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Open Access 01-12-2022 | Bone Defect | Research

Bone defect development in experimental canine peri-implantitis models: a systematic review

Authors: A. Solderer, M. de Boer, D. B. Wiedemeier, M. Solderer, C. C. Liu, P. R. Schmidlin

Published in: Systematic Reviews | Issue 1/2022

Abstract

Purpose

To provide a systematic overview of preclinical research regarding bone defect formation around different implant surfaces after ligature-induced peri-implantitis models in dogs. Two focused questions were formulated: ‘How much bone loss can be expected after a certain time of ligature induced peri-implantitis?’ and ‘Do different implant types, dog breeds and study protocols differ in their extent of bone loss?’

Materials and methods

A systematic literature search was conducted on four databases (MEDLINE, Web of Science, EMBASE and Scopus). Observations, which consisted of bone defects measured directly after ligature removal in canine models, were included and analysed. Two approaches were used to analyse the relatively heterogeneous studies that fulfilled the inclusion criteria. First, separate simple linear regressions were calculated for each study and implant surface, for which observations were available across multiple time points. Second, a linear mixed model was specified for the observations at 12 weeks after ligature initiation, and assessing the potential influencing factors on defect depth was explored using lasso regularisation.

Results

Thirty-six studies with a total of 1082 implants were included after. Bone loss was determined at different time points, either with clinical measurements radiographically or histologically. Different implant groups [e.g. turned, sand-blasted-acid-etched (SLA), titanium-plasma-sprayed (TPS) and other rough surfaces] were assessed and described in the studies. A mean incremental defect depth increase of 0.08 mm (SD: −0.01–0.28 mm) per week was observed. After 12 weeks, the defect depths ranged between 0.7 and 5 mm. Based on the current data set, implant surface could not be statistically identified as an essential factor in defect depth after 12 weeks of ligature-induced peri-implantitis.

Conclusion

Expectable defect depth after a specific time of ligature-induced peri-implantitis can vary robustly. It is currently impossible to delineate apparent differences in bone loss around different implant surfaces.

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Elani HW, Starr JR, Da Silva JD, Gallucci GO. Trends in dental implant use in the U.S., 1999-2016, and projections to 2026. J Dent Res. 2018;97(13):1424–30. https://doi.org/10.1177/0022034518792567.CrossRefPubMedPubMedCentral

Renvert S, Hirooka H, Polyzois I, Kelekis-Cholakis A, Wang HL, Working, G. Diagnosis and non-surgical treatment of peri-implant diseases and maintenance care of patients with dental implants - consensus report of working group 3. Int Dent J. 2019;69(Suppl 2):12–7. https://doi.org/10.1111/idj.12490.CrossRefPubMed

Bäumer A, Toekan S, Saure D, Körner G. Survival and success of implants in a private periodontal practice: a 10 year retrospective study. BMC Oral Health. 2020;20(1):92. https://doi.org/10.1186/s12903-020-01064-z.CrossRefPubMedPubMedCentral

Derks J, Tomasi C. Peri-implant health and disease. A systematic review of current epidemiology. J Clin Periodontol. 2015;42(Suppl 16):S158–71. https://doi.org/10.1111/jcpe.12334.CrossRefPubMed

Solderer A, Pippenger BE, Donnet M, Wiedemeier D, Ramenzoni LL, Schmidlin PR. Evaluation of air polishing with a sterile powder and mechanical debridement during regenerative surgical periimplantitis treatment: a study in dogs. Clin Oral Investig. 2020. https://doi.org/10.1007/s00784-020-03572-2.

Mombelli A. Microbiology and antimicrobial therapy of peri-implantitis. Periodontol. 2002;28:177–89. https://doi.org/10.1034/j.1600-0757.2002.280107.x.CrossRef

Esposito M, Grusovin MG, Worthington HV. Treatment of peri-implantitis: what interventions are effective? A Cochrane systematic review. Eur J Oral Implantol. 2012;5(Suppl):S21–41.PubMed

Rovin S, Costich ER, Gordon HA. The influence of bacteria and irritation in the initiation of periodontal disease in germfree and conventional rats. J Periodontal Res. 1966;1(3):193–204. https://doi.org/10.1111/j.1600-0765.1966.tb01860.x.CrossRefPubMed

Lindhe J, Hamp SE, Loe H. Experimental periodontitis in the beagle dog. Int Dent J. 1973;23(3):432–7.PubMed

10.

