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      Tongue Microbiota and Oral Health Status in Community-Dwelling Elderly Adults

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          Abstract

          Aspiration of oral contents can lead to pneumonia, which is a major cause of death among elderly adults susceptible to swallowing impairments. Tongue microbiota are a dominant source of oral microbial populations that are ingested with saliva. This large-scale population-based study revealed variations in the tongue microbiota among community-dwelling elderly adults. The total bacterial density was independent of the conditions of teeth surrounding the tongue, whereas the microbiota composition, especially the relative abundances of predominant commensals, showed an association with tooth conditions. Our results demonstrate that the elderly with fewer teeth, poorer dental hygiene, and more dental caries experience constantly ingest more dysbiotic microbiota, which could be harmful for their respiratory health.

          ABSTRACT

          Tongue microbiota are a dominant source of oral microbial populations that are ingested with saliva, and therefore careful attention is required for the maintenance of health of elderly adults, who are susceptible to aspiration of oral contents. This study aimed to investigate the variation in tongue microbiota among community-dwelling elderly adults. Following a dental examination, tongue coating was collected from a 15-mm-diameter circular area at the center of the tongue dorsum of 506 elderly adults aged 70 to 80 years inhabiting the town of Hisayama, Japan. The microbial composition and density were determined by a 16S rRNA gene sequencing approach using a next-generation sequencer and quantitative PCR analysis, respectively. Co-occurrence network analysis identified two cohabiting groups of predominant commensals, one of which was primarily composed of Prevotella histicola, Veillonella atypica, Streptococcus salivarius, and Streptococcus parasanguinis; these organisms have been previously associated with an increased risk of mortality due to pneumonia in the frail elderly. This bacterial group was more predominant in the elderly with fewer teeth, a higher plaque index, and more dental caries experience, whereas the total bacterial density was independent of these traits. A higher density of fungi was also observed in the elderly with these traits, as well as in individuals who wore dentures. These results suggest that elderly adults with poorer oral health swallow a more dysbiotic microbiota formed on the tongue.

          IMPORTANCE Aspiration of oral contents can lead to pneumonia, which is a major cause of death among elderly adults susceptible to swallowing impairments. Tongue microbiota are a dominant source of oral microbial populations that are ingested with saliva. This large-scale population-based study revealed variations in the tongue microbiota among community-dwelling elderly adults. The total bacterial density was independent of the conditions of teeth surrounding the tongue, whereas the microbiota composition, especially the relative abundances of predominant commensals, showed an association with tooth conditions. Our results demonstrate that the elderly with fewer teeth, poorer dental hygiene, and more dental caries experience constantly ingest more dysbiotic microbiota, which could be harmful for their respiratory health.

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          Most cited references30

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          ITS as an environmental DNA barcode for fungi: an in silico approach reveals potential PCR biases

          Background During the last 15 years the internal transcribed spacer (ITS) of nuclear DNA has been used as a target for analyzing fungal diversity in environmental samples, and has recently been selected as the standard marker for fungal DNA barcoding. In this study we explored the potential amplification biases that various commonly utilized ITS primers might introduce during amplification of different parts of the ITS region in samples containing mixed templates ('environmental barcoding'). We performed in silico PCR analyses with commonly used primer combinations using various ITS datasets obtained from public databases as templates. Results Some of the ITS primers, such as ITS1-F, were hampered with a high proportion of mismatches relative to the target sequences, and most of them appeared to introduce taxonomic biases during PCR. Some primers, e.g. ITS1-F, ITS1 and ITS5, were biased towards amplification of basidiomycetes, whereas others, e.g. ITS2, ITS3 and ITS4, were biased towards ascomycetes. The assumed basidiomycete-specific primer ITS4-B only amplified a minor proportion of basidiomycete ITS sequences, even under relaxed PCR conditions. Due to systematic length differences in the ITS2 region as well as the entire ITS, we found that ascomycetes will more easily amplify than basidiomycetes using these regions as targets. This bias can be avoided by using primers amplifying ITS1 only, but this would imply preferential amplification of 'non-dikarya' fungi. Conclusions We conclude that ITS primers have to be selected carefully, especially when used for high-throughput sequencing of environmental samples. We suggest that different primer combinations or different parts of the ITS region should be analyzed in parallel, or that alternative ITS primers should be searched for.
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            Enrichment of the lung microbiome with oral taxa is associated with lung inflammation of a Th17 phenotype.

