Vertical Bone Augmentation Using Two Bioactive Glasses in a Rabbit Tibia Model: A Comparative Study with Literature Review

Timur V. Melkumyan, Nuritdin Kh. Kamilov, Zurab S. Khabadze, Maria K. Makeeva, Gerhard K. Seeberger, Sargis S. Gevorgyan, Angela D. Dadamova

 
International Journal of Biomedicine. 2023;13(3):148-153.
DOI: 10.21103/Article13(3)_OA17
Originally published September 5, 2023

Abstract: 

Background: Recently, synthetic materials based on bioactive glasses have been in special demand in dental implantology, which, according to the mechanism of their action, are not only osteo-conductors, but also osteo-inductors. Of even greater interest is the fact that the biological degradation of these materials causes alkalization of the area and inhibits the growth of many pathogens. Considering the unique properties of this group of osteoplastic fillers and the problems associated with healing after guided bone regeneration, this study aimed to compare the effectiveness of using bioactive glasses S53P4 and 45S5 when performing vertical bone augmentation in an experiment applying a rabbit tibia model.
Methods and Results: Six adult outbred rabbits aged from 1.5 to 2 years and weighing from 2.5 kg to 3.2 kg were used in the study. A titanium mesh was used to perform a true vertical guided bone regeneration technique. In each animal, two titanium tents were placed: one on the left tibia and one on the right tibia. On the left limb, empty spaces were filled with bioactive synthetic bone filler NovaBone® Morsels (USA); on the right limb, we used a mixture of bioactive glass Bonalive® granules CMF (Finland) and mineralized bone MedPark Bone-D XB (Bovine Xenograft, South Korea) in a ratio of 1:1. The quantity and quality of regenerated tissues were assessed after 8-10 weeks.
The NovaBone application has allowed a gain of 2.6±2.67 mm in extra-skeletal hard tissue growth. No signs of guided bone regeneration were observed in all cases of application of an osteoplastic mixture of Bonalive and Bone-D XB granules.
Conclusion: Within the limits of this study, it was found that the use of a mixture of bioactive glass Bonalive (S53P4) with bovine hydroxyapatite in a 1:1 ratio was not effective in vertically guided bone regeneration, but the application of NovaBone (45S5) could promote a new bone formation.

