Skip to main content

Advertisement

Log in

From Periodontitis to Periimplantitis—the Quest for the Missing Link

  • Host Parasite Interactions in Periodontal Disease (C Genco and D Kinane, Section Editors)
  • Published:
Current Oral Health Reports Aims and scope Submit manuscript

Abstract

Purpose of Review

In this narrated review, we shall study the commonality and discord in the anatomy, bacterial flora, immune response, rate of progression, and response to therapy. Finally, we shall explore the unique, periimplantitis-related risk factors.

Recent Findings

The absence of PDL around implants, combined with poor periimplant vascularization and weaker attachment apparatus, might account for the poor cellular response to bacterial implant in periimplantitis. Using 16S ribosomal gene sequencing, it has been recently shown that although certain known periodontal pathogens may also be found around dental implants with periimplantitis, apparently, the multiplicity of bacterial flora in this condition is great with some distinct microorganisms associated with periimplantitis. The inflammatory cell infiltrate is more pronounced than in periodontitis and extended more apically. Mean bone loss in periimplantitis is generally much greater than around natural teeth with periodontitis. Risk factors that are uniquely associated with dental implants include bone type, prosthetic and surgical variables, and implant surface characteristics. The role of titanium particles found in the periimplantitis lesion is yet unclear. Lastly, the possibility of foreign body reaction being the trigger for periimplantitis is plausible but as of yet requires further substantiation.

Summary

The search to improve our treatment strategies in periimplantitis should first focus on establishing or declining the primary mode of breakdown. The results of such studies will help guide us to either improve our current anti-infective therapies targeting the unique characteristics of periimplantitis or else put us on a new road to understanding how to modify or restrict the natural immunological response as might be the case for a foreign body response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Levignac J. Periimplantation osteolysis- periimplantosis – periimplanti. Rev Fr Odontostomatol. 1965;12:1251–60.

    CAS  PubMed  Google Scholar 

  2. Meffert RM. Periodontitis vs. peri-implantitis: the same disease? The same treatment? Crit Rev Oral Biol Med. 1996;7:278–91.

    CAS  PubMed  Google Scholar 

  3. Cocchetto R, Canullo L, Celletti R. Infraposition of implant-retained maxillary incisor crown placed in an adult patient: case report. Int J Oral Maxillofac Implants. 2018;33:e107–11.

    PubMed  Google Scholar 

  4. Birdi H, Schulte J, Kovacs A, Weed M, Chuang SK. Crown-to-implant ratios of short-length implants. J Oral Implantol. 2010;36:425–33.

    PubMed  Google Scholar 

  5. Kat PS, Sampson WJ, Wilson DF, Wiebkin OW. Distribution of the epithelial rests of Malassez and their relationship to blood vessels of the periodontal ligament during rat tooth development. Aust Orthod J. 2003;19:77–86.

    PubMed  Google Scholar 

  6. Glauser R, Schüpbach P, Gottlow J, Hämmerle CH. Periimplant soft tissue barrier at experimental one-piece mini-implants with different surface topography in humans: a light-microscopic overview and histometric analysis. Clin Implant Dent Relat Res. 2005;7(Suppl 1):S44–51.

    PubMed  Google Scholar 

  7. Serino G, Ström C. Peri-implantitis in partially edentulous patients: association with inadequate plaque control. Clin Oral Implants Res. 2009;20:169–74.

    PubMed  Google Scholar 

  8. Ozgur GO, Kazancioglu HO, Demirtas N, Deger S, Ak G. Risk factors associated with implant marginal bone loss: a retrospective 6-year follow-up study. Implant Dent. 2016;25:122–7.

    PubMed  Google Scholar 

  9. Tuna T, Kuhlmann L, Bishti S, Sirazitdinova E, Deserno T, Wolfart S. Removal of simulated biofilm at different implant crown designs with interproximal oral hygiene aids: an in vitro study. Clin Oral Implants Res. 2019;30:627–36.

    PubMed  Google Scholar 

  10. De Bruyn H, Christiaens V, Doornewaard R, Jacobsson M, Cosyn J, Jacquet W, Vervaeke S. Implant surface roughness and patient factors on long-term peri-implant bone loss. Periodontol 2000 2017;73:218–27.

  11. Teughels W, Van Assche N, Sliepen I, Quirynen M. Effect of material characteristics and/or surface topography on biofilm development. Clin Oral Implants Res 2006;17Suppl2:68–81.

    PubMed  Google Scholar 

  12. Bahrami B, Shahrbaf S, Mirzakouchaki B, Ghalichi F, Ashtiani M, Martin N. Effect of surface treatment on stress distribution in immediately loaded dental implants--a 3D finite element analysis. Dent Mater. 2014;30:e89–97.

