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Peri-Implant Infections of Oral Biofilm Etiology

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Book cover Biofilm-based Healthcare-associated Infections

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

Abstract

Biofilms are complex microbial communities that grow on various surfaces in nature. The oral micobiota tend to form polymicrobial biofilms, particularly on the hard mineralized surfaces of teeth, which may impact on oral health and disease. They can cause inflammation of the adjacent tooth-supporting (periodontal) tissues, leading to destructive periodontal disease and tooth loss. The emergence of osseointegrated dental implants as a restorative treatment option for replacing missing teeth has also brought along new artificial surfaces within the oral cavity, on which oral bacteria can form biofilms. As in the case of natural teeth, biofilms on implant surfaces may also trigger infection and cause inflammatory destruction of the peri-implant tissue (i.e. peri-implantitis). While there are strong similarities in the composition of the mixed microbial flora between periodontal and peri-implant infections, there are also a few distinctive differences. The immunological events underlying the pathogenesis of peri-implant infections are qualitatively similar, yet more extensive, compared to periodontal infections, resulting in a faster progression of tissue destruction. This chapter summarizes the current knowledge on the microbiology and immunology of peri-implant infections, including findings from the peri-implant crevicular fluid, the inflammatory exudate of the peri-implant tissue. Moreover, it discusses the diagnosis and current approaches for the treatment of oral infections.

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References

  • Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE (2005) Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 43(11):5721–5732

    PubMed Central  PubMed  Google Scholar 

  • Abrahamsson I, Berglundh T (2009) Effects of different implant surfaces and designs on marginal bone-level alterations: a review. Clin Oral Implants Res 20(Suppl 4):207–215

    PubMed  Google Scholar 

  • Adonogianaki E, Mooney J, Wennstrom JL, Lekholm U, Kinane DF (1995) Acute-phase proteins and immunoglobulin G against Porphyromonas gingivalis in peri-implant crevicular fluid: a comparison with gingival crevicular fluid. Clin Oral Implants Res 6(1):14–23

    CAS  PubMed  Google Scholar 

  • Albouy JP, Abrahamsson I, Persson LG, Berglundh T (2011) Implant surface characteristics influence the outcome of treatment of peri-implantitis: an experimental study in dogs. J Clin Periodontol 38(1):58–64. doi:10.1111/j.1600-051X.2010.01631.x

    PubMed  Google Scholar 

  • Alcoforado GA, Rams TE, Feik D, Slots J (1991) Microbial aspects of failing osseointegrated dental implants in humans. J Parodontol 10(1):11–18

    CAS  PubMed  Google Scholar 

  • Aloise JP, Curcio R, Laporta MZ, Rossi L, da Silva AM, Rapoport A (2010) Microbial leakage through the implant-abutment interface of Morse taper implants in vitro. Clin Oral Implants Res 21(3):328–335

    PubMed  Google Scholar 

  • Andreiotelli M, Koutayas SO, Madianos PN, Strub JR (2008) Relationship between interleukin-1 genotype and peri-implantitis: a literature review. Quintessence Int 39(4):289–298

    PubMed  Google Scholar 

  • Arakawa H, Uehara J, Hara ES, Sonoyama W, Kimura A, Kanyama M, Matsuka Y, Kuboki T (2012) Matrix metalloproteinase-8 is the major potential collagenase in active peri-implantitis. J Prosthodont Res 56(4):249–255

    PubMed  Google Scholar 

  • Arciola CR (2009) New concepts and new weapons in implant infections. Int J Artif Organs 32(9):533–536

    PubMed  Google Scholar 

  • Arikan F, Buduneli N, Kutukculer N (2008) Osteoprotegerin levels in peri-implant crevicular fluid. Clin Oral Implants Res 19(3):283–288

    PubMed  Google Scholar 

  • Arikan F, Buduneli N, Lappin DF (2011) C-telopeptide pyridinoline crosslinks of type I collagen, soluble RANKL, and osteoprotegerin levels in crevicular fluid of dental implants with peri-implantitis: a case-control study. Int J Oral Maxillofac Implants 26(2):282–289

