Skip to main content

Advertisement

Log in

Evaluation of a novel dog animal model for peri-implant disease: clinical, radiographic, microbiological and histological assessment

  • Original Article
  • Published:
Clinical Oral Investigations Aims and scope Submit manuscript

Abstract

Objective

To assess longitudinal peri-implant tissue evaluation in a plaque compromised ligature free dog model, clinically, radiographically, microbiologically and histologically.

Materials and methods

Six beagle mandibular premolars and first molars were extracted. Plaque accumulated for 16 weeks. Two implants were placed per hemi-mandible. For 17 weeks, control implants (CI) in one hemi-mandible were brushed daily; test implants (TI) in the other were not. These parameters were then assessed: clinically, probing depth (PD), bleeding-on-probing (BOP), presence of plaque (PP) and clinical attachment level (CAL); radiographically, marginal bone level; microbiologically, counts for Streptococcus spp., Fusobacterium spp., Porphyromonas gingivalis, Aggregatibacter actinomycetemcomitans, Prevotella intermedia and total bacterial load. At week 17, histomorphometric analysis was performed (MM-ISH (mucosal margin–implant shoulder); ISH-fBIC (implant shoulder–first bone-to-implant contact); MM-aJE (mucosal margin–apical area junctional epithelium); MM-aINF (mucosal margin–apical limit of the inflammatory infiltrate); %INF (percentage of inflammatory infiltrate)).

Results

At week 17, TI had significant increased PD, BOP, PP and CAL versus baseline. All clinical variables presented intergroup differences. There was no intergroup difference for radiographic bone loss (p > 0.05). Total bacteria, Fusobacterium spp., A. actinomycetemcomitans and P. gingivalis had intergroup differences. There was no statistically significant intergroup difference for ISH-fBIC.

Conclusions

Longitudinal microbiology evaluation detected a shift period. Final intergroup microbiological differences were the basis of W17 clinical intergroup differences, with higher values in TI. Microbiological and clinical changes detected in peri-implant tissues were compatible with onset of peri-implant disease. Despite histological inflammatory intergroup difference, no histological or radiographic intergroup bone loss was detected.

Clinical relevance

This study set-up describes a valuable method for generating “true” early peri-implant defects without mechanical trauma.

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
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Albrektsson T, Dahlin C, Jemt T, Sennerby L, Turri A, Wennerberg A (2014) Is marginal bone loss around oral implants the result of a provoked foreign body reaction? Clin Implant Dent Relat Res 16(2):155–165. https://doi.org/10.1111/cid.12142

    Article  PubMed  Google Scholar 

  2. de Waal YC, van Winkelhoff AJ, Meijer HJ, Raghoebar GM, Winkel EG (2013) Differences in peri-implant conditions between fully and partially edentulous subjects: a systematic review. J Clin Periodontol 40(3):266–286. https://doi.org/10.1111/jcpe.12013

    Article  PubMed  Google Scholar 

  3. Jepsen S, Berglundh T, Genco R, Aass AM, Demirel K, Derks J, Figuero E, Giovannoli JL, Goldstein M, Lambert F, Ortiz-Vigon A, Polyzois I, Salvi GE, Schwarz F, Serino G, Tomasi C, Zitzmann NU (2015) Primary prevention of peri-implantitis: managing peri-implant mucositis. J Clin Periodontol 42(Suppl 16):S152–S157. https://doi.org/10.1111/jcpe.12369

    Article  PubMed  Google Scholar 

  4. 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

    Article  Google Scholar 

  5. Abrahamsson I, Berglundh T, Lindhe J (1998) Soft tissue response to plaque formation at different implant systems. A comparative study in the dog. Clin Oral Implants Res 9(2):73–79

    Article  Google Scholar 

  6. Martins O, Ramos JC, Baptista IP, Dard MM (2014) The dog as a model for peri-implantitis: a review. J Investig Surg 27(1):50–56. https://doi.org/10.3109/08941939.2013.828805

    Article  Google Scholar 

  7. Albouy JP, Abrahamsson I, Persson LG, Berglundh T (2009) Spontaneous progression of ligatured induced peri-implantitis at implants with different surface characteristics. An experimental study in dogs II: histological observations. Clin Oral Implants Res 20(4):366–371

    Article  Google Scholar 

  8. Faggion CM Jr, Chambrone L, Gondim V, Schmitter M, Tu YK (2010) Comparison of the effects of treatment of peri-implant infection in animal and human studies: systematic review and meta-analysis. Clin Oral Implants Res 21(2):137–147. https://doi.org/10.1111/j.1600-0501.2009.01753.x

