Abstract
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.
Highlights
The oral cavity is a special ecological habitat composed of soft and non-shedding hard tissues, colonized with a plethora of microorganisms (Wade, 2013; Belibasakis et al, 2019)
We longitudinally characterized the salivary microbiome of 103 regularly menstruating women in reproductive age during the course of one full menstrual cycle, using whole genome sequencing, and evaluated its potential deviations caused by the use of oral contraceptives and changes during the menstrual cycle
To the best of our knowledge, 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 exogenous risk factors. The analysis of this cohort cumulatively identified 50 bacterial genera belonging to eight phyla, all well represented in the human oral microbiome database and previously identified as members of the human salivary microbiome (Dewhirst et al, 2010; Segata et al, 2012; Hasan et al, 2014).This diversity may be considered much lower compared to most salivary microbiome studies that have been using 16S rRNA gene sequencing instead, a method which may overestimate diversity
Summary
The oral cavity is a special ecological habitat composed of soft and non-shedding hard tissues, colonized with a plethora of microorganisms (Wade, 2013; Belibasakis et al, 2019). The oral microbiota constitutes the second most diverse microbial community of the human body, which under normal circumstances remains mostly stable (Human Microbiome Project, 2012; David et al, 2014; Rosier et al, 2018; Lif Holgerson et al, 2020). Estrogens, may suppress the physiological salivary flow rate (Streckfus et al, 1998; Lu et al, 1999). This results in reduction of the natural antimicrobial capacity of saliva, disrupting the local microbial homeostasis and increasing susceptibility to gingivitis and dental caries in the affected women (Lukacs and Largaespada, 2006; Gursoy et al, 2008; Silva de Araujo Figueiredo et al, 2017)
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