Steroid myopathy in patients with myasthenia gravis: a literature review
https://doi.org/10.17650/2222-8721-2024-14-3-90-101
Abstract
Steroid myopathy is a common drug-induced non-inflammatory myopathy that affects patients requiring long-term glucocorticoid treatment for various autoimmune, inflammatory and oncological diseases. According to the neurology clinical practice guidelines, non-fluorinated glucocorticoids are the first-line pathogen-directed therapy for a number of dysimmune neuromuscular disorders, including myasthenia gravis. Long-term high-dose steroid treatment regime for myasthenia gravis leads to both acute and chronic development of glucocorticoids-induced proximal muscle weakness and atrophy. Steroid myopathy, along with other undesirable side effects of glucocorticoids therapy, impact health-related quality of life, patient satisfaction and adherence to treatment. Hence, further studies are required to expand our knowledge of clinical evaluation, diagnostic testing and prevention approaches for glucocorticoids-induced myopathy. The aim of this literature review is to analyze existing data on pathogenesis, diagnostic tools and treatment strategies for steroid myopathy.
Supporting agencies: The work was performed without external funding
About the Authors
S. A. Zaytsevskaya
Research Center of Neurology
Russian Federation
Russian Federation
Sofya Aleksandrovna
80 Volokolamskoe Shosse, Moscow 125367
N. A. Suponeva
Research Center of Neurology
Russian Federation
Russian Federation
80 Volokolamskoe Shosse, Moscow 125367
K. V. Antonova
Research Center of Neurology
Russian Federation
Russian Federation
80 Volokolamskoe Shosse, Moscow 125367
D. A. Grishina
Research Center of Neurology
Russian Federation
Russian Federation
80 Volokolamskoe Shosse, Moscow 125367
A. M. Narbut
Research Center of Neurology
Russian Federation
Russian Federation
80 Volokolamskoe Shosse, Moscow 125367
References
1. Bowyer S., Lamothe M., Hollister J. Steroid myopathy: Incidence and detection in a population with asthma. J Allergy Clin Immunol 1985;76(2):234–42. DOI: 10.1016/0091-6749(85)90708-0
2. Dubois E. Triamcinolone in the treatment of systemic lupus erythematosus. J Am Med Assoc 1958;167(13):1590–9. DOI: 10.1001/jama.1958.02990300016004
3. Perkoff G., Silber R., Tyler F. et al. Studies in disorders of muscle. XII. Myopathy due to the administration of therapeutic amounts of 17-hydroxycorticosteroids. Am J Med 1959;26(6):891–8. DOI: 10.1016/0002-9343(59)90211-6
4. Narayanaswami P., Sanders D., Wolfe G. et al. International Consensus Guidance for Management of Myasthenia Gravis. Neurology 2021;96(3):114–22. DOI: 10.1212/ WNL.0000000000011124
5. Sussman J., Farrugia M., Maddison P. et al. Myasthenia gravis: Association of British neurologists’ management guidelines. Pract Neurol 2015;15(3):199–206. DOI: 10.1136/practneurol-2015-001126
6. Murai H., Utsugisawa K., Motomura M. et al. The Japanese clinical guidelines 2022 for myasthenia gravis and Lambert–Eaton myasthenic syndrome. Clinical and Experimental Neuroimmunology 2023;14:19–27.DOI: 10.1111/cen3.12739
7. Wiendl H., Abicht A., Chan A. et al. Guideline for the management of myasthenic syndromes. Ther Adv Neurol Disord 2023;16:17562864231213240. DOI: 10.1177/17562864231213240
8. Gupta A., Gupta Y. Glucocorticoid-induced myopathy: Pathophysiology, diagnosis, and treatment. Indian J Endocrinol Metab 2013;17(5):913–6. DOI: 10.4103/2230-8210.117215
9. Batchelor T., Taylor L., Thaler H. et al. Steroid myopathy in cancer patients. Neurology 1997;48(5):1234–8. DOI: 10.1212/WNL.48.5.1234
