Fracture of bone tissue: The 'hows' and the 'whys'

Medical Engineering and Physics

Volumn 30, Issue 10, 2008, Pages 1209-1226

  Gupta, H S ^a   Zioupos, P ^b  

^a MAX PLANCK INSTITUTE OF COLLOIDS AND INTERFACES   (Germany)

^b CRANFIELD UNIVERSITY   (United Kingdom)

Author keywords

Bone; Fracture; Hierarchy; Mechanisms; Organisation; Properties; Structure

Indexed keywords

BONE; MECHANICAL PROPERTIES;

BONE FRACTURES; BONE TISSUES; HIERARCHICAL STRUCTURES; HIERARCHY; LOADING SCENARIOS; MECHANICAL BEHAVIOURS; MECHANICAL PERFORMANCES; ORGANISATION; PROPERTIES; QUALITY OF LIVES; STRUCTURE;

FRACTURE;

NANOMATERIAL;

ARTICLE; BIOPHYSICS; BONE DEFORMATION; BONE RADIOGRAPHY; BONE TISSUE; CANCELLOUS BONE; CORTICAL BONE; EXERCISE; FRACTURE; HAVERSIAN CANAL; HUMAN; PRIORITY JOURNAL; TRABECULAR BONE;

BONE AND BONES; CALCIFICATION, PHYSIOLOGIC; FRACTURES, BONE; HUMANS; MODELS, BIOLOGICAL;

EID: 56249142300     PISSN: 13504533     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.medengphy.2008.09.007     Document Type: Article

References (140)

