Associations of Circulating Estrogens and Estrogen Metabolites with Fecal and Oral Microbiome in Postmenopausal Women in the Ghana Breast Health Study
The human fecal and oral microbiome may play a role in the etiology of breast cancer through modulation of endogenous estrogen metabolism. This study aimed to investigate associations of circulating estrogens and estrogen metabolites with the fecal and oral microbiome in postmenopausal African women...
Autores principales: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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American Society for Microbiology
2023
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Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10433996/ https://www.ncbi.nlm.nih.gov/pubmed/37341612 http://dx.doi.org/10.1128/spectrum.01572-23 |
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author | Wu, Zeni Pfeiffer, Ruth M. Byrd, Doratha A. Wan, Yunhu Ansong, Daniel Clegg-Lamptey, Joe-Nat Wiafe-Addai, Beatrice Edusei, Lawrence Adjei, Ernest Titiloye, Nicholas Dedey, Florence Aitpillah, Francis Oppong, Joseph Vanderpuye, Verna Osei-Bonsu, Ernest Dagnall, Casey L. Jones, Kristine Hutchinson, Amy Hicks, Belynda D. Ahearn, Thomas U. Knight, Rob Biritwum, Richard Yarney, Joel Wiafe, Seth Awuah, Baffour Nyarko, Kofi Garcia-Closas, Montserrat Sinha, Rashmi Figueroa, Jonine D. Brinton, Louise A. Trabert, Britton Vogtmann, Emily |
author_facet | Wu, Zeni Pfeiffer, Ruth M. Byrd, Doratha A. Wan, Yunhu Ansong, Daniel Clegg-Lamptey, Joe-Nat Wiafe-Addai, Beatrice Edusei, Lawrence Adjei, Ernest Titiloye, Nicholas Dedey, Florence Aitpillah, Francis Oppong, Joseph Vanderpuye, Verna Osei-Bonsu, Ernest Dagnall, Casey L. Jones, Kristine Hutchinson, Amy Hicks, Belynda D. Ahearn, Thomas U. Knight, Rob Biritwum, Richard Yarney, Joel Wiafe, Seth Awuah, Baffour Nyarko, Kofi Garcia-Closas, Montserrat Sinha, Rashmi Figueroa, Jonine D. Brinton, Louise A. Trabert, Britton Vogtmann, Emily |
author_sort | Wu, Zeni |
collection | PubMed |
description | The human fecal and oral microbiome may play a role in the etiology of breast cancer through modulation of endogenous estrogen metabolism. This study aimed to investigate associations of circulating estrogens and estrogen metabolites with the fecal and oral microbiome in postmenopausal African women. A total of 117 women with fecal (N = 110) and oral (N = 114) microbiome data measured by 16S rRNA gene sequencing, and estrogens and estrogen metabolites data measured by liquid chromatography tandem mass spectrometry were included. The outcomes were measures of the microbiome and the independent variables were the estrogens and estrogen metabolites. Estrogens and estrogen metabolites were associated with the fecal microbial Shannon index (global P < 0.01). In particular, higher levels of estrone (β = 0.36, P = 0.03), 2-hydroxyestradiol (β = 0.30, P = 0.02), 4-methoxyestrone (β = 0.51, P = 0.01), and estriol (β = 0.36, P = 0.04) were associated with higher levels of the Shannon index, while 16alpha-hydroxyestrone (β = −0.57, P < 0.01) was inversely associated with the Shannon index as indicated by linear regression. Conjugated 2-methoxyestrone was associated with oral microbial unweighted UniFrac as indicated by MiRKAT (P < 0.01) and PERMANOVA, where conjugated 2-methoxyestrone explained 2.67% of the oral microbial variability, but no other estrogens or estrogen metabolites were associated with any other beta diversity measures. The presence and abundance of multiple fecal and oral genera, such as fecal genera from families Lachnospiraceae and Ruminococcaceae, were associated with several estrogens and estrogen metabolites as indicated by zero-inflated negative binomial regression. Overall, we found several associations of specific estrogens and estrogen metabolites and the fecal and oral microbiome. IMPORTANCE Several epidemiologic studies have found associations of urinary estrogens and estrogen metabolites with the fecal microbiome. However, urinary estrogen concentrations are not strongly correlated with serum estrogens, a known risk factor for breast cancer. To better understand whether the human fecal and oral microbiome were associated with breast cancer risk via the regulation of estrogen metabolism, we conducted this study to investigate the associations of circulating estrogens and estrogen metabolites with the fecal and oral microbiome in postmenopausal African women. We found several associations of parent estrogens and several estrogen metabolites with the microbial communities, and multiple individual associations of estrogens and estrogen metabolites with the presence and abundance of multiple fecal and oral genera, such as fecal genera from families Lachnospiraceae and Ruminococcaceae, which have estrogen metabolizing properties. Future large, longitudinal studies to investigate the dynamic changes of the fecal and oral microbiome and estrogen relationship are needed. |
format | Online Article Text |
id | pubmed-10433996 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | American Society for Microbiology |
record_format | MEDLINE/PubMed |
