Fracture mechanics of cortical bone tissue: A hierarchical perspective

Critical Reviews in Biomedical Engineering

Volumn 32, Issue 5-6, 2004, Pages 379-425

  Akkus, Ozan ^a   Yeni, Yener N ^b   Wasserman, Nicholas ^a  

^a The University of Toledo   (United States)

^b HENRY FORD HOSPITAL   (United States)

Author keywords

Aging; Cortical bone; Fracture mechanics; Microdamage

Indexed keywords

BIOLOGICAL ORGANS; BIOMECHANICS; BIOMEDICAL ENGINEERING; BIOMIMETIC MATERIALS; BONE; DISEASES; FRACTURE;

BONE FRACTURE; EVOLUTIONARY PROCESSES; SKELETAL ORGANS; TISSUE FRACTURES;

FRACTURE MECHANICS;

BIOMIMETIC MATERIAL;

AGING; BONE; BONE TISSUE; CORTICAL BONE; FRACTURE; FRACTURE MECHANICS; INJURY; MECHANICS; PRIORITY JOURNAL; REVIEW; SKELETON;

ANIMALS; BONE AND BONES; COMPRESSIVE STRENGTH; ELASTICITY; FRACTURE HEALING; FRACTURES, BONE; HUMANS; MODELS, BIOLOGICAL; STRESS, MECHANICAL; TENSILE STRENGTH; WEIGHT-BEARING;

EID: 12744274622     PISSN: 0278940X     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevBiomedEng.v32.i56.10     Document Type: Review

References (207)

