Success and Limitation of Equine Influenza Vaccination: The First Incursion in a Decade of a Florida Clade 1 Equine Influenza Virus that Shakes Protection Despite High Vaccine Coverage

Abstract

Every year, several epizooties of equine influenza (EI) are reported worldwide. However, no EI case has been identified in France between 2015 and late 2018, despite an effective field surveillance of the pathogen and the disease. Vaccination against equine influenza virus (EIV) remains to this day one of the most effective methods to prevent or limit EI outbreaks and the lack of detection of the pathogen could be linked to vaccination coverage. The aim of this study was to evaluate EI immunity and vaccine coverage in France through a large-scale serological study. A total of 3004 archived surplus serums from French horses of all ages, breeds and sexes were selected from four different geographical regions and categories (i.e., sanitary check prior to exportation, sale, breeding protocol or illness diagnosis). EIV-specific antibody response was measured by single radial hemolysis (SRH) and an EIV-nucleoprotein (NP) ELISA (used as a DIVA test). Overall immunity coverage against EIV infection (i.e., titers induced by vaccination and/or natural infection above the clinical protection threshold) reached 87.6%. The EIV NP ELISA results showed that 83% of SRH positive serum samples from young horses (≤3 years old) did not have NP antibodies, which indicates that the SRH antibody response was likely induced by EI vaccination alone (the HA recombinant canarypoxvirus-based EI vaccine is mostly used in France) and supports the absence of EIV circulation in French horse populations between 2015 and late 2018, as reported by the French equine infectious diseases surveillance network (RESPE). Results from this study confirm a strong EI immunity in a large cohort of French horses, which provides an explanation to the lack of clinical EI in France in recent years and highlights the success of vaccination against this disease. However, such EI protection has been challenged since late 2018 by the incursion in the EU of a Florida Clade 1 sub-lineage EIV (undetected in France since 2009), which is also reported here.

Protection against the New Equine Influenza Virus Florida Clade I Outbreak Strain Provided by a Whole Inactivated Virus Vaccine

“…In addition, virus excretion was absent in the vaccinated group, while from 1–7 dpc the virus was excreted by the unvaccinated controls, indicating that sterile immunity was induced in the vaccinates. This was an interesting finding, since field experience with this new EIV FC1 strain as reported from France was that several outbreaks had involved correctly vaccinated animals, the vast majority vaccinated with a vaccine fully in line with OIE recommendations [ 4 , 7 ]. One of the main differences between the predominant vaccine used in France and Equilis Prequenza is that the former only expresses HA, while the latter contains all viral proteins, as it is a whole inactivated virus vaccine.…”

“…From early 2018 to late 2018/early 2019, major EIV outbreaks were reported in South America and a great part of Europe [ 4 , 5 , 6 ]. Genetic analysis revealed the outbreak strains belonged to the FC1 sub-lineage, which is present in most commercially available vaccines.…”

“…In most countries with a high vaccination rate, the number of outbreaks was low. However, in France, many outbreaks still occurred, despite a very high vaccination rate with the vast majority of horses vaccinated with a fully-updated vaccine in line with OIE recommendations [ 4 , 7 ]. This raises the question of whether other attributes of EIV vaccines, such as whether the antigen is whole virus or subunit, and the type of adjuvant may be equally important factors affecting the performance of vaccines in the field.…”

Evaluation of Current Equine Influenza Vaccination Protocols Prior to Shipment, Guided by OIE Standards

“…More recently, in 2018 and 2019, widespread outbreaks in South America [11] and Africa affected thousands of horses and donkeys, respectively [12]. In 2019, many European countries experienced an increase in equine influenza activity [13], and in the United Kingdom horse racing was cancelled for six days, with media reports of revenue loss in excess of £100 million.…”

Special Issue “Equine Viruses”: Old “Friends” and New Foes?

“…The authors highlight the potential protective role of eqMx1, which primarily targets the virus nucleoprotein (NP), against the transmission of new IAVs in horses (i.e., eqMx1 could only inhibit the polymerase activity of IAVs of avian and human origin but remained inactive against the equine IAVs tested). To date, equine influenza virus remains one of the most important respiratory pathogens of horses worldwide, with a potential damaging impact on the equine industry, as clearly illustrated in 2007 in Australia and in 2019 in Europe [20,21]. In 1989, an equine influenza epizootic was reported in the Jilin and Heilongjiang provinces of northeastern China, with up to 20% mortality, which is quite high when compared with conventional equine influenza outbreaks.…”