1. Rho J.Y., Kuhn-Spearing L., and Zioupos P. Mechanical properties and the hierarchical structure of bone. Medical Engineering & Physics 20 (1998) 92-102
2. Zioupos P. Recent developments in the study of failure of solid biomaterials and bone. 'fracture' and 'pre-fracture' toughness. Materials Science & Engineering C: Biomimetic Materials, Sensors & Systems C6 (1998) 33-40
3. Piekarski K. Fractography of bone. In: Hastings G.W., and Ducheyne P. (Eds). Natural and living biomaterials (1984), CRC Press Inc., Boca Raton, FL
4. Peterlik H., Roschger P., Klaushofer K., and Fratzl P. From brittle to ductile fracture of bone. Nature Materials 5 (2006) 52-55
5. Jackson A.P., Vincent J.F.V., and Turner R.M. A physical model of nacre. Composites Science and Technology 36 (1989) 255-266
6. Wang R.Z., Wen H.B., Cui F.Z., Zhang H.B., and Li H.D. Observations of damage morphologies in nacre during deformation and fracture. Journal of Materials Science 30 (1995) 2299-2304
7. Robertson D.M., Robertson D., and Barrett C.R. Fracture toughness, critical crack length and plastic zone size in bone. Journal of Biomechanics 11 (1978) 359-364
8. Melvin J.W. Fracture mechanics of bone. Journal of Biomechanical Engineering-Transactions of the ASME 115 (1993) 549-554
9. Koester K.J., Ager J.W., and Ritchie R.O. The true toughness of human cortical bone measured with realistically short cracks. Nature Materials 7 (2008) 672-677
10. Vashishth D., Behiri J.C., Tanner K.E., and Bonfield W. Toughening mechanisms in cortical bone. 42nd Annual Meeting ORS, February 19-22. Atlanta, GA, USA. In: (1996)
11. Kruzic J.J., Scott J.A., Nalla R.K., and Ritchie R.O. Propagation of surface fatigue cracks in human cortical bone. Journal of Biomechanics 39 (2006) 968-972
12. Nalla R.K., Stolken J.S., Kinney J.H., and Ritchie R.O. Fracture in human cortical bone. Local fracture criteria and toughening mechanisms. Journal of Biomechanics 38 (2005) 1517-1525
13. Ritchie R.O., Kinney J.H., Kruzic J.J., and Nalla R.K. A fracture mechanics and mechanistic approach to the failure of cortical bone. Fatigue & Fracture of Engineering Materials & Structures 28 (2005) 345-371
14. Nalla R.K., Kruzic J.J., Kinney J.H., and Ritchie R.O. Mechanistic aspects of fracture and R-curve behavior in human cortical bone. Biomaterials 26 (2005) 217-231
15. Nalla R.K., Kruzic J.J., Kinney J.H., and Ritchie R.O. Effect of aging on the toughness of human cortical bone: evaluation by R-curves. Bone 35 (2004) 1240-1246
16. Nalla R.K., Kinney J.H., and Ritchie R.O. Mechanistic fracture criteria for the failure of human cortical bone. Nature Materials 2 (2003) 164-168
17. Zioupos P., and Currey J.D. Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone 22 (1998) 57-66
18. Hansen U., Zioupos P., Simpson R., Currey J.D., and Hynd D. The effect of strain rate on the mechanical properties of human cortical bone. Journal of Biomechanical Engineering-Transactions of the ASME 130 (2008) 011011-11018
19. Currey J.D., Brear K., and Zioupos P. The effects of ageing and changes in mineral content in degrading the toughness of human femora. Journal of Biomechanics 29 (1996) 257-260
20. Currey J.D. Tensile yield in compact bone is determined by strain, post-yield behaviour by mineral content. Journal of Biomechanics 37 (2004) 549-556
21. Currey J.D., Brear K., and Zioupos P. Notch sensitivity of mineralised tissues in impact. Proceedings of the Royal Society of London Series B-Biological Sciences 271 (2004) 517-522
22. Zioupos P., and Currey J.D. The extent of microcracking and the morphology of microcracks in damaged bone. Journal of Materials Science 29 (1994) 978-986
23. Zioupos P., Currey J.D., and Sedman A.J. An examination of the micromechanics of failure of bone and antler by acoustic-emission tests and laser-scanning-confocal-microscopy. Medical Engineering & Physics 16 (1994) 203-212