1. Bonfield W. Advances in the fracture mechanics of cortical bone. J Biomech 1987; 20(11-12):1071-81.
2. Melvin JW. Fracture mechanics of bone. J Biomech Eng 1993; 115(4B):549-54.
3. Brear K, Currey JD, Pond CM. Ontogenetic changes in the mechanical properties of the femur of the polar bear ursus-maritimus. J Zool 1990; 222:49-58.
4. Wollf J. Das Gesetz der Transformation der Knochen. Berlin: A. Hirschwald, 1892.
5. Kerley ER. The microscopic determination of age in human bone. Am J Phys Anthropol 1965; 23(2):149-163.
6. Martin RB, Pickett JC, Zinaich S. Studies of skeletal remodeling in aging men. Clin Orthop 1980(149):268-282.
7. Burr DB, Martin RB, Schaffler MB, Radin EL. Bone remodeling in response to in vivo fatigue damage. J Biomech 1985; 18:189-200.
8. Burr DB. Targeted and nontargeted remodeling. Bone 2002; 30(1):2-4.
9. Wright TM, Vosburgh F, Burstein AH. Permanent deformation of compact bone monitored by acoustic emission. J Biomech 1981; 14(6):405-409.
10. 2 space" components in a unit volume of dog bone. J Bone Joint Surg Am 1957; 39A:167-188.
11. Kadler KE, Hojima Y, Prockop DJ. Assembly of collagen fibrils de novo by cleavage of the type I pC-collagen with procollagen C-proteinase. Assay of critical concentration demonstrates that collagen self-assembly is a classical example of an entropy-driven process. J Biol Chem 1987; 262(32):15696-15701.
12. Petruska JA, Hodge AJ. A subunit model for the tropocollagen macromolecule. 1964; 51:871-876.
13. Eyre DR. Crosslink maturation in bone collagen. In: Veiss A, editor. The Chemistry and Biology of Mineralized Connective Tissues. New York: Elsevier North-Holland, 1981.
14. Knott L, Bailey AJ. Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone 1998; 22(3):181-187.
15. Parkinson J, Brass A, Canova G, Brechet Y. The mechanical properties of simulated collagen fibrils. J Biomech 1997; 30(6):549-554.
16. Hulmes DJ. Building collagen molecules, fibrils, and suprafibrillar structures. J Struct Biol 2002; 137(1-2):2-10.
17. Parry DAD, Craig AS. Growth and development of collagen fibrils in connective tissue. In: Motta PM, Ruggeri A, editors. Ultrastructure of the Connective Tissue Matrix. Norwell, MA: Kluwer Academic, 1984.
18. Rey C, Miquel JL, Facchini L, Legrand AP, Glimcher MJ. Hydroxyl groups in bone mineral. Bone 1995; 16(5):583-586.
19. Fratzl P, Fratzl-Zelman N, Klaushofer K, Vogl G, Koller K. Nucleation and growth of mineral crystals in bone studied by small-angle X-ray scattering. Calcif Tissue Int 1991; 48(6):407-413.
20. Landis WJ. 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 1995; 16(5):533-544.
21. Heywood BR, Sparks NH, Shellis RP, Weiner S, Mann S. Ultrastructure, morphology and crystal growth of biogenic and synthetic apatites. Connect Tissue Res 1990; 25(2):103-119.
22. Akkus O, Adar F, Schaffler MB. Prestresses on mineral crystals of bone are relieved upon fracture. In: 49th Annual Meeting of the Orthopaedic Research Society, 2003, New Orleans.
23. Amprino R, Engstrom A. Studies on x-ray absorption and diffraction of bone tissue. Acta Anat 1952; 15:1-22.
24. Wergedal JE, Baylink DJ. Electron microprobe measurements of bone mineralization rate in vivo. Am J Physiol 1974; 226(2):345-352.
25. Marotti G, Favia A, Zallone AZ. Quantitative analysis on the rate of secondary bone mineralization. Connect Tissue Res 1972; 10(1):67-81.
26. Lees S, Prostak KS, Ingle VK, Kjoller K. The loci of mineral in turkey leg tendon as seen by atomic force microscope and electron microscopy. Calcif Tissue Int 1994; 55(3):180-189.
27. Lees S, Prostak K. The locus of mineral crystallites in bone. Connect Tissue Res 1988; 18(1):41-54.
28. Su X, Sun K, Cui FZ, Landis WJ. Organization of apatite crystals in human woven bone. Bone 2003; 32(2):150-162.
29. Akkus O, Polyakova-Akkus A, Adar F, Schaffler MB. Aging of microstructural compartments in human compact bone. J Bone Miner Res 2003; 18:1012-1019.
30. Handschin RG, Stern WB. Crystallographic and chemical analysis of human bone apatite (Crista Iliaca). Clin Rheumatol 1994; 13(Suppl 1):75-90.
31. Baig AA, Fox JL, Young RA, Wang Z, Hsu J, Higuchi WI, et al. Relationships among carbonated apatite solubility, crystallite size, and microstrain parameters. Calcif Tissue Int 1999; 64(5):437-449.
32. Yeni YN, Schaffler MB, Gibson G, Fyhrie DP. Prestress due to dimensional changes caused by demineralization: a potential mechanism for microcracking in bone. Ann Biomed Eng 2002; 30(2):217-225.
