New laboratory tools in the assessment of bone quality

Osteoporosis International

Volumn 22, Issue 8, 2011, Pages 2225-2240

  Chappard, D ^a   Basle M F ^a   Legrand, E ^a   Audran, M ^a  

^a ANGERS UNIVERSITY HOSPITAL   (France)

Author keywords

Bone microarchitecture; Bone mineralization; Bone quality; FTIRI; MicroCT; Raman spectroscopy

Indexed keywords

COLLAGEN TYPE 1; DEOXYPYRIDINOLINE;

ATOMIC FORCE MICROSCOPY; BONE; BONE DENSITOMETRY; BONE DENSITY; BONE FRAGILITY; BONE MATRIX; BONE MINERALIZATION; BONE QUALITY; BONE REMODELING; BONE STRUCTURE; FINITE ELEMENT ANALYSIS; FLUORESCENCE MICROSCOPY; GENE MUTATION; INFRARED SPECTROSCOPY; LABORATORY TEST; MICRO-COMPUTED TOMOGRAPHY; MICRORADIOGRAPHY; MICROSCOPY; NUCLEAR MAGNETIC RESONANCE IMAGING; OSSIFICATION; OSTEOBLAST; PRIORITY JOURNAL; RAMAN SPECTROMETRY; REVIEW; SCANNING ACOUSTIC MICROSCOPY; SCANNING ELECTRON MICROSCOPY; TRABECULAR BONE;

BONE AND BONES; BONE DENSITY; BONE REMODELING; CLINICAL LABORATORY TECHNIQUES; HUMANS; OSTEOPOROSIS; OSTEOPOROTIC FRACTURES;

EID: 79960227990     PISSN: 0937941X     EISSN: 14332965     Source Type: Journal    
DOI: 10.1007/s00198-011-1573-6     Document Type: Review

References (115)

1. JA Kanis O Johnell A Oden H Johansson E McCloskey 2008 FRAX and the assessment of fracture probability in men and women from the UK Osteoporos Int 19 385 397 18292978 1:STN:280:DC%2BD1c7nvF2ntA%3D%3D
2. PD Miller ES Siris E Barrett-Connor KG Faulkner LE Wehren TA Abbott YT Chen ML Berger AC Santora LM Sherwood 2002 Prediction of fracture risk in postmenopausal white women with peripheral bone densitometry: evidence from the National Osteoporosis Risk Assessment J Bone Miner Res 17 2222 2230 12469916 (Pubitemid 35416756)
3. SR Cummings D Bates DM Black 2002 Clinical use of bone densitometry: scientific review JAMA 288 1889 1897 12377088 (Pubitemid 35168145)
4. D Marshall O Johnell H Wedel 1996 Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures BMJ 312 1254 1259 8634613 1:STN:280:DyaK283isFejtw%3D%3D (Pubitemid 26147662)
5. T Sandor D Felsenberg E Brown 1999 Comments on the hypotheses underlying fracture risk assessment in osteoporosis as proposed by the World Health Organization Calcif Tissue Int 64 267 270 10024389 1:CAS:528:DyaK1MXhs1ylsLY%3D (Pubitemid 29107249)
6. SC Schuit M van der Klift AE Weel CE de Laet H Burger E Seeman A Hofman AG Uitterlinden JP van Leeuwen HA Pols 2004 Fracture incidence and association with bone mineral density in elderly men and women: the Rotterdam Study Bone 34 195 202 14751578 1:STN:280:DC%2BD2c%2FltVCjsg%3D%3D (Pubitemid 38142449)
7. B Bouvard E Legrand M Audran D Chappard 2010 Glucocorticoid-induced osteoporosis: a review Clin Rev Bone Miner Metab 8 15 26 1:CAS:528: DC%2BC3cXhtleiurc%3D
8. N Dahl G Holmgren S Holmberg H Ersmark 1992 Fracture patterns in malignant osteopetrosis (Albers-Schonberg disease) Arch Orthop Trauma Surg 111 121 123 1562422 1:STN:280:DyaK383it1Oktg%3D%3D
9. SL Silverman 2008 Paget disease of bone: therapeutic options J Clin Rheumatol 14 299 305 18838910
10. JR Curtis AO Westfall H Cheng KG Saag E Delzell 2009 RisedronatE and ALendronate Intervention over Three Years (REALITY): minimal differences in fracture risk reduction Osteoporos Int 20 973 978 18946630 1:CAS:528: DC%2BD1MXls12kt74%3D
