In vivo reproducibility of three‐dimensional structural properties of noninvasive bone biopsies using 3D‐pQCT

wbldb

Müller, R.¹; Hildebrand, T.¹; Häuselmann, H. J.²; Rüegsegger, P.¹

In vivo reproducibility of three‐dimensional structural properties of noninvasive bone biopsies using 3D‐pQCT

J Bone Miner Res. November 1996;11(11):1745-1750

©1996 American Society for Bone and Mineral Research

Affiliations

¹Institute for Biomedical Engineering, University of Zürich and Swiss Federal Institute of Technology (ETH), Zürich. Switzerland

²Department of Rheumatology, University Hospital, Zürich, Switzerland
Abstract

Trabecular bone architecture is one of the main factors influencing the mechanical behavior of cancellous bone. To assess the three‐dimensional trabecular microstructure of intact bones, we introduced the concept of noninvasive bone biopsy, a method to assess and analyze cancellous bone based upon three‐dimensional peripheral quantitative computed tomography in vivo (3D‐pQCT). The aim of this work was to demonstrate the potential of noninvasive bone biopsies as a basis for structural and mechanical analysis of trabecular bone in the process of rapid bone loss. A group of six healthy young male volunteers was measured to provide data on the reproducibility of structural parameters. Baseline and 1‐month follow‐up measurements were performed to provide data on short‐term precision of the procedure, and three of the controls were reanalyzed within 3–6 months to estimate long‐term precision. Prior to structural evaluation, the baseline and follow‐up measurements were repositioned three‐dimensionally to ensure matching volumes of interest (VOI). Trabecular bone density (TBD) as well as structural indices were analyzed for all measurements. The VOIs were analyzed morphometrically by evaluating bone volume (BV/TV) and trabecular number (Tb.N) based on a direct three‐dimensional approach. Trabecular thickness (Tb.Th) and trabecular separation (Tb.Sp) were derived from these two indices. The data of the measurements at 1 month to determine the short‐term precision was in excellent agreement with the baseline measurements. The results showed that structural parameters can be reproduced in vivo with a coefficient of variation of less than 0.5%. With a typical spread of 4% for the structural indices within the group of healthy volunteers, an intraclass correlation of better than 0.98 was reached. We conclude that high‐resolution 3D‐pQCT has the potential to detect structural changes in trabecular bone during therapeutic and diagnostic trials.
Links

DOI: 10.1002/jbmr.5650111118

PubMed: 8915782

WoS: A1996VQ70500017

Cited Works (12)

Year	Entry
1995	Kinney JH, Lane NE, Haupt DL. In vivo, three‐dimensional microscopy of trabecular bone. J Bone Miner Res. February 1995;10(2):264-270.
1995	Majumdar S, Newitt D, Jergas M, Gies A, Chiu E, Osman D, Keltner J, Keyak J, Genant H. Evaluation of technical factors affecting the quantification of trabecular bone structure using magnetic resonance imaging. Bone. October 1995;17(4):417-430.
1984	Harrigan TP, Mann RW. Characterization of microstructural anisotropy in orthotropic materials using a second rank tensor. J Mater Sci. March 1984;19(3):761-767.
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.
1992	Hahn M, Vogel M, Pompesius-Kempa M, Delling G. Trabecular bone pattern factor: a new parameter for simple quantification of bone microarchitecture. Bone. 1992;13(4):327-330.
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.
1990	Odgaard A, Andersen K, Melsen F, Gundersen HJG. A direct method for fast three-dimensional serial reconstruction. J Microsc (Oxford). September 1990;159(pt 3):335-342.
1996	Müller R, Hahn M, Vogel M, Delling G, Rüegsegger P. Morphometric analysis of noninvasively assessed bone biopsies: comparison of high-resolution computed tomography and histologic sections. Bone. March 1996;18(3):215-220.
1994	Müller R, Hildebrand T, Rüegsegger P. Non-invasive bone biopsy: a new method to analyse and display the three-dimensional structure of trabecular bone. Phys Med Biol. January 1994;39(1):145-164.
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.
1988	Mosekilde L. Age-related changes in vertebral trabecular bone architecture—assessed by a new method. Bone. 1988;9(4):247-250.
1993	Jara H, Wehrli FW, Chung H, Ford JC. High-resolution variable flip angle 3D MR imaging of trabecular microstructure in vivo. Mag Reson Med. April 1993;29(4):528-539.

Cited By (31)

