Journal of Periodontal and Implant Science

Korean Academy of Periodontology (대한치주과학회)
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Prevalence and abundance of 9 periodontal pathogens in the saliva of periodontally healthy adults and patients undergoing supportive periodontal therapy

  • Jung, Woo-Ri (Department of Periodontology, Dental and Life Science Institute, Pusan National University School of Dentistry) ;
  • Joo, Ji-Young (Department of Periodontology, Dental and Life Science Institute, Pusan National University School of Dentistry) ;
  • Lee, Ju-Youn (Department of Periodontology, Dental and Life Science Institute, Pusan National University School of Dentistry) ;
  • Kim, Hyun-Joo (Department of Periodontology, Dental and Life Science Institute, Pusan National University School of Dentistry)
  • Received : 2020.10.05
  • Accepted : 2021.03.05
  • Published : 2021.10.30
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Abstract

Purpose: This study aimed to examine the prevalence and abundance of 9 representative periodontal pathogens in the saliva samples of periodontally healthy subjects (PH) and patients with periodontitis who underwent supportive periodontal therapy (SPT). The age-specific distribution of these pathogens in periodontally healthy individuals was also analyzed. Methods: One hundred subjects (aged >35 years) were recruited (50 each in the PH and SPT groups) between August 2016 and April 2019. The prevalence and abundance of periodontal pathogens in the PH group were compared with those in periodontally healthy young subjects (94 subjects; aged <35 years), who were included in our previous study. DNA copy numbers of Aggregatibacter actinomycetemcomitans (Aa), Porphyromonas gingivalis (Pg), Tannerella forsythia (Tf), Treponema denticola (Td), Prevotella intermedia (Pi), Fusobacterium nucleatum (Fn), Campylobacter rectus (Cr), Peptostreptococcus anaerobius (Pa), and Eikenella corrodens (Ec) were analyzed using real-time polymerase chain reaction. Results: The detection frequencies of all pathogens, except Aa, were high in the PH and SPT groups. The ranking order of pathogen DNA copy numbers was similar in both groups. In both groups, Fn had the highest abundance, Aa had the lowest abundance. Additionally, Td was significantly more abundant in men than in women in both groups (P<0.05). Compared with the PH group, the SPT group exhibited significantly lower total bacteria and Fn abundance and higher Pg abundance (P<0.05). The age-specific pathogen distribution analysis revealed a significantly low Aa abundance and high Tf and Cr abundance in the PH group. Conclusions: The clinical parameters and microbial profiles were similar between the SPT and PH groups. However, patients with periodontitis require supportive care to prevent recurrence. As the abundance of some bacteria varied with age, future studies must elucidate the correlation between age-related physiological changes and periodontal bacterial composition.

Keywords

Acknowledgement

This work was supported by the Dental Research Institute (PNUDH DRI-2019-03), Pusan National University Dental Hospital (Yangsan, Korea).

