Animal models for bone tissue engineering purposes

Source Book of Models for Biomedical Research

Volumn , Issue , 2008, Pages 725-736

  Viateau, Véronique ^a   Logeart Avramoglou, Delphine ^b   Guillemin, Geneviève ^b   Petite, Hervé ^b  

^a ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

^b Paris university   (France)

Author keywords

Biomechanics; Bone; Bone healing; Growth factors; Stem cells; Tissue engineering

Indexed keywords

EID: 76849104230     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-59745-285-4_74     Document Type: Chapter

References (104)

1. Logeart-Avramoglou D, Anagnostou F, Bizios R, Petite H. Engineering bone: Challenges and obstacles. J Cell Mol Med 2005;9:72-84.
2. Einhorn TA. Clinically applied models of bone regeneration in tissue engineering research. Clin Orthop Relat Res 1999;(367Suppl.): S59-67.
3. Phinney DG, Kopen G, Isaacson RL, Prockop DJ. Plastic adherent stromal cells from the bone marrow of commonly used strains of inbred mice: Variations in yield, growth, and differentiation. J Cell Biochem 1999;72:570-585.
4. Solchaga LA, Johnstone B, Yoo JU, Goldberg VM, Caplan AI. High variability in rabbit bone marrow-derived mesenchymal cell preparations. Cell Transplant 1999;8:511-519.
5. Krebsbach PH, et al. Bone formation in vivo: Comparison of osteogenesis by transplanted mouse and human marrow stromal fi broblasts. Transplantation 1997;63:1059-1069.
6. Bab I, et al. Osteogenesis in in vivo diffusion chamber cultures of human marrow cells. Bone Miner 1988;4:373-386.
7. Friedenstein AJ, Chailakhyan RK, Gerasimov UV. Bone marrow osteogenic stem cells: In vitro cultivation and transplantation in diffusion chambers. Cell Tissue Kinet 1987;20:263-272.
8. Brazelton TR, Blau HM. Optimizing techniques for tracking transplanted stem cells in vivo. Stem Cells 2005;23:1251-1265.
9. de Boer J, van Blitterswijk C, Lowik C. Bioluminescent imaging: Emerging technology for non-invasive imaging of bone tissue engineering. Biomaterials 2006;27:1851-1858.
10. Yang M, Baranov E, Moossa AR, Penman S, Hoffman RM. Visualizing gene expression by whole-body fluorescence imaging. Proc Natl Acad Sci USA 2000;97:12278-12282.
11. Wozney JM, Rosen V. Bone morphogenetic protein and bone morphogenetic protein gene family in bone formation and repair. Clin Orthop Relat Res 1998;346:26-37.
12. Bouhadir KH, Mooney DJ. Promoting angiogenesis in engineered tissues. J Drug Target 2001;9:397-406.
13. Gosain AK, et al. A 1-year study of osteoinduction in hydroxyapatitederived biomaterials in an adult sheep model: Part I. Plast Reconstr Surg 2002;109:619-630.
14. Kruyt MC, et al. Bone tissue engineering and spinal fusion: The potential of hybrid constructs by combining osteoprogenitor cells and scaffolds. Biomaterials 2004;25:1463-1473.
15. Budenz R, Bernard GW. Osteogenesis and leukopoiesis within diffusion chamber implants of isolated bone marrow subpopulation. Am J Anat 1980;159:455-474.
16. Ashton BA, Allen TD, Howlet CR, Eaglesom CC, Hattori A, Owen M. Formation of bone and cartilage by marrow stromal cells in diffusion chambers in vivo. Clin Orthop Related Res 1980;151: 294-307.
17. Haynesworth SE, Goshima J, Goldberg VM, Caplan AI. Characterization of cells with osteogenic potential from human marrow. Bone 1992;13:81-88.
18. Schmitz JP, Hollinger JO. The critical size defect as an experimental model for craniomandibulofacial nonunions. Clin Orthop Related Res 1986;205:299-308.
19. Bosch C, Melsen B, Vargervik K. Importance of the critical-size bone defect in testing bone-regenerating materials. J Craniofac Surg 1998;9:310-316.
