Нервно-мышечные болезни

Расширенный поиск

Роль количественной магнитно-резонансной томографии и спектроскопии скелетных мышц в оценке результатов клинических исследований (часть II)

Полный текст:

Об авторах

P. G. Carlier
Institute of Myology, Pitie-Salpetriere University Hospital CEA, DSV, I2BM, MIRCen, NMR Laboratory National Academy of Sciences, United Institute for Informatics Problems

France, Paris

France, Paris

Belarus, Minsk

B. Marty
Institute of Myology, Pitie-Salpetriere University Hospital CEA, DSV, I2BM, MIRCen, NMR Laboratory
France, Paris

O. Scheidegger
Institute of Myology, Pitie-Salpetriere University Hospital Support Center for Advanced Neuroimaging (SCAN), Institute of Diagnostic and Interventional Neuroradiology, Inselspital, Bern University Hospital, and University of Bern

France, Paris


P. Loureiro de Sousa
Strasbourg University, CNRS, ICube
France, Strasbourg

P.-Y. Baudin
Consultants for Research in Imaging and Spectroscopy
Belgium, Tournai

E. Snezhko
National Academy of Sciences, United Institute for Informatics Problems
Belarus, Minsk

D. Vlodavets
N.I. Pirogov Russian National Medical Research University, Clinical Research Institute of Pediatrics
Russian Federation, Moscow

Список литературы

1. McIntosh L.M., Baker R. E., Anderson J. E. Magnetic resonance imaging of regenerating and dystrophic mouse muscle. Biochem Cell Biol 1998;76:532–41.

2. Tardif-de Gery S., Vilquin J., Carlier P. et al. Muscular transverse relaxation time measurement by magnetic resonance imaging at 4 Tesla in normal and dystrophic dy/dy and dy (2j)/dy (2j) mice. Neuromuscul Disord 2000;10:507–13.

3. Thibaud J.-L., Azzabou N., Barthelemy I. et al. Comprehensive longitudinal characterization of canine muscular dystrophy by serial NMR imaging of GRMD dogs. Neuromuscul Disord 2012;22(Suppl 2):85–99.

4. Thibaud J-L., Monnet A., Bertoldi D. et al. Characterization of dystrophic muscle in golden retriever muscular dystrophy dogs by nuclear magnetic resonance imaging. Neuromuscul Disord 2007;17:575–84.

5. Wang J., Fan Z., Vandenborne K. et al. Acomputerized MRI biomarker quantification scheme for a canine model of Duchenne muscular dystrophy. Int J Comput Assist Radiol Surg 2013;8(5):763–74.

6. Pacak C. A., Walter G. A., Gaidosh G. et al. Long-term skeletal muscle protection after gene transfer in a mouse model of LGMD-2D. Mol Ther 2007;15:1775–81.

7. Walter G., Cordier L., Bloy D. et al. Noninvasive monitoring of gene correction in dystrophic muscle. Magn Reson Med 2005;54:1369–76.

8. Yokota T., Lu Q-L., Partridge T. et al. Efficacy of systemic morpholino exonskipping in Duchenne dystrophy dogs. Ann Neurol 2009;65:667–76.

9. Henkelman R. M., Stanisz G. J., Graham S. J. Magnetization transfer in MRI: A review. NMR Biomed 2001;14:57–64.

10. Pratt S. J., Xu S., Mullins R. J. et al. Temporal changes in magnetic resonance imaging in the mdx mouse. BMC Res Notes 2013;6:262.

11. Vohra R. S., Mathur S., Bryant N. D. et al. Age-related T2 changes in hindlimb muscles of mdx mice. Muscle Nerve 2015;53(1):84–90.

12. Martins-Bach A. B., Malheiros J., Matot B. et al. Quantitative T2 combined with texture analysis of nuclear magnetic resonance images identify different degrees of muscle involvement in three mouse models of muscle dystrophy: mdx, Largemyd and mdx/Largemyd. PLoS One 2015. DOI: 10.1371/jornal.pone.0117835.

13. Vohra R., Accorsi A., Kumar A. et al. Magnetic resonance imaging is sensitive to pathological amelioration in a model for laminin-deficient congenital muscular dystrophy (MDC1A). PLoS One 2015. DOI: 10.1371/jornal.pone.0138254.

14. Mathur S., Vohra R. S., Germain S. A. et al. Changes in muscle T2 and tissue damage after downhill running in mdx mice. Muscle Nerve 2011;43:878–86.

15. Park J., Wicki J., Knoblaugh S. E. et al. Multi-parametric MRI at 14T for muscular dystrophy mice treated with AAV vector-mediated gene therapy. PLoS One 2015. DOI: 10.1371/jornal.pone.0124914.

16. Le Guiner C., Montus M., Servais L. et al. Forelimb treatment in a large cohort of dystrophic dogs supports delivery of a recombinant AAV for exon skipping in Duchenne patients. Mol Ther 2014;22:1923–35.

17. Bryant N. D., Li K., Does M. D. et al. Multi-parametric MRI characterization of inflammation in murine skeletal muscle. NMR Biomed 2014;27:716–25.

18. Ha D-H., Choi S., Kang E-J. et al. Diffusion tensor imaging and T2 mapping in early denervated skeletal muscle in rats. J Magn Reson Imaging 2015;42:617–23.

19. Heemskerk A. M., Strijkers G. J., Drost M. R. et al. Skeletal muscle degeneration and regeneration after femoral artery ligation in mice: Monitoring with diffusion MR imaging. Radiology 2007;243:413–21.

20. Wishnia A., Alameddine H., Tardif de Gery S. et al. Use of magnetic resonance imaging for noninvasive characterization and follow-up of an experimental injury to normal mouse muscles. Neuromuscul Disord 2001;11:50–5.

