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International Journal of Biomaterials
Volume 2014 (2014), Article ID 134521, 11 pages
http://dx.doi.org/10.1155/2014/134521
Research Article

Controlled Release of Granulocyte Colony-Stimulating Factor Enhances Osteoconductive and Biodegradable Properties of Beta-Tricalcium Phosphate in a Rat Calvarial Defect Model

1Department of Plastic and Reconstructive Surgery, Hokkaido University Graduate School of Medicine, Sapporo, Hokkaido 060-8638, Japan
2Department of Plastic and Reconstructive Surgery, Otaru Kyokai Hospital, Suminoe-1-6-15, Otaru, Hokkaido 047-8510, Japan
3Department of Biomaterials, Field of Tissue Engineering, Institute for Frontier Medical Sciences, Kyoto University, Kyoto 606-8507, Japan

Received 13 August 2013; Revised 27 November 2013; Accepted 27 November 2013; Published 14 April 2014

Academic Editor: Traian V. Chirila

Copyright © 2014 Tomohiro Minagawa et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. J. Boyne, “Use of marrow cancellous bone grafts in maxillary alveolar and palatal clefts,” Journal of Dental Research, vol. 53, no. 4, pp. 821–824, 1974. View at Scopus
  2. F. E. Abyholm, O. Bergland, and G. Semb, “Secondary bone grafting of alveolar clefts. A surgical/orthodontic treatment enabling a non-prosthodontic rehabilitation in cleft lip and palate patients,” Scandinavian Journal of Plastic and Reconstructive Surgery, vol. 15, no. 2, pp. 127–140, 1981. View at Scopus
  3. I. T. Jackson, L. R. Scheker, J. G. Vandervord, and J. G. McLennan, “Bone marrow grafting in the secondary closure of alveolar-palatal defects in children,” British Journal of Plastic Surgery, vol. 34, no. 4, pp. 422–425, 1981. View at Scopus
  4. H. Enemark, S. Sindet-Pedersen, and M. Bundgaard, “Long-term results after secondary bone grafting of alveolar clefts,” Journal of Oral and Maxillofacial Surgery, vol. 45, no. 11, pp. 913–918, 1987. View at Scopus
  5. M. Cohen, J. W. Polley, and A. A. Figueroa, “Secondary (intermediate) alveolar bone grafting,” Clinics in Plastic Surgery, vol. 20, no. 4, pp. 691–705, 1993. View at Scopus
  6. D. LaRossa, S. Buchman, D. M. Rothkopf, R. Mayro, P. Randall, and S. A. Wolfe, “A comparison of iliac and cranial bone in secondary grafting of alveolar clefts,” Plastic and Reconstructive Surgery, vol. 96, no. 4, pp. 789–799, 1995. View at Scopus
  7. A. K. Bajaj, A. A. Wongworawat, and A. Punjabi, “Management of alveolar clefts,” The Journal of Craniofacial Surgery, vol. 14, no. 6, pp. 840–846, 2003. View at Scopus
  8. W. M. M. T. van Hout, A. B. M. van der Molen, C. C. Breugem, R. Koole, and E. M. van Cann, “Reconstruction of the alveolar cleft: can growth factor-aided tissue engineering replace autologous bone grafting? A literature review and systematic review of results obtained with bone morphogenetic protein-2,” Clinical Oral Investigations, vol. 15, no. 3, pp. 297–303, 2011. View at Publisher · View at Google Scholar · View at Scopus
  9. A. M. Sadove, C. L. Nelson, B. L. Eppley, and B. Nguyen, “An evaluation of calvarial and iliac donor sites in alveolar cleft grafting,” Cleft Palate Journal, vol. 27, no. 3, pp. 225–228, 1990. View at Scopus
  10. K. H. Dawson, M. A. Egbert, and R. W. T. Myall, “Pain following iliac crest bone grafting of alveolar clefts,” Journal of Cranio-Maxillo-Facial Surgery, vol. 24, no. 3, pp. 151–154, 1996. View at Publisher · View at Google Scholar · View at Scopus
  11. M. C. Swan and T. E. E. Goodacre, “Morbidity at the iliac crest donor site following bone grafting of the cleft alveolus,” British Journal of Oral and Maxillofacial Surgery, vol. 44, no. 2, pp. 129–133, 2006. View at Publisher · View at Google Scholar · View at Scopus
