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Review

The Long and Evolving Relationship between Viruses and Multiple Sclerosis

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Pages 871-883 | Published online: 21 Sep 2012

References

  • Compston A , ColesA. Multiple sclerosis. Lancet372 , 1502–1517 (2008).
  • Weiner HL . Multiple sclerosis is an inflammatory T-cell-mediated autoimmune disease. Arch. Neurol.61 , 1613–1615 (2004).
  • Roach ES . Is multiple sclerosis an autoimmune disorder? Arch. Neurol.61 , 1615–1616 (2004).
  • Zamvil SS , SteinmanL. The T lymphocyte in experimental allergic encephalomyelitis. Annu. Rev. Immunol.8 , 579–621 (1990).
  • Gran B , HemmerB, VergelliM, McFarlandHF, MartinR. Molecular mimicry and multiple sclerosis: degenerate T-cell recognition and the induction of autoimmunity. Ann. Neurol.45(5) , 559–567 (1999).
  • Hemmer B , NesslerS, ZhouD, KieseierB, HartungHP. Immunopathogenesis and immunotherapy of multiple sclerosis. Nat. Clin. Pract. Neurol.2(4) , 201–211 (2006).
  • Poskanzer DC , OksenbergJR. The neurobiology of multiple sclerosis: genes, inflammation and neurodegeneration. Neuron52 , 61–76 (2006).
  • Herna MA , ZhangSM, LipworthL et al. Multiple Sclerosis and age at infection with common viruses. Epidemiology 13 , 301–306 (2001).
  • Kurtzke JF . Epidemiologic evidence for multiple sclerosis as an infection. Clin. Microb. Rev.6(4) , 382–427 (1993).
  • Kurtzke JF , HeltbergA. Multiple sclerosis in the Faroe Islands: an epitome. J. Clin. Epidemiol.54 , 1–22 (2001).
  • Poskanzer DC , SchapiraK, MillerH. Multiple sclerosis and poliomyelitis. Lancet2 , 917–921 (1963).
  • Zilber N , Kutai-BermanM, KahanaE, KorczynAD. Multiple sclerosis and birth order. Acta Neurol. Scand.78 , 313–317 (1988).
  • Martyn CN . The epidemiology of multiple sclerosis. In: McAlpine‘s Multiple Sclerosis. Matthews WB, Compston A, Allen IV, Martyn CN (Eds). Churchill Livingstone, PA, USA (1991).
  • Bansil S , TroianoR, Rohowsky-KochanC et al. Multiple sclerosis: pathogenesis and treatment. Semin. Neurol. 14(2) , 146–153 (1994).
  • Oleszak EL , ChangJR, FriedmanH, KatsetosCD, PlatsoucasCD. Theiler‘s virus infection: a model for multiple sclerosis. Clin. Microbiol. Rev.17(1) , 174–207 (2004).
  • Tsunoda I , FujinamiRS. Neuropathogenesis of Theiler‘s murine encephalomyelitis virus infection, an animal model for multiple sclerosis. J. Neuroimmune. Pharmacol.5(3) , 355–369 (2010).
  • Pawate S , SriramS. The role of infections in the pathogenesis and course of multiple sclerosis. Ann. Indian. Acad. Neurol.13(2) , 80–86 (2010).
  • Hunter SF , HaflerDA. Ubiquitous pathogens: links between infection and autoimmunity in MS? Neurology55(2) , 164–165 (2000).
  • Fujinami RS , OldstoneMB. Amino acid homology between the encephalitogenic site of myelin basic protein and virus: mechanism for autoimmunity. Science230 , 1043–1045 (1985).
  • Wucherpfennig KW , StromingerJL. Molecular mimicry in T cell-mediated autoimmunity: viral peptides activate human T cell clones specific for myelin basic protein. Cell80 , 695–705 (1995).
  • Olson JK , CroxfordJL, CalenoffMA, Dal Canto MC, Miller SD. A virus-induced molecular mimicry model of multiple sclerosis. J. Clin. Invest.108(2) , 311–318 (2001).
  • Lang HL , JacobsenH, IkemizuS et al. A functional and structural basis for TCR cross-reactivity in multiple sclerosis. Nat. Immunol. 3(10) , 940–943 (2002).
  • Jilek S , KuhleJ, MeylanP et al. Severe post-EBV encephalopathy associated with myelin oligodendrocyte glycoprotein-specific immune response. J. Neuroimmunol. 192 , 192–197 (2007).