24. Zioupos P., and Currey J.D. Pre-failure toughening mechanisms in the dentine of the narwhal tusk. Microscopic examination of stress/strain induced microcracking. Journal of Materials Science Letters 15 (1996) 991-994
25. Zioupos P., Wang X.T., and Currey J.D. Experimental and theoretical quantification of the development of damage in fatigue tests of bone and antler. Journal of Biomechanics 29 (1996) 989-1002
26. Zioupos P., Currey J.D., Casinos A., and Buffrénil de V. Mechanical properties of the rostrum of the whale Mesoplodon Densirostris: a remarkably dense bony tissue. Journal of Zoology 241 (1997) 725-737
27. Weiner S., and Wagner H.D. The material bone. Structure mechanical function relations. Annual Review of Materials Science 28 (1998) 271-298
28. Carter D.R., and Hayes W. The compressive behavior of bone as a two-phase porous structure. Journal of Bone and Joint Surgery 59A (1977) 954-962
29. Gibson L.J. The mechanical behavior of cancellous bone. Journal of Biomechanics 18 (1985) 317-328
30. Enlow D.H. Principles of bone remodeling (1963), Charles C Thomas, Springfield, IL
31. Enlow D.H. The human face. An account of the postnatal growth and development of the craniofacial skeleton (1968), Harper and Row, New York
32. Keller T.S., Mao Z., and Spengler D.M. Young's modulus, bending strength, and tissue physical-properties of human compact-bone. Journal of Orthopaedic Research 8 (1990) 592-603
33. Carter D.R., Schwab G.H., and Spengler D.M. Tensile fracture of cancellous bone. Acta Orthopaedica Scandinavica 51 (1980) 733-741
34. Zioupos P., Cook R.B., and Hutchinson J.R. Some basic relationships between density values in cancellous and cortical bone. Journal of Biomechanics 41 (2008) 1961-1968
35. Choi K., Kuhn J.L., Ciarelli M.J., and Goldstein S.A. The elastic-moduli of human subchondral, trabecular, and cortical bone tissue and the size-dependency of cortical bone modulus. Journal of Biomechanics 23 (1990) 1103-1113
36. Choi K.W., and Goldstein S.A. The fatigues properties of bone tissues on a microstructural level. Transactions of the Orthopaedics Research Society 16 2 (1991) 485
37. Rice J.C., Cowin S.C., and Bowman J.A. On the dependence of the elasticity and strength of cancellous bone on apparent density. Journal of Biomechanics 21 (1988) 155-168
38. Ashman R.B., and Rho J.Y. Elastic-modulus of trabecular bone material. Journal of Biomechanics 21 (1988) 177-181
39. Zioupos P., Gresle M., and Winwood K. Fatigue strength of human cortical bone: age, physical and material heterogeneity effects. Journal of Biomedical Materials Research 86 (2008) 627-636
40. Turner C.H., Rho J., Takano Y., Tsui T.Y., and Pharr G.M. The elastic properties of trabecular and cortical bone tissues are similar: results from two microscopic measurement techniques. Journal of Biomechanics 32 (1999) 437-441
41. Gupta H.S., Stachewicz U., Wagermaier W., Roschger P., Wagner H.D., and Fratzl P. Mechanical modulation at the lamellar level in osteonal bone. Journal of Materials Research 21 (2006) 1913-1921
42. Juist J. In vivo determination of the elastic response of bone-2: Ulnar resonant frequency in osteoporotic, diabetic and normal subjects. Physics in Medicine and Biology (1970) 15.427-434
43. Christensen A.B., Ammitzboll F., Dyrbye C., Cornelissen M., Cornelissen P., and Vanderperre G. Assessment of tibial stiffness by vibration testing in-situ-1: identification of mode shapes in different supporting conditions. Journal of Biomechanics 19 (1986) 53-60
44. Rho J.Y., Hobatho M.C., and Ashman R.B. Relations of mechanical-properties to density and CT numbers in human bone. Medical Engineering & Physics 17 (1995) 347-355
45. Goldstein S. The mechanical properties of trabecular bone. Dependence on anatomic location and function. Journal of Biomechanics 20 (1987) 1055-1061
46. VanRietbergen B., Odgaard A., Kabel J., and Huiskes R. Direct mechanics assessment of elastic symmetries and properties of trabecular bone architecture. Journal of Biomechanics 29 (1996) 1653-1657
