Stages of research and development of therapeutic approaches for Duchenne myodystrophy. Part I: the period before etiotropic approaches introduction

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Abstract

Duchenne muscular dystrophy is one of the most common inherited muscular dystrophies. The cause of this disease with an X‑linked recessive type of inheritance is mutations of the DMD gene, leading to the absence of the dystrophin protein this gene encodes or its impaired function. Loss of dystrophin leads to severe degenerative processes in patients, especially in muscle tissue, with impaired muscle function, loss of ability to move independently, respiratory failure, cardiomyopathies, etc.

More than 160 years have passed since the work of Guillaume‑Benjamin‑Armand Duchenne in the 19th century. Despite the efforts of many researchers who have developed various therapeutic approaches designed to alleviate the condition of patients if not cure it, few of them have significantly changed the course of the disease. Different approaches related to specific therapy of ischemia and fibrosis in affected muscles, correction of hormonal regulation of muscle tissue growth, therapeutic methods aimed at preventing damaged myocytes from excessive accumulation of calcium ions, which enhance proteolytic processes, suppression of oxidative stress in muscles, etc. have not yet shown high effectiveness both independently and in combination with glucocorticoids. The introduction of corticosteroid drugs made it possible to slow down disease development, but the average survival still does not exceed 30–40 years and patients spend many of them in a wheelchair. At the same time, the patients’ quality of life can be additionally diminished due to the common corticosteroids’ side effects.

About the authors

K. S. Kochergin-Nikitskiy

Research Centre for Medical Genetics

Author for correspondence.
Email: KochNik.KS@gmail.com
ORCID iD: 0000-0002-0096-4542