21. Arpan I., Forbes S. C., Lott D. J. et al. T2 mapping provides multiple approaches for the characterization of muscle involvement in neuromuscular diseases: A crosssectional study of lower leg muscles in 5–15-year-old boys with Duchenne muscular dystrophy. NMR Biomed 2013;26:320–8.

22. 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 2014. DOI: 10.1371/jornal.pone.106435.

23. 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 2009;30:1130–8.

24. 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 2010;255:899–908.

25. Kim H. K., Serai S., Lindquist D. et al. Quantitative Skeletal Muscle MRI: Part 2, MR Spectroscopy and T2 Relaxation Time Mapping-Comparison Between Boys With Duchenne Muscular Dystrophy and Healthy Boys. Am J Roentgenol 2015;205:216–23.

26. Willcocks R. J., Arpan I. A., Forbes S. C. et al. Longitudinal measurements of MRIT2 in boys with Duchenne muscular dystrophy: Effects of age and disease progression. Neuromuscul Disord 2014;24:393–401.

27. 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;28:1150–62.

28. Azzabou N., Loureiro de Sousa P., Caldas E. et al. Validation of a generic approach to muscle water T2 determination at 3T in fat-infiltrated skeletal muscle. J Magn Reson Imaging 2015;41:645–53.

29. Carlier P. G. Global T2 versus water T2 in NMR imaging of fatty infiltrated muscles: Different methodology, different information and different implications. Neuromuscul Disord 2014;24:390–2.

30. Wokke B. H., van den Bergen J. C., Hooijmans M. T. et al. T2 relaxation times are increased in skeletal muscle of DMD but not BMD patients. Muscle Nerve 2016;53:38–43.

31. Carlier P. G., Azzabou N., de Sousa P. L. et al. Skeletal muscle quantitative nuclear magnetic resonance imaging follow-up of adult Pompe patients. J Inherit Metab Dis 2015;38:565–72.

32. Maillard S. M., Jones R., Owens C. et al. Quantitative assessment of MRI T2 relaxation time of thigh muscles in juvenile dermatomyositis. Rheumatology (Oxford) 2004;43:603–8.

33. Park J. H., Vansant J. P., Kumar N. G. et al. Dermatomyositis: Correlative MR imaging and P-31 MR spectroscopy for quantitative characterization of inflammatory disease. Radiology 1990;177:473–9.

34. Yao L., Gai N. Fat-corrected T2 measurement as a marker of active muscle disease in inflammatory myopathy. Am J Roentgenol 2012;198:475–81.

35. Degardin A., Morillon D., Lacour A. et al. Morphologic imaging in muscular dystrophies and inflammatory myopathies. Skeletal Radiol 2010;39:1219–27.

36. Walker U. A. Imaging tools for the clinical assessment of idiopathic inflammatory myositis. Curr Opin Rheumatol 2008;20:656–61.

37. Tasca G., Pescatori M., Monforte M. et al. Different molecular signatures in magnetic resonance imaging-staged facioscapulohumeral muscular dystrophy muscles. PLoS One 2012. DOI: 10.1371/jornal.pone.38779.

38. Carlier P. G., Azzabou N., de Sousa P. L. et al. P. 14.4 Diagnostic role of quantitative NMR imaging exemplified by 3 cases of juvenile dermatomyositis. Neuromuscul Disord 2013;23:814.

39. Gineste C., DeWinter J.M., Kohl C. et al. In vivo and in vitro investigations of heterozygous nebulin knock-out mice disclose a mild skeletal muscle phenotype. Neuromuscul Disord 2013;23:357–69.

40. Gineste C., Duhamel G., Le Fur Y. et al. Multimodal MRI and (31)P-MRS investigations of the ACTA1 (Asp286Gly) mouse model of nemaline myopathy provide evidence of impaired in vivo muscle function, altered muscle structure and disturbed energy metabolism. PLoS One 2013. DOI: 10.1371/jornal.pone.72294.

41. Gineste C., Le Fur Y., Vilmen C. et al. Combined MRI and (31)P-MRS investigations of the ACTA1 (H40Y) mouse model of nemaline myopathy show impaired muscle function and altered energy metabolism. PLoS One 2013. DOI: 10.1371/jornal.pone.61517.

42. Martins Bach A., Matot B., Wary C. et al. Non-invasive NMR study of the mouse model for centronuclear myopathy with mutation in the dynamin-2 gene. Neuromuscul Disord 2015;25:275.

43. Fleckenstein J. L., Watumull D., Conner K. E. et al. Denervated human skeletal muscle: MR imaging evaluation. Radiology 1993;187:213–8.

44. Karampinos D. C., King K. F., Sutton B. P. et al. Intravoxel partially coherent motion technique: Characterization of the anisotropy of skeletal muscle microvasculature. J Magn Reson Imaging 2010;31:942–53.

45. Polak J. F., Jolesz F. A., Adams D. F. Magnetic resonance imaging of skeletal muscle. Prolongation of T1 and T2 subsequent to denervation. Invest Radiol 1988;23:365–9.

46. 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 2014;83:974–80.

47. Friedman S. D., Poliachik S. L., Otto R. K. et al. Longitudinal features of stir bright signal in FSHD. Muscle Nerve 2014;49:257–60.

48. Janssen B. H., Voet N. B.M., Nabuurs C. I. et al. Distinct disease phases in muscles of facioscapulohumera dystrophy patients identified by MR detected fat Infiltration. PLoS One 2014. DOI: 10.1371/jornal.pone.85416.

