Exportation of Monkeypox Virus From the African Continent

Matthew R. Mauldin; Andrea M. McCollum; Yoshinori J. Nakazawa; Anna Mandra; Erin R. Whitehouse; Whitni Davidson; Hui Zhao; Jinxin Gao; Yu Li; Jeffrey Doty; Adesola Yinka-Ogunleye; Afolabi Akinpelu; Olusola Aruna; Dhamari Naidoo; Kuiama Lewandowski; Babak Afrough; Victoria Graham; Emma Aarons; Roger Hewson; Richard Vipond; Jake Dunning; Meera Chand; Colin Brown; Inbar Cohen-Gihon; Noam Erez; Ohad Shifman; Ofir Israeli; Melamed Sharon; Eli Schwartz; Adi Beth-Din; Anat Zvi; Tze Minn Mak; Yi Kai Ng; Lin Cui; Raymond T.P. Lin; Victoria A. Olson; Tim Brooks; Nir Paran; Chikwe Ihekweazu; Mary G. Reynolds

doi:10.1093/infdis/jiaa559

Exportation of Monkeypox Virus From the African Continent

Matthew R. Mauldin^*, Andrea M. McCollum, Yoshinori J. Nakazawa, Anna Mandra, Erin R. Whitehouse, Whitni Davidson, Hui Zhao, Jinxin Gao, Yu Li, Jeffrey Doty, Adesola Yinka-Ogunleye, Afolabi Akinpelu, Olusola Aruna, Dhamari Naidoo, Kuiama Lewandowski, Babak Afrough, Victoria Graham, Emma Aarons, Roger Hewson, Richard VipondJake Dunning, Meera Chand, Colin Brown, Inbar Cohen-Gihon, Noam Erez, Ohad Shifman, Ofir Israeli, Melamed Sharon, Eli Schwartz, Adi Beth-Din, Anat Zvi, Tze Minn Mak, Yi Kai Ng, Lin Cui, Raymond T.P. Lin, Victoria A. Olson, Tim Brooks, Nir Paran, Chikwe Ihekweazu, Mary G. Reynolds

^*Corresponding author for this work

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Abstract

Background: The largest West African monkeypox outbreak began September 2017, in Nigeria. Four individuals traveling from Nigeria to the United Kingdom (n = 2), Israel (n = 1), and Singapore (n = 1) became the first human monkeypox cases exported from Africa, and a related nosocomial transmission event in the United Kingdom became the first confirmed human-to-human monkeypox transmission event outside of Africa.

Methods: Epidemiological and molecular data for exported and Nigerian cases were analyzed jointly to better understand the exportations in the temporal and geographic context of the outbreak.

Results: Isolates from all travelers and a Bayelsa case shared a most recent common ancestor and traveled to Bayelsa, Delta, or Rivers states. Genetic variation for this cluster was lower than would be expected from a random sampling of genomes from this outbreak, but data did not support direct links between travelers.

Conclusions: Monophyly of exportation cases and the Bayelsa sample, along with the intermediate levels of genetic variation, suggest a small pool of related isolates is the likely source for the exported infections. This may be the result of the level of genetic variation present in monkeypox isolates circulating within the contiguous region of Bayelsa, Delta, and Rivers states, or another more restricted, yet unidentified source pool.

Original language	English
Pages (from-to)	1367-1376
Number of pages	10
Journal	Journal of Infectious Diseases
Volume	225
Issue number	8
Early online date	3 Sept 2020
DOIs	https://doi.org/10.1093/infdis/jiaa559
Publication status	Published - 15 Apr 2022

Bibliographical note

Funding Information: A portion of funding for this project came from the PHE Public Health Budget and Rare and Imported Pathogens Laboratory budget, as well as the CDC’s Global Disease Detection Program.

Open Access: This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited.

Publisher Copyright: © 2020 The Author(s) 2020. Published by Oxford University Press for the Infectious Diseases Society of America.

