ABSTRACT
Dengue, chikungunya, and Zika virus epidemics transmitted by Aedes aegypti mosquitoes have recently (re)emerged and spread throughout the Americas, Southeast Asia and the Pacific Islands, and elsewhere. Understanding how environmental conditions affect epidemic magnitude and duration is critical for predicting and responding to the geographic and seasonal spread of disease. Here, we develop the first dynamic disease transmission model for dengue virus and Aedes aegypti mosquitoes that integrates mechanistic, empirically parameterized, and independently validated mosquito and virus trait thermal responses under seasonally varying temperatures. With the model, we examine the influence of variation in seasonal temperature regime on epidemic dynamics. We find that at both constant and seasonally varying temperatures, warmer temperatures at the start of epidemics promote more rapid epidemics due to faster burnout of the susceptible population. By contrast, intermediate temperatures (˜24°C) at epidemic onset produced the largest epidemics in a seasonally varying temperature regime. When seasonal temperature variation was low, 25-35°C annual average temperatures produced the largest epidemics, but this range shifts to cooler temperatures as seasonal temperature variation increases. Tropical and subtropical cities such as Rio de Janeiro, Fortaleza, and Salvador, Brazil; Cali, Cartagena, and Baranquilla, Colombia; Delhi, India; Guangzhou, China; and Manila, Philippines have mean annual temperatures and seasonal temperature ranges that produce the largest epidemics. However, more temperate cities like Shanghai, China had high epidemic suitability because large seasonal variation offset moderate annual average temperatures. By accounting for seasonal variation in temperature, our model provides a baseline for mechanistically understanding environmental suitability for virus transmission by Aedes aegypti. Overlaying the impact of human activities and socioeconomic factors onto this mechanistic temperature-dependent framework is critical for understanding likelihood and magnitude of outbreaks.
NON-TECHNICAL SUMMARY Mosquito-borne viruses like dengue, Zika, and chikungunya have recently caused large epidemics that are partly driven by temperature. Using a mathematical model built from laboratory experimental data for Aedes aegypti mosquitoes and dengue virus, we examine the impact of variation in seasonal temperature regimes on epidemic size and duration. At constant temperatures, both low and high temperatures (20°C and 35°C) produce small epidemics, while intermediate temperatures like 25°C and 30°C produce much larger epidemics. In seasonally varying temperature environments, epidemics peak more rapidly at higher starting temperatures. Intermediate starting temperatures produce the largest epidemics. Seasonal mean temperatures of 25-35°C are most suitable for large epidemics when seasonality is low, but in more variable seasonal environments epidemic suitability peaks at lower annual average temperatures. Tropical and sub-tropical cities have the highest temperature suitability for epidemics, but more temperate cities with high seasonal variation also have the potential for very large epidemics.