49. Janiczek R. L., Gambarota G., Sinclair C. D.J. et al. Simultaneous T2 and lipid quantitation using IDEAL–CPMG. Magn Reson Med 2011;66: 1293–302.

50. Hollingsworth K. G., de Sousa P. L., Straub V. et al. Towards harmonization of protocols for MRI outcome measures in skeletal muscle studies: Consensus recommendations from two TREAT-NMD NMR workshops, 2 May 2010, Stockholm, Sweden, 1–2 October 2009, Paris, France. Neuromuscul Disord 2012;22(Suppl 2): S54–67.

51. Yarnykh V. L. Actual flip-angle imaging in the pulsed steady state: A method for rapid three-dimensional mapping of the transmitted radiofrequency field. Magn Reson Med 2007;57:192–200.

52. Lebel R. M., Wilman A. H. Transverse relaxometry with stimulated echo compensation. Magn Reson Med 2010;64:1005–14.

53. Rooney W. D., Pollaro J. R., Forbes S. C. et al. Application of the Extended Phase Graph Technique to Improve T2 Quantitation Across Sites. 2011. In: Proceedings ISMRM 5419.

54. Liu G.-C., Jong Y.-J., Chiang C.-H. et al. Duchenne muscular Dystrophy: MR grading system with functional correlation. Radiology 1993;186:475–80.

55. Fischmann A., Hafner P., Gloor M. et al. Quantitative MRI and loss of free ambulation in Duchenne muscular dystrophy. J Neurol 2013;260:969–74.

56. 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 2012;41:955–61.

57. 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 2012;41:437–45.

58. Vohra R. S., Lott D., Mathur S. et al. Magnetic resonance assessment of hypertrophic and pseudo-hypertrophic hanges in lower leg muscles of boys with Duchenne muscular dystrophy and their relationship to functional measurements. PLoS One 2015. DOI: 10.1371/jornal.pone.0128915.

59. Wokke B. H., van den Bergen J. C., Versluis M. J. et al. Quantitative MRI and strength measurements in the assessment of muscle quality in Duchenne muscular dystrophy. Neuromuscul Disord 2014;24:409–16.

60. 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 Am J Roentgenol 2008;190:W8–12.

61. Heule R., Ganter C., Bieri O. Triple echo steady-state (TESS) relaxometry. Magn Reson Med 2014;71:230–7.

62. Morrow J. M., Sinclair C. D.J., Fischmann A. et al. MRI biomarker assessment of neuromuscular disease progression: A prospective observational cohort study. Lancet Neurol 2015;4422:1–13.

63. Nardo L., Karampinos D. C., Lansdown D. A. et al. Quantitative assessment of fat infiltration in the rotator cuff muscles using water-fat MRI. J Magn Reson Imaging 2014;39:1178–85.

64. Csapo R., Malis V., Sinha U. et al. Age-associated differences in triceps surae muscle composition and strength – an MRI-based cross-sectional comparison of contractile, adipose and connective tissue. BMC Musculoskelet Disord 2014;15:209.

65. Voit T. The challenge of making therapies happen for neuromuscular diseases. Neuromuscul Disord 2014;24:918–9.

66. Hogrel J.-Y., Barnouin Y., Azzabou N. et al. NMR imaging estimates of muscle volume and intramuscular fat infiltration in the thigh: Variations with muscle, gender, and age. Age 2015;37(3):9798.

67. Bonati U., Hafner P., Schadelin S. et al. Quantitative muscle MRI: Apowerful surrogate outcome measure in Duchenne muscular dystrophy. Neuromuscul Disord 2015;25:679–85.

68. Hiba B., Richard N., Hebert L. J. et al. Quantitative assessment of skeletal muscle degeneration in patients with myotonic dystrophy type 1 using MRI. J Magn Reson Imaging 2012;35:678–85.

69. Leong K. M., Lau P., Ramadan S. Utilisation of MR spectroscopy and diffusion weighted imaging in predicting and monitoring of breast cancer response to chemotherapy. J Med Imaging Radiat Oncol 2015;59:268–77.

70. Redmond O. M., Stack J. P., O’Connor N. G. et al. 31P MRS as an early prognostic indicator of patient response to chemotherapy. Magn Reson Med 1992;25:30–44.

71. Shin H. J., Baek H.-M., Ahn J.-H. et al. Prediction of pathologic response to neoadjuvant chemotherapy in patients with breast cancer using diffusionweighted imaging and MRS. NMR Biomed 2012;25:1349–59.

72. Edwards R. H., Dawson M. J., Wilkie D. R. et al. Clinical use of nuclear magnetic resonance in the investigation of myopathy. Lancet 1982;725–30.

73. Kemp G. J., Taylor D. J., Dunn J. F. et al. Cellular energetics of dystrophic muscle. J Neurol Sci 1993;116:201–6.

74. 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;28:1150–62.

75. Wokke B. H., Hooijmans M. T., van den Bergen J. C. et al. Muscle MRS detects elevated PDE/ATP ratios prior to fatty infiltration in Becker muscular dystrophy. NMR Biomed 2014;27:1371–7.

76. Boesch C. Musculoskeletal spectroscopy. J Magn Reson Imaging 2007;25:321–38.

77. Kemp G. J., Meyerspeer M., Moser E. Review article absolute quantification of phosphorus metabolite concentrations in human muscle in vivo by 31 PMRS: A quantitative review. NMR Biomed 2007;20:555–65.

78. Argov Z., Lofberg M., Arnold D. L. Insights into muscle diseases gained by phosphorus magnetic resonance spectroscopy. Muscle Nerve 2000;23:1316–34.

79. Chance B., Younkin D. P., Kelley R. et al. Magnetic resonance spectroscopy of normal and diseased muscles. Am J Med Genet 1986;25:659–79.

