Progressive multifocal leukoencephalopathy as a complication of disease-modifying treatment of multiple sclerosis

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Abstract

The review provides modern understanding of the pathogenesis of progressive multifocal leukoencephalopathy (PML), a severe and potentially fatal form of multiple-lesion disorder of the brain white matter. Information about the frequency of its development in patients with disease-modifying treatment of multiple sclerosis is analyzed. The algorithms of optimization of PML risks in this category of patients with multiple sclerosis are described in detail. Summarized are the data on most significant PML biomarkers, the search for which is currently under way in many centers across the world. The first case of PML in Russia is briefly described.

About the authors

Maria N. Zakharova

Research Center of Neurology

Email: Lysogorskaya@neurology.ru
Россия, Moscow

Elena V. Lysogorskaia

Research Сenter of Neurology

Author for correspondence.
Email: Lysogorskaya@neurology.ru
Россия, Moscow

Maria V. Ivanova

Research Сenter of Neurology

Email: Lysogorskaya@neurology.ru
Россия, Moscow

Ivan А. Kochergin

Research Сenter of Neurology

Email: Lysogorskaya@neurology.ru
Россия, Moscow

Yulia E. Korzhova

Research Сenter of Neurology

Email: Lysogorskaya@neurology.ru
Россия, Moscow

References

  1. Zavalishin I.A., Zakharova M.N. [Multiple sclerosis: results and perspectives of the study]. Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova 1982; 82(2): 161–167. (In Russ.)
  2. Zavalishin I.A., Zakharova M.N., Zhuchenko T.D., Peresedova A.V. [Etiology and pathogenesis of multiple sclerosis]. In: Zavalishin I.A., Golovkin V.I. (eds.) Rasseyannyi skleros. Izbrannye voprosy teorii i praktiki [Multiple Sclerosis. Selected issues of theory and practice]. Moscow: Ministry of Health of Russia, Research center of neurology, RAMS, 2000: 537–579. (In Russ.)
  3. Bisaga G.N., Kovalenko A.V., Isayeva G.E. et al. [The use of mesenchymal stem cells in optic atrophy in patients with multiple sclerosis: a pilot study]. Annals of clinical and experimental neurology 2017; 11(2): 26–31. (In Russ.)
  4. Ryabtseva M.S., Negudova N.P., Batuashvili T.A., Simutenko L.V. [Experimental evaluation of bioequivalence of original and reproduced peptide preparations in multiple sclerosis]. Annals of clinical and experimental neurology 2018; 12(2): 39–44. (In Russ.)
  5. Votintseva M.V., Petrov A.M., Stolyarov I.D. [Drugs based on monoclonal antibodies: the present and the future in the treatment of multiple sclerosis (based on the materials of the 32nd Congress of the European Committee for the Treatment and Research of Multiple Sclerosis – ECTRIMS)]. Annals of clinical and experimental neurology 2017; 11(2): 83–88. (In Russ.)
  6. Zakharova M.N., Logunov D.Yu., Kochergin I.A., Bakulin I.S. [Endogenous retroviruses: from basic research to etiotropic therapy for multiple sclerosis]. Annals of clinical and experimental neurology 2015; 9(4): 49–53. (In Russ.)
  7. Zakharova M.N. Lipid myelin. In: Multiple sclerosis. Selected questions of theory and practice. In: Zavalishin I.A., Golovkin V.I. (eds.) Rasseyannyi skleros. Izbrannye voprosy teorii i praktiki [Multiple Sclerosis. Selected issues of theory and practice]. Moscow: Ministry of Health of Russia, Research center of neurology, RAMS, 2000: 69–96. (In Russ.)
  8. Boyko A.N., Lash N.Yu., Sharanova S.N. et al. A comparative placebo-controlled clinical trial of the efficacy and safety of glatiramer acetate 20 mg in patients with relapsing multiple sclerosis: the results of the first year of follow-up. Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova 2016. 10(2): 61–62. (In Russ.)
  9. Korzhova Yu.E., Vorobyova A.A., Ivanova M.V. et al. A comparison of the efficacy of natalizumab or fingolimod as second-line drugs in patients with multiple sclerosis. Medica mente. Lechim s umom 2016; (1): 63–66. (In Russ.)
