Maternal Serum and Placental Metabolomes in Association with Prenatal Phthalate Exposure and Neurodevelopmental Outcomes in the MARBLES Cohort

Prenatal exposure to phthalates, a family of endocrine-disrupting plasticizers, is associated with disruption of maternal metabolism and impaired neurodevelopment. We investigated associations between prenatal phthalate exposure and alterations of both the maternal third trimester serum metabolome a...

Full description

Bibliographic Details
Main Authors: Mariana Parenti, Rebecca J. Schmidt, Sally Ozonoff, Hyeong-Moo Shin, Daniel J. Tancredi, Paula Krakowiak, Irva Hertz-Picciotto, Cheryl K. Walker, Carolyn M. Slupsky
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:Metabolites
Subjects:
Online Access:https://www.mdpi.com/2218-1989/12/9/829
_version_ 1797484910512963584
author Mariana Parenti
Rebecca J. Schmidt
Sally Ozonoff
Hyeong-Moo Shin
Daniel J. Tancredi
Paula Krakowiak
Irva Hertz-Picciotto
Cheryl K. Walker
Carolyn M. Slupsky
author_facet Mariana Parenti
Rebecca J. Schmidt
Sally Ozonoff
Hyeong-Moo Shin
Daniel J. Tancredi
Paula Krakowiak
Irva Hertz-Picciotto
Cheryl K. Walker
Carolyn M. Slupsky
author_sort Mariana Parenti
collection DOAJ
description Prenatal exposure to phthalates, a family of endocrine-disrupting plasticizers, is associated with disruption of maternal metabolism and impaired neurodevelopment. We investigated associations between prenatal phthalate exposure and alterations of both the maternal third trimester serum metabolome and the placental metabolome at birth, and associations of these with child neurodevelopmental outcomes using data and samples from the Markers of Autism Risk in Babies Learning Early Signs (MARBLES) cohort. The third trimester serum (<i>n</i> = 106) and placental (<i>n</i> = 132) metabolomes were investigated using <sup>1</sup>H nuclear magnetic resonance spectroscopy. Children were assessed clinically for autism spectrum disorder (ASD) and cognitive development. Although none of the urinary phthalate metabolite concentrations were associated with maternal serum metabolites after adjustment for covariates, mixture analysis using quantile g-computation revealed alterations in placental metabolites with increasing concentrations of phthalate metabolites that included reduced concentrations of 2-hydoxybutyrate, carnitine, <i>O</i>-acetylcarnitine, glucitol, and <i>N</i>-acetylneuraminate. Child neurodevelopmental outcome was not associated with the third trimester serum metabolome, but it was correlated with the placental metabolome in male children only. Maternal phthalate exposure during pregnancy is associated with differences in the placental metabolome at delivery, and the placental metabolome is associated with neurodevelopmental outcomes in males in a cohort with high familial ASD risk.
first_indexed 2024-03-09T23:11:12Z
format Article
id doaj.art-db10e6a701d74eee88595fbcd73b8561
institution Directory Open Access Journal
issn 2218-1989
language English
last_indexed 2024-03-09T23:11:12Z
publishDate 2022-09-01
publisher MDPI AG
record_format Article
series Metabolites
spelling doaj.art-db10e6a701d74eee88595fbcd73b85612023-11-23T17:44:20ZengMDPI AGMetabolites2218-19892022-09-0112982910.3390/metabo12090829Maternal Serum and Placental Metabolomes in Association with Prenatal Phthalate Exposure and Neurodevelopmental Outcomes in the MARBLES CohortMariana Parenti0Rebecca J. Schmidt1Sally Ozonoff2Hyeong-Moo Shin3Daniel J. Tancredi4Paula Krakowiak5Irva Hertz-Picciotto6Cheryl K. Walker7Carolyn M. Slupsky8Department of Nutrition, University of California, Davis, CA 95616, USADepartment of Public Health Sciences, University of California, Davis, CA 95616, USAMedical Investigation of Neurodevelopmental Disorders (MIND) Institute, University of California, Davis, CA 95616, USADepartment of Environmental Science, Baylor University, Waco, TX 76798, USADepartment of Pediatrics, School of Medicine, University of California, Davis, CA 95616, USADepartment of Public Health Sciences, University of California, Davis, CA 95616, USADepartment of Public Health Sciences, University of California, Davis, CA 95616, USAMedical Investigation of Neurodevelopmental Disorders (MIND) Institute, University of California, Davis, CA 95616, USADepartment of Nutrition, University of California, Davis, CA 95616, USAPrenatal exposure to phthalates, a family