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Evolution, Transmission, and Pathogenicity of High Pathogenicity Avian Influenza Virus A (H5N8) Clade 2.3.4.4, South Korea, 2014-2016.

ABSTRACT: During 2014-2016, clade 2.3.4.4 H5N8 high pathogenicity avian influenza virus (HPAIV) caused the largest known avian influenza epidemic in South Korea. Based on data from earlier H5N8 outbreaks, primitive H5N8 virus in South Korea was classified into five subgroups: C1, C2, C3, C4, and C5. The present study investigated the pathogenic and molecular epidemiologic characteristics of H5N8 viruses obtained from 388 cases of poultry farms and 85 cases of wild bird infections in South Korea during 2014-2016. Representative viruses of subgroups C1, C2, and C4 showed significant pathobiological differences in specific pathogen-free (SPF) chickens, with the H1731 (C1) virus showing substantially lower infectivity, transmissibility, and pathogenicity than the H2102 (C2) and H1924 (C4) viruses. Full genome sequence analysis showed the number of mutations that significantly increased in domestic duck-origin H5N8 HPAIVs compared to the viruses from gallinaceous poultry. These differences may have been due to the long-term circulation of viruses in domestic duck farms. The same mutations, at positions 219 and 757 of PB1, independently evolving in the C0, C1, and C2 subgroups may have been positively selected, resulting in convergent evolution at the amino acid level. Bayesian discrete trait phylodynamic analysis (DTA) indicated multiple introductions of H5N8 HPAIV from wild birds into domestic poultry in various regions in South Korea. Following initial viral introduction into domestic duck farms in the western part of Korea, domestic ducks played a major role in viral transmission and maintenance. These findings highlight the need for continued genomic surveillance and pathobiological characterization of HPAIV in birds. Enhanced biosecurity in poultry farms should be implemented to prevent the introduction, maintenance, and spread of HPAIV.

SUBMITTER: Baek YG

PROVIDER: S-EPMC9253604 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Waterfowl is the natural reservoir for avian influenza viruses (AIV), where the infection is mostly asymptomatic. In 2016, the panzootic high pathogenicity (HP) AIV H5N8 of clade 2.3.4.4B (designated H5N8-B) caused significant mortality in wild and domestic ducks, in stark contrast to the predecessor 2.3.4.4A virus from 2014 (designated H5N8-A). Here, we studied the genetic determinants for virulence and transmission of H5N8 clade 2.3.4.4 in Pekin ducks. While ducks inoculated with recombinant H5N8-A did not develop any clinical signs, H5N8-B-inoculated and cohoused ducks died after showing neurological signs. Swapping of the HA gene segments did not increase virulence of H5N8-A but abolished virulence and reduced systemic replication of H5N8-B. Only H5N8-A carrying H5N8-B HA, NP, and NS with or without NA exhibited high virulence in inoculated and contact ducks, similar to H5N8-B. Compared to H5N8-A, HA, NA, NS, and NP proteins of H5N8-B possess peculiar differences, which conferred increased receptor binding affinity, neuraminidase activity, efficiency to inhibit interferon-alpha induction, and replication in vitro, respectively. Taken together, this comprehensive study showed that HA is not the only virulence determinant of the panzootic H5N8-B in Pekin ducks, but NP, NS, and to a lesser extent NA were also necessary for the exhibition of high virulence in vivo. These proteins acted synergistically to increase receptor binding affinity, sialidase activity, interferon antagonism, and replication. This is the first ad-hoc study to investigate the mechanism underlying the high virulence of HPAIV in Pekin ducks. IMPORTANCE Since 2014, several waves of avian influenza virus (AIV) H5N8 of clade 2.3.4.4 occurred globally on unprecedented levels. Unlike viruses in the first wave in 2014-2015 (H5N8-A), viruses in 2015-2016 (H5N8-B) exhibited unusually high pathogenicity (HP) in wild and domestic ducks. Here, we found that the high virulence of H5N8-B in Pekin ducks could be attributed to multiple factors in combination, namely, hemagglutinin (HA), neuraminidase (NA), nucleoprotein (NP), and nonstructural protein 1 (NS1). Compared to H5N8-A, H5N8-B possesses distinct genetic and biological properties including increased HA receptor-binding affinity and neuraminidase activity. Likewise, H5N8-B NS1 and NP were more efficient to inhibit interferon induction and enhance replication in primary duck cells, respectively. These results indicate the polygenic trait of virulence of HPAIV in domestic ducks and the altered biological properties of the HPAIV H5N8 clade 2.3.4.4B. These findings may explain the unusual high mortality in Pekin ducks during the panzootic H5N8 outbreaks.

Dataset Information

Evolution, Transmission, and Pathogenicity of High Pathogenicity Avian Influenza Virus A (H5N8) Clade 2.3.4.4, South Korea, 2014-2016.

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