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Erschienen in: Current Osteoporosis Reports 4/2016

04.06.2016 | Biomechanics (M Silva and K Jepsen, Section Editors)

Tissue-Level Mechanical Properties of Bone Contributing to Fracture Risk

verfasst von: Jeffry S. Nyman, Mathilde Granke, Robert C. Singleton, George M. Pharr

Erschienen in: Current Osteoporosis Reports | Ausgabe 4/2016

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Abstract

Tissue-level mechanical properties characterize mechanical behavior independently of microscopic porosity. Specifically, quasi-static nanoindentation provides measurements of modulus (stiffness) and hardness (resistance to yielding) of tissue at the length scale of the lamella, while dynamic nanoindentation assesses time-dependent behavior in the form of storage modulus (stiffness), loss modulus (dampening), and loss factor (ratio of the two). While these properties are useful in establishing how a gene, signaling pathway, or disease of interest affects bone tissue, they generally do not vary with aging after skeletal maturation or with osteoporosis. Heterogeneity in tissue-level mechanical properties or in compositional properties may contribute to fracture risk, but a consensus on whether the contribution is negative or positive has not emerged. In vivo indentation of bone tissue is now possible, and the mechanical resistance to microindentation has the potential for improving fracture risk assessment, though determinants are currently unknown.
Literatur
1.
Zurück zum Zitat Miller LM, Little W, Schirmer A, Sheik F, Busa B, Judex S. Accretion of bone quantity and quality in the developing mouse skeleton. J Bone Miner Res. 2007;22(7):1037–45.CrossRefPubMed Miller LM, Little W, Schirmer A, Sheik F, Busa B, Judex S. Accretion of bone quantity and quality in the developing mouse skeleton. J Bone Miner Res. 2007;22(7):1037–45.CrossRefPubMed
2.
Zurück zum Zitat Donnelly E, Boskey AL, Baker SP, van der Meulen MC. Effects of tissue age on bone tissue material composition and nanomechanical properties in the rat cortex. J Biomed Mater Res A. 2010;92(3):1048–56.PubMedPubMedCentral Donnelly E, Boskey AL, Baker SP, van der Meulen MC. Effects of tissue age on bone tissue material composition and nanomechanical properties in the rat cortex. J Biomed Mater Res A. 2010;92(3):1048–56.PubMedPubMedCentral
3.
Zurück zum Zitat Burket J, Gourion-Arsiquaud S, Havill LM, Baker SP, Boskey AL, van der Meulen MC. Microstructure and nanomechanical properties in osteons relate to tissue and animal age. J Biomech. 2011;44(2):277–84.CrossRefPubMed Burket J, Gourion-Arsiquaud S, Havill LM, Baker SP, Boskey AL, van der Meulen MC. Microstructure and nanomechanical properties in osteons relate to tissue and animal age. J Biomech. 2011;44(2):277–84.CrossRefPubMed
4.•
Zurück zum Zitat Raghavan M, Sahar ND, Kohn DH, Morris MD. Age-specific profiles of tissue-level composition and mechanical properties in murine cortical bone. Bone. 2012;50(4):942–53. The relationships between compositional and tissue-level mechanical properties change with advance aging in mice.CrossRefPubMedPubMedCentral Raghavan M, Sahar ND, Kohn DH, Morris MD. Age-specific profiles of tissue-level composition and mechanical properties in murine cortical bone. Bone. 2012;50(4):942–53. The relationships between compositional and tissue-level mechanical properties change with advance aging in mice.CrossRefPubMedPubMedCentral
5.
Zurück zum Zitat Pathak S, Vachhani SJ, Jepsen KJ, Goldman HM, Kalidindi SR. Assessment of lamellar level properties in mouse bone utilizing a novel spherical nanoindentation data analysis method. J Mech Behav Biomed Mater. 2012;13:102–17.CrossRefPubMedPubMedCentral Pathak S, Vachhani SJ, Jepsen KJ, Goldman HM, Kalidindi SR. Assessment of lamellar level properties in mouse bone utilizing a novel spherical nanoindentation data analysis method. J Mech Behav Biomed Mater. 2012;13:102–17.CrossRefPubMedPubMedCentral
6.
Zurück zum Zitat Wu Z, Ovaert TC, Niebur GL. Viscoelastic properties of human cortical bone tissue depend on gender and elastic modulus. J Orthop Res. 2012;30(5):693–9.CrossRefPubMed Wu Z, Ovaert TC, Niebur GL. Viscoelastic properties of human cortical bone tissue depend on gender and elastic modulus. J Orthop Res. 2012;30(5):693–9.CrossRefPubMed
7.•
Zurück zum Zitat Zhang R, Gong H, Zhu D, Ma R, Fang J, Fan Y. Multi-level femoral morphology and mechanical properties of rats of different ages. Bone. 2015;76:76–87. Tissue-level modulus and hardness increases with skeletal maturation but not with advanced aging in rodents.CrossRefPubMed Zhang R, Gong H, Zhu D, Ma R, Fang J, Fan Y. Multi-level femoral morphology and mechanical properties of rats of different ages. Bone. 2015;76:76–87. Tissue-level modulus and hardness increases with skeletal maturation but not with advanced aging in rodents.CrossRefPubMed
8.
Zurück zum Zitat Lewis G, Nyman JS. The use of nanoindentation for characterizing the properties of mineralized hard tissues: state-of-the art review. J Biomed Mater Res B Appl Biomater. 2008;87(1):286–301.CrossRefPubMed Lewis G, Nyman JS. The use of nanoindentation for characterizing the properties of mineralized hard tissues: state-of-the art review. J Biomed Mater Res B Appl Biomater. 2008;87(1):286–301.CrossRefPubMed
9.
Zurück zum Zitat Thurner PJ. Atomic force microscopy and indentation force measurement of bone. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2009;1(6):624–49.CrossRefPubMed Thurner PJ. Atomic force microscopy and indentation force measurement of bone. Wiley Interdiscip Rev Nanomed Nanobiotechnol. 2009;1(6):624–49.CrossRefPubMed
10.
