Relationship of viral infections and multiple sclerosis. Modern trends in the diagnosis and treatment of multiple sclerosis
Keywords:
multiple sclerosis, herpes virus 6, Epstein-Barr virus, reviewAbstract
Multiple sclerosis (MS) is a polyethiological disease that develops as an interaction between the immune system and external factors in genetically susceptible individuals. There is growing evidence that viruses can play a role in the pathogenesis of MS, acting as external triggers. However, it is not fully known whether a single virus is causal or several viruses can act as an impulse to the development of the disease. We examined the association of various viruses with MS, focusing on two herpesviruses: human herpesvirus 6 (HHV-6) and Epstein-Barr virus (EBV).
In recent years, the researchers have indicated that these two agents had the greatest impact as possible co-factors in the development of the disease. The most important evidence in favor HHV-6 and EBV association is the link between symptoms infectious mononucleosis and the persistent chronic process caused by EBV and HHV-6 with MS, serological data and viral load detection in MS patients. But it is know that the mononucleosis symptoms can be caused by other members of the herpes group. HHV-6 is significantly more likely detected in MS plaques, in contrast to EBV, in comparison with the results studies brain tissue and non-MS patients. And it was observed HHV-6 activation during MS relapses. Herpes viral load peripheral blood mononuclear cells (PBMCs), primarily EBV and HHV-6, was significantly higher in patients with MS than in the control group and was combined with changes in some parameters cellular and humoral immunity, significantly increasing in relapse periods of the disease. In this review, we propose new strategies, including the development of promising directions virological and immunological protocols MS diagnosis and treatment and formation clinical trials tactics, to find out the roles of different viruses and autoimmune processes in the MS pathogenesis to find a recovery algorithm for improving the life quality and possible MS problem solution.
For the large-scale clinical studies that could confirm or refute viruses participation in the MS pathogenesis, especially herpes, the advisability of antiviral and immunotherapy, we offer the method of direct immunofluorescence, which has a number of advantages: speed processing; the ability to investigate the viral load in the affected cells in the body fluids and tissues; highly specific; informative and economically sound.
Conclusions. This review discussed the role of infectious agents, mostly viruses, in the MS development and pathogenesis. Despite the presence links between MS and several viruses, it has not been proven that the virus is the cause of this neurological disease. Recently strong evidence focuses on the herpesvirus family member, such as EBV and HHV-6. Because these viruses are widespread among humankind, it creates unique challenges in establishing causation with MS. The isolation of the predicted agent from MS affected tissue, such as active plaques in the CNS; viral load PBMCs; and increasing the humoral and cellular immune response to these viruses in peripheral blood and liquor are strong arguments in support these viruses as triggers in the disease process. After all, only due to well-controlled trials of antiviral treatment causative or other pathogenetic link between these viruses and MS can be established.
References
Ahlgren C, Oden A, Toren K. et al. Multiple sclerosis incidence in the era of measles-mumps-rubella mass vaccinations . Acta Neurol Scand. 2013. № 119. Р. 313–320.
Baranzini SE, Mudge J, van Velkinburgh J. et al. Genome, epigenome and RNA sequences of monozygotic twins discordant for multiple sclerosis . Nature. 2010. № 464. Р. 1351–1356.
Tarlinton RE, Khaibullin T, Granatov E. The Interaction between viral and environmental risk factors in the pathogenesis of Multiple Sclerosis .Int J Mol Sci. 2019 Jan; № 20(2). P. 303-341.
Krone B, Grange JM. Multiple sclerosis: are protective immune mechanisms compromised by a complex infectious background? . Autoimmune Dis. 2011. Р. 708–750.
Thompson AJ, Baranzini SE, Geurts J. Multiple sclerosis (Review) . Lancet. 2018 Apr 21; № 391. P. 1622-1636.
Pol S, Schweser F, Bertolino N. et al. Characterization of leptomeningeal inflammation in rodent experimental autoimmune encephalomyelitis (EAE) model of multiple sclerosis . Exp Neurol. 2019 Apr. № 314. P. 82-90.
Maltsev DV. Herpes virus neuroinfection in humans: [Monograph]. Kyiv: Center for Educational Literature. 2015. pp. 371–445.