    PubMed  Google Scholar 

  • Astrand P, Engquist B, Dahlgren S, Grondahl K, Engquist E, Feldmann H (2004) Astra Tech and Branemark system implants: a 5-year prospective study of marginal bone reactions. Clin Oral Implants Res 15(4):413–420

    PubMed  Google Scholar 

  • Ataoglu H, Alptekin NO, Haliloglu S, Gursel M, Ataoglu T, Serpek B, Durmus E (2002) Interleukin-1beta, tumor necrosis factor-alpha levels and neutrophil elastase activity in peri-implant crevicular fluid. Clin Oral Implants Res 13(5):470–476

    PubMed  Google Scholar 

  • Bassetti M, Schar D, Wicki B, Eick S, Ramseier CA, Arweiler NB, Sculean A, Salvi GE (2013) Anti-infective therapy of peri-implantitis with adjunctive local drug delivery or photodynamic therapy: 12-month outcomes of a randomized controlled clinical trial. Clin Oral Implants Res. doi:10.1111/clr.12155

    PubMed  Google Scholar 

  • Belibasakis GN (2014) Microbiological and immuno-pathological aspects of peri-implant diseases. Arch Oral Biol 59(1):66–72

    CAS  PubMed  Google Scholar 

  • Belibasakis GN, Bostanci N (2012) The RANKL-OPG system in clinical periodontology. J Clin Periodontol 39(3):239–248

    CAS  PubMed  Google Scholar 

  • Berglundh T, Lindhe J, Ericsson I, Marinello CP, Liljenberg B, Thomsen P (1991) The soft tissue barrier at implants and teeth. Clin Oral Implants Res 2(2):81–90

    CAS  PubMed  Google Scholar 

  • Berglundh T, Lindhe J, Marinello C, Ericsson I, Liljenberg B (1992) Soft tissue reaction to de novo plaque formation on implants and teeth. An experimental study in the dog. Clin Oral Implants Res 3(1):1–8

    CAS  PubMed  Google Scholar 

  • Binon PP (2000) Implants and components: entering the new millennium. Int J Oral Maxillofac Implants 15(1):76–94

    CAS  PubMed  Google Scholar 

  • Bormann KH, Stuhmer C, Z’Graggen M, Kokemoller H, Rucker M, Gellrich NC (2010) IL-1 polymorphism and periimplantitis. A literature review. Schweiz Monatsschr Zahnmed = Rev mensuelle suisse d’odonto-stomatol = Riv mensile svizzera di odontol e stomatologia/SSO 120(6):510–520

    Google Scholar 

  • Bostanci N, Emingil G, Saygan B, Turkoglu O, Atilla G, Curtis MA, Belibasakis GN (2009) Expression and regulation of the NALP3 inflammasome complex in periodontal diseases. Clin Exp Immunol 157(3):415–422

    CAS  PubMed Central  PubMed  Google Scholar 

  • Botero JE, Gonzalez AM, Mercado RA, Olave G, Contreras A (2005) Subgingival microbiota in peri-implant mucosa lesions and adjacent teeth in partially edentulous patients. J Periodontol 76(9):1490–1495

    PubMed  Google Scholar 

  • Bower RC, Radny NR, Wall CD, Henry PJ (1989) Clinical and microscopic findings in edentulous patients 3 years after incorporation of osseointegrated implant-supported bridgework. J Clin Periodontol 16(9):580–587

    CAS  PubMed  Google Scholar 

  • Busscher HJ, Rinastiti M, Siswomihardjo W, van der Mei HC (2010) Biofilm formation on dental restorative and implant materials. J Dent Res 89(7):657–665

    CAS  PubMed  Google Scholar 

  • Callan DP, Cobb CM, Williams KB (2005) DNA probe identification of bacteria colonizing internal surfaces of the implant-abutment interface: a preliminary study. J Periodontol 76(1):115–120

    PubMed  Google Scholar 

  • Carcuac O, Abrahamsson I, Albouy JP, Linder E, Larsson L, Berglundh T (2013) Experimental periodontitis and peri-implantitis in dogs. Clin Oral Implants Res 24(4):363–371

