Three‐dimensional nuclear magnetic resonance microimaging of trabecular bone

Chung, Hsiao‐Wen; Wehrli, Felix W.; Williams, John L.; Wehrli, Suzanne L.

Affiliations

¹Department of Radiology, University of Pennsylvania Medical Center, Philadelphia, Pennsylvania

²Present address: 448 Department of Electrical Engineering, National Taiwan University, Taipei, Taiwan, R.O.C.

³Department of Orthopedic Surgery, University of Pennsylvania Medical Center, Philadelphia, Pennsylvania

⁴Joseph Stokes Jr. Research Center, Children's Hospital of Philadelphia, Philadelphia, Pennsylvania

Abstract

The conventional approach to measuring structural parameters in trabecular bone rests on stereology from optical images, derived from sections of embedded bone. In order to provide data that are statistically representative of a sufficiently large volume, multiple sections need to be analyzed in each of the three orthogonal planes. In this work, an alternative technique is presented which is based on three‐dimensional (3D) volumetric proton nuclear magnetic resonance (NMR) microimaging. The method presented provides images from 9 × 9 × 4 mm³ volumes of defatted bone specimens in 15–20 minutes scan time at isotropic resolution corresponding to (78 μm)³ voxel size. Surface‐rendered images of bovine and human trabecular bone are shown and an algorithm was developed and implemented for determining the orientation and magnitude of the principal axes of the mean intercept length tensor.

Links

DOI: 10.1002/jbmr.5650101005

PubMed: 8686500

WoS: A1995RX78000004

History

Received: 1994-08-22

Revised: 1995-05-15

Accepted: 1995-06-15

Cited Works (24)

Year	Entry
1993	Snyder BD, Piazza S, Edwards WT, Hayes WC. Role of trabecular morphology in the etiology of age-related vertebral fractures. Calcif Tiss Int. February 1993;53(suppl 1):S14-S22.
1993	Goldstein SA, Goulet R, McCubbrey D. Measurement and significance of three-dimensional architecture to the mechanical integrity of trabecular bone. Calcif Tiss Int. February 1993;53(suppl 1):S127-S133.
1985	Gibson LJ. The mechanical behaviour of cancellous bone. J Biomech. 1985;18(5):317-328.
1990	Hodgskinson R, Currey JD. Effects of structural variation on Young's modulus of non-human cancellous bone. Proc Inst Mech Eng Part H-J Eng Med. 1990;204(1):43-52.
1974	Lanyon LE. Experimental support for the trajectorial theory of bone structure. J Bone Joint Surg. 1974;56B(1):160-166.
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.
1993	Dalstra M, Huiskes R, Odgaard A, van Erning L. Mechanical and textural properties of pelvic trabecular bone. J Biomech. April–May 1993;26(4-5):523-535.
1985	Kleerekoper M, Villanueva AR, Stanciu J, Rao DS, Parfitt AM. The role of three-dimensional trabecular microstructure in the pathogenesis of vertebral compression fractures. Calcif Tiss Int. 1985;37(6):594-597.
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.
1993	Chung H, Wehrli FW, Williams JL, Kugelmass SD. Relationship between NMR transverse relaxation, trabecular bone architecture, and strength. Proc Natl Acad Sci USA. November 1993;90(5):10250-10254.
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.
1994	Bonse U, Busch F, Günnewig O, Beckmann F, Pahl R, Delling G, Hahn M, Graeff W. 3D computed X-ray tomography of human cancellous bone at 8 μm spatial and 10⁻⁴ energy resolution. Bone Miner. April 1994;25(1):25-38.
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.
1983	Recker RR, ed. Bone Histomorphometry: Techniques and Interpretation. Boca Raton, FL: Inc., CRC Press; 1983.
1990	Turner CH, Cowin SC, Rho JY, Ashman RB, Rice JC. The fabric dependence of the orthotropic elastic constants of cancellous bone. J Biomech. 1990;23(6):549-561.
1983	Parfitt AM. Stereologic basis of bone histomorphometry: theory of quantitative micorscopy and reconstruction of the third dimension. In: Recker RR, ed. Bone Histomorphometry: Techniques and Interpretation. Boca Raton, FL: Inc., CRC Press; 1983:53-87.
1982	Williams JL, Lewis JL. Properties and an anisotropic model of cancellous bone from the proximal tibial epiphysis. J Biomech Eng. February 1982;104(1):50-56.
1974	Whitehouse WJ. The quantitative morphology of anisotropic trabecular bone. J Microsc (Oxford). July 1974;101:153-168.
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.
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.
1990	Mosekilde L. Consequences of the remodelling process for vertebral trabecular bone structure: a scanning electron microscopy study (uncoupling of unloaded structures). Bone Miner. July 1990;10(1):13-35.
1990	Kuhn JL, Goldstein SA, Feldkamp LA, Goulet RW, Jesion G. Evaluation of a microcomputed tomography system to study trabecular bone structure. J Orthop Res. 1990;8(6):833-842.
1985	Cowin SC. The relationship between the elasticity tensor and the fabric tensor. Mech Mater. 1985;4(2):137-147.
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.

