J Korean Assoc Oral Maxillofac Surg.  2012 Oct;38(5):264-270. 10.5125/jkaoms.2012.38.5.264.

Biomaterial development for oral and maxillofacial bone regeneration

Affiliations
  • 1Oral Biotechnology and Bioengineering, Department of Cranio-Maxillofacial and Oral Surgery, University Hospital Zurich, Zurich, Switzerland. franz.weber@zzm.uzh.ch

Abstract

Many oral and maxillofacial bone defects are not self-healing. Guided bone regeneration (GBR), which uses a barrier membrane to prevent the soft tissues from invading the defect to enable slower-growing bone cells to penetrate the area, was developed as a therapy in the 1980s. Although there has been some success with GBR in some clinical situations, better treatments are needed. This review discusses the concept of GBR focusing on bioactive membranes that incorporate osteoconductive materials, growth factors and cells for improved oral and maxillofacial bone regeneration.

Keyword

Bone; Guided bone regeneration; Barrier membrane; Bone substitutes; Drug delivery; Stem cells

MeSH Terms

Bone Regeneration
Bone Substitutes
Intercellular Signaling Peptides and Proteins
Membranes
Stem Cells
Bone Substitutes
Intercellular Signaling Peptides and Proteins

Cited by  2 articles

Guided bone regeneration
Young-Kyun Kim, Jeong-Kui Ku
J Korean Assoc Oral Maxillofac Surg. 2020;46(5):361-366.    doi: 10.5125/jkaoms.2020.46.5.361.

Tooth-derived bone graft material
Young-Kyun Kim, Junho Lee, In-Woong Um, Kyung-Wook Kim, Masaru Murata, Toshiyuki Akazawa, Masaharu Mitsugi
J Korean Assoc Oral Maxillofac Surg. 2013;39(3):103-111.    doi: 10.5125/jkaoms.2013.39.3.103.