Mentis AA, Dardiotis E, Grigoriadis N. et al. Viruses and endogenous retroviruses in multiple sclerosis: From correlation to causation . Acta Neurol Scand. 2017 Dec №136(6). P. 606-616.
Abdelhak A, Weber MS, Tumani H. Primary Progressive Multiple Sclerosis: Putting Together the Puzzle . Front Neurol. 2017 May № 31. P. 234-265.
Pormohammad A, Azimi T, Falah F. et al. Relationship of human herpes virus 6 and multiple sclerosis: A systematic review and meta-analysis . J Cell Physiol. 2018 Apr № 233(4). P. 2850-2862.
Geginat J, Paroni M, Pagani M. et al. The Enigmatic Role of Viruses in Multiple Sclerosis: Molecular Mimicry or Disturbed Immune Surveillance? . Trends Immunol. 2017. № 38(7). P. 498-512.
Ramasamy R, Joseph B, Whittall T. Potential molecular mimicry between the human endogenous retrovirus W family envelope proteins and myelin proteins in multiple sclerosis . Immunol Lett. 2017. № 183. P. 79-85.
Dreyfus DH, Farina A, Farina GA. Molecular mimicry, genetic homology, and gene sharing proteomic "molecular fingerprints" using an EBV (Epstein-Barr virus)-derived microarray as a potential diagnostic method in autoimmune disease . Immunol Res. 2018. № 66(6). P. 686-695.
Langer-Gould A, Wu J, Lucas R. et al. Epstein-Barr virus, cytomegalovirus, and multiple sclerosis susceptibility: A multiethnic study . Neurology. 2017. № 89(13). P. 1330-1337.
Jog NR, McClain MT, Heinlen LD. et al. Epstein Barr virus nuclear antigen 1 (EBNA-1) peptides recognized by adult multiple sclerosis patient sera induce neurologic symptoms in a murine model . J Autoimmun. 2019. № 9. P. 102- 133.
Simon KC, Yang X, Munger KL. et al. EBNA1 and LMP1 variants in multiple sclerosis cases and controls . Acta Neurol Scand. 2011. № 124(1). P. 53-8.
Rabinstein A. A. Herpes Virus Encephalitis in Adults: Current Knowledge and Old Myths. Neurol Clin. 2017. N 35 (4). P. 695–705. doi: 10.1016/j.ncl.2017.06.006.
Vanderlugt C. L., Miller S. D. Epitope spreading in immune-mediated diseases: implications for immunotherapy / Nat Rev Immunol. 2002. N 2. P. 85–95.
Cornaby C, Gibbons L, Mayhew V. et al. B cell epitope spreading: mechanisms and contribution to autoimmune diseases . Immunol Lett. 2015. № 163(1). P. 56-68.
Mentis AA, Dardiotis E, Grigoriadis N. et al. Viruses and Multiple Sclerosis: From Mechanisms and Pathways to Translational Research Opportunities . Mol Neurobiol. 2017. № 54(5). P. 234-251.
Robinson AP, Harp CT, Noronha A. et al. The experimental autoimmune encephalomyelitis (EAE) model of MS: utility for understanding disease pathophysiology and treatment . Handb Clin Neurol. 2014. № 122. P. 73-89.
Dendrou CA, Fugger L, Friese MA. Immunopathology of multiple sclerosis . Nat Rev Immunol. 2015. № 15(9). P. 545-558.
Wekerle H. B cells in multiple sclerosis . Autoimmunity. 2017. № 50(1). P. 57-60.
Elyaman W, Khoury SJ. Th9 cells in the pathogenesis of EAE and multiple sclerosis . Semin Immunopathol. 2017. № 39(1). P. 79-87.
Glatigny S, Bettelli E. Experimental Autoimmune Encephalomyelitis (EAE) as Animal Models of Multiple Sclerosis (MS) . Cold Spring Harb Perspect Med. 2018. № 1. P. 8- 21.
Dobson R, Giovannoni G. Multiple sclerosis – a review . Eur J Neurol. 2019. № 26(1). P. 27-40.
Epstein DJ, Dunn J, Deresinski S. Infectious Complications of Multiple Sclerosis Therapies: Implications for Screening, Prophylaxis, and Management . Open Forum Infect Dis. 2018. № 5(8). P. 174-186.
