The importance of the intracortical canal network for murine bone mechanics

Bone

Volumn 53, Issue 1, 2013, Pages 120-128

  Schneider, Philipp ^a   Voide, Romain ^a   Stampanoni, Marco ^a,b   Donahue, Leah Rae ^c   Müller, Ralph ^a  

^a ETH ZURICH   (Switzerland)

^b PAUL SCHERRER INSTITUTE   (Switzerland)

^c JACKSON LABORATORY   (United States)

Author keywords

CT; Biomechanics; Canal network; Cortical bone; Synchrotron radiation; Ultimate force; Work to fracture

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOMECHANICS; BONE MASS; BONE STRUCTURE; BONE TISSUE; CONTROLLED STUDY; CORTICAL BONE; FEMUR; INTRACORTICAL CANAL NETWORK; MICRO-COMPUTED TOMOGRAPHY; MORPHOMETRICS; MOUSE; NONHUMAN; POROSITY; SYNCHROTRON RADIATION; TRABECULAR BONE;

ANIMALS; BIOMECHANICS; BONE AND BONES; MICE; MICE, INBRED C57BL; REGRESSION ANALYSIS;

EID: 84871826148     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2012.11.024     Document Type: Article

References (80)

1. Evans F.G., Bang S. Differences and relationships between the physical properties and the microscopic structure of human femoral, tibial and fibular cortical bone. Am J Anat 1967, 120:79-88.
2. Evans F.G., Vincentelli R. Relations of the compressive properties of human cortical bone to histological structure and calcification. J Biomech 1974, 7:1-10.
3. Saha S., Hayes W.C. Relations between tensile impact properties and microstructure of compact bone. Calcif Tissue Res 1977, 24:65-72.
4. Currey J.D. Changes in the impact energy absorption of bone with age. J Biomech 1979, 12:459-469.
5. Dickenson R.P., Hutton W.C., Stott J.R. The mechanical properties of bone in osteoporosis. J Bone Joint Surg Br 1981, 63-B:233-238.
6. Vincentelli R., Grigorov M. The effect of Haversian remodeling on the tensile properties of human cortical bone. J Biomech 1985, 18:201-207.
7. Rho J.Y., Zioupos P., Currey J.D., Pharr G.M. Microstructural elasticity and regional heterogeneity in human femoral bone of various ages examined by nano-indentation. J Biomech 2002, 35:189-198.
8. Wachter N.J., Augat P., Krischak G.D., Sarkar M.R., Mentzel M., Kinzl L., et al. Prediction of strength of cortical bone in vitro by microcomputed tomography. Clin Biomech 2001, 16:252-256.
9. Wachter N.J., Krischak G.D., Mentzel M., Sarkar M.R., Ebinger T., Kinzl L., et al. Correlation of bone mineral density with strength and microstructural parameters of cortical bone in vitro. Bone 2002, 31:90-95.
10. Currey J.D. The effect of porosity and mineral content on the Young's modulus of elasticity of compact bone. J Biomech 1988, 21:131-139.
11. Schaffler M.B., Burr D.B. Stiffness of compact bone: effects of porosity and density. J Biomech 1988, 21:13-16.
12. Martin R.B., Ishida J. The relative effects of collagen fiber orientation, porosity, density, and mineralization on bone strength. J Biomech 1989, 22:419-426.
13. Martin R.B., Boardman D.L. The effects of collagen fiber orientation, porosity, density, and mineralization on bovine cortical bone bending properties. J Biomech 1993, 26:1047-1054.
14. Barth R.W., Williams J.L., Kaplan F.S. Osteon morphometry in females with femoral neck fractures. Clin Orthop Relat Res 1992, 283:178-186.
15. Squillante R.G., Williams J.L. Videodensitometry of osteons in females with femoral neck fractures. Calcif Tissue Int 1993, 52:273-277.
16. Bell K.L., Loveridge N., Power J., Garrahan N., Meggitt B.F., Reeve J. Regional differences in cortical porosity in the fractured femoral neck. Bone 1999, 24:57-64.
17. Boyce T.M., Bloebaum R.D. Cortical aging differences and fracture implications for the human femoral neck. Bone 1993, 14:769-778.
18. Brockstedt H., Kassem M., Eriksen E.F., Mosekilde L., Melsen F. Age- and sex-related changes in iliac cortical bone mass and remodeling. Bone 1993, 14:681-691.
19. Stein M.S., Feik S.A., Thomas C.D., Clement J.G., Wark J.D. An automated analysis of intracortical porosity in human femoral bone across age. J Bone Miner Res 1999, 14:624-632.
