Skip to main content
Top
Published in: Globalization and Health 1/2023

Open Access 01-12-2023 | Mpox Virus | Research

Mapping global zoonotic niche and interregional transmission risk of monkeypox: a retrospective observational study

Authors: Yan-Qun Sun, Jin-Jin Chen, Mei-Chen Liu, Yuan-Yuan Zhang, Tao Wang, Tian-Le Che, Ting-Ting Li, Yan-Ning Liu, Ai-Ying Teng, Bing-Zheng Wu, Xue-Geng Hong, Qiang Xu, Chen-Long Lv, Bao-Gui Jiang, Wei Liu, Li-Qun Fang

Published in: Globalization and Health | Issue 1/2023

Login to get access

Abstract

Background

Outbreaks of monkeypox have been ongoing in non-endemic countries since May 2022. A thorough assessment of its global zoonotic niche and potential transmission risk is lacking.

Methods

We established an integrated database on global monkeypox virus (MPXV) occurrence during 1958 − 2022. Phylogenetic analysis was performed to examine the evolution of MPXV and effective reproductive number (Rt) was estimated over time to examine the dynamic of MPXV transmissibility. The potential ecological drivers of zoonotic transmission and inter-regional transmission risks of MPXV were examined.

Results

As of 24 July 2022, a total of 49 432 human patients with MPXV infections have been reported in 78 countries. Based on 525 whole genome sequences, two main clades of MPXV were formed, of which Congo Basin clade has a higher transmissibility than West African clade before the 2022-monkeypox, estimated by the overall Rt (0.81 vs. 0.56), and the latter significantly increased in the recent decade. Rt of 2022-monkeypox varied from 1.14 to 4.24 among the 15 continuously epidemic countries outside Africa, with the top three as Peru (4.24, 95% CI: 2.89–6.71), Brazil (3.45, 95% CI: 1.62–7.00) and the United States (2.44, 95% CI: 1.62–3.60). The zoonotic niche of MPXV was associated with the distributions of Graphiurus lorraineus and Graphiurus crassicaudatus, the richness of Rodentia, and four ecoclimatic indicators. Besides endemic areas in Africa, more areas of South America, the Caribbean States, and Southeast and South Asia are ecologically suitable for the occurrence of MPXV once the virus has invaded. Most of Western Europe has a high-imported risk of monkeypox from Western Africa, whereas France and the United Kingdom have a potential imported risk of Congo Basin clade MPXV from Central Africa. Eleven of the top 15 countries with a high risk of MPXV importation from the main countries of 2022-monkeypox outbreaks are located at Europe with the highest risk in Italy, Ireland and Poland.

