Imaging of Myopathies

Radiologic Clinics of North America

Volumn 55, Issue 5, 2017, Pages 1055-1070

  Filli, Lukas ^a   Winklhofer, Sebastian ^b   Andreisek, Gustav ^c,d   Del Grande, Filippo ^d,e  

^a University Hospital Zurich Institut fur Diagnostische Radiologie   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^c Kantonsspital Muensterlingen   (Switzerland)

^d UNIVERSITY OF ZURICH   (Switzerland)

^e REGIONAL HOSPITAL OF LUGANO   (Switzerland)

Author keywords

MR imaging; Muscle dystrophy; Myopathy; Myositis; Skeletal muscle

Indexed keywords

ARTERIAL SPIN LABELING; BECKER MUSCULAR DYSTROPHY; BODY COMPOSITION; BOLD SIGNAL; DERMATOMYOSITIS; DIFFUSION TENSOR IMAGING; DISEASE COURSE; DUCHENNE MUSCULAR DYSTROPHY; GENETIC ANALYSIS; HUMAN; INCLUSION BODY MYOSITIS; LIMB GIRDLE MUSCULAR DYSTROPHY; MAGNETIC RESONANCE ELASTOGRAPHY; MUSCLE BIOPSY; MYOTONIC DYSTROPHY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; POLYMYOSITIS; PRIORITY JOURNAL; QUALITATIVE ANALYSIS; QUANTITATIVE ANALYSIS; REVIEW; SENSITIVITY AND SPECIFICITY; SYSTEMIC SCLEROSIS; WHOLE BODY MRI; DIAGNOSTIC IMAGING; MUSCLE DISEASE; NUCLEAR MAGNETIC RESONANCE IMAGING; PROCEDURES; SKELETAL MUSCLE;

HUMANS; MAGNETIC RESONANCE IMAGING; MUSCLE, SKELETAL; MUSCULAR DISEASES;

EID: 85030417027     PISSN: 00338389     EISSN: 15578275     Source Type: Journal    
DOI: 10.1016/j.rcl.2017.04.010     Document Type: Review

References (95)

