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

View ORCID ProfileNuno R. Faria, Josh Quick, Ingra Morales, Julien Theze, Jacqueline G. de Jesus, Marta Giovanetti, Moritz U. G. Kraemer, Sarah C. Hill, Allison Black, Antonio C. da Costa, Luciano C. Franco, Sandro P. Silva, Chiej-Hsi Wu, Jayna Ragwhani, Simon Cauchemez, Louis du Plessis, Mariana P. Verotti, Wanderson K. Oliveira, Eduardo H. Carmo, Giovanini Evelim Coelho, Ana Carolina Faria E. Silva Santelli, Livia C. Vinhal, Claudio Maierovitch Pessanha Henriques, Jared Simpson, Matt Loose, Kristian G. Andersen, Nathan Grubaugh, Sneha Somasekar, Charles Y. Chiu, Lia Laura Lewis-Ximenez, Sally A. Baylis, Alexandre Otavio Chieppe, Shirlei Ferreira Aguiar, Carlos Augusto Fernandes, Poliana da Silva Lemos, Bruna L. S. Nascimento, Hamilton Antonio de Oliveira Monteiro, Isadora Cristina Siqueira, Maria Goretti Lins de Queiroz, Themis Rocha Souza, Joao Filipe Bezerra, Marta Rejane Lemos, Gilberto Fernandes Pereira, Dalane Loudal Florentino Teixeira, Lucia C. A. C. Moura, Rafael Dhalia, Rafel F. Franca, Tereza Magalhaes, Ernesto Torres de Azevedo Marques Jr., Gabriel da Luz Wallau, Magliones Carneiro de Lima, Valeria Nascimento, Erenilde Marques de Cerqueira, Maricelia Maia de Lima, Denise Lima Mascarenhas, Jose Pereira de Moura Neto, Anna Sara Shafferman Levin, Tania Regina Tozetto Mendoza, Silvia Fonseca, Maria Cassia Mendes-Correa, Flavio Padua Milagres, Aluisio Segurado, Edward C. Holmes, Andrew Rambaut, Trevor Bedford, Marcio Nunes Roberto Teixeira, Ester Cerdeira Sabino, Luiz Carlos Junior Alcantara, Nicholas Loman, Oliver G. Pybus
doi: https://doi.org/10.1101/105171
Nuno R. Faria
Department of Zoology, University of Oxford, Oxford OX1 3PS, UK;
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Josh Quick
Institute of Microbiology and Infection, University of Birmingham, UK;
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Ingra Morales
Department of Infectious Disease, Institute of Tropical Medicine, University of Sao Paulo, Brazil;
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Julien Theze
Department of Zoology, University of Oxford, Oxford OX1 3PS, UK;
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Jacqueline G. de Jesus
Fundacao Oswaldo Cruz (FIOCRUZ), Salvador, Bahia, Brazil;
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Marta Giovanetti
Fundacao Oswaldo Cruz (FIOCRUZ), Salvador, Bahia, Brazil;
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Moritz U. G. Kraemer
Department of Zoology, University of Oxford, Oxford OX1 3PS, UK;
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Sarah C. Hill
Department of Zoology, University of Oxford, Oxford OX1 3PS, UK;
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Allison Black
Fred Hutchinson Cancer Research Center, USA;
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Antonio C. da Costa
Department of Infectious Disease, Institute of Tropical Medicine, University of Sao Paulo, Brazil;
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Luciano C. Franco
Evandro Chagas Institute, Ministry of Health, Ananindeua, Brazil;
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Sandro P. Silva
Evandro Chagas Institute, Ministry of Health, Ananindeua, Brazil;
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Chiej-Hsi Wu
Department of Statistics, University of Oxford, UK;
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Jayna Ragwhani
Department of Zoology, University of Oxford, Oxford OX1 3PS, UK;
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Simon Cauchemez
Mathematical Modelling of Infectious Diseases and Center of Bioinformatics and Biostatistics;
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Louis du Plessis
Department of Zoology, University of Oxford, Oxford OX1 3PS, UK;
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Mariana P. Verotti
Coordenacao dos Laboratorios de Saude Publica, Ministry of Health, Brasilia, Brazil;
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Wanderson K. Oliveira
Coordenacao Geral Vigilancia e Resposta as Emergencias em Saude Publica, Ministry of Health, Brazil;
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Eduardo H. Carmo
