Skip to main content
Log in

Critical-sized marginal defects around implants in the rabbit mandible

  • Research
  • Published:
Oral and Maxillofacial Surgery Aims and scope Submit manuscript

Abstract

Background

The mandible of the rabbit is considered a reliable model to be used to study bone regeneration in defects. The aim of the present study was to evaluate the formation of new bone around implants installed in defects of either 5 or 10 mm in the mandible of rabbits.

Materials and methods

In 12 rabbits, 3 mm deep circumferential defect, either 5 or 10 mm in diameter, were prepared bilaterally and an implant was placed in the center. A collagen membrane was placed to close the entrance. After 10 weeks, biopsies were taken, histological slides were prepared, and different regions of the defects were analyzed.

Results

Similar amounts of new bone were found in both defects. However, most of the 5 mm defects were filled with new bone. New bone was observed closing the entrance of the defect and laid onto the implant surface. Only in a few cases the healing was incomplete. Despite a similar percentage of new bone found within the 10 mm defects, the healing was incomplete in most of the cases, presenting a low rate of bone formation onto the implant surface within the defect. Only one case presented the closure of the entrance.

Conclusions

The dimensions of the defect strongly influenced the healing so that a circumferential marginal defect of 10 mm around an implant in the mandible body should be considered a critical-sized defect. The presence of the implant and of residues of teeth might have strongly influenced the healing.

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

Data availability

No datasets were generated or analysed during the current study.

References

  1. Guo J, Meng Z, Chen G, Xie D, Chen Y, Wang H, Tang W, Liu L, Jing W, Long J, Guo W, Tian W (2012) Restoration of critical-size defects in the rabbit mandible using porous nanohydroxyapatite-polyamide scaffolds. Tissue Eng Part A 18(11–12):1239–1252. https://doi.org/10.1089/ten.TEA.2011.0503Epub 2012 Mar 19. PMID: 22320360

    Article  CAS  PubMed  Google Scholar 

  2. Bos GD, Goldberg VM, Powell AE, Heiple KG, Zika JM (1983) The effect of histocompatibility matching on canine frozen bone allografts. J Bone Joint Surg 65:89–96

    Article  CAS  PubMed  Google Scholar 

  3. Hollinger JO, Kleinschmidt JC (1990) The critical size defect as an experimental model to test bone repair materials. J Craniofac Surg. ;1(1):60 – 8. https://doi.org/10.1097/00001665-199001000-00011. PMID: 1965154

  4. Schmitz JP, Hollinger JO (1996) The critical size defect as an experimental model for craniomandibulofacial non-unions. Clin Orthop Relat Res 205:299–308

    Google Scholar 

  5. Cooper GM, Mooney MP, Gosain AK, Campbell PG, Losee JE, Huard J (2010) Testing the critical size in calvarial bone defects: revisiting the concept of a critical-size defect. Plast Reconstr Surg 125(6):1685–1692. https://doi.org/10.1097/PRS.0b013e3181cb63a3PMID: 20517092; PMCID: PMC2946111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Monir A, Mukaibo T, Abd El-Aal ABM, Nodai T, Munemasa T, Kondo Y, Masaki C, El-Shair MA, Matsuo K, Hosokawa R (2021) Local administration of HMGB-1 promotes bone regeneration on the critical-sized mandibular defects in rabbits. Sci Rep 11(1):8950. https://doi.org/10.1038/s41598-021-88195-7PMID: 33903607; PMCID: PMC8076241

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Awadeen MA, Al-Belasy FA, Ameen LE, Helal ME, Grawish ME (2020) Early therapeutic effect of platelet-rich fibrin combined with allogeneic bone marrow-derived stem cells on rats’ critical-sized mandibular defects. World J Stem Cells 12(1):55–69. https://doi.org/10.4252/wjsc.v12.i1.55PMID: 32110275; PMCID: PMC7031757

    Article  PubMed  PubMed Central  Google Scholar 

  8. Trejo-Iriarte CG, Serrano-Bello J, Gutiérrez-Escalona R, Mercado-Marques C, García-Honduvilla N, Buján-Varela J, Me-dina LA (2019) Evaluation of bone regeneration in a critical size cortical bone defect in rat mandible using microCT and his-tological analysis. Arch Oral Biol. ;101:165–171. doi: 10.1016/j.archoralbio.2019.01.010. Epub 2019 Feb 5. PMID: 30951954

