Craniofacial Repair

  • Bruce A. Doll
  • Charles Sfeir
  • Kodi Azari
  • Sarah Holland
  • Jeffrey O. Hollinger

Abstract

Annually, skeletal injury and specifically craniofacial injury total approx 12.2 million people in the United States (1). Advances in craniofacial therapy, founded on developing knowledge of the molecular signals and intercellular communication, has greatly improved the restoration of form and function. Fracture healing is a complex physiological process. Cellular and biochemical processes that occur during fracture healing parallel those that take place in the growth plate during development, except in fracture healing these processes occur on a temporal scale (2, 3, 4). Similarities in the processes occurring at the growth plate and at the fracture site permit some knowledge from growthplate analysis to comprehend events in fracture healing. Fracture healing involves a series of distinct cellular responses. Specific paracrine and autocrine intercellular signaling pathways control cellular and osseous tissue mineralization (Fig. 1). However, extrapolation of knowledge of growth-plate molecular dynamics is insufficient to achieve consistently optimal bone regeneration during primary and secondary fracture healing.

Keywords

Migration Mold Osteoarthritis Doxorubicin Sponge 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Furner, S. E. and Kozak, L. J. (1993) Health data on older Americans: United States, 1992. Acute care. Vital Health Stat 3, 115–142.Google Scholar
  2. 2.
    Böstrom, M. P. (1998) Expression of bone mrophogenetic proteins in fracture healing. Clin. Orthop. Rel. Res. 355S, S116–S123.Google Scholar
  3. 3.
    Johari, A. N. and Sinha, M. (1999) Remodeling of forearm fractures in children. J. Pediatr. Orthop. B 8(2), 84–87.PubMedGoogle Scholar
  4. 4.
    Ekholm, E. C., Ravanti, L., Kahari, V., Paavolainen, P., and Penttinen, R. P. (2000) Expression of extracellular matrix genes: transforming growth factor (TGF)-beta1 and ras in tibial fracture healing of lathyritic rats. Bone 27(4), 551–557.PubMedGoogle Scholar
  5. 5.
    Kusuzaki, K., Kageyama, N., Shinjo, H., et al. (2000) Development of bone canaliculi during bone repair. Bone 27(5), 655–659.PubMedGoogle Scholar
  6. 6.
    Bebchuk, T. N., Degner, D. A., Walshaw, R., et al. (2000) Evaluation of a free vascularized medial tibial bone graft in dogs. Vet. Surg. 29(2), 128–144.PubMedGoogle Scholar
  7. 7.
    McKibbin, B. (1978) The biology of fracure healing in long bones. J. Bone Joint Surg. 60B(2), 150–162.Google Scholar
  8. 8.
    Kleinschmidt, J. and Hollinger, J. O. (1992) Animal models in bone research, in Bone Grafts and Bone Substitutes (Habal, M. and Reddi, A. H., eds.), Saunders, Philadelphia, pp. 133–147.Google Scholar
  9. 9.
    Weinzweig, J., Pantaloni, M., Spangenberger, A., Marler, J., and Zienowicz, R. J. (2000) Osteochondral reconstruction of a non-weight-bearing joint using a high-density porous polyethylene implant. Plast. Reconstr. Surg. 106(7), 1547–1554.PubMedGoogle Scholar
  10. 10.
    Craft, P. D. and Sargent, L. A. (1989) Membranous bone healing and techniques in calvarial bone grafting. Clin. Plast. Surg. 16(1), 11–19.PubMedGoogle Scholar
  11. 11.
    Verdi, G. D. and Alpert, B. (1986) Bone grafts in orthognathic and craniofacial surgery. Ear Nose Throat J. 65(11), 506–511.PubMedGoogle Scholar
  12. 12.
    Reddi, A. H. (1998) Initiation of fracture repair by bone morphogenetic proteins. Clin. Orthop. Rel. Res. 355S, S66–S72.Google Scholar
  13. 13.
    Burgess, E. A., Mayer, M. H., and Hollinger, J. O.(2000) Bone grafting and substitutes, in Plastic Surgery: Indications Operations Outcomes (Coleman, J. J., Vander Kolk, C. A., and Achauer, B. M., eds.), Mosby-Year Book, Philadelphia, in press.Google Scholar
  14. 14.
    Adami, R. C., Collard, W. T., Gupta, S. A., Kwok, K. Y., Bonadio, J., and Rice, K. G. (1998) Stability of peptidecondensed plasmid DNA formulations. J. Pharm. Sci. 87, 678–683.PubMedGoogle Scholar
  15. 15.
    Bonadio, J., Smiley, E., Patil, P., and Goldstein, S. (1999) Localized, direct plasmid gene therapy in vivo: prolonged therapy results in reproducible tissue regeneration. Nat. Med. 5(7), 753–759.PubMedGoogle Scholar
  16. 16.
    Perry, C. (1999) Bone repair techniques, bone graft, and bone graft substitutes. Clin. Orthop. Rel. Res. 360, 71–86.Google Scholar
  17. 17.
    Baltzer, A., Lattermann, C., Whalen, J., et al. (2000) Potential role of direct adenoviral gene transfer in enhancing fracture repair. Clin. Orthop. Rel. Res. S379(3), S120–S125.Google Scholar
  18. 18.
    Chow, K. M. and Rabie, A. B. (2000) Vascular endothelial growth pattern of endochondral bone graft in the presence of demineralized intramembranous bone matrix—quantitative analysis. Cleft Palate Craniofac. J. 37(4), 385–394.PubMedGoogle Scholar
  19. 19.
