Virus genomes reveal factors that spread and sustained the Ebola epidemic

Gytis Dudas; Luiz Max Carvalho; Trevor Bedford; Andrew J. Tatem; Guy Baele; Nuno R. Faria; Daniel J. Park; Jason T. Ladner; Armando Arias; Danny Asogun; Filip Bielejec; Sarah L. Caddy; Matthew Cotten; Jonathan D'Ambrozio; Simon Dellicour; Antonino Di Caro; Joseph W. Diclaro; Sophie Duraffour; Michael J. Elmore; Lawrence S. Fakoli; Ousmane Faye; Merle L. Gilbert; Sahr M. Gevao; Stephen Gire; Adrianne Gladden-Young; Andreas Gnirke; Augustine Goba; Donald S. Grant; Bart L. Haagmans; Julian A. Hiscox; Umaru Jah; Jeffrey R. Kugelman; Di Liu; Jia Lu; Christine M. Malboeuf; Suzanne Mate; David A. Matthews; Christian B. Matranga; Luke W. Meredith; James Qu; Joshua Quick; Suzan D. Pas; My V.T. Phan; Georgios Pollakis; Chantal B. Reusken; Mariano Sanchez-Lockhart; Stephen F. Schaffner; John S. Schieffelin; Rachel S. Sealfon; Etienne Simon-Loriere; Saskia L. Smits; Kilian Stoecker; Lucy Thorne; Ekaete Alice Tobin; Mohamed A. Vandi; Simon J. Watson; Kendra West; Shannon Whitmer; Michael R. Wiley; Sarah M. Winnicki; Shirlee Wohl; Roman Wölfel; Nathan L. Yozwiak; Kristian G. Andersen; Sylvia O. Blyden; Fatorma Bolay; Miles W. Carroll; Bernice Dahn; Boubacar Diallo; Pierre Formenty; Christophe Fraser; George F. Gao; Robert F. Garry; Ian Goodfellow; Stephan Günther; Christian T. Happi; Edward C. Holmes; Brima Kargbo; Sakoba Keïta; Paul Kellam; Marion P.G. Koopmans; Jens H. Kuhn; Nicholas J. Loman; N'Faly Magassouba; Dhamari Naidoo; Stuart T. Nichol; Tolbert Nyenswah; Gustavo Palacios; Oliver G. Pybus; Pardis C. Sabeti; Amadou Sall; Ute Ströher; Isatta Wurie; Marc A. Suchard; Philippe Lemey; Andrew Rambaut

doi:10.1038/nature22040

Virus genomes reveal factors that spread and sustained the Ebola epidemic

Gytis Dudas, Luiz Max Carvalho, Trevor Bedford, Andrew J. Tatem, Guy Baele, Nuno R. Faria, Daniel J. Park, Jason T. Ladner, Armando Arias, Danny Asogun, Filip Bielejec, Sarah L. Caddy, Matthew Cotten, Jonathan D'Ambrozio, Simon Dellicour, Antonino Di Caro, Joseph W. Diclaro, Sophie Duraffour, Michael J. Elmore, Lawrence S. FakoliOusmane Faye, Merle L. Gilbert, Sahr M. Gevao, Stephen Gire, Adrianne Gladden-Young, Andreas Gnirke, Augustine Goba, Donald S. Grant, Bart L. Haagmans, Julian A. Hiscox, Umaru Jah, Jeffrey R. Kugelman, Di Liu, Jia Lu, Christine M. Malboeuf, Suzanne Mate, David A. Matthews, Christian B. Matranga, Luke W. Meredith, James Qu, Joshua Quick, Suzan D. Pas, My V.T. Phan, Georgios Pollakis, Chantal B. Reusken, Mariano Sanchez-Lockhart, Stephen F. Schaffner, John S. Schieffelin, Rachel S. Sealfon, Etienne Simon-Loriere, Saskia L. Smits, Kilian Stoecker, Lucy Thorne, Ekaete Alice Tobin, Mohamed A. Vandi, Simon J. Watson, Kendra West, Shannon Whitmer, Michael R. Wiley, Sarah M. Winnicki, Shirlee Wohl, Roman Wölfel, Nathan L. Yozwiak, Kristian G. Andersen, Sylvia O. Blyden, Fatorma Bolay, Miles W. Carroll, Bernice Dahn, Boubacar Diallo, Pierre Formenty, Christophe Fraser, George F. Gao, Robert F. Garry, Ian Goodfellow, Stephan Günther, Christian T. Happi, Edward C. Holmes, Brima Kargbo, Sakoba Keïta, Paul Kellam, Marion P.G. Koopmans, Jens H. Kuhn, Nicholas J. Loman, N'Faly Magassouba, Dhamari Naidoo, Stuart T. Nichol, Tolbert Nyenswah, Gustavo Palacios, Oliver G. Pybus, Pardis C. Sabeti, Amadou Sall, Ute Ströher, Isatta Wurie, Marc A. Suchard, Philippe Lemey, Andrew Rambaut

