Peri-Implantitis: A Clinical Update on Prevalence and Surgical Treatment Outcomes

Andrea Roccuzzo, Alexandra Stähli, Alberto Monje, Anton Sculean, Giovanni E Salvi, Andrea Roccuzzo, Alexandra Stähli, Alberto Monje, Anton Sculean, Giovanni E Salvi

Abstract

Dental implants may be considered a reliable routine procedure in clinical practice for the replacement of missing teeth. Results from long-term studies indicate that implant-supported dental prostheses constitute a predictable treatment method for the management of fully and partially edentulous patients. Implants and their restorations, however, are not free from biological complications. In fact, peri-implantitis, defined as progressive bone loss associated to clinical inflammation, is not a rare finding nowadays. This constitutes a concern for clinicians and patients given the negative impact on the quality of life and the sequelae originated by peri-implantitis lesions. The purpose of this narrative review is to report on the prevalence of peri-implantitis and to overview the indications, contraindications, complexity, predictability and effectiveness of the different surgical therapeutic modalities to manage this disorder.

Keywords: biological complications; bone regeneration; dental implants; peri-implantitis.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
(a) Mandibular left premolar implant showing an increase in probing pocket depth as compared with previous records, bleeding and pus exhibiting shortly after probing. Note, the shallow vestibulum at the buccal aspect of the infected implant; (b) Radiographic image revealing significant bone loss. Note, the remaining particles of an anorganic bovine bone previously used for grafting; (c) Intra-operative appearance of the peri-implant infra-osseous defect after debridement. Note, the remaining particles of an anorganic bovine bone previously used for grafting simultaneously at implant placement stage.
Figure 2
Figure 2
(a) Clinical appearance of implants placed in bone augmented with anorganic bovine bone and autogenous bone 5 years after placement in a smoker patient. Note, the poor plaque control and the inadequate prosthesis design that precluded adequate self-performed oral hygiene measures; (b) Intra-operative appearance of the peri-implant defects after debridement. Note, the predominant horizontal pattern of bone resorption.
Figure 3
Figure 3
(a) Clinical appearance at several implant-supported fixed prosthesis involved affected of advanced peri-implantitis; (b) clinical probing indicates advanced attachment loss; (c) implant removal is suggested in advanced forms of peri-implantitis.
Figure 4
Figure 4
(a) Clinical presentation of peri-implantitis; (b) Access flap reveals moderate bone loss (<50%) (frontal view). Note the supra-crestal defect morphology; (c) Occlusal view of moderate bone loss; (d) Implantoplasty was performed as adjunct to the surgical resective therapy of peri-implantitis (frontal view); (e) Occlusal view of the implantoplasty and bone topography after osteoplasty to reach a flat bone architecture; (f) clinical resolution of peri-implantitis at 6-month follow-up; (g) bone stability is noted upon radiographic assessment.
Figure 5
Figure 5
(a) Mandibular right premolar implant installed in pristine bone showing increased probing pocket depth as compared with previous records, bleeding and pus exhibiting shortly after probing; (b) Intra-operative appearance of the peri-implant infra-osseous defect after debridement; (c) Anorganic bovine bone mineral with 10% collagen is applied in the infra-osseous component; (d) Six-month follow-up after non-submerged healing, no signs of inflammation and peri-implant probing depth was noted to be consistent with health; (e) One-year follow-up after delivery of the final restoration. Note, peri-implant stability; (f) Radiographic image, at 1-year follow-up, reveals substantial bone fill.
Figure 6
Figure 6
(a) Clinical presentation of peri-implantitis; (b) Radiographic image compatible showing moderate (<50%) bone loss; (c) Inadequate prosthesis emergence profile; (d) Partial-thickness apical position flap; (e) Soft tissue conditioning by means of free epithelial graft; (f) Prosthesis contour modification to facilitate proximal access during self-performed oral hygiene; (g) Clinical resolution of peri-implantitis associated with a gain of keratinized mucosa.
