Semin Musculoskelet Radiol 2019; 23(03): e82-e106
DOI: 10.1055/s-0039-1684022
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Advanced MRI Patterns of Muscle Disease in Inherited and Acquired Myopathies: What the Radiologist Should Know

António Proença Caetano
1   Centro Hospitalar Universitário Lisboa Central, Lisboa, Portugal
,
Pedro Alves
1   Centro Hospitalar Universitário Lisboa Central, Lisboa, Portugal
› Author Affiliations
Further Information

Publication History

Publication Date:
04 June 2019 (online)

Abstract

Myopathies represent a heterogeneous group of skeletal muscle disorders characterized by morphological and functional changes in the muscle, such as replacement of muscle tissue by connective tissue, fatty infiltration, and/or inflammation. They can be classified as hereditary, acquired idiopathic, and secondary myopathies.

Diagnosis of hereditary and acquired myopathies is challenging, with often overlapping clinical and pathologic features, and it generally relies on a multimodal approach. Current imaging modalities used in neuromuscular imaging include computed tomography, ultrasound, and magnetic resonance imaging (MRI).

Topographical patterns of muscle involvement have been described for several myopathies, and they can be identified using whole-body MRI. Indeed, this technique has proven to be an invaluable tool for diagnostic work-up, guidance of muscle biopsy, and biochemical and genetic investigation, as well as disease monitoring and follow-up.

 
  • References

  • 1 Wattjes MP, Fischer D. Neuromuscular Imaging. New York, NY: Springer; 2013
  • 2 Domingo-Horne RM, Salajegheh MK. An approach to myopathy for the primary care clinician. Am J Med 2018; 131 (03) 237-243
  • 3 Ortolan P, Zanato R, Coran A, Beltrame V, Stramare R. Role of radiologic imaging in genetic and acquired neuromuscular disorders. Eur J Transl Myol 2015; 25 (02) 5014
  • 4 Frontera WR, Ochala J. Skeletal muscle: a brief review of structure and function. Calcif Tissue Int 2015; 96 (03) 183-195
  • 5 – Hall JE. Textbook of Medical Physiology. 13th ed. Philadelphia, PA: Saunders; 2015
  • 6 Huxley HE. Fifty years of muscle and the sliding filament hypothesis. Eur J Biochem 2004; 271 (08) 1403-1415
  • 7 Rahimov F, Kunkel LM. The cell biology of disease: cellular and molecular mechanisms underlying muscular dystrophy. J Cell Biol 2013; 201 (04) 499-510
  • 8 Janin A, Bauer D, Ratti F, Millat G, Méjat A. Nuclear envelopathies: a complex LINC between nuclear envelope and pathology. Orphanet J Rare Dis 2017; 12 (01) 147
  • 9 Rayavarapu S, Coley W, Kinder TB, Nagaraju K. Idiopathic inflammatory myopathies: pathogenic mechanisms of muscle weakness. Skelet Muscle 2013; 3 (01) 13
  • 10 Mercuri E, Pichiecchio A, Allsop J, Messina S, Pane M, Muntoni F. Muscle MRI in inherited neuromuscular disorders: past, present, and future. J Magn Reson Imaging 2007; 25 (02) 433-440
  • 11 Jungbluth H. Myopathology in times of modern imaging. Neuropathol Appl Neurobiol 2017; 43 (01) 24-43
  • 12 Politano L, Nigro G. Magnetic resonance imaging in muscular dystrophies. Acta Myol 2015; 34 (2-3): 93-94
  • 13 Carlier PG, Mercuri E, Straub V. Applications of MRI in muscle diseases. Neuromuscul Disord 2012; 22 (Suppl. 02) S41
