Osteoporosis International

, Volume 22, Issue 8, pp 2225–2240 | Cite as

New laboratory tools in the assessment of bone quality

Review
First Online:
Received:
Accepted:

Abstract

Bone quality is a complex set of intricated and interdependent factors that influence bone strength. A number of methods have emerged to measure bone quality, taking into account the organic or the mineral phase of the bone matrix, in the laboratory. Bone quality is a complex set of different factors that are interdependent. The bone matrix organization can be described at five different levels of anatomical organization: nature (organic and mineral), texture (woven or lamellar), structure (osteons in the cortices and arch-like packets in trabecular bone), microarchitecture, and macroarchitecture. Any change in one of these levels can alter bone quality. An altered bone remodeling can affect bone quality by influencing one or more of these factors. We have reviewed here the main methods that can be used in the laboratory to explore bone quality on bone samples. Bone remodeling can be evaluated by histomorphometry; microarchitecture is explored in 2D on histological sections and in 3D by microCT or synchrotron. Microradiography and scanning electron microscopy in the backscattered electron mode can measure the mineral distribution; Raman and Fourier-transformed infra-red spectroscopy and imaging can simultaneously explore the organic and mineral phase of the matrix on multispectral images; scanning acoustic microscopy and nanoindentation provide biomechanical information on individual trabeculae. Finally, some histological methods (polarization, surface staining, fluorescence, osteocyte staining) may also be of interest in the understanding of quality as a component of bone fragility. A growing number of laboratory techniques are now available. Some of them have been described many years ago and can find a new youth; others having benefited from improvements in physical and computer techniques are now available.

Keywords

Bone microarchitecture Bone mineralization Bone quality FTIRI MicroCT Raman spectroscopy 
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Notes

Acknowledgments

This work was made possible by grants from INSERM and Contrat Région Pays de la Loire (Bioregos2 program). The authors thank Mrs. Florence Pascaretti, Christine Gaudin, Nadine Gaborit, Guénaelle Brossard, and Robert Filmon for skillful assistance with the histological techniques and scanning electron microscopy. SEM analysis was done at SCIAM (Service Commun d'Imagerie et Analyses Microscopiques), Université d'Angers.

Conflicts of interest

None.

