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      An appraisal of the role of specific bacteria in the initial pathogenesis of periodontitis

      1 , 2
      Journal of Clinical Periodontology
      Wiley

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          Abstract

          Historically, inflammatory periodontal diseases (gingivitis and periodontitis) have been recognized as being primarily of bacterial origin. Bacteria are necessary for disease development, but the presence of specific bacteria does not guarantee progression to periodontitis. Periodontitis is a multifactorial disease; specific bacteria are associated with disease, but may not be the target of treatment. Gingivitis and periodontitis are inflammatory conditions associated with bacterial overgrowth. To analyse evidence for established thought that specific bacteria directly participate in the pathogenesis of periodontitis and question the long-held tenet that penetration of the periodontal connective tissues by bacteria and their products is a significant phase in the initial development of periodontitis. The literature was searched for studies on initiation of gingivitis and periodontitis by specific pathogens. The search results were insufficient for a systematic review and have been summarized in a commentary instead. There is very little evidence in the literature to support the commonly held concept that specific bacteria initiate periodontitis. We present evidence for a paradigm supporting the central role of inflammation, rather than specific microbiota, in the early pathogenesis of periodontitis, and discuss whether controlling the inflammation can influence the character and composition of the periodontal infection.

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          Most cited references32

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          Oral multispecies biofilm development and the key role of cell-cell distance.

          Growth of oral bacteria in situ requires adhesion to a surface because the constant flow of host secretions thwarts the ability of planktonic cells to grow before they are swallowed. Therefore, oral bacteria evolved to form biofilms on hard tooth surfaces and on soft epithelial tissues, which often contain multiple bacterial species. Because these biofilms are easy to study, they have become the paradigm of multispecies biofilms. In this Review we describe the factors involved in the formation of these biofilms, including the initial adherence to the oral tissues and teeth, cooperation between bacterial species in the biofilm, signalling between the bacteria and its role in pathogenesis, and the transfer of DNA between bacteria. In all these aspects distance between cells of different species is integral for oral biofilm growth.
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            Microbial ecology of dental plaque and its significance in health and disease.

            P.D. Marsh (1994)
            Dental plaque forms naturally on teeth and is of benefit to the host by helping to prevent colonization by exogenous species. The bacterial composition of plaque remains relatively stable despite regular exposure to minor environmental perturbations. This stability (microbial homeostasis) is due in part to a dynamic balance of both synergistic and antagonistic microbial interactions. However, homeostasis can break down, leading to shifts in the balance of the microflora, thereby predisposing sites to disease. For example, the frequent exposure of plaque to low pH leads to inhibition of acid-sensitive species and the selection of organisms with an aciduric physiology, such as mutans streptococci and lactobacilli. Similarly, plaque accumulation around the gingival margin leads to an inflammatory host response and an increased flow of gingival crevicular fluid. The subgingival microflora shifts from being mainly Gram-positive to being comprised of increased levels of obligately anaerobic, asaccharolytic Gram-negative organisms. It is proposed that disease can be prevented or treated not only by targeting the putative pathogens but also by interfering with the processes that drive the breakdown in homeostasis. Thus, the rate of acid production following sugar intake could be reduced by fluoride, alternative sweeteners, and low concentrations of antimicrobial agents, while oxygenating or redox agents could raise the Eh of periodontal pockets and prevent the growth and metabolism of obligately anaerobic species. These views have been incorporated into a modified hypothesis (the "ecological plaque hypothesis") to explain the relationship between the plaque microflora and the host in health and disease, and to identify new strategies for disease prevention.
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              Polymicrobial synergy and dysbiosis in inflammatory disease.

              Uncontrolled inflammation of the periodontal area may arise when complex microbial communities transition from a commensal to a pathogenic entity. Communication among constituent species leads to polymicrobial synergy between metabolically compatible organisms that acquire functional specialization within the developing community. Keystone pathogens, even at low abundance, elevate community virulence, and the resulting dysbiotic community targets specific aspects of host immunity to further disable immune surveillance while promoting an overall inflammatory response. Inflammophilic organisms benefit from proteinaceous substrates derived from inflammatory tissue breakdown. Inflammation and dysbiosis reinforce each other, and the escalating environmental changes further select for a pathobiotic community. We have synthesized the polymicrobial synergy and dysbiotic components of the process into a new model for inflammatory diseases.
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                Author and article information

                Contributors
                (View ORCID Profile)
                Journal
                Journal of Clinical Periodontology
                J Clin Periodontol
                Wiley
                03036979
                January 2019
                January 2019
                January 20 2019
                : 46
                : 1
                : 6-11
                Affiliations
                [1 ]School of Dentistry; University of Adelaide; Adelaide South Australia Australia
                [2 ]Forsyth Institute; Cambridge Massachusetts
                Article
                10.1111/jcpe.13046
                6357965
                30556922
                3c9af259-e277-4c07-b77f-684add02936f
                © 2019

                http://doi.wiley.com/10.1002/tdm_license_1.1

                http://onlinelibrary.wiley.com/termsAndConditions#vor

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