20. Viljanen VV, Lindholm TC, Gao TJ, Lindholm TS. Low dosage of native allogeneic bone morphogenetic protein in repair of sheep calvaria defects. Int J Oral Maxillofac Surg 1997;26:389-393.
21. Hollinger JO, Kleinschmidt JC. The critical size defect as an experimental model to test bone repair materials. J Craniofac Surg 1990;1:60-68.
22. Schmitz JP, Schwartz Z, Hollinger JO, Boyan B. Characterization of rat calvarial nonunion defects. Acta Anat 1990;138:185-192.
23. Indovina A, Block MS. Comparison of three bone substitutes in canine extraction sites. J Oral Maxillofac Surg 2002;60:53-58.
24. Buser D, Hoffmann B, Bernard JP, Lussi A, Mettler D. Evaluation of filling materials in membrane-protected bone defects. A comparative histomorphometric study in the mandible of miniature pigs. Clin Oral Implants Res 1998;9:137-150.
25. Salmon R, Duncan W. Determination of the critical size for nonhealing defects in the mandibular bone of sheep. Part 1: A pilot study. J NZ Soc Periodontol 1997;81:6-15.
26. Lindsey WH, Franz DA, Toung JS, London SD, Ogle RO. A nasal critical size defect. Arch Otolaryngol Head Neck Surg 1998;124:912-915.
27. Schliephake H, Knebel JW, Aufderheide M, Tauscher M. Use of cultivated osteoprogenitor cells to increase bone formation in segmental mandibular defects: An experimental pilot study in sheep. Int J Oral Maxillofac Surg 2001;30:531-537.
28. Hanson LJ, Donovan MG, Hellstein JW, Dickerson NC. Experimental evaluation of expanded polytetrafluoroethylene for reconstruction of orbital floor defects. Int J Oral Maxillofac Surg 1994;52:1050-1055.
29. Frame JW. A convenient animal model for testing bone substitute materials. J Oral Surg 1980;38:176-180.
30. Prolo D, Pedrotti PW, Burres KP, Oklund S. Superior osteogenesis in transplanted allogeneic canine skull following chemical sterilization. Clin Orthop 1980;108:230.
31. Hjorting-Hansen E, Andreasen JO. Incomplete bone healing of experimental cavities in dog mandibles. Br J Oral Surg 1971;9:33.
32. Leake DL, Rappoport M. Mandibular reconstruction: Bone induction in an alloplastic tray. Surgery 1972;72:332.
33. Lindholm TC, Lindholm TS, Marttinen A, Urist M. Bovine bone morphogenetic protein (bBMP/NCP)-induced repair of skull trephine defects in pigs. Clin Orthop Relat Res 1994;301:263-270.
34. Pasquier G, Flautre B, Blary MC, Anselme K, Hardouin P. Injectable percutaneous bone biomaterials: An experimental study in a rabbit model. J Mater Sci Mater Med 1996;7:683-690.
35. Flautre B, Delecourt C, Blary MC, Van Landuyt P, Lemaitre J, Hardouin P. Volume effect on biological properties of a calcium phosphate hydraulic cement: An experimental study in the sheep. Bone 1999;25:35S-39S.
36. Frankenburg EP, Goldstein SA, Bauer TW, Harris SA, Poser RD. Biomechanical and histological evaluation of a calcium phosphate cement. J Bone Joint Surg Am 1998;80-A:1112-1124.
37. Anderson ML, Dhert WJ, de Bruijn JD, Dalmeijer RA, Leenders H, van Blitterswijk Verbout AJ. Critical size defect in the goat's ilium. Clin Orthop Relat Res 1999;364:231-239.
38. Cunin G, Boissonnet H, Petite H, Blanchat C, Guillemenin G. Experimental vertebroplasty using osteoconductive granular material. Spine 2000;25:1070-1076.
39. Key J. The effect of local calcium depot on osteogenesis and healing of fractures. J Bone Joint Surg Am 1934;16-A:176-184.
40. Toombs JP, Wallace LJ, Bjorling DE, Rowland G. Evaluation of Key's hypothesis in the feline tibia: An experimental model for augmented bone healing studies. Am J Vet Res 1985;46:513-518.
