Segmental mandibular bone reconstruction with a carbonate-substituted hydroxyapatite-coated modular endoprosthetic poly(ɛ-caprolactone) scaffold in Macaca fascicularis
Corresponding Author
Nattharee Chanchareonsook
Department of Oral and Maxillofacial Surgery, National Dental Centre, Singapore, Singapore
Correspondence to: N. Chanchareonsook (e-mail: [email protected])Search for more papers by this authorHenk Tideman
Department of Oral and Maxillofacial Surgery, Research advisor, National Dental Centre, Singapore, Singapore
Search for more papers by this authorStephen E. Feinberg
Department of Oral and Maxillofacial Surgery, University of Michigan, Ann Arbor, Michigan
Department of Biomedical Engineering, College of Engineering, University of Michigan, Ann Arbor, Michigan
Search for more papers by this authorLeenaporn Jongpaiboonkit
Tissue Regeneration Systems, Inc, Ann Arbor, Michigan
Search for more papers by this authorShermin Lee
Department of Oral and Maxillofacial Surgery, National Dental Centre, Singapore, Singapore
Search for more papers by this authorColleen Flanagan
Department of Biomedical Engineering, College of Engineering, University of Michigan, Ann Arbor, Michigan
Search for more papers by this authorGita Krishnaswamy
Centre for Quantitative Medicine, Duke-NUS Graduate Medical School, Singapore, Singapore
Search for more papers by this authorJohn Jansen
Department of Biomaterials, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
Search for more papers by this authorCorresponding Author
Nattharee Chanchareonsook
Department of Oral and Maxillofacial Surgery, National Dental Centre, Singapore, Singapore
Correspondence to: N. Chanchareonsook (e-mail: [email protected])Search for more papers by this authorHenk Tideman
Department of Oral and Maxillofacial Surgery, Research advisor, National Dental Centre, Singapore, Singapore
Search for more papers by this authorStephen E. Feinberg
Department of Oral and Maxillofacial Surgery, University of Michigan, Ann Arbor, Michigan
Department of Biomedical Engineering, College of Engineering, University of Michigan, Ann Arbor, Michigan
Search for more papers by this authorLeenaporn Jongpaiboonkit
Tissue Regeneration Systems, Inc, Ann Arbor, Michigan
Search for more papers by this authorShermin Lee
Department of Oral and Maxillofacial Surgery, National Dental Centre, Singapore, Singapore
Search for more papers by this authorColleen Flanagan
Department of Biomedical Engineering, College of Engineering, University of Michigan, Ann Arbor, Michigan
Search for more papers by this authorGita Krishnaswamy
Centre for Quantitative Medicine, Duke-NUS Graduate Medical School, Singapore, Singapore
Search for more papers by this authorJohn Jansen
Department of Biomaterials, Radboud University Nijmegen Medical Centre, Nijmegen, The Netherlands
Search for more papers by this authorAbstract
A bio-degradable scaffold incorporating osteoinductive factors is one of the alternative methods for achieving the regeneration of a mandibular bone defect. The current pilot study addressed such a bone reconstruction in a non-human primate model, Macaca fascicularis monkeys, with an engineered poly(ɛ-caprolactone) (PCL) scaffold, provided with a carbonate-substituted hydroxyapatite coating. The scaffolds were implanted into unilaterally created mandibular segmental defects in 24 monkeys. Three experimental groups were formed: (1) scaffolds with rhBMP-2 (n = 8), (2) scaffolds with autologous mixed bone marrow cells (n = 8), and (3) empty scaffolds as a control group (n = 8). Evaluation was based on clinical observation as well as micro-CT, mechanical, and histological analyses. Despite a high infection rate, the overall results showed that the currently designed PCL scaffolds had insufficient load-bearing capability, and complete bone union was not achieved after 6 months of implantation. Nevertheless, the group of PCL scaffolds loaded with rhBMP-2 showed evidence of bone-regenerative potential, in contrast to PCL with autologous mixed bone marrow cells and the control group. © 2013 Wiley Periodicals, Inc. J Biomed Mater Res Part B: Appl Biomater, 102B: 962–976, 2014.