33. Les CM, Stover SM, Keyak JH, Taylor KT, Kaneps AJ. Stiff and strong compressive properties are associated with brittle post-yield behavior in equine compact bone material. J Orthop Res 2002; 20(3):607-614.
34. Currey JD. Tensile yield in compact bone is determined by strain, post-yield behaviour by mineral content. J Biomech 2004; 37(4):549-556.
35. Biltz RM, Pellegrino ED. The nature of bone carbonate. Clin Orthop 1977(129): 279-292.
36. Penel G, Leroy G, Rey C, Bres E. MicroRaman spectral study of the PO4 and CO3 vibrational modes in synthetic and biological apatites. Calcif Tissue Int 1998; 63(6):475-481.
37. Eshelby JD. The determination of the elastic field of an ellipsoidal inclusion, and related problems. Proc R Soc Lond A Math Phys Sci 1957; A241:376-396.
38. Dry ME, Beebe RA. Adsorption studies on bone mineral and synthetic hydroxyapatite. J Phys Chem 1960; 64:1300-1304.
39. Schreiner LJ, Cameron IG, Funduk N, Miljkovic L, Pintar MM, Kydon DN. Proton NMR spin grouping and exchange in dentin. Biophys J 1991; 59(3):629-639.
40. Magne D, Weiss P, Bouler JM, Laboux O, Daculsi G. Study of the maturation of the organic (type I collagen) and mineral (nonstoichiometric apatite) constituents of a calcified tissue (dentin) as a function of location: a Fourier transform infrared microspectroscopic investigation. J Bone Miner Res 2001; 16(4):750-757.
41. Bonar LC, Lees S, Mook HA. Neutron diffraction studies of collagen in fully mineralized bone. J Mol Biol 1985; 181(2):265-270.
42. Cox BN, Marshall DB. Crack bridging in the fatigue of fibrous composites. Fatg Frac Eng Mat 1991; 14:847-861.
43. Braidotti P, Branca FP, Stagni L. Scanning electron microscopy of human cortical bone failure surfaces. J Biomech 1997; 30(2):155-162.
44. Corondan G, Haworth WL. A fractographic study of human long bone. J Biomech. 1986; 19(3):207-218.
45. Yeni YN, Patel B, Gibson GJ, Fyhrie DP. Relief of mineralization pre-strains on collagen causes strains equivalent to toe-in strains observed in tensile testing of demineralized cortical bone. In: ASME Summer Meeting; 2001; Snowbird, Utah; 2001.
46. Yeni YN, Fyhrie DP. A rate-dependent microcrack-bridging model that can explain the strain rate dependency of cortical bone apparent yield strength. J Biomech 2003; 36(9):1343-1353.
47. Birk DE, Linsenmayer TF. Collagen fibril assembly, deposition and organization into tissue-specific matrices. In: Yurchenko D, Birk DE, Mecham RP, editors. Extracellular Matrix Assembly and Structure. New York: Academic Press, 1994.
48. Cooke FW, Zeidman H, Scheifele SJ. The fracture mechanics of bone-another look at composite modeling. J Biomed Mater Res 1973; 7(3):383-399.
49. Cook J, Gordon JE. A mechanism for the control of crack propagation in all brittle systems. Proc R Soc Lond A Math Phsy Sci 1964; 282A:508-520.
50. Reilly GC. Observations of microdamage around osteocyte lacunae in bone. J Biomech 2000; 33(9):1131-1134.
51. Marotti G. A new theory of bone lamellation. Calcif Tissue Int 1993; 53 Suppl 1:S47-55; discussion S56.
52. Frost HL. Human haversian system measurements. Henry Ford Hosp. Med. Bull. 1961; 9:145-147.
53. Ashman RB, Cowin SC, Van Buskirk WC, Rice JC. A continuous wave technique for the measurement of the elastic properties of cortical bone. J Biomech 1984; 17(5):349-361.
54. Yoon HS, Katz JL. Ultrasonic wave propagation in human cortical bone-II. Measurements of elastic properties and microhardness. J Biomech 1976; 9(7):459-464.
55. Bentolik V, Boyce TM, Fyhrie DP, Drumb R, Skerry TM, Schaffler MB. Intracortical remodeling in adult rat long bones after fatigue loading. Bone 1998; 23(3):275-281.
56. Burr DB, Schaffler MB, Frederickson RG. Composition of the cement line and its possible mechanical role as a local interface in human compact bone. J Biomech 1988; 21(11):939-945.
57. Taylor D, Prendergast PJ. A model for fatigue crack propagation and remodeling in compact bone. Proc Inst Mech Eng [H] 1997; 211(5):369-375.
58. Taylor D. Microcrack growth parameters for compact bone deduced from stiffness variations. J Biomech 1998; 31(7):587-592.
59. Kruzic JJ, Campbell JP, Ritchie RO. On the fatigue behavior of gamma-based titanium aluminides: role of small cracks. Acta Mater 1999; 47(3):801-816.
60. Taylor D, Knott JF. Fatigue crack propagation behaviour of short cracks; the effect of microstructure. Fatigue Eng Mater 1981; 4:147-155.
61. Akkus O, Rimnac CM. Cortical bone tissue resists fatigue fracture by deceleration and arrest of microcrack growth. J Biomech 2001; 34(6):757-764.
