TY - JOUR

T1 - West Nile virus spread in Europe

T2 - Phylogeographic pattern analysis and key drivers

AU - Lu, Lu

AU - Zhang, Feifei

AU - Munnink, Bas B.Oude

AU - Munger, Emmanuelle

AU - Sikkema, Reina S.

AU - Pappa, Styliani

AU - Tsioka, Katerina

AU - Sinigaglia, Alessandro

AU - Dal Molin, Emanuela

AU - Shih, Barbara B.

AU - Günther, Anne

AU - Pohlmann, Anne

AU - Ziegler, Ute

AU - Beer, Martin

AU - Taylor, Rachel A.

AU - Bartumeus, Frederic

AU - Woolhouse, Mark

AU - Aarestrup, Frank M.

AU - Barzon, Luisa

AU - Papa, Anna

AU - Lycett, Samantha

AU - Koopmans, Marion P.G.

N1 - Publisher Copyright: © 2024 Lu et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

PY - 2024/1/25

Y1 - 2024/1/25

N2 - Background West Nile virus (WNV) outbreaks in birds, humans, and livestock have occurred in multiple areas in Europe and have had a significant impact on animal and human health. The patterns of emergence and spread of WNV in Europe are very different from those in the US and understanding these are important for guiding preparedness activities. Methods We mapped the evolution and spread history of WNV in Europe by incorporating viral genome sequences and epidemiological data into phylodynamic models. Spatially explicit phylogeographic models were developed to explore the possible contribution of different drivers to viral dispersal direction and velocity. A "skygrid-GLM"approach was used to identify how changes in environments would predict viral genetic diversity variations over time. Findings Among the six lineages found in Europe, WNV-2a (a sub-lineage of WNV-2) has been predominant (accounting for 73% of all sequences obtained in Europe that have been shared in the public domain) and has spread to at least 14 countries. In the past two decades, WNV- 2a has evolved into two major co-circulating clusters, both originating from Central Europe, but with distinct dynamic history and transmission patterns. WNV-2a spreads at a high dispersal velocity (88km/yr-215 km/yr) which is correlated to bird movements. Notably, amongst multiple drivers that could affect the spread of WNV, factors related to land use were found to strongly influence the spread of WNV. Specifically, the intensity of agricultural activities (defined by factors related to crops and livestock production, such as coverage of cropland, pasture, cultivated and managed vegetation, livestock density) were positively associated with both spread direction and velocity. In addition, WNV spread direction was associated with high coverage of wetlands and migratory bird flyways. Conclusion Our results suggest that-in addition to ecological conditions favouring bird- and mosquitopresence- agricultural land use may be a significant driver of WNV emergence and spread. Our study also identified significant gaps in data and the need to strengthen virological surveillance in countries of Central Europe from where WNV outbreaks are likely seeded. Enhanced monitoring for early detection of further dispersal could be targeted to areas with high agricultural activities and habitats of migratory birds.

AB - Background West Nile virus (WNV) outbreaks in birds, humans, and livestock have occurred in multiple areas in Europe and have had a significant impact on animal and human health. The patterns of emergence and spread of WNV in Europe are very different from those in the US and understanding these are important for guiding preparedness activities. Methods We mapped the evolution and spread history of WNV in Europe by incorporating viral genome sequences and epidemiological data into phylodynamic models. Spatially explicit phylogeographic models were developed to explore the possible contribution of different drivers to viral dispersal direction and velocity. A "skygrid-GLM"approach was used to identify how changes in environments would predict viral genetic diversity variations over time. Findings Among the six lineages found in Europe, WNV-2a (a sub-lineage of WNV-2) has been predominant (accounting for 73% of all sequences obtained in Europe that have been shared in the public domain) and has spread to at least 14 countries. In the past two decades, WNV- 2a has evolved into two major co-circulating clusters, both originating from Central Europe, but with distinct dynamic history and transmission patterns. WNV-2a spreads at a high dispersal velocity (88km/yr-215 km/yr) which is correlated to bird movements. Notably, amongst multiple drivers that could affect the spread of WNV, factors related to land use were found to strongly influence the spread of WNV. Specifically, the intensity of agricultural activities (defined by factors related to crops and livestock production, such as coverage of cropland, pasture, cultivated and managed vegetation, livestock density) were positively associated with both spread direction and velocity. In addition, WNV spread direction was associated with high coverage of wetlands and migratory bird flyways. Conclusion Our results suggest that-in addition to ecological conditions favouring bird- and mosquitopresence- agricultural land use may be a significant driver of WNV emergence and spread. Our study also identified significant gaps in data and the need to strengthen virological surveillance in countries of Central Europe from where WNV outbreaks are likely seeded. Enhanced monitoring for early detection of further dispersal could be targeted to areas with high agricultural activities and habitats of migratory birds.

U2 - 10.1371/journal.ppat.1011880

DO - 10.1371/journal.ppat.1011880

M3 - Journal article

C2 - 38271294

AN - SCOPUS:85183452103

VL - 20

SP - e1011880

JO - PLoS Pathogens

JF - PLoS Pathogens

SN - 1553-7366

IS - 1

M1 - e1011880

ER -