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Microbiological Diversity of Peri-Implantitis Biofilms

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Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 830))

Abstract

The open-ended microbial diagnostic approaches such as the complete or partial sequencing of the 16S ribosomal gene by Sanger sequencing or by pyrosequencing have provided new insights into the diversity of the oral microbiota. These techniques have recently been used to evaluate the microbiota associated with osseointegrated implants and these results have expanded the knowledge on the diversity of the microbial communities associated with peri-implantitis. Taken together, the results of these studies suggest that the diversity of the microbial community of peri-implantitis and periodontitis might not be as similar as previously thought. Although certain known periodontal pathogens may also be associated with the etiology of peri-implantitis, apparently there were many differences between these two clinical conditions, involving distinct microorganisms. Further investigations on the diversity of peri-implant microbiota would be essential in order to define effective preventive and therapeutic strategies for peri-implantitis. It is also important to standardize laboratory protocols to make the results of the open-ended diagnostic techniques based on PCR amplification more comparable throughout the different research groups.

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References

  • Abusleme L, Hong BY, Dupuy AK, Strausbaugh LD, Diaz PI (2014) Influence of DNA extraction on oral microbial profiles obtained via 16S rRNA gene sequencing. J Oral Microbiol 23:1–7

    Google Scholar 

  • Al-Radha AS, Pal A, Pettemerides AP, Jenkinson HF (2012) Molecular analysis of microbiota associated with peri-implant diseases. J Dent 40:989–998

    Article  CAS  PubMed  Google Scholar 

  • Atieh MA, Alsabeeha NH, Faggion CM Jr, Duncan WJ (2013) The frequency of peri-implant diseases: a systematic review and meta-analysis. J Periodontol 84:1586–1598

    PubMed  Google Scholar 

  • Becker W, Becker BE, Newman MG, Nyman S (1990) Clinical and microbiologic findings that may contribute to dental implant failure. Int J Oral Maxillofac Implants 5:31–38

    CAS  PubMed  Google Scholar 

  • Case RJ, Boucher Y, Dahllöf I, Holmström C, Doolittle WF, Kjelleberg S (2007) Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies. Appl Environ Microbiol 73:278–288

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Charalampakis G, Abrahamsson I, Carcuac O, Dahlén G, Berglundh T (2014) Microbiota in experimental periodontitis and peri-implantitis in dogs. Clin Oral Implants Res 25:1094–1098

    Google Scholar 

  • Cilia V, Lafay B, Christen R (1996) Sequence heterogeneities among 16S ribosomal RNA sequences, and their effect on phylogenetic analyses at the species level. Mol Biol Evol 13:451–461

    Article  CAS  PubMed  Google Scholar 

  • da Silva ES, Feres M, Figueiredo LC, Shibli JA, Ramiro FS, Faveri M (2014) Microbiological diversity of peri-implantitis biofilm by Sanger sequencing. Clin Oral Implants Res 25:1192–1199

    Article  PubMed  Google Scholar 

  • Dabdoub SM1, Tsigarida AA, Kumar PS (2013) Patient-specific analysis of periodontal and peri-implant microbiomes. J Dent Res 92(12 Suppl):168S–175S

    Article  CAS  PubMed  Google Scholar 

  • de Lillo A, Booth V, Kyriacou L, Weightman AJ, Wade WG (2004) Culture-independent identification of periodontitis-associated Porphyromonas and Tannerella populations by targeted molecular analysis. J Clin Microbiol 42:5523–5527

    Article  PubMed Central  PubMed  Google Scholar 

  • Diaz PI, Dupuy AK, Abusleme L, Reese B, Obergfell C, Choquette L, Dongari-Bagtzoglou A, Peterson DE, Terzi E, Strausbaugh LD (2012) Using high throughput sequencing to explore the biodiversity in oral bacterial communities. Mol Oral Microbiol 27:182–201

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Eke PI, Braswell LD, Fritz ME (1998) Microbiota associated with experimental peri-implantitis and periodontitis in adult macaca mulatta monkeys. J Periodontol 69:190–194

