Tracing the accumulation of in vivo human oral microbiota elucidates microbial community dynamics at the gateway to the GI tract

Wang, Jinfeng; Jia, Zhen; Zhang, Bing; Peng, Lei; Zhao, Fangqing

doi:10.1136/gutjnl-2019-318977

Cited by 53 publications

(52 citation statements)

References 10 publications

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“…Taken together, these results showed that treatment with S. dentisani probiotic results in a microbial shift in composition which is consistent with a healthier microbiota, as there is a decrease of microorganisms associated with dental caries such as Scardovia wiggsiae (Tanner et al, 2011 ), Actinomyces sp., Veillonella sp. (Belda-Ferre et al, 2012 ; Simón-Soro et al, 2014 ), and Atopobium parvulum (Obata et al, 2014 ); a decrease in bacteria associated with periodontal diseases and halitosis such as Dialister (Silva-Boghossian et al, 2013 ), Prevotella (Camelo-Castillo et al, 2015 ), and Fusobacterium nucleatum (Wang et al, 2019 ); and an increase in some bacteria associated with oral health such as Gemella (Luo et al, 2012 ) and Kingella (Belda-Ferre et al, 2012 ).…”

Section: Resultsmentioning

confidence: 99%

Topic Application of the Probiotic Streptococcus dentisani Improves Clinical and Microbiological Parameters Associated With Oral Health

Ferrer

López-López

Nicolescu

et al. 2020

Front. Cell. Infect. Microbiol.

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Streptococcus dentisani 7746, isolated from dental plaque of caries-free individuals, has been shown to have several beneficial effects in vitro which could contribute to promote oral health, including an antimicrobial activity against oral pathogens by the production of bacteriocins and a pH buffering capacity through ammonia production. Previous work has shown that S. dentisani was able to colonize the oral cavity for 2–4 weeks after application. The aim of the present work was to evaluate its clinical efficacy by a randomized, double-blind, placebo-controlled parallel group study. Fifty nine volunteers were enrolled in the study and randomly assigned to a treatment or placebo group. The treatment consisted of a bucco-adhesive gel application (2.5 10 9 cfu/dose) with a dental splint for 5 min every 48 h, for a period of 1 month (i.e., 14 doses). Dental plaque and saliva samples were collected at baseline, 15 and 30 days after first application, and 15 days after the end of treatment. At baseline, there was a significant correlation between S. dentisani levels and frequency of toothbrushing. Salivary flow, a major factor influencing oral health, was significantly higher in the probiotic group at day 15 compared with the placebo (4.4 and 3.4 ml/5 min, respectively). In the probiotic group, there was a decrease in the amount of dental plaque and in gingival inflammation, but no differences were observed in the placebo group. The probiotic group showed a significant increase in the levels of salivary ammonia and calcium. Finally, Illumina sequencing of plaque samples showed a beneficial shift in bacterial composition at day 30 relative to baseline, with a reduction of several cariogenic organisms and the key players in plaque formation, probably as a result of bacteriocins production. Only 58% of the participants in the probiotic group showed increased plaque levels of S. dentisani at day 30 and 71% by day 45, indicating that the benefits of S. dentisani application could be augmented by improving colonization efficiency. In conclusion, the application of S. dentisani 7746 improved several clinical and microbiological parameters associated with oral health, supporting its use as a probiotic to prevent tooth decay.

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Section: Resultsmentioning

confidence: 99%

Topic Application of the Probiotic Streptococcus dentisani Improves Clinical and Microbiological Parameters Associated With Oral Health

Ferrer

López-López

Nicolescu

et al. 2020

Front. Cell. Infect. Microbiol.

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“…We chose saliva as an oral sample not only because it is easy to obtain, but also because the salivary microbial community is more stable than that of dental plaque. 56 Given the heterogeneity of F. nucleatum at the species and subspecies levels, we used MED to analyze 16S rRNA genes to achieve resolution beyond the subspecies level. Fusobacterium 16S rRNA genes were amplified by PCR, followed by cloning and Sanger sequencing.…”