Cusick MF, Libbey JE, Fujinami RS. Multiple sclerosis: autoimmunity and viruses . Curr Opin Rheumatol. 2013. № 25(4). P. 496-501.
Foxman E. F, Iwasaki A. Genome-virome interactions: examining the role of common viral infections in complex disease. Nat Rev Microbiol. 2011. N 9. P. 254–264.
Thorley-Lawson DA. Epstein-Barr virus: exploiting the immune system . Nat Rev Immunol. 2001. № 1. P. 75–82.
Langer-Gould A, Wu J, Lucas R. et al. Epstein-Barr virus, cytomegalovirus, and multiple sclerosis susceptibility: A multiethnic study . Neurology. 2017. № 89 (13). P. 1330-1337.
Fierz W. Multiple sclerosis: an example of pathogenic viral interaction? Virol J. 2017. № 14 (1). P. 42.
Otto C, Oltmann A, Stein A. et al. Intrathecal EBV antibodies are part of the polyspecific immune response in multiple sclerosis . Neurology. 2011. № 76. P. 1316–1321.
Lassmann H, Niedobitek G, Aloisi F. et al. Epstein-Barr virus in the multiple sclerosis brain: a controversial issue–report on a focused workshop held in the Centre for Brain Research of the Medical University of Vienna . Austria. Brain. 2011. № 134. P. 2772–2786.
Morandi E, Jagessar SA, Hart BA. et al. EBV Infection Empowers Human B Cells for Autoimmunity: Role of Autophagy and Relevance to Multiple Sclerosis . J Immunol. 2017. № 199 (2). P. 435–448.
Willis SN, Stadelmann C, Rodig SJ. et al. Epstein-Barr virus infection is not a characteristic feature of multiple sclerosis brain . Brain. 2009. № 132. P. 3318–3328.
Handel AE, Williamson AJ, Disanto G. et al. An updated meta-analysis of risk of multiple sclerosis following infectious mononucleosis . PLoS One. 2010. № 5. P. 23-25.
Nielsen TR, Rostgaard K, Askling J. et al. Effects of infectious mononucleosis and HLA-DRB1*15 in multiple sclerosis . Mult Scler. 2009. № 15. P. 431–436.
Sheik-Ali S. Infectious mononucleosis and multiple sclerosis - Updated review on associated risk . Mult Scler Relat Disord. 2017. № 14. P. 56-59.
Ascherio A., Munger K. L. Environmental risk factors for multiple sclerosis. Part I: the role of infection. Ann Neurol. 2007. N 61. P. 288–299.
Downham C, Visser E, Vickers M. et al. Season of infectious mononucleosis as a risk factor for multiple sclerosis: A UK primary care case-control study . Mult Scler Relat Disord. 2017. № 17. P. 103-106.
Wang YF, He DD, Liang HW. et al. The identification of up-regulated ebv-miR-BHRF1-2-5p targeting MALT1 and ebv-miR-BHRF1-3 in the circulation of patients with multiple sclerosis . Clin Exp Immunol. 2017. N 189 (1). P. 120–126. doi: 10.1111/cei.12954.
Hollsberg P, Kusk M, Bech E. Presence of Epstein-Barr virus and human herpesvirus 6B DNA in multiple sclerosis patients: associations with disease activity . Acta Neurol Scand. 2005. № 112. P. 395–402.
Höllsberg P, Haahr S. Multiple sclerosis is linked to Epstein-Barr virus infection . Rev Med Virol. 2006. № 16(5). P. 297-310.
Sotelo J., Ordonez G., Pineda B. Varicella-zoster virus at relapses of multiple sclerosis. J Neurol. 2007. № 254. P. 493–500.
Alvarez R, Cour I, Kanaan A. et al. Detection of viral genomes of the Herpesviridae family in multiple sclerosis patients by means of the polymerase chain reaction (PCR) . Enferm Infec Microbiol Clin. 2000. № 18. P. 223–228.
Hassani A, Corboy JR, Al-Salam S. et al. Epstein-Barr virus is present in the brain of most cases of multiple sclerosis and may engage more than just B cells . PLoS One. 2018. № 13(2). P. 237-254.
