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DOI: 10.1055/s-0040-1712955
Quantitative Imaging in Muscle Diseases with Focus on Non-proton MRI and Other Advanced MRI Techniques
Abstract
The role of neuromuscular imaging in the diagnosis of inherited and acquired muscle diseases has gained clinical relevance. In particular, magnetic resonance imaging (MRI), especially whole-body applications, is increasingly being used for the diagnosis and monitoring of disease progression. In addition, they are considered as a powerful outcome measure in clinical trials. Because many muscle diseases have a distinct muscle involvement pattern, whole-body imaging can be of diagnostic value by identifying this pattern and thus narrowing the differential diagnosis and supporting the clinical diagnosis. In addition, more advanced MRI applications including non-proton MRI, diffusion tensor imaging, perfusion MRI, T2 mapping, and magnetic resonance spectroscopy provide deeper insights into muscle pathophysiology beyond the mere detection of fatty degeneration and/or muscle edema. In this review article, we present and discuss recent data on these quantitative MRI techniques in muscle diseases, with a particular focus on non-proton imaging techniques.
Publikationsverlauf
Artikel online veröffentlicht:
29. September 2020
© 2020. Thieme. All rights reserved.
Thieme Medical Publishers
333 Seventh Avenue, New York, NY 10001, USA.
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References
- 1 Wattjes MP, Fischer D. , eds. Neuromuscular Imaging. New York, NY: Springer Science+Business Media; 2013
- 2 Paoletti M, Pichiecchio A, Cotti Piccinelli S. , et al. Advances in quantitative imaging of genetic and acquired myopathies: clinical applications and perspectives. Front Neurol 2019; 10: 78
- 3 Hobson-Webb LD. Emerging Technologies in Neuromuscular Ultrasound. Muscle Nerve 2020 ; February 3; (Epub ahead of print)
- 4 Wattjes MP, Kley RA, Fischer D. Neuromuscular imaging in inherited muscle diseases. Eur Radiol 2010; 20 (10) 2447-2460
- 5 Díaz-Manera J, Llauger J, Gallardo E, Illa I. Muscle MRI in muscular dystrophies. Acta Myol 2015; 34 (2–3): 95-108
- 6 Ten Dam L, van der Kooi AJ, Verhamme C, Wattjes MP, de Visser M. Muscle imaging in inherited ad acquired muscle diseases. Eur J Neurol 2016; 23 (04) 688-703
- 7 Wattjes MP, Fischmann A, Fischer D. Imaging of primary muscular diseases: What do neurologists expect from radiologists? [in German]. Radiologe 2017; 57 (12) 1005-1011
- 8 Warman Chardon J, Díaz-Manera J, Tasca G. , et al; MYO-MRI Working Group. MYO-MRI diagnostic protocols in genetic myopathies. Neuromuscul Disord 2019; 29 (11) 827-841
- 9 Leung DG. Magnetic resonance imaging patterns of muscle involvement in genetic muscle diseases: a systematic review. J Neurol 2017; 264 (07) 1320-1333
- 10 Kornblum C, Lutterbey GG, Czermin B. , et al. Whole-body high-field MRI shows no skeletal muscle degeneration in young patients with recessive myotonia congenita. Acta Neurol Scand 2010; 121 (02) 131-135
- 11 Kesper K, Kornblum C, Reimann J, Lutterbey G, Schröder R, Wattjes MP. Pattern of skeletal muscle involvement in primary dysferlinopathies: a whole-body 3.0-T magnetic resonance imaging study. Acta Neurol Scand 2009; 120 (02) 111-118
