Insights into reference point indentation involving human cortical bone: Sensitivity to tissue anisotropy and mechanical behavior

Journal of the Mechanical Behavior of Biomedical Materials

Volumn 37, Issue , 2014, Pages 174-185

  Granke, Mathilde ^a   Coulmier, Aurélie ^a,b   Uppuganti, Sasidhar ^a   Gaddy, Jennifer A ^a,c   Does, Mark D ^a,d   Nyman, Jeffry S ^a,c,d  

^a VANDERBILT UNIVERSITY   (United States)

^b AIX MARSEILLE UNIVERSITY   (France)

^c DEPARTMENT OF VETERANS AFFAIRS   (United States)

^d VANDERBILT UNIVERSITY   (United States)

Author keywords

Anisotropy; Human cortical bone; Mechanical behavior; Reference point indentation; Toughness

Indexed keywords

ANISOTROPY; BIOMECHANICS; BONE; FRACTURE; MECHANICAL PROPERTIES; STRESS ANALYSIS; TOUGHNESS;

ELASTIC AND PLASTIC BEHAVIORS; HUMAN CORTICAL BONE; MECHANICAL BEHAVIOR; MICRO- AND NANO-INDENTATION; MICRO-INDENTATION TECHNIQUE; ORTHOGONAL DIRECTIONS; REFERENCE POINTS; TRANSVERSE ISOTROPIC;

TISSUE;

STAINLESS STEEL;

AGE; ANATOMICAL VARIATION; ANISOTROPY; ARTICLE; BIOMECHANICS; BONE TISSUE; CORTICAL BONE; FEMUR SHAFT; HARDNESS; HUMAN; HUMAN TISSUE; MUSCULOSKELETAL SYSTEM PARAMETERS; ORTHOPEDIC EQUIPMENT; PRIORITY JOURNAL; REFERENCE POINT INDENTATION; REFERENCE VALUE; ADULT; AGED; AGING; FEMALE; FEMUR; MALE; MATERIALS TESTING; MECHANICS; MICROTECHNOLOGY; PHYSIOLOGY; PROCEDURES; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; AGING; ANISOTROPY; BIOMECHANICAL PHENOMENA; FEMALE; FEMUR; HUMANS; MALE; MATERIALS TESTING; MECHANICAL PROCESSES; MICROTECHNOLOGY;

EID: 84920197088     PISSN: 17516161     EISSN: 18780180     Source Type: Journal    
DOI: 10.1016/j.jmbbm.2014.05.016     Document Type: Article

References (53)

