Skip to main content
Top
Published in: Clinical Orthopaedics and Related Research® 8/2008

01-08-2008 | Symposium: New Approaches to Allograft Transplantation

A Perspective: Engineering Periosteum for Structural Bone Graft Healing

Authors: Xinping Zhang, PhD, Hani A. Awad, PhD, Regis J. O’Keefe, MD, PhD, Robert E. Guldberg, PhD, Edward M. Schwarz, PhD

Published in: Clinical Orthopaedics and Related Research® | Issue 8/2008

Login to get access

Abstract

Autograft is superior to both allograft and synthetic bone graft in repair of large structural bone defect largely due to the presence of multipotent mesenchymal stem cells in periosteum. Recent studies have provided further evidence that activation, expansion and differentiation of the donor periosteal progenitor cells are essential for the initiation of osteogenesis and angiogenesis of donor bone graft healing. The formation of donor cell-derived periosteal callus enables efficient host-dependent graft repair and remodeling at the later stage of healing. Removal of periosteum from bone autograft markedly impairs healing whereas engraftment of multipotent mesenchymal stem cells on bone allograft improves healing and graft incorporation. These studies provide rationale for fabrication of a biomimetic periosteum substitute that could fit bone of any size and shape for enhanced allograft healing and repair. The success of such an approach will depend on further understanding of the molecular signals that control inflammation, cellular recruitment as well as mesenchymal stem cell differentiation and expansion during the early phase of the repair process. It will also depend on multidisciplinary collaborations between biologists, material scientists and bioengineers to address issues of material selection and modification, biological and biomechanical parameters for functional evaluation of bone allograft healing.
Literature
1.
go back to reference Abe Y, Takahata M, Ito M, Irie K, Abumi K, Minami A. Enhancement of graft bone healing by intermittent administration of human parathyroid hormone (1–34) in a rat spinal arthrodesis model. Bone. 2007;41:775–785.PubMed Abe Y, Takahata M, Ito M, Irie K, Abumi K, Minami A. Enhancement of graft bone healing by intermittent administration of human parathyroid hormone (1–34) in a rat spinal arthrodesis model. Bone. 2007;41:775–785.PubMed
2.
go back to reference Allen MR, Hock JM, Burr DB. Periosteum: biology, regulation, and response to osteoporosis therapies. Bone. 2004; 35:1003–1012.PubMed Allen MR, Hock JM, Burr DB. Periosteum: biology, regulation, and response to osteoporosis therapies. Bone. 2004; 35:1003–1012.PubMed
3.
go back to reference Andreassen TT, Ejersted C, Oxlund H. Intermittent parathyroid hormone (1–34) treatment increases callus formation and mechanical strength of healing rat fractures. J Bone Miner Res. 1999;14:960–968.PubMed Andreassen TT, Ejersted C, Oxlund H. Intermittent parathyroid hormone (1–34) treatment increases callus formation and mechanical strength of healing rat fractures. J Bone Miner Res. 1999;14:960–968.PubMed
4.
go back to reference Ashammakhi N, Ndreu A, Piras A, Nikkola L, Sindelar T, Ylikauppila H, Harlin A, Chiellini E, Hasirci V, Redl H. Biodegradable nanomats produced by electrospinning: expanding multifunctionality and potential for tissue engineering. J Nanosci Nanotechnol. 2006;6:2693–2711.PubMed Ashammakhi N, Ndreu A, Piras A, Nikkola L, Sindelar T, Ylikauppila H, Harlin A, Chiellini E, Hasirci V, Redl H. Biodegradable nanomats produced by electrospinning: expanding multifunctionality and potential for tissue engineering. J Nanosci Nanotechnol. 2006;6:2693–2711.PubMed
5.
go back to reference Augustin G, Antabak A, Davila S. The periosteum Part 1: Anatomy, histology and molecular biology. Injury. 2007;38:1115–1130.PubMed Augustin G, Antabak A, Davila S. The periosteum Part 1: Anatomy, histology and molecular biology. Injury. 2007;38:1115–1130.PubMed
6.
go back to reference Bauer TW, Muschler GF. Bone graft materials. An overview of the basic science. Clin Orthop Relat Res. 2000;371:10–27.PubMed Bauer TW, Muschler GF. Bone graft materials. An overview of the basic science. Clin Orthop Relat Res. 2000;371:10–27.PubMed
7.
go back to reference Beachy PA, Karhadkar SS, Berman DM. Tissue repair and stem cell renewal in carcinogenesis. Nature. 2004;432:324–331.PubMed Beachy PA, Karhadkar SS, Berman DM. Tissue repair and stem cell renewal in carcinogenesis. Nature. 2004;432:324–331.PubMed
8.
go back to reference Berrey BH Jr, Lord CF, Gebhardt MC, Mankin HJ. Fractures of allografts. Frequency, treatment, and end-results. J Bone Joint Surg Am. 1990;72:825–833.PubMed Berrey BH Jr, Lord CF, Gebhardt MC, Mankin HJ. Fractures of allografts. Frequency, treatment, and end-results. J Bone Joint Surg Am. 1990;72:825–833.PubMed
9.
go back to reference Bianco P, Riminucci M, Gronthos S, Robey PG. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells. 2001;19:180–192.PubMed Bianco P, Riminucci M, Gronthos S, Robey PG. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells. 2001;19:180–192.PubMed
