitle><addtitle>Int J Hyg Environ Health</addtitle><date>2024-07</date><risdate>2024</risdate><volume>260</volume><spage>114407</spage><pages>114407-</pages><artnum>114407</artnum><issn>1438-4639</issn><issn>1618-131X</issn><eissn>1618-131X</eissn><abstract>Executive functions develop rapidly in childhood, enabling problem-solving, focused attention, and planning. Exposures to environmental toxicants in pregnancy may impair healthy executive function development in children. There is increasing concern regarding polycyclic aromatic hydrocarbons (PAHs) given their ability to transfer across the placenta and the fetal blood-brain barrier, yet evidence from epidemiological studies is limited.
We examined associations between prenatal PAH exposure and executive functions in 814 children of non-smoking mothers from two U.S. cohorts in the ECHO-PATHWAYS Consortium. Seven mono-hydroxylated PAH metabolites were measured in mid-pregnancy urine and analyzed individually and as mixtures. Three executive function domains were measured at age 8–9: cognitive flexibility, working memory, and inhibitory control. A composite score quantifying overall performance was further calculated. We fitted linear regressions adjusted for socio-demographics, maternal health behaviors, and psychological measures, and examined modification by child sex and stressful life events in pregnancy. Bayesian kernel machine regression was performed to estimate the interactive and overall effects of the PAH mixture.
The results from primary analysis of linear regressions were generally null, and no modification by child sex or maternal stress was indicated. Mixture analyses suggested several pairwise interactions between individual PAH metabolites in varied directions on working memory, particularly interactions between 2/3/9-FLUO and other PAH metabolites, but no overall or individual effects were evident.
We conducted a novel exploration of PAH-executive functions association in a large, combined sample from two cohorts. Although findings were predominantly null, the study carries important implications for future research and contributes to evolving science regarding developmental origins of diseases.
•The PAH-executive functions associations were predominantly null.•Evidence suggested pairwise interactions between PAH metabolites on working memory.•Results did not support the “double jeopardy” of PAHs and maternal stress on executive functions.</abstract><cop>Germany</cop><pub>Elsevier GmbH</pub><pmid>38879913</pmid><doi>10.1016/j.ijheh.2024.114407</doi><orcidid>https://orcid.org/0000-0003-1399-6583</orcidid><orcidid>https://orcid.org/0000-0002-8245-7279</orcidid><orcidid>https://orcid.org/0000-0003-0217-9975</orcidid><orcidid>https://orcid.org/0000-0001-8753-0220</orcidid><orcidid>https://orcid.org/0000-0001-5662-278X</orcidid><orcidid>https://orcid.org/0000-0002-0729-4326</orcidid><orcidid>https://orcid.org/0000-0003-1024-8184</orcidid><orcidid>https://orcid.org/0000-0001-6552-898X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Adult Child Cohort Studies Environmental Pollutants - urine Executive Function - drug effects Executive functions Female Humans Male Maternal Exposure Maternal psychosocial stress Memory, Short-Term - drug effects Mixture analysis Polycyclic aromatic hydrocarbons Polycyclic Aromatic Hydrocarbons - urine Pregnancy Prenatal Exposure Delayed Effects |
title | Prenatal exposure to polycyclic aromatic hydrocarbons and executive functions at school age: Results from a combined cohort study |
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