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Virus genomes reveal factors that spread and sustained the Ebola epidemic

Author

Listed:
  • Gytis Dudas

    (Institute of Evolutionary Biology, University of Edinburgh
    Fred Hutchinson Cancer Research Center)

  • Luiz Max Carvalho

    (Institute of Evolutionary Biology, University of Edinburgh)

  • Trevor Bedford

    (Fred Hutchinson Cancer Research Center)

  • Andrew J. Tatem

    (WorldPop, University of Southampton
    Flowminder Foundation)

  • Guy Baele

    (Rega Institute, KU Leuven – University of Leuven)

  • Nuno R. Faria

    (University of Oxford)

  • Daniel J. Park

    (Broad Institute of Harvard and MIT)

  • Jason T. Ladner

    (Center for Genome Sciences, US Army Medical Research Institute of Infectious Diseases)

  • Armando Arias

    (University of Cambridge, Addenbrooke’s Hospital
    National Veterinary Institute, Technical University of Denmark)

  • Danny Asogun

    (Institute of Lassa Fever Research and Control, Irrua Specialist Teaching Hospital
    The European Mobile Laboratory Consortium)

  • Filip Bielejec

    (Rega Institute, KU Leuven – University of Leuven)

  • Sarah L. Caddy

    (University of Cambridge, Addenbrooke’s Hospital)

  • Matthew Cotten

    (Virus Genomics, Wellcome Trust Sanger Institute
    Erasmus University Medical Centre)

  • Jonathan D’Ambrozio

    (Center for Genome Sciences, US Army Medical Research Institute of Infectious Diseases)

  • Simon Dellicour

    (Rega Institute, KU Leuven – University of Leuven)

  • Antonino Di Caro

    (The European Mobile Laboratory Consortium
    National Institute for Infectious Diseases ‘L. Spallanzani’—IRCCS)

  • Joseph W. Diclaro

    (Naval Medical Research Unit 3)

  • Sophie Duraffour

    (The European Mobile Laboratory Consortium
    Bernhard Nocht Institute for Tropical Medicine)

  • Michael J. Elmore

    (National Infections Service, Public Health England)

  • Lawrence S. Fakoli

    (Liberian Institute for Biomedical Research)

  • Ousmane Faye

    (Institut Pasteur de Dakar, Arbovirus and Viral Hemorrhagic Fever Unit)

  • Merle L. Gilbert

    (Center for Genome Sciences, US Army Medical Research Institute of Infectious Diseases)

  • Sahr M. Gevao

    (University of Sierra Leone)

  • Stephen Gire

    (Broad Institute of Harvard and MIT
    Center for Systems Biology, Harvard University)

  • Adrianne Gladden-Young

    (Broad Institute of Harvard and MIT)

  • Andreas Gnirke

    (Broad Institute of Harvard and MIT)

  • Augustine Goba

    (Viral Hemorrhagic Fever Program, Kenema Government Hospital
    Ministry of Health and Sanitation)

  • Donald S. Grant

    (Viral Hemorrhagic Fever Program, Kenema Government Hospital
    Ministry of Health and Sanitation)

  • Bart L. Haagmans

    (Erasmus University Medical Centre)

  • Julian A. Hiscox

    (Institute of Infection and Global Health, University of Liverpool
    NIHR Health Protection Research Unit in Emerging and Zoonotic Infections, University of Liverpool)

  • Umaru Jah

    (University of Makeni)

  • Jeffrey R. Kugelman

    (Center for Genome Sciences, US Army Medical Research Institute of Infectious Diseases)

  • Di Liu

    (Institute of Microbiology, Chinese Academy of Sciences)

  • Jia Lu

    (University of Cambridge, Addenbrooke’s Hospital)

  • Christine M. Malboeuf

    (Broad Institute of Harvard and MIT)

  • Suzanne Mate

    (Center for Genome Sciences, US Army Medical Research Institute of Infectious Diseases)

  • David A. Matthews

    (University of Bristol)

  • Christian B. Matranga

    (Broad Institute of Harvard and MIT)

  • Luke W. Meredith

    (University of Cambridge, Addenbrooke’s Hospital
    University of Makeni)

  • James Qu

    (Broad Institute of Harvard and MIT)