11. PD Delmas Z Li C Cooper 2004 Relationship between changes in bone mineral density and fracture risk reduction with antiresorptive drugs: some issues with meta-analyses J Bone Miner Res 19 330 337 14969404 1:CAS:528: DC%2BD2cXhs1elsrg%3D (Pubitemid 38116748)
12. SA Quandt DE Thompson DL Schneider MC Nevitt DM Black 2005 Effect of alendronate on vertebral fracture risk in women with bone mineral density T scores of -1.6 to -2.5 at the femoral neck: the Fracture Intervention Trial Mayo Clin Proc 80 343 349 15757015 1:CAS:528:DC%2BD2MXis1SltL0%3D (Pubitemid 40316296)
13. PJ Meunier P Chavassieux 1985 L'histomorphométrie moyen d'évaluation de la masse osseuse Rev Rhum Malad Osteo Art 52 669 673 1:STN:280:DyaL287ltFalsw%3D%3D (Pubitemid 16217861)
14. AM Parfitt CHE Matthews AR Villanueva M Kleerekoper B Frame DS Rao 1983 Relationships between surface, volume and thickness of iliac trabecular bone in aging and in osteoporosis. Implications for the microanatomic and cellular mechanisms of bone loss J Clin Invest 72 1396 1409 6630513 1:STN:280: DyaL2c%2FjtlWlug%3D%3D (Pubitemid 13013772)
15. D Chappard C Alexandre G Riffat 1988 Spatial distribution of trabeculae in iliac bone from 145 osteoporotic females Acta Anat 132 137 142 3414359 1:STN:280:DyaL1czitlKntg%3D%3D
16. DP Fyhrie 2005 Summary-measuring "bone quality" J Muscul Skel Neur Interact 5 318 320 1:STN:280:DC%2BD2MnlslOjtg%3D%3D
17. D Felsenberg S Boonen 2005 The bone quality framework: determinants of bone strength and their interrelationships, and implications for osteoporosis management Clin Ther 27 1 11 15763602 (Pubitemid 40342573)
18. J Wei P Ducy 2010 Co-dependence of bone and energy metabolisms Arch Biochem Biophys 503 35 40 20515647 1:CAS:528:DC%2BC3cXhtFygtLjN
19. HD Barth ME Launey AA MacDowell JW Ager III RO Ritchie 2010 On the effect of X-ray irradiation on the deformation and fracture behavior of human cortical bone Bone 46 1475 1485 20206724
20. ME Launey MJ Buehler RO Ritchie 2010 On the mechanistic origins of toughness in bone Ann Rev Mater Res 40 1
21. D Chappard MF Baslé E Legrand M Audran 2008 Trabecular bone microarchitecture: a review Morphologie 92 162 170 19019718 1:STN:280: DC%2BD1cjovFygsQ%3D%3D
22. Chapurlat R, Chappard D (2009) L'ostéoporose, mieux la comprendre pour mieux la traiter. Wolters Kluwer, Lippincott Williams & Wilkins, Rueil-Malmaison
23. PJ Roughley F Rauch FH Glorieux 2003 Osteogenesis imperfecta-clinical and molecular diversity Eur Cell Mater 5 41 77 14562271 1:CAS:528: DC%2BD3sXntFCqu7s%3D
24. P Zioupos 2001 Ageing human bone: factors affecting its biomechanical properties and the role of collagen J Biomater Appl 15 187 229 11261600 1:CAS:528:DC%2BD3MXisVCisLw%3D (Pubitemid 32293197)
25. RD Blank TH Baldini M Kaufman S Bailey R Gupta Y Yershov AL Boskey SN Coppersmith P Demant EP Paschalis 2003 Spectroscopically determined collagen Pyr/deH-DHLNL cross-link ratio and crystallinity indices differ markedly in recombinant congenic mice with divergent calculated bone tissue strength Connect Tissue Res 44 134 142 14504033 1:CAS:528:DC%2BD3sXntlaqtL0%3D (Pubitemid 37304545)
26. X Banse JP Devogelaer A Lafosse TJ Sims M Grynpas AJ Bailey 2002 Cross-link profile of bone collagen correlates with structural organization of trabeculae Bone 31 70 76 12110415 1:CAS:528:DC%2BD38XltFWgsr8%3D (Pubitemid 34754428)
