Atomic force microscopy and indentation force measurement of bone

Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology

Volumn 1, Issue 6, 2009, Pages 624-649

  Thurner, Philipp J ^a  

^a UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANISOTROPIC SOLIDS; BONE ULTRASTRUCTURE; DERIVED PARAMETERS; MICROSTRUCTURAL ELEMENTS; NANO-INDENTATION MEASUREMENTS; NANOINDENTATION EXPERIMENTS; OLIVER-PHARR METHOD; SELF HEALING EFFECT;

ATOMIC FORCE MICROSCOPY; EXPERIMENTS; NANOINDENTATION; TESTING;

BONE;

ANIMAL; ATOMIC FORCE MICROSCOPY; BONE; FEMUR; HUMAN; METHODOLOGY; NANOTECHNOLOGY; REVIEW; ULTRASTRUCTURE;

ANIMALS; BONE AND BONES; FEMUR; HUMANS; MICROSCOPY, ATOMIC FORCE; NANOTECHNOLOGY;

EID: 77949332733     PISSN: 19395116     EISSN: 19390041     Source Type: Journal    
DOI: 10.1002/wnan.56     Document Type: Article

References (149)

1. Wolff J. Das Gesetz der Transformation der Knochen (The Law of Bone Remodelling). Berlin: Springer- Verlag; 1892.
2. Gao HJ, Ji BH, Jager IL, Arzt E, Fratzl P. Materials become insensitive to flaws at nanoscale: Lessons from nature. Proc Natl Acad Sci U S A 2003, 100:5597-5600.
3. Binnig G, Quate CF, Gerber C. Atomic force microscope. Phys Rev Lett 1986, 56:930-933.
4. Hinterdorfer P, Baumgartner W, Gruber HJ, Schilcher K, Schindler H. Detection and localization of individual antibody-antigen recognition events by atomic force microscopy. Proc Natl Acad Sci U S A 1996, 93:3477-3481.
5. Rief M, Oesterhelt F, Heymann B, Gaub HE. Single molecule force spectroscopy on polysaccharides by atomic force microscopy. Science 1997, 275:1295-1297.
6. Oberhauser AF, Marszalek PE, Carrion-Vazquez M, Fernandez JM. Single protein misfolding events captured by atomic force microscopy. Nat Struct Biol 1999, 6:1025-1028.
7. Newey D, Wilkins MA, Pollock HM. An Ultra-Low- Load Penetration Hardness Tester. J Phys E: Sci Instrum 1982, 15:119-122.
8. Olmeda A, Greco F, Timar J, Malgaroli E. Death rate in patients submitted to the surgical treatment of fracture of the proximal femur. Chir Organi Mov 1995, 80:179-181.
9. Osteoporosis Facts and Figures V1.1. National Osteoporosis Society; 2006, http://www.nos.org.uk/ NetCommunity/admin/Document/Doc?id=47.
10. Praemer A, Furner S, Rice DP. Musculoskeletal Conditions in the United States. American Academy of Orthopaedic Surgeons Rosemont, IL.
11. Accidents, Falls, Fractures and Osteoporosis: A Strategy for Primary Care Groups. National Osteoporosis Society, Bath, UK; 2000.
12. WHO. Assessment of Osteoporotic Fracture Risk and Its Role in Screening for Postmenopausal Osteoporosis. Geneva: World Health Organization; 1994.
13. Ciarelli MJ, Goldstein SA, Kuhn JL, Cody DD, Brown MB. Evaluation of orthogonal mechanical properties and density of human trabecular bone from the major metaphyseal regions with materials testing and computed tomography. J Orthop Res 1991, 9:674-682.
14. Wainwright SA, Marshall LM, Ensrud KE, Cauley JA, Black DM, et al. Hip fracture in women without osteoporosis. J Clin Endocrinol Metab 2005, 90:2787-2793.
15. Muller R. The Zurich experience: one decade of threedimensional high-resolution computed tomography. Top Magn Reson Imaging 2002, 13:307-322.