  12. M. A. Rawashdeh and H. Telfah, “Secondary alveolar bone grafting: the dilemma of donor site selection and morbidity,” British Journal of Oral and Maxillofacial Surgery, vol. 46, no. 8, pp. 665–670, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. Z. H. Baqain, M. Anabtawi, A. A. Karaky, and Z. Malkawi, “Morbidity from anterior Iliac crest bone harvesting for secondary alveolar bone grafting: an outcome assessment study,” Journal of Oral and Maxillofacial Surgery, vol. 67, no. 3, pp. 570–575, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. G. Szabó, L. Huys, P. Coulthard et al., “A prospective multicenter randomized clinical trial of autogenous bone versus β-tricalcium phosphate graft alone for bilateral sinus elevation: histologic and histomorphometric evaluation,” International Journal of Oral and Maxillofacial Implants, vol. 20, no. 3, pp. 371–381, 2005. View at Scopus
  15. S. A. Zijderveld, I. R. Zerbo, J. P. A. van den Bergh, E. A. J. M. Schulten, and C. M. Ten Bruggenkate, “Maxillary sinus floor augmentation using a β-tricalcium phosphate (Cerasorb) alone compared to autogenous bone grafts,” International Journal of Oral and Maxillofacial Implants, vol. 20, no. 3, pp. 432–440, 2005. View at Scopus
  16. L.-Y. Dai and L.-S. Jiang, “Single-level instrumented posterolateral fusion of lumbar spine with β-tricalcium phosphate versus autograft: a prospective, randomized study with 3-year follow-up,” Spine, vol. 33, no. 12, pp. 1299–1304, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. A. de Ruiter, G. Meijer, T. Dormaar et al., “β-TCP versus autologous bone for repair of alveolar clefts in a goat model,” Cleft Palate-Craniofacial Journal, vol. 48, no. 6, pp. 654–662, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. D. Zhang, F. Chu, Y. Yang et al., “Orthodontic tooth movement in alveolar cleft repaired with a tissue engineering bone: an experimental study in dogs,” Tissue Engineering A, vol. 17, no. 9-10, pp. 1313–1325, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. J. A. Jadlowiec, A. B. Celil, and J. O. Hollinger, “Bone tissue engineering: recent advances and promising therapeutic agents,” Expert Opinion on Biological Therapy, vol. 3, no. 3, pp. 409–423, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. A. J. Salgado, O. P. Coutinho, and R. L. Reis, “Bone tissue engineering: state of the art and future trends,” Macromolecular Bioscience, vol. 4, no. 8, pp. 743–765, 2004. View at Publisher · View at Google Scholar · View at Scopus
  21. J. L. Moreau, J. F. Caccamese, D. P. Coletti, J. J. Sauk, and J. P. Fisher, “Tissue engineering solutions for cleft palates,” Journal of Oral and Maxillofacial Surgery, vol. 65, no. 12, pp. 2503–2511, 2007. View at Publisher · View at Google Scholar · View at Scopus
  22. P. Alvarez, C. K. Hee, L. Solchaga et al., “Growth factors and craniofacial surgery,” Journal of Craniofacial Surgery, vol. 23, no. 1, pp. 20–29, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. B. Behr, M. Sorkin, M. Lehnhardt, A. Renda, M. T. Longaker, and N. Quarto, “A comparative analysis of the osteogenic effects of BMP-2, FGF-2, and VEGFA in a calvarial defect model,” Tissue Engineering A, vol. 18, no. 9-10, pp. 1079–1086, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. M. Mayer, J. Hollinger, E. Ron, and J. Wozney, “Maxillary alveolar cleft repair in dogs using recombinant human bone morphogenetic protein-2 and a polymer carrier,” Plastic and Reconstructive Surgery, vol. 98, no. 2, pp. 247–259, 1996. View at Publisher · View at Google Scholar · View at Scopus
  25. L. Hong, Y. Tabata, M. Yamamoto et al., “Comparison of bone regeneration in a rabbit skull defect by recombinant human BMP-2 incorporated in biodegradable hydrogel and in solution,” Journal of Biomaterials Science, Polymer Edition, vol. 9, no. 9, pp. 1001–1014, 1998. View at Scopus
