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; Steven Pullan; Miles 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

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. ObolskiL. 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, Steven Pullan, Miles 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

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

215 Citations (Scopus)

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.

Original language	English
Pages (from-to)	894-899
Number of pages	6
Journal	Science
Volume	361
Issue number	6405
DOIs	https://doi.org/10.1126/science.aat7115
Publication status	Published - 31 Aug 2018

Bibliographical note

Funding Information:
We thank FUNED-MG and the Brazilian YFV surveillance network for their contributions. N.R.F. thanks J. F. Drexler for sharing data, N. Trovão for discussions, F. Campos for proof imaging, and P. Fonseca for proofreading. We thank Oxford Nanopore Technologies for technical support. L.C.J.A. thanks QIAGEN for reagents and equipment. A.C.d.C. and E.C.S. thank Illumina, Zymo Research, Sage Science, and Promega for donation of reagents. This work was supported in part by CNPq 400354/ 2016-0 and FAPESP 2016/01735-2. N.R.F. is supported by a Sir Henry Dale Fellowship (204311/Z/16/Z), internal GCRF grant 005073, and John Fell Research Fund grant 005166. This research received funding from the ERC (grant agreement 614725-PATHPHYLODYN) and from the Oxford Martin School. M.U.G.K. acknowledges funding from a Branco Weiss Fellowship, administered by ETH Zurich, a Training Grant from the National Institute of Child Health and Human Development (T32HD040128), and the National Library of Medicine of the National Institutes of Health (R01LM010812 and R01LM011965). S.D. is funded by the Fonds Wetenschappelijk Onderzoek (FWO, Flanders, Belgium). G.B. acknowledges support from the Interne Fondsen KU Leuven/Internal Funds KU Leuven. A.C.d.C. is funded by FAPESP 2017/00021-9. B.B.N. and S.C. are supported by the EU’s Horizon 2020 Programme through ZIKAlliance (grant 734548), the Investissement d’Avenir program, the Laboratoire d’Excellence Integrative Biology of Emerging Infectious Diseases program (grant ANR-10-LABX-62-IBEID), the Models of Infectious Disease Agent Study of the National Institute of General Medical Sciences, the AXA Research Fund, and the Association Robert Debré. P.L. and M.A.S. acknowledge funding from the European Research Council (grant agreement 725422-ReservoirDOCS) and from the Wellcome Trust Collaborative Award 206298/Z/17/Z. P.L. acknowledges support from the Research Foundation, Flanders (Fonds voor Wetenschappelijk Onderzoek, Vlaanderen, G066215N, G0D5117N, and G0B9317N).

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2017 © The Authors,

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Faria, N. R., Kraemer, M. U. G., Hill, S. C., De Jesus, J. G., 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., ... Pybus, O. G. (2018). Genomic and epidemiological monitoring of yellow fever virus transmission potential. Science, 361(6405), 894-899. https://doi.org/10.1126/science.aat7115

@article{3536aa6e14e74740afbbb65409e65730,

title = "Genomic and epidemiological monitoring of yellow fever virus transmission potential",

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.",

author = "Faria, {N. R.} and Kraemer, {M. U.G.} and Hill, {S. C.} and {De Jesus}, {J. Goes} and Aguiar, {R. S.} and Iani, {F. C.M.} and J. Xavier and J. Quick and {Du Plessis}, L. and S. Dellicour and J. Th{\'e}z{\'e} and Carvalho, {R. D.O.} and G. Baele and Wu, {C. H.} and Silveira, {P. P.} and Arruda, {M. B.} and Pereira, {M. A.} and Pereira, {G. C.} and J. Louren{\c c}o and U. Obolski and L. Abade and Vasylyeva, {T. I.} and M. Giovanetti and D. Yi and Weiss, {D. J.} and Wint, {G. R.W.} and Shearer, {F. M.} and S. Funk and B. Nikolay and V. Fonseca and Adelino, {T. E.R.} and Oliveira, {M. A.A.} and Silva, {M. V.F.} and L. Sacchetto and Figueiredo, {P. O.} and Rezende, {I. M.} and Mello, {E. M.} and Said, {R. F.C.} and Santos, {D. A.} and Ferraz, {M. L.} and Brito, {M. G.} and Santana, {L. F.} and Menezes, {M. T.} and Brindeiro, {R. M.} and A. Tanuri and {Dos Santos}, {F. C.P.} and Cunha, {M. S.} and Nogueira, {J. S.} and Rocco, {I. M.} and {Da Costa}, {A. C.} and Komninakis, {S. C.V.} and V. Azevedo and Chieppe, {A. O.} and Araujo, {E. S.M.} and Mendon{\c c}a, {M. C.L.} and {Dos Santos}, {C. C.} and {Dos Santos}, {C. D.} and Mares-Guia, {A. M.} and Nogueira, {R. M.R.} and Sequeira, {P. C.} and Abreu, {R. G.} and Garcia, {M. H.O.} and Abreu, {A. L.} and O. Okumoto and Kroon, {E. G.} and {De Albuquerque}, {C. F.C.} and K. Lewandowski and Steven Pullan and Miles Carroll and {De Oliveira}, T. and Sabino, {E. C.} and Souza, {R. P.} and Suchard, {M. A.} and P. Lemey and Trindade, {G. S.} and Drumond, {B. P.} and Filippis, {A. M.B.} and Loman, {N. J.} and S. Cauchemez and Alcantara, {L. C.J.} and Pybus, {O. G.}",