16. Grynpas MD, Tupy JH, Sodek J. The distribution of soluble, mineral-bound, and matrix-bound proteins in osteoporotic and normal bones. Bone 1994, 15:505-513.
17. Nalla RK, Kruzic JJ, Kinney JH, Ritchie RO. Mechanistic aspects of fracture and R-curve behavior in human cortical bone. Biomaterials 2005, 26:217-231.
18. Weiner S, Traub W. Bone structure: from angstroms to microns. Faseb J 1992, 6:879-885.
19. Weiner S, Wagner HD. The material bone: Structure mechanical function relations. Annu Rev Mater Sci 1998, 28:271-298.
20. Rubin MA, Jasiuk I, Taylor J, Rubin J, Ganey T, et al. TEM analysis of the nanostructure of normal and osteoporotic human trabecular bone. Bone 2003, 33:270-282.
21. Landis WJ, Hodgens KJ, Arena J, Song MJ, Mcewen BF. Structural relations between collagen and mineral in bone as determined by high voltage electron microscopic tomography. Microsc Res Tech 1996, 33:192-202.
22. Mckee MD, Nanci A. Osteopontin at mineralized tissue interfaces in bone, teeth, and osseointegrated implants: ultrastructural distribution and implications for mineralized tissue formation, turnover, and repair. Microsc Res Tech 1996, 33:141-164.
23. Nanci A. Content and distribution of noncollagenous matrix proteins in bone and cementum: relationship to speed of formation and collagen packing density. J Struct Biol 1999, 126:256-269.
24. Carden A, Morris MD. Application of vibrational spectroscopy to the study of mineralized tissues (review). J Biomed Opt 2000, 5:259-268.
25. Boskey A, Pleshko Camacho N. FT-IR imaging of native and tissue-engineered bone and cartilage. Biomaterials 2007, 28:2465-2478.
26. Baselt DR, Revel JP, Baldeschwieler JD. Subfibrillar structure of type I collagen observed by atomic force microscopy. Biophys J 1993, 65:2644-2655.
27. Revenko I, Sommer F, Minh DT, Garrone R, Franc JM. Atomic force microscopy study of the collagen fibre structure. Biol Cell 1994, 80:67-69.
28. Hodge AJ, Petruska JA. Recent studies with the electron microscope on ordered aggregates of the tropocollagen molecule. In: Ramachandran GN ed. Aspects of Protein Structure. New York: Academic Press; 1963, 289-300.
29. Bozec L, van der Heijden G, Horton M. Collagen fibrils: nanoscale ropes. Biophys J 2007, 92:70-75.
30. Gutsmann T, Fantner GE, Venturoni M, Ekani-nkodo A, Thompson JB, et al. Evidence that collagen fibrils in tendons are inhomogeneously structured in a tubelike manner. Biophys J 2003, 84:2593-2598.
31. Gutsmann T, Fantner GE, Kindt JH, Venturoni M, Danielsen S, et al. Force spectroscopy of collagen fibers to investigate their mechanical properties and structural organization. Biophys J 2004, 86:3186-3193.
32. Graham JS, Vomund AN, Phillips CL, Grandbois M. Structural changes in human type I collagen fibrils investigated by force spectroscopy. Exp Cell Res 2004, 299:335-342.
33. Shaw GA, McDaniel DP, Elliott JT, Tona A, Plant AL. Mechanical stability of collagen fibril networks. In: Bushby AJ, Ferguson VL, Ko CC, Oyen ML. eds. Materials Research Society Symposium Proceedings. Boston: Materials Research Society; 2005, L15.02.1-L15.02.6.
34. Bouchiat C, Wang MD, Allemand J, Strick T, Block SM, et al. Estimating the persistence length of a worm-like chain molecule from force-extension measurements. Biophys J 1999, 76:409-413.
