Article | Published:

Virus genomes reveal factors that spread and sustained the Ebola epidemic

Nature volume 544, pages 309315 (20 April 2017) | Download Citation

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.

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Acknowledgements

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.

Author information

Affiliations

  1. Institute of Evolutionary Biology, University of Edinburgh, King’s Buildings, Edinburgh EH9 3FL, UK

    • Gytis Dudas
    • , Luiz Max Carvalho
    •  & Andrew Rambaut
  2. Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, Washington 98109, USA

    • Gytis Dudas
    •  & Trevor Bedford
  3. WorldPop, Department of Geography and Environment, University of Southampton, Highfield, Southampton SO17 1BJ, UK

    • Andrew J. Tatem
  4. Flowminder Foundation, Stockholm, Sweden

    • Andrew J. Tatem
  5. Department of Microbiology and Immunology, Rega Institute, KU Leuven – University of Leuven, 3000 Leuven, Belgium

    • Guy Baele
    • , Filip Bielejec
    • , Simon Dellicour
    •  & Philippe Lemey
  6. Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK

    • Nuno R. Faria
    •  & Oliver G. Pybus
  7. Broad Institute of Harvard and MIT, Cambridge, Massachusetts 02142, USA

    • Daniel J. Park
    • , Stephen Gire
    • , Adrianne Gladden-Young
    • , Andreas Gnirke
    • , Christine M. Malboeuf
    • , Christian B. Matranga
    • , James Qu
    • , Stephen F. Schaffner
    • , Rachel S. Sealfon
    • , Kendra West
    • , Sarah M. Winnicki
    • , Shirlee Wohl
    • , Nathan L. Yozwiak
    •  & Pardis C. Sabeti
  8. Center for Genome Sciences, US Army Medical Research Institute of Infectious Diseases, Fort Detrick, Frederick, Maryland 21702, USA

    • Jason T. Ladner
    • , Jonathan D’Ambrozio
    • , Merle L. Gilbert
    • , Jeffrey R. Kugelman
    • , Suzanne Mate
    • , Mariano Sanchez-Lockhart
    • , Michael R. Wiley
    •  & Gustavo Palacios
  9. Department of Pathology, University of Cambridge, Addenbrooke’s Hospital, Cambridge CB2 2QQ, UK

    • Armando Arias
    • , Sarah L. Caddy
    • , Jia Lu
    • , Luke W. Meredith
    • , Lucy Thorne
    •  & Ian Goodfellow
  10. National Veterinary Institute, Technical University of Denmark, Bülowsvej 27, 1870, Frederiksberg C, Denmark

    • Armando Arias
  11. Institute of Lassa Fever Research and Control, Irrua Specialist Teaching Hospital, Irrua, Nigeria

    • Danny Asogun
    •  & Ekaete Alice Tobin
  12. The European Mobile Laboratory Consortium, 20359 Hamburg, Germany

    • Danny Asogun
    • , Antonino Di Caro
    • , Sophie Duraffour
    • , Kilian Stoecker
    • , Ekaete Alice Tobin
    • , Roman Wölfel
    • , Miles W. Carroll
    •  & Stephan Günther
  13. Virus Genomics, Wellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, UK

    • Matthew Cotten
    • , My V. T. Phan
    • , Simon J. Watson
    •  & Paul Kellam
  14. Department of Viroscience, Erasmus University Medical Centre, PO Box 2040, 300 CA Rotterdam, the Netherlands

    • Matthew Cotten
    • , Bart L. Haagmans
    • , Suzan D. Pas
    • , My V. T. Phan
    • , Chantal B. Reusken
    • , Saskia L. Smits
    •  & Marion P. G. Koopmans
  15. National Institute for Infectious Diseases ‘L. Spallanzani’—IRCCS, Via Portuense 292, 00149 Rome, Italy

    • Antonino Di Caro
  16. Naval Medical Research Unit 3, 3A Imtidad Ramses Street, Cairo 11517, Egypt

    • Joseph W. Diclaro
  17. Bernhard Nocht Institute for Tropical Medicine, 20359 Hamburg, Germany

    • Sophie Duraffour
    •  & Stephan Günther
  18. National Infections Service, Public Health England, Porton Down, Salisbury, Wilts SP4 0JG, UK

    • Michael J. Elmore
    •  & Miles W. Carroll
  19. Liberian Institute for Biomedical Research, Charlesville, Liberia