References

  1. 1.
    Kanis JA, Johnell O, Oden A, Johansson H, McCloskey E (2008) FRAX and the assessment of fracture probability in men and women from the UK. Osteoporos Int 19:385–397PubMedCrossRefGoogle Scholar
  2. 2.
    Miller PD, Siris ES, Barrett-Connor E, Faulkner KG, Wehren LE, Abbott TA, Chen YT, Berger ML, Santora AC, Sherwood LM (2002) Prediction of fracture risk in postmenopausal white women with peripheral bone densitometry: evidence from the National Osteoporosis Risk Assessment. J Bone Miner Res 17:2222–2230PubMedCrossRefGoogle Scholar
  3. 3.
    Cummings SR, Bates D, Black DM (2002) Clinical use of bone densitometry: scientific review. JAMA 288:1889–1897PubMedCrossRefGoogle Scholar
  4. 4.
    Marshall D, Johnell O, Wedel H (1996) Meta-analysis of how well measures of bone mineral density predict occurrence of osteoporotic fractures. BMJ 312:1254–1259PubMedGoogle Scholar
  5. 5.
    Sandor T, Felsenberg D, Brown E (1999) Comments on the hypotheses underlying fracture risk assessment in osteoporosis as proposed by the World Health Organization. Calcif Tissue Int 64:267–270PubMedCrossRefGoogle Scholar
  6. 6.
    Schuit SC, van der Klift M, Weel AE, de Laet CE, Burger H, Seeman E, Hofman A, Uitterlinden AG, van Leeuwen JP, Pols HA (2004) Fracture incidence and association with bone mineral density in elderly men and women: the Rotterdam Study. Bone 34:195–202PubMedCrossRefGoogle Scholar
  7. 7.
    Bouvard B, Legrand E, Audran M, Chappard D (2010) Glucocorticoid-induced osteoporosis: a review. Clin Rev Bone Miner Metab 8:15–26CrossRefGoogle Scholar
  8. 8.
    Dahl N, Holmgren G, Holmberg S, Ersmark H (1992) Fracture patterns in malignant osteopetrosis (Albers-Schonberg disease). Arch Orthop Trauma Surg 111:121–123PubMedCrossRefGoogle Scholar
  9. 9.
    Silverman SL (2008) Paget disease of bone: therapeutic options. J Clin Rheumatol 14:299–305PubMedCrossRefGoogle Scholar
  10. 10.
    Curtis JR, Westfall AO, Cheng H, Saag KG, Delzell E (2009) RisedronatE and ALendronate Intervention over Three Years (REALITY): minimal differences in fracture risk reduction. Osteoporos Int 20:973–978PubMedCrossRefGoogle Scholar
  11. 11.
    Delmas PD, Li Z, Cooper C (2004) Relationship between changes in bone mineral density and fracture risk reduction with antiresorptive drugs: some issues with meta-analyses. J Bone Miner Res 19:330–337PubMedCrossRefGoogle Scholar
  12. 12.
    Quandt SA, Thompson DE, Schneider DL, Nevitt MC, Black DM (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 80:343–349PubMedCrossRefGoogle Scholar
  13. 13.
    Meunier PJ, Chavassieux P (1985) L'histomorphométrie moyen d'évaluation de la masse osseuse. Rev Rhum Malad Osteo Art 52:669–673Google Scholar
  14. 14.
    Parfitt AM, Matthews CHE, Villanueva AR, Kleerekoper M, Frame B, Rao DS (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 72:1396–1409PubMedCrossRefGoogle Scholar
  15. 15.
    Chappard D, Alexandre C, Riffat G (1988) Spatial distribution of trabeculae in iliac bone from 145 osteoporotic females. Acta Anat 132:137–142PubMedCrossRefGoogle Scholar
  16. 16.
    Fyhrie DP (2005) Summary—measuring “bone quality”. J Muscul Skel Neur Interact 5:318–320Google Scholar
  17. 17.
    Felsenberg D, Boonen S (2005) The bone quality framework: determinants of bone strength and their interrelationships, and implications for osteoporosis management. Clin Ther 27:1–11PubMedCrossRefGoogle Scholar
  18. 18.
    Wei J, Ducy P (2010) Co-dependence of bone and energy metabolisms. Arch Biochem Biophys 503:35–40PubMedCrossRefGoogle Scholar
  19. 19.
    Barth HD, Launey ME, MacDowell AA, Ager JW III, Ritchie RO (2010) On the effect of X-ray irradiation on the deformation and fracture behavior of human cortical bone. Bone 46:1475–1485PubMedCrossRefGoogle Scholar
  20. 20.
    Launey ME, Buehler MJ, Ritchie RO (2010) On the mechanistic origins of toughness in bone. Ann Rev Mater Res 40:1CrossRefGoogle Scholar