1. Lenk, S., Fischer, S., Kotter, I., et al. Possibilities of whole-body MRI for investigating musculoskeletal diseases. Radiologe 44:9 (2004), 844–853 [in German].
2. Schmidt, G.P., Reiser, M.F., Baur-Melnyk, A., Whole-body imaging of the musculoskeletal system: the value of MR imaging. Skeletal Radiol 36:12 (2007), 1109–1119.
3. Filli, L., Maurer, B., Manoliu, A., et al. Whole-body MRI in adult inflammatory myopathies: do we need imaging of the trunk?. Eur Radiol 25:12 (2015), 3499–3507.
4. Schulze, M., Kotter, I., Ernemann, U., et al. MRI findings in inflammatory muscle diseases and their noninflammatory mimics. AJR Am J Roentgenol 192:6 (2009), 1708–1716.
5. Garcia, J., MRI in inflammatory myopathies. Skeletal Radiol 29:8 (2000), 425–438.
6. May, D.A., Disler, D.G., Jones, E.A., et al. Abnormal signal intensity in skeletal muscle at MR imaging: patterns, pearls, and pitfalls. Radiographics 20 (2000), S295–S315.
7. Van De Vlekkert, J., Maas, M., Hoogendijk, J.E., et al. Combining MRI and muscle biopsy improves diagnostic accuracy in subacute-onset idiopathic inflammatory myopathy. Muscle Nerve 51:2 (2015), 253–258.
8. Del Grande, F., Carrino, J.A., Del Grande, M., et al. Magnetic resonance imaging of inflammatory myopathies. Top Magn Reson Imaging 22:2 (2011), 39–43.
9. Boutry, N., Hachulla, E., Zanetti-Musielak, C., et al. Imaging features of musculoskeletal involvement in systemic sclerosis. Eur Radiol 17:5 (2007), 1172–1180.
10. Schick, F., Whole-body MRI at high field: technical limits and clinical potential. Eur Radiol 15:5 (2005), 946–959.
11. Sookhoo, S., Mackinnon, I., Bushby, K., et al. MRI for the demonstration of subclinical muscle involvement in muscular dystrophy. Clin Radiol 62:2 (2007), 160–165.
12. Shelly, M.J., Bolster, F., Foran, P., et al. Whole-body magnetic resonance imaging in skeletal muscle disease. Semin Musculoskelet Radiol 14:1 (2010), 47–56.
13. Connor, A., Stebbings, S., Anne Hung, N., et al. STIR MRI to direct muscle biopsy in suspected idiopathic inflammatory myopathy. J Clin Rheumatol 13:6 (2007), 341–345.
14. Bashir, W.A., O'Donnell, P., The myositides: the role of imaging in diagnosis and treatment. Semin Musculoskelet Radiol 14:2 (2010), 217–226.
15. Dalakas, M.C., Inflammatory muscle diseases. N Engl J Med 373:4 (2015), 393–394.
16. Dobloug, C., Garen, T., Bitter, H., et al. Prevalence and clinical characteristics of adult polymyositis and dermatomyositis; data from a large and unselected Norwegian cohort. Ann Rheum Dis 74:8 (2015), 1551–1556.
17. O'Connell, M.J., Powell, T., Brennan, D., et al. Whole-body MR imaging in the diagnosis of polymyositis. AJR Am J Roentgenol 179:4 (2002), 967–971.
18. Schweitzer, M.E., Fort, J., Cost-effectiveness of MR imaging in evaluating polymyositis. AJR Am J Roentgenol 165:6 (1995), 1469–1471.
19. Dion, E., Cherin, P., Payan, C., et al. Magnetic resonance imaging criteria for distinguishing between inclusion body myositis and polymyositis. J Rheumatol 29:9 (2002), 1897–1906.
20. Harris-Love, M.O., Shrader, J.A., Koziol, D., et al. Distribution and severity of weakness among patients with polymyositis, dermatomyositis and juvenile dermatomyositis. Rheumatology 48:2 (2009), 134–139.
21. Maurer, B., Walker, U.A., Role of MRI in diagnosis and management of idiopathic inflammatory myopathies. Curr Rheumatol Rep, 17(11), 2015, 67.
22. Tomasova Studynkova, J., Charvat, F., Jarosova, K., et al. The role of MRI in the assessment of polymyositis and dermatomyositis. Rheumatology 46:7 (2007), 1174–1179.
23. Greenberg, S.A., Inclusion body myositis. Curr Opin Rheumatol 23:6 (2011), 574–578.
24. Kissel, J.T., Misunderstandings, misperceptions, and mistakes in the management of the inflammatory myopathies. Semin Neurol 22:1 (2002), 41–51.
25. Cox, F.M., Reijnierse, M., van Rijswijk, C.S., et al. Magnetic resonance imaging of skeletal muscles in sporadic inclusion body myositis. Rheumatology 50:6 (2011), 1153–1161.
26. Tasca, G., Monforte, M., De Fino, C., et al. Magnetic resonance imaging pattern recognition in sporadic inclusion-body myositis. Muscle Nerve 52:6 (2015), 956–962.
27. Badrising, U.A., Maat-Schieman, M.L., van Houwelingen, J.C., et al. Inclusion body myositis. Clinical features and clinical course of the disease in 64 patients. J Neurol 252:12 (2005), 1448–1454.