  26. M. Yamamoto, Y. Tabata, and Y. Ikada, “Ectopic bone formation induced by biodegradable hydrogels incorporating bone morphogenetic protein,” Journal of Biomaterials Science, Polymer Edition, vol. 9, no. 5, pp. 439–458, 1998. View at Scopus
  27. T. Higuchi, A. Kinoshita, K. Takahashi, S. Oda, and I. Ishikawa, “Bone regeneration by recombinant human bone morphogenetic protein-2 in rat mandibular defects. An experimental model of defect filling,” Journal of Periodontology, vol. 70, no. 9, pp. 1026–1031, 1999. View at Publisher · View at Google Scholar · View at Scopus
  28. P. J. Boyne, “Application of bone morphogenetic proteins in the treatment of clinical oral and maxillofacial osseous defects,” The Journal of Bone & Joint Surgery A, vol. 83, supplement 1, pp. S146–S150, 2001. View at Scopus
  29. M. Yamamoto, Y. Takahashi, and Y. Tabata, “Controlled release by biodegradable hydrogels enhances the ectopic bone formation of bone morphogenetic protein,” Biomaterials, vol. 24, no. 24, pp. 4375–4383, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Chin, T. Ng, W. K. Tom, and M. Carstens, “Repair of alveolar clefts with recombinant human bone morphogenetic protein (rhBMP-2) in patients with clefts,” Journal of Craniofacial Surgery, vol. 16, no. 5, pp. 778–789, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Yamamoto, Y. Takahashi, and Y. Tabata, “Enhanced bone regeneration at a segmental bone defect by controlled release of bone morphogenetic protein-2 from a biodegradable hydrogel,” Tissue Engineering, vol. 12, no. 5, pp. 1305–1311, 2006. View at Publisher · View at Google Scholar · View at Scopus
  32. A. S. Herford, P. J. Boyne, R. Rawson, and R. P. Williams, “Bone morphogenetic protein-induced repair of the premaxillary cleft,” Journal of Oral and Maxillofacial Surgery, vol. 65, no. 11, pp. 2136–2141, 2007. View at Publisher · View at Google Scholar · View at Scopus
  33. A. S. Herford, P. J. Boyne, and R. P. Williams, “Clinical applications of rhBMP-2 in maxillofacial surgery,” Journal of the California Dental Association, vol. 35, no. 5, pp. 335–341, 2007. View at Scopus
  34. B. P. Dickinson, R. K. Ashley, K. L. Wasson et al., “Reduced morbidity and improved healing with bone morphogenic protein-2 in older patients with alveolar cleft defects,” Plastic and Reconstructive Surgery, vol. 121, no. 1, pp. 209–217, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. N. Alonso, D. Y. S. Tanikawa, R. D. S. Freitas, L. Canan Jr., T. O. Ozawa, and D. L. Rocha, “Evaluation of maxillary alveolar reconstruction using a resorbable collagen sponge with recombinant human bone morphogenetic protein-2 in cleft lip and palate patients,” Tissue Engineering C: Methods, vol. 16, no. 5, pp. 1183–1189, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. S. Asamura, Y. Mochizuki, M. Yamamoto, Y. Tabata, and N. Isogai, “Bone regeneration using a bone morphogenetic protein-2 saturated slow-release gelatin hydrogel sheet: evaluation in a canine orbital floor fracture model,” Annals of Plastic Surgery, vol. 64, no. 4, pp. 496–502, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. K. Yamada, Y. Tabata, K. Yamamoto et al., “Potential efficacy of basic fibroblast growth factor incorporated in biodegradable hydrogels for skull bone regeneration,” Journal of Neurosurgery, vol. 86, no. 5, pp. 871–875, 1997. View at Scopus
  38. Y. Tabata, K. Yamada, S. Miyamoto et al., “Bone regeneration by basic fibroblast growth factor complexed with biodegradable hydrogels,” Biomaterials, vol. 19, no. 7–9, pp. 807–815, 1998. View at Publisher · View at Google Scholar · View at Scopus
  39. Y. Tabata, K. Yamada, L. Hong, S. Miyamoto, N. Hashimoto, and Y. Ikada, “Skull bone regeneration in primates in response to basic fibroblast growth factor,” Journal of Neurosurgery, vol. 91, no. 5, pp. 851–856, 1999. View at Scopus