    PubMed  Google Scholar 

  • Casado PL, Canullo L, de Almeida Filardy A, Granjeiro JM, Barboza EP, Leite Duarte ME (2013) Interleukins 1beta and 10 expressions in the periimplant crevicular fluid from patients with untreated periimplant disease. Implant Dent 22(2):143–150

    PubMed  Google Scholar 

  • Chan HL, Lin GH, Suarez F, Maceachern M, Wang HL (2014) Surgical management of peri-implantitis: a systematic review and meta-analysis of treatment outcomes. J Periodontol 85:(8):1027-1041

    Google Scholar 

  • Charalampakis G, Leonhardt A, Rabe P, Dahlen G (2012) Clinical and microbiological characteristics of peri-implantitis cases: a retrospective multicentre study. Clin Oral Implants Res 23(9):1045–1054

    CAS  PubMed  Google Scholar 

  • Charalampakis G, Ramberg P, Dahlen G, Berglundh T, Abrahamsson I (2014) Effect of cleansing of biofilm formed on titanium discs. Clin Oral Implants Res Apr 16 doi:10.1111/clr.12397

  • Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM (1995) Microbial biofilms. Annu Rev Microbiol 49:711–745

    CAS  PubMed  Google Scholar 

  • Curtis DA, Kao R, Plesh O, Finzen F, Franz L (1997) Crevicular fluid analysis around two failing dental implants: a clinical report. J Prosthodont 6(3):210–214

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Darabi E, Kadkhoda Z, Amirzargar A (2013) Comparison of the levels of tumor necrosis factor-alpha and Interleukin-17 in gingival crevicular fluid of patients with peri-implantitis and a control group with healthy implants. Iran J Allergy Asthma Immunol 12(1):75–80, doi:012.01/ijaai.7580

    CAS  PubMed  Google Scholar 

  • Darouiche RO, Landon GC, Patti JM, Nguyen LL, Fernau RC, McDevitt D, Greene C, Foster T, Klima M (1997) Role of Staphylococcus aureus surface adhesins in orthopaedic device infections: are results model-dependent? J Med Microbiol 46(1):75–79

    CAS  PubMed  Google Scholar 

  • de Mendonca AC, Santos VR, Cesar-Neto JB, Duarte PM (2009) Tumor necrosis factor-alpha levels after surgical anti-infective mechanical therapy for peri-implantitis: a 12-month follow-up. J Periodontol 80(4):693–699

    PubMed  Google Scholar 

  • do Nascimento C, Barbosa RE, Issa JP, Watanabe E, Ito IY, Albuquerque RF Jr (2008) Bacterial leakage along the implant-abutment interface of premachined or cast components. Int J Oral Maxillofac Surg 37(2):177–180

    PubMed  Google Scholar 

  • do Nascimento C, Barbosa RE, Issa JP, Watanabe E, Ito IY, de Albuquerque Junior RF (2009) Use of checkerboard DNA-DNA hybridization to evaluate the internal contamination of dental implants and comparison of bacterial leakage with cast or pre-machined abutments. Clin Oral Implants Res 20(6):571–577

    PubMed  Google Scholar 

  • Duarte PM, de Mendonca AC, Maximo MB, Santos VR, Bastos MF, Nociti FH (2009a) Effect of anti-infective mechanical therapy on clinical parameters and cytokine levels in human peri-implant diseases. J Periodontol 80(2):234–243

    CAS  PubMed  Google Scholar 

  • Duarte PM, de Mendonca AC, Maximo MB, Santos VR, Bastos MF, Nociti Junior FH (2009b) Differential cytokine expressions affect the severity of peri-implant disease. Clin Oral Implants Res 20(5):514–520

    PubMed  Google Scholar 

  • Ericsson I, Berglundh T, Marinello C, Liljenberg B, Lindhe J (1992) Long-standing plaque and gingivitis at implants and teeth in the dog. Clin Oral Implants Res 3(3):99–103

    CAS  PubMed  Google Scholar 

  • Esposito M, Murray-Curtis L, Grusovin MG, Coulthard P, Worthington HV (2007) Interventions for replacing missing teeth: different types of dental implants. Cochrane Database Syst Rev 4:CD003815