  21. 21.
    Chappard D, Baslé MF, Legrand E, Audran M (2008) Trabecular bone microarchitecture: a review. Morphologie 92:162–170PubMedCrossRefGoogle Scholar
  22. 22.
    Chapurlat R, Chappard D (2009) L'ostéoporose, mieux la comprendre pour mieux la traiter. Wolters Kluwer, Lippincott Williams & Wilkins, Rueil-MalmaisonGoogle Scholar
  23. 23.
    Roughley PJ, Rauch F, Glorieux FH (2003) Osteogenesis imperfecta—clinical and molecular diversity. Eur Cell Mater 5:41–77PubMedGoogle Scholar
  24. 24.
    Zioupos P (2001) Ageing human bone: factors affecting its biomechanical properties and the role of collagen. J Biomater Appl 15:187–229PubMedCrossRefGoogle Scholar
  25. 25.
    Blank RD, Baldini TH, Kaufman M, Bailey S, Gupta R, Yershov Y, Boskey AL, Coppersmith SN, Demant P, Paschalis EP (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 44:134–142PubMedGoogle Scholar
  26. 26.
    Banse X, Devogelaer JP, Lafosse A, Sims TJ, Grynpas M, Bailey AJ (2002) Cross-link profile of bone collagen correlates with structural organization of trabeculae. Bone 31:70–76PubMedCrossRefGoogle Scholar
  27. 27.
    Saito M, Marumo K (2010) Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int 21:195–214PubMedCrossRefGoogle Scholar
  28. 28.
    Oxlund H, Mosekilde L, Ortoft G (1996) Reduced concentration of collagen reducible cross links in human trabecular bone with respect to age and osteoporosis. Bone 19:479–484PubMedCrossRefGoogle Scholar
  29. 29.
    Blouin S, Thaler HW, Korninger C, Schmid R, Hofstaetter JG, Zoehrer R, Phipps R, Klaushofer K, Roschger P, Paschalis EP (2009) Bone matrix quality and plasma homocysteine levels. Bone 44:959–964PubMedCrossRefGoogle Scholar
  30. 30.
    Libouban H, Filmon R, Maureac A, Baslé MF, Chappard D (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 40:1234–1239CrossRefGoogle Scholar
  31. 31.
    Holden JL, Clement JG, Phakey PP (1995) Age and temperature related changes to the ultrastructure and composition of human bone mineral. J Bone Miner Res 10:1400–1409PubMedCrossRefGoogle Scholar
  32. 32.
    Iyo T, Maki Y, Sasaki N, Nakata M (2004) Anisotropic viscoelastic properties of cortical bone. J Biomech 37:1433–1437PubMedCrossRefGoogle Scholar
  33. 33.
    Boivin G, Meunier PJ (2003) The mineralization of bone tissue: a forgotten dimension in osteoporosis research. Osteoporos Int 14(Suppl 3):S19–24PubMedGoogle Scholar
  34. 34.
    Gupta HS, Seto J, Wagermaier W, Zaslansky P, Boesecke P, Fratzl P (2006) Cooperative deformation of mineral and collagen in bone at the nanoscale. Proc Natl Acad Sci USA 103:17741–17746PubMedCrossRefGoogle Scholar
  35. 35.
    Gorski JP (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 9:201–223PubMedCrossRefGoogle Scholar
  36. 36.
    Mulder L, Koolstra JH, den Toonder JM, van Eijden TM (2008) Relationship between tissue stiffness and degree of mineralization of developing trabecular bone. J Biomed Mater Res A 84:508–515PubMedGoogle Scholar
  37. 37.
    Seeman E (2003) Periosteal bone formation—a neglected determinant of bone strength. N Engl J Med 349:320–323PubMedCrossRefGoogle Scholar
  38. 38.
    Singh I (1978) The architecture of cancellous bone. J Anat 127:305–310PubMedGoogle Scholar
  39. 39.
    Bertram JE, Biewener AA (1988) Bone curvature: sacrificing strength for load predictability? J Theor Biol 131:75–92PubMedCrossRefGoogle Scholar
  40. 40.
    Lanyon LE, Bourn S (1979) The influence of mechanical function on the development and remodeling of the tibia. An experimental study in sheep. J Bone Joint Surg Am 61:263–273PubMedGoogle Scholar
  41. 41.
    Boonen S, Koutri R, Dequeker J, Aerssens J, Lowet G, Nijs J, Verbeke G, Lesaffre E, Geusens P (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 10:1908–1912PubMedCrossRefGoogle Scholar
  42. 42.
