Low-Abundance Biofilm Species Orchestrates Inflammatory Periodontal Disease through the Commensal Microbiota and Complement

Hajishengallis, George; Liang, Shuang; Payne, Mark; Hashim, Ahmed; Jotwani, Ravi; Eskan, Mehmet A.; McIntosh, Megan L.; Alsam, Asil; Kirkwood, Keith L.; Lambris, John D.; Darveau, Richard P.; Curtis, Michael A.

doi:10.1016/j.chom.2011.10.006

Cited by 955 publications

(1,165 citation statements)

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“…Although it appeared logical that Actinomyces, a prominent genus in health, negatively correlated with microbial load in periodontitis, it was unexpected to find lower proportions of periodontitis-associated taxa when microbial load was high. Recent studies in mice demonstrated that, low-levels of colonization by periodontitis-associated microorganisms such as Porphyromonas gingivalis are sufficient to dysregulate innate immunity pathways, facilitate an increase in overall community biomass and trigger periodontal destruction (Hajishengallis et al, 2011). Indeed, in the current study, Porphyromonas was among the genera showing a trend negative correlation with bacterial load in periodontitis.…”

Section: Subgingival Microbiome Periodontal Destruction and Inflammasupporting

confidence: 49%

The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation

et al. 2013

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The goals of this study were to better understand the ecology of oral subgingival communities in health and periodontitis and elucidate the relationship between inflammation and the subgingival microbiome. Accordingly, we used 454-pyrosequencing of 16S rRNA gene libraries and quantitative PCR to characterize the subgingival microbiome of 22 subjects with chronic periodontitis. Each subject was sampled at two sites with similar periodontal destruction but differing in the presence of bleeding, a clinical indicator of increased inflammation. Communities in periodontitis were also compared with those from 10 healthy individuals. In periodontitis, presence of bleeding was not associated with different a-diversity or with a distinct microbiome, however, bleeding sites showed higher total bacterial load. In contrast, communities in health and periodontitis largely differed, with higher diversity and biomass in periodontitis. Shifts in community structure from health to periodontitis resembled ecological succession, with emergence of newly dominant taxa in periodontitis without replacement of primary health-associated species. That is, periodontitis communities had higher proportions of Spirochetes, Synergistetes, Firmicutes and Chloroflexi, among other taxa, while the proportions of Actinobacteria, particularly Actinomyces, were higher in health. Total Actinomyces load, however, remained constant from health to periodontitis. Moreover, an association existed between biomass and community structure in periodontitis, with the proportion of specific taxa correlating with bacterial load. Our study provides a global-scale framework for the ecological events in subgingival communities that underline the development of periodontitis. The association, in periodontitis, between inflammation, community biomass and community structure and their role in disease progression warrant further investigation.

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Section: Subgingival Microbiome Periodontal Destruction and Inflammasupporting

confidence: 49%

The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation

et al. 2013

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“…Therefore, elucidating the mechanisms for the pathogenesis of NASH may be valuable for drafting prophylactic and therapeutic strategies. P. gingivalis is part of a bacterial group called the keystone, of which a small amount plays a central role in the progression of chronic periodontitis (Hajishengallis et al, 2012; Hajishengallis et al, 2011). Lipopolysaccharide and various proteases produced by P. gingivalis are known to be associated with various systemic diseases, in addition to periodontal pathogens (Seymour et al, 2007; Mikuls, 2009).…”

Section: Discussionmentioning

confidence: 99%

“…Porphyromonas gingivalis ( P. gingivalis ) is a primary causative agent of periodontitis (Socransky, Haffajee, Cugini, Smith, & Kent, 1998; Hajishengallis, Darveau, & Curtis, 2012; Hajishengallis et al, 2011), and a number of studies have detected P. gingivalis in various organs throughout the body as well as in the oral cavity; thus, it might be a risk factor for systemic diseases including cardiovascular disease, diabetes, and rheumatoid arthritis (Seymour, Ford, Cullinan, Leishman, & Yamazak, 2007; Pizzo, Guiglia, Russo, & Campisi, 2011; Figuero & Sanchez‐Beltran, 2011). A recent epidemiological study showing that P. gingivalis at high frequency was present in NAFLD/NASH patients suggested a close relationship between periodontitis and NASH (Yoneda et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

Porphyromonas gingivalis induced periodontitis exacerbates progression of non‐alcoholic steatohepatitis in rats