10. Wu K., Michalski A., Cortes D. et al. Glucocorticoid-induced myopathy in people with asthma: A systematic review. J Asthma 2022;59(7):1396–409. DOI: 10.1080/02770903.2021.1926488
11. Buttgereit F., Da Silva J., Boers M. et al. Standardised nomenclature for glucocorticoid dosages and glucocorticoid treatment regimens: Current questions and tentative answers in rheumatology. Ann Rheum Dis 2002;61(8):718–22. DOI: 10.1136/ard.61.8.718
12. Al Efraij K., Johnson K., Wiebe D. et al. A systematic review of the adverse events and economic impact associated with oral corticosteroids in asthma. J Asthma 2019;56(12):1334–46. DOI: 10.1080/02770903.2018.1539100
13. Esteves G., Mazzolani B., Smaira F. et al. Nutritional recommendations for patients undergoing prolonged glucocorticoid therapy. Rheumatol Adv Pract 2022;6(2):rkac029. DOI: 10.1093/rap/rkac029
14. Nagashima M., Takahashi D., Mizushima T. et al. Effects of exercise in patients with connective tissue disease receiving highdose glucocorticoids: A pilot prospective cohort study. Eur J Appl Physiol 2021;121(8):2253–63. DOI: 10.1007/s00421-021-04697-2
15. Zamecnik J., Vesely D., Jakubicka B. et al. Atrophy of type II fibres in myasthenia gravis muscle in thymectomized patients: Steroid-induced change with prognostic impact. J Cell Mol Med 2009;13(8 B):2008–18. DOI: 10.1111/j.1582-4934.2008.00431.x
16. Berr C., Stieg M., Deutschbein T. et al. Persistence of myopathy in Cushing’s syndrome: Evaluation of the German Cushing’s Registry. Eur J Endocrinol 2017;176(6):737–46. DOI: 10.1530/EJE-16-0689
17. Bolland M., Holdaway I., Berkeley J. et al. Mortality and morbidity in Cushing’s syndrome in New Zealand. Clin Endocrinol (Oxf) 2011;75(4):436–42. DOI: 10.1111/j.1365-2265.2011.04124.x
18. Giraldi F., Moro M., Cavagnini F. Gender-related differences in the presentation and course of Cushing’s disease. J Clin Endocrinol Metab 2003;88(4):1554–8. DOI: 10.1210/jc.2002-021518
19. Macedo A., Almeida T., Massini D. et al. Effects of exercise training on glucocorticoid-induced muscle atrophy: Literature review. Steroids 2023;195(5):109240. DOI: 10.1016/j.steroids.2023.109240
20. Costa M., Violato N., Taboga S. et al. Reduction of insulin signalling pathway IRS-1/IRS-2/AKT/mTOR and decrease of epithelial cell proliferation in the prostate of glucocorticoid-treated rats. Int J Exp Pathol 2012;93(3):188–95. DOI: 10.1111/j.1365-2613.2012.00817.x
21. Macedo A., Krug A., Herrera N. et al. Low-intensity resistance training attenuates dexamethasone-induced atrophy in the flexor hallucis longus muscle. J Steroid Biochem Mol Biol 2014;143:357–64. DOI: 10.1016/j.jsbmb.2014.05.010
22. Ma K., Mallidis C., Bhasin S. et al. Glucocorticoid-induced skeletal muscle atrophy is associated with upregulation of myostatin gene expression. Am J Physiol Metab 2003;285(2):363–71. DOI: 10.1152/ajpendo.00487.2002
23. Cho J., Fournier M., Da X. et al. Time course expression of Foxo transcription factors in skeletal muscle following corticosteroid administration. J Appl Physiol 2010;108(1):137–45. DOI: 10.1152/japplphysiol.00704.2009
24. Fappi A., De Carvalho Neves J., Sanches L. et al. Skeletal muscle response to deflazacort, dexamethasone and methylprednisolone. Cells 2019;8(5):406. DOI: 10.3390/cells8050406
25. Kanda F., Okuda S., Matsushita T. et al. Steroid myopathy: Pathogenesis and effects of growth hormone and insulin-like growth factor-I administration. Horm Res Paediatr 2001;56(1):24–8. DOI: 10.1159/000048130
26. Afifi A., Bergman R., Harvey J. Steroid myopathy. Clinical, histologic and cytologic observations. Johns Hopkins Med J 1968;123(4):158–73.
