Multifocal outbreak of equine influenza in vaccinated horses in Argentina in 2018: Epidemiological aspects and molecular characterisation of the involved virus strains

Abstract

Summary Background Equine influenza is an important cause of respiratory disease of horses worldwide. The equine influenza virus (EIV) undergoes antigenic drift through the accumulation of amino acid substitutions in the viral proteins, which may lead to vaccine breakdown. Objectives To describe the epidemiological findings and the molecular characteristics of the EIV detected during the multifocal outbreak that occurred in Argentina between March and July 2018 and evidence a vaccine breakdown. Study design Observational, descriptive study. Methods Virus was detected in nasopharyngeal swabs using real‐time reverse transcriptase PCR (RT‐PCR). Nucleotide and deduced amino acid sequences of the haemagglutinin (HA) and neuraminidase (NA) genes were obtained from EIV positive nasopharyngeal swabs, and phylogenetic analysis was undertaken. Amino acid sequences were compared against the current World Organisation for Animal Health (OIE)‐recommended Florida clade 1 vaccine strain and strain components of vaccines used in Argentina. Serum samples were tested using haemagglutination inhibition test. Results Equine influenza virus infection was confirmed using real‐time RT‐PCR and serological testing. The phylogenetic analysis of the HA and NA genes revealed that all the EIV identified during the outbreak belong to the H3N8 subtype, Florida clade 1. Multiple amino acid changes, some of them at antigenic sites, were observed in the circulating virus when compared with the strains included in the most commonly used vaccine in Argentina. Seventy‐six percent of the affected horses had been vaccinated with this vaccine, suggesting the occurrence of vaccine breakdown. Main limitations The study does not include antigenic characterisation and full genome sequencing of Argentinian strains, that could provide additional information. Conclusions The occurrence of this multifocal equine influenza outbreak in regularly vaccinated horses is a field evidence of vaccine breakdown, reinforcing the necessity of keeping vaccine strains updated according to OIE recommendations. It also underlines the importance of the implementation of appropriate quarantine measures and restriction of horse movement in the face of disease.

An Overview of Equine Influenza in South America

“…More recently, a huge outbreak of EI occurred in Argentina between March and July 2018, while EIV was affecting other countries in South America [ 23 ]. Again, during this EI occurrence, thoroughbred, polo and jumping horses in six different provinces around the country were involved.…”

“…The index cases occurred in Mendoza province, which is geographically located in the border with Chile, suggesting the virus entered from Chile and it subsequently disseminated into the country. During this outbreak, the movement of horses, competitions and equestrian events were not officially restricted, favoring the spread of the virus throughout the country [ 23 ].…”

“…In the early 2000s, the Florida sublineage evolved into Florida clade 1 and Florida clade 2 and has been the predominant circulating sub-lineage since then [ 12 ]. Florida clade 1 virus has been isolated in North America since 2003 and has been associated with EI outbreaks in South Africa, Japan, Australia, Europe, the United Arab Emirates, South America and more recently in Africa [ 12 , 18 , 19 , 20 , 21 , 22 , 23 , 24 , 25 , 26 , 27 , 28 , 29 ]. Florida clade 2 EIV strains are the predominant EIV strains circulating in European and Asian countries, and although it has been isolated in horses imported into the United States, it has never been detected in South America [ 19 , 20 , 30 , 31 , 32 , 33 , 34 , 35 , 36 ].…”

“…Vaccination is widely used to prevent or limit the disease’s spread, strength, and negative impact [ 2 , 37 ]. However, like other influenza A viruses, EIV undergoes antigenic drift by accumulating amino acid substitutions in the HA protein, which has led to vaccine breakdown [ 23 , 38 , 39 , 40 ]. Consequently, the composition of EIV vaccines needs to be reviewed and updated periodically.…”

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

“…Similar equine influenza virus incursions in Hong Kong [5], Japan [6], South Africa [7,8], Turkey [9], Malaysia [10] and other countries have also resulted in economic loss, due to movement restrictions and cancellation of equestrian events. 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.…”