1. Akkus O., Jepsen K.J., Rimnac C.M. Microstructural aspects of the fracture process in human cortical bone. J. Mater. Sci. 2000, 35:6065-6074.
2. Allen M.R., Burr D.B. Mineralization, microdamage, and matrix: how bisphosphonates influence material properties of bone. BoneKEy-Osteov. 2007, 4:49-60.
3. Amprino R. Investigations on some physical properties of bone tissue. Cells Tissues Organs 1958, 34:161-186.
4. Aref M., Gallant M.A., Organ J.M., Wallace J.M., Newman C.L., Burr D.B., Brown D.M., Allen M.R. 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, 56:449-453.
5. Boivin G., Bala Y., Doublier A., Farlay D., Ste-Marie L.G., Meunier P.J., Delmas P.D. The role of mineralization and organic matrix in the microhardness of bone tissue from controls and osteoporotic patients. Bone 2008, 43:532-538.
6. Boivin G.Y., Chavassieux P.M., Santora A.C., Yates J., Meunier P.J. Alendronate increases bone strength by increasing the mean degree of mineralization of bone tissue in osteoporotic women. Bone 2000, 27:687-694.
7. Diez-Perez A., Guerri R., Nogues X., Caceres E., Pena M.J., Mellibovsky L., Randall C., Bridges D., Weaver J.C., Proctor A., Brimer D., Koester K.J., Ritchie R.O., Hansma P.K. Microindentation for in vivo measurement of bone tissue mechanical properties in humans. J. Bone Miner. Res. 2010, 25:1877-1885.
8. Donnelly E., Meredith D.S., Nguyen J.T., Gladnick B.P., Rebolledo B.J., Shaffer A.D., Lorich D.G., Lane J.M., Boskey A.L. Reduced cortical bone compositional heterogeneity with bisphosphonate treatment in postmenopausal women with intertrochanteric and subtrochanteric fractures. J. Bone Miner. Res. 2012, 27:672-678.
9. Ettinger B., Burr D.B., Ritchie R.O. Proposed pathogenesis for atypical femoral fractures: lessons from materials research. Bone 2013, 55:495-500.
10. Fan Z., Swadener J.G., Rho J.Y., Roy M.E., Pharr G.M. Anisotropic properties of human tibiae cortical bone as measured by nanoindentation. J. Orthop. Res. 2002, 20:806-810.
11. Ferguson V.L., Olesiak S.E. Nanoindentation of bone. Handbook of Nanoindentation with Biological Applications 2010, World Scientific Press. M.L. Oyen (Ed.).
12. Franzoso G., Zysset P.K. Elastic anisotropy of human cortical bone secondary osteons measured by nanoindentation. J. Biomech. Eng. 2009, 131:021001.
13. Fratzl-Zelman N., Roschger P., Gourrier A., Weber M., Misof B.M., Loveridge N., Reeve J., Klaushofer K., Fratzl P. Combination of nanoindentation and quantitative backscattered electron imaging revealed altered bone material properties associated with femoral neck fragility. Calcif. Tissue Int. 2009, 85:335-343.
14. Friedman A.W. Important determinants of bone strength: beyond bone mineral density. J. Clin. Rheumatol. 2006, 12:70-77.
15. Gallant M.A., Brown D.M., Organ J.M., Allen M.R., Burr D.B. Reference-point indentation correlates with bone toughness assessed using whole-bone traditional mechanical testing. Bone 2013, 53:301-305.
16. Glüer C.C., Blake G., Lu Y., Blunt B.A., Jergas M., Genant H.K. Accurate assessment of precision errors: how to measure the reproducibility of bone densitometry techniques. Osteoporos. Int. 1995, 5:262-270.
17. Goldman H.M., Bromage T.G., Boyde A., Thomas C.D.L., Clement J.G. Intrapopulation variability in mineralization density at the human femoral mid-shaft. J. Anat. 2003, 203:243-255.
18. Goldman H.M., Bromage T.G., Thomas C.D., Clement J.G. Preferred collagen fiber orientation in the human mid-shaft femur. Anat. Rec. Part A: Discoveries Mol. Cell. Evol. Biol. 2003, 272:434-445.
19. Gourion-Arsiquaud S., Allen M.R., Burr D.B., Vashishth D., Tang S.Y., Boskey A.L. Bisphosphonate treatment modifies canine bone mineral and matrix properties and their heterogeneity. Bone 2010, 46:666-672.
20. Granke M., Grimal Q., Saied A., Nauleau P., Peyrin F., Laugier P. Change in porosity is the major determinant of the variation of cortical bone elasticity at the millimeter scale in aged women. Bone 2011, 49:1020-1026.
21. Guerri-Fernandez R.C., Nogues X., Quesada Gomez J.M., Torres Del Pliego E., Puig L., Garcia-Giralt N., Yoskovitz G., Mellibovsky L., Hansma P.K., Diez-Perez A. Microindentation for in vivo measurement of bone tissue material properties in atypical femoral fracture patients and controls. J. Bone Miner. Res. 2013, 28:162-168.
22. Hansma P., Turner P., Drake B., Yurtsev E., Proctor A., Mathews P., Lulejian J., Randall C., Adams J., Jungmann R., Garza-de-Leon F., Fantner G., Mkrtchyan H., Pontin M., Weaver A., Brown M.B., Sahar N., Rossello R., Kohn D. The bone diagnostic instrument II: Indentation distance increase. Rev. Sci. Instrum. 2008, 79:064303.
23. Hengsberger S., Enstroem J., Peyrin F., Zysset P. How is the indentation modulus of bone tissue related to its macroscopic elastic response? A validation study. J. Biomech. 2003, 36:1503-1509.
24. Hoffler C.E., Guo X.E., Zysset P.K., Goldstein S.A. An application of nanoindentation technique to measure bone tissue Lamellae properties. J. Biomech. Eng. 2005, 127:1046-1053.