47. Odgaard A., Kabel J., VanRietbergen B., Dalstra M., and Huiskes R. Fabric and elastic principal directions of cancellous bone are closely related. Journal of Biomechanics 30 (1997) 487-495
48. Linde F., and Hvid I. The effect of constraint on the mechanical behaviour of trabecular bone specimens. Journal of Biomechanics 22 (1989) 485-490
49. Odgaard A., and Linde F. The underestimation of Young modulus in compressive testing of cancellous bone specimens. Journal of Biomechanics 24 (1991) 691-698
50. Keaveny T.M., Pinilla T.P., Crawford R.P., Kopperdahl D.L., and Lou A. Systematic and random errors in compression testing of trabecular bone. Journal of Orthopaedic Research 15 (1997) 101-110
51. Ascenzi A., and Bonucci E. The tensile properties of single osteons. Anatomical Record 158 (1967) 375-386
52. Ascenzi A., and Bonucci E. The compressive properties of single osteons. Anatomical Record 161 (1968) 377-392
53. Ascenzi A., and Bonucci E. The bending properties of single osteons. Journal of Biomechanics 23 (1990) 763-771
54. Ascenzi A., Baschieri P., and Benvenuti A. The torsional properties of single selected osteons. Journal of Biomechanics 27 (1994) 875
55. Mercer C., He M.Y., Wang R., and Evans A.G. Mechanisms governing the inelastic deformation of cortical bone and application to trabecular bone. Acta Biomaterials 2 (2006) 59-68
56. Marotti G. A new theory of bone lamellation. Calcified Tissue International (1993) 53.S47-S56
57. Weiner S., Traub W., and Wagner H.D. Lamellar bone. Structure-function relations. Journal of Structural Biology 126 (1999) 241-255
58. Giraud-Guille M.M. Twisted plywood architecture of collagen fibrils in human compact-bone osteons. Calcified Tissue International 42 (1988) 167-180
59. Weiner S., Arad T., Sabanay I., and Traub W. Rotated plywood structure of primary lamellar bone in the rat: orientations of the collagen fibril arrays. Bone 20 (1997) 509-514
60. Weiner S., and Traub W. Bone-structure-from angstroms to microns. Faseb Journal 6 (1992) 879-885
61. Giraud-Guille M.M. Cholesteric twist of collagen in vivo and in vitro. Molecular Crystals and Liquid Crystals 153 (1987) 15-30
62. Frasca P., Harper R.A., and Katz J.L. Collagen fiber orientations in human secondary osteons. Acta Anatomica 98 (1977) 1-13
63. Hasegawa K., Turner C.H., and Burr D.B. Contribution of collagen and mineral to the elastic-anisotropy of bone. Calcified Tissue International 55 (1994) 381-386
64. Turner C.H., and Burr D.B. Orientation of collagen in osteonal bone. Calcified Tissue International 60 (1997) 90
65. Pidaparti R.M., Chandran A., Takano Y., and Turner C.H. Bone mineral lies mainly outside of collagen fibrils. Predictions of a composite model for osteonal bone. Journal of Biomechanics 29 (1996) 909-916
66. Rho J.Y., Roy M., Tsui T.Y., and Pharr G.M. Young's modulus and hardness of trabecular and cortical bone in various directions determined by nanoindentation. Transactions of the 43rd Annual Meetings of the Orthopaedic Research Society. San Francisco, CA (1997) 891
67. Willems G., Celis J.P., Lambrechts P., Braem M., and Vanherle G. Hardness and Young's modulus determined by nanoindentation technique of filler particles of dental restorative materials compared with human enamel. Journal of Biomedical Materials Research 27 (1993) 747-755
68. Wagermaier W., Gupta H.S., Gourrier A., Paris O., Roschger P., Burghammer M., et al. Scanning texture analysis of lamellar bone using microbeam synchrotron X-ray radiation. Journal of Applied Crystallography 40 (2007) 115-120
69. Wagermaier W., Gupta H.S., Gourrier A., Burghammer M., Roschger P., and Fratzl P. Spiral twisting of fiber orientation inside bone lamellae. Biointerphases 1 (2006) 1-5
70. Rho J.Y., Zioupos P., Currey J.D., and Pharr G.M. Variations in the individual lamellar properties within osteons by nanoindentation. Bone 25 (1999) 295-300
71. Xu J., Rho J.Y., Mishra S.R., and Fan Z. Atomic force microscopy and nanoindentation characterization of human lamellar bone prepared by microtome sectioning and mechanical polishing technique. Journal of Biomedical Materials Research Part A 67A (2003) 719-726