  • 14 Filli L, Winklhofer S, Andreisek G, Del Grande F. Imaging of myopathies. Radiol Clin North Am 2017; 55 (05) 1055-1070
  • 15 Cieszanowski A, Maj E, Kulisiewicz P. , et al. Non-contrast-enhanced whole-body magnetic resonance imaging in the general population: the incidence of abnormal findings in patients 50 years old and younger compared to older subjects. PLoS One 2014; 9 (09) e107840
  • 16 - Díaz JD, Suazo RL, Castiglioni TC, Bevilacqua RJ. Utility of magnetic resonance imaging in the diagnosis of hereditary muscle diseases. Rev Chil Radiol 2015; 21 (04) 144-150
  • 17 Quijano-Roy S, Avila-Smirnow D, Carlier RY. ; WB-MRI muscle study group. Whole body muscle MRI protocol: pattern recognition in early onset NM disorders. Neuromuscul Disord 2012; 22 (Suppl. 02) S68-S84
  • 18 Elessawy SS, Abdelsalam EM, Abdel Razek E, Tharwat S. Whole-body MRI for full assessment and characterization of diffuse inflammatory myopathy. Acta Radiol Open 2016 ;5(9):2058460116668216
  • 19 Garrood P, Hollingsworth KG, Eagle M. , et al. MR imaging in Duchenne muscular dystrophy: quantification of T1-weighted signal, contrast uptake, and the effects of exercise. J Magn Reson Imaging 2009; 30 (05) 1130-1138
  • 20 Fischer D, Wattjes MP. MRI in muscle dystrophies and primary myopathies. In: Weber MA. , ed. Magnetic Resonance Imaging of the Skeletal Musculature. New York, NY: Springer; 2013: 241-254
  • 21 Dimachkie MM, Barohn RJ, Amato AA. Idiopathic inflammatory myopathies. Neurol Clin 2014; 32 (03) 595-628 , vii
  • 22 Damon BM, Li K, Dortch RD. , et al. Quantitative magnetic resonance imaging of skeletal muscle disease. J Vis Exp 2016; ;118. DOI: 10.3791/52352.
  • 23 Wong AK, Manske SL. A comparison of peripheral imaging technologies for bone and muscle quantification: a review of segmentation techniques. J Clin Densitom 2018 ; April 17 (Epub ahead of print)
  • 24 Weber MA, Nagel AM, Marschar AM. , et al. 7-T Cl and 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; 281 (01) 326
  • 25 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
  • 26 Noseworthy MD, Davis AD, Elzibak AH. Advanced MR imaging techniques for skeletal muscle evaluation. Semin Musculoskelet Radiol 2010; 14 (02) 257-268
  • 27 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
  • 28 Wokke BH, Van Den Bergen JC, Hooijmans MT, Verschuuren JJ, Niks EH, Kan HE. T2 relaxation times are increased in skeletal muscle of DMD but not BMD patients. Muscle Nerve 2016; 53 (01) 38-43
  • 29 Lareau-Trudel E, Le Troter A, Ghattas B. , et al. Muscle quantitative MR imaging and clustering analysis in patients with facioscapulohumeral muscular dystrophy type 1. PLoS One 2015; 10 (07) e0132717
  • 30 Al-Nahhas A, Jawad AS. PET/CT imaging in inflammatory myopathies. Ann N Y Acad Sci 2011; 1228 (01) 39-45
  • 31 Fischer D, Bonati U, Wattjes MP. Recent developments in muscle imaging of neuromuscular disorders. Curr Opin Neurol 2016; 29 (05) 614-620
  • 32 Weber MA, Wolf M, Wattjes MP. Imaging patterns of muscle atrophy. Semin Musculoskelet Radiol 2018; 22 (03) 299-306
  • 33 Ten Dam L, van der Kooi AJ, Verhamme C, Wattjes MP, de Visser M. Muscle imaging in inherited and acquired muscle diseases. Eur J Neurol 2016; 23 (04) 688-703
