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Erschienen in: Clinical Reviews in Bone and Mineral Metabolism 3/2016

22.08.2016 | Bone quality

Bone Quality Assessment Techniques: Geometric, Compositional, and Mechanical Characterization from Macroscale to Nanoscale

verfasst von: Heather B. Hunt, Eve Donnelly

Erschienen in: Clinical & Translational Metabolism | Ausgabe 3/2016

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Abstract

This review presents an overview of the characterization techniques available to experimentally evaluate bone quality, defined as the geometric and material factors that contribute to fracture resistance independently of areal bone mineral density (aBMD) assessed by dual-energy X-ray absorptiometry. The methods available for characterization of the geometric, compositional, and mechanical properties of bone across multiple length scales are summarized, along with their outcomes and their advantages and disadvantages. Examples of how each technique is used are discussed, as well as practical concerns such as sample preparation and whether or not each testing method is destructive. Techniques that can be used in vivo and those that have been recently improved or developed are emphasized, including high-resolution peripheral quantitative computed tomography to evaluate geometric properties and reference point indentation to evaluate material properties. Because no single method can completely characterize bone quality, we provide a framework for how multiple characterization methods can be used together to generate a more comprehensive analysis of bone quality to complement aBMD in fracture risk assessment.
Literatur
1.
Zurück zum Zitat Kanis JA, 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(12):989–95.PubMedCrossRef Kanis JA, 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(12):989–95.PubMedCrossRef
2.
Zurück zum Zitat Donnelly E, Lane JM, Boskey AL. Research perspectives: the 2013 AAOS/ORS research symposium on bone quality and fracture prevention. J Orthop Res. 2014;32(7):855–64.PubMedPubMedCentralCrossRef Donnelly E, Lane JM, Boskey AL. Research perspectives: the 2013 AAOS/ORS research symposium on bone quality and fracture prevention. J Orthop Res. 2014;32(7):855–64.PubMedPubMedCentralCrossRef
4.
Zurück zum Zitat Choël L, Last D, Duboeuf F, Seurin MJ, Lissac M, Briguet A, Guillot G, Choel L, Last D, Duboeuf F, Seurin MJ, Lissac M, Briguet A, Guillot G. Trabecular alveolar bone microarchitecture in the human mandible using high resolution magnetic resonance imaging. Dentomaxillofacial Radiol. 2004;33(3):177–82.CrossRef Choël L, Last D, Duboeuf F, Seurin MJ, Lissac M, Briguet A, Guillot G, Choel L, Last D, Duboeuf F, Seurin MJ, Lissac M, Briguet A, Guillot G. Trabecular alveolar bone microarchitecture in the human mandible using high resolution magnetic resonance imaging. Dentomaxillofacial Radiol. 2004;33(3):177–82.CrossRef
5.
Zurück zum Zitat Krug R, Burghardt AJ, Majumdar S, Link TM. High-resolution imaging techniques for the assessment of osteoporosis. Radiol Clin N Am. 2010;48(3):601–21.PubMedPubMedCentralCrossRef Krug R, Burghardt AJ, Majumdar S, Link TM. High-resolution imaging techniques for the assessment of osteoporosis. Radiol Clin N Am. 2010;48(3):601–21.PubMedPubMedCentralCrossRef
6.
Zurück zum Zitat Chang G, Deniz CM, Honig S, Egol K, Regatte RR, Zhu Y, Sodickson DK, Brown R. MRI of the hip at 7T: feasibility of bone microarchitecture, high-resolution cartilage, and clinical imaging. J Magn Reson Imaging. 2014;39(6):1384–93.PubMedCrossRef Chang G, Deniz CM, Honig S, Egol K, Regatte RR, Zhu Y, Sodickson DK, Brown R. MRI of the hip at 7T: feasibility of bone microarchitecture, high-resolution cartilage, and clinical imaging. J Magn Reson Imaging. 2014;39(6):1384–93.PubMedCrossRef
7.
Zurück zum Zitat Magland JF, Rajapakse CS, Wright AC, Acciavatti R, Wehrli FW. 3D fast spin echo with out-of-slab cancellation: a technique for high-resolution structural imaging of trabecular bone at 7 Tesla. Magn Reson Med. 2010;63(3):719–27.PubMedPubMedCentralCrossRef Magland JF, Rajapakse CS, Wright AC, Acciavatti R, Wehrli FW. 3D fast spin echo with out-of-slab cancellation: a technique for high-resolution structural imaging of trabecular bone at 7 Tesla. Magn Reson Med. 2010;63(3):719–27.PubMedPubMedCentralCrossRef
8.
Zurück zum Zitat Majumdar S. Magnetic resonance imaging of trabecular bone structure. Top Magn Reson Imaging. 2002;13(5):323–34.PubMedCrossRef Majumdar S. Magnetic resonance imaging of trabecular bone structure. Top Magn Reson Imaging. 2002;13(5):323–34.PubMedCrossRef
9.
Zurück zum Zitat Wehrli FW, Ladinsky GA, Jones C, Benito M, Magland J, Vasilic B, Popescu AM, Zemel B, Cucchiara AJ, Wright AC, Song HK, Saha PK, Peachey H, Snyder PJ. In vivo magnetic resonance detects rapid remodeling changes in the topology of the trabecular bone network after menopause and the protective effect of estradiol. J Bone Miner Res. 2008;23(5):730–40.PubMedPubMedCentralCrossRef Wehrli FW, Ladinsky GA, Jones C, Benito M, Magland J, Vasilic B, Popescu AM, Zemel B, Cucchiara AJ, Wright AC, Song HK, Saha PK, Peachey H, Snyder PJ. In vivo magnetic resonance detects rapid remodeling changes in the topology of the trabecular bone network after menopause and the protective effect of estradiol. J Bone Miner Res. 2008;23(5):730–40.PubMedPubMedCentralCrossRef
10.
Zurück zum Zitat Majumdar S, Genant HK, Grampp S, Newitt DC, Truong VH, Lin JC, Mathur A. Correlation of trabecular bone structure with age, bone mineral density, and osteoporotic status: in vivo studies in the distal radius using high resolution magnetic resonance imaging. J Bone Miner Res. 1997;12(1):111–8.PubMedCrossRef Majumdar S, Genant HK, Grampp S, Newitt DC, Truong VH, Lin JC, Mathur A. Correlation of trabecular bone structure with age, bone mineral density, and osteoporotic status: in vivo studies in the distal radius using high resolution magnetic resonance imaging. J Bone Miner Res. 1997;12(1):111–8.PubMedCrossRef
11.
Zurück zum Zitat Rajapakse CS, Magland J, Zhang H, Liu XS, Wehrli SL, Guo XE, Wehrli FW. Implications of noise and resolution on mechanical properties of trabecular bone estimated by image-based finite-element analysis. J Orthop Res. 2009;27(10):1263–71.PubMedPubMedCentralCrossRef Rajapakse CS, Magland J, Zhang H, Liu XS, Wehrli SL, Guo XE, Wehrli FW. Implications of noise and resolution on mechanical properties of trabecular bone estimated by image-based finite-element analysis. J Orthop Res. 2009;27(10):1263–71.PubMedPubMedCentralCrossRef
12.
Zurück zum Zitat Wehrli FW, Song HK, Saha PK, Wright AC. Quantitative MRI for the assessment of bone structure and function. NMR Biomed. 2006;19(7):731–64.PubMedCrossRef Wehrli FW, Song HK, Saha PK, Wright AC. Quantitative MRI for the assessment of bone structure and function. NMR Biomed. 2006;19(7):731–64.PubMedCrossRef
13.
Zurück zum Zitat Engelke K, Adams JE, Armbrecht G, Augat P, Bogado CE, Bouxsein ML, Felsenberg D, Ito M, Prevrhal S, Hans DB, Lewiecki EM. Clinical use of quantitative computed tomography and peripheral quantitative computed tomography in the management of osteoporosis in adults: the 2007 ISCD official positions. Engelke K, Adams JE, Armbrecht G, Augat P, Bogado CE, Bouxsein ML, Felsenberg D, Ito M, Prevrhal S, Hans DB, Lewiecki EM. Clinical use of quantitative computed tomography and peripheral quantitative computed tomography in the management of osteoporosis in adults: the 2007 ISCD official positions.
