Abstract
São Paulo, a densely inhabited state in southeast Brazil that contains the fourth most populated city in the world, recently experienced its largest yellow fever virus (YFV) outbreak in decades. YFV does not normally circulate extensively in São Paulo, so most people were unvaccinated when the outbreak began. Surveillance in non-human primates (NHPs) is important for determining the magnitude and geographic extent of an epizootic, thereby helping to evaluate the risk of YFV spillover to humans. Data from infected NHPs can give more accurate insights into YFV spread than when using data from human cases alone. To contextualise human cases, identify epizootic foci and uncover the rate and direction of YFV spread in São Paulo, we generated and analysed virus genomic data and epizootic case data from NHPs in São Paulo. We report the occurrence of three spatiotemporally distinct phases of the outbreak in São Paulo prior to February 2018. We generated 51 new virus genomes from YFV positive cases identified in 23 different municipalities in São Paulo, mostly sampled from NHPs between October 2016 and January 2018. Although we observe substantial heterogeneity in lineage dispersal velocities between phylogenetic branches, continuous phylogeographic analyses of generated YFV genomes suggest that YFV lineages spread in São Paulo at a mean rate of approximately 1km per day during all phases of the outbreak. Viral lineages from the first epizootic phase in northern São Paulo subsequently dispersed towards the south of the state to cause the second and third epizootic phases there. This alters our understanding of how YFV was introduced into the densely populated south of São Paulo state. Our results shed light on the sylvatic transmission of YFV in highly fragmented forested regions in São Paulo state and highlight the importance of continued surveillance of zoonotic pathogens in sentinel species.
Highlights
Yellow fever (YF) is an acute haemorrhagic disease caused by yellow fever virus (YFV), a single-stranded positive-sense RNA virus from the Flavivirus genus
In Brazil, YFV typically circulates among non-human primates (NHPs), and human cases represent isolated spill over events from this predominantly sylvatic cycle
Understanding the epidemiological dynamics and spread of YFV in NHPs is critical for contextualising human cases, and guiding vaccination strategies that can better protect local human populations
Summary
Yellow fever (YF) is an acute haemorrhagic disease caused by yellow fever virus (YFV), a single-stranded positive-sense RNA virus from the Flavivirus genus. Clinical manifestations of YF in humans range from inapparent or mild disease in up to 80% of infected cases, to severe hepatitis and haemorrhagic disease. The fatality rate among patients who develop visceral disease can range from 20% to 60% [2]. YFV is primarily transmitted in the Americas in a sylvatic cycle between non-human primates (NHPs) and tree-dwelling mosquitoes (primarily Haemagogus janthinomys, Haemagogus leucocelaenus and more rarely mosquitoes of the Sabethes genus) [3,4,5]. The urban cycle of YFV, in which YFV is transmitted between humans and Aedes aegypti mosquitoes, has not been observed in the Americas since the 1940s [2,6].
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