  • Lünemann JD , JelcicI, RobertsS et al. EBNA1-specific T cells from patients with multiple sclerosis cross react with myelin antigens and co-produce INF-gamma and IL-2. J. Exp. Med. 205 , 1763–1773 (2008).
  • Challoner PB , SmithKT, ParkerJD et al. Plaque-associated expression of human herpesvirus 6 in multiple sclerosis. Proc. Natl Acad. Sci. USA 92(16) , 7440–7444 (1995).
  • Buljevac D , van Doornum GJ, Flach HZ et al. Epstein–Barr virus and disease activity in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry76(10) , 1377–1381 (2005).
  • Ordoñez G , PinedaB, Garcia-NavarreteR, SoteloJ. Brief presence of varicella-zoster vral DNA in mononuclear cells during relapses of multiple sclerosis. Arch. Neurol.61(4) , 529–532 (2004).
  • Ross RT , CheangM. Geographic similarities between varicella and multiple sclerosis: an hypothesis on the environmental factor of multiple sclerosis. J. Clin. Epidemiol.48 , 731–737 (1995).
  • Marrie RA , WolfsonC. Multiple sclerosis and varicella zoster virus infection: a review. Epidemiol. Infect.127 , 315–325 (2001).
  • Mancuso R , DelbueS, BorghiE et al. Increased prevalence of varicella zoster virus DNA in cerebrospinal fluid from patients with multiple sclerosis. J. Med. Virol. 79(2) , 192–199 (2007).
  • Mancuso R , HernisA, CavarrettaR et al. Detection of viral DNA sequences in the cerebrospinal fluid of patients with multiple sclerosis. J. Med. Virol. 82(6) , 1051–1057 (2010).
  • Kang JH , SheuJJ, KaoS, LinHC. Increased risk of multiple sclerosis following herpes zoster: a nationwide, population-based study. J. Infect. Dis.204 , 188–192 (2011).
  • Sotelo J , CoronaT. Varicella zoster virus and relapsing remitting multiple sclerosis. Mult. Scler. Int.2147–2163 (2011).
  • Mainka C , FussB, GeigerH, HöfelmayrH, WolffMH. Characterization of viremia at different stages of Varicella zoster virus infection. J. Med. Virol.56(1) , 91–98 (1998).
  • Pineda B , SanigerMDM, Chánez-CárdenasME et al. Solid-phase assay for the detection of varicella zoster virus. Future Virol. 4(6) , 543–551 (2009).
  • Burgoon MP , CohrsRJ, BennettJL et al. Varicella zoster virus is not a disease-relevant antigen in multiple sclerosis. Ann. Neurol. 65(4) , 474–479 (2009).
  • Kleinschmidt-DeMasters BK , GildenDH. Varicella-zoster virus infections of the nervous system: clinical and pathologic correlates. Arch. Pathol. Lab. Med.125(6) , 770–780 (2001).
  • Yuki N . Infectious origins of, and molecular mimicry in, Guillain–Barré and Fisher syndromes. Lancet Infect. Dis.1(1) , 29–37 (2001).
  • Scarisbrick IA , RodriguezM. Hit–hit and hit–run: viruses in the playing field of multiple sclerosis. Curr. Neurol. Neurosci. Rep.3(3) , 265–271 (2003).
  • Braun DK , DominguezG, PellettPE. Human herpesvirus 6. Clin. Microb. Rev.10 , 521–567 (1997).
  • Dockrell DH , SmithTF, PayaCV. Human herpes virus 6. Mayo. Clin. Proc.74 , 163–170 (1999).
  • Meinl E . Concepts of viral pathogenesis of multiple sclerosis. Curr. Opin. Neurol.12 , 303–307 (1999).
  • Kakalacheva K , LünemannJD. Environmental triggers of multiple sclerosis. FEBS Lett.585(23) , 3724–3729 (2011).
  • Moore FG , WolfsonC. Human herpes virus 6 and multiple sclerosis. Acta Neurol. Scand.106(2) , 63–83 (2002).
  • Voumvourakis KI , KitsosDK, TsiodrasS, PetrikkosG, StamboulisE. Human herpesvirus 6 infection as a trigger of multiple sclerosis. Mayo Clin. Proc.85(11) , 1023–1030 (2010).
