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.

The role of airborne particles in the epidemiology of clade 2.3.4.4b H5N1 high pathogenicity avian influenza virus in commercial poultry production units

“…Interestingly, we did observe greater detection of HPAIV in the air from the duck, compared to the turkey and chicken premises. This observation mirrors experimental findings where ducks have exhibited particularly elevated levels of environmental contamination following experimental infection with AIVs in comparison to other poultry species such as galliformes (chickens and turkeys) (18, 52, 54).…”

“…While we assayed for the presence of infectious virus, we did not quantify infectious virus in these samples and thus infectious titre was not determined. However, with reference to previous comparison data between infectious virus and vRNA concentration (relative equivalency units [REUs]), we estimate that the lowest Ct values (highest vRNA quantity) collected from the air samples, may be below the equivalent minimum infectious dose for ducks (18). Although, these assumptions are based the minimum infectious dose following intranasal inoculation and not from aerosols, the latter having been shown for historic H5N1 HPAIVs to be around 30 times less efficient (39).…”

“…Infectious virus was only detected in the samples collected from the duck premises. We have previously reported that vRNA could not be detected in air samples collected following experimental infection of ducks and chickens with contemporary H5N1 2021 HPAIV clade 2.3.4.4b (18). However, these animals were housed under negative air pressure within a high containment environment which may have impacted upon airflow and the ability to detect particulate material bound to infectious virus or viral products.…”

“…In birds, transmission most frequently occurs via environmental contamination through liquid fomites (i.e. faecal-oral route) (12,13,17,18). However, transmission via airborne particles may be relevant for some strains of AIV (e.g., H9N2) (13,14,(19)(20)(21)(22)(23)(24)(25).…”

“…(7). We previously demonstrated limited airborne detection of vRNA from ducks and chickens infected with contemporary 2021 H5N1 HPAIV clade 2.3.4.4b, albeit under experimental conditions (18). However, currently no data exists for the field detection of H5N1 HPAIV in airborne particles from the current global panzootic.…”