Viscoelastic properties of human cortical bone tissue depend on gender and elastic modulus

Journal of Orthopaedic Research

Volumn 30, Issue 5, 2012, Pages 693-699

  Wu, Ziheng ^a   Ovaert, Timothy C ^a   Niebur, Glen L ^a  

^a University of Notre Dame   (United States)

Author keywords

bone quality; collagen; gender; mineralization; nanoindentation

Indexed keywords

COLLAGEN; MATRIX PROTEIN;

ARTICLE; BONE DENSITY; BONE MINERALIZATION; BONE STRUCTURE; CONTROLLED STUDY; CORTICAL BONE; FRACTURE; HUMAN; HUMAN TISSUE; PRIORITY JOURNAL; PROTEIN CROSS LINKING; SEX DIFFERENCE; VISCOELASTICITY; YOUNG MODULUS;

AGE FACTORS; AGED; AGED, 80 AND OVER; CALCIFICATION, PHYSIOLOGIC; COLLAGEN; ELASTIC MODULUS; FEMALE; FEMUR; HAVERSIAN SYSTEM; HUMANS; MALE; MIDDLE AGED; SEX CHARACTERISTICS;

EID: 84858298559     PISSN: 07360266     EISSN: 1554527X     Source Type: Journal    
DOI: 10.1002/jor.22001     Document Type: Article

References (49)