  • Kieff ED , RickinsonAB. Epstein–Barr virus and its replication. In: Fields Virology Volume 2. Knipe DM, Howley PM (Eds). Wolters Kluwer Health/Lippincott Williams & Wilkins, PA, USA, 2603–2654 (2007).
  • Lucas RM , HughesAM, LayML et al. Epstein–Barr virus and multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 82(10) , 1142–1148 (2011).
  • Ascherio A , MungerKL Environmental risk factors for multiple sclerosis. Part I: the role of infection. Ann. Neurol.61(4) , 288–299 (2007).
  • Nielsen TR , RostgaardK, NielsenNM et al. Multiple sclerosis after infectious mononucleosis. Arch. Neurol. 64(1) , 72–75 (2007).
  • Takeuchi K , Tanaka-TayaK, KazuyamaY et al. Prevalence of Epstein–Barr virus in Japan: trends and future prediction. Pathol. Int. 56(3) , 112–116 (2006).
  • Melbye M Ebbesen P, Levine PH et al. Early primary infection and high Epstein–Barr virus antibody titers in Greenland Eskimos at high risk for nasopharyngeal carcinoma. Int. J. Cancer.34 , 619–623 (1984).
  • Ahlgren C , TorenK, OdenA et al. A population-based case-control study on viral infections and vaccinations and subsequent multiple sclerosis risk. Eur. J. Epidemiol. 24 , 541–552 (2009).
  • Thacker EL Mirzaei F, Ascherio A. Infectious mononucleosis and risk for multiple sclerosis: a meta-analysis. Ann. Neurol.59(3) , 499–503 (2006).
  • Ascherio A , MungerKL. 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: Epstein–Barr virus and multiple sclerosis: epidemiological evidence. Clin. Exp. Immunol.160(1) , 120–124 (2010).
  • DeLorenze GN , MungerKL, LennetteE, OrentreichN, VogelmanJ, AscherioA. Epstein–Barr virus and multiple sclerosis: evidence of association from a prospective study with long-term follow-up. Arch. Neurol.63(6) , 839–844 (2006).
  • Klutts JS , FordBA, PerezNR et al. Evidence-based approach for interpretation of Epstein–Barr virus serological patterns. J. Clin. Microbiol. 47 , 3204–3210 (2009).
  • Cepok S , ZhouD, SrivastavaR, NesslerS et al. Identification of Epstein–Barr virus proteins as putative targets of the immune response in multiple sclerosis. J. Clin. Invest. 115(5) , 1352–1360 (2005).
  • Jaquiery E , JilekS, SchluepM et al. Intrathecal immune responses to EBV in early MS. Eur. J. Immunol. 40 , 878–887 (2010).
  • Larsen PD , BloomerLC, BrayPF. Epstein–Barr nuclear antigen and viral capsid antigen antibody titers in multiple sclerosis. Neurology35 , 435– 438 (1985).
  • Shirodaria PV , HaireM, FlemingE et al. Viral antibody titers. Comparison in patients with multiple sclerosis and rheumatoid arthritis. Arch. Neurol. 44 , 1237–1241 (1987).
  • Zivadinov R , ZorzonM, Weinstock-GuttmanB et al. Epstein–Barr virus is associated with gray matter atrophy in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 80(6) , 620–625 (2009).
  • Farrell RA , AntonyD, WallGR et al. Humoral immune response to EBV in multiple sclerosis is associated with disease activity on MRI. Neurology 73(1) , 32–38 (2009).
  • Ben Fredj N , RotolaA, NefziF et al. Identification of human herpesviruses 1 to 8 in Tunisian multiple sclerosis patients and healthy blood donors. J. Neurovirol. 18(1) , 12–19 (2012).
  • Ferrante P , Omodeo-ZoriniE, ZuffolatoMR et al. Human T-cell lymphotropic virus tax and Epstein–Barr virus DNA in peripheral blood of multiple sclerosis patients during acute attack. Acta Neurol. Scand. 169 , 79–85 (1997).
  • Lunemann JD , HuppkeP, RobertsS et al. Broadened and elevated humoral immune response to EBNA1 in pediatric multiple sclerosis. Neurology 71 , 1033–1035 (2008).
  • Alvarez-Lafuente R , García-MontojoM, De las Heras V, Bartolomé M, Arroyo R. Clinical parameters and HHV-6 active replication in relapsing-remitting multiple sclerosis patients. J. Clin. Virol.37(Suppl. 1) , S24–S6 (2006).
