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Abstract

Background

In 2022, a global monkeypox virus (MPXV) clade II epidemic occurred mainly among men who have sex with men. Until early 1980s, European smallpox vaccination programmes were part of worldwide smallpox eradication efforts. Having received smallpox vaccine > 20 years ago may provide some cross-protection against MPXV.

Aim

To assess the effectiveness of historical smallpox vaccination against laboratory-confirmed mpox in 2022 in Europe.

Methods

European countries with sufficient data on case vaccination status and historical smallpox vaccination coverage were included. We selected mpox cases born in these countries during the height of the national smallpox vaccination campaigns (latest 1971), male, with date of onset before 1 August 2022. We estimated vaccine effectiveness (VE) and corresponding 95% CI for each country using logistic regression as per the Farrington screening method. We calculated a pooled estimate using a random effects model.

Results

In Denmark, France, the Netherlands and Spain, historical smallpox vaccination coverage was high (80–90%) until the end of the 1960s. VE estimates varied widely (40–80%, I2 = 82%), possibly reflecting different booster strategies. The pooled VE estimate was 70% (95% CI: 23–89%).

Conclusion

Our findings suggest residual cross-protection by historical smallpox vaccination against mpox caused by MPXV clade II in men with high uncertainty and heterogeneity. Individuals at high-risk of exposure should be offered mpox vaccination, following national recommendations, regardless of prior smallpox vaccine history, until further evidence becomes available. There is an urgent need to conduct similar studies in sub-Saharan countries currently affected by the MPXV clade I outbreak.

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2024-08-22
2024-11-21
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.34.2400139
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References