14.
Zurück zum Zitat Genant HK, Engelke K, Prevrhal S. Advanced CT bone imaging in osteoporosis. Rheumatology. 2008;47(SUPPL. 4):iv9–16.PubMedPubMedCentral Genant HK, Engelke K, Prevrhal S. Advanced CT bone imaging in osteoporosis. Rheumatology. 2008;47(SUPPL. 4):iv9–16.PubMedPubMedCentral
15.
Zurück zum Zitat Bousson V, Le Le Bras A, Roqueplan F, Kang Y, Mitton D, Kolta S, Bergot C, Skalli W, Vicaut E, Kalender W, Engelke K, Laredo J-D. Volumetric quantitative computed tomography of the proximal femur: relationships linking geometric and densitometric variables to bone strength. Role for compact bone. Osteoporos Int. 2006;17(6):855–64.PubMedCrossRef Bousson V, Le Le Bras A, Roqueplan F, Kang Y, Mitton D, Kolta S, Bergot C, Skalli W, Vicaut E, Kalender W, Engelke K, Laredo J-D. Volumetric quantitative computed tomography of the proximal femur: relationships linking geometric and densitometric variables to bone strength. Role for compact bone. Osteoporos Int. 2006;17(6):855–64.PubMedCrossRef
16.
Zurück zum Zitat Lala D, Cheung AM, Lynch CL, Inglis D, Gordon C, Tomlinson G, Giangregorio L. Measuring apparent trabecular structure with pQCT: a comparison with HR-pQCT. J Clin Densitom. 2014;17(1):47–53.PubMedCrossRef Lala D, Cheung AM, Lynch CL, Inglis D, Gordon C, Tomlinson G, Giangregorio L. Measuring apparent trabecular structure with pQCT: a comparison with HR-pQCT. J Clin Densitom. 2014;17(1):47–53.PubMedCrossRef
17.
Zurück zum Zitat Damilakis J, Adams JE, Guglielmi G, Link TM. Radiation exposure in X-ray-based imaging techniques used in osteoporosis. Eur Radiol. 2010;20(11):2707–14.PubMedPubMedCentralCrossRef Damilakis J, Adams JE, Guglielmi G, Link TM. Radiation exposure in X-ray-based imaging techniques used in osteoporosis. Eur Radiol. 2010;20(11):2707–14.PubMedPubMedCentralCrossRef
18.
Zurück zum Zitat Geusens P, Chapurlat R, Schett G, Ghasem-Zadeh A, Seeman E, de Jong J, van den Bergh J. High-resolution in vivo imaging of bone and joints: a window to microarchitecture. Nat Rev Rheumatol. 2014;10(5):304–13.PubMedCrossRef Geusens P, Chapurlat R, Schett G, Ghasem-Zadeh A, Seeman E, de Jong J, van den Bergh J. High-resolution in vivo imaging of bone and joints: a window to microarchitecture. Nat Rev Rheumatol. 2014;10(5):304–13.PubMedCrossRef
19.
Zurück zum Zitat Boutroy S, Bouxsein ML, Munoz F, Delmas PD. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab. 2005;90(12):6508–15.PubMedCrossRef Boutroy S, Bouxsein ML, Munoz F, Delmas PD. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab. 2005;90(12):6508–15.PubMedCrossRef
20.
Zurück zum Zitat Burghardt AJ, Buie HR, Laib A, Majumdar S, Boyd SK. Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone. 2010;47(3):519–28.PubMedPubMedCentralCrossRef Burghardt AJ, Buie HR, Laib A, Majumdar S, Boyd SK. Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone. 2010;47(3):519–28.PubMedPubMedCentralCrossRef
21.
Zurück zum Zitat Burghardt AJ, Issever AS, Schwartz AV, Davis KA, Masharani U, Majumdar S, Link TM. High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab. 2010;95(11):5045–55.PubMedPubMedCentralCrossRef Burghardt AJ, Issever AS, Schwartz AV, Davis KA, Masharani U, Majumdar S, Link TM. High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab. 2010;95(11):5045–55.PubMedPubMedCentralCrossRef
22.
Zurück zum Zitat Bala Y, Chapurlat R, Cheung AM, Felsenberg D, Laroche M, Morris E, Reeve J, Thomas T, Zanchetta J, Bock O, Ghasem-Zadeh A, Djoumessi RMZ, Seeman E, Rizzoli R. Risedronate slows or partly reverses cortical and trabecular microarchitectural deterioration in postmenopausal women. J Bone Miner Res. 2014;29(2):380–8.PubMedCrossRef Bala Y, Chapurlat R, Cheung AM, Felsenberg D, Laroche M, Morris E, Reeve J, Thomas T, Zanchetta J, Bock O, Ghasem-Zadeh A, Djoumessi RMZ, Seeman E, Rizzoli R. Risedronate slows or partly reverses cortical and trabecular microarchitectural deterioration in postmenopausal women. J Bone Miner Res. 2014;29(2):380–8.PubMedCrossRef
23.
Zurück zum Zitat Vilayphiou N, Boutroy S, Szulc P, Van Rietbergen B, Munoz F, Delmas PD, Chapurlat R. Finite element analysis performed on radius and tibia HR-pQCT images and fragility fractures at all sites in men. J Bone Miner Res. 2011;26(5):965–73.PubMedCrossRef Vilayphiou N, Boutroy S, Szulc P, Van Rietbergen B, Munoz F, Delmas PD, Chapurlat R. Finite element analysis performed on radius and tibia HR-pQCT images and fragility fractures at all sites in men. J Bone Miner Res. 2011;26(5):965–73.PubMedCrossRef
25.
Zurück zum Zitat Cheung AM, Adachi JD, Hanley DA, Kendler DL, Davison KS, Josse R, Brown JP, Ste-Marie LG, Kremer R, Erlandson MC, Dian L, Burghardt AJ, Boyd SK. High-resolution peripheral quantitative computed tomography for the assessment of bone strength and structure: a review by the canadian bone strength working group. Curr Osteoporos Rep. 2013;11(2):136–46.PubMedPubMedCentralCrossRef Cheung AM, Adachi JD, Hanley DA, Kendler DL, Davison KS, Josse R, Brown JP, Ste-Marie LG, Kremer R, Erlandson MC, Dian L, Burghardt AJ, Boyd SK. High-resolution peripheral quantitative computed tomography for the assessment of bone strength and structure: a review by the canadian bone strength working group. Curr Osteoporos Rep. 2013;11(2):136–46.PubMedPubMedCentralCrossRef
26.
Zurück zum Zitat Cooper D, Turinsky A, Sensen C, Hallgrimsson B. Effect of voxel size on 3D micro-CT analysis of cortical bone porosity. Calcif Tissue Int. 2007;80(3):211–9.PubMedCrossRef Cooper D, Turinsky A, Sensen C, Hallgrimsson B. Effect of voxel size on 3D micro-CT analysis of cortical bone porosity. Calcif Tissue Int. 2007;80(3):211–9.PubMedCrossRef
27.
Zurück zum Zitat Boyd SK, Davison P, Müller R, Gasser JA. Monitoring individual morphological changes over time in ovariectomized rats by in vivo micro-computed tomography. Bone. 2006;39(4):854–62.PubMedCrossRef Boyd SK, Davison P, Müller R, Gasser JA. Monitoring individual morphological changes over time in ovariectomized rats by in vivo micro-computed tomography. Bone. 2006;39(4):854–62.PubMedCrossRef
28.
Zurück zum Zitat Dempster DW, Cosman F, Kurland ES, Zhou H, Nieves J, Woelfert L, Shane E, Plavetić K, Müller R, Bilezikian J, Lindsay R. Effects of daily treatment with parathyroid hormone on bone microarchitecture and turnover in patients with osteoporosis: a paired biopsy study. J Bone Miner Res. 2001;16(10):1846–53.PubMedCrossRef Dempster DW, Cosman F, Kurland ES, Zhou H, Nieves J, Woelfert L, Shane E, Plavetić K, Müller R, Bilezikian J, Lindsay R. Effects of daily treatment with parathyroid hormone on bone microarchitecture and turnover in patients with osteoporosis: a paired biopsy study. J Bone Miner Res. 2001;16(10):1846–53.PubMedCrossRef
29.