Kuraji

Fujita

et al. 2016

Clinical & Exp Dental Res

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Non‐alcoholic steatohepatitis (NASH) is a chronic liver disease that can develop into hepatocirrhosis and hepatic carcinoma. In recent years, epidemiological and animal studies have reported that Porphyromonas gingivalis (P. gingivalis), a known periodontopathic bacteria, is closely related to NASH. However, previous studies could not demonstrate a direct relationship between periodontitis, P. gingivalis infection, and NASH. The purpose of the present study was to examine the impact of P. gingivalis‐associated periodontitis on the onset and progression of NASH. Forty‐two male Wistar rats were used in this study. Rats were fed a high‐fat diet (HFD) for 12 weeks in order to induce fatty liver. At 4 weeks from the start of feeding, the animals were performed ligature placement around the maxillary first molar tooth in order to induce experimental periodontitis, and then a P. gingivalis slurry was applied around the ligature twice in a week for 8 weeks (HFD/Pg(+) group). Controls were given the slurry without P. gingivalis after ligature placement using the same protocol (HFD/Pg(−) group). Significant increases in alveolar bone resorption and inflammation in periodontal tissue around the molar tooth in the HFD/Pg(+) group were observed when compared with the HFD/Pg(−) group. Moreover, histological images showing NASH characterized by perivenular lipid deposition including big fatty drops, ballooning degeneration, and focal necrosis with inflammatory cells were confirmed in the liver of rats in the HFD/Pg(+) group. Significant increases in alanine aminotransaminase, aspartate aminotransferase, and C‐reactive protein levels were observed in the HFD/Pg(+) group. Furthermore, endotoxin levels in serum in the HFD/Pg(+) group were significantly higher than those in the HFD/Pg(−) group. The present study demonstrated that experimental periodontitis induced by P. gingivalis led to the progression of NASH in rats with fatty liver. Increased levels of endotoxin derived from P. gingivalis infection appear to play a considerable role in the progression of NASH.

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“…Based on this hypothesis, individuals with chronic periodontal diseases would eventually establish a disturbed gut microbiome commonly seen in individuals affected by systemic inflammatory diseases. In fact, the novel pathogenesis model of periodontitis (the ‘keystone-pathogen hypothesis’) proposes that periodontal pathogens can orchestrate inflammatory periodontal disease by remodelling a symbiotic periodontal microbiota into a dysbiotic one, as demonstrated in animal model studies [43,44]. However, no clinical studies in humans have evaluated the ability of periodontal pathogens to cause a dysbiosis in the gut microbiome.…”

Section: Introductionmentioning

confidence: 99%

Defining the gut microbiota in individuals with periodontal diseases: an exploratory study

Lourenςo

Spencer

Alm

et al. 2018

Journal of Oral Microbiology

116

109

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Background: This exploratory study aimed to characterize the gut microbiome of individuals with different periodontal conditions, and correlate it with periodontal inflammation and tissue destruction.Methods: Stool samples were obtained from individuals presenting periodontal health (PH = 7), gingivitis (G = 14) and chronic periodontitis (CP = 23). The intestinal microbiome composition was determined by Illumina MiSeq sequencing.Results: A lower alpha-diversity in the gut microbiome of individuals with CP was observed, although no significant difference among groups was found (p > 0.01). Firmicutes, Proteobacteria, Verrucomicrobia and Euryarchaeota were increased, whereas Bacteroidetes were decreased in abundance in patients with periodontitis compared to PH. Prevotella (genus), Comamonadaceae (family) and Lactobacillales (order) were detected in higher numbers in G, while Bacteroidales (order) was predominant in PH (p < 0.01). Significant correlations (rho = 0.337–0.468, p < 0.01) were found between OTUs representative of periodontal pathogens and attachment loss. Mogibacteriaceae, Ruminococcaceae and Prevotella were able to discriminate individuals with periodontal diseases from PH (overall accuracy = 84%). Oral taxa were detected in high numbers in all stool samples.Conclusions: Individuals with periodontal diseases present a less diverse gut microbiome consistent with other systemic inflammatory diseases. High numbers of oral taxa related to periodontal destruction and inflammation were detected in the gut microbiome of individuals regardless of periodontal status.

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Low-Abundance Biofilm Species Orchestrates Inflammatory Periodontal Disease through the Commensal Microbiota and Complement

Cited by 955 publications

References 50 publications

The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation

The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation

Porphyromonas gingivalis induced periodontitis exacerbates progression of non‐alcoholic steatohepatitis in rats

Defining the gut microbiota in individuals with periodontal diseases: an exploratory study

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