25. Hoffler C.E., Moore K.E., Kozloff K., Zysset P.K., Goldstein S.A. Age, gender, and bone lamellae elastic moduli. J. Orthop. Res. 2000, 18:432-437.
26. 1H NMR compared with high resolution X-ray. PLoS One 2011, 6:e16359.
27. Houde J., Marchetti M., Duquette J., Hoffman A., Steinberg G., Crane G.K., Baran D. Correlation of bone mineral density and femoral neck hardness in bovine and human samples. Calcif. Tissue Int. 1995, 57:201-205.
28. Johnell O., Kanis J.A., Oden A., Johansson H., De Laet C., Delmas P., Eisman J.A., Fujiwara S., Kroger H., Mellstrom D., Meunier P.J., Melton L.J., O'Neill T., Pols H., Reeve J., Silman A., Tenenhouse A. Predictive value of BMD for hip and other fractures. J. Bone Miner. Res. 2005, 20:1185-1194.
29. Kanis J.A., Johnell O., Oden A., Dawson A., De Laet C., Jonsson B. Ten year probabilities of osteoporotic fractures according to BMD and diagnostic thresholds. Osteoporos. Int. 2001, 12:989-995.
30. Keller T.S., Mao Z., Spengler D.M. Young's modulus, bending strength, and tissue physical properties of human compact bone. J. Orthop. Res. 1990, 8:592-603.
31. Koester K.J., Ager J.W., Ritchie R.O. The true toughness of human cortical bone measured with realistically short cracks. Nat. Mater. 2008, 7:672-677.
32. McCalden R.W., McGeough J.A., Barker M.B., Court-Brown 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.
33. Nalla R.K., Stolken J.S., Kinney J.H., Ritchie R.O. Fracture in human cortical bone: local fracture criteria and toughening mechanisms. J. Biomech. 2005, 38:1517-1525.
34. Oei L., Zillikens M.C., Dehghan A., Buitendijk G.H., Castano-Betancourt M.C., Estrada K., Stolk L., Oei E.H., van Meurs J.B., Janssen J.A., Hofman A., van Leeuwen J.P., Witteman J.C., Pols H.A., Uitterlinden A.G., Klaver C.C., Franco O.H., Rivadeneira F. High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control: the Rotterdam Study. Diabetes Care 2013, 36:1619-1628.
35. Rasoulian R., Raeisi Najafi A., Chittenden M., Jasiuk I. Reference point indentation study of age-related changes in porcine femoral cortical bone. J. Biomech. 2013, 46:1689-1696.
36. Rho J.Y., Roy M.E., Tsui T.Y., Pharr G.M. Elastic properties of microstructural components of human bone tissue as measured by nanoindentation. J. Biomed. Mater. Res. 1999, 45:48-54.
37. 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.
38. Ruppel M.E., Miller L.M., Burr D.B. The effect of the microscopic and nanoscale structure on bone fragility. Osteoporos. Int. 2008, 19:1251-1265.
39. Saito M., Marumo K. Bone quality in diabetes. Front. Endocrinol. (Lausanne) 2013, 4:72.
40. Schaffler M.B., Choi K., Milgrom C. Aging and matrix microdamage accumulation in human compact bone. Bone 1995, 17:521-525.
41. Shane E., Burr D., Abrahamsen B., Adler R.A., Brown T.D., Cheung A.M., Cosman F., Curtis J.R., Dell R., Dempster D.W., Ebeling P.R., Einhorn T.A., Genant H.K., Geusens P., Klaushofer K., Lane J.M., McKiernan F., McKinney R., Ng A., Nieves J., O'Keefe R., Papapoulos S., Howe T.S., van der Meulen M.C., Weinstein R.S., Whyte M.P. Atypical subtrochanteric and diaphyseal femoral fractures: second report of a task force of the american society for bone and mineral research. J. Bone Miner. Res. 2014, 29:1-23.
42. Silva M.J., Brodt M.D., Fan Z., Rho J.Y. Nanoindentation and whole-bone bending estimates of material properties in bones from the senescence accelerated mouse SAMP6. J. Biomech. 2004, 37:1639-1646.
43. Thompson W.R. On a criterion for the rejection of observations and the distribution of the ratio of deviation to sample standard deviation. Ann. Math. Stat. 1935, 6:214-219.
44. Turner C.H., Burr D.B. Basic biomechanical measurements of bone: a tutorial. Bone 1993, 14:595-608.
45. Ural A., Vashishth D. Anisotropy of age-related toughness loss in human cortical bone: a finite element study. J. Biomech. 2007, 40:1606-1614.
46. Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes-a meta-analysis. Osteoporos. Int. 2007, 18:427-444.
47. Wang X., Shen X., Li X., Agrawal C.M. Age-related changes in the collagen network and toughness of bone. Bone 2002, 31:1-7.
48. Yoon H.S., Katz J.L. Ultrasonic wave propagation in human cortical bone-II. Measurements of elastic properties and microhardness. J. Biomech. 1976, 9:459-464.
49. Zebaze R.M., Ghasem-Zadeh A., Bohte A., Iuliano-Burns S., Mirams M., Price R.I., Mackie E.J., Seeman E. Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet 2010, 375:1729-1736.
50. Zioupos P., Gresle M., Winwood K. Fatigue strength of human cortical bone: age, physical, and material heterogeneity effects. J. Biomed. Mater. Res. Part A 2008, 86:627-636.
51. Zwierzak I., Baleani M., Viceconti M. Microindentation on cortical human bone: effects of tissue condition and indentation location on hardness values. Proc. Inst. Mech. Eng. Part H J. Eng. Med. 2009, 223:913-918.
52. Zysset P.K., Guo X.E., Hoffler C.E., Moore K.E., Goldstein S.A. Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J. Biomech. 1999, 32:1005-1012.
53. Zysset P.K. Indentation of bone tissue: a short review. Osteoporos. Int. 2009, 20:1049-1055.