Semin Musculoskelet Radiol 2024; 28(01): 062-077
DOI: 10.1055/s-0043-1776431
Review Article

Bone Biomarkers Based on Magnetic Resonance Imaging

1   Department of Radiology, University of California, San Diego, La Jolla, California
,
Hyungseok Jang
1   Department of Radiology, University of California, San Diego, La Jolla, California
,
Eric Y. Chang
1   Department of Radiology, University of California, San Diego, La Jolla, California
2   Research Service, Veterans Affairs San Diego Healthcare System, San Diego, California
,
Susan Bukata
3   Department of Orthopaedic Surgery, University of California, San Diego, La Jolla, California
,
Jiang Du
1   Department of Radiology, University of California, San Diego, La Jolla, California
2   Research Service, Veterans Affairs San Diego Healthcare System, San Diego, California
4   Department of Bioengineering, University of California, San Diego, La Jolla, California
,
Christine B. Chung
1   Department of Radiology, University of California, San Diego, La Jolla, California
2   Research Service, Veterans Affairs San Diego Healthcare System, San Diego, California
› Author Affiliations
Source of Funding The authors acknowledge grant support from the National Institutes of Health (K01AR080257, R01AR068987, R01AR062581, R01AR075825, R01AR078877, and 5P30AR073761) and Veterans Affairs Clinical Science and Rehabilitation R&D (I01CX001388, I01BX005952, and I01CX000625).

Abstract

Magnetic resonance imaging (MRI) is increasingly used to evaluate the microstructural and compositional properties of bone. MRI-based biomarkers can characterize all major compartments of bone: organic, water, fat, and mineral components. However, with a short apparent spin-spin relaxation time (T2*), bone is invisible to conventional MRI sequences that use long echo times. To address this shortcoming, ultrashort echo time MRI sequences have been developed to provide direct imaging of bone and establish a set of MRI-based biomarkers sensitive to the structural and compositional changes of bone. This review article describes the MRI-based bone biomarkers representing total water, pore water, bound water, fat fraction, macromolecular fraction in the organic matrix, and surrogates for mineral density. MRI-based morphological bone imaging techniques are also briefly described.



Publication History

Article published online:
08 February 2024

© 2024. Thieme. All rights reserved.

Thieme Medical Publishers, Inc.
333 Seventh Avenue, 18th Floor, New York, NY 10001, USA

 
  • References

  • 1 Clarke B. Normal bone anatomy and physiology. Clin J Am Soc Nephrol 2008; 3 (Suppl. 03) S131-S139
  • 2 Cowin SC. Bone poroelasticity. J Biomech 1999; 32 (03) 217-238
  • 3 Ritchie RO, Buehler MJ, Hansma P. Plasticity and toughness in bone. Phys Today 2009; 62 (06) 41-47
  • 4 Ott SM. Cortical or trabecular bone: what's the difference?. Am J Nephrol 2018; 47 (06) 373-375
  • 5 Macdonald HM, Nishiyama KK, Kang J, Hanley DA, Boyd SK. Age-related patterns of trabecular and cortical bone loss differ between sexes and skeletal sites: a population-based HR-pQCT study. J Bone Miner Res 2011; 26 (01) 50-62
  • 6 Wang X, Ni Q. Determination of cortical bone porosity and pore size distribution using a low field pulsed NMR approach. J Orthop Res 2003; 21 (02) 312-319
  • 7 Nyman JS, Ni Q, Nicolella DP, Wang X. Measurements of mobile and bound water by nuclear magnetic resonance correlate with mechanical properties of bone. Bone 2008; 42 (01) 193-199
  • 8 Horch RA, Nyman JS, Gochberg DF, Dortch RD, Does MD. Characterization of 1H NMR signal in human cortical bone for magnetic resonance imaging. Magn Reson Med 2010; 64 (03) 680-687