Konstantin Sergeevich Kochergin‑Nikitskiy

1 Moskvorechye St., Moscow 115522

Russian Federation

S. A. Smirnikhina

Research Centre for Medical Genetics

Email: fake@neicon.ru
ORCID iD: 0000-0002-1558-3048

1 Moskvorechye St., Moscow 115522

Russian Federation

A. V. Lavrov

Research Centre for Medical Genetics

Email: fake@neicon.ru
ORCID iD: 0000-0003-4962-6947

1 Moskvorechye St., Moscow 115522

Russian Federation

References

  1. Bladen C.L., Salgado D., Mongeset S. et al. The TREAT-NMD DMD Global Database: Analysis of more than 7,000 Duchenne muscular dystrophy mutations. Hum Mutat 2015;36(4):395–402. doi: 10.1002/humu.22758
  2. Blake D.J., Weir A., Newey S.E., Davies K.E. Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 2002;82(2):291–329. doi: 10.1002/humu.22758
  3. Van der Pijl E.M., van Putten M., Niks E.H. et al. Characterization of neuromuscular synapse function abnormalities in multiple Duchenne muscular dystrophy mouse models. Eur J Neurosci 2016;43(12):1623–35. doi: 10.1111/ejn.13249
  4. Tuffery-Giraud S., Béroud C., Leturcq F. et al. Genotype– phenotype analysis in 2,405 patients with a dystrophinopathy using the UMD–DMD database: A model of nationwide knowledgebase. Hum Mutat 2009;30(6):934–45. doi: 10.1002/humu.20976
  5. Oshima J., Magner D.B., Lee J.A. et al. Regional genomic instability predisposes to complex dystrophin gene rearrangements. Hum Genet 2009;126(3):411–23. doi: 10.1007/s00439-009-0679-9
  6. Pegoraro E., Hoffman E.P., Pivaet L. et al. SPP1 genotype is a deter minant of disease severity in Duchenne muscular dystrophy. Neurology 2011;76(3):219–26. doi: 10.1212/WNL.0b013e318207afeb
  7. Nowak K.J., Davies K.E. Duchenne muscular dystrophy and dystro phin: pathogenesis and opportunities for treatment. EMBO Rep 2004;5(9):872–6. doi: 10.1038/sj.embor.7400221
  8. Crisafulli S., Sultana J., Fontana A. et al. Global epidemiology of Duchenne muscular dystrophy: An updated systematic review and meta-analysis. Orphanet J Rare Dis 2020;15(1):141. doi: 10.1186/s13023-020-01430-8
  9. Mercuri E., Bönnemann C.G., Muntoni F. Muscular dystrophies. Lancet 2019;394(10213):2025–38. doi: 10.1016/S0140-6736(19)32910-1
  10. Landfeldt E., Thompson R., Sejersen T. et al. Life expectancy at birth in Duchenne muscular dystrophy: A systematic review and meta-analysis. Eur J Epidemiol 2020;35(7):643–53. doi: 10.1007/s10654-020-00613-8
  11. Nigro G., Comi L.I., Limongelli F.M. et al. Prospective study of X-linked progressive muscular dystrophy in campania. Muscle Nerve 1983;6(4):253–62. doi: 10.1002/mus.880060403
  12. Kilroy E.A., Ignacz A.C., Brann K.L. et al. Beneficial impacts of neuromuscular electrical stimulation on muscle structure and function in the zebrafish model of Duchenne muscular dystrophy. eLife 2022;11:e62760. doi: 10.7554/eLife.62760
  13. Werneck L.C., Lorenzoni P.J., Dal-Prá Ducci R. et al. Duchenne muscular dystrophy: an historical treatment review. Arq Neuropsiquiatr 2019;77:579–89. doi: 10.1590/0004-282X20190088
  14. Zupan A. Long-term electrical stimulation of muscles in children with duchenne and becker muscular dystrophy. Muscle Nerve 1992;15(3):362–7. doi: 10.1002/mus.880150316
  15. Yoshida M., Matsuzaki T., Date M. et al. Skeletal muscle fiber degeneration in mdx mice induced by electrical stimulation. Muscle Nerve 1997;20(11):1422–32. doi: 10.1002/(sici)1097-4598(199711)20:113.0.co;2-3
  16. Kar N.C., Pearson C.M. Cholinesterase and esterase activity in normal and dystrophic human muscle. Biochem Med 1973;7(3):452–9. doi: 10.1016/0006-2944(73)90066-5
  17. Serafini L., Bonvini E. Therapeutic trials with galantamine in Duchenne–Griesinger-type progressive muscular dystrophy. Rass Clin Sci 1961;37:20–4.
  18. Gamstorp I. Clinical evaluation of an oral anabolic steroid (methandrostenolone, dianabol CIBA) in children with muscular weakness and wasting. Acta Paediatr 1964;53(6):570–7. doi: 10.1111/j.1651-2227.1964.tb07269.x