80. Heerschap A., Houtman C., Zandt H. J., et al. Introduction to in vivo 31P magnetic resonance spectroscopy of (human) skeletal muscle. Proc Nutr Soc 1999;58:861–70.

81. Newman R. J., Bore P. J., Chan L. et al. Nuclear magnetic resonance studies of forearm muscle in Duchenne dystrophy. Br Med J (Clin Res Ed) 1982;284: 1072–74.

82. 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 2015;41:1558–69.

83. Tosetti M., Linsalata S., Battini R. et al. Muscle metabolic alterations assessed by 31- phosphorus magnetic resonance spectroscopy in mild Becker muscular dystrophy. Muscle Nerve 2011;44:816–9.

84. Younkin D. P., Berman P., Sladky J. et al. 31P NMR studies in Duchenne muscular dystrophy: Age-related metabolic changes. Neurology 1987;37:165–9.

85. Wary C., Naulet T., Thibaud J.-L. et al. Splitting of Pi and other 31P NMR anomalies of skeletal muscle metabolites in canine muscular dystrophy. NMR Biomed 2012;25:1160–9.

86. Barbiroli B., Funicello R., Ferlini A. et al. Muscle energy metabolism in female DMD/BMD carriers: A 31P-MR spectroscopy study. Muscle Nerve 1992;15:344–8.

87. Barbiroli B., Funicello R., Iotti S. et al. 31P-NMR spectroscopy of skeletal muscle in Becker dystrophy and DMD/BMD carriers. Altered rate of phosphate transport. J Neurol Sci 1992;109:188–95.

88. Barbiroli B., McCully K.K., Iotti S. et al. Further impairment of muscle phosphate kinetics by lengthening exercise in DMD/ BMD carriers. An in vivo 31P-NMR spectroscopy study. J Neurol Sci 1993;119:65–73.

89. Lodi R., Kemp G. J., Muntoni F. et al. Reduced cytosolic acidification during exercise suggests defective glycolytic activity in skeletal muscle of patients with Becker muscular dystrophy. An in vivo 31P magnetic resonance spectroscopy study. Brain 1999;122:121–30.

90. Kharraz Y., Guerra J., Pessina P. et al. Understanding the process of fibrosis in Duchenne muscular dystrophy. BioMed Res Int 2014. DOI: 10.1155/2014/965631.

91. Klingler W., Jurkat-Rott K., Lehmann-Horn F. et al. The role of fibrosis in Duchenne muscular dystrophy. Acta Myol 2012;31:184–95.

92. Wynn T. A. Cellular and molecular mechanisms of fibrosis. J Pathol 2008;214:199–210.

93. Desguerre I., Mayer M., Leturcq F. et al. Endomysial Fibrosis in Duchenne Muscular Dystrophy. J Neuropathol Exp Neurol 2009;68:762–73.

94. Zhou L., Lu H. Targeting fibrosis in Duchenne muscular dystrophy. J Ne uropathol Exp Neurol 2010;69:771–6.

95. Edzes H., Samulski E. T. The measurement of crossrelaxation effects in the proton NMR spin-lattice relaxation of water in biological systems: Hydrated collagen and muscle. J Magn Reson 1978;31: 207–29.

96. Siu A. G., Ramadeen A., Hu X. et al. Characterization of the ultrashort-TE (UTE) MR collagen signal. NMR Biomed 2015;28:1236–44.

97. Perie S., Trollet C., Mouly V. et al. Autologous myoblast transplantation for oculopharyngeal muscular dystrophy: A phase I/IIa clinical study. Mol Ther 2014;22:219–25.

98. Saab G., Thompson R. T., Marsh G. D. Effects of exercise on muscle transverse relaxation determined by MR imaging and in vivo relaxometry. J Appl Physiol 2000;88:226–33.

99. Saab G., Thompson R. T., Marsh G. D. Multicomponent T2 relaxation of in vivo skeletal muscle. Magn Reson Med 1999;157:150–7.

100. Araujo E. C.A., Fromes Y., Carlier P. G. New insights on human skeletal muscle tissue compartments revealed by in vivo T2 NMR relaxometry. Biophys J 2014;106:2267–74.

101. Morrison C., Henkelman R. M. A model for magnetization transfer in tissues. Magn Reson Med 1995;33:475–82.

102. Yarnykh V. L., Tartaglione E. V., Ioannou G. N. Fast macromolecular proton fraction mapping of the human liver in vivo for quantitative assessment of hepatic fibrosis. NMR Biomed 2015;28:1716–25.

103. Li K., Dortch R. D., Kroop S. F. et al. A rapid approach for quantitative magnetization transfer imaging in thigh muscles using the pulsed saturation method. Magn Reson Imaging 2015;33:709–17.

104. Li K., Dortch R. D., Welch E. B. et al. Multi-parametric MRI characterization of healthy human thigh muscles at 3.0 T – relaxation, magnetization transfer, fat/ water, and diffusion tensor imaging. NMR Biomed 2014;27:1070–84.

105. Morrow J. M., Sinclair C. D.J., Fischmann A. et al. Reproducibility, and age, body-weight and gender dependency of candidate skeletal muscle MRI outcome measures in healthy volunteers. Eur Radiol 2014;24:1610–20.

106. Schwenzer N. F., Martirosian P., Machann J. et al. Aging effects on human calf muscle properties assessed by MRI at 3 Tesla. J Magn Reson Imaging 2009;29:1346–54.

107. Sinclair C. D.J., Morrow J. M., Miranda M. A. et al. Skeletal muscle MRI magnetisation transfer ratio reflects clinical severity in peripheral neuropathies. J Neurol Neurosurg Psychiatry 2012;83:29–32.