27. Engel A. Electron microscopic observations in thyrotoxic and corticosteroid-induced myopathies. Mayo Clin Proc 1966;41(11):785–96.
28. Walsh G., DeVivo D., Olson W. Histochemical and ultrastructural changes in rat muscle. Occurrence following adrenal corticotrophic hormone, glucocorticoids, and starvation. Arch Neurol 1971;24(1):83–93. DOI: 10.1001/archneur.1971.00480310111012
29. Horber F., Hoppeler H., Herren D. et al. Altered skeletal muscle ultrastructure in renal transplant patients on prednisone. Kidney Int 1986;30(3):411–6. DOI: 10.1038/ki.1986.199
30. Vallet B., Fourrier F., Hurtevent J. et al. Myasthenia gravis and steroid-induced myopathy of the respiratory muscles. Intensive Care Med 1992;18:424–6. DOI: 10.1007/BF01694346
31. Waclawik A., Sufit R., Beinlich B. et al. Acute myopathy with selective degeneration of myosin filaments following status asthmaticus treated with methylprednisolone and vecuronium. Neuromuscul Disord 1992;2(1):19–26. DOI: 10.1016/0960-8966(92)90022-x
32. Hatakenaka M., Soeda H., Okafuji T. et al. Steroid myopathy: Evaluation of fiber atrophy with T2 relaxation time – rabbit and human study. Radiology 2006;238(2):650–7. DOI: 10.1148/radiol.2381041720
33. Williams T., O’Hehir R., Czarny D. et al. Acute myopathy in severe acute asthma treated with intravenously administered corticosteroids. Am Rev Respir Dis 1988;137(2):460–3. DOI: 10.1164/ajrccm/137.2.460
34. Khaleeli A., Edwards R., Gohil K. et al. Corticosteroid myopathy: A clinical and pathological study. Clin Endocrinol 1983;18(2):155–66. DOI: 10.1111/j.1365-2265.1983.tb03198.x
35. Minetto M., D’Angelo V., Arvat E. et al. Diagnostic work-up in steroid myopathy. Endocrine 2018;60:219–23. DOI: 10.1007/s12020-017-1472-5
36. Weber M., Krakowski-Roosen H., Schröder L. et al. Morphology, metabolism, microcirculation, and strength of skeletal muscles in cancer-related cachexia. Acta Oncol 2009;48(1):116–24. DOI: 10.1080/02841860802130001
37. D’Antona G., Pellegrino M., Adami R. et al. The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol 2003;552(2):499–511. DOI: 10.1113/jphysiol.2003.046276
38. Brooke M., Engel W. The histographic analysis of human muscle biopsies with regard to fiber types. Neurology 1969;19(5):469–77. DOI: 10.1212/WNL.19.5.469
39. Russell D. Histological changes in the striped muscles in myasthenia gravis. J Pathol Bacteriol 1953;65(2):279–89. DOI: 10.1002/path.1700650202
40. Fenichel G. Muscle lesions in myasthenia gravis. Ann NY Acad Sci 1966;135(1):60–7. DOI: 10.1111/j.1749-6632.1966.tb45463.x
41. Martignago S., Fanin M., Albertini E. et al. Muscle histopathology in myasthenia gravis with antibodies against MuSK and AChR. Neuropathol Appl Neurobiol 2009;35(1):103–10. DOI: 10.1111/j.1365-2990.2008.00965.x
42. Pereira R., Freire de Carvalho J. Glucocorticoid-induced myopathy. Joint Bone Spine 2011;78:41–4. DOI: 10.1016/j.jbspin.2010.02.025
43. Ammini A., Tandon N., Gupta N. et al. Etiology and clinical profile of patients with Cushing’s syndrome: A single center experience. Indian J Endocrinol Metab 2014;18(1):99–105. DOI: 10.4103/2230-8210.126586
44. Olafsson E., Jones H., Guay A. et al. Myopathy of endogenous Cushing’s syndrome: A review of the clinical and electromyographic features in 8 patients. Muscle Nerve 1994;17(6):692, 693. DOI: 10.1002/mus.880170625