    Ahn, D. K., Sims, C. D., Randolph, M. A., et al. (1997) Craniofacial skeletal fixation using biodegradable plates and cyanoacrylate glue. Plast. Reconstr. Surg. 99(6), 1508–1515; discussion 16-17.PubMedGoogle Scholar
  20. 20.
    Bensinger, W. I., Maloney, D., and Storb, R. (2001) Allogeneic hematopoietic cell transplantation for multiple myeloma. Semin. Hematol. 38(3), 243–249.PubMedGoogle Scholar
  21. 21.
    Einhorn, T. A. (1998) The cell and molecular biology of fracture healing. Clin. Orthop. 355(Suppl), S7–S21.PubMedGoogle Scholar
  22. 22.
    Clark, R. A. F. (1996) The Molecular and Cellular Biology of Wound Repair. 22nd ed. Plenum, New York.Google Scholar
  23. 23.
    Bolander, M. E. (1992) Regulation of fracture repair by growth factors. Proc. Soc. Exp. Biol. Med. 200, 165–170.PubMedGoogle Scholar
  24. 24.
    Macias, M. P., Fitzpatrick, L. A., Brenneise, I., McGarry, M. P., Lee, J. J., and Lee, N. A. (2001) Expression of IL-5 alters bone metabolism and induces ossification of the spleen in transgenic mice. J. Clin. Invest. 107(8), 949–959.PubMedGoogle Scholar
  25. 25.
    Hollinger, J. O., Buck, D. C., and Bruder, S. (1998) Biology of bone healing: its impact on clinical therapy, in Tissue Engineering: Applications in Maxillofacial Surgery and Periodontics (Lynch, S., Marx, R., and Genco, R., eds.), Quintessence, San Diego, pp. 17–53.Google Scholar
  26. 26.
    Le, A. X., Miclau, T., Hu, D., and Helms, J. A. (2001) Molecular aspects of healing in stabilized and non-stabilized fractures. J. Orthop. Res. 19(1), 78–84.PubMedGoogle Scholar
  27. 27.
    Alhopuro, S. (1978) Premature fusion of facial sutures with free periosteal grafts. An experimental study with special reference to bone formation with free periosteal grafts from the tibia, the scapula and the calvarium. Scand. J. Plast. Reconstr. Surg. Suppl. 17, 1–68.PubMedGoogle Scholar
  28. 28.
    Jones, D., Leivseth, G., and Tenbosch, J. (1995) Mechano-reception in osteoblast-like cells. Biochem. Cell Biol. 73 (7-8), 525–534.PubMedGoogle Scholar
  29. 29.
    Harter, L. V., Hruska, K. A., and Duncan, R. L. (1995) Human osteoblast-like cells respond to mechanical strain with increased bone matrix protein production independent of hormonal regulation. Endocrinology 136(2), 528–535.PubMedGoogle Scholar
  30. 30.
    Schierle, H. P. and Hausamen, J. E. (1997) [Modern principles in treatment of complex injuries of the facial bones]. Unfallchirurg 100(5), 330–337.PubMedGoogle Scholar
  31. 31.
    Mathog, R. H., Toma, V., Clayman, L., and Wolf, S. (2000) Nonunion of the mandible: an analysis of contributing factors. J. Oral Maxillofac. Surg. 58(7), 746–752; discussion 52-53.PubMedGoogle Scholar
  32. 32.
    Caplanis, N., Lee, M. B., Zimmerman, G. J., Selvig, K. A., and Wikesjo, U. M. (1998) Effect of allogeneic freezedried demineralized bone matrix on regeneration of alveolar bone and periodontal attachment in dogs. J. Clin. Periodontol. 25(10), 801–806.PubMedGoogle Scholar
  33. 33.
    Brighton, C. T. and Hunt, R. M. (1986) Histochemical localization of calcium in the fracture callus with potassium pyroantimonate. Possible role of chondrocyte mitochondrial calcium in callus calcification. J. Bone Joint Surg. 68(5), 703–715.PubMedGoogle Scholar
  34. 34.
    Einhorn, T. (1995) Current concepts review. Enhancement of fracture healing. J. Bone Joint Surg. 77A(6), 940–956.Google Scholar
  35. 35.
    Yamazaki, M., Majeska, R. J., Yoshioka, H., Moriya, H., and Einhorn, T. A. (1997) Spatial and temporal expression of fibril-forming minor collagen genes (types V and XI) during fracture healing. J. Orthop. Res. 15(5), 757–764.PubMedGoogle Scholar
  36. 36.
    Jingushi, S., Heydemann, A., Kana, S. K., Macey, L. R., and Bolander, M. E. (1990) Acidic fibroblast growth factor (aFGF) injection stimulates cartilage enlargement and inhibits cartilage gene expression in rat fracture healing. J. Orthop. Res. 8(3), 364–371.PubMedGoogle Scholar
  37. 37.
    Jingushi, S., Joyce, M. E., and Bolander, M. E. (1992) Genetic expression of extracellular matrix proteins correlates with histologic changes during fracture repair. J. Bone Miner. Res. 7(9), 1045–1055.PubMedGoogle Scholar
  38. 38.
    Hiltunen, A., Metsaranta, M., Perala, M., Saamanen, A. M., Aro, H. T., and Vuorio, E. (1995) Expression of type VI, IX and XI collagen genes and alternative splicing of type II collagen transcripts in fracture callus tissue in mice. FEBS Lett. 364(2), 171–174.PubMedGoogle Scholar
  39. 39.
    Hiltunen, A., Metsaranta, M., Virolainen, P., Aro, H. T., and Vuorio, E. (1994) Retarded chondrogenesis in transgenic mice with a type II collagen defect results in fracture healing abnormalities. Dev. Dyn. 200(4), 340–349.PubMedGoogle Scholar
  40. 40.