Departamento de Vigilancia das Doencas Transmissiveis, Ministry of Health, Brasilia, Brazil;
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Giovanini Evelim Coelho
Coordenacao Geral Controle e Prevencao, Ministry of Health, Brazil;
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Ana Carolina Faria E. Silva Santelli
Coordenacao Geral Controle e Prevencao, Ministry of Health, Brazil;
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Livia C. Vinhal
Programa Nacional de Controle da Dengue Zika Chikungunya Malaria, Ministry of Health, Brazil;
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Claudio Maierovitch Pessanha Henriques
Departamento de Vigilancia das Doencas Transmissiveis, Ministry of Health, Brasilia, Brazil;
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Jared Simpson
Ontario Institute for Cancer Research, Toronto, Canada;
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Matt Loose
University of Nottingham, Nottingham, United Kingdom;
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Kristian G. Andersen
Department of Immunology and Microbial Science, The Scripps Research Institute, USA;
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Nathan Grubaugh
Department of Immunology and Microbial Science, The Scripps Research Institute, USA;
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Sneha Somasekar
Departments of Laboratory Medicine and Medicine & Infectious Diseases, University of California, USA;
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Charles Y. Chiu
Departments of Laboratory Medicine and Medicine & Infectious Diseases, University of California, USA;
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Lia Laura Lewis-Ximenez
Fundacao Oswaldo Cruz (FIOCRUZ), Rio de Janeiro, Brazil;
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Sally A. Baylis
Paul-Ehrlich-Institut, Langen, Germany;
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Alexandre Otavio Chieppe
Laboratorio Central de Saude Publica Noel Nutels, Rio de Janeiro, Brazil;
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Shirlei Ferreira Aguiar
Laboratorio Central de Saude Publica Noel Nutels, Rio de Janeiro, Brazil;
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Carlos Augusto Fernandes
Laboratorio Central de Saude Publica Noel Nutels, Rio de Janeiro, Brazil;
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Poliana da Silva Lemos
Evandro Chagas Institute, Ministry of Health, Ananindeua, Brazil;
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Bruna L. S. Nascimento
Evandro Chagas Institute, Ministry of Health, Ananindeua, Brazil;
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Hamilton Antonio de Oliveira Monteiro
Evandro Chagas Institute, Ministry of Health, Ananindeua, Brazil;
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Isadora Cristina Siqueira
Fundacao Oswaldo Cruz (FIOCRUZ), Salvador, Bahia, Brazil;
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Maria Goretti Lins de Queiroz
Laboratorio Central de Saude Publica do Estado do Rio Grande do Norte, Natal, Brazil;
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Themis Rocha Souza
Laboratorio Central de Saude Publica do Estado do Rio Grande do Norte, Natal, Brazil;
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Joao Filipe Bezerra
Laboratorio Central de Saude Publica do Estado do Rio Grande do Norte, Natal, Brazil;
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Marta Rejane Lemos
Laboratorio Central de Saude Publica do Estado da Paraiba, Joao Pessoa, Brazil;
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Gilberto Fernandes Pereira
Laboratorio Central de Saude Publica do Estado da Paraiba, Joao Pessoa, Brazil;
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Dalane Loudal Florentino Teixeira
Laboratorio Central de Saude Publica do Estado da Paraiba, Joao Pessoa, Brazil;
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Lucia C. A. C. Moura
Laboratorio Central de Saude Publica do Estado da Paraiba, Joao Pessoa, Brazil;
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Rafael Dhalia
Fundacao Oswaldo Cruz (FIOCRUZ), Recife, Pernambuco, Brazil;