  19. Dowben R.M., Perlstein M.A. Muscular dystrophy treated with norethandrolone. Arch Intern Med 1961;107:245–51. doi: 10.1001/archinte.1961.03620020095009
  20. Rudman D., Chyatte S.B., Pattersonet J.H. et al. Metabolic effects of human growth hormone and of estrogens in boys with Duchenne muscular dystrophy. J Clin Invest 1972;51(5):1118–24. doi: 10.1172/JCI106904
  21. Heckmatt J.Z., Heckmatt J.Z., Hyde S.A. et al. Therapeutic trial of isaxonine in duchenne muscular dystrophy. Muscle Nerve 1988;11(8):836–47. doi: 10.1002/mus.880110807
  22. Zavadenko N.N., Kamennykh L.N. Effect of sinestrol on the course of the myodystrophic process in progressive Duchenne muscular dystrophy. Zh Nevropatol Psikhiatr Im S S Korsakova 1989;89(8):41–5.
  23. Zatz M., Betti R.T.B., Levy J.A. Begnign duchenne muscular dystrophy in a patient with growth hormone deficiency. Am J Med Genet 1981;10(3):301–4. doi: 10.1002/ajmg.1320240323
  24. Fenichel G.M., Griggs R.C, Kissel J. et al. A randomized efficacy and safety trial of oxandrolone in the treatment of Duchenne dystrophy. Neurology 2001;56(8):1075–9. doi: 10.1212/wnl.56.8.1075
  25. Collipp P.J., Kelemen J., Chen S.Y. et al. Growth hormone inhibition causes increased selenium levels in Duchenne muscular dystrophy: A possible new approach to therapy. J Med Genet 1984; 21(4):254–6. doi: 10.1136/jmg.21.4.254
  26. Coakley J.H., Moorcraft J., Hipkin L.J. et al. The effect of mazindol on growth hormone secretion in boys with Duchenne muscular dystrophy. J Neurol Neurosurg Psychiatry 1988;51(12):1551–7. doi: 10.1136/jnnp.51.12.1551
  27. Tidball J.G., Wehling-Henricks M. Evolving therapeutic strategies for Duchenne muscular dystrophy: Targeting downstream events. Pediatr Res 2004;56(6):831–41. doi: 10.1203/01.PDR.0000145578.01985.D0
  28. Spencer M.J., Mellgren R.L. Overexpression of a calpastatin transgene in mdx muscle reduces dystrophic pathology. Hum Mol Genet 2002;11(21):2645–55. doi: 10.1093/hmg/11.21.2645
  29. Kitaura T. How β2-adrenergic agonists induce skeletal muscle hypertrophy? J Phys Fit Sports Med 2013;2(4):423–8. doi: 10.7600/jpfsm.2.423
  30. Skura C.L., Fowler E.G., Wetzel G.T. et al. Albuterol increases lean body mass in ambulatory boys with Duchenne or Becker muscular dystrophy. Neurology 2008;70(2):137–43. doi: 10.1212/01.WNL.0000287070.00149.a9
  31. Fowler E.G., Graves M.C., Wetzel G.T., Spencer M.J. Pilot trial of albuterol in Duchenne and Becker muscular dystrophy. Neurology 2004;62(6):1006–8. doi: 10.1212/01.wnl.0000118530.71646.0f
  32. Lavi E., Cohen A., Dor T. et al. Growth hormone therapy for children with Duchenne muscular dystrophy and glucocorticoid induced short stature. J Endocr Soc 2021;5(Suppl 1):A715. doi: 10.1210/jendso/bvab048.1455
  33. Rutter M.M., Collins J., Rose S.R. et al. Growth hormone treatment in boys with Duchenne muscular dystrophy and glucocorticoid-induced growth failure. Neuromuscul Disord 2012;22(12): 1046–56. doi: 10.1016/j.nmd.2012.07.009
  34. Cittadini A., Comi L.I., Longobardi S. et al. A preliminary randomized study of growth hormone administration in Becker and Duchenne muscular dystrophies. Eur Heart J 2003;24(7):664–72. doi: 10.1016/s0195-668x(02)00740-6
  35. Frank G.R., Smith R.E. Effective growth hormone therapy in a growth hormone deficient patient with Duchenne muscular dystrophy without evidence of acceleration of the dystrophic process. J Pediatr Endocrinol Metab 2001;14(2):211–4. doi: 10.1515/jpem.2001.14.2.211
  36. Shavlakadze T., White J., Hoh J.F.Y. et al. Targeted expression of insulin-like growth factor-I reduces early myofiber necrosis in dystrophic mdx mice. Mol Ther Elsevier 2004;10(5):829–43. doi: 10.1016/j.ymthe.2004.07.026