REFERENCES
- 1Chim H, Salgado CJ, Mardini S, Chen HC. Reconstruction of mandibular defects. Semin Plast Surg 2010; 24: 188–197.
- 2Hadlock TA, Vacanti JP, Cheney ML. Tissue engineering in facial plastic and reconstructive surgery. Facial Plast Surg 1998; 14: 197–203.
- 3Lee S, Goh BT, Tideman H, Stoelinga PJ. Modular endoprosthesis for mandibular reconstruction: A preliminary animal study. Int J Oral Maxillofac Surg 2008; 37: 935–942.
- 4Wong RC, Lee S, Tideman H, Merkx MA, Jansen J, Liao K. Effect of replacement of mandibular defects with a modular endoprosthesis on bone mineral density in a monkey model. Int J Oral Maxillofac Surg 2011; 40: 633–639.
- 5Lee S, Goh BT, Tideman H, Stoelinga PJ, Jansen JA. Modular endoprosthesis for mandibular body reconstruction: A clinical, micro-CT and histologic evaluation in eight Macaca fascicularis. Int J Oral Maxillofac Surg 2009; 38: 40–47.
- 6Rai B, Ho KH, Lei Y, Si-Hoe KM, Jeremy Teo CM, Yacob KB, Chen F, Ng FC, Teoh SH. Polycaprolactone-20% tricalcium phosphate scaffolds in combination with platelet-rich plasma for the treatment of critical-sized defects of the mandible: A pilot study. J Oral Maxillofac Surg 2007; 65: 2195–2205.
- 7Schuckert KH, Jopp S, Teoh SH. Mandibular defect reconstruction using three-dimensional polycaprolactone scaffold in combination with platelet-rich plasma and recombinant human bone morphogenetic protein-2: De novo synthesis of bone in a single case. Tissue Eng Part A 2009; 15: 493–499.
- 8Hollister SJ, Lin CY, Saito E, Lin CY, Schek RD, Taboas JM, Williams JM, Partee B, Flanagan CL, Diggs A, Wilke EN, Van Lenthe GH, Müller R, Wirtz T, Das S, Feinberg SE, Krebsbach PH. Engineering craniofacial scaffolds. Orthod Craniofac Res 2005; 8: 162–173.
- 9Williams JM, Adewunmi A, Schek RM, Flanagan CL, Krebsbach PH, Feinberg SE, Hollister SJ, Das S. Bone tissue engineering using polycaprolactone scaffolds fabricated via selective laser sintering. Biomaterials 2005; 26: 4817–4827.
- 10Urist MR, Silverman BF, Buring K, Dubuc FL, Rosenberg JM. The bone induction principle. Clin Orthop Relat Res 1967; 53: 243–283.
- 11Barradas AM, Yuan H, van Blitterswijk CA, Habibovic P. Osteoinductive biomaterials: Current knowledge of properties, experimental models and biological mechanisms. Eur Cell Mater 2011; 21: 407–429; discussion 29.
- 12Suárez-González D, Barnhart K, Migneco F, Flanagan C, Hollister SJ, Murphy WL. Controllable mineral coatings on PCL scaffolds as carriers for growth factor release. Biomaterials 2012; 33: 713–721.
- 13Jongpaiboonkit L, Franklin-Ford T, Murphy WL. Growth of hydroxyapatite coatings on biodegradable polymer microspheres. ACS Appl Mater Interfaces 2009; 1: 1504–1511.
- 14Kim M, Choe S. BMPs and their clinical potentials. BMB Rep 2011; 44: 619–634.
- 15Herford AS, Cicciu M. Recombinant human bone morphogenetic protein type 2 jaw reconstruction in patients affected by giant cell tumor. J Craniofac Surg 2010; 21: 1970–1975.