72. Rho J.Y., Mishra S.R., Chung K., Bai J., and Pharr G.M. Relationship between ultrastructure and the nanoindentation properties of intramuscular herring bones. Annals of Biomedical Engineering 29 (2001) 1082-1088
73. Fratzl P., Gupta H.S., Paschalis E.P., and Roschger P. Structure and mechanical quality of the collagen-mineral nano-composite in bone. Journal of Materials Chemistry 14 (2004) 2115-2123
74. Lakes R., and Saha S. Cement line motion in bone. Science 204 (1979) 501-503
75. Katz J.L., and Meunier A. Scanning acoustic microscope studies of the elastic properties of osteons and osteon lamellae. Journal of Biomechanical Engineering-Transactions of the ASME 115 (1993) 543-548
76. Rho J.Y., Ashman R.B., and Turner C.H. Youngs modulus of trabecular and cortical bone material-ultrasonic and microtensile measurements. Journal of Biomechanics 26 (1993) 111-119
77. Reilly D.T., Burstein A.H., and Frankel V.H. Elastic-modulus for bone. Journal of Biomechanics 7 (1974) 271
78. Wolff J. Das Gesetz der Transformation der Knochen (1892), Hirschwald, Berlin
79. Runkle J.C., and Pugh J. The micro-mechanics of cancellous bone. Bulletin of Hospital Joint Diseases 36 (1975) 2-10
80. Townsend P.R., Rose R.M., and Radin E.L. Buckling studies of single human trabeculae. Journal of Biomechanics 8 (1975) 199-201
81. Williams J.L., and Lewis J.L. Properties and an anisotropic model of cancellous bone from the proximal tibial epiphysis. Journal of Biomechanical Engineering-Transactions of the ASME 104 (1982) 50-56
82. Hodgkinston R., Currey J.D., and Evans G.P. Hardness, an indicator of the mechanical competence of cancellous bone. Journal of Orthopaedic Research 7 (1989) 754-758
83. Kuhn J.L., Goldstein S.A., Choi K.W., London M., Feldkamp L.A., and Matthews L.S. Comparison of the trabecular and cortical tissue moduli from human iliac crests. Journal of Orthopaedic Research 7 (1989) 876-884
84. Mente P.L., and Lewis J.L. Experimental method for the measurement of the elastic modulus of trabecular bone tissue. Journal of Orthopaedic Research 7 (1989) 456-461
85. Ryan C.B., and Williams J.L. Tensile testing of rodlike trabeculae excised from bovine femoral bone. Journal of Biomechanics 22 (1989) 351-355
86. Glimcher M.J. Mechanisms of calcification. role of collagen fibrils and collagen-phsophoprotein complexes in vitro and in vivo. Anatomical Record 224 (1989) 139-153
87. Kuhn-Spearing L., Rey C., Kim H.M., and Glimcher M.J. Carbonated apatite nanocrystals of bone. In: Bourell D.L. (Ed). Synthesis and processing of nanocrystalline powder (1996), The Minerals, Metals and Materials Society, Warrendale, PA, USA
88. Landis W.J. The strength of a calcified tissue depends in part on the molecular structure and organization of its constituent mineral crystals in their organic matrix. Bone 16 (1995) 533-544
89. Ziv V., and Weiner S. Bone crystal size: a comparison of transmission electron microscopic and X-ray diffraction line-width-broadening techniques. Connective Tissue Research 30 (1994) 165-175
90. Sodek J., Ganss B., and McKee M.D. Osteopontin. Critical Reviews in Oral Biology & Medicine 11 (2000) 279-303
91. McKee M.D., and Nanci A. Osteopontin at mineralized tissue interfaces in bone, teeth, and osseointegrated implants: ultrastructural distribution and implications for mineralized tissue formation, turnover, and repair. Microscopy Research and Technique 33 (1996) 141-164
92. Young M.F., Kerr J.M., Ibaraki K., Heegaard A.M., and Robey P.G. Structure, expression, and regulation of the major noncollagenous matrix proteins of bone. Clinical Orthopaedics and Related Research (1992) 275-294
93. Hauschka P.V., Lian J.B., Cole D.E.C., and Gundberg C.M. Osteocalcin and matrix GLA protein-Vitamin K dependent proteins in bone. Physiological Reviews 69 (1989) 990-1047