20. Chai B., Tang X., Li H. Osteoclastic resorption of Haversian systems in cortical bone of femoral neck in aged women. A scanning electron microscopic study. Chin Med J (Engl) 1996, 109:705-710.
21. Bousson V., Meunier A., Bergot C., Vicaut E., Rocha M.A., Morais M.H., et al. Distribution of intracortical porosity in human midfemoral cortex by age and gender. J Bone Miner Res 2001, 16:1308-1317.
22. Ural A., Vashishth D. Interactions between microstructural and geometrical adaptation in human cortical bone. J Orthop Res 2006, 24:1489-1498.
23. Cooper D.M., Thomas C.D., Clement J.G., Turinsky A.L., Sensen C.W., Hallgrimsson B. Age-dependent change in the 3D structure of cortical porosity at the human femoral midshaft. Bone 2007, 40:957-965.
24. Burghardt A.J., Kazakia G.J., Ramachandran S., Link T.M., Majumdar S. Age- and gender-related differences in the geometric properties and biomechanical significance of intracortical porosity in the distal radius and tibia. J Bone Miner Res 2010, 25:983-993.
25. Busse B., Hahn M., Schinke T., Puschel K., Duda G.N., Amling M. Reorganization of the femoral cortex due to age-, sex-, and endoprosthetic-related effects emphasized by osteonal dimensions and remodeling. J Biomed Mater Res A 2010, 92A:1440-1451.
26. Nishiyama K.K., Macdonald H.M., Buie H.R., Hanley D.A., Boyd S.K. Postmenopausal women with osteopenia have higher cortical porosity and thinner cortices at the distal radius and tibia than women with normal aBMD: an in vivo HR-pQCT study. J Bone Miner Res 2010, 25:882-890.
27. Zebaze R.M.D., Ghasem-Zadeh A., Bohte A., Iuliano-Burns S., Mirams M., Price R.I., et al. Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet 2010, 375:1729-1736.
28. Macdonald H.M., Nishiyama K.K., Kang J.A., Hanley D.A., Boyd S.K. Age-related patterns of trabecular and cortical bone loss differ between sexes and skeletal sites: a population-based HR-pQCT study. J Bone Miner Res 2011, 26:50-62.
29. McCalden R.W., McGeough J.A., Barker M.B., Courtbrown C.M. Age-related changes in the tensile properties of cortical bone. The relative importance of changes in porosity, mineralization, and microstructure. J Bone Joint Surg Am 1993, 75:1193-1205.
30. Nishihara A. Femoral neck and iliac bone histomorphometry in femoral neck fracture. Nippon Seikeigeka Gakkai Zasshi 1995, 69:156-167.
31. Yeni Y.N., Brown C.U., Wang Z., Norman T.L. The influence of bone morphology on fracture toughness of the human femur and tibia. Bone 1997, 21:453-459.
32. Bell K.L., Loveridge N., Jordan G.R., Power J., Constant C.R., Reeve J. A novel mechanism for induction of increased cortical porosity in cases of intracapsular hip fracture. Bone 2000, 27:297-304.
33. Jordan G.R., Loveridge N., Bell K.L., Power J., Rushton N., Reeve J. Spatial clustering of remodeling osteons in the femoral neck cortex: a cause of weakness in hip fracture?. Bone 2000, 26:305-313.
34. Turner C.H. Biomechanics of bone: determinants of skeletal fragility and bone quality. Osteoporos Int 2002, 13:97-104.
35. Ural A., Vashishth D. Effects of intracortical porosity on fracture toughness in aging human bone: a mu CT-based cohesive finite element study. J Biomech Eng-Trans ASME 2007, 129:625-631.
36. Ostertag A., Cohen-Solal M., Audran M., Legrand E., Marty C., Chappard D., et al. Vertebral fractures are associated with increased cortical porosity in iliac crest bone biopsy of men with idiopathic osteoporosis. Bone 2009, 44:413-417.
37. Burr D.B. Cortical bone: a target for fracture prevention?. Lancet 2010, 375:1672-1673.
38. Boutroy S., Bouxsein M.L., Munoz F., Delmas P.D. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab 2005, 90:6508-6515.
39. Kirmani S., Christen D., van Lenthe G.H., Fischer P.R., Bouxsein M.L., McCready L.K., et al. Bone structure at the distal radius during adolescent growth. J Bone Miner Res 2009, 24:1033-1042.
