Association of microbial dynamics with urinary estrogens and estrogen metabolites in patients with endometriosis.

Endometriosis is an estrogen dependent gynecological disease associated with altered microbial phenotypes. The association among endogenous estrogen, estrogen metabolites, and microbial dynamics on disease pathogenesis has not been fully investigated. Here, we identified estrogen metabolites as well...

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Main Authors: Nhung Le, Melissa Cregger, Veronica Brown, Julio Loret de Mola, Pamela Bremer, Lyn Nguyen, Kathleen Groesch, Teresa Wilson, Paula Diaz-Sylvester, Andrea Braundmeier-Fleming
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0261362
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author Nhung Le
Melissa Cregger
Veronica Brown
Julio Loret de Mola
Pamela Bremer
Lyn Nguyen
Kathleen Groesch
Teresa Wilson
Paula Diaz-Sylvester
Andrea Braundmeier-Fleming
author_facet Nhung Le
Melissa Cregger
Veronica Brown
Julio Loret de Mola
Pamela Bremer
Lyn Nguyen
Kathleen Groesch
Teresa Wilson
Paula Diaz-Sylvester
Andrea Braundmeier-Fleming
author_sort Nhung Le
collection DOAJ
description Endometriosis is an estrogen dependent gynecological disease associated with altered microbial phenotypes. The association among endogenous estrogen, estrogen metabolites, and microbial dynamics on disease pathogenesis has not been fully investigated. Here, we identified estrogen metabolites as well as microbial phenotypes in non-diseased patients (n = 9) and those with pathologically confirmed endometriosis (P-EOSIS, n = 20), on day of surgery (DOS) and ~1-3 weeks post-surgical intervention (PSI). Then, we examined the effects of surgical intervention with or without hormonal therapy (OCPs) on estrogen and microbial profiles of both study groups. For estrogen metabolism analysis, liquid chromatography/tandem mass spectrometry was used to quantify urinary estrogens. The microbiome data assessment was performed with Next generation sequencing to V4 region of 16S rRNA. Surgical intervention and hormonal therapy altered gastrointestinal (GI), urogenital (UG) microbiomes, urinary estrogen and estrogen metabolite levels in P-EOSIS. At DOS, 17β-estradiol was enhanced in P-EOSIS treated with OCPs. At PSI, 16-keto-17β-estradiol was increased in P-EOSIS not receiving OCPs while 2-hydroxyestradiol and 2-hydroxyestrone were decreased in P-EOSIS receiving OCPs. GI bacterial α-diversity was greater for controls and P-EOSIS that did not receive OCPs. P-EOSIS not utilizing OCPs exhibited a decrease in UG bacterial α-diversity and differences in dominant taxa, while P-EOSIS utilizing OCPs had an increase in UG bacterial α-diversity. P-EOSIS had a strong positive correlation between the GI/UG bacteria species and the concentrations of urinary estrogen and its metabolites. These results indicate an association between microbial dysbiosis and altered urinary estrogens in P-EOSIS, which may impact disease progression.
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spelling doaj.art-86e18029bca84adabf92bfb024b143e12022-12-22T04:10:12ZengPublic Library of Science (PLoS)PLoS ONE1932-62032021-01-011612e026136210.1371/journal.pone.0261362Association of microbial dynamics with urinary estrogens and estrogen metabolites in patients with endometriosis.Nhung LeMelissa CreggerVeronica BrownJulio Loret de MolaPamela BremerLyn NguyenKathleen GroeschTeresa WilsonPaula Diaz-SylvesterAndrea Braundmeier-FlemingEndometriosis is an estrogen dependent gynecological disease associated with altered microbial phenotypes. The association among endogenous estrogen, estrogen metabolites, and microbial dynamics on disease pathogenesis has not been fully investigated. Here, we identified estrogen metabolites as well as microbial phenotypes in non-diseased patients (n = 9) and those with pathologically confirmed endometriosis (P-EOSIS, n = 20), on day of surgery (DOS) and ~1-3 weeks post-surgical intervention (PSI). Then, we examined the effects of surgical intervention with or without hormonal therapy (OCPs) on estrogen and microbial profiles of both study groups. For estrogen metabolism analysis, liquid chromatography/tandem mass spectrometry was used to quantify urinary estrogens. The microbiome data assessment was performed with Next generation sequencing to V4 region of 16S rRNA. Surgical intervention and hormonal therapy altered gastrointestinal (GI), urogenital (UG) microbiomes, urinary estrogen and estrogen metabolite levels in P-EOSIS. At DOS, 17β-estradiol was enhanced in P-EOSIS treated with OCPs. At PSI, 16-keto-17β-estradiol was increased in P-EOSIS not receiving OCPs while 2-hydroxyestradiol and 2-hydroxyestrone were decreased in P-EOSIS receiving OCPs. GI bacterial α-diversity was greater for controls and P-EOSIS that did not receive OCPs. P-EOSIS not utilizing OCPs exhibited a decrease in UG bacterial α-diversity and differences in dominant taxa, while P-EOSIS utilizing OCPs had an increase in UG bacterial α-diversity. P-EOSIS had a strong positive correlation between the GI/UG bacteria species and the concentrations of urinary estrogen and its metabolites. These results indicate an association between microbial dysbiosis and altered urinary estrogens in P-EOSIS, which may impact disease progression.https://doi.org/10.1371/journal.pone.0261362
spellingShingle Nhung Le
Melissa Cregger
Veronica Brown
Julio Loret de Mola
Pamela Bremer
Lyn Nguyen
Kathleen Groesch
Teresa Wilson
Paula Diaz-Sylvester
Andrea Braundmeier-Fleming
Association of microbial dynamics with urinary estrogens and estrogen metabolites in patients with endometriosis.
PLoS ONE
title Association of microbial dynamics with urinary estrogens and estrogen metabolites in patients with endometriosis.
title_full Association of microbial dynamics with urinary estrogens and estrogen metabolites in patients with endometriosis.
title_fullStr Association of microbial dynamics with urinary estrogens and estrogen metabolites in patients with endometriosis.
title_full_unstemmed Association of microbial dynamics with urinary estrogens and estrogen metabolites in patients with endometriosis.
title_short Association of microbial dynamics with urinary estrogens and estrogen metabolites in patients with endometriosis.
title_sort association of microbial dynamics with urinary estrogens and estrogen metabolites in patients with endometriosis
url https://doi.org/10.1371/journal.pone.0261362
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