Genomic and epidemiological monitoring of yellow fever virus transmission potential

N R Faria; M U G Kraemer; S C Hill; J Goes de Jesus; R S Aguiar; F C M Iani; J Xavier; J Quick; L du Plessis; S Dellicour; J Thézé; R D O Carvalho; G Baele; C-H Wu; P P Silveira; M B Arruda; M A Pereira; G C Pereira; J Lourenço; U Obolski; L Abade; T I Vasylyeva; M Giovanetti; D Yi; D J Weiss; G R W Wint; F M Shearer; S Funk; B Nikolay; V Fonseca; T E R Adelino; M A A Oliveira; M V F Silva; L Sacchetto; P O Figueiredo; I M Rezende; E M Mello; R F C Said; D A Santos; M L Ferraz; M G Brito; L F Santana; M T Menezes; R M Brindeiro; A Tanuri; F C P Dos Santos; M S Cunha; J S Nogueira; I M Rocco; A C da Costa; S C V Komninakis; V Azevedo; A O Chieppe; E S M Araujo; M C L Mendonça; C C Dos Santos; C D Dos Santos; A M Mares-Guia; R M R Nogueira; P C Sequeira; R G Abreu; M H O Garcia; A L Abreu; O Okumoto; E G Kroon; C F C de Albuquerque; K Lewandowski; S T Pullan; M Carroll; T de Oliveira; E C Sabino; R P Souza; M A Suchard; P Lemey; G S Trindade; B P Drumond; A M B Filippis; N J Loman; S Cauchemez; L C J Alcantara; O G Pybus

doi:10.1126/science.aat7115

Genomic and epidemiological monitoring of yellow fever virus transmission potential

Science. 2018 Aug 31;361(6405):894-899. doi: 10.1126/science.aat7115. Epub 2018 Aug 23.

Authors

N R Faria¹, M U G Kraemer^{2

3

4}, S C Hill², J Goes de Jesus⁵, R S Aguiar⁶, F C M Iani^{7

8}, J Xavier⁵, J Quick⁹, L du Plessis², S Dellicour¹⁰, J Thézé², R D O Carvalho⁸, G Baele¹⁰, C-H Wu¹¹, P P Silveira⁶, M B Arruda⁶, M A Pereira⁷, G C Pereira⁷, J Lourenço², U Obolski², L Abade^{2

12}, T I Vasylyeva², M Giovanetti^{5

8}, D Yi¹³, D J Weiss¹⁴, G R W Wint², F M Shearer¹⁴, S Funk¹⁵, B Nikolay^{16

17}, V Fonseca^{8

18}, T E R Adelino⁷, M A A Oliveira⁷, M V F Silva⁷, L Sacchetto⁸, P O Figueiredo⁸, I M Rezende⁸, E M Mello⁸, R F C Said¹⁹, D A Santos¹⁹, M L Ferraz¹⁹, M G Brito¹⁹, L F Santana¹⁹, M T Menezes⁶, R M Brindeiro⁶, A Tanuri⁶, F C P Dos Santos²⁰, M S Cunha²⁰, J S Nogueira²⁰, I M Rocco²⁰, A C da Costa²¹, S C V Komninakis^{22

23}, V Azevedo⁸, A O Chieppe²⁴, E S M Araujo⁵, M C L Mendonça⁵, C C Dos Santos⁵, C D Dos Santos⁵, A M Mares-Guia⁵, R M R Nogueira⁵, P C Sequeira⁵, R G Abreu²⁵, M H O Garcia²⁵, A L Abreu²⁶, O Okumoto²⁶, E G Kroon⁸, C F C de Albuquerque²⁷, K Lewandowski²⁸, S T Pullan²⁸, M Carroll²⁹, T de Oliveira^{5

18

30}, E C Sabino²¹, R P Souza²⁰, M A Suchard^{31

32}, P Lemey¹⁰, G S Trindade⁸, B P Drumond⁸, A M B Filippis⁵, N J Loman⁹, S Cauchemez^{16

