Live-bird markets in the Northeastern United States: a source of avian influenza in commercial poultry

Abstract

In 1994, an H7N2 subtype avian influenza virus of low pathogenicity was detected in live-bird markets (LBMs) of the Northeast United States. Since that time the H7N2 virus continues to circulate in the LBMs despite efforts to eradicate the virus by market closures followed by extensive cleaning and disinfection. Since 1996, the LBMs have been implicated as the source of virus in five outbreaks of H7N2 avian influenza in commercial poultry. Although the H7N2 virus is of low pathogenicity, several mutations have occurred at, or near, the cleavage site of the haemagglutinin (H) protein, a region of the protein known to influence pathogenicity of H5 and H7 avian influenza viruses. From 1994 to 2002, the amino-acid motif at the H cleavage site has gradually changed from PENPKTR/GLF to PEKPKKR/GLF, with the addition of two lysine (K) residues. Also, a 24-nucleotide deletion, believed to be part of the receptor-binding region, was first observed in LBM H7N2 isolates in 1996 and is seen in all isolates tested since 2000. These findings support the need to continue avian influenza virus (AIV) surveillance in the LBMs and to develop new and innovative methods to prevent the introduction of AIV into the LBMs and to find ways to eliminate it when it is detected. Live-bird markets (LBMs) have been intensely studied in recent years because avian influenza viruses in the markets are closely associated with avian influenza in commercial poultry and the markets may serve as a ‘fertile ground’ for virus mutations and emergence of new influenza viruses with increased virulence or ability to infect other species, including humans. In 1997, an H5N1 avian influenza virus (AIV) emerged in Hong Kong LBMs to infect 18 people; 6 of whom died (Claas et al. 1998). The source of human infections was due to direct contact with infected chickens in the LBMs; there was no human-tohuman spread. Subsequent studies on the H5N1 virus showed that the virus most likely evolved by the reassortment of virus genes from at least 3 different avian influenza viruses that were circulating within the LBMs in Hong Kong (Guan et al. 1999; Hoffmann et al. 2000). In the United States, the LBMs were first recognized as a potential source of AIV in 1986 following the re-emergence in Pennsylvania of an H5N2 AIV of low pathogenicity believed to be the precursor virus that caused the outbreak of highly pathogenic H5N2 in 1983-84. The source of the low-pathogenic H5 virus was traced to the LBMs in the Northeast United States. Eradication of the H5N2 virus from the LBMs was accomplished by the end of 1987. Since that time, extensive surveillance was conducted to monitor for AIV circulating in the LBMs. In 1994, an H7N2 AIV of low pathogenicity was detected in the LBMs and has persisted since, despite efforts to eliminate the virus. Since 1996, the LBMs have been implicated as a source of H7N2 AIV in at least 5 outbreaks in commercial poultry in the Northeast United States (Akey 2003; Davison et al. 2003; Dunn et al. 2003, D. Senne unpublished observation). In this paper we: 1. briefly describe the LBM system in the USA; 2. review surveillance activities in the LBMs; 3. review the recent outbreaks of AI for which the LBMs were implicated as a source of virus in commercial poultry; 4. summarize the molecular changes in an H7N2 AIV that has continued to circulate in the markets since 1994; and 5. present past and future plans for the control of AIV in the LBMs.