Abstract

BackgroundWest Nile virus (WNV) is a highly pathogenic flavivirus transmitted by Culex spp. mosquitoes. In North America (NA), lineage 1 WNV caused the largest outbreak of neuroinvasive disease to date, while a novel pathogenic lineage 2 strain circulates in southern Europe. To estimate WNV lineage 2 epidemic potential it is paramount to know if mosquitoes from currently WNV-free areas can support further spread of this epidemic.Methodology/Principal FindingsWe assessed WNV vector competence of Culex pipiens mosquitoes originating from north-western Europe (NWE) in direct comparison with those from NA. We exposed mosquitoes to infectious blood meals of lineage 1 or 2 WNV and determined the infection and transmission rates. We explored reasons for vector competence differences by comparing intrathoracic injection versus blood meal infection, and we investigated the influence of temperature. We found that NWE mosquitoes are highly competent for both WNV lineages, with transmission rates up to 25%. Compared to NA mosquitoes, transmission rates for lineage 2 WNV were significantly elevated in NWE mosquitoes due to better virus dissemination from the midgut and a shorter extrinsic incubation time. WNV infection rates further increased with temperature increase.Conclusions/SignificanceOur study provides experimental evidence to indicate markedly different risk levels between both continents for lineage 2 WNV transmission and suggests a degree of genotype-genotype specificity in the interaction between virus and vector. Our experiments with varying temperatures explain the current localized WNV activity in southern Europe, yet imply further epidemic spread throughout NWE during periods with favourable climatic conditions. This emphasizes the need for intensified surveillance of virus activity in current WNV disease-free regions and warrants increased awareness in clinics throughout Europe.

Highlights

  • West Nile virus (WNV; family Flaviviridae, genus Flavivirus) is an important mosquito-borne human pathogen associated with febrile illness, which may develop into severe neuroinvasive disease and death [1]

  • West Nile virus (WNV) is on the rise in Europe, with increasing numbers of human cases of neurological disease and death since 2010. It is currently unknown whether or not WNV will continue to spread to north-western Europe (NWE), in a fashion similar to the WNV epidemic sweep in the United States (1999–2004)

  • Our study is the first to investigate transmissibility in NWE Culex pipiens for lineage 2 WNV in a systematic, direct comparison with North American Culex pipiens and with the lineage 1 WNV strain

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Summary

Introduction

West Nile virus (WNV; family Flaviviridae, genus Flavivirus) is an important mosquito-borne human pathogen associated with febrile illness, which may develop into severe neuroinvasive disease and death [1]. Lineage 1 WNV strains have long been endemic in Africa, Australia, the Middle East, Asia and southern Europe [2,3]. In the 1990s, lineage 1 WNV re-emerged in southern Europe and the Middle-East [4,5,6]. In 2010, a highly pathogenic lineage 2 WNV isolate caused a large outbreak in Greece [9], which resulted in 262 cases of human disease and 35 deaths. Lineage 2 WNV quickly became endemic in South-East Europe and with annual outbreaks to date WNV disease in the region has increased seven-fold [10,11,12]. In North America (NA), lineage 1 WNV caused the largest outbreak of neuroinvasive disease to date, while a novel pathogenic lineage 2 strain circulates in southern Europe. To estimate WNV lineage 2 epidemic potential it is paramount to know if mosquitoes from currently WNV-free areas can support further spread of this epidemic

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