  9. Frame JW (1980) A convenient animal model for testing bone substitute materials. J Oral Surg 38(3):176–180 PMID: 6928181

    CAS  PubMed  Google Scholar 

  10. Gilsanz V, Roe TF, Gibbens DT, Schulz EE, Carlson ME, Gonzalez O, Boechat MI (1988) Effect of sex steroids on peak bone density of growing rabbits. Am J Physiology-Endocrinology Metabolism 255:416–421

    Article  Google Scholar 

  11. Pearce AI, Richards RG, Milz S, Schneider E, Pearce SG (2007) Animal models for implant biomaterial research in bone: a review. Eur Cell Mater. ;13:1–10. https://doi.org/10.22203/ecm.v013a01. PMID: 17334975

  12. Newman E, Turner AS, Wark JD (1995) The potential of sheep for the study of osteopenia: current status and comparison with other animal models. Bone 16:277–284

    Article  Google Scholar 

  13. Castaneda S, Largo R, Calvo E, Rodriguez-Salvanes F, Marcos ME, Diaz-Curiel M, Herrero-Beaumont G (2006) Bone mineral measurements of subchondral and trabecular bone in healthy and osteoporotic rabbits. Skeletal Radiol 35:34–41

    Article  CAS  PubMed  Google Scholar 

  14. Cheng G, Li Z, Wan Q, Lv K, Li D, Xing X, Li Z (2015) A novel animal model treated with tooth extraction to repair the full-thickness defects in the mandible of rabbits. J Surg Res 194(2):706–716 Epub 2014 Nov 14. PMID: 25491176

    Article  PubMed  Google Scholar 

  15. Jianqi H, Hong H, Lieping S, Genghua G (2002) Comparison of calcium alginate film with collagen membrane for guided bone regeneration in mandibular defects in rabbits. J Oral Maxillofac Surg. ;60(12):1449-54. https://doi.org/10.1053/joms.2002.36108. PMID: 12465009

  16. Kazakos K, Lyras DN, Thomaidis V, Agrogiannis G, Botaitis S, Drosos G, Kokka A, Verettas D (2011) Application of PRP gel alone or in combination with guided bone regeneration does not enhance bone healing process: an experimental study in rabbits. J Craniomaxillofac Surg 39(1):49–53 Epub 2010 Apr 24. PMID: 20456969

    Article  PubMed  Google Scholar 

  17. Wang Y, Zhang X, Mei S, Li Y, Khan AA, Guan S, Li X (2023) Determination of critical-sized defect of mandible in a rabbit model: micro-computed tomography, and histological evaluation. Heliyon 9(7):e18047. https://doi.org/10.1016/j.heliyon.2023.e18047PMID: 37539284; PMCID: PMC10393617

    Article  PubMed  PubMed Central  Google Scholar 

  18. Sakaguchi R, Xavier SP, Morinaga K, Botticelli D, Silva ER, Nakajima Y, Baba S (2023) Histological comparison of Collagenated Cancellous equine bone blocks used as inlay or onlay for lateral bone augmentation in rabbits. Mater (Basel) 16(20):6742. https://doi.org/10.3390/ma16206742PMID: 37895725; PMCID: PMC10608602Xxxxxxx

    Article  CAS  Google Scholar 

  19. Asano A, Xavier SP, Ricardo Silva E, Morinaga K, Botticelli D, Nakajima Y, Baba S Critical-sized marginal defects around implants treated with xenografts in rabbits. Accepted for publication in Oral Maxillofac Surg

  20. Botticelli D, Berglundh T, Lindhe J (2004) Resolution of bone defects of varying dimension and configuration in the marginal portion of the peri-implant bone. An experimental study in the dog. J Clin Periodontol. ;31(4):309 – 17. https://doi.org/10.1111/j.1600-051X.2004.00502.x. PMID: 15016260

  21. Faul F, Erdfelder E, Buchner A, Lang AG (2009) Statistical power analyses using G*Power 3.1: tests for correlation and regression analyses. Behav Res Methods. ;41(4):1149-60. https://doi.org/10.3758/BRM.41.4.1149. PMID: 19897823

  22. Faul F, Erdfelder E, Lang AG, Buchner A (2007) G*Power 3: a flexible statistical power analysis program for the social, be-havioral, and biomedical sciences. Behav Res Methods. ;39(2):175 – 91. https://doi.org/10.3758/bf03193146. PMID: 17695343