  • 9 Diaz E, Chung CB, Bae WC. et al. Ultrashort echo time spectroscopic imaging (UTESI): an efficient method for quantifying bound and free water. NMR Biomed 2012; 25 (01) 161-168
  • 10 Biswas R, Bae W, Diaz E. et al. Ultrashort echo time (UTE) imaging with bi-component analysis: bound and free water evaluation of bovine cortical bone subject to sequential drying. Bone 2012; 50 (03) 749-755
  • 11 Ong HH, Wright AC, Wehrli FW. Deuterium nuclear magnetic resonance unambiguously quantifies pore and collagen-bound water in cortical bone. J Bone Miner Res 2012; 27 (12) 2573-2581
  • 12 Du J, Bydder GM. Qualitative and quantitative ultrashort-TE MRI of cortical bone. NMR Biomed 2013; 26 (05) 489-506
  • 13 Teitelbaum SL. Bone resorption by osteoclasts. Science 2000; 289 (5484) 1504-1508
  • 14 Wu Y, Humphrey MB, Nakamura MC. Osteoclasts—the innate immune cells of the bone. Autoimmunity 2008; 41 (03) 183-194
  • 15 Cabral HWS, Andolphi BFG, Ferreira BVC. et al. The use of biomarkers in clinical osteoporosis. Rev Assoc Med Bras 2016; 62 (04) 368-376
  • 16 Kuo TR, Chen CH. Bone biomarker for the clinical assessment of osteoporosis: recent developments and future perspectives. Biomark Res 2017; 5 (01) 18
  • 17 Shetty S, Kapoor N, Bondu JD, Thomas N, Paul TV. Bone turnover markers: emerging tool in the management of osteoporosis. Indian J Endocrinol Metab 2016; 20 (06) 846-852
  • 18 Vasikaran S, Eastell R, Bruyère O. et al; IOF-IFCC Bone Marker Standards Working Group. Markers of bone turnover for the prediction of fracture risk and monitoring of osteoporosis treatment: a need for international reference standards. Osteoporos Int 2011; 22 (02) 391-420
  • 19 Edwards MH, Dennison EM, Aihie Sayer A, Fielding R, Cooper C. Osteoporosis and sarcopenia in older age. Bone 2015; 80: 126-130
  • 20 Kaplan SJ, Pham TN, Arbabi S. et al. Association of radiologic indicators of frailty with 1-year mortality in older trauma patients: opportunistic screening for sarcopenia and osteopenia. JAMA Surg 2017; 152 (02) e164604
  • 21 Zioupos P, Currey JD, Hamer AJ. The role of collagen in the declining mechanical properties of aging human cortical bone. J Biomed Mater Res 1999; 45 (02) 108-116
  • 22 Wang X, Shen X, Li X, Agrawal CM. Age-related changes in the collagen network and toughness of bone. Bone 2002; 31 (01) 1-7
  • 23 Nyman JS, Roy A, Shen X, Acuna RL, Tyler JH, Wang X. The influence of water removal on the strength and toughness of cortical bone. J Biomech 2006; 39 (05) 931-938
  • 24 Wehrli FW, Fernández-Seara MA. Nuclear magnetic resonance studies of bone water. Ann Biomed Eng 2005; 33 (01) 79-86
  • 25 Baffour FI, Glazebrook KN, Ferrero A. et al. Photon-counting detector CT for musculoskeletal imaging: a clinical perspective. AJR Am J Roentgenol 2023; 220 (04) 551-560
  • 26 Laugier P. Instrumentation for in vivo ultrasonic characterization of bone strength. IEEE Trans Ultrason Ferroelectr Freq Control 2008; 55 (06) 1179-1196
  • 27 Raum K, Grimal Q, Varga P, Barkmann R, Glüer CC, Laugier P. Ultrasound to assess bone quality. Curr Osteoporos Rep 2014; 12 (02) 154-162
  • 28 Jenson F, Padilla F, Bousson V, Bergot C, Laredo JD, Laugier P. In vitro ultrasonic characterization of human cancellous femoral bone using transmission and backscatter measurements: relationships to bone mineral density. J Acoust Soc Am 2006; 119 (01) 654-663
  • 29 Karjalainen JP, Riekkinen O, Kröger H. Pulse-echo ultrasound method for detection of post-menopausal women with osteoporotic BMD. Osteoporos Int 2018; 29 (05) 1193-1199
  • 30 Grimal Q, Laugier P. Quantitative ultrasound assessment of cortical bone properties beyond bone mineral density. IRBM 2019; 40 (01) 16-24