  37. Rutter M.M., Wong B.L., Collins J.J. et al. Recombinant human insulin-like growth factor-1 therapy for 6 months improves growth but not motor function in boys with Duchenne muscular dystrophy. Muscle Nerve 2020;61(5):623–31. doi: 10.1002/mus.26846
  38. Schuelke M., Wagner K.R., Stolz L.E. et al. Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med 2004;350(26):2682–8. doi: 10.1056/NEJMoa040933
  39. Wagner K.R., McPherron A.C., Winik N. et al. Loss of myostatin attenuates severity of muscular dystrophy in mdx mice. Ann Neurol 2002;52(6):832–6. doi: 10.1002/ana.10385
  40. Bogdanovich S., Krag T.O.B., Barton E.R. et al. Functional improvement of dystrophic muscle by myostatin blockade. Nature 2002;420(6914):418–21. doi: 10.1038/nature01154
  41. Campbell C., McMillan H.J., Mah J.K. et al. Myostatin inhibitor ACE-031 treatment of ambulatory boys with Duchenne muscular dystrophy: Results of a randomized, placebo-controlled clinical trial. Muscle Nerve 2017;55(4):458–64. doi: 10.1002/mus.25268
  42. Wagner K.R., Abdel-Hamid H.Z., Mah J.K. et al. Randomized phase 2 trial and open-label extension of domagrozumab in Duchenne muscular dystrophy. Neuromuscul Disord 2020;30(6):492–502. doi: 10.1016/j.nmd.2020.05.002
  43. Thomson W.H.S., Guest K.E. A trial of therapy by nucleosides and nucleotides in muscular dystrophy. J Neurol Neurosurg Psychiatry 1963;26(2):111–22. doi: 10.1136/jnnp.26.2.111
  44. Pearce J.M.S., Gubbay S.S., Hardy J. et al. Laevadosin in treatment of the duchenne type of muscular dystrophy: Preliminary results of a double-blind controlled trial. Br Med J 1964;2(5414):915–7. doi: 10.1136/bmj.2.5414.915
  45. Rybalka E., Timpani C.A., Stathi C.G. et al. Metabogenic and nutriceutical approaches to address energy dysregulation and skeletal muscle wasting in Duchenne muscular dystrophy. Nutrients 2015;7(12)9734–67. doi: 10.3390/nu7125498
  46. Thomson W.H.S., Smith I. X-linked recessive (Duchenne) muscular dystrophy (DMD) and purine metabolism: Effects of oral allopurinol and adenylate. Metabolism 1978;27(2):151–63. doi: 10.1016/0026-0495(78)90161-0
  47. Hellsten-Westing Y. Immunohistochemical localization of xanthine oxidase in human cardiac and skeletal muscle. Histochemistry 1993;100(3):215–22. doi: 10.1007/BF00269094
  48. Camiña F., Novo-Rodriguez M.I., Rodriguez-Segade S., Castro-Gago M. Purine and carnitine metabolism in muscle of patients with Duchenne muscular dystrophy. Clin Chim Acta 1995;243(2):151–64. doi: 10.1016/0009-8981(95)06164-9
  49. Thomson W.H., Smith I. Allopurinol in Duchenne’s muscular dystrophy. N Engl J Med 1978;299(2):101.
  50. Castro-Gago M., Lojo S., Novo I. et al. Effects of chronic allopurinol therapy on purine metabolism in Duchenne muscular dystrophy. Biochem Biophys Res Commun 1987;147(1):152–7. doi: 10.1016/s0006-291x(87)80100-6
  51. De Bruyn C.H., Kulakowski S., van Bennekom C.A. et al. Purine Metabolism in Duchenne Muscular Dystrophy. Purine Metabolism in Man-III: Clinical and Therapeutic Aspects. Boston: Springer US, 1980. Pp. 177–182. doi: 10.1007/978-1-4615-9140-5_29
  52. Kulakowski S., Renoirte P., de Bruyn C.H. Dynamometric and biochemical observations in Duchenne patients receiving allopurinol. Neuropediatrics 1981;12(1):92–4.
  53. Tamari H., Ohtani Y., Higashi A. et al. Xanthine oxidase inhibitor in Duchenne muscular dystrophy. Brain Dev 1982;4(2):137–43. doi: 10.1016/s0387-7604(82)80007-7
  54. Mendell J.R., Wiechers D.O. Lack of benefit of allopurinol in Duchenne dystrophy. Muscle Nerve 1979;2(1):53–6. doi: 10.1002/mus.880020108
  55. Doriguzzi C., Bertolotto A., Ganzit G.P. et al. Ineffectiveness of allopurinol in Duchenne muscular dystrophy. Muscle Nerve 1981;4(2):176–8. doi: 10.1002/mus.880040216
  56. Hunter J.R., Galloway J.R., Brooke M.M. et al. Effects of allopurinol in Duchenne’s muscular dystrophy. Arch Neurol 1983; 40(5):294–9. doi: 10.1001/archneur.1983.04050050062009
