1887

Abstract

Micro-organisms are important triggers of peri-implant inflammation and analysing their diversity is necessary for peri-implantitis treatment. This study aimed to analyse and compare the microbiota associated with individuals with peri-implantitis, as well as clinically healthy implant sites.

Subgingival biofilm samples were taken from 10 individuals with peri-implantitis and from at least 1 clinically healthy implant. DNA was extracted and bacterial 16S rRNA genes were amplified using universal primers. After cloning the PCR-products, amplified inserts of positive clones were digested using restriction endonucleases, and the chosen clones were sequenced. The 16S rDNA-sequences were compared to those from the public sequence databases GenBank, EMBL and DDBJ to determine the corresponding taxa.

Differing distributions of taxa belonging to the phyla , , , , , , and TM 7 were detected in both the healthy implant (HI) and the peri-implantitis (PI) groups. A significantly higher relative abundance of phylum , as well as of the species were found in the PI group (<0.05). The putative periodontal red complex () was also detected at significantly higher levels in the PI group (<0.05), whereas the yellow group, as well as the species tended to be associated with the HI group.

A shift in the healthy subgingival microbiota was shown in peri-implantitis-associated biofilm. Anaerobic Gram-negative periopathogens, including and , seem to play an important role in peri-implantitis development and should be considered in treatment and prevention strategies.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000682
2018-03-01
2020-01-22
Loading full text...

Full text loading...

/deliver/fulltext/jmm/67/3/332.html?itemId=/content/journal/jmm/10.1099/jmm.0.000682&mimeType=html&fmt=ahah

