The burden of arbovirus diseases in Brazil has increased within the past decade due to the emergence of chikungunya and Zika and endemic circulation of all four dengue serotypes. Changes in temperature and rainfall patterns may alter conditions to favor vector-host transmission and allow for cyclic re-emergence of disease. We sought to determine the impact of climate conditions on arbovirus co-circulation in Rio de Janeiro, Brazil. We assessed the spatial and temporal distributions of chikungunya, dengue, and Zika cases from Brazil's national notifiable disease information system (SINAN) and created autoregressive integrated moving average models (ARIMA) to predict arbovirus incidence accounting for the lagged effect of temperature and rainfall. Each year, we estimate that the combined arboviruses were associated with an average of 8429 to 10,047 lost Disability-Adjusted Life Years (DALYs). After controlling for temperature and precipitation, our model predicted a three cycle pattern where large arbovirus outbreaks appear to be primed by a smaller scale surge and followed by a lull of cases. These dynamic arbovirus patterns in Rio de Janeiro support a mechanism of susceptibility enhancement until the theoretical threshold of population immunity allows for temporary cross protection among certain arboviruses. This suspected synergy presents a major public health challenge due to overlapping locations and seasonality of arbovirus diseases, which may perpetuate disease burden and overwhelm the health system.

Background

The 2017-2018 yellow fever virus (YFV) outbreak in southeastern Brazil marked a reemergence of YFV in urban states that had been YFV-free for nearly a century. Unlike earlier urban YFV transmission, this epidemic was driven by forest mosquitoes. The objective of this study was to evaluate environmental drivers of this outbreak.

Methodology/principal findings

Using surveillance data from the Brazilian Ministry of Health on human and non-human primate (NHP) cases of YFV, we traced the spatiotemporal progression of the outbreak. We then assessed the epidemic timing in relation to drought using a monthly Standardized Precipitation Evapotranspiration Index (SPEI) and evaluated demographic risk factors for rural or outdoor exposure amongst YFV cases. Finally, we developed a mechanistic framework to map the relationship between drought and YFV. Both human and NHP cases were first identified in a hot, dry, rural area in northern Minas Gerais before spreading southeast into the more cool, wet urban states. Outbreaks coincided with drought in all four southeastern states of Brazil and an extreme drought in Minas Gerais. Confirmed YFV cases had an increased odds of being male (OR 2.6; 95% CI 2.2-3.0), working age (OR: 1.8; 95% CI: 1.5-2.1), and reporting any recent travel (OR: 2.8; 95% CI: 2.3-3.3). Based on this data as well as mosquito and non-human primate biology, we created the "Mono-DrY" mechanistic framework showing how an unusual drought in this region could have amplified YFV transmission at the rural-urban interface and sparked the spread of this epidemic.

Conclusions/significance

The 2017-2018 YFV epidemic in Brazil originated in hot, dry rural areas of Minas Gerais before expanding south into urban centers. An unusually severe drought in this region may have created environmental pressures that sparked the reemergence of YFV in Brazil's southeastern cities.