Reference

1. Hitti RA, Kerns DG. Guided bone regeneration in the oral cavity: a review. Open Pathol J. 2011. 5:33–45.
Article
2. Johner R. Dependence of bone healing on defect size. Helv Chir Acta. 1972. 39:409–411.
3. Bottino MC, Thomas V, Schmidt G, Vohra YK, Chu TM, Kowolik MJ, et al. Recent advances in the development of GTR/GBR membranes for periodontal regeneration--a materials perspective. Dent Mater. 2012. 28:703–721.
Article
4. Hughes FJ, Ghuman M, Talal A. Periodontal regeneration: a challenge for the tissue engineer? Proc Inst Mech Eng H. 2010. 224:1345–1358.
Article
5. Hämmerle CH, Karring T. Guided bone regeneration at oral implant sites. Periodontol 2000. 1998. 17:151–175.
Article
6. Araujo MG, Lindhe J. Dimensional ridge alterations following tooth extraction. An experimental study in the dog. J Clin Periodontol. 2005. 32:212–218.
Article
7. Mikos AG, Herring SW, Ochareon P, Elisseeff J, Lu HH, Kandel R, et al. Engineering complex tissues. Tissue Eng. 2006. 12:3307–3339.
Article
8. Dahlin C, Linde A, Gottlow J, Nyman S. Healing of bone defects by guided tissue regeneration. Plast Reconstr Surg. 1988. 81:672–676.
Article
9. Nyman S, Lindhe J, Karring T, Rylander H. New attachment following surgical treatment of human periodontal disease. J Clin Periodontol. 1982. 9:290–296.
Article
10. Buser D. 20 years of guided bone regeneration in implant dentistry. 2009. 2nd ed. Berlin: Quintessence.
11. Retzepi M, Donos N. Guided Bone Regeneration: biological principle and therapeutic applications. Clin Oral Implants Res. 2010. 21:567–576.
Article
12. Murray G, Holden R, Roschlau W. Experimental and clinical study of new growth of bone in a cavity. Am J Surg. 1957. 93:385–387.
Article
13. Kahnberg KE. Restoration of mandibular jaw defects in the rabbit by subperiosteally implanted Teflon mantle leaf. Int J Oral Surg. 1979. 8:449–456.
Article
14. Melcher AH. Role of the periosteum in repair of wounds of the parietal bone of the rat. Arch Oral Biol. 1969. 14:1101–1109.
Article
15. Karring T, Nyman S, Lindhe J. Healing following implantation of periodontitis affected roots into bone tissue. J Clin Periodontol. 1980. 7:96–105.
Article
16. Gottlow J, Nyman S, Karring T, Lindhe J. New attachment formation as the result of controlled tissue regeneration. J Clin Periodontol. 1984. 11:494–503.
Article
17. Karring T, Nyman S, Gottlow J, Laurell L. Development of the biological concept of guided tissue regeneration--animal and human studies. Periodontol 2000. 1993. 1:26–35.
Article
18. McAllister BS, Haghighat K. Bone augmentation techniques. J Periodontol. 2007. 78:377–396.
Article
19. Hammerle CH, Jung RE. Bone augmentation by means of barrier membranes. Periodontol 2000. 2003. 33:36–53.
Article
20. Murphy KG. P. Int J Periodontics Restorative Dent. 1995. 15:363–375.
21. Wang HL, Carroll MJ. Guided bone regeneration using bone grafts and collagen membranes. Quintessence Int. 2001. 32:504–515.
22. Gentile P, Chiono V, Tonda-Turo C, Ferreira AM, Ciardelli G. Polymeric membranes for guided bone regeneration. Biotechnol J. 2011. 6:1187–1197.
Article
23. Geurs NC, Korostoff JM, Vassilopoulos PJ, Kang TH, Jeffcoat M, Kellar R, et al. Clinical and histologic assessment of lateral alveolar ridge augmentation using a synthetic long-term bioabsorbable membrane and an allograft. J Periodontol. 2008. 79:1133–1140.
Article
24. Sculean A, Nikolidakis D, Schwarz F. Regeneration of periodontal tissues: combinations of barrier membranes and grafting materials-biological foundation and preclinical evidence: a systematic review. J Clin Periodontol. 2008. 35:8 Suppl. 106–116.
Article