Cited By (17)

Year	Entry
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.
2001	Rüegsegger P. Imaging of bone structure. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:9-1–9-24.
2001	Odgaard A. Quantification of cancellous bone architecture. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:14-1–14-19.
2001	Keaveny TM. Strength of trabecular bone. In: Cowin SC, ed. Bone Mechanics Handbook. 2nd ed. Boca Raton, FL: CRC Press; 2001:16-1–16-42.
1997	Beck JD, Canfield BL, Haddock SM, Chen TJH, Kothari M, Keaveny TM. Three-dimensional imaging of trabecular bone using the computer numerically controlled milling technique. Bone. 1997;21(3):281-287.
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.
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.
1997	Uchiyama T, Tanizawa T, Muramatsu H, Endo N, Takahashi HE, Hara T. A morphometric comparison of trabecular structure of human ilium between microcomputed tomography and conventional histomorphometry. Calcif Tiss Int. December 1997;61(6):493-498.
1997	Majumdar S, Genant HK. High resolution magnetic resonance imaging of trabecular structure. Eur Radiol. February 1997;7(suppl 2):S51-S55.
1998	Link TM, Majumdar S, Lin JC, Newitt D, Augat P, Ouyang X, Mathur A, Genant HK. A comparative study of trabecular bone properties in the spine and femur using high resolution mri and ct. J Bone Miner Res. January 1998;13(1):122-132.
1997	Hwang SN, Wehrli FW, Williams JL. Probability‐based structural parameters from three‐dimensional nuclear magnetic resonance images as predictors of trabecular bone strength. Med Phys. August 1997;24(8):1255-1261.
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.
2002	Newitt DC, van Rietbergen B, Majumdar S. Processing and analysis of in vivo high-resolution MR images of trabecular bone for longitudinal studies: reproducibility of structural measures and micro-finite element analysis derived mechanical properties. Osteoporos Int. 2002;13(4):278-287.
1998	Wehrli FW, Hwang SN, Ma J, Song HK, Ford JC, Haddad JG. Cancellous bone volume and structure in the forearm: noninvasive assessment with MR microimaging and image processing. Radiology. February 1998;206(2):347-357.
1998	Majumdar S. A review of magnetic resonance (MR) imaging of trabecular bone micro-architecture: contribution to the prediction of biomechanical properties and fracture prevalence. Technol Health Care. 1998;6(5-6):321-327.
2007	Schneider P. Ultrastructural Phenotyping of Murine Bone Using Synchrotron Micro- and Nano-Computed Tomography [PhD thesis]. Swiss Federal Institute of Technology Zürich; 2007.
2003	Fox JC. Biomechanics of the Proximal Femur: Role of Bone Distribution and Architecture [PhD thesis]. Berkeley, CA: Berkeley, University of California; 2003.