10.
go back to reference Bianco P, Robey PG. Stem cells in tissue engineering. Nature. 2001;414:118–121.PubMed Bianco P, Robey PG. Stem cells in tissue engineering. Nature. 2001;414:118–121.PubMed
11.
go back to reference Bostrom MP, Lane JM, Berberian WS, Missri AA, Tomin E, Weiland A, Doty SB, Glaser D, Rosen VM. Immunolocalization and expression of bone morphogenetic proteins 2 and 4 in fracture healing. J Orthop Res. 1995;13:357–367.PubMed Bostrom MP, Lane JM, Berberian WS, Missri AA, Tomin E, Weiland A, Doty SB, Glaser D, Rosen VM. Immunolocalization and expression of bone morphogenetic proteins 2 and 4 in fracture healing. J Orthop Res. 1995;13:357–367.PubMed
12.
go back to reference Burchardt H. The biology of bone graft repair. Clin Orthop Relat Res. 1983;174:28–42.PubMed Burchardt H. The biology of bone graft repair. Clin Orthop Relat Res. 1983;174:28–42.PubMed
13.
go back to reference Burchardt H. Biology of bone transplantation. Orthop Clin North Am. 1987;18:187–196.PubMed Burchardt H. Biology of bone transplantation. Orthop Clin North Am. 1987;18:187–196.PubMed
14.
go back to reference Burchardt H, Enneking WF. Transplantation of bone. Surg Clin North Am. 1978;58:403–427.PubMed Burchardt H, Enneking WF. Transplantation of bone. Surg Clin North Am. 1978;58:403–427.PubMed
15.
go back to reference Cancedda R, Giannoni P, Mastrogiacomo M. A tissue engineering approach to bone repair in large animal models and in clinical practice. Biomaterials. 2007;28:4240–4250.PubMed Cancedda R, Giannoni P, Mastrogiacomo M. A tissue engineering approach to bone repair in large animal models and in clinical practice. Biomaterials. 2007;28:4240–4250.PubMed
17.
go back to reference Carter DR, Beaupre GS, Giori NJ, Helms JA. Mechanobiology of skeletal regeneration. Clin Orthop Relat Res. 1998;355 Suppl:S41–55.PubMed Carter DR, Beaupre GS, Giori NJ, Helms JA. Mechanobiology of skeletal regeneration. Clin Orthop Relat Res. 1998;355 Suppl:S41–55.PubMed
18.
go back to reference Davy DT. Biomechanical issues in bone transplantation. Orthop Clin North Am. 1999;30:553–563.PubMed Davy DT. Biomechanical issues in bone transplantation. Orthop Clin North Am. 1999;30:553–563.PubMed
19.
go back to reference Dawson E, Mapili G, Erickson K, Taqvi S, Roy K. Biomaterials for stem cell differentiation. Adv Drug Deliv Rev. 2008;60:215–228.PubMed Dawson E, Mapili G, Erickson K, Taqvi S, Roy K. Biomaterials for stem cell differentiation. Adv Drug Deliv Rev. 2008;60:215–228.PubMed
20.
go back to reference Delloye C, Simon P, Nyssen-Behets C, Banse X, Bresler F, Schmitt D. Perforations of cortical bone allografts improve their incorporation. Clin Orthop Relat. Res. 2002;396:240–247.PubMed Delloye C, Simon P, Nyssen-Behets C, Banse X, Bresler F, Schmitt D. Perforations of cortical bone allografts improve their incorporation. Clin Orthop Relat. Res. 2002;396:240–247.PubMed
21.
go back to reference Duvall CL, Robert Taylor W, Weiss D, Guldberg RE. Quantitative microcomputed tomography analysis of collateral vessel development after ischemic injury. Am J Physiol Heart Circ Physiol. 2004;287:H302–310.PubMed Duvall CL, Robert Taylor W, Weiss D, Guldberg RE. Quantitative microcomputed tomography analysis of collateral vessel development after ischemic injury. Am J Physiol Heart Circ Physiol. 2004;287:H302–310.PubMed
22.
go back to reference Enneking WF, Campanacci DA. Retrieved human allografts: a clinicopathological study. J Bone Joint Surg Am. 2001;83:971–986.PubMed Enneking WF, Campanacci DA. Retrieved human allografts: a clinicopathological study. J Bone Joint Surg Am. 2001;83:971–986.PubMed
23.
go back to reference Enneking WF, Mindell ER. Observations on massive retrieved human allografts. J Bone Joint Surg Am. 1991;73:1123–1142.PubMed Enneking WF, Mindell ER. Observations on massive retrieved human allografts. J Bone Joint Surg Am. 1991;73:1123–1142.PubMed
24.
go back to reference Eyre-Brook AL. The periosteum: its function reassessed. Clin Orthop Relat Res. 1984;189:300–307. Eyre-Brook AL. The periosteum: its function reassessed. Clin Orthop Relat Res. 1984;189:300–307.
25.
go back to reference Ferguson C, Alpern E, Miclau T, Helms JA. Does adult fracture repair recapitulate embryonic skeletal formation? Mech Dev. 1999;87:57–66.PubMed Ferguson C, Alpern E, Miclau T, Helms JA. Does adult fracture repair recapitulate embryonic skeletal formation? Mech Dev. 1999;87:57–66.PubMed
26.
go back to reference Fox EJ, Hau MA, Gebhardt MC, Hornicek FJ, Tomford WW, Mankin HJ. Long-term followup of proximal femoral allografts. Clin OrthopRelat Res. 2002;397:106–113. Fox EJ, Hau MA, Gebhardt MC, Hornicek FJ, Tomford WW, Mankin HJ. Long-term followup of proximal femoral allografts. Clin OrthopRelat Res. 2002;397:106–113.
27.
go back to reference Garbuz DS, Masri BA, Czitrom AA. Biology of allografting. Orthop Clin North Am. 1998;29:199–204.PubMed Garbuz DS, Masri BA, Czitrom AA. Biology of allografting. Orthop Clin North Am. 1998;29:199–204.PubMed
