Abstract
Atraumatic fractures of the skeleton in osteoporotic patients are directly related to a deterioration of bone strength. However, the failure of the bone tissue to withstand functional load bearing cannot be explained as a simple decrease in bone mineral density (quantity); strength is also significantly dependent upon bone quality. While a formal definition of bone quality is somewhat elusive, at the very least, it incorporates architectural, physical, and biologic factors that are critical to bone strength. Such factors include bone morphology (ie, trabecular connectivity, cross-sectional geometry, longitudinal curvature); the tissue’s material properties (eg, stiffness, strength); its chemical composition and architecture (eg, ratio of calcium to other components of the organic and/or inorganic phase, collagen orientation, porosity, permeability); and the viability of the tissue (eg, responsivity of the bone cell population). Combining high-resolution structural indices of bone, as determined by micro-computed tomography; material properties determined by nanoindentation; and the chemical make-up of bone, as determined by infrared spectroscopy, helps to provide critical information toward a more comprehensive assessment of the interdependence of bone quality, quantity, and fracture risk.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References and Recommended Reading
Kleerekoper M: The role of fluoride in the prevention of osteoporosis. Endocrinol Metab Clin North Am 1998, 27:441–452.
Riggs BL, Hodgson SF, O’Fallon WM, et al.: Effect of fluoride treatment on the fracture rate in postmenopausal women with osteoporosis. N Engl J Med 1990, 322:802–809.
Ensrud KE, Black DM, Palermo L, et al.: Treatment with alendronate prevents fractures in women at highest risk: results from the Fracture Intervention Trial. Arch Intern Med 1997, 157:2617–2624.
Mashiba T, Hirano T, Turner CH, et al.: Suppressed bone turnover by bisphosphonates increases microdamage accumulation and reduces some biomechanical properties in dog rib. J Bone Miner Res 2000, 15:613–620.
Kellie SE: Diagnostic and therapeutic technology assessment. Measurement of bone density with dual-energy X-ray absorptiometry (DEXA). JAMA 1992, 267:286–294.
Ciarelli MJ, Goldstein SA, Kuhn JL, et al.: Evaluation of orthogonal mechanical properties and density of human trabecular bone from the major metaphyseal regions with materials testing and computed tomography. J Orthop Res 1991, 9:674–682.
Lin W, Qin YX, Rubin C: Ultrasonic wave propagation in trabecular bone predicted by the stratified model. Ann Biomed Eng 2001, 29:781–790.
Judex S, Gross TS, Zernicke RF: Strain gradients correlate with sites of exercise-induced bone-forming surfaces in the adult skeleton. J Bone Miner Res 1997, 12:1737–1745.
Hildebrand T, Laib A, Muller R, et al.: Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res 1999, 14:1167–1174.
Muller R, Hildebrand T, Ruegsegger P: Non-invasive bone biopsy: a new method to analyse and display the threedimensional structure of trabecular bone. Phys Med Biol 1994, 39:145–164.
Ruegsegger P, Koller B, Muller R: A microtomographic system for the nondestructive evaluation of bone architecture. Calcif Tissue Int 1996, 58:24–29.
Muller R, Van Campenhout H, Van Damme B, et al.: Morphometric analysis of human bone biopsies: a quantitative structural comparison of histological sections and microcomputed tomography. Bone 1998, 23:59–66.
Muller R: The zurich experience: one decade of threedimensional high-resolution computed tomography. Top Magn Reson Imaging 2002, 13:307–322. This paper gives a state-of-the-art overview of micro-CT scanning.
Boyd SK, Muller R, Zernicke RF: Mechanical and architectural bone adaptation in early stage experimental osteoarthritis. J Bone Miner Res 2002, 17:687–694.
Rubin C, Turner AS, Muller R, et al.: Quantity and quality of trabecular bone in the femur are enhanced by a strongly anabolic, noninvasive mechanical intervention. J Bone Miner Res 2002, 17:349–357.
Hildebrand T, Ruegsegger P: Quantification of bone microarchitecture with the Structure Model Index. Comput Methods Biomech Biomed Engin 1997, 1:15–23.
Odgaard A, Gundersen HJ: Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone 1993, 14:173–182.
Hildebrand T, Laib A, Muller R, et al.: Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus. J Bone Miner Res 1999, 14:1167–1174.
Odgaard A: Three-dimensional methods for quantification of cancellous bone architecture. Bone 1997, 20:315–328.
Boyd SK, Matyas JR, Wohl GR, et al.: Early regional adaptation of periarticular bone mineral density after anterior cruciate ligament injury. J Appl Physiol 2000, 89:2359–2364.
Boyd SK, Muller R, Matyas JR, et al.: Early morphometric and anisotropic change in periarticular cancellous bone in a model of experimental knee osteoarthritis quantified using microcomputed tomography. Clin Biomech (Bristol, Avon) 2000, 15:624–631.
Gasser JA, Yam J: In vivo non-invasive monitoring of changes in structural cancellous bone parameters with a novel prototype microCT in rats. Paper presented at the 24th Annual Meeting of the American Society for Bone and Mineral Research. San Antonio, TX. September 2002.
Pistoia W, Van Rietbergen B, Laib A, et al.: High-resolution three-dimensional-pQCT images can be an adequate basis for in-vivo microFE analysis of bone. J Biomech Eng 2001, 123:176–183.
Keaveny TM, Hayes WC: A 20-year perspective on the mechanical properties of trabecular bone. J Biomech Eng 1993, 115:534–542.
Keaveny TM, Pinilla TP, Crawford RP, et al.: Systematic and random errors in compression testing of trabecular bone. J Orthop Res 1997, 15:101–110.
