Clade 2.3.4.4b H5N1 high pathogenicity avian influenza virus (HPAIV) from the 2021/22 epizootic is highly duck adapted and poorly adapted to chickens

Abstract

The 2021/2022 epizootic of high pathogenicity avian influenza (HPAIV) remains one of the largest ever in the UK, being caused by a clade 2.3.4.4b H5N1 HPAIV. This epizootic affected more than 145 poultry premises, most likely through independent incursion from infected wild birds, supported by more than 1700 individual detections of H5N1 from wild bird mortalities. Here an H5N1 HPAIV, representative of this epizootic (H5N1-21), was used to investigate its virulence, pathogenesis and transmission in layer chickens and Pekin ducks, two species of epidemiological importance. We inoculated both avian species with decreasing H5N1-21 doses. The virus was highly infectious in ducks, with high infection levels and accompanying shedding of viral RNA, even in ducks inoculated with the lowest dose, reflecting the strong waterfowl adaptation of the clade 2.3.4.4 HPAIVs. Duck-to-duck transmission was very efficient, coupled with high environmental contamination. H5N1-21 was frequently detected in water sources, serving as likely sources of infection for ducks, but inhalable dust and aerosols represented low transmission risks. In contrast, chickens inoculated with the highest dose exhibited lower rates of infection compared to ducks. There was no evidence for experimental H5N1-21 transmission to any naive chickens, in two stocking density scenarios, coupled with minimal and infrequent contamination being detected in the chicken environment. Systemic viral dissemination to multiple organs reflected the pathogenesis and high mortalities in both species. In summary, the H5N1-21 virus is highly infectious and transmissible in anseriformes, yet comparatively poorly adapted to galliformes, supporting strong host preferences for wild waterfowl. Key environmental matrices were also identified as being important in the epidemiological spread of this virus during the continuing epizootic.

Transmission dynamics and pathogenesis differ between pheasants and partridges infected with clade 2.3.4.4b H5N8 and H5N1 high-pathogenicity avian influenza viruses

“…High pheasant mortality was observed among all the H5N8-2021 and H5N1-2021 infected pheasants and may well have registered 100% in all groups, but for the pre-emptive culls prompted by welfare concerns. This observation resembled the high mortalities caused by recent (isolated since autumn 2020) UK H5N8 and H5N1 clade 2.3.4.4 HPAIVs in chickens [45,49]. H5N8-2021 and H5N1-2021 pheasant infections caused severe neurological signs prior to death.…”

“…In assessing gamebirds as a bridging host, pheasants were more likely than partridges to transmit onwards to chickens, with H5N1-2021 representing a greater risk than H5N8-2021 (see Figure1which summarises the transmission outcomes).High pheasant mortality was observed among all the H5N8-2021 and H5N1-2021 infected pheasants and may well have registered 100% in all groups, but for the pre-emptive culls prompted by welfare concerns. This observation resembled the high mortalities caused by recent (isolated since autumn 2020) UK H5N8 and H5N1 clade 2.3.4.4 HPAIVs in chickens[45,49]. H5N8-2021 and H5N1-2021 pheasant infections caused severe neurological signs prior to death.…”

“…There was no significant difference when pheasant H5N8-2021 and H5N1-2021 shedding were compared separately for each tract (data not shown). Efficient spread of both H5N8-2021 and H5N1-2021 among pheasants resembled the sustained transmission of UK-origin H5Nx clade 2.3.4.4 HPAIVs among ducks [35], where viral environmental contamination followed shedding and coincided with efficient onward transmission [40,45].…”

“…It is uncertain whether other factors linked to prior transmission among pheasants may have assisted the relatively successful onward transmission of H5N1-2020 among chickens, but onward spread of H5N8-2020 among chickens was relatively less effective. Other clade 2.3.4.4 chicken-to-chicken transmission attempts featured similar numbers of prior infected chickens, but resulted in zero or inefficient transmission [35,45,49,53].…”

Weathering the Storm of High Pathogenicity Avian Influenza in Waterbirds

“…While previous waves have been discrete, with distinct periods of high activity (winter) and low or no activity (summer), and with multiple examples of the virus going extinct in wild waterbirds (e.g., 2005, 2014), this panzootic is characterized by constant high-level activity in wild birds, with outbreaks occurring throughout the year (European Food Safety Authority et al 2023). These changes have likely occurred due to entrenchment of HPAI in wild waterbird populations, driven by efficient replication in waterbirds (particularly ducks; Foret-Lucas et al 2023;James et al 2023). In prior outbreaks, HPAI was still a preferentially poultry-adapted virus and therefore outbreaks in wild waterbirds were routinely seeded from poultry, which explains extinction of HPAI from Europe in 2005, and North American in 2014 (e.g., Krauss et al 2016).…”