108. Sinclair C. D.J., Samson R. S., Thomas D. L. et al. Quantitative magnetization transfer in in vivo healthy human skeletal muscle at 3 T. Magn Reson Med 2010;64:1739–48.

109. Eliav U., Komlosh M. E., Basser P. J. et al. Collagen composition and contentdependent contrast in porcine annulus fibrosus achieved by using double quantum and magnetization transfer filtered UTE MRI. Magn Reson Med 2014;71:388–93.

110. Kusmia S., Eliav U., Navon G. et al. DQF-MT MRI of connective tissues: Application to tendon and muscle. Magma 2013;26:203–14.

111. Miller C. A., Naish J. H., Bishop P. et al. Comprehensive validation of cardiovascular magnetic extracellular volume. Circ Cardiovasc Imaging 2013;6:373–83.

112. Moon J. C., Messroghli D. R., Kellman P. et al. Myocardial T1 mapping and extracellular volume quantification: A Society for Cardiovascular Magnetic Resonance (SCMR) and CMR Working Group of the European Society of Cardiology consensus statement. J Cardiovasc Magn Reson 2013;15:92–103.

113. Horn M. 23Na magnetic resonance imaging for the determination of myocardial viability: The status and the challenges. Curr Vasc Pharmacol 2004;2:329–33.

114. Madelin G., Regatte R. R. Biomedical applications of sodium MRI in vivo. J Magn Reson Imaging 2013;38:511–29.

115. Glaser K. J., Manduca A., Ehman R. L. Review of MR elastography applications and recent developments. J Magn Reson Imaging 2012;36:757–74.

116. Ringleb S. I., Bensamoun S. F., Chen Q. et al. Applications of magnetic resonance elastography to healthy and pathologic skeletal muscle. J Magn Reson Imaging 2007;25:301–9.

117. McCullough M.B., Domire Z. J., Reed A. M. et al. Evaluation of muscles affected by myositis using magnetic resonance elastography. Muscle Nerve 2011;43:585–90.

118. Drakonaki E. E., Allen G. M., Wilson D. J. Ultrasound elastography for musculoskeletal applications. Br J Radiol 2012;85:1435–45.

119. Caravan P., Das B., Dumas S. et al. Collagen-targeted MRI contrast agent for molecular imaging of fibrosis. Angew Chem Int Ed Engl 2007;46:8171–3.

120. Caravan P., Yang Y., Zachariah R. et al. Molecular magnetic resonance imaging of pulmonary fibrosis in mice. Am J Respir Cell Mol Biol 2013;49:1120–6.

121. Fuchs B. C., Wang H., Yang Y. et al. Molecular MRI of collagen to diagnose and stage liver fibrosis. J Hepatol 2013;59:992–8.

122. Tyler D. J., Robson M. D., Henkelman R. M. et al. Magnetic resonance imaging with ultrashort TE (UTE) PULSE sequences: Technical considerations. J Magn Reson Imaging 2007;25:279–89.

123. Li C., Magland J. F., Rad H. S. et al. Comparison of optimized soft-tissue suppression schemes for ultrashort echo time MRI. Magn Reson Med 2012;68:680–9.

124. Caldas de A. Araujo E., Azzabou N., Vignaud A. et al. Quantitative NMR imaging of the short-T2 components in the SKM tissue: Alterations observed in myopathic patients. In: ISMRM 23rd Annual Meeting & Exhibition. Toronto, Ontario, Canada, 2015. P. 251.

125. Wang K., Yu H., Brittain J. k space water fat decomposition with T2* estimation and multifrequency fat spectrum modeling for ultrashort echo time imaging. J Magn Reson Imaging 2010;31(4):1027–34.

126. Du J., Bydder M., Takahashi A. M. et al. Short T2 contrast with three-dimensional ultrashort echo time imaging. Magn Reson Imaging 2011;29:470–82.

127. Du J., Takahashi A. M., Chung C. B. Ultrashort TE spectroscopic imaging (UTESI): Application to the imaging of short T2 relaxation tissues in the musculoskeletal system. J Magn Reson Imaging 2009;29:412–21.

128. Robson M. D., Bydder G. M. Clinical ultrashort echo time imaging of bone and other connective tissues. NMR Biomed 2006;19:765–80.

129. de Jong S., Zwanenburg J. J., Visser F. et al. Direct detection of myocardial fibrosis by MRI. J Mol Cell Cardiol 2011;51:974–9.

130. Vignaud A., Guillot G., Caldas de Almeida Ara´ujo E. et al. NMR imaging of short T2- components in skeletal muscle tissue. Neuromuscul Disord 2014;24:837.

131. Detre J. A., Wang J. Technical aspects and utility of fMRI using BOLD and ASL. Clin Neurophysiol 2002;113:621–34.

132. Ogawa S., Lee T. M., Kay A. R. et al. Brain magnetic resonance imaging with contrast dependent on blood oxygenation. Proc Natl Acad Sci U S A 1990;87:9868–72.

133. Carlier P. G., Bertoldi D., Baligand C. et al. Muscle blood flow and oxygenation measured by NMR. NMR Biomed 2006;19:954–67.

134. Partovi S., von Tengg-Kobligk H., Bhojwani N. et al. Advanced noncontrast MR imaging in musculoskeletal radiology. Radiol Clin North Am 2015;53:549–67.

135. 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 2001;46:305–11.

136. Schewzow K., Fiedler G. B., Meyerspeer M. et al. Dynamic ASL and T2*-weighted MRI in exercising calf muscle at 7 T: A feasibility study. Magn Reson Med 2014;73:1190–5.

