MRI of the Musculoskeletal System: Advanced Applications using High and Ultrahigh Field MRI

 

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Abstract

In vivo MRI has revolutionized the diagnosis and treatment of musculoskeletal disorders over the past 3 decades. Traditionally performed at 1.5 T, MRI at higher field strengths offers several advantages over lower field strengths including increased signal-to-noise ratio, higher spatial resolution, improved spectral resolution for spectroscopy, improved sensitivity for X-nucleus imaging, and decreased image acquisition times. However, the physics of imaging at higher field strengths also presents technical challenges. These include B₀ and B₁₊ field inhomogeneity, design and construction of dedicated radiofrequency (RF) coils for use at high field, increased chemical shift and susceptibility artifacts, increased RF energy deposition (specific absorption rate), increased metal artifacts, and changes in relaxation times compared with the lower field scanners. These challenges were overcome in optimizing high-field (HF) (3 T) MRI over a decade ago. HF MRI systems have since gained universal acceptance for clinical musculoskeletal imaging and have also been widely utilized for the study of musculoskeletal anatomy and physiology. Recently there has been an increasing interest in exploring musculoskeletal applications of ultrahigh field (UHF) (7 T) systems. However, technical challenges similar to those encountered when moving from 1.5 T to 3 T have to be overcome to optimize 7 T musculoskeletal imaging. In this narrative review, we discuss the many potential opportunities and technical challenges presented by the HF and UHF MRI systems. We highlight recent developments in in vivo imaging of musculoskeletal tissues that benefit most from HF imaging including cartilage, skeletal muscle, and bone.

• References

• 1 Runge VM. Highfield MRI—the new clinical standard?. Invest Radiol 2009; 44 (9) 491
  CrossrefPubMedGoogle Scholar
• 2 Collins C. Radiofrequency field calculations for high field MRI. In: Ultra High Field Magnetic Resonance Imaging. Robitaille PM, Berliner LJ, , eds. New York, NY: Springer; 2006: 209-248
  CrossrefGoogle Scholar
• 3 Moser E, Stahlberg F, Ladd ME, Trattnig S. 7-T MR—from research to clinical applications?. NMR Biomed 2012; 25 (5) 695-716
  CrossrefPubMedGoogle Scholar
• 4 Krug R, Stehling C, Kelley DA, Majumdar S, Link TM. Imaging of the musculoskeletal system in vivo using ultra-high field magnetic resonance at 7 T. Invest Radiol 2009; 44 (9) 613-618
  CrossrefPubMedGoogle Scholar
• 5 Wiesinger F, Van de Moortele P-F, Adriany G, De Zanche N, Ugurbil K, Pruessmann KP. Potential and feasibility of parallel MRI at high field. NMR Biomed 2006; 19 (3) 368-378
  CrossrefPubMedGoogle Scholar
• 6 Scheenen TW, Heerschap A, Klomp DW. Towards 1H-MRSI of the human brain at 7T with slice-selective adiabatic refocusing pulses. MAGMA 2008; 21 (1–2) 95-101
  CrossrefPubMedGoogle Scholar
• 7 Staroswiecki E, Bangerter NK, Gurney PT, Grafendorfer T, Gold GE, Hargreaves BA. In vivo sodium imaging of human patellar cartilage with a 3D cones sequence at 3 T and 7 T. J Magn Reson Imaging 2010; 32 (2) 446-451
  CrossrefPubMedGoogle Scholar
• 8 Meyerspeer M, Robinson S, Nabuurs CI , et al. Comparing localized and nonlocalized dynamic 31P magnetic resonance spectroscopy in exercising muscle at 7 T. Magn Reson Med 2012; 68 (6) 1713-1723
  CrossrefPubMedGoogle Scholar
• 9 Van de Moortele P-F, Akgun C, Adriany G , et al. B(1) destructive interferences and spatial phase patterns at 7 T with a head transceiver array coil. Magn Reson Med 2005; 54 (6) 1503-1518