27. M Saito K Marumo 2010 Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus Osteoporos Int 21 195 214 19760059 1:CAS:528: DC%2BC3cXjtl2ntg%3D%3D
28. H Oxlund L Mosekilde G Ortoft 1996 Reduced concentration of collagen reducible cross links in human trabecular bone with respect to age and osteoporosis Bone 19 479 484 8922646 1:CAS:528:DyaK28XnsVakt7k%3D
29. S Blouin HW Thaler C Korninger R Schmid JG Hofstaetter R Zoehrer R Phipps K Klaushofer P Roschger EP Paschalis 2009 Bone matrix quality and plasma homocysteine levels Bone 44 959 964 19168164 1:CAS:528:DC%2BD1MXktFagtr8%3D
30. H Libouban R Filmon A Maureac MF Baslé D Chappard 2009 Fetuin and osteocalcin interact with calcospherite formation during the calcification process of poly(2-hydroxyethylmethacrylate) in vitro: a Raman microspectroscopic monitoring J Raman Spectrosc 40 1234 1239 1:CAS:528:DC%2BD1MXhtFGlsbrE
31. JL Holden JG Clement PP Phakey 1995 Age and temperature related changes to the ultrastructure and composition of human bone mineral J Bone Miner Res 10 1400 1409 7502713 1:CAS:528:DyaK2MXotlyhtrk%3D
32. T Iyo Y Maki N Sasaki M Nakata 2004 Anisotropic viscoelastic properties of cortical bone J Biomech 37 1433 1437 15275852 (Pubitemid 38953254)
33. G Boivin PJ Meunier 2003 The mineralization of bone tissue: a forgotten dimension in osteoporosis research Osteoporos Int 14 Suppl 3 S19 24 12730799
34. HS Gupta J Seto W Wagermaier P Zaslansky P Boesecke P Fratzl 2006 Cooperative deformation of mineral and collagen in bone at the nanoscale Proc Natl Acad Sci USA 103 17741 17746 17095608 1:CAS:528:DC%2BD28Xht1KnurfM (Pubitemid 44852230)
35. JP Gorski 1998 Is all bone the same? Distinctive distributions and properties of non-collagenous matrix proteins in lamellar vs. woven bone imply the existence of different underlying osteogenic mechanisms Crit Rev Oral Biol Med 9 201 223 9603236 1:CAS:528:DyaK1cXjt1Snsrs%3D (Pubitemid 28225856)
36. L Mulder JH Koolstra JM den Toonder TM van Eijden 2008 Relationship between tissue stiffness and degree of mineralization of developing trabecular bone J Biomed Mater Res A 84 508 515 17618500
37. E Seeman 2003 Periosteal bone formation-a neglected determinant of bone strength N Engl J Med 349 320 323 12878736 (Pubitemid 36886235)
38. I Singh 1978 The architecture of cancellous bone J Anat 127 305 310 721692 1:STN:280:DyaE1M%2FmslGjtQ%3D%3D (Pubitemid 9024983)
39. JE Bertram AA Biewener 1988 Bone curvature: sacrificing strength for load predictability? J Theor Biol 131 75 92 3419194 1:STN:280:DyaL1czjtlyrsw%3D%3D
40. LE Lanyon S Bourn 1979 The influence of mechanical function on the development and remodeling of the tibia. An experimental study in sheep J Bone Joint Surg Am 61 263 273 422613 1:STN:280:DyaE1M7jtVGitw%3D%3D (Pubitemid 9130299)
41. S Boonen R Koutri J Dequeker J Aerssens G Lowet J Nijs G Verbeke E Lesaffre P Geusens 1995 Measurement of femoral geometry in type I and type II osteoporosis: differences in hip axis length consistent with heterogeneity in the pathogenesis of osteoporotic fractures J Bone Miner Res 10 1908 1912 8619371 1:STN:280:DyaK287pt1Oisw%3D%3D
