Early-life exposure to per- and polyfluoroalkyl substances and infant gut microbial composition

Hannah E. Laue; Yuka Moroishi; Thomas J. Palys; Brock C. Christensen; Rachel L. Criswell; Lisa A. Peterson; Carin A. Huset; Emily R. Baker; Margaret R. Karagas; Juliette C. Madan; Megan E. Romano

doi:10.1097/EE9.0000000000000238

Early-life exposure to per- and polyfluoroalkyl substances and infant gut microbial composition

Hannah E. Laue, Yuka Moroishi, Thomas J. Palys, Brock C. Christensen, Rachel L. Criswell, Lisa A. Peterson, Carin A. Huset, Emily R. Baker, Margaret R. Karagas, Juliette C. Madan, Megan E. Romano

Environmental Health Sciences

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

8 Scopus citations

Abstract

Background: Human milk is rich in essential nutrients and immune-activating compounds but is also a source of toxicants including per- and polyfluoroalkyl infstances (PFAS). Evidence suggests that immune-related effects of PFAS may, in part, be due to alterations of the microbiome. We aimed to identify the association between milk PFAS exposure and the infant gut microbiome. Methods: PFAS [perfluorooctane sulfonic acid (PFOS) and perfluorooctanoate (PFOA)] were quantified in milk from ∼6 weeks postpartum using high-performance liquid chromatography with tandem mass spectrometry. A molar sum (ΣPFAS) was calculated. Caregivers collected infant stool samples at 6 weeks (n = 116) and/or 1 year postpartum (n = 119). Stool DNA underwent metagenomic sequencing. We estimated the association of PFAS with diversity and relative abundances of species with linear regression. Single- and multi-PFAS models adjusted for potential confounders in complete case analyses and with imputed missing covariate data for 6-week and 1-year microbiomes separately. We assessed sensitive populations with stratification. Results: PFOS and PFOA were detected in 94% and 83% of milk samples, respectively. PFOS was associated with increased diversity at 6 weeks among infants fed exclusively human milk [β = 0.24 per PFOS doubling, (95% CI = 0.03, 0.45), P = 0.03] and born to primiparous mothers [β = 0.37 (0.06, 0.67), P = 0.02]. Estimates were strongest in multi-PFAS models and among complete cases. ΣPFAS was associated with Bacteroides vulgatus relative abundance at 1 year [(β = -2.34% per doubling (-3.63, -1.05), FDR q = 0.099]. Conclusions: PFAS may increase infant gut microbiome diversity and alter the relative abundance of biologically relevant bacteria. Additional analyses may identify related health outcomes.

Original language	English (US)
Pages (from-to)	E238
Journal	Environmental Epidemiology
Volume	7
Issue number	1
DOIs	https://doi.org/10.1097/EE9.0000000000000238
State	Published - Feb 14 2023

Bibliographical note

Funding Information:
Sequencing data used in this study are available through the National Center for Biotechnology Information (NCBI) Sequence Read Archive ( https://ncbi.nlm.nih.gov/sra ) under accession number PRJNA296814. Publicly available human milk PFAS data used in this study was generated through grants supported by the National Institute of Environmental Health Sciences as part of the Children’s Environmental Health Analysis Resource (CHEAR). Additional epidemiologic data are not publicly available due to their sensitive nature and identifiable nature but may be available upon request. Code is available upon request from Hannah E. Laue ( [email protected] ).

Funding Information:
This work was supported by grants P01ES022832, P42ES007373, and Minnesota CHEAR/HHEAR ES026533 from the National Institute of Environmental Health Sciences, grant P20GM104416 from the National Institute of General Medical Sciences, grant UH3OD023275 from the National Institutes of Health Office of the Director. During the preparation of this manuscript, H.E.L. was supported by T32CA134286. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Publisher Copyright:
© 2023 Wolters Kluwer Health. All rights reserved.