62. Harris B, Guild FJ, Brown CR. Fracture mechanisms in glass reinforced plastics. J Mater Sci 1975; 10:2050-2061.
63. Reifsnider KL. Damage and damage mechanics. In: Reifsnider KL, editor. Fatigue of Composite Materials. New York: Elsevier, 1991.
64. Frost HL. Presence of microscopic cracks in vivo in bone. Henry Ford Hosp Med Bull 1960; 8:25-35.
65. Burr DB, Turner CH, Naick P, Forwood MR, Ambrosius W, Hasan MS, et al. Does microdamage accumulation affect the mechanical properties of bone? J Biomech 1998; 31(4):337-345.
66. Schaffler MB, Radin EL, Burr DB. Long-term fatigue behavior of compact bone at low strain magnitude and rate. Bone 1990; 11(5):321-326.
67. Schaffler MB, Choi K, Milgrom C. Aging and matrix microdamage accumulation in human compact bone. Bone 1995; 17(6):521-525.
68. Norman TL, Wang Z. Microdamage of human cortical bone: incidence and morphology in long bones. Bone 1997; 20(4):375-379.
69. Yeni YN, Fyhrie DP. Fatigue damage-fracture mechanics interaction in cortical bone. Bone 2002; 30(3):509-514.
70. Courtney AC, Hayes WC, Gibson LJ. Age-related differences in post-yield damage in human cortical bone. Experiment and model. J Biomech 1996; 29(11):1463-1471.
71. Jepsen KJ, Davy DT, Krzypow DJ. The role of the lamellar interface during torsional yielding of human cortical bone. J Biomech 1999; 32(3):303-310.
72. Jepsen KJ, Krzypow DJ, Dutta Roy T, Pizzuto T. Damage accumulation during tensile yielding of human cortical bone. Trans Orthop Res Soc, 1999.
73. Akkus O, Jepsen KJ, Rimnac CM. Microstructural aspects of the fracture process in human cortical bone. J Mater Sci 2000; 35:6065-6074.
74. Yeni YN, Norman TL. Calculation of porosity and osteonal cement line effects on the effective fracture toughness of cortical bone in longitudinal crack growth. J Biomed Mater Res 2000; 51(3):504-509.
75. Piekarski K. Fracture of bone. J Appl Physics 1970; 41:215-223.
76. Moyle DD, Gavens AJ. Fracture properties of bovine tibial bone. J Biomech 1986; 19(11):919-927.
77. Malik CL, Stover SM, Martin RB, Gibeling JC. Equine cortical bone exhibits rising R-curve fracture mechanics. J Biomech 2003; 36(2):191-198.
78. Martin RB, Stover SM, Gibson VA, Gibeling JC, Griffin LV. In vitro fatigue behavior of the equine third metacarpus: remodeling and microcrack damage analysis. J Orthop Res 1996; 14(5):794-801.
79. Hiller LP, Stover SM, Gibson VA, Gibeling JC, Prater CS, Hazelwood SJ, et al. Osteon pullout in the equine third metacarpal bone: effects of ex vivo fatigue. J Orthop Res 2003; 21(3):481-488.
80. Lakes R, Saha S. Cement line motion in bone. Science 1979; 204(4392):501-503.
81. Lakes RS, Nakamura S, Behiri JC, Bonfield W. Fracture mechanics of bone with short cracks. J Biomech 1990; 23(10):967-975.
82. Park HC, Lakes RS. Cosserat micromechanics of human bone: strain redistribution by a hydration sensitive constituent. J Biomech 1986; 19(5):385-397.
83. Zioupos P. Recent developments in the study of failure of solid biomaterials and bone: 'fracture'and 'pre-fracture' toughness. Mat Sci Eng 1998; 6:33-40.
84. Burr DB, Stafford T. Validity of the bulk-staining technique to separate artifactual from in vivo bone microdamage. Clin Orthop 1990; 260:305-308.
85. O'Brien FJ, Taylor D, Lee TC. An improved labeling technique for monitoring microcrack growth in compact bone. J Biomech 2002; 35(4):523-526.
86. Frost HM. Transient-steady state phenomena in microdamage physiology: a proposed algorithm for lamellar bone. Calcif Tissue Int 1989; 44(6):367-381.
87. Burr DB, Milgrom C, Boyd RD, Higgins WL, Robin G, Radin EL. Experimental stress fractures of the tibia. Biological and mechanical aetiology in rabbits. J Bone Joint Surg Br 1990; 72B(3):370-375.
88. Greaney RB, Gerber FH, Laughlin RL, Kmet JP, Metz CD, Kilcheski TS, et al. Distribution and natural history of stress fractures in U.S. Marine recruits. Radiology 1983; 146(2):339-346.
89. Hopson CN, Perry DR. Stress fractures of the calcaneus in women marine recruits. Clin Orthop 1977; 128:159-162.
90. Belkin SC. Stress fractures in athletes. Orthop Clin North Am 1980; 11(4):735-741.
91. Burrows HJ. Fatigue infraction of the middle of the tibiae in ballet dancers. J Bone Joint Surg Br 1956; 38B:83.
92. Burr DB, Forwood MR, Fyhrie DP, Martin RB, Schaffler MB, Turner CH. Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J Bone Miner Res 1997; 12(1):6-15.
93. Rubin CT, Harris JM, Jones BH. Stress fractures: the remodeling response to excessive repetitive loading. Trans Orthop Res Soc 1984:303.
