Exceptional Bluetongue virus (BTV) and Epizootic hemorrhagic disease virus (EHDV) circulation in France in 2023

Abstract

Bluetongue (BT) and Epizootic Hemorrhagic Disease (EHD) are two notifiable animal diseases transmitted to ruminants by small hematophagous midges belonging to the Culicoides genus. The etiological agents, Bluetongue virus (BTV) and Epizootic hemorrhagic disease virus (EHDV), are both members of the Sedoreoviridae family and Orbivirus genus, which include double-stranded (ds) RNA segmented genomes (10 segments). By the end of the summer 2023, first's outbreaks of EHD were reported from the south west of France, concurrently with unexpectedly severe BT cases in Central France and Corsica. Within a few weeks, numerous BT and EHD outbreaks were recorded with significant sanitary and economic impact on cattle and sheep farms (no sanitary impact of EHD for sheep). Using a customized SISPA approach and the nanopore sequencing technology we successfully recovered genomic sequences from viral isolates and blood samples from infected animals from EHD and BT outbreaks. Three different viruses were responsible for these outbreaks: EHDV-8, BTV-8 and BTV-4. The EHDV-8 strain detected in France corresponded to the strain circulating in Tunisia, Sardinia and Spain since 2021 and 2022. A new BTV-8 strain of unknown origin, clearly different from the enzootic strain circulating in France since 2015, was responsible of the BT outbreaks in domestic ruminants in 2023 on both mainland France and Corsica. A second BTV, BTV-4, also involved in BT outbreaks in Corsica, corresponded to a BTV-4 strain occasionally detected on Corsica island since 2016, suggesting either a new introduction of this strain or a silent circulation on the field. The exceptional nature of orbivirus epizootics in France in 2023, including new introduction, emergence or incursions, raises numerous questions regarding BTV and EHDV dynamics and epidemiology and stresses out the need to identify factors involved in these emergences.

Keywords: Bluetongue virus; Emergences; Epizootic hemorrhagic disease virus; France; genome sequencing; nanopore.

Fig. 1

Map of the French municipalities infected by EHDV-8 in 2023, on the 31st of May, 2024. Source: Direction Générale de l'Alimentation / Ministère de l'Agriculture et de la Souveraineté Alimentaire.

Fig. 2

Phylogenetic analysis of S2 (A) and S6 (B) sequences of the French BTV-8 strains. Phylogenetic analysis of S2 (A) and S6 (B) sequences of BTV-8 strains using the maximum likelihood method and Tamura-Nei model with 1000 bootstrap replicates in MEGA X. This analysis involved 34 (A) and 31 (B) nucleotide sequences, there were a total of 2940 (A) and 1610 (B) positions in the final dataset. Bootstrap values appeared at the corresponding nodes. In the phylogenetic tree, GenBank sequences, BT serotype, country and year of sample collection are given. In dark blue, sequences from the newly introduced BTV-8 strain; in light blue sequences from the endemic BTV-8 strain detected in 2023.

Fig. 3

Phylogenetic analysis of S2 (A) and S6 (B) sequences of BTV-4 strains. Phylogenetic analysis of S2 (A) and S6 (B) sequences of the BTV-4 strains using the maximum likelihood method and Tamura-Nei model with 1000 bootstrap replicates in MEGA X. This analysis involved 32 (A) and 36 (B) nucleotide sequences, there were a total of 2903 (A) and 1609 (B) positions in the final dataset. Bootstrap values appeared at the corresponding nodes. In the phylogenetic tree, GenBank sequences, BT serotype, country and year of sample collection are given. In red, sequences from the BTV-4 strain identified in Corsica in 2023 and described in this study; in orange, sequences of the BTV-4 strain detected in 2021 in Corsica.

Fig. 4

Phylogenetic analysis of S2 (A) and S6 (B) sequences of the EHDV strains. Phylogenetic analysis of S2 (A) and S6 (B) sequences of EHDV strains using the maximum likelihood method and Tamura-Nei model with 1000 bootstrap replicates in MEGA X. This analysis involved 36 (A) and 29 (B) nucleotide sequences, there were a total of 3040 (A) and 1585 (B) positions in the final dataset. Bootstrap values appeared at the corresponding nodes. In the phylogenetic tree, GenBank sequences, EHD serotype, country and year of sample collection are given. In red, sequences from the EHDV-8 strain introduced in France in 2023.