Zurück zum Zitat Liu XS, Stein EM, Zhou B, Zhang CA, Nickolas TL, Cohen A, et al. Individual trabecula segmentation (ITS)-based morphological analyses and microfinite element analysis of HR-pQCT images discriminate postmenopausal fragility fractures independent of DXA measurements. J Bone Miner Res. 2012;27(2):263–72.CrossRefPubMedPubMedCentral Liu XS, Stein EM, Zhou B, Zhang CA, Nickolas TL, Cohen A, et al. Individual trabecula segmentation (ITS)-based morphological analyses and microfinite element analysis of HR-pQCT images discriminate postmenopausal fragility fractures independent of DXA measurements. J Bone Miner Res. 2012;27(2):263–72.CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Nishiyama KK, Macdonald HM, Hanley DA, Boyd SK. Women with previous fragility fractures can be classified based on bone microarchitecture and finite element analysis measured with HR-pQCT. Osteoporos Int. 2013;24(5):1733–40.CrossRefPubMed Nishiyama KK, Macdonald HM, Hanley DA, Boyd SK. Women with previous fragility fractures can be classified based on bone microarchitecture and finite element analysis measured with HR-pQCT. Osteoporos Int. 2013;24(5):1733–40.CrossRefPubMed
12.
Zurück zum Zitat Chang G, Honig S, Liu Y, Chen C, Chu KK, Rajapakse CS, et al. 7 Tesla MRI of bone microarchitecture discriminates between women without and with fragility fractures who do not differ by bone mineral density. J Bone Miner Metab. 2015;33(3):285–93.CrossRefPubMed Chang G, Honig S, Liu Y, Chen C, Chu KK, Rajapakse CS, et al. 7 Tesla MRI of bone microarchitecture discriminates between women without and with fragility fractures who do not differ by bone mineral density. J Bone Miner Metab. 2015;33(3):285–93.CrossRefPubMed
13.
Zurück zum Zitat Bergot C, Laval-Jeantet AM, Hutchinson K, Dautraix I, Caulin F, Genant HK. A comparison of spinal quantitative computed tomography with dual energy X-ray absorptiometry in European women with vertebral and nonvertebral fractures. Calcif Tissue Int. 2001;68(2):74–82.CrossRefPubMed Bergot C, Laval-Jeantet AM, Hutchinson K, Dautraix I, Caulin F, Genant HK. A comparison of spinal quantitative computed tomography with dual energy X-ray absorptiometry in European women with vertebral and nonvertebral fractures. Calcif Tissue Int. 2001;68(2):74–82.CrossRefPubMed
14.•
Zurück zum Zitat Orwoll ES, Marshall LM, Nielson CM, Cummings SR, Lapidus J, Cauley JA, et al. Finite element analysis of the proximal femur and hip fracture risk in older men. J Bone Miner Res. 2009;24(3):475–83. There is overlap in predicted hip strength between fragility fracture cases and non-fracture cases suggesting the tissue quality is also important to fracture risk.CrossRefPubMed Orwoll ES, Marshall LM, Nielson CM, Cummings SR, Lapidus J, Cauley JA, et al. Finite element analysis of the proximal femur and hip fracture risk in older men. J Bone Miner Res. 2009;24(3):475–83. There is overlap in predicted hip strength between fragility fracture cases and non-fracture cases suggesting the tissue quality is also important to fracture risk.CrossRefPubMed
15.
Zurück zum Zitat Chang G, Honig S, Brown R, Deniz CM, Egol KA, Babb JS, et al. Finite element analysis applied to 3-T MR imaging of proximal femur microarchitecture: lower bone strength in patients with fragility fractures compared with control subjects. Radiology. 2014;272(2):464–74.CrossRefPubMedPubMedCentral Chang G, Honig S, Brown R, Deniz CM, Egol KA, Babb JS, et al. Finite element analysis applied to 3-T MR imaging of proximal femur microarchitecture: lower bone strength in patients with fragility fractures compared with control subjects. Radiology. 2014;272(2):464–74.CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Nishiyama KK, Ito M, Harada A, Boyd SK. Classification of women with and without hip fracture based on quantitative computed tomography and finite element analysis. Osteoporos Int. 2014;25(2):619–26.CrossRefPubMed Nishiyama KK, Ito M, Harada A, Boyd SK. Classification of women with and without hip fracture based on quantitative computed tomography and finite element analysis. Osteoporos Int. 2014;25(2):619–26.CrossRefPubMed
17.
Zurück zum Zitat Chevalley T, Bonjour JP, van Rietbergen B, Ferrari S, Rizzoli R. Fracture history of healthy premenopausal women is associated with a reduction of cortical microstructural components at the distal radius. Bone. 2013;55(2):377–83.CrossRefPubMed Chevalley T, Bonjour JP, van Rietbergen B, Ferrari S, Rizzoli R. Fracture history of healthy premenopausal women is associated with a reduction of cortical microstructural components at the distal radius. Bone. 2013;55(2):377–83.CrossRefPubMed
18.
Zurück zum Zitat Imai K, Ohnishi I, Matsumoto T, Yamamoto S, Nakamura K. Assessment of vertebral fracture risk and therapeutic effects of alendronate in postmenopausal women using a quantitative computed tomography-based nonlinear finite element method. Osteoporos Int. 2009;20(5):801–10.CrossRefPubMed Imai K, Ohnishi I, Matsumoto T, Yamamoto S, Nakamura K. Assessment of vertebral fracture risk and therapeutic effects of alendronate in postmenopausal women using a quantitative computed tomography-based nonlinear finite element method. Osteoporos Int. 2009;20(5):801–10.CrossRefPubMed
19.
Zurück zum Zitat Graeff C, Marin F, Petto H, Kayser O, Reisinger A, Pena J, et al. High resolution quantitative computed tomography-based assessment of trabecular microstructure and strength estimates by finite-element analysis of the spine, but not DXA, reflects vertebral fracture status in men with glucocorticoid-induced osteoporosis. Bone. 2013;52(2):568–77.CrossRefPubMed Graeff C, Marin F, Petto H, Kayser O, Reisinger A, Pena J, et al. High resolution quantitative computed tomography-based assessment of trabecular microstructure and strength estimates by finite-element analysis of the spine, but not DXA, reflects vertebral fracture status in men with glucocorticoid-induced osteoporosis. Bone. 2013;52(2):568–77.CrossRefPubMed
20.
Zurück zum Zitat Nyman JS, Makowski AJ. The contribution of the extracellular matrix to the fracture resistance of bone. Curr Osteoporos Rep. 2012;10(2):169–77.CrossRefPubMed Nyman JS, Makowski AJ. The contribution of the extracellular matrix to the fracture resistance of bone. Curr Osteoporos Rep. 2012;10(2):169–77.CrossRefPubMed
21.
22.
23.
Zurück zum Zitat Maruyama N, Shibata Y, Wurihan, Swain MV, Kataoka Y, Takiguchi Y, et al. Strain-rate stiffening of cortical bone: observations and implications from nanoindentation experiments. Nanoscale. 2014;6(24):14863–71.PubMed Maruyama N, Shibata Y, Wurihan, Swain MV, Kataoka Y, Takiguchi Y, et al. Strain-rate stiffening of cortical bone: observations and implications from nanoindentation experiments. Nanoscale. 2014;6(24):14863–71.PubMed
24.