    Article  CAS  PubMed  Google Scholar 

  • Faveri M, Mayer MP, Feres M, de Figueiredo LC, Dewhirst FE, Paster BJ (2008) Microbiological diversity of generalized aggressive periodontitis by 16S rRNA clonal analysis. Oral Microbiol Immunol 23:112–118

    Article  CAS  PubMed  Google Scholar 

  • Faveri M, Gonçalves LF, Feres M, Figueiredo LC, Gouveia LA, Shibli JA, Mayer MP (2011) Prevalence and microbiological diversity of archaea in peri-implantitis subjects by 16S ribosomal RNA clonal analysis. J Periodontal Res 46:338–344

    Article  CAS  PubMed  Google Scholar 

  • França LT, Carrilho E, Kist TB (2002) A review of DNA sequencing techniques. Q Rev Biophys 35:169–200

    Article  PubMed  Google Scholar 

  • Green PM, Giannelli F (1994) Direct sequencing of PCR-amplified DNA. Mol Biotechnol 1:117–124

    Article  CAS  PubMed  Google Scholar 

  • Harrington CT, Lin EI, Olson MT, Eshleman JR (2013) Fundamentals of pyrosequencing. Arch Pathol Lab Med 137:1296–1303

    Article  CAS  PubMed  Google Scholar 

  • Harris LG, Meredith DO, Eschbach L, Richards RG (2007) Staphylococcus aureus adhesion to standard micro-rough and electropolished implant materials. J Mater Sci Mater Med 18:1151–1156

    Article  CAS  PubMed  Google Scholar 

  • Heitz-Mayfield LJ (2008) Diagnosis and management of peri-implant diseases. Aust Dent J 53(Suppl 1):43–48

    Article  Google Scholar 

  • Heitz-Mayfield LJ, Lang NP (2010) Comparative biology of chronic and aggressive periodontitis vs. peri-implantitis. Periodontology 2000 53:167–181

    Article  PubMed  Google Scholar 

  • Heydenrijk K, Meijer HJA, van der Reijden WA, Raghoebar GM, Vissink A, Stegenga B (2002) Microbiota around root-form endosseous implants: a review of the literature. Int J Oral Maxillofac Implants 17:829–838

    PubMed  Google Scholar 

  • Hiyari S, Bennett KM (2011) Dental diagnostics: molecular analysis of oral biofilms. J Dent Hyg 85:256–263

    PubMed  Google Scholar 

  • Hudetz D, Ursic Hudetz S, Harris LG, Luginbühl R, Friederich NF, Landmann R (2008) Weak effect of metal type and ica genes on staphylococcal infection of titanium and stainless steel implants. Clin Microbiol Infect 14:1135–1145

    Article  CAS  PubMed  Google Scholar 

  • Hultin M, Gustafsson A, Hallström H, Johansson LA, Ekfeldt A, Klinge B (2002) Microbiological findings and host response in patients with peri-implantitis. Clin Oral Implants Res 13:349–358

    Article  PubMed  Google Scholar 

  • Koyanagi T, Sakamoto M, Takeuchi Y, Ohkuma M, Izumi Y (2010) Analysis of microbiota associated with peri-implantitis using 16S rRNA gene clone library. J Oral Microbiol 24:1–7

    Google Scholar 

  • Koyanagi T, Sakamoto M, Takeuchi Y, Maruyama N, Ohkuma M, Izumi Y (2013) Comprehensive microbiological findings in peri-implantitis and periodontitis. J Clin Periodontol 40:218–226

    Article  PubMed  Google Scholar 

  • Kumar PS, Leys EJ, Bryk JM, Martinez FJ, Moeschberger ML, Griffen AL (2006) Changes in periodontal health status are associated with bacterial community shifts as assessed by quantitative 16S cloning and sequencing. J Clin Microbiol 44:3665–3673

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Kumar PS, Mason MR, Brooker MR, O’Brien K (2012) Pyrosequencing reveals unique microbial signatures associated with healthy and failing dental implants. J Clin Periodontol 39:425–433

    Article  PubMed Central  PubMed  Google Scholar 

  • Lee KH, Maiden MF, Tanner AC, Weber HP (1999) Microbiota of successful osseointegrated dental implants. J Periodontol 70:131–138

