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Monkeypox in Multiple Sclerosis patients: Should we be alert?

  • Vinícius Oliveira Boldrini
    Correspondence
    Corresponding author.
    Affiliations
    Autoimmune Research Laboratory – Department of Genetics, Microbiology and Immunology – Institute of Biology – University of Campinas – Campinas, SP, Brazil

    Neuroimmunology Unit – Department of Genetics, Evolution, Microbiology and Immunology – Institute of Biology – University of Campinas – Campinas, SP, Brazil

    Neuroimaging Laboratory – Department of Neurology – University of Campinas – Campinas, SP, Brazil
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  • Alfredo Damasceno
    Affiliations
    Neuroimaging Laboratory – Department of Neurology – University of Campinas – Campinas, SP, Brazil

    The Brazilian Institute of Neuroscience and Neurotechnology – University of Campinas – Campinas, SP, Brazil
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  • Clarissa Lin Yasuda
    Correspondence
    Corresponding author.
    Affiliations
    Neuroimaging Laboratory – Department of Neurology – University of Campinas – Campinas, SP, Brazil

    The Brazilian Institute of Neuroscience and Neurotechnology – University of Campinas – Campinas, SP, Brazil
    Search for articles by this author
Published:October 07, 2022DOI:https://doi.org/10.1016/j.msard.2022.104228
      Dear Editor,
      Previously reported as sporadic outbreaks in West and Central Africa, monkeypox virus infection is now occurring worldwide and has been classified by World Health Organization (WHO) as a Public Health Emergency of International Concern (PHEIC). Until 25 June, 3,000 cases of monkeypox had been reported in 47 countries. Strikingly, by 23 July, more than 16,000 cases from 75 countries and territories were already reported causing five deaths (
      • Taylor L.
      Monkeypox: WHO declares a public health emergency of international concern.
      ). According to WHO, by 06 October, there are a total of 71,237 laboratory-confirmed cases of the disease and 1,097 probable cases, including 26 deaths. To date, the 10 most affected countries globally are: United States of America (n = 26,723), Brazil (n = 8,147), Spain (n = 7,209), France (n = 4,043), The United Kingdom (n = 3,654), Germany (n = 3,640), Peru (n = 2,587), Colombia (n = 2,453), Mexico (n = 1,968) and Canada (n = 1,400). Together, these countries account for 86.8% of the total cases reported for monkeypox worldwide (

      World Health Organization (WHO). 2022. 2022 Monkeypox Outbreack: Global Trends. Available online at: https://worldhealthorg.shinyapps.io/mpx_global/#2_Global_situation_update. (accessed October 10, 2022).