    PubMed  Google Scholar 

  • Fonseca FJ, Moraes Junior M, Lourenco EJ, Teles Dde M, Figueredo CM (2014) Cytokines expression in saliva and peri-implant crevicular fluid of patients with peri-implant disease. Clin Oral Implants Res 25(2):e68–e72

    PubMed  Google Scholar 

  • Furst MM, Salvi GE, Lang NP, Persson GR (2007) Bacterial colonization immediately after installation on oral titanium implants. Clin Oral Implants Res 18(4):501–508

    PubMed  Google Scholar 

  • Gotfredsen K, Karlsson U (2001) A prospective 5-year study of fixed partial prostheses supported by implants with machined and TiO2-blasted surface. J Prosthodont 10(1):2–7

    CAS  PubMed  Google Scholar 

  • Gross M, Abramovich I, Weiss EI (1999) Microleakage at the abutment-implant interface of osseointegrated implants: a comparative study. Int J Oral Maxillofac Implants 14(1):94–100

    CAS  PubMed  Google Scholar 

  • Gualini F, Berglundh T (2003) Immunohistochemical characteristics of inflammatory lesions at implants. J Clin Periodontol 30(1):14–18

    PubMed  Google Scholar 

  • Guncu GN, Akman AC, Gunday S, Yamalik N, Berker E (2012) Effect of inflammation on cytokine levels and bone remodelling markers in peri-implant sulcus fluid: a preliminary report. Cytokine 59(2):313–316

    CAS  PubMed  Google Scholar 

  • Hajishengallis G (2014) Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends Immunol 35(1):3–11

    CAS  PubMed  Google Scholar 

  • Hajishengallis G, Lamont RJ (2012) Beyond the red complex and into more complexity: the polymicrobial synergy and dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol 27(6):409–419

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hamedi M, Belibasakis GN, Cruchley AT, Rangarajan M, Curtis MA, Bostanci N (2009) Porphyromonas gingivalis culture supernatants differentially regulate interleukin-1beta and interleukin-18 in human monocytic cells. Cytokine 45(2):99–104

    CAS  PubMed  Google Scholar 

  • Hannig M (1997) Transmission electron microscopic study of in vivo pellicle formation on dental restorative materials. Eur J Oral Sci 105(5 Pt 1):422–433

    CAS  PubMed  Google Scholar 

  • Heitz-Mayfield LJ (2008) Peri-implant diseases: diagnosis and risk indicators. J Clin Periodontol 35(8 Suppl):292–304. doi:10.1111/j.1600-051X.2008.01275.x

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Heitz-Mayfield LJ, Mombelli A (2014) The therapy of peri-implantitis: a systematic review. Int J Oral Maxillofac Implants 29(Suppl):325–345

    PubMed  Google Scholar 

  • Heuer W, Kettenring A, Stumpp SN, Eberhard J, Gellermann E, Winkel A, Stiesch M (2012) Metagenomic analysis of the peri-implant and periodontal microflora in patients with clinical signs of gingivitis or mucositis. Clin Oral Investig 16(3):843–850

    PubMed  Google Scholar 

  • Huang R, Li M, Gregory RL (2014) Bacterial interactions in dental biofilm. Virulence 2(5):435–444

    Google Scholar 

  • Hultin M, Gustafsson A, Hallstrom H, Johansson LA, Ekfeldt A, Klinge B (2002) Microbiological findings and host response in patients with peri-implantitis. Clin Oral Implants Res 13(4):349–358

    PubMed  Google Scholar 

  • Jansson H, Hamberg K, De Bruyn H, Bratthall G (2005) Clinical consequences of IL-1 genotype on early implant failures in patients under periodontal maintenance. Clin Implant Dent Relat Res 7(1):51–59

    PubMed  Google Scholar 

  • Kaklamanos EG, Tsalikis L (2002) A review on peri-implant crevicular fluid assays potential in monitoring and predicting peri-implant tissue responses. J Int Acad Periodontol 4(2):49–59

    CAS  PubMed  Google Scholar 

  • Kao RT, Curtis DA, Murray PA (1997) Diagnosis and management of peri-implant disease. J Calif Dent Assoc 25(12):872–880