  CrossrefPubMedGoogle Scholar
• 10 Chang G, Wang L, Cárdenas-Blanco A, Schweitzer ME, Recht MP, Regatte RR. Biochemical and physiological MR imaging of skeletal muscle at 7 tesla and above. Semin Musculoskelet Radiol 2010; 14 (2) 269-278
  Article in Thieme ConnectPubMedGoogle Scholar
• 11 Setsompop K, Alagappan V, Zelinski AC , et al. High-flip-angle slice-selective parallel RF transmission with 8 channels at 7 T. J Magn Reson 2008; 195 (1) 76-84
  CrossrefPubMedGoogle Scholar
• 12 Hsu YC, Chu YH, Chern IL, Lattanzi R, Huang TY, Lin FH. Mitigate B₁(+) inhomogeneity by nonlinear gradients and RF shimming. Conf Proc IEEE Eng Med Biol Soc 2013; 2013: 1085-1088
  PubMedGoogle Scholar
• 13 Jordan CD, Saranathan M, Bangerter NK, Hargreaves BA, Gold GE. Musculoskeletal MRI at 3.0 T and 7.0 T: a comparison of relaxation times and image contrast. Eur J Radiol 2013; 82 (5) 734-739
  CrossrefPubMedGoogle Scholar
• 14 Pruessmann KP. Parallel imaging at high field strength: synergies and joint potential. Top Magn Reson Imaging 2004; 15 (4) 237-244
  CrossrefPubMedGoogle Scholar
• 15 Sengupta S, Welch EB, Zhao Y , et al. Dynamic B0 shimming at 7 T. Magn Reson Imaging 2011; 29 (4) 483-496
  CrossrefPubMedGoogle Scholar
• 16 Regatte RR, Schweitzer ME. Ultra-high-field MRI of the musculoskeletal system at 7.0T. J Magn Reson Imaging 2007; 25 (2) 262-269
  CrossrefPubMedGoogle Scholar
• 17 Balchandani P, Spielman D. Fat suppression for 1H MRSI at 7T using spectrally selective adiabatic inversion recovery. Magn Reson Med 2008; 59 (5) 980-988
  CrossrefPubMedGoogle Scholar
• 18 Schuster C, Dreher W, Stadler J, Bernarding J, Leibfritz D. Fast three-dimensional 1H MR spectroscopic imaging at 7 Tesla using “spectroscopic missing pulse—SSFP”. Magn Reson Med 2008; 60 (5) 1243-1249
  CrossrefPubMedGoogle Scholar
• 19 U.S. Department of Health and Human Services FaDA, Center for Devices and Radiological Health, Guidance for Industry and FDA Staff Criteria for Significant Risk Investigations of Magnetic Resonance Diagnostic Devices, July 14, 2003. Available at: http://www.fda.gov/downloads/medicaldevices/deviceregulationandguidance/guidancedocuments/ucm072688.pdf . Accessed September 1, 2015
  PubMed
• 20 Chakeres DW, Kangarlu A, Boudoulas H, Young DC. Effect of static magnetic field exposure of up to 8 Tesla on sequential human vital sign measurements. J Magn Reson Imaging 2003; 18 (3) 346-352
  CrossrefPubMedGoogle Scholar
• 21 de Vocht F, Stevens T, Glover P, Sunderland A, Gowland P, Kromhout H. Cognitive effects of head-movements in stray fields generated by a 7 Tesla whole-body MRI magnet. Bioelectromagnetics 2007; 28 (4) 247-255
  CrossrefPubMedGoogle Scholar
• 22 Binks DA, Hodgson RJ, Ries ME , et al. Quantitative parametric MRI of articular cartilage: a review of progress and open challenges. Br J Radiol 2013; 86 (1023) 20120163
  CrossrefPubMedGoogle Scholar
• 23 Sophia Fox AJ, Bedi A, Rodeo SA. The basic science of articular cartilage: structure, composition, and function. Sports Health 2009; 1 (6) 461-468
  CrossrefPubMedGoogle Scholar
• 24 Buckwalter JA, Mankin HJ. Articular cartilage: degeneration and osteoarthritis, repair, regeneration, and transplantation. Instr Course Lect 1998; 47: 487-504
  PubMedGoogle Scholar
• 25 Rubenstein JD, Li JG, Majumdar S, Henkelman RM. Image resolution and signal-to-noise ratio requirements for MR imaging of degenerative cartilage. AJR Am J Roentgenol 1997; 169 (4) 1089-1096
  CrossrefPubMedGoogle Scholar