Conclusions

The suitable ecological niche for MPXV is not limited to Africa, and the transmissibility of MPXV was significantly increased during the 2022-monkeypox outbreaks. The imported risk is higher in Europe, both from endemic areas and currently epidemic countries. Future surveillance and targeted intervention programs are needed in its high-risk areas informed by updated prediction.
Appendix
Available only for authorised users
Literature
1.
go back to reference Otu A, Ebenso B, Walley J, Barceló J, Ochu C. Global monkeypox outbreak: atypical presentation demanding urgent public health action. Lancet Microbe. 2022;3(8):00153–7. Otu A, Ebenso B, Walley J, Barceló J, Ochu C. Global monkeypox outbreak: atypical presentation demanding urgent public health action. Lancet Microbe. 2022;3(8):00153–7.
4.
go back to reference Adalja A, Inglesby T. A novel international monkeypox outbreak. Ann Intern Med. 2022;175(8):1175–6.PubMed Adalja A, Inglesby T. A novel international monkeypox outbreak. Ann Intern Med. 2022;175(8):1175–6.PubMed
5.
go back to reference León-Figueroa DA, Bonilla-Aldana DK, Pachar M, Romaní L, Saldaña-Cumpa HM, Anchay-Zuloeta C, et al. The never-ending global emergence of viral zoonoses after COVID-19? The rising concern of monkeypox in Europe, North America and beyond. Travel Med Infect Dis. 2022;49:102362.PubMedPubMedCentral León-Figueroa DA, Bonilla-Aldana DK, Pachar M, Romaní L, Saldaña-Cumpa HM, Anchay-Zuloeta C, et al. The never-ending global emergence of viral zoonoses after COVID-19? The rising concern of monkeypox in Europe, North America and beyond. Travel Med Infect Dis. 2022;49:102362.PubMedPubMedCentral
6.
go back to reference Wenham C, Eccleston-Turner M. Monkeypox as a PHEIC: implications for global health governance. Lancet. 2022;400(10369):2169–71.PubMedPubMedCentral Wenham C, Eccleston-Turner M. Monkeypox as a PHEIC: implications for global health governance. Lancet. 2022;400(10369):2169–71.PubMedPubMedCentral
7.
go back to reference Yinka-Ogunleye A, Aruna O, Dalhat M, Ogoina D, McCollum A, Disu Y, et al. Outbreak of human monkeypox in Nigeria in 2017–18: a clinical and epidemiological report. Lancet Infect Dis. 2019;19(8):872–9.PubMedPubMedCentral Yinka-Ogunleye A, Aruna O, Dalhat M, Ogoina D, McCollum A, Disu Y, et al. Outbreak of human monkeypox in Nigeria in 2017–18: a clinical and epidemiological report. Lancet Infect Dis. 2019;19(8):872–9.PubMedPubMedCentral
8.
go back to reference Prier JE, Sauer RM. A pox disease of monkeys. Ann N Y Acad Sci. 1960;85:951–9.PubMed Prier JE, Sauer RM. A pox disease of monkeys. Ann N Y Acad Sci. 1960;85:951–9.PubMed
10.
go back to reference Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 2019;20(4):1160–6.PubMed Katoh K, Rozewicki J, Yamada KD. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform. 2019;20(4):1160–6.PubMed
11.
go back to reference Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics. 2019;35(21):4453–5.PubMedPubMedCentral Kozlov AM, Darriba D, Flouri T, Morel B, Stamatakis A. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics. 2019;35(21):4453–5.PubMedPubMedCentral
12.
go back to reference Cauchemez S, Epperson S, Biggerstaff M, Swerdlow D, Finelli L, Ferguson NM. Using routine surveillance data to estimate the epidemic potential of emerging zoonoses: application to the emergence of US swine origin influenza A H3N2v virus. PLoS Med. 2013;10(3):e1001399.PubMedPubMedCentral Cauchemez S, Epperson S, Biggerstaff M, Swerdlow D, Finelli L, Ferguson NM. Using routine surveillance data to estimate the epidemic potential of emerging zoonoses: application to the emergence of US swine origin influenza A H3N2v virus. PLoS Med. 2013;10(3):e1001399.PubMedPubMedCentral