42. KG Faulkner SR Cummings D Black L Palermo CC Gluer HK Genant 1993 Simple measurement of femoral geometry predicts hip fracture: the study of osteoporotic fractures J Bone Miner Res 8 1211 1217 8256658 1:STN:280:DyaK2c%2FnvVyhsw%3D%3D (Pubitemid 23308114)
43. Y Duan A Parfitt E Seeman 1999 Vertebral bone mass, size, and volumetric density in women with spinal fractures J Bone Miner Res 14 1796 1802 10491228 1:STN:280:DyaK1MvitFCrsg%3D%3D (Pubitemid 29455829)
44. V Gilsanz DT Gibbens TF Roe M Carlson MO Senac MI Boechat HK Huang EE Schulz CR Libanati CC Cann 1988 Vertebral bone density in children: effect of puberty Radiology 166 847 850 3340782 1:STN:280:DyaL1c7isFyqsw%3D%3D (Pubitemid 18058955)
45. C Bergot V Bousson A Meunier M Laval-Jeantet JD Laredo 2002 Hip fracture risk and proximal femur geometry from DXA scans Osteoporos Int 13 542 550 12111014 1:STN:280:DC%2BD38zmslSnuw%3D%3D (Pubitemid 34790626)
46. AS Karlamangla E Barrett-Connor J Young GA Greendale 2004 Hip fracture risk assessment using composite indices of femoral neck strength: the Rancho Bernardo study Osteoporos Int 15 62 70 14605798 (Pubitemid 38252442)
47. E Seeman 2008 Bone quality: the material and structural basis of bone strength J Bone Miner Metab 26 1 8 18095057 (Pubitemid 350308006)
48. E Seeman PD Delmas 2006 Bone quality-the material and structural basis of bone strength and fragility N Engl J Med 354 2250 2261 16723616 1:CAS:528:DC%2BD28XkvVShsbw%3D
49. HK Genant JY Jiang 2006 Imaging assessment of bone quality in osteoporosis Clin Rev Bone Miner Metab 4 213 224 (Pubitemid 44337234)
50. CL Benhamou E Lespessailles G Jacquet R Harba R Jennane T Loussot D Tourliere W Ohley 1994 Fractal organization of trabecular bone images on calcaneus radiographs J Bone Miner Res 9 1909 1918 7872056 1:STN:280: DyaK2M7ns1yrsA%3D%3D (Pubitemid 24363147)
51. P Guggenbuhl F Bodic L Hamel MF Baslé D Chappard 2006 Texture analysis of X-ray radiographs of iliac bone is correlated with bone micro-CT Osteoporos Int 17 447 454 16416031 1:STN:280:DC%2BD287msF2guw%3D%3D
52. Frost HM (1976) A method of analysis of trabecular bone dynamics. In: Meunier PJ (ed) Bone histomorphometry-2nd international workshop. Armour Montagu Lab, Levallois-Perret, pp 445-476
53. Chappard D (2009) Technical aspects: how do we best prepare bone samples for proper histological analysis? In: Heymann D (ed) Bone cancer: progression and therapeutic approaches. Elsevier, London, pp 203-210
54. NL Fazzalari IH Parkinson 1996 Fractal dimension and architecture of trabecular bone J Pathol 178 100 105 8778308 1:STN:280:DyaK283msVaitQ%3D%3D (Pubitemid 26052088)
55. Z Tabor 2004 Analysis of the influence of image resolution on the discriminating power of trabecular bone architectural parameters Bone 34 170 179 14751575 (Pubitemid 38142446)
56. D Chappard E Legrand B Haettich G Chales B Auvinet JP Eschard JP Hamelin MF Baslé M Audran 2001 Fractal dimension of trabecular bone: comparison of three histomorphometric computed techniques for measuring the architectural two-dimensional complexity J Pathol 195 515 521 11745685 1:STN:280: DC%2BD3Mnps1Khtw%3D%3D (Pubitemid 33069678)
57. D Chappard E Legrand C Pascaretti MF Baslé M Audran 1999 Comparison of eight histomorphometric methods for measuring trabecular bone architecture by image analysis on histological sections Microsc Res Tech 45 303 312 10383123 1:STN:280:DyaK1MzhtVCqtA%3D%3D (Pubitemid 29264994)