28.
go back to reference Gerber HP, Vu TH, Ryan AM, Kowalski J, Werb Z, Ferrara N. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med. 1999;5:623–628.PubMed Gerber HP, Vu TH, Ryan AM, Kowalski J, Werb Z, Ferrara N. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med. 1999;5:623–628.PubMed
29.
go back to reference Goldberg VM, Stevenson S. The biology of bone grafts. Semin Arthroplasty. 1993;4:58–63.PubMed Goldberg VM, Stevenson S. The biology of bone grafts. Semin Arthroplasty. 1993;4:58–63.PubMed
30.
go back to reference Gray JC, Elves MW. Donor cells’ contribution to osteogenesis in experimental cancellous bone grafts. Clin Orthop Relat Res. 1982;163:261–271.PubMed Gray JC, Elves MW. Donor cells’ contribution to osteogenesis in experimental cancellous bone grafts. Clin Orthop Relat Res. 1982;163:261–271.PubMed
31.
go back to reference Griffith LG, Naughton G. Tissue engineering–current challenges and expanding opportunities. Science. 2002;295:1009–1014.PubMed Griffith LG, Naughton G. Tissue engineering–current challenges and expanding opportunities. Science. 2002;295:1009–1014.PubMed
32.
go back to reference Guilak F, Awad HA, Fermor B, Leddy HA, Gimble JM. Adipose-derived adult stem cells for cartilage tissue engineering. Biorheology. 2004;41:389–399.PubMed Guilak F, Awad HA, Fermor B, Leddy HA, Gimble JM. Adipose-derived adult stem cells for cartilage tissue engineering. Biorheology. 2004;41:389–399.PubMed
33.
go back to reference Guldberg RE, Ballock RT, Boyan BD, Duvall CL, Lin AS, Nagaraja S, Oest M, Phillips J, Porter BD, Robertson G, Taylor WR. Analyzing bone, blood vessels, and biomaterials with microcomputed tomography. IEEE Eng Med Biol Mag. 2003;22:77–83.PubMed Guldberg RE, Ballock RT, Boyan BD, Duvall CL, Lin AS, Nagaraja S, Oest M, Phillips J, Porter BD, Robertson G, Taylor WR. Analyzing bone, blood vessels, and biomaterials with microcomputed tomography. IEEE Eng Med Biol Mag. 2003;22:77–83.PubMed
34.
go back to reference Guldberg RE, Oest M, Lin AS, Ito H, Chao X, Gromov K, Goater JJ, Koefoed M, Schwarz EM, O’Keefe RJ, Zhang X. Functional integration of tissue-engineered bone constructs. J Musculoskelet Neuronal Interact. 2004;4:399–400.PubMed Guldberg RE, Oest M, Lin AS, Ito H, Chao X, Gromov K, Goater JJ, Koefoed M, Schwarz EM, O’Keefe RJ, Zhang X. Functional integration of tissue-engineered bone constructs. J Musculoskelet Neuronal Interact. 2004;4:399–400.PubMed
35.
go back to reference Hashimoto T, Shigetomi M, Ohno T, Matsunaga T, Muramatsu K, Tanaka H, Sugiyama T, Taguchi T. Sequential treatment with intermittent low-dose human parathyroid hormone (1–34) and bisphosphonate enhances large-size skeletal reconstruction by vascularized bone transplantation. Calcif Tissue Int. 2007;81:232–239.PubMed Hashimoto T, Shigetomi M, Ohno T, Matsunaga T, Muramatsu K, Tanaka H, Sugiyama T, Taguchi T. Sequential treatment with intermittent low-dose human parathyroid hormone (1–34) and bisphosphonate enhances large-size skeletal reconstruction by vascularized bone transplantation. Calcif Tissue Int. 2007;81:232–239.PubMed
36.
go back to reference Hee CK, Jonikas MA, Nicoll SB. Influence of three-dimensional scaffold on the expression of osteogenic differentiation markers by human dermal fibroblasts. Biomaterials. 2006;27:875–884.PubMed Hee CK, Jonikas MA, Nicoll SB. Influence of three-dimensional scaffold on the expression of osteogenic differentiation markers by human dermal fibroblasts. Biomaterials. 2006;27:875–884.PubMed
37.
go back to reference Herschman HR. Prostaglandin synthase 2. Biochem. Biophys. Acta. 1996;1229:125–140. Herschman HR. Prostaglandin synthase 2. Biochem. Biophys. Acta. 1996;1229:125–140.
38.
go back to reference Hirata K, Tsukazaki T, Kadowaki A, Furukawa K, Shibata Y, Moriishi T, Okubo Y, Bessho K, Komori T, Mizuno A, Yamaguchi A. Transplantation of skin fibroblasts expressing BMP-2 promotes bone repair more effectively than those expressing Runx2. Bone. 2003;32:502–512.PubMed Hirata K, Tsukazaki T, Kadowaki A, Furukawa K, Shibata Y, Moriishi T, Okubo Y, Bessho K, Komori T, Mizuno A, Yamaguchi A. Transplantation of skin fibroblasts expressing BMP-2 promotes bone repair more effectively than those expressing Runx2. Bone. 2003;32:502–512.PubMed
39.
go back to reference Ho ML, Chang JK, Wang GJ. Effects of ketorolac on bone repair: A radiographic study in modeled demineralized bone matrix grafted rabbits. Pharmacology. 1998;57:148–159.PubMed Ho ML, Chang JK, Wang GJ. Effects of ketorolac on bone repair: A radiographic study in modeled demineralized bone matrix grafted rabbits. Pharmacology. 1998;57:148–159.PubMed
40.
go back to reference Hutmacher DW, Sittinger M. Periosteal cells in bone tissue engineering. Tissue Eng. 2003;9 Suppl 1:S45–64.PubMed Hutmacher DW, Sittinger M. Periosteal cells in bone tissue engineering. Tissue Eng. 2003;9 Suppl 1:S45–64.PubMed
41.
