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      Periodontitis may induce gut microbiota dysbiosis via salivary microbiota

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          Abstract

          The aim of this study was to identify whether periodontitis induces gut microbiota dysbiosis via invasion by salivary microbes. First, faecal and salivary samples were collected from periodontally healthy participants (PH group, n = 16) and patients with severe periodontitis (SP group, n = 21) and analysed by 16S ribosomal RNA sequencing. Significant differences were observed in both the faecal and salivary microbiota between the PH and SP groups. Notably, more saliva-sourced microbes were observed in the faecal samples of the SP group. Then, the remaining salivary microbes were transplanted into C57BL6/J mice (the C-PH group and the C-SP group), and it was found that the composition of the gut microbiota of the C-SP group was significantly different from that of the C-PH group, with Porphyromonadaceae and Fusobacterium being significantly enriched in the C-SP group. In the colon, the C-SP group showed significantly reduced crypt depth and zonula occludens-1 expression. The mRNA expression levels of pro-inflammatory cytokines, chemokines and tight junction proteins were significantly higher in the C-SP group. To further investigate whether salivary bacteria could persist in the intestine, the salivary microbiota was stained with carboxyfluorescein diacetate succinimidyl ester and transplanted into mice. We found that salivary microbes from both the PH group and the SP group could persist in the gut for at least 24 h. Thus, our data demonstrate that periodontitis may induce gut microbiota dysbiosis through the influx of salivary microbes.

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          Most cited references54

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          Microbial complexes in subgingival plaque

          Journal of Clinical Periodontology, 25(2), 134-144
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            Global burden of severe periodontitis in 1990-2010: a systematic review and meta-regression.

            We aimed to consolidate all epidemiologic data about severe periodontitis (SP) and, subsequently, to generate internally consistent prevalence and incidence estimates for all countries, 20 age groups, and both sexes for 1990 and 2010. The systematic search of the literature yielded 6,394 unique citations. After screening titles and abstracts, we excluded 5,881 citations as clearly not relevant to this systematic review, leaving 513 for full-text review. A further 441 publications were excluded following the validity assessment. A total of 72 studies, including 291,170 individuals aged 15 yr or older in 37 countries, were included in the metaregression based on modeling resources of the Global Burden of Disease 2010 Study. SP was the sixth-most prevalent condition in the world. Between 1990 and 2010, the global age-standardized prevalence of SP was static at 11.2% (95% uncertainty interval: 10.4%-11.9% in 1990 and 10.5%-12.0% in 2010). The age-standardized incidence of SP in 2010 was 701 cases per 100,000 person-years (95% uncertainty interval: 599-823), a nonsignificant increase from the 1990 incidence of SP. Prevalence increased gradually with age, showing a steep increase between the third and fourth decades of life that was driven by a peak in incidence at around 38 yr of age. There were considerable variations in prevalence and incidence between regions and countries. Policy makers need to be aware of a predictable increasing burden of SP due to the growing world population associated with an increasing life expectancy and a significant decrease in the prevalence of total tooth loss throughout the world from 1990 to 2010.
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              Ectopic colonization of oral bacteria in the intestine drives TH1 cell induction and inflammation

              Intestinal colonization by bacteria of oral origin has been correlated with several negative health outcomes, including inflammatory bowel disease. However, a causal role of oral bacteria ectopically colonizing the intestine remains unclear. Using gnotobiotic techniques, we show that strains of Klebsiella spp. isolated from the salivary microbiota are strong inducers of T helper 1 (TH1) cells when they colonize in the gut. These Klebsiella strains are resistant to multiple antibiotics, tend to colonize when the intestinal microbiota is dysbiotic, and elicit a severe gut inflammation in the context of a genetically susceptible host. Our findings suggest that the oral cavity may serve as a reservoir for potential intestinal pathobionts that can exacerbate intestinal disease.
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                Author and article information

                Contributors
                361734128@qq.com
                yanfh@nju.edu.cn
                Journal
                Int J Oral Sci
                Int J Oral Sci
                International Journal of Oral Science
                Nature Publishing Group UK (London )
                1674-2818
                2049-3169
                23 June 2022
                23 June 2022
                2022
                : 14
                : 32
                Affiliations
                [1 ]GRID grid.41156.37, ISNI 0000 0001 2314 964X, Department of Periodontology, Nanjing Stomatological Hospital, , Medical School of Nanjing University, ; No.30 Zhongyang Road, Nanjing, China
                [2 ]GRID grid.233520.5, ISNI 0000 0004 1761 4404, State Key Laboratory of Military Stomatology & National Clinical Research Center for Oral Diseases & Shaanxi Clinical Research Center for Oral Diseases, Department of Periodontology, School of Stomatology, , Fourth Military Medical University, ; Xi’an, China
                [3 ]GRID grid.27255.37, ISNI 0000 0004 1761 1174, Department of Periodontology, School and Hospital of Stomatology, Cheeloo College of Medicine, , Shandong University & Shandong Key Laboratory of Oral Tissue Regeneration & Shandong Engineering Laboratory for Dental Materials and Oral Tissue Regeneration, ; Jinan, China
                Author information
                http://orcid.org/0000-0002-8398-2104
                http://orcid.org/0000-0002-6963-3530
                Article
                183
                10.1038/s41368-022-00183-3
                9217941
                35732628
                eb55a169-61a8-4f98-bcbd-0b071581f3af
                © The Author(s) 2022

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as 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 images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 9 January 2022
                : 23 May 2022
                : 28 May 2022
                Funding
                Funded by: The present study was supported by the National Science Foundation of China (No. 81970939), Nanjing Clinical Research Center for Oral Diseases (No. 2019060009).
                Categories
                Article
                Custom metadata
                © The Author(s) 2022

                Dentistry
                periodontitis,bacterial genomics,bacterial infection
                Dentistry
                periodontitis, bacterial genomics, bacterial infection

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