94. Frost HM. The pathomechanics of osteoporoses. Clin Orthop 1985; 200:198-225.
95. Freeman MA, Todd RC, Pirie CJ. The role of fatigue in the pathogenesis of senile femoral neck fractures. J Bone Joint Surg Br 1974; 56B(4):698-702.
96. Radin EL, Parker HG, Pugh JW, Steinberg RS, Paul IL, Rose RM. Response of joints to impact loading. 3. Relationship between trabecular microfractures and cartilage degeneration. J Biomech 1973; 6(1):51-57.
97. Fazzalari NL, Forwood MR, Smith K, Manthey BA, P. H. Assessment of cancellous bone quality in severe osteoarthrosis: bone mineral density, mechanics, and microdamage. Bone 1998; 22:381-388.
98. McCormack BA, Prendergast PJ. An analysis of crack propagation paths at implant/bone-cement interfaces. J Biomech Eng 1996; 118(4):579-585.
99. Boyce TM, Fyhrie DP, Glotkowski MC, Radin ER, Schaffler MB. Damage type and strain mode associations in human compact bone bending fatigue. J Orthop Res 1998; 16:322-329.
100. Parsamian GP, Norman TL. Diffuse damage accumulation in the fracture process zone of human cortical bone specimens and its influence on fracture toughness. J Mat Sci Mat Med 2001; 12(9):779-783.
101. Arthur Moore TL, Gibson LJ. Microdamage accumulation in bovine trabecular bone in uniaxial compression. J Biomech Eng 2002; 124(1):63-71.
102. Vashishth D, Koontz J, Qiu SJ, Lundin-Cannon D, Yeni YN, Schaffler MB, et al. In vivo diffuse damage in human vertebral cancellous bone. Bone 2000; 26(2):147-152.
103. Yeni YN, Hou FJ, Ciarelli T, Vashishth D, Fyhrie DP. Trabecular shear stresses predict in vivo linear microcrack density but not diffuse damage in human vertebral cancellous bone. Ann Biomed Eng 2003; 31(6):726-732.
104. Yeni YN, Hou FJ, Ciarelli T, Vashishth D, Fyhrie DP. Weak and nonsignificant correlations of in vivo diffuse damage with mechanical properties, tissue architecture and trabecular stress distributions in human vertebral cancellous bone: a direct association between in vivo diffuse damage and mechanical properties is not supported. 49th Annual Meeting, Orthopaedic Research Society; 2003 February 2-5; New Orleans, Louisiana; 2003.
105. Norman T, Parsamian G, Coleman C. In-vivo diffuse damage in human cortical bone does not compromise bone toughness. 47th Annual Meeting, Orthopaedic Research Society; 2001 February 25-28; San Francisco, California; 2001.
106. Schaffler MB, Pitchford WC, Choi K, Riddle JM. Examination of compact bone microdamage using back-scattered electron microscopy. Bone 1994; 15(5):483-488.
107. Zioupos P, Currey JD, Sedman AJ. An examination of the micromechanics of failure of bone and antler by acoustic emission tests and laser scanning confocal microscopy. Med Eng Phys 1994; 16(3):203-212.
108. Carter DR, Hayes WC. Compact bone fatigue damage: a microscopic examination. Clin Orthop 1977(127):265-274.
109. Mori S, Harruff R, Ambrosius W, Burr DB. Trabecular bone volume and microdamage accumulation in the femoral heads of women with and without femoral neck fractures. Bone 1997; 21(6):521-526.
110. Danova NA, Colopy SA, Radtke CL, Kalscheur VL, Markel MD, Vanderby R, et al. Degradation of bone structural properties by accumulation and coalescence of microcracks. Bone 2003; 33(2):197-205.
111. Frank JD, Ryan M, Kalscheur VL, Ruaux-Mason CP, Hozak RR, Muir P. Aging and accumulation of microdamage in canine bone. Bone 2002; 30(1):201-206.
112. Fazzalari NL, Forwood MR, Manthey BA, Smith K, Kolesik P. Three-dimensional confocal images of microdamage in cancellous bone. Bone 1998; 23(4):373-378.
113. Taylor D, Lee TC. Measuring the shape and size of microcracks in bone. J Biomech 1998; 31(12):1177-1180.
114. O'Brien FJ, Taylor D, Dickson GR, Lee TC. Visualisation of three-dimensional microcracks in compact bone. J Anat 2000; 197 Pt 3:413-420.
115. Duda GN, Heller M, Albinger J, Schulz O, Schneider E, Claes L. Influence of muscle forces on femoral strain distribution. J Biomech 1998; 31(9):841-846.
116. Bertram JE, Biewener AA. Bone curvature: sacrificing strength for load predictability? J Theor Biol 1988; 131(1):75-92.
117. Currey JD, Brear K. Tensile yield in bone. Calcif Tissue Res 1974; 15(3):173-179.
118. O'Brien FJ, Taylor D, Lee TC. Microcrack accumulation at different intervals during fatigue testing of compact bone. J Biomech 2003; 36(7):973-980.
119. Guo XE, Liang LC, Goldstein SA. Micromechanics of osteonal cortical bone fracture. 1998; 120(1):112-117.
