Virus adaption following experimental infection of chickens with a domestic duck low pathogenic avian influenza isolate from the 2017 USA H7N9 outbreak identifies polymorphic mutations in multiple gene segments

Authors: CHRZASTEK, KLAUDIA - Orise Fellow; SEGOVIA, KAREN - Orise Fellow; TORCHETTI, MIA - Animal And Plant Health Inspection Service (APHIS); KILLIAN, MARY - Animal And Plant Health Inspection Service (APHIS); Pantin Jackwood, Mary; Kapczynski, Darrell

Submitted to: Viruses
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/15/2021
Publication Date: 6/18/2021
Citation: Chrzastek, K., Segovia, K., Torchetti, M., Killian, M.L., Pantin Jackwood, M.J., Kapczynski, D.R. 2021. Virus adaption following experimental infection of chickens with a domestic duck low pathogenic avian influenza isolate from the 2017 USA H7N9 outbreak identifies polymorphic mutations in multiple gene segments. Viruses. 13(6):1166. https://doi.org/10.3390/v13061166.
DOI: https://doi.org/10.3390/v13061166

Interpretive Summary: Avian influenza viruses can be divided into highly pathogenic avian influenza (HPAI) viruses and low pathogenic avian influenza (LPAI) viruses. HPAI viruses are restricted to subtypes of H5 and H7 and cause severe illnesses in poultry species with high mortality rates, whereas LPAI viruses are typically maintained in waterfowl and can be transmitted to domestic poultry species resulting in subclinical infection or mild respiratory disease. After circulation in poultry species, some H5 and H7 LPAI viruses can mutate to HPAI form. In 2017, outbreaks of H7N9 LPAI virus and HPAI virus occurred at chicken poultry farms in Tennessee and were found in mixed species backyard farm and markets in Alabama, Kentucky and Georgia. This study aimed to characterize infection and transmissibility of a duck origin H7N9 isolate in chickens, to address the potential contribution of waterfowl in the spread of virus during the outbreak. The results demonstrate that infection resulted in all chickens developing viremia and transmitting virus to naive animals. In addition, this work support the potential transmission of LPAI and HAPI viruses from waterfowl to poultry.

Technical Abstract: In March 2017, highly pathogenic (HP) and low pathogenic (LP) avian influenza virus (AIV) subtype H7N9 were detected from poultry farms and backyard birds in several states in the southeast United States. Because interspecies transmission is a known mechanism for evolution of AIVs, we sought to characterize infection and transmission of a domestic duck-origin H7N9 LPAIV in chickens and genetically compare the viruses replicating in the chickens to the original H7N9 clinical field samples used as inoculum. The results of the experimental infection demonstrated virus replication and transmission in chickens, with overt clinical signs of disease and shedding through both oral and cloacal routes. Unexpectedly, higher levels of virus shedding were observed in some cloacal swabs. Next generation sequencing (NGS) analysis identified numerous non-synonymous mutations at the consensus level in the polymerase genes (i.e., PA, PB1, and PB2) and the hemagglutinin (HA) receptor binding site in viruses recovered from chickens, indicating possible virus adaptation in the new host. For comparison, NGS analysis of clinical samples obtained from duck specimen collected during the outbreak indicated three polymorphic sides in the M1 segment and a minor population of viruses carrying the D139N (21.4%) substitution in the NS1 segment. Interestingly, at consensus level, A/duck/Alabama (H7N9) had isoleucine at position 105 in NP protein, similar to HPAIV (H7N9) but not to LPAIV (H7N9) isolated from the same 2017 influenza outbreak in the US. Taken together, this work demonstrates that the H7N9 viruses could readily jump between avian species, which may have contributed to the evolution of the virus and its spread in the region.