Advances in the establishment of defined mouse models for the study of fracture healing and bone regeneration

Journal of Orthopaedic Trauma

Volumn 23, Issue SUPPL. 5, 2009, Pages

  Holstein, J H ^a   Garcia, P ^a   Histing, T ^a   Kristen, A ^a   Scheuer, C ^a   Menger, M D ^a   Pohlemann, T ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

Animal model; Bone repair; Fracture stabilization; Mice

Indexed keywords

BONE RADIOGRAPHY; BONE REGENERATION; BONE SCREW; CHEMICAL ANALYSIS; DISEASE MODEL; EXTERNAL FIXATOR; FEMUR; FRACTURE HEALING; GAIT; GENE TARGETING; IMPLANT; INTERLOCKING NAIL; INTRAMEDULLARY NAILING; METABOLIC BONE DISEASE; MOLECULAR MECHANICS; MORPHOMETRICS; MOUSE STRAIN; NICK END LABELING; NONHUMAN; OSTEOPOROSIS; OSTEOSYNTHESIS; OSTEOTOMY; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; REVIEW; SOFT TISSUE INJURY; TIBIA; TREADMILL; WESTERN BLOTTING; ANIMAL; FEMUR FRACTURE; HUMAN; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BONE REGENERATION; DISEASE MODELS, ANIMAL; FEMORAL FRACTURES; FRACTURE HEALING; HUMANS; MICE;

EID: 67649664210     PISSN: 08905339     EISSN: None     Source Type: Journal    
DOI: 10.1097/BOT.0b013e31819f27e5     Document Type: Review

References (70)