Citation: Matthew R Mauldin, Andrea M McCollum, Yoshinori J Nakazawa, Anna Mandra, Erin R Whitehouse, Whitni Davidson, Hui Zhao, Jinxin Gao, Yu Li, Jeffrey Doty, Adesola Yinka-Ogunleye, Afolabi Akinpelu, Olusola Aruna, Dhamari Naidoo, Kuiama Lewandowski, Babak Afrough, Victoria Graham, Emma Aarons, Roger Hewson, Richard Vipond, Jake Dunning, Meera Chand, Colin Brown, Inbar Cohen-Gihon, Noam Erez, Ohad Shifman, Ofir Israeli, Melamed Sharon, Eli Schwartz, Adi Beth-Din, Anat Zvi, Tze Minn Mak, Yi Kai Ng, Lin Cui, Raymond T P Lin, Victoria A Olson, Tim Brooks, Nir Paran, Chikwe Ihekweazu, Mary G Reynolds, Exportation of Monkeypox Virus From the African Continent, The Journal of Infectious Diseases, Volume 225, Issue 8, 15 April 2022, Pages 1367–1376,

DOI: https://doi.org/10.1093/infdis/jiaa559

Keywords

border health
exportation
haplotype networks
monkeypox virus
travel epidemiology
viral genomes

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Mauldin2022ExportationOfMonkeypoxVirusFromTheAfricanContinentJInfectDisFinal published version, 5.18 MBLicence: CC BY-NC-ND

Cite this

Mauldin, M. R., McCollum, A. M., Nakazawa, Y. J., Mandra, A., Whitehouse, E. R., Davidson, W., Zhao, H., Gao, J., Li, Y., Doty, J., Yinka-Ogunleye, A., Akinpelu, A., Aruna, O., Naidoo, D., Lewandowski, K., Afrough, B., Graham, V., Aarons, E., Hewson, R., ... Reynolds, M. G. (2022). Exportation of Monkeypox Virus From the African Continent. Journal of Infectious Diseases, 225(8), 1367-1376. https://doi.org/10.1093/infdis/jiaa559

@article{aab9963dbdb546918c9b4cdc5b94ded2,

title = "Exportation of Monkeypox Virus From the African Continent",

abstract = "Background: The largest West African monkeypox outbreak began September 2017, in Nigeria. Four individuals traveling from Nigeria to the United Kingdom (n = 2), Israel (n = 1), and Singapore (n = 1) became the first human monkeypox cases exported from Africa, and a related nosocomial transmission event in the United Kingdom became the first confirmed human-to-human monkeypox transmission event outside of Africa. Methods: Epidemiological and molecular data for exported and Nigerian cases were analyzed jointly to better understand the exportations in the temporal and geographic context of the outbreak. Results: Isolates from all travelers and a Bayelsa case shared a most recent common ancestor and traveled to Bayelsa, Delta, or Rivers states. Genetic variation for this cluster was lower than would be expected from a random sampling of genomes from this outbreak, but data did not support direct links between travelers. Conclusions: Monophyly of exportation cases and the Bayelsa sample, along with the intermediate levels of genetic variation, suggest a small pool of related isolates is the likely source for the exported infections. This may be the result of the level of genetic variation present in monkeypox isolates circulating within the contiguous region of Bayelsa, Delta, and Rivers states, or another more restricted, yet unidentified source pool.",

keywords = "border health, exportation, haplotype networks, monkeypox virus, travel epidemiology, viral genomes",

author = "Mauldin, {Matthew R.} and McCollum, {Andrea M.} and Nakazawa, {Yoshinori J.} and Anna Mandra and Whitehouse, {Erin R.} and Whitni Davidson and Hui Zhao and Jinxin Gao and Yu Li and Jeffrey Doty and Adesola Yinka-Ogunleye and Afolabi Akinpelu and Olusola Aruna and Dhamari Naidoo and Kuiama Lewandowski and Babak Afrough and Victoria Graham and Emma Aarons and Roger Hewson and Richard Vipond and Jake Dunning and Meera Chand and Colin Brown and Inbar Cohen-Gihon and Noam Erez and Ohad Shifman and Ofir Israeli and Melamed Sharon and Eli Schwartz and Adi Beth-Din and Anat Zvi and Mak, {Tze Minn} and Ng, {Yi Kai} and Lin Cui and Lin, {Raymond T.P.} and Olson, {Victoria A.} and Tim Brooks and Nir Paran and Chikwe Ihekweazu and Reynolds, {Mary G.}",