120. Sobelman OS, Gibeling JC, Stover SM, Hazelwood SJ, Yeh OC, Shelton DR, et al. Do microcracks decrease or increase fatigue resistance in cortical bone? J Biomech 2004; 37(9):1295-1303.
121. Gray RJ, Korbacher GK. Compressive fatique behaviour of bovine compact bone. J Biomech 1974; 7(3):287-292.
122. Swanson SA, Freeman MA, Day WH. The fatigue properties of human cortical bone. 1971; 9(1):23-32.
123. Griffin LV, Gibeling JC, Martin RB, Gibson VA, Stover SM. Model of flexural fatigue damage accumulation for cortical bone. J Orthop Res 1997; 15(4):607-614.
124. Behiri JC, Bonfield W. Crack velocity dependence of longitudinal fracture in bone. J Mat Sci 1980; 15:1841-1849.
125. Chamay A, Tschantz P. Mechanical influences in bone remodeling. Experimental research on Wolff's law. J Biomech 1972; 5(2):173-180.
126. Frost HM, Roth H, Villanueva AR. Physical characteristics of bone Part IV. Henry Ford Hosp Med Bull 1961; 9:163.
127. Jepsen KJ, Davy DT, Akkus O. Observations of damage in bone. In: Cowin SC, editor. Bone Mechanics Handbook. New York: CRC Press, 2001.
128. Fyhrie DP, Schaffler MB. Failure mechanisms in human vertebral cancellous bone. Bone 1994; 15:105.
129. Ascenzi A, Bonucci E. The compressive properties of single osteons. Anat Rec 1968; 161(3):377-391.
130. Taylor D, O'Reilly P, Vallet L, Lee TC. The fatigue strength of compact bone in torsion. J Biomech 2003; 36(8):1103-1109.
131. Vashishth D, Norman TL, Nivargikar S, Behiri JC, Bonfield W. Failure of longitudinal osteons under tensile and shear loading. Trans Orthop Res Soc; 1995; Orlando, Florida; 1995.
132. Turner CH, Wang T, Burr DB. Shear strength and fatigue properties of human cortical bone determined from pure shear tests. Calcif Tissue Int 2001; 69(6):373-378.
133. Melvin JW, Evans FG. Crack propagation in bone. In: Fung YC, Brighton JA, editors. Biomaterials Symposium, Society for Biomaterials, 1973.
134. Bonfield W, Datta PK. Young's modulus of compact bone. J Biomech 1974; 7(2):147-149.
135. Bonfield W, Datta PK. Fracture toughness of compact bone. J Biomech 1976; 9(3):131-134.
136. ASTM E399-90, Standard Test Method for Plane-Strain Fracture Toughness of Metallic Materials. 1990.
137. Wright TM, Hayes WC. Fracture mechanics parameters for compact bone-effects of density and specimen thickness. J Biomech 1977; 10(7):419-430.
138. Sih GC, Paris P, C., Irwin GR. On cracks in rectilinearly anisotropic bodies. Int J Frac Mech 1965; 1:189-202.
139. Reilly DT, Burstein AH. The elastic and ultimate properties of compact bone tissue. J Biomech 1975; 8(6):393-405.
140. Robertson DM, Robertson D, Barrett CR. Fracture toughness, critical crack length and plastic zone size in bone. J Biomech 1978; 11(8-9):359-364.
141. Bonfield W, Grynpas MD, Young RJ. Crack velocity and the fracture of bone. J Biomech 1978; 11(10-12):473-479.
142. Behiri JC, Bonfield W. Fracture mechanics of bone-the effects of density, specimen thickness and crack velocity on longitudinal fracture. J Biomech 1984; 17(1):25-34.
143. Burr DB, Milgrom C, Fyhrie D, Forwood M, Nyska M, Finestone A, et al. In vivo measurement of human tibial strains during vigorous activity. Bone 1996; 18:405-410.
144. ASTM E561-92a, Standard Practice for R-Curve Determination. 1992.
145. Malik CL, Gibeling JC, Martin RB, Stover SM. Compliance calibration for fracture testing of equine cortical bone. J Biomech 2002; 35(5):701-705.
146. Raftopoulos DD, Meissner J, Konsta-Gdoutos M, Gdoutos EE. A fracture mechanics study of human bone by birefringent coatings and caustics. Int J Frac 1998; 91:L51-L54.
147. Nalla RK, Kinney JH, Ritchie RO. Mechanistic fracture criteria for the failure of human cortical bone. Nat Mater 2003; 2(3):164-168.
148. Norman TL, Vashishth D, Burr DB. Fracture toughness of human bone under tension. J Biomech 1995; 28(3):309-320.
149. Wang X, Lankford J, Agrawal CM. Use of a compact sandwich specimen to evaluate fracture toughness and interfacial bonding of bone. J Appl Biomat 1994; 5(4):315-323.
150. Wang X, Mabrey JD, Agrawal CM. An interspecies comparison of bone fracture properties. Biomed Mater Eng 1998; 8(1):1-9.
151. Ruse ND, Troczynski T, MacEntee MI, Feduik D. Novel fracture toughness test using a notchless triangular prism (NTP) specimen. J Biomed Mater Res 1996; 31(4):457-463.
152. Iwamoto N, Ruse ND. Fracture toughness of human dentin. J Biomed Mater Res 2003; 66A(3):507-512.
