Elsevier

Veterinary Microbiology

Volume 124, Issues 1–2, 20 September 2007, Pages 35-46
Veterinary Microbiology

Low pathogenicity H5N2 avian influenza outbreak in Japan during the 2005–2006

https://doi.org/10.1016/j.vetmic.2007.04.025Get rights and content

Abstract

At the end of May 2005, a low-pathogenicity avian influenza (LPAI) virus of subtype H5N2 was isolated for the first time from chickens in Japan. Through active and epidemiological surveillance, 5.78 million chickens on 41 farms were found to be affected and 16 H5N2 viruses were isolated. Antigenic analysis revealed antigenic similarity of these isolates. Phylogenetic analysis showed that they originated from a common ancestor and clustered with the H5N2 strains prevalent in Central America that have been circulating since 1994. Experimental infection of chickens with the index isolate (A/chicken/Ibaraki/1/05) demonstrated that this virus replicated efficiently in the respiratory tract without clinical signs, and dust-borne and/or droplet-borne transmission was considered as a possible mode of transmission. These results suggested that the H5N2 LPAI viruses isolated in Japan were highly adapted to chickens.

Introduction

Influenza A viruses have been classified into subtypes according to their surface glycoproteins, hemagglutinin (HA) and neuraminidase (NA). Sixteen HA subtypes and nine NA subtypes are now recognized (Fouchier et al., 2005). Wild aquatic birds, predominantly ducks, geese, and shorebirds, are the natural reservoir of all subtypes of influenza A viruses in other species (Kawaoka et al., 1988, Webster et al., 1992). Avian influenza viruses (AIVs) sporadically infect poultry, resulting in clinical manifestations ranging from asymptomatic infection, decline in egg production, and mild respiratory disease, to death.

Influenza A viruses infecting chickens are categorized into two pathotypes based on their virulence to chickens; namely, low-pathogenicity avian influenza (LPAI) virus and highly pathogenic avian influenza (HPAI) virus. Among the 16 HA subtypes of AIV, HPAI virus has been associated with only a small proportion of the H5 or H7 subtypes (Wright and Webster, 2001). The HA molecules of HPAI viruses differ from those of LPAI viruses in that they possess multiple basic amino acids at the carboxyl terminus of HA1. This series of basic amino acids at the cleavage site is a motif that is recognized by ubiquitous intracellular proteases, allowing systemic infection with high mortality in poultry (Stieneke-Grober et al., 1992). In addition, some LPAI viruses of the H5 and H7 subtypes can mutate to HPAI viruses, and several mechanisms involved in the emergence of HPAI virus from LPAI virus precursor have been documented. It was shown that an LPAI virus evolved into an HPAI virus that caused a severe outbreak in Pennsylvania in 1983, by removing a carbohydrate side chain in the vicinity of the cleavage site (Kawaoka et al., 1984). The causative agents of Mexican outbreaks from 1994 to 1995 were derived from an LPAI virus that had accumulated a number of basic residues at the cleavage site (Garcia et al., 1996), as were the viruses that caused outbreaks in British Columbia (Pasick et al., 2005) and Chile (Suarez et al., 2004).

At the end of May 2005, an AIV of the H5N2 subtype was isolated for the first time from chickens in Japan. HPAI viruses of the same subtype have caused three large outbreaks in poultry: in Pennsylvania in 1983 (Bean et al., 1985, Kawaoka et al., 1984), in Mexico from 1994 to 1995 (Garcia et al., 1996, Horimoto et al., 1995), and in Italy from 1997 to 1998 (Capua et al., 2003, Donatelli et al., 2001). The H5N2 subtype became endemic in Central America in its low-pathogenicity form in the decade after 1994, despite years of eradication programs in combination with vaccination (Lee et al., 2004, Nguyen et al., 2005). Here, we describe the H5N2 LPAI outbreaks in Ibaraki and Sitama Prefectures in Japan during the period May 2005 to June 2006. Comprehensive studies, including molecular and antigenic characterization as well as experimental infection with the H5N2 Japanese isolates, were carried out to understand the nature of the causative agent of these outbreaks.

Section snippets

Viruses

A/chicken/Ibaraki/1/05 was isolated from embryonated eggs inoculated with tracheal homogenates from chickens at a commercial laboratory, and was subsequently submitted to the National Institute of Animal Health for further analysis. The rest of the isolates from the outbreak were isolated from tracheal swab pools of chickens at the livestock hygiene service center of Ibaraki Prefecture. A/chicken/Yokohama/aq-55/01 (H9N2) was used as a virus that efficiently infects chickens (Kishida et al., 2004

Outbreak information

In May 23, 2005, a hemagglutinating agent was isolated at a commercial laboratory using embryonated chicken eggs after inoculation with pooled tracheal homogenates from laying chickens that had shown a decline in egg production. The farm was located in Ibaraki Prefecture, 30 km east of Tokyo. Initially, infectious bronchitis virus was suspected; however, the virus could not be identified by the laboratory. It was subsequently turned over to the National Institute of Animal Health on June 25. On

Discussion

In this report, it is clearly shown that the H5N2 viruses isolated in the Ibaraki Prefecture in Japan were genetically and antigenically related to each other, suggesting that they arose from a common ancestor. Phylogenetic analysis showed that these viruses were closely related to viruses isolated in Central America, particularly those belonging to the B sublineage of the Mexican lineage (Lee et al., 2004). The H5N2 viruses isolated in Japan had features similar to those of the Mexican

Acknowledgment

We thank Dr. R.G. Webster at St. Jude Children's Research Hospital for providing H5 monoclonal antibodies.

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