  • 34 May DA, Disler DG, Jones EA, Balkissoon AA, Manaster BJ. Abnormal signal intensity in skeletal muscle at MR imaging: patterns, pearls, and pitfalls. Radiographics 2000; 20 (Spec No): S295-S315
  • 35 Cotta A, Carvalho E, da-Cunha-Júnior AL. , et al. Common recessive limb girdle muscular dystrophies differential diagnosis: why and how?. Arq Neuropsiquiatr 2014; 72 (09) 721-734
  • 36 Mulcahy H, Chew FS. MRI of nontumorous skeletal muscle disease: case-based review. AJR Am J Roentgenol 2011; 196 (6, Suppl): S77-S85
  • 37 Ozsarlak O, Schepens E, Parizel PM. , et al. Hereditary neuromuscular diseases. Eur J Radiol 2001; 40 (03) 184-197
  • 38 Maurer B, Walker UA. Role of MRI in diagnosis and management of idiopathic inflammatory myopathies. Curr Rheumatol Rep 2015; 17 (11) 67
  • 39 Poliachik SL, Friedman SD, Carter GT, Parnell SE, Shaw DW. Skeletal muscle edema in muscular dystrophy: clinical and diagnostic implications. Phys Med Rehabil Clin N Am 2012; 23 (01) 107-122 , xi
  • 40 Díaz-Manera J, Llauger J, Gallardo E, Illa I. Muscle MRI in muscular dystrophies. Acta Myol 2015; 34 (2–3(: 95-108
  • 41 Wattjes MP, Kley RA, Fischer D. Neuromuscular imaging in inherited muscle diseases. Eur Radiol 2010; 20 (10) 2447-2460
  • 42 Tomasová Studynková J, Charvát F, Jarosová K, Vencovsky J. The role of MRI in the assessment of polymyositis and dermatomyositis. Rheumatology (Oxford) 2007; 46 (07) 1174-1179
  • 43 Schulze M, Kötter I, Ernemann U. , et al. MRI findings in inflammatory muscle diseases and their noninflammatory mimics. AJR Am J Roentgenol 2009; 192 (06) 1708-1716
  • 44 Adams EM, Chow CK, Premkumar A, Plotz PH. The idiopathic inflammatory myopathies: spectrum of MR imaging findings. Radiographics 1995; 15 (03) 563-574
  • 45 Barohn RJ, Dimachkie MM, Jackson CE. A pattern recognition approach to patients with a suspected myopathy. Neurol Clin 2014; 32 (03) 569-593 , vii
  • 46 Statland J, Tawil R. Facioscapulohumeral muscular dystrophy. Neurol Clin 2014; 32 (03) 721-728 , ix PubMed
  • 47 Guimaraes JB, Zanoteli E, Link TM. , et al. Sporadic inclusion body myositis: MRI findings and correlation with clinical and functional parameters. AJR Am J Roentgenol 2017; 209 (06) 1340-1347
  • 48 Díaz-Manera J, Alejaldre A, González L. , et al. Muscle imaging in muscle dystrophies produced by mutations in the EMD and LMNA genes. Neuromuscul Disord 2016; 26 (01) 33-40
  • 49 Rosales XQ, Gastier-Foster JM, Lewis S. , et al. Novel diagnostic features of dysferlinopathies. Muscle Nerve 2010; 42 (01) 14-21
  • 50 Degardin A, Morillon D, Lacour A, Cotten A, Vermersch P, Stojkovic T. Morphologic imaging in muscular dystrophies and inflammatory myopathies. Skeletal Radiol 2010; 39 (12) 1219-1227
  • 51 Dlamini N, Jan W, Norwood F. , et al. Muscle MRI findings in siblings with juvenile-onset acid maltase deficiency (Pompe disease). Neuromuscul Disord 2008; 18 (05) 408-409
  • 52 Pichiecchio A, Uggetti C, Ravaglia S. , et al. Muscle MRI in adult-onset acid maltase deficiency. Neuromuscul Disord 2004; 14 (01) 51-55
  • 53 Figueroa-Bonaparte S, Segovia S, Llauger J. , et al; Spanish Pompe Study Group. Muscle MRI findings in childhood/adult onset Pompe disease correlate with muscle function. PLoS One 2016; 11 (10) e0163493
