Reproducing the Rift Valley fever virus mosquito-lamb-mosquito transmission cycle

Paul J Wichgers Schreur,Tessa M Visser,Jet Kant,Lucien Van Keulen,Constantianus J M Koenraadt,Jeroen Kortekaas,Chantal B F Vogels,Rianka P M Vloet,Jose L Gonzales

doi:10.1038/s41598-020-79267-1

Paul J Wichgers Schreur, Tessa M Visser + Show 7 more

Open Access

https://doi.org/10.1038/s41598-020-79267-1

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Abstract

Rift Valley fever virus (RVFV) is a mosquito-borne bunyavirus that is pathogenic to ruminants and humans. The virus is endemic to Africa and the Arabian Peninsula where outbreaks are characterized by abortion storms and mortality of newborns, particularly in sheep herds. Vector competence experiments in laboratory settings have suggested that over 50 mosquito species are capable of transmitting RVFV. Transmission of mosquito-borne viruses in the field is however influenced by numerous factors, including population densities, blood feeding behavior, extrinsic incubation period, longevity of vectors, and viremia levels in vertebrate hosts. Animal models to study these important aspects of RVFV transmission are currently lacking. In the present work, RVFV was transmitted to European (Texel-swifter cross-breed) lambs by laboratory-reared Aedes aegypti mosquitoes that were infected either by membrane feeding on a virus-spiked blood meal or by feeding on lambs that developed viremia after intravenous inoculation of RVFV. Feeding of mosquitoes on viremic lambs resulted in strikingly higher infection rates as compared to membrane feeding. Subsequent transmission of RVFV from lamb to lamb by infected mosquitoes was highly efficient in both models. The animal models described here can be used to study mosquito-mediated transmission of RVFV among the major natural target species and to evaluate the efficacy of vaccines against mosquito-mediated RVFV infection.

Highlights

Rift Valley fever virus (RVFV) is a mosquito-borne bunyavirus that is pathogenic to ruminants and humans
Analysis of daily collected plasma samples with reverse-transcriptase quantitative PCR (RT-qPCR) and virus isolation demonstrated that all lambs developed high viremia, which peaked on day 2 post inoculation (Fig. 2b), confirming that mosquito feeding occurred at peak viremia
One lamb (#159) acutely succumbed to the infection on day 4, one lamb acutely succumbed on day 5 (#157), one lamb had to be euthanized after reaching a humane end-point (HEP) on day 6 (#161) and one on day 7 (#162), resulting in a case fatality rate (CFR) of 67% (Fig. 2c)

Summary

Introduction

Rift Valley fever virus (RVFV) is a mosquito-borne bunyavirus that is pathogenic to ruminants and humans. Interepizootic maintenance of RVFV is possibly explained by vertical transmission of the virus to the eggs of floodwater Aedes mosquitoes[8] These species oviposit near shallow wetlands, known as dambos, which dry out during periods of drought and flood during heavy rains. To more firmly establish the ability of a mosquito species to act as a vector, experiments are required in which the virus is transmitted among susceptible animals via infected mosquitoes In such experiments, factors such as mosquito population density, blood feeding behavior, and longevity can be taken into account to determine the vectorial capacity of a mosquito vector[13].

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