Keywords: 
bioactive glasses • vertical bone augmentation• rabbit tibia model
References: 
  1. Liaw K, Delfini RH, Abrahams JJ. Dental Implant Complications. Semin Ultrasound CT MR. 2015 Oct;36(5):427-33. doi: 10.1053/j.sult.2015.09.007. Epub 2015 Oct 9. PMID: 26589696.
  2. Brägger U, Aeschlimann S, Bürgin W, Hämmerle CH, Lang NP. Biological and technical complications and failures with fixed partial dentures (FPD) on implants and teeth after four to five years of function. Clin Oral Implants Res. 2001 Feb;12(1):26-34. doi: 10.1034/j.1600-0501.2001.012001026.x. PMID: 11168268.
  3. Klimecs V, Grishulonoks A, Salma I, Neimane L, Locs J, Saurina E, Skagers A. Bone Loss around Dental Implants 5 Years after Implantation of Biphasic Calcium Phosphate (HAp/βTCP) Granules. J Healthc Eng. 2018 Dec 5;2018:4804902. doi: 10.1155/2018/4804902. PMID: 30631412; PMCID: PMC6304842.
  4. 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 Aug;21(4):723-733. doi: 10.1111/cid.12800. Epub 2019 Jun 20. PMID: 31219661.
  5. Noelken R, Al-Nawas B. Bone regeneration as treatment of peri-implant disease: A narrative review. Clin Implant Dent Relat Res. 2023 Aug;25(4):696-709. doi: 10.1111/cid.13209. Epub 2023 May 17. PMID: 37199027.
  6. Melkumyan TV, Seeberger GK, Khabadze ZS, Kamilov NKh, Makeeva MK, Dashtieva MU, Sheraliea SSh, Dadamova AD. Air Abrasion of Titanium Dental Implants with Water-Soluble Powders: An In Vitro Study. International Journal of Biomedicine. 2022;12(3):428-432.
  7. Beschnidt SM, Cacaci C, Dedeoglu K, Hildebrand D, Hulla H, Iglhaut G, Krennmair G, Schlee M, Sipos P, Stricker A, Ackermann KL. Implant success and survival rates in daily dental practice: 5-year results of a non-interventional study using CAMLOG SCREW-LINE implants with or without platform-switching abutments. Int J Implant Dent. 2018 Nov 2;4(1):33. doi: 10.1186/s40729-018-0145-3. PMID: 30386925; PMCID: PMC6212375.
  8. Canullo L, Caneva M, Tallarico M. Ten-year hard and soft tissue results of a pilot double-blinded randomized controlled trial on immediately loaded post-extractive implants using platform-switching concept. Clin Oral Implants Res. 2017 Oct;28(10):1195-1203. doi: 10.1111/clr.12940. Epub 2016 Aug 8. PMID: 27502452.
  9. Paul N, Jyotsna S, Keshini MP. Alveolar Ridge Augmentation Using Autogenous Bone Graft and Platelet-Rich Fibrin to Facilitate Implant Placement. Contemp Clin Dent. 2022 Jan-Mar;13(1):90-94. doi: 10.4103/ccd.ccd_154_20. Epub 2022 Mar 23. PMID: 35466292; PMCID: PMC9030314.
  10. Soldatos N, Al Ramli R, Nelson-Rabe L, Ferguson B, Soldatos K, Weltman R. Vertical ridge augmentation (VRA) with the use of a cross-linked resorbable membrane, tenting screws, and a combination grafting technique: a report of three cases. Quintessence Int. 2021;0(0):328-339. doi: 10.3290/j.qi.a45424. PMID: 33117997.
  11. Melkumyan T.V. Kamilov N.Kh., Daurova F.Yu. Dadamova A.D. Evaluation of vertical guided bone regeneration using a particulate form of experimental bioactive glass in rabbit: a case report with literature review. International Journal of Biomedicine. 2021;11(3):308-314.
  12. Diomede F, Marconi GD, Fonticoli L, Pizzicanella J, Merciaro I, Bramanti P, Mazzon E, Trubiani O. Functional Relationship between Osteogenesis and Angiogenesis in Tissue Regeneration. Int J Mol Sci. 2020 May 3;21(9):3242. doi: 10.3390/ijms21093242. PMID: 32375269; PMCID: PMC7247346.
  13.  Liu J, Kerns DG. Mechanisms of guided bone regeneration: a review. Open Dent J. 2014 May 16;8:56-65. doi: 10.2174/1874210601408010056. PMID: 24894890; PMCID: PMC4040931.
  14. Mendoza-Azpur G, de la Fuente A, Chavez E, Valdivia E, Khouly I. Horizontal ridge augmentation with guided bone regeneration using particulate xenogenic bone substitutes with or without autogenous block grafts: A randomized controlled trial. Clin Implant Dent Relat Res. 2019 Aug;21(4):521-530. doi: 10.1111/cid.12740. Epub 2019 Mar 18. PMID: 30884111.
  15. Jung RE, Fenner N, Hämmerle CH, 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 Implants Res. 2013 Oct;24(10):1065-73. doi: 10.1111/j.1600-0501.2012.02522.x. Epub 2012 Jun 15. PMID: 22697628.
  16. Ronda M, Rebaudi A, Torelli L, Stacchi C. Expanded vs. dense polytetrafluoroethylene membranes in vertical ridge augmentation around dental implants: a prospective randomized controlled clinical trial. Clin Oral Implants Res. 2014 Jul;25(7):859-66. doi: 10.1111/clr.12157. Epub 2013 Apr 8. PMID: 23560678.