Zurück zum Zitat Hansma P, Turner P, Drake B, Yurtsev E, Proctor A, Mathews P, et al. The bone diagnostic instrument II: indentation distance increase. Rev Sci Instrum. 2008;79(6):064303.CrossRefPubMedPubMedCentral Hansma P, Turner P, Drake B, Yurtsev E, Proctor A, Mathews P, et al. The bone diagnostic instrument II: indentation distance increase. Rev Sci Instrum. 2008;79(6):064303.CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Bridges D, Randall C, Hansma PK. A new device for performing reference point indentation without a reference probe. Rev Sci Instrum. 2012;83(4):044301.CrossRefPubMedPubMedCentral Bridges D, Randall C, Hansma PK. A new device for performing reference point indentation without a reference probe. Rev Sci Instrum. 2012;83(4):044301.CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Karim L, Van Vliet M, Bouxsein ML. Comparison of cyclic and impact-based reference point indentation measurements in human cadaveric tibia. Bone. 2015. Karim L, Van Vliet M, Bouxsein ML. Comparison of cyclic and impact-based reference point indentation measurements in human cadaveric tibia. Bone. 2015.
27.
Zurück zum Zitat Allen MR, McNerny E, Organ JM, Wallace JM. True gold or pyrite: a review of reference point indentation for assessing bone mechanical properties in vivo. J Bone Miner Res. 2015. Allen MR, McNerny E, Organ JM, Wallace JM. True gold or pyrite: a review of reference point indentation for assessing bone mechanical properties in vivo. J Bone Miner Res. 2015.
28.
Zurück zum Zitat Granke M, Coulmier A, Uppuganti S, Gaddy JA, Does MD, Nyman JS. 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.CrossRefPubMedPubMedCentral Granke M, Coulmier A, Uppuganti S, Gaddy JA, Does MD, Nyman JS. 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.CrossRefPubMedPubMedCentral
29.
Zurück zum Zitat Zebaze RM, Ghasem-Zadeh A, Bohte A, Iuliano-Burns S, Mirams M, Price RI, et al. Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet. 2010;375(9727):1729–36.CrossRefPubMed Zebaze RM, Ghasem-Zadeh A, Bohte A, Iuliano-Burns S, Mirams M, Price RI, et al. Intracortical remodelling and porosity in the distal radius and post-mortem femurs of women: a cross-sectional study. Lancet. 2010;375(9727):1729–36.CrossRefPubMed
30.•
Zurück zum Zitat Abraham AC, Agarwalla A, Yadavalli A, Liu JY, Tang SY. Microstructural and compositional contributions towards the mechanical behavior of aging human bone measured by cyclic and impact reference point indentation. Bone. 2016;In press. Tissue-level mechanical properties from reference point microindentation of cadaveric tibia with soft tissue in place are weakly correlated with regional cortical porosoity. Abraham AC, Agarwalla A, Yadavalli A, Liu JY, Tang SY. Microstructural and compositional contributions towards the mechanical behavior of aging human bone measured by cyclic and impact reference point indentation. Bone. 2016;In press. Tissue-level mechanical properties from reference point microindentation of cadaveric tibia with soft tissue in place are weakly correlated with regional cortical porosoity.
31.
Zurück zum Zitat Burstein AH, Reilly DT, Martens M. Aging of bone tissue: mechanical properties. J Bone Joint Surg Am. 1976;58(1):82–6.PubMed Burstein AH, Reilly DT, Martens M. Aging of bone tissue: mechanical properties. J Bone Joint Surg Am. 1976;58(1):82–6.PubMed
32.
Zurück zum Zitat McCalden RW, McGeough JA, Barker MB, Court-Brown CM. 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(8):1193–205.PubMed McCalden RW, McGeough JA, Barker MB, Court-Brown CM. 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(8):1193–205.PubMed
33.
Zurück zum Zitat Zioupos P, Currey JD. Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone. 1998;22(1):57–66.CrossRefPubMed Zioupos P, Currey JD. Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone. 1998;22(1):57–66.CrossRefPubMed
34.
Zurück zum Zitat Nyman JS, Roy A, Tyler JH, Acuna RL, Gayle HJ, Wang X. Age-related factors affecting the postyield energy dissipation of human cortical bone. J Orthop Res. 2007;25(5):646–55.CrossRefPubMedPubMedCentral Nyman JS, Roy A, Tyler JH, Acuna RL, Gayle HJ, Wang X. Age-related factors affecting the postyield energy dissipation of human cortical bone. J Orthop Res. 2007;25(5):646–55.CrossRefPubMedPubMedCentral
35.•
Zurück zum Zitat Granke M, Makowski AJ, Uppuganti S, Does MD, Nyman JS. Identifying novel clinical surrogates to assess human bone fracture toughness. J Bone Miner Res. 2015;30(7):1290–300. Tissue-level mechanical properties from cyclic reference point microindentation help explain the variance (R 2 ≈ 30%) in fracture toughness when age is included as covariate. Granke M, Makowski AJ, Uppuganti S, Does MD, Nyman JS. Identifying novel clinical surrogates to assess human bone fracture toughness. J Bone Miner Res. 2015;30(7):1290–300. Tissue-level mechanical properties from cyclic reference point microindentation help explain the variance (R 2 ≈ 30%) in fracture toughness when age is included as covariate.
36.••
Zurück zum Zitat Mirzaali MJ, Jakob Schwiedrzik J, Thaiwichai S, Best JP, Michler J, Zysset PK et al. Mechanical properties of cortical bone and their relationships with age, gender, composition and microindentation properties in the elderly. Bone. 2015;in press. Tissue-level mechanical properties from quasi-static indentation tests do not help explain the variance in the apparent-level mechancial propeties of human cortical bone. Mirzaali MJ, Jakob Schwiedrzik J, Thaiwichai S, Best JP, Michler J, Zysset PK et al. Mechanical properties of cortical bone and their relationships with age, gender, composition and microindentation properties in the elderly. Bone. 2015;in press. Tissue-level mechanical properties from quasi-static indentation tests do not help explain the variance in the apparent-level mechancial propeties of human cortical bone.
37.
Zurück zum Zitat Houde J, Marchetti M, Duquette J, Hoffman A, Steinberg G, Crane GK, et al. Correlation of bone mineral density and femoral neck hardness in bovine and human samples. Calcif Tissue Int. 1995;57(3):201–5.CrossRefPubMed Houde J, Marchetti M, Duquette J, Hoffman A, Steinberg G, Crane GK, et al. Correlation of bone mineral density and femoral neck hardness in bovine and human samples. Calcif Tissue Int. 1995;57(3):201–5.CrossRefPubMed
38.