  57. Griffiths R.D., Cady E.B., Edwards R.H., Wilkie D.R. Muscle energy metabolism in Duchenne dystrophy studied by 31P-NMR: Controlled trials show no effect of allopurinol or ribose. Muscle Nerve 1985;8(9):760–7. doi: 10.1002/mus.880080904
  58. Bertorini T.E., Palmieri G.M., Griffin J. et al. Chronic allopurinol and adenine therapy in Duchenne muscular dystrophy: Effects on muscle function, nucleotide degradation, and muscle ATP and ADP content. Neurology 1985;35(1):61–5. doi: 10.1212/wnl.35.1.61
  59. Bakouche P., Chaouat D., Nick J. Allopurinol not effective in muscular dystrophy. N Engl J Med 1979;301(14):785. doi: 10.1056/NEJM197910043011414
  60. Stern L.M., Fewings J.D., Bretag A.H. et al. The progression of Duchenne muscular dystrophy: Clinical trial of allopurinol therapy. Neurology 1981;31(4):422–6. doi: 10.1212/wnl.31.4.422
  61. Petrillo S., Pelosi L., Piemonte F. et al. Oxidative stress in Duchenne muscular dystrophy: Focus on the NRF2 redox pathway. Hum Mol Genet 2017;26(14):2781–90. doi: 10.1093/hmg/ddx173
  62. Renjini R., Gayathri N., Nalini A. et al. Oxidative damage in muscular dystrophy correlates with the severity of the pathology: role of glutathione metabolism. Neurochem Res 2012;37(4):885–98. doi: 10.1007/s11064-011-0683-z
  63. Kelly-Worden M., Thomas E. Mitochondrial dysfunction in Duchenne muscular dystrophy. Open J Endocr Metab Dis 2014;4(8): 211–8. doi: 10.4236/ojemd.2014.48020
  64. Bodensteiner J.B., Engel A.G. Intracellular calcium accumulation in Duchenne dystrophy and other myopathies: A study of 567,000 mus cle fibers in 114 biopsies. Neurology 1978;28(5):439. doi: 10.1212/wnl.28.5.439
  65. Brenman J.E., Chao D.S., Xia H. et al. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 1995;82(5):743–52. doi: 10.1016/0092-8674(95)90471-9
  66. Wink D.A., Cook J.A., Pacelli R. et al. Nitric oxide (NO) protects against cellular damage by reactive oxygen species. Toxicol Lett 1995;82–83:221–6. doi: 10.1016/0378-4274(95)03557-5
  67. Uberti F., Lattuada D., Morsanuto V. et al. Vitamin D protects human endothelial cells from oxidative stress through the autophagic and survival pathways. J Clin Endocrinol Metab 2014;99(4): 1367–74. doi: 10.1210/jc.2013-2103
  68. Sander M., Chavoshan B., Harris S.A. et al. Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy. Proc Nat Acad Sci USA 2000;97(25):13818–23. doi: 10.1073/pnas.250379497
  69. Gremiakova T.A., Souslov V.М., Sakbaeva G.Е., Stepanov А.А. Vitamin D in the prevention and treatment of comorbid conditions in Duchenne muscular dystrophy. Nevrologicheskiy zhurnal im. L.O. Badalyana = L.O. Badalyan Neurological Journal 2021;2(1): 38–50. (In Russ.). doi: 10.46563/2686-8997-2021-2-1-38-50
  70. Bhattacharyya S., Bhattacharyya K., Maitra A. Possible mechanisms of interaction between statins and vitamin D. QJM Mon J Assoc Phys 2012;105(5):487–91. doi: 10.1093/qjmed/hcs001
  71. Pleshcheva A.V., Pigarova E.A., Dzeranova L.K. Vitamin D and metabolism: facts, myths and prejudices. Ozhirenie i metabolizm = Obesity And Metabolism 2012;(2):33–42. (In Russ.). doi: 10.14341/omet2012233-42
  72. Bianchi M.L., Morandi L., Andreucci E. et al. Low bone density and bone metabolism alterations in Duchenne muscular dystrophy: response to calcium and vitamin D treatment. Osteoporos Int 2011;22(2):529–39. doi: 10.1007/s00198-010-1275-5
  73. Debruin D.A., Andreacchio N., Hanson E.D. et al. The effect of vitamin D supplementation on skeletal muscle in the mdx mouse model of Duchenne muscular dystrophy. Sports 2019;7(5):96. doi: 10.3390/sports7050096
  74. Bian Q., McAdam L., Grynpas M. et al. Increased rates of vitamin D insufficiency in boys with Duchenne muscular dystrophy despite higher vitamin D3 supplementation. Glob Pediatr Health 2019; 6:2333794X19835661. doi: 10.1177/2333794X19835661