• 26 Crema MD, Roemer FW, Marra MD , et al. Articular cartilage in the knee: current MR imaging techniques and applications in clinical practice and research. Radiographics 2011; 31 (1) 37-61
  CrossrefPubMedGoogle Scholar
• 27 Bobic V ; ICRS Articular Cartilage Imaging Committee. ICRS MR Imaging Protocol for Knee Articular Cartilage. Zollikon, Switzerland: International Cartilage Repair Society; 2000: 12
  Google Scholar
• 28 Mugler III JP. Optimized three-dimensional fast-spin-echo MRI. J Magn Reson Imaging 2014; 39 (4) 745-767
  CrossrefPubMedGoogle Scholar
• 29 Kijowski R, Davis KW, Woods MA , et al. Knee joint: comprehensive assessment with 3D isotropic resolution fast spin-echo MR imaging—diagnostic performance compared with that of conventional MR imaging at 3.0 T. Radiology 2009; 252 (2) 486-495
  CrossrefPubMedGoogle Scholar
• 30 Mohr A. The value of water-excitation 3D FLASH and fat-saturated PDw TSE MR imaging for detecting and grading articular cartilage lesions of the knee. Skeletal Radiol 2003; 32 (7) 396-402
  CrossrefPubMedGoogle Scholar
• 31 Blankenbaker DG, Ullrick SR, Kijowski R , et al. MR arthrography of the hip: comparison of IDEAL-SPGR volume sequence to standard MR sequences in the detection and grading of cartilage lesions. Radiology 2011; 261 (3) 863-871
  CrossrefPubMedGoogle Scholar
• 32 Duc SR, Pfirrmann CW, Schmid MR , et al. Articular cartilage defects detected with 3D water-excitation true FISP: prospective comparison with sequences commonly used for knee imaging. Radiology 2007; 245 (1) 216-223
  CrossrefPubMedGoogle Scholar
• 33 Juras V, Welsch G, Bär P, Kronnerwetter C, Fujita H, Trattnig S. Comparison of 3T and 7T MRI clinical sequences for ankle imaging. Eur J Radiol 2012; 81 (8) 1846-1850
  CrossrefPubMedGoogle Scholar
• 34 Friedrich KM, Chang G, Vieira RL , et al. In vivo 7.0-tesla magnetic resonance imaging of the wrist and hand: technical aspects and applications. Semin Musculoskelet Radiol 2009; 13 (1) 74-84
  Article in Thieme ConnectPubMedGoogle Scholar
• 35 Liess C, Lüsse S, Karger N, Heller M, Glüer CC. Detection of changes in cartilage water content using MRI T2-mapping in vivo. Osteoarthritis Cartilage 2002; 10 (12) 907-913
  CrossrefPubMedGoogle Scholar
• 36 Jungmann PM, Kraus MS, Alizai H , et al. Association of metabolic risk factors with cartilage degradation assessed by T2 relaxation time at the knee: data from the osteoarthritis initiative. Arthritis Care Res (Hoboken) 2013; 65 (12) 1942-1950
  CrossrefPubMedGoogle Scholar
• 37 Jungmann PM, Li X, Nardo L , et al. Do cartilage repair procedures prevent degenerative meniscus changes?: longitudinal t1ρ and morphological evaluation with 3.0-T MRI. Am J Sports Med 2012; 40 (12) 2700-2708
  CrossrefPubMedGoogle Scholar
• 38 Lin W, Alizai H, Joseph GB , et al. Physical activity in relation to knee cartilage T2 progression measured with 3 T MRI over a period of 4 years: data from the Osteoarthritis Initiative. Osteoarthritis Cartilage 2013; 21 (10) 1558-1566
  CrossrefPubMedGoogle Scholar
• 39 Joseph GB, Baum T, Alizai H , et al. Baseline mean and heterogeneity of MR cartilage T2 are associated with morphologic degeneration of cartilage, meniscus, and bone marrow over 3 years—data from the Osteoarthritis Initiative. Osteoarthritis Cartilage 2012; 20 (7) 727-735
  CrossrefPubMedGoogle Scholar
• 40 Prasad AP, Nardo L, Schooler J, Joseph GB, Link TM. T₁ρ and T₂ relaxation times predict progression of knee osteoarthritis. Osteoarthritis Cartilage 2013; 21 (1) 69-76
  CrossrefPubMedGoogle Scholar
• 41 Carballido-Gamio J, Blumenkrantz G, Lynch JA, Link TM, Majumdar S. Longitudinal analysis of MRI T(2) knee cartilage laminar organization in a subset of patients from the osteoarthritis initiative. Magn Reson Med 2010; 63 (2) 465-472