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Abstract

The 2013-2016 West African epidemic caused by the Ebola virus was of unprecedented magnitude, duration and impact. Here we reconstruct the dispersal, proliferation and decline of Ebola virus throughout the region by analysing 1,610 Ebola virus genomes, which represent over 5% of the known cases. We test the association of geography, climate and demography with viral movement among administrative regions, inferring a classic 'gravity' model, with intense dispersal between larger and closer populations. Despite attenuation of international dispersal after border closures, cross-border transmission had already sown the seeds for an international epidemic, rendering these measures ineffective at curbing the epidemic. We address why the epidemic did not spread into neighbouring countries, showing that these countries were susceptible to substantial outbreaks but at lower risk of introductions. Finally, we reveal that this large epidemic was a heterogeneous and spatially dissociated collection of transmission clusters of varying size, duration and connectivity. These insights will help to inform interventions in future epidemics.

Original language	English (US)
Pages (from-to)	309-315
Number of pages	7
Journal	Nature
Volume	544
Issue number	7650
DOIs	https://doi.org/10.1038/nature22040
State	Published - Apr 20 2017
Externally published	Yes

ASJC Scopus subject areas

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10.1038/nature22040

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Dudas, G., Carvalho, L. M., Bedford, T., Tatem, A. J., Baele, G., Faria, N. R., Park, D. J., Ladner, J. T., Arias, A., Asogun, D., Bielejec, F., Caddy, S. L., Cotten, M., D'Ambrozio, J., Dellicour, S., Di Caro, A., Diclaro, J. W., Duraffour, S., Elmore, M. J., ... Rambaut, A. (2017). Virus genomes reveal factors that spread and sustained the Ebola epidemic. Nature, 544(7650), 309-315. https://doi.org/10.1038/nature22040

Dudas, G, Carvalho, LM, Bedford, T, Tatem, AJ, Baele, G, Faria, NR, Park, DJ, Ladner, JT, Arias, A, Asogun, D, Bielejec, F, Caddy, SL, Cotten, M, D'Ambrozio, J, Dellicour, S, Di Caro, A, Diclaro, JW, Duraffour, S, Elmore, MJ, Fakoli, LS, Faye, O, Gilbert, ML, Gevao, SM, Gire, S, Gladden-Young, A, Gnirke, A, Goba, A, Grant, DS, Haagmans, BL, Hiscox, JA, Jah, U, Kugelman, JR, Liu, D, Lu, J, Malboeuf, CM, Mate, S, Matthews, DA, Matranga, CB, Meredith, LW, Qu, J, Quick, J, Pas, SD, Phan, MVT, Pollakis, G, Reusken, CB, Sanchez-Lockhart, M, Schaffner, SF, Schieffelin, JS, Sealfon, RS, Simon-Loriere, E, Smits, SL, Stoecker, K, Thorne, L, Tobin, EA, Vandi, MA, Watson, SJ, West, K, Whitmer, S, Wiley, MR, Winnicki, SM, Wohl, S, Wölfel, R, Yozwiak, NL, Andersen, KG, Blyden, SO, Bolay, F, Carroll, MW, Dahn, B, Diallo, B, Formenty, P, Fraser, C, Gao, GF, Garry, RF, Goodfellow, I, Günther, S, Happi, CT, Holmes, EC, Kargbo, B, Keïta, S, Kellam, P, Koopmans, MPG, Kuhn, JH, Loman, NJ, Magassouba, NF, Naidoo, D, Nichol, ST, Nyenswah, T, Palacios, G, Pybus, OG, Sabeti, PC, Sall, A, Ströher, U, Wurie, I, Suchard, MA, Lemey, P & Rambaut, A 2017, 'Virus genomes reveal factors that spread and sustained the Ebola epidemic', Nature, vol. 544, no. 7650, pp. 309-315. https://doi.org/10.1038/nature22040