go back to reference Ito Y, Fitzsimmons JS, Sanyal A, Mello MA, Mukherjee N, O’Driscoll SW. Localization of chondrocyte precursors in periosteum. Osteoarthritis Cartilage. 2001;9:215–223.PubMed Ito Y, Fitzsimmons JS, Sanyal A, Mello MA, Mukherjee N, O’Driscoll SW. Localization of chondrocyte precursors in periosteum. Osteoarthritis Cartilage. 2001;9:215–223.PubMed
42.
go back to reference Jayaraman K, Kotaki M, Zhang Y, Mo X, Ramakrishna S. Recent advances in polymer nanofibers. J Nanosci Nanotechnol. 2004;4:52–65.PubMed Jayaraman K, Kotaki M, Zhang Y, Mo X, Ramakrishna S. Recent advances in polymer nanofibers. J Nanosci Nanotechnol. 2004;4:52–65.PubMed
43.
go back to reference Kakar S, Einhorn TA, Vora S, Miara LJ, Hon G, Wigner NA, Toben D, Jacobsen KA, Al-Sebaei MO, Song M, Trackman PC, Morgan EF, Gerstenfeld LC, Barnes GL. Enhanced chondrogenesis and Wnt-signaling in parathyroid hormone treated fractures. J Bone Miner Res. 2007;22:1903–1912.PubMed Kakar S, Einhorn TA, Vora S, Miara LJ, Hon G, Wigner NA, Toben D, Jacobsen KA, Al-Sebaei MO, Song M, Trackman PC, Morgan EF, Gerstenfeld LC, Barnes GL. Enhanced chondrogenesis and Wnt-signaling in parathyroid hormone treated fractures. J Bone Miner Res. 2007;22:1903–1912.PubMed
44.
go back to reference Kandziora F, Pflugmacher R, Scholz M, Knispel C, Hiller T, Schollmeier G, Bail H, Schmidmaier G, Duda G, Raschke M, Haas NP. Comparison of BMP-2 and combined IGF-I/TGF-ss1 application in a sheep cervical spine fusion model. Eur Spine J. 2002;11:482–493.PubMed Kandziora F, Pflugmacher R, Scholz M, Knispel C, Hiller T, Schollmeier G, Bail H, Schmidmaier G, Duda G, Raschke M, Haas NP. Comparison of BMP-2 and combined IGF-I/TGF-ss1 application in a sheep cervical spine fusion model. Eur Spine J. 2002;11:482–493.PubMed
45.
go back to reference Kim HW, Jahng JS. Effect of intermittent administration of parathyroid hormone on fracture healing in ovariectomized rats. Iowa Orthop J. 1999;19:71–77.PubMed Kim HW, Jahng JS. Effect of intermittent administration of parathyroid hormone on fracture healing in ovariectomized rats. Iowa Orthop J. 1999;19:71–77.PubMed
46.
go back to reference Kim TG, Park TG. Biomimicking extracellular matrix: cell adhesive RGD peptide modified electrospun poly(D,L-lactic-co-glycolic acid) nanofiber mesh. Tissue Eng. 2006;12:221–233.PubMed Kim TG, Park TG. Biomimicking extracellular matrix: cell adhesive RGD peptide modified electrospun poly(D,L-lactic-co-glycolic acid) nanofiber mesh. Tissue Eng. 2006;12:221–233.PubMed
47.
go back to reference King KF. Periosteal pedicle grafting in dogs. J Bone Joint Surg Br. 1976;58:117–121.PubMed King KF. Periosteal pedicle grafting in dogs. J Bone Joint Surg Br. 1976;58:117–121.PubMed
48.
go back to reference Knothe Tate ML, Ritzman TF, Schneider E, Knothe UR. Testing of a new one-stage bone-transport surgical procedure exploiting the periosteum for the repair of long-bone defects. J Bone Joint Surg Am. 2007;89:307–316.PubMed Knothe Tate ML, Ritzman TF, Schneider E, Knothe UR. Testing of a new one-stage bone-transport surgical procedure exploiting the periosteum for the repair of long-bone defects. J Bone Joint Surg Am. 2007;89:307–316.PubMed
49.
go back to reference Kostopoulos L, Karring T. Role of periosteum in the formation of jaw bone. An experiment in the rat. J Clin Periodontol. 1995;22:247–254.PubMed Kostopoulos L, Karring T. Role of periosteum in the formation of jaw bone. An experiment in the rat. J Clin Periodontol. 1995;22:247–254.PubMed
50.
go back to reference Krebsbach PH, Gu K, Franceschi RT, Rutherford RB. Gene therapy-directed osteogenesis: BMP-7-transduced human fibroblasts form bone in vivo. Hum Gene Ther. 2000;11:1201–1210.PubMed Krebsbach PH, Gu K, Franceschi RT, Rutherford RB. Gene therapy-directed osteogenesis: BMP-7-transduced human fibroblasts form bone in vivo. Hum Gene Ther. 2000;11:1201–1210.PubMed
51.
go back to reference Le AX, Miclau T, Hu D, Helms JA. Molecular aspects of healing in stabilized and non-stabilized fractures. J Orthop Res. 2001;19:78–84.PubMed Le AX, Miclau T, Hu D, Helms JA. Molecular aspects of healing in stabilized and non-stabilized fractures. J Orthop Res. 2001;19:78–84.PubMed
52.
go back to reference Leunig M, Demhartner TJ, Sckell A, Fraitzl CR, Gries N, Schenk RK, Ganz R. Quantitative assessment of angiogenesis and osteogenesis after transplantation of bone: comparison of isograft and allograft bone in mice. Acta Orthop Scand. 1999;70:374–380.PubMedCrossRef Leunig M, Demhartner TJ, Sckell A, Fraitzl CR, Gries N, Schenk RK, Ganz R. Quantitative assessment of angiogenesis and osteogenesis after transplantation of bone: comparison of isograft and allograft bone in mice. Acta Orthop Scand. 1999;70:374–380.PubMedCrossRef
53.
go back to reference Leunig M, Yuan F, Berk DA, Gerweck LE, Jain RK. Angiogenesis and growth of isografted bone: quantitative in vivo assay in nude mice. Lab Invest. 1994;71:300–307.PubMed Leunig M, Yuan F, Berk DA, Gerweck LE, Jain RK. Angiogenesis and growth of isografted bone: quantitative in vivo assay in nude mice. Lab Invest. 1994;71:300–307.PubMed
54.