  CrossrefPubMedGoogle Scholar
• 42 Jungmann PM, Kraus MS, Nardo L , et al. T(2) relaxation time measurements are limited in monitoring progression, once advanced cartilage defects at the knee occur: longitudinal data from the osteoarthritis initiative. J Magn Reson Imaging 2013; 38 (6) 1415-1424
  CrossrefPubMedGoogle Scholar
• 43 Welsch GH, Apprich S, Zbyn S , et al. Biochemical (T2, T2* and magnetisation transfer ratio) MRI of knee cartilage: feasibility at ultra-high field (7T) compared with high field (3T) strength. Eur Radiol 2011; 21 (6) 1136-1143
  CrossrefPubMedGoogle Scholar
• 44 Chang G, Xia D, Sherman O , et al. High resolution morphologic imaging and T2 mapping of cartilage at 7 Tesla: comparison of cartilage repair patients and healthy controls. MAGMA 2013; 26 (6) 539-548
  CrossrefPubMedGoogle Scholar
• 45 Domayer SE, Apprich S, Stelzeneder D , et al. Cartilage repair of the ankle: first results of T2 mapping at 7.0 T after microfracture and matrix associated autologous cartilage transplantation. Osteoarthritis Cartilage 2012; 20 (8) 829-836
  CrossrefPubMedGoogle Scholar
• 46 Welsch GH, Mamisch TC, Hughes T , et al. In vivo biochemical 7.0 Tesla magnetic resonance: preliminary results of dGEMRIC, zonal T2, and T2* mapping of articular cartilage. Invest Radiol 2008; 43 (9) 619-626
  CrossrefPubMedGoogle Scholar
• 47 Welsch GH, Mamisch TC, Marlovits S , et al. Quantitative T2 mapping during follow-up after matrix-associated autologous chondrocyte transplantation (MACT): full-thickness and zonal evaluation to visualize the maturation of cartilage repair tissue. J Orthop Res 2009; 27 (7) 957-963
  CrossrefPubMedGoogle Scholar
• 48 Mamisch TC, Hughes T, Mosher TJ , et al. T2 star relaxation times for assessment of articular cartilage at 3 T: a feasibility study. Skeletal Radiol 2012; 41 (3) 287-292
  CrossrefPubMedGoogle Scholar
• 49 Sepponen RE, Pohjonen JA, Sipponen JT, Tanttu JI. A method for T1 rho imaging. J Comput Assist Tomogr 1985; 9 (6) 1007-1011
  CrossrefPubMedGoogle Scholar
• 50 Keenan KE, Besier TF, Pauly JM , et al. Prediction of glycosaminoglycan content in human cartilage by age, T1ρ and T2 MRI. Osteoarthritis Cartilage 2011; 19 (2) 171-179
  CrossrefPubMedGoogle Scholar
• 51 Singh A, Haris M, Cai K, Kogan F, Hariharan H, Reddy R. High resolution T1ρ mapping of in vivo human knee cartilage at 7T. PLoS ONE 2014; 9 (5) e97486
  CrossrefPubMedGoogle Scholar
• 52 Burstein D, Velyvis J, Scott KT , et al. Protocol issues for delayed Gd(DTPA)(2-)-enhanced MRI (dGEMRIC) for clinical evaluation of articular cartilage. Magn Reson Med 2001; 45 (1) 36-41
  CrossrefPubMedGoogle Scholar
• 53 Lazik A, Körsmeier K, Claßen T , et al. 3 Tesla high-resolution and delayed gadolinium enhanced MR imaging of cartilage (dGEMRIC) after autologous chondrocyte transplantation in the hip. J Magn Reson Imaging 2014; ; December 19 (Epub ahead of print)
  PubMedGoogle Scholar
• 54 Watanabe A, Wada Y, Obata T , et al. Delayed gadolinium-enhanced MR to determine glycosaminoglycan concentration in reparative cartilage after autologous chondrocyte implantation: preliminary results. Radiology 2006; 239 (1) 201-208
  CrossrefPubMedGoogle Scholar
• 55 d'Entremont AG, McCormack RG, Agbanlog K , et al. Cartilage health in high tibial osteotomy using dGEMRIC: relationships with joint kinematics. Knee 2015; 22 (3) 156-162
  CrossrefPubMedGoogle Scholar
• 56 Schleich C, Müller-Lutz A, Sewerin P , et al. Intra-individual assessment of inflammatory severity and cartilage composition of finger joints in rheumatoid arthritis. Skeletal Radiol 2015; 44 (4) 513-518
