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Article: Longitudinal Multi-omics and Microbiome Meta-analysis Identify an Asymptomatic Gingival State That Links Gingivitis, Periodontitis, and Aging

TitleLongitudinal Multi-omics and Microbiome Meta-analysis Identify an Asymptomatic Gingival State That Links Gingivitis, Periodontitis, and Aging
Authors
Keywordsgingivitis
periodontitis
microbiome
aging
disease prevention
Issue Date2021
PublisherAmerican Society for Microbiology: Open Access Journals. The Journal's web site is located at http://mbio.asm.org
Citation
mBio, 2021, v. 12 n. 2, article no. e03281-20 How to Cite?
AbstractMost adults experience episodes of gingivitis, which can progress to the irreversible, chronic state of periodontitis, yet roles of plaque in gingivitis onset and progression to periodontitis remain elusive. Here, we longitudinally profiled the plaque metagenome, the plaque metabolome, and salivary cytokines in 40 adults who transited from naturally occurring gingivitis (NG) to healthy gingivae (baseline) and then to experimental gingivitis (EG). During EG, rapid and consistent alterations in plaque microbiota, metabolites, and salivary cytokines emerged as early as 24 to 72 h after oral-hygiene pause, defining an asymptomatic suboptimal health (SoH) stage of the gingivae. SoH features a swift, full activation of 11 salivary cytokines but a steep synergetic decrease of plaque-derived betaine and Rothia spp., suggesting an anti-gum inflammation mechanism by health-promoting symbionts. Global, cross-cohort meta-analysis revealed, at SoH, a greatly elevated microbiome-based periodontitis index driven by its convergence of both taxonomical and functional profiles toward the periodontitis microbiome. Finally, post-SoH gingivitis development accelerates oral microbiota aging by over 1 year within 28 days, with Rothia spp. depletion and Porphyromonas gingivalis elevation as hallmarks. Thus, the microbiome-defined, transient gum SoH stage is a crucial link among gingivitis, periodontitis, and aging. IMPORTANCE A significant portion of world population still fails to brush teeth daily. As a result, the majority of the global adult population is afflicted with chronic gingivitis, and if it is left untreated, some of them will eventually suffer from periodontitis. Here, we identified periodontitis-like microbiome dysbiosis in an asymptomatic SoH stage as early as 24 to 72 h after oral-hygiene pause. SoH features a swift, full activation of multiple salivary cytokines but a steep synergetic decrease of plaque-derived betaine and Rothia spp. The microbial ecology during early gingivitis is highly similar to that in periodontitis under both taxonomical and functional contexts. Unexpectedly, exposures to gingivitis can accelerate over 10-fold the normal rate of oral microbiota aging. Our findings underscore the importance of intervening at the SoH stage of gingivitis via proper oral-hygiene practices on a daily basis, so as to maintain a periodontitis-preventive plaque and ensure the healthy aging of the oral ecosystem.
Persistent Identifierhttp://hdl.handle.net/10722/297627
ISSN
2023 Impact Factor: 5.1
2023 SCImago Journal Rankings: 2.028
PubMed Central ID
ISI Accession Number ID

 

DC FieldValueLanguage
dc.contributor.authorHuang, S-
dc.contributor.authorHe, T-
dc.contributor.authorYue, F-
dc.contributor.authorXu, X-
dc.contributor.authorWang, L-
dc.contributor.authorZhu, P-
dc.contributor.authorTeng, F-
dc.contributor.authorSun, Z-
dc.contributor.authorLiu, X-
dc.contributor.authorJing, G-
dc.contributor.authorSu, X-
dc.contributor.authorJin, L-
dc.contributor.authorLiu, J-
dc.contributor.authorXu, J-
dc.date.accessioned2021-03-23T04:19:36Z-
dc.date.available2021-03-23T04:19:36Z-
dc.date.issued2021-
dc.identifier.citationmBio, 2021, v. 12 n. 2, article no. e03281-20-
dc.identifier.issn2150-7511-
dc.identifier.urihttp://hdl.handle.net/10722/297627-
dc.description.abstractMost adults experience episodes of gingivitis, which can progress to the irreversible, chronic state of periodontitis, yet roles of plaque in gingivitis onset and progression to periodontitis remain elusive. Here, we longitudinally profiled the plaque metagenome, the plaque metabolome, and salivary cytokines in 40 adults who transited from naturally occurring gingivitis (NG) to healthy gingivae (baseline) and then to experimental gingivitis (EG). During EG, rapid and consistent alterations in plaque microbiota, metabolites, and salivary cytokines emerged as early as 24 to 72 h after oral-hygiene pause, defining an asymptomatic suboptimal health (SoH) stage of the gingivae. SoH features a swift, full activation of 11 salivary cytokines but a steep synergetic decrease of plaque-derived betaine and Rothia spp., suggesting an anti-gum inflammation mechanism by health-promoting symbionts. Global, cross-cohort meta-analysis revealed, at SoH, a greatly elevated microbiome-based periodontitis index driven by its convergence of both taxonomical and functional profiles toward the periodontitis microbiome. Finally, post-SoH gingivitis development accelerates oral microbiota aging by over 1 year within 28 days, with Rothia spp. depletion and Porphyromonas gingivalis elevation as hallmarks. Thus, the microbiome-defined, transient gum SoH stage is a crucial link among gingivitis, periodontitis, and aging. IMPORTANCE A significant portion of world population still fails to brush teeth daily. As a result, the majority of the global adult population is afflicted with chronic gingivitis, and if it is left untreated, some of them will eventually suffer from periodontitis. Here, we identified periodontitis-like microbiome dysbiosis in an asymptomatic SoH stage as early as 24 to 72 h after oral-hygiene pause. SoH features a swift, full activation of multiple salivary cytokines but a steep synergetic decrease of plaque-derived betaine and Rothia spp. The microbial ecology during early gingivitis is highly similar to that in periodontitis under both taxonomical and functional contexts. Unexpectedly, exposures to gingivitis can accelerate over 10-fold the normal rate of oral microbiota aging. Our findings underscore the importance of intervening at the SoH stage of gingivitis via proper oral-hygiene practices on a daily basis, so as to maintain a periodontitis-preventive plaque and ensure the healthy aging of the oral ecosystem.-
dc.languageeng-
dc.publisherAmerican Society for Microbiology: Open Access Journals. The Journal's web site is located at http://mbio.asm.org-
dc.relation.ispartofmBio-
dc.rightsThis work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.-
dc.subjectgingivitis-
dc.subjectperiodontitis-
dc.subjectmicrobiome-
dc.subjectaging-
dc.subjectdisease prevention-
dc.titleLongitudinal Multi-omics and Microbiome Meta-analysis Identify an Asymptomatic Gingival State That Links Gingivitis, Periodontitis, and Aging-
dc.typeArticle-
dc.identifier.emailJin, L: ljjin@hkucc.hku.hk-
dc.identifier.authorityJin, L=rp00028-
dc.description.naturepublished_or_final_version-
dc.identifier.doi10.1128/mBio.03281-20-
dc.identifier.pmid33688007-
dc.identifier.pmcidPMC8092283-
dc.identifier.scopuseid_2-s2.0-85102100074-
dc.identifier.hkuros321806-
dc.identifier.volume12-
dc.identifier.issue2-
dc.identifier.spagearticle no. e03281-20-
dc.identifier.epagearticle no. e03281-20-
dc.identifier.isiWOS:000643733900009-
dc.publisher.placeUnited States-

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