Identifying Novel Clinical Surrogates to Assess Human Bone Fracture Toughness

Journal of Bone and Mineral Research

Volumn 30, Issue 7, 2015, Pages 1290-1300

  Granke, Mathilde ^a   Makowski, Alexander J ^a,b,c   Uppuganti, Sasidhar ^a   Does, Mark D ^c,d,e   Nyman, Jeffry S ^a,b,c  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b DEPARTMENT OF VETERANS AFFAIRS   (United States)

^c VANDERBILT UNIVERSITY   (United States)

^d VANDERBILT UNIVERSITY   (United States)

^e VANDERBILT UNIVERSITY   (United States)

Author keywords

BOUND WATER; FRACTURE TOUGHNESS; HUMAN CORTICAL BONE; NON ENZYMATIC COLLAGEN CROSSLINKS; NUCLEAR MAGNETIC RESONANCE; POROSITY; REFERENCE POINT INDENTATION

Indexed keywords

COLLAGEN; DEOXYPYRIDINOLINE; PYRIDINOLINE; BIOLOGICAL MARKER;

ADULT; AGED; ARTICLE; BONE DENSITY; BONE MASS; CLINICAL ASSESSMENT; CORTICAL BONE; CRACK GROWTH; CRACK INITIATION; CROSS LINKING; FEMALE; FRACTURE; FRACTURE TOUGHNESS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN TISSUE; MALE; MICRO-COMPUTED TOMOGRAPHY; MUSCULOSKELETAL DISEASE ASSESSMENT; MUSCULOSKELETAL SYSTEM PARAMETERS; PERIOSTEUM; POROSITY; PROTON NUCLEAR MAGNETIC RESONANCE; RIGIDITY; RISK ASSESSMENT; STANDARD; AGE; BIOMECHANICS; DIAGNOSTIC IMAGING; MIDDLE AGED; MULTIVARIATE ANALYSIS; PATHOLOGY; PATHOPHYSIOLOGY; VERY ELDERLY; YOUNG ADULT;

ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; BIOMARKERS; BIOMECHANICAL PHENOMENA; FEMALE; FRACTURES, BONE; HUMANS; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; X-RAY MICROTOMOGRAPHY; YOUNG ADULT;

EID: 84931956266     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2452     Document Type: Article

References (85)