1. Nunamaker DM. Experimental models of fracture repair. Clin Orthop Relat Res. 1998;355:S56-S65.
2. Ashhurst DE, Hogg J, Perren SM. A method for making reproducible experimental fractures of the rabbit tibia. Injury. 1982;14:236-242.
3. Bonnarens F, Einhorn TA. Production of a standard closed fracture in laboratory animal bone. J Orthop Res. 1984;2:97-101.
4. Cheal EJ, Mansmann KA, DiGioia AM, et al. Role of interfragmentary strain in fracture healing: ovine model of a healing osteotomy. J Orthop Res. 1991;9:131-142.
5. Davy DT, Connolly JF. The biomechanical behavior of healing canine radii and ribs. J Biomech. 1982;15:235-247.
6. Hiltunen A, Vuorio E, Aro HT. A standardized experimental fracture in the mouse tibia. J Orthop Res. 1993;11:305-312.
7. Nunamaker DM, Richardson DW, Butterveck DM, et al. A new external skeletal fixation device that allows immediate full weightbearing: application in the horse. Vet Surg. 1986;15:1345-1355.
8. Toombs JP,Wallace LJ, Bjorling DE, et al. 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.
9. Jacenko O, Olsen BR. Transgenic mouse models in studies of skeletal disorders. J Rheumatol Suppl. 1995;43:39-41.
10. Houdebine LM. Transgenic animal models in biomedical research. Methods Mol Biol. 2007;360:163-202.
11. Silver LM. Mouse Genetics. New York, NY: Oxford University Press; 1995.
12. Lu C, Miclau T, Hu D, et al. Cellular basis for age-related changes in fracture repair. J Orthop Res. 2005;23:1300-1307.
13. Kilborn SH, Trudel G, Uhthoff H. Review of growth plate closure compared with age at sexual maturity and lifespan in laboratory animals. Contemp Top Lab Anim Sci. 2002;41:21-26.
14. Manigrasso MB, O'Connor JP. Characterization of a closed femur fracture model in mice. J Orthop Trauma. 2004;18:687-695.
15. Gazit D, Turgeman G, Kelley P, et al. Engineered pluripotent mesenchymal cells integrate and differentiate in regenerating bone: a novel cell-mediated gene therapy. J Gene Med. 1999;1: 121-133.
16. Meinel L, Fajardo R, Hofmann S, et al. Silk implants for the healing of critical size bone defects. Bone. 2005;37:688-698.
17. Nakase T, Nomura S, Yoshikawa H, et al. Transient and localized expression of bone morphogenetic protein 4 messenger RNA during fracture healing. J Bone Miner Res. 1994;9:651-659.
18. Paccione MF, Warren SM, Spector JA, et al. A mouse model of mandibular osteotomy healing. J Craniofac Surg. 2001;12:444-450.
19. Stone CA. Unravelling the secrets of foetal wound healing: an insight into fracture repair in the mouse foetus and perspectives for clinical application. Br J Plast Surg. 2000;53:337-341.
20. Zilberman Y, Kallai I, Gafni Y, et al. Fluorescence molecular tomography enables in vivo visualization and quantification of nonunion fracture repair induced by genetically engineered mesenchymal stem cells. J Orthop Res. 2008;26:522-530.
21. Cheung KM, Kaluarachi K, Andrew G, et al. An externally fixed femoral fracture model for mice. J Orthop Res. 2003;21:685-690.
22. Garcia P, Holstein JH, Histing T, et al. A new technique for internal fixation of femoral fractures in mice: impact of stability on fracture healing. J Biomech. 2008;41:1689-1696.
23. Bhandari M, Schemitsch EH. Bone formation following intramedullary femoral reaming is decreased by indomethacin and antibodies to insulinlike growth factors. J Orthop Trauma. 2002;16:717-722.
24. Street J, Bao M, deGuzman L, et al. Vascular endothelial growth factor stimulates bone repair by promoting angiogenesis and bone turnover. Proc Natl Acad Sci U S A. 2002;99:9656-9661.
25. Colnot C, Thompson Z, Miclau T, et al. Altered fracture repair in the absence of MMP9. Development. 2003;130:4123-4133.
26. Le AX, Miclau T, Hu D, et al. Molecular aspects of healing in stabilized and non-stabilized fractures. J Orthop Res. 2001;19:78-84.
27. Opolka A, Ratzinger S, Schubert T, et al. Collagen IX is indispensable for timely maturation of cartilage during fracture repair in mice. Matrix Biol. 2007;26:85-95.
28. Augat P, Burger J, Schorlemmer S, et al. Shear movement at the fracture site delays healing in a diaphyseal fracture model. J Orthop Res. 2003;21: 1011-1017.
29. Augat P, Simon U, Liedert A, et al. Mechanics and mechano-biology of fracture healing in normal and osteoporotic bone. Osteoporos Int. 2005; 16:S36-S43.
30. Claes L, Eckert-Hübner K, Augat P. The effect of mechanical stability on local vascularization and tissue differentiation in callus healing. J Orthop Res. 2002;20:1099-1105.
31. Schell H, Epari DR, Kassi JP, et al. The course of bone healing is influenced by the initial shear fixation stability. J Orthop Res. 2005;23: 1022-1028.
32. Lienau J, Schell H, Epari DR, et al. CYR61 (CCN1) protein expression during fracture healing in an ovine tibial model and its relation to the mechanical fixation stability. J Orthop Res. 2006;24:254-262.
33. Lienau J, Schell H, Duda GN, et al. Initial vascularization and tissue differentiation are influenced by fixation stability. J Orthop Res. 2005;23: 639-645.
34. Nomura S, Takano-Yamamoto T. Molecular events caused by mechanical stress in bone. Matrix Biol. 2000;19:91-96.
35. Auer JA, Goodship A, Arnoczky S, et al. Refining animal models in fracture research: seeking consensus in optimising both animal welfare and scientific validity for appropriate biomedical use. BMC Musculoskelet Disord. 2007;8:72.
36. Holstein JH, Menger MD, Culemann U, et al. Development of a locking femur nail for mice. J Biomech. 2007;40:215-219.