note = "Funding Information: We thank FUNED-MG and the Brazilian YFV surveillance network for their contributions. N.R.F. thanks J. F. Drexler for sharing data, N. Trov{\~a}o for discussions, F. Campos for proof imaging, and P. Fonseca for proofreading. We thank Oxford Nanopore Technologies for technical support. L.C.J.A. thanks QIAGEN for reagents and equipment. A.C.d.C. and E.C.S. thank Illumina, Zymo Research, Sage Science, and Promega for donation of reagents. This work was supported in part by CNPq 400354/ 2016-0 and FAPESP 2016/01735-2. N.R.F. is supported by a Sir Henry Dale Fellowship (204311/Z/16/Z), internal GCRF grant 005073, and John Fell Research Fund grant 005166. This research received funding from the ERC (grant agreement 614725-PATHPHYLODYN) and from the Oxford Martin School. M.U.G.K. acknowledges funding from a Branco Weiss Fellowship, administered by ETH Zurich, a Training Grant from the National Institute of Child Health and Human Development (T32HD040128), and the National Library of Medicine of the National Institutes of Health (R01LM010812 and R01LM011965). S.D. is funded by the Fonds Wetenschappelijk Onderzoek (FWO, Flanders, Belgium). G.B. acknowledges support from the Interne Fondsen KU Leuven/Internal Funds KU Leuven. A.C.d.C. is funded by FAPESP 2017/00021-9. B.B.N. and S.C. are supported by the EU{\textquoteright}s Horizon 2020 Programme through ZIKAlliance (grant 734548), the Investissement d{\textquoteright}Avenir program, the Laboratoire d{\textquoteright}Excellence Integrative Biology of Emerging Infectious Diseases program (grant ANR-10-LABX-62-IBEID), the Models of Infectious Disease Agent Study of the National Institute of General Medical Sciences, the AXA Research Fund, and the Association Robert Debr{\'e}. P.L. and M.A.S. acknowledge funding from the European Research Council (grant agreement 725422-ReservoirDOCS) and from the Wellcome Trust Collaborative Award 206298/Z/17/Z. P.L. acknowledges support from the Research Foundation, Flanders (Fonds voor Wetenschappelijk Onderzoek, Vlaanderen, G066215N, G0D5117N, and G0B9317N). Publisher Copyright: 2017 {\textcopyright} The Authors,",

year = "2018",

month = aug,

day = "31",

doi = "10.1126/science.aat7115",

language = "English",

volume = "361",

pages = "894--899",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

number = "6405",

}

Faria, NR, Kraemer, MUG, Hill, SC, De Jesus, JG, Aguiar, RS, Iani, FCM, Xavier, J, Quick, J, Du Plessis, L, Dellicour, S, Thézé, J, Carvalho, RDO, Baele, G, Wu, CH, Silveira, PP, Arruda, MB, Pereira, MA, Pereira, GC, Lourenço, J, Obolski, U, Abade, L, Vasylyeva, TI, Giovanetti, M, Yi, D, Weiss, DJ, Wint, GRW, Shearer, FM, Funk, S, Nikolay, B, Fonseca, V, Adelino, TER, Oliveira, MAA, Silva, MVF, Sacchetto, L, Figueiredo, PO, Rezende, IM, Mello, EM, Said, RFC, Santos, DA, Ferraz, ML, Brito, MG, Santana, LF, Menezes, MT, Brindeiro, RM, Tanuri, A, Dos Santos, FCP, Cunha, MS, Nogueira, JS, Rocco, IM, Da Costa, AC, Komninakis, SCV, Azevedo, V, Chieppe, AO, Araujo, ESM, Mendonça, MCL, Dos Santos, CC, Dos Santos, CD, Mares-Guia, AM, Nogueira, RMR, Sequeira, PC, Abreu, RG, Garcia, MHO, Abreu, AL, Okumoto, O, Kroon, EG, De Albuquerque, CFC, Lewandowski, K, Pullan, S, Carroll, M, De Oliveira, T, Sabino, EC, Souza, RP, Suchard, MA, Lemey, P, Trindade, GS, Drumond, BP, Filippis, AMB, Loman, NJ, Cauchemez, S, Alcantara, LCJ & Pybus, OG 2018, 'Genomic and epidemiological monitoring of yellow fever virus transmission potential', Science, vol. 361, no. 6405, pp. 894-899. https://doi.org/10.1126/science.aat7115

TY - JOUR

T1 - Genomic and epidemiological monitoring of yellow fever virus transmission potential

AU - Faria, N. R.

AU - Kraemer, M. U.G.

AU - Hill, S. C.

AU - De Jesus, J. Goes

AU - Aguiar, R. S.

AU - Iani, F. C.M.

AU - Xavier, J.

AU - Quick, J.

AU - Du Plessis, L.