1. Wang XD, Masilamani NS, Mabrey JD, et al., 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.
2. De Laet CE, van Hout BA, Burger H, et al., Bone density,risk of hip fracture in men,women: cross sectional analysis. BMJ. 1997; 315 (7102): 221-5.
3. van der Meulen MC, Boskey AL,. Atypical subtrochanteric femoral shaft fractures: role for mechanics and bone quality. Arthritis Res Ther. 2012; 14 (4): 220.
4. Ettinger B, Burr DB, Ritchie RO,. Proposed pathogenesis for atypical femoral fractures: lessons from materials research. Bone. 2013; 55 (2): 495-500.
5. Yamaguchi T, Sugimoto T., Bone metabolism and fracture risk in type 2 diabetes mellitus. Bonekey Rep. 2012; 1: 36.
6. Oei L, Zillikens MC, Dehghan A, et al., High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control: the Rotterdam Study. Diabetes Care. 2013; 36 (6): 1619-28.
7. Zioupos P, Currey JD,. Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone. 1998; 22 (1): 57-66.
8. Wang X, Shen X, Li X, et al., Age-related changes in the collagen network and toughness of bone. Bone. 2002; 31 (1): 1-7.
9. Nalla RK, Kruzic JJ, Kinney JH, et al., Effect of aging on the toughness of human cortical bone: evaluation by R-curves. Bone. 2004; 35 (6): 1240-6.
10. Koester KJ, Barth HD, Ritchie RO,. Effect of aging on the transverse toughness of human cortical bone: evaluation by R-curves. J Mech Behav Biomed Mater. 2011; 4 (7): 1504-13.
11. 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.
12. Bonfield W., Advances in the fracture mechanics of cortical bone. J Biomech. 1987; 20 (11-12): 1071-81.
13. Akkus O, Jepsen KJ, Rimnac CM,. Microstructural aspects of the fracture process in human cortical bone. J Mater Sci. 2000; 35 (24): 6065-74.
14. Ural A, Vashishth D., Anisotropy of age-related toughness loss in human cortical bone: a finite element study. J Biomech. 2007; 40 (7): 1606-14.
15. 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): 504-9.
16. Yeni YN, Brown CU, Wang Z, et al., The influence of bone morphology on fracture toughness of the human femur and tibia. Bone. 1997; 21 (5): 453-9.
17. Phelps JB, Hubbard GB, Wang X, et al., Microstructural heterogeneity and the fracture toughness of bone. J Biomed Mater Res. 2000; 51 (4): 735-41.
18. Yan J, Daga A, Kumar R, et al., Fracture toughness and work of fracture of hydrated, dehydrated, and ashed bovine bone. J Biomech. 2008; 41 (9): 1929-36.
19. Norman TL, Yeni YN, Brown CU, et al., Influence of microdamage on fracture toughness of the human femur and tibia. Bone. 1998; 23 (3): 303-6.
20. Zioupos P., Accumulation of in-vivo fatigue microdamage and its relation to biomechanical properties in ageing human cortical bone. J Microsc. 2001; 201 (Pt 2): 270-8.
21. Tang SY, Vashishth D., The relative contributions of non-enzymatic glycation and cortical porosity on the fracture toughness of aging bone. J Biomech. 2011; 44 (2): 330-6.
22. Cefalu CA,. Is bone mineral density predictive of fracture risk reduction ? Curr Med Res Opin. 2004; 20 (3): 341-9.
23. Geusens P, Van Geel T, Huntjens K, et al., Clinical fractures beyond low BMD. Int J Clin Rheumtol. 2011; 6 (4): 411-21.
24. McClung MR,. The relationship between bone mineral density and fracture risk. Curr Osteoporos Rep. 2005; 3 (2): 57-63.
25. Horch RA, Gochberg DF, Nyman JS, et al., Non-invasive predictors of human cortical bone mechanical properties: T2-discriminated 1H NMR compared with high resolution X-ray. PLoS One. 2011; 6 (1): e16359.
26. Horch RA, Nyman JS, Gochberg DF, et al., Characterization of 1H NMR signal in human cortical bone for magnetic resonance imaging. Magn Reson Med. 2010; 64 (3): 680-7.
27. Ong HH, Wright AC, Wehrli FW,. Deuterium nuclear magnetic resonance unambiguously quantifies pore and collagen-bound water in cortical bone. J Bone Miner Res. 2012; 27 (12): 2573-81.
28. Manhard MK, Horch RA, Harkins KD, et al., Validation of quantitative bound- and pore-water imaging in cortical bone. Magn Reson Med. 2014; 71 (6): 2166-71.
29. Horch RA, Gochberg DF, Nyman JS, et al., Clinically compatible MRI strategies for discriminating bound and pore water in cortical bone. Magn Reson Med. 2012; 68 (6): 1774-84.
30. Diez-Perez A, Guerri R, Nogues X, et al., Microindentation for in vivo measurement of bone tissue mechanical properties in humans. J Bone Miner Res. 2010; 25 (8): 1877-85.
31. Guerri-Fernandez RC, Nogues X, Quesada Gomez JM, et al., Microindentation for in vivo measurement of bone tissue material properties in atypical femoral fracture patients and controls. J Bone Miner Res. 2013; 28 (1): 162-8.
32. Koester KJ, Ager JW III, Ritchie RO,. The true toughness of human cortical bone measured with realistically short cracks. Nat Mater. 2008; 7 (8): 672-7.