      ).
      From April to June 2022, Thornhill and coworkers (
      • Thornhill J.P.
      • Barkati S.
      • Walmsley S.
      • Rockstroh J.
      • Antinori A.
      • Harrison L.B.
      • Palich R.
      • Nori A.
      • Reeves I.
      • Habibi M.S.
      • Apea V.
      • Boesecke C.
      • Vandekerckhove L.
      • Yakubovsky M.
      • Sendagorta E.
      • Blanco J.L.
      • Florence E.
      • Moschese D.
      • Maltez F.M.
      • Goorhuis A.
      • Pourcher V.
      • Migaud P.
      • Noe S.
      • Pintado C.
      • Maggi F.
      • Hansen A.-B.E.
      • Hoffmann C.
      • Lezama J.I.
      • Mussini C.
      • Cattelan A.
      • Makofane K.
      • Tan D.
      • Nozza S.
      • Nemeth J.
      • Klein M.B.
      • Orkin C.M.
      Monkeypox virus infection in humans across 16 countries — April–June 2022.
      ) reported a cohort of 528 infected individuals, in which transmission was almost totally (95%) suspected to occurring through sexual activity among white (75%), gay or bisexual men (98%) with the diagnosis (41%) of human immunodeficiency virus (HIV) infection. In this cohort, the most common clinical findings included: rash or skin lesions (95%), fever (62%), lymphadenopathy (56%), lethargy or exhaustion (41%), myalgia (31%), headache (27%), among others. Hospitalization was more likely associated with pain management and soft-tissue superinfection, less commonly with acute kidney injury and myocarditis.
      To date, as reported, amplification of transmission through sexual networks disproportionately affected men who have sex with men; however, besides sexual and close contact with skin lesions, nosocomial transmission and contaminated fomites (
      • Adler H.
      • Gould S.
      • Hine P.
      • Snell L.B.
      • Wong W.
      • Houlihan C.F.
      • Osborne J.C.
      • Rampling T.
      • Beadsworth M.B.
      • Duncan C.J.
      • Dunning J.
      • Fletcher T.E.
      • Hunter E.R.
      • Jacobs M.
      • Khoo S.H.
      • Newsholme W.
      • Porter D.
      • Porter R.J.
      • Ratcliffe L.
      • Schmid M.L.
      • Semple M.G.
      • Tunbridge A.J.
      • Wingfield T.
      • Price N.M.
      • Abouyannis M.
      • Al-Balushi A.
      • Aston S.
      • Ball R.
      • Beeching N.J.
      • Blanchard T.J.
      • Carlin F.
      • Davies G.
      • Gillespie A.
      • Hicks S.R.
      • Hoyle M.-.C.
      • Ilozue C.
      • Mair L.
      • Marshall S.
      • Neary A.
      • Nsutebu E.
      • Parker S.
      • Ryan H.
      • Turtle L.
      • Smith C.
      • van Aartsen J.
      • Walker N.F.
      • Woolley S.
      • Chawla A.
      • Hart I.
      • Smielewska A.
      • Joekes E.
      • Benson C.
      • Brindley C.
      • Das U.
      • Eyton-Chong C.K.
      • Gnanalingham C.
      • Halfhide C.
      • Larru B.
      • Mayell S.
      • McBride J.
      • Oliver C.
      • Paul P.
      • Riordan A.
      • Sridhar L.
      • Storey M.
      • Abdul A.
      • Abrahamsen J.
      • Athan B.
      • Bhagani S.
      • Brown C.S.
      • Carpenter O.
      • Cropley I.
      • Frost K.
      • Hopkins S.
      • Joyce J.
      • Lamb L.
      • Lyons A.
      • Mahungu T.
      • Mepham S.
      • Mukwaira E.
      • Rodger A.
      • Taylor C.
      • Warren S.
      • Williams A.
      • Levitt D.
      • Allen D.
      • Dixon J.
      • Evans A.
      • McNicholas P.
      • Payne B.
      • Price D.A.
      • Schwab U.
      • Sykes A.
      • Taha Y.
      • Ward M.
      • Emonts M.
      • Owens S.
      • Botgros A.
      • Douthwaite S.T.
      • Goodman A.
      • Luintel A.
      • MacMahon E.
      • Nebbia G.
      • O'Hara G.
      • Parsons J.
      • Sen A.
      • Stevenson D.
      • Sullivan T.
      • Taj U.
      • van Nipsen tot Pannerden C.
      • Winslow H.
      • Zatyka E.
      • Alozie-Otuka E.
      • Beviz C.
      • Ceesay Y.
      • Gargee L.
      • Kabia M.
      • Mitchell H.
      • Perkins S.
      • Sasson M.
      • Sehmbey K.
      • Tabios F.
      • Wigglesworth N.
      • Aarons E.J.
      • Brooks T.
      • Dryden M.
      • Furneaux J.
      • Gibney B.
      • Small J.
      • Truelove E.
      • Warrell C.E.
      • Firth R.
      • Hobson G.
      • Johnson C.
      • Dewynter A.
      • Nixon S.
      • Spence O.
      • Bugert J.J.
