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Epidemic establishment and cryptic transmission of Zika virus in Brazil and the Americas

View ORCID ProfileN. R. Faria, J. Quick, I. Morales, J. Thézé, J.G. Jesus, M. Giovanetti, M. U. G. Kraemer, S. C. Hill, A. Black, A. C. da Costa, L.C. Franco, S. P. Silva, C.-H. Wu, J. Raghwani, S. Cauchemez, L. du Plessis, M. P. Verotti, W. K. de Oliveira, E. H. Carmo, G. E. Coelho, A. C. F. S. Santelli, L. C. Vinhal, C. M. Henriques, J. T. Simpson, M. Loose, K. G. Andersen, N. D. Grubaugh, S. Somasekar, C. Y. Chiu, J. E. Muñoz-Medina, C. R. Gonzalez-Bonilla, C. F. Arias, L. L. Lewis-Ximenez, S.A. Baylis, A. O. Chieppe, S. F. Aguiar, C. A. Fernandes, P. S. Lemos, B. L. S. Nascimento, H. A. O. Monteiro, I. C. Siqueira, M. G. de Queiroz, T. R. de Souza, J. F. Bezerra, M. R. Lemos, G. F. Pereira, D. Loudal, L. C. Moura, R. Dhalia, R. F. França, T. Magalhães, E. T. Marques Jr., T. Jaenisch, G. L. Wallau, M. C. de Lima, V. Nascimento, E. M. de Cerqueira, M. M. de Lima, D. L. Mascarenhas, J. P. Moura Neto, A. S. Levin, T. R. Tozetto-Mendoza, S. N. Fonseca, M. C. Mendes-Correa, F.P. Milagres, A. Segurado, E. C. Holmes, A. Rambaut, T. Bedford, M. R. T. Nunes, E. C. Sabino, L. C. J. Alcantara, N. Loman, O. G. Pybus
doi: https://doi.org/10.1101/105171
N. R. Faria
1Department of Zoology, University of Oxford, Oxford OX3 1PS, UK
2Evandro Chagas Institute, Ministry of Health, Ananindeua, Brazil
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  • ORCID record for N. R. Faria
J. Quick
3Institute of Microbiology and Infection, University of Birmingham, UK
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I. Morales
4Department of Infectious Disease, School of Medicine & Institute of Tropical Medicine, University of São Paulo, Brazil
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J. Thézé
1Department of Zoology, University of Oxford, Oxford OX3 1PS, UK
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J.G. Jesus
5Fundação Oswaldo Cruz (FIOCRUZ), Salvador, Bahia, Brazil
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M. Giovanetti
5Fundação Oswaldo Cruz (FIOCRUZ), Salvador, Bahia, Brazil
6University of Rome Tor Vergata, Rome, Italy
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M. U. G. Kraemer
1Department of Zoology, University of Oxford, Oxford OX3 1PS, UK
7Harvard Medical School, Boston, MA, USA
8Boston Children’s Hospital, Boston, MA, USA
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S. C. Hill
1Department of Zoology, University of Oxford, Oxford OX3 1PS, UK
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A. Black
9Vaccine and Infectious Disease Division, Fred Hutchinson Cancer Research Center, Seattle, WA, USA
10Department of Epidemiology, University of Washington, Seattle, WA, USA
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A. C. da Costa
3Institute of Microbiology and Infection, University of Birmingham, UK
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L.C. Franco
2Evandro Chagas Institute, Ministry of Health, Ananindeua, Brazil
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S. P. Silva
2Evandro Chagas Institute, Ministry of Health, Ananindeua, Brazil
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C.-H. Wu
11Department of Statistics, University of Oxford, Oxford OX3 1PS, UK
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J. Raghwani
1Department of Zoology, University of Oxford, Oxford OX3 1PS, UK
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S. Cauchemez
12Mathematical Modelling of Infectious Diseases and Center of Bioinformatics, Biostatistics and Integrative Biology, Institut Pasteur, Paris, France
13Centre National de la Recherche Scientifique, URA3012, Paris, France
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L. du Plessis
1Department of Zoology, University of Oxford, Oxford OX3 1PS, UK
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M. P. Verotti
14Coordenação dos Laboratórios de Saúde (CGLAB/DEVIT/SVS), Ministry of Health, Brasília, Brazil
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W. K. de Oliveira
15Coordenação Geral de Vigilância e Resposta às Emergências em Saúde Pública (CGVR/DEVIT), Ministry of Health, Brasília, Brazil
16Center of Data and Knowledge Integration for Health (CIDACS), Fundação Oswaldo Cruz (FIOCRUZ), Brazil
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E. H. Carmo
17Departamento de Vigilância das Doenças Transmissíveis, Ministry of Health, Brasilia, Brazil
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G. E. Coelho
18, Brasília, Brazil
19Pan American Health Organization (PAHO), Buenos Aires, Argentina