@article{1d668e2dcbc140ebaed18ec30ac1e75d,

title = "Virus genomes reveal factors that spread and sustained the Ebola epidemic",

abstract = "The 2013-2016 West African epidemic caused by the Ebola virus was of unprecedented magnitude, duration and impact. Here we reconstruct the dispersal, proliferation and decline of Ebola virus throughout the region by analysing 1,610 Ebola virus genomes, which represent over 5% of the known cases. We test the association of geography, climate and demography with viral movement among administrative regions, inferring a classic 'gravity' model, with intense dispersal between larger and closer populations. Despite attenuation of international dispersal after border closures, cross-border transmission had already sown the seeds for an international epidemic, rendering these measures ineffective at curbing the epidemic. We address why the epidemic did not spread into neighbouring countries, showing that these countries were susceptible to substantial outbreaks but at lower risk of introductions. Finally, we reveal that this large epidemic was a heterogeneous and spatially dissociated collection of transmission clusters of varying size, duration and connectivity. These insights will help to inform interventions in future epidemics.",

author = "Gytis Dudas and Carvalho, {Luiz Max} and Trevor Bedford and Tatem, {Andrew J.} and Guy Baele and Faria, {Nuno R.} and Park, {Daniel J.} and Ladner, {Jason T.} and Armando Arias and Danny Asogun and Filip Bielejec and Caddy, {Sarah L.} and Matthew Cotten and Jonathan D'Ambrozio and Simon Dellicour and {Di Caro}, Antonino and Diclaro, {Joseph W.} and Sophie Duraffour and Elmore, {Michael J.} and Fakoli, {Lawrence S.} and Ousmane Faye and Gilbert, {Merle L.} and Gevao, {Sahr M.} and Stephen Gire and Adrianne Gladden-Young and Andreas Gnirke and Augustine Goba and Grant, {Donald S.} and Haagmans, {Bart L.} and Hiscox, {Julian A.} and Umaru Jah and Kugelman, {Jeffrey R.} and Di Liu and Jia Lu and Malboeuf, {Christine M.} and Suzanne Mate and Matthews, {David A.} and Matranga, {Christian B.} and Meredith, {Luke W.} and James Qu and Joshua Quick and Pas, {Suzan D.} and Phan, {My V.T.} and Georgios Pollakis and Reusken, {Chantal B.} and Mariano Sanchez-Lockhart and Schaffner, {Stephen F.} and Schieffelin, {John S.} and Sealfon, {Rachel S.} and Etienne Simon-Loriere and Smits, {Saskia L.} and Kilian Stoecker and Lucy Thorne and Tobin, {Ekaete Alice} and Vandi, {Mohamed A.} and Watson, {Simon J.} and Kendra West and Shannon Whitmer and Wiley, {Michael R.} and Winnicki, {Sarah M.} and Shirlee Wohl and Roman W{\"o}lfel and Yozwiak, {Nathan L.} and Andersen, {Kristian G.} and Blyden, {Sylvia O.} and Fatorma Bolay and Carroll, {Miles W.} and Bernice Dahn and Boubacar Diallo and Pierre Formenty and Christophe Fraser and Gao, {George F.} and Garry, {Robert F.} and Ian Goodfellow and Stephan G{\"u}nther and Happi, {Christian T.} and Holmes, {Edward C.} and Brima Kargbo and Sakoba Ke{\"i}ta and Paul Kellam and Koopmans, {Marion P.G.} and Kuhn, {Jens H.} and Loman, {Nicholas J.} and N'Faly Magassouba and Dhamari Naidoo and Nichol, {Stuart T.} and Tolbert Nyenswah and Gustavo Palacios and Pybus, {Oliver G.} and Sabeti, {Pardis C.} and Amadou Sall and Ute Str{\"o}her and Isatta Wurie and Suchard, {Marc A.} and Philippe Lemey and Andrew Rambaut",