41. Wippermann BW, Zwipp H, Saemann T, Tscherne H. 40th Annual Meeting, Orthopaedic Research Society, New Orleans, LA, February 21-24, 1994:545.
42. Aron DN, Toombs JP, Hollingsworth SC. Primary treatment of severe fractures by external skeletal fixation: Threaded pins compared with smooth pins. J Am Anim Hosp Assoc 1986;22;659-670.
43. Johnson KD, August A, Sciadini MF, Smith C. Evaluation of ground cortical autograft as a bone graft material in a new canine bilateral segmental long bone defect model. J Orthop Trauma 1996;10: 28-36.
44. Wolff D, Goldberg VM, Stevenson S. Histomorphometric analysis of the repair of a segmental diaphyseal defect with ceramic and titanium fibermetal implants: Effects of bone marrow. J Orthop Res 1994;12:439-446.
45. Einhorn TA, Lane JM, Burstein AH, Kopman CR, Vigorita VJ. The healing of segmental bone defects induced by demineralized bone matrix. J Bone Joint Surg Am 1984;66-A:274-279.
46. Bolander ME, Balian G. The use of demineralized bone matrix in repair of segmental defects: Augmentation with extracted matrix proteins and a comparison with autologous grafts. J Bone Joint Surg Am 1986;68-A:1264-1274.
47. Tuli SM, Singh AD. The osteoinductive property of decalcified bone matrix. J Bone Joint Surg Br 1978;60-B:116-123.
48. Perka C, Schultz O, Spitzer RS, Lindenhayn K, Burmester GR. Segmental bone repair by tissue-engineered periosteal transplants with bioresorbable fleece and fibrin scaffolds in rabbits. Biomaterials 2000;21:1145-1153.
49. Louisia S. 40 (Paris VII, Paris, 1994).
50. Wittbjer J, Palmer B, Rohlin M, Thorngren KG. Osteogenic activity in composite grafts of demineralized compact bone and marrow. Clin Orthop Relat Res 1983;173:229-238.
51. Kitsugi T, Yamamuro T, Kokubo A. Bonding behaviour of a glass ceramic containing apatite and wallatsonite in segmental replacement of the rabbit tibia under load-bearing condition. J Bone Joint Surg Am 1989;71-A:264-272.
52. Cong Z, Jianxin W, Huaizhi F, Bing L, Xingdong Z. Repairing segmental bone defects with living porous ceramic cylinders: An experimental study in the dog femora. J Biomed Mater Res 2000;55:28-32.
53. Bruder SP, Kraus KH, Golberg VM. The effect of implants loaded with autologous mesenchymal stem cells on the healing of canine segmental bone defects. J Bone Joint Surg Am 1998;80-A: 985-996.
54. Johnson AL, Stein LE, Roe SC. Evaluation of collagen as a retainer for autogenous cancellous bone used in repair of full thickness cortical bone defects. Vet Surg 1987;16:146-150.
55. Johnson EE, Urist MR, Schmalzried TP, Chotivichit A, Huang HK, Finerman AM. Autogeneic cancellous bone grafts in extensive segmental ulnar defects in dogs. Clin Orthop Relat Res 1989;243: 254-265.
56. Gao TJ. In: Wilson J, Hench L, Greenspan D, Eds. Bioceramics, Vol. 8. New York: Elsevier Science, 1995:199-204.
57. Muir P, Johnson KA. Tibial intercalary allograft incorporation: Comparison of fixation with locked intramedullary nail and dynamic compression plate. J Orthop Res 1995;13:132-137.
58. Viateau VT, Reviron T, Meunier A, Guillemin N, Petite H, Sedel L. 8th Annual Scientific Meeting of the European College of Veterinary Surgeons, Brugge, Belgium, 1999:118.
59. Meinig RP, Buesing CM, Helm J, Gogolewski S. Regeneration of diaphyseal bone defects using resorbable poly(L/DL-lactide) and poly(D-lactide) membranes in the Yucatan pig model. J Orthop Trauma 1997;11:551-558.
60. Sendowski JCP, Bazan JF, Grimaldi JF, Merrien YL, Martin DF. 21 Services Vétérinaires des Armées, D.M., No. 307, DEF, DCSSA, AST, 1986.
