4.5 Review

Polymicrobial communities in periodontal disease: Their quasi-organismal nature and dialogue with the host

Journal

PERIODONTOLOGY 2000
Volume 86, Issue 1, Pages 210-230

Publisher

WILEY
DOI: 10.1111/prd.12371

Keywords

dysbiosis; inflammation; keystone pathogen; pathobiont; periodontitis; polymicrobial community

Funding

  1. NIH [DE01111, DE012505, DE017921, DE023193, GM125504, DE024153, DE024716, DE026152, DE028561, DE029436]

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In health, indigenous polymicrobial communities at mucosal surfaces maintain an ecological balance via interactions that promote their own and the host's fitness. However, destabilizing factors may disrupt this balance, leading to dysbiosis and periodontitis. Dysbiotic community is a quasi-organismal entity with constituent organisms communicating and displaying functional specialization.
In health, indigenous polymicrobial communities at mucosal surfaces maintain an ecological balance via both inter-microbial and host-microbial interactions that promote their own and the host's fitness, while preventing invasion by exogenous pathogens. However, genetic and acquired destabilizing factors (including immune deficiencies, immunoregulatory defects, smoking, diet, obesity, diabetes and other systemic diseases, and aging) may disrupt this homeostatic balance, leading to selective outgrowth of species with the potential for destructive inflammation. This process, known as dysbiosis, underlies the development of periodontitis in susceptible hosts. The pathogenic process is not linear but involves a positive-feedback loop between dysbiosis and the host inflammatory response. The dysbiotic community is essentially a quasi-organismal entity, where constituent organisms communicate via sophisticated physical and chemical signals and display functional specialization (eg, accessory pathogens, keystone pathogens, pathobionts), which enables polymicrobial synergy and dictates the community's pathogenic potential or nososymbiocity. In this review, we discuss early and recent studies in support of the polymicrobial synergy and dysbiosis model of periodontal disease pathogenesis. According to this concept, disease is not caused by individual causative pathogens but rather by reciprocally reinforced interactions between physically and metabolically integrated polymicrobial communities and a dysregulated host inflammatory response.

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