Sanders VJ, Felisan S, Waddell A. et al. Detection of herpesviridae in postmortem multiple sclerosis brain tissue and controls by polymerase chain reaction . J Neurovirol. 1996. № 2(4). P. 249-258.
Alvarez-Lafuente R, García-Montojo M, De Las Heras V. et al. Herpesviruses and human endogenous retroviral sequences in the cerebrospinal fluid of multiple sclerosis patients . Mult Scler. 2008. № 14(5). P. 595-601.
Denne C, Kleines M, Dieckhöfer A. et al. Intrathecal synthesis of anti-viral antibodies in pediatric patients . Eur J Paediatr Neurol. 2007. № 11(1). P. 29-34.
Mancuso R, Hernis A, Cavarretta R. et al. Detection of viral DNA sequences in the cerebrospinal fluid of patients with multiple sclerosis . J Med Virol. 2010. № 82(6). P. 1051-1057.
Hogestyn JM, Mock DJ, Mayer-Proschel M. Contributions of neurotropic human herpesviruses herpes simplex virus 1 and human herpesvirus 6 to neurodegenerative disease pathology . Neural Regen Res. 2018. № 13(2) P. 211-221.
Moore FG, Wolfson C. Human herpes virus 6 and multiple sclerosis (Review) . Acta Neurol Scand. 2002. № 106(2). P. 63-83.
Voumvourakis KI, Kitsos DK, Tsiodras S. et al. Human herpesvirus 6 infection as a trigger of multiple sclerosis . Mayo Clin Proc. 2010. № 85(11). P. 1023-30.
Sola P, Merelli E, Marasca R. et al. Human herpesvirus 6 and multiple sclerosis: survey of anti-HHV-6 antibodies by immunofluorescence analysis and of viral sequences by polymerase chain reaction . J Neurol Neurosurg Psychiatry. 1993. № 56. P. 917–919.
Czarnowska A, Kapica-Topczewska K, Zajkowska O. et al. Herpesviridae Seropositivity in Patients with Multiple Sclerosis: First Polish Study . Eur Neurol. 2018. № 80(5-6). P. 229-235.
Wilborn F, Schmidt CA, Brinkmann V. et al. A potential role for human herpesvirus type 6 in nervous system disease . J Neuroimmunol. 1994. № 49. P. 213–214.
Ramroodi N, Sanadgol N, Ganjali Z. et al. Monitoring of active human herpes virus 6 infection in Iranian patients with different subtypes of multiple sclerosis . J Pathog. 2013. № 19. P.49-52.
Lisitsyn N, Lisitsyn N, Wigler M. Cloning the differences between two complex genomes. Science. 1993. № 259. P. 946–951.
Oikonen M, Laaksonen M, Aalto V. et al. Temporal relationship between environmental influenza A and Epstein-Barr viral infections and high multiple sclerosis relapse occurrence . Mult Scler. 2011. № 17. P. 672–680.
Buljevac D, Flach HZ, Hop WC. et al. Prospective study on the relationship between infections and multiple sclerosis exacerbations . Brain. 2002. № 125. P. 952–960.
Mailand MT, Frederiksen JL. Vaccines and multiple sclerosis: a systematic review . J Neurol. 2017. № 264(6). P. 1035-1050.
Confavreux C, Suissa S, Saddier P. et al. Vaccinations and the risk of relapse in multiple sclerosis. Vaccines in Multiple Sclerosis Study Group . N Engl J Med. 2001. № 344. P. 319–326.
Farez M. F., Correale J. Immunizations and risk of multiple sclerosis: systematic review and meta-analysis. J Neurol. 2011. № 258. P. 1197–1206.
Berti R, Brennan MB, Soldan SS. et al. Increased detection of serum HHV-6 DNA sequences during multiple sclerosis (MS) exacerbations and correlation with parameters of MS disease progression . J Neurovirol. 2002. № 8. P. 250–256.
Chapenko S, Millers A, Nora Z. et al. Correlation between HHV-6 reactivation and multiple sclerosis disease activity . J Med Virol. 2003. № 69. P. 111–117.
Alvarez-Lafuente R, De las Heras V, Bartolome M. et al. Relapsing-remitting multiple sclerosis and human herpesvirus 6 active infection . Arch Neurol. 2004. № 61. P. 1523–1527.