137. Bertoldi D., Loureiro de Sousa P., Fromes Y. et al. Quantitative, dynamic and non- invasive determination of skeletal muscle perfusion in mouse leg by NMR arterial spin- labeled imaging. Magn Reson Imaging 2008;26:1259–65.

138. 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 2012;35:1253–65.

139. Jordan B. F., Kimpalou J. Z., Beghein N. et al. Contribution of oxygenation to BOLD contrast in exercising muscle. Magn Reson Med 2004;52:391–6.

140. Baligand C., Wary C., Menard J. C. et al. Measuring perfusion and bioenergetics simultaneously in mouse skeletal muscle: A multiparametric functional-NMR approach. NMR Biomed 2011;24:281–90.

141. Damon B. M., Wadington M. C., Hornberger J. L. et al. Absolute and relative contributions of BOLD effects to the muscle functional MRI signal intensity time course: Effect of exercise intensity. Magn Reson Med 2007;58:335–45.

142. Dass S., Suttie J. J., Piechnik S. K. et al. Myocardial tissue characterization using magnetic resonance noncontrast T1 mapping in hypertrophic and dilated cardiomyopathy. Circ Cardiovasc Imaging 2012;5:726–33.

143. Lebon V., Brillaul-Salvat C., Bloch G. et al. Evidence of muscle BOLD effect revealed by simultaneous interleaved gradient-echo NMRI and myoglobin NMRS during leg ischemia. Magn Reson Med 1998;40:551–8.

144. 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 2004;17:392–8.

145. Duteil S., Wary C., Raynaud J. S. et al. Influence of vascular filling and perfusion on BOLD contrast during reactive hyperemia in human skeletal muscle. Magn Reson Med 2006;55:450–4.

146. Decorte N., Buehler T., Caldas de Almeida Araujo E. et al. Noninvasive estimation of oxygen consumption in human calf muscle through combined NMR measurements of ASL perfusion and T2 oxymetry. J Vasc Res 2014;51:360–8.

147. Englund E. K., Langham M. C., Li C. et al. Combined measurement of perfusion, venous oxygen saturation, and skeletal muscle T2* during reactive hyperemia in the leg. J Cardiovasc Magn Reson 2013;15:70.

148. Zheng J., An H., Coggan A. R. et al. Noncontrast skeletal muscle oximetry. Magn Reson Med 2013;71:318–25.

149. Aschwanden M., Partovi S., Jacobi B. et al. Assessing the end-organ in peripheral arterial occlusive disease-from contrastenhanced ultrasound to blood – oxygenlevel dependent MR imaging. Cardiovasc Diagn Ther 2014;4:165–72.

150. Englund E. K., Langham M. C., Ratcliffe S. J. et al. Multiparametric assessment of vascular function in peripheral artery disease: Dynamic measurement of skeletal muscle perfusion, blood – oxygen-level dependent signal, and venous oxygen saturation. Circ Cardiovasc Imaging 2015. DOI: 10.1161/circimaging.114.002673.

151. Grozinger G., Pohmann R., Schick F. et al. Perfusion measurements of the calf in patients with peripheral arterial occlusive disease before and after percutaneous transluminal angioplasty using MR arterial spin labeling. J Magn Reson Imaging 2013;40:980–7.

152. Ledermann H.-P., Schulte A.-C., Heidecker H.-G. et al. Blood oxygenation level- dependent magnetic resonance imaging of the skeletal muscle in patients with peripheral arterial occlusive disease. Circulation 2006;113:2929–35.

153. Zheng J., Hasting M. K., Zhang X. et al. A pilot study of regional perfusion and oxygenation in calf muscles of individuals with diabetes with a non-invasive measure. J Vasc Surg 2014;59:419–26.

154. Partovi S., Schulte A.-C., Aschwanden M. et al. Impaired skeletal muscle microcirculation in systemic sclerosis. Arthritis Res Ther 2012;14:R209.

155. 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. Am J Roentgenol 2009;193:327–33.

156. Wary C., Nadaj-Pakleza A., Laforet P. et al. Investigating glycogenosis type III patients with multi-parametric functional NMR imaging and spectroscopy. Neuromuscul Disord 2010;20:548–58.

157. Bertoldi D., Parzy E., Fromes Y. et al. New insight into abnormal muscle vasodilatory responses in aged hypertensive rats by in vivo nuclear magnetic resonance imaging of perfusion. J Vasc Res 2006;43:149–56.

158. Thomas G. D. Functional muscle ischemia in Duchenne and Becker muscular dystrophy. Front Physiol 2013;4:381–6.

159. Horster I., Weigt-Usinger K., Carmann C. et al. The Larginine/NO pathway and homoarginine are altered in Duchenne muscular dystrophy and improved by glucocorticoids. Amino Acids 2015;47:1853–63.

160. Nelson M. D., Rader F., Tang X. et al. PDE5 inhibition alleviates functional muscle ischemia in boys with Duchenne muscular dystrophy. Neurology 2014;82:2085–91.

161. Blat Y., Blat S. Drug discovery of therapies for duchenne muscular dystrophy. J Biomol Screen 2015;10:1189–203.

162. Ennen J. P., Verma M., Asakura A. Vascular-targeted therapies for Duchenne muscular dystrophy. Skelet Muscle 2013;3–9:1–12.

163. Lavini C., de Jonge M. C., van de Sande M. G.H. et al. Pixelby-pixel analysis of DCE MRI curve patterns and an illustration of its application to the imaging of the musculoskeletal system. Magn Reson Imaging 2007;25:604–12.

164. Tofts P. S. Modeling tracer kinetics in dynamic Gd-DTPA MR imaging. J Magn Reson Imaging 1997;7:91–101.

165. Tofts P. S., Brix G., Buckley D. L. et al. Contrast-wnhanced T1-weighted MRI of a diffusable tracer: Standardized quantities and symbols. J Magn Reson Imaging 1999;232:223–32.