- 16Boyne PJ. Application of bone morphogenetic proteins in the treatment of clinical oral and maxillofacial osseous defects. J Bone Joint Surg Am 2001; 83-A Suppl 1(Pt 2): S146–150.
- 17Wang EA, Rosen V, Cordes P, Hewick RM, Kriz MJ, Luxenberg DP, Sibley BS, Wozney JM. Purification and characterization of other distinct bone-inducing factors. Proc Natl Acad Sci USA 1988; 85: 9484–9488.
- 18Herford AS, Boyne PJ, Williams RP. Clinical applications of rhBMP-2 in maxillofacial surgery. J Calif Dent Assoc 2007; 35: 335–341.
- 19Wei G, Jin Q, Giannobile WV, Ma PX. The enhancement of osteogenesis by nano-fibrous scaffolds incorporating rhBMP-7 nanospheres. Biomaterials 2007; 28: 2087–2096.
- 20Forriol F, Longo UG, Concejo C, Ripalda P, Maffulli N, Denaro V. Platelet-rich plasma, rhOP-1 (rhBMP-7) and frozen rib allograft for the reconstruction of bony mandibular defects in sheep. A pilot experimental study. Injury 2009; 40 Suppl 3: S44–49.
- 21Busuttil Naudi K, Ayoub A, McMahon J, Di Silvio L, Lappin D, Hunter KD, Barbenel J. Mandibular reconstruction in the rabbit using beta-tricalcium phosphate (beta-TCP) scaffolding and recombinant bone morphogenetic protein 7 (rhBMP-7)—Histological, radiographic and mechanical evaluations. J Craniomaxillofac Surg 2012; 40: e461–469.
- 22Augello A, De Bari C. The regulation of differentiation in mesenchymal stem cells. Hum Gene Ther 2010; 21: 1226–1238.
- 23Caplan AI, Bruder SP. Mesenchymal stem cells: Building blocks for molecular medicine in the 21st century. Trends Mol Med 2001; 7: 259–264.
- 24Liu W, Cui L, Cao Y. Bone reconstruction with bone marrow stromal cells. Methods Enzymol 2006; 420: 362–380.
- 25Xiao Y, Mareddy S, Crawford R. Clonal characterization of bone marrow derived stem cells and their application for bone regeneration. Int J Oral Sci 2010; 2: 127–135.
- 26Yuan J, Zhang WJ, Liu G, Wei M, Qi ZL, Liu W, Cui L, Cao YL. Repair of canine mandibular bone defects with bone marrow stromal cells and coral. Tissue Eng Part A 2010; 16: 1385–1394.
- 27Alsberg E, Hill EE, Mooney DJ. Craniofacial tissue engineering. Crit Rev Oral Biol Med 2001; 12: 64–75.
- 28Wu W, Chen X, Mao T, Chen F, Feng X. Bone marrow-derived osteoblasts seeded into porous beta-tricalcium phosphate to repair segmental defect in canine's mandibula. Ulus Travma Acil Cerrahi Derg 2006; 12: 268–276.
- 29Yuan J, Cui L, Zhang WJ, Liu W, Cao Y. Repair of canine mandibular bone defects with bone marrow stromal cells and porous beta-tricalcium phosphate. Biomaterials 2007; 28: 1005–1013.
- 30Xi Q, Bu RF, Liu HC, Mao TQ. Reconstruction of caprine mandibular segmental defect by tissue engineered bone reinforced by titanium reticulum. Chin J Traumatol 2006; 9: 67–71.
- 31Jansen JA, Dhert WJ, van der Waerden JP, von Recum AF. Semi-quantitative and qualitative histologic analysis method for the evaluation of implant biocompatibility. J Invest Surg 1994; 7: 123–134.
- 32Bagi CM, Berryman E, Moalli MR. Comparative bone anatomy of commonly used laboratory animals: Implications for drug discovery. Comp Med 2011; 61: 76–85.