Rotola A, Ravaioli T, Gonelli A. et al. U94 of human herpesvirus 6 is expressed in latently infected peripheral blood mononuclear cells and blocks viral gene expression in transformed lymphocytes in culture . Proc Natl Acad Sci USA. 1998. № 95. P. 13911–13916.
Manouchehrinia A, Tanasescu R, Kareem H. et al. Prevalence of a history of prior varicella/herpes zoster infection in multiple sclerosis . J Neurovirol. 2017. № 23(6). P. 839-844.
Hernández-González O, Martínez-Palomo A, Sotelo J. et al. Varicella-Zoster Virus in Cerebrospinal Fluid at Relapses of Multiple Sclerosis is Infective in Vitro . Arch Med Res. 2018. № 49(5). P. 350-355.
Jarius S, Eichhorn P, Franciotta D. et al. The MRZ reaction as a highly specific marker of multiple sclerosis: re-evaluation and structured review of the literature . J Neurol. 2017. № 264(3). P. 453-466.
Kattimani Y, Veerappa AM. Complex interaction between mutant HNRNPA1 and gE of varicella zoster virus in pathogenesis of multiple sclerosis . Autoimmunity. 2018. № 51(4). P. 147-151.
Badihian S, Manouchehri N, Badihian N. More evidence is needed to show any role of cytomegalovisrus and varicella zoster virus in pathogenesis of multiple sclerosis . J Neuroimmunol. 2017. № 15 (313). P. 123-124.
Marrie RA, Wolfson C. Multiple sclerosis and varicella zoster virus infection: a review . Epidemiol Infect. 2001. Vol. 127. № 2. P. 315-25.
Sotelo J, Martinez-Palomo A, Ordonez G. et al. Varicella-zoster virus in cerebrospinal fluid at relapses of multiple sclerosis . Ann Neurol. 2008. № 63. P. 303–311.
Burgoon MP, Cohrs RJ, Bennett JL. et al. Varicella zoster virus is not a disease-relevant antigen in multiple sclerosis . Ann Neurol. 2009. № 65. P. 474–479.
Kang JH, Sheu JJ, Kao S. et al. Increased risk of multiple sclerosis following herpes zoster: a nationwide, population-based study . J Infect Dis. 2011. № 204. P. 188–192.
Perron H, Bernard C, Bertrand JB. et al. Endogenous retroviral genes, Herpesviruses and gender in Multiple Sclerosis . J Neurol Sci. 2009. № 286. P. 65–72.
Emmer A, Staege MS, Kornhuber ME. The retrovirus/superantigen hypothesis of multiple sclerosis . Cell Mol Neurobiol. 2014. № 34(8). P. 1087-1096.
Mostafa A, Jalilvand S, Shoja Z. Multiple sclerosis-associated retrovirus, Epstein-Barr virus, and vitamin D status in patients with relapsing remitting multiple sclerosis . J Med Virol. 2017. № 89(7). P. 1309-1313.
Oh J, Vidal-Jordana A, Montalban X. Multiple sclerosis: clinical aspects . Curr Opin Neurol. 2018. № 31(6). P. 752-759
Perron H, Garson JA, Bedin F. et al. Molecular identification of a novel retrovirus repeatedly isolated from patients with multiple sclerosis. The Collaborative Research Group on Multiple Sclerosis . Proc Natl Acad Sci USA. 1997. № 94. P. 7583–7588.
Blond JL, Beseme F, Duret L. et al. Molecular characterization and placental expression of HERV-W, a new human endogenous retrovirus family . J Virol. 1999. № 73. P. 1175–1185.
Hon GM, Erasmus RT, Matsha T. Multiple sclerosis-associated retrovirus and related human endogenous retrovirus-W in patients with multiple sclerosis: a literature review . J Neuroimmunol. 2013. № 263(1-2). P. 8-12.
Ramasamy R, Joseph B, Whittall T. Potential molecular mimicry between the human endogenous retrovirus W family envelope proteins and myelin proteins in multiple sclerosis . Immunol Lett. 2017. № 183. P. 79-85.