    Faulkner KG, Cummings SR, Black D, Palermo L, Gluer CC, Genant HK (1993) Simple measurement of femoral geometry predicts hip fracture: the study of osteoporotic fractures. J Bone Miner Res 8:1211–1217PubMedCrossRefGoogle Scholar
  43. 43.
    Duan Y, Parfitt A, Seeman E (1999) Vertebral bone mass, size, and volumetric density in women with spinal fractures. J Bone Miner Res 14:1796–1802PubMedCrossRefGoogle Scholar
  44. 44.
    Gilsanz V, Gibbens DT, Roe TF, Carlson M, Senac MO, Boechat MI, Huang HK, Schulz EE, Libanati CR, Cann CC (1988) Vertebral bone density in children: effect of puberty. Radiology 166:847–850PubMedGoogle Scholar
  45. 45.
    Bergot C, Bousson V, Meunier A, Laval-Jeantet M, Laredo JD (2002) Hip fracture risk and proximal femur geometry from DXA scans. Osteoporos Int 13:542–550PubMedCrossRefGoogle Scholar
  46. 46.
    Karlamangla AS, Barrett-Connor E, Young J, Greendale GA (2004) Hip fracture risk assessment using composite indices of femoral neck strength: the Rancho Bernardo study. Osteoporos Int 15:62–70PubMedCrossRefGoogle Scholar
  47. 47.
    Seeman E (2008) Bone quality: the material and structural basis of bone strength. J Bone Miner Metab 26:1–8PubMedCrossRefGoogle Scholar
  48. 48.
    Seeman E, Delmas PD (2006) Bone quality—the material and structural basis of bone strength and fragility. N Engl J Med 354:2250–2261PubMedCrossRefGoogle Scholar
  49. 49.
    Genant HK, Jiang JY (2006) Imaging assessment of bone quality in osteoporosis. Clin Rev Bone Miner Metab 4:213–224CrossRefGoogle Scholar
  50. 50.
    Benhamou CL, Lespessailles E, Jacquet G, Harba R, Jennane R, Loussot T, Tourliere D, Ohley W (1994) Fractal organization of trabecular bone images on calcaneus radiographs. J Bone Miner Res 9:1909–1918PubMedCrossRefGoogle Scholar
  51. 51.
    Guggenbuhl P, Bodic F, Hamel L, Baslé MF, Chappard D (2006) Texture analysis of X-ray radiographs of iliac bone is correlated with bone micro-CT. Osteoporos Int 17:447–454PubMedCrossRefGoogle Scholar
  52. 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 445–476Google Scholar
  53. 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 203–210Google Scholar
  54. 54.
    Fazzalari NL, Parkinson IH (1996) Fractal dimension and architecture of trabecular bone. J Pathol 178:100–105PubMedCrossRefGoogle Scholar
  55. 55.
    Tabor Z (2004) Analysis of the influence of image resolution on the discriminating power of trabecular bone architectural parameters. Bone 34:170–179PubMedCrossRefGoogle Scholar
  56. 56.
    Chappard D, Legrand E, Haettich B, Chales G, Auvinet B, Eschard JP, Hamelin JP, Baslé MF, Audran M (2001) Fractal dimension of trabecular bone: comparison of three histomorphometric computed techniques for measuring the architectural two-dimensional complexity. J Pathol 195:515–521PubMedCrossRefGoogle Scholar
  57. 57.
    Chappard D, Legrand E, Pascaretti C, Baslé MF, Audran M (1999) Comparison of eight histomorphometric methods for measuring trabecular bone architecture by image analysis on histological sections. Microsc Res Tech 45:303–312PubMedCrossRefGoogle Scholar
  58. 58.
    Ruegsegger P (1994) The use of peripheral QCT in the evaluation of bone remodelling. Endocrinol 4:167–176CrossRefGoogle Scholar
  59. 59.
    Sasov A, Van Dyck D (1998) Desktop X-ray microscopy and microtomography. J Microsc 191:151–158CrossRefGoogle Scholar
  60. 60.
    Rizzoli R, Laroche M, Krieg MA, Frieling I, Thomas T, Delmas P, Felsenberg D (2010) Strontium ranelate and alendronate have differing effects on distal tibia bone microstructure in women with osteoporosis. Rheumatol Int 30:1341–1348PubMedCrossRefGoogle Scholar
  61. 61.
    Peyrin F, Muller C, Carillon Y, Nuzzo S, Bonnassie A, Briguet A (2001) Synchrotron radiation microCT: a reference tool for the characterization of bone samples. Adv Exp Med Biol 496:129–142PubMedGoogle Scholar
  62. 62.