33. American Society for Testing and Materials International. E1820-13, Standard Test Method for Measurement of Fracture Toughness. West Conshohocken, PA, USA: American Society for Testing and Materials International; 2013.
34. Bouxsein ML, Boyd SK, Christiansen BA, et al., Guidelines for assessment of bone microstructure in rodents using micro-computed tomography. J Bone Miner Res. 2010; 25 (7): 1468-86.
35. Launey ME, Chen PY, McKittrick J, et al., Mechanistic aspects of the fracture toughness of elk antler bone. Acta Biomater. 2010; 6 (4): 1505-14.
36. Li S, Abdel-Wahab A, Silberschmidt VV,. Analysis of fracture processes in cortical bone tissue. Eng Fract Mech. 2013; 110: 448-58.
37. Zhu XK, Joyce JA,. Review of fracture toughness (G, K, J, CTOD, CTOA) testing and standardization. Eng Fract Mech. 2012; 85: 1-46.
38. Vashishth D., Rising crack-growth-resistance behavior in cortical bone: implications for toughness measurements. J Biomech. 2004; 37 (6): 943-6.
39. Does MD,. Multi-Exponential Relaxation Analysis (MERA) Toolbox, Version 2 [Internet]. Memphis (TN): Vanderbilt University; 2014. [cited 2015 Jan 31]. Available from: http://www.vuiis.vanderbilt.edu/∼doesmd/MERA/MERA-Toolbox.html.
40. Aref M, Gallant MA, Organ JM, et al., In vivo reference point indentation reveals positive effects of raloxifene on mechanical properties following 6 months of treatment in skeletally mature beagle dogs. Bone. 2013; 56 (2): 449-53.
41. Rasoulian R, Raeisi Najafi A, Chittenden M, et al., Reference point indentation study of age-related changes in porcine femoral cortical bone. J Biomech. 2013; 46 (10): 1689-96.
42. Hansma P, Turner P, Drake B, et al., The bone diagnostic instrument II: indentation distance increase. Rev Sci Instrum. 2008; 79 (6): 064303.
43. Granke M, Coulmier A, Uppuganti S, et al., Insights into reference point indentation involving human cortical bone: sensitivity to tissue anisotropy and mechanical behavior. J Mech Behav Biomed Mater. 2014; 37: 174-85.
44. Rosner B., Percentage points for a generalized ESD many-outlier procedure. Technometrics. 1983; 25 (2): 165-72.
45. Buckley A, Hill KE, Davison JS,. Collagen metabolism. In:, Di Sabato G, Abelson J, Simon M, editors Immunochemical techniques, Part M: Chemotaxis and inflammation. San Diego: Academic Press; 1988. (Methods in enzymology. vol. 163): pp 674-94.
46. Saito M, Marumo K, Fujii K, et al., Single-column high-performance liquid chromatographic-fluorescence detection of immature, mature, and senescent cross-links of collagen. Anal Biochem. 1997; 253 (1): 26-32.
47. Thurner PJ, Katsamenis OL,. The role of nanoscale toughening mechanisms in osteoporosis. Curr Osteoporos Rep. 2014 Sep; 12 (3): 351-6.
48. Diaz E, Chung CB, Bae WC, et al., Ultrashort echo time spectroscopic imaging (UTESI): an efficient method for quantifying bound and free water. NMR Biomed. 2012; 25 (1): 161-8.
49. Ritchie RO, Buehler MJ, Hansma P., Plasticity and toughness in bone. Physics Today. 2009; 62 (6): 41-7.
50. Fritsch A, Hellmich C., Dormieux L Ductile sliding between mineral crystals followed by rupture of collagen crosslinks: experimentally supported micromechanical explanation of bone strength. J Theor Biol. 2009; 260 (2): 230-52.
51. Gupta HS, Krauss S, Kerschnitzki M, et al., Intrafibrillar plasticity through mineral/collagen sliding is the dominant mechanism for the extreme toughness of antler bone. J Mech Behav Biomed Mater. 2013; 28: 366-82.
52. Zimmermann EA, Schaible E, Bale H, et al., Age-related changes in the plasticity,toughness of human cortical bone at multiple length scales. Proc Natl Acad Sci U S.A. 2011; 108 (35): 14416-21.
53. Zimmermann EA, Launey ME, Ritchie RO,. The significance of crack-resistance curves to the mixed-mode fracture toughness of human cortical bone. Biomaterials. 2010; 31 (20): 5297-305.
54. Vashishth D., Hierarchy of bone microdamage at multiple length scales. Int J Fatigue. 2007; 29 (6): 1024-33.
55. Augat P, Schorlemmer S., The role of cortical bone and its microstructure in bone strength. Age Ageing. 2006; 35 Suppl 2: ii27-31.
56. Nalla RK, Kruzic JJ, Ritchie RO,. On the origin of the toughness of mineralized tissue: microcracking or crack bridging ? Bone. 2004; 34 (5): 790-8.
57. Fantner GE, Birkedal H, Kindt JH, et al., Influence of the degradation of the organic matrix on the microscopic fracture behavior of trabecular bone. Bone. 2004; 35 (5): 1013-22.
58. Nalla RK, Stolken JS, Kinney JH, et al., Fracture in human cortical bone: local fracture criteria and toughening mechanisms. J Biomech. 2005; 38 (7): 1517-25.
59. Vashishth D, Tanner KE, Bonfield W., Experimental validation of a microcracking-based toughening mechanism for cortical bone. J Biomech. 2003; 36 (1): 121-4.