Balena R, Toolan BC, Shea M, et al.: The effects of 2-year treatment with the aminobisphosphonate alendronate on bone metabolism, bone histomorphometry, and bone strength in ovariectomized nonhuman primates. J Clin Invest 1993, 92:2577–2586.
Borchers RE, Gibson LJ, Burchardt H, et al.: Effects of selected thermal variables on the mechanical properties of trabecular bone. Biomaterials 1995, 16:545–551.
Ulrich D, Van Rietbergen B, Laib A, et al.: Load transfer analysis of the distal radius from in-vivo high-resolution CT-imaging. J Biomech 1999, 32:821–828.
Van Rietbergen B, Muller R, Ulrich D, et al.: Tissue stresses and strain in trabeculae of a canine proximal femur can be quantified from computer reconstructions. J Biomech 1999, 32:443–451.
Niebur GL, Yuen JC, Hsia AC, et al.: Convergence behavior of high-resolution finite element models of trabecular bone. J Biomech Eng 1999, 121:629–635.
Judex S, Boyd S, Qin YX, et al.: Adaptations of trabecular bone to low magnitude vibrations result in more uniform stress and strain under load. Ann Biomed Eng 2003, 31:12–20.
Kotha SP, Guzeslu N: Modeling the tensile mechanical behavior of bone along the longitudinal direction. J Theor Biol 2002, 219:269–279.
Gajko-Galicka A: Mutations in type I collagen genes resulting in osteogenesis imperfecta in humans. Acta Biochim Pol 2002, 49:433–441.
Currey JD: Mechanical properties of bone tissues with greatly differing functions. J Biomech 1979, 12:313–319.
Torzilli PA, Brustein AH, Takebe K, et al.: The mechanical and structural properties of maturing bone. In Mechanical Properties of Bone. New York: American Society of Mechanical Engineers; 1981:145–161.
Glimcher MJ: The nature of the mineral component of bone and the mechanisms of calcification. In Disorders of Bone and Mineral Metabolism. Edited by Coe FL, Favus MJ. New York: Raven Press; 1992:265–286.
Grynpas M: Age and disease-related changes in the mineral of bone. Calcif Tissue Int 1993, 53(Suppl):57–64.
Miller LM, Carlson CS, Carr GL, et al.: A method for examining the chemical basis for bone disease: synchrotron infrared microspectroscopy. Cell Mol Biol (Noisy -le-grand) 1998, 44:117–127.
Miller LM, Vairavamurthy V, Chance MR, et al.: In situ analysis of mineral content and crystallinity in bone using infrared micro-spectroscopy of the nu(4) PO(4)(3-) vibration. Biochim Biophys Acta 2001, 1527:11–19.
Huang RY, Miller LM, Carlson CS, et al.: Characterization of bone mineral composition in the proximal tibia of cynomolgus monkeys: effect of ovariectomy and nandrolone decanoate treatment. Bone 2002, 30:492–497. This paper demonstrates the efficacy of infrared spectroscopy to determine bone’s chemical properties.
Rho JY, Currey JD, Zioupos P, et al.: The anisotropic Young’s modulus of equine secondary osteones and interstitial bone determined by nanoindentation. J Exp Biol 2001, 204:1775–1781. The authors use nanoindentation to differentiate between mechanical properties of osteons and interstitial lamellae in cortices subjected to different habitual loading conditions.
Hengsberger S, Kulik A, Zysset P: Nanoindentation discriminates the elastic properties of individual human bone lamellae under dry and physiological conditions. Bone 2002, 30:178–184.
Roy ME, Rho JY, Tsui TY, et al.: Mechanical and morphological variation of the human lumbar vertebral cortical and trabecular bone. J Biomed Mater Res 1999, 44:191–197.
Rho JY, Tsui TY, Pharr GM: Elastic properties of human cortical and trabecular lamellar bone measured by nanoindentation. Biomaterials 1997, 18:1325–1330.
Zysset PK, Guo XE, Hoffler CE, et al.: Elastic modulus and hardness of cortical and trabecular bone lamellae measured by nanoindentation in the human femur. J Biomech 1999, 32:1005–1012.
Yeh OC, Keaveny TM: Biomechanical effects of intraspecimen variations in trabecular architecture: a three-dimensional finite element study. Bone 1999, 25:223–228.
Burr DB, Forwood MR, Fyhrie DP, et al.: Bone microdamage and skeletal fragility in osteoporotic and stress fractures. J Bone Miner Res 1997, 12:6–15.
Skedros JG, Mason MW, Nelson MC, et al.: Evidence of structural and material adaptation to specific strain features in cortical bone. Anat Rec 1996, 246:47–63.
Wang X, Li X, Bank RA, et al.: Effects of collagen unwinding and cleavage on the mechanical integrity of the collagen network in bone. Calcif Tissue Int 2002, 71:186–192.
Skerry TM, Suswillo R, el Haj AJ, et al.: Load-induced proteoglycan orientation in bone tissue in vivo and in vitro. Calcif Tissue Int 1990, 46:318–326.
Reszka AA, Rodan GA: Bisphosphonate mechanism of action. Curr Rheumatol Rep 2003, 5:65–74.
Judex S, Donahue LR, Rubin C: Genetic predisposition to low bone mass is paralleled by an enhanced sensitivity to signals anabolic to the skeleton. FASEB J 2002, 16:1280–1282.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Judex, S., Boyd, S., Qin, YX. et al. Combining high-resolution micro-computed tomography with material composition to define the quality of bone tissue. Curr Osteoporos Rep 1, 11–19 (2003). https://doi.org/10.1007/s11914-003-0003-x
Issue Date:
DOI: https://doi.org/10.1007/s11914-003-0003-x