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Composition and Diversity of the Subgingival Microbiome and Its Relationship with Age in Postmenopausal Women: an Epidemiologic Investigation Michael J

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Composition and Diversity of the Subgingival Microbiome and Its Relationship with Age in Postmenopausal Women: an Epidemiologic Investigation Michael J LaMonte et al. BMC Oral Health (2019) 19:246 https://doi.org/10.1186/s12903-019-0906-2 RESEARCH ARTICLE Open Access Composition and diversity of the subgingival microbiome and its relationship with age in postmenopausal women: an epidemiologic investigation Michael J. LaMonte1* , Robert J. Genco2ˆ, Michael J. Buck3, Daniel I. McSkimming4,LuLi5, Kathleen M. Hovey1, Christopher A. Andrews6, Wei Zheng5, Yijun Sun5, Amy E. Millen1, Maria Tsompana3, Hailey R. Banack1 and Jean Wactawski-Wende1 Abstract Background: The extent to which the composition and diversity of the oral microbiome varies with age is not clearly understood. Methods: The 16S rRNA gene of subgingival plaque in 1219 women, aged 53–81 years, was sequenced and its taxonomy annotated against the Human Oral Microbiome Database (v.14.5). Composition of the subgingival microbiome was described in terms of centered log(2)-ratio (CLR) transformed OTU values, relative abundance, and prevalence. Correlations between microbiota abundance and age were evelauted using Pearson Product Moment correlations. P-values were corrected for multiple testing using the Bonferroni method. Results: Of the 267 species identified overall, Veillonella dispar was the most abundant bacteria when described by CLR OTU (mean 8.3) or relative abundance (mean 8.9%); whereas Streptococcus oralis, Veillonella dispar and Veillonella parvula were most prevalent (100%, all) when described as being present at any amount. Linear correlations between age and several CLR OTUs (Pearson r = − 0.18 to 0.18), of which 82 (31%) achieved statistical significance (P <0.05).The correlations lost significance following Bonferroni correction. Twelve species that differed across age groups (each corrected P < 0.05); 5 (42%) were higher in women ages 50–59 compared to ≥70 (corrected P < 0.05), and 7 (48%) were higher in women 70 years and older. Conclusions: We identified associations between several bacterial species and age across the age range of postmenopausal women studied. Understanding the functions of these bacteria could identify intervention targets to enhance oral health in later life. Keywords: Aging, Women, Oral Microbiome, Epidemiology Background [1, 2]. Marked differences in composition and function of The availability of high throughput metagenomics microbiomes have been shown between various body sites sequencing technology has allowed for deeper under- among individuals [3, 4]. It has become increasingly clear standing of complex microbiota ecologies and their aggre- that the microbiota and microbiome are correlated with gate functional capacities within a defined microbiome both health and disease states in humans [5], and that the aging process could be an important determinant of these * Correspondence: [email protected] relationships [6, 7]. Aging is a complex, multifactorial ˆPrior to publication of this work, Dr. Robert Genco passed away unexpectedly. The manuscript is dedicated to his lasting memory as a pioneering scientist, process characterized by progressively lower resilience to teacher, mentor, colleague, and sorely missed friend. Rest in peace, Bob. stress, increased homeostatic imbalance, and greater 1 Department of Epidemiology and Environmental Health, School of Public susceptibility to pathologic insult and disease onset [8]. Health and Health Professions, University at Buffalo, 270 Farber Hall, 3435 Main Street, Buffalo, NY 14214, USA Changes in microbiome diversity and function have been Full list of author information is available at the end of the article © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. LaMonte et al. BMC Oral Health (2019) 19:246 Page 2 of 44 observed with increasing age [9]. Alterations in the host diversity expected in a population that then allow for environment that occur with physiologic aging processes hypotheses pertaining to disease-related variation that could enable untoward shifts in relative abundance of can then be accurately evaluated [24]. The objective of commensal and pathogenic bacteria, and enhanced ex- this current cross-sectional investigation was to describe pression of pathogen genomes which, in turn, could the composition and diversity of the subgingival plaque heighten disease susceptibility. In support of this hypoth- microbiome and its relationship with age in a cohort