25. Milella E, Barra G, Ramires PA, Leo G, Aversa P, Romito A. Poly(L-lactide)acid/alginate composite membranes for guided tissue regeneration. J Biomed Mater Res. 2001. 57:248–257.
Article
26. Tal H, Kozlovsky A, Artzi Z, Nemcovsky CE, Moses O. Cross-linked and non-cross-linked collagen barrier membranes disintegrate following surgical exposure to the oral environment: a histological study in the cat. Clin Oral Implants Res. 2008. 19:760–766.
Article
27. Parodi R, Carusi G, Santarelli G, Nanni F. Implant placement in large edentulous ridges expanded by GBR using a bioresorbable collagen membrane. Int J Periodontics Restorative Dent. 1998. 18:266–275.
28. Colangelo P, Piattelli A, Barrucci S, Trisi P, Formisano G, Caiazza S. Bone regeneration guided by resorbable collagen membranes in rabbits: a pilot study. Implant Dent. 1993. 2:101–105.
29. Coïc M, Placet V, Jacquet E, Meyer C. Mechanical properties of collagen membranes used in guided bone regeneration: a comparative study of three models. Rev Stomatol Chir Maxillofac. 2010. 111:286–290.
30. Makadia HK, Siegel SJ. Poly lactic-co-glycolic acid (PLGA) as biodegradable controlled drug delivery carrier. Polymers (Basel). 2011. 3:1377–1397.
Article
31. Vert M. Aliphatic polyesters: great degradable polymers that cannot do everything. Biomacromolecules. 2005. 6:538–546.
Article
32. Jung RE, Halg GA, Thoma DS, Hammerle CH. A randomized, controlled clinical trial to evaluate a new membrane for guided bone regeneration around dental implants. Clin Oral Implants Res. 2009. 20:162–168.
Article
33. Jung RE, Zwahlen R, Weber FE, Molenberg A, van Lenthe GH, Hammerle CH. Evaluation of an in situ formed synthetic hydrogel as a biodegradable membrane for guided bone regeneration. Clin Oral Implants Res. 2006. 17:426–433.
Article
34. Wechsler S, Fehr D, Molenberg A, Raeber G, Schense JC, Weber FE. A novel, tissue occlusive poly(ethylene glycol) hydrogel material. J Biomed Mater Res A. 2008. 85:285–292.
Article
35. Amini AR, Adams DJ, Laurencin CT, Nukavarapu SP. Optimally porous and biomechanically compatible scaffolds for large-area bone regeneration. Tissue Eng Part A. 2012. 18:1376–1388.
Article
36. Chen FM, Jin Y. Periodontal tissue engineering and regeneration: current approaches and expanding opportunities. Tissue Eng Part B Rev. 2010. 16:219–255.
Article
37. Calori GM, Mazza E, Colombo M, Ripamonti C. The use of bone-graft substitutes in large bone defects: any specific needs? Injury. 2011. 42:Suppl 2. S56–S63.
Article
38. Hanseler P, Jung UW, Jung RE, Choi KH, Cho KS, Hammerle CH, et al. Analysis of hydrolyzable polyethylene glycol hydrogels and deproteinized bone mineral as delivery systems for glycosylated and non-glycosylated bone morphogenetic protein-2. Acta Biomater. 2012. 8:116–123.
Article
39. Henkel KO, Gerber T, Lenz S, Gundlach KK, Bienengraber V. Macroscopical, histological, and morphometric studies of porous bone-replacement materials in minipigs 8 months after implantation. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2006. 102:606–613.
Article
40. Palarie V, Bicer C, Lehmann KM, Zahalka M, Draenert FG, Kammerer PW. Early outcome of an implant system with a resorbable adhesive calcium-phosphate coating--a prospective clinical study in partially dentate patients. Clin Oral Investig. 2012. 16:1039–1048.
Article
41. Hannink G, Arts JJ. Bioresorbability, porosity and mechanical strength of bone substitutes: what is optimal for bone regeneration? Injury. 2011. 42:Suppl 2. S22–S25.
Article
42. Kruse A, Jung RE, Nicholls F, Zwahlen RA, Hammerle CH, Weber FE. Bone regeneration in the presence of a synthetic hydroxyapatite/silica oxide-based and a xenogenic hydroxyapatite-based bone substitute material. Clin Oral Implants Res. 2011. 22:506–511.
Article
