Journal of Periodontal and Implant Science

  • 제53권1호
  • /
  • Pages.69-84
  • /
  • 2023
  • /
  • 2093-2278(pISSN)
  • /
  • 2093-2286(eISSN)
대한치주과학회 (Korean Academy of Periodontology)
권호 표지
DOI QR코드

DOI QR Code

Microbial profiling of peri-implantitis compared to the periodontal microbiota in health and disease using 16S rRNA sequencing

  • Hyun-Joo Kim (Department of Periodontology, Dental and Life Science Institute, Pusan National University School of Dentistry) ;
  • Dae-Hee Ahn (Department of Periodontology, Dental and Life Science Institute, Pusan National University School of Dentistry) ;
  • Yeuni Yu (Biomedical Research Institute, Pusan National University School of Medicine) ;
  • Hyejung Han (Department of Oral Microbiology, Pusan National University School of Dentistry) ;
  • Si Yeong Kim (Department of Oral Microbiology, Pusan National University School of Dentistry) ;
  • Ji-Young Joo (Department of Periodontology, Dental and Life Science Institute, Pusan National University School of Dentistry) ;
  • Jin Chung (Department of Oral Microbiology, Pusan National University School of Dentistry) ;
  • Hee Sam Na (Department of Oral Microbiology, Pusan National University School of Dentistry) ;
  • Ju-Youn Lee (Department of Periodontology, Dental and Life Science Institute, Pusan National University School of Dentistry)
  • 투고 : 2022.03.21
  • 심사 : 2022.07.05
  • 발행 : 2023.02.28
PDF 다운로드
⟨ 이전 논문 다음 논문 ⟩

초록

Purpose: The objective of this study was to analyze the microbial profile of individuals with peri-implantitis (PI) compared to those of periodontally healthy (PH) subjects and periodontitis (PT) subjects using Illumina sequencing. Methods: Buccal, supragingival, and subgingival plaque samples were collected from 109 subjects (PH: 30, PT: 49, and PI: 30). The V3-V4 region of 16S rRNA was sequenced and analyzed to profile the plaque microbiota. Results: Microbial community diversity in the PI group was higher than in the other groups, and the 3 groups showed significantly separated clusters in the buccal samples. The PI group showed different patterns of relative abundance from those in the PH and PT groups depending on the sampling site at both genus and phylum levels. In all samples, some bacterial species presented considerably higher relative abundances in the PI group than in the PH and PT groups, including Anaerotignum lactatifermentans, Bacteroides vulgatus, Faecalibacterium prausnitzii, Olsenella uli, Parasutterella excrementihominis, Prevotella buccae, Pseudoramibacter alactolyticus, Treponema parvum, and Slackia exigua. Network analysis identified that several well-known periodontal pathogens and newly recognized bacteria were closely correlated with each other. Conclusions: The composition of the microbiota was considerably different in PI subjects compared to PH and PT subjects, and these results could shed light on the mechanisms involved in the development of PI.

키워드

과제정보

This research was supported by the National Research Foundation of Korea (NRF) funded by the Ministry of Science & ICT (MEST; NRF-2017M3A9B6062021 and NRF2017M3A9B6062026).