1. Lakes RS, Katz JL, Sternstein SS,. 1979. Viscoelastic properties of wet cortical bone-I. Torsional and biaxial studies. J Biomech 12: 657-678. (Pubitemid 10231553)
2. Carter DR, Hayes WC,. 1977. The compressive behavior of bone as a two-phase porous structure. J Bone Joint Surg 59-A: 954-962. (Pubitemid 8218257)
3. Currey JD,. 1989. Strain rate dependence of the mechanical properties of reindeer antler and the cumulative damage model of bone fracture. J Biomech 22: 469-475. (Pubitemid 19208021)
4. Kulin RM, Jiang F, Vecchio KS,. 2011. Effects of age and loading rate on equine cortical bone failure. J Mech Behav Biomed Mater 4: 57-75.
5. Wright TM, Hayes WC,. 1976. The fracture mechanics of fatigue crack propagation in compact bone. J Biomed Mater Res 10: 637-648.
6. Nalla RK, Kruzic JJ, Kinney JH, et al. 2005. Aspects of in vitro fatigue in human cortical bone: Time and cycle dependent crack growth. Biomaterials 26: 2183-2195. (Pubitemid 39575362)
7. Williams ML,. 1967. Fracture in viscoealstic media. Fundam Phenomena Mater Sci 4: 23-32.
8. Sasaki N, Enyo A,. 1995. Viscoelastic properties of bone as a function of water content. J Biomech 28: 809-815.
9. Garner E, Lakes R, Lee T, et al. 2000. Viscoelastic dissipation in compact bone: Implications for stress-induced fluid flow in bone. J Biomechan Eng 122: 166-172. (Pubitemid 30318341)
10. Lakes RS, Saha S,. 1979. Cement line motion in bone. Science 204: 501-503. (Pubitemid 9186275)
11. Rho JY, Roy ME II, Tsui TY, et al. 1999. Elastic properties of microstructural components of human bone tissue as measured by nanoindentation. J Biomed Mater Res 45: 48-54. (Pubitemid 29068438)
12. Oyen ML, Cook RF,. 2009. A practical guide for analysis of nanoindentation data. J Mech Behav Biomed Mater 2: 396-407.
13. Wu Z, Baker TA, Ovaert TC, et al. 2011. The effect of holding time on nanoindentation measurements of creep in bone. J Biomech 44: 1066-1072.
14. Fan Z, Rho JY,. 2003. Effects of viscoelasticity and time-dependent plasticity on nanoindentation measurements of human cortical bone. J Biomed Mater Res A 67: 208-214. (Pubitemid 37517170)
15. Oyen ML, Ko CC,. 2007. Examination of local variations in viscous, elastic, and plastic indentation responses in healing bone. J Mater Sci Mater Med 18: 623-628. (Pubitemid 46876376)
16. Kim DG, Huja SS, Lee HR, et al. 2010. Relationships of viscosity with contact hardness and modulus of bone matrix measured by nanoindentation. J Biomech Eng 132: 024502.
17. Les CM, Spence CA, Vance JL, et al. 2004. Determinants of ovine compact bone viscoelastic properties: Effects of architecture, mineralization, and remodeling. Bone 35: 729-738. (Pubitemid 39144419)
18. Sasaki N, Yoshikawa M,. 1993. Stress relaxation in native and EDTA-treated bone as a function of mineral content. J Biomech 26: 77-83. (Pubitemid 23053757)
19. Bembey AK, Oyen ML, Bushby AJ, et al. 2006. Viscoelastic properties of bone as a function of hydration state determined by nanoindentation. Philos Mag 86: 5691-5703. (Pubitemid 44410596)
20. Donnelly E, Williams RM, Downs SA, et al. 2006. Quasistatic and dynamic nanomechanical properties of cancellous bone tissue relate to collagen content and organization. J Mater Res 21: 2106-2117. (Pubitemid 44472257)
21. Donnelly E, Boskey AL, Baker SP, et al. 2010. Effects of tissue age on bone tissue material composition and nanomechanical properties in the rat cortex. J Biomed Mater Res A 92: 1048-1056.
22. Nyman JS, Roy A, Acuna RL, et al. 2006. Age-related effect on the concentration of collagen cross-links in human osteonal and interstitial bone tissue. Bone 39: 1210-1217. (Pubitemid 44827935)
23. Lakes RS, Katz JL,. 1979. Viscoelastic properties of wet cortical bone-II. Relaxation mechanisms. J Biomech 12: 679-687. (Pubitemid 10231554)
24. Norman TL, Wang Z,. 1997. Microdamage of human cortical bone: Incidence and morphology in long bones. Bone 20: 375-379. (Pubitemid 27196661)
25. Schapery RA,. 1975. Theory of crack initiation and growth in viscoelastic media. 1. Theoretical development. Int J Fracture 11: 141-159.
26. Schapery RA,. 1975. Theory of crack initiation and growth in viscoelastic media. 2. Approximate methods of analysis. Int J Fracture 11: 369-388.
27. Fischer-Cripps AC,. 2004. A simple phenomenological approach to nanoindentation creep. Mater Sci Eng A 385: 74-82. (Pubitemid 39437098)
28. Oyen ML,. 2005. Spherical indentation creep following ramp loading. J Mater Res 20: 2094-2100. (Pubitemid 41763313)
29. Oliver WC,. 1992. An improved technique for determining hardness and elastic modulus using load and displacement sensing indentation experiments. J Mater Res 7: 1564.
30. Deuerling JM, Rudy DJ, Niebur GL, et al. 2010. Improved accuracy of cortical bone mineralization measured by polychromatic microcomputed tomography using a novel high mineral density composite calibration phantom. Med Phys 37: 5138-5145.
31. Boskey AL,. 2001. Bone mineralization. In:, Cowin SC, editor. Bone mechanics handbook. 2nd ed. Boca Raton: CRC. p 5.1-5.33.
32. Bank RA, Beekman B, Verzijl N, et al. 1997. Sensitive fluorimetric quantitation of pyridinium and pentosidine cross-links in biological samples in a single high-performance liquid chromatographic run. J Chromatogr B Biomed Sci Appl 703: 37-44. (Pubitemid 28011242)
33. Bank RA, Jansen EJ, Beekman B, et al. 1996. Amino acid analysis by reverse-phase high-performance liquid chromatography: Improved derivatization and detection conditions with 9-fluorenylmethyl chloroformate. Anal Biochem 240: 167-176. (Pubitemid 26304260)
34. Isaksson H, Malkiewicz M, Nowak R, et al. 2010. Rabbit cortical bone tissue increases its elastic stiffness but becomes less viscoelastic with age. Bone 47: 1030-1038.
35. Zebaze RM, Jones AC, Pandy MG, et al. 2011. Differences in the degree of bone tissue mineralization account for little of the differences in tissue elastic properties. Bone 48: 1246-1251.
36. Williams M,. 1966. Fracture in viscoelastic media. In:, Bonis L, Duga J, Gilman J, editors. Fundamental phenomena in the materials sciences. Boston: Plenum Press. p 23-32.
37. Bowman SM, Gibson LJ, Hayes WC, et al. 1999. Results from demineralized bone creep tests suggest that collagen is responsible for the creep behavior of bone. J Biomech Eng 121: 253-258. (Pubitemid 29181171)
38. Huja SS, Beck FM, Thurman DT,. 2006. Indentation properties of young and old osteons. Calcif Tissue Int 78: 392-397. (Pubitemid 44078538)
39. Isaksson H, Nagao S, Malkiewicz M, et al. 2010. Precision of nanoindentation protocols for measurement of viscoelasticity in cortical and trabecular bone. J Biomech 43: 2410-2417.
40. Mulder L, Koolstra JH, den Toonder JM, et al. 2007. Intratrabecular distribution of tissue stiffness and mineralization in developing trabecular bone. Bone 41: 256-265. (Pubitemid 47001817)
41. Moreno LD, Waldman SD, Grynpas MD,. 2006. Sex differences in long bone fatigue using a rat model. J Orthop Res 24: 1926-1932. (Pubitemid 44559953)
42. Nieves JW, Formica C, Ruffing J, et al. 2005. Males have larger skeletal size and bone mass than females, despite comparable body size. J Bone Miner Res 20: 529-535. (Pubitemid 40293502)
43. Pietrzak WS, Woodell-May J, McDonald N,. 2006. Assay of bone morphogenetic protein-2, -4, and -7 in human demineralized bone matrix. J Craniofac Surg 17: 84-90. (Pubitemid 44383852)
44. Bellof G, Most E, Pallauf J,. 2006. Concentration of Ca, P, Mg, Na and K in muscle, fat and bone tissue of lambs of the breed German Merino Landsheep in the course of the growing period. J Anim Physiol Anim Nutr (Berl) 90: 385-393. (Pubitemid 44337414)
45. Gourion-Arsiquaud S, Allen MR, Burr DB, et al. 2010. Bisphosphonate treatment modifies canine bone mineral and matrix properties and their heterogeneity. Bone 46: 666-672.
46. Ingram RT, Park YK, Clarke BL, et al. 1994. Age- and gender-related changes in the distribution of osteocalcin in the extracellular matrix of normal male and female bone. Possible involvement of osteocalcin in bone remodeling. J Clin Invest 93: 989-997.
47. Kavukcuoglu NB, Patterson-Buckendahl P, Mann AB,. 2009. Effect of osteocalcin deficiency on the nanomechanics and chemistry of mouse bones. J Mech Behav Biomed Mater 2: 348-354.
48. Mochida Y, Parisuthiman D, Pornprasertsuk-Damrongsri S, et al. 2009. Decorin modulates collagen matrix assembly and mineralization. Matrix Biol 28: 44-52.
49. Deuerling JM, Yue W, Espinoza Orias AA, et al. 2009. Specimen-specific multi-scale model for the anisotropic elastic constants of human cortical bone. J Biomech 42: 2061-2067.