  CrossrefPubMedGoogle Scholar
• 57 Owman H, Tiderius CJ, Ericsson YB, Dahlberg LE. Long-term effect of removal of knee joint loading on cartilage quality evaluated by delayed gadolinium-enhanced magnetic resonance imaging of cartilage. Osteoarthritis Cartilage 2014; 22 (7) 928-932
  CrossrefPubMedGoogle Scholar
• 58 Madelin G, Lee JS, Regatte RR, Jerschow A. Sodium MRI: methods and applications. Prog Nucl Magn Reson Spectrosc 2014; 79: 14-47
  CrossrefPubMedGoogle Scholar
• 59 Van Atta CM, Franath LP. The Nuclear Spin and Magnetic Moment of Sodium from Hyperfine Structure. Lancaster, PA: Lancaster Press; 1933
  Google Scholar
• 60 Newbould RD, Miller SR, Upadhyay N , et al. T1-weighted sodium MRI of the articulator cartilage in osteoarthritis: a cross sectional and longitudinal study. PLoS ONE 2013; 8 (8) e73067
  CrossrefPubMedGoogle Scholar
• 61 Madelin G, Babb J, Xia D , et al. Articular cartilage: evaluation with fluid-suppressed 7.0-T sodium MR imaging in subjects with and subjects without osteoarthritis. Radiology 2013; 268 (2) 481-491
  CrossrefPubMedGoogle Scholar
• 62 Trattnig S, Welsch GH, Juras V , et al. 23Na MR imaging at 7 T after knee matrix-associated autologous chondrocyte transplantation: preliminary results. Radiology 2010; 257 (1) 175-184
  CrossrefPubMedGoogle Scholar
• 63 Raya JG, Horng A, Dietrich O , et al. Articular cartilage: in vivo diffusion-tensor imaging. Radiology 2012; 262 (2) 550-559
  CrossrefPubMedGoogle Scholar
• 64 Raya JG, Melkus G, Adam-Neumair S , et al. Diffusion-tensor imaging of human articular cartilage specimens with early signs of cartilage damage. Radiology 2013; 266 (3) 831-841
  CrossrefPubMedGoogle Scholar
• 65 Ling W, Regatte RR, Navon G, Jerschow A. Assessment of glycosaminoglycan concentration in vivo by chemical exchange-dependent saturation transfer (gagCEST). Proc Natl Acad Sci U S A 2008; 105 (7) 2266-2270
  CrossrefPubMedGoogle Scholar
• 66 Schmitt B, Zbýn S, Stelzeneder D , et al. Cartilage quality assessment by using glycosaminoglycan chemical exchange saturation transfer and (23)Na MR imaging at 7 T. Radiology 2011; 260 (1) 257-264
  CrossrefPubMedGoogle Scholar
• 67 Bae WC, Du J, Bydder GM, Chung CB. Conventional and ultrashort time-to-echo magnetic resonance imaging of articular cartilage, meniscus, and intervertebral disk. Top Magn Reson Imaging 2010; 21 (5) 275-289
  CrossrefPubMedGoogle Scholar
• 68 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 (1) 77-85
  CrossrefPubMedGoogle Scholar
• 69 Pauli C, Bae WC, Lee M , et al. Ultrashort-echo time MR imaging of the patella with bicomponent analysis: correlation with histopathologic and polarized light microscopic findings. Radiology 2012; 264 (2) 484-493
  CrossrefPubMedGoogle Scholar
• 70 Bae WC, Dwek JR, Znamirowski R , et al. Ultrashort echo time MR imaging of osteochondral junction of the knee at 3 T: identification of anatomic structures contributing to signal intensity. Radiology 2010; 254 (3) 837-845
  CrossrefPubMedGoogle Scholar
• 71 Chang EY, Pallante-Kichura AL, Bae WC , et al. Development of a Comprehensive Osteochondral Allograft MRI Scoring System (OCAMRISS) with Histopathologic, Micro-Computed Tomography, and Biomechanical Validation. Cartilage 2014; 5 (1) 16-27
  CrossrefPubMedGoogle Scholar
• 72 Eggers H, Börnert P. Chemical shift encoding-based water-fat separation methods. J Magn Reson Imaging 2014; 40 (2) 251-268
  CrossrefPubMedGoogle Scholar