35. Bustamante C, Marko JF, Siggia ED, Smith S. Entropic elasticity of lambda-phage DNA. Science 1994, 265:1599-1600.
36. Marszalek PE, Oberhauser AF, Pang YP, Fernandez JM. Polysaccharide elasticity governed by chair-boat transitions of the glucopyranose ring. Nature 1998, 396:661-664.
37. Thurner PJ, Oroudjev E, Jungmann R, Kreutz C, Kindt JH, et al. Imaging of bone ultrastructure using atomic force microscopy. In: Mendez-Vilas A, Diaz J. eds. Modern Research and Educational Topics in Microscopy. Formatex, Badajoz, Spain; 2007, 37-48.
38. Tong W, Glimcher MJ, Katz JL, Kuhn L, Eppell SJ. Size and shape of mineralites in young bovine bone measured by atomic force microscopy. Calcif Tissue Int 2003, 72:592-598.
39. Fantner GE, Adams J, Turner P, Thurner PJ, Fisher LW, et al. Nanoscale ion mediated networks in bone: osteopontin can repeatedly dissipate large amounts of energy. Nano Lett 2007, 7:2491-2498.
40. Barragan-Adjemian C, Nicolella D, Dusevich V, DallasMR, Eick JD, et al. Mechanism by which MLO-A5 late osteoblasts/early osteocytes mineralize in culture: similarities with mineralization of lamellar bone. Calcif Tissue Int 2006, 79:340-353.
41. Baranauskas V, Garavello-Freitas I, Jingguo Z, Cruz-hofling MA. Observation of the bone matrix structure of intact and regenerative zones of tibias by atomic force microscopy. J Vac Sci Technol A 2001, 19:1042-1045.
42. Balooch M, Habelitz S, Kinney JH, Marshall SJ, Marshall GW. Mechanical properties of mineralized collagen fibrils as influenced by demineralization. J Struct Biol 2008, 162:404-410.
43. Bozec L, de Groot J, Odlyha M, Nicholls B, Horton MA.Mineralised tissues as nanomaterials: analysis by atomic force microscopy. IEE Proc Nanobiotechnol 2005, 152:183-186.
44. Bozec L, de Groot J, Odlyha M, Nicholls B, Nesbitt S, et al. Atomic force microscopy of collagen structure in bone and dentine revealed by osteoclastic resorption. Ultramicroscopy 2005, 105:79-89.
45. Eppell SJ, Tong W, Katz JL, Kuhn L, Glimcher MJ. Shape and size of isolated bone mineralites measured using atomic force microscopy. J Orthop Res 2001, 19:1027-1034.
46. Hassenkam T, Fantner GE, Cutroni JA, Weaver JC, Morse DE, et al. High-resolution AFM imaging of intact and fractured trabecular bone. Bone 2004, 35:4-10.
47. Hassenkam T, Jorgensen HL, Lauritzen JB. Mapping the imprint of bone remodeling by atomic force microscopy. Anat Rec A Discov Mol Cell Evol Biol 2006, 288:1087-1094.
48. Knapp HF, Reilly GC, Stemmer A, Niederer P, Knothe T. Development of preparation methods for and insights obtained from atomic force microscopy of fluid spaces in cortical bone. Scanning 2002, 24:25-33.
49. Sasaki N, Tagami A, Goto T, Taniguchi M, Nakata M, et al. Atomic force microscopic studies on the structure of bovine femoral cortical bone at the collagen fibril-mineral level. J Mater Sci Mater Med 2002, 13:333-337.
50. Habelitz S, Balooch M, Marshall SJ, Balooch G, Marshall GW Jr. In situ atomic force microscopy of partially demineralized human dentin collagen fibrils. J Struct Biol 2002, 138:227-236.
51. Kindt JH, Thurner PJ, Lauer ME, Bosma BL, Schitter G, et al. In situ observation of fluoride-ion-induced hydroxyapatite-collegen detachment on bone fracture surfaces by atomic forcemicroscopy. Nanotechnology 2007, 18:.1 .8 135102-135102.