  40. A. Iwakura, Y. Tabata, M. Miyao et al., “Novel method to enhance sternal healing after harvesting bilateral internal thoracic arteries with use of basic fibroblast growth factor,” Circulation, vol. 102, no. 19, pp. III307–III311, 2000. View at Scopus
  41. A. Iwakura, Y. Tabata, N. Tamura et al., “Gelatin sheet incorporating basic fibroblast growth factor enhances healing of devascularized sternum in diabetic rats,” Circulation, vol. 104, pp. I325–I329, 2001. View at Scopus
  42. K. Hayashi, T. Kubo, K. Doi, Y. Tabata, and Y. Akagawa, “Development of new drug delivery system for implant bone augmentation using a basic fibroblast growth factor-gelatin hydrogel complex,” Dental Materials Journal, vol. 26, no. 2, pp. 170–177, 2007. View at Scopus
  43. D. M. Arm, A. F. Tencer, S. D. Bain, and D. Celino, “Effect of controlled release of platelet-derived growth factor from a porous hydroxyapatite implant on bone ingrowth,” Biomaterials, vol. 17, no. 7, pp. 703–709, 1996. View at Publisher · View at Google Scholar · View at Scopus
  44. G. Pellegrini, Y. J. Seol, R. Gruber, and W. V. Giannobile, “Pre-clinical models for oral and periodontal reconstructive therapies,” Journal of Dental Research, vol. 88, no. 12, pp. 1065–1076, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. C. S. Young, P. A. Ladd, C. F. Browning et al., “Release, biological potency, and biochemical integrity of recombinant human platelet-derived growth factor-BB (rhPDGF-BB) combined with AugmentTM Bone Graft or GEM 21S beta-tricalcium phosphate (β-TCP),” Journal of Controlled Release, vol. 140, no. 3, pp. 250–255, 2009. View at Publisher · View at Google Scholar · View at Scopus
  46. T. Choo, V. Marino, and P. M. Bartold, “Effect of PDGF-BB and beta-tricalcium phosphate (β-TCP) on bone formation around dental implants: a pilot study in sheep,” Clinical Oral Implants Research, vol. 24, no. 2, pp. 158–166, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. L. Hong, S. Miyamoto, N. Hashimoto, and Y. Tabata, “Synergistic effect of gelatin microspheres incorporating TGF-β1 and a physical barrier for fibrous tissue infiltration on skull bone formation,” Journal of Biomaterials Science, Polymer Edition, vol. 11, no. 12, pp. 1357–1369, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. L. Hong, Y. Tabata, S. Miyamoto et al., “Promoted bone healing at a rabbit skull gap between autologous bone fragment and the surrounding intact bone with biodegradable microspheres containing transforming growth factor-β1,” Tissue Engineering, vol. 6, no. 4, pp. 331–340, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. L. Hong, Y. Tabata, S. Miyamoto et al., “Bone regeneration at rabbit skull defects treated with transforming growth factor-β1 incorporated into hydrogels with different levels of biodegradability,” Journal of Neurosurgery, vol. 92, no. 2, pp. 315–325, 2000. View at Scopus
  50. M. Yamamoto, Y. Tabata, L. Hong, S. Miyamoto, N. Hashimoto, and Y. Ikada, “Bone regeneration by transforming growth factor β1 released from a biodegradable hydrogel,” Journal of Controlled Release, vol. 64, no. 1–3, pp. 133–142, 2000. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Furumatsu, Z. N. Shen, A. Kawai et al., “Vascular endothelial growth factor principally acts as the main angiogenic factor in the early stage of human osteoblastogenesis,” The Journal of Biochemistry, vol. 133, no. 5, pp. 633–639, 2003. View at Publisher · View at Google Scholar · View at Scopus
  52. N. Casap, N. B. Venezia, A. Wilensky, and Y. Samuni, “VEGF facilitates periosteal distraction-induced osteogenesis in rabbits: a micro-computerized tomography study,” Tissue Engineering A, vol. 14, no. 2, pp. 247–253, 2008. View at Publisher · View at Google Scholar · View at Scopus
