DOI QR코드

DOI QR Code

Rodent peri-implantitis models: a systematic review and meta-analysis of morphological changes

  • 투고 : 2022.02.07
  • 심사 : 2022.05.17
  • 발행 : 2022.12.31

초록

Purpose: Rodent models have emerged as an alternative to established larger animal models for peri-implantitis research. However, the construct validity of rodent models is controversial due to a lack of consensus regarding their histological, morphological, and biochemical characteristics. This systematic review sought to validate rodent models by characterizing their morphological changes, particularly marginal bone loss (MBL), a hallmark of peri-implantitis. Methods: This review was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines. A literature search was performed electronically using MEDLINE (PubMed), and Embase, identifying pre-clinical studies reporting MBL after experimental peri-implantitis induction in rodents. Each study's risk of bias was assessed using the Systematic Review Center for Laboratory animal Experimentation (SYRCLE) risk of bias tool. A meta-analysis was performed for the difference in MBL, comparing healthy implants to those with experimental peri-implantitis. Results: Of the 1,014 unique records retrieved, 23 studies that met the eligibility criteria were included. Peri-implantitis was induced using 4 methods: ligatures, lipopolysaccharide, microbial infection, and titanium particles. Studies presented high to unclear risks of bias. During the osseointegration phase, 11.6% and 6.4%-11.3% of implants inserted in mice and rats, respectively, had failed to osseointegrate. Twelve studies were included in the meta-analysis of the linear MBL measured using micro-computed tomography. Following experimental peri-implantitis, the MBL was estimated to be 0.25 mm (95% confidence interval [CI], 0.14-0.36 mm) in mice and 0.26 mm (95% CI, 0.19-0.34 mm) in rats. The resulting peri-implant MBL was circumferential, consisting of supra- and infrabony components. Conclusions: Experimental peri-implantitis in rodent models results in circumferential MBL, with morphology consistent with the clinical presentation of peri-implantitis. While rodent models are promising, there is still a need to further characterize their healing potentials, standardize experiment protocols, and improve the reporting of results and methodology.

키워드

과제정보

This study was self-funded by the authors and their respective institutions.