  • 31 Chin KY, Ima-Nirwana S. Calcaneal quantitative ultrasound as a determinant of bone health status: what properties of bone does it reflect?. Int J Med Sci 2013; 10 (12) 1778-1783
  • 32 Han S, Rho J, Medige J, Ziv I, Medige J. Ultrasound velocity and broadband attenuation over a wide range of bone mineral density. Osteoporos Int 1996; 6 (04) 291-296
  • 33 Lasschuit JWJ, Center JR, Greenfield JR, Tonks KTT. Comparison of calcaneal quantitative ultrasound and bone densitometry parameters as fracture risk predictors in type 2 diabetes mellitus. Diabet Med 2020; 37 (11) 1902-1909
  • 34 Yen CC, Lin WC, Wang TH. et al. Pre-screening for osteoporosis with calcaneus quantitative ultrasound and dual-energy X-ray absorptiometry bone density. Sci Rep 2021; 11 (01) 15709
  • 35 Schraders K, Zatta G, Kruger M. et al. Quantitative ultrasound and dual X-ray absorptiometry as indicators of bone mineral density in young women and nutritional factors affecting it. Nutrients 2019; 11 (10) 2336
  • 36 Casciaro S, Conversano F, Pisani P, Muratore M. New perspectives in echographic diagnosis of osteoporosis on hip and spine. Clin Cases Miner Bone Metab 2015; 12 (02) 142-150
  • 37 McCloskey EV, Kanis JA, Odén A. et al. Predictive ability of heel quantitative ultrasound for incident fractures: an individual-level meta-analysis. Osteoporos Int 2015; 26 (07) 1979-1987
  • 38 Yang L, Udall WJM, McCloskey EV, Eastell R. Distribution of bone density and cortical thickness in the proximal femur and their association with hip fracture in postmenopausal women: a quantitative computed tomography study. Osteoporos Int 2014; 25 (01) 251-263
  • 39 Ma YJ, Jerban S, Jang H, Chang D, Chang EY, Du J. Quantitative ultrashort echo time (UTE) magnetic resonance imaging of bone: an update. Front Endocrinol (Lausanne) 2020; 11 (01) 567417
  • 40 Jerban S, Chang DG, Ma Y, Jang H, Chang EY, Du J. An update in qualitative imaging of bone using ultrashort echo time magnetic resonance. Front Endocrinol (Lausanne) 2020; 11 (01) 555756
  • 41 Jerban S, Ma Y, Wei Z, Jang H, Chang EY, Du J. Quantitative magnetic resonance imaging of cortical and trabecular bone. Semin Musculoskelet Radiol 2020; 24 (04) 386-401
  • 42 Ma Y, Jang H, Jerban S. et al. Making the invisible visible-ultrashort echo time magnetic resonance imaging: technical developments and applications. Appl Phys Rev 2022; 9 (04) 041303
  • 43 Reichert ILH, Robson MD, Gatehouse PD. et al. Magnetic resonance imaging of cortical bone with ultrashort TE pulse sequences. Magn Reson Imaging 2005; 23 (05) 611-618
  • 44 Robson MD, Gatehouse PD, Bydder GM, Neubauer S. Human imaging of phosphorus in cortical and trabecular bone in vivo. Magn Reson Med 2004; 51 (05) 888-892
  • 45 Chang EY, Du J, Chung CB. UTE imaging in the musculoskeletal system. J Magn Reson Imaging 2015; 41 (04) 870-883
  • 46 Manhard MK, Nyman JS, Does MD. Advances in imaging approaches to fracture risk evaluation. Transl Res 2017; 181: 1-14
  • 47 Wehrli FW. Magnetic resonance of calcified tissues. J Magn Reson 2013; 229: 35-48
  • 48 Wehrli FW, Song HK, Saha PK, Wright AC. Quantitative MRI for the assessment of bone structure and function. NMR Biomed 2006; 19 (07) 731-764
  • 49 Majumdar S. Magnetic resonance imaging of trabecular bone structure. Top Magn Reson Imaging 2002; 13 (05) 323-334
  • 50 Sharma AK, Toussaint ND, Elder GJ. et al. Magnetic resonance imaging based assessment of bone microstructure as a non-invasive alternative to histomorphometry in patients with chronic kidney disease. Bone 2018; 114 (114) 14-21