of endocrine-disrupting plasticizers, is associated with disruption of maternal metabolism and impaired neurodevelopment. We investigated associations between prenatal phthalate exposure and alterations of both the maternal third trimester serum metabolome and the placental metabolome at birth, and associations of these with child neurodevelopmental outcomes using data and samples from the Markers of Autism Risk in Babies Learning Early Signs (MARBLES) cohort. The third trimester serum (<i>n</i> = 106) and placental (<i>n</i> = 132) metabolomes were investigated using <sup>1</sup>H nuclear magnetic resonance spectroscopy. Children were assessed clinically for autism spectrum disorder (ASD) and cognitive development. Although none of the urinary phthalate metabolite concentrations were associated with maternal serum metabolites after adjustment for covariates, mixture analysis using quantile g-computation revealed alterations in placental metabolites with increasing concentrations of phthalate metabolites that included reduced concentrations of 2-hydoxybutyrate, carnitine, <i>O</i>-acetylcarnitine, glucitol, and <i>N</i>-acetylneuraminate. Child neurodevelopmental outcome was not associated with the third trimester serum metabolome, but it was correlated with the placental metabolome in male children only. Maternal phthalate exposure during pregnancy is associated with differences in the placental metabolome at delivery, and the placental metabolome is associated with neurodevelopmental outcomes in males in a cohort with high familial ASD risk.https://www.mdpi.com/2218-1989/12/9/829autismphthalatesprenatal exposureNMRplacentaserum
spellingShingle Mariana Parenti
Rebecca J. Schmidt
Sally Ozonoff
Hyeong-Moo Shin
Daniel J. Tancredi
Paula Krakowiak
Irva Hertz-Picciotto
Cheryl K. Walker
Carolyn M. Slupsky
Maternal Serum and Placental Metabolomes in Association with Prenatal Phthalate Exposure and Neurodevelopmental Outcomes in the MARBLES Cohort
Metabolites
autism
phthalates
prenatal exposure
NMR
placenta
serum
title Maternal Serum and Placental Metabolomes in Association with Prenatal Phthalate Exposure and Neurodevelopmental Outcomes in the MARBLES Cohort
title_full Maternal Serum and Placental Metabolomes in Association with Prenatal Phthalate Exposure and Neurodevelopmental Outcomes in the MARBLES Cohort
title_fullStr Maternal Serum and Placental Metabolomes in Association with Prenatal Phthalate Exposure and Neurodevelopmental Outcomes in the MARBLES Cohort
title_full_unstemmed Maternal Serum and Placental Metabolomes in Association with Prenatal Phthalate Exposure and Neurodevelopmental Outcomes in the MARBLES Cohort
title_short Maternal Serum and Placental Metabolomes in Association with Prenatal Phthalate Exposure and Neurodevelopmental Outcomes in the MARBLES Cohort
title_sort maternal serum and placental metabolomes in association with prenatal phthalate exposure and neurodevelopmental outcomes in the marbles cohort
topic autism
phthalates
prenatal exposure
NMR
placenta
serum
url https://www.mdpi.com/2218-1989/12/9/829
work_keys_str_mv AT marianaparenti maternalserumandplacentalmetabolomesinassociationwithprenatalphthalateexposureandneurodevelopmentaloutcomesinthemarblescohort
AT rebeccajschmidt maternalserumandplacentalmetabolomesinassociationwithprenatalphthalateexposureandneurodevelopmentaloutcomesinthemarblescohort
AT sallyozonoff maternalserumandplacentalmetabolomesinassociationwithprenatalphthalateexposureandneurodevelopmentaloutcomesinthemarblescohort
AT hyeongmooshin maternalserumandplacentalmetabolomesinassociationwithprenatalphthalateexposureandneurodevelopmentaloutcomesinthemarblescohort
AT danieljtancredi maternalserumandplacentalmetabolomesinassociationwithprenatalphthalateexposureandneurodevelopmentaloutcomesinthemarblescohort
AT paulakrakowiak maternalserumandplacentalmetabolomesinassociationwithprenatalphthalateexposureandneurodevelopmentaloutcomesinthemarblescohort
AT irvahertzpicciotto maternalserumandplacentalmetabolomesinassociationwithprenatalphthalateexposureandneurodevelopmentaloutcomesinthemarblescohort
AT cherylkwalker maternalserumandplacentalmetabolomesinassociationwithprenatalphthalateexposureandneurodevelopmentaloutcomesinthemarblescohort
AT carolynmslupsky maternalserumandplacentalmetabolomesinassociationwithprenatalphthalateexposureandneurodevelopmentaloutcomesinthemarblescohort