of esis are studies demonstrating links between human ambulatory postmenopausal women, aged 53–81 years, microbiomes and several diseases of aging including obes- whowereenrolledinanongoingstudyfromthe ity, diabetes, heart disease, and certain cancers [5, 7, 10]. communitydwellingwomenwithoutselectiononperi- The oral microbiota comprise one of the most complex odontal health status at enrollment. and diverse human microbiomes [3, 11, 12]. Oral bacteria have important functional roles that contribute to main- Methods tenance of oral health [13], to oral diseases such as caries Participants and periodontitis in the setting of dysbiosis [14, 15], and The present study included 1219 postmenopausal potentially to systemic diseases of aging by way of bacter- women enrolled in the Buffalo Osteoporosis and Peri- ial translocation through ulcerated oral epithelium, aspir- odontitis (OsteoPerio) Study, which is an ancillary ation, or ingestion [7, 16]. This could have important study conducted at the Buffalo (NY) clinical center of implications to public health given the rapid growth in the Women’s Health Initiative Observational Study numbers of older adults expected in coming decades. (WHI OS). Participants provided written informed Surprisingly, there exists a limited understanding of consent for all components of the studies, which were oral microbiota in aging populations. Feres et al. [17] conducted in accord with the Helsinki Declaration on conducted a comprehensive review of published litera- human subjects research. Experimental protocols for ture and concluded that the majority of oral micro- all aspects of the WHI study, the OsteoPerio Study, biome studies have included younger and middle-aged and the microbiome study detailed in this paper were adults. Only a small number of studies have described approved by the Institutional Review Board at the the microbiome in older adults, among which sample University at Buffalo. This manuscript conforms to sizes of adults 60 years and older tended to be, on the STROBE guidelines for human observational stud- average, modest (e.g., < 200), the majority of whom ies. Details about recruitment, enrollment criteria, were men and were selected to have moderate to study implementation and measurements have been severe periodontitis [17–19]. A majority of previous published for the WHI OS [25]andtheOsteoPerio studies have used low throughput microbial measurement study [26, 27]. Briefly, 2249 postmenopausal women, techniques, such as microbial culture and targeted DNA ages 50–79, enrolled into the WHI OS at the Buffalo probes, which result in an incomplete characterization of center between 1994 and 1998. Of these, 1362 the oral microbiome composition and diversity in rela- enrolled into the OsteoPerio study 3 years later in tionship to groups of men and women of differing ages. 1997–2001 (mean age 66; range 53–81 years). Enroll- Recent investigations have extended these previous studies ment into the OsteoPerio study required at least 6 by using next generation sequencing methods, but again teeth present and no history of bone disease other relatively small sample sizes (< 100) limited the contrasts than osteoporosis and no history of cancer in the that could be performed in relation to age in the majority previous 10 years. Women completed standardized of these studies [20–23]. questionnaires pertaining to demographic information, Thus, at present, an incomplete understanding of the lifestyle habits, and personal health history, as well as composition and characteristics of the oral microbiome undertaking a whole mouth oral examination conducted exists in the context of aging, particularly in women. A by trained and calibrated examiners. Neighborhood socio- critical step in advancing knowledge on how the oral economic status was derived from questionnaire responses microbiome relates with the frequency of oral (e.g., peri- and census tract information [28]. Detailed descriptions of odontitis) or systemic (e.g., breast cancer) diseases of the oral examination measures and their reproducibility aging, is to first understand the extent of the compos- have been published [26]. Figure 1 shows a flow chart of ition and how the microbiota vary with host characteris- participant enrollment into the OsteoPerio study. tics, such as age. This information will be important in later understanding the interplay of the microbiome Subgingival plaque samples with pathogenic changes over time. Application of epi- A protocol for obtaining subgingival plaque samples was demiologic study methods to study populations not developed for this study and has been published [29]. Fine selected on disease
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