28. Degardin, A., Morillon, D., Lacour, A., et al. Morphologic imaging in muscular dystrophies and inflammatory myopathies. Skeletal Radiol 39:12 (2010), 1219–1227.
29. Lamminen, A.E., Magnetic resonance imaging of primary skeletal muscle diseases: patterns of distribution and severity of involvement. Br J Radiol 63:756 (1990), 946–950.
30. Amato, A.A., Sivakumar, K., Goyal, N., et al. Treatment of sporadic inclusion body myositis with bimagrumab. Neurology 83:24 (2014), 2239–2246.
31. Schanz, S., Henes, J., Ulmer, A., et al. Magnetic resonance imaging findings in patients with systemic scleroderma and musculoskeletal symptoms. Eur Radiol 23:1 (2013), 212–221.
32. Low, A.H., Lax, M., Johnson, S.R., et al. Magnetic resonance imaging of the hand in systemic sclerosis. J Rheumatol 36:5 (2009), 961–964.
33. Finanger, E.L., Russman, B., Forbes, S.C., et al. Use of skeletal muscle MRI in diagnosis and monitoring disease progression in Duchenne muscular dystrophy. Phys Med Rehabil Clin N Am 23:1 (2012), 1–10 ix.
34. Mazzone, E., Vasco, G., Sormani, M.P., et al. Functional changes in Duchenne muscular dystrophy: a 12-month longitudinal cohort study. Neurology 77:3 (2011), 250–256.
35. 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 12:7–8 (2002), 631–638.
36. Forbes, S.C., Willcocks, R.J., Triplett, W.T., et al. Magnetic resonance imaging and spectroscopy assessment of lower extremity skeletal muscles in boys with Duchenne muscular dystrophy: a multicenter cross sectional study. PLoS One, 9(9), 2014, e106435.
37. Forbes, S.C., Lott, D.J., Finkel, R.S., et al. MRI/MRS evaluation of a female carrier of Duchenne muscular dystrophy. Neuromuscul Disord 22:Suppl 2 (2012), S111–S121.
38. Wren, T.A., Bluml, S., Tseng-Ong, L., et al. Three-point technique of fat quantification of muscle tissue as a marker of disease progression in Duchenne muscular dystrophy: preliminary study. AJR Am J Roentgenol 190:1 (2008), W8–W12.
39. Garrood, P., Hollingsworth, K.G., 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 30:5 (2009), 1130–1138.
40. Fischmann, A., Hafner, P., Gloor, M., et al. Quantitative MRI and loss of free ambulation in Duchenne muscular dystrophy. J Neurol 260:4 (2013), 969–974.
41. Willcocks, R.J., Arpan, I.A., Forbes, S.C., et al. Longitudinal measurements of MRI-T2 in boys with Duchenne muscular dystrophy: effects of age and disease progression. Neuromuscul Disord 24:5 (2014), 393–401.
42. Gaeta, M., Messina, S., Mileto, A., et al. Muscle fat-fraction and mapping in Duchenne muscular dystrophy: evaluation of disease distribution and correlation with clinical assessments. Preliminary experience. Skeletal Radiol 41:8 (2012), 955–961.
43. Bonati, U., Hafner, P., Schadelin, S., et al. Quantitative muscle MRI: a powerful surrogate outcome measure in Duchenne muscular dystrophy. Neuromuscul Disord 25:9 (2015), 679–685.
44. 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 28:9 (2015), 1150–1162.
45. Dixon, W.T., Simple proton spectroscopic imaging. Radiology 153:1 (1984), 189–194.
46. Filli, L., Ulbrich, E.J., Guggenberger, R., et al. Effect of Gd-DOTA on fat quantification in skeletal muscle using two-point Dixon technique - preliminary data. Eur J Radiol 85:1 (2016), 131–135.
47. Wokke, B.H., Bos, C., Reijnierse, M., et al. Comparison of dixon and T1-weighted MR methods to assess the degree of fat infiltration in Duchenne muscular dystrophy patients. J Magn Reson Imaging 38:3 (2013), 619–624.
48. Arpan, I., Forbes, S.C., Lott, D.J., et al. T(2) mapping provides multiple approaches for the characterization of muscle involvement in neuromuscular diseases: a cross-sectional study of lower leg muscles in 5-15-year-old boys with Duchenne muscular dystrophy. NMR Biomed 26:3 (2013), 320–328.
49. Kim, H.K., Laor, T., Horn, P.S., et al. T2 mapping in Duchenne muscular dystrophy: distribution of disease activity and correlation with clinical assessments. Radiology 255:3 (2010), 899–908.
50. Marden, F.A., Connolly, A.M., Siegel, M.J., et al. Compositional analysis of muscle in boys with Duchenne muscular dystrophy using MR imaging. Skeletal Radiol 34:3 (2005), 140–148.