  17. Khojasteh A, Kheiri L, Motamedian SR, Khoshkam V. Guided Bone Regeneration for the Reconstruction of Alveolar Bone Defects. Ann Maxillofac Surg. 2017 Jul-Dec;7(2):263-277. doi: 10.4103/ams.ams_76_17. PMID: 29264297; PMCID: PMC5717906.
  18. Elnayef B, Porta C, Suárez-López Del Amo F, Mordini L, Gargallo-Albiol J, Hernández-Alfaro F. The Fate of Lateral Ridge Augmentation: A Systematic Review and Meta-Analysis. Int J Oral Maxillofac Implants. 2018 May/Jun;33(3):622-635. doi: 10.11607/jomi.6290. PMID: 29763500.
  19. Shamsoddin E, Houshmand B, Golabgiran M. Biomaterial selection for bone augmentation in implant dentistry: A systematic review. J Adv Pharm Technol Res. 2019 Apr-Jun;10(2):46-50. doi: 10.4103/japtr.JAPTR_327_18. PMID: 31041181; PMCID: PMC6474167.
  20. Garcia DC, Mingrone LE, de Sá MJC. Evaluation of Osseointegration and Bone Healing Using Pure-Phase β - TCP Ceramic Implant in Bone Critical Defects. A Systematic Review. Front Vet Sci. 2022 Jul 12;9:859920. doi: 10.3389/fvets.2022.859920. PMID: 35909673; PMCID: PMC9327785.
  21. Tomas M, Čandrlić M, Juzbašić M, Ivanišević Z, Matijević N, Včev A, Cvijanović Peloza O, Matijević M, Perić Kačarević Ž. Synthetic Injectable Biomaterials for Alveolar Bone Regeneration in Animal and Human Studies. Materials (Basel). 2021 May 26;14(11):2858. doi: 10.3390/ma14112858. PMID: 34073551; PMCID: PMC8197881.
  22. Zhao F, Yang Z, Xiong H, Yan Y, Chen X, Shao L. A bioactive glass functional hydrogel enhances bone augmentation via synergistic angiogenesis, self-swelling and osteogenesis. Bioact Mater. 2022 Oct 3;22:201-210. doi: 10.1016/j.bioactmat.2022.09.007. PMID: 36246665; PMCID: PMC9535384.
  23. Skallevold HE, Rokaya D, Khurshid Z, Zafar MS. Bioactive Glass Applications in Dentistry. Int J Mol Sci. 2019 Nov 27;20(23):5960. doi: 10.3390/ijms20235960. PMID: 31783484; PMCID: PMC6928922.
  24. Wang YY, Chatzistavrou X, Faulk D, Badylak S, Zheng L, Papagerakis S, Ge L, Liu H, Papagerakis P. Biological and bactericidal properties of Ag-doped bioactive glass in a natural extracellular matrix hydrogel with potential application in dentistry. Eur Cell Mater. 2015 Jun 20;29:342-55. doi: 10.22203/ecm.v029a26. PMID: 26091732.
  25. Bellantone M, Williams HD, Hench LL. Broad-spectrum bactericidal activity of Ag(2)O-doped bioactive glass. Antimicrob Agents Chemother. 2002 Jun;46(6):1940-5. doi: 10.1128/AAC.46.6.1940-1945.2002. PMID: 12019112; PMCID: PMC127232.
  26. Fernandes HR, Gaddam A, Rebelo A, Brazete D, Stan GE, Ferreira JMF. Bioactive Glasses and Glass-Ceramics for Healthcare Applications in Bone Regeneration and Tissue Engineering. Materials (Basel). 2018 Dec 12;11(12):2530. doi: 10.3390/ma11122530. PMID: 30545136; PMCID: PMC6316906.
  27. Baino F, Fiorilli S, Vitale-Brovarone C. Bioactive glass-based materials with hierarchical porosity for medical applications: Review of recent advances. Acta Biomater. 2016 Sep 15;42:18-32. doi: 10.1016/j.actbio.2016.06.033. Epub 2016 Jun 28. PMID: 27370907.
  28. Cannio M, Bellucci D, Roether JA, Boccaccini DN, Cannillo V. Bioactive Glass Applications: A Literature Review of Human Clinical Trials. Materials (Basel). 2021 Sep 20;14(18):5440. doi: 10.3390/ma14185440. PMID: 34576662; PMCID: PMC8470635.
  29. Van Gestel NA, Geurts J, Hulsen DJ, van Rietbergen B, Hofmann S, Arts JJ. Clinical Applications of S53P4 Bioactive Glass in Bone Healing and Osteomyelitic Treatment: A Literature Review. Biomed Res Int. 2015;2015:684826. doi: 10.1155/2015/684826. Epub 2015 Oct 4. PMID: 26504821; PMCID: PMC4609389.
  30. Steinhausen E, Lefering R, Glombitza M, Brinkmann N, Vogel C, Mester B, Dudda M. Bioactive glass S53P4 vs. autologous bone graft for filling defects in patients with chronic osteomyelitis and infected non-unions - a single center experience. J Bone Jt Infect. 2021 Jan 12;6(4):73-83. doi: 10.5194/jbji-6-73-2021. PMID: 34084694; PMCID: PMC8132459.
  31. Tarek Al MalatMartin Glombitza, Janosch Dahmen, Peter-Michael Hax, Eva Steinhausen. 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; 156(02): 152-159 DOI: 10.1055/s-0043-124377
  32. Kaya S, Cresswell M, Boccaccini AR. Mesoporous silica-based bioactive glasses for antibiotic-free antibacterial applications. Mater Sci Eng C Mater Biol Appl. 2018 Feb 1;83:99-107. doi: 10.1016/j.msec.2017.11.003. Epub 2017 Nov 10. PMID: 29208293.
  33. 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.