    Article  CAS  PubMed  Google Scholar 

  • Leonhardt A, Renvert S, Dahlén G (1999) Microbial findings at failing implants. Clin Oral Implants Res 10:339–345

    Article  CAS  PubMed  Google Scholar 

  • Leonhardt A, Bergström C, Lekholm U (2003a) Microbiologic diagnostics at titanium implants. Clin Implant Dent Relat Res 5:226–232

    Article  PubMed  Google Scholar 

  • Leonhardt A, Dahlén G, Renvert S (2003b) Five-year clinical, microbiological, and radiological outcome following treatment of peri-implantitis in man. J Periodontol 74:1415–1422

    Article  PubMed  Google Scholar 

  • Lepp PW, Brinig MM, Ouverney CC, Palm K, Armitage GC, Relman DA (2004) Methanogenic archaea and human periodontal disease. Proc Natl Acad Sci U S A 101:6176–6681

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Matarazzo F, Ribeiro AC, Feres M, Faveri M, Mayer MP (2011) Diversity and quantitative analysis of Archaea in aggressive periodontitis and periodontally healthy subjects. J Clin Periodontol 38:621–627

    Article  PubMed  Google Scholar 

  • Mombelli A (1993) Microbiology of the dental implant. Adv Dent Res 7:202–206

    CAS  PubMed  Google Scholar 

  • Mombelli A (1999) Prevention and therapy of peri-implant infections. In: Lang NP, Karring T, Lindhe J (eds) Proceedings of the 3rd European workshop on periodontology. Quintessence Book, Berlin, pp 281–303

    Google Scholar 

  • Mombelli A, Décaillet F (2011) The characteristics of biofilms in peri-implant disease. J Clin Periodontol 38(Suppl 11):203–213

    Article  PubMed  Google Scholar 

  • Mombelli A, Lang NP (1998) The diagnosis and treatment of periimplantitis. Periodontology 2000 17:63–76

    Article  CAS  PubMed  Google Scholar 

  • Mombelli A, Mericske-Stern R (1990) Microbiological features of stable osseointegrated implants used as abutments for overdentures. Clin Oral Implants Res 1:1–7

    Article  CAS  PubMed  Google Scholar 

  • Mombelli A, van Oosten MA, Schurch E Jr, Land NP (1987) The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol 2:145–151

    Article  CAS  PubMed  Google Scholar 

  • Mombelli A, Marxer M, Gaberthüel T, Grunder U, Lang NP (1995) The microbiota of osseointegrated implants in patients with a history of periodontal disease. J Clin Periodontol 22:124–130

    Article  CAS  PubMed  Google Scholar 

  • Paster BJ, Boches SK, Galvin JL, Ericson RE, Lau CN, Levanos VA, Sahasrabudhe A, Dewhirst FE (2001) Bacterial diversity in human subgingival plaque. J Bacteriol 183:3770–3783

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Persson GR, Renvert S (2013) Cluster of bacteria associated with peri-implantitis. Clin Implant Dent Relat Res (in press)

    Google Scholar 

  • Persson GR, Samuelsson E, Lindahl C, Renvert S (2010) Mechanical non-surgical treatment of peri-implantitis: a single-blinded randomized longitudinal clinical study. II. Microbiological results. J Clin Periodontol 37:563–573

    Article  PubMed  Google Scholar 

  • Petrosino JF, Highlander S, Luna RA, Gibbs RA, Versalovic J (2009) Metagenomic pyrosequencing and microbial identification. Clin Chem 55:856–866

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pontoriero R, Tonelli MP, Carnevale G, Mombelli A, Nyman SR, Lang NP (1994) Experimentally induced peri-implant mucositis. A clinical study in humans. Clin Oral Implants Res 54:254–259

    Article  Google Scholar 

  • Prober JM, Trainor GL, Dam RJ et al (1987) A system for rapid DNA sequencing with fluorescent chain-terminating dideoxynucleotides. Science 238(4825):336–341

    Article  CAS  PubMed  Google Scholar 

  • Quirynen M, Vogels R, Peeters W, van Steenberghe D, Naert I, Haffajee A (2006) Dynamics of initial subgingival colonization of ‘pristine’ peri-implant pockets. Clin Oral Implants Res 17:25–37