References

  1. Bartold PM, Van Dyke TE. Host modulation: controlling the inflammation to control the infection. Periodontol 2000 2017;75:317-29. https://doi.org/10.1111/prd.12169
  2. Tartaglia GM, Gagliano N, Zarbin L, Tolomeo G, Sforza C. Antioxidant capacity of human saliva and periodontal screening assessment in healthy adults. Arch Oral Biol 2017;78:34-8. https://doi.org/10.1016/j.archoralbio.2017.02.003
  3. Bartold PM, Van Dyke TE. Periodontitis: a host-mediated disruption of microbial homeostasis. Unlearning learned concepts. Periodontol 2000 2013;62:203-17. https://doi.org/10.1111/j.1600-0757.2012.00450.x
  4. Darveau RP, Tanner A, Page RC. The microbial challenge in periodontitis. Periodontol 2000 1997;14:12-32. https://doi.org/10.1111/j.1600-0757.1997.tb00190.x
  5. Yoshida A, Suzuki N, Nakano Y, Oho T, Kawada M, Koga T. Development of a 5' fluorogenic nuclease-based real-time PCR assay for quantitative detection of Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. J Clin Microbiol 2003;41:863-6. https://doi.org/10.1128/JCM.41.2.863-866.2003
  6. Yun JH, Park JE, Kim DI, Lee SI, Choi SH, Cho KS, et al. Identification of putative periodontal pathogens in Korean chronic periodontitis patients. J Korean Acad Periodontol 2008;38:143-52. https://doi.org/10.5051/jkape.2008.38.2.143
  7. Umeda M, Contreras A, Chen C, Bakker I, Slots J. The utility of whole saliva to detect the oral presence of periodontopathic bacteria. J Periodontol 1998;69:828-33. https://doi.org/10.1902/jop.1998.69.7.828
  8. Paju S, Pussinen PJ, Suominen-Taipale L, Hyvonen M, Knuuttila M, Kononen E. Detection of multiple pathogenic species in saliva is associated with periodontal infection in adults. J Clin Microbiol 2009;47:235-8. https://doi.org/10.1128/JCM.01824-08
  9. Rodenburg JP, van Winkelhoff AJ, Winkel EG, Goene RJ, Abbas F, de Graff J. Occurrence of Bacteroides gingivalis, Bacteroides intermedius and Actinobacillus actinomycetemcomitans in severe periodontitis in relation to age and treatment history. J Clin Periodontol 1990;17:392-9. https://doi.org/10.1111/j.1600-051X.1990.tb00036.x
  10. Boutaga K, Savelkoul PH, Winkel EG, van Winkelhoff AJ. Comparison of subgingival bacterial sampling with oral lavage for detection and quantification of periodontal pathogens by real-time polymerase chain reaction. J Periodontol 2007;78:79-86. https://doi.org/10.1902/jop.2007.060078
  11. Sakamoto M, Takeuchi Y, Umeda M, Ishikawa I, Benno Y. Rapid detection and quantification of five periodontopathic bacteria by real-time PCR. Microbiol Immunol 2001;45:39-44. https://doi.org/10.1111/j.1348-0421.2001.tb01272.x
  12. Haffajee AD, Socransky SS. Microbial etiological agents of destructive periodontal diseases. Periodontol 2000 1994;5:78-111. https://doi.org/10.1111/j.1600-0757.1994.tb00020.x
  13. Socransky SS, Haffajee AD. Dental biofilms: difficult therapeutic targets. Periodontol 2000 2002;28:12-55. https://doi.org/10.1034/j.1600-0757.2002.280102.x
  14. Zhou X, Liu X, Li J, Aprecio RM, Zhang W, Li Y. Real-time PCR quantification of six periodontal pathogens in saliva samples from healthy young adults. Clin Oral Investig 2015;19:937-46. https://doi.org/10.1007/s00784-014-1316-0
  15. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 2005;43:5721-32. https://doi.org/10.1128/JCM.43.11.5721-5732.2005
  16. Haffajee AD, Japlit M, Bogren A, Kent RL Jr, Goodson JM, Socransky SS. Differences in the subgingival microbiota of Swedish and USA subjects who were periodontally healthy or exhibited minimal periodontal disease. J Clin Periodontol 2005;32:33-9. https://doi.org/10.1111/j.1600-051X.2004.00624.x
  17. Kanasi E, Ayilavarapu S, Jones J. The aging population: demographics and the biology of aging. Periodontol 2000 2016;72:13-8. https://doi.org/10.1111/prd.12126
  18. Feres M, Teles F, Teles R, Figueiredo LC, Faveri M. The subgingival periodontal microbiota of the aging mouth. Periodontol 2000 2016;72:30-53. https://doi.org/10.1111/prd.12136