Section: Discussionmentioning

confidence: 99%

Analysis of 16S rRNA genes reveals reduced Fusobacterial community diversity when translocating from saliva to GI sites

et al. 2020

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Fusobacterium nucleatum is a Gram-negative oral commensal anaerobe which has been increasingly implicated in various gastrointestinal (GI) disorders, including inflammatory bowel disease, appendicitis, GI cancers. The oral cavity harbors a diverse group of Fusobacterium , and it is postulated that F. nucleatum in the GI tract originate from the mouth. It is not known, however, if all oral Fusobacterium translocate to the GI sites with equal efficiencies. Therefore, we amplified 16S rRNA genes of F. nucleatum and F. periodonticum , two closely related oral species from matched saliva, gastric aspirates, and colon or ileal pouch aspirates of three patients with inflammatory bowel disease (IBD) and three healthy controls, and saliva alone from seven patients with either active IBD or IBD in remission. The 16S rRNA gene amplicons were cloned, and the DNA sequences determined by Sanger sequencing. The results demonstrate that fusobacterial community composition differs more significantly between the oral and GI sites than between different individuals. The oral communities demonstrate the highest level of variation and have the richest pool of unique sequences, with certain nodes/strains enriched in the GI tract and others diminished during translocation. The gastric and colon/pouch communities exhibit reduced diversity and are more closely related, possibly due to selective pressure in the GI tract. This study elucidates selective translocation of oral fusobacteria to the GI tract. Identification of specific transmissible clones will facilitate risk assessment for developing Fusobacterium -implicated GI disorders.

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“…Notably, although taxonomic shift in plaque took place as early as 24 hours after dental prophylaxis (by acquiring microbial colonizers from saliva (11,20)), it was accompanied by a delayed functional shift as revealed by plaque metabolome. This suggests that establishment of primary colonists in plaque altered within 48 hours (i.e., at or by Day 3) the plaque metabolome, which then elicits both gingival inflammation and subsequent plaque development, starting a detrimental cycle: periodontal tissue destruction by plaque dysbiosis provides nutrients for bacterial growth, which further promotes dysbiosis and tissue inflammation (11).…”

Section: Discussionmentioning

confidence: 99%

“…Surprisingly, the implication of this SoH stage finds support from our meta-analysis of past oral microbiome studies, which reveals a microbiome-mediated link between the very early (i.e., SoH of gingivitis) and very late stage (periodontitis) of the periodontal disease which can span decades and affects over half of the global population. Gingivitis and periodontitis patients can share a significant number of bacteria genera (18)(19)(20)23), and periodontal treatments can result in depletion of disease-associated bacteria and enrichment of health-associated ones in plaque (16,17,34). However, systematically tracking microbial associations across different stages for chronic periodontal diseases remains a challenge, since it is impractical to create or modulate advanced disease states directly in humans, while clinical studies can only induce mild or moderate disease states (notably, this holds true for many chronic diseases).…”

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Longitudinal multi-omics along gingivitis development reveal a suboptimal-health gum state with periodontitis-like microbiome

Huang

Feng³

et al. 2020

Preprint

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Most adults experience episodes of gingivitis, which can progress to the irreversible, chronic state of periodontitis. However the mechanistic roles of plaque in gingivitis onset and progression to periodontitis remain elusive. Here, we integrated the longitudinal multi-omics data from plaque metagenome, metabolome and salivary cytokines in 40 adults who transit 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 24-72 hours after pause of oral hygiene, defining an asymptomatic 'sub-optimal health' (SoH) stage. SoH also features a steep and synergetic decrease of plaque-derived betaine and Rothia spp., suggesting an anti-gum-inflammation mechanism by health-promoting microbial residents. Global, cross-cohort meta-analysis revealed a high Microbiome-based Periodontitis Index at SoH state, due to its convergent taxonomical and functional profiles towards those of periodontitis. In contrast, caries SoH features a microbial signature very distinct from caries. Thus SoH is a universal state of polymicrobial inflammations with disease-specific features, which is key to maintaining a disease-preventive plaque.

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Tracing the accumulation of in vivo human oral microbiota elucidates microbial community dynamics at the gateway to the GI tract

Cited by 53 publications

References 10 publications

Topic Application of the Probiotic Streptococcus dentisani Improves Clinical and Microbiological Parameters Associated With Oral Health

Topic Application of the Probiotic Streptococcus dentisani Improves Clinical and Microbiological Parameters Associated With Oral Health

Analysis of 16S rRNA genes reveals reduced Fusobacterial community diversity when translocating from saliva to GI sites

Longitudinal multi-omics along gingivitis development reveal a suboptimal-health gum state with periodontitis-like microbiome

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