Schwarz F, Iglhaut G, Becker J. Quality assessment of reporting of animal studies on pathogenesis and treatment of peri-implant mucositis and peri-implantitis. A systematic review using the ARRIVE guidelines. J Clin Periodontol. 2012;39(Suppl 12):63–72. https://doi.org/10.1111/j.1600-051X.2011.01838.x.CrossRefPubMed

11.

Berglundh T, Lindhe J, Marinello C, Ericsson I, Liljenberg B. Soft tissue reaction to de novo plaque formation on implants and teeth. An experimental study in the dog. Clin Oral Implants Res. 1992;3(1):1–8. https://doi.org/10.1034/j.1600-0501.1992.030101.x.CrossRefPubMed

12.

Kantarci A, Hasturk H, Van Dyke TE. Animal models for periodontal regeneration and peri-implant responses. Periodontol. 2015;68(1):66–82. https://doi.org/10.1111/prd.12052.CrossRef

13.

Schwarz F, Herten M, Sager M, Bieling K, Sculean A, Becker J. Comparison of naturally occurring and ligature-induced peri-implantitis bone defects in humans and dogs. Clin Oral Implants Res. 2007;18(2):161–70. https://doi.org/10.1111/j.1600-0501.2006.01320.x.CrossRefPubMed

14.

Reinedahl D, Chrcanovic B, Albrektsson T, Tengvall P, Wennerberg A. Ligature-induced experimental peri-implantitis- a systematic review. J Clin Med. 2018;7(12). https://doi.org/10.3390/jcm7120492.

15.

Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA, G. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg. 2010;8(5):336–41. https://doi.org/10.1016/j.ijsu.2010.02.007.CrossRefPubMed

16.

Team, R. C. R: a language and environment for statistical computing. Vienna: R Foundation for Statistical Computing; 2020.

17.

Wickham H, Averick M, Bryan J, Chang W. Welcome to the Tidyverse. J Open Source. 2019;4(43):1686.CrossRef

18.

Groll, A., & Groll, M. A. (2017). Package ‘glmmLasso. mirror.rcg.sfu.ca.

19.

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

20.

Albouy JP, Abrahamsson I, Berglundh T. Spontaneous progression of experimental peri-implantitis at implants with different surface characteristics: an experimental study in dogs. J Clin Periodontol. 2012;39(2):182–7. https://doi.org/10.1111/j.1600-051X.2011.01820.x.CrossRefPubMed

21.

Almohandes A, Carcuac O, Abrahamsson I, Lund H, Berglundh T. Re-osseointegration following reconstructive surgical therapy of experimental peri-implantitis. A pre-clinical in vivo study. Clin Oral Implants Res. 2019;30(5):447–56. https://doi.org/10.1111/clr.13430.CrossRefPubMed

22.

Battula S, Lee JW, Wen HB, Papanicolaou S, Collins M, Romanos GE. Evaluation of different implant designs in a ligature-induced peri-implantitis model: a canine study. Int J Oral Maxillofac Implants. 2015;30(3):534–45. https://doi.org/10.11607/jomi.3737.CrossRefPubMed

23.

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(5):655–61. https://doi.org/10.1111/j.1600-0501.2007.01397.x.CrossRefPubMed

24.

Carcuac O, Abrahamsson I, Albouy JP, Linder E, Larsson L, Berglundh T. Experimental periodontitis and peri-implantitis in dogs. Clin Oral Implants Res. 2013;24(4):363–71. https://doi.org/10.1111/clr.12067.CrossRefPubMed

25.

Carcuac O, Abrahamsson I, Charalampakis G, Berglundh T. The effect of the local use of chlorhexidine in surgical treatment of experimental peri-implantitis in dogs. J Clin Periodontol. 2015;42(2):196–203. https://doi.org/10.1111/jcpe.12332.CrossRefPubMed

26.

Deppe H, Horch HH, Henke J, Donath K. Peri-implant care of ailing implants with the carbon dioxide laser. Int J Oral Maxillofac Implants. 2001;16(5):659–67 Retrieved from https://pubmed.ncbi.nlm.nih.gov/11669248.PubMed

27.

Godoy-Gallardo M, Manzanares-Céspedes MC, Sevilla P, Nart J, Manzanares N, Manero JM, et al. Evaluation of bone loss in antibacterial coated dental implants: an experimental study in dogs. Mater Sci Eng C Mater Biol Appl. 2016;69:538–45. https://doi.org/10.1016/j.msec.2016.07.020.CrossRefPubMed

28.