  19. Percival RS, Challacombe SJ, Marsh PD. Age-related microbiological changes in the salivary and plaque microflora of healthy adults. J Med Microbiol 1991;35:5-11. https://doi.org/10.1099/00222615-35-1-5
  20. Preza D, Olsen I, Willumsen T, Boches SK, Cotton SL, Grinde B, et al. Microarray analysis of the microflora of root caries in elderly. Eur J Clin Microbiol Infect Dis 2009;28:509-17. https://doi.org/10.1007/s10096-008-0662-8
  21. Finoti LS, Corbi SC, Anovazzi G, Teixeira SR, Capela MV, Tanaka MH, et al. Pathogen levels and clinical response to periodontal treatment in patients with Interleukin 8 haplotypes. Pathog Dis 2013;69:21-8.
  22. Listgarten MA, Sullivan P, George C, Nitkin L, Rosenberg ES, Chilton NW, et al. Comparative longitudinal study of 2 methods of scheduling maintenance visits: 4-year data. J Clin Periodontol 1989;16:105-15. https://doi.org/10.1111/j.1600-051X.1989.tb01622.x
  23. Doungudomdacha S, Rawlinson A, Walsh TF, Douglas CW. 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;28:437-45. https://doi.org/10.1034/j.1600-051x.2001.028005437.x
  24. Choi H, Kim E, Kang J, Kim HJ, Lee JY, Choi J, et al. Real-time PCR quantification of 9 periodontal pathogens in saliva samples from periodontally healthy Korean young adults. J Periodontal Implant Sci 2018;48:261-71. https://doi.org/10.5051/jpis.2018.48.4.261
  25. Lundmark A, Hu YO, Huss M, Johannsen G, Andersson AF, Yucel-Lindberg T. Identification of salivary microbiota and its association with host inflammatory mediators in periodontitis. Front Cell Infect Microbiol 2019;9:216. https://doi.org/10.3389/fcimb.2019.00216
  26. Hyvarinen K, Laitinen S, Paju S, Hakala A, Suominen-Taipale L, Skurnik M, et al. Detection and quantification of five major periodontal pathogens by single copy gene-based real-time PCR. Innate Immun 2009;15:195-204. https://doi.org/10.1177/1753425908101920
  27. Han YW. Fusobacterium nucleatum: a commensal-turned pathogen. Curr Opin Microbiol 2015;23:141-7. https://doi.org/10.1016/j.mib.2014.11.013
  28. Zhuang LF, Watt RM, Mattheos N, Si MS, Lai HC, Lang NP. Periodontal and peri-implant microbiota in patients with healthy and inflamed periodontal and peri-implant tissues. Clin Oral Implants Res 2016;27:13-21.
  29. Signat B, Roques C, Poulet P, Duffaut D. Fusobacterium nucleatum in periodontal health and disease. Curr Issues Mol Biol 2011;13:25-36.
  30. Kim TS, Kang NW, Lee SB, Eickholz P, Pretzl B, Kim CK. Differences in subgingival microflora of Korean and German periodontal patients. Arch Oral Biol 2009;54:223-9. https://doi.org/10.1016/j.archoralbio.2008.10.005
  31. Shiau HJ, Reynolds MA. Sex differences in destructive periodontal disease: exploring the biologic basis. J Periodontol 2010;81:1505-17. https://doi.org/10.1902/jop.2010.100045
  32. Haffajee AD, Cugini MA, Tanner A, Pollack RP, Smith C, Kent RL Jr, et al. Subgingival microbiota in healthy, well-maintained elder and periodontitis subjects. J Clin Periodontol 1998;25:346-53. https://doi.org/10.1111/j.1600-051X.1998.tb02454.x
  33. Teles RP, Patel M, Socransky SS, Haffajee AD. Disease progression in periodontally healthy and maintenance subjects. J Periodontol 2008;79:784-94. https://doi.org/10.1902/jop.2008.070485
  34. Arenas Rodrigues VA, de Avila ED, Nakano V, Avila-Campos MJ. Qualitative, quantitative and genotypic evaluation of Aggregatibacter actinomycetemcomitans and Fusobacterium nucleatum isolated from individuals with different periodontal clinical conditions. Anaerobe 2018;52:50-8. https://doi.org/10.1016/j.anaerobe.2018.05.015
  35. Bourgeois D, Inquimbert C, Ottolenghi L, Carrouel F. Periodontal pathogens as risk factors of cardiovascular diseases, diabetes, rheumatoid arthritis, cancer, and chronic obstructive pulmonary disease-is there cause for consideration? Microorganisms 2019;7:424. https://doi.org/10.3390/microorganisms7100424