    CAS  PubMed  Google Scholar 

  13. Roy S, DAS M, Chakraborty P, Biswas JK, Chatterjee S, Khutia N, et al. Optimal selection of dental implant for different bone conditions based on the mechanical response. Acta Bioeng Biomech. 2017;19:11–20.

    PubMed  Google Scholar 

  14. Lee KH, Maiden MF, Tanner AC, Weber HP. Microbiota of successful osseointegrated dental implants. J Periodontol. 1999;70:131–8.

    CAS  PubMed  Google Scholar 

  15. Eke PI, Braswell LD, Fritz ME. Microbiota associated with experimental peri-implantitis and periodontitis in adult Macaca mulatta monkeys. J Periodontol. 1998;69:190–4.

    CAS  PubMed  Google Scholar 

  16. 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.

    PubMed  Google Scholar 

  17. Salvi GE, Fürst MM, Lang NP, Persson GR. One-year bacterial colonization patterns of Staphylococcus aureus and other bacteria at implants and adjacent teeth. Clin Oral Implants Res. 2008;19:242–8.

    PubMed  Google Scholar 

  18. Dabdoub SM, Tsigarida AA, Kumar PS. Patient-specific analysis of periodontal and peri-implant microbiomes. J Dent Res 2013;92(12 Suppl):S168–75. This study examines the microbial flora of neighboring teeth & implants.

    CAS  PubMed  PubMed Central  Google Scholar 

  19. 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;28:1521–9.

    PubMed  Google Scholar 

  20. Carcuac O, Berglundh T. Composition of human peri-implantitis and periodontitis lesions. J Dent Res 2014;93:1083–8. One of only few human biopsies to examine the immunopathology of periimplantitis.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Ghighi M, Llorens A, Baroukh B, Chaussain C, Bouchard P, Gosset M. Differences between inflammatory and catabolic mediators of peri-implantitis and periodontitis lesions following initial mechanical therapy: an exploratory study. J Periodontal Res. 2018;53:29–39.

    CAS  PubMed  Google Scholar 

  22. Berglundh T, Zitzmann NU, Donati M. Are peri-implantitis lesions different from periodontitis lesions? J Clin Periodontol. 2011;38(Suppl 11):188–202.

    PubMed  Google Scholar 

  23. Machtei EE, Dunford R, Hausmann E, Grossi SG, Powell J, Cummins D, et al. Longitudinal study of prognostic factors in established periodontitis patients. J Clin Periodontol. 1997;24:102–9.

    CAS  PubMed  Google Scholar 

  24. Onabolu O, Donos N, Tu YK, Darbar U, Nibali L. Periodontal progression based on radiographic records: an observational study in chronic and aggressive periodontitis. J Dent. 2015;43:673–82.

    PubMed  Google Scholar 

  25. Papapanou PN. Patterns of alveolar bone loss in the assessment of periodontal treatment priorities. Swed Dent J 1989;66:Suppl1–45.

  26. Machtei EE, Norderyd J, Koch G, Dunford R, Grossi S, Genco RJ. The rate of periodontal attachment loss in subjects with established periodontitis. J Periodontol. 1993;64:713–8.

    CAS  PubMed  Google Scholar 

  27. Needleman I, Garcia R, Gkranias N, Kirkwood KL, Kocher T, Iorio AD, Moreno F, Petrie A. Mean annual attachment, bone level, and tooth loss: a systematic review. J Clin Periodontol 2018;45 Suppl20:S112–29.

    PubMed  Google Scholar 

  28. Brown LF, Beck JD, Rozier RG. Incidence of attachment loss in community-dwelling older adults. J Periodontol. 1994;65:316–23.

    CAS  PubMed  Google Scholar 

  29. Berglundh T, Gotfredsen K, Zitzmann NU, Lang NP, Lindhe J. Spontaneous progression of ligature induced peri-implantitis at implants with different surface roughness: an experimental study in dogs. Clin Oral Implants Res. 2007;18:655–61.

    CAS  PubMed  Google Scholar 

  30. Derks J, Schaller D, Håkansson J, Wennström 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.

    CAS  PubMed  Google Scholar 

  31. Karlsson K, Derks J, Håkansson J, Wennström JL, Petzold M, Berglundh T. Interventions for peri-implantitis and their effects on further bone loss: a retrospective analysis of a registry-based cohort. J Clin Periodontol. 2019;46:872–9.

    PubMed  Google Scholar 

  32. Jemt T, Sundén Pikner S, Gröndahl K. Changes of marginal bone level in patients with “progressive bone loss” at Brånemark System® Implants: a radiographic follow-up study over an average of 9 years. Clin Implant Dent Relat Res 2015;17:619–28. A long-term follow-up of large cohort of treated patients showing little merit for surgical or non-surgical interventions.

