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      Assessing cortical bone mechanical properties using collagen proton fraction from ultrashort echo time magnetization transfer (UTE-MT) MRI modeling

      research-article
      a , a , b , a , c , d , e , f , c , a , b , a , *
      Bone Reports
      Elsevier
      MR, magnetic resonance, MRI, magnetic resonance imaging, 3D, three-dimensional, 3D-UTE, three-dimensional ultrashort echo time imaging, RF, radio frequency, FOV, field of view, MT, magnetization transfer, ROI, region of interest, TE, echo time, TR, repetition time, CT, computed tomography, μCT, micro-computed tomography, MMF, macromolecular proton fraction, T2MM, macromolecular T2, FA, flip angle, BMD, bone mineral density, PBS, phosphate-buffered saline, DEXA, dual-energy X-ray absorptiometry, Cortical bone, MRI, Ultrashort echo time, Mechanical properties, Bone microstructure, Magnetization transfer

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          Abstract

          Cortical bone shows as a signal void when using conventional clinical magnetic resonance imaging (MRI). Ultrashort echo time MRI (UTE-MRI) can acquire high signal from cortical bone, thus enabling quantitative assessments. Magnetization transfer (MT) imaging combined with UTE-MRI can indirectly assess protons in the organic matrix of bone. This study aimed to examine UTE-MT MRI techniques to estimate the mechanical properties of cortical bone. A total of 156 rectangular human cortical bone strips were harvested from the tibial and femoral midshafts of 43 donors (62 ± 22 years old, 62 specimens from females, 94 specimens from males). Bone specimens were scanned using UTE-MT sequences on a clinical 3 T MRI scanner and on a micro-computed tomography (μCT) scanner. A series of MT pulse saturation powers (400°, 600°, 800°) and frequency offsets (2, 5, 10, 20, 50 kHz) was used to measure the macromolecular fraction (MMF) utilizing a two-pool MT model. Failure mechanical properties of the bone specimens were measured using 4-point bending tests. MMF from MRI results showed significant strong correlations with cortical bone porosity (R = -0.72, P < 0.01) and bone mineral density (BMD) (R = +0.71, P < 0.01). MMF demonstrated significant moderate correlations with Young modulus, yield stress, and ultimate stress ( R = 0.60–0.61, P < 0.01). These results suggest that the two-pool UTE-MT model focusing on the organic matrix of bone can potentially serve as a novel tool to detect the variations of bone mechanical properties and intracortical porosity.

          Highlights

          • Correlations between two-pool UTE-MT MRI modeling and cortical bone mechanical properties was investigated.

          • UTE-MT MRI modeling showed significant moderate correlations with mechanical properties.

          • UTE-MT MRI also showed strong correlations with μCT-based bone porosity and BMD.

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          Most cited references28

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          A new method for the model-independent assessment of thickness in three-dimensional images

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            Design and analysis of a practical 3D cones trajectory.

            The 3D Cones k-space trajectory has many desirable properties for rapid and ultra-short echo time magnetic resonance imaging. An algorithm is presented that generates the 3D Cones gradient waveforms given a desired field of view and resolution. The algorithm enables a favorable trade-off between increases in readout time and decreases in the total number of required readouts. The resulting trajectory is very signal-to-noise ratio (SNR) efficient and has excellent aliasing properties. A rapid high-resolution ultra-short echo time imaging sequence is used to compare the 3D Cones trajectory to 3D projection reconstruction (3DPR) sampling schemes. For equivalent scan times, the 3D Cones trajectory has better SNR performance and fewer aliasing artifacts as compared to the 3DPR trajectory. Magn Reson Med, 2006. (c) 2006 Wiley-Liss, Inc.
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              The Role of Water Compartments in the Material Properties of Cortical Bone.

              Comprising ~20% of the volume, water is a key determinant of the mechanical behavior of cortical bone. It essentially exists in two general compartments: within pores and bound to the matrix. The amount of pore water-residing in the vascular-lacunar-canalicular space-primarily reflects intracortical porosity (i.e., open spaces within the matrix largely due to Haversian canals and resorption sites) and as such is inversely proportional to most mechanical properties of bone. Movement of water according to pressure gradients generated during dynamic loading likely confers hydraulic stiffening to the bone as well. Nonetheless, bound water is a primary contributor to the mechanical behavior of bone in that it is responsible for giving collagen the ability to confer ductility or plasticity to bone (i.e., allows deformation to continue once permanent damage begins to form in the matrix) and decreases with age along with fracture resistance. Thus, dehydration by air-drying or by solvents with less hydrogen bonding capacity causes bone to become brittle, but interestingly, it also increases stiffness and strength across the hierarchical levels of organization. Despite the importance of matrix hydration to fracture resistance, little is known about why bound water decreases with age in hydrated human bone. Using (1)H nuclear magnetic resonance (NMR), both bound and pore water concentrations in bone can be measured ex vivo because the proton relaxation times differ between the two water compartments, giving rise to two distinct signals. There are also emerging techniques to measure bound and pore water in vivo with magnetic resonance imaging (MRI). The NMR/MRI-derived bound water concentration is positively correlated with both the strength and toughness of hydrated bone and may become a useful clinical marker of fracture risk.
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                Author and article information

                Contributors
                Journal
                Bone Rep
                Bone Rep
                Bone Reports
                Elsevier
                2352-1872
                02 August 2019
                December 2019
                02 August 2019
                : 11
                : 100220
                Affiliations
                [a ]Department of Radiology, University of California, San Diego, CA 92093, USA
                [b ]Shiley Center for Orthopedic Research and Education at Scripps Clinic, La Jolla, CA 92037, USA
                [c ]Radiology Service, VA San Diego Healthcare System, San Diego, CA 92161, USA
                [d ]Research and Laboratories Sector, Saudi Food and Drug Authority, Riyadh 3292, Saudi Arabia
                [e ]Department of Bioengineering, University of California, San Diego, CA 92093, USA
                [f ]Department of Orthopaedic Surgery, University of California, San Diego, CA 92093, USA
                Author notes
                [* ]Corresponding author at: Department of Radiology, University of California, 9500 Gilman Drive, San Diego, CA 92093, USA. jiangdu@ 123456ucsd.edu
                Article
                S2352-1872(19)30026-9 100220
                10.1016/j.bonr.2019.100220
                6700521
                31440531
                85335eaf-c5e3-4ec2-a59e-9356fb7efacb
                © 2019 The Authors

                This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

                History
                : 26 July 2019
                : 2 August 2019
                Categories
                Article

                mr, magnetic resonance,mri, magnetic resonance imaging,3d, three-dimensional,3d-ute, three-dimensional ultrashort echo time imaging,rf, radio frequency,fov, field of view,mt, magnetization transfer,roi, region of interest,te, echo time,tr, repetition time,ct, computed tomography,μct, micro-computed tomography,mmf, macromolecular proton fraction,t2mm, macromolecular t2,fa, flip angle,bmd, bone mineral density,pbs, phosphate-buffered saline,dexa, dual-energy x-ray absorptiometry,cortical bone,mri,ultrashort echo time,mechanical properties,bone microstructure,magnetization transfer

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