    CAS  PubMed  Google Scholar 

  • Kivela-Rajamaki M, Maisi P, Srinivas R, Tervahartiala T, Teronen O, Husa V, Salo T, Sorsa T (2003a) Levels and molecular forms of MMP-7 (matrilysin-1) and MMP-8 (collagenase-2) in diseased human peri-implant sulcular fluid. J Periodontal Res 38(6):583–590

    CAS  PubMed  Google Scholar 

  • Kivela-Rajamaki MJ, Teronen OP, Maisi P, Husa V, Tervahartiala TI, Pirila EM, Salo TA, Mellanen L, Sorsa TA (2003b) Laminin-5 gamma2-chain and collagenase-2 (MMP-8) in human peri-implant sulcular fluid. Clin Oral Implants Res 14(2):158–165

    PubMed  Google Scholar 

  • Klinge B (2012) Peri-implant marginal bone loss: an academic controversy or a clinical challenge? Eur J Oral Implantol 5(Suppl):S13–S19

    PubMed  Google Scholar 

  • Kolenbrander PE, Palmer RJ Jr, Periasamy S, Jakubovics NS (2010) Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol 8(7):471–480

    CAS  PubMed  Google Scholar 

  • Konttinen YT, Lappalainen R, Laine P, Kitti U, Santavirta S, Teronen O (2006) Immunohistochemical evaluation of inflammatory mediators in failing implants. Int J Periodontics Restor Dent 26(2):135–141

    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(5):425–433

    PubMed Central  PubMed  Google Scholar 

  • Lachmann S, Kimmerle-Muller E, Axmann D, Scheideler L, Weber H, Haas R (2007) Associations between peri-implant crevicular fluid volume, concentrations of crevicular inflammatory mediators, and composite IL-1A–889 and IL-1B +3954 genotype. A cross-sectional study on implant recall patients with and without clinical signs of peri-implantitis. Clin Oral Implants Res 18(2):212–223. doi:10.1111/j.1600-0501.2006.01322.x

    PubMed  Google Scholar 

  • Lang NP, Mombelli A, Tonetti MS, Bragger U, Hammerle CH (1997) Clinical trials on therapies for peri-implant infections. Ann Periodontol 2(1):343–356

    CAS  PubMed  Google Scholar 

  • Leonhardt A, Renvert S, Dahlen G (1999) Microbial findings at failing implants. Clin Oral Implants Res 10(5):339–345

    CAS  PubMed  Google Scholar 

  • Leonhardt A, Grondahl K, Bergstrom C, Lekholm U (2002) Long-term follow-up of osseointegrated titanium implants using clinical, radiographic and microbiological parameters. Clin Oral Implants Res 13(2):127–132

    PubMed  Google Scholar 

  • Leonhardt A, Bergstrom C, Lekholm U (2003) Microbiologic diagnostics at titanium implants. Clin Implant Dent Relat Res 5(4):226–232

    PubMed  Google Scholar 

  • Levignac J (1965) Periimplantation osteolysis- periimplantosis – periimplantitis. Rev Fr Odontostomatol 12(8):1251–1260

    CAS  PubMed  Google Scholar 

  • Li J, Helmerhorst EJ, Leone CW, Troxler RF, Yaskell T, Haffajee AD, Socransky SS, Oppenheim FG (2004) Identification of early microbial colonizers in human dental biofilm. J Appl Microbiol 97(6):1311–1318

    CAS  PubMed  Google Scholar 

  • Lindhe J, Meyle J (2008) Peri-implant diseases: consensus report of the sixth European workshop on periodontology. J Clin Periodontol 35(8 Suppl):282–285

    PubMed  Google Scholar 

  • Lindhe J, Berglundh T, Ericsson I, Liljenberg B, Marinello C (1992) Experimental breakdown of peri-implant and periodontal tissues. A study in the beagle dog. Clin Oral Implants Res 3(1):9–16

    CAS  PubMed  Google Scholar 

  • Listgarten MA (1997) Clinical trials of endosseous implants: issues in analysis and interpretation. Ann Periodontol Am Acad Periodontol 2(1):299–313. doi:10.1902/annals.1997.2.1.299