    Hiltunen, A., Aro, H. T., and Vuorio, E. (1993) Regulation of extracellular matrix genes during fracture healing in mice. Clin. Orthop. 297, 23–27.PubMedGoogle Scholar
  41. 41.
    Sugimoto, M., Hirota, S., Sato, M., et al. (1998) Impaired expression of noncollagenous bone matrix protein mRNAs during fracture healing in ascorbic acid-deficient rats. J. Bone Miner. Res. 13(2), 271–278.PubMedGoogle Scholar
  42. 42.
    Termine, J. D. (1990) Cellular activity, matrix proteins, and aging bone. Exp. Gerontol. 25, 217–221.PubMedGoogle Scholar
  43. 43.
    Chen, J. H., Wang, X. C., Kan, M., and Sato, J. D. (2001) Effect of FGF-1 and FGF-2 on VEGF binding to human umbilical vein endothelial cells. Cell Biol. Int. 25(3), 257–260.PubMedGoogle Scholar
  44. 44.
    Montero, A., Okada, Y., Tomita, M., et al. (2000) Disruption of the fibroblast growth factor-2 gene results in decreased bone mass and bone formation. J. Clin. Invest. 105(8), 1085–1093.PubMedGoogle Scholar
  45. 45.
    Hosokawa, R., Kikuzaki, K., Kimoto, T., et al. (2000) Controlled local application of basic fibroblast growth factor (FGF-2) accelerates the healing of GBR. An experimental study in beagle dogs. Clin. Oral Implants Res. 11(4), 345–353.PubMedGoogle Scholar
  46. 46.
    Fitzpatrick, L. A. and Bilezkian, J. P. (1996) Actions of parathyroid hormone, in Principles of Bone Biology (Bilezkian, J. P., Raisz, L. G., and Rodan, G. A., eds.), Academic, New York, pp. 339–346.Google Scholar
  47. 47.
    Hill, P. A., Tumber, A., and Meikle, M. C. (1997) Multiple extracellular signals promote osteoblast survival and apoptosis. Endocrinology 138(9), 3849–3858.PubMedGoogle Scholar
  48. 48.
    Rodan, G. (1998) Control of bone formation and resorption: biological and clinical perspective. J. Cell Biochem. Suppl. 30, 55–61.PubMedGoogle Scholar
  49. 49.
    Ahrens, M., Ankenbauer, T., Schröder, D., Hollnagel, A., Mayer, H., and Gross, G. (1993) Expression of human morphogenetic proteins-2 or-4 in murine mesenchymal progenitor C3H10T1/2 cells induces differentiation into distinct mesenchymal cell lineages. DNA Cell Biol. 12(10), 871–880.PubMedGoogle Scholar
  50. 50.
    Chan, Y. S., Ueng, S. W., Wang, C. J., Lee, S. S., Chao, E. K., and Shin, C. H. (1998) Management of small infected tibial defects with antibiotic-impregnated autogenic cancellous bone grafting. J. Trauma 45(4), 758–764.PubMedGoogle Scholar
  51. 51.
    Celeste, A. J., Song, J. J., Cox, K., Rosen, V., and Wozney, J. M. (1994) Bone morphogenetic protein-9, a new member of the TGF-beta superfamily. J. Bone Miner. Res. 9(1), S137.Google Scholar
  52. 52.
    Amedee, J., Bareille, R., Rouais, F., Cunningham, N., Reddi, N., and Hamand, M. F. (1994) Osteogenin (bone morphogenetic protein-3) inhibits proliferation and stimulates differentiation of osteoprogenitors in human bone marrow. Differentiation 58, 157–164.PubMedGoogle Scholar
  53. 53.
    Ikeda, T., Nagai, A., Yamaguchi, A., Yokose, S., and Yoshiki, S. (1995) Age-related reduction in bone matrix protein mRNA expression in rat bone tissues: application of histomorphometry to in situ hybridization. Bone 16(1), 17–23.PubMedGoogle Scholar
  54. 54.
    Asahina, I., Sampath, T. K., and Hauschka, P. V. (1996) Human osteogenic protein-1 induces chondroblastic, osteoblastic, and/or adipocytic differentiation. Exp. Cell Res. 222, 38–47.PubMedGoogle Scholar
  55. 55.
    Reissmann, E., Ernsberger, U., Francis-West, P. H., Rueger, D., Brickell, P. M., and Rohrer, H. (1996) Involvement of bone morphogenetic protein-4 and bone morphogenetic protein-7 in the differentiation of the adrenergic phenotype in developing sympathetic neurons. Development 122, 2079–2088.PubMedGoogle Scholar
  56. 56.
    Ducy, P. and Karsenty, G. (1998) Genetic control of cell differentiation in the skeleton. Curr. Opin. Cell Biol. 10, 614–619.PubMedGoogle Scholar
  57. 57.
    Uusitalo, H., Hiltunen, A., Ahonen, M., Kahari, V., Aro, H., and Vuorio, E. (2001) Induction of periosteal callus formation by bone morphogenetic protein-2 employing adenovirus-mediated gene delivery.Matrix Biol. 20(2), 123–127.PubMedGoogle Scholar
  58. 58.
    Derynck, R., Zhang, Y., and Feng, X. (1998) Smads: transcription activatros of TGF-beta responses. Cell 95, 737–740.PubMedGoogle Scholar
  59. 59.
    Barnes, G., Kostenuik, P., Geerstenfeld, L., and Einhorn, T. (1999) Growth factor regulation of fracture repair. J. Bone Miner. Res. 14(11), 1805–1815.PubMedGoogle Scholar
  60. 60.