Year	Entry
2002	Müller R. The Zürich experience: one decade of three-dimensional high-resolution computed tomography. Top Magn Reson Imaging. 2002;13(5):307-322.
2002	Wehrli F, Saha P, Gomberg B, Song H, Snyder P, Benito M, Wright A, Weening R. Role of magnetic resonance for assessing structure and function of trabecular bone. Top Magn Reson Imaging. October 2002;13(5):335-355.
1997	Laib A, Hildebrand T, Häuselmann HJ, Rüegsegger P. Ridge number density: a new parameter for in vivo bone structure analysis. Bone. December 1997;21(6):541-546.
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.
1998	Majumdar S, Kothari M, Augat P, Newitt DC, Link TM, Lin JC, Lang T, Lu Y, Genant HK. High-resolution magnetic resonance imaging: three-dimensional trabecular bone architecture and biomechanical properties. Bone. May 1998;22(5):445-454.
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	Ulrich D, van Rietbergen B, Laib A, Rüegsegger P. The ability of three-dimensional structural indices to reflect mechanical aspects of trabecular bone. Bone. 1999;25(1):55-60.
1999	Genant HK, Gordon C, Jiang Y, Lang TF, Link TM, Majumdar S. Advanced imaging of bone macro and micro structure. Bone. July 1999;25(1):149-152.
2009	Mueller TL, Stauber M, Kohler T, Eckstein F, Müller R, van Lenthe GH. Non-invasive bone competence analysis by high-resolution pQCT: an in vitro reproducibility study on structural and mechanical properties at the human radius. Bone. February 2009;44(2):364-371.
2010	Sode M, Burghardt AJ, Kazakia GJ, Link TM, Majumdar S. Regional variations of gender-specific and age-related differences in trabecular bone structure of the distal radius and tibia. Bone. June 2010;46(6):1652-1660.
2010	Burghardt AJ, Buie HR, Laib A, Majumdar S, Boyd SK. Reproducibility of direct quantitative measures of cortical bone microarchitecture of the distal radius and tibia by HR-pQCT. Bone. September 2010;47(3):519-528.
2011	Sode M, Burghardt AJ, Pialat J-B, Link TM, Majumdar S. Quantitative characterization of subject motion in HR-pQCT images of the distal radius and tibia. Bone. June 1, 2011;48(6):1291-1297.
2011	Engelke K, Süß C, Kalender WA. Stereolithographic models simulating trabecular bone and their characterization by thin-slice- and micro-CT. Eur Radiol. 2011;11(10):2026-2040.
1998	Lane NE, Thompson JM, Haupt D, Kimmel DB, Modin G, Kinney JH. Acute changes in trabecular bone connectivity and osteoclast activity in the ovariectomized rat in vivo. J Bone Miner Res. February 1998;13(2):229-236.
2002	Riggs BL, Melton LJ III. Bone turnover matters: the raloxifene treatment paradox of dramatic decreases in vertebral fractures without commensurate increases in bone density. J Bone Miner Res. January 2002;17(1):11-14.
2004	Waarsing JH, Day JS, Weinans H. An improved segmentation method for in vivo μCT imaging. J Bone Miner Res. 2004;19(10):1640-1650.
2006	Khosla S, Riggs BL, Atkinson EJ, Oberg AL, McDaniel LJ, Holets M, .Peterson JM, Melton LJ III. Effects of sex and age on bone microstructure at the ultradistal radius: a population-based noninvasive in vivo assessment. J Bone Miner Res. January 2006;21(1):124-131.
2007	Melton LJ, Riggs BL, van Lenthe GH, Achenbach SJ, Müller R, Bouxsein ML, Amin S, Atkinson EJ, Khosla S. Contribution of in vivo structural measurements and load/strength ratios to the determination of forearm fracture risk in postmenopausal women. J Bone Miner Res. September 2007;22(9):1442-1448.
2010	Burghardt AJ, Kazakia GJ, Ramachandran S, Link TM, Majumdar S. Age- and gender-related differences in the geometric properties and biomechanical significance of intracortical porosity in the distal radius and tibia. J Bone Miner Res. May 2010;25(5):983-993.
2008	Engelke K, Adams JE, Armbrecht G, Augat P, Bogado CE, Bouxsein ML, Felsenberg D, Ito M, Prevrhal S, Hans DB, Lewiecki EM. Clinical use of quantitative computed tomography and peripheral quantitative computed tomography in the management of osteoporosis in adults: the 2007 ISCD official positions. J Clin Densitom. January–March 2008;11(1):123-162.
2005	Boutroy S, Bouxsein ML, Munoz F, Delmas PD. In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab. December 2005;90(12):6508-6515.
1999	Majumdar S, Link TM, Augat P, Lin JC, Newitt D, Lan NE, Genant HK. Trabecular bone architecture in the distal radius using magnetic resonance imaging in subjects with fractures of the proximal femur. Osteoporos Int. 1999;10(3):231-239.
2012	Engelke K, Stampa B, Timm W, Dardzinski B, de Papp AE, Genant HK, Fuerst T. Short-term in vivo precision of BMD and parameters of trabecular architecture at the distal forearm and tibia. Osteoporos Int. August 2012;23(8):2151-2158.
2003	Bredbenner TL. Damage Modeling of Vertebral Trabecular Bone [PhD thesis]. Cleveland, OH: Case Western Reserve University; January 2003.
2007	Liu XS. High-Resolution Image Based Micro-Mechanical Modeling of Trabecular Bone [PhD thesis]. Columbia University; 2007.
1999	Laib A. Microarchitecture of the Human Radius Assessed With High Resolution in Vivo 3D-QCT [PhD thesis]. Swiss Federal Institute of Technology Zürich; 1999.
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.
2010	Müller T. Bioimaging and Biomechanics of Bone Competence and Implant Stability [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2010.
2011	Lambers FM. Functional Bone Imaging in an in Vivo Mouse Model of Bone Adaptation, Aging and Disease [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2011.
2013	Christen P. Deciphering the Secret Message Within Bone Microstructure [PhD thesis]. Eindhoven University of Technology; 2013.
2010	Alberich Bayarri Á. In Vivo Morphometric and Mechanical Characterization of Trabecular Bone from High Resolution Magnetic Resonance Imaging [PhD thesis]. Universität Politècnica de València; 2010.