45. Silver E., Ochoa W. Glucocorticoid-Induced myopathy in a patient with systemic lupus erythematosus (SLE): A case report and review of the literature. Am J Case Rep 2018;19(3):277–83. DOI: 10.12659/ajcr.906377
46. Minetto M., Lanfranco F., Motta G. et al. Steroid myopathy: Some unresolved issues. J Endocrinol Invest 2011;34(5):370–5. DOI: 10.1007/BF03347462
47. Schakman O., Kalista S., Barbé C. et al. Glucocorticoid-induced skeletal muscle atrophy. Int J Biochem Cell Biol 2013;45(10): 2163–72. DOI: 10.1016/j.biocel.2013.05.036
48. Haran M., Schattner A., Kozak N. et al. Acute steroid myopathy: A highly overlooked entity. QJM 2018;111(5):307–11. DOI: 10.1093/qjmed/hcy031
49. Lacomis D., Smith T., Chad D. Acute myopathy and neuropathy in status asthmaticus: Case report and literature review. Muscle Nerve 1993;16(1):84–90. DOI: 10.1002/mus.880160114
50. Knox A., Mascie-Taylor B., Muers M. Acute hydrocortisone myopathy in acute severe asthma. Thorax 1986;41(5):411, 412. DOI: 10.1136/thx.41.5.411
51. Van Marle W., Woods K. Acute hydrocortisone myopathy. BMJ 1980;281(6235):271, 272. DOI: 10.1136/bmj.281.6235.271-a
52. Panegyres P., Squier M., Mills K. et al. Acute myopathy associated with large parenteral dose of corticosteroid in myasthenia gravis. J Neurol Neurosurg Psychiatry 1993;56(6):702–4. DOI: 10.1136/jnnp.56.6.702.
53. Dzherieva I.S., Brovkina S.S., Volkova N.I. Combination of corticosteroid-induced myopathy and myasthenia gravis: diagnostic difficulties. FOCUS Endokrinologiya = FOCUS Endocrinology 2020;1(1):66–70. (In Russ.). DOI: 10.47407/ef2020.1.1.0009
54. Lotan I., Hellmann M., Wilf-Yarkoni A. et al. Exacerbation of myasthenia gravis following corticosteroid treatment: What is the evidence? A systematic review. Neurology 2021;268:4573–86. DOI: 10.1007/s00415-020-10264-0
55. Simon N. A new diagnostic tool for the detection of steroid myopathy. Clin Neurophysiol 2019;130(8):1407, 1408. DOI: 10.1016/j.clinph.2019.05.019
56. Minetto M., Lanfranco F., Botter A. et al. Do muscle fiber conduction slowing and decreased levels of circulating muscle proteins represent sensitive markers of steroid myopathy? A pilot study in Cushing’s disease. Eur J Endocrinol 2011;164(6):985–93. DOI: 10.1530/EJE-10-1169
57. Yoshikawa N., Yamamoto M., Kuribara-Souta A. et al. Amino acid profile in 18 patients with rheumatic diseases treated with glucocorticoids and BCAAs. J Nutr Sci Vitaminol (Tokyo) 2021;67(3):180–8. DOI: 10.3177/jnsv.67.180
58. Stålberg E., Sonoo M. Assessment of variability in the shape of the motor unit action potential, the “jiggle”, at consecutive discharges. Muscle Nerve 1994;17(10):1135–44. DOI: 10.1002/mus.880171003
59. Juel V. Clinical neurophysiology of neuromuscular junction disease. In: Handbook of Clinical Neurology. Ed. by K.H. Levin and P. Chauvel. Elsevier B.V., 2019. Pp. 291–303. DOI: 10.1016/B978-0-444-64142-7.00055-2
60. Somnier F., Skeie G., Aarli J. et al. EMG evidence of myopathy and the occurrence of titin autoantibodies in patients with myasthenia gravis. Eur J Neurol 1999;6(5):555–63. DOI: 10.1046/j.1468-1331.1999.650555.x
61. Sanadze A.G., Sidnev D.V., Galkina O.I. et al. Myasthenic myopathy. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova = S.S. Korsakov Journal of Neurology and Psychiatry 2007;107(9):11–6. (In Russ.).
