Calcified Tissue International

, Volume 75, Issue 1, pp 15–22 | Cite as

Technical Considerations for Microstructural Analysis of Human Trabecular Bone from Specimens Excised from Various Skeletal Sites

  • E. Nägele
  • V. Kuhn
  • H. Vogt
  • T. M. Link
  • R. Müller
  • E. -M. Lochmüller
  • F. Eckstein
Article

Abstract

The purpose of this study was to test the effect of repositioning, systematic displacements of the region of interest (ROI), and acquisition parameters (scan mode and integration time) on quantitative analysis of human trabecular bone microstructure at various skeletal sites, using microcomputed tomographic (μCT) technology. We investigated 28 cylindrical specimens of human trabecular bone (length 14 mm, diameter 8 mm) from four skeletal sites (femoral neck, greater trochanter, second lumbar vertebra, and distal radius). These specimens were selected from over 200 μCT measurements, in order to cover a large range of bone volume fraction (BV/TV) observed at each site. Cylindrical ROIs (length 6 mm, diameter 6 mm) were examined twice at an isotropic resolution of 26 μm, 8 weeks apart. In addition, comparative analyses were performed for displacements of the volumes of interest (VOIs) by 1, 2, 3, and 4 mm (83.4%, 66.6%, 50%, and 33.3% overlap), respectively. Eventually, comparative measurements were obtained at different resolution scan modes and integration times. The results show that μCT measurements are highly reproducible (range of the root mean square coefficient variation % (RMS CV%) = 0.64% to 1.29% for BV/TV at different sites). Displacements of the VOI of up to 4 mm generally led to non significant systematic differences in mean values of <10%. When comparing various combinations of resolution scan modes and integration times, the use of an integration time of 100 ms was found to be preferable for determining microstructural parameters from human samples with this μCT scanner.