Charvet B, Reynaud JM, Gourru-Lesimple G. et al. Induction of Proinflammatory Multiple Sclerosis-Associated Retrovirus Envelope Protein by Human Herpesvirus-6A and CD46 Receptor Engagement . Front Immunol. 2018. № 9. P. 2803-2809.
Morandi E, Tarlinton RE, Tanasescu R. et al. Human endogenous retroviruses and multiple sclerosis: Causation, association, or after-effect? . Mult Scler. 2017. № 23(8). P. 1050-1055.
Küry P, Nath A, Créange A. Human Endogenous Retroviruses in Neurological Diseases . Trends Mol Med. 2018. № 24(4). P. 379-394.
Brütting C, Emmer A, Kornhuber M. et al. A survey of endogenous retrovirus (ERV) sequences in the vicinity of multiple sclerosis (MS)-associated single nucleotide polymorphisms (SNPs) . Mol Biol Rep. 2016. № 43(8). P. 827-36.
de Luca V, Martins Higa A, Malta Romano C. et al. Cross-reactivity between myelin oligodendrocyte glycoprotein and human endogenous retrovirus W protein: nanotechnological evidence for the potential trigger of multiple sclerosis . Micron. 2019. № 120. P. 66-73.
Adams J. M. Measles antibodies in patients with multiple sclerosis. Neurology. 1967. № 17. P. 707.
Brankin B, Osman M, Herlihy L. et al. Failure to detect measles virus RNA, by reverse transcription-polymerase chain reaction, in peripheral blood leucocytes of patients with multiple sclerosis . Mult Scler. 1996. № 1. P. 204–206.
Geeraedts F, Wilczak N, van Binnendijk R. et al. Search for morbillivirus proteins in multiple sclerosis brain tissue . J. Neuroreport. 2004. № 15. P. 27–32
Ahlgren C, Oden A, Haghighi S. et al. The effect of live, attenuated measles vaccine and measles infection on measles antibody levels in serum and CSF of patients with multiple sclerosis or clinically isolated syndrome . J Neuroimmunol. 2011. № 235. P. 98–103.
Abboud H, Hill E, Siddiqui J, Serra A. et al. Neuromodulation in multiple sclerosis . Mult Scler. 2017. № 23(13). P. 1663-1676.
Harris VK, Stark J, Vyshkina T. et al. Phase I Trial of Intrathecal Mesenchymal Stem Cell-derived Neural Progenitors in Progressive Multiple Sclerosis . EBioMedicine. 2018. № 29. P. 23-30.
Fainardi E., Castellazzi M., Tamborino C. et al. Chlamydia pneumoniae-specific intrathecal oligoclonal antibody response is predominantly detected in a subset of multiple sclerosis patients with progressive forms . J Neurovirol. 2009. № 15. P. 425–433.
Franciotta D, Di Stefano AL, Jarius S. et al. Cerebrospinal BAFF and Epstein-Barr virus-specific oligoclonal bands in multiple sclerosis and other inflammatory demyelinating neurological diseases . J Neuroimmunol. 2011. № 230. P. 160–163.
Virtanen JO, Pietilainen-Nicklen J, Uotila L. et al. Intrathecal human herpesvirus 6 antibodies in multiple sclerosis and other demyelinating diseases presenting as oligoclonal bands in cerebrospinal fluid . J Neuroimmunol. 2011. № 237. P. 93–97.
Salzer J, Svenningsson R, Alping P. et al. Rituximab in multiple sclerosis: A retrospective observational study on safety and efficacy . Neurology. 2016. № 87(20). P. 2074-2081.
Hu Y, Nie H, Yu HH. et al. Efficacy and safety of rituximab for relapsing-remitting multiple sclerosis: A systematic review and meta-analysis . Autoimmun Rev. 2019. № 18(5). P. 542-548.
Whitley R. The new age of molecular diagnostics for microbial agents. N Engl J Med. 2008. № 358. P. 988–989.
Wang D, Coscoy L, Zylberberg M. et al. Microarray-based detection and genotyping of viral pathogens . Proc Natl Acad Sci USA. 2002. № 99. P. 15687–15692.
Palacios G, Quan PL, Jabado OJ. et al. Panmicrobial oligonucleotide array for diagnosis of infectious diseases . Emerg Infect Dis. 2007. № 13. P. 73–81.