13.
go back to reference 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.PubMed 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.PubMed
14.
go back to reference Vivancos R, Anderson C, Blomquist P, Balasegaram S, Bell A, Bishop L, et al. Community transmission of monkeypox in the United Kingdom, April to May 2022. Euro Surveill. 2022;27(22):2200422.PubMedPubMedCentral Vivancos R, Anderson C, Blomquist P, Balasegaram S, Bell A, Bishop L, et al. Community transmission of monkeypox in the United Kingdom, April to May 2022. Euro Surveill. 2022;27(22):2200422.PubMedPubMedCentral
15.
go back to reference Nolen LD, Osadebe L, Katomba J, Likofata J, Mukadi D, Monroe B, et al. Extended human-to-human transmission during a monkeypox outbreak in the Democratic Republic of the Congo. Emerg Infect Dis. 2016;22(6):1014–21.PubMedPubMedCentral Nolen LD, Osadebe L, Katomba J, Likofata J, Mukadi D, Monroe B, et al. Extended human-to-human transmission during a monkeypox outbreak in the Democratic Republic of the Congo. Emerg Infect Dis. 2016;22(6):1014–21.PubMedPubMedCentral
16.
go back to reference Cori A, Ferguson NM, Fraser C, Cauchemez S. A new framework and software to estimate time-varying reproduction numbers during epidemics. Am J Epidemiol. 2013;178(9):1505–12.PubMed Cori A, Ferguson NM, Fraser C, Cauchemez S. A new framework and software to estimate time-varying reproduction numbers during epidemics. Am J Epidemiol. 2013;178(9):1505–12.PubMed
17.
go back to reference Fuller T, Thomassen HA, Mulembakani PM, Johnston SC, Lloyd-Smith JO, Kisalu NK, et al. Using remote sensing to map the risk of human monkeypox virus in the Congo Basin. EcoHealth. 2011;8(1):14–25.PubMed Fuller T, Thomassen HA, Mulembakani PM, Johnston SC, Lloyd-Smith JO, Kisalu NK, et al. Using remote sensing to map the risk of human monkeypox virus in the Congo Basin. EcoHealth. 2011;8(1):14–25.PubMed
18.
go back to reference Falendysz EA, Lopera JG, Doty JB, Nakazawa Y, Crill C, Lorenzsonn F, et al. Characterization of monkeypox virus infection in African rope squirrels (Funisciurus sp.). PLoS Negl Trop Dis. 2017;11(8):e0005809.PubMedPubMedCentral Falendysz EA, Lopera JG, Doty JB, Nakazawa Y, Crill C, Lorenzsonn F, et al. Characterization of monkeypox virus infection in African rope squirrels (Funisciurus sp.). PLoS Negl Trop Dis. 2017;11(8):e0005809.PubMedPubMedCentral
19.
go back to reference Guarner J, Johnson BJ, Paddock CD, Shieh WJ, Goldsmith CS, Reynolds MG, et al. Monkeypox transmission and pathogenesis in prairie dogs. Emerg Infect Dis. 2004;10(3):426–31.PubMedPubMedCentral Guarner J, Johnson BJ, Paddock CD, Shieh WJ, Goldsmith CS, Reynolds MG, et al. Monkeypox transmission and pathogenesis in prairie dogs. Emerg Infect Dis. 2004;10(3):426–31.PubMedPubMedCentral
20.
go back to reference Doty JB, Malekani JM, Kalemba LN, Stanley WT, Monroe BP, Nakazawa YU, et al. Assessing monkeypox virus prevalence in small mammals at the human-animal interface in the Democratic Republic of the Congo. Viruses. 2017;9(10):283.PubMedPubMedCentral Doty JB, Malekani JM, Kalemba LN, Stanley WT, Monroe BP, Nakazawa YU, et al. Assessing monkeypox virus prevalence in small mammals at the human-animal interface in the Democratic Republic of the Congo. Viruses. 2017;9(10):283.PubMedPubMedCentral
21.