참고문헌

  1. Derks J, Tomasi C. Peri-implant health and disease. A systematic review of current epidemiology. J Clin Periodontol 2015;42 Suppl 16:S158-71.
  2. Schwarz F, Derks J, Monje A, Wang HL. Peri-implantitis. J Clin Periodontol 2018;45 Suppl 20:S246-66.  https://doi.org/10.1111/jcpe.12954
  3. Meffert RM. Periodontitis vs. peri-implantitis: the same disease? The same treatment? Crit Rev Oral Biol Med 1996;7:278-91.  https://doi.org/10.1177/10454411960070030501
  4. Roccuzzo M, Layton DM, Roccuzzo A, Heitz-Mayfield LJ. Clinical outcomes of peri-implantitis treatment and supportive care: a systematic review. Clin Oral Implants Res 2018;29 Suppl 16:331-50. 
  5. Kotsakis GA, Olmedo DG. Peri-implantitis is not periodontitis: scientific discoveries shed light on microbiomebiomaterial interactions that may determine disease phenotype. Periodontol 2000 2021;86:231-40.  https://doi.org/10.1111/prd.12372
  6. Lafaurie GI, Sabogal MA, Castillo DM, Rincon MV, Gomez LA, Lesmes YA, et al. Microbiome and microbial biofilm profiles of peri-implantitis: a systematic review. J Periodontol 2017;88:1066-89.  https://doi.org/10.1902/jop.2017.170123
  7. Graves DT, Fine D, Teng YT, Van Dyke TE, Hajishengallis G. The use of rodent models to investigate hostbacteria interactions related to periodontal diseases. J Clin Periodontol 2008;35:89-105.  https://doi.org/10.1111/j.1600-051X.2007.01172.x
  8. Kantarci A, Hasturk H, Van Dyke TE. Animal models for periodontal regeneration and peri-implant responses. Periodontol 2000 2015;68:66-82.  https://doi.org/10.1111/prd.12052
  9. Hooijmans CR, Rovers MM, de Vries RB, Leenaars M, Ritskes-Hoitinga M, Langendam MW. SYRCLE's risk of bias tool for animal studies. BMC Med Res Methodol 2014;14:43. 
  10. Drevon D, Fursa SR, Malcolm AL. Intercoder reliability and validity of WebPlotDigitizer in extracting graphed data. Behav Modif 2017;41:323-39.  https://doi.org/10.1177/0145445516673998
  11. Sun J, Eberhard J, Glage S, Held N, Voigt H, Schwabe K, et al. Development of a peri-implantitis model in the rat. Clin Oral Implants Res 2020;31:203-14. 
  12. Wu X, Qiao S, Wang W, Zhang Y, Shi J, Zhang X, et al. Melatonin prevents peri-implantitis via suppression of TLR4/NF-κB. Acta Biomater 2021;134:325-36.  https://doi.org/10.1016/j.actbio.2021.07.017
  13. Varon-Shahar E, Shusterman A, Piattelli A, Iezzi G, Weiss EI, Houri-Haddad Y. Peri-implant alveolar bone resorption in an innovative peri-implantitis murine model: effect of implant surface and onset of infection. Clin Implant Dent Relat Res 2019;21:723-33.  https://doi.org/10.1111/cid.12800
  14. Tzach-Nahman R, Mizraji G, Shapira L, Nussbaum G, Wilensky A. Oral infection with Porphyromonas gingivalis induces peri-implantitis in a murine model: Evaluation of bone loss and the local inflammatory response. J Clin Periodontol 2017;44:739-48.  https://doi.org/10.1111/jcpe.12735
  15. Ding L, Zhang P, Wang X, Kasugai S. A doxycycline-treated hydroxyapatite implant surface attenuates the progression of peri-implantitis: a radiographic and histological study in mice. Clin Implant Dent Relat Res 2019;21:154-9.  https://doi.org/10.1111/cid.12695
  16. Ozawa R, Saita M, Sakaue S, Okada R, Sato T, Kawamata R, et al. Redox injectable gel protects osteoblastic function against oxidative stress and suppresses alveolar bone loss in a rat peri-implantitis model. Acta Biomater 2020;110:82-94.  https://doi.org/10.1016/j.actbio.2020.04.003
  17. He Q, Mu Z, Shrestha A, Wang C, Wang S, Tang H, et al. Development of a rat model for type 2 diabetes mellitus peri-implantitis: a preliminary study. Oral Dis 2021;odi.13845. 
  18. Hori Y, Kondo Y, Nodai T, Masaki C, Ono K, Hosokawa R. Xerostomia aggravates ligation-induced periimplantitis: a preclinical in vivo study. Clin Oral Implants Res 2021;32:581-9.  https://doi.org/10.1111/clr.13727
  19. Takamori Y, Atsuta I, Nakamura H, Sawase T, Koyano K, Hara Y. Histopathological comparison of the onset of peri-implantitis and periodontitis in rats. Clin Oral Implants Res 2017;28:163-70. 
  20. Wong RL, Hiyari S, Yaghsezian A, Davar M, Lin YL, Galvan M, et al. Comparing the healing potential of late-stage periodontitis and peri-implantitis. J Oral Implantol 2017;43:437-45. https://doi.org/10.1563/aaid-joi-D-17-00157
