The effect of microcomputed tomography scanning and reconstruction voxel size on the accuracy of stereological measurements in human cancellous bone

wbldb

Kim, Do-Gyoon¹; Christopherson, Gregory T.¹; Dong, X. Neil¹; Fyhrie, David P.²; Yeni, Yener N.¹

The effect of microcomputed tomography scanning and reconstruction voxel size on the accuracy of stereological measurements in human cancellous bone

Bone. December 2004;35(6):1375-1382

©2004 Elsevier Inc. All rights reserved.

Affiliations

¹Bone and Joint Center, Henry Ford Hospital, Detroit, MI, 48202, USA

²Orthopaedic Research Laboratories, UC Davis, School of Medicine, Sacramento, CA 95817, USA
Abstract and keywords

Stereological parameters have been used as an approximation for the architecture of trabecular bone. Structural indices such as bone volume fraction (BV/TV), trabecular number (Tb.N), trabecular thickness (Tb.Th), trabecular separation (Tb.Sp), bone surface-to-volume ratio (BS/BV), degree of anisotropy (MIL1/MIL3), and connectivity density (−Euler/Vol) have been widely studied to investigate pathological conditions in bone. Due to its high resolution and nondestructiveness, microcomputed tomography (micro-CT) has been utilized to take precise three-dimensional (3D) images of trabecular microstructures. However, spatial limitations for applying micro-CT-based analyses to large specimens, such as whole vertebral bodies, require using larger scanning and reconstruction voxel sizes.

In this study, combinations of three different scanning and reconstruction voxel size were used to represent best possible voxel size (21 μm; best in our scanner for the specimen size used) relative to other voxel sizes used in this study, commonly used intermediate voxel sizes (50 μm), and those applicable to scans of whole human vertebral bodies (110 μm) in order to examine the effect of scanning and reconstruction voxel size on stereological measures for human cancellous bone.

The error in stereological parameters calculated using combinations of large voxel sizes compared to the gold standard (best possible case) ranged from 0.1% to 102%. The signed magnitude of the error in other cases relative to the gold standard was a function of either scanning or reconstruction voxel size or both (r² = 0.55–0.95). For most of the structural indices, the results from analysis of images with larger voxel sizes were correlated with those from the gold standard (r² = 0.55–0.99) except for Tb.N at 110/110 μm, MIL1/MIL3 at larger than 110 μm reconstruction voxel size, and −Euler/Vol at any combination of voxel sizes. Overall, it was observed that resampling a high resolution image at lower resolutions (corresponding to increasing reconstruction voxel size in this study) had different effects on the calculated parameters than scanning at the same low resolution (corresponding to increasing scanning voxel size in this study). Our results show that investigations of image resolution should include actual scans at the resolution of interest rather than simply coarsening of high-resolution images as is customarily done.

Keywords: Stereology; Trabecular bone; Micro-CT; Resolution; Calibration
Links

DOI: 10.1016/j.bone.2004.09.007

PubMed: 15589219

WoS: 000225938700016
History

Received: 2004-03-16

Revised: 2004-09-14

Accepted: 2004-09-20

Cited Works (23)