Grunder U, Hürzeler MB, Schüpbach P, Strub JR. Treatment of ligature-induced peri-implantitis using guided tissue regeneration: a clinical and histologic study in the beagle dog. Int J Oral Maxillofac Implants. 1993;8(3):282–93 Retrieved from https://pubmed.ncbi.nlm.nih.gov/8225463.PubMed

29.

Huang B, Piao M, Zhang L, Wang X, Xu L, Zhu W, et al. Ligature-induced peri-implant infection in crestal and subcrestal implants: a clinical and radiographic study in dogs. PeerJ. 2015;3:e1139. https://doi.org/10.7717/peerj.1139.CrossRefPubMedPubMedCentral

30.

Huang B, Zhang L, Xu L, Zhu W, Witek L, Tovar N, et al. Effect of implant placement depth on the peri-implant bone defect configurations in ligature-induced peri-implantitis: an experimental study in dogs. Med Oral Patol Oral Cir Bucal. 2018;23(1):e30–7. https://doi.org/10.4317/medoral.22032.CrossRefPubMed

31.

Lang NP, Wetzel AC, Stich H, Caffesse RG. Histologic probe penetration in healthy and inflamed peri-implant tissues. Clin Oral Implants Res. 1994;5(4):191–201. https://doi.org/10.1034/j.1600-0501.1994.050401.x.CrossRefPubMed

32.

Madi M, Zakaria O, Kasugai S. Coated vs uncoated implants: bone defect configurations after progressive peri-implantitis in dogs. J Oral Implantol. 2014;40(6):661–9. https://doi.org/10.1563/AAID-JOI-D-12-00089.CrossRefPubMed

33.

Madi M, Zakaria O, Ichinose S, Kasugai S. Effect of induced periimplantitis on dental implants with and without ultrathin hydroxyapatite coating. Implant Dent. 2016;25(1):39–46. https://doi.org/10.1097/ID.0000000000000331.CrossRefPubMed

34.

Martins MC, Shibli JA, Abi-Rached RS, Marcantonio E. Progression of experimental chronic peri-implantitis in dogs: clinical and radiographic evaluation. J Periodontol. 2005;76(8):1367–73. https://doi.org/10.1902/jop.2005.76.8.1367.CrossRefPubMed

35.

Marinello CP, Berglundh T, Ericsson I, Klinge B, Glantz PO, Lindhe J. Resolution of ligature-induced peri-implantitis lesions in the dog. J Clin Periodontol. 1995;22(6):475–9. https://doi.org/10.1111/j.1600-051x.1995.tb00180.x.CrossRefPubMed

36.

Martinez A, Guitián F, López-Píriz R, Bartolomé JF, Cabal B, Esteban-Tejeda L, et al. Bone loss at implant with titanium abutments coated by soda lime glass containing silver nanoparticles: a histological study in the dog. PLoS One. 2014;9(1):e86926. https://doi.org/10.1371/journal.pone.0086926.CrossRefPubMedPubMedCentral

37.

Monje A, Insua A, Rakic M, Nart J, Moyano-Cuevas JL, Wang HL. Estimation of the diagnostic accuracy of clinical parameters for monitoring peri-implantitis progression: an experimental canine study. J Periodontol. 2018;89(12):1442–51. https://doi.org/10.1002/JPER.18-0081.CrossRefPubMed

38.

Monje A, Eick S, Buser D, Salvi GE. Microbial and host-derived biomarker changes during ligature-induced and spontaneous peri-implantitis in the Beagle dog. J Periodontal Res. 2021;56(1):93–100. https://doi.org/10.1111/jre.12797.CrossRefPubMed

39.

Namgoong H, Kim MD, Ku Y, Rhyu IC, Lee YM, Seol YJ, et al. Bone reconstruction after surgical treatment of experimental peri-implantitis defects at a sandblasted/acid-etched hydroxyapatite-coated implant: an experimental study in the dog. J Clin Periodontol. 2015;42(10):960–6. https://doi.org/10.1111/jcpe.12457.CrossRefPubMed

40.

Park SY, Kim KH, Rhee SH, Lee JC, Shin SY, Lee YM, et al. An immediate peri-implantitis induction model to study regenerative peri-implantitis treatments. Clin Oral Implants Res. 2017;28(1):36–42. https://doi.org/10.1111/clr.12611.CrossRefPubMed

41.

