Skip to main content

Advertisement

Log in

Analysis of bone formation and membrane resorption in guided bone regeneration using deproteinized bovine bone mineral versus calcium sulfate

  • Tissue Engineering Constructs and Cell Substrates
  • Original Research
  • Published:
Journal of Materials Science: Materials in Medicine Aims and scope Submit manuscript

Abstract

Guided Bone Regeneration (GBR) is a technique based on the use of a physical barrier that isolates the region of bone regeneration from adjacent tissues. The objective of this study was to compare GBR, adopting a critical-size defect model in rat calvaria and using collagen membrane separately combined with two filling materials, each having different resorption rates. A circular defect 8 mm in diameter was made in the calvaria of Wistar rats. The defects were then filled with calcium sulfate (CaS group) or deproteinized bovine bone mineral (DBBM group) and covered by resorbable collagen membrane. The animals were killed 15, 30, 45 and 60 days after the surgical procedure. Samples were collected, fixed in 4% paraformaldehyde and processed for paraffin embedding. The resultant sections were stained with H&E for histological and histomorphometric study. For the histomorphometric study, the area of membrane was quantified along with the amount of bone formed in the region of the membrane. Calcium sulfate was reabsorbed more rapidly compared to DBBM. The CaS group had the highest percentages of remaining membrane at 15, 30, 45 and 60 days, compared to the DBBM group. The DBBM group had the highest amount of new bone at 45 and 60 days compared to the CaS group. Based on these results, it was concluded that the type of filling material may influence both the resorption of collagen membrane and amount of bone formed.

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

Similar content being viewed by others

References

  1. Irinakis T, Tabesh M. Preserving the socket dimensions with bone grafting in single sites: an esthetic surgical approach when planning delayed implant placement. J Oral Implantol. 2007;33:156–63. https://doi.org/10.1563/0.824.1.

    Article  Google Scholar 

  2. Minabe M. A Critical review of the biologic rationale for Guided Tissue Regeneration. J Periodontol. 1991;62:171–9. https://doi.org/10.1902/jop.1991.62.3.171.

    Article  CAS  Google Scholar 

  3. Nyman S, Karring T, Lindhe J, Planten S. Healing following implantation of periodontitis affected roots into gingival connective tissue. J Clin Periodontol. 1980;7:394–401.

    Article  CAS  Google Scholar 

  4. Taga MLL, Granjeiro JM, Cestari TM, Taga R. Healing of critical-size cranial defects in guinea pigs using a bovine bone-derived resorbable membrane. Int J Oral Maxillofac Implants. 2008;23:427–36.

    Google Scholar 

  5. Thomaidis V, Kazakos K, Lyras DN, Dimitrakopoulos I, Lazaridis N, Karakasis D. et al. Comparative study of 5 different membranes for guided bone regeneration of rabbit mandibular defects beyond critical size. Med Sci Monit. 2008;14:67–73.

    Google Scholar 

  6. Chiapasco M, Zaniboni M. Clinical outcomes of GBR procedures to correct peri-implant dehiscences and fenestrations: a systematic review. Clin Oral Impl Res. 2009;20:113–23.

    Article  Google Scholar 

  7. Fontana F, Rocchietta I, Simion M. Clinical classification of complications in guided bone regeneration procedures by means of a nonresorbable membrane. Int J Periodo Rest. 2011;31:265–73. https://doi.org/10.1111/j.1600-0501.2009.01781.x.

    Article  Google Scholar 

  8. Jung RE, Fenner N, Hämmerle CHF, Zitzmann NU. Long-term outcome of implants placed with guided bone regeneration (GBR) using resorbable and non-resorbable membranes after 12-14 years. Clin Oral Impl Res. 2013;24:1065–73. https://doi.org/10.1111/j.1600-0501.2012.02522.x.

    Article  Google Scholar 

  9. Bunyaratavej P, Wang HL. Collagen membranes: a review. J Periodontol. 2001;72:215–29. https://doi.org/10.1902/jop.2001.72.2.215.

    Article  CAS  Google Scholar 

  10. Bornstein MM, Heynen G, Bosshardt DD, Buser D. Effect of two bioabsorbable barrier membranes on bone regeneration of standardized defects in calvarial bone: a comparative histomorphometric study in pigs. J Periodontol. 2009;80:1289–99. https://doi.org/10.1902/jop.2009.090075.