- 12 Weber MA, Wolf M, Wattjes MP. Imaging patterns of muscle atrophy. Semin Musculoskelet Radiol 2018; 22 (03) 299-306
- 13 Strijkers GJ, Araujo ECA, Azzabou N. , et al. Exploration of new contrasts, targets, and MR imaging and spectroscopy techniques for neuromuscular disease. A Workshop Report of Working Group 3 of the Biomedicine and Molecular Biosciences COST Action BM1304 MYO-MRI. J Neuromuscul Dis 2019; 6 (01) 1-30
- 14 Damon BM, Li K, Bryant ND. Magnetic resonance imaging of skeletal muscle disease. Handb Clin Neurol 2016; 136: 827-842
- 15 Carlier PG, Marty B, Scheidegger O. , et al. Skeletal muscle quantitative nuclear magnetic resonance imaging and spectroscopy as an outcome measure for clinical trials. J Neuromuscul Dis 2016; 3 (01) 1-28
- 16 Leung DG. Advancements in magnetic resonance imaging-based biomarkers for muscular dystrophy. Muscle Nerve 2019; 60 (04) 347-360
- 17 Fischmann A, Hafner P, Fasler S. , et al. Quantitative MRI can detect subclinical disease progression in muscular dystrophy. J Neurol 2012; 259 (08) 1648-1654
- 18 Figueroa-Bonaparte S, Llauger J, Segovia S. , et al; Spanish Pompe group. Quantitative muscle MRI to follow up late onset Pompe patients: a prospective study. Sci Rep 2018; 8 (01) 10898
- 19 Regula JU, Jestaedt L, Jende F, Bartsch A, Meinck HM, Weber MA. Clinical muscle testing compared with whole-body magnetic resonance imaging in facio-scapulo-humeral muscular dystrophy. Clin Neuroradiol 2016; 26 (04) 445-455
- 20 Ma J. Dixon techniques for water and fat imaging. J Magn Reson Imaging 2008; 28 (03) 543-558
- 21 Burakiewicz J, Sinclair CDJ, Fischer D, Walter GA, Kan HE, Hollingsworth KG. Quantifying fat replacement of muscle by quantitative MRI in muscular dystrophy. J Neurol 2017; 264 (10) 2053-2067
- 22 Weber MA, Nagel AM, Marschar AM. , et al. 7-T (35)Cl and (23)Na MR imaging for detection of mutation-dependent alterations in muscular edema and fat fraction with sodium and chloride concentrations in muscular periodic paralyses. Radiology 2016; 280 (03) 848-859
- 23 Fischer D, Bonati U, Wattjes MP. Recent developments in muscle imaging of neuromuscular disorders. Curr Opin Neurol 2016; 29 (05) 614-620
- 24 Bonati U, Schmid M, Hafner P. , et al. Longitudinal 2-point Dixon muscle magnetic resonance imaging in Becker muscular dystrophy. Muscle Nerve 2015; 51 (06) 918-921
- 25 Morrow JM, Sinclair CDJ, Fischmann A. , et al. MRI biomarker assessment of neuromuscular disease progression: a prospective observational cohort study. Lancet Neurol 2016; 15 (01) 65-77
- 26 Willcocks RJ, Rooney WD, Triplett WT. , et al. Multicenter prospective longitudinal study of magnetic resonance biomarkers in a large Duchenne muscular dystrophy cohort. Ann Neurol 2016; 79 (04) 535-547
- 27 Dahlqvist JR, Oestergaard ST, Poulsen NS, Knak KL, Thomsen C, Vissing J. Muscle contractility in spinobulbar muscular atrophy. Sci Rep 2019; 9 (01) 4680
- 28 Murphy AP, Morrow J, Dahlqvist JR. , et al. Natural history of limb girdle muscular dystrophy R9 over 6 years: searching for trial endpoints. Ann Clin Transl Neurol 2019; 6 (06) 1033-1045
- 29 Barnard AM, Willcocks RJ, Triplett WT. , et al. MR biomarkers predict clinical function in Duchenne muscular dystrophy. Neurology 2020; 94 (09) e897-e909