58. P Ruegsegger 1994 The use of peripheral QCT in the evaluation of bone remodelling Endocrinol 4 167 176 (Pubitemid 24174615)
59. A Sasov D Van Dyck 1998 Desktop X-ray microscopy and microtomography J Microsc 191 151 158 1:CAS:528:DyaK1cXlvF2gsr4%3D (Pubitemid 28378440)
60. R Rizzoli M Laroche MA Krieg I Frieling T Thomas P Delmas D Felsenberg 2010 Strontium ranelate and alendronate have differing effects on distal tibia bone microstructure in women with osteoporosis Rheumatol Int 30 1341 1348 20512336 1:CAS:528:DC%2BC3cXpt12msrw%3D
61. F Peyrin C Muller Y Carillon S Nuzzo A Bonnassie A Briguet 2001 Synchrotron radiation microCT: a reference tool for the characterization of bone samples Adv Exp Med Biol 496 129 142 11783615 1:STN:280: DC%2BD38%2FlvVeisA%3D%3D (Pubitemid 34106902)
62. D Chappard N Josselin C Rouge-Maillart E Legrand MF Baslé M Audran 2007 Bone microarchitecture in males with corticosteroid-induced osteoporosis Osteoporos Int 18 487 494 17120178 1:STN:280:DC%2BD2s7jtVGmsQ%3D%3D (Pubitemid 46354926)
63. LD Hordon M Itoda PA Shore RC Shore M Heald M Brown JA Kanis GA Rodan JE Aaron 2006 Preservation of thoracic spine microarchitecture by alendronate: comparison of histology and microCT Bone 38 444 449 16361121 1:CAS:528:DC%2BD28XhslyrtLY%3D (Pubitemid 43255439)
64. JM Alexander I Bab S Fish R Müller T Uchiyama G Gronowicz M Nahounou Q Zhao DW White M Chorev D Gazit M Rosenblatt 2001 Human parathyroid hormone 1-34 reverses bone loss in ovariectomized mice J Bone Miner Res 16 1665 1673 11547836 1:CAS:528:DC%2BD3MXmvV2qsLg%3D (Pubitemid 32786436)
65. D Chappard N Retailleau-Gaborit E Legrand MF Baslé M Audran 2005 Comparison insight bone measurements by histomorphometry and microCT J Bone Miner Res 20 1177 1184 15940370 (Pubitemid 40863805)
66. R Amprino 1952 Rapporti fra processi di ricostruzione e distribuzione dei minerali nelle ossa. I. Ricerche esguite col metodo dis tudio dei raggi Roentgen Z Zellforsch 37 144 183 13123251 1:STN:280:DyaG2c%2FksValtg%3D%3D
67. J Jowsey PJ Kelly BL Riggs AJ Bianco DA Scholz J Gershon-Cohen 1965 Quantitative microradiographic studies of normal and osteoporotic bone J Bone Joint Surg Am 47 785 872 14302381 1:STN:280:DyaF2M7gslSjtQ%3D%3D
68. A Dhem C Nyssen-Behets J Coppens 1998 Post-menopausal osteoporosis: microradiographic aspects It J Anat Embryol 103 343 352 1:STN:280: DC%2BD3M3jvVWktQ%3D%3D
69. G Boivin PJ Meunier 2002 The degree of mineralization of bone tissue measured by computerized quantitative contact microradiography Calcif Tissue Int 70 503 511 12019458 1:CAS:528:DC%2BD38XlvV2ktLo%3D (Pubitemid 36929589)
70. G Boivin Y Bala A Doublier D Farlay LG Ste-Marie PJ Meunier PD Delmas 2008 The role of mineralization and organic matrix in the microhardness of bone tissue from controls and osteoporotic patients Bone 43 532 538 18599391 1:STN:280:DC%2BD1critFyrsg%3D%3D
71. GY Boivin PM Chavassieux AC Santora J Yates PJ Meunier 2000 Alendronate increases bone strength by increasing the mean degree of mineralization of bone tissue in osteoporotic women Bone 27 687 694 11062357 1:CAS:528: DC%2BD3cXosFygtL8%3D
72. WJ Whitehouse ED Dyson CK Jackson 1971 The scanning electron microscope in studies of trabecular bone from a human vertebral body J Anat 108 481 496 4930228 1:STN:280:DyaE3M7oslKlsQ%3D%3D