51. Mathur, S., Lott, D.J., Senesac, C., et al. Age-related differences in lower-limb muscle cross-sectional area and torque production in boys with Duchenne muscular dystrophy. Arch Phys Med Rehabil 91:7 (2010), 1051–1058.
52. Mavrogeni, S., Papavasiliou, A., Douskou, M., et al. Effect of deflazacort on cardiac and sternocleidomastoid muscles in Duchenne muscular dystrophy: a magnetic resonance imaging study. Eur J paediatric Neurol 13:1 (2009), 34–40.
53. Arpan, I., Willcocks, R.J., Forbes, S.C., et al. Examination of effects of corticosteroids on skeletal muscles of boys with DMD using MRI and MRS. Neurology 83:11 (2014), 974–980.
54. Willcocks, R.J., Rooney, W.D., Triplett, W.T., et al. Multicenter prospective longitudinal study of magnetic resonance biomarkers in a large Duchenne muscular dystrophy cohort. Ann Neurol 79:4 (2016), 535–547.
55. Polavarapu, K., Manjunath, M., Preethish-Kumar, V., et al. Muscle MRI in Duchenne muscular dystrophy: evidence of a distinctive pattern. Neuromuscul Disord 26:11 (2016), 768–774.
56. Tasca, G., Iannaccone, E., Monforte, M., et al. Muscle MRI in Becker muscular dystrophy. Neuromuscul Disord 22:Suppl 2 (2012), S100–S106.
57. Faridian-Aragh, N., Wagner, K.R., Leung, D.G., et al. Magnetic resonance imaging phenotyping of Becker muscular dystrophy. Muscle Nerve 50:6 (2014), 962–967.
58. Fischer, D., Hafner, P., Rubino, D., et al. The 6-minute walk test, motor function measure and quantitative thigh muscle MRI in Becker muscular dystrophy: a cross-sectional study. Neuromuscul Disord 26:7 (2016), 414–422.
59. Wagner, K.R., Fleckenstein, J.L., Amato, A.A., et al. A phase I/II trial of MYO-029 in adult subjects with muscular dystrophy. Ann Neurol 63:5 (2008), 561–571.
60. Mercuri, E., Bushby, K., Ricci, E., et al. Muscle MRI findings in patients with limb girdle muscular dystrophy with calpain 3 deficiency (LGMD2A) and early contractures. Neuromuscul Disord 15:2 (2005), 164–171.
61. Fischer, D., Walter, M.C., Kesper, K., et al. Diagnostic value of muscle MRI in differentiating LGMD2I from other LGMDs. J Neurol 252:5 (2005), 538–547.
62. Wattjes, M.P., Kley, R.A., Fischer, D., Neuromuscular imaging in inherited muscle diseases. Eur Radiol 20:10 (2010), 2447–2460.
63. Hicks, D., Sarkozy, A., Muelas, N., et al. A founder mutation in Anoctamin 5 is a major cause of limb-girdle muscular dystrophy. Brain 134:Pt 1 (2011), 171–182.
64. Kesper, K., Kornblum, C., Reimann, J., et al. Pattern of skeletal muscle involvement in primary dysferlinopathies: a whole-body 3.0-T magnetic resonance imaging study. Acta Neurol Scand 120:2 (2009), 111–118.
65. Sarkozy, A., Deschauer, M., Carlier, R.Y., et al. Muscle MRI findings in limb girdle muscular dystrophy type 2L. Neuromuscul Disord 22:Suppl 2 (2012), S122–S129.
66. Brummer, D., Walter, M.C., Palmbach, M., et al. Long-term MRI and clinical follow-up of symptomatic and presymptomatic carriers of dysferlin gene mutations. Acta Myol 24:1 (2005), 6–16.
67. Kornblum, C., Lutterbey, G.G., Czermin, B., et al. Whole-body high-field MRI shows no skeletal muscle degeneration in young patients with recessive myotonia congenita. Acta Neurol Scand 121:2 (2010), 131–135.
68. Day, J.W., Ricker, K., Jacobsen, J.F., et al. Myotonic dystrophy type 2: molecular, diagnostic and clinical spectrum. Neurology 60:4 (2003), 657–664.
69. Fleckenstein, J.L., MRI of neuromuscular disease: the basics. Semin Musculoskelet Radiol 4:4 (2000), 393–419.
70. Jungbluth, H., Davis, M.R., Muller, C., et al. Magnetic resonance imaging of muscle in congenital myopathies associated with RYR1 mutations. Neuromuscul Disord 14:12 (2004), 785–790.
71. Klein, A., Jungbluth, H., Clement, E., et al. Muscle magnetic resonance imaging in congenital myopathies due to ryanodine receptor type 1 gene mutations. Arch Neurol 68:9 (2011), 1171–1179.
72. Quijano-Roy, S., Carlier, R.Y., Fischer, D., Muscle imaging in congenital myopathies. Semin Pediatr Neurol 18:4 (2011), 221–229.
73. Raynaud, J.S., Duteil, S., Vaughan, J.T., et al. Determination of skeletal muscle perfusion using arterial spin labeling NMRI: validation by comparison with venous occlusion plethysmography. Magn Reson Med 46:2 (2001), 305–311.