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A. C. F. S. Santelli
18, Brasília, Brazil
20Fundação Oswaldo Cruz (FIOCRUZ), Rio de Janeiro, Brazil
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L. C. Vinhal
18, Brasília, Brazil
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C. M. Henriques
17Departamento de Vigilância das Doenças Transmissíveis, Ministry of Health, Brasilia, Brazil
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J. T. Simpson
21Ontario Institute for Cancer Research, Toronto, Canada
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M. Loose
22University of Nottingham, Nottingham, UK
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K. G. Andersen
23Department of Immunology and Microbial Science, The Scripps Research Institute, La Jolla, CA 92037, USA
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N. D. Grubaugh
23Department of Immunology and Microbial Science, The Scripps Research Institute, La Jolla, CA 92037, USA
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S. Somasekar
24Departments of Laboratory Medicine and Medicine & Infectious Diseases, University of California, San Francisco, USA
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C. Y. Chiu
24Departments of Laboratory Medicine and Medicine & Infectious Diseases, University of California, San Francisco, USA
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J. E. Muñoz-Medina
25División de Laboratorios de Vigilancia e Investigación Epidemiológica, Instituto Mexicano del Seguro Social, Ciudad de México, Mexico
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C. R. Gonzalez-Bonilla
25División de Laboratorios de Vigilancia e Investigación Epidemiológica, Instituto Mexicano del Seguro Social, Ciudad de México, Mexico
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C. F. Arias
26Instituto de Biotecnología, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
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L. L. Lewis-Ximenez
27Instituto Oswaldo Cruz (FIOCRUZ), Rio de Janeiro, Brazil
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S.A. Baylis
28Paul-Ehrlich-Institut, Langen, Germany
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A. O. Chieppe
29Laboratório Central de Saúde Pública Noel Nutels, Rio de Janeiro, Brazil
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29Laboratório Central de Saúde Pública Noel Nutels, Rio de Janeiro, Brazil
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29Laboratório Central de Saúde Pública Noel Nutels, Rio de Janeiro, Brazil
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P. S. Lemos
2Evandro Chagas Institute, Ministry of Health, Ananindeua, Brazil
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B. L. S. Nascimento
2Evandro Chagas Institute, Ministry of Health, Ananindeua, Brazil
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H. A. O. Monteiro
2Evandro Chagas Institute, Ministry of Health, Ananindeua, Brazil
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I. C. Siqueira
5Fundação Oswaldo Cruz (FIOCRUZ), Salvador, Bahia, Brazil
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M. G. de Queiroz
30Laboratório Central de Saúde Pública do Estado do Rio Grande do Norte, Natal, Brazil
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T. R. de Souza
30Laboratório Central de Saúde Pública do Estado do Rio Grande do Norte, Natal, Brazil
31Universidade Potiguar do Rio Grande do Norte, Natal, Brazil
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J. F. Bezerra
30Laboratório Central de Saúde Pública do Estado do Rio Grande do Norte, Natal, Brazil
32Faculdade Natalense de Ensino e Cultura, Rio Grande do Norte, Natal, Brazil
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M. R. Lemos
33Laboratório Central de Saúde Pública do Estado da Paraíba, João Pessoa, Brazil
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G. F. Pereira
33Laboratório Central de Saúde Pública do Estado da Paraíba, João Pessoa, Brazil
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D. Loudal
33Laboratório Central de Saúde Pública do Estado da Paraíba, João Pessoa, Brazil
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L. C. Moura
33Laboratório Central de Saúde Pública do Estado da Paraíba, João Pessoa, Brazil
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R. Dhalia
34Fundação Oswaldo Cruz (FIOCRUZ), Recife, Pernambuco, Brazil
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R. F. França
34Fundação Oswaldo Cruz (FIOCRUZ), Recife, Pernambuco, Brazil
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T. Magalhães
34Fundação Oswaldo Cruz (FIOCRUZ), Recife, Pernambuco, Brazil
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E. T. Marques Jr.