Palacios G, Druce J, Du L. et al. A new arenavirus in a cluster of fatal transplant-associated diseases . N Engl J Med. 2008. № 358. P. 991–998.
Karpishchenko AI. Medical laboratory technology: [Guide to clinical laboratory diagnostics in 2 volumes]. T. 2. . GEOTAR-Media. 2013. P. 548-549.
Bech E, Lycke J, Gadeberg P. et al. A randomized, double-blind, placebo-controlled MRI study of anti-herpes virus therapy in MS . Neurology. 2002. № 58(1). P. 31-36.
Friedman JM, Bove R, Alwan S. et al. Management of multiple sclerosis during pregnancy and the reproductive years: a systematic review . Obstet Gynecol. 2014. № 124(6). P. 1157-1168.
Lycke J. Trials of antivirals in the treatment of multiple sclerosis . Acta Neurol Scand. 2017. № 136. P. 45-48.
Morre SA, van Beek J, De Groot CJ. et al. Epstein-Barr virus present in the CNS of patients with MS? . J Neurology. 2001. № 56. P. 692.
Montalban X, Gold R, Thompson AJ. et al. ECTRIMS/EAN Guideline on the pharmacological treatment of people with multiple sclerosis . Mult. Scler., 2018. № 24(2). P. 96–120.
La Mantia L, Di Pietrantonj C, Rovaris M. et al. Interferons-beta versus glatiramer acetate for relapsing-remitting multiple sclerosis . Cochrane Database Syst Rev. 2016. № 11. P. 45-56
Cohen J, Belova A, Selmaj K. et al. Equivalence of Generic Glatiramer Acetate in Multiple Sclerosis: A Randomized Clinical Trial . JAMA Neurol. 2015. № 72(12)/ P. 1433-1441.
Signori A, Gallo F, Bovis F. et al. Long-term impact of interferon or Glatiramer acetate in multiple sclerosis: A systematic review and meta-analysis . Mult Scler Relat Disord. 2016. № 6. P. 57-63.
Kaltsatou A, Flouris AD. Impact of pre-cooling therapy on the physical performance and functional capacity of multiple sclerosis patients: A systematic review . Mult Scler Relat Disord. 2019. № 27. P. 419-423.
Federle L, Puthenparampil M, Stenta G. et al. Alemtuzumab as rescue therapy in case of multiple sclerosis rebound following Natalizumab break: Clinical case and literature review . Mult Scler Relat Disord. 2019. № 30. P. 262-264.
Song Y, Lao Y, Liang F. et al. Efficacy and safety of siponimod for multiple sclerosis: Protocol for a systematic review and meta-analysis . Medicine (Baltimore). 2019. № 98(34). P. 1541-1545.
Kwiatkowski A, Gallois J, Bilbault N. et al. Herpes encephalitis during natalizumab treatment in multiple sclerosis . Mult. Scler. 2012. Vol. 18 (6). P. 909-911.
Shenoy ES, Mylonakis E, Hurtado RM. et al. Natalizumab and HSV meningitis . J. Neurovirol. 2011. Vol. 17 (3). P. 288-290.
Yao K, Gagnon S, Akhyani N. et al. Reactivation of human herpesvirus-6 in natalizumab treated multiple sclerosis patients . PLoS One. 2008. Vol. 3 (4). P. 2028-2034.
Schweikert A, Kremer M, Ringel F. et al. Primary central nervous system lymphoma in a patient treated with natalizumab . Ann. Neurol. 2009. Vol. 66 (3). P. 403-406.
Costelloe L, Jones J, Coles A. Secondary autoimmune diseases following alemtuzumab therapy for multiple sclerosis . Expert Rev. Neurother. 2012. Vol. 12 (3). P. 335-341.
Caruso A., Vecchio R., Patti F., Neri S. Drug rash with eosinophilia and systemic signs syndrome in a patient with multiple sclerosis . Clin. Ther. 2009. Vol. 31 (3). P. 580-584.
Aramideh Khouy R, Karampoor S, Keyvani H. et al. The frequency of varicella-zoster virus infection in patients with multiple sclerosis receiving fingolimod J Neuroimmunol. 2019. № 328. P. 94-97.
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2019 Annals of Mechnikov's Institute
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 Unported License.