go back to reference Lord CF, Gebhardt MC, Tomford WW, Mankin HJ. Infection in bone allografts. Incidence, nature, and treatment. J Bone Joint Surg Am. 1988;70:369–376.PubMed Lord CF, Gebhardt MC, Tomford WW, Mankin HJ. Infection in bone allografts. Incidence, nature, and treatment. J Bone Joint Surg Am. 1988;70:369–376.PubMed
55.
go back to reference Ma T, Gutnick J, Salazar B, Larsen MD, Suenaga E, Zilber S, Huang Z, Huddleston J, Smith RL, Goodman S. Modulation of allograft incorporation by continuous infusion of growth factors over a prolonged duration in vivo. Bone. 2007;41:386–392.PubMed Ma T, Gutnick J, Salazar B, Larsen MD, Suenaga E, Zilber S, Huang Z, Huddleston J, Smith RL, Goodman S. Modulation of allograft incorporation by continuous infusion of growth factors over a prolonged duration in vivo. Bone. 2007;41:386–392.PubMed
56.
go back to reference Ma Z, Kotaki M, Inai R, Ramakrishna S. Potential of nanofiber matrix as tissue-engineering scaffolds. Tissue Eng. 2005;11:101–109.PubMed Ma Z, Kotaki M, Inai R, Ramakrishna S. Potential of nanofiber matrix as tissue-engineering scaffolds. Tissue Eng. 2005;11:101–109.PubMed
57.
go back to reference Machold R, Hayashi S, Rutlin M, Muzumdar MD, Nery S, Corbin JG, Gritli-Linde A, Dellovade T, Porter JA, Rubin LL, Dudek H, McMahon AP, Fishell G. Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron. 2003;39:937–950.PubMed Machold R, Hayashi S, Rutlin M, Muzumdar MD, Nery S, Corbin JG, Gritli-Linde A, Dellovade T, Porter JA, Rubin LL, Dudek H, McMahon AP, Fishell G. Sonic hedgehog is required for progenitor cell maintenance in telencephalic stem cell niches. Neuron. 2003;39:937–950.PubMed
58.
go back to reference Mbalaviele G, Sheikh S, Stains JP, Salazar VS, Cheng SL, Chen D, Civitelli R. Beta-catenin and BMP-2 synergize to promote osteoblast differentiation and new bone formation. J Cell Biochem. 2005;94:403–418.PubMed Mbalaviele G, Sheikh S, Stains JP, Salazar VS, Cheng SL, Chen D, Civitelli R. Beta-catenin and BMP-2 synergize to promote osteoblast differentiation and new bone formation. J Cell Biochem. 2005;94:403–418.PubMed
59.
go back to reference Muramatsu K, Bishop AT. Cell repopulation in vascularized bone grafts. J Orthop Res. 2002;20:772–778.PubMed Muramatsu K, Bishop AT. Cell repopulation in vascularized bone grafts. J Orthop Res. 2002;20:772–778.PubMed
60.
go back to reference Muramatsu K, Valenzuela RG, Bishop AT. Detection of chimerism following vascularized bone allotransplantation by polymerase chain reaction using a Y-chromosome specific primer. J Orthop Res. 2003;21:1056–1062.PubMed Muramatsu K, Valenzuela RG, Bishop AT. Detection of chimerism following vascularized bone allotransplantation by polymerase chain reaction using a Y-chromosome specific primer. J Orthop Res. 2003;21:1056–1062.PubMed
61.
go back to reference Nakahara H, Bruder SP, Goldberg VM, Caplan AI. In vivo osteochondrogenic potential of cultured cells derived from the periosteum. Clin Orthop Relat Res. 1990;259:223–232.PubMed Nakahara H, Bruder SP, Goldberg VM, Caplan AI. In vivo osteochondrogenic potential of cultured cells derived from the periosteum. Clin Orthop Relat Res. 1990;259:223–232.PubMed
62.
go back to reference Nakahara H, Bruder SP, Haynesworth SE, Holecek JJ, Baber MA, Goldberg VM, Caplan AI. Bone and cartilage formation in diffusion chambers by subcultured cells derived from the periosteum. Bone. 1990;11:181–188.PubMed Nakahara H, Bruder SP, Haynesworth SE, Holecek JJ, Baber MA, Goldberg VM, Caplan AI. Bone and cartilage formation in diffusion chambers by subcultured cells derived from the periosteum. Bone. 1990;11:181–188.PubMed
63.
go back to reference Nakahara H, Goldberg VM, Caplan AI. Culture-expanded human periosteal-derived cells exhibit osteochondral potential in vivo. J Orthop Res. 1991;9:465–476.PubMed Nakahara H, Goldberg VM, Caplan AI. Culture-expanded human periosteal-derived cells exhibit osteochondral potential in vivo. J Orthop Res. 1991;9:465–476.PubMed
64.
go back to reference Nakazawa T, Nakajima A, Shiomi K, Moriya H, Einhorn TA, Yamazaki M. Effects of low-dose, intermittent treatment with recombinant human parathyroid hormone (1–34) on chondrogenesis in a model of experimental fracture healing. Bone. 2005;37:711–719.PubMed Nakazawa T, Nakajima A, Shiomi K, Moriya H, Einhorn TA, Yamazaki M. Effects of low-dose, intermittent treatment with recombinant human parathyroid hormone (1–34) on chondrogenesis in a model of experimental fracture healing. Bone. 2005;37:711–719.PubMed
65.
go back to reference O’Driscoll SW, Fitzsimmons JS. The role of periosteum in cartilage repair. Clin Orthop Relat Res. 2001;391 Suppl:S190–207.PubMed O’Driscoll SW, Fitzsimmons JS. The role of periosteum in cartilage repair. Clin Orthop Relat Res. 2001;391 Suppl:S190–207.PubMed
66.
go back to reference Okazaki K, Jingushi S, Ikenoue T, Urabe K, Sakai H, Iwamoto Y. Expression of parathyroid hormone-related peptide and insulin-like growth factor I during rat fracture healing. J Orthop Res. 2003;21:511–520.PubMed Okazaki K, Jingushi S, Ikenoue T, Urabe K, Sakai H, Iwamoto Y. Expression of parathyroid hormone-related peptide and insulin-like growth factor I during rat fracture healing. J Orthop Res. 2003;21:511–520.PubMed