52. Rho JY, Tsui TY, Pharr GM. Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. Biomaterials 1997, 18:1325-1330.
53. Rho, JY, ME Roy, 2nd, TY Tsui, and GM Pharr, Elastic properties of microstructural components of human bone tissue as measured by nanoindentation. J Biomed Mater Res 1999, 45:48-54.
54. Goodwin KJ, Sharkey NA. Material properties of interstitial lamellae reflect local strain environments. J Orthop Res 2002, 20:600-606.
55. Fan Z, Swadener JG, Rho JY, Roy ME, Pharr GM. Anisotropic properties of human tibial cortical bone as measured by nanoindentation. J Orthop Res 2002, 20:806-810.
56. Fan Z, Rho JY. Effects of viscoelasticity and timedependent plasticity on nanoindentation measurements of human cortical bone. J Biomed Mater Res A 2003, 67:208-214.
57. Lewis G, Xu J, Dunne N, Daly C, Orr J. Critical comparison of two methods for the determination of nanomechanical properties of a material: application to synthetic and natural biomaterials. J BiomedMater Res B Appl Biomater 2006, 78:312-317.
58. Fan Z, Smith PA, Eckstein EC, Harris GF. Mechanical properties of OI type III bone tissue measured by nanoindentation. J Biomed Mater Res A 2006, 79:71-77.
59. Hoffler CE, Moore KE, Kozloff K, Zysset PK, Brown MB, et al. Heterogeneity of bone lamellar-level elastic moduli. Bone 2000, 26:603-609.
60. Roy ME, Rho JY, Tsui TY, Evans ND, Pharr GM. Mechanical and morphological variation of the human lumbar vertebral cortical and trabecular bone. J BiomedMater Res 1999, 44:191-197.
61. Zysset PK, Guo XE, Hoffler CE,Moore KE, Goldstein SA. Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J Biomech 1999, 32:1005-1012.
62. Turner CH, Rho J, Takano Y, Tsui TY, Pharr GM. The elastic properties of trabecular and cortical bone tissues are similar: results from two microscopic measurement techniques. J Biomech 1999, 32:437-441.
63. Rho JY, Zioupos P, Currey JD, Pharr GM. Variations in the individual thick lamellar properties within osteons by nanoindentation. Bone 1999, 25:295-300.
64. Xu J, Rho JY, Mishra SR, Fan Z. Atomic force microscopy and nanoindentation characterization of human lamellar bone prepared by microtome sectioning and mechanical polishing technique. J Biomed Mater Res A 2003, 67:719-726.
65. Hofmann T, Heyroth F, Meinhard H, Franzel W, Raum K. Assessment of composition and anisotropic elastic properties of secondary osteon lamellae. J Biomech 2006, 39:2282-2294.
66. Zioupos P. In vivo fatigue microcracks in human bone: material properties of the surrounding bone matrix. Eur J Morphol 2005, 42:31-41.
67. Zysset PK, Guo XE, Hoffler CE, Moore KE, Goldstein SA. Mechanical properties of human trabecular bone lamellae quantified by nanoindentation. Technol Health Care 1998, 6:429-432.
68. Hengsberger S, Kulik A, Zysset P. Nanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological conditions. Bone 2002, 30:178-184.
69. Ferguson VL, Bushby AJ, Boyde A. Nanomechanical properties and mineral concentration in articular calcified cartilage and subchondral bone. J Anat 2003, 203:191-202.
70. Hengsberger S, Kulik A, Zysset P. A combined atomic force microscopy and nanoindentation technique to investigate the elastic properties of bone structural units. Eur Cell Mater 2001, 1:12-17.
71. Norman J, Shapter JG, Short K, Smith LJ, Fazzalari NL.Micromechanical properties of human trabecular bone: A hierarchical investigation using nanoindentation. J Biomed Mater Res A 2007, 87:196-202.
72. Chevalier Y, Pahr D, Allmer H, Charlebois M, Zysset P. Validation of a voxel-based FE method for prediction of the uniaxial apparent modulus of human trabecular bone using macroscopic mechanical tests and nanoindentation. J Biomech 2007, 40:3333-3340.