94. Bonar L.C., Lees S., and Mook H.A. Neutron-diffraction studies of collagen in fully mineralized bone. Journal of Molecular Biology 181 (1985) 265-270
95. Lees S., Tao N.J., and Lindsay S.M. Studies of compact hard tissues and collagen by means of Brillouin light scattering. Connective Tissue Research 24 (1990) 187-205
96. Lees S. Mineralization of type-I collagen. Biophysical Journal 85 (2003) 204-207
97. Landis W.J., Hodgens K.J., Arena J., Song M.J., and McEwen B.F. Structural relations between collagen and mineral in bone as determined by high voltage electron microscopic tomography. Microscopy Research and Technique 33 (1996) 192-202
98. Landis W.J., Hodgens K.J., Song M.J., Arena J., Kiyonaga S., Marko M., et al. Mineralization of collagen may occur on fibril surfaces. Evidence from conventional and high-voltage electron microscopy and three-dimensional imaging. Journal of Structural Biology 117 (1996) 24
99. Rubin M.A., Jasiuk L., Taylor J., Rubin J., Ganey T., and Apkarian R.P. TEM analysis of the nanostructure of normal and osteoporotic human trabecular bone. Bone 33 (2003) 270-282
100. Glimcher M.J. The nature of the mineral component of bone and the mechanism of calcification. Instructional Course Lectures 36 (1987) 49-69
101. Weiner S., and Traub W. Crystal size and organization in bone. Connective Tissue Research 21 (1989) 589-595
102. Weiner S., Arad T., and Traub W. Crystal organization in rat bone lamellae. FEBS Letters 285 (1991) 49-54
103. Rho J.Y., Tsui T.Y., and Pharr G.M. Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. Biomaterials 18 (1997) 1325-1330
104. Gupta H.S., Wagermaier W., Zickler G.A., Hartmann J., Funari S.S., Roschger P., et al. Fibrillar level fracture in bone beyond the yield point. International Journal of Fracture 139 (2006) 425-436
105. Gupta H.S., Seto J., Wagermaier W., Zaslansky P., Boesecke P., and Fratzl P. Cooperative deformation of mineral and collagen in bone at the nanoscale. Proceedings of the National Academy of Sciences of the United States of America 103 (2006) 17741-17746
106. Gupta H.S., Wagermaier W., Zickler G.A., Aroush D.R.B., Funari S.S., Roschger P., et al. Nanoscale deformation mechanisms in bone. Nano Letters 5 (2005) 2108-2111
107. Almer J.D., and Stock S.R. Internal strains and stresses measured in cortical bone via high-energy X-ray diffraction. Journal of Structural Biology 152 (2005) 14-27
108. Thompson J.B., Kindt J.H., Drake B., Hansma H.G., Morse D.E., and Hansma P.K. Bone indentation recovery time correlates with bond reforming time. Nature 414 (2001) 773-776
109. Fantner G., Hassenkam T., Kindt J.H., Weaver J.C., Birkedal H., Pechenik L., et al. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nature Materials 4 (2005) 612-616
110. Hansma P.K., Fantner G.E., Kindt J.H., Thurner P.J., Schitter G., Udwin S.F., et al. Sacrificial bonds in the interfibrillar matrix of bone. Journal of Musculoskeletal and Neuronal Interactions 5 (2005) 313-315
111. Tai K., Ulm F.J., and Ortiz C. Nanogranular origins of the strength of bone. Nano Letters 6 (2006) 2520-2525
112. Tai K., Dao M., Suresh S., Palazoglu A., and Ortiz C. Nanoscale heterogeneity promotes energy dissipation in bone. Nature Materials 6 (2007) 454-462
113. Hull D., and Clyne T.W. An introduction to composite materials. 2nd ed (1996), Cambridge University Press, Cambridge, UK
114. Wainwright S.A., Biggs W.D., Currey J.D., and Gosline J.M. Mechanical design in organisms (1982), Princeton University Press
115. Ruys A.J., Wei M., Sorrell C.C., Dickson M.R., Brandwood A., and Milthorpe B.K. Sintering effects on the strength of hydroxyapatite. Biomaterials 16 (1995) 409-415
116. Gao H.J., Ji B.H., Jäger I.L., Arzt E., and Fratzl P. Materials become insensitive to flaws at nanoscale: lessons from nature. Proceedings of the National Academy of Sciences of the United States of America 100 (2003) 5597-5600
117. Gupta HS, Krauß S, Kanawka K, Gourrier A, Seto J, Funari SS, et al., 2006. Mechanical and structural characterization of antler and nacre using small angle X-ray scattering. HASYLAB annual report. p. 1169-70.