34Fundação Oswaldo Cruz (FIOCRUZ), Recife, Pernambuco, Brazil
35Center for Vaccine Research, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA, USA
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T. Jaenisch
36Section Clinical Tropical Medicine, Department for Infectious Diseases, Heidelberg University Hospital, Heidelberg, Germany
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G. L. Wallau
34Fundação Oswaldo Cruz (FIOCRUZ), Recife, Pernambuco, Brazil
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M. C. de Lima
37Laboratório Central de Saúde Pública do Estado de Alagoas, Maceió, Brazil
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V. Nascimento
37Laboratório Central de Saúde Pública do Estado de Alagoas, Maceió, Brazil
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E. M. de Cerqueira
38Universidade Estadual de Feira de Santana, Feira de Santana, Bahia, Brazil
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M. M. de Lima
38Universidade Estadual de Feira de Santana, Feira de Santana, Bahia, Brazil
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D. L. Mascarenhas
39Secretaria de Saúde de Feira de Santana, Feira de Santana, Bahia, Brazil
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J. P. Moura Neto
40Universidade Federal do Amazonas, Manaus, Brazil
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A. S. Levin
4Department of Infectious Disease, School of Medicine & Institute of Tropical Medicine, University of São Paulo, Brazil
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T. R. Tozetto-Mendoza
4Department of Infectious Disease, School of Medicine & Institute of Tropical Medicine, University of São Paulo, Brazil
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S. N. Fonseca
41Hospital São Francisco, Ribeirão Preto, Brazil
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M. C. Mendes-Correa
4Department of Infectious Disease, School of Medicine & Institute of Tropical Medicine, University of São Paulo, Brazil
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F.P. Milagres
42Universidade Federal do Tocantins, Palmas, Brazil
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A. Segurado
4Department of Infectious Disease, School of Medicine & Institute of Tropical Medicine, University of São Paulo, Brazil
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E. C. Holmes
43University of Sydney, Sydney, Australia
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A. Rambaut
44Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3FL, UK
45Fogarty International Center, National Institutes of Health, Bethesda, MD 20892, USA
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T. Bedford
7Harvard Medical School, Boston, MA, USA
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M. R. T. Nunes
2Evandro Chagas Institute, Ministry of Health, Ananindeua, Brazil
46Department of Pathology, University of Texas Medical Branch, Galveston, TX 77555, USA
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E. C. Sabino
4Department of Infectious Disease, School of Medicine & Institute of Tropical Medicine, University of São Paulo, Brazil
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  • For correspondence: lalcan@bahia.fiocruz.br
L. C. J. Alcantara
5Fundação Oswaldo Cruz (FIOCRUZ), Salvador, Bahia, Brazil
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  • For correspondence: lalcan@bahia.fiocruz.br
N. Loman
3Institute of Microbiology and Infection, University of Birmingham, UK
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  • For correspondence: lalcan@bahia.fiocruz.br
O. G. Pybus
1Department of Zoology, University of Oxford, Oxford OX3 1PS, UK
47Metabiota, San Francisco, CA 94104, USA
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  • For correspondence: lalcan@bahia.fiocruz.br
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Abstract

Zika virus (ZIKV) transmission in the Americas was first confirmed in May 2015 in Northeast Brazil1. Brazil has the highest number of reported ZIKV cases worldwide (>200,000 by 24 Dec 20162) as well as the greatest number of cases associated with microcephaly and other birth defects (2,366 confirmed cases by 31 Dec 20162). Following the initial detection of ZIKV in Brazil, 47 countries and territories in the Americas have reported local ZIKV transmission, with 24 of these reporting ZIKV-associated severe disease3. Yet the origin and epidemic history of ZIKV in Brazil and the Americas remain poorly understood, despite the value of such information for interpreting past and future trends in reported microcephaly. To address this we generated 54 complete or partial ZIKV genomes, mostly from Brazil, and report data generated by the ZiBRA project – a mobile genomics lab that travelled across Northeast (NE) Brazil in 2016. One sequence represents the earliest confirmed ZIKV infection in Brazil. Joint analyses of viral genomes with ecological and epidemiological data estimate that ZIKV epidemic was present in NE Brazil by March 2014 and likely disseminated from there, both nationally and internationally, before the first detection of ZIKV in the Americas. Estimated dates of the international spread of ZIKV from Brazil indicate the duration of pre-detection cryptic transmission in recipient regions. NE Brazil’s role in the establishment of ZIKV in the Americas is further supported by geographic analysis of ZIKV transmission potential and by estimates of the virus’ basic reproduction number.

