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Genomic and epidemiological monitoring of yellow fever virus transmission potential

View ORCID ProfileFaria N. R., Kraemer M. U. G., Hill S. C., Goes de Jesus J., de Aguiar R. S., Iani F. C. M., Xavier J., Quick J., du Plessis L., Dellicour S., Thézé J., Carvalho R. D. O., Baele G., Wu C.-H., Silveira P. P., Arruda M. B., Pereira M. A., Pereira G. C., Lourenço J., Obolski U., Abade L., Vasylyeva T. I., Giovanetti M., Yi D., Weiss D.J., Wint G. R. W., Shearer F. M., Funk S., Nikolai B., Adelino T. E. R., Oliveira M. A. A., Silva M. V. F., Sacchetto L., Figueiredo P. O., Rezende I. M., Mello E. M., Said R. F. C., Santos D. A., Ferraz M. L., Brito M. G., Santana L. F., Menezes M. T., Brindeiro R. M., Tanuri A., dos Santos F. C. P., Cunha M. S., Nogueira J. S., Rocco I. M., da Costa A. C., Komninakis S. C. V., Azevedo V., Chieppe A. O., Araujo E. S. M., Mendonça M. C. L., dos Santos C. C., dos Santos C. D., Mares-Guia A. M., Nogueira R. M. R., Sequeira P. C., Abreu R. G., Garcia M. H. O., Alves R. V., Abreu A. L., Okumoto O., Kroon E. G., de Albuquerque C. F. C., Lewandowski K., Pullan S. T., Carroll M., Sabino E. C., Souza R. P., Suchard M. A., Lemey P., Trindade G. S., Drumond B. P., Filippis A. M. B., Loman N. J., Cauchemez S., Alcantara L. C. J., Pybus O. G.
doi: https://doi.org/10.1101/299842
Faria N. R.
1Department of Zoology, University of Oxford, OX1 3PS, United Kingdom
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  • ORCID record for Faria N. R.
  • For correspondence: nuno.faria@zoo.ox.ac.uk lalcan@bahia.fiocruz.br oliver.pybus@zoo.ox.ac.uk
Kraemer M. U. G.
1Department of Zoology, University of Oxford, OX1 3PS, United Kingdom
2Computational Epidemiology Lab, Boston Children’s Hospital, Boston, USA & Harvard Medical School, Boston, USA
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Hill S. C.
1Department of Zoology, University of Oxford, OX1 3PS, United Kingdom
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Goes de Jesus J.
3Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ Bahia, Salvador, Brazil
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de Aguiar R. S.
4Laboratory of Molecular Virology, Departamento de Genética, Instituto de Biologia, Rio De Janeiro, Brazil
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Iani F. C. M.
5Laboratório Central de Saúde Pública, Instituto Octávio Magalhães, FUNED, Belo Horizonte, Minas Gerais, Brazil
6Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro - RJ, Brazil
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Xavier J.
3Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ Bahia, Salvador, Brazil
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Quick J.
7Institute of Microbiology and Infection, University of Birmingham, Birmingham B15 2TT, United Kingdom
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du Plessis L.
1Department of Zoology, University of Oxford, OX1 3PS, United Kingdom
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Dellicour S.
9Department of Microbiology and Immunology, Rega Institute, KU Leuven – University of Leuven, Herestraat 49, 3000 Leuven, Belgium
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Thézé J.
1Department of Zoology, University of Oxford, OX1 3PS, United Kingdom
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Carvalho R. D. O.
8Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
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Baele G.
9Department of Microbiology and Immunology, Rega Institute, KU Leuven – University of Leuven, Herestraat 49, 3000 Leuven, Belgium
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Wu C.-H.
10Department of Statistics, University of Oxford, Oxford OX1 3LB, United Kingdom
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Silveira P. P.
4Laboratory of Molecular Virology, Departamento de Genética, Instituto de Biologia, Rio De Janeiro, Brazil
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Arruda M. B.
4Laboratory of Molecular Virology, Departamento de Genética, Instituto de Biologia, Rio De Janeiro, Brazil
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Pereira M. A.