118. Kanawka K, 2006. Ultrastructural deformation in the fibrillar matrix of demineralized bone. Master of Science, Biomaterials Department, Max Planck Institute of Colloids and Interfaces and Fachhochschule Muenster, Potsdam, Germany
119. Kastelic J., and Baer E. Deformation in tendon collagen. Symposia of the Society for Experimental Biology 34 (1980) 397-435
120. Taylor D., Hazenberg J.G., and Lee T.C. Living with cracks. Damage and repair in human bone. Nature Materials 6 (2007) 263-268
121. Diab T., Condon K.W., Burr D.B., and Vashishth D. Age-related change in the damage morphology of human cortical bone and its role in bone fragility. Bone 38 (2006) 427-431
122. Moore T.L.A., and Gibson L.J. Microdamage accumulation in bovine trabecular bone in uniaxial compression. Journal of Biomechanical Engineering-Transactions of the ASME 124 (2002) 63-71
123. Reilly G.C., and Currey J.D. The effects of damage and microcracking on the impact strength of bone. Journal of Biomechanics 33 (2000) 337-343
124. Gupta H.S., Fratzl P., Kerschnitzki M., Benecke G., Wagermaier W., and Kirchner H.O.K. Evidence for an elementary process in bone plasticity with an activation enthalpy of 1 eV. Journal of the Royal Society Interface 4 (2007) 277-282
125. Kirchner H. Ductility and brittleness of bone. International Journal of Fracture 139 (2006) 509-516
126. Benecke G, Kerschnitki M, Fratzl P, Gupta HS, in preparation. Digital image correlation shows localized deformation bands in inelastic loading of fibrolamellar bone. Journal Materials Research, in press.
127. Zioupos P. Ageing human bone. Factors affecting its biomechanical properties and the role of collagen. Journal of Biomaterials Applications 15 (2001) 187-229
128. Zioupos P., Currey J.D., and Hamer A.J. The role of collagen in the declining mechanical properties of aging human cortical bone. Journal of Biomedical Materials Research 45 (1999) 108-116
129. Jäger I.L. A model for the stability and creep of organic materials. Journal of Biomechanics 38 (2005) 1459-1467
130. Wang X.T., and Ker R.F. Creep-rupture of wallaby tail tendons. Journal of Experimental Biology 198 (1995) 831-845
131. Wang X.T., Ker R.F., and Alexander R.M. Fatigue rupture of wallaby tail tendons. Journal of Experimental Biology 198 (1995) 847-852
132. Ker R.F., and Zioupos P. Creep and Fatigue damage of mammalian tendon and bone. Comments in Theoretical Biology 4 (1997) 151-181
133. Hassenkam T., Fantner G.E., Cutroni J.A., Weaver J.C., Morse D.E., and Hansma P.K. High-resolution AFM imaging of intact and fractured trabecular bone. Bone 35 (2004) 4-10
134. Rubin M.A., Rubin J., and Jasiuk W. SEM and TEM study of the hierarchical structure of C57BL/6J and C3H/HeJ mice trabecular bone. Bone 35 (2004) 11-20
135. Gibson L.J. Cellular solids. MRS Bulletin 28 (2003) 270-271
136. Thurner P.J., Wyss P., Voide R., Stauber M., Stampanoni M., Sennhauser U., et al. Time-lapsed investigation of three-dimensional failure and damage accumulation in trabecular bone using synchrotron light. Bone 39 (2006) 289-299
137. Thurner P.J., Erickson B., Schriock Z., Langan J., Scott J., Zhao M., et al. High-speed photography of the development of microdamage in trabecular bone during compression. Journal of Materials Research 21 (2006) 1093-1100
138. Bini F., Marinozzi A., Marinozzi F., and Patane F. Microtensile measurements of single trabeculae stiffness in human femur. Journal of Biomechanics 35 (2002) 1515-1519
139. Coats A.M., Zioupos P., and Aspden R.M. Material properties of subchondral bone from patients with osteoporosis or osteoarthritis by microindentation testing and electron probe microanalysis. Calcified Tissue International 73 (2003) 66-71
140. Zioupos P., Hansen U., and Currey J.D. Microcracking damage and the fracture process in relation to strain rate in human cortical bone tensile failure. Journal of Biomechanics 41 (2008) 2932-2939