40. MacNeil J.A., Boyd S.K. Accuracy of high-resolution peripheral quantitative computed tomography for measurement of bone quality. Med Eng Phys 2007, 29:1096-1105.
41. Burghardt A.J., Buie H.R., Laib A., Majumdar S., Boyd S.K. Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone 2010, 47:519-528.
42. Liu X.S., Zhang X.H., Sekhon K.K., Adams M.F., McMahon D.J., Bilezikian J.P., et al. High-resolution peripheral quantitative computed tomography can assess microstructural and mechanical properties of human distal tibial bone. J Bone Miner Res 2010, 25:746-756.
43. Nishiyama K.K., Macdonald H.M., Moore S.A., Fung T., Boyd S.K., McKay H.A. Cortical porosity is higher in boys compared with girls at the distal radius and distal tibia during pubertal growth: an HR-pQCT study. J Bone Miner Res 2012, 27:273-282.
44. Burghardt A.J., Kazakia G.J., Sode M., de Papp A.E., Link T.M., Majumdar S. A longitudinal HR-pQCT study of alendronate treatment in postmenopausal women with low bone density: relations among density, cortical and trabecular microarchitecture, biomechanics, and bone turnover. J Bone Miner Res 2010, 25:2282-2295.
45. Schneider P., Stauber M., Voide R., Stampanoni M., Donahue L.R., Müller R. Ultrastructural properties in cortical bone vary greatly in two inbred strains of mice as assessed by synchrotron light based micro- and nano-CT. J Bone Miner Res 2007, 22:1557-1570.
46. Wachter N.J., Augat P., Krischak G.D., Mentzel M., Kinzl L., Claes L. Prediction of cortical bone porosity in vitro by microcomputed tomography. Calcif Tissue Int 2001, 68:38-42.
47. Cooper D.M., Turinsky A.L., Sensen C.W., Hallgrimsson B. Quantitative 3D analysis of the canal network in cortical bone by micro-computed tomography. Anat Rec B New Anat 2003, 274:169-179.
48. Bousson V., Peyrin F., Bergot C., Hausard M., Sautet A., Laredo J.D. Cortical bone in the human femoral neck: three-dimensional appearance and porosity using synchrotron radiation. J Bone Miner Res 2004, 19:794-801.
49. Jones A.C., Sheppard A.P., Sok R.M., Arns C.H., Limaye A., Averdunk H., et al. Three-dimensional analysis of cortical bone structure using X-ray micro-computed tomography. Phys A 2004, 339:125-130.
50. Donahue L.R., Guido V.E., Rosen C.J., Horton L.G., Ackert-Bicknell C.L., Bouxsein M.L., et al. GH/IGF-I independent genetic effects on BMD and skeletal morphology are both gender dependent and independent. J Bone Miner Res 2003, 18:S123.
51. Flurkey K., Papaconstantinou J., Miller R.A., Harrison D.E. Lifespan extension and delayed immune and collagen aging in mutant mice with defects in growth hormone production. Proc Natl Acad Sci U S A 2001, 98:6736-6741.
52. Sharma Y., Flurkey K., Astle C.M., Harrison D.E. Mice severely deficient in growth hormone have normal hematopoiesis. Exp Hematol 2005, 33:776-783.
53. Alexander J.M., Bab I., Fish S., Müller R., Uchiyama T., Gronowicz G., et al. Human parathyroid hormone 1-34 reverses bone loss in ovariectomized mice. J Bone Miner Res 2001, 16:1665-1673.
54. Bouxsein M.L., Boyd S.K., Christiansen B.A., Guldberg R.E., Jepsen K.J., Müller R. Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res 2010, 25:1468-1486.
55. Hildebrand T., Rüegsegger P. A new method for the model-independent assessment of thickness in three-dimensional images. J Microsc (Oxford) 1997, 185:67-75.
56. Stauber M., Müller R. Volumetric spatial decomposition of trabecular bone into rods and plates - a new method for local bone morphometry. Bone 2006, 38:475-484.
57. Voide R., van Lenthe G.H., Müller R. Bone morphometry strongly predicts cortical bone stiffness and strength, but not toughness, in inbred mouse models of high and low bone mass. J Bone Miner Res 2008, 23:1194-1203.
58. Turner C.H., Burr D.B. Basic biomechanical measurements of bone: a tutorial. Bone 1993, 14:595-608.
