Contrasted Epidemiological Patterns of West Nile Virus Lineages 1 and 2 Infections in France from 2015 to 2019

Abstract

Since 2015, annual West Nile virus (WNV) outbreaks of varying intensities have been reported in France. Recent intensification of enzootic WNV circulation was observed in the South of France with most horse cases detected in 2015 (n = 49), 2018 (n = 13), and 2019 (n = 13). A WNV lineage 1 strain was isolated from a horse suffering from West Nile neuro-invasive disease (WNND) during the 2015 episode in the Camargue area. A breaking point in WNV epidemiology was achieved in 2018, when WNV lineage 2 emerged in Southeastern areas. This virus most probably originated from WNV spread from Northern Italy and caused WNND in humans and the death of diurnal raptors. WNV lineage 2 emergence was associated with the most important human WNV epidemics identified so far in France (n = 26, including seven WNND cases and two infections in blood and organ donors). Two other major findings were the detection of WNV in areas with no or limited history of WNV circulation (Alpes-Maritimes in 2018, Corsica in 2018-2019, and Var in 2019) and distinct spatial distribution of human and horse WNV cases. These new data reinforce the necessity to enhance French WNV surveillance to better anticipate future WNV epidemics and epizootics and to improve the safety of blood and organ donations.

Keywords: France; West Nile; arbovirus; emerging infectious diseases; lineages 1 and 2; zoonotic.

Figure 1

A graph that shows the total number and clinical forms of human and equine laboratory-confirmed cases per year in France from 2015 to 2019. The highest number of human and equine cases for the 2015–2019 period was reported in 2018 and 2015 respectively.

Figure 2

(a) Weekly comparison of human and equine WNV cases notifications in 2015 in France and (b) weekly comparison of human and equine WNV cases notifications in 2018 in France. Diagrams depict dates of onset of symptoms whenever available, and in the absence of data on symptoms onset, date of veterinary samples (five cases in 2018) or sample reporting (one case in 2018) are shown.

Figure 3

(a,b) Comparison of WNV case distribution in humans (blue dots) and horses (red dots) during 2015–2019; (c,d) Period 2015; (e,f) Period 2017; (g,h) Period 2018; and (i,j) Period 2019. In 2018, distribution of bird cases is represented by an orange star.

Figure 4

(a) Number of Culex pipiens mosquitoes trapped in three departments of the Camargue area (Bouches-Du-Rhône, Gard, and Hérault) in June during the 2015–2019 seasons and (b) number of Culex pipiens mosquitoes trapped in three departments of the Camargue area (Bouches-Du-Rhône, Gard and Hérault) between June to October during the 2015–2019 seasons.

Figure 5

Molecular phylogenetic tree of WNV complete genome sequences detected in one horse (2015, black circle) and two birds (2018, black triangles) in France. The evolutionary history was inferred using the Neighbor–Joining and Maximum Likelihood methods in MEGA7 [36]. The optimal tree generated using the Neighbor–Joining method with the sum of branch length = 1,28228091 is shown. The percentage of replicate trees in which the associated taxa clustered together in the bootstrap test (1000 replicates) are shown next to the branches. The tree is drawn to scale, with branch lengths expressed in the same units as for the evolutionary distances used to infer the phylogenetic tree. The evolutionary distances were computed using the Jukes–Cantor method and are in the units of the number of base substitutions per site. The analysis involved 50 nucleotide sequences, including Japanese Encephalitis Virus as an outgroup. All positions containing gaps and missing data were eliminated. There were a total of 10,475 positions in the final dataset.