    Article  Google Scholar 

  11. von Arx T, Kurt B. Implant placement and simultaneous ridge augmentation using autogenous bone and a micro titanium mesh: a prospective clinical study with 20 implants. Clin Oral Impl Res. 1999;10:24–33.

    Article  Google Scholar 

  12. Lutz R, Neukam FW, Simion M, Schmitt CM. Long-term outcomes of bone augmentation on soft and hard tissue stability: a systematic review. Clin Oral Impl Res. 2015;26:103–22. https://doi.org/10.1111/clr.12635.

    Article  Google Scholar 

  13. Retzepi M, Donos N. Guided Bone Regeneration: biological principle and therapeutic applications. Clin Oral Impl Res. 2010;21:567–76. https://doi.org/10.1111/j.1600-0501.2010.01922.x.

    Article  Google Scholar 

  14. Baldini N, De Sanctis M, Ferrari M. Deproteinized bovine bone in periodontal and implant surgery. Dent Mater. 2011;27:61–70. https://doi.org/10.1016/j.dental.2010.10.017.

    Article  CAS  Google Scholar 

  15. Heinemann F, Hasan I, Schwahn C, Bourauel C, Mundt T. Bone level change of extraction sockets with Bio-Oss collagen and implant placement: A clinical study. Ann Anat. 2012;194:508–12. https://doi.org/10.1016/j.aanat.2011.11.012.

    Article  CAS  Google Scholar 

  16. Thomas MV, Puleo DA. Calcium sulfate: properties and clinical applications. J Biomed Mater Res Part B Appl Biomater. 2009;88B:597–610. https://doi.org/10.1002/jbm.b.31269.

    Article  CAS  Google Scholar 

  17. Turri A, Dahlin C. Comparative maxillary bone-defect healing by calcium sulphate or deproteinized bovine bone particles and extra cellular matrix membranes in a guided bone regeneration setting: an experimental study in rabbits. Clin Oral Impl Res. 2015;26:501–6. https://doi.org/10.1111/clr.12425.

    Article  Google Scholar 

  18. Martins TMA, Pavan AJ, Gavazzoni A, Bergamo ETP, Bonadio TGM, Weinand WR. Studying the behavior of calcium sulfate: bioactivity and solubility in simulated body fluid. Dent Press Implantol. 2015;9:58–65.

    Article  Google Scholar 

  19. Strocchi R, Orsini G, Iezzi G, Scarano A, Rubini C, Pecora G. et al. Bone regeneration with calcium sulfate: evidence for increased angiogenesis in rabbits. J Oral Impl. 2002;28:273–8. https://doi.org/10.1563/1548-1336(2002)028%3C0273:BRWCSE%3E2.3.CO;2.

    Article  Google Scholar 

  20. Dasmah A, Sennerby L, Rasmusson L, Hallman M. Intramembraneous bone tissue responses to calcium sulfate: an experimental study in the rabbit maxila. Clin Oral Impl Res. 2011;22:1404–8. https://doi.org/10.1111/j.1600-0501.2010.02129.x.

    Article  CAS  Google Scholar 

  21. Kokubo T, Takadama H. How useful is SBF in predicting in vivo bone bioactivity? Biomaterials. 2006;27:2907–15. https://doi.org/10.1016/j.biomaterials.2006.01.017.

    Article  CAS  Google Scholar 

  22. Mordenfeld A, Hallman M, Johansson CB, Albrektsson T. Histological and histomorphometrical analyses of biopsies harvested 11 years after maxillary sinus floor augmentation with deproteinized bovine and autogenous bone. Clin Oral Impl Res. 2010;21:961–70. https://doi.org/10.1111/j.1600-0501.2010.01939.x.

    Article  Google Scholar 

  23. Vajgel A, Mardas N, Farias BC, Petrie A, Cimões R, Donos N. A systematic review on the critical size defect model. Clin Oral Impl Res. 2014;25:879–93. https://doi.org/10.1111/clr.12194.

    Article  Google Scholar 

  24. Song JM, Shin SH, Kim YD, Lee JY, Baek YJ, Yoon SY. et al. Comparative study of chitosan/fibroin-hydroxyapatite and collagen membranes for guided bone regeneration in rat calvarial defects: micro-computed tomography analysis. Int J Oral Sci. 2014;6:87–93. https://doi.org/10.1038/ijos.2014.16.