• 73 Gaeta M, Scribano E, Mileto A , et al. Muscle fat fraction in neuromuscular disorders: dual-echo dual-flip-angle spoiled gradient-recalled MR imaging technique for quantification—a feasibility study. Radiology 2011; 259 (2) 487-494
  CrossrefPubMedGoogle Scholar
• 74 Alizai H, Nardo L, Karampinos DC , et al. Comparison of clinical semi-quantitative assessment of muscle fat infiltration with quantitative assessment using chemical shift-based water/fat separation in MR studies of the calf of post-menopausal women. Eur Radiol 2012; 22 (7) 1592-1600
  CrossrefPubMedGoogle Scholar
• 75 Karampinos DC, Baum T, Nardo L , et al. Characterization of the regional distribution of skeletal muscle adipose tissue in type 2 diabetes using chemical shift-based water/fat separation. J Magn Reson Imaging 2012; 35 (4) 899-907
  CrossrefPubMedGoogle Scholar
• 76 Kumar D, Karampinos DC, MacLeod TD , et al. Quadriceps intramuscular fat fraction rather than muscle size is associated with knee osteoarthritis. Osteoarthritis Cartilage 2014; 22 (2) 226-234
  CrossrefPubMedGoogle Scholar
• 77 Nardo L, Karampinos DC, Lansdown DA , et al. Quantitative assessment of fat infiltration in the rotator cuff muscles using water-fat MRI. J Magn Reson Imaging 2014; 39 (5) 1178-1185
  CrossrefPubMedGoogle Scholar
• 78 Boesch C. Musculoskeletal spectroscopy. J Magn Reson Imaging 2007; 25 (2) 321-338
  CrossrefPubMedGoogle Scholar
• 79 Jouvensal L, Carlier PG, Bloch G. Practical implementation of single-voxel double-quantum editing on a whole-body NMR spectrometer: localized monitoring of lactate in the human leg during and after exercise. Magn Reson Med 1996; 36 (3) 487-490
  CrossrefPubMedGoogle Scholar
• 80 Wang ZY, Noyszewski EA, Leigh Jr JS. In vivo MRS measurement of deoxymyoglobin in human forearms. Magn Reson Med 1990; 14 (3) 562-567
  CrossrefPubMedGoogle Scholar
• 81 Goodpaster BH, He J, Watkins S, Kelley DE. Skeletal muscle lipid content and insulin resistance: evidence for a paradox in endurance-trained athletes. J Clin Endocrinol Metab 2001; 86 (12) 5755-5761
  CrossrefPubMedGoogle Scholar
• 82 Wang L, Salibi N, Wu Y, Schweitzer ME, Regatte RR. Relaxation times of skeletal muscle metabolites at 7T. J Magn Reson Imaging 2009; 29 (6) 1457-1464
  CrossrefPubMedGoogle Scholar
• 83 Khuu A, Ren J, Dimitrov I , et al. Orientation of lipid strands in the extracellular compartment of muscle: effect on quantitation of intramyocellular lipids. Magn Reson Med 2009; 61 (1) 16-21
  CrossrefPubMedGoogle Scholar
• 84 Versluis MJ, Kan HE, van Buchem MA, Webb AG. Improved signal to noise in proton spectroscopy of the human calf muscle at 7 T using localized B1 calibration. Magn Reson Med 2010; 63 (1) 207-211
  PubMedGoogle Scholar
• 85 Fissoune R, Janier M, Briguet A, Hiba B. In vivo assessment of mouse hindleg intramyocellular lipids by 1H-MR spectroscopy. Acad Radiol 2009; 16 (7) 890-896
  CrossrefPubMedGoogle Scholar
• 86 Saab G, Thompson RT, Marsh GD. Effects of exercise on muscle transverse relaxation determined by MR imaging and in vivo relaxometry. J Appl Physiol (1985) 2000; 88 (1) 226-233
  PubMedGoogle Scholar
• 87 Kim HK, Laor T, Horn PS, Racadio JM, Wong B, Dardzinski BJ. T2 mapping in Duchenne muscular dystrophy: distribution of disease activity and correlation with clinical assessments. Radiology 2010; 255 (3) 899-908
  CrossrefPubMedGoogle Scholar
• 88 Carlier PG, Azzabou N, de Sousa PL , et al. Skeletal muscle quantitative nuclear magnetic resonance imaging follow-up of adult Pompe patients. J Inherit Metab Dis 2015; 38 (3) 565-572
  CrossrefPubMedGoogle Scholar
• 89 Arpan I, Willcocks RJ, Forbes SC , et al. Examination of effects of corticosteroids on skeletal muscles of boys with DMD using MRI and MRS. Neurology 2014; 83 (11) 974-980
