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DOI: 10.1055/a-1738-5356
Bildgebung der Muskulatur bei Neuromuskulären Erkrankungen – von der Initialdiagnostik bis zur Verlaufsbeurteilung
Muscular Imaging in Neuromuscular Diseases – from Initial Diagnostics to Follow-Up AssessmentZusammenfassung
Die bildgebende Diagnostik hat sich zu einem integralen Element der Betreuung von PatientInnen mit neuromuskulären Erkrankungen entwickelt. Als wesentliches Diagnostikum ist hierbei die Magnetresonanztomografie als breit verfügbares und vergleichsweise standardisiertes Untersuchungsverfahren etabliert, wobei die Sonografie der Muskulatur bei hinreichend erfahrenem Untersucher ebenfalls geeignet ist, wertvolle diagnostische Informationen zu liefern. Das CT hingegen spielt eine untergeordnete Rolle und sollte nur bei Kontraindikationen für eine MRT in Erwägung gezogen werden. Zunächst wurde die Bildgebung bei Muskelerkrankungen primär in der Initialdiagnostik unter vielfältigen Fragestellungen eingesetzt. Das Aufkommen innovativer Therapiekonzepte bei verschiedenen neuromuskulären Erkrankungen machen neben einer möglichst frühzeitigen Diagnosestellung insbesondere auch eine multimodale Verlaufsbeurteilung zur Evaluation des Therapieansprechens notwendig. Auch hier wird die Bildgebung der Muskulatur als objektiver Parameter des Therapieerfolges intensiv diskutiert und in Forschung wie Praxis zunehmend verwendet.
Abstract
Muscle imaging is an integral element in care and surveillance of patients with neuromuscular disorders. In this regard, magnetic resonance imaging (MRI) is widely available and is the standard procedure. Muscle sonography, however, offers valuable diagnostic information when carried out by highly experienced examiners. CT imaging only appears appropriate when other methods are not applicable (i. e., contraindications). While muscle imaging was primarily used in the context of initial diagnostics, recent developments in innovative therapeutic concepts necessitate not only the earliest possible diagnosis, but also a multimodal follow-up assessment to evaluate response to therapy. Thus, imaging of the musculature as an objective parameter of therapeutic success is intensively discussed and increasingly used in research and practice.
Schlüsselwörter
Neuromuskuläre Bildgebung - Muskel-MRT - Ganzkörper-MRT - quantitative MRT - MyosonografiePublication History
Article published online:
02 March 2022
© 2022. Thieme. All rights reserved.
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Literatur
- 1 Cartwright MS, Upadhya S. Selecting disease-modifying medications in 5q spinal muscular atrophy. Muscle Nerve 2021; 64: 404-412 DOI: 10.1002/mus.27358.
- 2 Lehmann Urban D, Schneider I. Genspezifische Therapieansätze bei Muskelerkrankungen. Der Nervenarzt 2020; 91: 318-323 DOI: 10.1007/s00115-020-00870-8.
- 3 Krenn M, Tomschik M, Rath J. et al. Genotype-guided diagnostic reassessment after exome sequencing in neuromuscular disorders: experiences with a two-step approach. Eur J Neurol 2020; 27: 51-61 DOI: 10.1111/ene.14033.
- 4 Lamminen AE. Magnetic resonance imaging of primary skeletal muscle diseases: patterns of distribution and severity of involvement. Br J Radiol 1990; 63: 946-950 DOI: 10.1259/0007-1285-63-756-946.
- 5 Lamminen AE, Hekali PE, Tiula E. et al. Acute rhabdomyolysis: evaluation with magnetic resonance imaging compared with computed tomography and ultrasonography. Br J Radiol 1989; 62: 326-330 DOI: 10.1259/0007-1285-62-736-326.
- 6 Mercuri E, Jungbluth H, Muntoni F. Muscle imaging in clinical practice: diagnostic value of muscle magnetic resonance imaging in inherited neuromuscular disorders. Curr Opin Neurol 2005; 18: 526-537 DOI: 10.1097/01.wco.0000183947.01362.fe.
- 7 Mercuri E, Pichiecchio A, Allsop J. et al. Muscle MRI in inherited neuromuscular disorders: past, present, and future. J Magn Reson Imaging 2007; 25: 433-440 DOI: 10.1002/jmri.20804.
- 8 Nuutila P, Kalliokoski K. Use of positron emission tomography in the assessment of skeletal muscle and tendon metabolism and perfusion. Scand J Med Sci Sports 2000; 10: 346-350 DOI: 10.1034/j.1600-0838.2000.010006346.x.
