Journal of Korean Dental Science

Korean Academy of Dental Science (대한치의학회)
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Bone Regeneration Using Block-type Deproteinized Porcine Bone Mineral with Collagen Membrane Using 3,4-Dihydroxyphenylalanine as Bone Adhesive

  • Kang, Joo Hyun (Department of Periodontology, Research Institute of Periodontal Regeneration, Yonsei University College of Dentistry) ;
  • Pae, Hyoung-Chul (Department of Periodontology, Research Institute of Periodontal Regeneration, Yonsei University College of Dentistry) ;
  • Cha, Jae-Kook (Department of Periodontology, Research Institute of Periodontal Regeneration, Yonsei University College of Dentistry) ;
  • Lee, Jung-Seok (Department of Periodontology, Research Institute of Periodontal Regeneration, Yonsei University College of Dentistry) ;
  • Paik, Jeong-Won (Department of Periodontology, Research Institute of Periodontal Regeneration, Yonsei University College of Dentistry) ;
  • Jung, Ui-Won (Department of Periodontology, Research Institute of Periodontal Regeneration, Yonsei University College of Dentistry) ;
  • Choi, Seong-Ho (Department of Periodontology, Research Institute of Periodontal Regeneration, Yonsei University College of Dentistry)
  • Received : 2018.11.30
  • Accepted : 2018.12.27
  • Published : 2018.12.30
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Abstract

Purpose: The purpose of this study was to assess the adhesiveness and cytotoxicity of 3, 4-dihydroxyphenylalanine (DOPA), and to evaluate the role of collagen membrane with DOPA in the guided bone regeneration. Materials and Methods: Peel resistance and cell cytotoxicity test were performed. Four defect types in nine rabbit calvaria were randomly allocated: i) control, ii) membrane, iii) deproteinized porcine bone mineral (DPBM) covered by membrane with DOPA, and iv) DPBM covered by membrane with cyanoacrylate. Animals were sacrificed at 2 (n=4) and 8 weeks (n=5) for microcomputed tomography and histomorphometric analysis. DOPA showed low peel resistance but high cell viability. Result: Cyanoacrylate and DOPA groups showed significantly higher mineralized tissue volume (MTV) compared to control and membrane groups at 2 weeks (P<0.05). At 8 weeks, DOPA group showed the highest MTV. Significantly higher new bone area was found in DOPA group at 8 weeks (P<0.05). Bone formation increased from 2 to 8 weeks in DOPA group (P<0.05). Conclusion: DOPA showed high cell viability and in vivo study revealed predictable performance in bone regeneration.

Keywords

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Fig. 1. Clinical photographs of the experimental sites. (A) Four circumferential defects with 8 mm diameter in rabbit calvarium. (B) Random assignment of defects, from top left in clockwise; membrane group, cyanoacrylate group, 3,4-dihydroxyphenylalanine (DOPA) group, and control group.

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Fig. 2. Peel resistance test. Cyanoacrylate, when applied to collagen membrane, shows higher resistance to peeling load compared to 3,4-dihydroxyphenylalanine (DOPA).

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Fig. 3. Cell cytotoxicity test. Cyanoacrylate (T1) shows the lowest cell viability whereas 3,4-dihydroxyphenylalanine (DOPA) (T2) shows the highest value. BC: blank control group, NC: negative control group, PC: positive control group, C: control group, T1: cyanoacrylate group, T2: DOPA group.

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Fig. 4. Three-dimensionally reconstructed micro-computed tomography images of defects at 2 weeks. (A) Control group. (B) Membrane group. (C) Cyanoacrylate group. (D) 3,4-Dihydroxyphenylalanine (DOPA) group.

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Fig. 5. Three-dimensionally reconstructed micro-computed tomography images of defects at 8 weeks. (A) Control group. (B) Membrane group. (C) Cyanoacrylate group. (D) 3,4-Dihydroxyphenylalanine (DOPA) group.

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Fig. 6. Histologic view after 2 weeks of healing showing (A) control group, defect space is mostly empty; (B) membrane group, collagen membrane is intact with good adaptation; (C) cyanoacrylate group, space is well-maintained by bone graft materials with overlying intact collagen membrane; (D) 3,4-dihydroxyphenylalanine (DOPA) group, collagen membrane is overlaid on defect with supporting bone graft particles. Masson trichrome staining. Scale bars=1 mm.