  • 51 Chang G, Deniz CM, Honig S. et al. Feasibility of three-dimensional MRI of proximal femur microarchitecture at 3 Tesla using 26 receive elements without and with parallel imaging. J Magn Reson Imaging 2014; 40 (01) 229-238
  • 52 Han M, Chiba K, Banerjee S, Carballido-Gamio J, Krug R. Variable flip angle three-dimensional fast spin-echo sequence combined with outer volume suppression for imaging trabecular bone structure of the proximal femur. J Magn Reson Imaging 2015; 41 (05) 1300-1310
  • 53 Wehrli FW. Structural and functional assessment of trabecular and cortical bone by micro magnetic resonance imaging. J Magn Reson Imaging 2007; 25 (02) 390-409
  • 54 Du J, Hermida JC, Diaz E. et al. Assessment of cortical bone with clinical and ultrashort echo time sequences. Magn Reson Med 2013; 70 (03) 697-704
  • 55 Bae WC, Patil S, Biswas R. et al. Magnetic resonance imaging assessed cortical porosity is highly correlated with μCT porosity. Bone 2014; 66: 56-61
  • 56 Bydder M, Carl M, Bydder GM, Du J. MRI chemical shift artifact produced by center-out radial sampling of k-space: a potential pitfall in clinical diagnosis. Quant Imaging Med Surg 2021; 11 (08) 3677-3683
  • 57 Manhard MK, Horch RA, Gochberg DF, Nyman JS, Does MD. In vivo quantitative MR imaging of bound and pore water in cortical bone. Radiology 2015; 277 (01) 221-229
  • 58 Zhao X, Song HK, Seifert AC, Li C, Wehrli FW. Feasibility of assessing bone matrix and mineral properties in vivo by combined solid-state 1H and 31P MRI. PLoS One 2017; 12 (03) e0173995
  • 59 Du J, Carl M, Bydder M, Takahashi A, Chung CB, Bydder GM. Qualitative and quantitative ultrashort echo time (UTE) imaging of cortical bone. J Magn Reson 2010; 207 (02) 304-311
  • 60 Li C, Seifert AC, Rad HS. et al. Cortical bone water concentration: dependence of MR imaging measures on age and pore volume fraction. Radiology 2014; 272 (03) 796-806
  • 61 Rad HS, Lam SCB, Magland JF. et al. Quantifying cortical bone water in vivo by three-dimensional ultra-short echo-time MRI. NMR Biomed 2011; 24 (07) 855-864
  • 62 Seifert AC, Wehrli FW. Solid-state quantitative (1)H and (31)P MRI of cortical bone in humans. Curr Osteoporos Rep 2016; 14 (03) 77-86
  • 63 Techawiboonwong A, Song HK, Leonard MB, Wehrli FW. Cortical bone water: in vivo quantification with ultrashort echo-time MR imaging. Radiology 2008; 248 (03) 824-833
  • 64 Jerban S, Ma Y, Li L. et al. Volumetric mapping of bound and pore water as well as collagen protons in cortical bone using 3D ultrashort echo time cones MR imaging techniques. Bone 2019; 127 (Oct): 120-128
  • 65 Jerban S, Ma Y, Jang H. et al. Water proton density in human cortical bone obtained from ultrashort echo time (UTE) MRI predicts bone microstructural properties. Magn Reson Imaging 2020; 67 (01) 85-89
  • 66 Jones BC, Wehrli FW, Kamona N. et al. Automated, calibration-free quantification of cortical bone porosity and geometry in postmenopausal osteoporosis from ultrashort echo time MRI and deep learning. Bone 2023; 171: 116743
  • 67 Ma YJ, Lu X, Carl M. et al. Accurate T1 mapping of short T2 tissues using a three-dimensional ultrashort echo time cones actual flip angle imaging-variable repetition time (3D UTE-Cones AFI-VTR) method. Magn Reson Med 2018; 80 (02) 598-608
  • 68 Du J, Takahashi AM, Bae WC, Chung CB, Bydder GM. Dual inversion recovery, ultrashort echo time (DIR UTE) imaging: creating high contrast for short-T(2) species. Magn Reson Med 2010; 63 (02) 447-455
  • 69 Horch RA, Gochberg DF, Nyman JS, Does MD. Clinically compatible MRI strategies for discriminating bound and pore water in cortical bone. Magn Reson Med 2012; 68 (06) 1774-1784