  1. Laurenson-Schafer H, Sklenovská N, Hoxha A, Kerr SM, Ndumbi P, Fitzner J, et al. Description of the first global outbreak of mpox: an analysis of global surveillance data. Lancet Glob Health. 2023;11(7):e1012-23.  https://doi.org/10.1016/S2214-109X(23)00198-5  PMID: 37349031 
  2. Gessain A, Nakoune E, Yazdanpanah Y. Monkeypox. N Engl J Med. 2022;387(19):1783-93.  https://doi.org/10.1056/NEJMra2208860  PMID: 36286263 
  3. Vaughan AM, Cenciarelli O, Colombe S, Alves de Sousa L, Fischer N, Gossner CM, et al. A large multi-country outbreak of monkeypox across 41 countries in the WHO European Region, 7 March to 23 August 2022. Euro Surveill. 2022;27(36):2200620.  https://doi.org/10.2807/1560-7917.ES.2022.27.36.2200620  PMID: 36082686 
  4. Fenner F, Henderson DA, Arita I, Jezek Z, Ladnyi ID. Smallpox and its eradication. Geneva: World Health Organization. 1988. [Accessed: 1 Dec 2023]. Available from: https://apps.who.int/iris/handle/10665/39485
  5. Rieckmann A, Villumsen M, Sørup S, Haugaard LK, Ravn H, Roth A, et al. Vaccinations against smallpox and tuberculosis are associated with better long-term survival: a Danish case-cohort study 1971-2010. Int J Epidemiol. 2017;46(2):695-705.  PMID: 27380797 
  6. Institut de Veille Sanitaire. Utilisation du virus de la variole comme arme biologique et estimation de l’impact épidémiologique et place de la vaccination [Use of smallpox virus as a biological threat and estimation of the epidemiological impact of vaccination]. St-Maurice: Santé Publique France, 2001. [Accessed: 1 Dec 2023]. French. Available from: https://www.santepubliquefrance.fr/determinants-de-sante/vaccination/documents/rapport-synthese/utilisation-du-virus-de-la-variole-comme-arme-biologique.-estimation-de-l-impact-epidemiologique-et-place-de-la-vaccination
  7. Dutch National Institute of Public Health and the Evironment (RIVM). Infectieziekten Bulletin [Infectious Diseases Bulletin]. Vol. 29, March 2003. Bilthoven: RIVM. [Accessed: 01 Dec 2023]. Dutch. Available from: https://www.rivm.nl/sites/default/files/2018-11/jaargang%2014%20nummer%203x.pdf
  8. Instituto de Salud Carlos III. Ministerio de Sanidad y consume. Análisis de la sanidad en españa a lo largo del siglo XX [Study on health in Spain during the 20th century]. Madrid: Institutode Salud Carlos III, 2002. [Accessed: 1 Dec 2023]. Spanish. Available from: https://vacunasaep.org/sites/vacunasaep.org/files/vacunacion-viruela-espana-segunda-mitad-siglo-xx.pdf
  9. Rimoin AW, Mulembakani PM, Johnston SC, Lloyd Smith JO, Kisalu NK, Kinkela TL, et al. Major increase in human monkeypox incidence 30 years after smallpox vaccination campaigns cease in the Democratic Republic of Congo. Proc Natl Acad Sci USA. 2010;107(37):16262-7.  https://doi.org/10.1073/pnas.1005769107  PMID: 20805472 
  10. Jezek Z, Marennikova SS, Mutumbo M, Nakano JH, Paluku KM, Szczeniowski M. Human monkeypox: a study of 2,510 contacts of 214 patients. J Infect Dis. 1986;154(4):551-5.  https://doi.org/10.1093/infdis/154.4.551  PMID: 3018091 
  11. Taube JC, Rest EC, Lloyd-Smith JO, Bansal S. The global landscape of smallpox vaccination history and implications for current and future orthopoxvirus susceptibility: a modelling study. Lancet Infect Dis. 2023;23(4):454-62.  https://doi.org/10.1016/S1473-3099(22)00664-8  PMID: 36455590 
  12. Luciani L, Lapidus N, Amroun A, Falchi A, Souksakhone C, Mayxay M, et al. Orthopoxvirus Seroprevalence and Infection Susceptibility in France, Bolivia, Laos, and Mali. Emerg Infect Dis. 2022;28(12):2463-71.  https://doi.org/10.3201/eid2812.221136  PMID: 36343384 
  13. Ježek Z, Grab B, Szczeniowski MV, Paluku KM, Mutombo M. Human monkeypox: secondary attack rates. Bull World Health Organ. 1988;66(4):465-70. PMID: 2844429 
  14. Fine PE, Jezek Z, Grab B, Dixon H. The transmission potential of monkeypox virus in human populations. Int J Epidemiol. 1988;17(3):643-50.  https://doi.org/10.1093/ije/17.3.643  PMID: 2850277 