  53. E. Schipani, C. Maes, G. Carmeliet, and G. L. Semenza, “Regulation of osteogenesis-angiogenesis coupling by HIFs and VEGF,” Journal of Bone and Mineral Research, vol. 24, no. 8, pp. 1347–1353, 2009. View at Publisher · View at Google Scholar · View at Scopus
  54. C.-J. Wang, K.-E. Huang, Y.-C. Sun et al., “VEGF modulates angiogenesis and osteogenesis in shockwave-promoted fracture healing in rabbits,” Journal of Surgical Research, vol. 171, no. 1, pp. 114–119, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. Y. Tabata, A. Nagano, Y. Ikada, and Y. Ikada, “Biodegradation of hydrogel carrier incorporating fibroblast growth factor,” Tissue Engineering, vol. 5, no. 2, pp. 127–138, 1999. View at Scopus
  56. A. Kanematsu, S. Yamamoto, M. Ozeki et al., “Collagenous matrices as release carriers of exogenous growth factors,” Biomaterials, vol. 25, no. 18, pp. 4513–4520, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Bozlar, B. Aslan, A. Kalaci, L. Baktiroglu, A. N. Yanat, and A. Tasci, “Effects of human granulocyte-colony stimulating factor on fracture healing in rats,” Saudi Medical Journal, vol. 26, no. 8, pp. 1250–1254, 2005. View at Scopus
  58. Y. Mifune, T. Matsumoto, A. Kawamoto et al., “Local delivery of granulocyte colony stimulating factor-mobilized CD34-positive progenitor cells using bioscaffold for modality of unhealing bone fracture,” Stem Cells, vol. 26, no. 6, pp. 1395–1405, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. K. Ishida, T. Matsumoto, K. Sasaki et al., “Bone regeneration properties of granulocyte colony-stimulating factor via neovascularization and osteogenesis,” Tissue Engineering A, vol. 16, no. 10, pp. 3271–3284, 2010. View at Publisher · View at Google Scholar · View at Scopus
  60. R. Kuroda, T. Matsumoto, M. Miwa et al., “Local transplantation of G-CSF-mobilized CD34+ cells in a patient with tibial nonunion: a case report,” Cell Transplantation, vol. 20, no. 9, pp. 1491–1496, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. A. Lindemann, F. Herrmann, W. Oster et al., “Hematologic effects of recombinant human granulocyte colony-stimulating factor in patients with malignancy,” Blood, vol. 74, no. 8, pp. 2644–2651, 1989. View at Scopus
  62. G. D. Demetri and J. D. Griffin, “Granulocyte colony-stimulating factor and its receptor,” Blood, vol. 78, no. 11, pp. 2791–2808, 1991. View at Scopus
  63. S. Kojima and T. Matsuyama, “Stimulation of granulopoiesis by high-dose recombinant human granulocyte colony-stimulating factor in children with aplastic anemia and very severe neutropenia,” Blood, vol. 83, no. 6, pp. 1474–1478, 1994. View at Scopus
  64. M. R. Bishop, S. R. Tarantolo, R. B. Geller et al., “A randomized, double-blind trial of filgrastim (granulocyte colony- stimulating factor) versus placebo following allogeneic blood stem cell transplantation,” Blood, vol. 96, no. 1, pp. 80–85, 2000. View at Scopus
  65. C. Patte, A. Laplanche, A. I. Bertozzi et al., “Granulocyte colony-stimulating factor in induction treatment of children with non-Hodgkin's lymphoma: a randomized study of the French Society of Pediatric Oncology,” Journal of Clinical Oncology, vol. 20, no. 2, pp. 441–448, 2002. View at Publisher · View at Google Scholar · View at Scopus
  66. J. A. Heath, P. G. Steinherz, A. Altman et al., “Human granulocyte colony-stimulating factor in children with high-risk acute lymphoblastic leukemia: a Children's Cancer Group Study,” Journal of Clinical Oncology, vol. 21, no. 8, pp. 1612–1617, 2003. View at Publisher · View at Google Scholar · View at Scopus