            Microaspiration is a common phenomenon in healthy subjects, but its frequency is increased in chronic inflammatory airway diseases, and its role in inflammatory and immune phenotypes is unclear. We have previously demonstrated that acellular bronchoalveolar lavage samples from half of the healthy people examined are enriched with oral taxa (here called pneumotypeSPT) and this finding is associated with increased numbers of lymphocytes and neutrophils in bronchoalveolar lavage. Here, we have characterized the inflammatory phenotype using a multi-omic approach. By evaluating both upper airway and acellular bronchoalveolar lavage samples from 49 subjects from three cohorts without known pulmonary disease, we observed that pneumotypeSPT was associated with a distinct metabolic profile, enhanced expression of inflammatory cytokines, a pro-inflammatory phenotype characterized by elevated Th-17 lymphocytes and, conversely, a blunted alveolar macrophage TLR4 response. The cellular immune responses observed in the lower airways of humans with pneumotypeSPT indicate a role for the aspiration-derived microbiota in regulating the basal inflammatory status at the pulmonary mucosal surface.
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              Newly identified pathogens associated with periodontitis: a systematic review.

              There is substantial evidence supporting the role of certain oral bacteria species in the onset and progression of periodontitis. Nevertheless, results of independent-culture diagnostic methods introduced about a decade ago have pointed to the existence of new periodontal pathogens. However, the data of these studies have not been evaluated together, which may generate some misunderstanding on the actual role of these microorganisms in the etiology of periodontitis. The aim of this systematic review was to determine the current weight of evidence for newly identified periodontal pathogens based on the results of "association" studies. This review was conducted and reported in accordance with the PRISMA statement. The MEDLINE, EMBASE, and Cochrane databases were searched up to September 2013 for studies (1) comparing microbial data of subgingival plaque samples collected from subjects with periodontitis and periodontal health and (2) evaluating at least 1 microorganism other than the already-known periodontal pathogens. From 1,450 papers identified, 41 studies were eligible. The data were extracted and registered in predefined piloted forms. The results suggested that there is moderate evidence in the literature to support the association of 17 species or phylotypes from the phyla Bacteroidetes, Candidatus Saccharibacteria, Firmicutes, Proteobacteria, Spirochaetes, and Synergistetes. The phylum Candidatus Saccharibacteria and the Archaea domain also seem to have an association with disease. These data point out the importance of previously unidentified species in the etiology of periodontitis and might guide future investigations on the actual role of these suspected new pathogens in the onset and progression of this infection. © International & American Associations for Dental Research.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                mSphere
                mSphere
                msph
                msph
                mSphere
                mSphere
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2379-5042
                15 August 2018
                Jul-Aug 2018
                : 3
                : 4
                : e00332-18
                Affiliations
                [a ]Section of Preventive and Public Health Dentistry, Division of Oral Health, Growth and Development, Faculty of Dental Science, Kyushu University, Fukuoka, Japan
                [b ]OBT Research Center, Faculty of Dental Science, Kyushu University, Fukuoka, Japan
                [c ]Department of Epidemiology and Public Health, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan
                [d ]Center for Cohort Studies, Graduate School of Medical Sciences, Kyushu University, Fukuoka, Japan
                University of Wisconsin—Madison
                Author notes
                Address correspondence to Yoshihisa Yamashita, yoshi@ 123456dent.kyushu-u.ac.jp .

                M.A. and T.T. contributed equally to this article.

                Citation Asakawa M, Takeshita T, Furuta M, Kageyama S, Takeuchi K, Hata J, Ninomiya T, Yamashita Y. 2018. Tongue microbiota and oral health status in community-dwelling elderly adults. mSphere 3:e00332-18. https://doi.org/10.1128/mSphere.00332-18.

                Article
                mSphere00332-18
                10.1128/mSphere.00332-18
                6094060
                30111628
                5e6efaaa-9e9a-452f-868c-a9c949e7f853
                Copyright © 2018 Asakawa et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                History
                : 20 June 2018
                : 17 July 2018
                Page count
                supplementary-material: 5, Figures: 5, Tables: 4, Equations: 0, References: 47, Pages: 13, Words: 8531
                Funding
                Funded by: MEXT | Japan Society for the Promotion of Science (JSPS), https://doi.org/10.13039/501100001691;
                Award ID: 16H05557
                Award ID: 16K15856
                Award Recipient :
                Funded by: MEXT | Japan Society for the Promotion of Science (JSPS), https://doi.org/10.13039/501100001691;
                Award ID: 16H02692
                Award ID: 16H05850
                Award Recipient :
                Categories
                Research Article
                Clinical Science and Epidemiology
                Custom metadata
                July/August 2018

                community-dwelling,dental,elderly,microbiota,oral,tongue
                community-dwelling, dental, elderly, microbiota, oral, tongue

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