Zurück zum Zitat Armas LAG, Akhter MP, Drincic A, Recker RR. Trabecular bone histomorphometry in humans with type 1 diabetes mellitus. Bone. 2012;50(1):91–6.PubMedCrossRef Armas LAG, Akhter MP, Drincic A, Recker RR. Trabecular bone histomorphometry in humans with type 1 diabetes mellitus. Bone. 2012;50(1):91–6.PubMedCrossRef
30.
Zurück zum Zitat Wang X, Masse DB, Leng H, Hess KP, Ross RD, Roeder RK, Niebur GL. Detection of trabecular bone microdamage by micro-computed tomography. J Biomech. 2007;40(15):3397–403.PubMedPubMedCentralCrossRef Wang X, Masse DB, Leng H, Hess KP, Ross RD, Roeder RK, Niebur GL. Detection of trabecular bone microdamage by micro-computed tomography. J Biomech. 2007;40(15):3397–403.PubMedPubMedCentralCrossRef
31.
Zurück zum Zitat Tang SY, Vashishth D. A non-invasive in vitro technique for the three-dimensional quantification of microdamage in trabecular bone. Bone. 2007;40(5):1259–64.PubMedPubMedCentralCrossRef Tang SY, Vashishth D. A non-invasive in vitro technique for the three-dimensional quantification of microdamage in trabecular bone. Bone. 2007;40(5):1259–64.PubMedPubMedCentralCrossRef
32.
Zurück zum Zitat Dong P, Haupert S, Hesse B, Langer M, Gouttenoire P-J, Bousson V, Peyrin F. 3D osteocyte lacunar morphometric properties and distributions in human femoral cortical bone using synchrotron radiation micro-CT images. Bone. 2014;60:172–85.PubMedCrossRef Dong P, Haupert S, Hesse B, Langer M, Gouttenoire P-J, Bousson V, Peyrin F. 3D osteocyte lacunar morphometric properties and distributions in human femoral cortical bone using synchrotron radiation micro-CT images. Bone. 2014;60:172–85.PubMedCrossRef
33.
Zurück zum Zitat Giessibl FJ. AFM’s path to atomic resolution. Mater Today. 2005;8(5):32–41.CrossRef Giessibl FJ. AFM’s path to atomic resolution. Mater Today. 2005;8(5):32–41.CrossRef
34.
Zurück zum Zitat Revenko I, Sommer F, Minh DT, Garrone R, Franc JM. Atomic force microscopy study of the collagen fibre structure. Biol Cell. 1994;80(1):67–9.PubMedCrossRef Revenko I, Sommer F, Minh DT, Garrone R, Franc JM. Atomic force microscopy study of the collagen fibre structure. Biol Cell. 1994;80(1):67–9.PubMedCrossRef
35.
Zurück zum Zitat Baselt DR, Revel JP, Baldeschwieler JD. Subfibrillar structure of type I collagen observed by atomic force microscopy. Biophys J. 1993;65(6):2644–55.PubMedPubMedCentralCrossRef Baselt DR, Revel JP, Baldeschwieler JD. Subfibrillar structure of type I collagen observed by atomic force microscopy. Biophys J. 1993;65(6):2644–55.PubMedPubMedCentralCrossRef
36.
Zurück zum Zitat Thurner PJ, Oroudjev E, Jungmann R, Kreutz C, Kindt JH, Schitter G, et al. Imaging of bone ultrastructure using atomic force microscopy. In: Modern research and educational topics in microscopy. 3rd ed. Badajoz: Formatex; 2007. pp. 37–48. Thurner PJ, Oroudjev E, Jungmann R, Kreutz C, Kindt JH, Schitter G, et al. Imaging of bone ultrastructure using atomic force microscopy. In: Modern research and educational topics in microscopy. 3rd ed. Badajoz: Formatex; 2007. pp. 37–48.
37.
Zurück zum Zitat Casuso I, Kodera N, Le Grimellec C, Ando T, Scheuring S. Contact-mode high-resolution high-speed atomic force microscopy movies of the purple membrane. Biophys J. 2009;97(5):1354–61.PubMedPubMedCentralCrossRef Casuso I, Kodera N, Le Grimellec C, Ando T, Scheuring S. Contact-mode high-resolution high-speed atomic force microscopy movies of the purple membrane. Biophys J. 2009;97(5):1354–61.PubMedPubMedCentralCrossRef
38.
Zurück zum Zitat de Jong WF. La substance minérale dans les os. Recl des Trav Chim des Pays-Bas. 2010;45(6):445–8.CrossRef de Jong WF. La substance minérale dans les os. Recl des Trav Chim des Pays-Bas. 2010;45(6):445–8.CrossRef
39.
Zurück zum Zitat Bonar LC, Roufosse AH, Sabine WK, Grynpas MD, Glimcher MJ. X-ray diffraction studies of the crystallinity of bone mineral in newly synthesized and density fractionated bone. Calcif Tissue Int. 1983;35(1):202–9.PubMedCrossRef Bonar LC, Roufosse AH, Sabine WK, Grynpas MD, Glimcher MJ. X-ray diffraction studies of the crystallinity of bone mineral in newly synthesized and density fractionated bone. Calcif Tissue Int. 1983;35(1):202–9.PubMedCrossRef
40.
Zurück zum Zitat Handschin RG, Stern WB. X-ray diffraction studies on the lattice perfection of human bone apatite (Crista Iliaca). Bone. 1995;16(4 SUPPL.):S355–63.CrossRef Handschin RG, Stern WB. X-ray diffraction studies on the lattice perfection of human bone apatite (Crista Iliaca). Bone. 1995;16(4 SUPPL.):S355–63.CrossRef
41.
Zurück zum Zitat Eanes ED, Hailer AW. The effect of fluoride on the size and morphology of apatite crystals grown from physiologic solutions. Calcif Tissue Int. 1998;63(3):250–7.PubMedCrossRef Eanes ED, Hailer AW. The effect of fluoride on the size and morphology of apatite crystals grown from physiologic solutions. Calcif Tissue Int. 1998;63(3):250–7.PubMedCrossRef
42.
Zurück zum Zitat Tadano S, Giri B. X-ray diffraction as a promising tool to characterize bone nanocomposites. Sci Technol Adv Mater. 2016;12(6):064708.CrossRef Tadano S, Giri B. X-ray diffraction as a promising tool to characterize bone nanocomposites. Sci Technol Adv Mater. 2016;12(6):064708.CrossRef
43.
Zurück zum Zitat Fratzl P, Groschner M, Vogl G, Plenk H, Eschberger J, Fratzl-Zelman N, Koller K, Klaushofer K. Mineral crystals in calcified tissues: a comparative study by SAXS. J Bone Miner Res. 1992;7(3):329–34.PubMedCrossRef Fratzl P, Groschner M, Vogl G, Plenk H, Eschberger J, Fratzl-Zelman N, Koller K, Klaushofer K. Mineral crystals in calcified tissues: a comparative study by SAXS. J Bone Miner Res. 1992;7(3):329–34.PubMedCrossRef
44.
Zurück zum Zitat Georgiadis M, Guizar-Sicairos M, Zwahlen A, Trüssel AJ, Bunk O, Müller R, Schneider P. 3D scanning SAXS: a novel method for the assessment of bone ultrastructure orientation. Bone. 2015;71:42–52.PubMedCrossRef Georgiadis M, Guizar-Sicairos M, Zwahlen A, Trüssel AJ, Bunk O, Müller R, Schneider P. 3D scanning SAXS: a novel method for the assessment of bone ultrastructure orientation. Bone. 2015;71:42–52.PubMedCrossRef
45.
Zurück zum Zitat Almer JD, Stock SR. Internal strains and stresses measured in cortical bone via high-energy X-ray diffraction. J Struct Biol. 2005;152(1):14–27.PubMedCrossRef Almer JD, Stock SR. Internal strains and stresses measured in cortical bone via high-energy X-ray diffraction. J Struct Biol. 2005;152(1):14–27.PubMedCrossRef
46.