  67. B. Wittman, J. Horan, and G. H. Lyman, “Prophylactic colony-stimulating factors in children receiving myelosuppressive chemotherapy: a meta-analysis of randomized controlled trials,” Cancer Treatment Reviews, vol. 32, no. 4, pp. 289–303, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. T. Lehrnbecher, M. Zimmermann, D. Reinhardt, M. Dworzak, J. Stary, and U. Creutzig, “Prophylactic human granulocyte colony-stimulating factor after induction therapy in pediatric acute myeloid leukemia,” Blood, vol. 109, no. 3, pp. 936–943, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. H. Inaba, X. Cao, S. Pounds et al., “Randomized trial of 2 dosages of prophylactic granulocyte-colony- stimulating factor after induction chemotherapy in pediatric acute myeloid leukemia,” Cancer, vol. 117, no. 6, pp. 1313–1320, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. E. R. Luvizuto, S. Tangl, G. Zanoni et al., “The effect of BMP-2 on the osteoconductive properties of β-tricalcium phosphate in rat calvaria defects,” Biomaterials, vol. 32, no. 15, pp. 3855–3861, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. H. Rojbani, M. Nyan, K. Ohya, and S. Kasugai, “Evaluation of the osteoconductivity of α-tricalcium phosphate, β-tricalcium phosphate, and hydroxyapatite combined with or without simvastatin in rat calvarial defect,” Journal of Biomedical Materials Research A, vol. 98, no. 4, pp. 488–498, 2011. View at Publisher · View at Google Scholar · View at Scopus
  72. E. Kato, J. Lemler, K. Sakurai, and M. Yamada, “Biodegradation property of beta-tricalcium phosphate-collagen composite in accordance with bone formation: a comparative study with bio-oss collagen in a rat critical-size defect model,” Clinical Implant Dentistry and Related Research, 2012. View at Publisher · View at Google Scholar
  73. P. Zanchetta, N. Lagarde, A. Uguen, and P. Marcorelles, “Mixture of hyaluronic acid, chondroitin 6 sulphate and dermatan sulphate used to completely regenerate bone in rat critical size defect model,” Journal of Cranio-Maxillofacial Surgery, vol. 40, no. 8, pp. 783–787, 2012. View at Publisher · View at Google Scholar · View at Scopus
  74. Y. Tabata, S. Hijikata, and Y. Ikada, “Enhanced vascularization and tissue granulation by basic fibroblast growth factor impregnated in gelatin hydrogels,” Journal of Controlled Release, vol. 31, no. 2, pp. 189–199, 1994. View at Publisher · View at Google Scholar · View at Scopus
  75. B. Levi, E. R. Nelson, K. Brown et al., “Differences in osteogenic differentiation of adipose-derived stromal cells from murine, canine, and human sources in vitro and in vivo,” Plastic & Reconstructive Surgery, vol. 128, no. 2, pp. 373–386, 2011. View at Publisher · View at Google Scholar · View at Scopus
  76. S. V. Dorozhkin, “Calcium orthophosphate cements for biomedical application,” Journal of Materials Science, vol. 43, no. 9, pp. 3028–3057, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. H.-H. Horch, R. Sader, C. Pautke, A. Neff, H. Deppe, and A. Kolk, “Synthetic, pure-phase beta-tricalcium phosphate ceramic granules (Cerasorb) for bone regeneration in the reconstructive surgery of the jaws,” International Journal of Oral and Maxillofacial Surgery, vol. 35, no. 8, pp. 708–713, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. W. L. J. Weijs, T. J. H. Siebers, A. M. Kuijpers-Jagtman, S. J. Bergé, G. J. Meijer, and W. A. Borstlap, “Early secondary closure of alveolar clefts with mandibular symphyseal bone grafts and β-tri calcium phosphate (β-TCP),” International Journal of Oral and Maxillofacial Surgery, vol. 39, no. 5, pp. 424–429, 2010. View at Publisher · View at Google Scholar · View at Scopus
  79. J. H. Park, C. G. Choi, S. R. Jeon, S. C. Rhim, C. J. Kim, and S. W. Roh, “Radiographic analysis of instrumented posterolateral fusion mass using mixture of local autologous bone and b-TCP (polybone) in a lumbar spinal fusion surgery,” Journal of Korean Neurosurgical Society, vol. 49, no. 5, pp. 267–272, 2011. View at Publisher · View at Google Scholar · View at Scopus
