1887

Journal of Medical Microbiology logo

Volume 70, Issue 1

Understanding the microbial components of periodontal diseases and periodontal treatment-induced microbiological shifts Free

Abstract

In the mid-1960s the microbial aetiology of periodontal diseases was introduced based on classical experimental gingivitis studies . Since then, numerous studies have addressed the fundamental role that oral microbiota plays in the initiation and progression of periodontal diseases. Recent advances in laboratory identification techniques have contributed to a better understanding of the complexity of the oral microbiome in both health and disease. Modern culture-independent methods such as human oral microbial identification microarray and next-generation sequencing have been used to identify a wide variety of microbial taxa residing in the gingival sulcus and the periodontal pocket. The first theory of the ‘non-specific plaque’ hypothesis gave rise to the ‘ecological plaque’ hypothesis and more recently to the ‘polymicrobial synergy and dysbiosis hypothesis’. Periodontitis is now considered to be a multimicrobial inflammatory disease in which the various bacterial species within the dental biofilm are in a dysbiotic state and this imbalance favours the establishment of chronic inflammatory conditions and ultimately the destruction of tooth-supporting tissues. Apart from the known putative periodontal pathogens, the whole biofilm community is now considered to play a role in the establishment of inflammation and the initiation and progression of periodontitis in a susceptible host. Treatment is unlikely to eliminate putative pathogens but, when it is thoroughly performed it has the potential to establish a healthy ecosystem by altering the microbial community in numbers and composition and also contribute to the maturation of the host immune response.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): dysbiosis , host response , microbiome , periodontal therapy , periodontitis and putative periodontal pathogens
© 2021 The Authors
Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.001247
2020-12-09
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jmm/70/1/jmm001247.html?itemId=/content/journal/jmm/10.1099/jmm.0.001247&mimeType=html&fmt=ahah

References

  1. Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M et al. Periodontitis: consensus report of Workgroup 2 of the 2017 world workshop on the classification of periodontal and peri-implant diseases and conditions. J Clin Periodontol 2018; 45:S162–S170 [View Article]
     [Google Scholar]
  2. Eke PI, Borgnakke WS, Genco RJ. Recent epidemiologic trends in periodontitis in the USA. Periodontol 2000 2020; 82:257–267 [View Article]
     [Google Scholar]
  3. Peres MA, Macpherson LMD, Weyant RJ et al. Oral diseases: a global public health challenge [published correction appears in Lancet. 2019 Sep 21;394(10203):1010]. Lancet 2019; 394:249–260
     [Google Scholar]
  4. Kinane DF. Single-visit, full-mouth ultrasonic debridement: a paradigm shift in periodontal therapy?. J Clin Periodontol 2005; 32:732–733 [View Article]
     [Google Scholar]
  5. Graziani F, Tsakos G. Patient‐based outcomes and quality of life. Periodontol 2000 2020; 83:277–294 [View Article]
     [Google Scholar]
  6. Apatzidou DA, Kinane DF. Nonsurgical mechanical treatment strategies for periodontal disease. Dent Clin North Am 2010; 54:1–12 [View Article]
     [Google Scholar]
  7. Apatzidou DA. Modern approaches to non-surgical biofilm management. Front Oral Biol 2012; 15:99–116
     [Google Scholar]
  8. Mira A, Simon-Soro A, Curtis MA. Role of microbial communities in the pathogenesis of periodontal diseases and caries. J Clin Periodontol 2017; 44:S23–S38 [View Article]
     [Google Scholar]
  9. Sultan AS, Kong EF, Rizk AM, Jabra-Rizk MA. The oral microbiome: a lesson in coexistence. PLoS Pathog 2018; 14:e1006719 [View Article]
     [Google Scholar]
  10. Chen HA, Johnson BD, Sims TJ, Darveau RP, Monda BJ et al. Humoral Immune Responses to Porphyromonas gingivalis Before and Following Therapy in Rapidly Progressive Periodontitis Patients. J Periodontol 1991; 62:781–791 [View Article]
     [Google Scholar]