Zurück zum Zitat Gupta HS, Seto J, Wagermaier W, Zaslansky P, Boesecke P, Fratzl P. Cooperative deformation of mineral and collagen in bone at the nanoscale. Proc Natl Acad Sci. 2006;103(47):17741–6.PubMedPubMedCentralCrossRef Gupta HS, Seto J, Wagermaier W, Zaslansky P, Boesecke P, Fratzl P. Cooperative deformation of mineral and collagen in bone at the nanoscale. Proc Natl Acad Sci. 2006;103(47):17741–6.PubMedPubMedCentralCrossRef
47.
Zurück zum Zitat Brock GR, Kim G, Ingraffea AR, Andrews JC, Pianetta P, van der Meulen MCH. Nanoscale examination of microdamage in sheep cortical bone using synchrotron radiation transmission X-ray microscopy. PLoS ONE. 2013;8(3):e57942.PubMedPubMedCentralCrossRef Brock GR, Kim G, Ingraffea AR, Andrews JC, Pianetta P, van der Meulen MCH. Nanoscale examination of microdamage in sheep cortical bone using synchrotron radiation transmission X-ray microscopy. PLoS ONE. 2013;8(3):e57942.PubMedPubMedCentralCrossRef
48.
Zurück zum Zitat Currey JD. Effects of differences in mineralization on the mechanical properties of bone. Philos Trans R Soc B Biol Sci. 1984;304(1121):509–18.CrossRef Currey JD. Effects of differences in mineralization on the mechanical properties of bone. Philos Trans R Soc B Biol Sci. 1984;304(1121):509–18.CrossRef
49.
Zurück zum Zitat Sasaki N, Enyot A. Viscoelastic properties of bone as a function of water content. J Biomech. 1995;28(1):130–815. Sasaki N, Enyot A. Viscoelastic properties of bone as a function of water content. J Biomech. 1995;28(1):130–815.
50.
Zurück zum Zitat Bailey AJ, Sims TJ, Ebbesen EN, Mansell JP, Thomsen JS, Mosekilde L. Age-related changes in the biochemical properties of human cancellous bone collagen: relationship to bone strength. Calcif Tissue Int. 1999;65(3):203–10.PubMedCrossRef Bailey AJ, Sims TJ, Ebbesen EN, Mansell JP, Thomsen JS, Mosekilde L. Age-related changes in the biochemical properties of human cancellous bone collagen: relationship to bone strength. Calcif Tissue Int. 1999;65(3):203–10.PubMedCrossRef
51.
Zurück zum Zitat Burstein AH, Zika JM, Heiple KG, Klein L. Contribution of collagen and mineral to the elastic-plastic properties of bone. J Bone Joint Surg Am. 1975;57(7):956–61.PubMed Burstein AH, Zika JM, Heiple KG, Klein L. Contribution of collagen and mineral to the elastic-plastic properties of bone. J Bone Joint Surg Am. 1975;57(7):956–61.PubMed
52.
Zurück zum Zitat Robson MD, Gatehouse PD, Bydder GM, Neubauer S. Human Imaging of phosphorus in cortical and trabecular bone in vivo. Magn Reson Med. 2004;51(5):888–92.PubMedCrossRef Robson MD, Gatehouse PD, Bydder GM, Neubauer S. Human Imaging of phosphorus in cortical and trabecular bone in vivo. Magn Reson Med. 2004;51(5):888–92.PubMedCrossRef
53.
Zurück zum Zitat Kuhn LT, Grynpas MD, Rey CC, Wu Y, Ackerman JL, Glimcher MJ. A comparison of the physical and chemical differences between cancellous and cortical bovine bone mineral at two ages. Calcif Tissue Int. 2008;83(2):146–54.PubMedCrossRef Kuhn LT, Grynpas MD, Rey CC, Wu Y, Ackerman JL, Glimcher MJ. A comparison of the physical and chemical differences between cancellous and cortical bovine bone mineral at two ages. Calcif Tissue Int. 2008;83(2):146–54.PubMedCrossRef
54.
Zurück zum Zitat Wehrli FW, Fernandez-Seara MA. Nuclear magnetic resonance studies of bone water. Ann Biomed Eng. 2005;33(1):79–86.PubMedCrossRef Wehrli FW, Fernandez-Seara MA. Nuclear magnetic resonance studies of bone water. Ann Biomed Eng. 2005;33(1):79–86.PubMedCrossRef
55.
Zurück zum Zitat Granke M, Does MD, Nyman JS. The role of water compartments in the material properties of cortical bone. Calcif Tissue Int. 2015;97(3):292–307.PubMedPubMedCentralCrossRef Granke M, Does MD, Nyman JS. The role of water compartments in the material properties of cortical bone. Calcif Tissue Int. 2015;97(3):292–307.PubMedPubMedCentralCrossRef
56.
Zurück zum Zitat Nyman JS, Ni Q, Nicolella DP, Wang X. Measurements of mobile and bound water by nuclear magnetic resonance correlate with mechanical properties of bone. Bone. 2008;42(1):193–9.PubMedCrossRef Nyman JS, Ni Q, Nicolella DP, Wang X. Measurements of mobile and bound water by nuclear magnetic resonance correlate with mechanical properties of bone. Bone. 2008;42(1):193–9.PubMedCrossRef
57.
Zurück zum Zitat Singh C, Rai RK, Kayastha AM, Sinha N. Ultra fast magic angle spinning solid-state NMR spectroscopy of intact bone. Magn Reson Chem. 2016;54(2):132–5.PubMedCrossRef Singh C, Rai RK, Kayastha AM, Sinha N. Ultra fast magic angle spinning solid-state NMR spectroscopy of intact bone. Magn Reson Chem. 2016;54(2):132–5.PubMedCrossRef
58.
Zurück zum Zitat Mroue KH, Nishiyama Y, Kumar Pandey M, Gong B, McNerny E, Kohn DH, Morris MD, Ramamoorthy A. Proton-detected solid-state NMR spectroscopy of bone with ultrafast magic angle spinning. Sci Rep. 2015;5:11991.PubMedPubMedCentralCrossRef Mroue KH, Nishiyama Y, Kumar Pandey M, Gong B, McNerny E, Kohn DH, Morris MD, Ramamoorthy A. Proton-detected solid-state NMR spectroscopy of bone with ultrafast magic angle spinning. Sci Rep. 2015;5:11991.PubMedPubMedCentralCrossRef
60.
Zurück zum Zitat Boskey A, Mendelsohn R. Infrared analysis of bone in health and disease. J Biomed Opt. 2005;10(3):031102–0311029.PubMedCrossRef Boskey A, Mendelsohn R. Infrared analysis of bone in health and disease. J Biomed Opt. 2005;10(3):031102–0311029.PubMedCrossRef
61.
Zurück zum Zitat Spevak L, Flach CR, Hunter T, Mendelsohn R, Boskey AL. FTIRI parameters describing acid phosphate substitution in biologic hydroxyapatite. Calcif Tissue Int. 2013;92(5):418–28.PubMedPubMedCentralCrossRef Spevak L, Flach CR, Hunter T, Mendelsohn R, Boskey AL. FTIRI parameters describing acid phosphate substitution in biologic hydroxyapatite. Calcif Tissue Int. 2013;92(5):418–28.PubMedPubMedCentralCrossRef
62.
Zurück zum Zitat Paschalis EP, Jacenko O, Olsen B, de Crombrugghe B, Boskey AL. The role of type X collagen in endochondral ossification as deduced by Fourier transform infrared microscopy analysis. Connect Tissue Res. 1996;35(1–4):371–7.PubMedCrossRef Paschalis EP, Jacenko O, Olsen B, de Crombrugghe B, Boskey AL. The role of type X collagen in endochondral ossification as deduced by Fourier transform infrared microscopy analysis. Connect Tissue Res. 1996;35(1–4):371–7.PubMedCrossRef
63.
