Evaluation of Vertical Guided Bone Regeneration Using a Particulate Form of Experimental Bioactive Glass in a Rabbit: A Case Report with Literature Review

CASE REPORT
Timur V. Melkumyan, Nuritdin Kh. Kamilov, Fatima Yu. Daurova, Angela D. Dadamova

 
International Journal of Biomedicine. 2021;11(3):308-314.
DOI: 10.21103/Article11(3)_CR2
Originally published September 9, 2021

Abstract: 

Background: There are a large number of different types of bone-grafting materials that are used for the regeneration of atrophied alveolar ridges in order to make dental implantation possible. However, available surgical techniques and materials for bone augmentation do not contribute to the achievement of the desired reliable results and require a search for new solutions to an existing problem. A group of synthetic osteoplastic materials based on bioactive glass (BAG) may become a matter of choice in bone tissue regeneration because of special osteogenic properties. The aim of this study was to visually and histologically evaluate the behavior of an experimental BAG in rabbit tibia bone samples, which were collected from the animal 6 weeks after filling the bone defects.
Methods and Results: The observation was carried out on one outbred rabbit whose tibia bone defects were filled with an experimental osteoplastic material based on the BAG. The chemical composition of the experimental osteoplastic material included SiO2 (41%), Na2O (21%), CaO (28.5%), P2O5 (6%), CaF2 (1.5%), MgO (1%), Al2O3 (1%). For histological analysis, H&E staining of paraffin-embedded tissues was performed according to the standard technique. Light microscopy of tissue samples was performed using a Leitz HM-LUX microscope (Germany).
Six weeks after filling the bone defects, a strong bond between the augmented hard tissue and rabbit tibia was recognized.     Also, a dense fusion of adjacent soft tissues with a newly formed bone without signs of chronic inflammation or graft particles in granular tissue was noted. Microscopic examination of the stained sections showed the presence of mature viable BT with a uniform distribution of osteocytes. Also, residual fragments of the degraded biomaterial surrounded by the fibers of a woven bone were revealed in several slices.
Conclusion: In accordance with the results of this experiment, it can be concluded that the usage of BAG related to the system SiO2(41%)-Na2O(21%)-CaO(28.5%)-P2O5(6%)-CaF2(1.5%)-MgO(1%)-Al2O3(1%) may increase the volume of bone without application of barrier membrane. However, further research involving more animals needs to be done to estimate the scientific significance of the obtained data and to evaluate the mechanical properties of augmented bone.

Keywords: 
bioactive glass • bone tissue • vertical guided bone regeneration
References: 
  1. Zimmer CM, Zimmer WM, Williams J, Liesener J. Public awareness and acceptance of dental implants. Int J Oral Maxillofac Implants. 1992 Summer;7(2):228-32. 
  2. 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 Dec;97(13):1424-1430. doi: 10.1177/0022034518792567. 
  3. Pope JD. Implantology Techniques to Avoid Complications. Decisions in Dentistry. February 2020;6(2):17–18,21–22.
  4. Greenberg AM. Digital technologies for dental implant treatment planning and guided surgery. Oral Maxillofac Surg Clin North Am. 2015 May;27(2):319-40. doi: 10.1016/j.coms.2015.01.010. 
  5. Jabero M, Sarment DP. Advanced surgical guidance technology: a review. Implant Dent. 2006 Jun;15(2):135-42. doi: 10.1097/01.id.0000217790.68814.1e. 
  6. Xuereb M, Camilleri J, Attard NJ. Systematic review of current dental implant coating materials and novel coating techniques. Int J Prosthodont. 2015 Jan-Feb;28(1):51-9. doi: 10.11607/ijp.4124. 
  7. Schrott AR, Jimenez M, Hwang JW, Fiorellini J, Weber HP. Five-year evaluation of the influence of keratinized mucosa on peri-implant soft-tissue health and stability around implants supporting full-arch mandibular fixed prostheses. Clin Oral Implants Res. 2009 Oct;20(10):1170-7. doi: 10.1111/j.1600-0501.2009.01795.x. 