- 9 Martis N, Viau P, Zenone T. et al. Clinical value of a [18F]-FDG PET-CT muscle-to-muscle SUV ratio for the diagnosis of active dermatomyositis. Eur Radiol 2019; 29: 6708-6716 DOI: 10.1007/s00330-019-06302-9.
- 10 Matuszak J, Blondet C, Hubele F. et al. Muscle fluorodeoxyglucose uptake assessed by positron emission tomography-computed tomography as a biomarker of inflammatory myopathies disease activity. Rheumatology (Oxford) 2019; DOI: 10.1093/rheumatology/kez040.
- 11 Walker UA. Imaging tools for the clinical assessment of idiopathic inflammatory myositis. Curr Opin Rheumatol 2008; 20: 656-661 DOI: 10.1097/BOR.0b013e3283118711.
- 12 Wijntjes J, van Alfen N. Muscle ultrasound: Present state and future opportunities. Muscle Nerve 2021; 63: 455-466 DOI: 10.1002/mus.27081.
- 13 Boon AJ, Wijntjes J, O'Brien TG. et al. Diagnostic accuracy of gray scale muscle ultrasound screening for pediatric neuromuscular disease. Muscle Nerve 2021; 64: 50-58 DOI: 10.1002/mus.27211.
- 14 Brockmann K, Becker P, Schreiber G. et al. Sensitivity and specificity of qualitative muscle ultrasound in assessment of suspected neuromuscular disease in childhood. Neuromuscul Disord 2007; 17: 517-523 DOI: 10.1016/j.nmd.2007.03.015.
- 15 Rahmani N, Mohseni-Bandpei MA, Vameghi R. et al. Application of ultrasonography in the assessment of skeletal muscles in children with and without neuromuscular disorders: a systematic review. Ultrasound Med Biol 2015; 41: 2275-2283 DOI: 10.1016/j.ultrasmedbio.2015.04.027.
- 16 Veltsista D, Chroni E. Ultrasound pattern of anterolateral leg muscles in facioscapulohumeral muscular dystrophy. Acta Neurol Scand 2021; 144: 216-220 DOI: 10.1111/ane.13428.
- 17 Guimaraes JB, Cavalcante WCP, Cruz IAN. et al. Musculoskeletal Ultrasound in Inclusion Body Myositis: A Comparative Study with Magnetic Resonance Imaging. Ultrasound Med Biol 2021; 47: 2186-2192 DOI: 10.1016/j.ultrasmedbio.2021.04.019.
- 18 Arts IM, Overeem S, Pillen S. et al. Muscle ultrasonography: a diagnostic tool for amyotrophic lateral sclerosis. Clin Neurophysiol 2012; 123: 1662-1667 DOI: 10.1016/j.clinph.2011.11.262.
- 19 Tsuji Y, Noto YI, Shiga K. et al. A muscle ultrasound score in the diagnosis of amyotrophic lateral sclerosis. Clin Neurophysiol 2017; 128: 1069-1074 DOI: 10.1016/j.clinph.2017.02.015.
- 20 Reimers CD, Fleckenstein JL, Witt TN. et al. Muscular ultrasound in idiopathic inflammatory myopathies of adults. J Neurol Sci 1993; 116: 82-92 DOI: 10.1016/0022-510x(93)90093-e.
- 21 Zaidman CM, Malkus EC, Connolly AM. Muscle ultrasound quantifies disease progression over time in infants and young boys with duchenne muscular dystrophy. Muscle Nerve 2015; 52: 334-338 DOI: 10.1002/mus.24609.
- 22 Alfuraih AM, O'Connor P, Tan AL. et al. Muscle shear wave elastography in idiopathic inflammatory myopathies: a case-control study with MRI correlation. Skeletal Radiol 2019; 48: 1209-1219 DOI: 10.1007/s00256-019-03175-3.
- 23 van Alfen N, Gijsbertse K, de Korte CL. How useful is muscle ultrasound in the diagnostic workup of neuromuscular diseases?. Curr Opin Neurol 2018; 31: 568-574 DOI: 10.1097/WCO.0000000000000589.
- 24 Weber MA, Krix M, Jappe U. et al. Pathologic skeletal muscle perfusion in patients with myositis: detection with quantitative contrast-enhanced US – initial results. Radiology 2006; 238: 640-649 DOI: 10.1148/radiol.2382041822.