  21. Yamazaki S, Masaki C, Nodai T, Tsuka S, Tamura A, Mukaibo T, et al. The effects of hyperglycaemia on peri-implant tissues after osseointegration. J Prosthodont Res 2020;64:217-23.  https://doi.org/10.1016/j.jpor.2019.07.007
  22. Nguyen Vo TN, Hao J, Chou J, Oshima M, Aoki K, Kuroda S, et al. Ligature induced peri-implantitis: tissue destruction and inflammatory progression in a murine model. Clin Oral Implants Res 2017;28:129-36. 
  23. Hiyari S, Naghibi A, Wong R, Sadreshkevary R, Yi-Ling L, Tetradis S, et al. Susceptibility of different mouse strains to peri-implantitis. J Periodontal Res 2018;53:107-16.  https://doi.org/10.1111/jre.12493
  24. Wang X, Li Y, Feng Y, Cheng H, Li D. Macrophage polarization in aseptic bone resorption around dental implants induced by Ti particles in a murine model. J Periodontal Res 2019;54:329-38.  https://doi.org/10.1111/jre.12633
  25. Koutouzis T, Eastman C, Chukkapalli S, Larjava H, Kesavalu L. A novel rat model of polymicrobial periimplantitis: a preliminary study. J Periodontol 2017;88:e32-41.  https://doi.org/10.1902/jop.2016.160273
  26. Wong RL, Hiyari S, Yaghsezian A, Davar M, Casarin M, Lin YL, et al. Early intervention of peri-implantitis and periodontitis using a mouse model. J Periodontol 2018;89:669-79.  https://doi.org/10.1002/JPER.17-0541
  27. Li H, Wang Y, Zhang D, Chen T, Hu A, Han X. Glycemic fluctuation exacerbates inflammation and bone loss and alters microbiota profile around implants in diabetic mice with experimental peri-implantitis. Int J Implant Dent 2021;7:79. 
  28. Pirih FQ, Hiyari S, Barroso AD, Jorge AC, Perussolo J, Atti E, et al. Ligature-induced peri-implantitis in mice. J Periodontal Res 2015;50:519-24.  https://doi.org/10.1111/jre.12234
  29. Pirih FQ, Hiyari S, Leung HY, Barroso AD, Jorge AC, Perussolo J, et al. A murine model of lipopolysaccharide-induced peri-implant mucositis and peri-implantitis. J Oral Implantol 2015;41:e158-64.  https://doi.org/10.1563/aaid-joi-D-14-00068
  30. Hiyari S, Wong RL, Yaghsezian A, Naghibi A, Tetradis S, Camargo PM, et al. Ligature-induced periimplantitis and periodontitis in mice. J Clin Periodontol 2018;45:89-99. 
  31. Renvert S, Persson GR, Pirih FQ, Camargo PM. Peri-implant health, peri-implant mucositis, and periimplantitis: case definitions and diagnostic considerations. J Periodontol 2018;89 Suppl 1:S304-12.  https://doi.org/10.1002/JPER.17-0588
  32. Deng S, Hu Y, Zhou J, Wang Y, Wang Y, Li S, et al. TLR4 mediates alveolar bone resorption in experimental peri-implantitis through regulation of CD45+ cell infiltration, RANKL/OPG ratio, and inflammatory cytokine production. J Periodontol 2020;91:671-82.  https://doi.org/10.1002/JPER.18-0748
  33. Li H, Chen Z, Zhong X, Li J, Li W. Mangiferin alleviates experimental peri-implantitis via suppressing interleukin-6 production and Toll-like receptor 2 signaling pathway. J Orthop Surg 2019;14:325. 
  34. Pan K, Hu Y, Wang Y, Li H, Patel M, Wang D, et al. RANKL blockade alleviates peri-implant bone loss and is enhanced by anti-inflammatory microRNA-146a through TLR2/4 signaling. Int J Implant Dent 2020;6:15. 
  35. 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;18:161-70.  https://doi.org/10.1111/j.1600-0501.2006.01320.x
  36. Freire MO, Devaraj A, Young A, Navarro JB, Downey JS, Chen C, et al. A bacterial-biofilm-induced oral osteolytic infection can be successfully treated by immuno-targeting an extracellular nucleoid-associated protein. Mol Oral Microbiol 2017;32:74-88.  https://doi.org/10.1111/omi.12155
  37. Gao SS, Zhang YR, Zhu ZL, Yu HY. Micromotions and combined damages at the dental implant/bone interface. Int J Oral Sci 2012;4:182-8.  https://doi.org/10.1038/ijos.2012.68
  38. Watanabe T, Nakagawa E, Saito K, Ohshima H. Differences in healing patterns of the bone-implant interface between immediately and delayed-placed titanium implants in mouse maxillae. Clin Implant Dent Relat Res 2016;18:146-60. https://doi.org/10.1111/cid.12280
  39. Fujii N, Kusakari H, Maeda T. A histological study on tissue responses to titanium implantation in rat maxilla: the process of epithelial regeneration and bone reaction. J Periodontol 1998;69:485-95.  https://doi.org/10.1902/jop.1998.69.4.485
  40. Albrektsson T, Chrcanovic B, Molne J, Wennerberg A. Foreign body reactions, marginal bone loss and allergies in relation to titanium implants. Eur J Oral Implantology 2018;11 Suppl 1:S37-46.