  • 70 Lombardi AF, Ma YJ, Jang H. et al. Synthetic CT in musculoskeletal disorders: a systematic review. Invest Radiol 2023; 58 (01) 43-59
  • 71 Du J, Chiang AJT, Chung CB. et al. Orientational analysis of the Achilles tendon and enthesis using an ultrashort echo time spectroscopic imaging sequence. Magn Reson Imaging 2010; 28 (02) 178-184
  • 72 Manhard MK, Uppuganti S, Granke M, Gochberg DF, Nyman JS, Does MD. MRI-derived bound and pore water concentrations as predictors of fracture resistance. Bone 2016; 87: 1-10
  • 73 Chen J, Grogan SP, Shao H. et al. Evaluation of bound and pore water in cortical bone using ultrashort-TE MRI. NMR Biomed 2015; 28 (12) 1754-1762
  • 74 Abbasi-Rad S, Saligheh Rad H. Quantification of human cortical bone bound and free water in vivo with ultrashort echo time MR imaging: a model-based approach. Radiology 2017; 283 (03) 862-872
  • 75 Wurnig MC, Calcagni M, Kenkel D. et al. Characterization of trabecular bone density with ultra-short echo-time MRI at 1.5, 3.0 and 7.0 T—comparison with micro-computed tomography. NMR Biomed 2014; 27 (10) 1159-1166
  • 76 Ma YJ, Chen Y, Li L. et al. Trabecular bone imaging using a 3D adiabatic inversion recovery prepared ultrashort TE Cones sequence at 3T. Magn Reson Med 2020; 83 (05) 1640-1651
  • 77 Jerban S, Ma Y, Moazamian D. et al. MRI-based porosity index (PI) and suppression ratio (SR) in the tibial cortex show significant differences between normal, osteopenic, and osteoporotic female subjects. Front Endocrinol (Lausanne) 2023; 14: 1148345
  • 78 Jerban S, Ma Y, Alenezi S. et al. Ultrashort echo time (UTE) MRI porosity index (PI) and suppression ratio (SR) correlate with the cortical bone microstructural and mechanical properties: ex vivo study. Bone 2023; 169: 116676
  • 79 Rajapakse CS, Bashoor-Zadeh M, Li C, Sun W, Wright AC, Wehrli FW. Volumetric cortical bone porosity assessment with MR imaging: validation and clinical feasibility. Radiology 2015; 276 (02) 526-535
  • 80 Hong AL, Ispiryan M, Padalkar MV. et al. MRI-derived bone porosity index correlates to bone composition and mechanical stiffness. Bone Rep 2019; 11 (February): 100213
  • 81 Bae WC, Chen PC, Chung CB, Masuda K, D'Lima D, Du J. Quantitative ultrashort echo time (UTE) MRI of human cortical bone: correlation with porosity and biomechanical properties. J Bone Miner Res 2012; 27 (04) 848-857
  • 82 Jerban S, Ma Y, Dorthe EW. et al. Assessing cortical bone mechanical properties using collagen proton fraction from ultrashort echo time magnetization transfer (UTE-MT) MRI modeling. Bone Rep 2019; 11 (02) 100220
  • 83 Jerban S, Ma Y, Wong JH. et al. Ultrashort echo time magnetic resonance imaging (UTE-MRI) of cortical bone correlates well with histomorphometric assessment of bone microstructure. Bone 2019; 123 (123) 8-17
  • 84 Seifert AC, Wehrli SL, Wehrli FW. Bi-component T2 * analysis of bound and pore bone water fractions fails at high field strengths. NMR Biomed 2015; 28 (07) 861-872
  • 85 Du J, Bydder M, Takahashi AM, Chung CB. Two-dimensional ultrashort echo time imaging using a spiral trajectory. Magn Reson Imaging 2008; 26 (03) 304-312
  • 86 Nazaran A, Carl M, Ma Y. et al. Three-dimensional adiabatic inversion recovery prepared ultrashort echo time cones (3D IR-UTE-Cones) imaging of cortical bone in the hip. Magn Reson Imaging 2017; 44 (Dec): 60-64
  • 87 Li S, Ma L, Chang EY. et al. Effects of inversion time on inversion recovery prepared ultrashort echo time (IR-UTE) imaging of bound and pore water in cortical bone. NMR Biomed 2015; 28 (01) 70-78
  • 88 Ma YJ, Jerban S, Jang H, Chang EY, Du J. Fat suppression for ultrashort echo time imaging using a novel soft-hard composite radiofrequency pulse. Magn Reson Med 2019; 82 (06) 2178-2187