Year	Entry
2001	Homminga J, Huiskes R, Van Rietbergen B, Rüegsegger P, Weinans H. Introduction and evaluation of a gray-value voxel conversion technique. J Biomech. April 2001;34(4):513-517.
1993	Engelke K, Graeff W, Meiss L, Hahn M, Delling G. High spatial resolution imaging of bone mineral using computed microtomography: comparison with microradiography and undecalcified histologic sections. Invest Radiol. April 1993;28(4):341-349.
1996	Rüegsegger P, Koller B, Müller R. A microtomographic system for the nondestructive evaluation of bone architecture. Calcif Tiss Int. 1996;58(1):24-29.
1997	Silva MJ, Gibson LJ. Modeling the mechanical behavior of vertebral trabecular bone: effects of age-related changes in microstructure. Bone. 1997;21(2):191-199.
2000	Ciarelli TE, Fyhrie DP, Schaffler MB, Goldstein SA. Variations in three‐dimensional cancellous bone architecture of the proximal femur in female hip fractures and in controls. J Bone Miner Res. 2000;15(1):32-40.
1994	Goulet RW, Goldstein SA, Ciarelli MJ, Kuhn JL, Brown MB, Feldkamp LA. The relationship between the structural and orthogonal compressive properties of trabecular bone. J Biomech. April 1994;27(4):375-389.
1998	Müller R, Van Campenhout H, Van Damme B, Van der Perre G, Dequeker J, Hildebrand T, Rüegsegger P. Morphometric analysis of human bone biopsies: a quantitative structural comparison of histological sections and micro-computed tomography. Bone. July 1998;23(1):59-66.
1999	Jacobs CR, Davis BR, Rieger CJ, Francis JJ, Saad M, Fyhrie DP. The impact of boundary conditions and mesh size on the accuracy of cancellous bone tissue modulus determination using large-scale finite-element modeling. J Biomech. November 1999;32(11):1159-1164.
1998	Kinney JH, Ladd AJC. The relationship between three-dimensional connectivity and the elastic properties of trabecular bone. J Bone Miner Res. May 1998;13(5):839-845.
2003	Ding M, Day JS, Burr DB, Mashiba T, Hirano T, Weinans H, Sumner DR, Hvid I. Canine cancellous bone microarchitecture after one year of high-dose bisphosphonates. Calcif Tiss Int. June 2003;72(6):737-744.
2000	Ding M, Hvid I. Quantification of age-related changes in the structure model type and trabecular thickness of human tibial cancellous bone. Bone. March 2000;26(3):291-295.
2001	Yeni YN, Fyhrie DP. Finite element calculated uniaxial apparent stiffness is a consistent predictor of uniaxial apparent strength in human vertebral cancellous bone tested with different boundary conditions. J Biomech. December 2001;34(12):1649-1654.
1983	Parfitt AM, Mathews CH, Villanueva AR, Kleerekoper M, Frame B, Rao DS. 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. October 1983;72(4):1396-1409.
1984	Feldkamp LA, Davis LC, Kress JW. Practical cone-beam algorithm. J Opt Soc Am. 1984;A1(6):612-619.
1989	Feldkamp LA, Goldstein SA, Parfitt MA, Jesion G, Kleerekoper M. The direct examination of three‐dimensional bone architecture in vitro by computed tomography. J Bone Miner Res. 1989;4(1):3-11.
1998	Ladd AJC, Kinney JH, Haupt DL, Goldstein SA. Finite‐element modeling of trabecular bone: comparison with mechanical testing and determination of tissue modulus. J Orthop Res. September 1998;16(5):622-628.
2002	Ito M, Nishida A, Nakamura T, Uetani M, Hayashi K. Differences of three-dimensional trabecular microstructure in osteopenic rat models caused by ovariectomy and neurectomy. Bone. April 2002;30(4):594-598.
1995	van Rietbergen B, Weinans H, Huiskes R, Odgaard A. A new method to determine trabecular bone elastic properties and loading using micromechanical finite-element models. J Biomech. January 1995;28(1):69-81.
1993	Odgaard A, Gundersen HJG. Quantification of connectivity in cancellous bone, with special emphasis on 3-D reconstructions. Bone. March–April 1993;14(2):173-182.
1997	Odgaard A. Three-dimensional methods for quantification of cancellous bone architecture. Bone. 1997;20(4):315-328.
1998	Kothari M, Keaveny TM, Lin JC, Newitt DC, Genant HK, Majumdar S. Impact of spatial resolution on the prediction of trabecular architecture parameters. Bone. May 1998;22(5):437-443.
1999	Van Rietbergen B, Müller R, Ulrich D, Rüegsegger P, Huiskes R. Tissue stresses and strain in trabeculae of a canine proximal femur can be quantified from computer reconstructions. J Biomech. February 1999;32(2):165-173.
1999	Laib A, Rüegsegger P. Calibration of trabecular bone structure measurements of in vivo three-dimensional peripheral quantitative computed tomography with 28-μm-resolution microcomputed tomography. Bone. January 1999;24(1):35-39.

Cited By (26)