  • Joshua Quick

    (Institute of Microbiology and Infection, University of Birmingham)

  • Suzan D. Pas

    (Erasmus University Medical Centre)

  • My V. T. Phan

    (Virus Genomics, Wellcome Trust Sanger Institute
    Erasmus University Medical Centre)

  • Georgios Pollakis

    (Institute of Infection and Global Health, University of Liverpool)

  • Chantal B. Reusken

    (Erasmus University Medical Centre)

  • Mariano Sanchez-Lockhart

    (Center for Genome Sciences, US Army Medical Research Institute of Infectious Diseases
    University of Nebraska Medical Center)

  • Stephen F. Schaffner

    (Broad Institute of Harvard and MIT)

  • John S. Schieffelin

    (Section of Infectious Diseases)

  • Rachel S. Sealfon

    (Broad Institute of Harvard and MIT
    Center for Computational Biology, Flatiron Institute
    Lewis-Sigler Institute for Integrative Genomics, Princeton University)

  • Etienne Simon-Loriere

    (Institut Pasteur, Functional Genetics of Infectious Diseases Unit
    Génétique Fonctionelle des Maladies Infectieuses)

  • Saskia L. Smits

    (Erasmus University Medical Centre)

  • Kilian Stoecker

    (The European Mobile Laboratory Consortium
    Bundeswehr Institute of Microbiology)

  • Lucy Thorne

    (University of Cambridge, Addenbrooke’s Hospital)

  • Ekaete Alice Tobin

    (Institute of Lassa Fever Research and Control, Irrua Specialist Teaching Hospital
    The European Mobile Laboratory Consortium)

  • Mohamed A. Vandi

    (Viral Hemorrhagic Fever Program, Kenema Government Hospital
    Ministry of Health and Sanitation)

  • Simon J. Watson

    (Virus Genomics, Wellcome Trust Sanger Institute)

  • Kendra West

    (Broad Institute of Harvard and MIT)

  • Shannon Whitmer

    (Viral Special Pathogens Branch, Centers for Disease Control and Prevention)

  • Michael R. Wiley

    (Center for Genome Sciences, US Army Medical Research Institute of Infectious Diseases
    University of Nebraska Medical Center)

  • Sarah M. Winnicki

    (Broad Institute of Harvard and MIT
    Section of Infectious Diseases)

  • Shirlee Wohl

    (Broad Institute of Harvard and MIT
    Center for Systems Biology, Harvard University)

  • Roman Wölfel

    (The European Mobile Laboratory Consortium
    Bundeswehr Institute of Microbiology)

  • Nathan L. Yozwiak

    (Broad Institute of Harvard and MIT
    Center for Systems Biology, Harvard University)

  • Kristian G. Andersen

    (The Scripps Research Institute
    Scripps Translational Science Institute)

  • Sylvia O. Blyden

    (Ministry of Social Welfare, Gender and Children’s Affairs)

  • Fatorma Bolay

    (Liberian Institute for Biomedical Research)

  • Miles W. Carroll

    (The European Mobile Laboratory Consortium
    National Infections Service, Public Health England
    NIHR Health Protection Research Unit in Emerging and Zoonotic Infections, University of Liverpool
    University of Southampton, South General Hospital)

  • Bernice Dahn

    (Minstry of Health Liberia)

  • Boubacar Diallo

    (World Health Organization)

  • Pierre Formenty

    (World Health Organization)

  • Christophe Fraser

    (Oxford Big Data Institute, Li Ka Shing Centre for Health Information and Discovery, University of Oxford)

  • George F. Gao

    (Institute of Microbiology, Chinese Academy of Sciences
    Chinese Center for Disease Control and Prevention (China CDC))

  • Robert F. Garry

    (Department of Microbiology and Immunology)

  • Ian Goodfellow

    (University of Cambridge, Addenbrooke’s Hospital
    University of Makeni)

  • Stephan Günther

    (The European Mobile Laboratory Consortium
    Bernhard Nocht Institute for Tropical Medicine)

  • Christian T. Happi

    (Redeemer’s University
    African Center of Excellence for Genomics of Infectious Diseases (ACEGID), Redeemer’s University)

  • Edward C. Holmes

    (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)

  • Brima Kargbo

    (Ministry of Health and Sanitation)