  10. Hallervorden J. Eigennartige and nicht rubriziebare prozesse. In: Bumke O. (ed.) Handbuch der Geiteskranheiten, Die Anatomie der Phychosen. Berlin: Springer; 1930; 2: 1063–1107.
  11. Astrom K.E., Mancell E.L., Richardson E.P.J. Progressive multifocal encephalopathy: A hitharto unrecognized complication of chronic lymphocytic leukemia and lymphoma. Brain 1958; 81: 99–111. PMID: 13523006.
  12. ZuRhein G.M., Chou S.M. Particles resembling papova-virus in human cerebral demyelinating disease. Science 1965; 148: 1477–1479. PMID: 14301897.
  13. ZuRhein G.M. Association of papova-virions with a human demyelination disease (progressive multifocal leukoencephalopathy). Prog Med Virol 1969; 11: 185–248. PMID: 4906870.
  14. Padgett B.L., Walker D.L., ZuRhein G.M. et al. Cultivation of papova-like virus from human brain with progressive multifocal leukoencephalopathy. Lancet 1971; 1: 1257–1260. PMID: 4104715.
  15. Frisque R.J., Bream G.L., Cannella M.T. Human polyomavirus JC virus genome. J Virol 1984; 51: 458–469. PMID: 6086957.
  16. Gardner S.D., Feild A.M., Colleman D.V., Hulme B. New human papovavirus (BK) isolated from urine after renal transplantation. Lancet 1971. 1: 1253–1257. PMID: 4104714.
  17. Knowles W.A. Discovery and epidemiology of the human polyomaviruses BK virus (BKV) and JC virus (JCV). Adv Exp Med Biol 2006; 577: 19–45. doi: 10.1007/0-387-32957-9_2. PMID: 16626025.
  18. Reid C.E., Li H., Sur G. et al. Sequencing and analysis of JC virus DNA from natalizumab-treated PML patients. J Infect Dis 2011; 204: 237–244. doi: 10.1093/infdis/jir256. PMID: 21673034.
  19. Warnke C., Adams O., Kieseier B. Relevance of CD34+ cells as a reservoir for JC virus in patients with multiple sclerosis. JAMA Neurol 2014; 71: 1192. doi: 10.1001/jamaneurol.2014.1858. PMID: 25200546.
  20. Zakharova M.N. [Progressive multifocal leukoencephalopathy (literature review)]. Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova 2012; 112(9-2): 29–33. (In Russ.)
  21. Physician Information and Management Guidelines for Multiple Sclerosis patients on TYSABRI Therapy. European Medicines Agency. 2016. https://www.medicines.org.uk/emc/rmm/1199/Document
  22. Carrillo-Infante C., Richman S., Yu B. et al. Functional and survival outcomes of asymptomatic progressive multifocal leukoencephalopathy in natalizumab-treated multiple sclerosis patients: 2015 update. ECTRIMS Online Library 2016: EP1528.
  23. Power C., Gladden J.G., Halliday W. et al. AIDS- and non-AIDS-related PML association with distinct p53 polymorphism. Neurology 2000; 54: 743–746. PMID: 10680816.
  24. Antinori A., Ammassari A., Giancola M.L. et al. Epidemiology and prognosis of AIDS-associated progressive multifocal leukoencephalopathy in the HAART era. J Neurovirol 2001; 7: 323–328. doi: 10.1080/13550280152537184. PMID: 11517411.
  25. Garcia-Suarez J., de Miguel D., Krsnik I. et al. Changes in the natural history of progressive multifocal leukoencephalopathy in HIV-negative lymphoproliferative disorders: impact of novel therapies. Am J Hematol 2005; 80: 271–281. doi: 10.1002/ajh.20492. PMID: 16315252.
  26. Clavel G., Moulignier A., Semerano L. Progressive multifocal leukoencephalopathy and rheumatoid arthritis treatments. Joint Bone Spine. 2017; 84: 671–675. doi: 10.1016/j.jbspin.2017.03.002. PMID: 28323224.
  27. Molloy E.S., Calabrese L.H. Progressive multifocal leukoencephalopathy: a national estimate of frequency in systemic lupus erythematosus and other rheumatic diseases. Arthritis Rheum 2009; 60: 3761–3765. doi: 10.1002/art.24966. PMID: 19950261.
  28. Asztely F., Gilland E., Wattjes M.P., Lycke J. Rituximab treatment did not aggravate ongoing progressive multifocal leukoencephalopathy in a patient with multiple sclerosis. J Neurol Sci 2015; 353: 155–157. doi: 10.1016/j.jns.2015.04.010. PMID: 25908254.