    Chappard D, Josselin N, Rouge-Maillart C, Legrand E, Baslé MF, Audran M (2007) Bone microarchitecture in males with corticosteroid-induced osteoporosis. Osteoporos Int 18:487–494PubMedCrossRefGoogle Scholar
  63. 63.
    Hordon LD, Itoda M, Shore PA, Shore RC, Heald M, Brown M, Kanis JA, Rodan GA, Aaron JE (2006) Preservation of thoracic spine microarchitecture by alendronate: comparison of histology and microCT. Bone 38:444–449PubMedCrossRefGoogle Scholar
  64. 64.
    Alexander JM, Bab I, Fish S, Müller R, Uchiyama T, Gronowicz G, Nahounou M, Zhao Q, White DW, Chorev M, Gazit D, Rosenblatt M (2001) Human parathyroid hormone 1–34 reverses bone loss in ovariectomized mice. J Bone Miner Res 16:1665–1673PubMedCrossRefGoogle Scholar
  65. 65.
    Chappard D, Retailleau-Gaborit N, Legrand E, Baslé MF, Audran M (2005) Comparison insight bone measurements by histomorphometry and microCT. J Bone Miner Res 20:1177–1184PubMedCrossRefGoogle Scholar
  66. 66.
    Amprino R (1952) Rapporti fra processi di ricostruzione e distribuzione dei minerali nelle ossa. I. Ricerche esguite col metodo dis tudio dei raggi Roentgen. Z Zellforsch 37:144–183PubMedCrossRefGoogle Scholar
  67. 67.
    Jowsey J, Kelly PJ, Riggs BL, Bianco AJ, Scholz DA, Gershon-Cohen J (1965) Quantitative microradiographic studies of normal and osteoporotic bone. J Bone Joint Surg Am 47:785–872PubMedGoogle Scholar
  68. 68.
    Dhem A, Nyssen-Behets C, Coppens J (1998) Post-menopausal osteoporosis: microradiographic aspects. It J Anat Embryol 103:343–352Google Scholar
  69. 69.
    Boivin G, Meunier PJ (2002) The degree of mineralization of bone tissue measured by computerized quantitative contact microradiography. Calcif Tissue Int 70:503–511PubMedCrossRefGoogle Scholar
  70. 70.
    Boivin G, Bala Y, Doublier A, Farlay D, Ste-Marie LG, Meunier PJ, Delmas PD (2008) The role of mineralization and organic matrix in the microhardness of bone tissue from controls and osteoporotic patients. Bone 43:532–538PubMedCrossRefGoogle Scholar
  71. 71.
    Boivin GY, Chavassieux PM, Santora AC, Yates J, Meunier PJ (2000) Alendronate increases bone strength by increasing the mean degree of mineralization of bone tissue in osteoporotic women. Bone 27:687–694PubMedCrossRefGoogle Scholar
  72. 72.
    Whitehouse WJ, Dyson ED, Jackson CK (1971) The scanning electron microscope in studies of trabecular bone from a human vertebral body. J Anat 108:481–496PubMedGoogle Scholar
  73. 73.
    Boyde A, Jones SJ (1983) Back-scattered electron imaging of skeletal tissues. Metab Bone Dis Relat Res 5:145–150PubMedCrossRefGoogle Scholar
  74. 74.
    Roschger P, Fratzl P, Eschberger J, Klaushofer K (1998) Validation of quantitative backscattered electron imaging for the measurement of mineral density distribution in human bone biopsies. Bone 23:319–326PubMedCrossRefGoogle Scholar
  75. 75.
    Corsi A, Collins MT, Riminucci M, Howell PGT, Boyde A, Gehron Robey P, Bianco P (2003) Osteomalacic and hyperparathyroid changes in fibrous dysplasia of bone: core biopsy studies and clinical correlations. J Bone Miner Res 18:1235–1246PubMedCrossRefGoogle Scholar
  76. 76.
    Roschger P, Paschalis EP, Fratzl P, Klaushofer K (2008) Bone mineralization density distribution in health and disease. Bone 42:456–466PubMedCrossRefGoogle Scholar
  77. 77.
    Smith LJ, Schirer JP, Fazzalari NL (2010) The role of mineral content in determining the micromechanical properties of discrete trabecular bone remodeling packets. J Biomech 43:3144–3149PubMedCrossRefGoogle Scholar
  78. 78.
    Boskey AL, Camacho NP, Mendelsohn R, Doty SB, Binderman I (1992) FT-IR microscopic mappings of early mineralization in chick limb bud mesenchymal cell cultures. Calcif Tissue Int 51:443–448PubMedCrossRefGoogle Scholar
  79. 79.
    Akkus O, Adar F, Schaffler MB (2004) Age-related changes in physicochemical properties of mineral crystals are related to impaired mechanical function of cortical bone. Bone 34:443–453PubMedCrossRefGoogle Scholar
