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Cited by 116Oral microbiology and periodontitis researchDental Health and Care UtilizationGut microbiota and health

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Tongue microbiota and oral health status in community-dwelling elderly adults.

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Asakawa, Mikari, Takeshita, Toru, Furuta, Michiko, Kageyama, Shinya, Takeuchi, Kenji, Hata, Jun, Ninomiya, Toshiharu, Yamashita, Yoshihisa·2018·mSphere
DOI 10.1128/msphere.00332-18PMC PMC6094060
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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.

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Crossref · 10.1128/msphere.00332-18

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FIG 1 Co-occurrence network in tongue microbiota of 506 elderly adults built from SparCC correlation coefficients between sequence abundances. Nodes corresponding to operational taxonomic units (OTUs) and connecting edges indicate the correlation between them. Only correlations with values greater than 0.40 are represented as edges. The node size indicates a mean relative abundance of each OTU. (A) All OTUs excluding isolated nodes corresponding to the OTUs with a mean relative abundance of <1% are shown as nodes in the diagram (72 of all 730 OTUs). Most of the predominant OTUs (with mean relative abundance of >1%) belonged to either of the two major networks including multiple predominant OTUs (cohabiting commensal groups I and II). The nodes belonging to commensal groups I and II are colored red and blue, respectively. (B) Only the co-occurrence network of OTUs belonging to commensal group I is shown. The bacterial taxa corresponding to the predominant OTUs are described. Oral taxon IDs in the Human Oral Microbiome database are given in parentheses following the bacterial names. Abbreviations: Pre., Prevotella; Vei., Veillonella; Str., Streptococcus. (C) Here, only the co-occurrence network of OTUs belonging to commensal group II is shown. The bacterial taxa corresponding to the predominant OTUs are described. Oral taxon IDs in the Human Oral Microbiome database are given in parentheses following bacterial names. Abbreviations: Nei., Neisseria; Hae., Haemophilus; Por., Porphyromonas; Gra., Granulicatella; Fus., Fusobacterium; Pre., Prevotella; Act., Actinomyces; Lep., Leptotorichia; All., Alloprevotella.
FIG 1 Co-occurrence network in tongue microbiota of 506 elderly adults built from SparCC correlation coefficients between sequence abundances. Nodes corresponding to operational taxonomic units (OTUs) and connecting edges indicate the correlation between them. Only correlations with values greater than 0.40 are represented as edges. The node size indicates a mean relative abundance of each OTU. (A) All OTUs excluding isolated nodes corresponding to the OTUs with a mean relative abundance of <1% are shown as nodes in the diagram (72 of all 730 OTUs). Most of the predominant OTUs (with mean relative abundance of >1%) belonged to either of the two major networks including multiple predominant OTUs (cohabiting commensal groups I and II). The nodes belonging to commensal groups I and II are colored red and blue, respectively. (B) Only the co-occurrence network of OTUs belonging to commensal group I is shown. The bacterial taxa corresponding to the predominant OTUs are described. Oral taxon IDs in the Human Oral Microbiome database are given in parentheses following the bacterial names. Abbreviations: Pre., Prevotella; Vei., Veillonella; Str., Streptococcus. (C) Here, only the co-occurrence network of OTUs belonging to commensal group II is shown. The bacterial taxa corresponding to the predominant OTUs are described. Oral taxon IDs in the Human Oral Microbiome database are given in parentheses following bacterial names. Abbreviations: Nei., Neisseria; Hae., Haemophilus; Por., Porphyromonas; Gra., Granulicatella; Fus., Fusobacterium; Pre., Prevotella; Act., Actinomyces; Lep., Leptotorichia; All., Alloprevotella.CC BY · PubMed Central
FIG 2 SparCC correlation coefficients between sequence abundances of predominant operational taxonomic units (OTUs) (with a mean relative abundance of >1%) belonging to cohabiting commensal groups I and II. The pairwise correlation coefficient is shown in each grid by the color intensity. The OTUs are ordered according to the result of a hierarchical cluster analysis using the Euclidean distance with average linkage (shown as a dendrogram on the left). Correlations with values greater than 0.40 are represented as edges in Fig. 1.
FIG 2 SparCC correlation coefficients between sequence abundances of predominant operational taxonomic units (OTUs) (with a mean relative abundance of >1%) belonging to cohabiting commensal groups I and II. The pairwise correlation coefficient is shown in each grid by the color intensity. The OTUs are ordered according to the result of a hierarchical cluster analysis using the Euclidean distance with average linkage (shown as a dendrogram on the left). Correlations with values greater than 0.40 are represented as edges in Fig. 1.CC BY · PubMed Central
FIG 3 Tongue coating score and total bacterial and fungal density per 15-mm-diameter circular area at the center of the tongue dorsum of the elderly adults with various oral conditions. Of the 506 individuals, the 16 edentulous elderly were excluded from the maximum plaque index, percentage of decayed and filled teeth (DFT), number of decayed teeth (DT), percentage of teeth with bleeding on probing (BOP), and mean periodontal pocket depth (PPD), whereas 349 individuals with ≥20 teeth were excluded from denture use. The individuals were categorized into the tertile of percentage of DFT, percentage of teeth with BOP, and mean PPD, and then the parameters of the microbiota status were compared. Dots indicate the mean; the error bars indicate 95% confidence intervals. ***, P < 0.001, **, P < 0.01, and *, P < 0.05, by Kruskal-Wallis analysis.
FIG 3 Tongue coating score and total bacterial and fungal density per 15-mm-diameter circular area at the center of the tongue dorsum of the elderly adults with various oral conditions. Of the 506 individuals, the 16 edentulous elderly were excluded from the maximum plaque index, percentage of decayed and filled teeth (DFT), number of decayed teeth (DT), percentage of teeth with bleeding on probing (BOP), and mean periodontal pocket depth (PPD), whereas 349 individuals with ≥20 teeth were excluded from denture use. The individuals were categorized into the tertile of percentage of DFT, percentage of teeth with BOP, and mean PPD, and then the parameters of the microbiota status were compared. Dots indicate the mean; the error bars indicate 95% confidence intervals. ***, P < 0.001, **, P < 0.01, and *, P < 0.05, by Kruskal-Wallis analysis.CC BY · PubMed Central
FIG 4 Alpha diversity and relative abundances of periodontitis- and dental caries-associated taxa in tongue microbiota of the elderly adults with various oral conditions. Of the 506 individuals, the 16 edentulous elderly were excluded from the maximum plaque index, percentage of decayed and filled teeth (DFT), number of decayed teeth (DT), percentage of teeth with bleeding on probing (BOP), and mean periodontal pocket depth (PPD), whereas 349 participants with ≥20 teeth were excluded from denture use. The individuals were categorized into the tertile of percentage of DFT, percentage of teeth with BOP, and mean PPD, and the parameters of the microbiota status were compared. Dots indicate the mean; the error bars indicate 95% confidence intervals. ***, P < 0.001, **, P < 0.01, and *, P < 0.05, by Kruskal-Wallis analysis.
FIG 4 Alpha diversity and relative abundances of periodontitis- and dental caries-associated taxa in tongue microbiota of the elderly adults with various oral conditions. Of the 506 individuals, the 16 edentulous elderly were excluded from the maximum plaque index, percentage of decayed and filled teeth (DFT), number of decayed teeth (DT), percentage of teeth with bleeding on probing (BOP), and mean periodontal pocket depth (PPD), whereas 349 participants with ≥20 teeth were excluded from denture use. The individuals were categorized into the tertile of percentage of DFT, percentage of teeth with BOP, and mean PPD, and the parameters of the microbiota status were compared. Dots indicate the mean; the error bars indicate 95% confidence intervals. ***, P < 0.001, **, P < 0.01, and *, P < 0.05, by Kruskal-Wallis analysis.CC BY · PubMed Central
FIG 5 Relative abundances of two cohabiting commensal groups in tongue microbiota of elderly adults with various oral conditions. Of the 506 individuals, the 16 edentulous elderly were excluded from the maximum plaque index, percentage of decayed and filled teeth (DFT), number of decayed teeth (DT), percentage of teeth with bleeding on probing (BOP), and mean periodontal pocket depth (PPD), whereas 349 participants with ≥20 teeth were excluded from denture use. The individuals were categorized into the tertile of percentage of DFT, percentage of teeth with BOP, and mean PPD, and the parameters of the microbiota status were compared. Dots indicate the mean; the error bars indicate 95% confidence intervals. ***, P < 0.001, **, P < 0.01, and *, P < 0.05, in Kruskal-Wallis analysis.
FIG 5 Relative abundances of two cohabiting commensal groups in tongue microbiota of elderly adults with various oral conditions. Of the 506 individuals, the 16 edentulous elderly were excluded from the maximum plaque index, percentage of decayed and filled teeth (DFT), number of decayed teeth (DT), percentage of teeth with bleeding on probing (BOP), and mean periodontal pocket depth (PPD), whereas 349 participants with ≥20 teeth were excluded from denture use. The individuals were categorized into the tertile of percentage of DFT, percentage of teeth with BOP, and mean PPD, and the parameters of the microbiota status were compared. Dots indicate the mean; the error bars indicate 95% confidence intervals. ***, P < 0.001, **, P < 0.01, and *, P < 0.05, in Kruskal-Wallis analysis.CC BY · PubMed Central