Zurück zum Zitat Hoffler CE, Moore KE, Kozloff K, Zysset PK, Goldstein SA. Age, gender, and bone lamellae elastic moduli. J Orthop Res. 2000;18(3):432–7.CrossRefPubMed Hoffler CE, Moore KE, Kozloff K, Zysset PK, Goldstein SA. Age, gender, and bone lamellae elastic moduli. J Orthop Res. 2000;18(3):432–7.CrossRefPubMed
39.
Zurück zum Zitat Zioupos P, Gresle M, Winwood K. Fatigue strength of human cortical bone: age, physical, and material heterogeneity effects. J Biomed Mater Res A. 2008;86(3):627–36.CrossRefPubMed Zioupos P, Gresle M, Winwood K. Fatigue strength of human cortical bone: age, physical, and material heterogeneity effects. J Biomed Mater Res A. 2008;86(3):627–36.CrossRefPubMed
40.
Zurück zum Zitat Wolfram U, Wilke HJ, Zysset PK. Rehydration of vertebral trabecular bone: influences on its anisotropy, its stiffness and the indentation work with a view to age, gender and vertebral level. Bone. 2010;46(2):348–54.CrossRefPubMed Wolfram U, Wilke HJ, Zysset PK. Rehydration of vertebral trabecular bone: influences on its anisotropy, its stiffness and the indentation work with a view to age, gender and vertebral level. Bone. 2010;46(2):348–54.CrossRefPubMed
41.
Zurück zum Zitat Rho JY, Zioupos P, Currey JD, Pharr GM. Microstructural elasticity and regional heterogeneity in human femoral bone of various ages examined by nano-indentation. J Biomech. 2002;35:189–98.CrossRefPubMed Rho JY, Zioupos P, Currey JD, Pharr GM. Microstructural elasticity and regional heterogeneity in human femoral bone of various ages examined by nano-indentation. J Biomech. 2002;35:189–98.CrossRefPubMed
42.
Zurück zum Zitat Sinder BP, Lloyd WR, Salemi JD, Marini JC, Caird MS, Morris MD, et al. Effect of anti-sclerostin therapy and osteogenesis imperfecta on tissue-level properties in growing and adult mice while controlling for tissue age. Bone. 2016;84:222–9.CrossRefPubMed Sinder BP, Lloyd WR, Salemi JD, Marini JC, Caird MS, Morris MD, et al. Effect of anti-sclerostin therapy and osteogenesis imperfecta on tissue-level properties in growing and adult mice while controlling for tissue age. Bone. 2016;84:222–9.CrossRefPubMed
43.••
Zurück zum Zitat Malgo F, Hamdy NAT, Papapoulos SE, Appelman-Dijkstra NM. Bone material strength as measured by microindentation in vivo is decreased in patients with fragility fractures independently of bone mineral density. J Clin Endocrinol Metab. 2015;100(5):2039–45. Tissue resistance to impact microindentation of human subjects is lower for those with a fragility fracture than for those without a fracture.CrossRefPubMed Malgo F, Hamdy NAT, Papapoulos SE, Appelman-Dijkstra NM. Bone material strength as measured by microindentation in vivo is decreased in patients with fragility fractures independently of bone mineral density. J Clin Endocrinol Metab. 2015;100(5):2039–45. Tissue resistance to impact microindentation of human subjects is lower for those with a fragility fracture than for those without a fracture.CrossRefPubMed
44.
Zurück zum Zitat Duarte Sosa D, Vilaplana L, Guerri R, Nogues X, Wang-Fagerland M, Diez-Perez A, et al. Are the high hip fracture rates among Norwegian women explained by impaired bone material properties? J Bone Miner Res. 2015;30(10):1784–9.CrossRefPubMed Duarte Sosa D, Vilaplana L, Guerri R, Nogues X, Wang-Fagerland M, Diez-Perez A, et al. Are the high hip fracture rates among Norwegian women explained by impaired bone material properties? J Bone Miner Res. 2015;30(10):1784–9.CrossRefPubMed
45.
Zurück zum Zitat Ojanen X, Isaksson H, Toyras J, Turunen MJ, Malo MK, Halvari A, et al. Relationships between tissue composition and viscoelastic properties in human trabecular bone. J Biomech. 2015;48(2):269–75.CrossRefPubMed Ojanen X, Isaksson H, Toyras J, Turunen MJ, Malo MK, Halvari A, et al. Relationships between tissue composition and viscoelastic properties in human trabecular bone. J Biomech. 2015;48(2):269–75.CrossRefPubMed
46.
Zurück zum Zitat 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(06):1564–83.CrossRef 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(06):1564–83.CrossRef
47.
Zurück zum Zitat Gao J, Gong H, Zhang R, Zhu D. Age-related regional deterioration patterns and changes in nanoscale characterizations of trabeculae in the femoral head. Exp Gerontol. 2015;62:63–72.CrossRefPubMed Gao J, Gong H, Zhang R, Zhu D. Age-related regional deterioration patterns and changes in nanoscale characterizations of trabeculae in the femoral head. Exp Gerontol. 2015;62:63–72.CrossRefPubMed
48.
Zurück zum Zitat Milovanovic P, Potocnik J, Djonic D, Nikolic S, Zivkovic V, Djuric M, et al. Age-related deterioration in trabecular bone mechanical properties at material level: nanoindentation study of the femoral neck in women by using AFM. Exp Gerontol. 2012;47(2):154–9.CrossRefPubMed Milovanovic P, Potocnik J, Djonic D, Nikolic S, Zivkovic V, Djuric M, et al. Age-related deterioration in trabecular bone mechanical properties at material level: nanoindentation study of the femoral neck in women by using AFM. Exp Gerontol. 2012;47(2):154–9.CrossRefPubMed
49.
Zurück zum Zitat Isaksson H, Malkiewicz M, Nowak R, Helminen HJ, Jurvelin JS. Rabbit cortical bone tissue increases its elastic stiffness but becomes less viscoelastic with age. Bone. 2010;47(6):1030–8.CrossRefPubMed Isaksson H, Malkiewicz M, Nowak R, Helminen HJ, Jurvelin JS. Rabbit cortical bone tissue increases its elastic stiffness but becomes less viscoelastic with age. Bone. 2010;47(6):1030–8.CrossRefPubMed
50.
