Design and evaluation of a novel sub-scaffold dental implant system based on the osteoinduction of micro-nano bioactive glass
Alveolar ridge atrophy brings great challenges for endosteal implantation due to the lack of adequate vertical bone mass to hold the implants. To overcome this limitation, we developed a novel dental implant design: sub-scaffold dental implant system (SDIS), which is composed of a metal implant and a micro-nano bioactive glass scaffold. This implant system can be directly implanted under mucous membranes without adding any biomolecules or destroying the alveolar ridge. To evaluate the performance of the novel implant system in vivo, SDISs were implanted into the sub-epicranial aponeurosis space of Sprague-Dawley rats. After 6 weeks, the SDIS and surrounding tissues were collected and analysed by micro-CT, scanning electron microscopy and histology. Our results showed that SDISs implanted into the sub-epicranial aponeurosis had integrated with the skull without any mobility and could stably support a denture. Moreover, this design achieved alveolar ridge augmentation, as active osteogenesis could be observed outside the cortical bone. Considering that the microenvironment of the sub-epicranial aponeurosis space is similar to that of the alveolar ridge, SDISs have great potential for clinical applications in the treatment of atrophic alveolar ridges. The study was approved by the Animal Care Committee of Guangdong Pharmaceutical University (approval No. 2017370).
Below is the content of the Citations in the paper which has been de-formatted, however, the content stays consistent with the original.
1. von Stein-Lausnitz, M.; Nickenig, H. J.; Wolfart, S.; Neumann, K.; von Stein-Lausnitz, A.; Spies, B. C.; Beuer, F. Survival rates and complication behaviour of tooth implant-supported, fixed dental prostheses: A systematic review and meta-analysis. J Dent. 2019, 88, 103167.
2. Bohner, L.; Hanisch, M.; Kleinheinz, J.; Jung, S. Dental implants in growing patients: a systematic review. Br J Oral Maxillofac Surg. 2019, 57, 397-406.
3. Liaw, K.; Delfini, R. H.; Abrahams, J. J. Dental implant complications. Semin Ultrasound CT MR. 2015, 36, 427-433.
4. Hansson, S.; Halldin, A. Alveolar ridge resorption after tooth extraction: A consequence of a fundamental principle of bone physiology. J Dent Biomech. 2012, 3, 1758736012456543.
5. Li, J.; Jansen, J. A.; Walboomers, X. F.; van den Beucken, J. J. Mechanical aspects of dental implants and osseointegration: A narrative review. J Mech Behav Biomed Mater. 2020, 103, 103574.
6. Chavda, S.; Levin, L. Human studies of vertical and horizontal alveolar ridge augmentation comparing different types of bone graft materials: a systematic review. J Oral Implantol. 2018, 44, 74-84.
7. Chiapasco, M.; Casentini, P.; Zaniboni, M. Bone augmentation procedures in implant dentistry. Int J Oral Maxillofac Implants. 2009, 24 Suppl, 237-259.
8. McAllister, B. S.; Haghighat, K. Bone augmentation techniques. J Periodontol. 2007, 78, 377-396.
9. Ribeiro, M.; Fraguas, E. H.; Brito, K. I. C.; Kim, Y. J.; Pallos, D.; Sendyk, W. R. Bone autografts & allografts placed simultaneously with dental implants in rabbits. J Craniomaxillofac Surg. 2018, 46, 142-147.
10. Maiorana, C.; Poli, P. P.; Mascellaro, A.; Ferrario, S.; Beretta, M. Dental implants placed in resorbed alveolar ridges reconstructed with iliac crest autogenous onlay grafts: a 26-year median follow-up retrospective study. J Craniomaxillofac Surg. 2019, 47, 805-814.
11. Asa’ad, F.; Pagni, G.; Pilipchuk, S. P.; Giannì, A. B.; Giannobile, W. V.; Rasperini, G. 3D-printed scaffolds and biomaterials: review of alveolar bone augmentation and periodontal regeneration applications. Int J Dent. 2016, 2016, 1239842.
12. Sheikh, Z.; Sima, C.; Glogauer, M. Bone replacement materials and techniques used for achieving vertical alveolar bone augmentation. Materials. 2015, 8, 2953-2993.