Zurück zum Zitat Paschalis EP, Tatakis DN, Robins S, Fratzl P, Manjubala I, Zoehrer R, Gamsjaeger S, Buchinger B, Roschger A, Phipps R, Boskey AL, Dall’Ara E, Varga P, Zysset P, Klaushofer K, Roschger P. Lathyrism-induced alterations in collagen cross-links influence the mechanical properties of bone material without affecting the mineral. Bone. 2011;49(6):1232–41.PubMedPubMedCentralCrossRef Paschalis EP, Tatakis DN, Robins S, Fratzl P, Manjubala I, Zoehrer R, Gamsjaeger S, Buchinger B, Roschger A, Phipps R, Boskey AL, Dall’Ara E, Varga P, Zysset P, Klaushofer K, Roschger P. Lathyrism-induced alterations in collagen cross-links influence the mechanical properties of bone material without affecting the mineral. Bone. 2011;49(6):1232–41.PubMedPubMedCentralCrossRef
64.
Zurück zum Zitat Donnelly E, Meredith DS, Nguyen JT, Gladnick BP, Rebolledo BJ, Shaffer AD, Lorich DG, Lane JM, Boskey AL. Reduced cortical bone compositional heterogeneity with bisphosphonate treatment in postmenopausal women with intertrochanteric and subtrochanteric fractures. J Bone Miner Res. 2012;27(3):672–8.PubMedPubMedCentralCrossRef Donnelly E, Meredith DS, Nguyen JT, Gladnick BP, Rebolledo BJ, Shaffer AD, Lorich DG, Lane JM, Boskey AL. Reduced cortical bone compositional heterogeneity with bisphosphonate treatment in postmenopausal women with intertrochanteric and subtrochanteric fractures. J Bone Miner Res. 2012;27(3):672–8.PubMedPubMedCentralCrossRef
65.
Zurück zum Zitat Carden A, Morris MD. Application of vibrational spectroscopy to the study of mineralized tissues (review). J Biomed Opt. 2000;5(3):259–68.PubMedCrossRef Carden A, Morris MD. Application of vibrational spectroscopy to the study of mineralized tissues (review). J Biomed Opt. 2000;5(3):259–68.PubMedCrossRef
67.
Zurück zum Zitat Matousek P, Stone N. Recent advances in the development of Raman spectroscopy for deep non-invasive medical diagnosis. J Biophotonics. 2013;6(1):7–19.PubMedCrossRef Matousek P, Stone N. Recent advances in the development of Raman spectroscopy for deep non-invasive medical diagnosis. J Biophotonics. 2013;6(1):7–19.PubMedCrossRef
68.
Zurück zum Zitat Buckley K, Kerns JG, Parker AW, Goodship AE, Matousek P. Decomposition of in vivo spatially offset Raman spectroscopy data using multivariate analysis techniques. J Raman Spectrosc. 2014;45(2):188–92.CrossRef Buckley K, Kerns JG, Parker AW, Goodship AE, Matousek P. Decomposition of in vivo spatially offset Raman spectroscopy data using multivariate analysis techniques. J Raman Spectrosc. 2014;45(2):188–92.CrossRef
69.
Zurück zum Zitat Hanlon E, Manoharan R, Koo T, Shafer K, Motz J, Fitzmaurice M, Kramer J, Itzkan I, Dasari R, Feld M. Prospects for in vivo Raman spectroscopy. Phys Med Biol. 2000;45(2):R1–59.PubMedCrossRef Hanlon E, Manoharan R, Koo T, Shafer K, Motz J, Fitzmaurice M, Kramer J, Itzkan I, Dasari R, Feld M. Prospects for in vivo Raman spectroscopy. Phys Med Biol. 2000;45(2):R1–59.PubMedCrossRef
70.
Zurück zum Zitat Geith T, Amarie S, Milz S, Bamberg F, Keilmann F. Visualisation of methacrylate-embedded human bone sections by infrared nanoscopy. J Biophotonics. 2014;7(6):418–24.PubMedCrossRef Geith T, Amarie S, Milz S, Bamberg F, Keilmann F. Visualisation of methacrylate-embedded human bone sections by infrared nanoscopy. J Biophotonics. 2014;7(6):418–24.PubMedCrossRef
71.
Zurück zum Zitat Boyde A. Improved digital SEM of cancellous bone: scanning direction of detection, through focus for in-focus and sample orientation. J Anat. 2003;202(2):183–94.PubMedPubMedCentralCrossRef Boyde A. Improved digital SEM of cancellous bone: scanning direction of detection, through focus for in-focus and sample orientation. J Anat. 2003;202(2):183–94.PubMedPubMedCentralCrossRef
72.
Zurück zum Zitat Boyde A, Jones SJ. Scanning electron microscopy of bone: instrument, specimen, and issues. Microsc Res Tech. 1996;33(2):92–120.PubMedCrossRef Boyde A, Jones SJ. Scanning electron microscopy of bone: instrument, specimen, and issues. Microsc Res Tech. 1996;33(2):92–120.PubMedCrossRef
73.
Zurück zum Zitat Braidotti P, Branca FP, Stagni L. Scanning electron microscopy of human cortical bone failure surfaces. J Biomech. 1997;30(2):155–62.PubMedCrossRef Braidotti P, Branca FP, Stagni L. Scanning electron microscopy of human cortical bone failure surfaces. J Biomech. 1997;30(2):155–62.PubMedCrossRef
74.
Zurück zum Zitat Perdikouri C, Tagil M, Isaksson H. Characterizing the composition of bone formed during fracture healing using scanning electron microscopy techniques. Calcif Tissue Int. 2015;96(1):11–7.PubMedCrossRef Perdikouri C, Tagil M, Isaksson H. Characterizing the composition of bone formed during fracture healing using scanning electron microscopy techniques. Calcif Tissue Int. 2015;96(1):11–7.PubMedCrossRef
75.
Zurück zum Zitat Boyde A, Maconnachie E, Reid SA, Delling G, Mundy GR. Scanning electron microscopy in bone pathology: review of methods, potential and applications. Scan Electron Microsc. 1986;Pt 4:1537–54.PubMed Boyde A, Maconnachie E, Reid SA, Delling G, Mundy GR. Scanning electron microscopy in bone pathology: review of methods, potential and applications. Scan Electron Microsc. 1986;Pt 4:1537–54.PubMed
76.
Zurück zum Zitat Roschger P, Fratzl P, Eschberger J, Klaushofer K. Validation of quantitative backscattered electron imaging for the measurement of mineral density distribution in human bone biopsies. Bone. 1998;23(4):319–26.PubMedCrossRef Roschger P, Fratzl P, Eschberger J, Klaushofer K. Validation of quantitative backscattered electron imaging for the measurement of mineral density distribution in human bone biopsies. Bone. 1998;23(4):319–26.PubMedCrossRef
77.
Zurück zum Zitat Sutton-Smith P, Beard H, Fazzalari N. Quantitative backscattered electron imaging of bone in proximal femur fragility fracture and medical illness. J Microsc. 2008;229(1):60–6.PubMedCrossRef Sutton-Smith P, Beard H, Fazzalari N. Quantitative backscattered electron imaging of bone in proximal femur fragility fracture and medical illness. J Microsc. 2008;229(1):60–6.PubMedCrossRef
78.
Zurück zum Zitat Blouin S, Puchegger S, Roschger A, Berzlanovich A, Fratzl P, Klaushofer K, Roschger P. Mapping dynamical mechanical properties of osteonal bone by scanning acoustic microscopy in time-of-flight mode. Microsc Microanal. 2014;20(3):1–13.CrossRef Blouin S, Puchegger S, Roschger A, Berzlanovich A, Fratzl P, Klaushofer K, Roschger P. Mapping dynamical mechanical properties of osteonal bone by scanning acoustic microscopy in time-of-flight mode. Microsc Microanal. 2014;20(3):1–13.CrossRef
79.
Zurück zum Zitat Eyre DR, Dickson IR, Van Ness K. Collagen cross-linking in human bone and articular cartilage. Age-related changes in the content of mature hydroxypyridinium residues. Biochem J. 1988;252(2):495–500.PubMedPubMedCentralCrossRef Eyre DR, Dickson IR, Van Ness K. Collagen cross-linking in human bone and articular cartilage. Age-related changes in the content of mature hydroxypyridinium residues. Biochem J. 1988;252(2):495–500.PubMedPubMedCentralCrossRef
80.