- 30 Naarding KJ, Reyngoudt H, van Zwet EW. , et al. MRI vastus lateralis fat fraction predicts loss of ambulation in Duchenne muscular dystrophy. Neurology 2020; 94 (13) e1386-e1394
- 31 Straub V, Balabanov P, Bushby K. , et al. Stakeholder cooperation to overcome challenges in orphan medicine development: the example of Duchenne muscular dystrophy. Lancet Neurol 2016; 15 (08) 882-890
- 32 Ladd ME, Bachert P, Meyerspeer M. , et al. Pros and cons of ultra-high-field MRI/MRS for human application. Prog Nucl Magn Reson Spectrosc 2018; 109: 1-50
- 33 Niesporek SC, Nagel AM, Platt T. Multinuclear MRI at ultrahigh fields. Top Magn Reson Imaging 2019; 28 (03) 173-188
- 34 Madelin G, Regatte RR. Biomedical applications of sodium MRI in vivo. J Magn Reson Imaging 2013; 38 (03) 511-529
- 35 Nagel AM, Weber MA, Borthakur A, Reddy R. Skeletal muscle MR imaging beyond protons: with a focus on sodium MRI in musculoskeletal applications. In: Weber MA. , ed. Magnetic Resonance Imaging of the Skeletal Musculature. New York, NY: Springer; 2014: 115-133
- 36 Gerhalter T, Gast LV, Marty B, Uder M, Carlier PG, Nagel AM. Assessing the variability of 23Na MRI in skeletal muscle tissue: reproducibility and repeatability of tissue sodium concentration measurements in the lower leg at 3 T. NMR Biomed 2020; 33 (05) e4279
- 37 Lehmann-Horn F, Jurkat-Rott K. Voltage-gated ion channels and hereditary disease. Physiol Rev 1999; 79 (04) 1317-1372
- 38 Jurkat-Rott K, Weber MA, Lehmann-Horn F. MRI in muscle channelopathies. In: Weber MA. , ed. Magnetic Resonance Imaging of the Skeletal Musculature. New York, NY: Springer; 2014: 271-288
- 39 Kornblum C, Lutterbey G, Bogdanow M. , et al. Distinct neuromuscular phenotypes in myotonic dystrophy types 1 and 2 : a whole body highfield MRI study. J Neurol 2006; 253 (06) 753-761
- 40 Nagel AM, Amarteifio E, Lehmann-Horn F. , et al. 3 Tesla sodium inversion recovery magnetic resonance imaging allows for improved visualization of intracellular sodium content changes in muscular channelopathies. Invest Radiol 2011; 46 (12) 759-766
- 41 Jurkat-Rott K, Lehmann-Horn F, Elbaz A. , et al. A calcium channel mutation causing hypokalemic periodic paralysis. Hum Mol Genet 1994; 3 (08) 1415-1419
- 42 Jurkat-Rott K, Weber MA, Fauler M. , et al. K+-dependent paradoxical membrane depolarization and Na+ overload, major and reversible contributors to weakness by ion channel leaks. Proc Natl Acad Sci U S A 2009; 106 (10) 4036-4041
- 43 Fan C, Lehmann-Horn F, Weber MA. , et al. Transient compartment-like syndrome and normokalaemic periodic paralysis due to a Ca(v)1.1 mutation. Brain 2013; 136 (Pt 12): 3775-3786
- 44 Resnick JS, Engel WK, Griggs RC, Stam AC. Acetazolamide prophylaxis in hypokalemic periodic paralysis. N Engl J Med 1968; 278 (11) 582-586
- 45 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
- 46 Amarteifio E, Nagel AM, Weber MA, Jurkat-Rott K, Lehmann-Horn F. Hyperkalemic periodic paralysis and permanent weakness: 3-T MR imaging depicts intracellular 23Na overload—initial results. Radiology 2012; 264 (01) 154-163
- 47 Chang G, Wang L, Schweitzer ME, Regatte III RR. 3D 23Na MRI of human skeletal muscle at 7 Tesla: initial experience. Eur Radiol 2010; 20 (08) 2039-2046