5Laboratório Central de Saúde Pública, Instituto Octávio Magalhães, FUNED, Belo Horizonte, Minas Gerais, Brazil
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Pereira G. C.
5Laboratório Central de Saúde Pública, Instituto Octávio Magalhães, FUNED, Belo Horizonte, Minas Gerais, Brazil
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Lourenço J.
1Department of Zoology, University of Oxford, OX1 3PS, United Kingdom
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Obolski U.
1Department of Zoology, University of Oxford, OX1 3PS, United Kingdom
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Abade L.
1Department of Zoology, University of Oxford, OX1 3PS, United Kingdom
11The Global Health Network, University of Oxford, United Kingdom
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Vasylyeva T. I.
1Department of Zoology, University of Oxford, OX1 3PS, United Kingdom
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Giovanetti M.
3Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ Bahia, Salvador, Brazil
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Yi D.
12Department of Statistics, Harvard University, Cambridge, MA, USA
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Weiss D.J.
13Malaria Atlas Project, Big Data Institute, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FY, UK
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Wint G. R. W.
1Department of Zoology, University of Oxford, OX1 3PS, United Kingdom
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Shearer F. M.
13Malaria Atlas Project, Big Data Institute, Nuffield Department of Medicine, University of Oxford, Roosevelt Drive, Oxford OX3 7FY, UK
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Funk S.
14London School of Tropical Medicine and Hygiene, London, United Kingdom
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Nikolai B.
15Mathematical Modelling of Infectious Diseases and Center of Bioinformatics, Biostatistics and Integrative Biology, Institut Pasteur, Paris, France
16CNRS UMR2000: Génomique évolutive, modélisation et santé, Institut Pasteur, Paris, France
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Adelino T. E. R.
5Laboratório Central de Saúde Pública, Instituto Octávio Magalhães, FUNED, Belo Horizonte, Minas Gerais, Brazil
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Oliveira M. A. A.
5Laboratório Central de Saúde Pública, Instituto Octávio Magalhães, FUNED, Belo Horizonte, Minas Gerais, Brazil
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Silva M. V. F.
5Laboratório Central de Saúde Pública, Instituto Octávio Magalhães, FUNED, Belo Horizonte, Minas Gerais, Brazil
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Sacchetto L.
17Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
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Figueiredo P. O.
17Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
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Rezende I. M.
17Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
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Mello E. M.
17Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
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Said R. F. C.
18Secretaria de Estad de Saúde de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
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Santos D. A.
18Secretaria de Estad de Saúde de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
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Ferraz M. L.
18Secretaria de Estad de Saúde de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
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Brito M. G.
18Secretaria de Estad de Saúde de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
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Santana L. F.
18Secretaria de Estad de Saúde de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil
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Menezes M. T.
19Laboratory of Medical Virology, Departamento de Genética Instituto de Biologia, Rio de Janeiro, Brazil
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Brindeiro R. M.
19Laboratory of Medical Virology, Departamento de Genética Instituto de Biologia, Rio de Janeiro, Brazil
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Tanuri A.
19Laboratory of Medical Virology, Departamento de Genética Instituto de Biologia, Rio de Janeiro, Brazil
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dos Santos F. C. P.
20Núcleo de Doenças de Transmissão Vetorial, Instituto Adolfo Lutz, São Paulo, Brazil
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Cunha M. S.
20Núcleo de Doenças de Transmissão Vetorial, Instituto Adolfo Lutz, São Paulo, Brazil
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Nogueira J. S.
20Núcleo de Doenças de Transmissão Vetorial, Instituto Adolfo Lutz, São Paulo, Brazil
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Rocco I. M.
20Núcleo de Doenças de Transmissão Vetorial, Instituto Adolfo Lutz, São Paulo, Brazil
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da Costa A. C.
21Instituto de Medicina Tropical e Faculdade de Medicina da Universidade de São Paulo, São Paulo, Brazil
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Komninakis S. C. V.
22Retrovirology Laboratory, Federal University of São Paulo, Brazil, School of Medicine of ABC (FMABC), Clinical Immunology Laboratory, Santo André, São Paulo, Brazil
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Azevedo V.