  34. Garcia J, Dodge A, Luepke P, Wang HL, Kapila Y, Lin GH. Effect of membrane exposure on guided bone regeneration: A systematic review and meta-analysis. Clin Oral Implants Res. 2018 Mar;29(3):328-338. doi: 10.1111/clr.13121. Epub 2018 Jan 24. PMID: 29368353.
  35. Urban IA, Monje A, Lozada JL, Wang HL. Long-term Evaluation of Peri-implant Bone Level after Reconstruction of Severely Atrophic Edentulous Maxilla via Vertical and Horizontal Guided Bone Regeneration in Combination with Sinus Augmentation: A Case Series with 1 to 15 Years of Loading. Clin Implant Dent Relat Res. 2017 Feb;19(1):46-55. doi: 10.1111/cid.12431. Epub 2016 May 30. PMID: 27238406.
  36. Thomas MV, Puleo DA. Infection, inflammation, and bone regeneration: a paradoxical relationship. J Dent Res. 2011 Sep;90(9):1052-61. doi: 10.1177/0022034510393967. Epub 2011 Jan 19. PMID: 21248364; PMCID: PMC3169879.
  37. Lee JS, Lee JS, Kang MH, Jung UW, Choi SH and Cho KS: Proof‐of‐concept study of vertical augmentation using block‐type allogenic bone grafts: A preclinical experimental study on rabbit calvaria. J Biomed Mater Res B Appl Biomater 106: 2700‐2707, 2018.
  38. Tamimi F, Torres J, Al‐Abedalla K, Lopez‐Cabarcos E, Alkhraisat MH, Bassett DC, Gbureck U and Barralet JE: Osseointegration of dental implants in 3D‐printed synthetic onlay grafts customized according to bone metabolic activity in recipient site. Biomaterials 35: 5436‐5445, 2014.
  39. Kim JW, Jung IH, Lee KI, Jung UW, Kim CS, Choi SH, Cho KS and Yun JH: Volumetric bone regenerative efficacy of biphasic calcium phosphate‐collagen composite block loaded with rhBMP‐2 in vertical bone augmentation model of a rabbit calvarium. J Biomed Mater Res A 100: 3304‐3313, 2012.       
  40. Sam G, Pillai BR. Evolution of Barrier Membranes in Periodontal Regeneration-"Are the third Generation Membranes really here?". J Clin Diagn Res. 2014 Dec;8(12):ZE14-7. doi: 10.7860/JCDR/2014/9957.5272. Epub 2014 Dec 5. PMID: 25654055; PMCID: PMC4316361.
  41. Rakhmatia YD, Ayukawa Y, Furuhashi A, Koyano K. Current barrier membranes: titanium mesh and other membranes for guided bone regeneration in dental applications. J Prosthodont Res. 2013 Jan;57(1):3-14. doi: 10.1016/j.jpor.2012.12.001. Epub 2013 Jan 21. PMID: 23347794.
  42. Hasegawa H, Kaneko T, Endo M, Kanno C, Yamazaki M, Yaginuma S, Igarashi H, Honma H, Masui S, Suto M, Sakisaka Y, Ishihata H. Comparing the Efficacy of a Microperforated Titanium Membrane for Guided Bone Regeneration with an Existing Mesh Retainer in Dog Mandibles. Materials (Basel). 2021 Jun 17;14(12):3358. doi: 10.3390/ma14123358. PMID: 34204390; PMCID: PMC8234924.
  43. Murai M, Sato S, Fukase Y, Yamada Y, Komiyama K, Ito K. Effects of different sizes of beta-tricalcium phosphate particles on bone augmentation within a titanium cap in rabbit calvarium. Dent Mater J. 2006 Mar;25(1):87-96. doi: 10.4012/dmj.25.87. PMID: 16706302.

Download Article
Received July 20, 2023.
Accepted August 29, 2023.
©2023 International Medical Research and Development Corporation.