    Article  PubMed  Google Scholar 

  9. Zitzmann NU, Berglundh T, Ericsson I, Lindhe J (2004) Spontaneous progression of experimentally induced periimplantitis. J Clin Periodontol 31(10):845–849. https://doi.org/10.1111/j.1600-051X.2004.00567.x

    Article  PubMed  Google Scholar 

  10. Berglundh T, Gotfredsen K, Zitzmann NU, Lang NP, Lindhe J (2007) Spontaneous progression of ligature induced peri-implantitis at implants with different surface roughness: an experimental study in dogs. Clin Oral Implants Res 18(5):655–661. https://doi.org/10.1111/j.1600-0501.2007.01397.x

    Article  PubMed  Google Scholar 

  11. Albouy JP, Abrahamsson I, Berglundh T (2012) Spontaneous progression of experimental peri-implantitis at implants with different surface characteristics: an experimental study in dogs. J Clin Periodontol 39(2):182–187. https://doi.org/10.1111/j.1600-051X.2011.01820.x

    Article  PubMed  Google Scholar 

  12. Albouy JP, Abrahamsson I, Persson LG, Berglundh T (2008) Spontaneous progression of peri-implantitis at different types of implants. An experimental study in dogs. I: clinical and radiographic observations. Clin Oral Implants Res 19(10):997–1002. https://doi.org/10.1111/j.1600-0501.2008.01589.x

    Article  PubMed  Google Scholar 

  13. Marinello CP, Berglundh T, Ericsson I, Klinge B, Glantz PO, Lindhe J (1995) Resolution of ligature-induced peri-implantitis lesions in the dog. J Clin Periodontol 22(6):475–479

    Article  Google Scholar 

  14. Berglundh T, Stavropoulos A, Working Group 1 of the VEWoP (2012) Preclinical in vivo research in implant dentistry. Consensus of the eighth European workshop on periodontology. J Clin Periodontol 39(Suppl 12):1–5. https://doi.org/10.1111/j.1600-051X.2011.01827.x

    Article  PubMed  Google Scholar 

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

  16. Becker W (2012) Osseointegration: have we tinkered with the process too much? Clin Implant Dent Relat Res 14(6):779–780. https://doi.org/10.1111/cid.12009

    Article  PubMed  Google Scholar 

  17. 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. https://doi.org/10.1111/j.1600-0501.2011.02220.x

    Article  PubMed  Google Scholar 

  18. Lindhe J, Meyle J, Group DoEWoP (2008) Peri-implant diseases: consensus report of the Sixth European Workshop on Periodontology. J Clin Periodontol 35(8 Suppl):282–285. https://doi.org/10.1111/j.1600-051X.2008.01283.x

    Article  PubMed  Google Scholar 

  19. Augthun M, Conrads G (1997) Microbial findings of deep peri-implant bone defects. Int J Oral Maxillofac Implants 12(1):106–112

    PubMed  Google Scholar 

  20. Heitz-Mayfield LJ, Lang, NP (2010) Comparative biology of chronic and aggressive periodontitis vs. peri-implantitis. Periodontol 53:167–181. doi:https://doi.org/10.1111/j.1600-0757.2010.00348.x

  21. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, National Centre for the Replacement R, Reduction of Amimals in R (2011) Animal research: reporting in vivo experiments—the ARRIVE guidelines. J Cereb Blood Flow Metab 31(4):991–993. https://doi.org/10.1038/jcbfm.2010.220

    Article  PubMed  PubMed Central  Google Scholar 

  22. Cochran DL, Nummikoski PV, Schoolfield JD, Jones AA, Oates TW (2009) A prospective multicenter 5-year radiographic evaluation of crestal bone levels over time in 596 dental implants placed in 192 patients. J Periodontol 80(5):725–733. https://doi.org/10.1902/jop.2009.080401

    Article  PubMed  Google Scholar 

  23. Donath K, Breuner G (1982) A method for the study of undecalcified bones and teeth with attached soft tissues. The Sage-Schliff (sawing and grinding) technique. J Oral Pathol 11(4):318–326

    Article  Google Scholar 

  24. Schwarz F, Jepsen S, Herten M, Sager M, Rothamel D, Becker J (2006) Influence of different treatment approaches on non-submerged and submerged healing of ligature induced peri-implantitis lesions: an experimental study in dogs. J Clin Periodontol 33(8):584–595. https://doi.org/10.1111/j.1600-051X.2006.00956.x

    Article  PubMed  Google Scholar 

  25. Ericsson I, Persson LG, Berglundh T, Marinello CP, Lindhe J, Klinge B (1995) Different types of inflammatory reactions in peri-implant soft tissues. J Clin Periodontol 22(3):255–261