73. A Boyde SJ Jones 1983 Back-scattered electron imaging of skeletal tissues Metab Bone Dis Relat Res 5 145 150 6676627 (Pubitemid 14143238)
74. P Roschger P Fratzl J Eschberger K Klaushofer 1998 Validation of quantitative backscattered electron imaging for the measurement of mineral density distribution in human bone biopsies Bone 23 319 326 9763143 1:STN:280:DyaK1cvjsVWjtQ%3D%3D (Pubitemid 28454623)
75. A Corsi MT Collins M Riminucci PGT Howell A Boyde P Gehron Robey P Bianco 2003 Osteomalacic and hyperparathyroid changes in fibrous dysplasia of bone: core biopsy studies and clinical correlations J Bone Miner Res 18 1235 1246 12854833 (Pubitemid 37294916)
76. P Roschger EP Paschalis P Fratzl K Klaushofer 2008 Bone mineralization density distribution in health and disease Bone 42 456 466 18096457 1:STN:280:DC%2BD1c7itVCrtw%3D%3D
77. LJ Smith JP Schirer NL Fazzalari 2010 The role of mineral content in determining the micromechanical properties of discrete trabecular bone remodeling packets J Biomech 43 3144 3149 20723898
78. AL Boskey NP Camacho R Mendelsohn SB Doty I Binderman 1992 FT-IR microscopic mappings of early mineralization in chick limb bud mesenchymal cell cultures Calcif Tissue Int 51 443 448 1451012 1:STN:280:DyaK3s%2Fot1Gltg%3D%3D (Pubitemid 23039980)
79. O Akkus F Adar MB Schaffler 2004 Age-related changes in physicochemical properties of mineral crystals are related to impaired mechanical function of cortical bone Bone 34 443 453 15003792 1:CAS:528:DC%2BD2cXhvFalu7Y%3D (Pubitemid 38314909)
80. EP Paschalis E DiCarlo F Betts P Sherman R Mendelsohn AL Boskey 1996 FTIR microspectroscopic analysis of human osteonal bone Calcif Tissue Int 59 480 487 8939775 1:CAS:528:DyaK28XnsVWitLg%3D (Pubitemid 26397169)
81. 3 vibrational modes in synthetic and biological apatites Calcif Tissue Int 63 475 481 9817941 1:CAS:528:DyaK1cXnsVOhsbg%3D (Pubitemid 28531796)
82. A Boskey 2003 Bone mineral crystal size Osteoporos Int 14 S16 S20
83. EP Paschalis K Verdelis SB Doty AL Boskey R Mendelsohn M Yamauchi 2001 Spectroscopic characterization of collagen cross-links in bone J Bone Miner Res 16 1821 1828 11585346 1:CAS:528:DC%2BD3MXnsVKqt7c%3D (Pubitemid 32911488)
84. JL Katz A Meunier 1993 Scanning acoustic microscope studies of the elastic properties of osteons and osteon lamellae J Biomech Eng 115 543 548 8302038 1:STN:280:DyaK2c7jtlKmsg%3D%3D (Pubitemid 24000879)
85. M Regauer P Jurgens U Budenhofer M Hartstock W Bocker D Burklein W Mutschler R Sader M Schieker 2006 Quantitative scanning acoustic microscopy compared to microradiography for assessment of new bone formation Bone 38 564 570 16253577
86. S Bumrerraj JL Katz 2001 Scanning acoustic microscopy study of human cortical and trabecular bone Ann Biomed Eng 29 1034 1042 11853252 1:STN:280:DC%2BD387hvFCqtQ%3D%3D (Pubitemid 34167814)
87. SE Olesiak ML Oyen VL Ferguson 2010 Viscous-elastic-plastic behavior of bone using Berkovich nanoindentation Mechan Time Dep Mater 14 111 124 1:CAS:528:DC%2BC3cXktVahsrw%3D
88. ME Roy JY Rho TY Tsui ND Evans GM Pharr 1999 Mechanical and morphological variation of the human lumbar vertebral cortical and trabecular bone J Biomed Mater Res 44 191 197 10397920 1:CAS:528:DyaK1cXotVWjs7w%3D (Pubitemid 28566807)