Keywords

Trabecular bone Microstructure Microcomputed tomography Human Microarchitecture 

References

  1. 1.
    Feldkamp, LA, Goldstein, SA, Parfitt, AM, Jesion, G, Kleerekoper, M 1989The direct examination of three-dimensional bone architecture in vitro by computed tomography.J Bone Miner Res4311PubMedGoogle Scholar
  2. 2.
    Kuhn, JL, Goldstein, SA, Feldkamp, LA, Goulet, RW, Jesion, G 1990Evaluation of a microcomputed tomography system to study trabecular bone structure.J Orthop Res8833842PubMedGoogle Scholar
  3. 3.
    Durand, EP, Rüegsegger, P 1992High-contrast resolution of CT images for bone structure analysis.Med Phys19569573CrossRefPubMedGoogle Scholar
  4. 4.
    Rüegsegger, P, Koller, B, Müller, R 1996A microtomographic system for the nondestructive evaluation of bone architecture.Calcif Tissue Int582429CrossRefPubMedGoogle Scholar
  5. 5.
    Müller, R, Rüegsegger, P 1997Micro-tomographic imaging for the nondestructive evaluation of trabecular bone architecture.Stud Health Technol Inform406179PubMedGoogle Scholar
  6. 6.
    Odgaard, A 1997Three-dimensional methods for quantification of cancellous bone architecture.Bone20315328CrossRefPubMedGoogle Scholar
  7. 7.
    Hildebrand, T, Rüegsegger, E 1997Quantification of bone microarchitecture with the structure model index.Comp Meth Biomech Biomed Eng11523Google Scholar
  8. 8.
    Hildebrand, T, Laib, A, Müller, R, Dequeker, J, Rüegsegger, P 1999Direct three-dimensional morphometric analysis of human cancellous bone: microstructural data from spine, femur, iliac crest, and calcaneus.J Bone Miner Res1411671174PubMedGoogle Scholar
  9. 9.
    Genant, HK, Gordon, C, Jiang, Y, Link, TM, Hans, D, Majumdar, S, Lang, TF 2000Advanced imaging of the macrostructure and microstructure of bone.Horm Res542430CrossRefPubMedGoogle Scholar
  10. 10.
    Legrand, E, Chappard, D, Pascaretti, C, Duquenne, M, Krebs, S, Rohmer, V, Basle, MF, Audran, M 2000Trabecular bone microarchitecture, bone mineral density, and vertebral fractures in male osteoporosis.J Bone Miner Res151319PubMedGoogle Scholar
  11. 11.
    Ding, M, Odgaard, A, Linde, F, Hvid, I 2002Age-related variations in the microstructure of human tibial cancellous bone.J Orthop Res20615621CrossRefPubMedGoogle Scholar
  12. 12.
    Dalle, CL, Arlot, ME, Chavassieux, PM, Roux, JP, Portero, NR, Meunier P, J 2001Comparison of trabecular bone microarchitecture and remodeling in glucocorticoid-induced and postmenopausal osteoporosis.J Bone Miner Res1697103PubMedGoogle Scholar
  13. 13.
    Ciarelli, TE, Fyhrie, DP, Schaffler, MB, Goldstein, SA 2000Variations in three-dimensional cancellous bone architecture of the proximal femur in female hip fractures and in controls.J Bone Miner Res153240PubMedGoogle Scholar
  14. 14.
    Ulrich, D, Hildebrand, T, Rietbergen, B, Müller, R, Rüegsegger, P 1997The quality of trabecular bone evaluated with micro-computed tomography, FEA and mechanical testing.Stud Health Technol Inform4097112PubMedGoogle Scholar
  15. 15.
    Ulrich, D, Rietbergen, B, Laib, A, Rüegsegger, P 1999The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone.Bone255560CrossRefPubMedGoogle Scholar
  16. 16.
    Pistoia, W, Rietbergen, B, Lochmüller, EM, Lill, CA, Eckstein, F, Rüegsegger, P 2002Estimation of distal radius failure load with micro-finite element analysis models based on three-dimensional peripheral quantitative computed tomography images.Bone30842848CrossRefPubMedGoogle Scholar
  17. 17.
    Rietbergen, B, Odgaard, A, Kabel, J, Huiskes, R 1998Relationships between bone morphology and bone elastic properties can be accurately quantified using high-resolution computer reconstructions.J Orthop Res162328PubMedGoogle Scholar
  18. 18.
    Müller, R., Rüegsegger, P 1996Analysis of mechanical properties of cancellous bone under conditions of simulated bone atrophy.J Biomech2910531060CrossRefPubMedGoogle Scholar
  19. 19.
    Lane, NE, Kumer, JL, Majumdar, S, Khan, M, Lotz, J, Stevens, RE, Klein, R, Phelps, KV 2002The effects of synthetic conjugated estrogens, a (cenestin) on trabecular bone structure and strength in the ovariectomized rat model.Osteoporos Int13816823CrossRefPubMedGoogle Scholar
  20. 20.
    Lespessailles, E, Poupon, S, Niamane, R, Loiseau-Peres, S, Derommelaere, G, Harba, R, Courteix, D, Benhamou, CL 2002Fractal analysis of trabecular bone texture on calcaneus radiographs: effects of age, time since menopause and hormone replacement therapy.Osteoporos Int13366372CrossRefPubMedGoogle Scholar
  21. 21.
    Ito, M 2003[Effects of bisphosphonate on trabecular microstructure.]Nippon Rinsho61213218Google Scholar
  22. 22.
    Shiraishi, A, Higashi, S, Masaki, T, Saito, M, Ito, M, Ikeda, S, Nakamura, T 2002A comparison of alfacalcidol and menatetrenone for the treatment of bone loss in an ovariectomized rat model of osteoporosis.Calcif Tissue Int716979CrossRefPubMedGoogle Scholar
  23. 23.
    Dempster, DW, Cosman, F, Kurland, ES, Zhou, H, Nieves, J, Woelfert, L, Shane, E, Plavetic, K, Muller, R, Bilezikian, J, Lindsay, R 2001Effects of daily treatment with parathyroid hormone on bone microarchitecture and turnover in patients with osteoporosis: a paired biopsy study.J Bone Miner Res1618461853PubMedGoogle Scholar
  24. 24.
    Jiang, Y, Zhao, J, Genant, HK, Dequeker, J, Geusens, P 1998Bone mineral density and biomechanical properties of spine and femur of ovariectomized rats treated with naproxen.Bone22509504CrossRefPubMedGoogle Scholar
  25. 25.