  11. Darby IB, Mooney J, Kinane DF. Changes in subgingival microflora and humoral immune response following periodontal therapy. J Clin Periodontol 2001; 28:796–805 [View Article]
     [Google Scholar]
  12. Slots J, Mashimo P, Levine MJ, Genco RJ. Periodontal therapy in humans: I. microbiological and clinical effects of a single course of periodontal scaling and root planing, and of adjunctive tetracycline therapy. J Periodontol 1979; 50:495–509 [View Article]
     [Google Scholar]
  13. Haffajee AD, Cugini MA, Dibart S, Smith C, Kent RL et al. The effect of SRP on the clinical and microbiological parameters of periodontal diseases. J Clin Periodontol 1997; 24:324–334 [View Article]
     [Google Scholar]
  14. Rosier BT, De Jager M, Zaura E, Krom BP. Historical and contemporary hypotheses on the development of oral diseases: are we there yet?. Front Cell Infect Microbiol 2014; 4:1–11 [View Article]
     [Google Scholar]
  15. Miller WD. The Micro-Organism of the Human Mouth. The Local and General Diseases Which are Caused by Them. Unaltered reprint from the original work by Miller, W.D. (1853-1907) published in 1890 in Philadelphia With an introductory essay by G.K. König (Nijmegen) Basel: Karger; 1973 pp 1–0
     [Google Scholar]
  16. Black G. The Formation of Poisons by Micro-Organisms. A Biological Study of the Germ Theory of Disease Philadelphia, PA: P. Blakiston, son &co; 1884
     [Google Scholar]
  17. Loesche WJ. Chemotherapy of dental plaque infections. Oral Sci Rev 1976; 9:65–107[PubMed]
     [Google Scholar]
  18. Loesche WJ, Nafe D. Reduction of supragingival plaque accumulations in institutionalized Down’s syndrome patients by periodic treatment with topical kanamycin. Arch Oral Biol 1973; 18:1131–1143 [View Article]
     [Google Scholar]
  19. Loesche WJ. Role of Streptococcus mutans in human dental decay. Microbiol Rev 1986; 50:353–380 [View Article]
     [Google Scholar]
  20. Theilade E. The non-specific theory in microbial etiology of inflammatory periodontal diseases. J Clin Periodontol 1986; 13:905–911 [View Article]
     [Google Scholar]
  21. Marsh PD. Microbial ecology of dental plaque and its significance in health and disease. Adv Dent Res 1994; 8:263–271 [View Article]
     [Google Scholar]
  22. Marsh PD. Are dental diseases examples of ecological catastrophes?. Microbiology 2003; 149:279–294 [View Article]
     [Google Scholar]
  23. Mason MR, Nagaraja HN, Camerlengo T, Joshi V, Kumar PS. Deep sequencing identifies ethnicity-specific bacterial signatures in the oral microbiome. PLoS One 2013; 8:e77287–7 [View Article]
     [Google Scholar]
  24. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL. Microbial complexes in subgingival plaque. J Clin Periodontol 1998; 25:134–144 [View Article]
     [Google Scholar]
  25. Socransky SS, Haffajee AD. Dental biofilms: difficult therapeutic targets. Periodontol 2000 2002; 28:12–55 [View Article]
     [Google Scholar]
  26. Meyer DH, Lippmann JE, Fives-Taylor PM. Invasion of epithelial cells by Actinobacillus actinomycetemcomitans: a dynamic, multistep process. Infect Immun 1996; 64:2988–2997 [View Article]
     [Google Scholar]
  27. Mohanty R, Asopa SJ, Joseph MD, Singh B, Rajguru JP et al. Red complex: polymicrobial conglomerate in oral flora: a review. J Fam Med Prim care 2019 Nov 15; 8:3480–3486
     [Google Scholar]
  28. Holt SC, Ebersole JL. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the ‘red complex’, a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 2005; 38:72–122 [View Article]
     [Google Scholar]
  29. Thurnheer T, Belibasakis GN, Bostanci N. Colonisation of gingival epithelia by subgingival biofilms in vitro: Role of “red complex” bacteria. Arch Oral Biol 2014; 59:977–986 [View Article]
     [Google Scholar]
  30. Bostanci N, Belibasakis GN. Porphyromonas gingivalis: an invasive and evasive opportunistic oral pathogen. FEMS Microbiol Lett 2012; 333:1–9 [View Article]
     [Google Scholar]
  31. Curtis MA, Slaney JM, Aduse-Opoku J. Critical pathways in microbial virulence. J Clin Periodontol 2005; 32:28–38 [View Article]
     [Google Scholar]
  32. Darveau RP, Hajishengallis G, Curtis MA. Porphyromonas gingivalis as a potential community activist for disease. J Dent Res 2012; 91:816–820 [View Article]