67.
go back to reference O’Keefe RJ, Tiyapatanaputi P, Xie C, Li TF, Clark C, Zuscik MJ, Chen D, Drissi H, Schwarz E, Zhang X. COX-2 has a critical role during incorporation of structural bone allografts. Ann NY Acad Sci. 2006;1068:532–542.PubMed O’Keefe RJ, Tiyapatanaputi P, Xie C, Li TF, Clark C, Zuscik MJ, Chen D, Drissi H, Schwarz E, Zhang X. COX-2 has a critical role during incorporation of structural bone allografts. Ann NY Acad Sci. 2006;1068:532–542.PubMed
68.
go back to reference Orwoll ES. Toward an expanded understanding of the role of the periosteum in skeletal health. J Bone Miner Res. 2003;18:949–954.PubMed Orwoll ES. Toward an expanded understanding of the role of the periosteum in skeletal health. J Bone Miner Res. 2003;18:949–954.PubMed
69.
go back to reference Ouyang HW, Cao T, Zou XH, Heng BC, Wang LL, Song XH, Huang HF. Mesenchymal stem cell sheets revitalize nonviable dense grafts: implications for repair of large-bone and tendon defects. Transplantation. 2006;82:170–174.PubMed Ouyang HW, Cao T, Zou XH, Heng BC, Wang LL, Song XH, Huang HF. Mesenchymal stem cell sheets revitalize nonviable dense grafts: implications for repair of large-bone and tendon defects. Transplantation. 2006;82:170–174.PubMed
70.
go back to reference Owen GR, Jackson J, Chehroudi B, Burt H, Brunette DM. A PLGA membrane controlling cell behaviour for promoting tissue regeneration. Biomaterials. 2005;26:7447–7456.PubMed Owen GR, Jackson J, Chehroudi B, Burt H, Brunette DM. A PLGA membrane controlling cell behaviour for promoting tissue regeneration. Biomaterials. 2005;26:7447–7456.PubMed
71.
go back to reference Park KE, Kang HK, Lee SJ, Min BM, Park WH. Biomimetic nanofibrous scaffolds: preparation and characterization of PGA/chitin blend nanofibers. Biomacromolecules. 2006;7:635–643.PubMed Park KE, Kang HK, Lee SJ, Min BM, Park WH. Biomimetic nanofibrous scaffolds: preparation and characterization of PGA/chitin blend nanofibers. Biomacromolecules. 2006;7:635–643.PubMed
72.
go back to reference Peng H, Wright V, Usas A, Gearhart B, Shen HC, Cummins J, Huard J. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J Clin Invest. 2002;110:751–759.PubMed Peng H, Wright V, Usas A, Gearhart B, Shen HC, Cummins J, Huard J. Synergistic enhancement of bone formation and healing by stem cell-expressed VEGF and bone morphogenetic protein-4. J Clin Invest. 2002;110:751–759.PubMed
73.
go back to reference Phillips JE, Guldberg RE, Garcia AJ. Dermal fibroblasts genetically modified to express Runx2/Cbfa1 as a mineralizing cell source for bone tissue engineering. Tissue Eng. 2007;13:2029–2040.PubMed Phillips JE, Guldberg RE, Garcia AJ. Dermal fibroblasts genetically modified to express Runx2/Cbfa1 as a mineralizing cell source for bone tissue engineering. Tissue Eng. 2007;13:2029–2040.PubMed
74.
go back to reference Phillips JE, Hutmacher DW, Guldberg RE, Garcia AJ. Mineralization capacity of Runx2/Cbfa1-genetically engineered fibroblasts is scaffold dependent. Biomaterials. 2006;27:5535–5545.PubMed Phillips JE, Hutmacher DW, Guldberg RE, Garcia AJ. Mineralization capacity of Runx2/Cbfa1-genetically engineered fibroblasts is scaffold dependent. Biomaterials. 2006;27:5535–5545.PubMed
75.
go back to reference Reynolds DG, Hock C, Shaikh S, Jacobson J, Zhang X, Rubery PT, Beck CA, O’Keefe RJ, Lerner AL, Schwarz EM, Awad HA. Micro-computed tomography prediction of biomechanical strength in murine structural bone grafts. J Biomech. 2007;40:3178–3186.PubMed Reynolds DG, Hock C, Shaikh S, Jacobson J, Zhang X, Rubery PT, Beck CA, O’Keefe RJ, Lerner AL, Schwarz EM, Awad HA. Micro-computed tomography prediction of biomechanical strength in murine structural bone grafts. J Biomech. 2007;40:3178–3186.PubMed
76.
go back to reference Rutherford RB, Moalli M, Franceschi RT, Wang D, Gu K, Krebsbach PH. Bone morphogenetic protein-transduced human fibroblasts convert to osteoblasts and form bone in vivo. Tissue Eng. 2002;8:441–452.PubMed Rutherford RB, Moalli M, Franceschi RT, Wang D, Gu K, Krebsbach PH. Bone morphogenetic protein-transduced human fibroblasts convert to osteoblasts and form bone in vivo. Tissue Eng. 2002;8:441–452.PubMed
77.
go back to reference Sandell LJ, Adler P. Developmental patterns of cartilage. Front Biosci. 1999;4:D731–742.PubMed Sandell LJ, Adler P. Developmental patterns of cartilage. Front Biosci. 1999;4:D731–742.PubMed
78.
go back to reference Shefelbine SJ, Augat P, Claes L, Simon U. Trabecular bone fracture healing simulation with finite element analysis and fuzzy logic. J Biomech. 2005;38:2440–2450.PubMed Shefelbine SJ, Augat P, Claes L, Simon U. Trabecular bone fracture healing simulation with finite element analysis and fuzzy logic. J Biomech. 2005;38:2440–2450.PubMed
79.
