Molecular Mechanism of the Airborne Transmissibility of H9N2 Avian Influenza A Viruses in Chickens

Abstract

H9N2 avian influenza virus has been prevalent in poultry in many parts of the world since the 1990s and occasionally crosses the host barrier, transmitting to mammals, including humans. In recent years, these viruses have contributed genes to H5N1 and H7N9 influenza viruses, threatening public health. To explore the molecular mechanism for the airborne transmission of H9N2 virus, we compared two genetically close strains isolated from chickens in 2001, A/chicken/Shanghai/7/2001(SH7) and A/chicken/Shanghai/14/2001 (SH14). SH7 is airborne transmissible between chickens, whereas SH14 is not. We used reverse genetics and gene swapping to derive recombinant SH7 (rSH7), rSH14, and a panel of reassortant viruses. Among the reassortant viruses, we identified segments HA and PA as governing the airborne transmission among chickens. In addition, the NP and NS genes also contributed to a lesser extent. Furthermore, the mutational analyses showed the transmissibility phenotype predominantly mapped to the HA and PA genes, with HA-K363 and PA-L672 being important for airborne transmissibility among chickens. In addition, the viral infectivity and acid stability are related to the airborne transmissibility. Importantly, airborne transmission studies of 18 arbitrarily chosen H9N2 viruses from our collections confirmed the importance of both 363K in HA and 672L in PA in determining their levels of transmissibility. Our finding elucidates the genetic contributions to H9N2 transmissibility in chickens and highlights the importance of their prevalence in poultry. IMPORTANCEOur study investigates the airborne transmissibility of H9N2 viruses in chickens and the subsequent epidemic. H9N2 virus is the donor for several prevalent reassortant influenza viruses, such as H7N9/2013 and the H5N1 viruses. Poultry as the reservoir hosts of influenza virus is closely associated with human society. Airborne transmission is an efficient pathway for influenza virus transmission among flocks and individuals. Exploring the mechanism of the airborne transmission of the H9N2 virus in chickens could provide essential data regarding prevention and control of influenza endemics and pandemics.

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

“…These results showed that the chicken flocks infected by H9N2 AIV form and transmit viral aerosols. In addition, the results support previously published papers where exposure to H9N2 AIV aerosols is considered an important route of airborne transmission within chicken flocks [25][26][27].…”

Endemicity of H9N2 and H5N1 avian influenza viruses in poultry in China poses a serious threat to poultry industry and public health

“…Zhong et al further identified that the amino acids 363K in the HA gene and 672L in the PA gene contribute to the airborne transmissibility of the H9N2 AIVs in chickens and they also confirmed the importance of these two residues by evaluating the airborne transmission ability of 18 casually chosen natural H9N2 viruses carrying these two residues in chickens [160] . Notably, the proportion of strains with both PA 672L and HA 363K increased in 1998, which coincided with the epidemicity of H9N2 viruses in China [39] .…”

“…The H9N2 virus can be transmitted by airborne droplets to chickens which may account partially for their fast spread among flocks and to individual birds [66,159,160] . Zhang et al have shown that most of the H9N2 viruses isolated before 2000 fail to be transmitted efficiently to aerosol contact groups of chickens [66] .…”

Avian influenza H9N2 virus isolated from air samples in LPMs in Jiangxi, China

“…Aerosol transmission is one of the most important pathways for influenza virus to spread among poultry, from poultry to mammals, and among mammals [9–11]. In recent years, human infection with many subtypes of AIVs has been reported, including H5N1, H5N6, H7N9, H10N8, H6N1, and H9N2 AIVs, and field epidemiological investigation showed some patients had no history of direct contact with any live poultry before illness onset [3, 12, 13].…”