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Research works printed but not linked: 1

  1. Yanou Y. 2011. Components of oral malodor caused by aging and its origin. Shikoku Dent Res 24. (In Japanese.)

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Metadata

Authors
Asakawa, M., Takeshita, T., Furuta, M., Kageyama, S., Takeuchi, K., Hata, J., Ninomiya, T., & Yamashita, Y.
Affiliations
Kyushu University (JP)
Corresponding author
Yamashita, Yoshihisa
ORCID
Venue
mSphere
Publisher
American Society for Microbiology
Published
2018-08-29
Volume
3
Issue
4
ISSN
2379-5042 (ISSN-L)
DOI
10.1128/msphere.00332-18
PMC
PMC6094060
OpenAlex
W2885874599
Cited by
113
References
47
Citations by year
2026: 8 · 2025: 12 · 2024: 14 · 2023: 8 · 2022: 13 · 2021: 22 · 2020: 24 · 2019: 12
FWCI
16.63
Type
journal article
Language
en
Open access
Licence
Locations
  • mSphere (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Kyushu University Institutional Repository (QIR) (Kyushu University) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
MEXT | Japan Society for the Promotion of Science (16H05557, 16K15856, 16H02692, 16H05850)
Topics
  • Health Sciences › Dentistry › Periodontics › Oral microbiology and periodontitis research
  • Health Sciences › Dentistry › General Dentistry › Dental Health and Care Utilization
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
Keywords
tongue microbiota, oral microbiota, community-dwelling older adults, oral health, aspiration, pneumonia, dysbiosis, tooth loss, dental caries, dental hygiene, commensal bacteria, respiratory health, swallowing impairment
MeSH terms
Aged, Bacteria, DNA, Bacterial, DNA, Ribosomal, Fungi, Humans, Japan, Oral Health, RNA, Ribosomal, 16S, Tongue, Cluster Analysis, Sequence Analysis, DNA, Independent Living, High-Throughput Nucleotide Sequencing, Real-Time Polymerase Chain Reaction, Microbiota

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