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Multiple Zika Introductions Into Florida - Nature

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Genomic epidemiology reveals multiple introductions of Zika virus into the United States

Nature
 
 
doi:10.1038/nature22400
Received
 
Accepted
 
Published online
 
  1. These authors contributed equally to this work.

    • Nathan D. Grubaugh, 
    • Jason T. Ladner, 
    • Moritz U. G. Kraemer, 
    • Gytis Dudas, 
    • Amanda L. Tan,
    • Karthik Gangavarapu, 
    • Michael R. Wiley, 
    • Stephen White & 
    • Julien Thézé
  2. These authors jointly supervised this work.

    • Pardis C. Sabeti, 
    • Leah D. Gillis, 
    • Scott F. Michael, 
    • Trevor Bedford, 
    • Oliver G. Pybus, 
    • Sharon Isern,
    • Gustavo Palacios & 
    • Kristian G. Andersen

Affiliations

  1. Department of Immunology and Microbial Science, The Scripps Research Institute, La Jolla, California 92037, USA

    • Nathan D. Grubaugh,
    •  
    • Karthik Gangavarapu,
    •  
    • Refugio Robles-Sikisaka &
    •  
    • Kristian G. Andersen
  2. Center for Genome Sciences, US Army Medical Research Institute of Infectious Diseases, Fort Detrick, Maryland 21702, USA

    • Jason T. Ladner,
    •  
    • Michael R. Wiley,
    •  
    • Karla Prieto,
    •  
    • Daniel Reyes,
    •  
    • Elyse R. Nagle,
    •  
    • Mariano Sanchez-Lockhart &
    •  
    • Gustavo Palacios
  3. Department of Zoology, University of Oxford, Oxford OX1 3PS, UK

    • Moritz U. G. Kraemer,
    •  
    • Julien Thézé,
    •  
    • Nuno R. Faria &
    •  
    • Oliver G. Pybus
  4. Boston Children’s Hospital, Boston, Massachusetts 02115, USA

    • Moritz U. G. Kraemer
  5. Harvard Medical School, Boston, Massachusetts 02115, USA

    • Moritz U. G. Kraemer
  6. Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, Washington 98109, USA

    • Gytis Dudas &
    •  
    • Trevor Bedford
  7. Department of Biological Sciences, College of Arts and Sciences, Florida Gulf Coast University, Fort Myers, Florida 33965, USA

    • Amanda L. Tan,
    •  
    • Lauren M. Paul,
    •  
    • Carolyn M. Barcellona,
    •  
    • Scott F. Michael &
    •  
    • Sharon Isern
  8. College of Public Health, University of Nebraska Medical Center, Omaha, Nebraska 68198, USA

    • Michael R. Wiley &
    •  
    • Karla Prieto
  9. Bureau of Public Health Laboratories, Division of Disease Control and Health Protection, Florida Department of Health, Miami, Florida 33125, USA

    • Stephen White,
    •  
    • Darryl Pronty &
    •  
    • Leah D. Gillis
  10. Department of Pathology, University of Miami Miller School of Medicine, Miami, Florida 33136, USA

    • Diogo M. Magnani,
    •  
    • Michael J. Ricciardi,
    •  
    • Varian K. Bailey &
    •  
    • David I. Watkins
  11. Department of Pathology and Microbiology, University of Nebraska Medical Center, Omaha, Nebraska 68198, USA

    • Daniel Reyes,
    •  
    • Elyse R. Nagle &
    •  
    • Mariano Sanchez-Lockhart
  12. Bureau of Epidemiology, Division of Disease Control and Health Protection, Florida Department of Health, Tallahassee, Florida 32399, USA

    • Andrea M. Bingham &
    •  
    • Danielle Stanek
  13. Scripps Translational Science Institute, La Jolla, California 92037, USA

    • Glenn Oliveira &
    •  
    • Kristian G. Andersen
  14. The Broad Institute of MIT and Harvard, Cambridge, Massachusetts 02142, USA

    • Hayden C. Metsky,
    •  
    • Mary Lynn Baniecki,
    •  
    • Kayla G. Barnes,
    •  
    • Bridget Chak,
    •  
    • Catherine A. Freije,
    • Adrianne Gladden-Young,
    •  
    • Andreas Gnirke,
    •  
    • Cynthia Luo,
    •  
    • Bronwyn MacInnis,
    •  
    • Christian B. Matranga,
    •  
    • Daniel J. Park,
    •  
    • James Qu,
    •  
    • Stephen F. Schaffner,
    •  
    • Christopher Tomkins-Tinch,
    •  
    • Kendra L. West,
    •  
    • Sarah M. Winnicki,
    •  
    • Shirlee Wohl,
    •  
    • Nathan L. Yozwiak &
    •  
    • Pardis C. Sabeti
  15. Institute of Microbiology and Infection, University of Birmingham, Birmingham B15 2TT, UK

    • Joshua Quick &
    •  
    • Nicholas J. Loman
  16. Department of Microbiology, Immunology, and Pathology, Colorado State University, Fort Collins, Colorado 80523, USA