  • 89 Jang H, Carl M, Ma Y. et al. Fat suppression for ultrashort echo time imaging using a single-point Dixon method. NMR Biomed 2019; 32 (05) e4069
  • 90 Lu X, Jerban S, Wan L. et al. Three-dimensional ultrashort echo time imaging with tricomponent analysis for human cortical bone. Magn Reson Med 2019; 82 (01) 348-355
  • 91 Jerban S, Lu X, Dorthe EW. et al. Correlations of cortical bone microstructural and mechanical properties with water proton fractions obtained from ultrashort echo time (UTE) MRI tricomponent T2* model. NMR Biomed 2020; 33 (03) e4233
  • 92 Ma YJ, Chang EY, Bydder GM, Du J. Can ultrashort-TE (UTE) MRI sequences on a 3-T clinical scanner detect signal directly from collagen protons: freeze-dry and D2 O exchange studies of cortical bone and Achilles tendon specimens. NMR Biomed 2016; 29 (07) 912-917
  • 93 Ma YJ, Chang EY, Carl M, Du J. Quantitative magnetization transfer ultrashort echo time imaging using a time-efficient 3D multispoke Cones sequence. Magn Reson Med 2018; 79 (02) 692-700
  • 94 Jerban S, Ma Y, Wan L. et al. Collagen proton fraction from ultrashort echo time magnetization transfer (UTE-MT) MRI modelling correlates significantly with cortical bone porosity measured with micro-computed tomography (μCT). NMR Biomed 2019; 32 (02) e4045
  • 95 Chang EY, Bae WC, Shao H. et al. Ultrashort echo time magnetization transfer (UTE-MT) imaging of cortical bone. NMR Biomed 2015; 28 (07) 873-880
  • 96 Dimov AV, Liu Z, Spincemaille P, Prince MR, Du J, Wang Y. Bone quantitative susceptibility mapping using a chemical species-specific R2* signal model with ultrashort and conventional echo data. Magn Reson Med 2018; 79 (01) 121-128
  • 97 Jerban S, Lu X, Jang H. et al. Significant correlations between human cortical bone mineral density and quantitative susceptibility mapping (QSM) obtained with 3D Cones ultrashort echo time magnetic resonance imaging (UTE-MRI). Magn Reson Imaging 2019; 62 (October): 104-110
  • 98 Seifert AC, Li C, Rajapakse CS. et al. Bone mineral (31)P and matrix-bound water densities measured by solid-state (31)P and (1)H MRI. NMR Biomed 2014; 27 (07) 739-748
  • 99 Anumula S, Wehrli SL, Magland J, Wright AC, Wehrli FW. Ultra-short echo-time MRI detects changes in bone mineralization and water content in OVX rat bone in response to alendronate treatment. Bone 2010; 46 (05) 1391-1399
  • 100 Anumula S, Magland J, Wehrli SL. et al. Measurement of phosphorus content in normal and osteomalacic rabbit bone by solid-state 3D radial imaging. Magn Reson Med 2006; 56 (05) 946-952
  • 101 Anumula S, Magland J, Wehrli SL, Ong H, Song HK, Wehrli FW. Multi-modality study of the compositional and mechanical implications of hypomineralization in a rabbit model of osteomalacia. Bone 2008; 42 (02) 405-413
  • 102 Jones BC, Lee H, Cheng CC. et al. MRI quantification of cortical bone porosity, mineralization, and morphologic structure in postmenopausal osteoporosis. Radiology 2023; 307 (02) e221810
  • 103 Majumdar S, Thomasson D, Shimakawa A, Genant HK. Quantitation of the susceptibility difference between trabecular bone and bone marrow: experimental studies. Magn Reson Med 1991; 22 (01) 111-127
  • 104 Ford JC, Wehrli FW. In vivo quantitative characterization of trabecular bone by NMR interferometry and localized proton spectroscopy. Magn Reson Med 1991; 17 (02) 543-551
  • 105 Diefenbach MN, Meineke J, Ruschke S, Baum T, Gersing A, Karampinos DC. On the sensitivity of quantitative susceptibility mapping for measuring trabecular bone density. Magn Reson Med 2019; 81 (03) 1739-1754
