Volume 18, Number 3—March 2012
Highly Pathogenic Avian Influenza (H5N1) Outbreaks in Wild Birds and Poultry, South Korea
AbstractHighly pathogenic avian influenza (H5N1) among wild birds emerged simultaneously with outbreaks in domestic poultry in South Korea during November 2010–May 2011. Phylogenetic analysis showed that these viruses belonged to clade 2.3.2, as did viruses found in Mongolia, the People’s Republic of China, and Russia in 2009 and 2010.
Three previous outbreaks in South Korea are assumed, on the basis of epidemiologic evidence, to have been caused by HPAI (H5N1) viruses introduced by migratory birds, although a carcass or moribund wild bird infected with these viruses (which would serve as a link to the introduction of infection in domestic poultry) was not found (4–6). On December 7, 2010, an HPAI (H5N1) virus was isolated from a healthy mallard in South Korea (7). After that, subtype H5N1 viruses were frequently detected in wild birds and poultry until May 2011. In this study, we analyzed the epidemiologic features of this outbreak and investigated the characteristics of strains through genetic analysis.
Fourteen bird species were found to be positive for subtype H5N1 (Table). The affected poultry included species of the order Galliformes (chickens, quail, etc.), which exhibited sudden death with severe clinical signs, and domestic ducks (order Anseriformes), which died suddenly or exhibited a decrease in egg production, depending on age. Most infected birds of species that belonged to the orders Anseriformes, Falconiformes, and Strigiformes were found dead, but a few infections were detected in swab specimens from healthy mallards and feces of wild birds. Moreover, species of Anseriformes, such as the Mandarin duck, were dominant among the wild birds with HPAI until the beginning of January 2011. After that time, many HPAI infections were found in birds of prey, such as the Eurasian eagle owl (Table).
All viruses were isolated by inoculating embryonated chicken eggs with specimens from cloacal swab specimens, feces, and homogenized organs from birds with suspected infections. The hemagglutinin (HA) and neuraminidase (NA) proteins were subtyped as previously described (6). We selected 27 viruses, taking into consideration the outbreak period, the region, and the host species (Table A1) and conducted sequencing and phylogenetic analysis of 8 gene segments. The genome sequences of 27 viruses are available from GenBank under accession numbers JN807892–JN808107.
All 27 viruses characterized were highly pathogenic and had variations in the multibasic cleavage site in the HA molecule (PQRERRRKR) and a 20-aa deletion in the stalk region of NA. They did not have amino acid substitutions that conferred resistance to amantadine or oseltamivir and were associated with the increased virulence of subtype H5N1 viruses in mammalian hosts (8).
The intravenous pathogenicity test was conducted by using the A/duck/Korea/Cheonan/2010 virus, the first isolate from poultry. The intravenous pathogenicity index was 3.0 for chickens.
During the initial stage of the 2010–2011 outbreak, HPAI viruses were detected in several wild birds, and the viruses were assumed to have been introduced into domestic poultry by migratory birds. The detection of HPAI (H5N1) virus in free-ranging migratory bird might predict a poultry outbreak if biosecurity measures in poultry are inadequate, but during 2006, several European countries reported HPAI (H5N1) virus infections in wild birds without concurrent poultry outbreaks. In the 2010-2011 outbreak in South Korea, the subsequent outbreak cases suggest that the subtype H5N1 virus was spread from farm to farm by humans and associated agricultural practices so that strains of poultry were grouped in sublineages by region.
Clade 2.3.2 subtype H5N1 viruses have been circulating in poultry and migratory birds in Asia and have accumulated antigenic mutations. We can conclude that early detection of HPAI outbreaks and a rapid response to them are essential in controlling the introduction of virus from migratory birds to poultry and in preventing farm-to-farm spread.
Dr Kim is a veterinary researcher at the Animal, Plant and Fisheries Quarantine and Inspection Agency, Anyang, South Korea. Her research interests are molecular epidemiology of avian influenza virus.
This research was supported by a grant from the National Animal Disease Control Project of the Ministry of Food, Agriculture, Forest and Fisheries of South Korea.
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