    PubMed  Google Scholar 

  33. Garrett S, Johnson L, Drisko CH, Adams DF, Bandt C, Beiswanger B, et al. Two multi-center studies evaluating locally delivered doxycycline hyclate, placebo control, oral hygiene, and scaling and root planing in the treatment of periodontitis. J Periodontol. 1999;70:490–503.

    CAS  PubMed  Google Scholar 

  34. Polson AM, Stoller NH, Hanes PJ, Bandt CL, Garrett S, Southard GL. 2 multi-center trials assessing the clinical efficacy of 5% sanguinarine in a biodegradable drug delivery system. J Clin Periodontol. 1996;23:782–8.

    CAS  PubMed  Google Scholar 

  35. Walsh MM, Buchanan SA, Hoover CI, Newbrun E, Taggart EJ, Armitage GC, et al. Clinical and microbiologic effects of single-dose metronidazole or scaling and root planing in treatment of adult periodontitis. J Clin Periodontol. 1986;13:151–7.

    CAS  PubMed  Google Scholar 

  36. Griffiths GS, Smart GJ, Bulman JS, Weiss G, Shrowder J, Newman HN. Comparison of clinical outcomes following treatment of chronic adult periodontitis with subgingival scaling or subgingival scaling plus metronidazole gel. J Clin Periodontol. 2000;27:910–7.

    CAS  PubMed  Google Scholar 

  37. Paolantonio M, D’Ercole S, Pilloni A, D’Archivio D, Lisanti L, Graziani F, et al. Clinical, microbiologic, and biochemical effects of subgingival administration of a xanthan-based chlorhexidine gel in the treatment of periodontitis: a randomized multicenter trial. J Periodontol. 2009;80:1479–92.

    CAS  PubMed  Google Scholar 

  38. Hung HC, Douglass CW. Meta-analysis of the effect of scaling and root planing, surgical treatment and antibiotic therapies on periodontal probing depth and attachment loss. J Clin Periodontol. 2002;29:975–86.

    PubMed  Google Scholar 

  39. Roos-Jansåker AM, Almhöjd US, Jansson H. Treatment of peri-implantitis: clinical outcome of chloramine as an adjunctive to non-surgical therapy, a randomized clinical trial. Clin Oral Implants Res. 2017;28:43–8.

    PubMed  Google Scholar 

  40. Suárez-López Del Amo F, Yu SH, Wang HL. Non-surgical therapy for peri-implant diseases: a systematic review. J Oral Maxillofac Res. 2016;7:e13.

    PubMed  PubMed Central  Google Scholar 

  41. Becker W, Becker BE, Ochsenbein C, Kerry G, Caffesse R, Morrison EC, et al. A longitudinal study comparing scaling, osseous surgery and modified Widman procedures. Results after one year. J Periodontol. 1988;59:351–65.

    CAS  PubMed  Google Scholar 

  42. Isidor F, Karring T, Attström R. The effect of root planing as compared to that of surgical treatment. J Clin Periodontol. 1984;11:669–81.

    CAS  PubMed  Google Scholar 

  43. Kaldahl WB, Kalkwarf KL, Patil KD, Molvar MP, Dyer JK. Long-term evaluation of periodontal therapy: I. response to 4 therapeutic modalities. J Periodontol. 1996;67:93–102.

    CAS  PubMed  Google Scholar 

  44. Graziani F, Gennai S, Cei S, Cairo F, Baggiani A, Miccoli M, et al. Clinical performance of access flap surgery in the treatment of the intrabony defect. A systematic review and meta-analysis of randomized clinical trials. J Clin Periodontol. 2012;39:145–56.

    PubMed  Google Scholar 

  45. Needleman I, Worthington HV, Giedrys-Leeper E, Tucker R. Guided tissue regeneration for periodontal infra-bony defects. Cochrane Database Syst Rev. 2006;2:CD001724.

    Google Scholar 

  46. De Bartolo AM, Veitz-Keenan A. Inconclusive evidence of treatment modalities for peri-implantitis. Evid Based Dent 2019;20:24–5. This meta-analysis shows that the outcomes of the currently available surgical interventions for periimplantitis remain unpredictable, including regenerative techniques.

    PubMed  Google Scholar 

  47. Oliver RC, Tervonen T. Diabetes--a risk factor for periodontitis in adults? J Periodontol. 1994;65(5 Suppl):530–8.

    CAS  PubMed  Google Scholar 

  48. Heitz-Mayfield LJ. Peri-implant diseases: diagnosis and risk indicators. J Clin Periodontol. 2008;35(8 Suppl):292–304.

    PubMed  Google Scholar 

  49. Eke PI, Wei L, Thornton-Evans GO, Borrell LN, Borgnakke WS, Dye B, et al. Risk indicators for periodontitis in US adults: NHANES 2009 to 2012. J Periodontol. 2016;87:1174–85.