  • 106 Majumdar S, Genant HK. A review of the recent advances in magnetic resonance imaging in the assessment of osteoporosis. Osteoporos Int 1995; 5 (02) 79-92
  • 107 Beuf O, Newitt DC, Mosekilde L, Majumdar S. Trabecular structure assessment in lumbar vertebrae specimens using quantitative magnetic resonance imaging and relationship with mechanical competence. J Bone Miner Res 2001; 16 (08) 1511-1519
  • 108 Link TM, Majumdar S, Augat P. et al. Proximal femur: assessment for osteoporosis with T2* decay characteristics at MR imaging. Radiology 1998; 209 (02) 531-536
  • 109 Chen Y, Guo Y, Zhang X, Mei Y, Feng Y, Zhang X. Bone susceptibility mapping with MRI is an alternative and reliable biomarker of osteoporosis in postmenopausal women. Eur Radiol 2018; 28 (12) 5027-5034
  • 110 Griffith JF, Yeung DKW, Antonio GE. et al. Vertebral bone mineral density, marrow perfusion, and fat content in healthy men and men with osteoporosis: dynamic contrast-enhanced MR imaging and MR spectroscopy. Radiology 2005; 236 (03) 945-951
  • 111 Shih TTF, Chang CJ, Hsu CY, Wei SY, Su KC, Chung HW. Correlation of bone marrow lipid water content with bone mineral density on the lumbar spine. Spine 2004; 29 (24) 2844-2850
  • 112 Griffith JF, Yeung DKW, Antonio GE. et al. Vertebral marrow fat content and diffusion and perfusion indexes in women with varying bone density: MR evaluation. Radiology 2006; 241 (03) 831-838
  • 113 Griffith JF, Yeung DKW, Ma HT, Leung JCS, Kwok TCY, Leung PC. Bone marrow fat content in the elderly: a reversal of sex difference seen in younger subjects. J Magn Reson Imaging 2012; 36 (01) 225-230
  • 114 Li X, Kuo D, Schafer AL. et al. Quantification of vertebral bone marrow fat content using 3 Tesla MR spectroscopy: reproducibility, vertebral variation, and applications in osteoporosis. J Magn Reson Imaging 2011; 33 (04) 974-979
  • 115 Mostoufi-Moab S, Magland J, Isaacoff EJ. et al. Adverse fat depots and marrow adiposity are associated with skeletal deficits and insulin resistance in long-term survivors of pediatric hematopoietic stem cell transplantation. J Bone Miner Res 2015; 30 (09) 1657-1666
  • 116 Karampinos DC, Melkus G, Baum T, Bauer JS, Rummeny EJ, Krug R. Bone marrow fat quantification in the presence of trabecular bone: initial comparison between water-fat imaging and single-voxel MRS. Magn Reson Med 2014; 71 (03) 1158-1165
  • 117 Gee CS, Nguyen JTK, Marquez CJ. et al. Validation of bone marrow fat quantification in the presence of trabecular bone using MRI. J Magn Reson Imaging 2015; 42 (02) 539-544
  • 118 Reeder SB, Robson PM, Yu H. et al. Quantification of hepatic steatosis with MRI: the effects of accurate fat spectral modeling. J Magn Reson Imaging 2009; 29 (06) 1332-1339
  • 119 Yu H, Shimakawa A, McKenzie CA, Brodsky E, Brittain JH, Reeder SB. Multiecho water-fat separation and simultaneous R2* estimation with multifrequency fat spectrum modeling. Magn Reson Med 2008; 60 (05) 1122-1134
  • 120 Akbari A, Abbasi-Rad S, Rad HS. T1 correlates age: a short-TE MR relaxometry study in vivo on human cortical bone free water at 1.5T. Bone 2016; 83: 17-22
  • 121 Du J, Bydder M, Takahashi AM, Carl M, Chung CB, Bydder GM. Short T2 contrast with three-dimensional ultrashort echo time imaging. Magn Reson Imaging 2011; 29 (04) 470-482
  • 122 Johnson EM, Vyas U, Ghanouni P, Pauly KB, Pauly JM. Improved cortical bone specificity in UTE MR imaging. Magn Reson Med 2017; 77 (02) 684-695
  • 123 Breighner RE, Endo Y, Konin GP, Gulotta LV, Koff MF, Potter HG. Zero echo time imaging of the shoulder: enhanced osseous detail by using MR imaging. Radiology 2018; 286 (03) 960-966
  • 124 Weiger M, Pruessmann KP. MRI with zero echo time. Encyclopedia of Magnetic Resonance 2012; 1 (02) 311-322