    • Lawrence S. Fakoli
    •  & Fatorma Bolay
  20. Institut Pasteur de Dakar, Arbovirus and Viral Hemorrhagic Fever Unit, 36 Avenue Pasteur, BP 220, Dakar, Sénégal

    • Ousmane Faye
    •  & Amadou Sall
  21. University of Sierra Leone, Freetown, Sierra Leone

    • Sahr M. Gevao
    •  & Isatta Wurie
  22. Center for Systems Biology, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA

    • Stephen Gire
    • , Shirlee Wohl
    • , Nathan L. Yozwiak
    •  & Pardis C. Sabeti
  23. Viral Hemorrhagic Fever Program, Kenema Government Hospital, 1 Combema Road, Kenema, Sierra Leone

    • Augustine Goba
    • , Donald S. Grant
    •  & Mohamed A. Vandi
  24. Ministry of Health and Sanitation, 4th Floor Youyi Building, Freetown, Sierra Leone

    • Augustine Goba
    • , Donald S. Grant
    • , Mohamed A. Vandi
    •  & Brima Kargbo
  25. Institute of Infection and Global Health, University of Liverpool, Liverpool L69 2BE, UK

    • Julian A. Hiscox
    •  & Georgios Pollakis
  26. NIHR Health Protection Research Unit in Emerging and Zoonotic Infections, University of Liverpool, Liverpool L69 3GL, UK

    • Julian A. Hiscox
    •  & Miles W. Carroll
  27. University of Makeni, Makeni, Sierra Leone

    • Umaru Jah
    • , Luke W. Meredith
    •  & Ian Goodfellow
  28. Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, China

    • Di Liu
    •  & George F. Gao
  29. University of Bristol, Bristol BS8 1TD, UK

    • David A. Matthews
  30. Institute of Microbiology and Infection, University of Birmingham, Birmingham B15 2TT, UK

    • Joshua Quick
    •  & Nicholas J. Loman
  31. University of Nebraska Medical Center, Omaha, Nebraska 68198, USA

    • Mariano Sanchez-Lockhart
    •  & Michael R. Wiley
  32. Department of Pediatrics, Section of Infectious Diseases, New Orleans, Louisiana 70112, USA

    • John S. Schieffelin
    •  & Sarah M. Winnicki
  33. Center for Computational Biology, Flatiron Institute, New York, New York 10010, USA

    • Rachel S. Sealfon
  34. Lewis-Sigler Institute for Integrative Genomics, Princeton University, Princeton, New Jersey 08544, USA

    • Rachel S. Sealfon
  35. Institut Pasteur, Functional Genetics of Infectious Diseases Unit, 28 rue du Docteur Roux, 75724 Paris Cedex 15, France

    • Etienne Simon-Loriere
  36. Génétique Fonctionelle des Maladies Infectieuses, CNRS URA3012, Paris 75015, France

    • Etienne Simon-Loriere
  37. Bundeswehr Institute of Microbiology, Neuherbergstrasse 11, 80937 Munich, Germany

    • Kilian Stoecker
    •  & Roman Wölfel
  38. Viral Special Pathogens Branch, Centers for Disease Control and Prevention, 1600 Clifton Road NE, Atlanta, Georgia 30333, USA

    • Shannon Whitmer
    • , Stuart T. Nichol
    •  & Ute Ströher
  39. The Scripps Research Institute, Department of Immunology and Microbial Science, La Jolla, California 92037, USA

    • Kristian G. Andersen
  40. Scripps Translational Science Institute, La Jolla, California 92037, USA

    • Kristian G. Andersen
  41. Ministry of Social Welfare, Gender and Children’s Affairs, New Englandville, Freetown, Sierra Leone

    • Sylvia O. Blyden
  42. University of Southampton, South General Hospital, Southampton SO16 6YD, UK

    • Miles W. Carroll
  43. Minstry of Health Liberia, Monrovia, Liberia

    • Bernice Dahn
    •  & Tolbert Nyenswah
  44. World Health Organization, Conakry, Guinea

    • Boubacar Diallo
  45. World Health Organization, Geneva, Switzerland

    • Pierre Formenty
    •  & Dhamari Naidoo
  46. Oxford Big Data Institute, Li Ka Shing Centre for Health Information and Discovery, Nuffield Department of Medicine, University of Oxford, Oxford OX3 7FZ, UK