참고문헌

  1. Hasegawa T, Kawabata S, Takeda D, Iwata E, Saito I, Arimoto S, et al. Survival of Branemark System Mk III implants and analysis of risk factors associated with implant failure. Int J Oral Maxillofac Implants 2017;46:267-73.  https://doi.org/10.1016/j.ijom.2016.10.014
  2. Derks J, Schaller D, Hakansson J, Wennstrom JL, Tomasi C, Berglundh T. Effectiveness of implant therapy analyzed in a Swedish population: prevalence of peri-implantitis. J Dent Res 2016;95:43-9.  https://doi.org/10.1177/0022034515608832
  3. Renvert S, Persson GR, Pirih FQ, Camargo PM. Peri-implant health, peri-implant mucositis, and periimplantitis: case definitions and diagnostic considerations. J Clin Periodontol 2018;45 Suppl 20:S278-85.  https://doi.org/10.1111/jcpe.12956
  4. Berglundh T, Armitage G, Araujo MG, Avila-Ortiz G, Blanco J, Camargo PM, et al. Peri-implant diseases and conditions: consensus report of workgroup 4 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol 2018;89 Suppl 1:S313-8.  https://doi.org/10.1002/JPER.17-0739
  5. Esposito M, Hirsch JM, Lekholm U, Thomsen P. Biological factors contributing to failures of osseointegrated oral implants. (II). Etiopathogenesis. Eur J Oral Sci 1998;106:721-64.  https://doi.org/10.1046/j.0909-8836..t01-6-.x
  6. Page RC, Kornman KS. The pathogenesis of human periodontitis: an introduction. Periodontol 2000 1997;14:9-11.  https://doi.org/10.1111/j.1600-0757.1997.tb00189.x
  7. Charalampakis G, Leonhardt A, Rabe P, Dahlen G. Clinical and microbiological characteristics of periimplantitis cases: a retrospective multicentre study. Clin Oral Implants Res 2012;23:1045-54.  https://doi.org/10.1111/j.1600-0501.2011.02258.x
  8. Belibasakis GN, Charalampakis G, Bostanci N, Stadlinger B. Peri-implant infections of oral biofilm etiology. Adv Exp Med Biol 2015;830:69-84.  https://doi.org/10.1007/978-3-319-11038-7_4
  9. Carcuac O, Berglundh T. Composition of human peri-implantitis and periodontitis lesions. J Dent Res 2014;93:1083-8.  https://doi.org/10.1177/0022034514551754
  10. Shibli JA, Melo L, Ferrari DS, Figueiredo LC, Faveri M, Feres M. Composition of supra- and subgingival biofilm of subjects with healthy and diseased implants. Clin Oral Implants Res 2008;19:975-82.  https://doi.org/10.1111/j.1600-0501.2008.01566.x
  11. Socransky SS, Haffajee AD. Periodontal microbial ecology. Periodontol 2000 2005;38:135-87.  https://doi.org/10.1111/j.1600-0757.2005.00107.x
  12. Botero JE, Gonzalez AM, Mercado RA, Olave G, Contreras A. Subgingival microbiota in peri-implant mucosa lesions and adjacent teeth in partially edentulous patients. J Periodontol 2005;76:1490-5.  https://doi.org/10.1902/jop.2005.76.9.1490
  13. Frey KG, Herrera-Galeano JE, Redden CL, Luu TV, Servetas SL, Mateczun AJ, et al. Comparison of three next-generation sequencing platforms for metagenomic sequencing and identification of pathogens in blood. BMC Genomics 2014;15:96. 
  14. Wei Y, Shi M, Zhen M, Wang C, Hu W, Nie Y, et al. Comparison of subgingival and buccal mucosa microbiome in chronic and aggressive periodontitis: a pilot study. Front Cell Infect Microbiol 2019;9:53. 
  15. Nakagaki T, Tamura M, Kobashi K, Omori A, Koyama R, Idogawa M, et al. Targeted next-generation sequencing of 50 cancer-related genes in Japanese patients with oral squamous cell carcinoma. Tumour Biol 2018;40:1010428318800180. 
  16. Sembler-Moller ML, Belstrom D, Locht H, Enevold C, Pedersen AM. Next-generation sequencing of whole saliva from patients with primary Sjogren's syndrome and non-Sjogren's sicca reveals comparable salivary microbiota. J Oral Microbiol 2019;11:1660566. 
  17. Caton JG, Armitage G, Berglundh T, Chapple IL, Jepsen S, Kornman KS, et al. A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification. J Periodontol 2018;89 Suppl 1:S1-8. https://doi.org/10.1002/JPER.18-0157
  18. Duarte PM, de Mendonca AC, Maximo MB, Santos VR, Bastos MF, Nociti FH Jr. Effect of anti-infective mechanical therapy on clinical parameters and cytokine levels in human peri-implant diseases. J Periodontol 2009;80:234-43.  https://doi.org/10.1902/jop.2009.070672