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Fig. 7. Histologic view after 8 weeks of healing showing (A) control group, almost full closure of defect by bony bridge is observed; (B) membrane group, only a small amount of bony islands is formed with partially resorbed collagen membrane; (C) cyanoacrylate group, newly formed bone from the margin of defect is present; (D) 3,4-dihydroxyphenylalanine (DOPA) group, more mature bone is present inside the bone graft scaffold compared to 2 weeks. Masson trichrome staining. Scale bars=1 mm.

Table 1. Values of MTV measured by micro-computed tomography grey value

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Table 2. Histomorphometric analysis

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References

  1. Albandar JM. Epidemiology and risk factors of periodontal diseases. Dent Clin North Am. 2005; 49: 517-32, v-vi. https://doi.org/10.1016/j.cden.2005.03.003
  2. Hammerle CH, Jung RE. Bone augmentation by means of barrier membranes. Periodontol 2000. 2003; 33: 36-53. https://doi.org/10.1046/j.0906-6713.2003.03304.x
  3. McAllister BS, Haghighat K. Bone augmentation techniques. J Periodontol. 2007; 78: 377-96. https://doi.org/10.1902/jop.2007.060048
  4. Nannmark U, Sennerby L. The bone tissue responses to prehydrated and collagenated corticocancellous porcine bone grafts: a study in rabbit maxillary defects. Clin Implant Dent Relat Res. 2008; 10: 264-70.
  5. Kim SH, Shin JW, Park SA, Kim YK, Park MS, Mok JM, Yang WI, Lee JW. Chemical, structural properties, and osteoconductive effectiveness of bone block derived from porcine cancellous bone. J Biomed Mater Res B Appl Biomater. 2004; 68: 69-74.
  6. Lee JS, Shin HK, Yun JH, Cho KS. Randomized clinical trial of maxillary sinus grafting using deproteinized porcine and bovine bone mineral. Clin Implant Dent Relat Res. 2017; 19: 140-50. https://doi.org/10.1111/cid.12430
  7. Festa VM, Addabbo F, Laino L, Femiano F, Rullo R. Porcine-derived xenograft combined with a soft cortical membrane versus extraction alone for implant site development: a clinical study in humans. Clin Implant Dent Relat Res. 2013; 15: 707-13.
  8. 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. https://doi.org/10.1111/j.1600-051X.1980.tb02012.x
  9. Karring T, Isidor F, Nyman S, Lindhe J. New attachment formation on teeth with a reduced but healthy periodontal ligament. J Clin Periodontol. 1985; 12: 51-60. https://doi.org/10.1111/j.1600-051X.1985.tb01353.x
  10. Wang HL, Boyapati L. “PASS” principles for predictable bone regeneration. Implant Dent. 2006; 15: 8-17. https://doi.org/10.1097/01.id.0000204762.39826.0f
  11. Suuronen R, Kallela I, Lindqvist C. Bioabsorbable plates and screws: current state of the art in facial fracture repair. J Craniomaxillofac Trauma. 2000; 6: 19-27; discussion 28-30.
  12. Bas B, Ozden B, Bekcioglu B, Sanal KO, Gulbahar MY, Kabak YB. Screw fixation is superior to N-butyl-2-cyanoacrylate in onlay grafting procedure: a histomorphologic study. Int J Oral Maxillofac Surg. 2012; 41: 537-43. https://doi.org/10.1016/j.ijom.2011.10.025
  13. Perez M, Fernandez I, Marquez D, Bretana RM. Use of N-butyl-2-cyanoacrylate in oral surgery: biological and clinical evaluation. Artif Organs. 2000; 24: 241-3. https://doi.org/10.1046/j.1525-1594.2000.06519.x