  • 54 ten Dam L, van der Kooi AJ, van Wattingen M, de Haan RJ, de Visser M. Reliability and accuracy of skeletal muscle imaging in limb-girdle muscular dystrophies. Neurology 2012; 79 (16) 1716-1723
  • 55 Tasca G, Monforte M, Díaz-Manera J. , et al; MRI in sarcoglycanopathies: a large international cohort study. J Neurol Neurosurg Psychiatry 2017; 0: 1-6
  • 56 Tasca G, Monforte M, Iannaccone E. , et al. Upper girdle imaging in facioscapulohumeral muscular dystrophy. PLoS One 2014; 9 (06) e100292
  • 57 Bönnemann CG. The collagen VI-related myopathies Ullrich congenital muscular dystrophy and Bethlem myopathy. Handb Clin Neurol 2011; 101: 81-96
  • 58 Palmio J, Udd B. Borderlines between sarcopenia and mild late-onset muscle disease. Front Aging Neurosci 2014; 6: 267
  • 59 Mercuri E, Talim B, Moghadaszadeh B. , et al. Clinical and imaging findings in six cases of congenital muscular dystrophy with rigid spine syndrome linked to chromosome 1p (RSMD1). Neuromuscul Disord 2002; 12 (7-8): 631-638
  • 60 Finanger EL, Russman B, Forbes SC, Rooney WD, Walter GA, Vandenborne K. Use of skeletal muscle MRI in diagnosis and monitoring disease progression in Duchenne muscular dystrophy. Phys Med Rehabil Clin N Am 2012; 23 (01) 1-10 , ix
  • 61 Barp A, Bello L, Caumo L. , et al. Muscle MRI and functional outcome measures in Becker muscular dystrophy. Sci Rep 2017; 7 (01) 16060
  • 62 Polavarapu K, Manjunath M, Preethish-Kumar V. , et al. Muscle MRI in Duchenne muscular dystrophy: evidence of a distinctive pattern. Neuromuscul Disord 2016; 26 (11) 768-774
  • 63 Flanigan KM. Duchenne and Becker muscular dystrophies. Neurol Clin 2014; 32 (03) 671-688 , viii
  • 64 Cox FM, Reijnierse M, van Rijswijk CS, Wintzen AR, Verschuuren JJ, Badrising UA. Magnetic resonance imaging of skeletal muscles in sporadic inclusion body myositis. Rheumatology (Oxford) 2011; 50 (06) 1153-1161
  • 65 Liewluck T, Milone M. Liewluck T1. Untangling the complexity of limb-girdle muscular dystrophies. Muscle Nerve 2018; 58 (02) 167-177
  • 66 Stramare R, Beltrame V, Dal Borgo R. , et al. MRI in the assessment of muscular pathology: a comparison between limb-girdle muscular dystrophies, hyaline body myopathies and myotonic dystrophies. Radiol Med (Torino) 2010; 115 (04) 585-599
  • 67 - ten Dam L, van der Kooi AJ, van Wattingen M, de Haan RJ, Visser M. Reliability and accuracy of skeletal muscle imaging in limb-girdle muscular dystrophies. Neurology 2013; 80 (24) 2276
  • 68 Shieh PB. Muscular dystrophies and other genetic myopathies. Neurol Clin 2013; 31 (04) 1009-1029
  • 69 Deenen JC, Arnts H, van der Maarel SM. , et al. Population-based incidence and prevalence of facioscapulohumeral dystrophy. Neurology 2014; 83 (12) 1056-1059
  • 70 Wijmenga C, Hewitt JE, Sandkuijl LA. , et al. Chromosome 4q DNA rearrangements associated with facioscapulohumeral muscular dystrophy. Nat Genet 1992; 2 (01) 26-30
  • 71 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
  • 72 Fatehi F, Salort-Campana E, Le Troter A, Bendahan D, Attarian S. Muscle MRI of facioscapulohumeral dystrophy (FSHD): a growing demand and a promising approach. Rev Neurol (Paris) 2016; 172 (10) 566-571
  • 73 Reed UC. Congenital muscular dystrophy. Part I: a review of phenotypical and diagnostic aspects. Arq Neuropsiquiatr 2009; 67 (01) 144-168
