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Abstract

Background

Following the 2022–2023 mpox outbreak, crucial knowledge gaps exist regarding orthopoxvirus-specific immunity in risk groups and its impact on future outbreaks.

Aim

We combined cross-sectional seroprevalence studies in two cities in the Netherlands with mathematical modelling to evaluate scenarios of future mpox outbreaks among men who have sex with men (MSM).

Methods

Serum samples were obtained from 1,065 MSM attending Centres for Sexual Health (CSH) in Rotterdam or Amsterdam following the peak of the Dutch mpox outbreak and the introduction of vaccination. For MSM visiting the Rotterdam CSH, sera were linked to epidemiological and vaccination data. An in-house developed ELISA was used to detect vaccinia virus (VACV)-specific IgG. These observations were combined with published data on serial interval and vaccine effectiveness to inform a stochastic transmission model that estimates the risk of future mpox outbreaks.

Results

The seroprevalence of VACV-specific antibodies was 45.4% and 47.1% in Rotterdam and Amsterdam, respectively. Transmission modelling showed that the impact of risk group vaccination on the original outbreak was likely small. However, assuming different scenarios, the number of mpox cases in a future outbreak would be markedly reduced because of vaccination. Simultaneously, the current level of immunity alone may not prevent future outbreaks. Maintaining a short time-to-diagnosis is a key component of any strategy to prevent new outbreaks.

Conclusion

Our findings indicate a reduced likelihood of large future mpox outbreaks among MSM in the Netherlands under current conditions, but emphasise the importance of maintaining population immunity, diagnostic capacities and disease awareness.

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/content/10.2807/1560-7917.ES.2024.29.17.2300532
2024-04-25
2024-12-22
/content/10.2807/1560-7917.ES.2024.29.17.2300532
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References

