What should be the characteristics of the ideal bone graft substitute? Combining scaffolds with growth factors and/or stem cells

Injury

Volumn 42, Issue SUPPL. 2, 2011, Pages

  Janicki, Patricia ^a   Schmidmaier, Gerhard ^a  

^a UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

Bone graft; Growth factor; Scaffold; Stem cell

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN 2; CALCIUM PHOSPHATE CERAMIC; FIBROBLAST GROWTH FACTOR; GROWTH FACTOR; HYDROXYAPATITE; OSTEOGENIC PROTEIN 1; PLATELET DERIVED GROWTH FACTOR; SOMATOMEDIN B; SOMATOMEDIN C; TISSUE SCAFFOLD; TRANSFORMING GROWTH FACTOR;

BONE DEVELOPMENT; BONE MATRIX; BONE PROSTHESIS; BONE REGENERATION; BONE REMODELING; DEMINERALIZED BONE MATRIX; HUMAN; MESENCHYMAL STEM CELL; MESENCHYMAL STEM CELL TRANSPLANTATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; TISSUE ENGINEERING;

EID: 80052846092     PISSN: 00201383     EISSN: 18790267     Source Type: Journal    
DOI: 10.1016/j.injury.2011.06.014     Document Type: Article

References (97)

1. E.D. Arrington, W.J. Smith, and H.G. Chambers Complications of iliac crest bone graft harvesting Clin Orthop Relat Res 329 1996 300 309 (Pubitemid 26274684)
2. A. Arthur, A. Zannettino, and S. Gronthos The therapeutic applications of multipotential mesenchymal/stromal stem cells in skeletal tissue repair J Cell Physiol 218 2 2009 237 245
3. H.W. Bae, L. Zhao, and L.E. Kanim Intervariability and intravariability of bone morphogenetic proteins in commercially available demineralized bone matrix products Spine (Phila Pa 1976) 31 12 2006 1299 1306 (Pubitemid 43833072)
4. A. Banfi, A. Muraglia, and B. Dozin Proliferation kinetics and differentiation potential of ex vivo expanded human bone marrow stromal cells: implications for their use in cell therapy Exp Hematol 28 6 2000 707 715 (Pubitemid 30398528)
5. J.C. Banwart, M.A. Asher, and R.S. Hassanein Iliac crest bone graft harvest donor site morbidity. A statistical evaluation Spine (Phila Pa 1976) 20 9 1995 1055 1060
6. O.B. Betz, V.M. Betz, and A. Nazarian Delayed administration of adenoviral BMP-2 vector improves the formation of bone in osseous defects Gene Ther 14 13 2007 1039 1044 (Pubitemid 46965273)
7. O.B. Betz, V.M. Betz, and A. Nazarian Direct percutaneous gene delivery to enhance healing of segmental bone defects J Bone Joint Surg Am 88 2 2006 355 365 (Pubitemid 43185138)
8. M. Bohner Calcium orthophosphates in medicine: from ceramics to calcium phosphate cements Injury 31 Suppl. 2000 437 447
9. S.P. Bruder, N. Jaiswal, and S.E. Haynesworth Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation J Cell Biochem 64 2 1997 278 294 (Pubitemid 27065442)
10. S.P. Bruder, K.H. Kraus, and V.M. Goldberg The effect of implants loaded with autologous mesenchymal stem cells on the healing of canine segmental bone defects J Bone Joint Surg Am 80 7 1998 985 996 (Pubitemid 28355669)
11. S.P. Bruder, A.A. Kurth, and M. Shea Bone regeneration by implantation of purified, culture-expanded human mesenchymal stem cells J Orthop Res 16 2 1998 155 162 (Pubitemid 28249153)
12. G.M. Calori, M. D'Avino, and L. Tagliabue An ongoing research for evaluation of treatment with BMPs or AGFs in long bone non-union: protocol description and preliminary results Injury 37 Suppl. 3 2006 S43 S50
13. R. Cancedda, G. Bianchi, and A. Derubeis Cell therapy for bone disease: a review of current status Stem Cells 21 5 2003 610 619 (Pubitemid 37444117)
14. R. Cancedda, B. Dozin, and P. Giannoni Tissue engineering and cell therapy of cartilage and bone Matrix Biol 22 1 2003 81 91 (Pubitemid 36444510)
15. A.I. Caplan Mesenchymal stem cells J Orthop Res 9 5 1991 641 650
16. A.I. Caplan Why are MSCs therapeutic? New data: new insight J Pathol 217 2 2009 318 324
17. E.Y. Chao, and N. Inoue Biophysical stimulation of bone fracture repair, regeneration and remodelling Eur Cell Mater 2003 672 684