go back to reference Shefelbine SJ, Simon U, Claes L, Gold A, Gabet Y, Bab I, Muller R, Augat P. Prediction of fracture callus mechanical properties using micro-CT images and voxel-based finite element analysis. Bone. 2005;36:480–488.PubMed Shefelbine SJ, Simon U, Claes L, Gold A, Gabet Y, Bab I, Muller R, Augat P. Prediction of fracture callus mechanical properties using micro-CT images and voxel-based finite element analysis. Bone. 2005;36:480–488.PubMed
80.
go back to reference Shih YR, Chen CN, Tsai SW, Wang YJ, Lee OK. Growth of mesenchymal stem cells on electrospun type I collagen nanofibers. Stem Cells. 2006;24:2391–2397.PubMed Shih YR, Chen CN, Tsai SW, Wang YJ, Lee OK. Growth of mesenchymal stem cells on electrospun type I collagen nanofibers. Stem Cells. 2006;24:2391–2397.PubMed
81.
go back to reference Siebers MC, ter Brugge PJ, Walboomers XF, Jansen JA. Integrins as linker proteins between osteoblasts and bone replacing materials. A critical review. Biomaterials. 2005;26:137–146.PubMed Siebers MC, ter Brugge PJ, Walboomers XF, Jansen JA. Integrins as linker proteins between osteoblasts and bone replacing materials. A critical review. Biomaterials. 2005;26:137–146.PubMed
82.
go back to reference Simon AM, Manigrasso MB, O’Connor JP. Cyclo-oxygenase 2 function is essential for bone fracture healing. J Bone Miner Res. 2002;17:963–976.PubMed Simon AM, Manigrasso MB, O’Connor JP. Cyclo-oxygenase 2 function is essential for bone fracture healing. J Bone Miner Res. 2002;17:963–976.PubMed
83.
go back to reference Srouji S, Blumenfeld I, Rachmiel A, Livne E. Bone defect repair in rat tibia by TGF-beta1 and IGF-1 released from hydrogel scaffold. Cell Tissue Bank. 2004;5:223–230.PubMed Srouji S, Blumenfeld I, Rachmiel A, Livne E. Bone defect repair in rat tibia by TGF-beta1 and IGF-1 released from hydrogel scaffold. Cell Tissue Bank. 2004;5:223–230.PubMed
84.
go back to reference Stankus JJ, Guan J, Fujimoto K, Wagner WR. Microintegrating smooth muscle cells into a biodegradable, elastomeric fiber matrix. Biomaterials. 2006;27:735–744.PubMed Stankus JJ, Guan J, Fujimoto K, Wagner WR. Microintegrating smooth muscle cells into a biodegradable, elastomeric fiber matrix. Biomaterials. 2006;27:735–744.PubMed
85.
go back to reference Stevenson S. Biology of bone grafts. Orthop Clin North Am. 1999;30:543–552.PubMed Stevenson S. Biology of bone grafts. Orthop Clin North Am. 1999;30:543–552.PubMed
86.
go back to reference Stevenson S, Emery SE, Goldberg VM. Factors affecting bone graft incorporation. Clin Orthop Relat Res. 1996;324:66–74.PubMed Stevenson S, Emery SE, Goldberg VM. Factors affecting bone graft incorporation. Clin Orthop Relat Res. 1996;324:66–74.PubMed
87.
go back to reference Street J, Bao M, deGuzman L, Bunting S, Peale FV Jr, Ferrara N, Steinmetz H, Hoeffel J, Cleland JL, Daugherty A, van Bruggen N, Redmond HP, Carano RA, Filvaroff EH. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci USA. 2002;99:9656–9661.PubMed Street J, Bao M, deGuzman L, Bunting S, Peale FV Jr, Ferrara N, Steinmetz H, Hoeffel J, Cleland JL, Daugherty A, van Bruggen N, Redmond HP, Carano RA, Filvaroff EH. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci USA. 2002;99:9656–9661.PubMed
88.
go back to reference Sudmann E, Hagen T. Indomethacin-induced delayed fracture healing. Arch Orthop Unfallchir. 1976;85:151–154.PubMed Sudmann E, Hagen T. Indomethacin-induced delayed fracture healing. Arch Orthop Unfallchir. 1976;85:151–154.PubMed
89.
go back to reference Takeda K, Gosiewska A, Peterkofsky B. Similar, but not identical, modulation of expression of extracellular matrix components during in vitro and in vivo aging of human skin fibroblasts. J Cell Physiol. 1992;153:450–459.PubMed Takeda K, Gosiewska A, Peterkofsky B. Similar, but not identical, modulation of expression of extracellular matrix components during in vitro and in vivo aging of human skin fibroblasts. J Cell Physiol. 1992;153:450–459.PubMed
90.
go back to reference Tencer A, Johnson K. Biomechanics in Orthopaedic Trauma. Philadelphia PA: JB Lippincott; 1994:109. Tencer A, Johnson K. Biomechanics in Orthopaedic Trauma. Philadelphia PA: JB Lippincott; 1994:109.
91.
go back to reference Tiyapatanaputi P, Rubery PT, Carmouche J, Schwarz EM, O’Keefe RJ, Zhang X. A novel murine segmental femoral graft model. J Orthop Res. 2004;22:1254–1260.PubMed Tiyapatanaputi P, Rubery PT, Carmouche J, Schwarz EM, O’Keefe RJ, Zhang X. A novel murine segmental femoral graft model. J Orthop Res. 2004;22:1254–1260.PubMed
92.
go back to reference Tomford WW, Mankin HJ. Bone banking. Update on methods and materials. Orthop Clin North Am. 1999;30:565–570.PubMed Tomford WW, Mankin HJ. Bone banking. Update on methods and materials. Orthop Clin North Am. 1999;30:565–570.PubMed
93.
go back to reference Tsuji K, Bandyopadhyay A, Harfe BD, Cox K, Kakar S, Gerstenfeld L, Einhorn T, Tabin CJ, Rosen V. BMP2 activity, although dispensable for bone formation, is required for the initiation of fracture healing. Nat Genet. 2006;38:1424–1429.PubMed Tsuji K, Bandyopadhyay A, Harfe BD, Cox K, Kakar S, Gerstenfeld L, Einhorn T, Tabin CJ, Rosen V. BMP2 activity, although dispensable for bone formation, is required for the initiation of fracture healing. Nat Genet. 2006;38:1424–1429.PubMed