  29. Carson K.R., Evens A.M., Richey E.A. et al. Progressive multifocal leukoencephalopathy after rituximab therapy in HIV-negative patients: a report of 57 cases from the Research on Adverse Drug Events and Reports Project. Blood 2009; 113: 4834–4840. doi: 10.1182/blood-2008-10-186999. PMID: 19264918.
  30. Ho P.R., Koendgen H., Campbell N. et al. Risk of natalizumab-associated progressive multifocal leukoencephalopathy in patients with multiple sclerosis: a retrospective analysis of data from four clinical studies. Lancet Neurol 2017; 16: 925–933. doi: 10.1016/S1474-4422(17)30282-X. PMID: 28969984.
  31. Mills E.A., Mao-Draayer Y. Understanding progressive multifocal leukoencephalopathy risk in multiple sclerosis patients treated with immunomodulatory therapies: a bird’s eye view. Front Immunol 2018; 9: 138. doi: 10.3389/fimmu.2018.00138. PMID: 29456537.
  32. Гусев Е.И., Гехт А.Б. (ред). Всероссийское общество неврологов. Клинические рекомендации. Рассеянный склероз. М.: Минздрав России, 2018. 129 c.
  33. Gusev E.I., Gekht A.B. (eds.). Vserossiyskoye obshchestvo nevrologov. Klinicheskiye rekomendatsii. Rasseyannyy skleroz [Russian Society of Neurologists. Clinical recommendations. Multiple sclerosis]. Moscow: Ministry of Health of Russia, 2018. 129 p. (In Russ.)
  34. Motte J., Kneiphof J., Straßburger-Krogias K. et al. Detection of JC virus archetype in cerebrospinal fluid in a MS patient with dimethylfumarate treatment without lymphopenia or signs of PML. J Neurol 2018; 265: 1880–1882. doi: 10.1007/s00415-018-8931-7. PMID: 29948248.
  35. Bloomgren G., Richman S., Hotermans C. et al. Risk of natalizumab-associated progressive multifocal leukoencephalopathy. N Engl J Med 2012; 366: 1870–1880. doi: 10.1056/NEJMoa1107829. PMID: 22591293.
  36. Carotenuto A., Scalia G., Ausiello F. et al. CD4/CD8 ratio during natalizumab treatment in multiple sclerosis patients. J Neuroimmunol 2017; 309: 47–50. doi: 10.1016/j.jneuroim.2017.05.006. PMID: 28601287.
  37. Iannetta M., Zingaropoli M.A., Bellizzi A. et al. Natalizumab affects T-cell phenotype in multiple sclerosis: implications for JCV reactivation. PLoS One 2016; 11: e0160277. doi: 10.1371/journal.pone.0160277. PMID: 27486658.
  38. Jilek S., Mathias A., Canales M. et al. Natalizumab treatment alters the expression of T-cell trafficking marker LFA-1 α-chain (CD11a) in MS patients. Mult Scler 2014; 20: 837–842. doi: 10.1177/1352458513513208. PMID: 24258149.
  39. Savage N.D., Harris S.H., Rossi A.G. et al Inhibition of TCR-mediated shedding of L-selectin (CD62L) on human and mouse CD4+ T cells by metalloproteinase inhibition: analysis of the regulation of Th1/Th2 function. Eur J Immunol 2002; 32: 2905–2914. doi: 10.1002/1521-4141(2002010)32:10<2905::AID-IMMU2905>3.0.CO;2-6. PMID: 12355444.
  40. Basnyat P., Hagman S., Kolasa M. et al. Association between soluble L-selectin and anti-JCV antibodies in natalizumab-treated relapsing-remitting MS patients. Mult Scler Relat Disord 2015; 4: 334–338. doi: 10.1016/j.msard.2015.06.008. PMID: 26195052.
  41. Schwab N., Schneider-Hohendorf T., Posevitz V. et al. L-selectin is a possible biomarker for individual PML risk in natalizumab-treated MS patients. Neurology 2013; 81: 865–871. doi: 10.1212/WNL.0b013e3182a351fb. PMID: 23925765.
  42. Lieberman L.A., Zeng W., Singh C. et al. CD62L is not a reliable biomarker for predicting PML risk in natalizumab-treated R-MS patients. Neurology 2016; 86: 375–381. doi: 10.1212/WNL.0000000000002314. PMID: 26718566.
  43. Zakharova M.N., Lysogorskaia E.V., Trushnikova T.N., Zhelnin A.V. [The case of development of progressive multifocal leukoencephalopathy in a patient with multiple sclerosis on the background of taking natalizumab]. Zhurnal nevrologii i psikhiatrii imeni S.S. Korsakova 2018; 8(2): 106–108. (In Russ.)

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