Micro-computed tomography assessment of human femoral trabecular bone for two disease groups (fragility fracture and coxarthrosis): Age and gender related effects on the microstructure


The aim of this study was to identify three-dimensional microstructural changes of trabecular bone with age and gender, using micro-computed tomography. Human trabecular bone from two disease groups, osteoporosis and osteoarthritis was analyzed. A prior analysis of the effects of some procedure variables on the micro-CT results was performed. Preliminary micro-CT scans were performed with three voxel resolutions and two acquisition conditions. On the reconstruction step, the image segmentation was performed with three different threshold values. Samples were collected from patients, with coxarthrosis (osteoarthritis) or fragility fracture (osteoporosis). The specimens of the coxarthrosis group include twenty females and fifteen males, while the fragility fracture group was composed by twenty three females and seven males. The mean age of the population was 69 ± 11 (females) and 67 ± 10 years (males), in the coxarthrosis group, while in the fragility fracture group was 81 ± 6 (females) and 78 ± 6 (males) years. The 30 μm voxel size provided lower percentage difference for the microarchitecture parameters. Acquisition conditions with 160 μA and 60 kV permit the evaluation of all the volume’s sample, with low average values of the coefficients of variation of the microstructural parameters. No statistically significant differences were found between the two diseases groups, neither between genders. However, with aging, there is a decrease of bone volume fraction, trabecular number and fractal dimension, and an increase of structural model index and trabecular separation, for both disease groups and genders. The parameters bone specific surface, trabecular thickness and degree of anisotropy have different behaviors with age, depending on the type of disease. While in coxarthrosis patients, trabecular thickness increases with age, in the fragility fracture group, there is a decrease of trabecular thickness with increasing age. Our findings indicate that disease, age and gender do not provide significant differences in trabecular microstructure. With aging, some parameters exhibit different trends which are possibly related to different mechanisms for different diseases.

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Vale, A. , Pereira, M. , Maurício, A. , Vidal, B. , Rodrigues, A. , Caetano-Lopes, J. , Nazarian, A. , Fonseca, J. , Canhão, H. and Vaz, M. (2013) Micro-computed tomography assessment of human femoral trabecular bone for two disease groups (fragility fracture and coxarthrosis): Age and gender related effects on the microstructure. Journal of Biomedical Science and Engineering, 6, 175-184. doi: 10.4236/jbise.2013.62021.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] Feldkamp, L.A., Goldstein, S.A., Parfitt, A.M., et al. (1989) The direct examination of three-dimensional bone archi tecture in vitro by computed tomography. Journal of Bone and Mineral Research, 4, 3-11. doi:10.1002/jbmr.5650040103
[2] Kim, D.G., Christopherson, G.T., Dong, X.N., et al. (2004) The effect of microcomputed tomography scanning and reconstruction voxel size on the accuracy of stereological measurements in human cancellous bone. Bone, 34, 1375 1382. doi:10.1016/j.bone.2004.09.007
[3] Bouxsein, M.L., Boyd, S.K., Christiansen, B.A., et al. (2010) Guidelines for assessment of bone microstructure in Rodents using micro-computed tomography. Journal of Bone and Mineral Research, 25, 1468-1486. doi:10.1002/jbmr.141