  CrossrefPubMedGoogle Scholar
• 90 Towse TF, Childs BT, Sabin SA, Bush EC, Elder CP, Damon BM. Comparison of muscle BOLD responses to arterial occlusion at 3 and 7 Tesla. Magn Reson Med 2015; ; April 17 (Epub ahead of print)
  PubMedGoogle Scholar
• 91 Du J, Chiang AJ, 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 (2) 178-184
  CrossrefPubMedGoogle Scholar
• 92 Constantinides CD, Gillen JS, Boada FE, Pomper MG, Bottomley PA. Human skeletal muscle: sodium MR imaging and quantification-potential applications in exercise and disease. Radiology 2000; 216 (2) 559-568
  CrossrefPubMedGoogle Scholar
• 93 Weber MA, Nagel AM, Jurkat-Rott K, Lehmann-Horn F. Sodium (23Na) MRI detects elevated muscular sodium concentration in Duchenne muscular dystrophy. Neurology 2011; 77 (23) 2017-2024
  CrossrefPubMedGoogle Scholar
• 94 Weber MA, Nielles-Vallespin S, Huttner HB , et al. Evaluation of patients with paramyotonia at 23Na MR imaging during cold-induced weakness. Radiology 2006; 240 (2) 489-500
  CrossrefPubMedGoogle Scholar
• 95 Chang G, Wang L, Schweitzer ME, Regatte RR. 3D 23Na MRI of human skeletal muscle at 7 Tesla: initial experience. Eur Radiol 2010; 20 (8) 2039-2046
  CrossrefPubMedGoogle Scholar
• 96 Minotti JR, Johnson EC, Hudson TL , et al. Training-induced skeletal muscle adaptations are independent of systemic adaptations. J Appl Physiol (1985) 1990; 68 (1) 289-294
  PubMedGoogle Scholar
• 97 van Oorschot JW, Schmitz JP, Webb A, Nicolay K, Jeneson JA, Kan HE. 31P MR spectroscopy and computational modeling identify a direct relation between Pi content of an alkaline compartment in resting muscle and phosphocreatine resynthesis kinetics in active muscle in humans. PLoS ONE 2013; 8 (9) e76628
  CrossrefPubMedGoogle Scholar
• 98 Zange J, Grehl T, Disselhorst-Klug C , et al. Breakdown of adenine nucleotide pool in fatiguing skeletal muscle in McArdle's disease: a noninvasive 31P-MRS and EMG study. Muscle Nerve 2003; 27 (6) 728-736
  CrossrefPubMedGoogle Scholar
• 99 Kuhl CK, Layer G, Träber F, Zierz S, Block W, Reiser M. Mitochondrial encephalomyopathy: correlation of P-31 exercise MR spectroscopy with clinical findings. Radiology 1994; 192 (1) 223-230
  CrossrefPubMedGoogle Scholar
• 100 Schunk K, Romaneehsen B, Rieker O , et al. Dynamic phosphorus-31 magnetic resonance spectroscopy in arterial occlusive disease: effects of vascular therapy on spectroscopic results. Invest Radiol 1998; 33 (6) 329-335
  CrossrefPubMedGoogle Scholar
• 101 Scheuermann-Freestone M, Madsen PL, Manners D , et al. Abnormal cardiac and skeletal muscle energy metabolism in patients with type 2 diabetes. Circulation 2003; 107 (24) 3040-3046
  CrossrefPubMedGoogle Scholar
• 102 Bogner W, Chmelik M, Schmid AI, Moser E, Trattnig S, Gruber S. Assessment of (31)P relaxation times in the human calf muscle: a comparison between 3 T and 7 T in vivo. Magn Reson Med 2009; 62 (3) 574-582
  CrossrefPubMedGoogle Scholar
• 103 Parasoglou P, Xia D, Chang G, Regatte RR. Dynamic three-dimensional imaging of phosphocreatine recovery kinetics in the human lower leg muscles at 3T and 7T: a preliminary study. NMR Biomed 2013; 26 (3) 348-356
  CrossrefPubMedGoogle Scholar
• 104 Johnell O, Kanis JA. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int 2006; 17 (12) 1726-1733
  CrossrefPubMedGoogle Scholar
• 105 Link TM. Osteoporosis imaging: state of the art and advanced imaging. Radiology 2012; 263 (1) 3-17
  CrossrefPubMedGoogle Scholar
• 106 Krug R, Burghardt AJ, Majumdar S, Link TM. High-resolution imaging techniques for the assessment of osteoporosis. Radiol Clin North Am 2010; 48 (3) 601-621