Figure 6
Figure 6
(a) Clinical presentation of peri-implantitis; (b) Radiographic image compatible showing moderate (<50%) bone loss; (c) Inadequate prosthesis emergence profile; (d) Partial-thickness apical position flap; (e) Soft tissue conditioning by means of free epithelial graft; (f) Prosthesis contour modification to facilitate proximal access during self-performed oral hygiene; (g) Clinical resolution of peri-implantitis associated with a gain of keratinized mucosa.

References

    1. Berglundh T., Armitage G., Araujo M.G., Gustavo A.-O., Juan B., Paulo M.C., Stephen C., David C., Jan D., Elena F., 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:S313–S318. doi: 10.1002/JPER.17-0739.
    1. Derks J., Schaller D., Håkansson J., Wennström J.L., Tomasi C., Berglundh T. Effectiveness of implant therapy analyzed in a Swedish population: Prevalence of peri-implantitis. J. Dent. Res. 2016;95:43–49. doi: 10.1177/0022034515608832.
    1. Derks J., Tomasi C. Peri-implant health and disease. A systematic review of current epidemiology. J. Clin. Periodontol. 2015;42:S158–S171. doi: 10.1111/jcpe.12334.
    1. Aguirre-Zorzano L.A., Estefania-Fresco R., Telletxea O., Bravo M. Prevalence of peri-implant inflammatory disease in patients with a history of periodontal disease who receive supportive periodontal therapy. Clin. Oral Implant Res. 2015;26:1338–1344. doi: 10.1111/clr.12462.
    1. Daubert D.M., Weinstein B.F., Bordin S., Leroux B.G., Flemming T.F. Prevalence and predictive factors for peri-implant disease and implant failure: A cross-sectional analysis. J. Periodontol. 2015;86:337–347. doi: 10.1902/jop.2014.140438.
    1. Konstantinidis I.K., Kotsakis G.A., Gerdes S., Walter M.H. Cross-sectional study on the prevalence and risk indicators of peri-implant diseases. Eur. J. Oral Implantol. 2015;8:75–88.
    1. Dalago H.R., Schuldt Filho G., Rodrigues M.A., Renvert S., Bianchini M.A. Risk indicators for peri-implantitis. A cross-sectional study with 916 implants. Clin. Oral Implant Res. 2017;28:144–150. doi: 10.1111/clr.12772.
    1. Monje A., Wang H.L., Nart J. Association of preventive maintenance therapy compliance and peri-implant diseases: A cross-sectional study. J. Periodontol. 2017;88:1030–1041. doi: 10.1902/jop.2017.170135.
    1. Rokn A., Aslroosta H., Akbari S., Najafi H., Zayeri F., Hashemi K. Prevalence of peri-implantitis in patients not participating in well-designed supportive periodontal treatments: A cross-sectional study. Clin. Oral Implant Res. 2017;28:314–319. doi: 10.1111/clr.12800.
    1. Schwarz F., Becker K., Sahm N., Horstkemper T., Rousi K., Becker J. The prevalence of peri-implant diseases for two-piece implants with an internal tube-in-tube connection: A cross-sectional analysis of 512 implants. Clin. Oral Implant Res. 2017;28:24–28. doi: 10.1111/clr.12609.
    1. Buser D., Chappuis V., Kuchler U., Bornstein M.M., Wittneben J.G., Buser R., Cavusoglu Y., Belser U.C. Long-term stability of early implant placement with contour augmentation. J. Dent. Res. 2013;92:176S–182S. doi: 10.1177/0022034513504949.
    1. Jung R.E., Benic G.I., Scherrer D., Hammerle C.H. Cone beam computed tomography evaluation of regenerated buccal bone 5 years after simultaneous implant placement and guided bone regeneration procedures—A randomized, controlled clinical trial. Clin. Oral Implant Res. 2015;26:28–34. doi: 10.1111/clr.12296.
    1. Elnayef B., Monje A., Gargallo-Albiol J., Galindo-Moreno P., Wang H.L., Hernández-Alfaro F. Vertical ridge augmentation in the atrophic mandible: A systematic review and meta-analysis. Int. J. Oral Maxillofac. Implant. 2017;32:291–312. doi: 10.11607/jomi.4861.
    1. Chappuis V., Cavusoglu Y., Buser D., von Arx T. Lateral ridge augmentation using autogenous block grafts and guided bone regeneration: A 10-year prospective case series study. Clin. Implant Dent. Relat. Res. 2017;19:85–96. doi: 10.1111/cid.12438.