  1. 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 
  2. World Health Organization (WHO). Multi-country outbreak of mpox: external Situation Report #25 – 24 June 2023.Geneva: WHO; 2023. Available from: https://www.who.int/publications/m/item/multi-country-outbreak-of-mpox--external-situation-report--25---24-june-2023
  3. 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 
  4. 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 
  5. 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 
  6. Leendertz SAJ, Stern D, Theophil D, Anoh E, Mossoun A, Schubert G, et al. A Cross-Sectional Serosurvey of Anti-Orthopoxvirus Antibodies in Central and Western Africa. Viruses. 2017;9(10):278.  https://doi.org/10.3390/v9100278  PMID: 28961172 
  7. 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 
  8. 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 
  9. 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 
  10. Hazra A, Zucker J, Bell E, Flores J, Gordon L, Mitjà O, et al. Mpox in people with past infection or a complete vaccination course: a global case series. Lancet Infect Dis. 2024;24(1):57-64.  https://doi.org/10.1016/S1473-3099(23)00492-9  PMID: 37678309 
  11. Zaeck LM, Lamers MM, Verstrepen BE, Bestebroer TM, van Royen ME, Götz H, et al. Low levels of monkeypox virus-neutralizing antibodies after MVA-BN vaccination in healthy individuals. Nat Med. 2023;29(1):270-8.  https://doi.org/10.1038/s41591-022-02090-w  PMID: 36257333 
  12. Gilchuk I, Gilchuk P, Sapparapu G, Lampley R, Singh V, Kose N, et al. Cross-Neutralizing and Protective Human Antibody Specificities to Poxvirus Infections. Cell. 2016;167(3):684-694.e9.  https://doi.org/10.1016/j.cell.2016.09.049  PMID: 27768891 
  13. Criscuolo E, Giuliani B, Ferrarese R, Ferrari D, Locatelli M, Clementi M, et al. Smallpox vaccination-elicited antibodies cross-neutralize 2022-Monkeypox virus Clade II. J Med Virol. 2023;95(3):e28643.  https://doi.org/10.1002/jmv.28643  PMID: 36890648 
  14. Hubert M, Guivel-Benhassine F, Bruel T, Porrot F, Planas D, Vanhomwegen J, et al. Complement-dependent mpox-virus-neutralizing antibodies in infected and vaccinated individuals. Cell Host Microbe. 2023;31(6):937-948.e4.  https://doi.org/10.1016/j.chom.2023.05.001  PMID: 37196656 
  15. 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 
  16. Xu M, Liu C, Du Z, Bai Y, Wang Z, Gao C. Real-world effectiveness of monkeypox vaccines: a systematic review. J Travel Med. 2023;30(5):taad048.  https://doi.org/10.1093/jtm/taad048  PMID: 37040341 
  17. Jezek 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 
  18. Raccagni AR, Candela C, Mileto D, Bruzzesi E, Canetti D, Bertoni C, et al. Breakthrough monkeypox infection among individuals previously immunized with smallpox or monkeypox vaccination. J Infect. 2023;86(2):154-225.  https://doi.org/10.1016/j.jinf.2022.12.001  PMID: 36481365 
  19. Jamard S, Handala L, Faussat C, Vincent N, Stefic K, Gaudy-Graffin C, et al. Resurgence of symptomatic Mpox among vaccinated patients: First clues from a new-onset local cluster. Infect Dis Now. 2023;53(4):104714.  https://doi.org/10.1016/j.idnow.2023.104714  PMID: 37120092 
  20. Raccagni AR, Canetti D, Mileto D, Tamburini AM, Candela C, Albarello L, et al. Two individuals with potential monkeypox virus reinfection. Lancet Infect Dis. 2023;23(5):522-4.  https://doi.org/10.1016/S1473-3099(23)00185-8  PMID: 37031694 
  21. Golden J, Harryman L, Crofts M, Muir P, Donati M, Gillett S, et al. Case of apparent mpox reinfection. Sex Transm Infect. 2023;99(4):283-4.  https://doi.org/10.1136/sextrans-2022-055736  PMID: 36707246 
  22. Musumeci S, Najjar I, Amari EBE, Schibler M, Jacquerioz F, Yerly S, et al. A Case of Mpox Reinfection. Clin Infect Dis. 2023;77(1):135-7.  https://doi.org/10.1093/cid/ciad147  PMID: 36905148 
  23. Reed KD, Melski JW, Graham MB, Regnery RL, Sotir MJ, Wegner MV, et al. The detection of monkeypox in humans in the Western Hemisphere. N Engl J Med. 2004;350(4):342-50.  https://doi.org/10.1056/NEJMoa032299  PMID: 14736926 
  24. Mauldin MR, McCollum AM, Nakazawa YJ, Mandra A, Whitehouse ER, Davidson W, et al. Exportation of Monkeypox Virus From the African Continent. J Infect Dis. 2022;225(8):1367-76.  https://doi.org/10.1093/infdis/jiaa559  PMID: 32880628 
  25. Thornhill JP, Barkati S, Walmsley S, Rockstroh J, Antinori A, Harrison LB, et al. Monkeypox Virus Infection in Humans across 16 Countries - April-June 2022. N Engl J Med. 2022;387(8):679-91.  https://doi.org/10.1056/NEJMoa2207323  PMID: 35866746 
  26. Endo A, Murayama H, Abbott S, Ratnayake R, Pearson CAB, Edmunds WJ, et al. Heavy-tailed sexual contact networks and monkeypox epidemiology in the global outbreak, 2022. Science. 2022;378(6615):90-4.  https://doi.org/10.1126/science.add4507  PMID: 36137054 
  27. Wang H, de Paulo KJID, Gültzow T, Zimmermann HML, Jonas KJ. Brief report: Determinants of potential sexual activity reduction in the face of the Monkeypox epidemic. Int J Behav Med. 2024.  https://doi.org/10.1007/s12529-023-10252-4  PMID: 38233626 
  28. Pollock EDC, Clay PA, Keen A, Currie DW, Carter RJ, Quilter LAS, et al. Potential for Recurrent Mpox Outbreaks Among Gay, Bisexual, and Other Men Who Have Sex with Men - United States, 2023. MMWR Morb Mortal Wkly Rep. 2023;72(21):568-73.  https://doi.org/10.15585/mmwr.mm7221a1  PMID: 37227964 