Zurück zum Zitat Polly BJ, Yuya PA, Akhter MP, Recker RR, Turner JA. Intrinsic material properties of trabecular bone by nanoindentation testing of biopsies taken from healthy women before and after menopause. Calcif Tissue Int. 2012;90(4):286–93.CrossRefPubMed Polly BJ, Yuya PA, Akhter MP, Recker RR, Turner JA. Intrinsic material properties of trabecular bone by nanoindentation testing of biopsies taken from healthy women before and after menopause. Calcif Tissue Int. 2012;90(4):286–93.CrossRefPubMed
51.
Zurück zum Zitat Kim DG, Huja SS, Lee HR, Tee BC, Hueni S. Relationships of viscosity with contact hardness and modulus of bone matrix measured by nanoindentation. J Biomech Eng. 2010;132(2):024502.CrossRefPubMed Kim DG, Huja SS, Lee HR, Tee BC, Hueni S. Relationships of viscosity with contact hardness and modulus of bone matrix measured by nanoindentation. J Biomech Eng. 2010;132(2):024502.CrossRefPubMed
52.
Zurück zum Zitat Guo XE, Goldstein SA. Vertebral trabecular bone microscopic tissue elastic modulus and hardness do not change in ovariectomized rats. J Orthop Res. 2000;18(2):333–6.CrossRefPubMed Guo XE, Goldstein SA. Vertebral trabecular bone microscopic tissue elastic modulus and hardness do not change in ovariectomized rats. J Orthop Res. 2000;18(2):333–6.CrossRefPubMed
53.
Zurück zum Zitat Peng S, Liu XS, Huang S, Pan H, Zhen W, Zhou G, et al. Intervention timing of strontium treatment on estrogen depletion-induced osteoporosis in rats: bone microstructure and mechanics. J Orthop Res. 2014;32(3):477–84.CrossRefPubMed Peng S, Liu XS, Huang S, Pan H, Zhen W, Zhou G, et al. Intervention timing of strontium treatment on estrogen depletion-induced osteoporosis in rats: bone microstructure and mechanics. J Orthop Res. 2014;32(3):477–84.CrossRefPubMed
54.
Zurück zum Zitat Kim DG, Huja SS, Navalgund A, D’Atri A, Tee B, Reeder S, et al. Effect of estrogen deficiency on regional variation of a viscoelastic tissue property of bone. J Biomech. 2013;46(1):110–5.CrossRefPubMed Kim DG, Huja SS, Navalgund A, D’Atri A, Tee B, Reeder S, et al. Effect of estrogen deficiency on regional variation of a viscoelastic tissue property of bone. J Biomech. 2013;46(1):110–5.CrossRefPubMed
55.
Zurück zum Zitat 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(1):134–41.CrossRefPubMed 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(1):134–41.CrossRefPubMed
56.
Zurück zum Zitat Wen XX, Wang FQ, Xu C, Wu ZX, Zhang Y, Feng YF, et al. Time related changes of mineral and collagen and their roles in cortical bone mechanics of ovariectomized rabbits. PLoS One. 2015;10(6), e0127973.CrossRefPubMedPubMedCentral Wen XX, Wang FQ, Xu C, Wu ZX, Zhang Y, Feng YF, et al. Time related changes of mineral and collagen and their roles in cortical bone mechanics of ovariectomized rabbits. PLoS One. 2015;10(6), e0127973.CrossRefPubMedPubMedCentral
57.
Zurück zum Zitat Brennan O, Kennedy OD, Lee TC, Rackard SM, O’Brien FJ. Biomechanical properties across trabeculae from the proximal femur of normal and ovariectomised sheep. J Biomech. 2009;42(4):498–503.CrossRefPubMed Brennan O, Kennedy OD, Lee TC, Rackard SM, O’Brien FJ. Biomechanical properties across trabeculae from the proximal femur of normal and ovariectomised sheep. J Biomech. 2009;42(4):498–503.CrossRefPubMed
58.
Zurück zum Zitat Ganeko K, Masaki C, Shibata Y, Mukaibo T, Kondo Y, Nakamoto T, et al. Bone aging by advanced glycation end products: a multiscale mechanical analysis. J Dent Res. 2015;94(12):1684–90.CrossRefPubMed Ganeko K, Masaki C, Shibata Y, Mukaibo T, Kondo Y, Nakamoto T, et al. Bone aging by advanced glycation end products: a multiscale mechanical analysis. J Dent Res. 2015;94(12):1684–90.CrossRefPubMed
59.••
Zurück zum Zitat Wang X, Sudhaker Rao D, Ajdelsztajn L, Ciarelli TE, Lavernia EJ, Fyhrie DP. 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(1):68–77. Tissue-level mechanical properties are not necessarily different between osteoporotic and otherwise normal bone.CrossRefPubMed Wang X, Sudhaker Rao D, Ajdelsztajn L, Ciarelli TE, Lavernia EJ, Fyhrie DP. 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(1):68–77. Tissue-level mechanical properties are not necessarily different between osteoporotic and otherwise normal bone.CrossRefPubMed
60.•
Zurück zum Zitat Tjhia CK, Odvina CV, Rao DS, Stover SM, Wang X, Fyhrie DP. Mechanical property and tissue mineral density differences among severely suppressed bone turnover (SSBT) patients, osteoporotic patients, and normal subjects. Bone. 2011;49(6):1279–89. The variance in tissue-level mechanical properties can be lower for patients with long-term bisphophonate use.CrossRefPubMedPubMedCentral Tjhia CK, Odvina CV, Rao DS, Stover SM, Wang X, Fyhrie DP. Mechanical property and tissue mineral density differences among severely suppressed bone turnover (SSBT) patients, osteoporotic patients, and normal subjects. Bone. 2011;49(6):1279–89. The variance in tissue-level mechanical properties can be lower for patients with long-term bisphophonate use.CrossRefPubMedPubMedCentral
61.•
Zurück zum Zitat Fratzl-Zelman N, Roschger P, Gourrier A, Weber M, Misof BM, Loveridge N, et al. Combination of nanoindentation and quantitative backscattered electron imaging revealed altered bone material properties associated with femoral neck fragility. Calcif Tissue Int. 2009;85(4):335–43. Tissue-level mechanical properties do not vary between osteoporotic and non-osteoporotic bone even though degree of mineralization was higher in the former than in the latter.CrossRefPubMedPubMedCentral Fratzl-Zelman N, Roschger P, Gourrier A, Weber M, Misof BM, Loveridge N, et al. Combination of nanoindentation and quantitative backscattered electron imaging revealed altered bone material properties associated with femoral neck fragility. Calcif Tissue Int. 2009;85(4):335–43. Tissue-level mechanical properties do not vary between osteoporotic and non-osteoporotic bone even though degree of mineralization was higher in the former than in the latter.CrossRefPubMedPubMedCentral
62.