go back to reference Falendysz EA, Lopera JG, Lorenzsonn F, Salzer JS, Hutson CL, Doty J, et al. Further assessment of monkeypox virus infection in gambian pouched rats (Cricetomys gambianus) using in vivo bioluminescent Imaging. PloS Negl Trop Dis. 2015;9(10):e0004130.PubMedPubMedCentral Falendysz EA, Lopera JG, Lorenzsonn F, Salzer JS, Hutson CL, Doty J, et al. Further assessment of monkeypox virus infection in gambian pouched rats (Cricetomys gambianus) using in vivo bioluminescent Imaging. PloS Negl Trop Dis. 2015;9(10):e0004130.PubMedPubMedCentral
22.
go back to reference Miao D, Dai K, Zhao GP, Li XL, Shi WQ, Zhang JS, et al. Mapping the global potential transmission hotspots for severe fever with thrombocytopenia syndrome by machine learning methods. Emerg Microbes Infect. 2020;9(1):817–26.PubMedPubMedCentral Miao D, Dai K, Zhao GP, Li XL, Shi WQ, Zhang JS, et al. Mapping the global potential transmission hotspots for severe fever with thrombocytopenia syndrome by machine learning methods. Emerg Microbes Infect. 2020;9(1):817–26.PubMedPubMedCentral
23.
go back to reference Zhao GP, Wang YX, Fan ZW, Ji Y, Liu MJ, Zhang WH, et al. Mapping ticks and tick-borne pathogens in China. Nat Commun. 2021;12(1):1075.PubMedPubMedCentral Zhao GP, Wang YX, Fan ZW, Ji Y, Liu MJ, Zhang WH, et al. Mapping ticks and tick-borne pathogens in China. Nat Commun. 2021;12(1):1075.PubMedPubMedCentral
24.
go back to reference Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez J-C, et al. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics. 2011;12(1):1–8. Robin X, Turck N, Hainard A, Tiberti N, Lisacek F, Sanchez J-C, et al. pROC: an open-source package for R and S+ to analyze and compare ROC curves. BMC Bioinformatics. 2011;12(1):1–8.
25.
go back to reference Sing T, Sander O, Beerenwinkel N, Lengauer T. ROCR: visualizing classifier performance in R. Bioinformatics. 2005;21:3940–1.PubMed Sing T, Sander O, Beerenwinkel N, Lengauer T. ROCR: visualizing classifier performance in R. Bioinformatics. 2005;21:3940–1.PubMed
27.
go back to reference Baker RE, Mahmud AS, Miller IF, Rajeev M, Rasambainarivo F, Rice BL, et al. Infectious disease in an era of global change. Nat Rev Microbiol. 2022;20(4):193–205.PubMed Baker RE, Mahmud AS, Miller IF, Rajeev M, Rasambainarivo F, Rice BL, et al. Infectious disease in an era of global change. Nat Rev Microbiol. 2022;20(4):193–205.PubMed
28.
go back to reference Fischer C, Gerstmeier R, Wagner TC. Seasonal and temporal patterns of rainfall shape arthropod community composition and multi-trophic interactions in an arid environment. Sci Rep. 2022;12(1):3742.PubMedPubMedCentral Fischer C, Gerstmeier R, Wagner TC. Seasonal and temporal patterns of rainfall shape arthropod community composition and multi-trophic interactions in an arid environment. Sci Rep. 2022;12(1):3742.PubMedPubMedCentral
29.
go back to reference Rohr JR, Cohen JM. Understanding how temperature shifts could impact infectious disease. PLoS Biol. 2020;18(11):e3000938.PubMedPubMedCentral Rohr JR, Cohen JM. Understanding how temperature shifts could impact infectious disease. PLoS Biol. 2020;18(11):e3000938.PubMedPubMedCentral
30.
go back to reference Esposito MM, Turku S, Lehrfield L, Shoman A. The Impact of Human Activities on Zoonotic Infection Transmissions. Animals (Basel). 2023;13(10):1646.PubMed Esposito MM, Turku S, Lehrfield L, Shoman A. The Impact of Human Activities on Zoonotic Infection Transmissions. Animals (Basel). 2023;13(10):1646.PubMed
31.
