Ecological drivers of sustained enzootic yellow fever virus transmission in Brazil, 2017–2021

Author:

Silva Natália Ingrid Oliveira,Albery Gregory F.,Arruda Matheus Soares,Oliveira Gabriela Fernanda Garcia,Costa Thaís Alkifeles,de Mello Érica Munhoz,Moreira Gabriel Dias,Reis Erik Vinícius,Silva Simone Agostinho da,Silva Marlise Costa,de Almeida Munique Guimarães,Becker Daniel J.,Carlson Colin J.,Vasilakis Nikos,Hanley Kathryn A.,Drumond Betânia PaivaORCID

Abstract

Beginning December 2016, sylvatic yellow fever (YF) outbreaks spread into southeastern Brazil, and Minas Gerais state experienced two sylvatic YF waves (2017 and 2018). Following these massive YF waves, we screened 187 free-living non-human primate (NHPs) carcasses collected throughout the state between January 2019 and June 2021 for YF virus (YFV) using RTqPCR. One sample belonging to a Callithrix, collected in June 2020, was positive for YFV. The viral strain belonged to the same lineage associated with 2017–2018 outbreaks, showing the continued enzootic circulation of YFV in the state. Next, using data from 781 NHPs carcasses collected in 2017–18, we used generalized additive mixed models (GAMMs) to identify the spatiotemporal and host-level drivers of YFV infection and intensity (an estimation of genomic viral load in the liver of infected NHP). Our GAMMs explained 65% and 68% of variation in virus infection and intensity, respectively, and uncovered strong temporal and spatial patterns for YFV infection and intensity. NHP infection was higher in the eastern part of Minas Gerais state, where 2017–2018 outbreaks affecting humans and NHPs were concentrated. The odds of YFV infection were significantly lower in NHPs from urban areas than from urban-rural or rural areas, while infection intensity was significantly lower in NHPs from urban areas or the urban-rural interface relative to rural areas. Both YFV infection and intensity were higher during the warm/rainy season compared to the cold/dry season. The higher YFV intensity in NHPs in warm/rainy periods could be a result of higher exposure to vectors and/or higher virus titers in vectors during this time resulting in the delivery of a higher virus dose and higher viral replication levels within NHPs. Further studies are needed to better test this hypothesis and further compare the dynamics of YFV enzootic cycles between different seasons.

Funder

National Institute of Allergy and Infectious Diseases

National Science Foundation

Conselho Nacional de Desenvolvimento Científico e Tecnológico

FAPEMIG

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior

Publisher

Public Library of Science (PLoS)

Subject

Infectious Diseases,Public Health, Environmental and Occupational Health

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