Elsevier

Veterinary Microbiology

Volume 214, February 2018, Pages 1-6
Veterinary Microbiology

Short communication
Emergence of H3N8 equine influenza virus in donkeys in China in 2017

https://doi.org/10.1016/j.vetmic.2017.11.033Get rights and content

Highlights

  • An influenza outbreak caused by H3N8 EIV occurred in donkeys in China.

  • The virus originated from influenza A(H3N8) clade 2 of the Florida sub-lineage.

  • Amino acid substitutions in the antigenic regions of HA protein of the strain occurs compared with vaccine strain.

Abstract

Equine influenza virus is a major respiratory pathogen in horses. Although both horses and donkeys belong to the genus Equus, donkey infection with influenza viruses is rare. In March 2017, an influenza outbreak occurred in donkeys in Shandong province, China. The causative virus, A/donkey/Shandong/1/2017(H3N8), was isolated from a dead donkey. Genetic analysis indicated that the virus originated from influenza A (H3N8) clade 2 of the Florida sub-lineage that has been circulating in Asian equine populations. Comparison of the deduced amino acid sequence of the HA gene of this causative virus with that of the A/equine/Richmond/1/2007 vaccine strain showed that substitutions had occurred in the antigenic regions A, B, and C. This study provides insight into the currently circulating and newly emerging H3N8 strains in donkeys in China.

Introduction

Equine influenza (EI) is a major infectious respiratory disease caused by equine influenza A virus (EIV) in equids worldwide (Alves Beuttemmuller et al., 2016, Fougerolle et al., 2017, Legrand et al., 2015, Rosanowski et al., 2016). The infection damages respiratory epithelia, reducing mucociliary clearance and inducing inflammation; it can be severe and even fatal, particularly if exacerbated by other pathogens or factors. H3N8 EIV was first isolated in 1963 in Miami, Florida, and continues to circulate in most horse populations in the world. The H3N8 viruses have been subdivided into two different evolutionary lineages since 1986: the American lineage and the European lineage (Daly et al., 1996). Both lineages have been circulating together without geographic barriers. The American lineage has been further divided into three sub-lineages: the Florida, Kentucky, and South American sub-lineages (Lai et al., 2001). The Florida sub-lineage had evolved further into two genetic groups with divergent hemagglutinin (HA) sequences: clade 1 and clade 2 (Bryant et al., 2009). Influenza A viruses infect many different species, and these viruses occasionally cross the species barrier to infect other species. The H3N8 EIVs have caused infection and disease in canines, swine, camels, and donkeys (Crawford et al., 2005, Qi et al., 2010, Tu et al., 2009, Yondon et al., 2014).

China is the second largest equid-raising country in the world; however, no vaccines against influenza viruses have yet been licensed and used in equids. In March 1989, the first severe outbreak of equine influenza caused by H3N8 virus occurred in Jilin province, China, with morbidity and mortality rates reaching 81% and 20%, respectively, in certain herds (Guo et al., 1992). In 1993, a second H3N8 influenza outbreak occurred among equine species in Gansu province. Phylogenetic analysis of the HA gene of the causative virus indicated that the virus belonged to the European lineage (Guo et al., 1995). Since 2007, Florida sub-lineage clade 2 H3N8 viruses have been the predominant subtype isolated from equine species in China. A Florida sub-lineage clade 2 H3N8 virus also caused an outbreak among donkeys in Xinjiang, China in 2007 (Qi et al., 2010). In this study, we performed a detailed characterization of the influenza virus that caused a disease outbreak in donkeys in Shandong province in 2017.

Section snippets

Collection of clinical material

In March 2017, an outbreak of donkey influenza occurred in a 300-head donkey farm in Shandong province, East China. The donkeys showed severe disease symptoms, including depression, anorexia, asthma, nasal discharge, and fever. The period of illness lasted for 2 weeks and resulted in a mortality of 25%. Tissues from dead donkeys were submitted to the Animal Influenza Laboratory of the Ministry of Agriculture, which belongs to Harbin Veterinary Research Institute, CAAS, for respiratory disease

H3N8 virus was isolated from a dead donkey that had severe lung lesions

Three dead donkeys (deaths occurred 7 to 10 days after initial clinical signs) were subjected to post-mortem investigation. The lungs were heavy and dark red. Microscopically, the alveoli were extremely swollen, with variably extensive formation of hyaline membranes and fibrinous exudation. Typical bronchointerstitial pneumonia, characterized by necrotizing bronchiolitis and hemorrhage, was observed (Fig. 1). Part of the lung sample of one donkey was homogenized and inoculated into MDCK cells

Discussion

Although both horses and donkeys belong to the genus Equus, influenza virus infection in donkeys is less common than in horses. The transmission of equine influenza virus to dogs, pigs, donkeys, and camels in recent years suggests that the viruses circulating in horses are exceptionally transmissible. An explosive epizootic of equine influenza that resulted in an estimated 76,000 horses being infected over a 5-month period in Australia (Paillot and El-Hage, 2016) demonstrates the capability of

Acknowledgments

This research was supported by National Key Research and Development Program (2016YFD0500201), Heilongjiang Natural Science Foundation (C2016066), and Funds from the Shandong “Double Tops” Program.

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