  23. Kotagudda Ranganath S, Schlund M, Delattre J, Ferri J, Chai F (2022) Bilateral double site (calvarial and mandibular) critical-size bone defect model in rabbits for evaluation of a craniofacial tissue engineering constructs. Mater Today Bio 14:100267. https://doi.org/10.1016/j.mtbio.2022.100267

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Wang Y, Zhang X, Mei S, Li Y, Khan AA, Guan S, Li X (2023) Determination of critical-sized defect of mandible in a rabbit model: micro-computed tomography, and histological evaluation. Heliyon 9(7):e18047. https://doi.org/10.1016/j.heliyon.2023.e18047

    Article  PubMed  PubMed Central  Google Scholar 

  25. Carmagnola D, Berglundh T, Lindhe J (2002) The effect of a fibrin glue on the integration of Bio-Oss with bone tissue. A ex-perimental study in labrador dogs. J Clin Periodontol. ;29(5):377 – 83. https://doi.org/10.1034/j.1600-051x.2002.290501.x. PMID: 12060419

  26. Cardaropoli G, Araújo M, Hayacibara R, Sukekava F, Lindhe J (2005) Healing of extraction sockets and surgically produced - augmented and non-augmented - defects in the alveolar ridge. An experimental study in the dog. J Clin Periodontol. ;32(5):435 – 40. https://doi.org/10.1111/j.1600-051X.2005.00692.x. PMID: 15842256

  27. Botticelli D, Berglundh T, Buser D, Lindhe J (2003) Appositional bone formation in marginal defects at implants. Clin Oral Implants Res. ;14(1):1–9. https://doi.org/10.1034/j.1600-0501.2003.140101.x. PMID: 12562359

  28. Botticelli D, Berglundh T, Buser D, Lindhe J (2003) The jumping distance revisited: An experimental study in the dog. Clin Oral Implants Res. ;14(1):35–42. https://doi.org/10.1034/j.1600-0501.2003.140105.x. PMID: 12562363

  29. Cardaropoli G, Araújo M, Lindhe J (2003) Dynamics of bone tissue formation in tooth extraction sites. An experimental study in dogs. J Clin Periodontol. ;30(9):809 – 18. https://doi.org/10.1034/j.1600-051x.2003.00366.x. PMID: 12956657

  30. Araújo MG, Lindhe J (2005) Dimensional ridge alterations following tooth extraction. An experimental study in the dog. J Clin Periodontol. ;32(2):212-8. https://doi.org/10.1111/j.1600-051X.2005.00642.x. PMID: 15691354

  31. Scala A, Lang NP, Schweikert MT, de Oliveira JA, Rangel-Garcia I Jr, Botticelli D (2014) Sequential healing of open extraction sockets. An experimental study in monkeys. Clin Oral Implants Res. ;25(3):288–295. https://doi.org/10.1111/clr.12148. Epub 2013 Apr 1. PMID: 23551527

  32. Akimoto K, Becker W, Persson R, Baker DA, Rohrer MD, O’Neal RB (1999 May-Jun) Evaluation of titanium implants placed into simulated extraction sockets: a study in dogs. Int J Oral Maxillofac Implants 14(3):351–360 PMID: 10379108

  33. Botticelli D, Berglundh T, Persson LG, Lindhe J (2005) Bone regeneration at implants with turned or rough surfaces in self-contained defects. An experimental study in the dog. J Clin Periodontol. ;32(5):448 – 55. https://doi.org/10.1111/j.1600-051X.2005.00693.x. PMID: 15842258

  34. Li J, Zheng Y, Yu Z, Kankala RK, Lin Q, Shi J, Chen C, Luo K, Chen A, Zhong Q (2023) Surface-modified titanium and titanium-based alloys for improved osteogenesis: a critical review. Heliyon 10(1):e23779 PMID: 38223705; PMCID: PMC10784177

    Article  PubMed  PubMed Central  Google Scholar 

  35. Liang J, Lu X, Zheng X, Li YR, Geng X, Sun K, Cai H, Jia Q, Jiang HB, Liu K (2023) Modification of titanium orthopedic implants with bioactive glass: a systematic review of in vivo and in vitro studies. Front Bioeng Biotechnol 11:1269223. https://doi.org/10.3389/fbioe.2023.1269223PMID: 38033819; PMCID: PMC10686101

    Article  PubMed  PubMed Central  Google Scholar 

  36. Yang S, Jiang W, Ma X, Wang Z, Sah RL, Wang J, Sun Y (2023) Nanoscale morphologies on the surface of 3D-Printed Titanium implants for Improved Osseointegration: a systematic review of the literature. Int J Nanomed 18:4171–4191 PMID: 37525692; PMCID: PMC10387278