  80. 80.
    Paschalis EP, DiCarlo E, Betts F, Sherman P, Mendelsohn R, Boskey AL (1996) FTIR microspectroscopic analysis of human osteonal bone. Calcif Tissue Int 59:480–487PubMedGoogle Scholar
  81. 81.
    Penel G, Leroy G, Rey C, Bres E (1998) MicroRaman spectral study of the PO4 and CO3 vibrational modes in synthetic and biological apatites. Calcif Tissue Int 63:475–481PubMedCrossRefGoogle Scholar
  82. 82.
    Boskey A (2003) Bone mineral crystal size. Osteoporos Int 14:S16–S20CrossRefGoogle Scholar
  83. 83.
    Paschalis EP, Verdelis K, Doty SB, Boskey AL, Mendelsohn R, Yamauchi M (2001) Spectroscopic characterization of collagen cross-links in bone. J Bone Miner Res 16:1821–1828PubMedCrossRefGoogle Scholar
  84. 84.
    Katz JL, Meunier A (1993) Scanning acoustic microscope studies of the elastic properties of osteons and osteon lamellae. J Biomech Eng 115:543–548PubMedCrossRefGoogle Scholar
  85. 85.
    Regauer M, Jurgens P, Budenhofer U, Hartstock M, Bocker W, Burklein D, Mutschler W, Sader R, Schieker M (2006) Quantitative scanning acoustic microscopy compared to microradiography for assessment of new bone formation. Bone 38:564–570PubMedCrossRefGoogle Scholar
  86. 86.
    Bumrerraj S, Katz JL (2001) Scanning acoustic microscopy study of human cortical and trabecular bone. Ann Biomed Eng 29:1034–1042PubMedCrossRefGoogle Scholar
  87. 87.
    Olesiak SE, Oyen ML, Ferguson VL (2010) Viscous–elastic–plastic behavior of bone using Berkovich nanoindentation. Mechan Time Dep Mater 14:111–124CrossRefGoogle Scholar
  88. 88.
    Roy ME, Rho JY, Tsui TY, Evans ND, Pharr GM (1999) Mechanical and morphological variation of the human lumbar vertebral cortical and trabecular bone. J Biomed Mater Res 44:191–197PubMedCrossRefGoogle Scholar
  89. 89.
    Rho JY, Roy ME 2nd, Tsui TY, Pharr GM (1999) Elastic properties of microstructural components of human bone tissue as measured by nanoindentation. J Biomed Mater Res 45:48–54PubMedCrossRefGoogle Scholar
  90. 90.
    Rho JY, Zioupos P, Currey JD, Pharr GM (1999) Variations in the individual thick lamellar properties within osteons by nanoindentation. Bone 25:295–300PubMedCrossRefGoogle Scholar
  91. 91.
    Fan Z, Swadener JG, Rho JY, Roy ME, Pharr GM (2002) Anisotropic properties of human tibial cortical bone as measured by nanoindentation. J Orthop Res 20:806–810PubMedCrossRefGoogle Scholar
  92. 92.
    Ammann P, Badoud I, Barraud S, Dayer R, Rizzoli R (2007) Strontium ranelate treatment improves trabecular and cortical intrinsic bone tissue quality, a determinant of bone strength. J Bone Miner Res 22:1419–1425PubMedCrossRefGoogle Scholar
  93. 93.
    Fratzl-Zelman N, Roschger P, Gourrier A, Weber M, Misof BM, Loveridge N, Reeve J, Klaushofer K, Fratzl P (2009) Combination of nanoindentation and quantitative backscattered electron imaging revealed altered bone material properties associated with femoral neck fragility. Calcif Tissue Int 85:335–343PubMedCrossRefGoogle Scholar
  94. 94.
    Silva MJ, Brodt MD, Fan Z, Rho JY (2004) Nanoindentation and whole-bone bending estimates of material properties in bones from the senescence accelerated mouse SAMP6. J Biomech 37:1639–1646PubMedCrossRefGoogle Scholar
  95. 95.
    Zhao H, Jin H, Cai J, Ding S (2010) The process of collagen biomineralization observed by AFM in a model dual membrane diffusion system. Ultramicroscopy 110:1306–1311PubMedCrossRefGoogle Scholar
  96. 96.
    Hassenkam T, Fantner GE, Cutroni JA, Weaver JC, Morse DE, Hansma PK (2004) High-resolution AFM imaging of intact and fractured trabecular bone. Bone 35:4–10PubMedCrossRefGoogle Scholar
  97. 97.
    Dumas A, Gaudin-Audrain C, Mabilleau G, Massin P, Hubert L, Baslé MF, Chappard D (2006) The influence of processes for the purification of human bone allografts on the matrix surface and cytocompatibility. Biomaterials 27:4204–4211PubMedCrossRefGoogle Scholar