     [Google Scholar]
  33. Lamont RJ, Jenkinson HF. Subgingival colonization by Porphyromonas gingivalis . Oral Microbiol Immunol 2000; 15:341–349 [View Article]
     [Google Scholar]
  34. Takayama A, Satoh A, Ngai T, Nishimura T, Ikawa K et al. Augmentation of Actinobacillus actinomycetemcomitans invasion of human oral epithelial cells and up-regulation of interleukin-8 production by saliva CD14. Infect Immun 2003; 71:5598–5604 [View Article]
     [Google Scholar]
  35. Belibasakis GN, Kast JI, Thurnheer T, Akdis CA, Bostanci N. The expression of gingival epithelial junctions in response to subgingival biofilms. Virulence 2015; 6:704–709 [View Article]
     [Google Scholar]
  36. Bostanci N, Bao K, Wahlander A, Grossmann J, Thurnheer T et al. Secretome of gingival epithelium in response to subgingival biofilms. Mol Oral Microbiol 2015; 30:323–335 [View Article]
     [Google Scholar]
  37. Belibasakis GN, Bao K, Bostanci N. Transcriptional profiling of human gingival fibroblasts in response to multi-species in vitro subgingival biofilms. Mol Oral Microbiol 2014; 29:174–183 [View Article]
     [Google Scholar]
  38. Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN et al. Bacterial diversity in human subgingival plaque. J Bacteriol 2001; 183:3770–3783 [View Article]
     [Google Scholar]
  39. Kumar PS, Griffen AL, Barton JA, Paster BJ, Moeschberger ML et al. New bacterial species associated with chronic periodontitis. J Dent Res 2003; 82:338–344 [View Article]
     [Google Scholar]
  40. Abusleme L, Dupuy AK, Dutzan N, Silva N, Burleson JA et al. The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. Isme J 2013; 7:1016–1025 [View Article]
     [Google Scholar]
  41. Griffen AL, Beall CJ, Campbell JH, Firestone ND, Kumar PS et al. Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. Isme J 2012; 6:1176–1185 [View Article]
     [Google Scholar]
  42. Pérez-Chaparro PJ, Gonçalves C, Figueiredo LC et al. Newly identified pathogens associated with periodontitis: a systematic review. J Dent Res 2014; 93:846–858
     [Google Scholar]
  43. Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nat Rev Microbiol 2012; 10:717–725 [View Article]
     [Google Scholar]
  44. Hajishengallis G. Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends Immunol 2014; 35:3–11 [View Article]
     [Google Scholar]
  45. Lamont RJ, Hajishengallis G. Polymicrobial synergy and dysbiosis in inflammatory disease. Trends Mol Med 2015; 21:172–183 [View Article]
     [Google Scholar]
  46. Haffajee AD, Cugini MA, Tanner A, Pollack RP, Smith C et al. Subgingival microbiota in healthy, well-maintained elder and periodontitis subjects. J Clin Periodontol 1998; 25:346–353 [View Article]
     [Google Scholar]
  47. Lopez R, Hujoel P, Belibasakis GN. On putative periodontal pathogens: an epidemiological perspective. Virulence 2015; 6:249–257 [View Article]
     [Google Scholar]
  48. Hajishengallis G, Lamont RJ. Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol 2012; 27:409–419 [View Article]
     [Google Scholar]
  49. Hill DA, Artis D. Intestinal bacteria and the regulation of immune cell homeostasis. Annu Rev Immunol 2010; 28:623–667 [View Article]
     [Google Scholar]
  50. Kilian M, Chapple ILC, Hannig M, Marsh PD, Meuric V et al. The oral microbiome – an update for oral healthcare professionals. Br Dent J 2016; 221:657–666 [View Article]
     [Google Scholar]
  51. Hong B-Y, Furtado Araujo MV, Strausbaugh LD, Terzi E, Ioannidou E et al. Microbiome profiles in periodontitis in relation to host and disease characteristics. PLoS One 2015; 10:e0127077–14 [View Article]
     [Google Scholar]
  52. Aruni AW, Mishra A, Dou Y, Chioma O, Hamilton BN et al. Filifactor alocis – a new emerging periodontal pathogen. Microbes and Infection 2015; 17:517–530 [View Article]
     [Google Scholar]
  53. Diaz PI, Hoare A, Hong B-Y. Subgingival microbiome shifts and community dynamics in periodontal diseases. J Calif Dent Assoc 2016; 44:421–435
     [Google Scholar]
  54. Camelo-Castillo AJ, Mira A, Pico A, Nibali L, Henderson B et al. Subgingival microbiota in health compared to periodontitis and the influence of smoking. Front Microbiol 2015; 6:119 [View Article]