18. P. Chistolini, I. Ruspantini, and P. Bianco Biomechanical evaluation of cell-loaded and cell-free hydroxyapatite implants for the reconstruction of segmental bone defects J Mater Sci Mater Med 10 12 1999 739 742 (Pubitemid 30064192)
19. M. Crisan, S. Yap, and L. Casteilla A perivascular origin for mesenchymal stem cells in multiple human organs Cell Stem Cell 3 3 2008 301 313
20. G. D'Ippolito, P.C. Schiller, and C. Ricordi Age-related osteogenic potential of mesenchymal stromal stem cells from human vertebral bone marrow J Bone Miner Res 14 7 1999 1115 1122 (Pubitemid 29314054)
21. M.L. da Silva, A.I. Caplan, and N.B. Nardi In search of the in vivo identity of mesenchymal stem cells Stem Cells 26 9 2008 2287 2299
22. C. De Bari, F. Dell'Accio, and P. Tylzanowski Multipotent mesenchymal stem cells from adult human synovial membrane Arthritis Rheum 44 8 2001 1928 1942 (Pubitemid 32758241)
23. C. Demers, C.R. Hamdy, and K. Corsi Natural coral exoskeleton as a bone graft substitute: a review Biomed Mater Eng 12 1 2002 15 35 (Pubitemid 34177340)
24. A. Dickhut, K. Pelttari, and P. Janicki Calcification or dedifferentiation: requirement to lock mesenchymal stem cells in a desired differentiation stage J Cell Physiol 219 1 2009 219 226
25. M. Dominici, K. Le Blanc, and I. Mueller Minimal criteria for defining multipotent mesenchymal stromal cells The International Society for Cellular Therapy position statement Cytotherapy 8 4 2006 315 317 (Pubitemid 44269669)
26. G.E. Friedlaender, C.R. Perry, and J.D. Cole Osteogenic protein-1 (bone morphogenetic protein-7) in the treatment of tibial nonunions J Bone Joint Surg Am 83-A Suppl. 1 (Pt 2) 2001 S151 S158
27. O. Gauthier, J.M. Bouler, and E. Aguado Macroporous biphasic calcium phosphate ceramics: influence of macropore diameter and macroporosity percentage on bone ingrowth Biomaterials 19 1-3 1998 133 139 (Pubitemid 28239476)
28. P.V. Giannoudis, T.A. Einhorn, and D. Marsh Fracture healing: the diamond concept Injury 38 Suppl. 4 2007 S3 S6
29. S. Govender, C. Csimma, and H.K. Genant Recombinant human bone morphogenetic protein-2 for treatment of open tibial fractures: a prospective, controlled, randomized study of four hundred and fifty patients J Bone Joint Surg Am 84-A 12 2002 2123 2134 (Pubitemid 35417689)
30. S. Gronthos, A.C. Zannettino, and S.J. Hay Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow J Cell Sci 116 Pt 9 2003 1827 1835 (Pubitemid 36582169)
31. S.E. Haynesworth, J. Goshima, and V.M. Goldberg Characterization of cells with osteogenic potential from human marrow Bone 13 1 1992 81 88
32. P. Hernigou, G. Mathieu, and A. Poignard Percutaneous autologous bone-marrow grafting for nonunions Surgical technique J Bone Joint Surg Am 88 Suppl. 1 Pt 2006 2322 2327
33. P. Hernigou, A. Poignard, and F. Beaujean Percutaneous autologous bone-marrow grafting for nonunions Influence of the number and concentration of progenitor cells J Bone Joint Surg Am 87 7 2005 1430 1437 (Pubitemid 40917741)
34. P. Janicki, P. Kasten, and K. Kleinschmidt Chondrogenic pre-induction of human mesenchymal stem cells on beta-TCP: enhanced bone quality by endochondral heterotopic bone formation Acta Biomater 6 8 2010 3292 3301
35. E. Jones, A. English, and S.M. Churchman Large-scale extraction and characterization of CD271+ multipotential stromal cells from trabecular bone in health and osteoarthritis: implications for bone regeneration strategies based on uncultured or minimally cultured multipotential stromal cells Arthritis Rheum 62 7 2010 1944 1954
36. F. Kandziora, G. Schmidmaier, and G. Schollmeier IGF-I and TGF-beta1 application by a poly-(d,l-lactide)-coated cage promotes intervertebral bone matrix formation in the sheep cervical spine Spine (Phila Pa 1976) 27 16 2002 1710 1723