[4] Griffith, J.F. and Genant, H.K. (2008) Bone mass and architecture determination: State of the art. Best Practice & Research Clinical Endocrinology & Metabolism, 22, 737-764. doi:10.1016/j.beem.2008.07.003
[5] Chappard, D., Baslé, M.-L., Legrand, E. and Audran, M. (2008) Trabecular bone microarchitecture: A review. Morphologie, 92, 162-170. doi:10.1016/j.morpho.2008.10.003
[6] Benhamou, C.-L. and Roux, C. (2007) First meeting on bone quality, abbaye des Vaux de Cernay, France, 15-16 June 2006: Bone architecture. Osteoporosis International, 18, 837-889. doi:10.1007/s00198-007-0366-4
[7] Lespessailles, E., Chappard, C., Bonnet, N. and Benhamou, C.L. (2006) Imaging techniques for evaluating bone microarchitecture. Joint Bone Spine, 73, 254-261. doi:10.1016/j.jbspin.2005.12.002
[8] Adams, J.E. (2009) Quantitative computed tomography. European Journal of Radiology, 71, 415-424. doi:10.1016/j.ejrad.2009.04.074
[9] Steines, D., Liew, S.W., Arnaud, C., Vargas-Voracek, R., Nazarian, A., Müller, R., Snyder, B., Hess, P. and Lang, P. (2009) Radiographic trabecular 2D and 3D parameters of proximal femoral bone cores correlate with each other and with yield stress. Osteoporos International, 20, 1929-1938. doi:10.1007/s00198-009-0908-z
[10] Ding, M. and Hvid, I. (2000) Quantification of age-related changes in the structure model type and trabecular thickness of human tibial cancellous bone. Bone, 26, 291-295. doi:10.1016/S8756-3282(99)00281-1
[11] Rüegsegger, P., Koller, B. and Müller, R. (1996) A mi crotomographic system for the nondestructive evaluation of bone architecture. Calcified Tissue International, 58, 24-29. doi:10.1007/BF02509542
[12] Ciarelli, M.J., Goldstein, S.A., Kuhn, J.L., Cody, D.D. and Brown, M.B. (1991) Evaluation of orthogonal mechanical properties and density of human trabecular bone from the major metaphyseal regions with materials testing and computed tomography. Journal of Orthopaedic Research, 9, 674-682. doi:10.1002/jor.1100090507
[13] Müller, R. and Rüegsegger, P. (1997) Micro-tomographic imaging for the nondestructive evaluation of trabecular bone architecture. Studies in Health Technology and Informatics, 40, 61-79.
[14] Arlot, M., Burt-Pichat, B., Roux, J., et al. (2008) Micro architecture influences microdamage accumulation in human vertebral trabecular bone. Journal of Bone and Mineral Research, 23, 1613-1618. doi:10.1359/jbmr.080517
[15] Hildebrand, T., Laib, A., Müller, R., Dequeker, J. and Rüegsegger, P. (1999) Direct threedimensional morpho metric analysis of human cancellous bone: Microstructural data from spine, femur, iliac crest, and calcaneus. Journal of Bone and Mineral Research, 14, 1167-1174. doi:10.1359/jbmr.1999.14.7.1167
[16] Tamminen, I.S., Isaksson, H., Aula, A.S., et al. (2011) Reproducibility and agreement of micro-CT and histomorphometry in human trabecular bone with different metabolic status. Journal of Bone and Mineral Metabolism, 29, 442-448. doi:10.1007/s00774-010-0236-6
[17] Müller, R., Van Campenhout, H., Van Damme, B., et al. (1998) Morphometric analysis of human bone biopsies: A quantitative structural comparison of histological sections and micro-computed tomography. Bone, 23, 59-66. doi:10.1016/S8756-3282(98)00068-4
[18] Djuric, M., Djonic, D., Milovanovic, P., et al. (2010) Region-specific sex-dependent pattern of age related changes of proximal femoral cancellous bone and its implications on differential bone fragility. Calcified Tissue International, 86, 192 201. doi:10.1007/s00223-009-9325-8
[19] Macho, G.A., Abel, R.L. and Schutkowski, H. (2005) Age changes in bone microstructure: Do they occur uniformly? International Journal of Osteoarchaeology, 15, 421-430. doi:10.1002/oa.797