73. Wang X, Sudhaker Rao D, Ajdelsztajn L, Ciarelli TE, Lavernia EJ, et al. Human iliac crest cancellous bone elastic modulus and hardness differ with bone formation rate per bone surface but not by existence of prevalent vertebral fracture. J Biomed Mater Res B Appl Biomater 2008, 85:68-77.
74. Gupta HS, Schratter S, Tesch W, Roschger P, Berzlanovich A, et al. Two different correlations between nanoindentation modulus and mineral content in the bone-cartilage interface. J Struct Biol 2005, 149:138-148.
75. Fan Z, Smith PA, Harris GF, Rauch F, Bajorunaite R. Comparison of nanoindentation measurements between osteogenesis imperfecta Type III and Type IV and between different anatomic locations (femur/tibia versus iliac crest). Connect Tissue Res 2007, 48:70-75.
76. 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, 48:407-413.
77. Tye CE, Hunter GK, Goldberg HA. Identification of the type I collagen-binding domain of bone sialoprotein and characterization of the mechanism of interaction. J Biol Chem2005, 280:13487-13492.
78. Hunter GK, Goldberg HA. Nucleation of hydroxyapatite by bone sialoprotein. Proc Natl Acad Sci U S A 1993, 90:8562-8565.
79. Ingram RT, Clarke BL, Fisher LW, Fitzpatrick LA. Distribution of noncollagenous proteins in the matrix of adult human bone: evidence of anatomic and functional heterogeneity. J Bone Miner Res 1993, 8:1019-1029.
80. Young, MF, JM Kerr, K Ibaraki, AM Heegaard, and PG Robey, Structure, expression, and regulation of the major noncollagenous matrix proteins of bone. Clin Orthop Relat Res, 1992, 281:275-294.
81. George A, Hao J. Role of phosphophoryn in dentin mineralization. Cells Tissues Organs 2005, 181:232-240.
82. Qiu SR, Wierzbicki A, Orme CA, Cody AM, Hoyer JR, et al. Molecular modulation of calcium oxalate crystallization by osteopontin and citrate. Proc Natl Acad Sci U S A 2004, 101:1811-1815.
83. Habelitz S, Kullar A, Marshall SJ, DenBesten PK, Balooch M, et al. Amelogenin-guided crystal growth on fluoroapatite glass-ceramics. J Dent Res 2004, 83:698-702.
84. Zappone B, Thurner P, Adams J, FantnerGE, Hansma PK. Effect of Ca2+ ions on the adhesion and mechanical properties of adsorbed layers of human Osteopontin. Biophys J 2008, 95:2939-50.
85. Adams J, Fantner GE, Fisher LW, Hansma PK.Molecular energy dissipation in nanoscale networks of dentin matrix protein 1 is strongly dependent on ion valence. Nanotechnology 2008, 19:384008-340015.
86. Fantner GE, Oroudjev E, Schitter G, Golde LS, Thurner P, et al. Sacrificial bonds and hidden length: Unraveling molecular mesostructures in tough materials. Biophys J 2006, 90:1411-1418.
87. Fantner GE, Hassenkam T, Kindt JH, Weaver JC, Birkedal H, et al. Sacrificial bonds and hidden length dissipate energy as mineralized fibrils separate during bone fracture. Nat Mater 2005, 4:612-616.
88. Hansma PK, Fantner GE, Kindt JH, Thurner PJ, Schitter G, et al. Sacrificial bonds in the interfibrillarmatrix of bone. J Musculoskelet Neuronal Interact 2005, 5:313-315.
89. Thompson JB, Kindt JH, Drake B, Hansma HG, Morse DE, et al. Bone indentation recovery time correlates with bond reforming time. Nature 2001, 414:773-776.
90. Tai K, Qi HJ, Ortiz C. Effect of mineral content on the nanoindentation properties and nanoscale deformation mechanisms of bovine tibial cortical bone. J Mater Sci Mater Med 2005, 16:947-959.