    Article  CAS  Google Scholar 

  37. Scarano A, Orsini T, Di Carlo F, Valbonetti L, Lorusso F (2021) Graphene-Doped Poly (Methyl-Methacrylate) (Pmma) implants: a Micro-CT and histomorphometrical study in rabbits. Int J Mol Sci 22(3):1441. https://doi.org/10.3390/ijms22031441PMID: 33535482; PMCID: PMC7867091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Rahmani R, Lyubartsev AP (2023) Biomolecular Adsorprion at ZnS nanomaterials: a Molecular Dynamics Simulation Study of the Adsorption preferences, effects of the Surface curvature and coating. Nanomaterials (Basel) 13(15):2239. https://doi.org/10.3390/nano13152239PMID: 37570556; PMCID: PMC10421200

    Article  CAS  PubMed  Google Scholar 

  39. Araújo MG, Sonohara M, Hayacibara R, Cardaropoli G, Lindhe J (2002) Lateral ridge augmentation by the use of grafts comprised of autologous bone or a biomaterial. An experiment in the dog. J Clin Periodontol. ;29(12):1122-31. https://doi.org/10.1034/j.1600-051x.2002.291213.x. PMID: 12492915

  40. Santis E, Lang NP, Favero G, Beolchini M, Morelli F, Botticelli D (2015) Healing at mandibular block-grafted sites. An experimental study in dogs. Clin Oral Implants Res 26(5):516–522. https://doi.org/10.1111/clr.12434Epub 2014 Jun 12. PMID: 24921198

    Article  PubMed  Google Scholar 

  41. Kanayama M, Botticelli D, Apaza Alccayhuaman KA, Yonezawa D, Silva ER, Xavier SP (2021) Jul-Aug;36(4):703–714 The Impact on the Healing of Bioactivation with Argon Plasma of a Xenogeneic Graft with Adequate Fixation but Poor Adaptation to the Recipient Site: An Experimental Study in Rabbits. Int J Oral Maxillofac Implants. https://doi.org/10.11607/jomi.8695. PMID: 34411209

  42. Herford AS, Boyne PJ (2008) Reconstruction of mandibular continuity defects with bone morphogenetic protein-2 (rhBMP-2). J Oral Maxillofac Surg 66:616–624

    Article  PubMed  Google Scholar 

  43. Chim H, Gosain AK (2009) Biomaterials in craniofacial surgery: experimental studies and clinical application. J Craniofac Surg 20:29–33

    Article  PubMed  Google Scholar 

  44. Misch CE, Qu Z, Bidez MW (1999) Mechanical properties of trabecular bone in the human mandible: implications for dental implant treatment planning and surgical placement. J Oral Maxillofac Surg 57:700–706 discussion 706-8

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Dr. Vitor Ferreira Balan for the surgical procedures and Mr. Sebas-tiao Blanco (University of São Paulo, Faculty of Dentistry of Ribeirão Preto) for processing the histological slides. The scientific contribution in the histological assessment by Dr. Alí Karol Apaza Alccayhuaman (Department of Oral Biology, Medical University of Vienna, 1090 Vienna, Austria) was greatly appreciated. The implants were donated by Leader Medica, Padua, Italy.

Funding

The study was economically supported by ARDEC Academy, Italy.

Author information

Authors and Affiliations

Authors

Contributions

A.M. contributed in the conceptualization, methodology, formal analysis, data curation, writing the original draft and reviewing the final version of the article.S.P.X. reviewing the final version of the article in the conceptualization, methodology, and investigation.E.R.S. in investigation.K.M. contributed contributed in conceptualization and reviewing and editing the article.D.B. contributed contributed in conceptualization, methodology, formal analysis, data curation, writing the original draft and reviewing and editing the article, project administration and funding acquisition.Y.N. contributed in methodology, project administration and funding acquisition.S.B. contributed in conceptualization, supervision of the project, reviewing and editing the article.All authors have read and approved the article before submission for publication.

Corresponding author

Correspondence to Daniele Botticelli.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Morimoto, A., Porfirio Xavier, S., Ricardo Silva, E. et al. Critical-sized marginal defects around implants in the rabbit mandible. Oral Maxillofac Surg (2024). https://doi.org/10.1007/s10006-024-01233-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10006-024-01233-2

Keywords

Navigation