  15. Karem KL, Reynolds M, Hughes C, Braden Z, Nigam P, Crotty S, et al. Monkeypox-induced immunity and failure of childhood smallpox vaccination to provide complete protection. Clin Vaccine Immunol. 2007;14(10):1318-27.  https://doi.org/10.1128/CVI.00148-07  PMID: 17715329 
  16. Hammarlund E, Lewis MW, Carter SV, Amanna I, Hansen SG, Strelow LI, et al. Multiple diagnostic techniques identify previously vaccinated individuals with protective immunity against monkeypox. Nat Med. 2005;11(9):1005-11.  https://doi.org/10.1038/nm1273  PMID: 16086024 
  17. European Medicines Agency (EMA). Product Information. Imvanex. EMA: Amsterdam; 2023. [Accessed: 1 Dec 2023]. Available from: https://www.ema.europa.eu/en/documents/product-information/imvanex-epar-product-information_en.pdf
  18. Dutch National Institute of Public Health and the Environment (RIVM). Pokken Richtlijn. [Factsheet smallpox]. Bilthoven: RIVM. [Accessed: 01 Dec 2023]. Dutch. Available from: https://lci.rivm.nl/richtlijnen/pokken
  19. Santé Publique France. Healthworker Information Vaccination. Mpox. St-Maurice: Santé Publique France. [Accessed: 12 Feb 2024]. French. Available from: https://professionnels.vaccination-info-service.fr/Maladies-et-leurs-vaccins/Variole-du-singe-mpox
  20. Statens Serum Institute (SSI). Vaccinations. Mpox. Copenhagen: SSI. [Accessed: 12 Feb 2024]. Danish. Available from: https://www.ssi.dk/vaccinationer/vaccineleksikon/k/koppe--og-mpox-vaccine-imvanex
  21. Spanish Ministry of Health. Vaccinions. Mpox Strategy for Vaccinatino. [Vaccinations. Mpox strategy for vaccinations.]. Madrid: Ministerio de Sanidad. [Accessed: 12 Feb 2024]. Spanish. Available from: https://www.sanidad.gob.es/areas/promocionPrevencion/vacunaciones/MonkeyPox/docs/Estrategia_vacunacion_Monkeypox_07122022.pdf
  22. European Centre for Disease Prevention and Control (ECDC). Monkeypox multi-country outbreak, first update – 8 July 2022. ECDC: Stockholm; 2022. Available from: https://www.ecdc.europa.eu/sites/default/files/documents/Monkeypox-multi-country-outbreak-first-update-8-July-FINAL3.pdf
  23. Dalton AF, Diallo AO, Chard AN, Moulia DL, Deputy NP, Fothergill A, et al. Estimated Effectiveness of JYNNEOS Vaccine in Preventing Mpox: A Multijurisdictional Case-Control Study - United States, August 19, 2022-March 31, 2023. MMWR Morb Mortal Wkly Rep. 2023;72(20):553-8.  https://doi.org/10.15585/mmwr.mm7220a3  PMID: 37200229 
  24. Deputy NP, Deckert J, Chard AN, Sandberg N, Moulia DL, Barkley E, et al. Vaccine Effectiveness of JYNNEOS against Mpox Disease in the United States. N Engl J Med. 2023;388(26):2434-43.  https://doi.org/10.1056/NEJMoa2215201  PMID: 37199451 
  25. Wolff Sagy Y, Zucker R, Hammerman A, Markovits H, Arieh NG, Abu Ahmad W, et al. Real-world effectiveness of a single dose of mpox vaccine in males. Nat Med. 2023;29(3):748-52.  https://doi.org/10.1038/s41591-023-02229-3  PMID: 36720271 
  26. Rosenberg ES, Dorabawila V, Hart-Malloy R, Anderson BJ, Miranda W, O’Donnell T, et al. Effectiveness of JYNNEOS Vaccine Against Diagnosed Mpox Infection - New York, 2022. MMWR Morb Mortal Wkly Rep. 2023;72(20):559-63.  https://doi.org/10.15585/mmwr.mm7220a4  PMID: 37339074 
  27. Bertran M, Andrews N, Davison C, Dugbazah B, Boateng J, Lunt R, et al. Effectiveness of one dose of MVA-BN smallpox vaccine against mpox in England using the case-coverage method: an observational study. Lancet Infect Dis. 2023;23(7):828-35.  https://doi.org/10.1016/S1473-3099(23)00057-9  PMID: 36924787 
  28. Fontán-Vela M, Hernando V, Olmedo C, Coma E, Martinez M, Moreno-Perez D, et al. Effectiveness of MVA-BN vaccination in a population at high-risk of mpox: a Spanish cohort study. Clin Infect Dis. 2023;ciad645.; Epub ahead of print.  PMID: 37864849 
  29. van Ewijk CE, Miura F, van Rijckevorsel G, de Vries HJ, Welkers MR, van den Berg OE, et al. Mpox outbreak in the Netherlands, 2022: public health response, characteristics of the first 1,000 cases and protection of the first-generation smallpox vaccine. Euro Surveill. 2023;28(12):2200772.  https://doi.org/10.2807/1560-7917.ES.2023.28.12.2200772  PMID: 36951783 