  75. Bessman S.P., Geiger P.J. Transport of energy in muscle: the phosphorylcreatine shuttle. Science 1981;211(4481):448–52. doi: 10.1126/science.6450446
  76. Bessman S.P., Carpenter C.L. The creatine-creatine phosphate energy shuttle. Annu Rev Biochem 1985;54:831–62. doi: 10.1146/annurev.bi.54.070185.004151
  77. Krzanowski J., Matschinsky F.M. Regulation of phosphofructokinase by phosphocreatine and phosphorylated glycolytic intermediates. Biochem Biophys Res Commun 1969;34(6):816–23. doi: 10.1016/0006-291x(69)90253-8
  78. Willoughby D.S., Rosene J. Effects of oral creatine and resistance training on myosin heavy chain expression. Med Sci Sports Exerc 2001;33(10):1674–81. doi: 10.1097/00005768-200110000-00010
  79. Louis M., Lebacq J., Poortmans J.R. et al. Beneficial effects of creatine supplementation in dystrophic patients. Muscle Nerve 2003;27(5):604–10. doi: 10.1002/mus.10355
  80. Walter M.C., Lochmüller H., Reilich P. et al. Creatine monohydrate in muscular dystrophies: A double-blind, placebo-controlled clinical study. Neurology 2000;54(9):1848–50. doi: 10.1212/wnl.54.9.1848
  81. Tarnopolsky M.A., Mahoney D.J., Vajsar J. et al. Creatine monohyd rate enhances strength and body composition in Duchenne muscular dystrophy. Neurology 2004;62(10):1771–7. doi: 10.1212/01.wnl.0000125178.18862.9d
  82. Banerjee B., Sharma U., Balasubramanian K. et al. Effect of creatine monohydrate in improving cellular energetics and muscle strength in ambulatory Duchenne muscular dystrophy patients: A randomized, placebo-controlled 31P MRS study. Magn Reson Imaging 2010;28(5):698–707. doi: 10.1016/j.mri.2010.03.008
  83. Hankard R.G., Hammond D., Haymond M.W., Darmaun D. Oral glutamine slows down whole body protein breakdown in Duchenne muscular dystrophy. Pediatr Res 1998;43(2):222–6. doi: 10.1203/00006450-199802000-00011
  84. Mok E., Eléouet-Da Violante C., Daubrosse C. et al. Oral glutamine and amino acid supplementation inhibit whole-body protein degradation in children with Duchenne muscular dystrophy. Am J Clin Nutr 2006;83(4):823–8. doi: 10.1093/ajcn/83.4.823
  85. Escolar D.M., Buyse G., Henricson E. et al. CINRG randomized controlled trial of creatine and glutamine in Duchenne muscular dystrophy. Ann Neurol 2005;58(1):151–5. doi: 10.1002/ana.20523
  86. Klyuchnikov S.O., Gnetneva E.S. Ubiquinone (coenzyme Q10): theory and clinical practice. Pediatria = Pediatrics 2008;87(3):103–10. (In Russ.)
  87. Folkers K., Simonsen R. Two successful double-blind trials with coenzyme Q10 (vitamin Q10) on muscular dystrophies and neurogenic atrophies. Biochim Biophys Acta 1995;1271(1):281–6. doi: 10.1016/0925-4439(95)00040-b
  88. Spurney C.F., Rocha C.T., Henricson E. et al. CINRG pilot trial of coenzyme Q10 in steroid treated Duchenne muscular dystrophy. Muscle Nerve 2011;44(2):174–8. doi: 10.1002/mus.22047
  89. Wang R.T., Silverstein Fadlon C.A., Ulm J.W. et al. Online self-report data for Duchenne muscular dystrophy confirms natural history and can be used to assess for therapeutic benefits. PLoS Curr 2014. doi: 10.1371/currents.md.e1e8f2be7c949f9ffe81ec6fca1cce6a
  90. Hodgens A., Sharman T. Corticosteroids. StatPearls. Treasure Island: StatPearls Publishing, 2023.
  91. Ericson-Neilsen W., Kaye A.D. Steroids: Pharmacology, complications, and practice delivery issues. Ochsner J 2014;14(2):203–7.
  92. Siegel I.M., Miller J.E., Ray R.D. Failure of corticosteroid in the treatment of Duchenne (pseudo-hypertrophic) muscular dystrophy. Report of a clinically matched three year double-blind study. IMJ Ill Med J 1974;145(1):32, 33.
  93. Angelini C., Peterle E. Old and new therapeutic developments in steroid treatment in Duchenne muscular dystrophy. Acta Myol 2012;31(1):9–15.