    Article  Google Scholar 

  26. 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

    Article  Google Scholar 

  27. Struillou X, Boutigny H, Soueidan A, Layrolle P (2010) Experimental animal models in periodontology: a review. Open Dent J 4:37–47. https://doi.org/10.2174/1874210601004010037

    Article  PubMed  PubMed Central  Google Scholar 

  28. Kortegaard HE, Eriksen T, Baelum V (2008) Periodontal disease in research beagle dogs—an epidemiological study. J Small Anim Pract 49(12):610–616. https://doi.org/10.1111/j.1748-5827.2008.00609.x

    Article  PubMed  Google Scholar 

  29. 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

    Article  Google Scholar 

  30. Wennerberg A, Albrektsson T (2010) On implant surfaces: a review of current knowledge and opinions. Int J Oral Maxillofac Implants 25(1):63–74

    PubMed  Google Scholar 

  31. Pesce P, Menini M, Tealdo T, Bevilacqua M, Pera F, Pera P (2014) Peri-implantitis: a systematic review of recently published papers. Int J Prosthodont 27(1):15–25. https://doi.org/10.11607/ijp.3785

    Article  PubMed  Google Scholar 

  32. 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

    Article  Google Scholar 

  33. Mombelli A, Decaillet F (2011) The characteristics of biofilms in peri-implant disease. J Clin Periodontol 38(Suppl 11):203–213. https://doi.org/10.1111/j.1600-051X.2010.01666.x

    Article  PubMed  Google Scholar 

  34. Derks J, Schaller D, Hakansson J, Wennstrom JL, Tomasi C, Berglundh T (2016) Peri-implantitis—onset and pattern of progression. J Clin Periodontol 43(4):383–388. https://doi.org/10.1111/jcpe.12535

    Article  PubMed  Google Scholar 

  35. Heyman O, Koren N, Mizraji G, Capucha T, Wald S, Nassar M, Tabib Y, Shapira L, Hovav AH, Wilensky A (2018) Impaired differentiation of Langerhans cells in the murine oral epithelium adjacent to titanium dental implants. Front Immunol 9:1712. https://doi.org/10.3389/fimmu.2018.01712

    Article  PubMed  PubMed Central  Google Scholar 

  36. Ferreira SD, Silva GL, Cortelli JR, Costa JE, Costa FO (2006) Prevalence and risk variables for peri-implant disease in Brazilian subjects. J Clin Periodontol 33(12):929–935. https://doi.org/10.1111/j.1600-051X.2006.01001.x

    Article  PubMed  Google Scholar 

  37. Lang NP, Wetzel AC, Stich H, Caffesse RG (1994) Histologic probe penetration in healthy and inflamed peri-implant tissues. Clin Oral Implants Res 5(4):191–201

    Article  Google Scholar 

  38. Charalampakis G, Abrahamsson I, Carcuac O, Dahlen G, Berglundh T (2014) Microbiota in experimental periodontitis and peri-implantitis in dogs. Clin Oral Implants Res 25(9):1094–1098. https://doi.org/10.1111/clr.12235

    Article  PubMed  Google Scholar 

  39. Derks J, Tomasi C (2015) Peri-implant health and disease. A systematic review of current epidemiology. J Clin Periodontol 42(Suppl 16):S158–S171. https://doi.org/10.1111/jcpe.12334

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors are very grateful to Dr. Philipp Sahrmann (Center of Dental Medicine, University of Zurich) for his contribution to this study.

Funding

The work was supported by Institut Straumann, Basel, Switzerland.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Orlando Martins.

Ethics declarations

Conflict of interest

Orlando Martins declares that he has no conflict of interest. João Carlos Ramos declares that he has no conflict of interest. Marta Mota declares that she has no conflict of interest. Michel Dard is the Global Medical Director at Institut Straumann, Basel, Switzerland. Carlos Viegas declares that he has no conflict of interest. Francisco Caramelo declares that he has no conflict of interest. Célia Nogueira declares that she has no conflict of interest. Teresa Gonçalves declares that she has no conflict of interest. Isabel Poiares Baptista declares that she has no conflict of interest.

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Informed consent

For this type of study, formal consent is not required.

Additional information

Publisher’s note

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

Electronic supplementary material

ESM 1

(DOCX 27 kb)

ESM 2

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martins, O., Ramos, J.C., Mota, M. et al. Evaluation of a novel dog animal model for peri-implant disease: clinical, radiographic, microbiological and histological assessment. Clin Oral Invest 24, 3121–3132 (2020). https://doi.org/10.1007/s00784-019-03186-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00784-019-03186-3

Keywords

Navigation