- 25 Warman Chardon J, Diaz-Manera J, Tasca G. et al. MYO-MRI diagnostic protocols in genetic myopathies. Neuromuscul Disord 2019; 29: 827-841 DOI: 10.1016/j.nmd.2019.08.011.
- 26 Albayda J, van Alfen N. Diagnostic Value of Muscle Ultrasound for Myopathies and Myositis. Curr Rheumatol Rep 2020; 22: 82 DOI: 10.1007/s11926-020-00947-y.
- 27 Deschauer M, Sproß J, Gläser D. et al. Diagnostik von Myopathien, S1-Leitlinie. In Leitlinien für Diagnostik und Therapie in der Neurologie: Deutsche Gesellschaft für Neurologie. 2021
- 28 Gomez-Andres D, Dabaj I, Mompoint D. et al. Pediatric laminopathies: Whole-body magnetic resonance imaging fingerprint and comparison with Sepn1 myopathy. Muscle Nerve 2016; 54: 192-202 DOI: 10.1002/mus.25018.
- 29 Jarraya M, Quijano-Roy S, Monnier N. et al. Whole-Body muscle MRI in a series of patients with congenital myopathy related to TPM2 gene mutations. Neuromuscul Disord 2012; 22: S137-S147 DOI: 10.1016/j.nmd.2012.06.347.
- 30 Mensch A, Kraya T, Koester F. et al. Whole-body muscle MRI of patients with MATR3-associated distal myopathy reveals a distinct pattern of muscular involvement and highlights the value of whole-body examination. J Neurol 2020; 267: 2408-2420 DOI: 10.1007/s00415-020-09862-9.
- 31 Morrow JM, Sinclair CD, Fischmann A. et al. MRI biomarker assessment of neuromuscular disease progression: a prospective observational cohort study. Lancet Neurol 2016; 15: 65-77 DOI: 10.1016/S1474-4422(15)00242-2.
- 32 Quijano-Roy S, Carlier RY. Muscle magnetic resonance imaging: a new diagnostic tool with promising avenues in therapeutic trials. Neuropediatrics 2014; 45: 273-274 DOI: 10.1055/s-0034-1389894.
- 33 Dixon WT. Simple proton spectroscopic imaging. Radiology 1984; 153: 189-194 DOI: 10.1148/radiology.153.1.6089263.
- 34 Fischer MA, Pfirrmann CW, Espinosa N. et al. Dixon-based MRI for assessment of muscle-fat content in phantoms, healthy volunteers and patients with achillodynia: comparison to visual assessment of calf muscle quality. Eur Radiol 2014; 24: 1366-1375 DOI: 10.1007/s00330-014-3121-1.
- 35 Argentieri EC, Tan ET, Whang JS. et al. Quantitative T2 -mapping magnetic resonance imaging for assessment of muscle motor unit recruitment patterns. Muscle Nerve 2021; 63: 703-709 DOI: 10.1002/mus.27186.
- 36 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: 1-28 DOI: 10.3233/JND-160145.
- 37 Chianca V, Albano D, Messina C. et al. Diffusion tensor imaging in the musculoskeletal and peripheral nerve systems: from experimental to clinical applications. Eur Radiol Exp 2017; 1: 12 DOI: 10.1186/s41747-017-0018-1.
- 38 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: 1-30 DOI: 10.3233/JND-180333.
- 39 Reimers CD, Schedel H, Fleckenstein JL. et al. Magnetic resonance imaging of skeletal muscles in idiopathic inflammatory myopathies of adults. J Neurol 1994; 241: 306-314 DOI: 10.1007/BF00868438.
- 40 Stiglbauer R, Graninger W, Prayer L. et al. Polymyositis: MRI-appearance at 1.5 T and correlation to clinical findings. Clin Radiol 1993; 48: 244-248 DOI: 10.1016/s0009-9260(05)80305-8.
- 41 Malartre S, Bachasson D, Mercy G. et al. MRI and muscle imaging for idiopathic inflammatory myopathies. Brain Pathol 2021; 31: e12954 DOI: 10.1111/bpa.12954.
- 42 Nunez-Peralta C, Alonso-Perez J, Diaz-Manera J. The increasing role of muscle MRI to monitor changes over time in untreated and treated muscle diseases. Curr Opin Neurol 2020; 33: 611-620 DOI: 10.1097/WCO.0000000000000851.
- 43 Fischer D, Kley RA, Strach K. et al. Distinct muscle imaging patterns in myofibrillar myopathies. Neurology 2008; 71: 758-765 DOI: 10.1212/01.wnl.0000324927.28817.9b.