note = "Funding Information: A portion of funding for this project came from the PHE Public Health Budget and Rare and Imported Pathogens Laboratory budget, as well as the CDC{\textquoteright}s Global Disease Detection Program. Open Access: This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. Publisher Copyright: {\textcopyright} 2020 The Author(s) 2020. Published by Oxford University Press for the Infectious Diseases Society of America. Citation: Matthew R Mauldin, Andrea M McCollum, Yoshinori J Nakazawa, Anna Mandra, Erin R Whitehouse, Whitni Davidson, Hui Zhao, Jinxin Gao, Yu Li, Jeffrey Doty, Adesola Yinka-Ogunleye, Afolabi Akinpelu, Olusola Aruna, Dhamari Naidoo, Kuiama Lewandowski, Babak Afrough, Victoria Graham, Emma Aarons, Roger Hewson, Richard Vipond, Jake Dunning, Meera Chand, Colin Brown, Inbar Cohen-Gihon, Noam Erez, Ohad Shifman, Ofir Israeli, Melamed Sharon, Eli Schwartz, Adi Beth-Din, Anat Zvi, Tze Minn Mak, Yi Kai Ng, Lin Cui, Raymond T P Lin, Victoria A Olson, Tim Brooks, Nir Paran, Chikwe Ihekweazu, Mary G Reynolds, Exportation of Monkeypox Virus From the African Continent, The Journal of Infectious Diseases, Volume 225, Issue 8, 15 April 2022, Pages 1367–1376, DOI: https://doi.org/10.1093/infdis/jiaa559 ",

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Mauldin, MR, McCollum, AM, Nakazawa, YJ, Mandra, A, Whitehouse, ER, Davidson, W, Zhao, H, Gao, J, Li, Y, Doty, J, Yinka-Ogunleye, A, Akinpelu, A, Aruna, O, Naidoo, D, Lewandowski, K , Afrough, B, Graham, V, Aarons, E, Hewson, R, Vipond, R, Dunning, J, Chand, M , Brown, C, Cohen-Gihon, I, Erez, N, Shifman, O, Israeli, O, Sharon, M, Schwartz, E, Beth-Din, A, Zvi, A, Mak, TM, Ng, YK, Cui, L, Lin, RTP, Olson, VA, Brooks, T, Paran, N, Ihekweazu, C & Reynolds, MG 2022, 'Exportation of Monkeypox Virus From the African Continent', Journal of Infectious Diseases, vol. 225, no. 8, pp. 1367-1376. https://doi.org/10.1093/infdis/jiaa559

TY - JOUR

T1 - Exportation of Monkeypox Virus From the African Continent

AU - Mauldin, Matthew R.

AU - McCollum, Andrea M.

AU - Nakazawa, Yoshinori J.

AU - Mandra, Anna

AU - Whitehouse, Erin R.

AU - Davidson, Whitni

AU - Zhao, Hui

AU - Gao, Jinxin

AU - Li, Yu

AU - Doty, Jeffrey

AU - Yinka-Ogunleye, Adesola

AU - Akinpelu, Afolabi

AU - Aruna, Olusola

AU - Naidoo, Dhamari

AU - Lewandowski, Kuiama

AU - Afrough, Babak

AU - Graham, Victoria

AU - Aarons, Emma

AU - Hewson, Roger

AU - Vipond, Richard

AU - Dunning, Jake

AU - Chand, Meera

AU - Brown, Colin

AU - Cohen-Gihon, Inbar

AU - Erez, Noam

AU - Shifman, Ohad

AU - Israeli, Ofir

AU - Sharon, Melamed

AU - Schwartz, Eli

AU - Beth-Din, Adi

AU - Zvi, Anat

AU - Mak, Tze Minn

AU - Ng, Yi Kai

AU - Cui, Lin

AU - Lin, Raymond T.P.

AU - Olson, Victoria A.

AU - Brooks, Tim

AU - Paran, Nir

AU - Ihekweazu, Chikwe

AU - Reynolds, Mary G.