    Article  CAS  Google Scholar 

  25. Silveira EMV. Mecanismos envolvidos na resposta imune e inflamatória frente à implantação de membrana de cortical óssea bovina no tecido subcutâneo de camundongos: caracterização histomorfométrica, imunoenzimática e molecular. Bauru: Faculdade de Odontologia de Bauru, 2012, 40. https://doi.org/10.11606/T.25.2012.tde-05112012-195013

  26. Costa NMF, Yassuda DH, Sader MS, Fernandes GVO, Soares GDA, Granjeiro JM. Osteogenic effect of tricalcium phosphate substituted by magnesium associated with Genderm® membrane in rat calvarial defect model. Mater Sci Eng C Mater Biol Appl. 2016;61:63–71. https://doi.org/10.1016/j.msec.2015.12.003.

    Article  Google Scholar 

  27. Sandberg E, Dahlin C, Linde A. Bone regeneration by the osteopromotion technique using bioabsorbable membranes: an experimental study in rats. J Oral Maxillofac Surg. 1993;51:1106–14.

    Article  CAS  Google Scholar 

  28. Zelin G, Gritli-Linde A, Linde A. Healing of mandibular defects with different biodegradable and non-biodegradable membranes: an experimental study in rats. Biomaterials. 1995;16:601–9.

    Article  Google Scholar 

  29. Zahedi S, Legrand R, Brunel G, Albert A, Dewe W, Coumans B. et al. Evaluation of a diphenylphosphorylazide-crosslinked collagen membrane for guided bone regeneration in mandibular defects in rats. J Periodontol. 1998;69:1238–46. https://doi.org/10.1902/jop.1998.69.11.1238.

    Article  CAS  Google Scholar 

  30. Mundell RD, Mooney MP, Siegel MI, Losken A. Osseous guided tissue regeneration using a collagen barrier membrane. J Oral Maxillofac Surg. 1993;51:1004–12.

    Article  CAS  Google Scholar 

  31. Lundgren AK, Sennerby L, Lundgren D. Guided jaw-bone regeneration using an experimental rabbit model. Int J Oral Maxillofac Surg. 1998;27:135–40.

    Article  CAS  Google Scholar 

  32. Bernabé PF, Gomes-Filho JE, Cintra LT, Moretto MJ, Lodi CS, Nery MJ. et al.Histologic evaluation of the use of membrane, bone graft, and MTA in apical surgery. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010;109:309–14.https://doi.org/10.1016/j.tripleo.2009.07.019.

    Article  Google Scholar 

  33. Zitzmann NU, Naef R, Schärer P. Resorbable versus nonresorbable membranes in combination with Bio-Oss for guided bone regeneration. Int J Oral Maxillofac Implants. 1997;12:844–52.

    CAS  Google Scholar 

  34. Hürzeler MB, Kohal RJ, Naghshbandi J, Mota LF, Conradt J, Hutmacher D. et al. Evaluation of a new bioresorbable barrier to facilitate guided bone regeneration around exposed implant threads. An experimental study in the monkey. Int J Oral Maxillofac Surg. 1998;27:315–20.

    Article  Google Scholar 

  35. Orellana BR, Hilt JZ, Puleo DA. Drug release from calcium sulfate-based composites. J Biomed Mater Res Part B Appl Biomater. 2015;103B:135–42. https://doi.org/10.1002/jbm.b.33181.

    Article  CAS  Google Scholar 

  36. Al Ruhaimi KA. Effect of adding resorbable calcium sulfate to grafting materials on early bone regeneration in osseous defects in rabbits. Int J Oral Maxillofac Implants. 2000;15:859–64.

    CAS  Google Scholar 

  37. Slater N, Dasmah A, Sennerby L, Hallman M, Piattelli A, Sammons R. Back-scatterred electron imaging and elemental microanalysis of retrieved bone tissue following maxillary sinus floor augmentation with calcium sulphate. Clin Oral Impl Res. 2008;19:814–22. https://doi.org/10.1111/j.1600-0501.2008.01550.x.