62. Sanadze A.G., Gilvanova O.V. Myasthenia gravis and muscle atrophy. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova = S.S. Korsakov Journal of Neurology and Psychiatry 2021;121(2):79–87. (In Russ.). DOI: 10.17116/jnevro202112102179
63. Lexell J., Henriksson-larsén K., Sjöström M. Distribution of different fibre types in human skeletal muscles 2. A study of cross-sections of whole m. vastus lateralis. Acta Physiol Scand 1983;117(1):115–22. DOI: 10.1111/j.1748-1716.1983.tb07185.x
64. Minetto M., Botter A., Lanfranco F. et al. Muscle fiber conduction slowing and decreased levels of circulating muscle proteins after short-term dexamethasone administration in healthy subjects. J Clin Endocrinol Metab 2010;95(4):1663–71. DOI: 10.1210/jc.2009-2161
65. Beck R. Muscle fiber conduction velocity. In: Wiley Encyclopedia of Biomedical Engineering. Wiley, 2006. DOI: 10.1002/9780471740360.ebs0306
66. Blijham P., Ter Laak H., Schelhaas H. et al. Relation between muscle fiber conduction velocity and fiber size in neuromuscular disorders. J Appl Physiol 2006;100(6):1837–41. DOI: 10.1152/japplphysiol.01009.2005
67. Kemink S., Frijns J., Hermus A. et al. Body composition determined by six different methods in women bilaterally adrenalectomized for treatment of Cushing’s disease. J Clin Endocrinol Metab 1999;84(11):3991–9. DOI: 10.1210/jcem.84.11.6143
68. Hosono O., Yoshikawa N., Shimizu N. et al. Quantitative analysis of skeletal muscle mass in patients with rheumatic diseases under glucocorticoid therapy – comparison among bioelectrical impedance analysis, computed tomography, and magnetic resonance imaging. Mod Rheumatol 2015;25:257–63. DOI: 10.3109/14397595.2014.935078
69. Martucci M., McIlduff C., Shin C. et al. Quantitative ultrasound of muscle can detect corticosteroid effects. Clin Neurophysiol 2019;130(8):1460–4. DOI: 10.1016/j.clinph.2019.04.709
70. Minetto M., Caresio C., Salvi M. et al. Ultrasound-based detection of glucocorticoid-induced impairments of muscle mass and structure in Cushing’s disease. J Endocrinol Invest 2019;42(7):757–68. DOI: 10.1007/s40618-018-0979-9
71. Dunlap K., Steiner J., Hickner R. et al. The duration of glucocorticoid treatment alters the anabolic response to high-force muscle contractions. J Appl Physiol 2023;135(1):183–95. DOI: 10.1152/japplphysiol.00113.2023
72. Braith R., Welsch M., Mills R. et al. Resistance exercise prevents glucocorticoid-induced myopathy in heart transplant recipients. Med Sci Sport Exerc 1998;30(4):483–9. DOI: 10.1097/00005768-199804000-00003
73. Horber F., Scheidegger J., Grunig B. et al. Evidence that prednisone-induced myopathy is reversed by physical training. J Clin Endocrinol Metab 1985;61(1):83–8. DOI: 10.1210/jcem-61-1-83
74. LaPier T. Glucocorticoid-induced muscle atrophy. J Cardiopulm Rehabil 1997;17(2):76–84. DOI: 10.1097/00008483-199703000-00002
75. Yoshikawa N., Shimizu N., Uehara M. et al. The effects of bolus supplementation of branched-chain amino acids on skeletal muscle mass, strength, and function in patients with rheumatic disorders during glucocorticoid treatment. Mod Rheumatol 2017;27(3):508–17. DOI: 10.1080/14397595.2016.1213480
76. Ulla A., Uchida T., Miki Y. et al. Morin attenuates dexamethasonemediated oxidative stress and atrophy in mouse C2C12 skeletal myotubes. Arch Biochem Biophys 2021;704:108873. DOI: 10.1016/j.abb.2021.108873