  94. Mendell J.R., Moxley R.T., Griggs R.C. et al. Randomized, double-blind six-month trial of prednisone in Duchenne’s muscular dystrophy. N Engl J Med 1989;320(24):1592–7. doi: 10.1056/NEJM198906153202405
  95. Brooke M.H., Fenichel G.M., Griggs R.C. et al. Clinical investigation of Duchenne muscular dystrophy. Interesting results in a trial of prednisone. Arch Neurol 1987;44(8):812–7. doi: 10.1001/archneur.1987.00520200016010
  96. Fenichel G.M., Florence J.M., Pestronk A. et al. Long-term benefit from prednisone therapy in Duchenne muscular dystrophy. Neurology 1991;41(12):1874–7. doi: 10.1212/wnl.41.12.1874
  97. Griggs R.C., Moxley R.T.3rd, Mendell J.R. et al. Duchenne dystrophy: Randomized, controlled trial of prednisone (18 months) and azathioprine (12 months). Neurology 1993;43(3 Pt 1):520. doi: 10.1212/wnl.43.3_part_1.520
  98. Griggs R.C., Moxley R.T., Mendell J.R. et al. Prednisone in Duchenne dystrophy: A Randomized, controlled trial defining the time course and dose response. Arch Neurol 1991;48(4):383–8. doi: 10.1001/archneur.1991.00530160047012
  99. Angelini C., Pegoraro E., Turella E. et al. Deflazacort in Duchenne dystrophy: Study of long-term effect. Muscle Nerve 1994;17(4):386–91. doi: 10.1002/mus.880170405
  100. Shieh P.B., Mcintosh J., Jin F. et al. Deflazacort versus prednisone/prednisolone for maintaining motor function and delaying loss of ambulation: A post HOC analysis from the ACT DMD trial. Muscle Nerve 2018;58(5):639–45. doi: 10.1002/mus.26191
  101. Biggar W.D., Skalsky A., McDonald C.M. Comparing deflazacort and prednisone in Duchenne muscular dystrophy. J Neuromuscul Dis 2022;9(4):463–76. doi: 10.3233/JND-210776
  102. Parente L. Deflazacort: Therapeutic index, relative potency and equivalent doses versus other corticosteroids. BMC Pharmacol Toxicol 2017;18(1):1. doi: 10.1186/s40360-016-0111-8
  103. Bonifati M.D., Ruzza G., Bonometto P. et al. A multicenter, double-blind, randomized trial of deflazacort versus prednisone in Duchenne muscular dystrophy. Muscle Nerve 2000;23(9):1344–7. doi: 10.1002/1097-4598(200009)23:93.0.co;2-f
  104. Angelini C. The role of corticosteroids in muscular dystrophy: A critical appraisal. Muscle Nerve 2007;36(4):424–35. doi: 10.1002/mus.20812
  105. Silversides C.K., Webb G.D., Harris V.A., Biggar D.W. Effects of deflazacort on left ventricular function in patients with Duchenne muscular dystrophy. Am J Cardiol 2003;91(6):769–72. doi: 10.1016/s0002-9149(02)03429-x
  106. Koeks Z., Bladen C.L., Salgado D. et al. Clinical outcomes in Duchenne muscular dystrophy: A study of 5345 patients from the TREAT-NMD DMD Global Database. J Neuromuscul Dis 2017;4(4):293–306. doi: 10.3233/JND-170280
  107. Kissel J.T., Lynn D.J., Rammohan K.W. et al. Mononuclear cell analysis of muscle biopsies in prednisone- and azathioprine-treated Duchenne muscular dystrophy. Neurology 1993;43(3 Pt 1):532. doi: 10.1212/wnl.43.3_part_1.532
  108. Kirschner J., Schessl J., Schara U. et al. Treatment of Duchenne muscular dystrophy with ciclosporin A: A randomised, double-blind, placebo-controlled multicentre trial. Lancet Neurol 2010;9(11):1053–9. doi: 10.1016/S1474-4422(10)70196-4
  109. Hoffman E.P., Riddle V., Siegler M.A. et al. Phase 1 trial of vamorolone, a first-in-class steroid, shows improvements in side effects via biomarkers bridged to clinical outcomes. Steroids 2018;134:43–52. doi: 10.1016/j.steroids.2018.02.010
  110. Hoffman E.P., Schwartz B.D., Mengle-Gaw L.J. et al. Vamorolone trial in Duchenne muscular dystrophy shows dose-related improvement of muscle function. Neurology 2019;93(13):e1312–e1323. doi: 10.1212/WNL.0000000000008168
  111. Klingler W., Jurkat-Rott K., Lehmann-Horn F., Schleip R. The role of fibrosis in Duchenne muscular dystrophy. Acta Myol 2012;31(3):184–95.
  112. Papich M.G. Penicillamine. Saunders Handbook of Veterinary Drugs. Elsevier, 2016. Pp. 612–613.