  8. Mittal Y, Jindal G, Garg S. Bone manipulation procedures in dental implants. Indian J Dent. 2016 Apr-Jun;7(2):86-94. doi: 10.4103/0975-962X.184650. 
  9. Liu J, Kerns DG. Mechanisms of guided bone regeneration: a review. Open Dent J. 2014 May 16;8:56-65. doi: 10.2174/1874210601408010056.
  10. Nyman S, Lindhe J, Karring T, Rylander H. New attachment following surgical treatment of human periodontal disease. J Clin Periodontol. 1982 Jul;9(4):290-6. doi: 10.1111/j.1600-051x.1982.tb02095.x.
  11. Caballé-Serrano J, Munar-Frau A, Ortiz-Puigpelat O, Soto-Penaloza D, Peñarrocha M, Hernández-Alfaro F. On the search of the ideal barrier membrane for guided bone regeneration. J Clin Exp Dent. 2018 May 1;10(5):e477-e483. doi: 10.4317/jced.54767. PMID: 29849973; 
  12. Wessing B, Emmerich M, Bozkurt A. Horizontal Ridge Augmentation with a Novel Resorbable Collagen Membrane: A Retrospective Analysis of 36 Consecutive Patients. Int J Periodontics Restorative Dent. 2016 Mar-Apr;36(2):179-87. doi: 10.11607/prd.2065. 
  13. Urban IA, Nagursky H, Lozada JL, Nagy K. Horizontal ridge augmentation with a collagen membrane and a combination of particulated autogenous bone and anorganic bovine bone-derived mineral: a prospective case series in 25 patients. Int J Periodontics Restorative Dent. 2013 May-Jun;33(3):299-307. doi: 10.11607/prd.1407. 
  14. Jensen AT, Jensen SS, Worsaae N. Complications related to bone augmentation procedures of localized defects in the alveolar ridge. A retrospective clinical study. Oral Maxillofac Surg. 2016 Jun;20(2):115-22. doi: 10.1007/s10006-016-0551-8. 
  15. Rocchietta I, Fontana F, Simion M. Clinical outcomes of vertical bone augmentation to enable dental implant placement: a systematic review. J Clin Periodontol. 2008 Sep;35(8 Suppl):203-15. doi: 10.1111/j.1600-051X.2008.01271.x.
  16. Merli M, Migani M, Bernardelli F, Esposito M. Vertical bone augmentation with dental implant placement: efficacy and complications associated with 2 different techniques. A retrospective cohort study. Int J Oral Maxillofac Implants. 2006 Jul-Aug;21(4):600-6.
  17. Merli M, Migani M, Esposito M. Vertical ridge augmentation with autogenous bone grafts: resorbable barriers supported by ostheosynthesis plates versus titanium-reinforced barriers. A preliminary report of a blinded, randomized controlled clinical trial. Int J Oral Maxillofac Implants. 2007 May-Jun;22(3):373-82. 
  18. Aghaloo TL, Moy PK. Which hard tissue augmentation techniques are the most successful in furnishing bony support for implant placement? Int J Oral Maxillofac Implants. 2007;22 Suppl:49-70. Erratum in: Int J Oral Maxillofac Implants. 2008 Jan-Feb;23(1):56. 
  19. Jensen AT, Jensen SS, Worsaae N. Complications related to bone augmentation procedures of localized defects in the alveolar ridge. A retrospective clinical study. Oral Maxillofac Surg. 2016 Jun;20(2):115-22. doi: 10.1007/s10006-016-0551-8. 
  20. Aloy-Prósper A, Peñarrocha-Oltra D, Peñarrocha-Diago M, Peñarrocha-Diago M. The outcome of intraoral onlay block bone grafts on alveolar ridge augmentations: a systematic review. Med Oral Patol Oral Cir Bucal. 2015 Mar 1;20(2):e251-8. doi: 10.4317/medoral.20194. 
  21. Urban IA, Saleh MHA, Ravidà A, Forster A, Wang HL, Barath Z. Vertical bone augmentation utilizing a titanium-reinforced PTFE mesh: A multi-variate analysis of influencing factors. Clin Oral Implants Res. 2021 Jul;32(7):828-839. doi: 10.1111/clr.13755. 