    CAS  Google Scholar 

  • Marsh PD (2003) Are dental diseases examples of ecological catastrophes? Microbiology 149(Pt 2):279–294

    CAS  PubMed  Google Scholar 

  • Marsh PD, Devine DA (2011) How is the development of dental biofilms influenced by the host? J Clin Periodontol 38(Suppl 11):28–35

    PubMed  Google Scholar 

  • Melo RF, Lopes BM, Shibli JA, Marcantonio E Jr, Marcantonio RA, Galli GM (2012) Interleukin-1beta and interleukin-6 expression and gene polymorphisms in subjects with peri-implant disease. Clin Implant Dent Relat Res 14(6):905–914

    PubMed  Google Scholar 

  • Mishler O, Shiau HJ (2014) Management of peri-implant disease: a current appraisal. J Evid Based Dent Pract Suppl:53–59. doi: 10.1016/j.jebdp.2014.04.010

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

    PubMed  Google Scholar 

  • Mombelli A, Lang NP (1998) The diagnosis and treatment of peri-implantitis. Periodontol 2000 17:63–76

    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(4):145–151

    CAS  PubMed  Google Scholar 

  • Murata M, Tatsumi J, Kato Y, Suda S, Nunokawa Y, Kobayashi Y, Takeda H, Araki H, Shin K, Okuda K, Miyata T, Yoshie H (2002) Osteocalcin, deoxypyridinoline and interleukin-1beta in peri-implant crevicular fluid of patients with peri-implantitis. Clin Oral Implants Res 13(6):637–643

    PubMed  Google Scholar 

  • Naert I, Duyck J, Vandamme K (2012) Occlusal overload and bone/implant loss. Clin Oral Implants Res 23(Suppl 6):95–107

    PubMed  Google Scholar 

  • Nakazato G, Tsuchiya H, Sato M, Yamauchi M (1989) In vivo plaque formation on implant materials. Int J Oral Maxillofac Implants 4(4):321–326

    CAS  PubMed  Google Scholar 

  • Nowzari H, Botero JE, DeGiacomo M, Villacres MC, Rich SK (2008a) Microbiology and cytokine levels around healthy dental implants and teeth. Clin Implant Dent Relat Res 10(3):166–173

    PubMed  Google Scholar 

  • Nowzari H, Yi K, Chee W, Rich SK (2008b) Immunology, microbiology, and virology following placement of NobelPerfect scalloped dental implants: analysis of a case series. Clin Implant Dent Relat Res 10(3):157–165

    PubMed  Google Scholar 

  • Ozcakir-Tomruk C, Chiquet M, Mericske-Stern R (2012) Tenascin-C and matrix metalloproteinase-9 levels in crevicular fluid of teeth and implants. Clin Implant Dent Relat Res 14(5):672–681

    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(12):3770–3783

    CAS  PubMed Central  PubMed  Google Scholar 

  • Patti JM, Allen BL, McGavin MJ, Hook M (1994) MSCRAMM-mediated adherence of microorganisms to host tissues. Annu Rev Microbiol 48:585–617

    CAS  PubMed  Google Scholar 

  • Persson GR, Renvert S (2014) Cluster of bacteria associated with peri-implantitis. Clin Implant Dent Relat Res doi:10.1111/cid.12052

  • 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 5(4):254–259

    CAS  PubMed  Google Scholar 

  • Quirynen M, Vogels R, Pauwels M, Haffajee AD, Socransky SS, Uzel NG, van Steenberghe D (2005) Initial subgingival colonization of ‘pristine’ pockets. J Dent Res 84(4):340–344

    CAS  PubMed  Google Scholar 

  • Rakic M, Lekovic V, Nikolic-Jakoba N, Vojvodic D, Petkovic-Curcin A, Sanz M (2013) Bone loss biomarkers associated with peri-implantitis. A cross-sectional study. Clin Oral Implants Res 24(10):1110–1116

    PubMed  Google Scholar 

  • Rams TE, Link CC Jr (1983) Microbiology of failing dental implants in humans: electron microscopic observations. J Oral Implantol 11(1):93–100