Year	Entry
2019	Abu Bakar NN, Saidi B, Yamin LSM. Measurement of trabecular bone parameters with different bone thicknesses and voxel sizes in mice using micro-CT. Malays J Fundam Appl Sci. January–February 2019;15(1):65-68.
2019	Zenzes M, Bortel EL, Fratzl P, Mundlos S, Schuetz M, Schmidt H, Duda GN, Witte F, Zaslansky P. Normal trabecular vertebral bone is formed via rapid transformation of mineralized spicules: a high-resolution 3D ex-vivo murine study. Acta Biomater. March 1, 2019;86:429-440.
2007	Kim D-G, Hunt CA, Zauel R, Fyhrie DP, Yeni YN. The effect of regional variations of the trabecular bone properties on the compressive strength of human vertebral bodies. Ann Biomed Eng. November 2007;35(11):1907-1913.
2019	Knowles NK, Ip K, Ferreira LM. The effect of material heterogeneity, element type, and down-sampling on trabecular stiffness in micro finite element models. Ann Biomed Eng. February 2019;47(2):615-623.
2013	Harrison NM, McDonnell P, Mullins L, Wilson N, O’Mahoney D, McHugh PE. Failure modelling of trabecular bone using a non-linear combined damage and fracture voxel finite element approach. Biomech Model Mechanobiol. April 2013;12(2):225-241.
2008	Yeni YN, Zelman EA, Divine GW, Kim D-G, Fyhrie DP. Trabecular shear stress amplification and variability in human vertebral cancellous bone: relationship with age, gender, spine level and trabecular architecture. Bone. March 2008;42(3):591-596.
2008	Chappard C, Marchadier A, Benhamou CL. Side-to-side and within-side variability of 3D bone microarchitecture by conventional micro-computed tomography of paired iliac crest biopsies. Bone. July 2008;43(1):203-208.
2009	Bevill G, Keaveny TM. Trabecular bone strength predictions using finite element analysis of micro-scale images at limited spatial resolution. Bone. April 2009;44(4):579-584.
2009	Meganck JA, Kozloff KM, Thornton MM, Broski SM, Goldstein SA. Beam hardening artifacts in micro-computed tomography scanning can be reduced by X-ray beam filtration and the resulting images can be used to accurately measure BMD. Bone. December 2009;45(6):1104-1116.
2021	Mys K, Varga P, Stockmans F, Gueorguiev B, Wyers CE, van den Bergh JPW, van Lenthe GH. Quantification of 3D microstructural parameters of trabecular bone is affected by the analysis software. Bone. January 2021;142:115653.
2016	Christiansen BA. Effect of micro-computed tomography voxel size and segmentation method on trabecular bone microstructure measures in mice. Bone Rep. December 2016;5:136-140.
2011	Kim D-G, Shertok D, Tee BC, Yeni YN. Variability of tissue mineral density can determine physiological creep of human vertebral cancellous bone. J Biomech. June 3, 2011;44(9):1660-1665.
2008	Chappard C, Marchadier A, Benhamou L. Interindividual and intraspecimen variability of 3-D bone microarchitectural parameters in iliac crest biopsies imaged by conventional micro-computed tomography. J Bone Min Metab. 2008;26(5):506-513.
2013	Depalle B, Chapurlat R, Walter-Le-Berre H, Bou-Saïd B, Follet H. Finite element dependence of stress evaluation for human trabecular bone. J Mech Behav Biomed Mater. February 2013;18:200-212.
2016	Wen X-X, Xua C, Zong C-L, Feng Y-F, Ma X-Y, Wang F-Q, Yan Y-B, Lei W. Relationship between sample volumes and modulus of human vertebral trabecular bone in micro-finite element analysis. J Mech Behav Biomed Mater. July 2016;60:468-475.
2019	Molino G, Dalpozzi A, Ciapetti G, Lorusso M, Novara C, Cavallo M, Baldini N, Giorgis F, Fiorilli S, Vitale-Brovarone C. Osteoporosis-related variations of trabecular bone properties of proximal human humeral heads at different scale lengths. J Mech Behav Biomed Mater. December 2019;100:103373.
2006	Sierpowska J, Hakulinen MA, Töyräs J, Day JS, Weinans H, Kiviranta I, Jurvelin JS, Lappalainen R. Interrelationships between electrical properties and microstructure of human trabecular bone. Phys Med Biol. 2006;51(20):5289-5303.
2007	Kohler T. A Service-Oriented Platform for Visualization and High-Throughput Structural Characterization in Bone Phenomics [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2007.
2011	Wu Z. Measures of Bone Quality and Their Relationship to Bone Mechanical Properties [PhD thesis]. University of Notre Dame; December 2011.
2007	Yao H. Mechanical Testing of Bone and Bone-Like Materials Using Image Correlation Strain Measurement Technique [Master's thesis]. Southern Methodist University; August 2007.
2011	Su A. The Functional Morphology of Subchondral and Trabecular Bone in the Hominoid Tibiotalar Joint [PhD thesis]. Stony Brook, NY: Stony Brook University; August 2011.
2014	Colombo A. La micro-architecture de l’os trabéculaire en croissance: Variabilité tridimensionnelle normale et pathologique analysée par microtomodensitométrie [PhD thesis]. Université de Bordeaux; December 15, 2014.
2005	Cooper DML. 3D Micro-CT Imaging of Human Cortical Bone Porosity: A Novel Method for Estimating Age At Death [PhD thesis]. Calgary, AB: University of Calgary; December 2005.
2008	Bevill GR. Micromechanical Modeling of Failure in Trabecular Bone [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2008.
2010	Meganck JA. Fracture Healing and Regeneration in the Context of an Altered Collagenous Extracellular Matrix [PhD thesis]. University of Michigan; 2010.
2019	Knowles NK. Improving Material Mapping in Glenohumeral Finite Element Models: A Multi-Level Evaluation [PhD thesis]. University of Western Ontario; 2019.