  22. Cucchi A, Vignudelli E, Fiorino A, Pellegrino G, Corinaldesi G. Vertical ridge augmentation (VRA) with Ti-reinforced d-PTFE membranes or Ti meshes and collagen membranes: 1-year results of a randomized clinical trial. Clin Oral Implants Res. 2021 Jan;32(1):1-14. doi: 10.1111/clr.13673. 
  23. Cucchi A, Vignudelli E, Napolitano A, Marchetti C, Corinaldesi G. Evaluation of complication rates and vertical bone gain after guided bone regeneration with non-resorbable membranes versus titanium meshes and resorbable membranes. A randomized clinical trial. Clin Implant Dent Relat Res. 2017 Oct;19(5):821-832. doi: 10.1111/cid.12520. 
  24. Tessier P, Kawamoto H, Posnick J, Raulo Y, Tulasne JF, Wolfe SA. Complications of harvesting autogenous bone grafts: a group experience of 20,000 cases. Plast Reconstr Surg. 2005 Oct;116(5 Suppl):72S-73S. doi: 10.1097/01.prs.0000173841.59063.7e. 
  25. Maiorana C, Beretta M, Salina S, Santoro F. Reduction of autogenous bone graft resorption by means of bio-oss coverage: a prospective study. Int J Periodontics Restorative Dent. 2005 Feb;25(1):19-25. PMID: 15736775.
  26. Sakkas A, Ioannis K, Winter K, Schramm A, Wilde F. Clinical results of autologous bone augmentation harvested from the mandibular ramus prior to implant placement. An analysis of 104 cases. GMS Interdiscip Plast Reconstr Surg DGPW. 2016 Oct 6;5:Doc21. doi: 10.3205/iprs000100. 
  27. Kaing L, Grubor D, Chandu A. Assessment of bone grafts placed within an oral and maxillofacial training programme for implant rehabilitation. Aust Dent J. 2011 Dec;56(4):406-11. doi: 10.1111/j.1834-7819.2011.01369.x.
  28. Draenert FG, Kämmerer PW, Berthold M, Neff A. Complications with allogeneic, cancellous bone blocks in vertical alveolar ridge augmentation: prospective clinical case study and review of the literature. Oral Surg Oral Med Oral Pathol Oral Radiol. 2016 Aug;122(2):e31-43. doi: 10.1016/j.oooo.2016.02.018.
  29. Starch-Jensen T, Deluiz D, Tinoco EMB. Horizontal Alveolar Ridge Augmentation with Allogeneic Bone Block Graft Compared with Autogenous Bone Block Graft: a Systematic Review. J Oral Maxillofac Res. 2020 Mar 31;11(1):e1. doi: 10.5037/jomr.2020.11101.
  30. Ang CY, Yew AK, Tay DK, Chia SL, Yeo SJ, Lo NN, Chin PL. Reducing allograft contamination and disease transmission: intraosseous temperatures of femoral head allografts during autoclaving. Singapore Med J. 2014 Oct;55(10):526-8. doi: 10.11622/smedj.2014135.
  31. Fishman JA, Greenwald MA, Grossi PA. Transmission of infection with human allografts: essential considerations in donor screening. Clin Infect Dis. 2012 Sep;55(5):720-7. doi: 10.1093/cid/cis519. 
  32. Giraddi GB, Saifi AM. Bone Ring Augmentation Around Immediate Implants: A Clinical and Radiographic Study. Ann Maxillofac Surg. 2017 Jan-Jun;7(1):92-97. doi: 10.4103/ams.ams_58_17.
  33. Saulacić N, Somosa Martín M, de Los Angeles Leon Camacho M, García García A. Complications in alveolar distraction osteogenesis: A clinical investigation. J Oral Maxillofac Surg. 2007 Feb;65(2):267-74. doi: 10.1016/j.joms.2006.03.049. 
  34. Ettl T, Gerlach T, Schüsselbauer T, Gosau M, Reichert TE, Driemel O. Bone resorption and complications in alveolar distraction osteogenesis. Clin Oral Investig. 2010 Oct;14(5):481-9. doi: 10.1007/s00784-009-0340-y.