    1. Urban I.A., Monje A., Nevins M., Nevins M.L., Lozada J., Wang H.L. Surgical management of significant maxillary anterior vertical ridge defects. Int. J. Periodont. Restor. Dent. 2016;36:329–337. doi: 10.11607/prd.2644.
    1. Tran D.T., Gay I.C., Diaz-Rodriguez J., Parthasarathy K., Weltman R., Friedman L. Survival of dental implants placed in grafted and nongrafted bone: A retrospective study in a university setting. Int. J. Oral Maxillofac. Implant. 2016;31:310–317. doi: 10.11607/jomi.4681.
    1. Visser A., Stellingsma C., Raghoebar G.M., Meijer H.J., Vissink A. A 15-year comparative prospective study of surgical and prosthetic care and aftercare of overdenture treatment in the atrophied mandible: Augmentation versus nonaugmentation. Clin. Implant Dent. Relat. Res. 2016;18:1218–1226. doi: 10.1111/cid.12386.
    1. Ramanauskaite A., Borges T., Almeida B.L., Correia A. Dental Implant Outcomes in Grafted Sockets: A Systematic Review and Meta-Analysis. J. Oral Maxillofac. Res. 2019;10 doi: 10.5037/jomr.2019.10308.
    1. Carcuac O., Abrahamsson I., Derks J., Petzold M., Berglundh T. Spontaneous progression of experimental peri-implantitis in augmented and pristine bone: A pre-clinical in vivo study. Clin. Oral Implant Res. 2020;31:192–200. doi: 10.1111/clr.13564.
    1. Jemt T. Implant Survival in the Edentulous Jaw-30 Years of Experience. Part I: A Retro-Prospective Multivariate Regression Analysis of Overall Implant Failure in 4,585 Consecutively Treated Arches. Int. J. Prosthodont. 2018;31:425–435. doi: 10.11607/ijp.5875.
    1. Pontoriero R., Tonelli M.P., Carnevale G., Mombelli A., Nyman S.R., Lang N.P. Experimentally induced peri-implant mucositis. A clinical study in humans. Clin. Oral Implant Res. 1994:254–259. doi: 10.1034/j.1600-0501.1994.050409.x.
    1. Zitzmann N.U., Berglundh T., Marinello C.P., Lindhe J. Experimental peri-implant mucositis in man. J. Clin. Periodontol. 2001;28:517–523. doi: 10.1034/j.1600-051x.2001.028006517.x.
    1. Salvi G.E., Aglietta M., Eick S., Sculean A., Lang N.P., Ramseier C.A. Reversibility of experimental peri-implant mucositis compared with experimental gingivitis in humans. Clin. Oral Implant Res. 2012;23:182–190. doi: 10.1111/j.1600-0501.2011.02220.x.
    1. Renvert S., Lindahl C., Persson G.R. Occurrence of cases with peri-implant mucositis or peri-implantitis in a 21–26 years follow-up study. J. Clin. Periodontol. 2018;45:233–240. doi: 10.1111/jcpe.12822.
    1. Zetterqvist L., Feldman S., Rotter B., Vincenzi G., Wennstrom J.L., Chierico A., Kenealy J.N. A prospective, multicenter, randomized-controlled 5-year study of hybrid and fully etched implants for the incidence of peri-implantitis. J. Periodontol. 2010;81:493–501. doi: 10.1902/jop.2009.090492.
    1. Koldsland O.C., Scheie A.A., Aass A.M. Prevalence of peri-implantitis related to severity of the disease with different degrees of bone loss. J. Periodontol. 2010;81:231–238. doi: 10.1902/jop.2009.090269.
    1. Sanz M., Chapple I.L., Working Group 4 of the VIII European Workshop on Periodontology Clinical research on peri-implant diseases: Consensus report of Working Group 4. J. Clin. Periodontol. 2012;39:202–206. doi: 10.1111/j.1600-051X.2011.01837.x.
    1. Leblebicioglu B., Hegde R., Yildiz V.O., Tatakis D.N. Immediate effects of tooth extraction on ridge integrity and dimensions. Clin. Oral Investig. 2015;19:1777–1784. doi: 10.1007/s00784-014-1392-1.