- 44 Barnard AM, Willcocks RJ, Finanger EL. et al. Skeletal muscle magnetic resonance biomarkers correlate with function and sentinel events in Duchenne muscular dystrophy. PLoS One 2018; 13: e0194283 DOI: 10.1371/journal.pone.0194283.
- 45 Figueroa-Bonaparte S, Segovia S, Llauger J. et al. Muscle MRI Findings in Childhood/Adult Onset Pompe Disease Correlate with Muscle Function. PLoS One 2016; 11: e0163493 DOI: 10.1371/journal.pone.0163493.
- 46 Schmidt S, Hafner P, Klein A. et al. Timed function tests, motor function measure, and quantitative thigh muscle MRI in ambulant children with Duchenne muscular dystrophy: A cross-sectional analysis. Neuromuscul Disord 2018; 28: 16-23 DOI: 10.1016/j.nmd.2017.10.003.
- 47 Burakiewicz J, Sinclair CDJ, Fischer D. et al. Quantifying fat replacement of muscle by quantitative MRI in muscular dystrophy. J Neurol 2017; 264: 2053-2067 DOI: 10.1007/s00415-017-8547-3.
- 48 Mersmann F, Bohm S, Schroll A. et al. Validation of a simplified method for muscle volume assessment. J Biomech 2014; 47: 1348-1352 DOI: 10.1016/j.jbiomech.2014.02.007.
- 49 Brunner G, Nambi V, Yang E. et al. Automatic quantification of muscle volumes in magnetic resonance imaging scans of the lower extremities. Magn Reson Imaging 2011; 29: 1065-1075 DOI: 10.1016/j.mri.2011.02.033.
- 50 Pons C, Borotikar B, Garetier M. et al. Quantifying skeletal muscle volume and shape in humans using MRI: A systematic review of validity and reliability. PLoS One 2018; 13: e0207847 DOI: 10.1371/journal.pone.0207847.
- 51 Leung DG, Carrino JA, Wagner KR. et al. Whole-body magnetic resonance imaging evaluation of facioscapulohumeral muscular dystrophy. Muscle Nerve 2015; 52: 512-520 DOI: 10.1002/mus.24569.
- 52 Ten Dam L, van der Kooi AJ, Rovekamp F. et al. Comparing clinical data and muscle imaging of DYSF and ANO5 related muscular dystrophies. Neuromuscul Disord 2014; 24: 1097-1102 DOI: 10.1016/j.nmd.2014.07.004.
- 53 Diaz-Manera J, Llauger J, Gallardo E. et al. Muscle MRI in muscular dystrophies. Acta Myol 2015; 34: 95-108
- 54 Leung DG. Magnetic resonance imaging patterns of muscle involvement in genetic muscle diseases: a systematic review. J Neurol 2017; 264: 1320-1333 DOI: 10.1007/s00415-016-8350-6.
- 55 Pestronk A. Neuromuscular disease center (section: ‘MRI’). Washington University; St. Louis, MO, USA: Im Internet: https://neuromuscular.wustl.edu/pathol/diagrams/musclemri.htm Stand: 02.01.2022.
- 56 Andersen G, Dahlqvist JR, Vissing CR. et al. MRI as outcome measure in facioscapulohumeral muscular dystrophy: 1-year follow-up of 45 patients. J Neurol 2017; 264: 438-447 DOI: 10.1007/s00415-016-8361-3.
- 57 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: 565-572 DOI: 10.1007/s10545-015-9825-9.
- 58 Figueroa-Bonaparte S, Llauger J, Segovia S. et al. Quantitative muscle MRI to follow up late onset Pompe patients: a prospective study. Sci Rep 2018; 8: 10898 DOI: 10.1038/s41598-018-29170-7.
- 59 Hogrel JY, Wary C, Moraux A. et al. Longitudinal functional and NMR assessment of upper limbs in Duchenne muscular dystrophy. Neurology 2016; 86: 1022-1030 DOI: 10.1212/WNL.0000000000002464.
- 60 Nunez-Peralta C, Alonso-Perez J, Llauger J. et al. Follow-up of late-onset Pompe disease patients with muscle magnetic resonance imaging reveals increase in fat replacement in skeletal muscles. J Cachexia Sarcopenia Muscle 2020; 11: 1032-1046 DOI: 10.1002/jcsm.12555.