  30. Tarín-Vicente EJ, Alemany A, Agud-Dios M, Ubals M, Suñer C, Antón A, et al. Clinical presentation and virological assessment of confirmed human monkeypox virus cases in Spain: a prospective observational cohort study. Lancet. 2022;400(10353):661-9.  https://doi.org/10.1016/S0140-6736(22)01436-2  PMID: 35952705 
  31. Krug C, Chazelle E, Tarantola A, Noël H, Spaccaferri G, Parent du Châtelet I, et al. History of smallpox vaccination and marked clinical expression of mpox among cases notified in France from May to July 2022. Clin Microbiol Infect. 2024;30(8):1061-6.  https://doi.org/10.1016/j.cmi.2024.03.038  PMID: 38588877 
  32. Farrington CP. Estimation of vaccine effectiveness using the screening method. Int J Epidemiol. 1993;22(4):742-6.  https://doi.org/10.1093/ije/22.4.742  PMID: 8225751 
  33. Sørup S, Villumsen M, Ravn H, Benn CS, Sørensen TIA, Aaby P, et al. Smallpox vaccination and all-cause infectious disease hospitalization: a Danish register-based cohort study. Int J Epidemiol. 2011;40(4):955-63.  https://doi.org/10.1093/ije/dyr063  PMID: 21543446 
  34. Paule RC, Mandel J. Consensus values and weighting factors. J Res Natl Bur Stand. 1982;87(5):377-85.  https://doi.org/10.6028/jres.087.022  PMID: 34566088 
  35. R Core Team. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; 2020. Available from: http://www.Rproject.org/
  36. Akter F, Hasan TB, Alam F, Das A, Afrin S, Maisha S, et al. Effect of prior immunisation with smallpox vaccine for protection against human Mpox: A systematic review. Rev Med Virol. 2023;33(4):e2444.  https://doi.org/10.1002/rmv.2444  PMID: 36999223 
  37. Titanji BK, Eick-Cost A, Partan ES, Epstein L, Wells N, Stahlman SL, et al. Effectiveness of Smallpox Vaccination to Prevent Mpox in Military Personnel. N Engl J Med. 2023;389(12):1147-8.  https://doi.org/10.1056/NEJMc2300805  PMID: 37733313 
  38. Taub DD, Ershler WB, Janowski M, Artz A, Key ML, McKelvey J, et al. Immunity from smallpox vaccine persists for decades: a longitudinal study. Am J Med. 2008;121(12):1058-64.  https://doi.org/10.1016/j.amjmed.2008.08.019  PMID: 19028201 
  39. Kunasekaran MP, Chen X, Costantino V, Chughtai AA, MacIntyre CR. Evidence for Residual Immunity to Smallpox After Vaccination and Implications for Re-emergence. Mil Med. 2019;184(11-12):e668-79.  https://doi.org/10.1093/milmed/usz181  PMID: 31369103 
  40. Gallwitz S, Schutzbank T, Heberling RL, Kalter SS, Galpin JE. Smallpox: residual antibody after vaccination. J Clin Microbiol. 2003;41(9):4068-70.  https://doi.org/10.1128/JCM.41.9.4068-4070.2003  PMID: 12958227 
  41. Hammarlund E, Lewis MW, Hansen SG, Strelow LI, Nelson JA, Sexton GJ, et al. Duration of antiviral immunity after smallpox vaccination. Nat Med. 2003;9(9):1131-7.  https://doi.org/10.1038/nm917  PMID: 12925846 
  42. Edghill-Smith Y, Golding H, Manischewitz J, King LR, Scott D, Bray M, et al. Smallpox vaccine-induced antibodies are necessary and sufficient for protection against monkeypox virus. Nat Med. 2005;11(7):740-7.  https://doi.org/10.1038/nm1261  PMID: 15951823 
  43. Metzger W, Mordmueller BG. Vaccines for preventing smallpox. Cochrane Database Syst Rev. 2007;2007(3):CD004913.  PMID: 17636779 
  44. Arita I. Duration of immunity after smallpox vaccination: a study on vaccination policy against smallpox bioterrorism in Japan. Jpn J Infect Dis. 2002;55(4):112-6. PMID: 12403907 
  45. Pütz MM, Alberini I, Midgley CM, Manini I, Montomoli E, Smith GL. Prevalence of antibodies to Vaccinia virus after smallpox vaccination in Italy. J Gen Virol. 2005;86(Pt 11):2955-60.  https://doi.org/10.1099/vir.0.81265-0  PMID: 16227216 
  46. Vallgårda S. Folkesundhed som politik: Danmark og Sverige fra 1930 til i dag. [Public health as policy: Denmark and Sweden from 1930 to the present day]. Aarhus Universitetsforlag, 2003. Danish. Available from: https://unipress.dk/udgivelser/f/folkesundhed-som-politik/
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