West Nile virus transmission in the Metropolitan Area of Barcelona (Spain): A One-Health surveillance approach

Abstract

West Nile virus (WNV), mainly transmitted by Culex mosquitoes, poses significant health risks to humans and horses, particularly in endemic regions. The first detection of WNV lineage 2 in Spain was in 2017 in Catalonia (northeastern Spain). In 2023, WNV was confirmed in a young yellow-legged gull and a probable human case was notified within the urban settings. We aimed to define the zone of WNV circulation in the Barcelona Metropolitan Area where these infections occurred and the effectiveness of the One Health approach for early WNV detection. The Catalan WNV surveillance and control programs includes the testing of horses, birds, mosquitoes and humans following molecular and serological methods. Phylogenetic analyses were performed to determine the origin of the circulating virus. IgM-positive data from both active and passive surveillance in horses identified the area of WNV circulation and suggested that WNV circulation happened either before or concurrently with human and bird infections in the agricultural and peri-urban areas. Furthermore, a new WNV introduction was discarded by phylogenetic studies, demonstrating that WNV lineage 2 has been established in Catalonia, albeit at a low level of circulation since the virus was not detected in blood donors. Our findings underscore the importance of integrating active and passive surveillance strategies to early assess WNV circulation and activate public health responses. The study highlights the role of wildlife in the WNV transmission and emphasizes the need for ongoing monitoring in animals and also mosquito control measures to mitigate the risk of animal and human infections.

Keywords: Animal health; Arbovirus; Flavivirus; Human health; Mosquito vectors; Public health surveillance; Vector-borne diseases; Zoonosis.

Fig. 1

Location of the regular mosquito traps for mosquito surveillance (empty squares), mosquito traps added in 2023 for WNV surveillance (black circles), and mosquito traps previously used for mosquito surveillance that were used in 2023 for WNV detection (black squares).

Fig. 2

A) Distribution of the West Nile virus (WNV) outbreak in the Barcelona Metropolitan Area in 2023. The red triangle marks the location of the WNV-positive yellow-legged gull, the inverted red triangle indicates the probable human case, and the circles show the WNV IgM-positive (red) or WNV IgM-negative (green) horse herds. B) Timeline of the WNV outbreak. The top section illustrates suspected cases (black arrows) and confirmed or probable cases (red arrow) detected by passive surveillance in birds, horses and humans. The middle section represents the equine serosurvey, with red squares denoting WNV IgM-positive horse herds and green squares representing WNV IgM-negative herds. The bottom section shows mosquito surveillance, with all samples testing WNV RT-qPCR negative (green). The number within the squares correspond to the order of sampling sequence shown in Fig. 2A. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 3

Counts of Cx. pipiens females collected with EVS-CO₂ traps by the Mosquito Control Service in different environments from week 18 to week 46, from 2021 to 2023. Pre and post indicate the period before and after WNV detection in the yellow-legged gull. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 4

The dates of positive (red) and negative (black) WNV IgM results in individual horses from the study in the BMA. Red diamond represents sample obtained by passive surveillance. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

Fig. 5

Phylogenetic tree of West Nile virus lineage 2 isolates constructed using the Maximum Likelihood method and Tamura-Nei model [31]. The tree with the highest log likelihood (−21,778.50) is shown, with bootstrap support values displayed next to branches. The Italian Lombardy cluster, highlighted in purple, includes our 2023 isolate (AC1720, which has the following GenBank code number: PQ641624 and is highlighted in red). The tree is scaled to substitutions per site using 51 nucleotide sequences and10312 positions. Evolutionary analyses were conducted in MEGA11 [30]. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)