  98. 98.
    Chevalier Y, Quek E, Borah B, Gross G, Stewart J, Lang T, Zysset P (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 46:41–48PubMedCrossRefGoogle Scholar
  99. 99.
    Kim CH, Takai E, Zhou H, von Stechow D, Muller R, Dempster DW, Guo XE (2003) Trabecular bone response to mechanical and parathyroid hormone stimulation: the role of mechanical microenvironment. J Bone Miner Res 18:2116–2125PubMedCrossRefGoogle Scholar
  100. 100.
    Homminga J, McCreadie BR, Ciarelli TE, Weinans H, Goldstein SA, Huiskes R (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 30:759–764PubMedCrossRefGoogle Scholar
  101. 101.
    Saha PK, Xu Y, Duan H, Heiner A, Liang G (2010) Volumetric topological analysis: a novel approach for trabecular bone classification on the continuum between plates and rods. IEEE Trans Med Imaging 29:1821–1838PubMedCrossRefGoogle Scholar
  102. 102.
    Boyle C, Kim IY (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. doi: 10.1016/j.jbiomech.2010.1011.1029 Google Scholar
  103. 103.
    Liu XS, Cohen A, Shane E, Stein E, Rogers H, Kokolus SL, Yin PT, McMahon DJ, Lappe JM, Recker RR, Guo XE (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 25:1496–1505PubMedCrossRefGoogle Scholar
  104. 104.
    Cristofolini L, Schileo E, Juszczyk M, Taddei F, Martelli S, Viceconti M (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 368:2725–2763CrossRefGoogle Scholar
  105. 105.
    Weinstein RS, Nicholas RW, Manolagas SC (2000) Apoptosis of osteocytes in glucocorticoid-induced osteonecrosis of the hip. J Clin Endocrinol Metab 85:2907–2912PubMedCrossRefGoogle Scholar
  106. 106.
    Mori S, Harruff R, Ambrosius W, Burr DB (1997) Trabecular bone volume and microdamage accumulation in the femoral heads of women with and without femoral neck fractures. Bone 21:521–526PubMedCrossRefGoogle Scholar
  107. 107.
    Gaudin-Audrain C, Gallois Y, Pascaretti-Grizon F, Hubert L, Massin P, Baslé MF, Chappard D (2008) Osteopontin is histochemically detected by the AgNOR acid-silver staining. Histol Histopathol 23:469–478PubMedGoogle Scholar
  108. 108.
    Pascaretti-Grizon F, Gaudin-Audrain C, Gallois Y, Retaillaud-Gaborit N, Baslé MF, Chappard D (2007) Osteopontin is an argentophilic protein in the bone matrix and in cells of kidney convoluted tubules. Morphologie 91:180–185PubMedGoogle Scholar
  109. 109.
    Kusuzaki K, Kageyama N, Shinjo H, Takeshita H, Murata H, Hashiguchi S, Ashihara T, Hirasawa Y (2000) Development of bone canaliculi during bone repair. Bone 27:655–659PubMedCrossRefGoogle Scholar
  110. 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 1–56Google Scholar
  111. 111.
    Qin L, Hung L, Leung K, Guo X, Bumrerraj S, Katz L (2001) Staining intensity of individual osteons correlated with elastic properties and degrees of mineralization. J Bone Miner Metab 19:359–364PubMedCrossRefGoogle Scholar
  112. 112.
    Prentice AI (1967) Autofluorescence of bone tissues. J Clin Pathol 20:717–719PubMedCrossRefGoogle Scholar
  113. 113.
    Pascaretti-Grizon F, Mabilleau G, Baslé MF, Chappard D (2011) Measurement by vertical scanning profilometry of resorption volume and lacunae depth caused by osteoclasts on dentine slices. J Microscopy 241:147–152CrossRefGoogle Scholar
  114. 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 A09002775Google Scholar
  115. 115.
    Bouxsein ML (2003) Bone quality: where do we go from here? Osteoporos Int 14(Suppl 5):S118–127PubMedCrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2011

Authors and Affiliations

  • D. Chappard
    • 1
  • M.F. Baslé
    • 1
  • E. Legrand
    • 1
    • 2
  • M. Audran
    • 1
    • 2
  1. 1.INSERM, U922—IRIS-IBS Institut de Biologie en SantéCHU d′AngersAngersFrance
  2. 2.Rheumatology UnitCHU d′AngersAngersFrance

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