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Rafel F. Franca
Fundacao Oswaldo Cruz (FIOCRUZ), Recife, Pernambuco, Brazil;
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Tereza Magalhaes
Fundacao Oswaldo Cruz (FIOCRUZ), Recife, Pernambuco, Brazil;
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Ernesto Torres de Azevedo Marques
Fundacao Oswaldo Cruz (FIOCRUZ), Recife, Pernambuco, Brazil;
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Gabriel da Luz Wallau
Fundacao Oswaldo Cruz (FIOCRUZ), Recife, Pernambuco, Brazil;
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Magliones Carneiro de Lima
Laboratorio Central de Saude Publica do Estado de Alagoas, Maceio, Brazil;
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Valeria Nascimento
Laboratorio Central de Saude Publica do Estado de Alagoas, Maceio, Brazil;
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Erenilde Marques de Cerqueira
Universidade Estadual de Feira de Santana, Feira de Santana, Bahia, Brazil;
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Maricelia Maia de Lima
Universidade Estadual de Feira de Santana, Feira de Santana, Bahia, Brazil;
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Denise Lima Mascarenhas
Secretaria de Saude de Feira de Santana, Feira de Santana, Bahia, Brazil;
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Jose Pereira de Moura Neto
Universidade Federal do Amazonas, Manaus;
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Anna Sara Shafferman Levin
Department of Infectious Disease, Institute of Tropical Medicine, University of Sao Paulo, Brazil;
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Tania Regina Tozetto Mendoza
Department of Infectious Disease, Institute of Tropical Medicine, University of Sao Paulo, Brazil;
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Silvia Fonseca
Hospital Sao Francisco, Ribeirao Preto, Brazil;
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Maria Cassia Mendes-Correa
Department of Infectious Disease, Institute of Tropical Medicine, University of Sao Paulo, Brazil;
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Flavio Padua Milagres
Universidade Federal do Tocantins, Palmas, Brazil;
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Aluisio Segurado
Department of Infectious Disease, Institute of Tropical Medicine, University of Sao Paulo, Brazil;
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Edward C. Holmes
University of Sydney, Australia;
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Andrew Rambaut
University of Edinburgh, United Kingdom;
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Trevor Bedford
Fred Hutchinson Cancer Research Center, United States
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Marcio Nunes Roberto Teixeira
Evandro Chagas Institute, Ministry of Health, Ananindeua, Brazil;
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Ester Cerdeira Sabino
Department of Infectious Disease, Institute of Tropical Medicine, University of Sao Paulo, Brazil;
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Luiz Carlos Junior Alcantara
Fundacao Oswaldo Cruz (FIOCRUZ), Salvador, Bahia, Brazil;
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Nicholas Loman
Institute of Microbiology and Infection, University of Birmingham, UK;
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Oliver G. Pybus
Department of Zoology, University of Oxford, Oxford OX1 3PS, UK;
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  • For correspondence: oliver.pybus@zoo.ox.ac.uk
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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 2016) as well as the greatest number of cases associated with microcephaly and other birth defects (2,366 confirmed cases by 31 Dec 2016). 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 disease. 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.

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The copyright holder for this preprint is the author/funder. It is made available under a CC-BY-NC-ND 4.0 International license.
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  • Posted March 27, 2017.