go back to reference Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature. 2010;468(7324):647–52.PubMedPubMedCentral Keesing F, Belden LK, Daszak P, Dobson A, Harvell CD, Holt RD, et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature. 2010;468(7324):647–52.PubMedPubMedCentral
32.
go back to reference Min KD, Hwang J, Schneider MC, So Y, Lee JY, Cho SI. An exploration of the protective effect of rodent species richness on the geographical expansion of Lassa fever in West Africa. PLoS Negl Trop Dis. 2021;15(2):e0009108.PubMedPubMedCentral Min KD, Hwang J, Schneider MC, So Y, Lee JY, Cho SI. An exploration of the protective effect of rodent species richness on the geographical expansion of Lassa fever in West Africa. PLoS Negl Trop Dis. 2021;15(2):e0009108.PubMedPubMedCentral
33.
go back to reference Houlihan C, Behrens R. Lassa fever. BMJ (Clinical research ed). 2017;358:j2986.PubMed Houlihan C, Behrens R. Lassa fever. BMJ (Clinical research ed). 2017;358:j2986.PubMed
34.
go back to reference Ihekweazu C, Abubakar I. Tackling viral haemorrhagic fever in Africa. Lancet. 2017;390(10113):2612–4.PubMed Ihekweazu C, Abubakar I. Tackling viral haemorrhagic fever in Africa. Lancet. 2017;390(10113):2612–4.PubMed
35.
go back to reference Curaudeau M, Besombes C, Nakouné E, Fontanet A, Gessain A, Hassanin A. Identifying the most probable mammal reservoir hosts for monkeypox virus based on ecological niche comparisons. Viruses. 2023;15(3):727.PubMedPubMedCentral Curaudeau M, Besombes C, Nakouné E, Fontanet A, Gessain A, Hassanin A. Identifying the most probable mammal reservoir hosts for monkeypox virus based on ecological niche comparisons. Viruses. 2023;15(3):727.PubMedPubMedCentral
36.
go back to reference Jones JE, Le Sage V, Lakdawala SS. Viral and host heterogeneity and their effects on the viral life cycle. Nat Rev Microbiol. 2021;19(4):272–82.PubMed Jones JE, Le Sage V, Lakdawala SS. Viral and host heterogeneity and their effects on the viral life cycle. Nat Rev Microbiol. 2021;19(4):272–82.PubMed
37.
go back to reference Whitehouse ER, Bonwitt J, Hughes CM, Lushima RS, Likafi T, Nguete B, et al. Clinical and epidemiological findings from enhanced monkeypox surveillance in Tshuapa Province, Democratic Republic of the Congo during 2011–2015. J Infect Dis. 2021;223(11):1870–8.PubMed Whitehouse ER, Bonwitt J, Hughes CM, Lushima RS, Likafi T, Nguete B, et al. Clinical and epidemiological findings from enhanced monkeypox surveillance in Tshuapa Province, Democratic Republic of the Congo during 2011–2015. J Infect Dis. 2021;223(11):1870–8.PubMed
39.
go back to reference Du Z, Shao Z, Bai Y, Wang L, Herrera-Diestra JL, Fox SJ, et al. Reproduction number of monkeypox in the early stage of the 2022 multi-country outbreak. J Travel Med. 2022;29(8):taac099.PubMed Du Z, Shao Z, Bai Y, Wang L, Herrera-Diestra JL, Fox SJ, et al. Reproduction number of monkeypox in the early stage of the 2022 multi-country outbreak. J Travel Med. 2022;29(8):taac099.PubMed
40.
go back to reference Branda F, Pierini M, Mazzoli S. Monkeypox: Early estimation of basic reproduction number R0 in Europe. J Med Virol. 2023;95(1):e28270.PubMed Branda F, Pierini M, Mazzoli S. Monkeypox: Early estimation of basic reproduction number R0 in Europe. J Med Virol. 2023;95(1):e28270.PubMed
41.
go back to reference Nakazawa Y, Emerson GL, Carroll DS, et al. Phylogenetic and ecologic perspectives of a monkeypox outbreak, southern Sudan, 2005. Emerg Infect Dis. 2013;19(2):237–45.PubMedPubMedCentral Nakazawa Y, Emerson GL, Carroll DS, et al. Phylogenetic and ecologic perspectives of a monkeypox outbreak, southern Sudan, 2005. Emerg Infect Dis. 2013;19(2):237–45.PubMedPubMedCentral