Keywords

Human milk
Metagenomics
Microbiome
Per- and polyfluoroalkyl infstances

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10.1097/EE9.0000000000000238

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title = "Early-life exposure to per- and polyfluoroalkyl substances and infant gut microbial composition",

abstract = "Background: Human milk is rich in essential nutrients and immune-activating compounds but is also a source of toxicants including per- and polyfluoroalkyl infstances (PFAS). Evidence suggests that immune-related effects of PFAS may, in part, be due to alterations of the microbiome. We aimed to identify the association between milk PFAS exposure and the infant gut microbiome. Methods: PFAS [perfluorooctane sulfonic acid (PFOS) and perfluorooctanoate (PFOA)] were quantified in milk from ∼6 weeks postpartum using high-performance liquid chromatography with tandem mass spectrometry. A molar sum (ΣPFAS) was calculated. Caregivers collected infant stool samples at 6 weeks (n = 116) and/or 1 year postpartum (n = 119). Stool DNA underwent metagenomic sequencing. We estimated the association of PFAS with diversity and relative abundances of species with linear regression. Single- and multi-PFAS models adjusted for potential confounders in complete case analyses and with imputed missing covariate data for 6-week and 1-year microbiomes separately. We assessed sensitive populations with stratification. Results: PFOS and PFOA were detected in 94% and 83% of milk samples, respectively. PFOS was associated with increased diversity at 6 weeks among infants fed exclusively human milk [β = 0.24 per PFOS doubling, (95% CI = 0.03, 0.45), P = 0.03] and born to primiparous mothers [β = 0.37 (0.06, 0.67), P = 0.02]. Estimates were strongest in multi-PFAS models and among complete cases. ΣPFAS was associated with Bacteroides vulgatus relative abundance at 1 year [(β = -2.34% per doubling (-3.63, -1.05), FDR q = 0.099]. Conclusions: PFAS may increase infant gut microbiome diversity and alter the relative abundance of biologically relevant bacteria. Additional analyses may identify related health outcomes.",

keywords = "Human milk, Metagenomics, Microbiome, Per- and polyfluoroalkyl infstances",

author = "Laue, {Hannah E.} and Yuka Moroishi and Palys, {Thomas J.} and Christensen, {Brock C.} and Criswell, {Rachel L.} and Peterson, {Lisa A.} and Huset, {Carin A.} and Baker, {Emily R.} and Karagas, {Margaret R.} and Madan, {Juliette C.} and Romano, {Megan E.}",

note = "Funding Information: Sequencing data used in this study are available through the National Center for Biotechnology Information (NCBI) Sequence Read Archive ( https://ncbi.nlm.nih.gov/sra ) under accession number PRJNA296814. Publicly available human milk PFAS data used in this study was generated through grants supported by the National Institute of Environmental Health Sciences as part of the Children{\textquoteright}s Environmental Health Analysis Resource (CHEAR). Additional epidemiologic data are not publicly available due to their sensitive nature and identifiable nature but may be available upon request. Code is available upon request from Hannah E. Laue ( [email protected] ). Funding Information: This work was supported by grants P01ES022832, P42ES007373, and Minnesota CHEAR/HHEAR ES026533 from the National Institute of Environmental Health Sciences, grant P20GM104416 from the National Institute of General Medical Sciences, grant UH3OD023275 from the National Institutes of Health Office of the Director. During the preparation of this manuscript, H.E.L. was supported by T32CA134286. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Publisher Copyright: {\textcopyright} 2023 Wolters Kluwer Health. All rights reserved.",

year = "2023",

month = feb,

day = "14",

doi = "10.1097/EE9.0000000000000238",

language = "English (US)",

volume = "7",

pages = "E238",

journal = "Environmental Epidemiology",

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TY - JOUR

T1 - Early-life exposure to per- and polyfluoroalkyl substances and infant gut microbial composition

AU - Laue, Hannah E.

AU - Moroishi, Yuka

AU - Palys, Thomas J.

AU - Christensen, Brock C.

AU - Criswell, Rachel L.

AU - Peterson, Lisa A.

AU - Huset, Carin A.

AU - Baker, Emily R.

AU - Karagas, Margaret R.

AU - Madan, Juliette C.

AU - Romano, Megan E.

N1 - Funding Information: Sequencing data used in this study are available through the National Center for Biotechnology Information (NCBI) Sequence Read Archive ( https://ncbi.nlm.nih.gov/sra ) under accession number PRJNA296814. Publicly available human milk PFAS data used in this study was generated through grants supported by the National Institute of Environmental Health Sciences as part of the Children’s Environmental Health Analysis Resource (CHEAR). Additional epidemiologic data are not publicly available due to their sensitive nature and identifiable nature but may be available upon request. Code is available upon request from Hannah E. Laue ( [email protected] ). Funding Information: This work was supported by grants P01ES022832, P42ES007373, and Minnesota CHEAR/HHEAR ES026533 from the National Institute of Environmental Health Sciences, grant P20GM104416 from the National Institute of General Medical Sciences, grant UH3OD023275 from the National Institutes of Health Office of the Director. During the preparation of this manuscript, H.E.L. was supported by T32CA134286. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health. Publisher Copyright: © 2023 Wolters Kluwer Health. All rights reserved.