  14. Saska S, Hochuli-Vieira E, Minarelli-Gaspar AM, Gabrielli MF, Capela MV, Gabrielli MA. Fixation of autogenous bone grafts with ethyl-cyanoacrylate glue or titanium screws in the calvaria of rabbits. Int J Oral Maxillofac Surg. 2009; 38: 180-6. https://doi.org/10.1016/j.ijom.2008.12.004
  15. Salata LA, Mariguela VC, Antunes AA, Grossi-Oliveira G, Almeida A, Taba M Jr. Short-term evaluation of grafts fixed with either N-butyl-2-cyanocrylate or screws. J Oral Maxillofac Surg. 2014; 72: 676-82. https://doi.org/10.1016/j.joms.2013.11.016
  16. Trott AT. Cyanoacrylate tissue adhesives. An advance in wound care. JAMA. 1997; 277: 1559-60. https://doi.org/10.1001/jama.1997.03540430071037
  17. De Santis E, Silva ER, Martins ENC, Favero R, Botticelli D, Xavier SP. Healing at the interface between autologous block bone grafts and recipient sites using n-butyl-2-cyanoacrylate adhesive as fixation: histomorphometric study in rabbits. J Oral Implantol. 2017; 43: 447-55. https://doi.org/10.1563/aaid-joi-D-17-00108
  18. Maurer P, Bekes K, Gernhardt CR, Schaller HG, Schubert J. Tensile bond strength of different adhesive systems between bone and composite compared: an in vitro study. J Craniomaxillofac Surg. 2004; 32: 85-9. https://doi.org/10.1016/j.jcms.2003.11.001
  19. Kaushik NK, Kaushik N, Pardeshi S, Sharma JG, Lee SH, Choi EH. Biomedical and clinical importance of mussel-inspired polymers and materials. Mar Drugs. 2015; 13: 6792-817. https://doi.org/10.3390/md13116792
  20. Silverman HG, Roberto FF. Understanding marine mussel adhesion. Mar Biotechnol (NY). 2007; 9: 661-81. https://doi.org/10.1007/s10126-007-9053-x
  21. Cha HJ, Hwang DS, Lim S. Development of bioadhesives from marine mussels. Biotechnol J. 2008; 3: 631-8. https://doi.org/10.1002/biot.200700258
  22. Sever MJ, Weisser JT, Monahan J, Srinivasan S, Wilker JJ. Metal-mediated cross-linking in the generation of a marine-mussel adhesive. Angew Chem Int Ed Engl. 2004; 43: 448-50. https://doi.org/10.1002/anie.200352759
  23. Lee H, Dellatore SM, Miller WM, Messersmith PB. Mussel-inspired surface chemistry for multifunctional coatings. Science. 2007; 318: 426-30. https://doi.org/10.1126/science.1147241
  24. Ai Y, Nie J, Wu G, Yang D. The DOPAfunctionalized bioadhesive with properties of photocrosslinked and thermoresponsive. J Appl Polym Sci. 2014; 131: 41102.
  25. Sedo J, Saiz-Poseu J, Busque F, Ruiz-Molina D. Catechol-based biomimetic functional materials. Adv Mater. 2013; 25: 653-701. https://doi.org/10.1002/adma.201202343
  26. Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS Biol. 2010; 8: e1000412. https://doi.org/10.1371/journal.pbio.1000412
  27. Lee H, Scherer NF, Messersmith PB. Singlemolecule mechanics of mussel adhesion. Proc Natl Acad Sci U S A. 2006; 103: 12999-3003. https://doi.org/10.1073/pnas.0605552103
  28. Ho CC, Ding SJ. Structure, properties and applications of mussel-inspired polydopamine. J Biomed Nanotechnol. 2014; 10: 3063-84. https://doi.org/10.1166/jbn.2014.1888
  29. Brodie M, Vollenweider L, Murphy JL, Xu F, Lyman A, Lew WD, Lee BP. Biomechanical properties of Achilles tendon repair augmented with a bioadhesive-coated scaffold. Biomed Mater. 2011; 6: 015014. https://doi.org/10.1088/1748-6041/6/1/015014
  30. Cha JK, Joo MJ, Yoon S, Lee JS, Choi SH, Jung UW. Sequential healing of onlay bone grafts using combining biomaterials with cross-linked collagen in dogs. Clin Oral Implants Res. 2017; 28: 76-85.