spelling | pubmed-104339962023-08-18 Associations of Circulating Estrogens and Estrogen Metabolites with Fecal and Oral Microbiome in Postmenopausal Women in the Ghana Breast Health Study Wu, Zeni Pfeiffer, Ruth M. Byrd, Doratha A. Wan, Yunhu Ansong, Daniel Clegg-Lamptey, Joe-Nat Wiafe-Addai, Beatrice Edusei, Lawrence Adjei, Ernest Titiloye, Nicholas Dedey, Florence Aitpillah, Francis Oppong, Joseph Vanderpuye, Verna Osei-Bonsu, Ernest Dagnall, Casey L. Jones, Kristine Hutchinson, Amy Hicks, Belynda D. Ahearn, Thomas U. Knight, Rob Biritwum, Richard Yarney, Joel Wiafe, Seth Awuah, Baffour Nyarko, Kofi Garcia-Closas, Montserrat Sinha, Rashmi Figueroa, Jonine D. Brinton, Louise A. Trabert, Britton Vogtmann, Emily Microbiol Spectr Research Article The human fecal and oral microbiome may play a role in the etiology of breast cancer through modulation of endogenous estrogen metabolism. This study aimed to investigate associations of circulating estrogens and estrogen metabolites with the fecal and oral microbiome in postmenopausal African women. A total of 117 women with fecal (N = 110) and oral (N = 114) microbiome data measured by 16S rRNA gene sequencing, and estrogens and estrogen metabolites data measured by liquid chromatography tandem mass spectrometry were included. The outcomes were measures of the microbiome and the independent variables were the estrogens and estrogen metabolites. Estrogens and estrogen metabolites were associated with the fecal microbial Shannon index (global P < 0.01). In particular, higher levels of estrone (β = 0.36, P = 0.03), 2-hydroxyestradiol (β = 0.30, P = 0.02), 4-methoxyestrone (β = 0.51, P = 0.01), and estriol (β = 0.36, P = 0.04) were associated with higher levels of the Shannon index, while 16alpha-hydroxyestrone (β = −0.57, P < 0.01) was inversely associated with the Shannon index as indicated by linear regression. Conjugated 2-methoxyestrone was associated with oral microbial unweighted UniFrac as indicated by MiRKAT (P < 0.01) and PERMANOVA, where conjugated 2-methoxyestrone explained 2.67% of the oral microbial variability, but no other estrogens or estrogen metabolites were associated with any other beta diversity measures. The presence and abundance of multiple fecal and oral genera, such as fecal genera from families Lachnospiraceae and Ruminococcaceae, were associated with several estrogens and estrogen metabolites as indicated by zero-inflated negative binomial regression. Overall, we found several associations of specific estrogens and estrogen metabolites and the fecal and oral microbiome. IMPORTANCE Several epidemiologic studies have found associations of urinary estrogens and estrogen metabolites with the fecal microbiome. However, urinary estrogen concentrations are not strongly correlated with serum estrogens, a known risk factor for breast cancer. To better understand whether the human fecal and oral microbiome were associated with breast cancer risk via the regulation of estrogen metabolism, we conducted this study to investigate the associations of circulating estrogens and estrogen metabolites with the fecal and oral microbiome in postmenopausal African women. We found several associations of parent estrogens and several estrogen metabolites with the microbial communities, and multiple individual associations of estrogens and estrogen metabolites with the presence and abundance of multiple fecal and oral genera, such as fecal genera from families Lachnospiraceae and Ruminococcaceae, which have estrogen metabolizing properties. Future large, longitudinal studies to investigate the dynamic changes of the fecal and oral microbiome and estrogen relationship are needed. American Society for Microbiology 2023-06-21 /pmc/articles/PMC10433996/ /pubmed/37341612 http://dx.doi.org/10.1128/spectrum.01572-23 Text en https://doi.org/10.1128/AuthorWarrantyLicense.v1This is a work of the U.S. Government and is not subject to copyright protection in the United States. Foreign copyrights may apply. |
spellingShingle | Research Article Wu, Zeni Pfeiffer, Ruth M. Byrd, Doratha A. Wan, Yunhu Ansong, Daniel Clegg-Lamptey, Joe-Nat Wiafe-Addai, Beatrice Edusei, Lawrence Adjei, Ernest Titiloye, Nicholas Dedey, Florence Aitpillah, Francis Oppong, Joseph Vanderpuye, Verna Osei-Bonsu, Ernest Dagnall, Casey L. Jones, Kristine Hutchinson, Amy Hicks, Belynda D. Ahearn, Thomas U. Knight, Rob Biritwum, Richard Yarney, Joel Wiafe, Seth Awuah, Baffour Nyarko, Kofi Garcia-Closas, Montserrat Sinha, Rashmi Figueroa, Jonine D. Brinton, Louise A. Trabert, Britton Vogtmann, Emily Associations of Circulating Estrogens and Estrogen Metabolites with Fecal and Oral Microbiome in Postmenopausal Women in the Ghana Breast Health Study |
title | Associations of Circulating Estrogens and Estrogen Metabolites with Fecal and Oral Microbiome in Postmenopausal Women in the Ghana Breast Health Study |
title_full | Associations of Circulating Estrogens and Estrogen Metabolites with Fecal and Oral Microbiome in Postmenopausal Women in the Ghana Breast Health Study |
title_fullStr | Associations of Circulating Estrogens and Estrogen Metabolites with Fecal and Oral Microbiome in Postmenopausal Women in the Ghana Breast Health Study |
title_full_unstemmed | Associations of Circulating Estrogens and Estrogen Metabolites with Fecal and Oral Microbiome in Postmenopausal Women in the Ghana Breast Health Study |
title_short | Associations of Circulating Estrogens and Estrogen Metabolites with Fecal and Oral Microbiome in Postmenopausal Women in the Ghana Breast Health Study |
title_sort | associations of circulating estrogens and estrogen metabolites with fecal and oral microbiome in postmenopausal women in the ghana breast health study |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10433996/ https://www.ncbi.nlm.nih.gov/pubmed/37341612 http://dx.doi.org/10.1128/spectrum.01572-23 |
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