7Institute of Microbiology and Infection, University of Birmingham, Birmingham B15 2TT, United Kingdom
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Chieppe A. O.
23Coordenação de Vigilância Epidemiológica do Estado do Rio de Janeiro, Brazil
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Araujo E. S. M.
6Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro - RJ, Brazil
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Mendonça M. C. L.
6Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro - RJ, Brazil
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dos Santos C. C.
6Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro - RJ, Brazil
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dos Santos C. D.
6Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro - RJ, Brazil
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Mares-Guia A. M.
6Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro - RJ, Brazil
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Nogueira R. M. R.
6Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro - RJ, Brazil
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Sequeira P. C.
6Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro - RJ, Brazil
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Abreu R. G.
24Departamento de Vigilância das Doenças Transmissíveis da Secretaria de Vigilância em Saúde, Ministério da Saúde, Brasília-DF, Brazil
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Garcia M. H. O.
24Departamento de Vigilância das Doenças Transmissíveis da Secretaria de Vigilância em Saúde, Ministério da Saúde, Brasília-DF, Brazil
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Alves R. V.
24Departamento de Vigilância das Doenças Transmissíveis da Secretaria de Vigilância em Saúde, Ministério da Saúde, Brasília-DF, Brazil
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Abreu A. L.
25Secretaria de Vigilância em Saúde, Coordenação Geral de Laboratórios de Saúde Pública, Ministério da Saúde, Brasília-DF, Brazil
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Okumoto O.
25Secretaria de Vigilância em Saúde, Coordenação Geral de Laboratórios de Saúde Pública, Ministério da Saúde, Brasília-DF, Brazil
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Kroon E. G.
8Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
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de Albuquerque C. F. C.
26Organização Pan - Americana da Saúde - OPAS/OMS, Brasília-DF, Brazil
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Lewandowski K.
27Public Health England, National Infections Service, Porton Down, UK
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Pullan S. T.
27Public Health England, National Infections Service, Porton Down, UK
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Carroll M.
28NIHR HPRU in Emerging and Zoonotic Infections, Public Health England, United Kingdom
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Sabino E. C.
21Instituto de Medicina Tropical e Faculdade de Medicina da Universidade de São Paulo, São Paulo, Brazil
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Souza R. P.
20Núcleo de Doenças de Transmissão Vetorial, Instituto Adolfo Lutz, São Paulo, Brazil
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Suchard M. A.
29Department of Biostatistics, UCLA Fielding School of Public Health, University of California, Los Angeles, CA, USA
30Department of Biomathematics and Human Genetics, David Geffen School of Medicine at UCLA, University of California, Los Angeles, CA, USA
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Lemey P.
9Department of Microbiology and Immunology, Rega Institute, KU Leuven – University of Leuven, Herestraat 49, 3000 Leuven, Belgium
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Trindade G. S.
8Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
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Drumond B. P.
8Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil
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Filippis A. M. B.
6Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro - RJ, Brazil
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Loman N. J.
7Institute of Microbiology and Infection, University of Birmingham, Birmingham B15 2TT, United Kingdom
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Cauchemez S.
14London School of Tropical Medicine and Hygiene, London, United Kingdom
15Mathematical Modelling of Infectious Diseases and Center of Bioinformatics, Biostatistics and Integrative Biology, Institut Pasteur, Paris, France
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Alcantara L. C. J.
3Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ Bahia, Salvador, Brazil
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  • For correspondence: nuno.faria@zoo.ox.ac.uk lalcan@bahia.fiocruz.br oliver.pybus@zoo.ox.ac.uk
Pybus O. G.
1Department of Zoology, University of Oxford, OX1 3PS, United Kingdom
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  • For correspondence: nuno.faria@zoo.ox.ac.uk lalcan@bahia.fiocruz.br oliver.pybus@zoo.ox.ac.uk
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Abstract

The yellow fever virus (YFV) epidemic that began in Dec 2016 in Brazil is the largest in decades. The recent discovery of YFV in Brazilian Aedes sp. vectors highlights the urgent need to monitor the risk of re-establishment of domestic YFV transmission in the Americas. We use a suite of epidemiological, spatial and genomic approaches to characterize YFV transmission. We show that the age- and sex-distribution of human cases in Brazil is characteristic of sylvatic transmission. Analysis of YFV cases combined with genomes generated locally using a new protocol reveals an early phase of sylvatic YFV transmission restricted to Minas Gerais, followed in late 2016 by a rise in viral spillover to humans, and the southwards spatial expansion of the epidemic towards previously YFV-free areas. Our results establish a framework for monitoring YFV transmission in real-time, contributing to the global strategy of eliminating future yellow fever epidemics.