    1. Salvi G.E., Monje A., Tomasi C. Long-term biological complications of dental implants placed either in pristine or in augmented sites: A systematic review and meta-analysis. Clin. Oral Implant Res. 2018;29:294–310. doi: 10.1111/clr.13123.
    1. Roccuzzo M., Bonino L., Dalmasso P., Aglietta M. Long-term results of a three arms prospective cohort study on implants in periodontally compromised patients: 10-year data around sandblasted and acid-etched (SLA) surface. Clin. Oral Implant Res. 2014;25:1105–1112. doi: 10.1111/clr.12227.
    1. Tenenbaum H., Bogen O., Séverac F., Elkaim R., Davideau J.L., Huck O. Long-term prospective cohort study on dental implants: Clinical and microbiological parameters. Clin. Oral Implant Res. 2017;28:86–94. doi: 10.1111/clr.12764.
    1. Roccuzzo A., De Ry S., Sculean A., Roccuzzo M., Salvi G.E. Current approaches for the non-surgical management of peri-implant diseases. Curr. Oral Health Rep. 2020 doi: 10.1007/s40496-020-00279-x.
    1. De Ry S.P., Roccuzzo A., Sculean A., Salvi G.E. Nichtchirurgische Therapie periimplantärer Erkrankungen. Implantologie. 2020;28:117–127.
    1. Schwarz F., Schmucker A., Becker J. Efficacy of alternative or adjunctive measures to conventional treatment of peri-implant mucositis and peri-implantitis: A systematic review and meta-analysis. Int. J. Implant Dent. 2015;22 doi: 10.1186/s40729-015-0023-1.
    1. Heitz-Mayfield L.J.A., Salvi G.E., Mombelli A., Loup P.J., Heitz F., Kruger E., Lang N.P. Supportive peri-implant therapy following anti-infective surgical peri-implantitis treatment: 5-year survival and success. Clin. Oral Implant Res. 2018;29:1–6. doi: 10.1111/clr.12910.
    1. Roccuzzo M., Layton D.M., Roccuzzo A., Heitz-Mayfield L.J. Clinical outcomes of peri-implantitis treatment and supportive care: A systematic review. Clin. Oral Implant Res. 2018;29:331–350. doi: 10.1111/clr.13287.
    1. Carcuac O., Derks J., Abrahamsson I., Wennström J.L., Berglundh T. Risk for recurrence of disease following surgical therapy of peri-implantitis-A prospective longitudinal study. Clin. Oral Implant Res. 2020;31:1072–1077. doi: 10.1111/clr.13653.
    1. Berglundh T., Wennström J.L., Lindhe J. Long-term outcome of surgical treatment of peri-implantitis. A 2-11-year retrospective study. Clin. Oral Implant Res. 2018;29:404–410. doi: 10.1111/clr.13138.
    1. Roccuzzo M., Pittoni D., Roccuzzo A., Charrier L., Dalmasso P. Surgical treatment of peri-implantitis intrabony lesions by means of deproteinized bovine bone mineral with 10% collagen: 7-year-results. Clin. Oral Implant Res. 2017;28:1577–1583. doi: 10.1111/clr.13028.
    1. Roccuzzo M., Fierravanti L., Pittoni D., Dalmasso P., Roccuzzo A. Implant survival after surgical treatment of peri-implantitis lesions by means of deproteinized bovine bone mineral with 10% collagen: 10-year results from a prospective study. Clin. Oral Implant Res. 2020;31:768–776. doi: 10.1111/clr.13628.
    1. Parma-Benfenati S., Tinti C., Romano F., Roncati M., Aimetti M. Long-Term Outcome of Surgical Regenerative Treatment of Peri-implantitis: A 2- to 21-Year Retrospective Evaluation. Int. J. Periodont. Restor. Dent. 2020;40:487–496. doi: 10.11607/prd.4647.
    1. Romeo E., Lops D., Chiapasco M., Ghisolfi M., Vogel G. Therapy of peri-implantitis with resective surgery. A 3-year clinical trial on rough screw-shaped oral implants. Part II: Radiographic outcome. Clin. Oral Implant Res. 2007;18:179–187. doi: 10.1111/j.1600-0501.2006.01318.x.