13. Zigdon-Giladi, H.; Lewinson, D.; Bick, T.; Machtei, E. E. Mesenchymal stem cells combined with barrier domes enhance vertical bone formation. J Clin Periodontol. 2013, 40, 196-202.
14. Tamimi, F.; Torres, J.; Al-Abedalla, K.; Lopez-Cabarcos, E.; Alkhraisat, M. H.; Bassett, D. C.; Gbureck, U.; Barralet, J. E. Osseointegration of dental implants in 3D-printed synthetic onlay grafts customized according to bone metabolic activity in recipient site. Biomaterials. 2014, 35, 5436-5445.
15. Yang, J.; Kang, Y.; Browne, C.; Jiang, T.; Yang, Y. Graded porous β-tricalcium phosphate scaffolds enhance bone regeneration in mandible augmentation. J Craniofac Surg. 2015, 26, e148-153.
16. Singh, A.; Daing, A.; Anand, V.; Dixit, J. Two dimensional alveolar ridge augmentation using particulate hydroxyapatite and collagen membrane: A case report. J Oral Biol Craniofac Res. 2014, 4, 151-154.
17. Kinard, L. A.; Dahlin, R. L.; Lam, J.; Lu, S.; Lee, E. J.; Kasper, F. K.; Mikos, A. G. Synthetic biodegradable hydrogel delivery of demineralized bone matrix for bone augmentation in a rat model. Acta Biomater. 2014, 10, 4574-4582.
18. Kinard, L. A.; Dahlin, R. L.; Henslee, A. M.; Spicer, P. P.; Chu, C. Y.; Tabata, Y.; van den Beucken, J. J.; Jansen, J. A.; Young, S.; Wong, M. E.; Kasper, F. K.; Mikos, A. G. Tissue response to composite hydrogels for vertical bone augmentation in the rat. J Biomed Mater Res A. 2014, 102, 2079-2088.
19. Sheikh, Z.; Hamdan, N.; Ikeda, Y.; Grynpas, M.; Ganss, B.; Glogauer, M. Natural graft tissues and synthetic biomaterials for periodontal and alveolar bone reconstructive applications: a review. Biomater Res. 2017, 21, 9.
20. Titsinides, S.; Agrogiannis, G.; Karatzas, T. Bone grafting materials in dentoalveolar reconstruction: A comprehensive review. Jpn Dent Sci Rev. 2019, 55, 26-32.
21. Hu, Q.; Jiang, W.; Li, Y.; Chen, X.; Liu, J.; Chen, T.; Miao, G. The effects of morphology on physicochemical properties, bioactivity and biocompatibility of micro-/nano-bioactive glasses. Adv Powder Technol. 2018, 29, 1812-1819.
22. Jones, J. R. Review of bioactive glass: from Hench to hybrids. Acta Biomater. 2013, 9, 4457-4486.
23. El-Rashidy, A. A.; Roether, J. A.; Harhaus, L.; Kneser, U.; Boccaccini, A. R. Regenerating bone with bioactive glass scaffolds: A review of in vivo studies in bone defect models. Acta Biomater. 2017, 62, 1-28.
24. Zhao, F.; Xie, W.; Zhang, W.; Fu, X.; Gao, W.; Lei, B.; Chen, X. 3D printing nanoscale bioactive glass scaffolds enhance osteoblast migration and extramembranous osteogenesis through stimulating immunomodulation. Adv Healthc Mater. 2018, 7, e1800361.
25. Sheikh, Z.; Drager, J.; Zhang, Y. L.; Abdallah, M. N.; Tamimi, F.; Barralet, J. Controlling bone graft substitute microstructure to improve bone augmentation. Adv Healthc Mater. 2016, 5, 1646-1655.
26. Armitage, J.; Natiella, J.; Greene, G. Jr.; Meenaghan, M. An evaluation of early bone changes after the insertion of mental endosseous implants into the jaws of rhesus monkeys. Oral Surg Oral Med Oral Pathol. 1971, 32, 558-568.
27. Grenoble, D. E.; Voss, R. Materials and designs for implant dentistry. Biomater Med Devices Artif Organs. 1976, 4, 133-169.