Zurück zum Zitat Nazarian A, von Stechow D, Zurakowski D, Muller R, Snyder BD. Bone volume fraction explains the variation in strength and stiffness of cancellous bone affected by metastatic cancer and osteoporosis. Calcif Tissue Int. 2008;83(6):368–79.CrossRefPubMed Nazarian A, von Stechow D, Zurakowski D, Muller R, Snyder BD. Bone volume fraction explains the variation in strength and stiffness of cancellous bone affected by metastatic cancer and osteoporosis. Calcif Tissue Int. 2008;83(6):368–79.CrossRefPubMed
63.
Zurück zum Zitat Loveridge N, Power J, Reeve J, Boyde A. Bone mineralization density and femoral neck fragility. Bone. 2004;35(4):929–41.CrossRefPubMed Loveridge N, Power J, Reeve J, Boyde A. Bone mineralization density and femoral neck fragility. Bone. 2004;35(4):929–41.CrossRefPubMed
64.
Zurück zum Zitat Sutton-Smith P, Beard H, Fazzalari N. Quantitative backscattered electron imaging of bone in proximal femur fragility and medical illness. J Microsc. 2008;229(1):60–6.CrossRefPubMed Sutton-Smith P, Beard H, Fazzalari N. Quantitative backscattered electron imaging of bone in proximal femur fragility and medical illness. J Microsc. 2008;229(1):60–6.CrossRefPubMed
65.
Zurück zum Zitat Carpentier VT, Wong J, Yeap Y, Gan C, Sutton-Smith P, Badiei A, et al. Increased proportion of hypermineralized osteocyte lacunae in osteoporotic and osteoarthritic human trabecular bone: implications for bone remodeling. Bone. 2012;50(3):688–94.CrossRefPubMed Carpentier VT, Wong J, Yeap Y, Gan C, Sutton-Smith P, Badiei A, et al. Increased proportion of hypermineralized osteocyte lacunae in osteoporotic and osteoarthritic human trabecular bone: implications for bone remodeling. Bone. 2012;50(3):688–94.CrossRefPubMed
66.
Zurück zum Zitat Milovanovic P, Rakocevic Z, Djonic D, Zivkovic V, Hahn M, Nikolic S, et al. Nano-structural, compositional and micro-architectural signs of cortical bone fragility at the superolateral femoral neck in elderly hip fracture patients vs. healthy aged controls. Exp Gerontol. 2014;55:19–28.CrossRefPubMed Milovanovic P, Rakocevic Z, Djonic D, Zivkovic V, Hahn M, Nikolic S, et al. Nano-structural, compositional and micro-architectural signs of cortical bone fragility at the superolateral femoral neck in elderly hip fracture patients vs. healthy aged controls. Exp Gerontol. 2014;55:19–28.CrossRefPubMed
67.
Zurück zum Zitat Ciarelli TE, Fyhrie DP, Parfitt AM. Effects of vertebral bone fragility and bone formation rate on the mineralization levels of cancellous bone from white females. Bone. 2003;32(3):311–5.CrossRefPubMed Ciarelli TE, Fyhrie DP, Parfitt AM. Effects of vertebral bone fragility and bone formation rate on the mineralization levels of cancellous bone from white females. Bone. 2003;32(3):311–5.CrossRefPubMed
68.
Zurück zum Zitat Ciarelli TE, Tjhia C, Rao DS, Qiu S, Parfitt AM, Fyhrie DP. Trabecular packet-level lamellar density patterns differ by fracture status and bone formation rate in white females. Bone. 2009;45(5):903–8.CrossRefPubMed Ciarelli TE, Tjhia C, Rao DS, Qiu S, Parfitt AM, Fyhrie DP. Trabecular packet-level lamellar density patterns differ by fracture status and bone formation rate in white females. Bone. 2009;45(5):903–8.CrossRefPubMed
69.
Zurück zum Zitat Bousson V, Bergot C, Wu Y, Jolivet E, Zhou LQ, Laredo JD. Greater tissue mineralization heterogeneity in femoral neck cortex from hip-fractured females than controls. A microradiographic study. Bone. 2011;48(6):1252–9.CrossRefPubMed Bousson V, Bergot C, Wu Y, Jolivet E, Zhou LQ, Laredo JD. Greater tissue mineralization heterogeneity in femoral neck cortex from hip-fractured females than controls. A microradiographic study. Bone. 2011;48(6):1252–9.CrossRefPubMed
70.
Zurück zum Zitat Wu Y, Zhou L, Bergot C, Peyrin F, Bousson V. Cortical bone mineralization in the human femoral neck in cases and controls from synchrotron radiation study. Cell Biochem Biophys. 2015;73(1):51–7.CrossRef Wu Y, Zhou L, Bergot C, Peyrin F, Bousson V. Cortical bone mineralization in the human femoral neck in cases and controls from synchrotron radiation study. Cell Biochem Biophys. 2015;73(1):51–7.CrossRef
71.
Zurück zum Zitat Gourion-Arsiquaud S, Faibish D, Myers E, Spevak L, Compston J, Hodsman A, et al. Use of FTIR spectroscopic imaging to identify parameters associated with fragility fracture. J Bone Miner Res. 2009;24(9):1565–71.CrossRefPubMedPubMedCentral Gourion-Arsiquaud S, Faibish D, Myers E, Spevak L, Compston J, Hodsman A, et al. Use of FTIR spectroscopic imaging to identify parameters associated with fragility fracture. J Bone Miner Res. 2009;24(9):1565–71.CrossRefPubMedPubMedCentral
72.
Zurück zum Zitat Gourion-Arsiquaud S, Lukashova L, Power J, Loveridge N, Reeve J, Boskey 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.CrossRefPubMedPubMedCentral Gourion-Arsiquaud S, Lukashova L, Power J, Loveridge N, Reeve J, Boskey 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.CrossRefPubMedPubMedCentral
73.
Zurück zum Zitat Wang ZX, Lloyd AA, Burket JC, Gourion-Arsiquaud S, Donnelly E. Altered distributions of bone tissue mineral and collagen properties in women with fragility fractures. Bone. 2016;84:237–44.CrossRefPubMed Wang ZX, Lloyd AA, Burket JC, Gourion-Arsiquaud S, Donnelly E. Altered distributions of bone tissue mineral and collagen properties in women with fragility fractures. Bone. 2016;84:237–44.CrossRefPubMed
74.••
Zurück zum Zitat Boskey AL, Donnelly E, Boskey E, Spevak L, Ma Y, Zhang W et al. Examining the relationships between bone tissue composition, compositional heterogeneity and fragility fracture: a matched case controlled FTIRI study. J Bone Miner Res. 2016;31:1070–81. Heterogenetiy in composition does not differ between gender- and aBMD-matched fracture and non-fracture cases. Boskey AL, Donnelly E, Boskey E, Spevak L, Ma Y, Zhang W et al. Examining the relationships between bone tissue composition, compositional heterogeneity and fragility fracture: a matched case controlled FTIRI study. J Bone Miner Res. 2016;31:1070–81. Heterogenetiy in composition does not differ between gender- and aBMD-matched fracture and non-fracture cases.