    • Christophe Fraser
  47. Chinese Center for Disease Control and Prevention (China CDC), Beijing 102206, China

    • George F. Gao
  48. Department of Microbiology and Immunology, New Orleans, Louisiana 70112, USA

    • Robert F. Garry
  49. Department of Biological Sciences, Redeemer’s University, Ede, Osun State, Nigeria

    • Christian T. Happi
  50. African Center of Excellence for Genomics of Infectious Diseases (ACEGID), Redeemer’s University, Ede, Osun State, Nigeria

    • Christian T. Happi
  51. Marie Bashir Institute for Infectious Diseases and Biosecurity, Charles Perkins Centre, School of Life and Environmental Sciences and Sydney Medical School, the University of Sydney, Sydney, New South Wales 2006, Australia

    • Edward C. Holmes
  52. Ministry of Health Guinea, Conakry, Guinea

    • Sakoba Keïta
  53. Division of Infectious Diseases, Faculty of Medicine, Imperial College London, London W2 1PG, UK

    • Paul Kellam
  54. Integrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious Diseases, National Institutes of Health, B-8200 Research Plaza, Fort Detrick, Frederick, Maryland 21702, USA

    • Jens H. Kuhn
  55. Université Gamal Abdel Nasser de Conakry, Laboratoire des Fièvres Hémorragiques en Guinée, Conakry, Guinea

    • N’Faly Magassouba
  56. Department of Biostatistics, UCLA Fielding School of Public Health, University of California, Los Angeles, California 90095, USA

    • Marc A. Suchard
  57. Department of Biomathematics David Geffen School of Medicine at UCLA, University of California, Los Angeles, California 90095, USA

    • Marc A. Suchard
  58. Department of Human Genetics, David Geffen School of Medicine at UCLA, University of California, Los Angeles, California 90095, USA

    • Marc A. Suchard
  59. Centre for Immunology, Infection and Evolution, University of Edinburgh, King’s Buildings, Edinburgh, EH9 3FL, UK

    • Andrew Rambaut
  60. Fogarty International Center, National Institutes of Health, Bethesda, Maryland 20892, USA

    • Andrew Rambaut

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Contributions

G.D., L.M.C., T.B., C.F., M.A.S., P.L. and A.R. designed the study. G.D., L.M.C., T.B., A.J.T., G.B., P.L. and A.R. performed the analysis. G.D., T.B., M.A.S, P.L. and A.R. wrote the manuscript. L.M.C., A.J.T., G.B., N.R.F., J.T.L., M.C., S.F.S., K.G.A., M.W.C., R.F.G., I.G., E.C.H., P.K., M.P.G.K., J.H.K., S.T.N., G.Pa., O.G.P., P.C.S. and U.S. edited the manuscript. The other authors were critical for the coordination, collection, processing of virus samples or the sequencing and bioinformatics of virus genomes. All authors read and approved the contents of the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Gytis Dudas or Philippe Lemey or Andrew Rambaut.

Reviewer Information Nature thanks R. Biek, C. Viboud, M. Worobey and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Extended data

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    Supplementary Table

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Videos

  1. 1.

    Video 1: Reconstructed history of the West African Ebola virus epidemic

    Map of the three most affected countries - Guinea, Liberia and Sierra Leone - is shown on the left. Colours indicate country - Guinea is green, Liberia is red and Sierra Leone is blue. Weekly incidence of EVD cases is indicated by shading of administrative divisions (darker shades correspond to more cases, on a logarithmic scale) within each country. Cases are linearly interpolated between successive reporting weeks. Inferred movements of Ebola virus are indicated with tapered projectiles, coloured by its origin country (Guinea in green, Sierra Leone in blue, Liberia in red) if lineage is crossing an international border and black otherwise. Red circles at population centroids of each administrative division indicate the number of lineages estimated to be present within the location. Phylogenetic tree in the upper right shows the relationships between sampled Ebola lineages, with branches coloured by location (lighter shades indicate locations further west within each country). Migrations inferred between any two locations in the tree are animated on the map on the left. Plot on the lower right shows the sum of weekly cases reported for each administrative division, for each individual country (Guinea in green, Sierra Leone in blue, Liberia in red). Weekly cases for individual administrative divisions are animated as changes in administrative division's colour on the map on the left.

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https://doi.org/10.1038/nature22040

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