    Hirano, T. (1999) Molecular basis underlying functional pleiotropy of cytokines and growth factors. Biochem. Biophys. Res. Commun. 260, 303–308.PubMedGoogle Scholar
  61. 61.
    Sakou, T., Onishi, T., Yamamoto, T., Nagamine, T., Sampath, K., and Ten Dijke, P. (1999) Localization of Smads, the TGF-beta family intracellular signaling components during endochondral ossification. J. Bone Miner. Res. 14(7), 1145–1152.PubMedGoogle Scholar
  62. 62.
    Schmitt, J. M., Hwang, K., Winn, S. R., and Hollinger, J. O. (1999) Bone morphogenetic proteins: an update on basic biology and clinical relevance. J. Orthop. Res. 17(2), 269–278.PubMedGoogle Scholar
  63. 63.
    Weinstein, M., Yang, X., and Deng, C. (2000) Functions of mammalian Smad genes as revealed by targeted gene disruption in mice. Cytokine Growth Factor Rev. 11(1-2), 49–58.PubMedGoogle Scholar
  64. 64.
    Yanagisawa, K., Uchida, K., Nagatake, M., et al. (2000) Heterogeneities in the biological and biochemical functions of Smad2 and Smad4 mutants naturally occurring in human lung cancers. Oncogene 19(19), 2305–2311.PubMedGoogle Scholar
  65. 65.
    Mont, M. A., Jones, L. C., Einhorn, T. A., Hungerford, D. S., and Reddi, A. H. (1998) Osteonecrosis of the femoral head. Potential treatment with growth and differentiation factors. Clin. Orthop. 355(Suppl),S314–S335.PubMedGoogle Scholar
  66. 66.
    Hay, E., Lemonnier, J., Fromigue, O., and Marie, P. J. (2001) Bone morphogenetic protein-2 promotes osteoblast apoptosis through a Smad-independent, protein kinase C-dependent signaling pathway. J. Biol. Chem. 276(31), 29028–29036.PubMedGoogle Scholar
  67. 67.
    Lee, K. S., Kim, H. J., Li, Q. L., et al. (2000) Runx2 is a common target of transforming growth factor beta1 and bone morphogenetic protein 2, and cooperation between Runx2 and Smad5 induces osteoblast-specific gene expression in the pluripotent mesenchymal precursor cell line C2C12. Mol. Cell Biol. 20(23), 8783–8792.PubMedGoogle Scholar
  68. 68.
    Zhang, Y. W., Yasui, N., Ito, K., et al. (2000) A RUNX2/PEBP2alpha A/CBFA1 mutation displaying impaired transactivation and Smad interaction in cleidocranial dysplasia. Proc. Natl. Acad. Sci. USA 97(19), 10549–10554.PubMedGoogle Scholar
  69. 69.
    Ducy, P., Zhang, R., Geoffroy, V., Ridall, A., and Karsenty, G. (1997) Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89, 747–754.PubMedGoogle Scholar
  70. 70.
    Simonet, W., Lacey, D., Dunstan, C., et al. (1997) Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell 89, 309–319.PubMedGoogle Scholar
  71. 71.
    Itonaga, I., Sabokbar, A., Murray, D. W., and Athanasou, N. A. (2000) Effect of osteoprotegerin and osteoprotegerin ligand on osteoclast formation by arthroplasty membrane derived macrophages. Ann. Rheum. Dis. 59(1), 26–31.PubMedGoogle Scholar
  72. 72.
    Mentaverri, R., Lorget, F., Wattel, A., Maamer, M., Kamel, S., and Brazier, M. (2000) [Osteoblastic regulation of osteoclast survival: effect of calcitriol]. C. R. Acad. Sci. III 323(11), 951–957.PubMedGoogle Scholar
  73. 73.
    Mayer, M. H. (1994) Clinical perspectives on bone grafting: avoiding the complications of developmental malformations, in Bone Repair and Regeneration (Seyfer, A. and Hollinger, J., eds.), Saunders, Philadelphia, pp. 365–376.Google Scholar
  74. 74.
    Hollinger, J. O., Mayer, M., Buck, D., et al. (1996) Poly(alpha-hydroxy acid) carrier for delivering recombinant human bone morphogenetic protein-2 for bone regeneration. J. Controlled Rel. 39, 287–304.Google Scholar
  75. 75.
    Hanamura, H., Higuchi, Y., Nakagawa, M., Iwata, H., Nogami, H., and Urist, M. R. (1980) Solubilized bone morphogenetic protein (BMP) from mouse osteosarcoma and rat demineralized bone matrix. Clin. Orthop. Rel. Res. 148, 281–290.Google Scholar
  76. 76.
    Goldberg, V. M. and Stevenson, S. (1987) Natural history of autografts and allografts. Clin. Orthop. Rel. Res. 225, 7–16.Google Scholar
  77. 77.
    Stevenson, S. (1998) Enhancement of fracture healing with autogenous and allogeneic bone grafts. Clin. Orthop. Rel. Res. 355S, S239–S246.Google Scholar
  78. 78.
    Nishibori, M., Betts, N. J., Salama, H., and Listgarten, M. A. (1994) Short-term healing of autogenous and allogeneic bone grafts after sinus augmentation: a report of 2 cases. J. Periodontol. 65(10), 958–966.PubMedGoogle Scholar
  79. 79.
    Chanavaz, M. (2000) Sinus graft procedures and implant dentistry: a review of 21 years of surgical experience (1979-2000). Implant Dent. 9(3), 197–206.PubMedGoogle Scholar
  80. 80.