    1. Bianchini M.A., Galarraga-Vinueza M.E., Apaza-Bedoya K., De Souza J.M., Magini R., Schwarz F. Two to six-year disease resolution and marginal bone stability rates of a modified resective-implantoplasty therapy in 32 peri-implantitis cases. Clin. Implant Dent. Relat. Res. 2019;21:758–765. doi: 10.1111/cid.12773.
    1. Lasserre J.F., Brecx M.C., Toma S. Implantoplasty Versus Glycine Air Abrasion for the Surgical Treatment of Peri-implantitis: A Randomized Clinical Trial. Int. J. Oral Maxillofac. Implant. 2020;35:197–206. doi: 10.11607/jomi.6677.
    1. Stavropoulos A., Bertl K., Eren S., Gotfredsen K. Mechanical and biological complications after implantoplasty-A systematic review. Clin. Oral Implant Res. 2019;30:833–848. doi: 10.1111/clr.13499.
    1. Persson L.G., Berglundh T., Lindhe J., Sennerby L. Re-osseointegration after treatment of peri-implantitis at different implant surfaces. An experimental study in the dog. Clin. Oral Implant Res. 2001;12:595–603. doi: 10.1034/j.1600-0501.2001.120607.x.
    1. Fletcher P., Deluiz D., Tinoco E.M., Ricci J.L., Tarnow D.P., Tinoco J.M. Human Histologic Evidence of Reosseointegration Around an Implant Affected with Peri- implantitis Following Decontamination with Sterile Saline and Antiseptics: A Case History Report. Int. J. Periodont. Restor. Dent. 2017;37:499–508. doi: 10.11607/prd.3037.
    1. Behneke A., Behneke N., d’Hoedt B. Treatment of peri-implantitis defects with autogenous bone grafts: Six-month to 3-year results of a prospective study in 17 patients. Int. J. Oral Maxillofac. Implant. 2000;15:125–138.
    1. Khoury F., Buchmann R. Surgical therapy of peri-implant disease: A 3-year follow-up study of cases treated with 3 different techniques of bone regeneration. J. Periodontol. 2001;72:1498–1508. doi: 10.1902/jop.2001.72.11.1498.
    1. Roos-Jansåker A.M., Renvert H., Lindahl C., Renvert S. Surgical treatment of peri-implantitis using a bone substitute with or without a resorbable membrane: A prospective cohort study. J. Clin. Periodontol. 2007;34:625–632. doi: 10.1111/j.1600-051X.2007.01102.x.
    1. Schwarz F., Sculean A., Bieling K., Ferrari D., Rothamel D., Becker J. Two-year clinical results following treatment of peri-implantitis lesions using a nanocrystalline hydroxyapatite or a natural bone mineral in combination with a collagen membrane. J. Clin. Periodontol. 2008;35:80–87. doi: 10.1111/j.1600-051X.2007.01168.x.
    1. Schwarz F., Sahm N., Schwarz K., Becker J. Impact of defect configuration on the clinical outcome following surgical regenerative therapy of peri-implantitis. J. Clin. Periodontol. 2010;37:449–455. doi: 10.1111/j.1600-051X.2010.01540.x.
    1. Roccuzzo M., Bonino F., Bonino L., Dalmasso P. Surgical therapy of peri-implantitis lesions by means of a bovine-derived xenograft: Comparative results of a prospective study on two different implant surfaces. J. Clin. Periodontol. 2011;28:738–745. doi: 10.1111/j.1600-051X.2011.01742.x.
    1. Aghazadeh A., Persson R.G., Renvert S. A single-centre randomized controlled clinical trial on the adjunct treatment of intra-bony defects with autogenous bone or a xenograft: Results after 12 months. J. Clin. Periodontol. 2012;39:666–673. doi: 10.1111/j.1600-051X.2012.01880.x.
    1. Roccuzzo M., Gaudioso L., Lungo M., Dalmasso P. Surgical therapy of single peri-implantitis intrabony defects, by means of deproteinized bovine bone mineral with 10% collagen. J. Clin. Periodontol. 2016;43:311–318. doi: 10.1111/jcpe.12516.