One Sentence Summary Virus genomes reveal the establishment of Zika virus in Brazil and the Americas, and provide an appropriate timeframe for baseline (pre-Zika) microcephaly in different regions.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Epidemic establishment and cryptic transmission of Zika virus in Brazil and the Americas
N. R. Faria, J. Quick, I. Morales, J. Thézé, J.G. Jesus, M. Giovanetti, M. U. G. Kraemer, S. C. Hill, A. Black, A. C. da Costa, L.C. Franco, S. P. Silva, C.-H. Wu, J. Raghwani, S. Cauchemez, L. du Plessis, M. P. Verotti, W. K. de Oliveira, E. H. Carmo, G. E. Coelho, A. C. F. S. Santelli, L. C. Vinhal, C. M. Henriques, J. T. Simpson, M. Loose, K. G. Andersen, N. D. Grubaugh, S. Somasekar, C. Y. Chiu, J. E. Muñoz-Medina, C. R. Gonzalez-Bonilla, C. F. Arias, L. L. Lewis-Ximenez, S.A. Baylis, A. O. Chieppe, S. F. Aguiar, C. A. Fernandes, P. S. Lemos, B. L. S. Nascimento, H. A. O. Monteiro, I. C. Siqueira, M. G. de Queiroz, T. R. de Souza, J. F. Bezerra, M. R. Lemos, G. F. Pereira, D. Loudal, L. C. Moura, R. Dhalia, R. F. França, T. Magalhães, E. T. Marques Jr., T. Jaenisch, G. L. Wallau, M. C. de Lima, V. Nascimento, E. M. de Cerqueira, M. M. de Lima, D. L. Mascarenhas, J. P. Moura Neto, A. S. Levin, T. R. Tozetto-Mendoza, S. N. Fonseca, M. C. Mendes-Correa, F.P. Milagres, A. Segurado, E. C. Holmes, A. Rambaut, T. Bedford, M. R. T. Nunes, E. C. Sabino, L. C. J. Alcantara, N. Loman, O. G. Pybus
bioRxiv 105171; doi: https://doi.org/10.1101/105171
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Epidemic establishment and cryptic transmission of Zika virus in Brazil and the Americas
N. R. Faria, J. Quick, I. Morales, J. Thézé, J.G. Jesus, M. Giovanetti, M. U. G. Kraemer, S. C. Hill, A. Black, A. C. da Costa, L.C. Franco, S. P. Silva, C.-H. Wu, J. Raghwani, S. Cauchemez, L. du Plessis, M. P. Verotti, W. K. de Oliveira, E. H. Carmo, G. E. Coelho, A. C. F. S. Santelli, L. C. Vinhal, C. M. Henriques, J. T. Simpson, M. Loose, K. G. Andersen, N. D. Grubaugh, S. Somasekar, C. Y. Chiu, J. E. Muñoz-Medina, C. R. Gonzalez-Bonilla, C. F. Arias, L. L. Lewis-Ximenez, S.A. Baylis, A. O. Chieppe, S. F. Aguiar, C. A. Fernandes, P. S. Lemos, B. L. S. Nascimento, H. A. O. Monteiro, I. C. Siqueira, M. G. de Queiroz, T. R. de Souza, J. F. Bezerra, M. R. Lemos, G. F. Pereira, D. Loudal, L. C. Moura, R. Dhalia, R. F. França, T. Magalhães, E. T. Marques Jr., T. Jaenisch, G. L. Wallau, M. C. de Lima, V. Nascimento, E. M. de Cerqueira, M. M. de Lima, D. L. Mascarenhas, J. P. Moura Neto, A. S. Levin, T. R. Tozetto-Mendoza, S. N. Fonseca, M. C. Mendes-Correa, F.P. Milagres, A. Segurado, E. C. Holmes, A. Rambaut, T. Bedford, M. R. T. Nunes, E. C. Sabino, L. C. J. Alcantara, N. Loman, O. G. Pybus
bioRxiv 105171; doi: https://doi.org/10.1101/105171

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