Impact of temperature on the extrinsic incubation period of Zika virus in Aedes aegypti

Abstract

Since Zika virus (ZIKV) emerged as a global human health threat, numerous studies have pointed to Aedes aegypti as the primary vector due to its high competence and propensity to feed on humans. The majority of vector competence studies have been conducted between 26-28˚C, but arboviral extrinsic incubation periods (EIPs), and therefore transmission efficiency, are known to be affected strongly by temperature. To better understand the relationship between ZIKV EIPs and temperature, we evaluated the effect of adult mosquito exposure temperature on ZIKV infection, dissemination, and transmission in Ae. aegypti at four temperatures: 18˚C, 21˚C, 26˚C, and 30˚C. Mosquitoes were exposed to viremic mice infected with a 2015 Puerto Rican ZIKV strain, and engorged mosquitoes were sorted into the four temperatures with 80% RH and constant access to 10% sucrose. ZIKV infection, dissemination, and transmission rates were assessed via RT-qPCR from individual mosquito bodies, legs and wings, and saliva, respectively, at three to five time points per temperature from three to 31 days, based on expectations from other flavivirus EIPs. The median time from ZIKV ingestion to transmission (median EIP, EIP 50) at each temperature was estimated by fitting a generalized linear mixed model for each temperature. EIP 50 ranged from 5.1 days at 30˚C to 24.2 days at 21˚C. At 26˚C, EIP 50 was 9.6 days. At 18˚C, only 15% transmitted by day 31 so EIP 50 could not be estimated. This is among the first studies to characterize the effects of temperature on ZIKV EIP in Ae. aegypti, and the first to do so based on feeding of mosquitoes on a live, viremic host. This information is critical for modeling ZIKV transmission dynamics to understand geographic and seasonal limits of ZIKV risk; it is especially relevant for determining risk in subtropical regions with established Ae. aegypti populations and relatively high rates of return travel from the tropics (e.g. California or Florida), as these regions typically experience cooler temperature ranges than tropical regions.

Asynchronicity of endemic and emerging mosquito-borne disease outbreaks in the Dominican Republic

“…We assumed that climatological factors did not vary widely between provinces during a given season. Our reasoning followed that the rate of viral transmission is limited by the extrinsic incubation period (EIP) of the virus in the mosquito vector 37 , and the EIP for Aedes mosquitoes is mainly influenced by temperature 38 – 40 . Therefore, because we did not expect transmission rates to vary widely between provinces, provincial outbreaks that peaked soon after the reporting system was implemented would indicate that transmission in those provinces preceded the establishment of this system.…”

The Genetic Basis for Salivary Gland Barriers to Arboviral Transmission

“…A low percentage of mosquitoes injected with DENV2 genotypes remained uninfected, but all mosquitoes injected with CHIKV or ZIKV genotypes were infected ( Table 1 ). The extrinsic incubation period varies among virus genotype and mosquito strain, and it is greatly dependent on environmental factors, such as temperature and effective dose of virus [ 50 , 51 , 52 ]. However, a minimum of one week after initial infection is required for DENV to be released and detected in saliva, indicating an absence of SGEB and SGIB [ 51 ].…”

Modeling intra-mosquito dynamics of Zika virus and its dose-dependence confirms the low epidemic potential of Aedes albopictus

“…g ., mosquito virome [ 43 ], endogenous non-retroviral elements [ 44 , 45 ], or bacterial microbiome [ 46 ]) or environmental ( e . g ., temperature [ 47 , 48 ], rearing or experimental settings) conditions might further impede comparisons across vector competence studies [ 49 ]. Systemic infection dynamic was strongly influenced by the infectious blood meal dose, with a 30 days shift of median time estimates to reach 50% systemic infection between 5 log 10 FFU/mL and 8 log 10 FFU/mL.…”

“…In addition, transmission efficiency was reported to be strongly affected by temperature: median EIP was shown to shift from 9.6 days at 26°C to 5.1 days at 30°C for Ae . aegypti mosquitoes infected with ZIKV [ 47 ]. ZIKV might also have the opportunity to evolve towards shorter intra-mosquito dynamics, as had already occurred in other system [ 58 ].…”