37. P. Kasten, I. Beyen, and P. Niemeyer Porosity and pore size of beta-tricalcium phosphate scaffold can influence protein production and osteogenic differentiation of human mesenchymal stem cells: an in vitro and in vivo study Acta Biomater 4 6 2008 1904 1915
38. P. Kasten, J. Vogel, and R. Luginbuhl Ectopic bone formation associated with mesenchymal stem cells in a resorbable calcium deficient hydroxyapatite carrier Biomaterials 26 29 2005 5879 5889 (Pubitemid 40798279)
39. E. Kon, A. Muraglia, and A. Corsi Autologous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep long bones J Biomed Mater Res 49 3 2000 328 337 (Pubitemid 30030478)
40. P.H. Krebsbach, S.A. Kuznetsov, and K. Satomura Bone formation in vivo: comparison of osteogenesis by transplanted mouse and human marrow stromal fibroblasts Transplantation 63 8 1997 1059 1069 (Pubitemid 27190967)
41. P.H. Krebsbach, M.H. Mankani, and K. Satomura Repair of craniotomy defects using bone marrow stromal cells Transplantation 66 10 1998 1272 1278 (Pubitemid 28551005)
42. J.M. Lane Bone morphogenic protein science and studies J Orthop Trauma 19 10 Suppl. 2005 S17 S22
43. R. Langer Tissue engineering Mol Ther 1 1 2000 12 15
44. Le Blanc K Mesenchymal stromal cells: tissue repair and immune modulation Cytotherapy 8 6 2006 559 561 (Pubitemid 44869856)
45. C.H. Lee, A. Singla, and Y. Lee Biomedical applications of collagen Int J Pharm 221 1-2 2001 1 22 (Pubitemid 32524031)
46. R.Z. LeGeros Properties of osteoconductive biomaterials: calcium phosphates Clin Orthop Relat Res 395 2002 81 98
47. R.H. Li, M.L. Bouxsein, and C.A. Blake rhBMP-2 injected in a calcium phosphate paste (alpha-BSM) accelerates healing in the rabbit ulnar osteotomy model J Orthop Res 21 6 2003 997 1004 (Pubitemid 37322380)
48. J.R. Lieberman, A. Daluiski, and T.A. Einhorn The role of growth factors in the repair of bone. Biology and clinical applications J Bone Joint Surg Am 84-A 6 2002 1032 1044
49. O. Mahony, and J.R. Jones Porous bioactive nanostructured scaffolds for bone regeneration: a sol-gel solution Nanomedicine (London) 3 2 2008 233 245 (Pubitemid 351621748)
50. A.K. Majors, C.A. Boehm, and H. Nitto Characterization of human bone marrow stromal cells with respect to osteoblastic differentiation J Orthop Res 15 4 1997 546 557 (Pubitemid 27433368)
51. M.H. Mankani, S.A. Kuznetsov, and B. Fowler In vivo bone formation by human bone marrow stromal cells: effect of carrier particle size and shape Biotechnol Bioeng 72 1 2001 96 107 (Pubitemid 32085898)
52. F. Mannello, and G.A. Tonti Concise review: no breakthroughs for human mesenchymal and embryonic stem cell culture: conditioned medium, feeder layer, or feeder-free; medium with fetal calf serum, human serum, or enriched plasma; serum-free, serum replacement nonconditioned medium, or ad hoc formula? All that glitters is not gold! Stem Cells 25 7 2007 1603 1609 (Pubitemid 47121836)
53. M. Marcacci, E. Kon, and V. Moukhachev Stem cells associated with macroporous bioceramics for long bone repair: 6- to 7-year outcome of a pilot clinical study Tissue Eng 13 5 2007 947 955 (Pubitemid 46870419)
54. K. Mareschi, I. Ferrero, and D. Rustichelli Expansion of mesenchymal stem cells isolated from pediatric and adult donor bone marrow J Cell Biochem 97 4 2006 744 754
55. P.J. Marie, and O. Fromigue Osteogenic differentiation of human marrow-derived mesenchymal stem cells Regen Med 1 4 2006 539 548
56. R.F. McLain, J.E. Fleming, and C.A. Boehm Aspiration of osteoprogenitor cells for augmenting spinal fusion: comparison of progenitor cell concentrations from the vertebral body and iliac crest J Bone Joint Surg Am 87 12 2005 2655 2661 (Pubitemid 41747032)
57. S.C. Mendes, J.M. Tibbe, and M. Veenhof Bone tissue-engineered implants using human bone marrow stromal cells: effect of culture conditions and donor age Tissue Eng 8 6 2002 911 920 (Pubitemid 35397237)