    1. Renvert S., Roos-Jansaker A.M., Persson G.R. Surgical treatment of peri-implantitis lesions with or without the use of a bone substitute-a randomized clinical trial. J. Clin. Periodontol. 2018;45:1266–1274. doi: 10.1111/jcpe.12986.
    1. Tomasi C., Regidor E., Ortiz-Vigón A., Derks J. Efficacy of reconstructive surgical therapy at peri-implantitis-related bone defects. A systematic review and meta-analysis. J. Clin. Periodontol. 2019;46:340–356. doi: 10.1111/jcpe.13070.
    1. Isehed C., Holmlund A., Renvert S., Svenson B., Johansson I., Lundberg P. Effectiveness of enamel matrix derivative on the clinical and microbiological outcomes following surgical regenerative treatment of peri-implantitis. A randomized controlled trial. J. Clin. Periodontol. 2016;43:863–873. doi: 10.1111/jcpe.12583.
    1. Wohlfahrt J.C., Lyngstadaas S.P., Rønold H.J., Saxegaard E., Ellingsen J.E., Karlsson S., Aass A.M. Porous titanium granules in the surgical treatment of peri-implant osseous defects: A randomized clinical trial. Int. J. Oral Maxillofac. Implant. 2012;27:401–410.
    1. Jepsen K., Jepsen S., Laine M.L., Anssari Moin D., Pilloni A., Zeza B., Sanz M., Ortiz-Vigon A., Roos-Jansåker A.M., Renvert S. Reconstruction of Peri-implant Osseous Defects: A Multicenter Randomized Trial. J. Dent. Res. 2016;95:58–66. doi: 10.1177/0022034515610056.
    1. Matarasso S., Iorio Siciliano V., Aglietta M., Andreuccetti G., Salvi G.E. Clinical and radiographic outcomes of a combined resective and regenerative approach in the treatment of peri-implantitis: A prospective case series. Clin. Oral Implant Res. 2014;25:761–767. doi: 10.1111/clr.12183.
    1. Schwarz F., John G., Schmucker A., Sahm N., Becker J. Combined surgical therapy of advanced peri-implantitis evaluating two methods of surface decontamination: A 7-year follow-up observation. J. Clin. Periodontol. 2017;44:337–342. doi: 10.1111/jcpe.12648.
    1. Monje A., Pons R., Roccuzzo A., Salvi G.E., Nart J. Reconstructive therapy for the management of peri-implantitis via submerged guided bone regeneration: A prospective case series. Clincal Implant Dent. Relat. Res. 2020;22:342–350. doi: 10.1111/cid.12913.
    1. Roccuzzo M., Dalmasso P., Pittoni D., Roccuzzo A. Treatment of buccal soft tissue dehiscence around single implant: 5-year results from a prospective study. Clin. Oral Investig. 2019;23:1977–1983. doi: 10.1007/s00784-018-2634-4.
    1. Monje A., Blasi G. Significance of keratinized mucosa/gingiva on peri-implant and adjacent periodontal conditions in erratic maintenance compliers. J. Periodontol. 2019;5:445–453. doi: 10.1002/JPER.18-0471.
    1. Roccuzzo M., Grasso G., Dalmasso P. Keratinized mucosa around implants in partially edentulous posterior mandible: 10-year results of a prospective comparative study. Clin. Oral. Implant Res. 2016;4:491–496. doi: 10.1111/clr.12563.
    1. Ravidà A., Saleh I., Siqueira R., Garaicoa-Pazmiño C., Saleh M.H.A., Monje A., Wang H.L. Influence of keratinized mucosa on the surgical therapeutical outcomes of peri-implantitis. J. Clin. Periodontol. 2020;4:529–539. doi: 10.1111/jcpe.13250.
    1. Monje A., Blasi G., Nart J., Urban I.A., Nevins M., Wang H.L. Soft Tissue Conditioning for the Surgical Therapy of Peri-implantitis: A Prospective 12-Month Study. Int. J. Periodont. Restor. Dent. 2020;6:899–906. doi: 10.11607/prd.4554.

Source: PubMed

3
Suscribir