    Article  Google Scholar 

  38. Ricci J, Alexander H, Nadkarni P, Hawkins M, Turner J, Rosenblum S et al. Biological mechanisms of calcium sulfate replacement by bone. In: Davies JE Bone engineering. Toronto: Em2 Inc, Ch. 30, 2000; 332–44.

  39. Walsh WR, Morberg P, Yu Y, Yang JL, Haggard W, Sheat PC. et al. Response of a calcium sulfate bone graft substitute in a confined cancellous defect. Clin Orthop Relat Res. 2003;406:228–36. https://doi.org/10.1097/01.blo.0000030062.92399.6a.

    Article  Google Scholar 

  40. Carinci F, Piattelli A, Stabellini G, Palmieri A, Scapoli L, Laino G. et al. Calcium sulfate: analysis of MG63 osteoblast-like cell response by means of a microarray technology. J Biomed Mater Res B Appl Biomater. 2004;71B:260–7. https://doi.org/10.1002/jbm.b.30133.

    Article  CAS  Google Scholar 

  41. Dasmah A, Hallman M, Sennerby L, Rasmusson L. A clinical and histological case series study on calcium sulfate for maxillary sinus floor augmentation and delayed placement of dental implants. Clin Implant Dent Relat Res. 2012;14:259–65. https://doi.org/10.1111/j.1708-8208.2009.00249.x.

    Article  Google Scholar 

  42. Pang C, Ding Y, Zhou H, Qin R, Hou R, Zhang G. et al. Alveolar ridge preservation with deproteinized bovine bone graft and collagen membrane and delayed implants. J Craniofac Surg. 2014;25:1698–702. https://doi.org/10.1097/SCS.0000000000000887.

    Article  Google Scholar 

  43. Owens KW, Yukna RA. Collagen membrane resorption in dogs: a comparative study. Implant Dent. 2001;10:48–58.

    Article  Google Scholar 

  44. Kodama T, Minabe M, Hori T, Watanabe Y. The effect of concentrations of collagen barrier of periodontal wound healing. J Periodontol. 1989;60:205–10. https://doi.org/10.1902/jop.1989.60.4.205.

    Article  CAS  Google Scholar 

  45. Hyder P, Dowell P, Singh G, Dolby AE. Freeze-dried, cross-linked bovine type I collagen analysis of properties. J Periodontol. 1992;63:182–6. https://doi.org/10.1902/jop.1992.63.3.182.

    Article  CAS  Google Scholar 

  46. Kozlovsky A, Aboodi G, Moses O, Tal H, Artzi Z, Weinreb M. et al. Bio-degradation of a resorbable collagen membrane (Bio-Gide) applied in a double-layer technique in rats. Clin Oral Impl Res. 2009;20:1116–23. https://doi.org/10.1111/j.1600-0501.2009.01740.x.

    Article  Google Scholar 

  47. Accorsi-Mendonça T, Zambuzzi WF, Bramante CM, Cestari TM, Taga R, Sader M. et al. Biological monitoring of a xenomaterial for grafting: an evaluation in critical-size calvarial defects. J Mater Sci Mater Med. 2011;22:997–1004. https://doi.org/10.1007/s10856-011-4278-7.

    Article  Google Scholar 

  48. Taguchi Y, Amizuka N, Nakadate M, Ohnishi H, Fujii N, Oda K. et al. A histological evaluation for guided bone regeneration induced by a collagenous membrane. Biomaterials. 2005;26:6158–66. https://doi.org/10.1016/j.biomaterials.2005.03.023.

    Article  CAS  Google Scholar 

  49. Chou J, Komuro M, Hao J, Kuroda S, Hattori Y, Ben-Nissan B. et al. Bioresorbable zinc hydroxyapatite guided bone regeneration membrane for bone regeneration. Clin Oral Impl Res. 2016;27:354–60. https://doi.org/10.1111/clr.12520.

    Article  Google Scholar 

Download references

Acknowledgements

Maria Euride Carlos Cancino and Maria dos Anjos Fortunato for technical support.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Luzmarina Hernandes.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gavazzoni, A., Filho, L.I. & Hernandes, L. Analysis of bone formation and membrane resorption in guided bone regeneration using deproteinized bovine bone mineral versus calcium sulfate. J Mater Sci: Mater Med 29, 167 (2018). https://doi.org/10.1007/s10856-018-6167-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10856-018-6167-9

Navigation