  80. S. Jingushi, K. Urabe, K. Okazaki et al., “Intramuscular bone induction by human recombinant bone morphogenetic protein-2 with beta-tricalcium phosphate as a carrier: in vivo bone banking for muscle-pedicle autograft,” Journal of Orthopaedic Science, vol. 7, no. 4, pp. 490–494, 2002. View at Publisher · View at Google Scholar · View at Scopus
  81. A. Abarrategi, C. Moreno-Vicente, V. Ramos, I. Aranaz, J. V. Sanz Casado, and J. L. López-Lacomba, “Improvement of porous β-TCP scaffolds with rhBMP-2 chitosan carrier film for bone tissue application,” Tissue Engineering A, vol. 14, no. 8, pp. 1305–1319, 2008. View at Publisher · View at Google Scholar · View at Scopus
  82. U. Maus, S. Andereya, S. Gravius, J. A. K. Ohnsorge, C. Niedhart, and C. H. Siebert, “BMP-2 incorporated in a tricalcium phosphate bone substitute enhances bone remodeling in sheep,” Journal of Biomaterials Applications, vol. 22, no. 6, pp. 559–576, 2008. View at Publisher · View at Google Scholar · View at Scopus
  83. G. Matsumoto, Y. Omi, E. Kubota et al., “Enhanced regeneration of critical bone defects using a biodegradable gelatin sponge and β-tricalcium phosphate with bone morphogenetic protein-2,” Journal of Biomaterials Applications, vol. 24, no. 4, pp. 327–342, 2009. View at Publisher · View at Google Scholar · View at Scopus
  84. J. Sohier, G. Daculsi, S. Sourice, K. de Groot, and P. Layrolle, “Porous beta tricalcium phosphate scaffolds used as a BMP-2 delivery system for bone tissue engineering,” Journal of Biomedical Materials Research A, vol. 92, no. 3, pp. 1105–1114, 2010. View at Publisher · View at Google Scholar · View at Scopus
  85. Y. Takahashi, M. Yamamoto, and Y. Tabata, “Osteogenic differentiation of mesenchymal stem cells in biodegradable sponges composed of gelatin and β-tricalcium phosphate,” Biomaterials, vol. 26, no. 17, pp. 3587–3596, 2005. View at Publisher · View at Google Scholar · View at Scopus
  86. L. Xu, K. Lv, W. Zhang, X. Zhang, X. Jiang, and F. Zhang, “The healing of critical-size calvarial bone defects in rat with rhPDGF-BB, BMSCs, and β-TCP scaffolds,” Journal of Materials Science: Materials in Medicine, vol. 23, no. 4, pp. 1073–1084, 2012. View at Publisher · View at Google Scholar · View at Scopus
  87. T. Matsumoto, A. Kawamoto, R. Kuroda et al., “Therapeutic potential of vasculogenesis and osteogenesis promoted by peripheral blood CD34-positive cells for functional bone healing,” The American Journal of Pathology, vol. 169, no. 4, pp. 1440–1457, 2006. View at Publisher · View at Google Scholar · View at Scopus
  88. A. J. Laing, J. P. Dillon, E. T. Condon et al., “Mobilization of endothelial precursor cells: systemic vascular response to musculoskeletal trauma,” Journal of Orthopaedic Research, vol. 25, no. 1, pp. 44–50, 2007. View at Publisher · View at Google Scholar · View at Scopus
  89. T. Matsumoto, Y. Mifune, A. Kawamoto et al., “Fracture induced mobilization and incorporation of bone marrow-derived endothelial progenitor cells for bone healing,” Journal of Cellular Physiology, vol. 215, no. 1, pp. 234–242, 2008. View at Publisher · View at Google Scholar · View at Scopus
  90. A. Janowska-Wleczorek, M. Majka, J. Ratajczak, and M. Z. Ratajczak, “Autocrine/paracrine mechanisms in human hematopoiesis,” Stem Cells, vol. 19, no. 2, pp. 99–107, 2001. View at Scopus
  91. M. Majka, A. Janowska-Wieczorek, J. Ratajczak et al., “Numerous growth factors, cytokines, and chemokines are secreted by human CD34+ cells, myeloblasts, erythroblasts, and megakaryoblasts and regulate normal hematopoiesis in an autocrine/paracrine manner,” Blood, vol. 97, no. 10, pp. 3075–3085, 2001. View at Publisher · View at Google Scholar · View at Scopus