    CAS  PubMed  Google Scholar 

  • Rams TE, Roberts TW, Feik D, Molzan AK, Slots J (1991) Clinical and microbiological findings on newly inserted hydroxyapatite-coated and pure titanium human dental implants. Clin Oral Implants Res 2(3):121–127

    CAS  PubMed  Google Scholar 

  • Rams TE, Degener JE, van Winkelhoff AJ (2013) Antibiotic resistance in human peri-implantitis microbiota. Clin Oral Implants Res. doi:10.1111/clr.12160

    PubMed  Google Scholar 

  • Renvert S, Roos-Jansaker 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(4):509–516

    PubMed  Google Scholar 

  • Renvert S, Lindahl C, Renvert H, Persson GR (2008) Clinical and microbiological analysis of subjects treated with Branemark or AstraTech implants: a 7-year follow-up study. Clin Oral Implants Res 19(4):342–347

    CAS  PubMed  Google Scholar 

  • Rosenberg ES, Torosian JP, Slots J (1991) Microbial differences in 2 clinically distinct types of failures of osseointegrated implants. Clin Oral Implants Res 2(3):135–144

    CAS  PubMed  Google Scholar 

  • Salvi GE, Zitzmann NU (2014) The effects of anti-infective preventive measures on the occurrence of biologic implant complications and implant loss: a systematic review. Int J Oral Maxillofac Implants 29(Suppl):292–307

    PubMed  Google Scholar 

  • Salvi GE, Furst MM, Lang NP, Persson GR (2008) One-year bacterial colonization patterns of Staphylococcus aureus and other bacteria at implants and adjacent teeth. Clin Oral Implants Res 19(3):242–248

    PubMed  Google Scholar 

  • Salvi GE, Franco LM, Braun TM, Lee A, Rutger Persson G, Lang NP, Giannobile WV (2010) Pro-inflammatory biomarkers during experimental gingivitis in patients with type 1 diabetes mellitus: a proof-of-concept study. J Clin Periodontol 37(1):9–16

    CAS  PubMed  Google Scholar 

  • Salvi GE, Aglietta M, Eick S, Sculean A, Lang NP, Ramseier CA (2012) Reversibility of experimental peri-implant mucositis compared with experimental gingivitis in humans. Clin Oral Implants Res 23(2):182–190

    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(3):247–253

    CAS  PubMed  Google Scholar 

  • Sarlati F, Sattari M, Gazar AG, Rafsenjani AN (2010) Receptor activator of nuclear factor kappa B ligand (RANKL) levels in peri-implant crevicular fluid. Iran J Immunol 7(4):226–233

    PubMed  Google Scholar 

  • Schaudinn C, Gorur A, Keller D, Sedghizadeh PP, Costerton JW (2009) Periodontitis: an archetypical biofilm disease. J Am Dent Assoc 140(8):978–986

    PubMed  Google Scholar 

  • Schierano G, Pejrone G, Brusco P, Trombetta A, Martinasso G, Preti G, Canuto RA (2008) TNF-alpha TGF-beta2 and IL-1beta levels in gingival and peri-implant crevicular fluid before and after de novo plaque accumulation. J Clin Periodontol 35(6):532–538

    PubMed  Google Scholar 

  • Schwarz F, Sahm N, Schwarz K, Becker J (2010) Impact of defect configuration on the clinical outcome following surgical regenerative therapy of peri-implantitis. J Clin Periodontol 37(5):449–455

    PubMed  Google Scholar 

  • Schwarz F, Hegewald A, John G, Sahm N, Becker J (2013) Four-year follow-up of combined surgical therapy of advanced peri-implantitis evaluating two methods of surface decontamination. J Clin Periodontol 40(10):962–967

    PubMed  Google Scholar 

  • Severino VO, Napimoga MH, de Lima Pereira SA (2011) Expression of IL-6, IL-10, IL-17 and IL-8 in the peri-implant crevicular fluid of patients with peri-implantitis. Arch Oral Biol 56(8):823–828. doi:10.1016/j.archoralbio.2011.01.006