60. Fantner GE, Rabinovych O, Schitter G, et al., Hierarchical interconnections in the nano-composite material bone: fibrillar cross-links resist fracture on several length scales. Compos Sci Technol. 2006; 66 (9): 1205-11.
61. Nobakhti S, Limbert G, Thurner PJ,. Cement lines and interlamellar areas in compact bone as strain amplifiers-contributors to elasticity, fracture toughness and mechanotransduction. J Mech Behav Biomed Mater. 2014; 29: 235-51.
62. Mischinski S, Ural A., Interaction of microstructure and microcrack growth in cortical bone: a finite element study. Comput Methods Biomech Biomed Engin. 2013; 16 (1): 81-94.
63. Chan KS, Chan CK, Nicolella DP,. Relating crack-tip deformation to mineralization and fracture resistance in human femur cortical bone. Bone. 2009; 45 (3): 427-34.
64. Zimmermann EA, Gludovatz B, Schaible E, et al., Fracture resistance of human cortical bone across multiple length-scales at physiological strain rates. Biomaterials. 2014; 35 (21): 5472-81.
65. Nyman JS, Roy A, Tyler JH, et al., Age-related factors affecting the postyield energy dissipation of human cortical bone. J Orthop Res. 2007; 25 (5): 646-55.
66. Vashishth D, Gibson GJ, Khoury JI, et al., Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone. 2001; 28 (2): 195-201.
67. Siegmund T, Allen MR, Burr DB,. Failure of mineralized collagen fibrils: modeling the role of collagen cross-linking. J Biomech. 2008; 41 (7): 1427-35.
68. Nyman JS, Ni Q, Nicolella DP, et al., Measurements of mobile and bound water by nuclear magnetic resonance correlate with mechanical properties of bone. Bone. 2008; 42 (1): 193-9.
69. Bae WC, Patil S, Biswas R, et al., Magnetic resonance imaging assessed cortical porosity is highly correlated with μCT porosity. Bone. 2014; 66: 56-61.
70. Fathima NN, Baias M, Blumich B, et al., Structure and dynamics of water in native and tanned collagen fibers: effect of crosslinking. Int J Biol Macromol. 2010; 47 (5): 590-6.
71. Miles CA, Avery NC, Rodin VV, et al., The increase in denaturation temperature following cross-linking of collagen is caused by dehydration of the fibres. J Mol Biol. 2005; 346 (2): 551-6.
72. Behari J., Elements of bone biophysics biophysical bone behavior: principles and applications. Hoboken, NJ: John Wiley and Sons Ltd; 2009. p. 1-52.
73. Robinson RA,. Bone tissue: composition and function. Johns Hopkins Med J. 1979; 145 (1): 10-24.
74. Timmins PA, Wall JC,. Bone water. Calcif Tissue Res. 1977; 23 (1): 1-5.
75. Samuel J, Sinha D, Zhao JC, et al., Water residing in small ultrastructural spaces plays a critical role in the mechanical behavior of bone. Bone. 2014; 59: 199-206.
76. Gallant MA, Brown DM, Hammond M, et al., Bone cell-independent benefits of raloxifene on the skeleton: a novel mechanism for improving bone material properties. Bone. 2014; 61: 191-200.
77. Nyman JS, Roy A, Shen X, et al., The influence of water removal on the strength and toughness of cortical bone. J Biomech. 2006; 39 (5): 931-8.
78. Bae WC, Chen PC, Chung CB, et al., Quantitative ultrashort echo time (UTE) MRI of human cortical bone: correlation with porosity and biomechanical properties. J Bone Miner Res. 2012; 27 (4): 848-57.
79. Yamashita J, Li X, Furman BR, et al., Collagen and bone viscoelasticity: a dynamic mechanical analysis. J Biomed Mater Res. 2002; 63 (1): 31-6.
80. Sen D, Buehler MJ,. Structural hierarchies define toughness and defect-tolerance despite simple and mechanically inferior brittle building blocks. Sci Rep. 2011; 1: 35.
81. Gourion-Arsiquaud S, Lukashova L, Power J, et al., Fourier transform infrared imaging of femoral neck bone: reduced heterogeneity of mineral-to-matrix and carbonate-to-phosphate and more variable crystallinity in treatment-naive fracture cases compared with fracture-free controls. J Bone Miner Res. 2013; 28 (1): 150-61.
82. Donnelly E, Meredith DS, Nguyen JT, et al., Reduced cortical bone compositional heterogeneity with bisphosphonate treatment in postmenopausal women with intertrochanteric and subtrochanteric fractures. J Bone Miner Res. 2012; 27 (3): 672-8.
83. Donnelly E, Lane JM, Boskey AL,. Research perspectives: The 2013 AAOS/ORS research symposium on Bone Quality and Fracture Prevention. J Orthop Res. 2014; 32 (7): 855-64.
84. Chan KS, Nicolella DP,. Micromechanical modeling of R-curve behaviors in human cortical bone. J Mech Behav Biomed Mater. 2012; 16: 136-52.
85. Nyman JS, Gorochow LE, Adam Horch R, et al., Partial removal of pore and loosely bound water by low-energy drying decreases cortical bone toughness in young and old donors. J Mech Behav Biomed Mater. 2013; 22: 136-45.