- 48 Weber MA, Jurkat-Rott K, Lerche H, Lehmann-Horn F. Strength and muscle structure preserved during long-term therapy in a patient with hypokalemic periodic paralysis (Cav1.1-R1239G). J Neurol 2019; 266 (07) 1623-1632
- 49 Weber MA, Nagel AM, Wolf MB. , et al. Permanent muscular sodium overload and persistent muscle edema in Duchenne muscular dystrophy: a possible contributor of progressive muscle degeneration. J Neurol 2012; 259 (11) 2385-2392
- 50 Glemser PA, Jaeger H, Nagel AM. , et al. 23Na MRI and myometry to compare eplerenone vs. glucocorticoid treatment in Duchenne dystrophy. Acta Myol 2017; 36 (01) 2-13
- 51 Gerhalter T, Gast LV, Marty B. , et al. 23Na MRI depicts early changes in ion homeostasis in skeletal muscle tissue of patients with Duchenne muscular dystrophy. J Magn Reson Imaging 2019; 50 (04) 1103-1113
- 52 Manzur AY, Kuntzer T, Pike M, Swan A. Glucocorticoid corticosteroids for Duchenne muscular dystrophy. Cochrane Database Syst Rev 2008; (01) CD003725
- 53 Lehmann-Horn F, Weber MA, Nagel AM. , et al. Rationale for treating oedema in Duchenne muscular dystrophy with eplerenone. Acta Myol 2012; 31 (01) 31-39
- 54 Statland JM, Barohn RJ. Muscle channelopathies: the nondystrophic myotonias and periodic paralyses. Continuum (Minneap Minn) 2013; 19 (6 Muscle Disease): 1598-1614
- 55 Tristani-Firouzi M, Etheridge SP. Kir 2.1 channelopathies: the Andersen-Tawil syndrome. Pflugers Arch 2010; 460 (02) 289-294
- 56 Harris RK, Becker ED, Cabral de Menezes SM, Goodfellow R, Granger P. NMR nomenclature: nuclear spin properties and conventions for chemical shifts. IUPAC Recommendations 2001. Solid State Nucl Magn Reson 2002; 22 (04) 458-483
- 57 Neeb H, Zilles K, Shah NJ. A new method for fast quantitative mapping of absolute water content in vivo. Neuroimage 2006; 31 (03) 1156-1168
- 58 Madelin G, Lee JS, Regatte RR, Jerschow A. Sodium MRI: methods and applications. Prog Nucl Magn Reson Spectrosc 2014; 79: 14-47
- 59 Nagel AM, Lehmann-Horn F, Weber MA. , et al. In vivo 35Cl MR imaging in humans: a feasibility study. Radiology 2014; 271 (02) 585-595
- 60 Umathum R, Roesler MB, Nagel AM. In vivo 39K MR imaging of human muscle and brain. Radiology 2013; 269 (02) 569-576
- 61 Koch MC, Steinmeyer K, Lorenz C. , et al. The skeletal muscle chloride channel in dominant and recessive human myotonia. Science 1992; 257 (5071): 797-800
- 62 Donahue KM, Weisskoff RM, Parmelee DJ. , et al. Dynamic Gd-DTPA enhanced MRI measurement of tissue cell volume fraction. Magn Reson Med 1995; 34 (03) 423-432
- 63 Syková E, Nicholson C. Diffusion in brain extracellular space. Physiol Rev 2008; 88 (04) 1277-1340
- 64 Thulborn KR, Gindin TS, Davis D, Erb P. Comprehensive MR imaging protocol for stroke management: tissue sodium concentration as a measure of tissue viability in nonhuman primate studies and in clinical studies. Radiology 1999; 213 (01) 156-166
- 65 Hodgkin AL, Huxley AF. A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 1952; 117 (04) 500-544
- 66 Niesporek SC, Umathum R, Fiedler TM, Bachert P, Ladd ME, Nagel AM. Improved T*2 determination in 23Na, 35Cl, and 17O MRI using iterative partial volume correction based on 1H MRI segmentation. MAGMA 2017; 30 (06) 519-536