37. Holstein JH, Matthys R, Histing T, et al. Development of a stable closed femoral fracture model in mice. J Surg Res. March 24, 2008 [Epub ahead of print].
38. Matthys R, Perren SM. Internal fixation systems for improved genetic and biomechanical studies in mice. Presented at: 54th Annual Meeting of the Orthopaedic Research Society; March 2-5, 2008; San Francisco, CA. Poster No. 1005.
39. Garcia P, Holstein JH, Maier S, et al. Development of a reliable non-union model in mice. J Surg Res. 2008;147:84-91.
40. Gröngröft ID, Heil P, Matthys-Mark R, et al. Fixation compliance in a murine fracture model induces two different processes of fracture healing but does not lead to delayed union. Paper presented at: 6th Combined Meeting of the Orthopaedic Research Societies; October 20-24, 2007; Honolulu, HI. Paper No. 138.
41. Egermann M, Goldhahn J, Schneider E. Animal models for fracture treatment in osteoporosis. Osteoporos Int. 2005;16:S129-S138.
42. Clarke KA, Still J. Development and consistency of gait in the mouse. Physiol Behav. 2001;73:159-164.
43. Lee SW, Padmanabhan P, Ray P, et al. Stem cell-mediated accelerated bone healing observed with in vivo molecular and small animal imaging technologies in a model of skeletal injury. J Orthop Res. 2009;27:295-302.
44. Zachos TA, Bertone AL,Wassenaar PA, et al. Rodent models for the study of articular fracture healing. J Invest Surg. 2007;20:87-95.
45. Mayer-Kuckuk P, Boskey AL. Molecular imaging promotes progress in orthopedic research. Bone. 2006;39:965-977.
46. Holstein JH, Menger MD, Scheuer C, et al. Erythropoietin (EPO): EPOreceptor signaling improves early endochondral ossification and mechanical strength in fracture healing. Life Sci. 2007;80:893-900.
47. Cano J, Campo J, Vaquero JJ, et al. High resolution image in bone biology I. Review of the literature. Med Oral Patol Oral Cir Bucal. 2007;12: E454-E458.
48. Cano J, Campo J, Vaquero JJ, et al. High resolution image in bone biology II. Reviewof the literature. Med Oral Patol Oral Cir Bucal. 2008;13:E31-E35.
49. Yang X, Ricciardi BF, Hernandez-Soria A, et al. Callus mineralization and maturation are delayed during fracture healing in interleukin-6 knockout mice. Bone. 2007;41:928-936.
50. Duvall CL, Taylor WR,Weiss D, et al. Impaired angiogenesis, early callus formation, and late stage remodeling in fracture healing of osteopontindeficient mice. J Bone Miner Res. 2007;22:286-297.
51. Gerstenfeld LC, Wronski TJ, Hollinger JO, et al. Application of histomorphometric methods to the study of bone repair. J Bone Miner Res. 2005;20:1715-1722.
52. Parfitt AM, Drezner MK, Glorieux FH, 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.
53. Holstein JH, Klein M, Garcia P, et al. Rapamycin affects early fracture healing in mice. Br J Pharmacol. 2008;154:1055-1062.
54. Donath K, Breuner G. A method for the study of undecalcified bones and teeth with attached soft tissues. The Säge-Schliff (sawing and grinding) technique. J Oral Pathol. 1982;11:318-326.
55. Murnaghan M, McIlmurray L, Mushipe MT, et al. Time for treating bone fracture using rhBMP-2: a randomised placebo controlled mouse fracture trial. J Orthop Res. 2005;23:625-631.
56. Toyosawa S, Kanatani N, Shintani S, et al. Expression of dentin matrix protein 1 (DMP1) during fracture healing. Bone. 2004;35:553-561.
57. Uusitalo H, Hiltunen A, Söderström M, et al. Expression of cathepsins B, H, K, L, and S and matrix metalloproteinases 9 and 13 during chondrocyte hypertrophy and endochondral ossification in mouse fracture callus. Calcif Tissue Int. 2000;67:382-390.
58. Matsumoto T, Mifune Y, Kawamoto A, et al. Fracture induced mobilization and incorporation of bone marrow-derived endothelial progenitor cells for bone healing. J Cell Physiol. 2008;215:234-242.
59. Lee FYH, Choi YW, Behrens FF, et al. Programmed removal of chondrocytes during endochondral fracture healing. J Orthop Res. 1998; 16:144-150.
60. Miller BS, Bronk JT, Nishiyama T, et al. Pregnancy associated plasma protein-A is necessary for expeditious fracture healing in mice. J Endocrinol. 2007;192:505-513.
61. Carter DR, Beaupré GS, Giori NJ, et al. Mechanobiology of skeletal regeneration. Clin Orthop Relat Res. 1998;35:S41-S55.
62. Buckwalter JA, Grodzinsky AJ. Loading of healing bone, fibrous tissue, and muscle: implications for orthopaedic practice. J Am Acad Orthop Surg. 1999;7:291-299.
63. Kershaw CJ, Cunningham JL, Kenwright J. Tibial external fixation, weight bearing, and fracture movement. Clin Orthop Relat Res. 1993;293: 28-36.
64. Sarmiento A, Schaeffer JF, Beckerman L, et al. Fracture healing in rat femora as affected by functional weight-bearing. J Bone Joint Surg Am. 1977;59:369-375.
65. Seebeck P, Thompson MS, Parwani A, et al. Gait evaluation: a tool to monitor bone healing? Clin Biomech. 2005;20:883-891.
66. Heglund NC, Taylor CR, McMahon TA. Scaling stride frequency and gait to animal size: mice to horses. Science. 1974;186:1112-1113.
67. Clarke KA, Still J. Gait analysis in the mouse. Physiol Behav. 1999;66: 723-729.
68. Herbin M, Gasc JP, Renous S. Symmetrical and asymmetrical gaits in the mouse: patterns to increase velocity. J Comp Physiol A Neuroethol Sens Neural Behav Physiol. 2004;190:895-906.
69. Costa AC, Walsh K, Davisson MT. Motor dysfunction in a mouse model for Down syndrome. Physiol Behav. 1999;68:211-220.
70. Williams JM, Zurawski J, Mikecz K, et al. Functional assessment of joint use in experimental inflammatory murine arthritis. J Orthop Res. 1993;11: 172-180.