91. Fantner GE, Rabinovych O, Schitter G, Thurner P, Kindt JH, et al. Hierarchical interconnections in the nano-composite material bone: Fibrillar cross-links resist fracture on several length scales. Compos Sci Technol 2006, 66:1205-1211.
92. TaoNJ, Lindsay SM, Lees S. Measuring the microelastic properties of biological material. Biophys J 1992, 63:1165-1169.
93. Fantner GE, Birkedal H, Kindt JH, Hassenkam T, Weaver JC, et al. Influence of the degradation of the organic matrix on the microscopic fracture behavior of trabecular bone. Bone 2004, 35:1013-1022.
94. Hassenkam T, Jorgensen HL, Pedersen MB, Kourakis AH, Simonsen L, et al. Atomic force microscopy on human trabecular bone from an old woman with osteoporotic fractures. Micron 2005, 36:681-687.
95. Thurner PJ, Lam S, Weaver JC, Morse DE, et al. Localization of phosphorylated serine, osteopontin, and bone sialoprotein on mineralized collagen fibrils in bone. J Adhes 2009, 85:526-545.
96. Xu S, Yu JJ. Beneath the minerals, a layer of round lipid particles was identified to mediate collagen calcification in compact bone formation. Biophys J 2006, 91:4221-4229.
97. Tye CE, Rattray KR, Warner KJ, Gordon JA, Sodek J, et al. Delineation of the hydroxyapatite-nucleating domains of bone sialoprotein. J Biol Chem 2003, 278:7949-7955.
98. Lane NE, Yao W, Kinney JH, Modin G, Balooch M, et al. Both hPTH(1-34) and bFGF increase trabecular bone mass in osteopenic rats but they have different effects on trabecular bone architecture. J Bone Miner Res 2003, 18:2105-2115.
99. Hengsberger S, Ammann P, Legros B, Rizzoli R, Zysset P. Intrinsic bone tissue properties in adult rat vertebrae: modulation by dietary protein. Bone 2005, 36:134-141.
100. Balooch G, Balooch M, Nalla RK, Schilling S, Filvaroff EH, et al. TGF-beta regulates the mechanical properties and composition of bone matrix. Proc Natl Acad Sci U S A 2005, 102:18813-18818.
101. Donnelly E, Baker SP, Boskey AL, van der Meulen MC. Effects of surface roughness and maximum load on the mechanical properties of cancellous bone measured by nanoindentation. J Biomed Mater Res A 2006, 77:426-435.
102. Zhang Y, Cui FZ, Wang XM, Feng QL, Zhu XD. Mechanical properties of skeletal bone in genemutated stopsel(dtl128d) and wild-type zebrafish (Danio rerio) measured by atomic force microscopybased nanoindentation. Bone 2002, 30:541-546.
103. Pelled G, Tai K, Sheyn D, Zilberman Y, Kumbar S, et al. Structural and nanoindentation studies of stem cell-based tissue-engineered bone. J Biomech 2007, 40:399-411.
104. Wenger MP, Bozec L, Horton MA, Mesquida P. Mechanical properties of collagen fibrils. Biophys J 2007, 93:1255-1263.
105. Oliver WC, Pharr GM. An Improved Technique for Determining Hardness and Elastic-Modulus Using Load and Displacement Sensing Indentation Experiments. J Mater Res 1992, 7:1564-1583.
106. Oliver WC, Pharr GM. Measurement of hardness and elastic modulus by instrumented indentation: Advances in understanding and refinements to methodology. Journal of Materials Research 2004, 19:3-20.
107. Sneddon IN. The relation between load and penetration in the axisymmetric boussinesq problem for a punch of arbitrary profile. Int J Eng Sci 1965, 3:47-57.
108. Swadener JG, Rho JY, Pharr GM. Effects of anisotropy on elastic moduli measured by nanoindentation in human tibial cortical bone. J Biomed Mater Res 2001, 57:108-112.
109. Carter DR, Hayes WC. Bone compressive strength: the influence of density and strain rate. Science 1976, 194:1174-1176.