note = "Funding Information: The authors acknowledge support from: European Union Seventh Framework 278433-PREDEMICS (P.L., A.R.) and ERC 260864 (P.L., A.R., M.A.S.) European Union Horizon 2020 643476-COMPARE (M.P.G.K., A.R.), 634650-VIROGENESIS (P.L., M.P.G.K.), 666100-EVIDENT and European Commission IFS/2011/272-372, EMLab (S.G.), National Institutes of Health R01 AI107034, R01 AI117011 and R01 HG006139 and National Science Foundation IIS 1251151 and DMS 1264153 (M.A.S.), NIH AI081982, AI082119, AI082805 AI088843, AI104216, AI104621, AI115754, HSN272200900049C, HHSN272201400048C (R.F.G.), NIH R35 GM119774-01 (T.B.) National Health & Medical Research Council (Australia) (E.C.H.). The Research Foundation - Flanders G0D5117N (G.B., P.L.), Work in Liberia was funded by the Defense Threat Reduction Agency, the Global Emerging Infections System and the Targeted Acquisition of Reference Materials Augmenting Capabilities (TARMAC) Initiative agencies from the US Department of Defense (G.Pa.), Bill and Melinda Gates Foundation OPP1106427, 1032350, OPP1134076, Wellcome Trust 106866/Z/15/Z, Clinton Health Access Initiative (A.J.T.), National Institute for Health Research Health Protection Research Unit in Emerging and Zoonotic Infections (J.A.H.), Key Research and Development Program from the Ministry of Science and Technology of China 2016YFC1200800 (D.L.), National Natural Science Foundation of China 81590760 and 81321063 (G.F.G.), Mahan Post-doctoral fellowship Fred Hutchinson Cancer Research Center (G.D.), National Institute of Allergy and Infectious Disease U19AI110818, 5R01AI114855-03, United States Agency for International Development OAA-G-15-00001 and the Bill and Melinda Gates Foundation OPP1123407 (P.C.S.), NIH 1U01HG007480-01 and the World Bank ACE019 (C.T.H.), PEW Biomedical Scholarship, NIH UL1TR001114, and NIAID contract HHSN272201400048C (K.G.A.). J.H.K., an employee of Tunnell Government Services, Inc., is a subcontractor under Battelle Memorial Institute's prime contract with the NIAID (contract HHSN272200700016I). Colour-blind-friendly colour palettes were designed by C. Brewer, Pennsylvania State University (http://colorbrewer2.org). Matplotlib (http://matplotlib.org) was used extensively throughout this article for data visualisation. We acknowledge support from NVIDIA Corporation with the donation of parallel computing resources used for this research. Finally, we recognize the contributions made by our colleagues who died from Ebola virus disease whilst fighting the epidemic. Publisher Copyright: {\textcopyright} 2017 Macmillan Publishers Limited, part of Springer Nature.",

year = "2017",

month = apr,

day = "20",

doi = "10.1038/nature22040",

language = "English (US)",

volume = "544",

pages = "309--315",

journal = "Nature",

issn = "0028-0836",

number = "7650",

}

TY - JOUR

T1 - Virus genomes reveal factors that spread and sustained the Ebola epidemic

AU - Dudas, Gytis

AU - Carvalho, Luiz Max

AU - Bedford, Trevor

AU - Tatem, Andrew J.

AU - Baele, Guy

AU - Faria, Nuno R.

AU - Park, Daniel J.

AU - Ladner, Jason T.

AU - Arias, Armando

AU - Asogun, Danny

AU - Bielejec, Filip

AU - Caddy, Sarah L.