  35. Zhang Z, Gan Y, Guo Y, Lu X, Li X. Animal models of vertical bone augmentation (Review). Exp Ther Med. 2021 Sep;22(3):919. doi: 10.3892/etm.2021.10351. 
  36. Roberts TT, Rosenbaum AJ. Bone grafts, bone substitutes and orthobiologics: the bridge between basic science and clinical advancements in fracture healing. Organogenesis. 2012 Oct-Dec;8(4):114-24. doi: 10.4161/org.23306. 
  37. Bellucci D, Sola A, Cannillo V. Hydroxyapatite and tricalcium phosphate composites with bioactive glass as second phase: State of the art and current applications. J Biomed Mater Res A. 2016 Apr;104(4):1030-56. doi: 10.1002/jbm.a.35619.
  38. Karadjian M, Essers C, Tsitlakidis S, Reible B, Moghaddam A, Boccaccini AR, Westhauser F. Biological Properties of Calcium Phosphate Bioactive Glass Composite Bone Substitutes: Current Experimental Evidence. Int J Mol Sci. 2019 Jan 14;20(2):305. doi: 10.3390/ijms20020305. 
  39. Hench LL, West JK. Biological applications of bioactive glasses. Life Chem Reports. 1996;13:187–241.
  40. Hench LL, Xynos ID, Buttery LD, Polak JM. Bioactive materials to control cell cycle. Mater Res Innovations. 2000;3:313–23. 
  41. Xynos ID, Hukkanen MV, Batten JJ, Buttery LD, Hench LL, Polak JM. Bioglass 45S5 stimulates osteoblast turnover and enhances bone formation In vitro: implications and applications for bone tissue engineering. Calcif Tissue Int. 2000 Oct;67(4):321-9. doi: 10.1007/s002230001134. 
  42. Xynos ID, Edgar AJ, Buttery LD, Hench LL, Polak JM. Ionic products of bioactive glass dissolution increase proliferation of human osteoblasts and induce insulin-like growth factor II mRNA expression and protein synthesis. Biochem Biophys Res Commun. 2000 Sep 24;276(2):461-5. doi: 10.1006/bbrc.2000.3503.
  43. Tripathi H, Rath C, Kumar AS, Manna PP, Singh SP. Structural, physico-mechanical and in-vitro bioactivity studies on SiO2-CaO-P2O5-SrO-Al2O3 bioactive glasses. Mater Sci Eng C Mater Biol Appl. 2019 Jan 1;94:279-290. doi: 10.1016/j.msec.2018.09.041. 
  44. Deliormanlı AM. Synthesis and characterization of cerium- and gallium-containing borate bioactive glass scaffolds for bone tissue engineering. J Mater Sci Mater Med. 2015 Feb;26(2):67. doi: 10.1007/s10856-014-5368-0.
  45. Bejarano J, Boccaccini AR, Covarrubias C, Palza H. Effect of Cu- and Zn-Doped Bioactive Glasses on the In Vitro Bioactivity, Mechanical and Degradation Behavior of Biodegradable PDLLA Scaffolds. Materials (Basel). 2020 Jun 29;13(13):2908. doi: 10.3390/ma13132908.
  46. Tabia Z, El Mabrouk Kh, Bricha M, Nouneh Kh. Mesoporous bioactive glass nanoparticles doped with magnesium: drug delivery and acellular in vitro bioactivity. RSC Advances. 2019; 9(22):12232-12246. doi: 10.1039/C9RA01133A 
  47. Kim YJ, de Molon RS, Horiguti FR, Contador GP, Coelho MA, Mascarenhas VI, de Souza Faloni AP, Cirelli JA, Sendyk WR. Vertical Bone Augmentation Using Deproteinized Bovine Bone Mineral, Absorbable Collagen Sponge, and Recombinant Human Bone Morphogenetic Protein-2: An In Vivo Study in Rabbits. Int J Oral Maxillofac Implants. 2018 May/June;33(3):512–522. doi: 10.11607/jomi.5959.