Zurück zum Zitat Knott L, Bailey AJ. Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone. 1998;22(3):181–7.PubMedCrossRef Knott L, Bailey AJ. Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone. 1998;22(3):181–7.PubMedCrossRef
81.
Zurück zum Zitat Uebelhart D, Gineyts E, Chapuy MC, Delmas PD. Urinary excretion of pyridinium crosslinks: a new marker of bone resorption in metabolic bone disease. Bone Miner. 1990;8(1):87–96.PubMedCrossRef Uebelhart D, Gineyts E, Chapuy MC, Delmas PD. Urinary excretion of pyridinium crosslinks: a new marker of bone resorption in metabolic bone disease. Bone Miner. 1990;8(1):87–96.PubMedCrossRef
82.
Zurück zum Zitat Saito M, Marumo K. Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int. 2010;21(2):195–214.PubMedCrossRef Saito M, Marumo K. Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int. 2010;21(2):195–214.PubMedCrossRef
83.
Zurück zum Zitat Odetti P, Rossi S, Monacelli F, Poggi A, Cirnigliaro M, Federici M, Federici A. Advanced glycation end products and bone loss during aging. Ann N Y Acad Sci. 2005;1043:710–7.PubMedCrossRef Odetti P, Rossi S, Monacelli F, Poggi A, Cirnigliaro M, Federici M, Federici A. Advanced glycation end products and bone loss during aging. Ann N Y Acad Sci. 2005;1043:710–7.PubMedCrossRef
84.
Zurück zum Zitat Iafisco M, Foltran I, Sabbatini S, Tosi G, Roveri N. Electrospun nanostructured fibers of collagen-biomimetic apatite on titanium alloy. Bioinorg Chem Appl. 2012;2012:123953.PubMedPubMedCentralCrossRef Iafisco M, Foltran I, Sabbatini S, Tosi G, Roveri N. Electrospun nanostructured fibers of collagen-biomimetic apatite on titanium alloy. Bioinorg Chem Appl. 2012;2012:123953.PubMedPubMedCentralCrossRef
86.
Zurück zum Zitat Carter DR, Hayes WC, Schurman DJ. Fatigue life of compact bone—II. Effects of microstructure and density. J Biomech. 1976;9(4):211–8.PubMedCrossRef Carter DR, Hayes WC, Schurman DJ. Fatigue life of compact bone—II. Effects of microstructure and density. J Biomech. 1976;9(4):211–8.PubMedCrossRef
87.
Zurück zum Zitat Carter DR, Hayes WC. Compact bone fatigue damage—I. Residual strength and stiffness. J Biomech. 1977;10(5–6):325–37.PubMedCrossRef Carter DR, Hayes WC. Compact bone fatigue damage—I. Residual strength and stiffness. J Biomech. 1977;10(5–6):325–37.PubMedCrossRef
88.
Zurück zum Zitat Ritchie RO, Koester KJ, Ionova S, Yao W, Lane NE, Ager JW. Measurement of the toughness of bone: a tutorial with special reference to small animal studies. Bone. 2008;43(5):798–812.PubMedPubMedCentralCrossRef Ritchie RO, Koester KJ, Ionova S, Yao W, Lane NE, Ager JW. Measurement of the toughness of bone: a tutorial with special reference to small animal studies. Bone. 2008;43(5):798–812.PubMedPubMedCentralCrossRef
89.
Zurück zum Zitat Bonfield W. Advances in the fracture mechanics of cortical bone. J Biomech. 1987;20(11–12):1071–81.PubMedCrossRef Bonfield W. Advances in the fracture mechanics of cortical bone. J Biomech. 1987;20(11–12):1071–81.PubMedCrossRef
90.
Zurück zum Zitat Ural A, Vashishth D. Hierarchical perspective of bone toughness—from molecules to fracture. Int Mater Rev. 2014;59(5):245–63.CrossRef Ural A, Vashishth D. Hierarchical perspective of bone toughness—from molecules to fracture. Int Mater Rev. 2014;59(5):245–63.CrossRef
91.
Zurück zum Zitat Turner CH, Burr DB. Basic biomechanical measurements of bone: a tutorial. Bone. 1993;14(4):595–608.PubMedCrossRef Turner CH, Burr DB. Basic biomechanical measurements of bone: a tutorial. Bone. 1993;14(4):595–608.PubMedCrossRef
92.
Zurück zum Zitat Nyman JS, Roy A, Shen X, Acuna RL, Tyler JH, Wang X. The influence of water removal on the strength and toughness of cortical bone. J Biomech. 2006;39(5):931–8.PubMedPubMedCentralCrossRef Nyman JS, Roy A, Shen X, Acuna RL, Tyler JH, Wang X. The influence of water removal on the strength and toughness of cortical bone. J Biomech. 2006;39(5):931–8.PubMedPubMedCentralCrossRef
93.
Zurück zum Zitat Currey JD. The structure and mechanics of bone. J Mater Sci. 2012;47(1):41–54.CrossRef Currey JD. The structure and mechanics of bone. J Mater Sci. 2012;47(1):41–54.CrossRef
94.
Zurück zum Zitat Van der Meulen MCH, Jepsen KJ, Miki B. Understanding bone strength: size isn’t everything. Bone. 2001;29(2):101–4.PubMedCrossRef Van der Meulen MCH, Jepsen KJ, Miki B. Understanding bone strength: size isn’t everything. Bone. 2001;29(2):101–4.PubMedCrossRef
95.
Zurück zum Zitat Müller R, Hannan M, Smith SY, Bauss F. Intermittent ibandronate preserves bone quality and bone strength in the lumbar spine after 16 months of treatment in the ovariectomized cynomolgus monkey. J Bone Miner Res. 2004;19(11):1787–96.PubMedCrossRef Müller R, Hannan M, Smith SY, Bauss F. Intermittent ibandronate preserves bone quality and bone strength in the lumbar spine after 16 months of treatment in the ovariectomized cynomolgus monkey. J Bone Miner Res. 2004;19(11):1787–96.PubMedCrossRef
96.
Zurück zum Zitat Saito M, Fujii K, Mori Y, Marumo K. Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos Int. 2006;17(10):1514–23.PubMedCrossRef Saito M, Fujii K, Mori Y, Marumo K. Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos Int. 2006;17(10):1514–23.PubMedCrossRef
97.
Zurück zum Zitat Currey JD. The effect of porosity and mineal content on the young’s modulus of elasticity of compact bone. J Biomech. 1988;21(2):131–9.PubMedCrossRef Currey JD. The effect of porosity and mineal content on the young’s modulus of elasticity of compact bone. J Biomech. 1988;21(2):131–9.PubMedCrossRef
98.
Zurück zum Zitat Seeman E. Bone quality: the material and structural basis of bone strength. J Bone Miner Metab. 2008;26(1):1–8.PubMedCrossRef Seeman E. Bone quality: the material and structural basis of bone strength. J Bone Miner Metab. 2008;26(1):1–8.PubMedCrossRef
99.
Zurück zum Zitat Goldstein SA. The mechanical properties of trabecular bone: dependence on anatomic location and function. J Biomech. 1987;20(11–12):1055–61.PubMedCrossRef Goldstein SA. The mechanical properties of trabecular bone: dependence on anatomic location and function. J Biomech. 1987;20(11–12):1055–61.PubMedCrossRef
100.
Zurück zum Zitat Reilly DT, Burstein AH. The elastic and ultimate properties of compact bone tissue. J Biomech. 1975;8(6):393IN9397–396IN11405.CrossRef Reilly DT, Burstein AH. The elastic and ultimate properties of compact bone tissue. J Biomech. 1975;8(6):393IN9397–396IN11405.CrossRef
101.