166. Amthor H., Egelhof T., McKinnell I. et al. Albumin targeting of damaged muscle fibres in the mdx mouse can be monitored by MRI. Neuromuscul Disord 2004;14:791–6.

167. Straub V., Donahue K. M., Allamand V. et al. Contrast agent enhanced magnetic resonance imaging of skeletal muscle damage in animal models of muscular dystrophy. Magn Reson Med 2000;44:655–9.

168. Friedrich M. G. Myocardial T1: The Rise of a Novel Biomarker Continues*. JACC Cardiovasc Imaging 2015;8:47–9.

169. Hinojar R., Foote L., Arroyo Ucar E. et al. Native T1 in discrimination of acute and convalescent stages in patients with clinical diagnosis of myocarditis. JACC Cardiovasc Imaging 2015;8:37–46.

170. Stejskal E. O., Tanner J. E. Spin diffusion measurements: Spin echoes in the presence of a time-dependant field gradient. J Chem Phys 1965;42:288–92.

171. Froeling M., Nederveen A. J., Heijtel D. F.R. et al. Diffusion-tensor MRI reveals the complex muscle architecture of the human forearm. J Magn Reson Imaging 2012;36:237–48.

172. Schwenzer N. F., Steidle G., Martirosian P. et al. Diffusion tensor imaging of the human calf muscle: Distinct changes in fractional anisotropy and mean diffusion due to passive muscle shortening and stretching. NMR Biomed 2009;22:1047–53.

173. Yanagisawa O., Shimao D., Maruyama K. et al. Diffusion-weighted magnetic resonance imaging of human skeletal muscles: Gender-, age- and musclerelated differences in apparent diffusion coefficient. Magn Reson Imaging 2009;27:69–78.

174. Damon B. M., Heemskerk A. M., Ding Z. Polynomial fitting of DT-MRI fiber tracts allows accurate estimation of muscle architectural parameters. Magn Reson Imaging 2012;30:589–600.

175. Karampinos D. C., King K. F., Sutton B. P. et al. Myofiber ellipticity as an explanation for transverse asymmetry of skeletal muscle diffusion MRI in vivo signal. Ann Biomed Eng 2009;37:2532–46.

176. Sigmund E. E., Novikov D. S., Sui D. et al. Time-dependent diffusion in skeletal muscle with the random permeable barrier model (RPBM): Application to normal controls and chronic exertional compartment syndrome patients. NMR Biomed 2014;27:519–28.

177. Sigmund E. E., Sui D., Ukpebor O. et al. Stimulated echo diffusion tensor imaging and SPAIR T2-weighted imaging in chronic exertional compartment syndrome of the lower leg muscles. J Magn Reson Imaging 2013;38:1073–82.

178. Froeling M., Nederveen A. J., Nicolay K. et al. DTI of human skeletal muscle: The effects of diffusion encoding parameters, signal-to-noise ratio and T2 on tensor indices and fiber tracts. NMR Biomed 2013;26:1339–52.

179. Froeling M., Oudeman J., van den Berg S. et al. Reproducibility of diffusion tensor imaging in human forearm muscles at 3.0 T in a clinical setting. Magn Reson Med 2010;64:1182–90.

180. Heemskerk A. M., Sinha T. K., Wilson K. J. et al. Repeatability of DTI-based skeletal muscle fiber tracking. NMR Biomed 2010;23:294–303.

181. Filli L., Boss A., Wurnig M. C. et al. Dynamic intravoxel incoherent motion imaging of skeletal muscle at rest and after exercise. NMR Biomed 2015;28:240–6.

182. Ponrartana S., Ramos-Platt L., Wren T. A. L. et al. Effectiveness of diffusion tensor imaging in assessing disease severity in Duchenne muscular dystrophy: Preliminary study. Pediatr Radiol 2015;45:582–9.

183. Qi J., Olsen N. J., Price R. R. et al. Diffusion-weighted imaging of inflammatory myopathies: Polymyositis and dermatomyositis. J Magn Reson Imaging 2008;27:212–7.

184. Zaraiskaya T., Kumbhare D., Noseworthy M. D. Diffusion tensor imaging in evaluation of human skeletal muscle injury. J Magn Reson Imaging 2006;24:402–8.

185. 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 2014; 87(1043):20140261.

186. Froeling M., Oudeman J., Strijkers G. J. et al. Muscle changes detected with diffusion- tensor imaging after longdistance running. Radiology 2015;274:548–62.

187. Hooijmans M. T., Damon B. M., Froeling M. et al. Evaluation of skeletal muscle DTI in patients with duchenne muscular dystrophy. NMR Biomed 2015;28:1589–97.

188. Parzy E., Fromes Y., Thiaudiere E. et al. Rapid communication refinement of cardiac NMR imaging in awake hamsters: Proof of feasibility and characterization of cardiomyopathy. NMR Biomed 2007;20:615–23.

189. Azzabou N., Hogrel J.-Y., Carlier P. G. NMR based biomarkers to study age-related changes in the human quadriceps. Exp Gerontol 2015;70:54–60.

190. Certaines J. D., de Larcher T., Duda D. et al. Application of texture analysis to muscle MRI: 1-What kind of information should be expected from texture analysis? EPJ Nonlinear Biomed Phys 2015;1–3:1–14.

191. Lerski R. A., de Certaines J. D., Duda D. et al. Application of texture analysis to muscle MRI: 2-technical recommendations. EPJ Nonlinear Biomed Phys 2015;3:1–20.

