Evolution of H9N2 influenza viruses from domestic poultry in Mainland China

Abstract

H9N2 viruses have circulated in domestic poultry in Mainland China since 1994, and an inactivated vaccine has been used in chickens to control the disease since 1998. The present study analyzed 27 H9N2 avian influenza viruses that were isolated from chickens and ducks from 1996 to 2002. Infection studies indicated that most of the viruses replicate efficiently but none of them is lethal for SPF chickens. However, these viruses exhibit different phenotypes of replication in a mouse model. Five viruses, including 4 early isolates and one 2000 isolate, are not able to replicate in mice; 14 viruses replicate to moderate titers in mouse lungs and cause less than 5% weight loss, while other 8 viruses could replicate to high titers in the lungs and 7 of them induce 10-20% weight loss of the mice on day 5 after inoculation. Most of the viruses isolated after 1996 are antigenically different from the vaccine strain that is currently used in China. Three viruses isolated in central China in 1998 are resistant to adamantanes. Phylogenetic analysis revealed that all of the viruses originated from CK/BJ/1/94-like virus and formed multiple genotypes through complicated reassortment with QA/HK/G1/97-, CK/HK/G9/97-, CK/SH/F/98-, and TY/WI/66-like viruses. This study is a description of the previously uncharacterized H9N2 avian influenza viruses recently circulating in chickens and ducks in Mainland China. Our findings suggest that urgent attention should be paid to the control of H9N2 influenza viruses in animals and to the human's influenza pandemic preparedness.

Evolution of the H9N2 influenza genotype that facilitated the genesis of the novel H7N9 virus

“…The vaccinated chickens were divided into groups with low antibody levels (HI titer,(6)(7)(8)(9) and high antibody levels (HI titer,(10)(11)(12). Nine viruses used in the above unvaccinated chicken experiment (Fig.…”

“…In 1994, the H9N2 subtype was first identified in chicken farms in the Guangdong province of south China (7); it has since become widespread in chickens and has caused great economic loss from reduced egg production and highly lethal coinfections (8)(9)(10)(11). To reduce the impact of H9N2 infection in chickens, the flocks have been vaccinated since 1998 with commercial inactivated vaccines, such as A/chicken/Guangdong/SS/1994 (Ck/GD/ SS/94), A/chicken/Shandong/6/1996 (Ck/SD/6/96), and A/chicken/ Shanghai/F/1998 (Ck/SH/F/98) (8,12,13). These H9N2 vaccines initially limited the outbreaks and virus spread.…”

“…These H9N2 vaccines initially limited the outbreaks and virus spread. However, despite multiple doses, the H9N2 vaccines became less effective, especially after 2007, and H9N2 influenza virus continues to circulate in vaccinated chicken flocks and has caused sporadic disease outbreaks (8,10,(12)(13)(14)(15)(16)(17)(18)(19)(20). However, the recent prevalence and molecular evolution of the H9N2 viruses in chickens especially in the flocks receiving large-scale vaccination, and their role in the emergence of human H7N9 virus, are not fully understood.…”

A small-scale study on airborne transmission of H9N2 avian influenza virus under field conditions

“…Although H9N2 AIV belongs to the low pathogenic avian influenza (LPAI) virus, it increases morbidity and mortality rates when poultry are co-infected with other pathogens, such as Escherichia coli and Staphylococcus aureus [4,5]. In China, since H9N2 AIV was first isolated from diseased chickens in Guangdong Province in 1994, the virus has become the most prevalent type nationwide [6][7][8][9][10][11].…”

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“…With the growth in the global monitoring efforts, and the widespread use of cheaper DNA sequencing technology there has been a rapid expansion in the number of available sequences. Previous phylogenetic studies of H9N2 hemagglutinin, have focussed on sequences from a single location (Banks et al 2000;Butt et al 2010;Kim et al 2006;Li et al 2005;Song et al 2011;Xu et al 2007a). The largest previous phylogeographical study was that of Fusaro et al who surveyed all of the H9N2 viral segments from the Middle East (Fusaro et al 2011).…”