    Article  PubMed  Google Scholar 

  • Rams TE, Balkin BE, Roberts TW, Molzan AK (2013) Microbiological aspects of human mandibular subperiosteal dental implants. J Oral Implantol 39:714–722

    Article  PubMed  Google Scholar 

  • Rastogi G, Coaker GL, Leveau JH (2013) New insights into the structure and function of phyllosphere microbiota through high-throughput molecular approaches. FEMS Microbiol Lett 348(1):1–10

    Article  CAS  PubMed  Google Scholar 

  • Renvert S, Roos-Jansåker AM, Lindahl C, Renvert H, Rutger Persson G (2007) Infection at titanium implants with or without a clinical diagnosis of inflammation. Clin Oral Implants Res 18:509–516

    Article  PubMed  Google Scholar 

  • Rutar A, Lang NP, Buser D, Bürgin W, Mombelli A (2001) Retrospective assessment of clinical and microbiological factors affecting periimplant tissue conditions. Clin Oral Implants Res 12:189–195

    Article  CAS  PubMed  Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74:5463–5467

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Sanz M, Newman MG, Nachnani S, Holt R, Stewart R, Flemmig T (1990) Characterization of the subgingival microbial flora around endosteal sapphire dental implants in partially edentulous patients. Int J Oral Maxillofac Implants 5:247–253

    CAS  PubMed  Google Scholar 

  • Shchipkova AY, Nagaraja HN, Kumar PS (2010) Subgingival microbial profiles of smokers with periodontitis. J Dent Res 89:1247–1253

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Shibli JA, Martins MC, Lotufo RFM, Marcantonio E Jr (2003) Microbiologic and radiographic analysis of ligature-induced peri-implantitis with different dental implant surfaces. Int J Oral Maxillofac Implants 18:383–390

    PubMed  Google Scholar 

  • Shibli JA, Melo L, Ferrari DS, Figueiredo LC, Faveri M, Feres M (2008) Composition of supra-and subgingival biofilm of subjects with healthy and diseased implants. Clin Oral Implants Res 19:975–982

    Article  PubMed  Google Scholar 

  • Silverstein LH, Kurtzman D, Garnick JJ, Schuster GS, Steflik DE, Moskowitz ME (1994) The microbiota of the peri-implant region in health and disease. Implant Dent 3:170–174

    Article  CAS  PubMed  Google Scholar 

  • Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr (1998) Microbial complexes in subgingival plaque. J Clin Periodontol 25:134–144

    Article  CAS  PubMed  Google Scholar 

  • Tabanella G, Nowzari H, Slots J (2009) Clinical and microbiological determinants of ailing dental implants. Clin Implant Dent Relat Res 11:24–36

    Article  PubMed  Google Scholar 

  • Tillmanns HWS, Hermann JS, Tiffee JC, Burgess AV, Meffert RM (1998) Evaluation of three different dental implants in ligature-induced peri-implantitis in the beagle dog. Part II. Histology and microbiology. Int J Oral Maxillofac Implants 13:59–68

    CAS  PubMed  Google Scholar 

  • Vianna ME, Conrads G, Gomes BP, Horz HP (2006) Identification and quantification of archaea involved in primary endodontic infections. J Clin Microbiol 44:1274–1282

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wade WG (2011) Has the use of molecular methods for the characterization of the human oral microbiome changed our understanding of the role of bacteria in the pathogenesis of periodontal disease? J Clin Periodontol 38(Suppl 11):7–16

    Article  PubMed  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zitzmann NU, Berglundh T (2008) Definition and prevalence of peri-implant diseases. J Clin Periodontol 35(8 Suppl):286–291

    Article  PubMed  Google Scholar 

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Correspondence to Marcelo Faveri .

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Faveri, M., Figueiredo, L.C., Shibli, J.A., Pérez-Chaparro, P.J., Feres, M. (2015). Microbiological Diversity of Peri-Implantitis Biofilms. In: Donelli, G. (eds) Biofilm-based Healthcare-associated Infections. Advances in Experimental Medicine and Biology, vol 830. Springer, Cham. https://doi.org/10.1007/978-3-319-11038-7_5

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