58. S.C. Mendes, J.M. Tibbe, and M. Veenhof Relation between in vitro and in vivo osteogenic potential of cultured human bone marrow stromal cells J Mater Sci Mater Med 15 10 2004 1123 1128 (Pubitemid 39491717)
59. A. Muraglia, R. Cancedda, and R. Quarto Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model J Cell Sci 113 Pt 7 2000 1161 1166 (Pubitemid 30229533)
60. A. Muraglia, I. Martin, and R. Cancedda A nude mouse model for human bone formation in unloaded conditions Bone 22 5 Suppl. 1998 131S 134S (Pubitemid 28223271)
61. G.F. Muschler, C. Boehm, and K. Easley Aspiration to obtain osteoblast progenitor cells from human bone marrow: the influence of aspiration volume J Bone Joint Surg Am 79 11 1997 1699 1709 (Pubitemid 27508530)
62. G.F. Muschler, H. Nitto, and C.A. Boehm Age- and gender-related changes in the cellularity of human bone marrow and the prevalence of osteoblastic progenitors J Orthop Res 19 1 2001 117 125 (Pubitemid 32288644)
63. H. Nakahara, V.M. Goldberg, and A.I. Caplan Culture-expanded human periosteal-derived cells exhibit osteochondral potential in vivo J Orthop Res 9 4 1991 465 476
64. R.E. Newman, D. Yoo, and M.A. LeRoux Treatment of inflammatory diseases with mesenchymal stem cells Inflamm Allergy Drug Targets 8 2 2009 110 123
65. D. Noel, F. Djouad, and C. Bouffi Multipotent mesenchymal stromal cells and immune tolerance Leuk Lymphoma 48 7 2007 1283 1289 (Pubitemid 47079355)
66. C. Ohtsuki, M. Kamitakahara, and T. Miyazaki Bioactive ceramic-based materials with designed reactivity for bone tissue regeneration J R Soc Interface 6 Suppl. 3 2009 S349 S360
67. Y. Okubo, K. Bessho, and K. Fujimura Osteoinduction by recombinant human bone morphogenetic protein-2 at intramuscular, intermuscular, subcutaneous and intrafatty sites Int J Oral Maxillofac Surg 29 1 2000 62 66
68. H. Petite, V. Viateau, and W. Bensaid Tissue-engineered bone regeneration Nat Biotechnol 18 9 2000 959 963 (Pubitemid 32977376)
69. D.G. Phinney, G. Kopen, and W. Righter Donor variation in the growth properties and osteogenic potential of human marrow stromal cells J Cell Biochem 75 3 1999 424 436 (Pubitemid 29521651)
70. M.F. Pittenger, A.M. Mackay, and S.C. Beck Multilineage potential of adult human mesenchymal stem cells Science 1999 284143 284147
71. R. Quarto, M. Mastrogiacomo, and R. Cancedda Repair of large bone defects with the use of autologous bone marrow stromal cells N Engl J Med 344 5 2001 385 386 (Pubitemid 32107654)
72. D.J. Rickard, M. Kassem, and T.E. Hefferan Isolation and characterization of osteoblast precursor cells from human bone marrow J Bone Miner Res 11 3 1996 312 324 (Pubitemid 26076381)
73. G. Ryan, A. Pandit, and D.P. Apatsidis Fabrication methods of porous metals for use in orthopaedic applications Biomaterials 27 13 2006 2651 2670 (Pubitemid 43122070)
74. B. Sacchetti, A. Funari, and S. Michienzi Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment Cell 131 2 2007 324 336 (Pubitemid 47592917)
75. G. Schmidmaier, S. Herrmann, and J. Green Quantitative assessment of growth factors in reaming aspirate, iliac crest, and platelet preparation Bone 39 5 2006 1156 1163 (Pubitemid 44540277)
76. G. Schmidmaier, P. Schwabe, and B. Wildemann Use of bone morphogenetic proteins for treatment of non-unions and future perspectives Injury 38 Suppl. 4 2007 S35 S41
77. G. Schmidmaier, B. Wildemann, and H. Bail Local application of growth factors (insulin-like growth factor-1 and transforming growth factor-beta1) from a biodegradable poly(d,l-lactide) coating of osteosynthetic implants accelerates fracture healing in rats Bone 28 4 2001 341 350 (Pubitemid 32390106)