  • Sakoba Keïta

    (Ministry of Health Guinea)

  • Paul Kellam

    (Virus Genomics, Wellcome Trust Sanger Institute
    Faculty of Medicine, Imperial College London)

  • Marion P. G. Koopmans

    (Erasmus University Medical Centre)

  • Jens H. Kuhn

    (Integrated Research Facility at Fort Detrick, National Institute of Allergy and Infectious Diseases, National Institutes of Health, B-8200 Research Plaza)

  • Nicholas J. Loman

    (Institute of Microbiology and Infection, University of Birmingham)

  • N’Faly Magassouba

    (Université Gamal Abdel Nasser de Conakry, Laboratoire des Fièvres Hémorragiques en Guinée)

  • Dhamari Naidoo

    (World Health Organization)

  • Stuart T. Nichol

    (Viral Special Pathogens Branch, Centers for Disease Control and Prevention)

  • Tolbert Nyenswah

    (Minstry of Health Liberia)

  • Gustavo Palacios

    (Center for Genome Sciences, US Army Medical Research Institute of Infectious Diseases)

  • Oliver G. Pybus

    (University of Oxford)

  • Pardis C. Sabeti

    (Broad Institute of Harvard and MIT
    Center for Systems Biology, Harvard University)

  • Amadou Sall

    (Institut Pasteur de Dakar, Arbovirus and Viral Hemorrhagic Fever Unit)

  • Ute Ströher

    (Viral Special Pathogens Branch, Centers for Disease Control and Prevention)

  • Isatta Wurie

    (University of Sierra Leone)

  • Marc A. Suchard

    (UCLA Fielding School of Public Health, University of California
    University of California
    David Geffen School of Medicine at UCLA, University of California)

  • Philippe Lemey

    (Rega Institute, KU Leuven – University of Leuven)

  • Andrew Rambaut

    (Institute of Evolutionary Biology, University of Edinburgh
    Centre for Immunology, Infection and Evolution, University of Edinburgh
    Fogarty International Center, National Institutes of Health)

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.

Suggested Citation

  • 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 & Mat, 2017. "Virus genomes reveal factors that spread and sustained the Ebola epidemic," Nature, Nature, vol. 544(7650), pages 309-315, April.
    • Handle: RePEc:nat:nature:v:544:y:2017:i:7650:d:10.1038_nature22040
    DOI: 10.1038/nature22040
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    Cited by:

    1. Jennifer L. Havens & Sébastien Calvignac-Spencer & Kevin Merkel & Sonia Burrel & David Boutolleau & Joel O. Wertheim, 2022. "Phylogeographic analysis reveals an ancient East African origin of human herpes simplex virus 2 dispersal out-of-Africa," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    2. Jessica E. Stockdale & Kurnia Susvitasari & Paul Tupper & Benjamin Sobkowiak & Nicola Mulberry & Anders Gonçalves da Silva & Anne E. Watt & Norelle L. Sherry & Corinna Minko & Benjamin P. Howden & Cou, 2023. "Genomic epidemiology offers high resolution estimates of serial intervals for COVID-19," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Yao-Tsun Li & Hui-Ying Ko & Joseph Hughes & Ming-Tsan Liu & Yi-Ling Lin & Katie Hampson & Kirstyn Brunker, 2024. "From emergence to endemicity of highly pathogenic H5 avian influenza viruses in Taiwan," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    4. Jonathon D. Gass & Nichola J. Hill & Lambodhar Damodaran & Elena N. Naumova & Felicia B. Nutter & Jonathan A. Runstadler, 2023. "Ecogeographic Drivers of the Spatial Spread of Highly Pathogenic Avian Influenza Outbreaks in Europe and the United States, 2016–Early 2022," IJERPH, MDPI, vol. 20(11), pages 1-17, June.
    5. Yankuo Sun & Jiabao Xing & Samuel L. Hong & Nena Bollen & Sijia Xu & Yue Li & Jianhao Zhong & Xiaopeng Gao & Dihua Zhu & Jing Liu & Lang Gong & Lei Zhou & Tongqing An & Mang Shi & Heng Wang & Guy Bael, 2024. "Untangling lineage introductions, persistence and transmission drivers of HP-PRRSV sublineage 8.7," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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