153. Bonfield W, Behiri JC, Charalambides B. Orientation and age-related dependence of fracture toughness of cortical bone. In: Perren SM, Schneider E, editors. Biomechanics: Current Interdisciplinary Research. Dordrecht: Martinus-Nijhoff, 1985.
154. Brown CU, Yeni YN, Norman TL. Fracture toughness is dependent on bone location-a study of the femoral neck, femoral shaft, and the tibial shaft. J Biomed Mater Res 2000; 49(3):380-389.
155. Behiri JC, Bonfield W. Orientation dependence of the fracture mechanics of cortical bone. J Biomech 1989; 22(8-9):863-872.
156. Norman TL, Vashishth D, Burr DB. Effect of groove on bone fracture toughness. J Biomech 1992; 25(12):1489-1492.
157. Wang X, Agrawal CM. Fracture toughness of bone using a compact sandwich specimen: effects of sampling sites and crack orientations. J Biomed Mater Res 1996; 33(1):13-21.
158. Norman TL, Nivargikar SV, Burr DB. Resistance to crack growth in human cortical bone is greater in shear than in tension. J Biomech 1996; 29(8):1023-1031.
159. Feng Z, Rho J, Han S, Ziv I. Orientation and loading condition dependence of fracture toughness in cortical bone. Mat Sci Eng 2000; 11:41-46.
160. Yeni YN, Brown CU, Norman TL. Influence of bone composition and apparent density on fracture toughness of the human femur and tibia. Bone 1998; 22(1):79-84.
161. Yeni YN, Brown CU, Wang Z, Norman TL. The influence of bone morphology on fracture toughness of the human femur and tibia. Bone 1997; 21(5):453-459.
162. Yeni YN, Norman TL. Fracture toughness of human femoral neck: effect of microstructure, composition, and age. 2000; 26(5):499-504.
163. Currey JD. The mechanical consequences of variation in the mineral content of bone. J Biomech 1969; 2:1-11.
164. Currey JD. Effects of differences in mineralization on the mechanical properties of bone. Phil Trans R Soc Lond B Biol Sci 1984; 304(1121):509-518.
165. Currey JD, Brear K, Zioupos P. The effects of ageing and changes in mineral content in degrading the toughness of human femora. J Biomech 1996; 29(2):257-260.
166. Wang XD, Masilamani NS, Mabrey JD, Alder ME, Agrawal CM. Changes in the fracture toughness of bone may not be reflected in its mineral density, porosity, and tensile properties. Bone 1998; 23(1):67-72.
167. Yeni YN. Fracture mechanics of human cortical bone: the relationship of geometry, microstructure and composition with the fracture of the tibia, femoral shaft and the femoral neck [Dissertation]. PhD Thesis: West Virginia University, 1998.
168. Wang X, Li X, Bank RA, Agrawal CM. Effects of collagen unwinding and cleavage on the mechanical integrity of the collagen network in bone. Calcif Tissue Int 2002; 71(2):186-192.
169. Wang X, Bank RA, TeKoppele JM, Hubbard GB, Athanasiou KA, Agrawal CM. Effect of collagen denaturation on the toughness of bone. Clin Orthop 2000(371): 228-239.
170. Wang X, Bank RA, TeKoppele JM, Agrawal CM. The role of collagen in determining bone mechanical properties. J Orthop Res 2001; 19(6):1021-1026.
171. Vashishth D, Gibson GJ, Khoury JI, Schaiffler MB, Kimura J, Fyhrie DP. Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone 2001; 28(2):195-201.
172. Currey JD, Foreman J, Laketic I, Mitchell J. Effects of ionizing radiation on the mechanical properties of human bone. J Orthop Res 1997; 15:111-117.
173. Cheung DT, Perelman N, Tong D, Nimni ME. The effect of gamma-irradiation on collagen molecules, isolated alpha-chains, and crosslinked native fibers. J Biomed Mater Res 1990; 24:581-589.
174. Akkus O, Rimnac CM. Fracture resistance of gamma radiation sterilized cortical bone allografts. J Orthop Res 2001; 19(5):927-934.
175. Phelps JB, Hubbard GB, Wang X, Agrawal CM. Microstructural heterogeneity and the fracture toughness of bone. J Biomed Mater Res 2000; 51(4):735-741.
176. Zioupos P, Currey JD. Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone 1998; 22(1):57-66.
177. Martin RB. A theory of fatigue damage accumulation and repair in cortical bone. J Orthop Res 1992; 10:818-825.
178. Paris PC, Erdogan F. A critical analysis of crack propagation laws. Trans ASME D J Basic Eng 1963; 85D:528-534.
179. Wright TM, Hayes WC. The fracture mechanics of fatigue crack propagation in compact bone. J Biomed Mater Res Symp 1976; 7:637-648.
180. Schaffler MB, Radin EL, Burr DB. Mechanical and morphological effects of strain rate on fatigue of compact bone. Bone 1989; 10:207-214.
181. Nalla RK, Kruzic JJ, Ritchie RO. On the origin of the toughness of mineralized tissue: microcracking or crack bridging? Bone 2004; 34(5):790-798.