28. Tamimi, F.; Torres, J.; Gbureck, U.; Lopez-Cabarcos, E.; Bassett, D. C.; Alkhraisat, M. H.; Barralet, J. E. Craniofacial vertical bone augmentation: a comparison between 3D printed monolithic monetite blocks and autologous onlay grafts in the rabbit. Biomaterials. 2009, 30, 6318-6326.
29. Pieri, F.; Lucarelli, E.; Corinaldesi, G.; Aldini, N. N.; Fini, M.; Parrilli, A.; Dozza, B.; Donati, D.; Marchetti, C. Dose-dependent effect of adipose-derived adult stem cells on vertical bone regeneration in rabbit calvarium. Biomaterials. 2010, 31, 3527-3535.
30. Wang, S.; Zhang, Z.; Zhao, J.; Zhang, X.; Sun, X.; Xia, L.; Chang, Q.; Ye, D.; Jiang, X. Vertical alveolar ridge augmentation with beta-tricalcium phosphate and autologous osteoblasts in canine mandible. Biomaterials. 2009, 30, 2489-2498.
31. Łączka, M.; Cholewa-Kowalska, K.; Osyczka, A. M. Bioactivity and osteoinductivity of glasses and glassceramics and their material determinants. Ceram Int. 2016, 42, 14313-14325.
32. Barradas, A. M.; Yuan, H.; van Blitterswijk, C. A.; Habibovic, P. Osteoinductive biomaterials: current knowledge of properties, experimental models and biological mechanisms. Eur Cell Mater. 2011, 21, 407-429; discussion 429.
33. Yuan, H.; de Bruijn, J. D.; Zhang, X.; van Blitterswijk, C. A.; de Groot, K. Bone induction by porous glass ceramic made from Bioglass (45S5). J Biomed Mater Res. 2001, 58, 270-276.
34. Miri, A. K.; Muja, N.; Kamranpour, N. O.; Lepry, W. C.; Boccaccini, A. R.; Clarke, S. A.; Nazhat, S. N. Ectopic bone formation in rapidly fabricated acellular injectable dense collagen-Bioglass hybrid scaffolds via gel aspiration-ejection. Biomaterials. 2016, 85, 128-141.
35. Tang, W.; Lin, D.; Yu, Y.; Niu, H.; Guo, H.; Yuan, Y.; Liu, C. Bioinspired trimodal macro/micro/nano-porous scaffolds loading rhBMP-2 for complete regeneration of critical size bone defect. Acta Biomater. 2016, 32, 309-323.
36. Meretoja, V. V.; Tirri, T.; Malin, M.; Seppälä, J. V.; Närhi, T. O. Ectopic bone formation in and soft-tissue response to P(CL/DLLA)/bioactive glass composite scaffolds. Clin Oral Implants Res. 2014, 25, 159-164.
37. Urist, M. R.; Silverman, B. F.; Büring, K.; Dubuc, F. L.; Rosenberg, J. M. The bone induction principle. Clin Orthop Relat Res. 1967, 53, 243-283.
38. García-Gareta, E.; Coathup, M. J.; Blunn, G. W. Osteoinduction of bone grafting materials for bone repair and regeneration. Bone. 2015, 81, 112-121.
39. Metzler, P.; von Wilmowsky, C.; Zimmermann, R.; Wiltfang, J.; Schlegel, K. A. The effect of current used bone substitution materials and platelet-rich plasma on periosteal cells by ectopic site implantation: an in-vivo pilot study. J Craniomaxillofac Surg. 2012, 40, 409-415.
40. Zhao, F.; Lei, B.; Li, X.; Mo, Y.; Wang, R.; Chen, D.; Chen, X. Promoting in vivo early angiogenesis with sub-micrometer strontium-contained bioactive microspheres through modulating macrophage phenotypes. Biomaterials. 2018, 178, 36-47.
41. Hench, L. L.; Splinter, R. J.; Allen, W. C.; Greenlee, T. K. Bonding mechanisms at the interface of ceramic prosthetic materials. J Biomed Mater Res. 1971, 5, 117-141.