  29. Van Dijck C, Hens N, Kenyon C, Tsoumanis A. The Roles of Unrecognized Mpox Cases, Contact Isolation and Vaccination in Determining Epidemic Size in Belgium: A Modeling Study. Clin Infect Dis. 2023;76(3):e1421-3.  https://doi.org/10.1093/cid/ciac723  PMID: 36052546 
  30. Ward T, Christie R, Paton RS, Cumming F, Overton CE. Transmission dynamics of monkeypox in the United Kingdom: contact tracing study. BMJ. 2022;379:e073153.  https://doi.org/10.1136/bmj-2022-073153  PMID: 36323407 
  31. Di Giulio DB, Eckburg PB. Human monkeypox: an emerging zoonosis. Lancet Infect Dis. 2004;4(1):15-25.  https://doi.org/10.1016/S1473-3099(03)00856-9  PMID: 14720564 
  32. Panovska-Griffiths J, Watkins NA, Cumming F, Hounsome L, Charlett A, Zhang XS, et al. Responsive modelling of the mpox epidemic in England as a cross-government and academia collaboration: the process, challenges, and lessons learned. Lancet Microbe. 2023;4(9):e658-60.  https://doi.org/10.1016/S2666-5247(23)00151-9  PMID: 37290464 
  33. Panovska-Griffiths J, Hinch R, Park J, Ward T, Charlett A, Cumming F, et al. Slowly declining growth rates and dynamic reporting delays characterise the Monkeypox epidemic in the UK over May-August 2022. PREPRINT (Version 1) available at Research Square 2022. Available from: https://www.researchsquare.com/article/rs-2298855/v1
  34. Statistics Netherlands (CBS). Birth; key figures, 1950-2022. The Hague: CBS. [Accessed: 1 Nov 2023]. Available from: https://www.cbs.nl/en-gb/figures/detail/37422ENG
  35. National Institute for Public Health and the Environment (RIVM). Mpox infections. Bilthoven: RIVM. [Accessed: 1 Nov 2023]. Available from: https://www.rivm.nl/en/mpox
  36. Xiridou M, Miura F, Adam P, Op de Coul E, de Wit J, Wallinga J. The fading of the mpox outbreak among men who have sex with men: a mathematical modelling study. J Infect Dis. 2023;jiad414. PMID: 37740556 
  37. Brand SPC, Cavallaro M, Cumming F, Turner C, Florence I, Blomquist P, et al. The role of vaccination and public awareness in forecasts of Mpox incidence in the United Kingdom. Nat Commun. 2023;14(1):4100.  https://doi.org/10.1038/s41467-023-38816-8  PMID: 37433797 
  38. Clay PA, Asher JM, Carnes N, Copen CE, Delaney KP, Payne DC, et al. Modelling the impact of vaccination and sexual behaviour adaptations on mpox cases in the USA during the 2022 outbreak. Sex Transm Infect. 2024;100(2):70-6.  https://doi.org/10.1136/sextrans-2023-055922  PMID: 38050171 
  39. Guzzetta G, Marziano V, Mammone A, Siddu A, Ferraro F, Caraglia A, et al. The decline of the 2022 Italian mpox epidemic: Role of behavior changes and control strategies. Nat Commun. 2024;15(1):2283.  https://doi.org/10.1038/s41467-024-46590-4  PMID: 38480715 
  40. Lin YC, Wen TH, Shih WL, Vermund SH, Fang CT. Impact of vaccination and high-risk group awareness on the mpox epidemic in the United States, 2022-2023: a modelling study. EClinicalMedicine. 2024;68:102407.  https://doi.org/10.1016/j.eclinm.2023.102407  PMID: 38235420 
  41. Chow EPF, Samra RS, Bradshaw CS, Chen MY, Williamson DA, Towns JM, et al. Mpox knowledge, vaccination and intention to reduce sexual risk practices among men who have sex with men and transgender people in response to the 2022 mpox outbreak: a cross-sectional study in Victoria, Australia. Sex Health. 2023;20(5):390-402.  https://doi.org/10.1071/SH23075  PMID: 37423606 
  42. Wang H, d’Abreu de Paulo KJI, Gültzow T, Zimmermann HML, Jonas KJ. Monkeypox self-diagnosis abilities, determinants of vaccination and self-isolation intention after diagnosis among MSM, the Netherlands, July 2022. Euro Surveill. 2022;27(33):2200603.  https://doi.org/10.2807/1560-7917.ES.2022.27.33.2200603  PMID: 35983772 
  43. Kottkamp AC, Samanovic MI, Duerr R, Oom AL, Belli HM, Zucker JR, et al. Antibody Titers against Mpox Virus after Vaccination. N Engl J Med. 2023;389(24):2299-301.  https://doi.org/10.1056/NEJMc2306239  PMID: 38091537 
  44. Oom AL, Kottkamp AC, Wilson KK, Yonatan M, Rettig S, Youn HA, et al. The Durability and Avidity of MPXV-specific Antibodies Induced by the Two-dose MVA-BN Mpox Vaccine. medRxiv. 2024;2024.01.28.24301893.
  45. Alexander ME, Moghadas SM, Rohani P, Summers AR. Modelling the effect of a booster vaccination on disease epidemiology. J Math Biol. 2006;52(3):290-306.  https://doi.org/10.1007/s00285-005-0356-0  PMID: 16283412 
  46. McCollum AM, Damon IK. Human monkeypox. Clin Infect Dis. 2014;58(2):260-7.  https://doi.org/10.1093/cid/cit703  PMID: 24158414 
  47. Likos AM, Sammons SA, Olson VA, Frace AM, Li Y, Olsen-Rasmussen M, et al. A tale of two clades: monkeypox viruses. J Gen Virol. 2005;86(Pt 10):2661-72.  https://doi.org/10.1099/vir.0.81215-0  PMID: 16186219 
  48. Kibungu EM, Vakaniaki EH, Kinganda-Lusamaki E, Kalonji-Mukendi T, Pukuta E, Hoff NA, et al. , International Mpox Research Consortium. Clade I-Associated Mpox Cases Associated with Sexual Contact, the Democratic Republic of the Congo. Emerg Infect Dis. 2024;30(1):172-6.  https://doi.org/10.3201/eid3001.231164  PMID: 38019211 
  49. World Health Organization (WHO). Disease Outbreak News; Mpox (monkeypox) in the Democratic Republic of the Congo. Geneva: WHO; 2023. Available from: https://www.who.int/emergencies/disease-outbreak-news/item/2023-DON493
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