  92. J.-L. Chen, P. Hunt, M. Mcelvain, T. Black, S. Kaufman, and E. S.-H. Choi, “Osteoblast precursor cells are found in CD34+ cells from human bone marrow,” Stem Cells, vol. 15, no. 5, pp. 368–377, 1997. View at Scopus
  93. A. Iwakura, Y. Tabata, T. Koyama et al., “Gelatin sheet incorporating basic fibroblast growth factor enhances sternal healing after harvesting bilateral internal thoracic arteries,” Journal of Thoracic and Cardiovascular Surgery, vol. 126, no. 4, pp. 1113–1120, 2003. View at Publisher · View at Google Scholar · View at Scopus
  94. Y. Tabata, “Tissue regeneration based on growth factor release,” Tissue Engineering, vol. 9, supplement 1, pp. S5–S15, 2003. View at Scopus
  95. M. Kamitakahara, C. Ohtsuki, and T. Miyazaki, “Review paper: behavior of ceramic biomaterials derived from tricalcium phosphate in physiological condition,” Journal of Biomaterials Applications, vol. 23, no. 3, pp. 197–212, 2008. View at Publisher · View at Google Scholar · View at Scopus
  96. S. Ghanaati, M. Barbeck, R. Detsch et al., “The chemical composition of synthetic bone substitutes influences tissue reactions in vivo: histological and histomorphometrical analysis of the cellular inflammatory response to hydroxyapatite, beta-tricalcium phosphate and biphasic calcium phosphate ceramics,” Biomedical Materials, vol. 7, no. 1, Article ID 015005, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. B. Liu and D. X. Lun, “Current application of beta-tricalcium phosphate composites in orthopaedics,” Orthopaedic Surgery, vol. 4, no. 3, pp. 139–144, 2012. View at Publisher · View at Google Scholar
  98. N. Brouard, R. Driessen, B. Short, and P. J. Simmons, “G-CSF increases mesenchymal precursor cell numbers in the bone marrow via an indirect mechanism involving osteoclast-mediated bone resorption,” Stem Cell Research, vol. 5, no. 1, pp. 65–75, 2010. View at Publisher · View at Google Scholar · View at Scopus
  99. J.-W. Jang, J.-H. Yun, K.-I. Lee et al., “Osteoinductive activity of biphasic calcium phosphate with different rhBMP-2 doses in rats,” Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology and Endodontology, vol. 113, no. 4, pp. 480–487, 2012. View at Publisher · View at Google Scholar · View at Scopus
  100. T. Asahara, H. Masuda, T. Takahashi et al., “Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization,” Circulation Research, vol. 85, no. 3, pp. 221–228, 1999. View at Scopus
  101. A. Taguchi, T. Soma, H. Tanaka et al., “Administration of CD34+ cells after stroke enhances neurogenesis via angiogenesis in a mouse model,” The Journal of Clinical Investigation, vol. 114, no. 3, pp. 330–338, 2004. View at Publisher · View at Google Scholar · View at Scopus
  102. H. Iwasaki, A. Kawamoto, M. Ishikawa et al., “Dose-dependent contribution of CD34-positive cell transplantation to concurrent vasculogenesis and cardiomyogenesis for functional regenerative recovery after myocardial infarction,” Circulation, vol. 113, no. 10, pp. 1311–1325, 2006. View at Publisher · View at Google Scholar · View at Scopus
  103. K. Sasaki, R. Kuroda, K. Ishida et al., “Enhancement of tendon-bone osteointegration of anterior cruciate ligament graft using granulocyte colony-stimulating factor,” The American Journal of Sports Medicine, vol. 36, no. 8, pp. 1519–1527, 2008. View at Publisher · View at Google Scholar · View at Scopus
  104. A. K. Lundgren, D. Lundgren, C. H. F. Hämmerle, S. Nyman, and L. Sennerby, “Influence of decortication of the donor bone on guided bone augmentation an experimental study in the rabbit skull bone,” Clinical Oral Implants Research, vol. 11, no. 2, pp. 99–106, 2000. View at Scopus