    CAS  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(10):975–982

    PubMed  Google Scholar 

  • Sorsa T, Tjaderhane L, Konttinen YT, Lauhio A, Salo T, Lee HM, Golub LM, Brown DL, Mantyla P (2006) Matrix metalloproteinases: contribution to pathogenesis, diagnosis and treatment of periodontal inflammation. Ann Med 38(5):306–321. doi:10.1080/07853890600800103

    CAS  PubMed  Google Scholar 

  • Speziale P, Pietrocola G, Rindi S, Provenzano M, Provenza G, Di Poto A, Visai L, Arciola CR (2009) Structural and functional role of Staphylococcus aureus surface components recognizing adhesive matrix molecules of the host. Future Microbiol 4(10):1337–1352

    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(1):24–36. doi:10.1111/j.1708-8208.2008.00088.x

    PubMed  Google Scholar 

  • Talarico GM, Neiders ME, Comeau RL, Cohen RE (1997) Phenotypic characterization of mononuclear cells from gingiva associated with periodontitis and peri-implantitis. J Oral Implantol 23(1–2):5–11

    CAS  PubMed  Google Scholar 

  • Teronen O, Konttinen YT, Lindqvist C, Salo T, Ingman T, Lauhio A, Ding Y, Santavirta S, Sorsa T (1997) Human neutrophil collagenase MMP-8 in peri-implant sulcus fluid and its inhibition by clodronate. J Dent Res 76(9):1529–1537

    CAS  PubMed  Google Scholar 

  • Teughels W, Van Assche N, Sliepen I, Quirynen M (2006) Effect of material characteristics and/or surface topography on biofilm development. Clin Oral Implants Res 17(Suppl 2):68–81

    PubMed  Google Scholar 

  • Venza I, Visalli M, Cucinotta M, De Grazia G, Teti D, Venza M (2010) Proinflammatory gene expression at chronic periodontitis and peri-implantitis sites in patients with or without type 2 diabetes. J Periodontol 81(1):99–108. doi:10.1902/jop.2009.090358

    CAS  PubMed  Google Scholar 

  • Vieira AE, Moura CC, de Souza MA, Zanetta-Barbosa D, Dechichi P (2013) Would nitric oxide be an effective marker for earlier stages of peri-implant disease? An analysis in human peri-implant sulcular fluid. J Oral Implantol 39(1):37–43. doi:10.1563/AAID-JOI-D-11-00158

    PubMed  Google Scholar 

  • Wennstrom JL, Ekestubbe A, Grondahl K, Karlsson S, Lindhe J (2004) Oral rehabilitation with implant-supported fixed partial dentures in periodontitis-susceptible subjects. A 5-year prospective study. J Clin Periodontol 31(9):713–724

    PubMed  Google Scholar 

  • Wohlfahrt JC, Aass AM, Granfeldt F, Lyngstadaas SP, Reseland JE (2014) Sulcus fluid bone marker levels and the outcome of surgical treatment of peri-implantitis. J Clin Periodontol 41(4):424–431

    CAS  PubMed  Google Scholar 

  • Xu L, Yu Z, Lee HM, Wolff MS, Golub LM, Sorsa T, Kuula H (2008) Characteristics of collagenase-2 from gingival crevicular fluid and peri-implant sulcular fluid in periodontitis and peri-implantitis patients: pilot study. Acta Odontol Scand 66(4):219–224

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Zitzmann NU, Abrahamsson I, Berglundh T, Lindhe J (2002) Soft tissue reactions to plaque formation at implant abutments with different surface topography. An experimental study in dogs. J Clin Periodontol 29(5):456–461

    PubMed  Google Scholar 

  • Zitzmann NU, Berglundh T, Ericsson I, Lindhe J (2004) Spontaneous progression of experimentally induced periimplantitis. J Clin Periodontol 31(10):845–849

    CAS  PubMed  Google Scholar 

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Correspondence to Georgios N. Belibasakis .

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Belibasakis, G.N., Charalampakis, G., Bostanci, N., Stadlinger, B. (2015). Peri-Implant Infections of Oral Biofilm Etiology. 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_4

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