17}, L C J Alcantara^{33

8}, O G Pybus¹

Affiliations

¹ Department of Zoology, University of Oxford, Oxford, UK. nuno.faria@zoo.ox.ac.uk luiz.alcantara@ioc.fiocruz.br oliver.pybus@zoo.ox.ac.uk.
² Department of Zoology, University of Oxford, Oxford, UK.
³ Computational Epidemiology Lab, Boston Children's Hospital, Boston, MA, USA.
⁴ Department of Pediatrics, Harvard Medical School, Boston, MA, USA.
⁵ Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil.
⁶ Laboratório de Virologia Molecular, Departamento de Genética, Instituto de Biologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil.
⁷ Laboratório Central de Saúde Pública, Instituto Octávio Magalhães, FUNED, Belo Horizonte, Minas Gerais, Brazil.
⁸ Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil.
⁹ Institute of Microbiology and Infection, University of Birmingham, Birmingham, UK.
¹⁰ Department of Microbiology and Immunology, Rega Institute, KU Leuven, Leuven, Belgium.
¹¹ Department of Statistics, University of Oxford, Oxford, UK.
¹² The Global Health Network, University of Oxford, Oxford, UK.
¹³ Department of Statistics, Harvard University, Cambridge, MA, USA.
¹⁴ Malaria Atlas Project, Big Data Institute, Nuffield Department of Medicine, University of Oxford, Oxford, UK.
¹⁵ Faculty of Epidemiology and Population Health, London School of Hygiene and Tropical Medicine, London, UK.
¹⁶ Mathematical Modelling of Infectious Diseases and Center of Bioinformatics, Institut Pasteur, Paris, France.
¹⁷ CNRS UMR2000: Génomique Évolutive, Modélisation et Santé, Institut Pasteur, Paris, France.
¹⁸ KwaZulu-Natal Research, Innovation and Sequencing Platform (KRISP), School of Laboratory Medicine and Medical Sciences, University of KwaZulu-Natal, Durban, South Africa.
¹⁹ Secretaria de Estado de Saúde de Minas Gerais, Belo Horizonte, Minas Gerais, Brazil.
²⁰ Núcleo de Doenças de Transmissão Vetorial, Instituto Adolfo Lutz, São Paulo, Brazil.
²¹ Instituto de Medicina Tropical e Faculdade de Medicina da Universidade de São Paulo, São Paulo, Brazil.
²² Retrovirology Laboratory, Federal University of São Paulo, São Paulo, Brazil.
²³ School of Medicine of ABC (FMABC), Clinical Immunology Laboratory, Santo André, São Paulo, Brazil.
²⁴ Coordenação de Vigilância Epidemiológica do Estado do Rio de Janeiro, Rio de Janeiro, Brazil.
²⁵ Departamento de Vigilância das Doenças Transmissíveis da Secretaria de Vigilância em Saúde, Ministério da Saúde, Brasília-DF, Brazil.
²⁶ Secretaria de Vigilância em Saúde, Coordenação Geral de Laboratórios de Saúde Pública, Ministério da Saúde, Brasília-DF, Brazil.
²⁷ Organização Pan - Americana da Saúde/Organização Mundial da Saúde - (OPAS/OMS), Brasília-DF, Brazil.
²⁸ Public Health England, National Infections Service, Porton Down, Salisbury, UK.
²⁹ NIHR HPRU in Emerging and Zoonotic Infections, Public Health England, London, UK.
³⁰ Centre for the AIDS Programme of Research in South Africa (CAPRISA), Durban, South Africa.
³¹ Department of Biostatistics, UCLA Fielding School of Public Health, University of California, Los Angeles, CA, USA.
³² Department of Biomathematics and Human Genetics, David Geffen School of Medicine at UCLA, University of California, Los Angeles, CA, USA.
³³ Laboratório de Flavivírus, Instituto Oswaldo Cruz, FIOCRUZ, Rio de Janeiro, Brazil. nuno.faria@zoo.ox.ac.uk luiz.alcantara@ioc.fiocruz.br oliver.pybus@zoo.ox.ac.uk.

Abstract

The yellow fever virus (YFV) epidemic in Brazil is the largest in decades. The recent discovery of YFV in Brazilian Aedes species mosquitos highlights a need to monitor the risk of reestablishment of urban 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 is characteristic of sylvatic transmission. Analysis of YFV cases combined with genomes generated locally reveals an early phase of sylvatic YFV transmission and spatial expansion toward previously YFV-free areas, followed by a rise in viral spillover to humans in late 2016. Our results establish a framework for monitoring YFV transmission in real time that will contribute to a global strategy to eliminate future YFV epidemics.

Publication types

Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't

MeSH terms

Aedes / virology
Age Factors
Animals
Brazil / epidemiology
Disease Outbreaks / prevention & control*
Disease Outbreaks / statistics & numerical data
Epidemiological Monitoring*
Evolution, Molecular
Genomics / methods*
Humans
Phylogeny
Polymerase Chain Reaction
Risk
Sex Factors
Spatio-Temporal Analysis
Yellow Fever / epidemiology
Yellow Fever / prevention & control*
Yellow Fever / transmission*
Yellow Fever / virology
Yellow fever virus / classification
Yellow fever virus / genetics
Yellow fever virus / isolation & purification*

Abstract

Publication types

MeSH terms

Grants and funding