PY - 2023/2/14

Y1 - 2023/2/14

N2 - Background: Human milk is rich in essential nutrients and immune-activating compounds but is also a source of toxicants including per- and polyfluoroalkyl infstances (PFAS). Evidence suggests that immune-related effects of PFAS may, in part, be due to alterations of the microbiome. We aimed to identify the association between milk PFAS exposure and the infant gut microbiome. Methods: PFAS [perfluorooctane sulfonic acid (PFOS) and perfluorooctanoate (PFOA)] were quantified in milk from ∼6 weeks postpartum using high-performance liquid chromatography with tandem mass spectrometry. A molar sum (ΣPFAS) was calculated. Caregivers collected infant stool samples at 6 weeks (n = 116) and/or 1 year postpartum (n = 119). Stool DNA underwent metagenomic sequencing. We estimated the association of PFAS with diversity and relative abundances of species with linear regression. Single- and multi-PFAS models adjusted for potential confounders in complete case analyses and with imputed missing covariate data for 6-week and 1-year microbiomes separately. We assessed sensitive populations with stratification. Results: PFOS and PFOA were detected in 94% and 83% of milk samples, respectively. PFOS was associated with increased diversity at 6 weeks among infants fed exclusively human milk [β = 0.24 per PFOS doubling, (95% CI = 0.03, 0.45), P = 0.03] and born to primiparous mothers [β = 0.37 (0.06, 0.67), P = 0.02]. Estimates were strongest in multi-PFAS models and among complete cases. ΣPFAS was associated with Bacteroides vulgatus relative abundance at 1 year [(β = -2.34% per doubling (-3.63, -1.05), FDR q = 0.099]. Conclusions: PFAS may increase infant gut microbiome diversity and alter the relative abundance of biologically relevant bacteria. Additional analyses may identify related health outcomes.

AB - Background: Human milk is rich in essential nutrients and immune-activating compounds but is also a source of toxicants including per- and polyfluoroalkyl infstances (PFAS). Evidence suggests that immune-related effects of PFAS may, in part, be due to alterations of the microbiome. We aimed to identify the association between milk PFAS exposure and the infant gut microbiome. Methods: PFAS [perfluorooctane sulfonic acid (PFOS) and perfluorooctanoate (PFOA)] were quantified in milk from ∼6 weeks postpartum using high-performance liquid chromatography with tandem mass spectrometry. A molar sum (ΣPFAS) was calculated. Caregivers collected infant stool samples at 6 weeks (n = 116) and/or 1 year postpartum (n = 119). Stool DNA underwent metagenomic sequencing. We estimated the association of PFAS with diversity and relative abundances of species with linear regression. Single- and multi-PFAS models adjusted for potential confounders in complete case analyses and with imputed missing covariate data for 6-week and 1-year microbiomes separately. We assessed sensitive populations with stratification. Results: PFOS and PFOA were detected in 94% and 83% of milk samples, respectively. PFOS was associated with increased diversity at 6 weeks among infants fed exclusively human milk [β = 0.24 per PFOS doubling, (95% CI = 0.03, 0.45), P = 0.03] and born to primiparous mothers [β = 0.37 (0.06, 0.67), P = 0.02]. Estimates were strongest in multi-PFAS models and among complete cases. ΣPFAS was associated with Bacteroides vulgatus relative abundance at 1 year [(β = -2.34% per doubling (-3.63, -1.05), FDR q = 0.099]. Conclusions: PFAS may increase infant gut microbiome diversity and alter the relative abundance of biologically relevant bacteria. Additional analyses may identify related health outcomes.

KW - Human milk

KW - Metagenomics

KW - Microbiome

KW - Per- and polyfluoroalkyl infstances

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JO - Environmental Epidemiology

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ER -

Early-life exposure to per- and polyfluoroalkyl substances and infant gut microbial composition

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