AU - Cotten, Matthew

AU - D'Ambrozio, Jonathan

AU - Dellicour, Simon

AU - Di Caro, Antonino

AU - Diclaro, Joseph W.

AU - Duraffour, Sophie

AU - Elmore, Michael J.

AU - Fakoli, Lawrence S.

AU - Faye, Ousmane

AU - Gilbert, Merle L.

AU - Gevao, Sahr M.

AU - Gire, Stephen

AU - Gladden-Young, Adrianne

AU - Gnirke, Andreas

AU - Goba, Augustine

AU - Grant, Donald S.

AU - Haagmans, Bart L.

AU - Hiscox, Julian A.

AU - Jah, Umaru

AU - Kugelman, Jeffrey R.

AU - Liu, Di

AU - Lu, Jia

AU - Malboeuf, Christine M.

AU - Mate, Suzanne

AU - Matthews, David A.

AU - Matranga, Christian B.

AU - Meredith, Luke W.

AU - Qu, James

AU - Quick, Joshua

AU - Pas, Suzan D.

AU - Phan, My V.T.

AU - Pollakis, Georgios

AU - Reusken, Chantal B.

AU - Sanchez-Lockhart, Mariano

AU - Schaffner, Stephen F.

AU - Schieffelin, John S.

AU - Sealfon, Rachel S.

AU - Simon-Loriere, Etienne

AU - Smits, Saskia L.

AU - Stoecker, Kilian

AU - Thorne, Lucy

AU - Tobin, Ekaete Alice

AU - Vandi, Mohamed A.

AU - Watson, Simon J.

AU - West, Kendra

AU - Whitmer, Shannon

AU - Wiley, Michael R.

AU - Winnicki, Sarah M.

AU - Wohl, Shirlee

AU - Wölfel, Roman

AU - Yozwiak, Nathan L.

AU - Andersen, Kristian G.

AU - Blyden, Sylvia O.

AU - Bolay, Fatorma

AU - Carroll, Miles W.

AU - Dahn, Bernice

AU - Diallo, Boubacar

AU - Formenty, Pierre

AU - Fraser, Christophe

AU - Gao, George F.

AU - Garry, Robert F.

AU - Goodfellow, Ian

AU - Günther, Stephan

AU - Happi, Christian T.

AU - Holmes, Edward C.

AU - Kargbo, Brima

AU - Keïta, Sakoba

AU - Kellam, Paul

AU - Koopmans, Marion P.G.

AU - Kuhn, Jens H.

AU - Loman, Nicholas J.

AU - Magassouba, N'Faly

AU - Naidoo, Dhamari

AU - Nichol, Stuart T.

AU - Nyenswah, Tolbert

AU - Palacios, Gustavo

AU - Pybus, Oliver G.

AU - Sabeti, Pardis C.

AU - Sall, Amadou

AU - Ströher, Ute

AU - Wurie, Isatta

AU - Suchard, Marc A.