61. Cook SD, Wolfe MW, Salked SL, Rueger DC. Recombinant human osteogenic protein 1 heals segmental defects in non-human primates. J Bone Joint Surg Am 1995;77-A:734-735.
62. Andersson G, Gaechter A, Galante J, Rostoker W. Segmental replacement of long bones in baboons using a fiber titanium implant. J Bone Joint Surg Am 1978;60-A:31-40.
63. Andersson G, Lereim P, Galante J, Rostoker W. Segmental replacement of long bones in baboons with fiber metal implants and autologous bone grafts of different particle size. Acta Orthop Scand 1982;53:349-354.
64. Werntz JR, Lane J, Klein C, Decarlo E. The osteogenic potential of bone marrow to heal segmental long bone defects. Proc 33rd Annu Meeting Orthop Res Soc 1987:441.
65. Dahners LE. Proc 34th Annu Meeting Orthop Res Soc 1988;390:3901988.
66. OG. 27 (Paris VII, 1996).
67. Toombs JP, Wallace LJ. Evaluation of autogeneic and allogeneic cortical chip grafting in a feline tibial nonunion model. Am J Vet Res 1985;46:519-528.
68. Ehrnberg A, De Pablos J, Martinez-Lotti G, Kreicbergs A. Comparison of demineralized allogeneic bone matrix grafting (the Urist procedure) and the Ilizarov procedure in large diaphyseal defects in sheep. J Orthop Res 1993;11:438-447.
69. Gehrart TN, Kirker-Head CA, Kriz MJ, Holtrop ME, Hennig GE, Hipp J, Schielling SH, Wang E. Healing segmental femoral defects in sheep using recombinant human bone morphogenetic protein. Clin Orthop Relat Res 1993;293:317-326.
70. Den Boer FC, Patka P, Bakker FC, Wippermann BW, Van Lingen A, Vink GQ, Boshuizen K, Haarman HJ. New segmental long bone defect model in sheep: Quantitative analysis of healing with dual energy x-ray absorptiometry. J Orthop Res 1999;17:654-660.
71. Mastrogiacomo M, et al. Reconstruction of extensive long bone defects in sheep using resorbable bioceramics based on silicon stabilized tricalcium phosphate. Tissue Eng 2006;12:1261-1273.
72. Khan SN, Lane JM. Spinal fusion surgery: Animal models for tissue-engineered bone constructs. Biomaterials 2004;25:1475-1485.
73. Louis-Ugbo J, Boden S. In: Bono CM, Garfin SR, Tornetta P, Einhorn TA, Eds. Spine. Philadelphia, PA: Lippincott Williams & Wilkins, 2004:343.
74. Cook SD, et al. In vivo evaluation of anterior cervical fusions with hydroxylapatite graft material. Spine 1994;19:1856-1866.
75. Kandziora F, et al. [Experimental fusion of the sheep cervical spine. Part I: Effect of cage design on interbody fusion]. Chirurg 2002;73:909-917.
76. Zdeblick TA, Cooke ME, Wilson D, Kunz DN, McCabe R. Anterior cervical discectomy, fusion, and plating. A comparative animal study. Spine 1993;18:1974-1983.
77. Zdeblick TA, et al. Cervical interbody fusion cages. An animal model with and without bone morphogenetic protein. Spine 1998;23:758-765; discussion 766.
78. Toth JM, et al. Evaluation of porous biphasic calcium phosphate ceramics for anterior cervical interbody fusion in a caprine model. Spine 1995;20:2203-2210.
79. Huang RC, et al. Alendronate inhibits spine fusion in a rat model. Spine 2005;30:2516-2522.
80. Boden SD, Schimandle JH, Hutton WC. An experimental lumbar intertransverse process spinal fusion model. Radiographic, histologic, and biomechanical healing characteristics. Spine 1995;20:412-420.
81. Sandhu HS, et al. Evaluation of rhBMP-2 with an OPLA carrier in a canine posterolateral (transverse process) spinal fusion model. Spine 1995;20:2669-2682.
82. Xue Q, et al. The influence of alendronate treatment and bone graft volume on posterior lateral spine fusion in a porcine model. Spine 2005;30:1116-1121.