  • 125 Garwood M, Idiyatullin D, Corum CA. et al. Capturing signals from fast-relaxing spins with frequency-swept MRI: SWIFT. Encyclopedia of Magnetic Resonance 2012; 1 (02) 322-332
  • 126 Grodzki DM, Jakob PM, Heismann B. Ultrashort echo time imaging using pointwise encoding time reduction with radial acquisition (PETRA). Magn Reson Med 2012; 67 (02) 510-518
  • 127 Weiger M, Wu M, Wurnig MC. et al. ZTE imaging with long-T2 suppression. NMR Biomed 2015; 28 (02) 247-254
  • 128 Du J, Takahashi AM, Chung CB. Ultrashort TE spectroscopic imaging (UTESI): application to the imaging of short T2 relaxation tissues in the musculoskeletal system. J Magn Reson Imaging 2009; 29 (02) 412-421
  • 129 Nyman JS, Gorochow LE, Adam Horch R. et al. Partial removal of pore and loosely bound water by low-energy drying decreases cortical bone toughness in young and old donors. J Mech Behav Biomed Mater 2013; 22: 136-145
  • 130 Ma YJ, West J, Nazaran A. et al. Feasibility of using an inversion-recovery ultrashort echo time (UTE) sequence for quantification of glenoid bone loss. Skeletal Radiol 2018; 47 (07) 973-980
  • 131 Du J, Carl M, Bae WC. et al. Dual inversion recovery ultrashort echo time (DIR-UTE) imaging and quantification of the zone of calcified cartilage (ZCC). Osteoarthritis Cartilage 2013; 21 (01) 77-85
  • 132 Garwood M, DelaBarre L. The return of the frequency sweep: designing adiabatic pulses for contemporary NMR. J Magn Reson 2001; 153 (02) 155-177
  • 133 Ma YJ, Zhu Y, Lu X, Carl M, Chang EY, Du J. Short T2 imaging using a 3D double adiabatic inversion recovery prepared ultrashort echo time cones (3D DIR-UTE-Cones) sequence. Magn Reson Med 2018; 79 (05) 2555-2563
  • 134 Wu Y, Ackerman JL, Chesler DA, Graham L, Wang Y, Glimcher MJ. Density of organic matrix of native mineralized bone measured by water- and fat-suppressed proton projection MRI. Magn Reson Med 2003; 50 (01) 59-68
  • 135 Cao H, Ackerman JL, Hrovat MI, Graham L, Glimcher MJ, Wu Y. Quantitative bone matrix density measurement by water- and fat-suppressed proton projection MRI (WASPI) with polymer calibration phantoms. Magn Reson Med 2008; 60 (06) 1433-1443
  • 136 Cao H, Nazarian A, Ackerman JL. et al. Quantitative (31)P NMR spectroscopy and (1)H MRI measurements of bone mineral and matrix density differentiate metabolic bone diseases in rat models. Bone 2010; 46 (06) 1582-1590
  • 137 Wu Y, Hrovat MI, Ackerman JL. et al. Bone matrix imaged in vivo by water- and fat-suppressed proton projection MRI (WASPI) of animal and human subjects. J Magn Reson Imaging 2010; 31 (04) 954-963
  • 138 Techawiboonwong A, Song HK, Wehrli FW. In vivo MRI of submillisecond T(2) species with two-dimensional and three-dimensional radial sequences and applications to the measurement of cortical bone water. NMR Biomed 2008; 21 (01) 59-70
  • 139 Li S, Chang EY, Bae WC. et al. Ultrashort echo time bi-component analysis of cortical bone–a field dependence study. Magn Reson Med 2014; 71 (03) 1075-1081
  • 140 Jerban S, Szeverenyi N, Ma Y. et al. Ultrashort echo time MRI (UTE-MRI) quantifications of cortical bone varied significantly at body temperature compared with room temperature. Investig Magn Reson Imaging 2019; 23 (03) 202
  • 141 Jerban S, Ma Y, Nazaran A. et al. Detecting stress injury (fatigue fracture) in fibular cortical bone using quantitative ultrashort echo time-magnetization transfer (UTE-MT): An ex vivo study. NMR Biomed 2018; 31 (11) e3994
  • 142 Techawiboonwong A, Song HK, Magland JF, Saha PK, Wehrli FW. Implications of pulse sequence in structural imaging of trabecular bone. J Magn Reson Imaging 2005; 22 (05) 647-655