Zurück zum Zitat Tang SY, Allen MR, Phipps R, Burr DB, Vashishth D. Changes in non-enzymatic glycation and its association with altered mechanical properties following 1-year treatment with risedronate or alendronate. Osteoporos Int. 2009;20(6):887–94.PubMedCrossRef Tang SY, Allen MR, Phipps R, Burr DB, Vashishth D. Changes in non-enzymatic glycation and its association with altered mechanical properties following 1-year treatment with risedronate or alendronate. Osteoporos Int. 2009;20(6):887–94.PubMedCrossRef
102.
Zurück zum Zitat Zimmermann EA, Schaible E, Bale H, Barth HD, Tang SY, Reichert P, Busse B, Alliston T, Ager JW, Ritchie RO. Age-related changes in the plasticity and toughness of human cortical bone at multiple length scales. Proc Natl Acad Sci USA. 2011;108(35):14416–21.PubMedPubMedCentralCrossRef Zimmermann EA, Schaible E, Bale H, Barth HD, Tang SY, Reichert P, Busse B, Alliston T, Ager JW, Ritchie RO. Age-related changes in the plasticity and toughness of human cortical bone at multiple length scales. Proc Natl Acad Sci USA. 2011;108(35):14416–21.PubMedPubMedCentralCrossRef
103.
Zurück zum Zitat Zioupos P, Currey J. Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone. 1998;22(1):57–66.PubMedCrossRef Zioupos P, Currey J. Changes in the stiffness, strength, and toughness of human cortical bone with age. Bone. 1998;22(1):57–66.PubMedCrossRef
104.
Zurück zum Zitat Fazzalari NL, Forwood MR, Smith K, Manthey BA, Herreen P. Assessment of cancellous bone quality in severe osteoarthrosis: bone mineral density, mechanics, and microdamage. Bone. 1998;22(4):381–8.PubMedCrossRef Fazzalari NL, Forwood MR, Smith K, Manthey BA, Herreen P. Assessment of cancellous bone quality in severe osteoarthrosis: bone mineral density, mechanics, and microdamage. Bone. 1998;22(4):381–8.PubMedCrossRef
105.
Zurück zum Zitat Hernandez CJ, Tang SY, Baumbach BM, Hwu PB, Sakkee AN, van der Ham F, DeGroot J, Banks RA, Keaveny TM. Trabecular microfracture and the influence of pyridinium and non- enzymatic glycation mediated collagen cross-links. Bone. 2005;37(6):825–32.PubMedPubMedCentralCrossRef Hernandez CJ, Tang SY, Baumbach BM, Hwu PB, Sakkee AN, van der Ham F, DeGroot J, Banks RA, Keaveny TM. Trabecular microfracture and the influence of pyridinium and non- enzymatic glycation mediated collagen cross-links. Bone. 2005;37(6):825–32.PubMedPubMedCentralCrossRef
106.
Zurück zum Zitat Silva MJ, Brodt MD, 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;37:1639–46.PubMedCrossRef Silva MJ, Brodt MD, 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;37:1639–46.PubMedCrossRef
107.
108.
Zurück zum Zitat Hoffler CE. An application of nanoindentation technique to measure bone tissue lamellae properties. J Biomech Eng. 2005;127(7):1046.PubMedCrossRef Hoffler CE. An application of nanoindentation technique to measure bone tissue lamellae properties. J Biomech Eng. 2005;127(7):1046.PubMedCrossRef
109.
Zurück zum Zitat Weaver JK. The microscopic hardness of bone. J Bone Joint Surg. 1966;48(2):273–88.PubMed Weaver JK. The microscopic hardness of bone. J Bone Joint Surg. 1966;48(2):273–88.PubMed
110.
Zurück zum Zitat Ziv V, Wagner HD, Weiner S. Microstructure-microhardness relations in parallel-fibered and lamellar bone. Bone. 1996;18(5):417–28.PubMedCrossRef Ziv V, Wagner HD, Weiner S. Microstructure-microhardness relations in parallel-fibered and lamellar bone. Bone. 1996;18(5):417–28.PubMedCrossRef
111.
Zurück zum Zitat Dall’Ara E, Schmidt R, Zysset P. Microindentation can discriminate between damaged and intact human bone tissue. Bone. 2012;50(4):925–9.PubMedCrossRef Dall’Ara E, Schmidt R, Zysset P. Microindentation can discriminate between damaged and intact human bone tissue. Bone. 2012;50(4):925–9.PubMedCrossRef
112.
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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
113.
Zurück zum Zitat Hansma P, Turner P, Drake B, Yurtsev E, Proctor A, Mathews P, Lulejian J, Lelujian J, Randall C, Adams J, Jungmann R, Garza-de-Leon F, Fantner G, Mkrtchyan H, Pontin M, Weaver A, Brown MB, Sahar N, Rossello R, Kohn D. The bone diagnostic instrument II: indentation distance increase. Rev Sci Instrum. 2008;79(6):064303.PubMedPubMedCentralCrossRef Hansma P, Turner P, Drake B, Yurtsev E, Proctor A, Mathews P, Lulejian J, Lelujian J, Randall C, Adams J, Jungmann R, Garza-de-Leon F, Fantner G, Mkrtchyan H, Pontin M, Weaver A, Brown MB, Sahar N, Rossello R, Kohn D. The bone diagnostic instrument II: indentation distance increase. Rev Sci Instrum. 2008;79(6):064303.PubMedPubMedCentralCrossRef
114.
Zurück zum Zitat Allen MR, McNerny EM, Organ JM, Wallace JM. Response to comments on ‘true gold or pyrite: a review of reference point indentation for assessing bone mechanical properties in vivo’. J Bone Miner Res. 2015;30(12):2327.PubMedCrossRef Allen MR, McNerny EM, Organ JM, Wallace JM. Response to comments on ‘true gold or pyrite: a review of reference point indentation for assessing bone mechanical properties in vivo’. J Bone Miner Res. 2015;30(12):2327.PubMedCrossRef
115.
Zurück zum Zitat Allen MR, McNerny EM, 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;30(9):1539–50.PubMedPubMedCentralCrossRef Allen MR, McNerny EM, 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;30(9):1539–50.PubMedPubMedCentralCrossRef
116.
Zurück zum Zitat Farr JN, Amin S, Khosla S. Regarding ‘true gold or pyrite: a review of reference point indentation for assessing bone mechanical properties in vivo’. J Bone Miner Res. 2015;30(12):2325–6.PubMedCrossRef Farr JN, Amin S, Khosla S. Regarding ‘true gold or pyrite: a review of reference point indentation for assessing bone mechanical properties in vivo’. J Bone Miner Res. 2015;30(12):2325–6.PubMedCrossRef
117.
Zurück zum Zitat Jepsen KJ, Schlecht SH. Biomechanical mechanisms: resolving the apparent conundrum of why individuals with type II diabetes show increased fracture incidence despite having normal BMD. J Bone Miner Res. 2014;29(4):784–6.PubMedPubMedCentralCrossRef Jepsen KJ, Schlecht SH. Biomechanical mechanisms: resolving the apparent conundrum of why individuals with type II diabetes show increased fracture incidence despite having normal BMD. J Bone Miner Res. 2014;29(4):784–6.PubMedPubMedCentralCrossRef
119.
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.PubMedPubMedCentralCrossRef 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.PubMedPubMedCentralCrossRef
120.
Zurück zum Zitat Mellibovsky L, Prieto-Alhambra D, Mellibovsky F, Güerri-Fernández R, Nogués X, Randall C, Hansma PK, Díez-Perez A. Bone tissue properties measurement by reference point indentation in glucocorticoid-induced osteoporosis. J Bone Miner Res. 2015;30(9):1651–6.PubMedCrossRef Mellibovsky L, Prieto-Alhambra D, Mellibovsky F, Güerri-Fernández R, Nogués X, Randall C, Hansma PK, Díez-Perez A. Bone tissue properties measurement by reference point indentation in glucocorticoid-induced osteoporosis. J Bone Miner Res. 2015;30(9):1651–6.PubMedCrossRef
121.