74. Andreisek, G., White, L.M., Sussman, M.S., et al. T2*-weighted and arterial spin labeling MRI of calf muscles in healthy volunteers and patients with chronic exertional compartment syndrome: preliminary experience. AJR Am J Roentgenol 193:4 (2009), W327–W333.
75. Partovi, S., Karimi, S., Jacobi, B., et al. Clinical implications of skeletal muscle blood-oxygenation-level-dependent (BOLD) MRI. Magma 25:4 (2012), 251–261.
76. Ledermann, H.P., Heidecker, H.G., Schulte, A.C., et al. Calf muscles imaged at BOLD MR: correlation with TcPO2 and flowmetry measurements during ischemia and reactive hyperemia–initial experience. Radiology 241:2 (2006), 477–484.
77. Meyer, R.A., Towse, T.F., Reid, R.W., et al. BOLD MRI mapping of transient hyperemia in skeletal muscle after single contractions. NMR Biomed 17:6 (2004), 392–398.
78. Jacobi, B., Bongartz, G., Partovi, S., et al. Skeletal muscle BOLD MRI: from underlying physiological concepts to its usefulness in clinical conditions. J Magn Reson Imaging 35:6 (2012), 1253–1265.
79. Partovi, S., Schulte, A.C., Aschwanden, M., et al. Impaired skeletal muscle microcirculation in systemic sclerosis. Arthritis Res Ther, 14(5), 2012, R209.
80. Qi, J., Olsen, N.J., Price, R.R., et al. Diffusion-weighted imaging of inflammatory myopathies: polymyositis and dermatomyositis. J Magn Reson Imaging 27:1 (2008), 212–217.
81. Ai, T., Yu, K., Gao, L., et al. Diffusion tensor imaging in evaluation of thigh muscles in patients with polymyositis and dermatomyositis. Br J Radiol, 87(1043), 2014, 20140261.
82. Filli, L., Piccirelli, M., Kenkel, D., et al. Simultaneous multislice echo planar imaging with blipped controlled aliasing in parallel imaging results in higher acceleration: a promising technique for accelerated diffusion tensor imaging of skeletal muscle. Invest Radiol 50:7 (2015), 456–463.
83. Ponrartana, S., Ramos-Platt, L., Wren, T.A., et al. Effectiveness of diffusion tensor imaging in assessing disease severity in Duchenne muscular dystrophy: preliminary study. Pediatr Radiol 45:4 (2015), 582–589.
84. Le Bihan, D., Breton, E., Lallemand, D., et al. MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161:2 (1986), 401–407.
85. Filli, L., Boss, A., Wurnig, M.C., et al. Dynamic intravoxel incoherent motion imaging of skeletal muscle at rest and after exercise. NMR Biomed 28:2 (2015), 240–246.
86. Torriani, M., Townsend, E., Thomas, B.J., et al. Lower leg muscle involvement in Duchenne muscular dystrophy: an MR imaging and spectroscopy study. Skeletal Radiol 41:4 (2012), 437–445.
87. Kan, H.E., Klomp, D.W., Wong, C.S., et al. In vivo 31P MRS detection of an alkaline inorganic phosphate pool with short T1 in human resting skeletal muscle. NMR Biomed 23:8 (2010), 995–1000.
88. Amarteifio, E., Nagel, A.M., Kauczor, H.U., et al. Functional imaging in muscular diseases. Insights Imaging 2:5 (2011), 609–619.
89. Okuma, H., Kurita, D., Ohnuki, T., et al. Muscle metabolism in patients with polymyositis simultaneously evaluated by using 31P-magnetic resonance spectroscopy and near-infrared spectroscopy. Int J Clin Pract 61:4 (2007), 684–689.
90. Park, J.H., Olsen, N.J., King, L. Jr., et al. Use of magnetic resonance imaging and P-31 magnetic resonance spectroscopy to detect and quantify muscle dysfunction in the amyopathic and myopathic variants of dermatomyositis. Arthritis Rheum 38:1 (1995), 68–77.
91. Hsieh, T.J., Jaw, T.S., Chuang, H.Y., et al. Muscle metabolism in Duchenne muscular dystrophy assessed by in vivo proton magnetic resonance spectroscopy. J Comput Assist Tomogr 33:1 (2009), 150–154.
92. McCullough, M.B., Domire, Z.J., Reed, A.M., et al. Evaluation of muscles affected by myositis using magnetic resonance elastography. Muscle Nerve 43:4 (2011), 585–590.
93. West, J., Dahlqvist Leinhard, O., Romu, T., et al. Feasibility of MR-based body composition analysis in large scale population studies. PLoS One, 11(9), 2016, e0163332.
94. Karlsson, A., Rosander, J., Romu, T., et al. Automatic and quantitative assessment of regional muscle volume by multi-atlas segmentation using whole-body water-fat MRI. J Magn Reson Imaging 41:6 (2015), 1558–1569.
95. Crawford, R.J., Filli, L., Elliott, J.M., et al. Age- and level-dependence of fatty infiltration in lumbar paravertebral muscles of healthy volunteers. AJNR Am J Neuroradiol 37:4 (2016), 742–748.