78. G. Schmidmaier, B. Wildemann, and F. Cromme Bone morphogenetic protein-2 coating of titanium implants increases biomechanical strength and accelerates bone remodeling in fracture treatment: a biomechanical and histological study in rats Bone 30 6 2002 816 822 (Pubitemid 34616007)
79. B. Schmidt-Rohlfing, C. Tzioupis, and C.L. Menzel Tissue engineering of bone tissue. Principles and clinical applications Unfallchirurg 112 9 2009 785 794
80. A. Shahdadfar, K. Fronsdal, and T. Haug In vitro expansion of human mesenchymal stem cells: choice of serum is a determinant of cell proliferation, differentiation, gene expression, and transcriptome stability Stem Cells 23 9 2005 1357 1366 (Pubitemid 41504923)
81. R. Siddappa, R. Licht, and C. van Blitterswijk Donor variation and loss of multipotency during in vitro expansion of human mesenchymal stem cells for bone tissue engineering J Orthop Res 25 8 2007 1029 1041 (Pubitemid 47233079)
82. P.A. Sotiropoulou, S.A. Perez, and M. Salagianni Characterization of the optimal culture conditions for clinical scale production of human mesenchymal stem cells Stem Cells 24 2 2006 462 471 (Pubitemid 44464816)
83. K. Stenderup, J. Justesen, and C. Clausen Aging is associated with decreased maximal life span and accelerated senescence of bone marrow stromal cells Bone 33 6 2003 919 926 (Pubitemid 37543568)
84. E. Tsiridis, Z. Ali, and A. Bhalla In vitro proliferation and differentiation of human mesenchymal stem cells on hydroxyapatite versus human demineralised bone matrix with and without osteogenic protein-1 Expert Opin Biol Ther 9 1 2009 9 19
85. M.R. Urist Bone: formation by autoinduction Science 150 698 1965 893 899
86. M.C. von Doernberg, B. von Rechenberg, and M. Bohner In vivo behavior of calcium phosphate scaffolds with four different pore sizes Biomaterials 27 30 2006 5186 5198 (Pubitemid 44096957)
87. W. Wagner, and A.D. Ho Mesenchymal stem cell preparations - comparing apples and oranges Stem Cell Rev 3 4 2007 239 248 (Pubitemid 351526200)
88. E.A. Wang, V. Rosen, and J.S. D'Alessandro Recombinant human bone morphogenetic protein induces bone formation Proc Natl Acad Sci USA 87 6 1990 2220 2224
89. B. Wildemann, P. Bamdad, and C. Holmer Local delivery of growth factors from coated titanium plates increases osteotomy healing in rats Bone 34 5 2004 862 868 (Pubitemid 38581132)
90. B. Wildemann, A. Kadow-Romacker, and N.P. Haas Quantification of various growth factors in different demineralized bone matrix preparations J Biomed Mater Res A 81 2 2007 437 442 (Pubitemid 46668858)
91. A. Winter, S. Breit, and D. Parsch Cartilage-like gene expression in differentiated human stem cell spheroids: a comparison of bone marrow-derived and adipose tissue-derived stromal cells Arthritis Rheum 48 2 2003 418 429 (Pubitemid 36278011)
92. J.M. Wozney, V. Rosen, and A.J. Celeste Novel regulators of bone formation: molecular clones and activities Science 242 4885 1988 1528 1534 (Pubitemid 19023695)
93. K. Yoshida, K. Bessho, and K. Fujimura Osteoinduction capability of recombinant human bone morphogenetic protein-2 in intramuscular and subcutaneous sites: an experimental study J Craniomaxillofac Surg 26 2 1998 112 115 (Pubitemid 28254720)
94. N.Y. Yu, A. Schindeler, and D.G. Little Biodegradable poly(alpha-hydroxy acid) polymer scaffolds for bone tissue engineering J Biomed Mater Res B: Appl Biomater 93 1 2010 285 295
95. A.C. Zannettino, S. Paton, and A. Arthur Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo J Cell Physiol 214 2 2008 413 421 (Pubitemid 350308998)
96. G. Zimmermann, C. Wagner, and K. Schmeckenbecher Treatment of tibial shaft non-unions: bone morphogenetic proteins versus autologous bone graft Injury 40 Suppl. 3 2009 S50 S53
97. P.A. Zuk, M. Zhu, and H. Mizuno Multilineage cells from human adipose tissue: implications for cell-based therapies Tissue Eng 7 2 2001 211 228 (Pubitemid 32295155)