  • Lünemann JD , EdwardsN, MuraroPA et al. Increased frequency and broadened specificity of latent EBV nuclear antigen-1-specific T cells in multiple sclerosis. Brain129(Pt 6) , 1493–1506 (2006).
  • Lindsey J , HatfieldL, CrawfordM, PatelS. Quantitative PCR for Epstein–Barr virus DNA and RNA in multiple sclerosis. Mult. Scler.15 , 153–158 (2009).
  • Serafini B , RosicarelliB, FranciottaD et al. Dysregulated Epstein–Barr virus infection in the multiple sclerosis brain. J. Exp. Med. 2899–2912 (2007).
  • Willis SN , StadelmannC, RodigSJ et al. Epstein–Barr virus infection is not a characteristic feature of multiple sclerosis brain. Brain 132(12) , 3318–3328 (2009).
  • Sargsyan SA , ShearerAJ, RitchieAM et al. Absence of Epstein–Barr virus in the brain and CSF of patients with multiple sclerosis. Neurology 74 , 1127–1135 (2010).
  • Tzartos JS , KhanG, VossenkamperA, Cruz-SadabaM et al. Association of innate immune activation with latent Epstein–Barr virus in active MS lesions. Neurology 78(1) , 15–23 (2012).
  • Peferoen LA , LamersF, LodderLN et al. Epstein Barr virus is not a characteristic feature in the central nervous system in established multiple sclerosis. Brain 133(Pt 5) , e137 (2010).
  • Otto C , OltmannA, SteinA et al. EBV antibodies are part of the polyspecific immune response in multiple sclerosis. Neurology 76(15) , 1316–1321 (2011).
  • Thorley-Lawson D . Epstein–Barr virus: exploiting the immune system. Nat. Rev. Immunol.1(1) , 75–82(2001).
  • Bryce J , Boschi-PintoC, ShibuyaK et al. WHO estimates of the causes of death in children. Lancet 365 , 1147–1152 (2005).
  • Gadoth N . Subacute sclerosing panencephalitis (SSPE) the story of a vanishing disease. Brain Dev. doi:10.1016/j.braindev.2011.12.008 (2012) (Epub ahead of print).
  • Khalili K , WhiteMK, LublinF, FerranteP, BergerJR. Reactivation of JC virus and development of PML in patients with multiple sclerosis. Neurology68(13) , 985–990 (2007).
  • Stoner GL . Implications of progressive multifocal leukoencephalopathy and JC virus for the etiology of MS. Acta Neurol. Scand.83 , 20–33 (1991).
  • Yednock TA , CannonC, FritzLC et al. Prevention of experimental autoimmune encephalomyelitisis by antibodies against α4β1 integrin. Nature 356 , 63–66 (1992).
  • Kleinschmidt-DeMasters BK , TylerKL. Progressive multifocal leukoencephalopathy complicating treatment with natalizumab and interferon beta-1a for multiple sclerosis. N. Engl. J. Med.353 , 369–374 (2005).
  • Langer-Gould A , AtlasSW, GreenAJ, BollenAW, PelletierD. Progressive multifocal leukoencephalopathy in a patient treated with natalizumab. N. Engl. J. Med.353 , 375–381 (2005).
  • Van Assche G , Van Ranst M, Sciot R et al. Progressive multifocal leukoencephalopathy after natalizumab therapy for Crohn‘s disease. N. Engl. J. Med.353 , 362–368 (2005).
  • Herroelen L , de Keyser J, Ebinger G. Central-nervous-system demyelination after immunisation with recombinant hepatitis B vaccine. Lancet338(8776) , 1174–1175 (1991).
  • Konstantinou D , PaschalisC, MaraziotisT, DimopoulosP, BassarisH, SkoutelisA. Two episodes of leukoencephalitis associated with recombinant hepatitis B vaccination in a single patient. Clin. Infect. Dis.33 , 1772–1773 (2001).
  • Vlacha V , FormanEN, MironD, PeterG. Recurrent thrombocytopenic purpura after repeated measles–mumps–rubella vaccination. Pediatrics97 , 738–739 (1996).
  • Rudick RA . Central nervous system complications of viral infections and vaccines. In: Cecil Textbook of Medicine 21st Edition. Goldman L, Claude Bennett J (Eds). Saunders, PA, USA, 2149–2151 (2000).