     [Google Scholar]
  55. Tsai C-Y, Tang CY, Tan T-S, Chen K-H, Liao K-H et al. Subgingival microbiota in individuals with severe chronic periodontitis. J Microbiol Immunol Infect 2018; 51:226–234 [View Article]
     [Google Scholar]
  56. Meuric V, Le Gall-David S, Boyer E, Acuña-Amador L, Martin B et al. Signature of microbial dysbiosis in periodontitis. Appl Environ Microbiol 2017; 83: [View Article]
     [Google Scholar]
  57. Cobb CM. Non-Surgical pocket therapy: mechanical. Ann Periodontol 1996; 1:443–490 [View Article]
     [Google Scholar]
  58. Lavanchy DL, Bickel M, Baehni PC. The effect of plaque control after scaling and root planing on the subgingival microflora in human periodontitis. J Clin Periodontol 1987; 14:295–299 [View Article]
     [Google Scholar]
  59. Sonnenschein SK, Kohnen R, Ruetters M, Krisam J, Kim T-S, Kim Ti‐Sun. Adherence to long-term supportive periodontal therapy in groups with different periodontal risk profiles. J Clin Periodontol 2020; 47:351–361 [View Article][PubMed]
     [Google Scholar]
  60. Apatzidou DA, Zygogianni P, Sakellari D, Konstantinidis A. Oral hygiene reinforcement in the simplified periodontal treatment of 1 hour. J Clin Periodontol 2014; 41:149–156 [View Article]
     [Google Scholar]
  61. van Winkelhof AJ, Velden U, Graaff J. Microbial succession in recolonizing deep periodontal pockets after a single course of supra- and subgingival debridement. J Clin Periodontol 1988; 15:116–122 [View Article]
     [Google Scholar]
  62. Singletary MM, Crawford JJ, Simpson DM. Dark-Field microscopic monitoring of subgingival bacteria during periodontal therapy. J Periodontol 1982; 53:671–681 [View Article]
     [Google Scholar]
  63. Listgarten MA, Helldén L. Relative distribution of bacteria at clinically healthy and periodontally diseased sites in humans. J Clin Periodontol 1978; 5:115–132 [View Article]
     [Google Scholar]
  64. Socransky SS, Haffajee AD. Periodontal microbial ecology. Periodontol 2000 2005; 38:135–187 [View Article]
     [Google Scholar]
  65. Listgarten MA. Structure of the microbial flora associated with periodontal health and disease in man: a light and electron microscopic study. J Periodontol 1976; 47:1–18 [View Article]
     [Google Scholar]
  66. Loos B, Claffey N, Egelberg J. Clinical and microbiological effects of root debridement in periodontal furcation pockets. J Clin Periodontol 1988; 15:453–463 [View Article]
     [Google Scholar]
  67. Hinrichs JE, Wolff LF, Pihlstrom BL, Schaffer EM, Liljemark WF et al. Effects of scaling and root planing on subgingival microbial proportions standardized in terms of their naturally occurring distribution. J Periodontol 1985; 56:187–194 [View Article]
     [Google Scholar]
  68. Mousquès T, Listgarten MA, Phillips RW. Effect of scaling and root planing on the composition of the human subgingival microbial flora. J Periodontal Res 1980; 15:144–151 [View Article]
     [Google Scholar]
  69. Müller HP, Hartmann J, Flores-de-Jacoby L. Clinical alterations in relation to the morphological composition of the subgingival microflora following scaling and root planing. J Clin Periodontol 1986; 13:825–832 [View Article][PubMed]
     [Google Scholar]
  70. Moore WEC, Moore LVH. The bacteria of periodontal diseases. Periodontol 1994; 5:66–77 [View Article]
     [Google Scholar]
  71. Moore WE, Holdeman LV, Cato EP, Smibert RM, Burmeister JA et al. Bacteriology of moderate (chronic) periodontitis in mature adult humans. Infect Immun 1983; 42:510–515 [View Article]
     [Google Scholar]
  72. Teles RP, Haffajee AD, Socransky SS. Microbiological goals of periodontal therapy. Periodontology 2006; 42:180–218 [View Article][PubMed]
     [Google Scholar]
  73. Renvert S, Wikström M, Dahlén G, Slots J, Egelberg J. Effect of root debridement on the elimination of Actinobacillus actinomycetemcomitans and Bacteroides gingivalis from periodontal pockets. J Clin Periodontol 1990; 17:345–350 [View Article]
     [Google Scholar]
  74. Pedrazzoli V, Kilian M, Karring T, Kirkegaard E. Effect of surgical and non-surgical periodontal treatment on periodontal status and subgingival microbiota. J Clin Periodontol.