  CrossrefPubMedGoogle Scholar
• 107 Wehrli FW. Structural and functional assessment of trabecular and cortical bone by micro magnetic resonance imaging. J Magn Reson Imaging 2007; 25 (2) 390-409
  CrossrefPubMedGoogle Scholar
• 108 Sell CA, Masi JN, Burghardt A, Newitt D, Link TM, Majumdar S. Quantification of trabecular bone structure using magnetic resonance imaging at 3 Tesla—calibration studies using microcomputed tomography as a standard of reference. Calcif Tissue Int 2005; 76 (5) 355-364
  CrossrefPubMedGoogle Scholar
• 109 Driban JB, Barbe MF, Amin M , et al. Validation of quantitative magnetic resonance imaging-based apparent bone volume fraction in peri-articular tibial bone of cadaveric knees. BMC Musculoskelet Disord 2014; 15: 143-143
  CrossrefPubMedGoogle Scholar
• 110 Wehrli FW, Leonard MB, Saha PK, Gomberg BR. Quantitative high-resolution magnetic resonance imaging reveals structural implications of renal osteodystrophy on trabecular and cortical bone. J Magn Reson Imaging 2004; 20 (1) 83-89
  CrossrefPubMedGoogle Scholar
• 111 Link TM, Majumdar S, Augat P , et al. In vivo high resolution MRI of the calcaneus: differences in trabecular structure in osteoporosis patients. J Bone Miner Res 1998; 13 (7) 1175-1182
  CrossrefPubMedGoogle Scholar
• 112 Phan CM, Matsuura M, Bauer JS , et al. Trabecular bone structure of the calcaneus: comparison of MR imaging at 3.0 and 1.5 T with micro-CT as the standard of reference. Radiology 2006; 239 (2) 488-496
  CrossrefPubMedGoogle Scholar
• 113 Chang G, Wang L, Liang G, Babb JS, Saha PK, Regatte RR. Reproducibility of subregional trabecular bone micro-architectural measures derived from 7-Tesla magnetic resonance images. MAGMA 2011; 24 (3) 121-125
  CrossrefPubMedGoogle Scholar
• 114 Chang G, Pakin SK, Schweitzer ME, Saha PK, Regatte RR. Adaptations in trabecular bone microarchitecture in Olympic athletes determined by 7T MRI. J Magn Reson Imaging 2008; 27 (5) 1089-1095
  CrossrefPubMedGoogle Scholar
• 115 Chang G, Rajapakse CS, Babb JS, Honig SP, Recht MP, Regatte RR. In vivo estimation of bone stiffness at the distal femur and proximal tibia using ultra-high-field 7-Tesla magnetic resonance imaging and micro-finite element analysis. J Bone Miner Metab 2012; 30 (2) 243-251
  CrossrefPubMedGoogle Scholar
• 116 Chang G, Rajapakse CS, Diamond M , et al. Micro-finite element analysis applied to high-resolution MRI reveals improved bone mechanical competence in the distal femur of female pre-professional dancers. Osteoporos Int 2013; 24 (4) 1407-1417
  CrossrefPubMedGoogle Scholar
• 117 Chang G, Wang L, Liang G , et al. Quantitative assessment of trabecular bone micro-architecture of the wrist via 7 Tesla MRI: preliminary results. MAGMA 2011; 24 (4) 191-199
  CrossrefPubMedGoogle Scholar
• 118 Chang G, Deniz CM, Honig S , et al. MRI of the hip at 7T: feasibility of bone microarchitecture, high-resolution cartilage, and clinical imaging. J Magn Reson Imaging 2014; 39 (6) 1384-1393
  CrossrefPubMedGoogle Scholar
• 119 Chang G, Honig S, Liu Y , et al. 7 Tesla MRI of bone microarchitecture discriminates between women without and with fragility fractures who do not differ by bone mineral density. J Bone Miner Metab 2015; 33 (3) 285-293
  CrossrefPubMedGoogle Scholar
• 120 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 (1) 59-70
  CrossrefPubMedGoogle Scholar
• 121 Du J, Hamilton G, Takahashi A, Bydder M, Chung CB. Ultrashort echo time spectroscopic imaging (UTESI) of cortical bone. Magn Reson Med 2007; 58 (5) 1001-1009
  CrossrefPubMedGoogle Scholar