    Hanisch, O., Lozada, J. L., Holmes, R. E., Calhoun, C. J., Kan, J. Y., and Spiekermann, H. (1999) Maxillary sinus augmentation prior to placement of endosseous implants: a histomorphometric analysis. Int. J. Oral Maxillofac. Implants 14(3), 329–336.PubMedGoogle Scholar
  81. 81.
    Kassolis, J. D., Rosen, P. S., and Reynolds, M. A. (2000) Alveolar ridge and sinus augmentation utilizing plateletrich plasma in combination with freeze-dried bone allograft: case series. J. Periodontol. 71(10), 1654–1661.PubMedGoogle Scholar
  82. 82.
    Lozada, J. L., Caplanis, N., Proussaefs, P., Willardsen, J., and Kammeyer, G. (2001) Platelet-rich plasma application in sinus graft surgery: Part I-Background and processing techniques. J. Oral Implantol. 27(1), 38–42.PubMedGoogle Scholar
  83. 83.
    van den Bergh, J. P., ten Bruggenkate, C. M., Groeneveld, H. H., Burger, E. H., and Tuinzing, D. B. (2000) Recombinant human bone morphogenetic protein-7 in maxillary sinus floor elevation surgery in 3 patients compared to autogenous bone grafts. A clinical pilot study. J. Clin. Periodontol. 27(9), 627–636.PubMedGoogle Scholar
  84. 84.
    Krauser, J. T., Rohrer, M. D., and Wallace, S. S. (2000) Human histologic and histomorphometric analysis comparing OsteoGraf/N with PepGen P-15 in the maxillary sinus elevation procedure: a case report. Implant Dent. 9(4), 298–302.PubMedGoogle Scholar
  85. 85.
    Ueda, M., Tohnai, I., and Nakai, H. (2001) Tissue engineering research in oral implant surgery. Artif. Organs 25(3), 164–171.PubMedGoogle Scholar
  86. 86.
    Costantino, P. D., Friedman, C. D., Shindo, M. L., Houston, G., and Sisson, G. A., Sr. (1993) Experimental mandibular regrowth by distraction osteogenesis. Long-term results. Arch. Otolaryngol. Head Neck Surg. 119(5), 511–516.PubMedGoogle Scholar
  87. 87.
    Wiltfang, J., Kessler, P., Merten, H. A., and Neukam, F. W. (2001) Continuous and intermittent bone distraction using a microhydraulic cylinder: an experimental study in minipigs. Br. J. Oral Maxillofac. Surg. 39(1), 2–7.PubMedGoogle Scholar
  88. 88.
    Vu, T., Shipley, J., Bergers, G., et al. (1998) MMP-9/gelatinase B is a key regulator of growth plates angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93, 411–422.PubMedGoogle Scholar
  89. 89.
    Al Ruhaimi, K. A. (2001) Bone graft substitutes: a comparative qualitative histologic review of current osteoconductive grafting materials. Int. J. Oral Maxillofac. Implants 16(1), 105–114.PubMedGoogle Scholar
  90. 90.
    Jorgensen, C., Noel, D., Apparailly, F., and Sany, J. (2001) Stem cells for repair of cartilage and bone: the next challenge in osteoarthritis and rheumatoid arthritis. Ann. Rheum. Dis. 60(4), 305–309.PubMedGoogle Scholar
  91. 91.
    Rozema, F. R., Bos, R. R., Pennings, A. J., and Jansen, H. W. (1990) Poly(L-lactide) implants in repair of defects of the orbital floor: an animal study. J. Oral Maxillofac. Surg. 48(12), 1305–1309; 1310.PubMedGoogle Scholar
  92. 92.
    Maves, M. D. and Matt, B. H. (1986) Calvarial bone grafting of facial defects. Otolaryngol. Head Neck Surg. 95(4), 464–470.PubMedGoogle Scholar
  93. 93.
    Copeland, M. and Meisner, J. (1991) Maxillary antral bone grafts for repair of orbital fractures. J. Craniofac. Surg. 2(1), 18–21.PubMedGoogle Scholar
  94. 94.
    Iatrou, I., Theologie-Lygidakis, N., and Angelopoulos, A. (2001) Use of membrane and bone grafts in the reconstruction of orbital fractures. Oral Surg. Oral Med. Oral. Pathol. Oral Radiol. Endodont. 91(3), 281–286.Google Scholar
  95. 95.
    Ascherman, J. A., Marin, V. P., Rogers, L., and Prisant, N. (2000) Palatal distraction in a canine cleft palate model. Plast. Reconstr. Surg. 105(5), 1687–1694.PubMedGoogle Scholar
  96. 96.
    Yukna, R. A. and Yukna, C. N. (1997) Six-year clinical evaluation of HTR synthetic bone grafts in human grade II molar furcations. J. Periodontal. Res. 32(8), 627–633.PubMedGoogle Scholar
  97. 97.
    Yukna, R. A. (1994) Clinical evaluation of HTR polymer bone replacement grafts in human mandibular Class II molar furcations. J. Periodontol. 65(4), 342–349.PubMedGoogle Scholar
  98. 98.
    Trombelli, L., Lee, M. B., Promsudthi, A., Guglielmoni, P. G., and Wikesjo, U. M. (1999) Periodontal repair in dogs: histologic observations of guided tissue regeneration with a prostaglandin E1 analog/methacrylate composite. J. Clin. Periodontol. 26(6), 381–387.PubMedGoogle Scholar
  99. 99.
    Eickholz, P., Kim, T. S., Holle, R., and Hausmann, E. (2001) Long-term results of guided tissue regeneration therapy with non-resorbable and bioabsorbable barriers. I. Class II furcations. J. Periodontol. 72(1), 35–42.PubMedGoogle Scholar
  100. 100.