110. Mittra E, Akella S, Qin YX. The effects of embedding material, loading rate and magnitude, and penetration depth in nanoindentation of trabecular bone. J Biomed Mater Res A 2006, 79:86-93.
111. Pharr GM, Oliver WC, Brotzen FR. On the Generality of the Relationship among Contact Stiffness, Contact Area, and Elastic-Modulus during Indentation. Journal of Materials Research 1992, 7:613-617.
112. Reilly DT, Burstein AH, Frankel VH. The elastic modulus for bone. J Biomech 1974, 7:271-275.
113. Swadener JG, Pharr GM. Indentation of elastically anisotropic half-spaces by cones and parabolae of revolution. Philos Mag A 2001, 81:447-466.
114. Vlassak JJ, Ciavarella M, Barber JR, Wang X. The indentation modulus of elastically anisotropic materials for indenters of arbitrary shape. J Mech Phys Solids 2003, 51:1701-1721.
115. Delafargue A, Ulm FJ. Explicit approximations of the indentation modulus of elastically orthotropic solids for conical indenters. Int J Solids Struct 2004, 41:7351-7360.
116. Fan Z, Rho J, Swadener JG. Three-dimensional finite element analysis of the effects of anistropy on bone mechanical properties measured by nanoindentation. Journal of Materials Research 2004, 19:114-123.
117. Oyen ML. Nanoindentation hardness of mineralized tissues. J Biomech 2006, 39:2699-2702.
118. Tang B, Ngan AH, Lu WW. An improved method for the measurement of mechanical properties of bone by nanoindentation. J Mater Sci Mater Med 2007, 18:1875-1881.
119. ChangMC, Ko CC, Liu CC, DouglasWH, DeLong R, et al. Elasticity of alveolar bone near dental implantbone interfaces after one month's healing. J Biomech 2003, 36:1209-1214.
120. Mulder L, Koolstra JH, den Toonder JM, van Eijden TM. Relationship between tissue stiffness and degree of mineralization of developing trabecular bone. J Biomed Mater Res A 2008, 84:508-515.
121. Guo L, Guo X, Leng Y, Cheng JC, Zhang X. Nanoindentation study of interfaces between calcium phosphate and bone in an animal spinal fusion model. J BiomedMater Res 2001, 54:554-559.
122. Lane NE, Yao W, Balooch M, Nalla RK, Balooch G, et al. Glucocorticoid-treated mice have localized changes in trabecular bone material properties and osteocyte lacunar size that are not observed in placebo-treated or estrogen-deficient mice. J Bone Miner Res 2006, 21:466-476.
123. Mankani MH, Kuznetsov SA, Wolfe RM, Marshall GW, Robey PG. In vivo bone formation by human bone marrow stromal cells: reconstruction of the mouse calvarium and mandible. Stem Cells 2006, 24:2140-2149.
124. Chen Q, Rho JY, Fan Z, Laulederkind SJ, Raghow R. Congenital lack of COX-2 affects mechanical and geometric properties of bone in mice. Calcif Tissue Int 2003, 73:387-392.
125. Silva MJ, Brodt MD, Fan Z, Rho JY. Nanoindentation and whole-bone bending estimates of material properties in bones from the senescence accelerated mouse SAMP6. J Biomech 2004, 37:1639-1646.
126. Akhter MP, Fan Z, Rho JY. Bone intrinsic material properties in three inbred mouse strains. Calcif Tissue Int 2004, 75:416-420.
127. Kavukcuoglu NB, Denhardt DT, Guzelsu N, Mann AB. Osteopontin deficiency and aging on nanomechanics of mouse bone. J BiomedMater Res A 2007, 83:136-144.
128. Miller LM, Little W, Schirmer A, Sheik F, Busa B, et al. Accretion of bone quantity and quality in the developing mouse skeleton. J Bone Miner Res 2007, 22:1037-1045.