83. Baramki HG, Steffen T, Lander P, Chang M, Marchesi D. The effi-cacy of interconnected porous hydroxyapatite in achieving posterolateral lumbar fusion in sheep. Spine 2000;25:1053-1060.
84. Barnes B, et al. Lower dose of rhBMP-2 achieves spine fusion when combined with an osteoconductive bulking agent in non-human primates. Spine 2005;30:1127-1133.
85. Kai T, Shao-qing G, Geng-ting D. In vivo evaluation of bone marrow stromal-derived osteoblasts-porous calcium phosphate ceramic composites as bone graft substitute for lumbar intervertebral spinal fusion. Spine 2003;28:1653-1658.
86. Sandhu HS, et al. Distractive properties of a threaded interbody fusion device. An in vivo model. Spine 1996;21:1201-1210.
87. Sandhu HS, Khan SN. Animal models for preclinical assessment of bone morphogenetic proteins in the spine. Spine 2002;27:S32-38.
88. Boden SD, Martin GJ Jr, Horton WC, Truss TL, Sandhu HS. Laparoscopic anterior spinal arthrodesis with rhBMP-2 in a titanium interbody threaded cage. J Spinal Disord 1998;11:95-101.
89. Hecht BP, et al. The use of recombinant human bone morphogenetic protein 2 (rhBMP-2) to promote spinal fusion in a nonhuman primate anterior interbody fusion model. Spine 1999;24:629-636.
90. Wang T, Dang G, Guo Z, Yang M. Evaluation of autologous bone marrow mesenchymal stem cell-calcium phosphate ceramic composite for lumbar fusion in rhesus monkey interbody fusion model. Tissue Eng 2005;11:1159-1167.
91. Schimandle JH, Boden SD. The use of animal models to study spinal fusion. Spine 1994;19:1998-2006.
92. Alden TD, et al. Percutaneous spinal fusion using bone morphogenetic protein-2 gene therapy. J Neurosurg 1999;90:109-114.
93. Boden SD. Biology of lumbar spine fusion and use of bone graft substitutes: Present, future, and next generation. Tissue Eng 2000;6:383-399.
94. Frenkel SR, Moskovich R, Spivak J, Zhang ZH, Prewett AB. Demineralized bone matrix. Enhancement of spinal fusion. Spine 1993;18:1634-1639.
95. Rubino F, et al. Minimally invasive spine surgery: An animal model for endoscopic approach to the anterior cervical and upper thoracic spine. J Laparoendosc Adv Surg Tech A 2000;10:309-313.
96. Cunningham BW, et al. Osteogenic protein versus autologous interbody arthrodesis in the sheep thoracic spine. A comparative endoscopic study using the Bagby and Kuslich interbody fusion device. Spine 1999;24:509-518.
97. Pintar FA, et al. Fusion rate and biomechanical stiffness of hydroxylapatite versus autogenous bone grafts for anterior discectomy. An in vivo animal study. Spine 1994;19:2524-2528.
98. Sidhu KS, et al. Anterior cervical interbody fusion with rhBMP-2 and tantalum in a goat model. Spine J 2001;1:331-340.
99. Genant HK, Jiang Y. Advanced imaging assessment of bone quality. Ann NY Acad Sci 2006;1068:410-428.
100. Parfitt AM, et al. Bone histomorphometry: Standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 1987;2: 595-610.
101. Gerstenfeld LC, Wronski TJ, Hollinger JO, Einhorn TA. Application of histomorphometric methods to the study of bone repair. J Bone Miner Res 2005;20:1715-1722.
102. Athanasiou KA, Zhu C, Lanctot DR, Agrawal CM, Wang X. Fundamentals of biomechanics in tissue engineering of bone. Tissue Eng 2000;6:361-381.
103. Turner CH, Burr DB. Basic biomechanical measurements of bone: A tutorial. Bone 1993;14:595-608.
104. Weiss S, Zimmerman MC, Harten RD, Alberta FG, Meunier A. The acoustic and structural properties of the human femur. J Biomech Eng 1998;120:71-76.