- 61 Wary C, Azzabou N, Giraudeau C. et al. Quantitative NMRI and NMRS identify augmented disease progression after loss of ambulation in forearms of boys with Duchenne muscular dystrophy. NMR Biomed 2015; 28: 1150-1162 DOI: 10.1002/nbm.3352.
- 62 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: 535-547 DOI: 10.1002/ana.24599.
- 63 Heskamp L, van Nimwegen M, Ploegmakers MJ. et al. Lower extremity muscle pathology in myotonic dystrophy type 1 assessed by quantitative MRI. Neurology 2019; 92: e2803-e2814 DOI: 10.1212/WNL.0000000000007648.
- 64 Mercuri E, Lampe A, Allsop J. et al. Muscle MRI in Ullrich congenital muscular dystrophy and Bethlem myopathy. Neuromuscul Disord 2005; 15: 303-310 DOI: 10.1016/j.nmd.2005.01.004.
- 65 Fu J, Zheng YM, Jin SQ. et al. “Target” and “Sandwich” Signs in Thigh Muscles have High Diagnostic Values for Collagen VI-related Myopathies. Chin Med J (Engl) 2016; 129: 1811-1816 DOI: 10.4103/0366-6999.186638.
- 66 Salim R, Dahlqvist JR, Khawajazada T. et al. Characteristic muscle signatures assessed by quantitative MRI in patients with Bethlem myopathy. J Neurol 2020; 267: 2432-2442 DOI: 10.1007/s00415-020-09860-x.
- 67 van de Velde NM, Hooijmans MT, Sardjoe Mishre ASD. et al. Selection Approach to Identify the Optimal Biomarker Using Quantitative Muscle MRI and Functional Assessments in Becker Muscular Dystrophy. Neurology 2021; 97: e513-e522 DOI: 10.1212/WNL.0000000000012233.
- 68 Lilien C, Reyngoudt H, Seferian AM. et al. Upper limb disease evolution in exon 53 skipping eligible patients with Duchenne muscular dystrophy. Ann Clin Transl Neurol 2021; DOI: 10.1002/acn3.51417.
- 69 Bonati U, Schmid M, Hafner P. et al. Longitudinal 2-point dixon muscle magnetic resonance imaging in becker muscular dystrophy. Muscle Nerve 2015; 51: 918-921 DOI: 10.1002/mus.24629.
- 70 Bonati U, Hafner P, Schadelin S. et al. Quantitative muscle MRI: A powerful surrogate outcome measure in Duchenne muscular dystrophy. Neuromuscul Disord 2015; 25: 679-685 DOI: 10.1016/j.nmd.2015.05.006.
- 71 Godi C, Ambrosi A, Nicastro F. et al. Longitudinal MRI quantification of muscle degeneration in Duchenne muscular dystrophy. Ann Clin Transl Neurol 2016; 3: 607-622 DOI: 10.1002/acn3.319.
- 72 Ricotti V, Evans MR, Sinclair CD. et al. Upper Limb Evaluation in Duchenne Muscular Dystrophy: Fat-Water Quantification by MRI, Muscle Force and Function Define Endpoints for Clinical Trials. PLoS One 2016; 11: e0162542 DOI: 10.1371/journal.pone.0162542.
- 73 Nagy S, Schadelin S, Hafner P. et al. Longitudinal reliability of outcome measures in patients with Duchenne muscular dystrophy. Muscle Nerve 2020; 61: 63-68 DOI: 10.1002/mus.26690.
- 74 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: 974-980 DOI: 10.1212/WNL.0000000000000775.
- 75 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: e1386-e1394 DOI: 10.1212/WNL.0000000000008939.
- 76 Rooney WD, Berlow YA, Triplett WT. et al. Modeling disease trajectory in Duchenne muscular dystrophy. Neurology 2020; 94: e1622-e1633 DOI: 10.1212/WNL.0000000000009244.
- 77 Barnard AM, Willcocks RJ, Triplett WT. et al. MR biomarkers predict clinical function in Duchenne muscular dystrophy. Neurology 2020; 94: e897-e909 DOI: 10.1212/WNL.0000000000009012.
- 78 Janssen B, Voet N, Geurts A. et al. Quantitative MRI reveals decelerated fatty infiltration in muscles of active FSHD patients. Neurology 2016; 86: 1700-1707 DOI: 10.1212/WNL.0000000000002640.
- 79 Monforte M, Laschena F, Ottaviani P. et al. Tracking muscle wasting and disease activity in facioscapulohumeral muscular dystrophy by qualitative longitudinal imaging. J Cachexia Sarcopenia Muscle 2019; 10: 1258-1265 DOI: 10.1002/jcsm.12473.