    Urist, M. R. and Strates, B. S. (1971) Bone morphogenetic protein. J. Dent. Res. 50, 1392–1406.PubMedGoogle Scholar
  101. 101.
    Carrington, J. L., Roberts, A. B., Flanders, K. C., Roche, N. S., and Reddi, A. H.(1988) Accumulation, localization, and compartmentation of transforming growth factor ² during endochondral bone development. J. Cell Biol. 107, 1969–1975.PubMedGoogle Scholar
  102. 102.
    Schmitz, J. P., Hollinger, J. O., and Milam, S. B. (1999) Reconstruction of bone using calcium phosphate bone cements: a critical review. J. Oral Maxillofac. Surg. 57, 1122–1126.PubMedGoogle Scholar
  103. 103.
    Burgess, E. A. and Hollinger, J. O. (1999) Options for engineering bone, in Frontiers in Tissue Engineering (Patrick, C. W., ed.), Elsevier, pp. 383–399.Google Scholar
  104. 104.
    Tsuruga, E., Takita, H., Itoh, H., Wakisaka, Y., and Kuboki, Y. (1997) Pore size of porous hydroxyapatite as the cellsubstratum controls BMP-induced osteogenesis. J. Biochem. 121(2), 317–324.PubMedGoogle Scholar
  105. 105.
    Chow, L., Takagi, S., Constantino, P. D., and Friedman, C. D. (1991) Self-setting calcium phosphate cements. Mater. Res. Soc. Symp. Proc. 179, 3–24.Google Scholar
  106. 106.
    Knaack, D., Goad, M. E., Aiolova, M., et al. (1998) Resorbable calcium phosphate bone substitute. J. Biomed. Mater. Res. 43(4), 399–409.PubMedGoogle Scholar
  107. 107.
    Baltzer, A. W., Lattermann, C., Whalen, J. D., Braunstein, S., Robbins, P. D., and Evans, C. H. (1999) A gene therapy approach to accelerating bone healing. Evaluation of gene expression in a New Zealand white rabbit model. Knee Surg. Sports Traumatol. Arthrosc. 7(3), 197–202.PubMedGoogle Scholar
  108. 108.
    Syftestad, G. T., Triffit, J. T., Urist, M. R., and Caplan, A. I. (1984) An osteo-inductive bone matrix extract stimulates the in vitro conversion of mesenchyme into chondrocytes. Calcif. Tissue Int. 36, 625–627.PubMedGoogle Scholar
  109. 109.
    Sampath, T. K., Muthukumaran, N., and Reddi, A. H. (1987) Isolation of osteogenin, an extracellular matrix-associated bone-inductive protein, by heparin affinity chromatography. Proc. Natl. Acad. Sci. USA 84, 7109–7113.PubMedGoogle Scholar
  110. 110.
    Hollinger, J. O. (1997) What’s new in bone biology? J. Histotech. 20(3), 235–240.Google Scholar
  111. 111.
    Boden, S. D. Hair, G. A., Viggeswarapu, M., Liu, Y., and Titus, L. (2000) Gene therapy for spine fusion. Clin. Orthop. 379(Suppl), S225–S233.PubMedGoogle Scholar
  112. 112.
    Lee, Y. M., Seol, Y. J., Lim, Y. T., et al. (2001) Tissue-engineered growth of bone by marrow cell transplantation using porous calcium metaphosphate matrices. J. Biomed. Mater. Res. 54(2), 216–223.PubMedGoogle Scholar
  113. 113.
    Sandhu, H. and Boden, S. (1998) Biologic enhancement of spine fusion. Orthop. Clin. N. Am. 29(4), 621–631.Google Scholar
  114. 114.
    Boden, S. (2000) Biology of lumbar spine fusion and use of bone graft substitutes: present, future, and next generation. Tissue Eng. 6(4), 383–400.PubMedGoogle Scholar
  115. 115.
    Boyne, P. J., Marx, R. E., Nevins, M., et al. (1997) A feasibility study on evaluation rhBMP-2/absorbable collagen sponge for maxillary sinus augmentation. Int. J. Periodont. Restor. Dent. 17(1), 11–25.Google Scholar
  116. 116.
    Howell, T. H., Fiorellini, J., Jones, A., et al. (1997) A feasibility study evaluating rhBMP-2/absorbable collagen sponge device for local alveolar ridge preservation of augmentation. Int. J. Periodont. Restor. Dent. 17(2), 125–139.Google Scholar
  117. 117.
    Riedel, G. E. and Valentin-Opran, A. (1999) Clinical evaluation of rhBMP-2/ACS in orthopedic trauma: a progress report. Orthopedics 22(7), 663–665.PubMedGoogle Scholar
  118. 118.
    Rodan, S. B. and Rodan, G. A. (1992) Fibroblast growth factor and platelet derived growth factor, in Cytokines and Bone and Metabolism (Gowan, M., ed.), CRC Press, Boca Raton, FL, pp. 116–140.Google Scholar
  119. 119.
    Dunstan, C. R., Boyce, B. F., Boyce, R., et al. (1999) Systemic administration of acidic fibroblast growth factor (FGF-1) prevents bone loss and increases new bone formation in ovariectomized rats. J. Bone Miner. Res. 14, 953–959.PubMedGoogle Scholar
  120. 120.
    Martin, P. (1997) Wound healing-aiming for the perfect skin. Science 276, 75–81.PubMedGoogle Scholar
  121. 121.
    Nakamura, T., Hanada, K., Tamura, M., et al. (1995) Stimulation of endosteal bone formation by systemic injection of recombinant basic fibroblastic growth factor in rats. Endocrinology 136(3), 1276–1284.PubMedGoogle Scholar
  122. 122.