    • Joseph R. Fauver
  17. Li Ka Shing Knowledge Institute, St Michael’s Hospital, Toronto, Ontario M5B 1T8, Canada

    • Kamran Khan &
    •  
    • Shannon E. Brent
  18. Division of Infectious Diseases, Department of Medicine, University of Toronto, Toronto, Ontario M5S 1A8, Canada

    • Kamran Khan
  19. Institute for Health Metrics and Evaluation, University of Washington, Seattle, Washington 98121, USA

    • Robert C. Reiner Jr
  20. Division of Infectious Diseases, University of Miami Miller School of Medicine, Miami, Florida 33136, USA

    • Paola N. Lichtenberger
  21. Bureau of Public Health Laboratories, Division of Disease Control and Health Protection, Florida Department of Health, Tampa, Florida 33612, USA

    • Marshall R. Cone,
    •  
    • Edgar W. Kopp IV,
    •  
    • Kelly N. Hogan &
    •  
    • Andrew C. Cannons
  22. Florida Department of Health in Miami-Dade County, Miami, Florida 33125, USA

    • Reynald Jean
  23. National Center for Atmospheric Research, Boulder, Colorado 80307, USA

    • Andrew J. Monaghan
  24. Department of Microbiology and Immunology, Tulane University School of Medicine, New Orleans, Louisiana 70112, USA

    • Robert F. Garry
  25. Miami-Dade County Mosquito Control, Miami, Florida 33178, USA

    • Mario C. Porcelli &
    •  
    • Chalmers Vasquez
  26. Department of Biology and Emerging Pathogens Institute, University of Florida, Gainesville, Florida 32610, USA

    • Derek A. T. Cummings
  27. Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3FL, UK

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

    • Andrew Rambaut
  29. Center for Systems Biology, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, Massachusetts 02138, USA

    • Pardis C. Sabeti
  30. Department of Immunology and Infectious Diseases, Harvard T.H. Chan School of Public Health, Harvard University, Boston, Massachusetts 02115, USA

    • Pardis C. Sabeti
  31. Howard Hughes Medical Institute, Chevy Chase, Maryland 20815, USA

    • Pardis C. Sabeti
  32. Department of Integrative Structural and Computational Biology, The Scripps Research Institute, La Jolla, California 92037, USA

    • Kristian G. Andersen

Contributions

All contributions are listed in order of authorship. Designed the experiments: N.D.G., J.T.L., G.D., M.U.G.K., D.A.T.C., P.C.S., L.D.G., S.F.M., T.B., O.G.P., S.I., G.P., and K.G.A. Collected samples: A.L.T., S.W., D.M.M., A.M.B., L.M.P., D.P., C.M.B., P.N.L., M.J.R., V.K.B., D.I.W., M.R.C., E.W.K., K.N.H., A.C.C., R.J., M.C.P., C.V., D.S., L.D.G., S.F.M., and S.I. Performed the sequencing: N.D.G., M.R.W., K.P., D.R., R.R.-S., G.O., and E.R.N. Provided data, reagents, or protocols: N.D.G., J.T.L., G.D., M.U.G.K., K.G., M.R.W., R.R.-S., G.O., H.C.M., M.L.B., K.G.B., B.C., C.A.F., A.G.-Y., A.G., C.L., B.M., C.B.M., D.J.P., J. Q.U, S.F.S., C.T.-T., K.L.W., S.M.W., S.W., N.L.Y., J.Qui., J.R.F., K.K., S.E.B., A.J.M., R.F.G., N.J.L., M.C.P., C.V., P.C.S., S.F.M., and S.I. Analysed the data: N.D.G., J.T.L., G.D., M.U.G.K., K.G., J.T., J.R.F., R.C.R., N.R.F., D.A.T.C., A.R., M.S.-L., T.B., S.F.M, O.G.P., S.I., and K.G.A. Edited manuscript: G.D., M.U.G.K., J.T., S.F.S., A.R., T.B., O.G.P., S.I., and G.P. Wrote manuscript: N.D.G., J.T.L., and K.G.A. All authors read and approved the manuscript.

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Zika virus (ZIKV) is causing an unprecedented epidemic linked to severe congenital abnormalities1, 2. In July 2016, mosquito-borne ZIKV transmission was reported in the continental United States; since then, hundreds of locally acquired infections have been reported in Florida3, 4. To gain insights into the timing, source, and likely route(s) of ZIKV introduction, we tracked the virus from its first detection in Florida by sequencing ZIKV genomes from infected patients and Aedes aegypti mosquitoes. We show that at least 4 introductions, but potentially as many as 40, contributed to the outbreak in Florida and that local transmission is likely to have started in the spring of 2016—several months before its initial detection. By analysing surveillance and genetic data, we show that ZIKV moved among transmission zones in Miami. Our analyses show that most introductions were linked to the Caribbean, a finding corroborated by the high incidence rates and traffic volumes from the region into the Miami area. Our study provides an understanding of how ZIKV initiates transmission in new regions.

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