- 67 Boesch C. MR spectroscopy and spectroscopic imaging for evaluation of skeletal muscle metabolism: basics and applications in metabolic diseases. In: Weber MA. , ed. Magnetic Resonance Imaging of the Skeletal Musculature. New York, NY: Springer; 2014: 135-163
- 68 Valkovič L, Chmelík M, Krššák M. In-vivo31P-MRS of skeletal muscle and liver: a way for non-invasive assessment of their metabolism. Anal Biochem 2017; 529: 193-215
- 69 Oudeman J, Nederveen AJ, Strijkers GJ, Maas M, Luijten PR, Froeling M. Techniques and applications of skeletal muscle diffusion tensor imaging: a review. J Magn Reson Imaging 2016; 43 (04) 773-788
- 70 Holl N, Echaniz-Laguna A, Bierry G. , et al. Diffusion-weighted MRI of denervated muscle: a clinical and experimental study. Skeletal Radiol 2008; 37 (12) 1111-1117
- 71 Qi J, Olsen NJ, Price RR, Winston JA, Park JH. Diffusion-weighted imaging of inflammatory myopathies: polymyositis and dermatomyositis. J Magn Reson Imaging 2008; 27 (01) 212-217
- 72 Hooijmans MT, Damon BM, Froeling M. , et al. Evaluation of skeletal muscle DTI in patients with Duchenne muscular dystrophy. NMR Biomed 2015; 28 (11) 1589-1597
- 73 Maggi L, Moscatelli M, Frangiamore R. , et al. Quantitative muscle MRI protocol as possible biomarker in Becker muscular dystrophy. Clin Neuroradiol 2020 ; January 23 ( Epub ahead of print)
- 74 Rehmann R, Schlaffke L, Froeling M. , et al. Muscle diffusion tensor imaging in glycogen storage disease V (McArdle disease). Eur Radiol 2019; 29 (06) 3224-3232
- 75 Li GD, Liang YY, Xu P, Ling J, Chen YM. Diffusion-tensor imaging of thigh muscles in Duchenne muscular dystrophy: correlation of apparent diffusion coefficient and fractional anisotropy values with fatty infiltration. AJR Am J Roentgenol 2016; 206 (04) 867-870
- 76 Ponrartana S, Ramos-Platt L, Wren TA. , et al. Effectiveness of diffusion tensor imaging in assessing disease severity in Duchenne muscular dystrophy: preliminary study. Pediatr Radiol 2015; 45 (04) 582-589
- 77 Winters KV, Reynaud O, Novikov DS, Fieremans E, Kim SG. Quantifying myofiber integrity using diffusion MRI and random permeable barrier modeling in skeletal muscle growth and Duchenne muscular dystrophy model in mice. Magn Reson Med 2018; 80 (05) 2094-2108
- 78 Porcari P, Hall MG, Clark CA, Greally E, Straub V, Blamire AM. Time-dependent diffusion MRI as a probe of microstructural changes in a mouse model of Duchenne muscular dystrophy. NMR Biomed 2020; 33 (05) e4276
- 79 Partovi S, Jacobi B, Gordon Y. , et al. Assessment of skeletal muscle microperfusion using MRI. In: Weber MA. , ed. Magnetic Resonance Imaging of the Skeletal Musculature. New York, NY: Springer; 2014: 87-114
- 80 Bendszus M, Koltzenburg M. Visualization of denervated muscle by gadolinium-enhanced MRI. Neurology 2001; 57 (09) 1709-1711
- 81 Goyault G, Bierry G, Holl N. , et al. Diffusion-weighted MRI, dynamic susceptibility contrast MRI and ultrasound perfusion quantification of denervated muscle in rabbits. Skeletal Radiol 2012; 41 (01) 33-40
- 82 Argov Z, Löfberg M, Arnold DL. Insights into muscle diseases gained by phosphorus magnetic resonance spectroscopy. Muscle Nerve 2000; 23 (09) 1316-1334
- 83 Kemp GJ, Taylor DJ, Thompson CH. , et al. Quantitative analysis by 31P magnetic resonance spectroscopy of abnormal mitochondrial oxidation in skeletal muscle during recovery from exercise. NMR Biomed 1993; 6 (05) 302-310