75.
Zurück zum Zitat Kim G, Cole JH, Boskey AL, Baker SP, van der Meulen MC. Reduced tissue-level stiffness and mineralization in osteoporotic cancellous bone. Calcif Tissue Int. 2014;95(2):125–31.CrossRefPubMedPubMedCentral Kim G, Cole JH, Boskey AL, Baker SP, van der Meulen MC. Reduced tissue-level stiffness and mineralization in osteoporotic cancellous bone. Calcif Tissue Int. 2014;95(2):125–31.CrossRefPubMedPubMedCentral
76.
Zurück zum Zitat Tjhia CK, Stover SM, Rao DS, Odvina CV, Fyhrie DP. Relating micromechanical properties and mineral densities in severely suppressed bone turnover patients, osteoporotic patients, and normal subjects. Bone. 2012;51(1):114–22.CrossRefPubMedPubMedCentral Tjhia CK, Stover SM, Rao DS, Odvina CV, Fyhrie DP. Relating micromechanical properties and mineral densities in severely suppressed bone turnover patients, osteoporotic patients, and normal subjects. Bone. 2012;51(1):114–22.CrossRefPubMedPubMedCentral
77.
Zurück zum Zitat Diez-Perez A, Guerri R, Nogues X, Caceres E, Pena MJ, Mellibovsky L, et al. Microindentation for in vivo measurement of bone tissue mechanical properties in humans. J Bone Miner Res. 2010;25(8):1877–85.CrossRefPubMedPubMedCentral Diez-Perez A, Guerri R, Nogues X, Caceres E, Pena MJ, Mellibovsky L, et al. Microindentation for in vivo measurement of bone tissue mechanical properties in humans. J Bone Miner Res. 2010;25(8):1877–85.CrossRefPubMedPubMedCentral
78.
Zurück zum Zitat Guerri-Fernandez RC, Nogues X, Quesada Gomez JM, Torres Del Pliego E, Puig L, Garcia-Giralt N, 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.CrossRefPubMed Guerri-Fernandez RC, Nogues X, Quesada Gomez JM, Torres Del Pliego E, Puig L, Garcia-Giralt N, 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.CrossRefPubMed
79.
Zurück zum Zitat Jenkins T, Coutts LV, D’Angelo S, Dunlop DG, Oreffo RO, Cooper C et al. Site-dependent reference point microindentation complements clinical measures for improved fracture risk assessment at the human femoral neck. J Bone Miner Res. 2015. Jenkins T, Coutts LV, D’Angelo S, Dunlop DG, Oreffo RO, Cooper C et al. Site-dependent reference point microindentation complements clinical measures for improved fracture risk assessment at the human femoral neck. J Bone Miner Res. 2015.
80.
Zurück zum Zitat Abraham AC, Agarwalla A, Yadavalli A, McAndrew C, Liu JY, Tang SY. Multiscale predictors of femoral neck in situ strength in aging women: contributions of BMD, cortical porosity, reference point indentation, and nonenzymatic glycation. J Bone Miner Res. 2015;30(12):2207–14.CrossRefPubMedPubMedCentral Abraham AC, Agarwalla A, Yadavalli A, McAndrew C, Liu JY, Tang SY. Multiscale predictors of femoral neck in situ strength in aging women: contributions of BMD, cortical porosity, reference point indentation, and nonenzymatic glycation. J Bone Miner Res. 2015;30(12):2207–14.CrossRefPubMedPubMedCentral
81.
Zurück zum Zitat Rudang R, Zoulakis M, Sundh D, Brisby H, Diez-Perez A, Johansson L et al. Bone material strength is associated with areal BMD but not with prevalent fractures in older women. Osteoporos Int. 2015. Rudang R, Zoulakis M, Sundh D, Brisby H, Diez-Perez A, Johansson L et al. Bone material strength is associated with areal BMD but not with prevalent fractures in older women. Osteoporos Int. 2015.
82.
Zurück zum Zitat Mellibovsky L, Prieto-Alhambra D, Mellibovsky F, Guerri-Fernandez R, Nogues X, Randall C, et al. Bone tissue properties measurement by reference point indentation in glucocorticoid-induced osteoporosis. J Bone Miner Res. 2015;30(9):1651–6.CrossRefPubMed Mellibovsky L, Prieto-Alhambra D, Mellibovsky F, Guerri-Fernandez R, Nogues X, Randall C, et al. Bone tissue properties measurement by reference point indentation in glucocorticoid-induced osteoporosis. J Bone Miner Res. 2015;30(9):1651–6.CrossRefPubMed
83.
Zurück zum Zitat Farr JN, Drake MT, Amin S, Melton LJ, McCready LK, Khosla S. In vivo assessment of bone quality in postmenopausal women with type 2 diabetes. J Bone Miner Res. 2014;29(4):787–95.CrossRefPubMedPubMedCentral Farr JN, Drake MT, Amin S, Melton LJ, McCready LK, Khosla S. In vivo assessment of bone quality in postmenopausal women with type 2 diabetes. J Bone Miner Res. 2014;29(4):787–95.CrossRefPubMedPubMedCentral
84.
Zurück zum Zitat Gallant MA, Brown DM, Organ JM, Allen MR, Burr DB. Reference-point indentation correlates with bone toughness assessed using whole-bone traditional mechanical testing. Bone. 2013;53(1):301–5.CrossRefPubMed Gallant MA, Brown DM, Organ JM, Allen MR, Burr DB. Reference-point indentation correlates with bone toughness assessed using whole-bone traditional mechanical testing. Bone. 2013;53(1):301–5.CrossRefPubMed
85.
Zurück zum Zitat Carriero A, Bruse JL, Oldknow KJ, Millan JL, Farquharson C, Shefelbine SJ. Reference point indentation is not indicative of whole mouse bone measures of stress intensity fracture toughness. Bone. 2014;69C:174–9.CrossRef Carriero A, Bruse JL, Oldknow KJ, Millan JL, Farquharson C, Shefelbine SJ. Reference point indentation is not indicative of whole mouse bone measures of stress intensity fracture toughness. Bone. 2014;69C:174–9.CrossRef
86.