42.
go back to reference Erez N, Achdout H, Milrot E, Zhao H, Li Y, Reynolds MG, et al. Diagnosis of imported monkeypox, Israel, 2018. Emerg Infect Dis. 2019;25(5):980–3.PubMedPubMedCentral Erez N, Achdout H, Milrot E, Zhao H, Li Y, Reynolds MG, et al. Diagnosis of imported monkeypox, Israel, 2018. Emerg Infect Dis. 2019;25(5):980–3.PubMedPubMedCentral
43.
go back to reference Perez Duque M, Ribeiro S, Martins JV, Casaca P, Leite PP, Tavares M, et al. Ongoing monkeypox virus outbreak, Portugal, 29 April to 23 May 2022. Euro Surveill. 2022;27(22):2200424.PubMedPubMedCentral Perez Duque M, Ribeiro S, Martins JV, Casaca P, Leite PP, Tavares M, et al. Ongoing monkeypox virus outbreak, Portugal, 29 April to 23 May 2022. Euro Surveill. 2022;27(22):2200424.PubMedPubMedCentral
44.
go back to reference Hammerschlag Y, MacLeod G, Papadakis G, Adan Sanchez A, Druce J, Taiaroa G, et al. Monkeypox infection presenting as genital rash, Australia, May 2022. Euro Surveill. 2022;27(22):2200411.PubMedPubMedCentral Hammerschlag Y, MacLeod G, Papadakis G, Adan Sanchez A, Druce J, Taiaroa G, et al. Monkeypox infection presenting as genital rash, Australia, May 2022. Euro Surveill. 2022;27(22):2200411.PubMedPubMedCentral
45.
go back to reference Antinori A, Mazzotta V, Vita S, Carletti F, Tacconi D, Lapini LE, et al. Epidemiological, clinical and virological characteristics of four cases of monkeypox support transmission through sexual contact, Italy, May 2022. Euro Surveill. 2022;27(22):2200421.PubMedPubMedCentral Antinori A, Mazzotta V, Vita S, Carletti F, Tacconi D, Lapini LE, et al. Epidemiological, clinical and virological characteristics of four cases of monkeypox support transmission through sexual contact, Italy, May 2022. Euro Surveill. 2022;27(22):2200421.PubMedPubMedCentral
46.
go back to reference Adler H, Gould S, Hine P, Snell LB, Wong W, Houlihan CF, et al. Clinical features and management of human monkeypox: a retrospective observational study in the UK. Lancet Infect Dis. 2022;22(8):1153–62.PubMedPubMedCentral Adler H, Gould S, Hine P, Snell LB, Wong W, Houlihan CF, et al. Clinical features and management of human monkeypox: a retrospective observational study in the UK. Lancet Infect Dis. 2022;22(8):1153–62.PubMedPubMedCentral
47.
go back to reference Spicknall IH, Pollock ED, Clay PA, Oster AM, Charniga K, Masters N, et al. Modeling the impact of sexual networks in the transmission of Monkeypox virus among gay, bisexual, and other men who have sex with men - United States, 2022. MMWR Morb Mortal Wkly Rep. 2022;71(35):1131–5.PubMedPubMedCentral Spicknall IH, Pollock ED, Clay PA, Oster AM, Charniga K, Masters N, et al. Modeling the impact of sexual networks in the transmission of Monkeypox virus among gay, bisexual, and other men who have sex with men - United States, 2022. MMWR Morb Mortal Wkly Rep. 2022;71(35):1131–5.PubMedPubMedCentral
48.
Metadata
Title
Mapping global zoonotic niche and interregional transmission risk of monkeypox: a retrospective observational study
Authors
Yan-Qun Sun
Jin-Jin Chen
Mei-Chen Liu
Yuan-Yuan Zhang
Tao Wang
Tian-Le Che
Ting-Ting Li
Yan-Ning Liu
Ai-Ying Teng
Bing-Zheng Wu
Xue-Geng Hong
Qiang Xu
Chen-Long Lv
Bao-Gui Jiang
Wei Liu
Li-Qun Fang
Publication date
01-12-2023
Publisher
BioMed Central
Keyword
Mpox Virus
Published in
Globalization and Health / Issue 1/2023
Electronic ISSN: 1744-8603
DOI
https://doi.org/10.1186/s12992-023-00959-0

Other articles of this Issue 1/2023

Globalization and Health 1/2023 Go to the issue