94.
go back to reference Vane JR. Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat New Biol. 1971;231:232–235.PubMed Vane JR. Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat New Biol. 1971;231:232–235.PubMed
95.
go back to reference Wheeler DL, Haynie JL, Berrey H, Scarborough M, Enneking W. Biomechanical evaluation of retrieved massive allografts: preliminary results. Biomed Sci Instrum. 2001;37:251–256.PubMed Wheeler DL, Haynie JL, Berrey H, Scarborough M, Enneking W. Biomechanical evaluation of retrieved massive allografts: preliminary results. Biomed Sci Instrum. 2001;37:251–256.PubMed
96.
go back to reference Whitfield JF. How to grow bone to treat osteoporosis and mend fractures. Curr Rheumatol Rep. 2003;5:45–56.PubMed Whitfield JF. How to grow bone to treat osteoporosis and mend fractures. Curr Rheumatol Rep. 2003;5:45–56.PubMed
97.
go back to reference Wlodarski KH. Normal and heterotopic periosteum. Clin Orthop Relat Res. 1989;241:265–277.PubMed Wlodarski KH. Normal and heterotopic periosteum. Clin Orthop Relat Res. 1989;241:265–277.PubMed
98.
go back to reference Xie C, Reynolds D, Awad H, Rubery PT, Pelled G, Gazit D, Guldberg RE, Schwarz EM, O’Keefe RJ, Zhang X. Structural bone allograft combined with genetically engineered mesenchymal stem cells as a novel platform for bone tissue engineering. Tissue Eng. 2007;13:435–445.PubMed Xie C, Reynolds D, Awad H, Rubery PT, Pelled G, Gazit D, Guldberg RE, Schwarz EM, O’Keefe RJ, Zhang X. Structural bone allograft combined with genetically engineered mesenchymal stem cells as a novel platform for bone tissue engineering. Tissue Eng. 2007;13:435–445.PubMed
99.
go back to reference Yuasa T, Kataoka H, Kinto N, Iwamoto M, Enomoto-Iwamoto M, Iemura S, Ueno N, Shibata Y, Kurosawa H, Yamaguchi A. Sonic hedgehog is involved in osteoblast differentiation by cooperating with BMP-2. J Cell Physiol. 2002;193:225–232.PubMed Yuasa T, Kataoka H, Kinto N, Iwamoto M, Enomoto-Iwamoto M, Iemura S, Ueno N, Shibata Y, Kurosawa H, Yamaguchi A. Sonic hedgehog is involved in osteoblast differentiation by cooperating with BMP-2. J Cell Physiol. 2002;193:225–232.PubMed
100.
go back to reference Zhang J, Li L. Stem cell niche - Microenvironment and beyond. J Biol Chem. 2008;283(15):9499–9503.PubMed Zhang J, Li L. Stem cell niche - Microenvironment and beyond. J Biol Chem. 2008;283(15):9499–9503.PubMed
101.
go back to reference Zhang X, Schwarz EM, Young DA, Puzas JE, Rosier RN, O’Keefe RJ. Cyclooxygenase-2 regulates mesenchymal cell differentiation into the osteoblast lineage and is critically involved in bone repair. J Clin Invest. 2002;109:1405–1415.PubMed Zhang X, Schwarz EM, Young DA, Puzas JE, Rosier RN, O’Keefe RJ. Cyclooxygenase-2 regulates mesenchymal cell differentiation into the osteoblast lineage and is critically involved in bone repair. J Clin Invest. 2002;109:1405–1415.PubMed
102.
go back to reference Zhang X, Xie C, Lin AS, Ito H, Awad H, Lieberman JR, Rubery PT, Schwarz EM, O’Keefe RJ, Guldberg RE. Periosteal progenitor cell fate in segmental cortical bone graft transplantations: implications for functional tissue engineering. J Bone Miner Res. 2005;20:2124–2137.PubMed Zhang X, Xie C, Lin AS, Ito H, Awad H, Lieberman JR, Rubery PT, Schwarz EM, O’Keefe RJ, Guldberg RE. Periosteal progenitor cell fate in segmental cortical bone graft transplantations: implications for functional tissue engineering. J Bone Miner Res. 2005;20:2124–2137.PubMed
103.
go back to reference Zhou Y, Chen F, Ho ST, Woodruff MA, Lim TM, Hutmacher DW. Combined marrow stromal cell-sheet techniques and high-strength biodegradable composite scaffolds for engineered functional bone grafts. Biomaterials. 2007;28:814–824.PubMed Zhou Y, Chen F, Ho ST, Woodruff MA, Lim TM, Hutmacher DW. Combined marrow stromal cell-sheet techniques and high-strength biodegradable composite scaffolds for engineered functional bone grafts. Biomaterials. 2007;28:814–824.PubMed
Metadata
Title
A Perspective: Engineering Periosteum for Structural Bone Graft Healing
Authors
Xinping Zhang, PhD
Hani A. Awad, PhD
Regis J. O’Keefe, MD, PhD
Robert E. Guldberg, PhD
Edward M. Schwarz, PhD
Publication date
01-08-2008
Publisher
Springer-Verlag
Published in
Clinical Orthopaedics and Related Research® / Issue 8/2008
Print ISSN: 0009-921X
Electronic ISSN: 1528-1132
DOI
https://doi.org/10.1007/s11999-008-0312-6

Other articles of this Issue 8/2008

Clinical Orthopaedics and Related Research® 8/2008 Go to the issue

Symposium: New Approaches to Allograft Transplantation

Radioprotectant and Radiosensitizer Effects on Sterility of γ-irradiated Bone

Letter to the Editor

Reply to Letter to Editor

Symposium: New Approaches to Allograft Transplantation

HLA Sensitization and Allograft Bone Graft Incorporation

Symposium: New Approaches to Allograft Transplantation

Radioprotection of Tendon Tissue via Crosslinking and Free Radical Scavenging