West Nile Virus Surveillance in 2013 via Mosquito Screening in Northern Italy and the Influence of Weather on Virus Circulation

Abstract

West Nile virus (WNV) is a recently re-emerged health problem in Europe. In Italy, an increasing number of outbreaks of West Nile disease, with occurrences of human cases, have been reported since 2008. This is particularly true in northern Italy, where entomological surveillance systems have been implemented at a regional level. The aim of this study was to use, for the first time, all the entomological data collected in the five regions undergoing surveillance for WNV in northern Italy to characterize the viral circulation (at a spatial and temporal scale), identify potential mosquito vectors, and specify relationships between virus circulation and meteorological conditions. In 2013, 286 sites covering the entire Pianura Padana area were monitored. A total of 757,461 mosquitoes were sampled. Of these, 562,079 were tested by real-time PCR in 9,268 pools, of which 180 (1.9%) were positive for WNV. The largest part of the detected WNV sequences belonged to lineage II, demonstrating that, unlike those in the past, the 2013 outbreak was mainly sustained by this WNV lineage. This surveillance also detected the Usutu virus, a WNV-related flavivirus, in 241 (2.6%) pools. The WNV surveillance systems precisely identified the area affected by the virus and detected the viral circulation approximately two weeks before the occurrence of onset of human cases. Ninety percent of the sampled mosquitoes were Culex pipiens, and 178/180 WNV-positive pools were composed of only this species, suggesting this mosquito is the main WNV vector in northern Italy. A significantly higher abundance of the vector was recorded in the WNV circulation area, which was characterized by warmer and less rainy conditions and greater evapotranspiration compared to the rest of the Pianura Padana, suggesting that areas exposed to these conditions are more suitable for WNV circulation. This observation highlights warmer and less rainy conditions as factors able to enhance WNV circulation and cause virus spillover outside the sylvatic cycle.

Usutu virus: current knowledge and future perspectives

“…51 During a regional WNV surveillance program based on reverse transcription polymerase chain reaction (RT-PCR) detection conducted in Italy in the same year, 56 pools (54 of C. pipiens and 2 of Aedes albopictus) out of 1,789 mosquito pools were USUV positive by RT-PCR, 52 and similar results have been reported since then in different regions of Italy. [53][54][55][56][57] These findings confirm the role of Culex species as the main vector in the virus cycle, although Aedes mosquitoes also play a role on it, and point to an association between the presence of USUV-positive mosquitoes and drought conditions and a wide temperature range. USUV was also isolated from a pool of C. pipiens mosquitoes trapped in summer of 2010 in Germany 58 and from Culex modestus in Czech Republic the same year.…”

Recent rapid changes in the spatio‐temporal distribution of West Nile Neuro‐invasive Disease in Italy

“…It has been hypothesized that meteorological anomalies during spring/summer might affect the seasonality of the disease by anticipating the starting time of the transmission period and favour an early increase in the number of infective mosquitoes (Paz, ). Interestingly in 2013, the year with the highest number of WNND cases during the study period was characterized by extraordinarily hot summer temperatures and areas where both infected humans and mosquitoes were observed were characterized by higher summer temperatures, compared to the areas without evidence of viral circulation (Calzolari et al, ). It has also been shown that periods characterized by high temperatures and above than average rainfall can affect incidence of human WNV infection cases in the following weeks (Moirano et al, ; Paz et al, ).…”

A quantitative comparison of West Nile virus incidence from 2013 to 2018 in Emilia-Romagna, Italy

“…Each trap site was geo-referenced and worked fortnightly for one night, from 17:00 to 9:00 the next day. Sampled mosquitoes were identified at the species level with morphological keys [24], then pooled, with a maximum of 200 specimens per pool, and screened for WNV detection via PCR [16,21].…”

“…Here, we provide a quantitative comparison between the 2018 transmission season and previous years (2013-2017), using a transmission dynamics temperature-dependent model [12] informed by data on Cx. pipiens abundance, the main WNV vector in the area [16]. Several mathematical models for WNV transmission dynamics have been proposed, from simpler models in a constant environment [17,18] to models that consider the dependence of parameters on environmental variables [19,20]; in our case, the model is fitted to WNV prevalence of mosquito pools collected from the trap sites across the region during the 6 years under study, while human cases are used for validation.…”