     [Google Scholar]
  75. van Oosten MAC, Mikx FHM, Renggli HH. Microbial and clinical measurements of periodontal pockets during sequential periods of non-treatment, mechanical debridement and metronidazole therapy. J Clin Periodontol 1987; 14:197–204 [View Article]
     [Google Scholar]
  76. Sato K, Yoneyama T, Okamoto H, Dahlén G, Lindhe J. The effect of subgingival debridement on periodontal disease parameters and the subgingival microbiota. J Clin Periodontol 1993; 20:359–365 [View Article][PubMed]
     [Google Scholar]
  77. Ali RW, Lie T, Skaug N. Early effects of periodontal therapy on the detection frequency of four putative periodontal pathogens in adults. J Periodontol 1992; 63:540–547 [View Article]
     [Google Scholar]
  78. Magnusson I, Lindhe J, Yoneyama T, Liljenberg B. Recolonization of a subgingival microbiota following scaling in deep pockets. J Clin Periodontol 1984; 11:193–207 [View Article]
     [Google Scholar]
  79. Papapanou PN, Madianos PN, Dahlén G, Sandros J. “Checkerboard” versus culture: a comparison between two methods for identification of subgingival microbiota. Eur J Oral Sci 1997; 105:389–396 [View Article]
     [Google Scholar]
  80. Riggio MP, Macfarlane TW, Mackenzie D, Lennon A, Smith AJ et al. Comparison of polymerase chain reaction and culture methods for detection of Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in subgingival plaque samples. J Periodontal Res 1996; 31:496–501 [View Article]
     [Google Scholar]
  81. Ashimoto A, Flynn MJ, Slots J. Molecular genetic detection of Bacteroides heparinolyticus in adult periodontitis. Oral Microbiol Immunol 1995; 10:284–287 [View Article]
     [Google Scholar]
  82. Doungudomdacha S, Rawlinson A, Walsh TF, Douglas CWI. Effect of non-surgical periodontal treatment on clinical parameters and the numbers of Porphyromonas gingivalis, Prevotella intermedia and Actinobacillus actinomycetemcomitans at adult periodontitis sites. J Clin Periodontol 2001; 28:437–445 [View Article]
     [Google Scholar]
  83. Paster BJ, Dewhirst FE. Molecular microbial diagnosis. Periodontol 2009; 51:38–44 [View Article]
     [Google Scholar]
  84. Garcia L, Jc T, Legido B, Ja R, Alemany J et al. Rapid detection of Actinobacillus Porphyromona gingivalis by multiplex PCR. J Periodontal Res 1998; 33:59–64
     [Google Scholar]
  85. Apatzidou DA, Kinane DF. Quadrant root planing versus same-day full-mouth root planing. III. dynamics of the immune response. J Clin Periodontol 2004; 31:152–159 [View Article]
     [Google Scholar]
  86. Colombo APV, Teles RP, Torres MC, Rosalém W, Mendes MCS et al. Effects of non-surgical mechanical therapy on the subgingival microbiota of Brazilians with untreated chronic periodontitis: 9-month results. J Periodontol 2005; 76:778–784 [View Article]
     [Google Scholar]
  87. Kolenbrander PE, Egland PG, Diaz PI, Palmer RJ. Genome–genome interactions: bacterial communities in initial dental plaque. Trends Microbiol 2005; 13:11–15 [View Article]
     [Google Scholar]
  88. Socransky SS, Smith C, Martin L, Paster BJ, Dewhirst FE et al. "Checkerboard" DNA-DNA hybridization. Biotechniques 1994; 17:788–792[PubMed]
     [Google Scholar]
  89. Socransky SS, Haffajee AD, Smith C, Martin L, Haffajee JA et al. Use of checkerboard DNA-DNA hybridization to study complex microbial ecosystems. Oral Microbiol Immunol 2004; 19:352–362 [View Article]
     [Google Scholar]
  90. Teles R, Teles F, Frias-Lopez J, Paster B, Haffajee A. Lessons learned and unlearned in periodontal microbiology. Periodontol 2013; 62:95–162 [View Article]
     [Google Scholar]