  • 74 Mercuri E, Muntoni F. The ever-expanding spectrum of congenital muscular dystrophies. Ann Neurol 2012; 72 (01) 9-17
  • 75 Bönnemann CG, Wang CH, Quijano-Roy S. , et al; Members of International Standard of Care Committee for Congenital Muscular Dystrophies. Diagnostic approach to the congenital muscular dystrophies. Neuromuscul Disord 2014; 24 (04) 289-311
  • 76 Kim SY, Kim WJ, Kim H. , et al. Collagen VI-related myopathy: expanding the clinical and genetic spectrum. Muscle Nerve 2018; 58 (03) 381-388
  • 77 Mercuri E, Lampe A, Allsop J. , et al. Muscle MRI in Ullrich congenital muscular dystrophy and Bethlem myopathy. Neuromuscul Disord 2005; 15 (04) 303-310
  • 78 Rodríguez MA, Del Rio Barquero LM, Ortez CI. , et al. Differences in adipose tissue and lean mass distribution in patients with collagen VI related myopathies are associated with disease severity and physical ability. Front Aging Neurosci 2017; 9: 268
  • 79 Chi YH, Chen ZJ, Jeang KT. The nuclear envelopathies and human diseases. J Biomed Sci 2009; 16: 96
  • 80 Dimachkie MM, Barohn RJ. Distal myopathies. Neurol Clin 2014; 32 (03) 817-842 , x
  • 81 Palmio J, Udd B. Myofibrillar and distal myopathies. Rev Neurol (Paris) 2016; 172 (10) 587-593
  • 82 Strach K, Sommer T, Grohé C. , et al. Clinical, genetic, and cardiac magnetic resonance imaging findings in primary desminopathies. Neuromuscul Disord 2008; 18 (06) 475-482
  • 83 Selcen D. Myofibrillar myopathies. Neuromuscul Disord 2011; 21 (03) 161-171
  • 84 Olivé M, Odgerel Z, Martínez A. , et al. Clinical and myopathological evaluation of early- and late-onset subtypes of myofibrillar myopathy. Neuromuscul Disord 2011; 21 (08) 533-542
  • 85 Timchenko L. Molecular mechanisms of muscle atrophy in myotonic dystrophies. Int J Biochem Cell Biol 2013; 45 (10) 2280-2287
  • 86 Mah JK, Korngut L, Fiest KM. , et al. A systematic review and meta-analysis on the epidemiology of the muscular dystrophies. Can J Neurol Sci 2016; 43 (01) 163-177
  • 87 Thornton CA. Myotonic dystrophy. Neurol Clin 2014; 32 (03) 705-719 , viii
  • 88 Castillo J, Pumar JM, Rodríguez JR. , et al. Magnetic resonance imaging of muscles in myotonic dystrophy. Eur J Radiol 1993; 17 (03) 141-144
  • 89 Bachmann G, Damian MS, Koch M, Schilling G, Fach B, Stöppler S. The clinical and genetic correlates of MRI findings in myotonic dystrophy. Neuroradiology 1996; 38 (07) 629-635
  • 90 Peric S, Maksimovic R, Banko B. , et al. Magnetic resonance imaging of leg muscles in patients with myotonic dystrophies. J Neurol 2017; 264 (09) 1899-1908
  • 91 Park D, Lee SH, Shin JH, Park JS. Lower limb muscle magnetic resonance imaging in myotonic dystrophy type 1 correlates with the six-minute walk test and CTG repeats. Neuromuscul Disord 2018; 28 (01) 29-37
  • 92 Hayashi K, Hamano T, Kawamura Y. , et al. Muscle MRI of the upper extremity in the myotonic dystrophy type 1. Eur Neurol 2016; 76 (1-2): 87-94
  • 93 Toscano A, Barca E, Musumeci O. Update on diagnostics of metabolic myopathies. Curr Opin Neurol 2017; 30 (05) 553-562
  • 94 Dasouki M, Jawdat O, Almadhoun O. , et al. Pompe disease: literature review and case series. Neurol Clin 2014; 32 (03) 751-776 , ix ix
  • 95 Alejaldre A, Díaz-Manera J, Ravaglia S. , et al. Trunk muscle involvement in late-onset Pompe disease: study of thirty patients. Neuromuscul Disord 2012; 22 (Suppl. 02) S148-S154