- 80 Wang LH, Shaw DWW, Faino A. et al. Longitudinal study of MRI and functional outcome measures in facioscapulohumeral muscular dystrophy. BMC Musculoskelet Disord 2021; 22: 262 DOI: 10.1186/s12891-021-04134-7.
- 81 Lollert A, Stihl C, Hotker AM. et al. Quantification of intramuscular fat in patients with late-onset Pompe disease by conventional magnetic resonance imaging for the long-term follow-up of enzyme replacement therapy. PLoS One 2018; 13: e0190784 DOI: 10.1371/journal.pone.0190784.
- 82 Khan AA, Boggs T, Bowling M. et al. Whole-body magnetic resonance imaging in late-onset Pompe disease: Clinical utility and correlation with functional measures. J Inherit Metab Dis 2020; 43: 549-557 DOI: 10.1002/jimd.12190.
- 83 Ravaglia S, Pichiecchio A, Ponzio M. et al. Changes in skeletal muscle qualities during enzyme replacement therapy in late-onset type II glycogenosis: temporal and spatial pattern of mass vs. strength response. J Inherit Metab Dis 2010; 33: 737-745 DOI: 10.1007/s10545-010-9204-5.
- 84 van der Ploeg A, Carlier PG, Carlier RY. et al. Prospective exploratory muscle biopsy, imaging, and functional assessment in patients with late-onset Pompe disease treated with alglucosidase alfa: The EMBASSY Study. Mol Genet Metab 2016; 119: 115-123 DOI: 10.1016/j.ymgme.2016.05.013.
- 85 Reyngoudt H, Marty B, Caldas de Almeida Araujo E. et al. Relationship between markers of disease activity and progression in skeletal muscle of GNE myopathy patients using quantitative nuclear magnetic resonance imaging and (31)P nuclear magnetic resonance spectroscopy. Quant Imaging Med Surg 2020; 10: 1450-1464 DOI: 10.21037/qims-20-39.
- 86 Gidaro T, Reyngoudt H, Le Louer J. et al. Quantitative nuclear magnetic resonance imaging detects subclinical changes over 1 year in skeletal muscle of GNE myopathy. J Neurol 2020; 267: 228-238 DOI: 10.1007/s00415-019-09569-6.
- 87 Leung DG, Bocchieri AE, Ahlawat S. et al. Longitudinal functional and imaging outcome measures in FKRP limb-girdle muscular dystrophy. BMC Neurol 2020; 20: 196 DOI: 10.1186/s12883-020-01774-5.
- 88 Willis TA, Hollingsworth KG, Coombs A. et al. Quantitative muscle MRI as an assessment tool for monitoring disease progression in LGMD2I: a multicentre longitudinal study. PLoS One 2013; 8: e70993 DOI: 10.1371/journal.pone.0070993.
- 89 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: 1033-1045 DOI: 10.1002/acn3.774.
- 90 Fischmann A, Hafner P, Fasler S. et al. Quantitative MRI can detect subclinical disease progression in muscular dystrophy. J Neurol 2012; 259: 1648-1654 DOI: 10.1007/s00415-011-6393-2.
- 91 Otto LAM, Froeling M, van Eijk RPA. et al. Quantification of disease progression in spinal muscular atrophy with muscle MRI-a pilot study. NMR Biomed 2021; 34: e4473 DOI: 10.1002/nbm.4473.
- 92 Bonati U, Holiga S, Hellbach N. et al. Longitudinal characterization of biomarkers for spinal muscular atrophy. Ann Clin Transl Neurol 2017; 4: 292-304 DOI: 10.1002/acn3.406.
- 93 Annoussamy M, Seferian AM, Daron A. et al. Natural history of Type 2 and 3 spinal muscular atrophy: 2-year NatHis-SMA study. Ann Clin Transl Neurol 2021; 8: 359-373 DOI: 10.1002/acn3.51281.
- 94 Savini G, Asteggiano C, Paoletti M. et al. Pilot Study on Quantitative Cervical Cord and Muscular MRI in Spinal Muscular Atrophy: Promising Biomarkers of Disease Evolution and Treatment?. Front Neurol 2021; 12: 613834 DOI: 10.3389/fneur.2021.613834.
- 95 Barp A, Carraro E, Albamonte E. et al. Muscle MRI in two SMA patients on nusinersen treatment: A two years follow-up. J Neurol Sci 2020; 417: 117067 DOI: 10.1016/j.jns.2020.117067.