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Epidemic establishment and cryptic transmission of Zika virus in Brazil and the Americas
Nuno R. Faria, Josh Quick, Ingra Morales, Julien Theze, Jacqueline G. de Jesus, Marta Giovanetti, Moritz U. G. Kraemer, Sarah C. Hill, Allison Black, Antonio C. da Costa, Luciano C. Franco, Sandro P. Silva, Chiej-Hsi Wu, Jayna Ragwhani, Simon Cauchemez, Louis du Plessis, Mariana P. Verotti, Wanderson K. Oliveira, Eduardo H. Carmo, Giovanini Evelim Coelho, Ana Carolina Faria E. Silva Santelli, Livia C. Vinhal, Claudio Maierovitch Pessanha Henriques, Jared Simpson, Matt Loose, Kristian G. Andersen, Nathan Grubaugh, Sneha Somasekar, Charles Y. Chiu, Lia Laura Lewis-Ximenez, Sally A. Baylis, Alexandre Otavio Chieppe, Shirlei Ferreira Aguiar, Carlos Augusto Fernandes, Poliana da Silva Lemos, Bruna L. S. Nascimento, Hamilton Antonio de Oliveira Monteiro, Isadora Cristina Siqueira, Maria Goretti Lins de Queiroz, Themis Rocha Souza, Joao Filipe Bezerra, Marta Rejane Lemos, Gilberto Fernandes Pereira, Dalane Loudal Florentino Teixeira, Lucia C. A. C. Moura, Rafael Dhalia, Rafel F. Franca, Tereza Magalhaes, Ernesto Torres de Azevedo Marques Jr., Gabriel da Luz Wallau, Magliones Carneiro de Lima, Valeria Nascimento, Erenilde Marques de Cerqueira, Maricelia Maia de Lima, Denise Lima Mascarenhas, Jose Pereira de Moura Neto, Anna Sara Shafferman Levin, Tania Regina Tozetto Mendoza, Silvia Fonseca, Maria Cassia Mendes-Correa, Flavio Padua Milagres, Aluisio Segurado, Edward C. Holmes, Andrew Rambaut, Trevor Bedford, Marcio Nunes Roberto Teixeira, Ester Cerdeira Sabino, Luiz Carlos Junior Alcantara, Nicholas Loman, Oliver 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
Nuno R. Faria, Josh Quick, Ingra Morales, Julien Theze, Jacqueline G. de Jesus, Marta Giovanetti, Moritz U. G. Kraemer, Sarah C. Hill, Allison Black, Antonio C. da Costa, Luciano C. Franco, Sandro P. Silva, Chiej-Hsi Wu, Jayna Ragwhani, Simon Cauchemez, Louis du Plessis, Mariana P. Verotti, Wanderson K. Oliveira, Eduardo H. Carmo, Giovanini Evelim Coelho, Ana Carolina Faria E. Silva Santelli, Livia C. Vinhal, Claudio Maierovitch Pessanha Henriques, Jared Simpson, Matt Loose, Kristian G. Andersen, Nathan Grubaugh, Sneha Somasekar, Charles Y. Chiu, Lia Laura Lewis-Ximenez, Sally A. Baylis, Alexandre Otavio Chieppe, Shirlei Ferreira Aguiar, Carlos Augusto Fernandes, Poliana da Silva Lemos, Bruna L. S. Nascimento, Hamilton Antonio de Oliveira Monteiro, Isadora Cristina Siqueira, Maria Goretti Lins de Queiroz, Themis Rocha Souza, Joao Filipe Bezerra, Marta Rejane Lemos, Gilberto Fernandes Pereira, Dalane Loudal Florentino Teixeira, Lucia C. A. C. Moura, Rafael Dhalia, Rafel F. Franca, Tereza Magalhaes, Ernesto Torres de Azevedo Marques Jr., Gabriel da Luz Wallau, Magliones Carneiro de Lima, Valeria Nascimento, Erenilde Marques de Cerqueira, Maricelia Maia de Lima, Denise Lima Mascarenhas, Jose Pereira de Moura Neto, Anna Sara Shafferman Levin, Tania Regina Tozetto Mendoza, Silvia Fonseca, Maria Cassia Mendes-Correa, Flavio Padua Milagres, Aluisio Segurado, Edward C. Holmes, Andrew Rambaut, Trevor Bedford, Marcio Nunes Roberto Teixeira, Ester Cerdeira Sabino, Luiz Carlos Junior Alcantara, Nicholas Loman, Oliver G. Pybus
bioRxiv 105171; doi: https://doi.org/10.1101/105171

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