  • Lévy-Bruhl D , DesenclosJC, RebièreI, DruckerJ. Central demyelinating disorders and hepatitis B vaccination: a risk-benefit approach for pre-adolescent vaccination in France. Vaccine20(16) , 2065–2071 (2002).
  • Schattner A . Consequence or coincidence? The occurrence, pathogenesis and significance of autoimmune manifestations after viral vaccines. Vaccine23(30) , 3876–3886 (2005).
  • Farez MF , CorrealeJ. Immunizations and risk of multiple sclerosis: systematic review and meta-analysis. J. Neurol.258(7) , 1197–1206 (2011).
  • DeStefano F , VerstraetenT, JacksonLA et al. Vaccinations and risk of central nervous system demyelinating diseases in adults. Arch. Neurol. 60(4) , 504–509 (2003).
  • Verstraeten T , DavisR, DeStefanoF. Immunity to tetanus is protective against the development of multiple sclerosis. Med. Hypotheses65(5) , 966–969 (2005).
  • Goldberg SH , AlbrightAV, LisakRP, Gonzalez-ScaranoF. Polymerase chain reaction analysis of human herpesvirus-6 sequences in the sera and cerebrospinal fluid of patients with multiple sclerosis. J. Neurovirol.5 , 134–139 (1999).
  • Berti R , BrennanMB, SoldanSS 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. 8 , 250–256 (2002).
  • Âlvarez-Lafuente R , Martín-EstefaníaC, De las Heras V et al. Prevalence of herpesvirus DNA in MS patients and healthy blood donors. Acta Neurol. Scand.105 , 95–99 (2002).
  • Giovannoni G , EbersG. Multiple sclerosis: the environment and causation. Curr. Opin. Neurol.20 , 261–268 (2007).
  • Soldan SS , BertiR, SalemN et al. Association of human herpes virus 6 (HHV-6) with multiple sclerosis: increased IgM response to HHV-6 early antigen and detection of serum HHV-6 DNA. Nat. Med. 3 , 1394–1397 (1997).
  • Ablashi DV , LappsW, KaplanM et al. Human herpesvirus-6 (HHV-6) infection in multiple sclerosis: a preliminary report. Mult. Scler. 4 , 490–496 (1998).
  • Ongradi J , RajdaC, MarodiCL et al. A pilot study on the antibodies to HHV-6 variants and HHV-7 in CSF of MS patients. J. Neurovirol. 5 , 529–532 (1999).
  • Behzad-Behbahani A , MikaeiliMH, EntezamM et al. Human herpesvirus-6 viral load and antibody titer in serum samples of patients with multiple sclerosis. J. Microbiol. Immunol. Infect. 44(4) , 247–251 (2011).
  • Ahlgren C , OdenA, HaghighiS 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. 235(1–2) , 98–103 (2011).
  • Ahlgren C , OdénA, BergströmT, LyckeJ. Serum and CSF measles antibody levels increase over time in patients with multiple sclerosis or clinically isolated syndrome. J. Neuroimmunol.247(1–2) , 70–74 (2012).
  • Brankin B , OsmanM, HerlihyL, HawkinsSA, CosbySL. Failure to detect measles virus RNA, by reverse transcription-polymerase chain reaction, in peripheral blood leucocytes of patients with multiple sclerosis. Mult. Scler.1(4) , 204–206 (1996).
  • Bogdanovic G , PriftakisP, HammarinAL et al. Detection of JC virus in cerebrospinal fluid (CSF) samples from patients with progressive multifocal leukoencephalopathy but not in CSF samples from patients with herpes simplex encephalitis, enteroviral meningitis, or multiple sclerosis. J. Clin. Microbiol. 36(4) , 1137–1138 (1998).
  • Buckle GJ , GodecMS, RubiJU et al. Lack of JC viral genomic sequences in multiple sclerosis brain tissue by polymerase chain reaction. Ann. Neurol. 32(6) , 829–831 (1992).
  • Ferrante P , Omodeo-ZoriniE, Caldarelli-StefanoR et al. Detection of JC virus in cerebrospinal fluid of Multiple sclerosis patients. Mult. Scler. 4 , 49–54 (1998).
  • Koralnik IJ , BodenD, MaiVX, LordCI, LetvinNL. JC virus DNA load in patients with and without progressive multifocal leukoencephalopathy. Neurology52(2) , 253–260 (1999).

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