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

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 qPCR. 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.

YELLOW ALERT: Persistent Yellow Fever Virus Circulation among Non-Human Primates in Urban Areas of Minas Gerais State, Brazil (2021–2023)

“…The majority of the 18 positive NHPs were Callithrix penicillata (89%), which were mostly obtained in urban areas (72%) ( Table 1 ). The low YFV genomic loads observed in Callithrix , indicated by high Cq values in RTqPCR, were also previously described in other studies during periods of intense YFV circulation during the outbreaks [ 11 , 12 , 13 ], or during periods with low viral circulation after the outbreaks [ 18 , 20 ]. The lower viral loads observed in Callithrix compared to specimens of other genera could be related to their susceptibility to YFV and their role in YFV maintenance and transmission cycles should be further investigated [ 11 , 12 , 13 ].…”

“…The regions where YFV was detected here were heavily affected during the YF outbreaks in 2017/2018, with subsequent records of YF in NHPs [ 31 , 32 ]. The enduring presence of YFV could be linked to the ongoing circulation of the virus associated with previous outbreaks [ 18 ] or to a new introduction of YFV in the region, as recently described in 2021 [ 20 ]. Silva and colleagues [ 18 ] have demonstrated the maintenance of the YFV lineage related to 2017/2018 outbreaks in the enzootic cycle in MG state up to 2020.…”

“…The enduring presence of YFV could be linked to the ongoing circulation of the virus associated with previous outbreaks [ 18 ] or to a new introduction of YFV in the region, as recently described in 2021 [ 20 ]. Silva and colleagues [ 18 ] have demonstrated the maintenance of the YFV lineage related to 2017/2018 outbreaks in the enzootic cycle in MG state up to 2020. Previous studies lend further support to the continued enzootic circulation of YFV within MG since the 2017/2018 outbreaks, in NHPs [ 18 , 20 , 31 , 32 ] and vectors [ 21 ] during rainy or dry seasons, and in rural/forested or urban areas, reinforcing the fact that YFV has suitable ecological conditions for its maintenance in the state [ 33 ].…”

“…After the outbreak and extending into the current monitoring period (from July 2023 to June 2024), vectors, NHPs, and human cases of YFV infection have been continuously reported outside the Amazon Basin in Brazil [ 14 , 15 , 16 , 17 , 18 , 19 , 20 , 21 ]. These reports underscore the ongoing circulation of YFV in Southern Brazil.…”

Beyond Borders: Investigating the Mysteries of Cacipacoré, a Lesser-Studied Arbovirus in Brazil

“…In this review, we summarize our current understanding of the Cacipacoré virus’ (CPCV) host range, transmission cycles, and epidemiology, as well as its pathogenesis and the clinical outcomes of infection against the backdrop of Brazil’s complex arboviral landscape. As the country grapples with the endemicity of DENVs [ 39 , 40 ], ZIKV [ 15 , 41 , 42 ], chikungunya virus (CHIKV) [ 43 , 44 , 45 , 46 ], and the perennial risk of yellow fever epizootics [ 26 , 47 , 48 ], the potential of emerging flaviviruses necessitates closer scrutiny. With lessons learned from the ZIKV introduction in the Western Hemisphere in 2013 and the subsequent epidemic [ 14 , 49 ], understanding the biology, transmission dynamics, and epidemiology of neglected orthoflaviviruses becomes imperative for public health preparedness and response.…”