  91. Shiloah J, Patters MR. Dna probe analyses of the survival of selected periodontal pathogens following scaling, root planing, and Intra-Pocket irrigation. J Periodontol 1994; 65:568–575 [View Article]
     [Google Scholar]
  92. Cugini MA, Haffajee AD, Smith C, Kent RL, Socransky SS. The effect of scaling and root planing on the clinical and microbiological parameters of periodontal diseases: 12-month results. J Clin Periodontol 2000; 27:30–36 [View Article]
     [Google Scholar]
  93. Haffajee AD, Teles RP, Socransky SS. The effect of periodontal therapy on the composition of the subgingival microbiota. Periodontol 2000 2006; 42:219–258 [View Article][PubMed]
     [Google Scholar]
  94. Aas JA, Barbuto SM, Alpagot T, Olsen I, Dewhirst FE et al. Subgingival plaque microbiota in HIV positive patients. J Clin Periodontol 2007; 34:189–195 [View Article]
     [Google Scholar]
  95. Colombo APV, Bennet S, Cotton SL, Goodson JM, Kent R et al. Impact of periodontal therapy on the subgingival microbiota of severe periodontitis: comparison between good responders and individuals with refractory periodontitis using the human oral microbe identification microarray. J Periodontol 2012; 83:1279–1287 [View Article]
     [Google Scholar]
  96. Kumar PS, Leys EJ, Bryk JM, Martinez FJ, Moeschberger ML et al. Changes in periodontal health status are associated with bacterial community shifts as assessed by quantitative 16S cloning and sequencing. J Clin Microbiol 2006; 44:3665–3673 [View Article]
     [Google Scholar]
  97. Levy SE, Myers RM. Advancements in next-generation sequencing. Annu Rev Genomics Hum Genet 2016; 17:95–115 [View Article]
     [Google Scholar]
  98. Benn AML, Heng NCK, Broadbent JM, Thomson WM. Studying the human oral microbiome: challenges and the evolution of solutions. Aust Dent J 2018; 63:14–24 [View Article]
     [Google Scholar]
  99. Belstrøm D, Grande MA, Sembler-Møller ML, Kirkby N, Cotton SL et al. Influence of periodontal treatment on subgingival and salivary microbiotas. J Periodontol 2018; 89:531–539 [View Article]
     [Google Scholar]
  100. Shi B, Chang M, Martin J, Mitreva M, Lux R et al. Dynamic changes in the subgingival microbiome and their potential for diagnosis and prognosis of periodontitis. MBio 2015; 6:1–11 [View Article]
     [Google Scholar]
  101. Kageyama S, Takeshita T, Asakawa M, Shibata Y, Takeuchi K et al. Relative abundance of total subgingival plaque-specific bacteria in salivary microbiota reflects the overall periodontal condition in patients with periodontitis. PLoS One 2017; 12:e0174782 [View Article]
     [Google Scholar]
  102. Greenwood D, Afacan B, Emingil G, Bostanci N, Belibasakis GN. Salivary microbiome shifts in response to periodontal treatment outcome. Proteomics Clin Appl 2020; 14:e2000011 [View Article]
     [Google Scholar]
  103. Lu H, He L, Xu J et al. Well-maintained patients with a history of periodontitis still harbor a more disbiotic microbiome than health [published online ahead of print, 2020 Jun 3]. J Periodontol 2020
     [Google Scholar]
  104. Socransky SS, Haffajee AD, Teles R, Wennstrom JL, Lindhe J et al. Effect of periodontal therapy on the subgingival microbiota over a 2-year monitoring period. I. overall effect and kinetics of change. J Clin Periodontol 2013; 40:771–780 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.001247
Loading
Understanding the microbial components of periodontal diseases and periodontal treatment-induced microbiological shifts
J. Med. Microbiol. 70, 001247 (2021); https://doi.org/10.1099/jmm.0.001247
/content/journal/jmm/10.1099/jmm.0.001247
/content/journal/jmm/10.1099/jmm.0.001247
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error