43. Qu Y, Wang P, Man Y, Li Y, Zuo Y, Li J. Preliminary biocompatible evaluation of nano-hydroxyapatite/polyamide 66 composite porous membrane. Int J Nanomedicine. 2010. 5:429–435.
Article
44. Kamitakahara M, Ohtsuki C, Miyazaki T. Coating of bone-like apatite for development of bioactive materials for bone reconstruction. Biomed Mater. 2007. 2:R17–R23.
Article
45. Darby I. Periodontal materials. Aust Dent J. 2011. 56:Suppl 1. 107–118.
Article
46. San Miguel B, Kriauciunas R, Tosatti S, Ehrbar M, Ghayor C, Textor M, et al. Enhanced osteoblastic activity and bone regeneration using surface-modified porous bioactive glass scaffolds. J Biomed Mater Res A. 2010. 94:1023–1033.
47. Mota J, Yu N, Caridade SG, Luz GM, Gomes ME, Reis RL, et al. Chitosan/bioactive glass nanoparticle composite membranes for periodontal regeneration. Acta Biomater. 2012. 8:4173–4180.
Article
48. Grandin HM, Gemperli AC, Dard M. Enamel matrix derivative: a review of cellular effects in vitro and a model of molecular arrangement and functioning. Tissue Eng Part B Rev. 2012. 18:181–202.
Article
49. Nikolidakis D, Jansen JA. The biology of platelet-rich plasma and its application in oral surgery: literature review. Tissue Eng Part B Rev. 2008. 14:249–258.
Article
50. Thoma DS, Jung RE, Hanseler P, Hammerle CH, Cochran DL, Weber FE. Impact of recombinant platelet-derived growth factor BB on bone regeneration: a study in rabbits. Int J Periodontics Restorative Dent. 2012. 32:195–202.
51. Hong KS, Kim EC, Bang SH, Chung CH, Lee YI, Hyun JK, et al. Bone regeneration by bioactive hybrid membrane containing FGF2 within rat calvarium. J Biomed Mater Res A. 2010. 94:1187–1194.
Article
52. Kang H, Sung J, Jung HM, Woo KM, Hong SD, Roh S. Insulin-like growth factor 2 promotes osteogenic cell differentiation in the parthenogenetic murine embryonic stem cells. Tissue Eng Part A. 2012. 18:331–341.
Article
53. Jung RE, Schmoekel HG, Zwahlen R, Kokovic V, Hammerle CH, Weber FE. Platelet-rich plasma and fibrin as delivery systems for recombinant human bone morphogenetic protein-2. Clin Oral Implants Res. 2005. 16:676–682.
Article
54. Urist MR. Bone: formation by autoinduction. Science. 1965. 150:893–899.
Article
55. Ripamonti U, Reddi AH. Tissue engineering, morphogenesis, and regeneration of the periodontal tissues by bone morphogenetic proteins. Crit Rev Oral Biol Med. 1997. 8:154–163.
Article
56. Elangovan S, Srinivasan S, Ayilavarapu S. Novel regenerative strategies to enhance periodontal therapy outcome. Expert Opin Biol Ther. 2009. 9:399–410.
Article
57. Wikesjo UM, Qahash M, Huang YH, Xiropaidis A, Polimeni G, Susin C. Bone morphogenetic proteins for periodontal and alveolar indications; biological observations-clinical implications. Orthod Craniofac Res. 2009. 12:263–270.
58. Jung RE, Glauser R, Scharer P, Hammerle CH, Sailer HF, Weber FE. Effect of rhBMP-2 on guided bone regeneration in humans. Clin Oral Implants Res. 2003. 14:556–568.
Article
59. Zhu W, Kim J, Cheng C, Rawlins BA, Boachie-Adjei O, Crystal RG, et al. Noggin regulation of bone morphogenetic protein (BMP) 2/7 heterodimer activity in vitro. Bone. 2006. 39:61–71.
Article
60. Carragee EJ, Hurwitz EL, Weiner BK. A critical review of recombinant human bone morphogenetic protein-2 trials in spinal surgery: emerging safety concerns and lessons learned. Spine J. 2011. 11:471–491.
Article
61. Miguel BS, Ghayor C, Ehrbar M, Jung RE, Zwahlen RA, Hortschansky P, et al. N-methyl pyrrolidone as a potent bone morphogenetic protein enhancer for bone tissue regeneration. Tissue Eng Part A. 2009. 15:2955–2963.
Article
62. Hunziker EB, Enggist L, Kuffer A, Buser D, Liu Y. Osseointegration: the slow delivery of BMP-2 enhances osteoinductivity. Bone. 2012. 51:98–106.