    Nakamura, K., Kawaguchi, H., Aoyama, I., et al. (1997) Stimulation of bone formation by intraosseous application of recombinant basic fibroblast growth factor in normal and ovariectomized rabbits. J. Bone Joint Surg. 15, 307–313.Google Scholar
  123. 123.
    Kato, T., Kawaguchi, H., Hanada, K., et al. (1998) Single local injection of recombinant fibroblast growth factor-2 stimulates healing of segmental bone defects in rabbits. J. Orthop. Res. 16, 654–659.PubMedGoogle Scholar
  124. 124.
    Nakamura, T., Hara, Y., Tagawa, M., et al. (1998) Recombinant human fibroblast growth factor accelerates fracture healing by enhancing callus remodeling in experimental dog tibial fracture. J. Bone Miner. Res. 13(6), 942–949.PubMedGoogle Scholar
  125. 125.
    Debiais, F., Hott, M., Graulet, A. M., and Marie, P. J. (1998) The effects of fibroblast growth factor-2 on human neonatal calvaria osteoblastic cells are differentiation stage specific. J. Bone Miner. Res. 13(4), 645–654.PubMedGoogle Scholar
  126. 126.
    Eppley, B. L., Delfino, J. J., Connolly, D. T., and Feder, J. (1988) Angiogenic enhancement in bone graft healing by basic fibroblast growth factor. Clin. Res. 36, A851.Google Scholar
  127. 127.
    Lu, S., Zhang, Z., and Wang, J. (1996) Guided bone regeneration in long bone. An experimental study. Chin. Med. J. (Engl.) 109(7), 551–554.Google Scholar
  128. 128.
    Wang, J. and Aspenberg, P. (1996) Basic fibroblast growth factor enhances bone-graft incorporation: dose and time dependence in rats. J. Orthop. Res. 34, 316–323.Google Scholar
  129. 129.
    Ducy, P., Schinke, T., and Karsenty, G. (2000) The osteoblast: a sophisticated fibroblast under central surveillance. Science 289, 1501–1504.PubMedGoogle Scholar
  130. 130.
    Harada, H., Tagashira, S., Fujiwara, M, et al. (1999) Cbfa1 isoforms exert functional differences in osteoblast differentiation. J. Biol. Chem. 274(11), 6972–6978.PubMedGoogle Scholar
  131. 131.
    Komori, T. and Ksihimoto, T. (1998) Cbfa1 in bone development. Curr. Opin. Genes Dev. 8, 494–499.Google Scholar
  132. 132.
    Yamaguchi, A., Komori, T., and Suda, T. (2000) Regulation of osteoblast differentiation mediated by bone morphogenetic proteins, hedgehogs, and Cbfa1. Endocr. Rev. 21(4), 393–411.PubMedGoogle Scholar
  133. 133.
    Fujimura, K., Bessho, K., Kusumoto, K., Konishi, Y., Ogawa, Y., and Iizuka, T. (2001) Experimental osteoinduction by recombinant human bone morphogenetic protein 2 in tissue with low blood flow: a study in rats. Br. J. Oral Maxillofac. Surg. 39(4), 294–300.PubMedGoogle Scholar
  134. 134.
    Linkhart, T. A., Mohan, S., and Baylink, D. J. (1996) Growth factors for bone growth and repair: IGF, TGF beta, and BMP. Bone 19(1), 1–12.Google Scholar
  135. 135.
    Becker, W., Urist, M., Becker, B. E., et al. (1996) Clinical and histologic observations of sites implanted with intraoral autologous bone grafts or allografts. 15 human case reports. J. Periodontol. 67(10), 1025–1033.PubMedGoogle Scholar
  136. 136.
    Gao, T. J., Lindholm, T. S., Kommonen, B., et al. (1997) The use of a coral composite implant containing bone morphogenetic protein to repair a segmental tibial defect in sheep. Int. Orthop. 21(3), 194–200.PubMedGoogle Scholar
  137. 137.
    Viljanen, V. V. and Lindholm, T. S. (1997) The search for new members of the BMP/TGF-beta family, in Skeletal Reconstruction and Bioimplantation: Demineralized Bone Matrix, Non-collagenous, Native, and Recombinant Bone Morphogenetic Proteins (Lindholm, T. S., ed.), Academic Press, New York, pp. 241–248.Google Scholar
  138. 138.
    Riedel, G. E. and Valentin-Opran, A. (1999) Preliminary report: new technology. Clinical evaluation of rhBMP-2/ACS in orthopedic trauma: a progress report. Orthopedics 22(7), 663–665.PubMedGoogle Scholar
  139. 139.
    Welch, R. D., Jones, A. L., Bucholz, R. W., et al. (1998) Effect of recombinant human bone morphogenetic protein-2 on fracture healing in a goat tibial fracture model. J. Bone Miner. Res. 13(9), 1483–1490.PubMedGoogle Scholar
  140. 140.
    Kingsley, D. (1994) What do BMPs do in mammals? Clues from the mouse short-ear mutation. Trends Genet. 10(1), 16–21.PubMedGoogle Scholar
  141. 141.
    Storm, E. E., Huynh, T. V., Copeland, N. G., Jenkins, N. A., Kingsley, D. M., and Lee, S. (1994) Limb alterations in brachypodism mice due to mutations in a new member of the TGF-beta superfamily. Nature 368, 639–643.PubMedGoogle Scholar
  142. 142.
    Francis, P. H., Richardson, M. K., Brickell, P. M., and Tickle, C. (1994) Bone morphogenetic proteins and a signaling pathway that controls patterning in the developing chick limb. Development 120, 209–218.PubMedGoogle Scholar
  143. 143.