  31. Baldini A, Zaffe D, Nicolini G. Bone-defects healing by high-molecular hyaluronic acid: preliminary results. Ann Stomatol (Roma). 2010; 1: 2-7.
  32. Schwartz Z, Goldstein M, Raviv E, Hirsch A, Ranly DM, Boyan BD. Clinical evaluation of demineralized bone allograft in a hyaluronic acid carrier for sinus lift augmentation in humans: a computed tomography and histomorphometric study. Clin Oral Implants Res. 2007; 18: 204-11. https://doi.org/10.1111/j.1600-0501.2006.01303.x
  33. Pineros-Fernandez A, Rodeheaver PF, Rodeheaver GT. Octyl 2-cyanoacrylate for repair of peripheral nerve. Ann Plast Surg. 2005; 55: 188-95. https://doi.org/10.1097/01.sap.0000164386.72523.3c
  34. Bruns TB, Robinson BS, Smith RJ, Kile DL, Davis TP, Sullivan KM, Quinn JV. A new tissue adhesive for laceration repair in children. J Pediatr. 1998; 132: 1067-70. https://doi.org/10.1016/S0022-3476(98)70415-9
  35. Gulalp B, Seyhan T, Gursoy S, Altinors MN. Emergency wounds treated with cyanoacrylate and long-term results in pediatrics: a series of cases; what are the advantages and boards? BMC Res Notes. 2009; 2: 132. https://doi.org/10.1186/1756-0500-2-132
  36. Sarikaya S, Biskin S, Damar M, Ugur MB, Sakalli E, Bektas S. Histopathological effects of fibrin glue and cyanoacrylate on the maxillary sinus. Turk Arch Otorhinolaryngol. 2016; 54: 63-8. https://doi.org/10.5152/tao.2016.1590
  37. Jones GT, Jian XC, Laskin DM. The effect of L-dopa on the healing of a rat mandibular defect. J Oral Maxillofac Surg. 1996; 54: 470-3. https://doi.org/10.1016/S0278-2391(96)90124-X
  38. Liu YT, Lee TM, Lui TS. Enhanced osteoblastic cell response on zirconia by bio-inspired surface modification. Colloids Surf B Biointerfaces. 2013; 106: 37-45. https://doi.org/10.1016/j.colsurfb.2013.01.023
  39. Choi BH, Cheong H, Ahn JS, Zhou C, Kwon JJ, Cha HJ, Jun SH. Engineered mussel bioglue as a functional osteoinductive binder for grafting of bone substitute particles to accelerate in vivo bone regeneration. J Mater Chem B. 2015; 3: 546-55. https://doi.org/10.1039/C4TB01197J
  40. Nagata MJ, Melo LG, Messora MR, Bomfim SR, Fucini SE, Garcia VG, Bosco AF, Okamoto T. Effect of platelet-rich plasma on bone healing of autogenous bone grafts in critical-size defects. J Clin Periodontol. 2009; 36: 775-83. https://doi.org/10.1111/j.1600-051X.2009.01450.x
  41. Li Y, Chen SK, Li L, Qin L, Wang XL, Lai YX. Bone defect animal models for testing efficacy of bone substitute biomaterials. J Orthop Translat. 2015; 3: 95-104. https://doi.org/10.1016/j.jot.2015.05.002
  42. Messora MR, Nagata MJ, Dornelles RC, Bomfim SR, Furlaneto FA, de Melo LG, Deliberador TM, Bosco AF, Garcia VG, Fucini SE. Bone healing in critical-size defects treated with platelet-rich plasma activated by two different methods. A histologic and histometric study in rat calvaria. J Periodontal Res. 2008; 43: 723-9. https://doi.org/10.1111/j.1600-0765.2008.01084.x
  43. Wang D, Tabassum A, Wu G, Deng L, Wismeijer D, Liu Y. Bone regeneration in critical-sized bone defect enhanced by introducing osteoinductivity to biphasic calcium phosphate granules. Clin Oral Implants Res. 2017; 28: 251-60.
  44. Sohn JY, Park JC, Um YJ, Jung UW, Kim CS, Cho KS, Choi SH. Spontaneous healing capacity of rabbit cranial defects of various sizes. J Periodontal Implant Sci. 2010; 40: 180-7. https://doi.org/10.5051/jpis.2010.40.4.180