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

Abstract

Since October 2021, Europe has experienced the largest avian influenza virus (AIV) epizootic, caused by clade 2.3.4.4b H5N1 high pathogenicity AIV (HPAIV), with over 284 poultry infected premises (IPs) and 2480 dead H5N1-positive wild birds detected in Great Britain alone. Many IPs have presented as geographical clusters, raising questions about the lateral spread between premises by airborne particles. Airborne transmission over short distances has been observed for some AIV strains. However, the risk of airborne spread of this strain remains to be elucidated. We conducted extensive sampling from IPs where clade 2.3.4.4b H5N1 HPAIVs were confirmed during the 2022/23 epizootic, each representing a major poultry species (ducks, turkeys, and chickens). A range of environmental samples were collected inside and outside houses, including deposited dust, feathers, and other potential fomites. Viral RNA (vRNA) and infectious viruses were detected in air samples collected from inside and outside but in close proximity to infected houses, with vRNA alone being detected at greater distances (≤10 m) outside. Some dust samples collected outside of the affected houses contained infectious viruses, while feathers from the affected houses, located up to 80 m away, only contained vRNA. Together, these data suggest that airborne particles harboring infectious HPAIV can be translocated short distances (<10 m) through the air, while macroscopic particles containing vRNA might travel further (≤80 m). Therefore, the potential for airborne transmission of clade 2.3.4.4b H5N1 HPAIV between premises is considered low. Other factors, including indirect contact with wild birds and the efficiency of biosecurity, represent greater importance in disease incursion.

Keywords: H5N1; aerosol; airborne; avian; avian influenza virus; droplet; dust; transmission.

Figure 1

Infected premises 1 (IP1): Environmental sampling and presence or absence of H5 HPAIV RNA at a duck IP. (A,B). Map showing the layout of the IP with the two affected houses indicated, wind direction at time of sampling, the site where carcasses were loaded onto trucks (red star), and mortality and culling indicated. (C–F). The location of the environmental sampling and H5 RRT-PCR results showing the presence (orange) or absence (blue) of H5 HPAIV RNA in the sample and the positive isolation of infectious virus (red outline) or negative isolation of infectious virus (black outline). Samples were collected from air filters (C), feathers (D), dust (E), and water (F). Locations of wet straw samples (n = 2) and an Op swab from a dead duck (n = 1) are not shown but are indicated in Table S1.

Figure 2

Infected premises 2 (IP2): Environmental sampling and presence or absence of H5 HPAIV RNA at a turkey IP. (A,B). Map showing the layout of the IP with the three affected houses indicated, wind direction at time of sampling, the site where carcasses were loaded onto trucks (red star), and mortality and culling indicated. (C–F). The location of the environmental sampling and H5 RRT-PCR results showing the presence (orange) or absence (blue) of H5 HPAIV RNA in the sample and the positive isolation of infectious virus (red outline) or negative isolation of infectious virus (black outline). Samples were collected from air filters (C), feathers (D), dust (E), and water (F). Op swabs from dead turkeys are not shown but indicated in Table S2.

Figure 3

Infected premises 3 (IP3): Environmental sampling and presence or absence of H5 HPAIV RNA at a turkey IP. (A,B). Map showing the layout of the IP with the three affected houses indicated, wind direction at time of sampling, and mortality indicated. (C–F). The location of the environmental sampling and H5 RRT-PCR results showing the presence (orange) or absence (blue) of H5 HPAIV RNA in the sample and the positive isolation of infectious virus (red outline) or negative isolation of infectious virus (black outline). Samples were collected from air filters (C), feathers (D), external dust (E), and internal dust (F). Water and Op and Cl swabs from dead chickens are not shown but indicated in Table S3.