Research Article: West Nile Virus: High Transmission Rate in North-Western European Mosquitoes Indicates Its Epidemic Potential and Warrants Increased Surveillance

Date Published: July 30, 2015

Publisher: Public Library of Science

Author(s): Jelke J. Fros, Corinne Geertsema, Chantal B. Vogels, Peter P. Roosjen, Anna-Bella Failloux, Just M. Vlak, Constantianus J. Koenraadt, Willem Takken, Gorben P. Pijlman, Song Liang.

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.

Partial Text: 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]. The pathogenic isolates of WNV can be classified into two lineages. 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 [4–6]. In 1999, lineage 1 WNV was unintentionally introduced into New York City from where it spread rapidly across the United States where it is now endemic [7]. With an accumulated 17,463 cases of neuroinvasive disease and 1,668 reported deaths between 1999 and 2013, this outbreak quickly evolved into the largest outbreak of neuroinvasive disease to date [8]. Lineage 2 WNV strains have been endemic in sub-Saharan Africa and Madagascar and were previously considered to be of low pathogenicity [2,3]. 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 then quickly became endemic in South-East Europe and with annual outbreaks to date WNV disease in the region has increased seven-fold [10–12]. At present, WNV disease does not extend into north-western Europe (NWE) [11].

Here we show that both pathogenic lineages of WNV can effectively infect mosquitoes from NWE. Our finding that two geographically separated Culex pipiens populations (NWE and NA) have a markedly different vector competence for WNV-lin2, suggests a degree of genotype-genotype specificity in the interaction between virus and vector. Alternatively, the presence of certain endosymbionts or insect-specific flaviviruses can have an effect on the vector competence as well [30,31]. As the differential infection rate is only apparent when WNV is infected orally and not via intrathoracic injections, this suggests that WNV-lin2 escapes more effectively from the midgut epithelial cells in mosquitoes from NWE compared to those from NA.



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