[20] Cui, W.-Q., Won, Y.-Y., Baek, M.-H., et al. (2008) Age and region-dependent changes in three-dimensional microstructural properties of proximal femoral trabeculae. Osteoporosis International, 19, 1579-1587. doi:10.1007/s00198-008-0601-7
[21] Chen, H., Zhou, X., Shoumura, S., Emura, S. and Bunai, Y. (2010) Age and gender-dependent changes in three di mensional microstructure of cortical and trabecular bone at the human femoral neck. Osteoporosis International, 21, 627-636. doi:10.1007/s00198-009-0993-z
[22] Issever, A.S., Vieth, V., Lotter, A., et al. (2002) Local differences in the trabecular bone structure of the proximal femur depicted with high-spatial-resolution MR imaging and multisection CT. Academic Radiology, 9, 1395 1406. doi:10.1016/S1076-6332(03)80667-0
[23] Nazarian, A., Müller, J., Zurakowski, D., Müller, R. and Snyder, B.D. (2007) Densitometric, morphometric and mechanical distributions in the human proximal femur. Journal of Biomechanics, 40, 2573-2579. doi:10.1016/j.jbiomech.2006.11.022
[24] Bauer, J.S. and Link, T.M. (2009) Advances in osteoporosis imaging. European Journal of Radiology, 71, 440 449. doi:10.1016/j.ejrad.2008.04.064
[25] Campbell, G.M., Buie, H.R. and Boyd, S.K. (2008) Signs of irreversible architectural changes occur early in the development of experimental osteoporosis as assessed by in vivo micro-CT. Osteoporosis International, 19, 1409-1419. doi:10.1007/s00198-008-0581-7
[26] Laib, A., Barou, O., Vico, L., et al. (2000) 3D micro computed tomography of trabecular and cortical bone architecture with application to a rat model of immobilisation osteoporosis. Medical and Biological Engineering and Computing, 38, 326-332. doi:10.1007/BF02347054
[27] Lill, C.A., Gerlach, U.V., Eckhardt, C., et al. (2002) Bone changes due to glucocorticoid application in an ovariectomized animal model for fracture treatment in osteopo rosis. Osteoporosis International, 13, 407-414. doi:10.1007/s001980200047
[28] Xiang, A., Kanematsu, M., Kumar, S., et al. (2007) Changes in micro-CT 3D bone parameters reflect effects of a potent cathepsin K inhibitor (SB-553484) on bone resorption and cortical bone formation in ovariectomized mice. Bone, 40, 1231-1237. doi:10.1016/j.bone.2007.01.010
[29] Nazarian, A., Snyder, B.D., Zurakowski, D. and Müller, R. (2008) Quantitative micro computed tomography: A non-invasive method to assess equivalent bone mineral density. Bone, 43, 302-311. doi:10.1016/j.bone.2008.04.009
[30] Sun, S.-S., Ma, H.-L., Liu, C.-L., et al. (2008) Difference in femoral head and neck material properties between osteoarthritis and osteoporosis. Clinical Biomechanics, 23, 39-47. doi:10.1016/j.clinbiomech.2007.11.018
[31] Genant, H.K., Engelke, K. and Prevrhal, S. (2008) Ad vanced CT bone imaging in osteoporosis. Rheumatology, 47, 9-16. doi:10.1093/rheumatology/ken180
[32] Wu, Z.-X., Lei, W., Hu, Y.Y., et al. (2008) Effect of ova riectomy on BMD, micro-architecture and biomechanics of cortical and cancellous bones in a sheep model. Medical Engineering & Physics, 30, 1112 1118. doi:10.1016/j.medengphy.2008.01.007
[33] Campbell, G.M., Ominsky, M.S. and Boyd, S.K. (2011) Bone quality is partially recovered after the discontinua tion of RANKL administration in rats by increased bone mass on existing trabeculae: An in vivo micro-CT study. Osteoporosis International, 22, 931-942. doi:10.1007/s00198-010-1283-5
[34] Kapadia, R.D., Stroup, G.B., Badger, A.M., et al. (1998) Applications of micro-CT and MR microscopy to study pre-clinical models of osteoporosis and osteoarthritis. Technology and Health Care, 6, 361-372.