Zurück zum Zitat Güerri-Fernández RC, Nogués X, Quesada Gõmez JM, Torres Del Pliego E, Puig L, García-Giralt N, Yoskovitz G, Mellibovsky L, Hansma PK, Díez-Pérez A, Quesada Gómez JM, Torres Del Pliego E, Puig L, García-Giralt N, Yoskovitz G, Mellibovsky L, Hansma PK, Díez-Pérez A. 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.PubMedCrossRef Güerri-Fernández RC, Nogués X, Quesada Gõmez JM, Torres Del Pliego E, Puig L, García-Giralt N, Yoskovitz G, Mellibovsky L, Hansma PK, Díez-Pérez A, Quesada Gómez JM, Torres Del Pliego E, Puig L, García-Giralt N, Yoskovitz G, Mellibovsky L, Hansma PK, Díez-Pérez A. 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.PubMedCrossRef
122.
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(6):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(6):1564–83.CrossRef
123.
Zurück zum Zitat Zysset PK, Edward Guo X, Edward Hoffler C, 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(10):1005–12.PubMedCrossRef Zysset PK, Edward Guo X, Edward Hoffler C, 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(10):1005–12.PubMedCrossRef
124.
Zurück zum Zitat Hengsberger S, Kulk A, Zysset P. A combined atomic force microscopy and nonoindentation technique to investigate the elastic properties of bine structural units. Eur Cells Mater. 2001;1:12–7. Hengsberger S, Kulk A, Zysset P. A combined atomic force microscopy and nonoindentation technique to investigate the elastic properties of bine structural units. Eur Cells Mater. 2001;1:12–7.
125.
Zurück zum Zitat Constantinides G, Ravi Chandran KS, Ulm FJ, Van Vliet KJ. Grid indentation analysis of composite microstructure and mechanics: principles and validation. Mater Sci Eng, A. 2006;430(1–2):189–202.CrossRef Constantinides G, Ravi Chandran KS, Ulm FJ, Van Vliet KJ. Grid indentation analysis of composite microstructure and mechanics: principles and validation. Mater Sci Eng, A. 2006;430(1–2):189–202.CrossRef
126.
Zurück zum Zitat Uskokovic PS, Tang CY, Tsui CP, Ignjatovic N, Uskokovic DP. Micromechanical properties of a hydroxyapatite/poly-l-lactide biocomposite using nanoindentation and modulus mapping. J Eur Ceram Soc. 2007;27(2–3):1559–64.CrossRef Uskokovic PS, Tang CY, Tsui CP, Ignjatovic N, Uskokovic DP. Micromechanical properties of a hydroxyapatite/poly-l-lactide biocomposite using nanoindentation and modulus mapping. J Eur Ceram Soc. 2007;27(2–3):1559–64.CrossRef
127.
Zurück zum Zitat Donnelly E, Williams RM, Downs SA, Dickinson ME, Baker SP, van der Meulen MCH. Quasistatic and dynamic nanomechanical properties of cancellous bone tissue relate to collagen content and organization. J Mater Res. 2006;21(08):2106–17.CrossRef Donnelly E, Williams RM, Downs SA, Dickinson ME, Baker SP, van der Meulen MCH. Quasistatic and dynamic nanomechanical properties of cancellous bone tissue relate to collagen content and organization. J Mater Res. 2006;21(08):2106–17.CrossRef
128.
Zurück zum Zitat 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(4):437–41.PubMedCrossRef 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(4):437–41.PubMedCrossRef
129.
Zurück zum Zitat 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(10):1503–9.PubMedCrossRef 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(10):1503–9.PubMedCrossRef
130.
Zurück zum Zitat Tai K, Dao M, Suresh S, Palazoglu A, Ortiz C. Nanoscale heterogeneity promotes energy dissipation in bone. Nat Mater. 2007;6(6):454–62.PubMedCrossRef Tai K, Dao M, Suresh S, Palazoglu A, Ortiz C. Nanoscale heterogeneity promotes energy dissipation in bone. Nat Mater. 2007;6(6):454–62.PubMedCrossRef
131.
Zurück zum Zitat Donnelly E, Baker SP, Boskey AL, van der Meulen MCH. Effects of surface roughness and maximum load on the mechanical properties of cancellous bone measured by nanoindentation. J Biomed Mater Res A. 2006;77(2):426–35.PubMedPubMedCentralCrossRef Donnelly E, Baker SP, Boskey AL, van der Meulen MCH. Effects of surface roughness and maximum load on the mechanical properties of cancellous bone measured by nanoindentation. J Biomed Mater Res A. 2006;77(2):426–35.PubMedPubMedCentralCrossRef
132.
Zurück zum Zitat Marshall D, Johnell O, Wedel H. Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ. 1996;312(7041):1254–9.PubMedPubMedCentralCrossRef Marshall D, Johnell O, Wedel H. Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ. 1996;312(7041):1254–9.PubMedPubMedCentralCrossRef
133.
Zurück zum Zitat Crawford RP, Cann CE, Keaveny TM. Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone. 2003;33(4):744–50.PubMedCrossRef Crawford RP, Cann CE, Keaveny TM. Finite element models predict in vitro vertebral body compressive strength better than quantitative computed tomography. Bone. 2003;33(4):744–50.PubMedCrossRef
134.
Zurück zum Zitat Keaveny TM, Hoffmann PF, Singh M, Palermo L, Bilezikian JP, Greenspan SL, Black DM. Femoral bone strength and its relation to cortical and trabecular changes after treatment with PTH, alendronate, and their combination as assessed by finite element analysis of quantitative CT scans. J Bone Miner Res. 2008;23(12):1974–82.PubMedPubMedCentralCrossRef Keaveny TM, Hoffmann PF, Singh M, Palermo L, Bilezikian JP, Greenspan SL, Black DM. Femoral bone strength and its relation to cortical and trabecular changes after treatment with PTH, alendronate, and their combination as assessed by finite element analysis of quantitative CT scans. J Bone Miner Res. 2008;23(12):1974–82.PubMedPubMedCentralCrossRef
135.
Zurück zum Zitat Liu XS, Stein EM, Zhou B, Zhang CA, Nickolas TL, Cohen A, Thomas V, McMahon DJ, Cosman F, Nieves J, Shane E, Guo XE. 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.PubMedPubMedCentralCrossRef Liu XS, Stein EM, Zhou B, Zhang CA, Nickolas TL, Cohen A, Thomas V, McMahon DJ, Cosman F, Nieves J, Shane E, Guo XE. 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.PubMedPubMedCentralCrossRef
136.
Zurück zum Zitat Milovanovic P, Zimmermann EA, Riedel C, vom Scheidt A, Herzog L, Krause M, Djonic D, Djuric M, Püschel K, Amling M, Ritchie RO, Busse B. Multi-level characterization of human femoral cortices and their underlying osteocyte network reveal trends in quality of young, aged, osteoporotic and antiresorptive-treated bone. Biomaterials. 2015;45:46–55.PubMedCrossRef Milovanovic P, Zimmermann EA, Riedel C, vom Scheidt A, Herzog L, Krause M, Djonic D, Djuric M, Püschel K, Amling M, Ritchie RO, Busse B. Multi-level characterization of human femoral cortices and their underlying osteocyte network reveal trends in quality of young, aged, osteoporotic and antiresorptive-treated bone. Biomaterials. 2015;45:46–55.PubMedCrossRef
138.
Zurück zum Zitat Wallace JM, Chen Q, Fang M, Erickson B, Orr BG, Banaszak MM. Holl, “type i collagen exists as a distribution of nanoscale morphologies in teeth, bones, and tendons”. Langmuir. 2010;26(10):7349–54.PubMedPubMedCentralCrossRef Wallace JM, Chen Q, Fang M, Erickson B, Orr BG, Banaszak MM. Holl, “type i collagen exists as a distribution of nanoscale morphologies in teeth, bones, and tendons”. Langmuir. 2010;26(10):7349–54.PubMedPubMedCentralCrossRef
Metadaten
Titel
Bone Quality Assessment Techniques: Geometric, Compositional, and Mechanical Characterization from Macroscale to Nanoscale
verfasst von
Heather B. Hunt
Eve Donnelly
Publikationsdatum
22.08.2016
Verlag
Springer US
Erschienen in
Clinical & Translational Metabolism / Ausgabe 3/2016
Print ISSN: 1534-8644
Elektronische ISSN: 2948-2445
DOI
https://doi.org/10.1007/s12018-016-9222-4

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