      • Hruby D.E.
      Clinical features and management of human monkeypox: a retrospective observational study in the UK.
      ;
      • Thornhill J.P.
      • Barkati S.
      • Walmsley S.
      • Rockstroh J.
      • Antinori A.
      • Harrison L.B.
      • Palich R.
      • Nori A.
      • Reeves I.
      • Habibi M.S.
      • Apea V.
      • Boesecke C.
      • Vandekerckhove L.
      • Yakubovsky M.
      • Sendagorta E.
      • Blanco J.L.
      • Florence E.
      • Moschese D.
      • Maltez F.M.
      • Goorhuis A.
      • Pourcher V.
      • Migaud P.
      • Noe S.
      • Pintado C.
      • Maggi F.
      • Hansen A.-B.E.
      • Hoffmann C.
      • Lezama J.I.
      • Mussini C.
      • Cattelan A.
      • Makofane K.
      • Tan D.
      • Nozza S.
      • Nemeth J.
      • Klein M.B.
      • Orkin C.M.
      Monkeypox virus infection in humans across 16 countries — April–June 2022.
      ) could rapidly spread monkeypox virus.
      Worldwide dissemination would particularly impact young children, pregnant women, and immunocompromised individuals who would be more prone to experience serious events such as encephalitis and secondary bacterial infections (
      • Thornhill J.P.
      • Barkati S.
      • Walmsley S.
      • Rockstroh J.
      • Antinori A.
      • Harrison L.B.
      • Palich R.
      • Nori A.
      • Reeves I.
      • Habibi M.S.
      • Apea V.
      • Boesecke C.
      • Vandekerckhove L.
      • Yakubovsky M.
      • Sendagorta E.
      • Blanco J.L.
      • Florence E.
      • Moschese D.
      • Maltez F.M.
      • Goorhuis A.
      • Pourcher V.
      • Migaud P.
      • Noe S.
      • Pintado C.
      • Maggi F.
      • Hansen A.-B.E.
      • Hoffmann C.
      • Lezama J.I.
      • Mussini C.
      • Cattelan A.
      • Makofane K.
      • Tan D.
      • Nozza S.
      • Nemeth J.
      • Klein M.B.
      • Orkin C.M.
      Monkeypox virus infection in humans across 16 countries — April–June 2022.
      ). Moreover, considering the impaired immune responses during autoimmunity, it is possible to speculate that Multiple Sclerosis (MS) patients (particularly under certain types of treatments) would also experience the worst outcomes during monkeypox infection.
      For instance, the recent experience with COVID-19 showed that MS patients with increased disability (as measured by EDSS) and using anti-CD20 therapies (rituximab and ocrelizumab) presented the worst outcomes including severe infection, hospitalization and mortality (
      • Barzegar M.
      • Mirmosayyeb O.
      • Nehzat N.
      • Sarrafi R.
      • Khorvash F.
      • Maghzi A.H.
      • Shaygannejad V.
      COVID-19 infection in a patient with multiple sclerosis treated with fingolimod.
      ;
      • Ponzano M.
      • Schiavetti I.
      • Bovis F.
      • Landi D.
      • Carmisciano L.
      • De Rossi N.
      • Cordioli C.
      • Moiola L.
      • Radaelli M.
      • Immovilli P.
      • Capobianco M.
      • Bragadin M.M.
      • Cocco E.
      • Scandellari C.
      • Cavalla P.
      • Pesci I.
      • Confalonieri P.
      • Perini P.
      • Bergamaschi R.
      • Inglese M.
      • Petracca M.
      • Trojano M.
      • Tedeschi G.
      • Comi G.
      • Battaglia M.A.
      • Patti F.
      • Fragoso Y.D.
      • Sen S.
      • Siva A.
      • Karabudak R.
      • Efendi H.
      • Furlan R.
      • Salvetti M.
      • Sormani M.P.
      A multiparametric score for assessing the individual risk of severe Covid-19 among patients with multiple sclerosis.
      ;
      • Salter A.
      • Fox R.J.
      • Newsome S.D.
      • Halper J.
      • Li D.K.B.
      • Kanellis P.
      • Costello K.
      • Bebo B.
      • Rammohan K.
      • Cutter G.R.
      • Cross A.H.
      Outcomes and risk factors associated with SARS-CoV-2 infection in a North American Registry of patients with multiple sclerosis.
      ;
      • Schiavetti I.
      • Ponzano M.
      • Signori A.
      • Bovis F.
      • Carmisciano L.
      • Sormani M.P.
      Severe outcomes of COVID-19 among patients with multiple sclerosis under anti-CD-20 therapies: a systematic review and meta-analysis.
      ).
