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Dysbiosis of the Human Oral Microbiome During the Menstrual Cycle and Vulnerability to the External Exposures of Smoking and Dietary Sugar

Physiological hormonal fluctuations exert endogenous pressures on the structure and function of the human microbiome. As such, the menstrual cycle may selectively disrupt the homeostasis of the resident oral microbiome, thus compromising oral health. Hence, the aim of the present study was to struct...

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Autores principales: Bostanci, Nagihan, Krog, Maria Christine, Hugerth, Luisa W., Bashir, Zahra, Fransson, Emma, Boulund, Fredrik, Belibasakis, Georgios N., Wannerberger, Kristin, Engstrand, Lars, Nielsen, Henriette Svarre, Schuppe-Koistinen, Ina
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8018275/
https://www.ncbi.nlm.nih.gov/pubmed/33816334
http://dx.doi.org/10.3389/fcimb.2021.625229
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author Bostanci, Nagihan
Krog, Maria Christine
Hugerth, Luisa W.
Bashir, Zahra
Fransson, Emma
Boulund, Fredrik
Belibasakis, Georgios N.
Wannerberger, Kristin
Engstrand, Lars
Nielsen, Henriette Svarre
Schuppe-Koistinen, Ina
author_facet Bostanci, Nagihan
Krog, Maria Christine
Hugerth, Luisa W.
Bashir, Zahra
Fransson, Emma
Boulund, Fredrik
Belibasakis, Georgios N.
Wannerberger, Kristin
Engstrand, Lars
Nielsen, Henriette Svarre
Schuppe-Koistinen, Ina
author_sort Bostanci, Nagihan
collection PubMed
description Physiological hormonal fluctuations exert endogenous pressures on the structure and function of the human microbiome. As such, the menstrual cycle may selectively disrupt the homeostasis of the resident oral microbiome, thus compromising oral health. Hence, the aim of the present study was to structurally and functionally profile the salivary microbiome of 103 women in reproductive age with regular menstrual cycle, while evaluating the modifying influences of hormonal contraceptives, sex hormones, diet, and smoking. Whole saliva was sampled during the menstrual, follicular, and luteal phases (n = 309) of the cycle, and the participants reported questionnaire-based data concerning their life habits and oral or systemic health. No significant differences in alpha-diversity or phase-specific clustering of the overall microbiome were observed. Nevertheless, the salivary abundances of genera Campylobacter, Haemophilus, Prevotella, and Oribacterium varied throughout the cycle, and a higher species-richness was observed during the luteal phase. While the overall community structure maintained relatively intact, its functional properties were drastically affected. In particular, 11 functional modules were differentially abundant throughout the menstrual cycle, including pentose phosphate metabolism, and biosynthesis of cobalamin and neurotransmitter gamma-aminobutyric acid. The menstrual cycle phase, but not oral contraceptive usage, was accountable for greater variations in the metabolic pathways of the salivary microbiome. Further co-risk factor analysis demonstrated that Prevotella and Veillonella were increased in current smokers, whereas high dietary sugar consumption modified the richness and diversity of the microbiome during the cycle. This is the first large study to systematically address dysbiotic variations of the oral microbiome during the course of menstrual cycle, and document the additive effect of smoking and sugar consumption as environmental risk factors. It reveals the structural resilience and functional adaptability of the oral microbiome to the endogenous hormonal pressures of the menstrual cycle, while revealing its vulnerability to the exogenous exposures of diet and smoking.