89. JY Rho ME Roy 2nd TY Tsui GM Pharr 1999 Elastic properties of microstructural components of human bone tissue as measured by nanoindentation J Biomed Mater Res 45 48 54 10397957 1:CAS:528:DyaK1MXhtVWrs7c%3D (Pubitemid 29068438)
90. JY Rho P Zioupos JD Currey GM Pharr 1999 Variations in the individual thick lamellar properties within osteons by nanoindentation Bone 25 295 300 10495133 1:STN:280:DyaK1Mvitlehtg%3D%3D (Pubitemid 29406055)
91. Z Fan JG Swadener JY Rho ME Roy GM Pharr 2002 Anisotropic properties of human tibial cortical bone as measured by nanoindentation J Orthop Res 20 806 810 12168671 1:STN:280:DC%2BD38vhsV2gtg%3D%3D (Pubitemid 34823002)
92. P Ammann I Badoud S Barraud R Dayer R Rizzoli 2007 Strontium ranelate treatment improves trabecular and cortical intrinsic bone tissue quality, a determinant of bone strength J Bone Miner Res 22 1419 1425 17547534 1:CAS:528:DC%2BD2sXhtVynsLjO (Pubitemid 351339686)
93. N Fratzl-Zelman P Roschger A Gourrier M Weber BM Misof N Loveridge J Reeve K Klaushofer P Fratzl 2009 Combination of nanoindentation and quantitative backscattered electron imaging revealed altered bone material properties associated with femoral neck fragility Calcif Tissue Int 85 335 343 19756347 1:CAS:528:DC%2BD1MXht1ektLvK
94. MJ Silva MD Brodt Z Fan JY Rho 2004 Nanoindentation and whole-bone bending estimates of material properties in bones from the senescence accelerated mouse SAMP6 J Biomech 37 1639 1646 15388305 (Pubitemid 39237576)
95. H Zhao H Jin J Cai S Ding 2010 The process of collagen biomineralization observed by AFM in a model dual membrane diffusion system Ultramicroscopy 110 1306 1311 20619970 1:CAS:528:DC%2BC3cXhtFWhu7%2FO
96. T Hassenkam GE Fantner JA Cutroni JC Weaver DE Morse PK Hansma 2004 High-resolution AFM imaging of intact and fractured trabecular bone Bone 35 4 10 15207735 (Pubitemid 38789142)
97. A Dumas C Gaudin-Audrain G Mabilleau P Massin L Hubert MF Baslé D Chappard 2006 The influence of processes for the purification of human bone allografts on the matrix surface and cytocompatibility Biomaterials 27 4204 4211 16618501 1:CAS:528:DC%2BD28XktVWrtb4%3D
98. Y Chevalier E Quek B Borah G Gross J Stewart T Lang P Zysset 2010 Biomechanical effects of teriparatide in women with osteoporosis treated previously with alendronate and risedronate: results from quantitative computed tomography-based finite element analysis of the vertebral body Bone 46 41 48 19800436 1:CAS:528:DC%2BD1MXhsFynsrvI
99. CH Kim E Takai H Zhou D von Stechow R Muller DW Dempster XE Guo 2003 Trabecular bone response to mechanical and parathyroid hormone stimulation: the role of mechanical microenvironment J Bone Miner Res 18 2116 2125 14672346 1:CAS:528:DC%2BD3sXhtVSqtr7L (Pubitemid 37463305)
100. J Homminga BR McCreadie TE Ciarelli H Weinans SA Goldstein R Huiskes 2002 Cancellous bone mechanical properties from normals and patients with hip fractures differ on the structure level, not on the bone hard tissue level Bone 30 759 764 11996916 1:STN:280:DC%2BD383lslGntw%3D%3D (Pubitemid 34467999)
101. PK Saha Y Xu H Duan A Heiner G Liang 2010 Volumetric topological analysis: a novel approach for trabecular bone classification on the continuum between plates and rods IEEE Trans Med Imaging 29 1821 1838 20562041