      Regarding vaccination, MS patients presented different neutralizing antibody responses against SARS-CoV-2 (77%) vs. healthy controls (93%). MS patients during disease-modifying therapies (DMTs) exhibited: >93% positive antibody responses during glatiramer acetate, beta-interferons, dimethyl-fumarate, teriflunomide, alemtuzumab, and natalizumab; while those treated with fingolimod (27%) and anti-CD20 therapies (44%) showed lower positive antibody responses (
      • Etemadifar M.
      • Nouri H.
      • Pitzalis M.
      • Idda M.L.
      • Salari M.
      • Baratian M.
      • Mahdavi S.
      • Abhari A.P.
      • Sedaghat N.
      Multiple sclerosis disease-modifying therapies and COVID-19 vaccines: a practical review and meta-analysis.
      ;
      • Gombolay G.Y.
      • Dutt M.
      • Tyor W.
      Immune responses to SARS-CoV-2 vaccination in multiple sclerosis: a systematic review/meta-analysis.
      ).
      Lower effective cellular immune responses through CD4+ and CD8+ T lymphocytes after SARS-CoV-2 vaccination were also suggested for MS patients during interferon, fingolimod and cladribine treatments (
      • Etemadifar M.
      • Nouri H.
      • Pitzalis M.
      • Idda M.L.
      • Salari M.
      • Baratian M.
      • Mahdavi S.
      • Abhari A.P.
      • Sedaghat N.
      Multiple sclerosis disease-modifying therapies and COVID-19 vaccines: a practical review and meta-analysis.
      ;
      • Gombolay G.Y.
      • Dutt M.
      • Tyor W.
      Immune responses to SARS-CoV-2 vaccination in multiple sclerosis: a systematic review/meta-analysis.
      ;
      • Iannetta M.
      • Landi D.
      • Cola G.
      • Campogiani L.
      • Malagnino V.
      • Teti E.
      • Coppola L.
      • Di Lorenzo A.
      • Fraboni D.
      • Buccisano F.
      • Grelli S.
      • Mozzani M.
      • Zingaropoli M.A.
      • Ciardi M.R.
      • Nisini R.
      • Bernardini S.
      • Andreoni M.
      • Marfia G.A.
      • Sarmati L.
      B- and T-cell responses after SARS-CoV-2 vaccination in patients with multiple sclerosis receiving disease modifying therapies: immunological patterns and clinical implications.
      ;
      • Tortorella C.
      • Aiello A.
      • Gasperini C.
      • Agrati C.
      • Castilletti C.
      • Ruggieri S.
      • Meschi S.
      • Matusali G.
      • Colavita F.
      • Farroni C.
      • Cuzzi G.
      • Cimini E.
      • Tartaglia E.
      • Vanini V.
      • Prosperini L.
      • Haggiag S.
      • Galgani S.
      • Quartuccio M.E.
      • Salmi A.
      • Repele F.
      • Altera A.M.G.
      • Cristofanelli F.
      • D'abramo A.
      • Bevilacqua N.
      • Corpolongo A.
      • Puro V.
      • Vaia F.
      • Capobianchi M.R.
      • Ippolito G.
      • Nicastri E.
      • Goletti D.
      • Lapa D.
      • Francalancia M.
      • Bettini A.
      • Gramigna G.
      • Forbici F.
      • Gall'i P.
      • Marani A.
      • Possi A.
      • Capri A.
      • Santoro A.
      • Orchi N.
      • Butera O.
      • Fard S.N.
      • Petrone L.
      • Petruccioli E.
      Humoral- and T-Cell-specific immune responses to SARS-CoV-2 mRNA vaccination in patients with MS using different disease-modifying therapies.
      ).
      We can hypothesize that similar features of defective antiviral immune responses observed with COVID-19 may occur in the event of monkeypox infection in MS patients treated with DMTs (summarized in Fig. 1).
      Fig. 1
      Fig. 1Proposed impaired immunological responses during Monkeypox infection/vaccination in MS patients using DMTs. Defective humoral/cellular immune adaptive responses were described for SARS-CoV-2 natural infection/vaccination in MS patients during disease modifying therapies (DMTs). Similarly, these mechanisms may also be impacted during monkeypox natural infection/vaccination in MS patients using DMTs. Created with BioRender.com.
      The risk of suboptimal immune responses in MS patients raises our concerns regarding the need for careful management of the DMTs schedule, the introduction of antiviral therapies, vaccination, and the eventual risk for disease exacerbation on the occasion of widespread monkeypox infection.

      Author's contributions

      V.O.B., A.D. and C.L.Y. wrote the manuscript.

      Declaration of Competing Interest

      The author declares no conflicts of interest.

      Funding sources

      No funding was received.

      Acknowledgment

      None.

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