  19. Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol 2019;37:852-7.  https://doi.org/10.1038/s41587-019-0209-9
  20. Chen T, Yu WH, Izard J, Baranova OV, Lakshmanan A, Dewhirst FE. The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database (Oxford) 2010;2010:baq013. 
  21. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol 2001;26:32-46.  https://doi.org/10.1046/j.1442-9993.2001.01070.x
  22. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, et al. Metagenomic biomarker discovery and explanation. Genome Biol 2011;12:R60. 
  23. Friedman J, Alm EJ. Inferring correlation networks from genomic survey data. PLOS Comput Biol 2012;8:e1002687. 
  24. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 2003;13:2498-504.  https://doi.org/10.1101/gr.1239303
  25. Hajishengallis G. Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends Immunol 2014;35:3-11.  https://doi.org/10.1016/j.it.2013.09.001
  26. Leonhardt A, Dahlen G, Renvert S. Five-year clinical, microbiological, and radiological outcome following treatment of peri-implantitis in man. J Periodontol 2003;74:1415-22.  https://doi.org/10.1902/jop.2003.74.10.1415
  27. Yu XL, Chan Y, Zhuang L, Lai HC, Lang NP, Keung Leung W, et al. Intra-oral single-site comparisons of periodontal and peri-implant microbiota in health and disease. Clin Oral Implants Res 2019;30:760-76.  https://doi.org/10.1111/clr.13459
  28. Maruyama N, Maruyama F, Takeuchi Y, Aikawa C, Izumi Y, Nakagawa I. Intraindividual variation in core microbiota in peri-implantitis and periodontitis. Sci Rep 2014;4:6602. 
  29. Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nat Rev Microbiol 2012;10:717-25.  https://doi.org/10.1038/nrmicro2873
  30. Na HS, Kim SY, Han H, Kim HJ, Lee JY, Lee JH, et al. Identification of potential oral microbial biomarkers for the diagnosis of periodontitis. J Clin Med 2020;9:1549. 
  31. Koyanagi T, Sakamoto M, Takeuchi Y, Maruyama N, Ohkuma M, Izumi Y. Comprehensive microbiological findings in peri-implantitis and periodontitis. J Clin Periodontol 2013;40:218-26.  https://doi.org/10.1111/jcpe.12047
  32. Neilands J, Wickstrom C, Kinnby B, Davies JR, Hall J, Friberg B, et al. Bacterial profiles and proteolytic activity in peri-implantitis versus healthy sites. Anaerobe 2015;35:28-34.  https://doi.org/10.1016/j.anaerobe.2015.04.004
  33. Zheng H, Xu L, Wang Z, Li L, Zhang J, Zhang Q, et al. Subgingival microbiome in patients with healthy and ailing dental implants. Sci Rep 2015;5:10948. 
  34. Rocas IN, Alves FR, Santos AL, Rosado AS, Siqueira JF Jr. Apical root canal microbiota as determined by reverse-capture checkerboard analysis of cryogenically ground root samples from teeth with apical periodontitis. J Endod 2010;36:1617-21.  https://doi.org/10.1016/j.joen.2010.07.001
  35. Ma N, Yang D, Okamura H, Teramachi J, Hasegawa T, Qiu L, et al. Involvement of interleukin-23 induced by Porphyromonas endodontalis lipopolysaccharide in osteoclastogenesis. Mol Med Rep 2017;15:559-66.  https://doi.org/10.3892/mmr.2016.6041
  36. Abusleme L, Dupuy AK, Dutzan N, Silva N, Burleson JA, Strausbaugh LD, et al. The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J 2013;7:1016-25. https://doi.org/10.1038/ismej.2012.174
  37. Mombelli A, Decaillet F. The characteristics of biofilms in peri-implant disease. J Clin Periodontol 2011;38 Suppl 11:203-13.  https://doi.org/10.1111/j.1600-051X.2010.01666.x
  38. Kim KS, Rowlinson MC, Bennion R, Liu C, Talan D, Summanen P, et al. Characterization of Slackia exigua isolated from human wound infections, including abscesses of intestinal origin. J Clin Microbiol 2010;48:1070-5.  https://doi.org/10.1128/JCM.01576-09
  39. Irani S. Orofacial bacterial infectious diseases: an update. J Int Soc Prev Community Dent 2017;7:S61-7.  https://doi.org/10.4103/jispcd.JISPCD_290_17
  40. Pokrowiecki R, Mielczarek A, Zareba T, Tyski S. Oral microbiome and peri-implant diseases: where are we now? Ther Clin Risk Manag 2017;13:1529-42. https://doi.org/10.2147/TCRM.S139795