77. Lee H., Kim Y., Nirmala F. et al. Chrysanthemum zawadskil Herbich attenuates dexamethasone-induced muscle atrophy through the regulation of proteostasis and mitochondrial function. Biomed Pharmacother 2021;136:111226. DOI: 10.1016/j.biopha.2021.111226
78. Shang Y., Kuang M., Wang Z. et al. An ultrashort peptide-based supramolecular hydrogel mimicking IGF-1 to alleviate glucocorticoid-induced sarcopenia. ACS Appl Mater Interfaces 2020;12(31):34678–88. DOI: 10.1021/acsami.0c09973
79. Chen H., Ma J., Ma X. Administration of tauroursodeoxycholic acid attenuates dexamethasone-induced skeletal muscle atrophy. Biochem Biophys Res Commun 2021;570:96–102. DOI: 10.1016/j.bbrc.2021.06.102
80. Lee M., Jeong H., Kim M.-J. et al. Nutrients against glucocorticoidinduced muscle atrophy. Foods 2022;11(5):687. DOI: 10.3390/foods11050687
81. Trush V.V., Sobolev V.I. Efficacy of the β2-adrenergic agonist formoterol in compensation of electrophysiological manifestations of steroid myopathy in animal experiments. Patologicheskaya fiziologiya i eksperimentalnaya terapiya = Pathological Physiology and Experimental Therapy 2019;63(3):35–47. (In Russ.). DOI: 10.25557/0031-2991.2019.03.35-47
82. Trush V.V., Sobolev V.I. Efficiency of α-lipoic acid in compensation of electrophysiological manifestations of steroid myopathy in animal experiments. Eksperimentalnaya i klinicheskaya farmakologiya = Experimental and Clinical Pharmacology 2021;84(12):20–8. (In Russ.). DOI: 10.30906/0869-2092-2021-84-12-20
83. Trush V.V., Sobolev V.I. Modulation by alphacalcidol of some electrophysiological manifestations of steroid myopathy in model experiments on animals. Uchenyye zapiski Krymskogo federalnogo universiteta im. V.I. Vernadskogo. Biologiya. Khimiya = Scientific notes of the Crimean Federal University named after V.I. Vernadsky. Biology. Chemistry 2022;8(2):198–217. (In Russ.).
84. Miyakoshi N., Sasaki H., Kasukawa Y. et al. Effects of a vitamin D analog, alfacalcidol, on bone and skeletal muscle in glucocorticoidtreated rats. Biomed Res 2010;31(6):329–36. DOI: 10.2220/biomedres.31.329
85. Ito S., Harada A., Kasai T. et al. Use of alfacalcidol in osteoporotic patients with low muscle mass might increase muscle mass: An investigation using a patient database. Geriatr Gerontol Int 2014;141:122–8. DOI: 10.1111/ggi.12222
86. Wang X., Yang X., Wang R. et al. Leucine alleviates dexamethasoneinduced suppression of muscle protein synthesis via synergy involvement of mTOR and AMPK pathways. Biosci Rep 2016;36(3):e00346. DOI: 10.1042/BSR20160096
87. Yamamoto D., Maki T., Herningtyas E. et al. Branched-chain amino acids protect against dexamethasone-induced soleus muscle atrophy in rats. Muscle Nerve 2010;41(6):819–27. DOI: 10.1002/mus.21621
88. Cochet C., Belloni G., Buondonno I. et al. The role of nutrition in the treatment of sarcopenia in old patients: From restoration of mitochondrial activity to improvement of muscle performance, a systematic review. Nutrients 2023;15(17):3703. DOI: 10.3390/nu15173703
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Zaytsevskaya S.A., Suponeva N.A., Antonova K.V., Grishina D.A., Narbut A.M. Steroid myopathy in patients with myasthenia gravis: a literature review. Neuromuscular Diseases. 2024;14(3):90-101. (In Russ.) https://doi.org/10.17650/2222-8721-2024-14-3-90-101
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