  113. Roelofs R.I., de Arango G.S., Law P.K. et al. Treatment of Duchenne’s muscular dystrophy with penicillamine: Results of a double-blind trial. Arch Neurol 1979;36(5):266–8. doi: 10.1001/archneur.1979.00500410044005
  114. Bradley W.G., Enomoto A., Gardner-Medwin D. A double-blind controlled trial of penicillamine therapy in Duchenne muscular dystrophy – interim comments. Proc R Soc Med 1977; 70(Suppl 3):94.
  115. Fenichel G.M., Brooke M.H., Griggs R.C. et al. Clinical investigation in Duchenne muscular dystrophy: Penicillamine and vitamin E. Muscle Nerve 1988;11(11):1164–8. doi: 10.1002/mus.880111110
  116. Romanelli R.G., Caligiuri A., Carloni V. et al. Effect of pentoxifylline on the degradation of procollagen type I produced by human hepatic stellate cells in response to transforming growth factor-beta 1. Br J Pharmacol 1997;122(6):1047–54. doi: 10.1038/sj.bjp.0701484
  117. Escolar D.M., Zimmerman A., Bertorini T. et al. Pentoxifylline as a rescue treatment for DMD. Neurology 2012;78(12):904–13. doi: 10.1212/WNL.0b013e31824c46be
  118. Lin P.-S., Chang H.-H., Yeh C.-Y. et al. Transforming growth factor beta 1 increases collagen content, and stimulates procollagen I and tissue inhibitor of metalloproteinase-1 production of dental pulp cells: Role of MEK/ERK and activin receptor-like kinase-5/ Smad signaling. J Formos Med Assoc 2017;116(5):351–8. doi: 10.1016/j.jfma.2016.07.014
  119. Zimmerman A., Clemens P.R., Tesi-Rocha C. et al. Liquid formulation of pentoxifylline is a poorly tolerated treatment for Duchenne dystrophy. Muscle Nerve 2011;44(2):170–3. doi: 10.1002/mus.22127
  120. Morales M.G., Gutierrez J., Cabello-Verrugio C. et al. Reducing CTGF/CCN2 slows down mdx muscle dystrophy and improves cell therapy. Hum Mol Genet 2013;22(24):4938–51. doi: 10.1093/hmg/ddt352
  121. Connolly A.M., Zaidman C.M., Brandsema J.F. et al. Pamrevlumab, a fully human monoclonal antibody targeting connective tissue growth factor, for non-ambulatory patients with Duchenne muscular dystrophy. J Neuromuscul Dis 2023;10(4):685–99. doi: 10.3233/JND-230019
  122. García A.M., Goldemberg A.L., Fernández H. et al. Effect of chronic administration of verapamil in Duchenne muscular dystrophy. Gen Pharmacol 1990;21(6):939–42. doi: 10.1016/0306-3623(90)90459-y
  123. Emery A.E., Skinner R., Howden L.C., Matthews M.B. et al. Verapamil in Duchenne muscular dystrophy. Lancet Lond Engl 1982;1(8271):559. doi: 10.1016/s0140-6736(82)92063-3
  124. Phillips M.F., Quinlivan R. Calcium antagonists for Duchenne muscular dystrophy. Cochrane Database Syst Rev 2008;4:CD004571. doi: 10.1002/14651858.CD004571.pub2
  125. Dick D.J., Gardner-Medwin D., Gates P.G. et al. A trial of flunarizine in the treatment of Duchenne muscular dystrophy. Muscle Nerve 1986;9(4):349–54. doi: 10.1002/mus.880090412
  126. Moxley R.T.3rd, Brooke M.H., Fenichel G.M. et al. Clinical investigation in Duchenne dystrophy. VI. Double-blind controlled trial of nifedipine. Muscle Nerve 1987;10(1):22–33. doi: 10.1002/mus.880100106
  127. Pernice W., Beckmann R., Ketelsen U.P. et al. A double-blind placebo controlled trial of diltiazem in Duchenne dystrophy. Klin Wochenschr 1988;66(13):565–70. doi: 10.1007/BF01720830
  128. Bertorini T.E., Palmieri G.M., Griffin J.W. et al. Effect of chronic treatment with the calcium antagonist diltiazem in Duchenne muscular dystrophy. Neurology 1988;38(4):609–13. doi: 10.1212/wnl.38.4.609
  129. Patten B.M., Zeller R.S. Clinical trials of vasoactive and antiserotonin drugs in Duchenne muscular dystrophy. Ann Clin Res 1983;15(4):164–6.
  130. Victor R.G., Sweeney H.L., Finkel R. et al. A phase 3 randomized placebo-controlled trial of tadalafil for Duchenne muscular dystrophy. Neurology 2017;89(17):1811–20. doi: 10.1212/WNL.0000000000004570

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