59. Marquard D.W. Generalized inverses, ridge regression, biased linear estimation, and nonlinear estimation. Technometrics 1970, 12:591-612.
60. O'Brien R.M. A caution regarding rules of thumb for variance inflation factors. Qual Quant 2007, 41:673-690.
61. Beamer W.G., Donahue L.R., Rosen C.J., Baylink D.J. Genetic variability in adult bone density among inbred strains of mice. Bone 1996, 18:397-403.
62. Turner C.H., Hsieh Y.F., Müller R., Bouxsein M.L., Baylink D.J., Rosen C.J., et al. Genetic regulation of cortical and trabecular bone strength and microstructure in inbred strains of mice. J Bone Miner Res 2000, 15:1126-1131.
63. Barth H.D., Launey M.E., Macdowell A.A., Ager J.W., Ritchie R.O. On the effect of X-ray irradiation on the deformation and fracture behavior of human cortical bone. Bone 2010, 46:1475-1485.
64. Turner C.H., Hsieh Y.F., Müller R., Bouxsein M.L., Rosen C.J., McCrann M.E., et al. Variation in bone biomechanical properties, microstructure, and density in BXH recombinant inbred mice. J Bone Miner Res 2001, 16:206-213.
65. Wergedal J.E., Sheng M.H., Ackert-Bicknell C.L., Beamer W.G., Baylink D.J. Genetic variation in femur extrinsic strength in 29 different inbred strains of mice is dependent on variations in femur cross-sectional geometry and bone density. Bone 2005, 36:111-122.
66. Ng A.H.M., Wang S.X., Turner C.H., Beamer W.G., Grynpas M.D. Bone quality and bone strength in BXH recombinant inbred mice. Calcif Tissue Int 2007, 81:215-223.
67. Voide R., van Lenthe G.H., Müller R. Differential effects of bone structural and material properties on bone competence in C57BL/6 and C3H/He inbred strains of mice. Calcif Tissue Int 2008, 83:61-69.
68. Ascenzi M.G., Roe A.K. The osteon: the micromechanical unit of compact bone. Front Biosci-Landmark 2012, 17:1551-1581.
69. Najafi A.R., Arshi A.R., Eslami M.R., Fariborz S., Moeinzadeh M.H. Micromechanics fracture in osteonal cortical bone: a study of the interactions between microcrack propagation, microstructure and the material properties. J Biomech 2007, 40:2788-2795.
70. Budyn E., Hoc T., Jonvaux J. Fracture strength assessment and aging signs detection in human cortical bone using an X-FEM multiple scale approach. Comput Mech 2008, 42:579-591.
71. Najafi A.R., Arshi A.R., Esiami M.R., Fariborz S., Moeinzadeh M. Haversian cortical bone model with many radial microcracks: an elastic analytic solution. Med Eng Phys 2007, 29:708-717.
72. Voide R., Schneider P., Stauber M., van Lenthe G.H., Stampanoni M., Müller R. The importance of murine cortical bone microstructure for microcrack initiation and propagation. Bone 2011, 49:1186-1193.
73. Thurner P.J., Erickson B., Jungmann R., Schriock Z., Weaver J.C., Fantner G.E., et al. High-speed photography of compressed human trabecular bone correlates whitening to microscopic damage. Eng Fract Mech 2007, 74:1928-1941.
74. Cooper D., Turinsky A., Sensen C., Hallgrimsson B. Effect of voxel size on 3D micro-CT analysis of cortical bone porosity. Calcif Tissue Int 2007, 80:211-219.
75. Schneider P., Voide R., Stampanoni M., Müller R. Post-processing technique for improved assessment of hard tissues in the submicrometer domain using local synchrotron radiation-based computed tomography. Biomed Tech 2009, 54:48-54.
76. Chatfield C. Model uncertainty, data mining and statistical inference. J R Stat Soc Ser A 1995, 158:419-466.
77. Anscombe F.J. Topics in the investigation of linear relations fitted by the method of least squares. J R Stat Soc Ser B Methodol 1967, 29:1-52.
78. Morgan J.A., Tatar J.F. Calculation of residual sum of squares for all possible regressions. Technometrics 1972, 14:317-325.
79. Akaike H. New look at statistical-model identification. IEEE Trans Autom Control 1974, 19:716-723.
80. Mela C.F., Kopalle P.K. The impact of collinearity on regression analysis: the asymmetric effect of negative and positive correlations. Appl Econ 2002, 34:667-677.