    PubMed  Google Scholar 

  50. Dreyer H, Grischke J, Tiede C, Eberhard J, Schweitzer A, Toikkanen SE, et al. Epidemiology and risk factors of peri-implantitis: a systematic review. J Periodontal Res. 2018;53:657–81.

    CAS  PubMed  Google Scholar 

  51. Dalago HR, Schuldt Filho G, Rodrigues MA, Renvert S, Bianchini MA. Risk indicators for peri-implantitis. A cross-sectional study with 916 implants. Clin Oral Implants Res. 2017;28:144–50.

    PubMed  Google Scholar 

  52. Machtei EE, Hausmann E, Dunford R, Grossi S, Ho A, Davis G, et al. Longitudinal study of predictive factors for periodontal disease and tooth loss. J Clin Periodontol. 1999;26:374–80.

    CAS  PubMed  Google Scholar 

  53. Kröger A, Hülsmann C, Fickl S, Spinell T, Hüttig F, Kaufmann F, et al. The severity of human peri-implantitis lesions correlates with the level of submucosal microbial dysbiosis. J Clin Periodontol. 2018;45:1498–509.

    PubMed  Google Scholar 

  54. Jemt T, Karouni M, Abitbol J, Zouiten O, Antoun H. A retrospective study on 1592 consecutively performed operations in one private referral clinic. Part II: Peri-implantitis and implant failures. Clin Implant Dent Relat Res. 2017;19:413–22.

    PubMed  Google Scholar 

  55. Pesce P, Canullo L, Grusovin MG, de Bruyn H, Cosyn J, Pera P. Systematic review of some prosthetic risk factors for periimplantitis. J Prosthet Dent. 2015;114:346–50.

    PubMed  Google Scholar 

  56. Canullo L, Tallarico M, Radovanovic S, Delibasic B, Covani U, Rakic M. Distinguishing predictive profiles for patient-based risk assessment and diagnostics of plaque induced, surgically and prosthetically triggered peri-implantitis. Clin Oral Implants Res. 2016;27:1243–50.

    PubMed  Google Scholar 

  57. Doornewaard R, Christiaens V, De Bruyn H, Jacobsson M, Cosyn J, Vervaeke S, et al. Long-term effect of surface roughness and Patients’ factors on crestal bone loss at dental implants. A systematic review and meta-analysis. Clin Implant Dent Relat Res. 2017;19:372–99.

    PubMed  Google Scholar 

  58. Suárez-López Del Amo F, Garaicoa-Pazmiño C, Fretwurst T, Castilho RM, Squarize CH. Dental implants-associated release of titanium particles: a systematic review. Clin Oral Implants Res. 2018 Oct 2. https://doi.org/10.1111/clr.13372[Epub ahead of print].

    Google Scholar 

  59. Kumazawa R1, Watari F, Takashi N, Tanimura Y, Uo M, Totsuka Y. Effects of Ti ions and particles on neutrophil function and morphology. Biomaterials 2002;23:3757–3764.

    CAS  PubMed  Google Scholar 

  60. Wachi T, Shuto T, Shinohara Y, Matono Y, Makihira S. Release of titanium ions from an implant surface and their effect on cytokine production related to alveolar bone resorption. Toxicology. 2015;327:1–9.

    CAS  PubMed  Google Scholar 

  61. Mombelli A, Hashim D, Cionca N. What is the impact of titanium particles and biocorrosion on implant survival and complications? A critical review. Clin Oral Implants Res 2018;29Suppl18:37–53.

    PubMed  Google Scholar 

  62. Albrektsson T, Dahlin C, Jemt T, Sennerby L, Turri A, Wennerberg A. Is marginal bone loss around oral implants the result of a provoked foreign body reaction? Clin Implant Dent Relat Res 2014;16:155–65. In this narrated review, the authors laid the grounds for the foreign body reaction theory as the primary etiology for periimplantitis.

    PubMed  Google Scholar 

  63. Wilson TG Jr, Valderrama P, Burbano M, Blansett J, Levine R, Kessler H, Rodrigues DC. Foreign bodies associated with peri-implantitis human biopsies. J Periodontol 2015;86:9–15. Found (under SEM) that titanium particles cement particles surrounded by inflammatory cells in periimplantitis sites.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Eli E. Machtei.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any authors.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Topical Collection on Host Parasite Interactions in Periodontal Disease

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Machtei, E.E. From Periodontitis to Periimplantitis—the Quest for the Missing Link. Curr Oral Health Rep 7, 72–78 (2020). https://doi.org/10.1007/s40496-020-00252-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40496-020-00252-8

Keywords

Navigation