  48. Queiroz TP, de Molon RS, Souza FÁ, Margonar R, Thomazini AH, Guastaldi AC, Hochuli-Vieira E. In vivo evaluation of cp Ti implants with modified surfaces by laser beam with and without hydroxyapatite chemical deposition and without and with thermal treatment: topographic characterization and histomorphometric analysis in rabbits. Clin Oral Investig. 2017 Mar;21(2):685-699. doi: 10.1007/s00784-016-1936-7.
  49. Faeda RS, Tavares HS, Sartori R, Guastaldi AC, Marcantonio E Jr. Biological performance of chemical hydroxyapatite coating associated with implant surface modification by laser beam: biomechanical study in rabbit tibias. J Oral Maxillofac Surg. 2009 Aug;67(8):1706-15. doi: 10.1016/j.joms.2009.03.046.
  50. Stoor P, Apajalahti S, Kontio R. Regeneration of Cystic Bone Cavities and Bone Defects With Bioactive Glass S53P4 in the Upper and Lower Jaws. J Craniofac Surg. 2017 Jul;28(5):1197-1205. doi: 10.1097/SCS.0000000000003649. PMID: 28538076.
  51. Malat TA, Glombitza M, Dahmen J, Hax PM, Steinhausen E. The Use of Bioactive Glass S53P4 as Bone Graft Substitute in the Treatment of Chronic Osteomyelitis and Infected Non-Unions - a Retrospective Study of 50 Patients. Z Orthop Unfall. 2018 Apr;156(2):152-159. doi: 10.1055/s-0043-124377.
  52. Trishala A, Jacob C. The anti-bacterial activity of bioactive glass. International Journal of Advanced Research. 2016;4(6):1070-1077
  53. Zhang D, Leppäranta O, Munukka E. Antibacterial effects and dissolution behaviour of six bioactive glasses. J Control Release. 2009;139:118–26. 
  54. Lindfors N, Geurts J, Drago L, Arts JJ, Juutilainen V, Hyvönen P, Suda AJ, Domenico A, Artiaco S, Alizadeh C, Brychcy A, Bialecki J, Romanò CL. Antibacterial Bioactive Glass, S53P4, for Chronic Bone Infections - A Multinational Study. Adv Exp Med Biol. 2017;971:81-92. doi: 10.1007/5584_2016_156. Erratum in: Adv Exp Med Biol. 2017;971:115-116.
  55. Axrap A, Wang J, Liu Y, Wang M, Yusuf A. Study on adhesion, proliferation and differentiation of osteoblasts promoted by new absorbable bioactive glass injection in vitro. Eur Rev Med Pharmacol Sci. 2016 Nov;20(22):4677-4681.
  56. Nordström EG, Sánchez Muñoz OL. Physics of bone bonding mechanism of different surface bioactive ceramic materials in vitro and in vivo. Biomed Mater Eng. 2001;11(3):221-31. 
  57. Margonar R, Queiroz TP, Luvizuto ER, Marcantonio É, Lia RC, Holzhausen M, Marcantonio-Júnior É. Bioactive glass for alveolar ridge augmentation. J Craniofac Surg. 2012 May;23(3):e220-2. doi: 10.1097/SCS.0b013e31824de5a4.
  58. Wang SA, Chen AY, Yu ZE, Huang ZJ, Wao YM. Alveolar ridge augmentation with bioactive glass ceramics: a histological study. J Oral Rehabil. 1989 May;16(3):229-39. doi: 10.1111/j.1365-2842.1989.tb01337.x.
  59. Rahaman MN, Day DE, Bal BS, Fu Q, Jung SB, Bonewald LF, Tomsia AP. Bioactive glass in tissue engineering. Acta Biomater. 2011 Jun;7(6):2355-73. doi: 10.1016/j.actbio.2011.03.016.
  60. Yukna RA, Evans GH, Aichelmann-Reidy MB, Mayer ET. Clinical comparison of bioactive glass bone replacement graft material and expanded polytetrafluoroethylene barrier membrane in treating human mandibular molar class II furcations. J Periodontol. 2001 Feb;72(2):125-33. doi: 10.1902/jop.2001.72.2.125. 

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Received July 24, 2021.
Accepted August 31, 2021.
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