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spelling pubmed-80182752021-04-03 Dysbiosis of the Human Oral Microbiome During the Menstrual Cycle and Vulnerability to the External Exposures of Smoking and Dietary Sugar Bostanci, Nagihan Krog, Maria Christine Hugerth, Luisa W. Bashir, Zahra Fransson, Emma Boulund, Fredrik Belibasakis, Georgios N. Wannerberger, Kristin Engstrand, Lars Nielsen, Henriette Svarre Schuppe-Koistinen, Ina Front Cell Infect Microbiol Cellular and Infection Microbiology Physiological hormonal fluctuations exert endogenous pressures on the structure and function of the human microbiome. As such, the menstrual cycle may selectively disrupt the homeostasis of the resident oral microbiome, thus compromising oral health. Hence, the aim of the present study was to structurally and functionally profile the salivary microbiome of 103 women in reproductive age with regular menstrual cycle, while evaluating the modifying influences of hormonal contraceptives, sex hormones, diet, and smoking. Whole saliva was sampled during the menstrual, follicular, and luteal phases (n = 309) of the cycle, and the participants reported questionnaire-based data concerning their life habits and oral or systemic health. No significant differences in alpha-diversity or phase-specific clustering of the overall microbiome were observed. Nevertheless, the salivary abundances of genera Campylobacter, Haemophilus, Prevotella, and Oribacterium varied throughout the cycle, and a higher species-richness was observed during the luteal phase. While the overall community structure maintained relatively intact, its functional properties were drastically affected. In particular, 11 functional modules were differentially abundant throughout the menstrual cycle, including pentose phosphate metabolism, and biosynthesis of cobalamin and neurotransmitter gamma-aminobutyric acid. The menstrual cycle phase, but not oral contraceptive usage, was accountable for greater variations in the metabolic pathways of the salivary microbiome. Further co-risk factor analysis demonstrated that Prevotella and Veillonella were increased in current smokers, whereas high dietary sugar consumption modified the richness and diversity of the microbiome during the cycle. This is the first large study to systematically address dysbiotic variations of the oral microbiome during the course of menstrual cycle, and document the additive effect of smoking and sugar consumption as environmental risk factors. It reveals the structural resilience and functional adaptability of the oral microbiome to the endogenous hormonal pressures of the menstrual cycle, while revealing its vulnerability to the exogenous exposures of diet and smoking. Frontiers Media S.A. 2021-03-19 /pmc/articles/PMC8018275/ /pubmed/33816334 http://dx.doi.org/10.3389/fcimb.2021.625229 Text en Copyright © 2021 Bostanci, Krog, Hugerth, Bashir, Fransson, Boulund, Belibasakis, Wannerberger, Engstrand, Nielsen and Schuppe-Koistinen http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Cellular and Infection Microbiology
Bostanci, Nagihan
Krog, Maria Christine
Hugerth, Luisa W.
Bashir, Zahra
Fransson, Emma
Boulund, Fredrik
Belibasakis, Georgios N.
Wannerberger, Kristin
Engstrand, Lars
Nielsen, Henriette Svarre
Schuppe-Koistinen, Ina
Dysbiosis of the Human Oral Microbiome During the Menstrual Cycle and Vulnerability to the External Exposures of Smoking and Dietary Sugar
title Dysbiosis of the Human Oral Microbiome During the Menstrual Cycle and Vulnerability to the External Exposures of Smoking and Dietary Sugar
title_full Dysbiosis of the Human Oral Microbiome During the Menstrual Cycle and Vulnerability to the External Exposures of Smoking and Dietary Sugar
title_fullStr Dysbiosis of the Human Oral Microbiome During the Menstrual Cycle and Vulnerability to the External Exposures of Smoking and Dietary Sugar
title_full_unstemmed Dysbiosis of the Human Oral Microbiome During the Menstrual Cycle and Vulnerability to the External Exposures of Smoking and Dietary Sugar
title_short Dysbiosis of the Human Oral Microbiome During the Menstrual Cycle and Vulnerability to the External Exposures of Smoking and Dietary Sugar
title_sort dysbiosis of the human oral microbiome during the menstrual cycle and vulnerability to the external exposures of smoking and dietary sugar
topic Cellular and Infection Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8018275/
https://www.ncbi.nlm.nih.gov/pubmed/33816334
http://dx.doi.org/10.3389/fcimb.2021.625229
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