- 33Boyne PJ. Animal studies of application of rhBMP-2 in maxillofacial reconstruction. Bone 1996; 19(1 Suppl): 83S–92S.
- 34Boyne PJ, Nakamura A, Shabahang S. Evaluation of the long-term effect of function on rhBMP-2 regenerated hemimandibulectomy defects. Br J Oral Maxillofac Surg 1999; 37: 344–352.
- 35Herford AS, Lu M, Buxton AN, Kim J, Henkin J, Boyne PJ, Caruso JM, Rungcharassaeng K, Hong J. Recombinant human bone morphogenetic protein 2 combined with an osteoconductive bulking agent for mandibular continuity defects in nonhuman primates. J Oral Maxillofac Surg 2012; 70: 703–716.
- 36Seto I, Marukawa E, Asahina I. Mandibular reconstruction using a combination graft of rhBMP-2 with bone marrow cells expanded in vitro. Plast Reconstr Surg 2006; 117: 902–908.
- 37Kneser U, Schaefer DJ, Polykandriotis E, Horch RE. Tissue engineering of bone: The reconstructive surgeon's point of view. J Cell Mol Med 2006; 10: 7–19.
- 38Amini AR, Laurencin CT, Nukavarapu SP. Bone tissue engineering: Recent advances and challenges. Crit Rev Biomed Eng 2012; 40: 363–408.
- 39Vaquette C, Fawzi-Grancher S, Lavalle P, Frochot C, Viriot ML, Muller S, Wang X. In vitro biocompatibility of different polyester membranes. Biomed Mater Eng 2006; 16(4 Suppl): S131–136.
- 40Seyednejad H, Ghassemi AH, van Nostrum CF, Vermonden T, Hennink WE. Functional aliphatic polyesters for biomedical and pharmaceutical applications. J Control Release 2011; 152: 168–176.
- 41Herford AS, Boyne PJ. Reconstruction of mandibular continuity defects with bone morphogenetic protein-2 (rhBMP-2). J Oral Maxillofac Surg 2008; 66: 616–624.
- 42Hussein KA, Zakhary IE, Elawady AR, Emam HA, Sharawy M, Baban B, Akeel S, Al-Shabrawey M, Elsalanty ME. Difference in soft tissue response between immediate and delayed delivery suggests a new mechanism for recombinant human bone morphogenetic protein 2 action in large segmental bone defects. Tissue Eng Part A 2012; 18: 665–675.
- 43Marukawa E, Asahina I, Oda M, Seto I, Alam M, Enomoto S. Functional reconstruction of the non-human primate mandible using recombinant human bone morphogenetic protein-2. Int J Oral Maxillofac Surg 2002; 31: 287–295.
- 44Seto I, Tachikawa N, Mori M, Hoshino S, Marukawa E, Asahina I, Enomoto S. Restoration of occlusal function using osseointegrated implants in the canine mandible reconstructed by rhBMP-2. Clin Oral Implants Res 2002; 13: 536–541.
- 45Seto I, Asahina I, Oda M, Enomoto S. Reconstruction of the primate mandible with a combination graft of recombinant human bone morphogenetic protein-2 and bone marrow. J Oral Maxillofac Surg 2001; 59: 53–61; discussion 62–63.
- 46Zhou Q, Price DD, Callam CS, Woodruff MA, Verne GN. Effects of the N-methyl-D-aspartate receptor on temporal summation of second pain (wind-up) in irritable bowel syndrome. J Pain 2011; 12: 297–303.
- 47Merkli ATC, Gurny R, Heller J. Biodegradable polymers for the controlled release of ocular drugs. Prog Polym Sci 1998; 23: 563–580.
- 48Corden TJ, Jones IA, Rudd CD, Christian P, Downes S, McDougall KE. Physical and biocompatibility properties of poly-epsilon-caprolactone produced using in situ polymerisation: A novel manufacturing technique for long-fibre composite materials. Biomaterials 2000; 21: 713–724.