Zurück zum Zitat Meisner MJ, Frantziskonis GN. Heterogeneous materials—scaling phenomena relevant to fracture and to fracture toughness. Chaos, Solitons Fractals. 1997;8(2):151–70.CrossRef Meisner MJ, Frantziskonis GN. Heterogeneous materials—scaling phenomena relevant to fracture and to fracture toughness. Chaos, Solitons Fractals. 1997;8(2):151–70.CrossRef
87.
Zurück zum Zitat Yerramshetty JS, Lind C, Akkus O. The compositional and physicochemical homogeneity of male femoral cortex increases after the sixth decade. Bone. 2006;39(6):1236–43.CrossRefPubMed Yerramshetty JS, Lind C, Akkus O. The compositional and physicochemical homogeneity of male femoral cortex increases after the sixth decade. Bone. 2006;39(6):1236–43.CrossRefPubMed
88.
Zurück zum Zitat Boivin G, Farlay D, Bala Y, Doublier A, Meunier PJ, Delmas PD. Influence of remodeling on the mineralization of bone tissue. Osteoporos Int. 2009;20(6):1023–6.CrossRefPubMedPubMedCentral Boivin G, Farlay D, Bala Y, Doublier A, Meunier PJ, Delmas PD. Influence of remodeling on the mineralization of bone tissue. Osteoporos Int. 2009;20(6):1023–6.CrossRefPubMedPubMedCentral
89.
Zurück zum Zitat Zoehrer R, Roschger P, Paschalis EP, Hofstaetter JG, Durchschlag E, Fratzl P, et al. Effects of 3- and 5-year treatment with risedronate on bone mineralization density distribution in triple biopsies of the iliac crest in postmenopausal women. J Bone Miner Res. 2006;21(7):1106–12.CrossRefPubMed Zoehrer R, Roschger P, Paschalis EP, Hofstaetter JG, Durchschlag E, Fratzl P, et al. Effects of 3- and 5-year treatment with risedronate on bone mineralization density distribution in triple biopsies of the iliac crest in postmenopausal women. J Bone Miner Res. 2006;21(7):1106–12.CrossRefPubMed
91.
Zurück zum Zitat Roschger P, Misof B, Paschalis E, Fratzl P, Klaushofer K. Changes in the degree of mineralization with osteoporosis and its treatment. Curr Osteoporos Rep. 2014;12(3):338–50.CrossRefPubMed Roschger P, Misof B, Paschalis E, Fratzl P, Klaushofer K. Changes in the degree of mineralization with osteoporosis and its treatment. Curr Osteoporos Rep. 2014;12(3):338–50.CrossRefPubMed
92.
Zurück zum Zitat Besdo S, Vashishth D. Extended finite element models of intracortical porosity and heterogeneity in cortical bone. Comput Mater Sci. 2012;64:301–5.CrossRef Besdo S, Vashishth D. Extended finite element models of intracortical porosity and heterogeneity in cortical bone. Comput Mater Sci. 2012;64:301–5.CrossRef
93.
Zurück zum Zitat Tamminen IS, Misof BM, Roschger P, Mayranpaa MK, Turunen MJ, Isaksson H, et al. Increased heterogeneity of bone matrix mineralization in pediatric patients prone to fractures: a biopsy study. J Bone Miner Res. 2014;29(5):1110–7.CrossRefPubMed Tamminen IS, Misof BM, Roschger P, Mayranpaa MK, Turunen MJ, Isaksson H, et al. Increased heterogeneity of bone matrix mineralization in pediatric patients prone to fractures: a biopsy study. J Bone Miner Res. 2014;29(5):1110–7.CrossRefPubMed
94.
Zurück zum Zitat Herbert EG, Johanns KE, Singleton RS, Pharr GM. On the measurement of energy dissipation using nanoindentation and the continuous stiffness measurement technique. J Mater Res. 2013;28(21):3029–42.CrossRef Herbert EG, Johanns KE, Singleton RS, Pharr GM. On the measurement of energy dissipation using nanoindentation and the continuous stiffness measurement technique. J Mater Res. 2013;28(21):3029–42.CrossRef
95.
Zurück zum Zitat Herbert EG, Oliver WC, Pharr GM. Nanoindentation and the dynamic characterization of viscoelastic solids. J Phys D Appl Phys. 2008;41(7):074021.CrossRef Herbert EG, Oliver WC, Pharr GM. Nanoindentation and the dynamic characterization of viscoelastic solids. J Phys D Appl Phys. 2008;41(7):074021.CrossRef
96.
Zurück zum Zitat Schwiedrzik J, Raghavan R, Burki A, LeNader V, Wolfram U, Michler J, et al. In situ micropillar compression reveals superior strength and ductility but an absence of damage in lamellar bone. Nat Mater. 2014;13(7):740–7.CrossRefPubMed Schwiedrzik J, Raghavan R, Burki A, LeNader V, Wolfram U, Michler J, et al. In situ micropillar compression reveals superior strength and ductility but an absence of damage in lamellar bone. Nat Mater. 2014;13(7):740–7.CrossRefPubMed
97.
Zurück zum Zitat Islam A, Neil Dong X, Wang X. Mechanistic modeling of a nanoscratch test for determination of in situ toughness of bone. J Mech Behav Biomed Mater. 2012;5(1):156–64.CrossRefPubMed Islam A, Neil Dong X, Wang X. Mechanistic modeling of a nanoscratch test for determination of in situ toughness of bone. J Mech Behav Biomed Mater. 2012;5(1):156–64.CrossRefPubMed
98.•
Zurück zum Zitat Wang X, Xu H, Huang Y, Gu S, Jiang JX. Coupling effect of water and proteoglycans on the in situ toughness of bone. J Bone Miner Res. 2015. Removing proteoglycans lowers tissue-level toughness as determined by nano-scratch testing. Wang X, Xu H, Huang Y, Gu S, Jiang JX. Coupling effect of water and proteoglycans on the in situ toughness of bone. J Bone Miner Res. 2015. Removing proteoglycans lowers tissue-level toughness as determined by nano-scratch testing.
Metadaten
Titel
Tissue-Level Mechanical Properties of Bone Contributing to Fracture Risk
verfasst von
Jeffry S. Nyman
Mathilde Granke
Robert C. Singleton
George M. Pharr
Publikationsdatum
04.06.2016
Verlag
Springer US
Erschienen in
Current Osteoporosis Reports / Ausgabe 4/2016
Print ISSN: 1544-1873
Elektronische ISSN: 1544-2241
DOI
https://doi.org/10.1007/s11914-016-0314-3

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