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Genomic and epidemiological monitoring of yellow fever virus transmission potential
Faria N. R., Kraemer M. U. G., Hill S. C., Goes de Jesus J., de Aguiar R. S., Iani F. C. M., Xavier J., Quick J., du Plessis L., Dellicour S., Thézé J., Carvalho R. D. O., Baele G., Wu C.-H., Silveira P. P., Arruda M. B., Pereira M. A., Pereira G. C., Lourenço J., Obolski U., Abade L., Vasylyeva T. I., Giovanetti M., Yi D., Weiss D.J., Wint G. R. W., Shearer F. M., Funk S., Nikolai B., Adelino T. E. R., Oliveira M. A. A., Silva M. V. F., Sacchetto L., Figueiredo P. O., Rezende I. M., Mello E. M., Said R. F. C., Santos D. A., Ferraz M. L., Brito M. G., Santana L. F., Menezes M. T., Brindeiro R. M., Tanuri A., dos Santos F. C. P., Cunha M. S., Nogueira J. S., Rocco I. M., da Costa A. C., Komninakis S. C. V., Azevedo V., Chieppe A. O., Araujo E. S. M., Mendonça M. C. L., dos Santos C. C., dos Santos C. D., Mares-Guia A. M., Nogueira R. M. R., Sequeira P. C., Abreu R. G., Garcia M. H. O., Alves R. V., Abreu A. L., Okumoto O., Kroon E. G., de Albuquerque C. F. C., Lewandowski K., Pullan S. T., Carroll M., Sabino E. C., Souza R. P., Suchard M. A., Lemey P., Trindade G. S., Drumond B. P., Filippis A. M. B., Loman N. J., Cauchemez S., Alcantara L. C. J., Pybus O. G.
bioRxiv 299842; doi: https://doi.org/10.1101/299842
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Genomic and epidemiological monitoring of yellow fever virus transmission potential
Faria N. R., Kraemer M. U. G., Hill S. C., Goes de Jesus J., de Aguiar R. S., Iani F. C. M., Xavier J., Quick J., du Plessis L., Dellicour S., Thézé J., Carvalho R. D. O., Baele G., Wu C.-H., Silveira P. P., Arruda M. B., Pereira M. A., Pereira G. C., Lourenço J., Obolski U., Abade L., Vasylyeva T. I., Giovanetti M., Yi D., Weiss D.J., Wint G. R. W., Shearer F. M., Funk S., Nikolai B., Adelino T. E. R., Oliveira M. A. A., Silva M. V. F., Sacchetto L., Figueiredo P. O., Rezende I. M., Mello E. M., Said R. F. C., Santos D. A., Ferraz M. L., Brito M. G., Santana L. F., Menezes M. T., Brindeiro R. M., Tanuri A., dos Santos F. C. P., Cunha M. S., Nogueira J. S., Rocco I. M., da Costa A. C., Komninakis S. C. V., Azevedo V., Chieppe A. O., Araujo E. S. M., Mendonça M. C. L., dos Santos C. C., dos Santos C. D., Mares-Guia A. M., Nogueira R. M. R., Sequeira P. C., Abreu R. G., Garcia M. H. O., Alves R. V., Abreu A. L., Okumoto O., Kroon E. G., de Albuquerque C. F. C., Lewandowski K., Pullan S. T., Carroll M., Sabino E. C., Souza R. P., Suchard M. A., Lemey P., Trindade G. S., Drumond B. P., Filippis A. M. B., Loman N. J., Cauchemez S., Alcantara L. C. J., Pybus O. G.
bioRxiv 299842; doi: https://doi.org/10.1101/299842

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