Park SY, Kim KH, Kim S, Rhee SH, Yeo IS, Heo SJ, et al. Comparison of experimental peri-implantitis models after application of ex vivo BMP2 gene therapy using periodontal ligament stem cells. Sci Rep. 2020;10(1):3590. https://doi.org/10.1038/s41598-020-60341-7.CrossRefPubMedPubMedCentral

42.

Persson LG, Araújo MG, Berglundh T, Gröndahl K, Lindhe J. Resolution of peri-implantitis following treatment. An experimental study in the dog. Clin Oral Implants Res. 1999;10(3):195–203. https://doi.org/10.1034/j.1600-0501.1999.100302.x.CrossRefPubMed

43.

Sanz-Esporrin J, Blanco J, Sanz-Casado JV, Muñoz F, Sanz M. The adjunctive effect of rhBMP-2 on the regeneration of peri-implant bone defects after experimental peri-implantitis. Clin Oral Implants Res. 2019;30(12):1209–19. https://doi.org/10.1111/clr.13534.CrossRefPubMed

44.

Shi Q, Song K, Zhou X, Xiong Z, Du T, Lu X, et al. Effects of non-equilibrium plasma in the treatment of ligature-induced peri-implantitis. J Clin Periodontol. 2015;42(5):478–87. https://doi.org/10.1111/jcpe.12403.CrossRefPubMed

45.

46.

Tillmanns HW, Hermann JS, Cagna DR, Burgess AV, Meffert RM. Evaluation of three different dental implants in ligature-induced peri-implantitis in the beagle dog. Part I. Clinical evaluation. Int J Oral Maxillofac Implants. 1997;12(5):611–20 Retrieved from https://pubmed.ncbi.nlm.nih.gov/9337021.PubMed

47.

Viganò P, Apaza Alccayhuaman KA, Sakuma S, Amari Y, Bengazi F, Botticelli D. Use of TiBrush for surface decontamination at peri-implantitis sites in dogs: radiographic and histological outcomes. J Investig Clin Dent. 2019;10(1):e12378. https://doi.org/10.1111/jicd.12378.CrossRefPubMed

48.

Wetzel AC, Vlassis J, Caffesse RG, Hämmerle CH, Lang NP. Attempts to obtain re-osseointegration following experimental peri-implantitis in dogs. Clin Oral Implants Res. 1999;10(2):111–9. https://doi.org/10.1034/j.1600-0501.1999.100205.x.CrossRefPubMed

49.

Xu L, Sun X, Bai J, Jiang L, Wang S, Zhao J, et al. Reosseointegration following regenerative therapy of tissue-engineered bone in a canine model of experimental peri-implantitis. Clin Implant Dent Relat Res. 2016;18(2):379–91. https://doi.org/10.1111/cid.12308.CrossRefPubMed

50.

Yang L, Zhu Q, Gong J, Xie M, Jiao T. CyPA and Emmprin play a role in peri-implantitis. Clin Implant Dent Relat Res. 2018;20(2):102–9. https://doi.org/10.1111/cid.12549.CrossRefPubMed

51.

Yoon SW, Kim MJ, Paeng KW, Yu KA, Lee CK, Song YW, et al. Efficacy of local minocycline agents in treating peri-implantitis: an experimental in vivo study in Beagle dogs. Pharmaceutics. 2020;12(11). https://doi.org/10.3390/pharmaceutics12111016.

52.

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

53.

Roehling S, Gahlert M, Janner S, Meng B, Woelfler H, Cochran DL. Ligature-induced peri-implant bone loss around loaded zirconia and titanium implants. Int J Oral Maxillofac Implants. 2019;34(2):357–65. https://doi.org/10.11607/jomi.7015.CrossRefPubMed

Title: Bone defect development in experimental canine peri-implantitis models: a systematic review
Authors: A. Solderer
M. de Boer
D. B. Wiedemeier
M. Solderer
C. C. Liu
P. R. Schmidlin
Publication date: 01-12-2022
Publisher: BioMed Central
Keyword: Bone Defect
Published in: Systematic Reviews / Issue 1/2022
Electronic ISSN: 2046-4053
DOI: https://doi.org/10.1186/s13643-022-02075-3

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Bone defect development in experimental canine peri-implantitis models: a systematic review

Abstract

Purpose

Materials and methods

Results

Conclusion

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Materials and methods

Results

Conclusion

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