References

  1. Benic GI, Mir-Mari J, Hämmerle CH. Loading protocols for single-implant crowns: a systematic review and meta-analysis. Int J Oral Maxillofac Implants 2014;29:222–238 [CrossRef][PubMed]
    [Google Scholar]
  2. Chen ST, Buser D. Esthetic outcomes following immediate and early implant placement in the anterior maxilla–a systematic review. Int J Oral Maxillofac Implants 2014;29:186–215 [CrossRef][PubMed]
    [Google Scholar]
  3. Derks J, Håkansson J, Wennström JL, Tomasi C, Larsson M et al. Effectiveness of implant therapy analyzed in a Swedish population: early and late implant loss. J Dent Res 2015;94:44s–51 [CrossRef][PubMed]
    [Google Scholar]
  4. Belibasakis GN. Microbiological and immuno-pathological aspects of peri-implant diseases. Arch Oral Biol 2014;59:66–72 [CrossRef][PubMed]
    [Google Scholar]
  5. Mombelli A, Lang NP. The diagnosis and treatment of peri-implantitis. Periodontol 2000 1998;17:63–76 [CrossRef][PubMed]
    [Google Scholar]
  6. Renvert S, Quirynen M. Risk indicators for peri-implantitis. a narrative review. Clin Oral Implants Res 2015;26:15–44 [CrossRef][PubMed]
    [Google Scholar]
  7. Levignac J. Periimplantation osteolysis- periimplantosis - periimplantitis. Rev Fr Odontostomatol 1965;12:1251–1260[PubMed]
    [Google Scholar]
  8. Albrektsson T, Canullo L, Cochran D, de Bruyn H. "Peri-Implantitis": a complication of a foreign body or a man-made "disease". Facts and fiction. Clin Implant Dent Relat Res 2016;18:840–849 [CrossRef][PubMed]
    [Google Scholar]
  9. Padial-Molina M, López-Martínez J, O'Valle F, Galindo-Moreno P. Microbial profiles and detection techniques in peri-implant diseases: a systematic review. J Oral Maxillofac Res 2016;7:e10 [CrossRef][PubMed]
    [Google Scholar]
  10. Faveri M, Figueiredo LC, Shibli JA, Pérez-Chaparro PJ, Feres M. Microbiological diversity of peri-implantitis biofilms. Adv Exp Med Biol 2015;830:85–96 [CrossRef][PubMed]
    [Google Scholar]
  11. Maruyama N, Maruyama F, Takeuchi Y, Aikawa C, Izumi Y et al. Intraindividual variation in core microbiota in peri-implantitis and periodontitis. Sci Rep 2014;4:6602 [CrossRef][PubMed]
    [Google Scholar]
  12. Koyanagi T, Sakamoto M, Takeuchi Y, Ohkuma M, Izumi Y. Analysis of microbiota associated with peri-implantitis using 16S rRNA gene clone library. J Oral Microbiol 2010;2:5104 [CrossRef][PubMed]
    [Google Scholar]
  13. Koyanagi T, Sakamoto M, Takeuchi Y, Maruyama N, Ohkuma M et al. Comprehensive microbiological findings in peri-implantitis and periodontitis. J Clin Periodontol 2013;40:218–226 [CrossRef][PubMed]
    [Google Scholar]
  14. Belibasakis GN, Charalampakis G, Bostanci N, Stadlinger B. Peri-implant infections of oral biofilm etiology. Adv Exp Med Biol 2015;830:69–84 [CrossRef][PubMed]
    [Google Scholar]
  15. Syed SA, Loesche WJ. Survival of human dental plaque flora in various transport media. Appl Microbiol 1972;24:638–644[PubMed]
    [Google Scholar]
  16. Anderson AC, Hellwig E, Vespermann R, Wittmer A, Schmid M et al. Comprehensive analysis of secondary dental root canal infections: a combination of culture and culture-independent approaches reveals new insights. PLoS One 2012;7:e49576 [CrossRef][PubMed]
    [Google Scholar]
  17. Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA et al. Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Appl Environ Microbiol 2008;74:2461–2470 [CrossRef][PubMed]
    [Google Scholar]
  18. Hall T. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 1999;41:95–98
    [Google Scholar]
  19. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol 1990;215:403–410 [CrossRef][PubMed]
    [Google Scholar]
  20. Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z et al. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997;25:3389–3402 [CrossRef][PubMed]
    [Google Scholar]
  21. Ashelford KE, Chuzhanova NA, Fry JC, Jones AJ, Weightman AJ. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl Environ Microbiol 2005;71:7724–7736 [CrossRef][PubMed]
    [Google Scholar]
  22. Cole JR, Wang Q, Cardenas E, Fish J, Chai B et al. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 2009;37:D141–D145 [CrossRef][PubMed]
    [Google Scholar]
  23. Chen T, Yu WH, Izard J, Baranova OV, Lakshmanan A et al. The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database 2010;2010:baq013 [CrossRef][PubMed]
    [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 [CrossRef][PubMed]
    [Google Scholar]
  25. Yu XL, Chan Y, Zhuang LF, Lai HC, Lang NP et al. Distributions of Synergistetes in clinically-healthy and diseased periodontal and peri-implant niches. Microb Pathog 2016;94:90–103 [CrossRef][PubMed]
    [Google Scholar]
  26. Kumar PS, Mason MR, Brooker MR, O'Brien K. Pyrosequencing reveals unique microbial signatures associated with healthy and failing dental implants. J Clin Periodontol 2012;39:425–433 [CrossRef][PubMed]
    [Google Scholar]
  27. Zheng H, Xu L, Wang Z, Li L, Zhang J et al. Subgingival microbiome in patients with healthy and ailing dental implants. Sci Rep 2015;5:10948 [CrossRef][PubMed]
    [Google Scholar]
  28. Canullo L, Radovanović S, Delibasic B, Blaya JA, Penarrocha D et al. The predictive value of microbiological findings on teeth, internal and external implant portions in clinical decision making. Clin Oral Implants Res 2017;28:512–519 [CrossRef][PubMed]
    [Google Scholar]
  29. da Silva ES, Feres M, Figueiredo LC, Shibli JA, Ramiro FS et al. Microbiological diversity of peri-implantitis biofilm by Sanger sequencing. Clin Oral Implants Res 2014;25:1192–1199 [CrossRef][PubMed]
    [Google Scholar]
  30. Tamura N, Ochi M, Miyakawa H, Nakazawa F. Analysis of bacterial flora associated with peri-implantitis using obligate anaerobic culture technique and 16S rDNA gene sequence. Int J Oral Maxillofac Implants 2013;28:1521–1529 [CrossRef][PubMed]
    [Google Scholar]
  31. van Brakel R, Cune MS, van Winkelhoff AJ, de Putter C, Verhoeven JW et al. Early bacterial colonization and soft tissue health around zirconia and titanium abutments: an in vivo study in man. Clin Oral Implants Res 2011;22:571–577 [CrossRef][PubMed]
    [Google Scholar]
  32. Zhuang LF, Watt RM, Mattheos N, Si MS, Lai HC et al. Periodontal and peri-implant microbiota in patients with healthy and inflamed periodontal and peri-implant tissues. Clin Oral Implants Res 2016;27:13–21 [CrossRef][PubMed]
    [Google Scholar]
  33. 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 [CrossRef][PubMed]
    [Google Scholar]
  34. Mombelli A, Décaillet F. The characteristics of biofilms in peri-implant disease. J Clin Periodontol 2011;38:203–213 [CrossRef][PubMed]
    [Google Scholar]
  35. Rakic M, Grusovin MG, Canullo L. The microbiologic profile associated with peri-implantitis in humans: a systematic review. Int J Oral Maxillofac Implants 2016;31:359–368 [CrossRef][PubMed]
    [Google Scholar]
  36. Riep B, Edesi-Neuss L, Claessen F, Skarabis H, Ehmke B et al. Are putative periodontal pathogens reliable diagnostic markers?. J Clin Microbiol 2009;47:1705–1711 [CrossRef][PubMed]
    [Google Scholar]
  37. Al-Ahmad A, Hellwig E, Wittmer A, Kist M, Waidner B. Re: the impact of the stone age diet on gingival conditions in the absence of oral hygiene. Baumgartner S, Imfeld T, Schicht O, Rath C, Persson RE, Persson GR. (J Periodontol 2009;80:759–768.). J Periodontol 2010;81:338–339 [CrossRef][PubMed]
    [Google Scholar]
  38. Al-Ahmad A, Kürschner A, Weckesser S, Wittmer A, Rauberger H et al. Is Helicobacter pylori resident or transient in the human oral cavity?. J Med Microbiol 2012;61:1146–1152 [CrossRef][PubMed]
    [Google Scholar]
  39. Persson GR, Renvert S. Cluster of bacteria associated with peri-implantitis. Clin Implant Dent Relat Res 2014;16:783–793 [CrossRef][PubMed]
    [Google Scholar]
  40. Delong EF, Preston CM, Mincer T, Rich V, Hallam SJ et al. Community genomics among stratified microbial assemblages in the ocean's interior. Science 2006;311:496–503 [CrossRef][PubMed]
    [Google Scholar]
  41. Hall-Stoodley L, Stoodley P, Kathju S, Høiby N, Moser C et al. Towards diagnostic guidelines for biofilm-associated infections. FEMS Immunol Med Microbiol 2012;65:127–145 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000682
Loading
/content/journal/jmm/10.1099/jmm.0.000682
Loading

Data & Media loading...

Supplements

Supplementary File 1

PDF
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