AU - Lemey, Philippe

AU - Rambaut, Andrew

N1 - Funding Information: The authors acknowledge support from: European Union Seventh Framework 278433-PREDEMICS (P.L., A.R.) and ERC 260864 (P.L., A.R., M.A.S.) European Union Horizon 2020 643476-COMPARE (M.P.G.K., A.R.), 634650-VIROGENESIS (P.L., M.P.G.K.), 666100-EVIDENT and European Commission IFS/2011/272-372, EMLab (S.G.), National Institutes of Health R01 AI107034, R01 AI117011 and R01 HG006139 and National Science Foundation IIS 1251151 and DMS 1264153 (M.A.S.), NIH AI081982, AI082119, AI082805 AI088843, AI104216, AI104621, AI115754, HSN272200900049C, HHSN272201400048C (R.F.G.), NIH R35 GM119774-01 (T.B.) National Health & Medical Research Council (Australia) (E.C.H.). The Research Foundation - Flanders G0D5117N (G.B., P.L.), Work in Liberia was funded by the Defense Threat Reduction Agency, the Global Emerging Infections System and the Targeted Acquisition of Reference Materials Augmenting Capabilities (TARMAC) Initiative agencies from the US Department of Defense (G.Pa.), Bill and Melinda Gates Foundation OPP1106427, 1032350, OPP1134076, Wellcome Trust 106866/Z/15/Z, Clinton Health Access Initiative (A.J.T.), National Institute for Health Research Health Protection Research Unit in Emerging and Zoonotic Infections (J.A.H.), Key Research and Development Program from the Ministry of Science and Technology of China 2016YFC1200800 (D.L.), National Natural Science Foundation of China 81590760 and 81321063 (G.F.G.), Mahan Post-doctoral fellowship Fred Hutchinson Cancer Research Center (G.D.), National Institute of Allergy and Infectious Disease U19AI110818, 5R01AI114855-03, United States Agency for International Development OAA-G-15-00001 and the Bill and Melinda Gates Foundation OPP1123407 (P.C.S.), NIH 1U01HG007480-01 and the World Bank ACE019 (C.T.H.), PEW Biomedical Scholarship, NIH UL1TR001114, and NIAID contract HHSN272201400048C (K.G.A.). J.H.K., an employee of Tunnell Government Services, Inc., is a subcontractor under Battelle Memorial Institute's prime contract with the NIAID (contract HHSN272200700016I). Colour-blind-friendly colour palettes were designed by C. Brewer, Pennsylvania State University (http://colorbrewer2.org). Matplotlib (http://matplotlib.org) was used extensively throughout this article for data visualisation. We acknowledge support from NVIDIA Corporation with the donation of parallel computing resources used for this research. Finally, we recognize the contributions made by our colleagues who died from Ebola virus disease whilst fighting the epidemic. Publisher Copyright: © 2017 Macmillan Publishers Limited, part of Springer Nature.

PY - 2017/4/20

Y1 - 2017/4/20

N2 - The 2013-2016 West African epidemic caused by the Ebola virus was of unprecedented magnitude, duration and impact. Here we reconstruct the dispersal, proliferation and decline of Ebola virus throughout the region by analysing 1,610 Ebola virus genomes, which represent over 5% of the known cases. We test the association of geography, climate and demography with viral movement among administrative regions, inferring a classic 'gravity' model, with intense dispersal between larger and closer populations. Despite attenuation of international dispersal after border closures, cross-border transmission had already sown the seeds for an international epidemic, rendering these measures ineffective at curbing the epidemic. We address why the epidemic did not spread into neighbouring countries, showing that these countries were susceptible to substantial outbreaks but at lower risk of introductions. Finally, we reveal that this large epidemic was a heterogeneous and spatially dissociated collection of transmission clusters of varying size, duration and connectivity. These insights will help to inform interventions in future epidemics.

AB - The 2013-2016 West African epidemic caused by the Ebola virus was of unprecedented magnitude, duration and impact. Here we reconstruct the dispersal, proliferation and decline of Ebola virus throughout the region by analysing 1,610 Ebola virus genomes, which represent over 5% of the known cases. We test the association of geography, climate and demography with viral movement among administrative regions, inferring a classic 'gravity' model, with intense dispersal between larger and closer populations. Despite attenuation of international dispersal after border closures, cross-border transmission had already sown the seeds for an international epidemic, rendering these measures ineffective at curbing the epidemic. We address why the epidemic did not spread into neighbouring countries, showing that these countries were susceptible to substantial outbreaks but at lower risk of introductions. Finally, we reveal that this large epidemic was a heterogeneous and spatially dissociated collection of transmission clusters of varying size, duration and connectivity. These insights will help to inform interventions in future epidemics.

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UR - http://www.scopus.com/inward/citedby.url?scp=85017439030&partnerID=8YFLogxK

U2 - 10.1038/nature22040

DO - 10.1038/nature22040

M3 - Article

C2 - 28405027

AN - SCOPUS:85017439030

VL - 544

SP - 309

EP - 315

JO - Nature

JF - Nature

SN - 0028-0836

IS - 7650

ER -

Virus genomes reveal factors that spread and sustained the Ebola epidemic

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