[35] Zhang, Z.M., Li, Z.C., Jiang, L.S., Jiang, S.D. and Dai, L.Y. (2010) Micro-CT and mechanical evaluation of sub chondral trabecular bone structure between postmenopausal women with osteoarthritis and osteoporosis. Osteoporosis International, 21, 1383-1390. doi:10.1007/s00198-009-1071-2
[36] Ito, M., Nakamura, T., Matsumoto, T., et al. (1998) Analysis of trabecular microarchitecture of human iliac bone using microcomputed tomography in patients with hip arthrosis with or without vertebral fracture. Bone, 23, 163-169. doi:10.1016/S8756-3282(98)00083-0
[37] Chappard, C., Peyrin, F., Bonnassie, A., et al. (2006) Sub chondral bone micro-architectural alterations in osteoarthritis: A synchrotron micro-computed tomography study. Osteoarthritis Cartilage, 14, 215-223. doi:10.1016/j.joca.2005.09.008
[38] Tassani, S., Particelli, F., Perilli, E., et al. (2011) De pendence of trabecular structure on bone quantity: A comparison between osteoarthritic and non-pathological bone. Clinical Biomechanics, 26, 632-639. doi:10.1016/j.clinbiomech.2011.01.010
[39] Nazarian, A. and Müller, R. (2004) Time-lapsed micro structural imaging of bone failure behaviour. Journal of Biomechanics, 37, 55-65. doi:10.1016/S0021-9290(03)00254-9
[40] Nazarian, A., Hermannsson, B.J., Müller, J., Zurakowski, D. and Snyder, B.D. (2009) Effects of tissue preservation on murine bone mechanical properties. Journal of Bio mechanics, 42, 82-86. doi:10.1016/j.jbiomech.2008.09.037
[41] Nazarian, A., Entezari, V., Vartanians, V., Müller, R. and Snyder, B.D. (2009) An improved method to assess torsional properties of rodent long bones. Journal of Bio mechanics, 42, 1720-1725. doi:10.1016/j.jbiomech.2009.04.019
[42] Nazarian, A., Bauernschmitt, M., Eberle, C., Meier, D., Müller, R. and Snyder, B.D. (2008) Design and validation of a testing system to assess torsional cancellous bone failure in conjunction with time-lapsed micro-computed tomographic imaging. Journal of Biomechanics, 41, 3496- 3501. doi:10.1016/j.jbiomech.2008.09.014
[43] Verdelis, K., Lukashova, L., Atti, E. et al. (2011) Micro CT morphometry analysis of mouse cancellous bone: Intra and inter-system reproducibility. Bone, 49, 580-587. doi:10.1016/j.bone.2011.05.013
[44] Beaupied, H., Chappard, C., Basillais, A., et al. (2006) Effect of specimen conditioning on the microstructural parameters of trabecular bone assessed by micro computed tomography. Physics in Medicine and Biology, 51, 4621-4634. doi:10.1088/0031-9155/51/18/011
[45] Dezna, C. and Sheehan, B. (1973) Theory and practice of histotechnology. 1st Edition, C.V. Mosby Company, Saint Louis.
[46] Erben, R.G. (1997) Embedding of bone samples in me thylmethacrylate: an improved method suitable for bone histomorphometry, histochemistry, and immunohistoche mistry. Journal of Histochemistry & Cytochemistry, 45, 307-313. doi:10.1177/002215549704500215
[47] Odgaard, A. (1997) Three-dimensional methods for quan tification of cancellous bone architecture. Bone, 20, 315-328. doi:10.1016/S8756-3282(97)00007-0
[48] Parfitt, A., Drezner, M., Glorieux, F. et al. (1987) Bone histomorphometry: Standardization of nomenclature, symbols, and units. Journal of Bone and Mineral Research, 2, 595-610. doi:10.1002/jbmr.5650020617
[49] SkyScan 1172, N.V. Vluchtenburgstraat 3C 2630-Kon tick Belgium. http://www.skyscan.be/home.htm
[50] Viguet-Carrin, S., Follet, H., Gineyts, E., et al. (2010) Association between collagen cross-links and trabecular microarchitecture properties of human vertebral bone. Bone, 46, 342-347. doi:10.1016/j.bone.2009.10.001

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