Article
63. Herford AS, Boyne PJ. Reconstruction of mandibular continuity defects with bone morphogenetic protein-2 (rhBMP-2). J Oral Maxillofac Surg. 2008. 66:616–624.
Article
64. Jung RE, Weber FE, Thoma DS, Ehrbar M, Cochran DL, Hammerle CH. Bone morphogenetic protein-2 enhances bone formation when delivered by a synthetic matrix containing hydroxyapatite/tricalciumphosphate. Clin Oral Implants Res. 2008. 19:188–195.
Article
65. Boerckel JD, Kolambkar YM, Dupont KM, Uhrig BA, Phelps EA, Stevens HY, et al. Effects of protein dose and delivery system on BMP-mediated bone regeneration. Biomaterials. 2011. 32:5241–5251.
Article
66. Luginbuehl V, Meinel L, Merkle HP, Gander B. Localized delivery of growth factors for bone repair. Eur J Pharm Biopharm. 2004. 58:197–208.
Article
67. Abbah SA, Liu J, Lam RW, Goh JC, Wong HK. In vivo bioactivity of rhBMP-2 delivered with novel polyelectrolyte complexation shells assembled on an alginate microbead core template. J Control Release. 2012. 162:364–372.
Article
68. Zellin G, Linde A. Importance of delivery systems for growth-stimulatory factors in combination with osteopromotive membranes. An experimental study using rhBMP-2 in rat mandibular defects. J Biomed Mater Res. 1997. 35:181–190.
Article
69. Matsuo T, Sugita T, Kubo T, Yasunaga Y, Ochi M, Murakami T. Injectable magnetic liposomes as a novel carrier of recombinant human BMP-2 for bone formation in a rat bone-defect model. J Biomed Mater Res A. 2003. 66:747–754.
Article
70. Machado R, Bessa PC, Reis RL, Rodriguez-Cabello JC, Casal M. Elastin-based nanoparticles for delivery of bone morphogenetic proteins. Methods Mol Biol. 2012. 906:353–363.
Article
71. Bulpitt P, Aeschlimann D. New strategy for chemical modification of hyaluronic acid: preparation of functionalized derivatives and their use in the formation of novel biocompatible hydrogels. J Biomed Mater Res. 1999. 47:152–169.
Article
72. Masters KS. Covalent growth factor immobilization strategies for tissue repair and regeneration. Macromol Biosci. 2011. 11:1149–1163.
Article
73. Park J, Bauer S, Pittrof A, Killian MS, Schmuki P, von der Mark K. Synergistic control of mesenchymal stem cell differentiation by nanoscale surface geometry and immobilized growth factors on TiO2 nanotubes. Small. 2012. 8:98–107.
Article
74. Yamachika E, Tsujigiwa H, Shirasu N, Ueno T, Sakata Y, Fukunaga J, et al. Immobilized recombinant human bone morphogenetic protein-2 enhances the phosphorylation of receptor-activated Smads. J Biomed Mater Res A. 2009. 88:599–607.
Article
75. Park YJ, Kim KH, Lee JY, Ku Y, Lee SJ, Min BM, et al. Immobilization of bone morphogenetic protein-2 on a nanofibrous chitosan membrane for enhanced guided bone regeneration. Biotechnol Appl Biochem. 2006. 43:17–24.
Article
76. Zhang H, Migneco F, Lin CY, Hollister SJ. Chemically-conjugated bone morphogenetic protein-2 on three-dimensional polycaprolactone scaffolds stimulates osteogenic activity in bone marrow stromal cells. Tissue Eng Part A. 2010. 16:3441–3448.
Article
77. Schmoekel HG, Weber FE, Schense JC, Gratz KW, Schawalder P, Hubbell JA. Bone repair with a form of BMP-2 engineered for incorporation into fibrin cell ingrowth matrices. Biotechnol Bioeng. 2005. 89:253–262.
Article
78. Rios HF, Lin Z, Oh B, Park CH, Giannobile WV. Cell- and gene-based therapeutic strategies for periodontal regenerative medicine. J Periodontol. 2011. 82:1223–1237.
Article
79. Miranda SC, Silva GA, Mendes RM, Abreu FA, Caliari MV, Alves JB, et al. Mesenchymal stem cells associated with porous chitosan-gelatin scaffold: A potential strategy for alveolar bone regeneration. J Biomed Mater Res A. 2012. 100:2775–2786.
Article