    Kingsley, D. M. (1995) Genes that define the number and shape of bones in the mouse skeleton, in Portland Bone Symposium (Hollinger, J. O. and Seyfer, A. E., eds.), Portland, OR, pp. 505–516.Google Scholar
  144. 144.
    Song, J. J., Celeste, A., Kong, F. M., Jirtle, R. L., Rosen, V., and Thies, R. S. (1995) Bone morphogenetic protein-9 binds to liver cells and stimulates proliferation. Endocrinology 136(10), 4293–4297.PubMedGoogle Scholar
  145. 145.
    Tomizawa, K., Matsui, H., Kondo, E., et al. (1995) Developmental alteration and neuron-specific expression of bone morphogenetic protein-6 (BMP-6) mRNA in rodent brain. Molec. Brain Res. 28, 122–128.PubMedGoogle Scholar
  146. 146.
    Chang, S. C., Hoang, B., Thomas, J. T., et al. (1994) Cartilage-derived morphogenetic proteins. J. Biol. Chem. 269, 28227–28234.PubMedGoogle Scholar
  147. 147.
    Lindholm, T. S. (1996) Bone Morphogenetic Proteins: Biology, Biochemistry and Reconstructive Surgery. Academic Press, San Diego, CA.Google Scholar
  148. 148.
    Basic, N., Basic, V., Bulic, K., et al. (1996) TGF-beta and basement membrane matrigel stimulate the chondrogenic phenotype in osteoblast cells derived from fetal rat calvaria. J. Bone Miner. Res. 11(3), 384–391.PubMedGoogle Scholar
  149. 149.
    Brunet, L., McMahon, J., McMahon, A., and Harland, R. (1998) Noggin, cartilage morphogenesis, and joint formation in the mammalian skeleton. Science 280, 1455–1457.PubMedGoogle Scholar
  150. 150.
    Fonseca, M., Storm, G., Hennik, W., Gerritsen, W., and Haisma, H. (1999) Cationic polymeric gene delivery of betaglucouronidase for doxorubicin pro-drug therapy. J. Genet. Med. 1(6), 407–414.Google Scholar
  151. 151.
    Mundlos, S., Engel, H., Michel-Behnke, I., and Zabel, B. (1990) Distribution of type I and type II collagen gene expression during the development of human long bones. Bone 11, 275–279.PubMedGoogle Scholar
  152. 152.
    Rodan, G. (1991) Perspectives: mechanical loading, estrogen deficiency, and the coupling of bone formation to bone resorption. J. Bone Miner. Res. 6, 527–530.PubMedGoogle Scholar
  153. 153.
    Kenley, R., Marden, L., Turek, T., Jin, L., Ron, E., and Hollinger, J. (1994) Osseous regeneration in the rat calvarium using novel delivery systems for recombinant human bone morphogenetic protein-2 (rhBMP-2). J. Biomed. Mater. Res. 28(10), 1139–1147.PubMedGoogle Scholar
  154. 154.
    Bostrom, M., Lane, J., Tomin, E., et al. (1996) Use of bone morphogenetic protein-2 in the rabbit ulnar nonunion model. Clin. Orthop. Rel. Res. 327, 272–282.Google Scholar
  155. 155.
    Zegzula, H. D., Buck, D., Brekke, J., Wozney, J., and Hollinger, J. O. (1997) Bone formation with use of rhBMP-2 (recombinant human bone morphogenetic protein-2). J. Bone Joint Surg. 79A(12), 1778–1790.Google Scholar
  156. 156.
    Geesink, R. G., Hoefnagels, N. H., and Bulstra, S. K. (1999) Osteogenic activity of OP-1 bone morphogenetic protein (BMP-7) in a human fibular defect. J. Bone Joint Surg. 81B(4), 710–718.Google Scholar
  157. 157.
    Hollinger, J. O., Joh, S. P., Suh, K. W., Buck, D. C., Schmitt, J., and Zegzula, H. D. (1998) Regenerating the radius in a rabbit CSD model with recombinant human bone morphogenetic protein-2 and a collagen carrier. J. Appl. Biomater. 43, 356–364.Google Scholar
  158. 158.
    Gazzerro, E., Gangji, V., and Canalis, E. (1998) Bone morphogenetic proteins induce the expression of noggin, which limits their activity in cultured rat osteoblasts. J. Clin. Invest. 102(12), 2106–2114.PubMedGoogle Scholar
  159. 159.
    Tarnow, D. P., Wallace, S. S., Froum, S. J., Rohrer, M. D., and Cho, S. C. (2000) Histologic and clinical comparison of bilateral sinus floor elevations with and without barrier membrane placement in 12 patients: Part 3 of an ongoing prospective study. Int. J. Periodontics Restorative Dent. 20, 117–125.PubMedGoogle Scholar

Copyright information

© Humana Press Inc., Totowa, NJ 2005

Authors and Affiliations

  • Bruce A. Doll
    • 1
  • Charles Sfeir
    • 2
  • Kodi Azari
    • 3
  • Sarah Holland
    • 3
  • Jeffrey O. Hollinger
    • 4
  1. 1.Department of PeriodonticsUniversity of Pittsburgh School of Dental MedicinePittsburgh
  2. 2.University of Pittsburgh School of Dental Medicine, and Bone Tissue Engineering CenterCarnegie Mellon UniversityPittsburgh
  3. 3.University of Pittsburgh School of MedicinePittsburgh
  4. 4.Bone Tissue Engineering Center, Departments of Biomedical Engineering and Biological SciencesCarnegie Mellon UniversityPittsburgh

Personalised recommendations