192. Brown A. M., Nagala S., McLean M.A. et al. Multiinstitutional validation of a novel textural analysis tool for preoperative stratification of suspected thyroid tumors on diffusion-weighted MRI. Magn Reson Med 2015. DOI: 10.1002/mrm.25743.

193. Thibaud J., Matot B., Barthelemy I. et al. Diaphragm structural abnormalities revealed by NMR imaging in the dystrophic dog. Neuromuscul Disord 2013;23:809–10.

194. Mead A. F., Petrov M., Malik A. S. et al. Diaphragm remodeling and compensatory respiratory mechanics in a canine model of Duchenne muscular dystrophy. J Appl Physiol 2014;116:807–15.

195. Deshmane A., Gulani V., Griswold M. A. et al. Parallel MR imaging. J Magn Reson Imaging 2012;36:55–72.

196. Griswold M. A., Jakob P. M., Heidemann R. M. et al. Generalized autocalibrating partially parallel acquisitions (GRAPPA). Magn Reson Med 2002;47:1202–10.

197. Pruessmann K. P., Weiger M., Scheidegger M. B., Boesiger P. SENSE: Sensitivity encoding for fast MRI. Magn Reson Med 1999;42:952–62.

198. Donoho D. L. Compressed sensing. IEEE Trans Inf Theory 2006;1289–1306.

199. Lustig M., Donoho D. L., Santos J. M. et al. Compressed sensing MRI. IEEE Signal Processing Magazine 2008;25:72–85.

200. Hollingsworth K. G., Higgins D. M., McCallum M. et al. Investigating the quantitative fidelity of prospectively undersampled chemical shift imaging in muscular dystrophy with compressed sensing and parallel imaging reconstruction. Magn Reson Med 2013b;72:1016– 19.

201. Loughran T., Higgins D. M., McCallum M. et al. Improving highly accelerated fat fraction measurements for clinical trials in muscular dystrophy: Origin and quantitative effect of R2* changes. Radiology 2015;275:570–78.

202. Feng L., Grimm R., Block K. T. et al. Golden-angle radial sparse parallel MRI: Combination of compressed sensing, parallel imaging, and golden-angle radial sampling for fast and flexible dynamic volumetric MRI. Magn Reson Med 2013;72:707–17.

203. Bieri O., Scheffler K., Welsch G. H. et al. Quantitative mapping of T2 using partial spoiling. Magn Reson Med 2011;66:410–8.

204. de Sousa P. L., Vignaud A., Caldas de Almeida Ara´ujo E. et al. Factors controlling T2 mapping from partially spoiled SSFP sequence: Optimization for skeletal muscle characterization. Magn Reson Med 2012;67:1379–90.

205. Brillault-Salvat C., Giacomini E., Jouvensal L. et al. Simultaneous determination of muscle perfusion and oxygenation by interleaved NMR plethysmography and deoxymyoglobin spectroscopy. NMR Biomed 1997;10:315–23.

206. Eleff S. M., Schnall M. D., Ligetti L. et al. Concurrent measurements of cerebral blood flow, sodium, lactate, and highenergy phosphate metabolism using 19F, 23Na, 1H, and 31P nuclear magnetic resonance spectroscopy. Magn Reson Med 1988;7:412–24.

207. Thulborn K., Soffe N., Kadda G. Simultaneous in vivo measurement of oxygen utilization and high-energy phosphate metabolism in rabbit skeletal muscle by multinuclear 1H and 31P NMR. J Magn Reson 1981;45:362–66.

208. Duteil S., Bourrilhon C., Raynaud J. S. et al. Metabolic and vascular support for the role of myoglobin in humans: A multiparametric NMR study. Am J Physiol Regul Integr Comp Physiol 2004;287:R1441–9.

209. Carlier P. G., Brillault-Salvat C., Giacomini E. et al. How to investigate oxygen supply, uptake, and utilization simultaneously by interleaved NMR imaging and spectroscopy of the skeletal muscle. Magn Reson Med 2005;54:1010–3.

210. de Sousa P. L., Vignaud A., Fleury S. et al. Fast monitoring of T (1), T (2), and relative proton density (M (0)) changes in skeletal muscles using an IR-TrueFISP sequence. J Magn Reson Imaging 2011;33:921–30.

211. Schmitt P., Griswold M. A., Jakob P. M. et al. Inversion recovery True FISP: Quantification of T (1), T (2), and spin density. Magn Reson Med 2004;51:661–7.

212. Hennig J., Weigel M., Scheffler K. Calculation of flip angles for echo trains with predefined amplitudes with the extended phase graph (EPG)- algorithm: Principles and applications to hyperecho and TRAPS sequences 2004; 49:527–35.

213. Weigel M. Extended phase graphs: Dephasing, RF pulses, and echoes – pure and simple. J Magn Reson Imaging 2014.

214. Hunter D. J., Zhang W., Conaghan P. G. et al. Systematic review of the concurrent and predictive validity of MRI biomarkers in OA. Osteoarthr Cartil 2011;19:557–88.


Для цитирования:

Carlier P.G., Marty B., Scheidegger O., Loureiro de Sousa P., Baudin P., Snezhko E., Vlodavets D. Роль количественной магнитно-резонансной томографии и спектроскопии скелетных мышц в оценке результатов клинических исследований (часть II). Нервно-мышечные болезни. 2017;7(1):11-29.

For citation:

Carlier P.G., Marty B., Scheidegger O., Loureiro de Sousa P., Baudin P., Snezhko E., Vlodavets D. Skeletal muscle quantitative nuclear magnetic resonance imaging and spectroscopy as an outcome measure for clinical trials (part II). Neuromuscular Diseases. 2017;7(1):11-29. (In Russ.)

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