N1 - Funding Information: A portion of funding for this project came from the PHE Public Health Budget and Rare and Imported Pathogens Laboratory budget, as well as the CDC’s Global Disease Detection Program. Open Access: This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (http://creativecommons.org/licenses/by-nc-nd/4.0/), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. Publisher Copyright: © 2020 The Author(s) 2020. Published by Oxford University Press for the Infectious Diseases Society of America. Citation: Matthew R Mauldin, Andrea M McCollum, Yoshinori J Nakazawa, Anna Mandra, Erin R Whitehouse, Whitni Davidson, Hui Zhao, Jinxin Gao, Yu Li, Jeffrey Doty, Adesola Yinka-Ogunleye, Afolabi Akinpelu, Olusola Aruna, Dhamari Naidoo, Kuiama Lewandowski, Babak Afrough, Victoria Graham, Emma Aarons, Roger Hewson, Richard Vipond, Jake Dunning, Meera Chand, Colin Brown, Inbar Cohen-Gihon, Noam Erez, Ohad Shifman, Ofir Israeli, Melamed Sharon, Eli Schwartz, Adi Beth-Din, Anat Zvi, Tze Minn Mak, Yi Kai Ng, Lin Cui, Raymond T P Lin, Victoria A Olson, Tim Brooks, Nir Paran, Chikwe Ihekweazu, Mary G Reynolds, Exportation of Monkeypox Virus From the African Continent, The Journal of Infectious Diseases, Volume 225, Issue 8, 15 April 2022, Pages 1367–1376, DOI: https://doi.org/10.1093/infdis/jiaa559

PY - 2022/4/15

Y1 - 2022/4/15

N2 - Background: The largest West African monkeypox outbreak began September 2017, in Nigeria. Four individuals traveling from Nigeria to the United Kingdom (n = 2), Israel (n = 1), and Singapore (n = 1) became the first human monkeypox cases exported from Africa, and a related nosocomial transmission event in the United Kingdom became the first confirmed human-to-human monkeypox transmission event outside of Africa. Methods: Epidemiological and molecular data for exported and Nigerian cases were analyzed jointly to better understand the exportations in the temporal and geographic context of the outbreak. Results: Isolates from all travelers and a Bayelsa case shared a most recent common ancestor and traveled to Bayelsa, Delta, or Rivers states. Genetic variation for this cluster was lower than would be expected from a random sampling of genomes from this outbreak, but data did not support direct links between travelers. Conclusions: Monophyly of exportation cases and the Bayelsa sample, along with the intermediate levels of genetic variation, suggest a small pool of related isolates is the likely source for the exported infections. This may be the result of the level of genetic variation present in monkeypox isolates circulating within the contiguous region of Bayelsa, Delta, and Rivers states, or another more restricted, yet unidentified source pool.

AB - Background: The largest West African monkeypox outbreak began September 2017, in Nigeria. Four individuals traveling from Nigeria to the United Kingdom (n = 2), Israel (n = 1), and Singapore (n = 1) became the first human monkeypox cases exported from Africa, and a related nosocomial transmission event in the United Kingdom became the first confirmed human-to-human monkeypox transmission event outside of Africa. Methods: Epidemiological and molecular data for exported and Nigerian cases were analyzed jointly to better understand the exportations in the temporal and geographic context of the outbreak. Results: Isolates from all travelers and a Bayelsa case shared a most recent common ancestor and traveled to Bayelsa, Delta, or Rivers states. Genetic variation for this cluster was lower than would be expected from a random sampling of genomes from this outbreak, but data did not support direct links between travelers. Conclusions: Monophyly of exportation cases and the Bayelsa sample, along with the intermediate levels of genetic variation, suggest a small pool of related isolates is the likely source for the exported infections. This may be the result of the level of genetic variation present in monkeypox isolates circulating within the contiguous region of Bayelsa, Delta, and Rivers states, or another more restricted, yet unidentified source pool.

KW - border health

KW - exportation

KW - haplotype networks

KW - monkeypox virus

KW - travel epidemiology

KW - viral genomes

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DO - 10.1093/infdis/jiaa559

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AN - SCOPUS:85128493485

SN - 0022-1899

VL - 225

SP - 1367

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JO - Journal of Infectious Diseases

JF - Journal of Infectious Diseases

IS - 8

ER -

Exportation of Monkeypox Virus From the African Continent

Abstract

Bibliographical note

Keywords

UN SDGs

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