    Shahtaheri, SM, Aaron, JE, Johnson, DR, Purdie, DW 1999Changes in trabecular bone architecture in women during pregnancy.Br J Obstet Gynaecol106432438PubMedGoogle Scholar
  26. 26.
    Kurth, AA, Muller, R 2001The effect of an osteolytic tumor on the three-dimensional trabecular bone morphology in an animal model.Skeletal Radiol309498CrossRefPubMedGoogle Scholar
  27. 27.
    Tamada, T 2000[Three-dimensional microstructural analysis of human lumbar vertebrae using microcomputed tomography in bone metastasis from prostate cancer.]Nippon Igaku Hoshasen Gakkai Zasshi60740751Google Scholar
  28. 28.
    Kamibayashi, L, Wyss, UP, Cooke, TD, Zee, B 1995Trabecular microstructure in the medial condyle of the proximal tibia of patients with knee osteoarthritis.Bone172735CrossRefPubMedGoogle Scholar
  29. 29.
    Beuf, O, Ghosh, S, Newitt, DC, Link, TM, Steinbach, L, Ries, M, Lane, N, Majumdar, S 2002Magnetic resonance imaging of normal and osteoarthritic trabecular bone structure in the human knee.Arthritis Rheum46385393CrossRefPubMedGoogle Scholar
  30. 30.
    Patel, V, Issever, AS, Burghardt, A, Laib, A, Ries, M, Majumdar, S 2003MicroCT evaluation of normal and osteoarthritic bone structure in human knee specimens.J Orthop Res.21613CrossRefPubMedGoogle Scholar
  31. 31.
    Day, JS, Ding, M, Linden, JC, Hvid, I, Sumner, DR, Weinans, H 2001A decreased subchondral trabecular bone tissue elastic modulus is associated with pre-arthritic cartilage damage.J Orthop Res19914918CrossRefPubMedGoogle Scholar
  32. 32.
    Boyd, SK, Müller, R, Zernicke, RF 2002Mechanical and architectural bone adaptation in early stage experimental osteoarthritis.J Bone Miner Res17687694Google Scholar
  33. 33.
    Dempster, DW, Ferguson-Pell, MW, Mellish, RW, Cochran, GV, Xie, F, Fey, C, Herbert, W, Parisien, M, Lindsay, R 1993Relationships between bone structure in the iliac crest and bone structure and strength in the lumbar spine.Osteoporos Int39096PubMedGoogle Scholar
  34. 34.
    Amling, M, Herden, S, Posl, M, Hahn, M, Ritzel, H, Delling, G 1996Heterogeneity of the skeleton: comparison of the trabecular microarchitecture of the spine, the iliac crest, the femur, and the calcaneus.J Bone Miner Res113645PubMedGoogle Scholar
  35. 35.
    Goldstein, SA 1987The mechanical properties of trabecular bone: dependence on anatomic location and function.J Biomech2010551061CrossRefPubMedGoogle Scholar
  36. 36.
    Thomsen, JS, Ebbesen, EN, Mosekilde, L 2002Zone-dependent changes in human vertebral trabecular bone: clinical implications.Bone30664669CrossRefPubMedGoogle Scholar
  37. 37.
    Issever, AS, Vieth, V, Letter, A, Meier, N, Laib, A, Newitt, D, Majumdar, S, Link, TM 2002Local differences in the trabecular bone structure of the proximal femur depicted with high-spatial-resolution MR imaging and multisection CT.Acad Radiol913951406CrossRefPubMedGoogle Scholar
  38. 38.
    Courtney, AC, Wachtel, EF, Myers, ER, Hayes, WC 1994Effects of loading rate on strength of the proximal femur.Calcif Tissue Int555358PubMedGoogle Scholar
  39. 39.
    Courtney, AC, Wachtel, EF, Myers, ER, Hayes, WC 1995Age-related reductions in the strength of the femur tested in a fall-loading configuration.J Bone Joint Surg Am77387395PubMedGoogle Scholar
  40. 40.
    Bouxsein, ML, Courtney, AC, Hayes, WC 1995Ultrasound and densitometry of the calcaneus correlate with the failure loads of cadaveric femurs.Calcif Tissue Int5699103PubMedGoogle Scholar
  41. 41.
    Lochmüller, EM, Lill, CA, Kuhn, V, Schneider, E, Eckstein, F 2002Radius bone strength in bending, compression, and falling and its correlation with clinical densitometry at multiple sites.J Bone Miner Res1716291638PubMedGoogle Scholar
  42. 42.
    Müller, R, Koller, B, Hildebrand, T, Laib, A, Gianolini, S, Rüegsegger, P 1996Resolution dependency of microstructural properties of cancellous bone based on three-dimensional μ-tomography.Technol Health Care4113119PubMedGoogle Scholar
  43. 43.
    Glüer, CC, Blake, G, Lu, Y, Blunt, BA, Jergas, M, Genant, HK 1995Accurate assessment of precision errors: how to measure the reproducibility of bone densitometry techniques.Osteoporos Int5262270PubMedGoogle Scholar
  44. 44.
    Riggs, BL, Melton, LJ,III 1995The worldwide problem of osteoporosis: insights afforded by epidemiology.Bone17505S511SCrossRefPubMedGoogle Scholar
  45. 45.
    Morgan, EF, Keaveny, TM 2001Dependence of yield strain of human trabecular bone on anatomic site.J Biomech34569577CrossRefPubMedGoogle Scholar
  46. 46.
    Turner, CH, Cowin, SC 1988Errors induced by off-axis measurement of the elastic properties of bone.J Biomech Eng110213215PubMedGoogle Scholar
  47. 47.
    Thomsen, JS, Ebbesen, EN, Mosekilde, L 2002Zone-dependent changes in human vertebral trabecular bone: clinical implications.Bone30664669CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2004

Authors and Affiliations

  • E. Nägele
    • 1
    • 2
  • V. Kuhn
    • 1
    • 2
  • H. Vogt
    • 1
    • 2
  • T. M. Link
    • 3
  • R. Müller
    • 4
  • E. -M. Lochmüller
    • 2
  • F. Eckstein
    • 1
    • 5
  1. 1.Musculoskeletal Research GroupInstitute of Anatomy, Ludwig-Maximilians-Universität MünchenMünchenGermany
  2. 2.Universitatsfrauenklinik der Ludwig-Maximilians-Universität MünchenMünchenGermany
  3. 3.Institute for Diagnostic RadiologyKlinikum rechts der IsarMünchenGermany
  4. 4.Institute for Biomedical EngineeringSwiss Federal institute of Technology (ETH) and University of ZürichZürichSwitzerland
  5. 5.Institute of Anatomy, Paracelsa’s Private Medical University, Müllner Hauptstr.Salzburg, Austria

Personalised recommendations