  • 96 Pichiecchio A, Rossi M, Cinnante C. , et al. Muscle MRI of classic infantile Pompe patients: fatty substitution and edema-like changes. Muscle Nerve 2017; 55 (06) 841-848
  • 97 North KN, Wang CH, Clarke N. , et al; International Standard of Care Committee for Congenital Myopathies. Approach to the diagnosis of congenital myopathies. Neuromuscul Disord 2014; 24 (02) 97-116
  • 98 Susman RD, Quijano-Roy S, Yang N. , et al. Expanding the clinical, pathological and MRI phenotype of DNM2-related centronuclear myopathy. Neuromuscul Disord 2010; 20 (04) 229-237
  • 99 Lehtokari VL, Pelin K, Herczegfalvi A. , et al. Nemaline myopathy caused by mutations in the nebulin gene may present as a distal myopathy. Neuromuscul Disord 2011; 21 (08) 556-562
  • 100 Romero NB, Lehtokari VL, Quijano-Roy S. , et al. Core-rod myopathy caused by mutations in the nebulin gene. Neurology 2009; 73 (14) 1159-1161
  • 101 Cassandrini D, Trovato R, Rubegni A. , et al; Italian Network on Congenital Myopathies. Congenital myopathies: clinical phenotypes and new diagnostic tools. Ital J Pediatr 2017; 43 (01) 101
  • 102 Quijano-Roy S, Carlier RY, Fischer D. Muscle imaging in congenital myopathies. Semin Pediatr Neurol 2011; 18 (04) 221-229
  • 103 Spillane J, Fialho D, Hanna MG. Diagnosis of skeletal muscle channelopathies. Expert Opin Med Diagn 2013; 7 (06) 517-529
  • 104 Morrow JM, Matthews E, Raja Rayan DL. , et al. Muscle MRI reveals distinct abnormalities in genetically proven non-dystrophic myotonias. Neuromuscul Disord 2013; 23 (08) 637-646
  • 105 Maggi L, Brugnoni R, Canioni E, Maccagnano E, Bernasconi P, Morandi L. Imaging alterations in skeletal muscle channelopathies: a study in 15 patients. Acta Myol 2015; 34 (2-3): 109-115
  • 106 Weber MA, Nielles-Vallespin S, Essig M, Jurkat-Rott K, Kauczor HU, Lehmann-Horn F. Muscle Na+ channelopathies: MRI detects intracellular 23Na accumulation during episodic weakness. Neurology 2006; 67 (07) 1151-1158
  • 107 O'Connell MJ, Powell T, Brennan D, Lynch T, McCarthy CJ, Eustace SJ. Whole-body MR imaging in the diagnosis of polymyositis. AJR Am J Roentgenol 2002; 179 (04) 967-971
  • 108 Kissel JT. Misunderstandings, misperceptions, and mistakes in the management of the inflammatory myopathies. Semin Neurol 2002; 22 (01) 41-51
  • 109 Allenbach Y, Benveniste O. Peculiar clinicopathological features of immune-mediated necrotizing myopathies. Curr Opin Rheumatol 2018; 30 (06) 655-663
  • 110 McGrath ER, Doughty CT, Amato AA. Autoimmune myopathies: updates on evaluation and treatment. Neurotherapeutics 2018; 15 (04) 976-994
  • 111 Khan NAJ, Khalid S, Ullah S, Malik MU, Makhoul S. Necrotizing autoimmune myopathy: a rare variant of idiopathic inflammatory myopathies. J Investig Med High Impact Case Rep 2017 ;5(2):2324709617709031
  • 112 Pinal-Fernandez I, Casal-Dominguez M, Carrino JA. , et al. Thigh muscle MRI in immune-mediated necrotising myopathy: extensive oedema, early muscle damage and role of anti-SRP autoantibodies as a marker of severity. Ann Rheum Dis 2017; 76 (04) 681-687
  • 113 Finsterer J, Löscher WN, Wanschitz J, Quasthoff S, Grisold W. Secondary myopathy due to systemic diseases. Acta Neurol Scand 2016; 134 (06) 388-402