129. Jiao Y, Chiu H, Fan Z, Jiao F, Eckstein EC, et al. Quantitative trait loci that determine mouse tibial nanoindentation properties in an F2 population derived from C57BL/6J x C3H/HeJ. Calcif Tissue Int 2007, 80:383-390.
130. Guo XE, Goldstein SA. Vertebral trabecular bone microscopic tissue elastic modulus and hardness do not change in ovariectomized rats. JOrthop Res 2000, 18:333-336.
131. Jamsa T, Rho JY, Fan Z, MacKay CA, Marks SC Jr, et al. Mechanical properties in long bones of rat osteopetrotic mutations. J Biomech 2002, 35:161-165.
132. Leong PL,Morgan EF.Measurement of fracture callus material properties via nanoindentation. Acta Biomater 2008, 4:1569-75.
133. Ammann P, Badoud I, Barraud S, Dayer R, Rizzoli R. Strontium ranelate treatment improves trabecular and cortical intrinsic bone tissue quality, a determinant of bone strength. J Bone Miner Res 2007, 22:1419-1425.
134. Wang X, Allen MR, Burr DB, Lavernia EJ, Jeremic B, et al. Identification of material parameters based on Mohr-Coulomb failure criterion for bisphosphonate treated canine vertebral cancellous bone. Bone 2008, 43:775-80.
135. 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.
136. Rho JY, Pharr GM. Effects of drying on the mechanical properties of bovine femur measured by nanoindentation. JMater Sci Mater Med 1999, 10:485-488.
137. Hoc T, Henry L, Verdier M, Aubry D, Sedel L, et al. Effect of microstructure on the mechanical properties of Haversian cortical bone. Bone 2006, 38:466-474.
138. Tai K, Dao M, Suresh S, Palazoglu A, Ortiz C. Nanoscale heterogeneity promotes energy dissipation in bone. Nat Mater 2007, 6:454-462.
139. Akhtar R, Daymond MR, Almer JD, Mummery PM. Elastic strains in antler trabecular bone determined by synchrotron X-ray diffraction. Acta Biomater 2008, 4:1677-87.
140. Rho JY, Currey JD, Zioupos P, Pharr GM. The anisotropic Young's modulus of equine secondary osteones and interstitial bone determined by nanoindentation. J Exp Biol 2001, 204:1775-1781.
141. Roy ME, Nishimoto SK, Rho JY, Bhattacharya SK, Lin JS, et al. Correlations between osteocalcin content, degree of mineralization, and mechanical properties of C. carpio rib bone. J BiomedMaterRes 2001, 54:547-553.
142. Rho JY, Mishra SR, Chung K, Bai J, Pharr GM. Relationship between ultrastructure and the nanoindentation properties of intramuscular herring bones. Ann Biomed Eng 2001, 29:1082-1088.
143. Wang XM, Cui FZ,Ge J, Zhang Y, Ma C. Variation of nanomechanical properties of bone by gene mutation in the zebrafish. Biomaterials 2002, 23:4557-4563.
144. Mullins LP, Bruzzi MS, McHugh PE. Measurement of the microstructural fracture toughness of cortical bone using indentation fracture. J Biomech 2007, 40:3285-3288.
145. Balooch G, Marshall GW, Marshall SJ, Warren OL, Asif SA, et al. Evaluation of a new modulus mapping technique to investigate microstructural features of human teeth. J Biomech 2004, 37:1223-1232.
146. Wang X, Yoon YJ, Ji H. A novel scratching approach for measuring age-related changes in the in situ toughness of bone. J Biomech 2007, 40:1401-1404.
147. Hansma PK, Turner PJ, Fantner GE. Bone diagnostic instrument. Rev Sci Instrum 2006, 77.
148. Hansma P, Turner P, Drake B, Yurtsev E, Proctor A, et al. The bone diagnostic instrument II: indentation distance increase. Rev Sci Instrum 2008, 79:064303.
149. Sahin O, Magonov S, Su C, Quate CF, Solgaard O. An atomic force microscope tip designed to measure time-varying nanomechanical forces. Nat Nanotechnol 2007, 2:507-514.