AU - Dellicour, S.

AU - Thézé, J.

AU - Carvalho, R. D.O.

AU - Baele, G.

AU - Wu, C. H.

AU - Silveira, P. P.

AU - Arruda, M. B.

AU - Pereira, M. A.

AU - Pereira, G. C.

AU - Lourenço, J.

AU - Obolski, U.

AU - Abade, L.

AU - Vasylyeva, T. I.

AU - Giovanetti, M.

AU - Yi, D.

AU - Weiss, D. J.

AU - Wint, G. R.W.

AU - Shearer, F. M.

AU - Funk, S.

AU - Nikolay, B.

AU - Fonseca, V.

AU - Adelino, T. E.R.

AU - Oliveira, M. A.A.

AU - Silva, M. V.F.

AU - Sacchetto, L.

AU - Figueiredo, P. O.

AU - Rezende, I. M.

AU - Mello, E. M.

AU - Said, R. F.C.

AU - Santos, D. A.

AU - Ferraz, M. L.

AU - Brito, M. G.

AU - Santana, L. F.

AU - Menezes, M. T.

AU - Brindeiro, R. M.

AU - Tanuri, A.

AU - Dos Santos, F. C.P.

AU - Cunha, M. S.

AU - Nogueira, J. S.

AU - Rocco, I. M.

AU - Da Costa, A. C.

AU - Komninakis, S. C.V.

AU - Azevedo, V.

AU - Chieppe, A. O.

AU - Araujo, E. S.M.

AU - Mendonça, M. C.L.

AU - Dos Santos, C. C.

AU - Dos Santos, C. D.

AU - Mares-Guia, A. M.

AU - Nogueira, R. M.R.

AU - Sequeira, P. C.

AU - Abreu, R. G.

AU - Garcia, M. H.O.

AU - Abreu, A. L.

AU - Okumoto, O.

AU - Kroon, E. G.

AU - De Albuquerque, C. F.C.

AU - Lewandowski, K.

AU - Pullan, Steven

AU - Carroll, Miles

AU - De Oliveira, T.

AU - Sabino, E. C.

AU - Souza, R. P.

AU - Suchard, M. A.

AU - Lemey, P.

AU - Trindade, G. S.

AU - Drumond, B. P.

AU - Filippis, A. M.B.

AU - Loman, N. J.

AU - Cauchemez, S.

AU - Alcantara, L. C.J.

AU - Pybus, O. G.

N1 - Funding Information: We thank FUNED-MG and the Brazilian YFV surveillance network for their contributions. N.R.F. thanks J. F. Drexler for sharing data, N. Trovão for discussions, F. Campos for proof imaging, and P. Fonseca for proofreading. We thank Oxford Nanopore Technologies for technical support. L.C.J.A. thanks QIAGEN for reagents and equipment. A.C.d.C. and E.C.S. thank Illumina, Zymo Research, Sage Science, and Promega for donation of reagents. This work was supported in part by CNPq 400354/ 2016-0 and FAPESP 2016/01735-2. N.R.F. is supported by a Sir Henry Dale Fellowship (204311/Z/16/Z), internal GCRF grant 005073, and John Fell Research Fund grant 005166. This research received funding from the ERC (grant agreement 614725-PATHPHYLODYN) and from the Oxford Martin School. M.U.G.K. acknowledges funding from a Branco Weiss Fellowship, administered by ETH Zurich, a Training Grant from the National Institute of Child Health and Human Development (T32HD040128), and the National Library of Medicine of the National Institutes of Health (R01LM010812 and R01LM011965). S.D. is funded by the Fonds Wetenschappelijk Onderzoek (FWO, Flanders, Belgium). G.B. acknowledges support from the Interne Fondsen KU Leuven/Internal Funds KU Leuven. A.C.d.C. is funded by FAPESP 2017/00021-9. B.B.N. and S.C. are supported by the EU’s Horizon 2020 Programme through ZIKAlliance (grant 734548), the Investissement d’Avenir program, the Laboratoire d’Excellence Integrative Biology of Emerging Infectious Diseases program (grant ANR-10-LABX-62-IBEID), the Models of Infectious Disease Agent Study of the National Institute of General Medical Sciences, the AXA Research Fund, and the Association Robert Debré. P.L. and M.A.S. acknowledge funding from the European Research Council (grant agreement 725422-ReservoirDOCS) and from the Wellcome Trust Collaborative Award 206298/Z/17/Z. P.L. acknowledges support from the Research Foundation, Flanders (Fonds voor Wetenschappelijk Onderzoek, Vlaanderen, G066215N, G0D5117N, and G0B9317N). Publisher Copyright: 2017 © The Authors,

PY - 2018/8/31

Y1 - 2018/8/31

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85052626601&partnerID=8YFLogxK

U2 - 10.1126/science.aat7115

DO - 10.1126/science.aat7115

M3 - Article

C2 - 30139911

AN - SCOPUS:85052626601

SN - 0036-8075

VL - 361

SP - 894

EP - 899

JO - Science

JF - Science

IS - 6405

ER -

Genomic and epidemiological monitoring of yellow fever virus transmission potential

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