182. Vashishth D, Tanner KE, Behiri JC, Bonfield W. Failure of osteons under differently applied loads. Trans Orthop Res Soc, 1994.
183. Mitchell E, Stawarz A, Rimnac CM. Gamma radiation sterilization reduces the fatigue crack propagation resistance of human cortical bone. Trans Orthop Res Soc 2001; San Fransisco, CA.
184. Kayacan R, Stawarz A, Mitchell E, Rimnac CM. Effects of age, gender and radiation sterilization on damage formation during fatigue crack propagation in human cortical bone. Trans Orthop Res Soc 2002, New Orleans, Louisiana.
185. Shelton DR, Gibeling JC, Martin RB, Stover SM. Fatigue crack growth rates in equine cortical bone. In: Annual Meeting of the American Society of Biomechanics, Chicago, IL, 2000.
186. Suresh S. Fatigue of Materials. Cambridge: Cambridge University Press, 1991.
187. Vashishth D, Tanner KE, Bonfield W. Contribution, development and morphology of microcracking in cortical bone during crack propagation. J Biomech 2000; 33(9):1169-1174.
188. Vashishth D, Tanner KE, Bonfield W. Experimental validation of a microcracking-based toughening mechanism for cortical bone. J Biomech 2003; 36(1):121-124.
189. Vashishth D, Behiri JC, Bonfield W. Crack growth resistance in cortical bone: concept of microcrack toughening. J Biomech 1997; 30(8):763-769.
190. Sedlin ED. A rheologic model for cortical bone. A study of the physical properties of human femoral samples. Acta Orthop Scand 1965; Suppl(83):1-77.
191. McElhaney JH. Dynamic response of bone and muscle tissue. J Appl Physiol 1966; 21(4):1231-1236.
192. Tanabe Y, Bonfield W, Tanner KE. Impact fracture toughness of bovine compact bone. 1996; 17:337-342.
193. Kikugawa H, Yasui Y, Tomatsu T. Effect of strain rate on the fracture toughness of cortical bone. J Soc Mat Sci Japan 2000; 49(3):327-333.
194. Evans GP, Behiri JC, Vaughan LC, Bonfield W. Fracture properties of cortical bone in thoroughbred racehorse; racecourse destruction cases compared with normal bones. J Biomech Int Soc Biomech Abs of XII Congress 1989; 22(10):1009.
195. Nalla RK, Kruzic JJ, Kinney JH, Ritchie RO. Mechanistic aspects of fracture and R-curve behavior in human cortical bone. Biomaterials 2005; 26(2):217-231.
196. Thompson JB, Kindt JH, Drake B, Hansma HG, Morse DE, Hansma PK. Bone indentation recovery time correlates with bond reforming time. Nature 2001; 414(6865):773-776.
197. Currey J. Sacrificial bonds heal bone. Nature 2001; 414(6865):699.
198. Dong XN, Yeni YN, Christopherson GT, Les CM, Turner AS, Fyhrie DP. The influence of sacrificial bonds on viscoelastic properties of cortical bone. In: 49th Annual Meeting of the Orthopaedic Research Society, February 2-5, 2003, New Orleans, LA.
199. Dong XN, Yeni YN, Les CM, Turner AS, Fyhrie DP. Are sacrificial bonds divalent calcium cross-links between collagen molecules? In: 50th Annual Meeting of the Orthopaedic Research Society, March 7-10, 2004, San Francisco, CA.
200. Martinez M, Aliabadi MH. Fracture mechanics of bone using the dual boundary element method. In: 1st International Conference on Simulation Modelling in Bioengineering, BIOSIM 96, Oct 23-25, 1996; Merida, Venezuela: Computational Mechanics, 1996.
201. Norman TL, Vashishth D, Burr DB. 2D finite element study of mode I fracture in human bone. In: Winter Annual Meeting of the American Society of Mechanical Engineers, Anaheim, CA, 1992: New York: ASME, 1992.
202. Grootenboer HJ, Weersink, A. F. J. A composite model of cortical bone for the prediction of crack propagation. In: Huiskes R, Van Campen D, De Wijn J, editors. Biomechanics: Principles and Applications. The Hague: Martinus Nijhoff; 1982.
203. Guo XE, McMahon TA, Keaveny TM, Hayes WC, Gibson LJ. Finite element modeling of damage accumulation in trabecular bone under cyclic loading. J Biomech 1994; 27(2):145-55.
204. De Santis R, Anderson P, Tanner KE, Ambrosio L, Nicolais L, Bonfield W, et al. Bone fracture analysis on the short rod chevron-notch specimens using the X-ray computer micro-tomography. J Mat Sci Mat Med 2000; 11(10):629-636.
205. Carol I, Lopez M, Roa O. Micromechanical analysis of quasi-brittle materials using fracture-based interface elements. Int J Num Meth Eng 2001; 52(1-2):193-215.
206. Stolken JS, Kinney JH. On the importance of geometric nonlinearity in finite-element simulations of trabecular bone failure. Bone 2003; 33(4):494-504.
207. Pezzotti G, Sakakura S. Study of the toughening mechanisms in bone and biomimetic hydroxyapatite materials using Raman microprobe spectroscopy. J Biomed Mater Res 2003; 65A(2):229-236.