A multi-species, multi-pathogen avian viral disease outbreak event: Investigating potential for virus transmission at the wild bird - poultry interface

Abstract

A free-range organic broiler (Gallus gallus domesticus) premises in Staffordshire was infected by high pathogenicity avian influenza virus (HPAIV) H5N8 during the 2020-2021 epizootic in the United Kingdom (UK). Following initial confirmation of the infection in poultry, multiple wild bird species were seen scavenging on chicken carcasses. Detected dead wild birds were subsequently demonstrated to have been infected and succumbed to HPAIV H5N8. Initially, scavenging species, magpie (Pica pica) and raven (Corvus corax) were found dead on the premises but over the following days, buzzards (Buteo buteo) were also found dead within the local area with positive detection of HPAIV in submitted carcasses. The subacute nature of microscopic lesions within a buzzard was consistent with the timeframe of infection. Finally, a considerable number of free-living pheasants (Phasianus colchicus) were also found dead in the surrounding area, with carcasses having higher viral antigen loads compared to infected chickens. Limited virus dissemination was observed in the carcasses of the magpie, raven, and buzzard. Further, an avirulent avian paramyxovirus type 1 (APMV-1) was detected within poultry samples as well as in the viscera of a magpie infected with HPAIV. Immunohistochemistry did not reveal colocalization of avian paramyxovirus antigens with lesions, supporting an avirulent APMV-1 infection. Overall, this case highlights scenarios in which bi-directional transmission of avian viral diseases between commercial and wild bird species may occur. It also underlines the importance of bio separation and reduced access when infection pressure from HPAIV is high.

Keywords: High pathogenicity avian influenza virus (HPAIV); H5N8; clade 2.3.4.4b; multi-species; avian paramyxovirus type 1.

Figure 1.

Ecological context of the site (A) (red rectangle denotes pasture, blue circle highlights the small lake) including evidence for wild animal and wild bird activity around poultry houses (B and C).

Figure 2.

AIV H5N8 sequences obtained from the IP demonstrated similarity to UK and global H5N8 sequences from 2020 to 2021. Maximum-likelihood phylogenetic tree of the HA gene from global H5N8 sequences from 2020 to 21. Sequences obtained from the IP and the UK are highlighted by coloured tip shapes.

Figure 3.

APMV-1 sequences obtained from the IP demonstrated it to be a genotype I.2 isolate clustering with global genotype I.2 sequences. Maximum-likelihood phylogenetic tree of the F-gene from global APMV-1 sequences. Sequences from different APMV-1 genotypes and that obtained from the IP are highlighted by coloured tip shapes.

Figure 4.

Gross pathological lesions detected within the HPAIV outbreak in a free-range organic broiler farm and associated wild bird infection. On-farm inspections of revealed cyanotic comb (a) and redenned legs (b). PME identified pancreatic necrosis (c; white arrows) in the broilers (c-1) and pheasants (c-2), and epicardial petechiae in the pheasant (d; red arrow).

Figure 5.

Comparative neuro- and cardiomyopathology of chickens (a, b), pheasants (c, d) and buzzard (e, f) infected with HPAIV H5N8. Mild neuronal necrosis with neuropil rarefaction (a) and co-localization of virus antigens (inset). Histological unremarkable brain from pheasant (c). Both chicken and pheasant have neuro and vascular tropism (c, d). Buzzard has lympho-plasmacytic perivascular cuffing (arrow) and oedema, endothelial hypertrophy and necrosis, thrombi deposition (black arrow heads), dispersed degenerate neutrophils in neuropil and neuronal necrosis (e) with viral neurotropism (inset). Mild myocardial degeneration in chickens (b) and absent in pheasant (d). Marked myocardial degeneration and disorganized myofibres along with lymphocytic infiltration in the buzzard (f). Images were taken at 200x magnification. H&E and IHC are from serial sections. Images were taken at 200x magnification.