80. Hasegawa N, Kawaguchi H, Hirachi A, Takeda K, Mizuno N, Nishimura M, et al. Behavior of transplanted bone marrow-derived mesenchymal stem cells in periodontal defects. J Periodontol. 2006. 77:1003–1007.
Article
81. Li H, Yan F, Lei L, Li Y, Xiao Y. Application of autologous cryopreserved bone marrow mesenchymal stem cells for periodontal regeneration in dogs. Cells Tissues Organs. 2009. 190:94–101.
Article
82. Chung VH, Chen AY, Kwan CC, Chen PK, Chang SC. Mandibular alveolar bony defect repair using bone morphogenetic protein 2-expressing autologous mesenchymal stem cells. J Craniofac Surg. 2011. 22:450–454.
Article
83. Thein-Han W, Liu J, Xu HH. Calcium phosphate cement with biofunctional agents and stem cell seeding for dental and craniofacial bone repair. Dent Mater. 2012. 28:1059–1070.
Article
84. Wang B, Huang S, Pan L, Jia S. Enhancement of bone formation by genetically engineered human umbilical cord-derived mesenchymal stem cells expressing osterix. Oral Surg Oral Med Oral Pathol Oral Radiol. 2012. 07. 19. [Epub ahead of print].
Article
85. Wen Y, Jiang B, Cui J, Li G, Yu M, Wang F, et al. Superior osteogenic capacity of different mesenchymal stem cells for bone tissue engineering. Oral Surg Oral Med Oral Pathol Oral Radiol. 2012. 07. 26. [Epub ahead of print].
Article
86. Zhao L, Burguera EF, Xu HH, Amin N, Ryou H, Arola DD. Fatigue and human umbilical cord stem cell seeding characteristics of calcium phosphate-chitosan-biodegradable fiber scaffolds. Biomaterials. 2010. 31:840–847.
Article
87. Lendeckel S, Jodicke A, Christophis P, Heidinger K, Wolff J, Fraser JK, et al. Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report. J Craniomaxillofac Surg. 2004. 32:370–373.
Article
88. Mesimaki K, Lindroos B, Tornwall J, Mauno J, Lindqvist C, Kontio R, et al. Novel maxillary reconstruction with ectopic bone formation by GMP adipose stem cells. Int J Oral Maxillofac Surg. 2009. 38:201–209.
Article
89. Liu H, Gronthos S, Shi S. Dental pulp stem cells. Methods Enzymol. 2006. 419:99–113.
Article
90. Liu HC, E LL, Wang DS, Su F, Wu X, Shi ZP, et al. Reconstruction of alveolar bone defects using bone morphogenetic protein 2 mediated rabbit dental pulp stem cells seeded on nanohydroxyapatite/collagen/poly(L-lactide). Tissue Eng Part A. 2011. 17:2417–2433.
Article
91. Liu Y, Zheng Y, Ding G, Fang D, Zhang C, Bartold PM, et al. Periodontal ligament stem cell-mediated treatment for periodontitis in miniature swine. Stem Cells. 2008. 26:1065–1073.
Article
92. Park JY, Jeon SH, Choung PH. Efficacy of periodontal stem cell transplantation in the treatment of advanced periodontitis. Cell Transplant. 2011. 20:271–285.
Article
93. Noshi T, Yoshikawa T, Ikeuchi M, Dohi Y, Ohgushi H, Horiuchi K, et al. Enhancement of the in vivo osteogenic potential of marrow/hydroxyapatite composites by bovine bone morphogenetic protein. J Biomed Mater Res. 2000. 52:621–630.
Article
94. Niu LN, Jiao K, Qi YP, Nikonov S, Yiu CK, Arola DD, et al. Intrafibrillar silicification of collagen scaffolds for sustained release of stem cell homing chemokine in hard tissue regeneration. FASEB J. 2012. 08. 02. [Epub ahead of print].
Article
95. Partridge K, Yang X, Clarke NM, Okubo Y, Bessho K, Sebald W, et al. Adenoviral BMP-2 gene transfer in mesenchymal stem cells: in vitro and in vivo bone formation on biodegradable polymer scaffolds. Biochem Biophys Res Commun. 2002. 292:144–152.
Article
96. Vahabi S, Amirizadeh N, Shokrgozar MA, Mofeed R, Mashhadi A, Aghaloo M, et al. A comparison between the efficacy of Bio-Oss, hydroxyapatite tricalcium phosphate and combination of mesenchymal stem cells in inducing bone regeneration. Chang Gung Med J. 2012. 35:28–37.
Article
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