102. C Boyle IY Kim 2011 Three-dimensional micro-level computational study of Wolff's law via trabecular bone remodeling in the human proximal femur using design space topology optimization J Biomech 10.1016/j.jbiomech.2010.1011.1029
103. XS Liu A Cohen E Shane E Stein H Rogers SL Kokolus PT Yin DJ McMahon JM Lappe RR Recker XE Guo 2010 Individual trabeculae segmentation (ITS)-based morphological analysis of high-resolution peripheral quantitative computed tomography images detects abnormal trabecular plate and rod microarchitecture in premenopausal women with idiopathic osteoporosis J Bone Miner Res 25 1496 1505 20200967
104. L Cristofolini E Schileo M Juszczyk F Taddei S Martelli M Viceconti 2010 Mechanical testing of bones: the positive synergy of finite-element models and in vitro experiments Philos Trans R Soc A Math Phys Eng Sci 368 2725 2763
105. RS Weinstein RW Nicholas SC Manolagas 2000 Apoptosis of osteocytes in glucocorticoid-induced osteonecrosis of the hip J Clin Endocrinol Metab 85 2907 2912 10946902 1:CAS:528:DC%2BD3cXnslahsbo%3D (Pubitemid 32269172)
106. S Mori R Harruff W Ambrosius DB Burr 1997 Trabecular bone volume and microdamage accumulation in the femoral heads of women with and without femoral neck fractures Bone 21 521 526 9430242 1:STN:280:DyaK1c%2FptVWjtQ%3D%3D (Pubitemid 28029695)
107. C Gaudin-Audrain Y Gallois F Pascaretti-Grizon L Hubert P Massin MF Baslé D Chappard 2008 Osteopontin is histochemically detected by the AgNOR acid-silver staining Histol Histopathol 23 469 478 18228204 1:CAS:528:DC%2BD1cXlslWktro%3D (Pubitemid 351552332)
108. F Pascaretti-Grizon C Gaudin-Audrain Y Gallois N Retaillaud-Gaborit MF Baslé D Chappard 2007 Osteopontin is an argentophilic protein in the bone matrix and in cells of kidney convoluted tubules Morphologie 91 180 185 18036861 1:STN:280:DC%2BD2sjktlWgsQ%3D%3D (Pubitemid 350235276)
109. K Kusuzaki N Kageyama H Shinjo H Takeshita H Murata S Hashiguchi T Ashihara Y Hirasawa 2000 Development of bone canaliculi during bone repair Bone 27 655 659 11062352 1:STN:280:DC%2BD3M%2FktlOquw%3D%3D
110. Schenk RK, Olah AJ, Herrmann W (1984) Preparation of calcified tissues for light microscopy. In: Dickson GR (ed) Methods of calcified tissue preparation. Elsevier, Amsterdam, pp 1-56
111. L Qin L Hung K Leung X Guo S Bumrerraj L Katz 2001 Staining intensity of individual osteons correlated with elastic properties and degrees of mineralization J Bone Miner Metab 19 359 364 11685651 1:STN:280: DC%2BD3MngvFGnug%3D%3D (Pubitemid 33041729)
112. AI Prentice 1967 Autofluorescence of bone tissues J Clin Pathol 20 717 719 5602982 1:STN:280:DyaF1M%2FjvVGqsw%3D%3D
113. F Pascaretti-Grizon G Mabilleau MF Baslé D Chappard 2011 Measurement by vertical scanning profilometry of resorption volume and lacunae depth caused by osteoclasts on dentine slices J Microscopy 241 147 152 10.1111/j.1365-2818.2010.03410.x 1:CAS:528:DC%2BC3MXisV2qsbk%3D
114. Chappard D, Pascaretti-Grizon F, Fontaine S, Mallet R, Filmon R, Baslé M, Mercier P (2009) Hydration of bone collagen is inversely related to mineral density as shown by vertical scanning microscopic interferometry. ASBMR Abstract A09002775
115. ML Bouxsein 2003 Bone quality: where do we go from here? Osteoporos Int 14 Suppl 5 S118 127 14504716