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

Amanda H Seekings1 Yuan Liang2 Caroline J Warren1 Charlotte K Hjulsager3 Saumya S Thomas1 Fabian Z X Lean4,5 Alejandro Nunez4 Paul Skinner1 David Selden4 Marco Falchieri1 Hugh Simmons4 Ian H Brown1 Lars E Larsen2 Ashley C Banyard1 Marek J Slomka1
Affiliations 5 institutions
  1. Department of Virology, Animal and Plant Health Agency (APHA), Woodham Lane, New Haw, Addlestone, KT15 3NB, UK.
  2. Department of Veterinary and Animal Sciences, University of Copenhagen, 1870 Frederiksberg, Denmark.
  3. Department of Virus and Microbiological Special Diagnostics, Statens Serum Institut, 2300 Copenhagen S, Denmark.
  4. Pathology and Animal Sciences Department, Animal and Plant Health Agency (APHA), Woodham Lane, New Haw, Addlestone, KT15 3NB, UK.
  5. Department of Pathobiology and Population Sciences, The Royal Veterinary College, Hawkshead Lane, North Mymms, Hatfield, AL9 7TA, UK.

Abstract

During the UK 2020-2021 epizootic of H5Nx clade 2.3.4.4b high-pathogenicity avian influenza viruses (HPAIVs), high mortality occurred during incursions in commercially farmed common pheasants (Phasianus colchicus). Two pheasant farms, affected separately by H5N8 and H5N1 subtypes, included adjacently housed red-legged partridges (Alectoris rufa), which appeared to be unaffected. Despite extensive ongoing epizootics, H5Nx HPAIV partridge outbreaks were not reported during 2020-2021 and 2021-2022 in the UK, so it is postulated that partridges are more resistant to HPAIV infection than other gamebirds. To assess this, pathogenesis and both intra- and inter-species transmission of UK pheasant-origin H5N8-2021 and H5N1-2021 HPAIVs were investigated. Onward transmission to chickens was also assessed to better understand the risk of spread from gamebirds to other commercial poultry sectors. A lower infectious dose was required to infect pheasants with H5N8-2021 compared to H5N1-2021. However, HPAIV systemic dissemination to multiple organs within pheasants was more rapid following infection with H5N1-2021 than H5N8-2021, with the former attaining generally higher viral RNA levels in tissues. Intraspecies transmission to contact pheasants was successful for both viruses and associated with viral environmental contamination, while interspecies transmission to a first chicken-contact group was also efficient. However, further onward transmission to additional chicken contacts was only achieved with H5N1-2021. Intra-partridge transmission was only successful when high-dose H5N1-2021 was administered, while partridges inoculated with H5N8-2021 failed to shed and transmit, although extensive tissue tropism was observed for both viruses. Mortalities among infected partridges featured a longer incubation period compared to that in pheasants, for both viruses. Therefore, the susceptibility of different gamebird species and pathogenicity outcomes to the ongoing H5Nx clade 2.3.4.4b HPAIVs varies, but pheasants represent a greater likelihood of H5Nx HPAIV introduction into galliforme poultry settings. Consequently, viral maintenance within gamebird populations and risks to poultry species warrant enhanced investigation.

Supporting text Virus Host Location
clade 2.3.4.4b 19 H5N1 82 H5N8 6 high-pathogenicity avian influenza viruses (HPAIVs) 1 partridges 1 pheasants 1 Galliformes 5 Influenza A virus 186 Influenza A Virus, H5N1 Subtype 300 Influenza A Virus, H5N8 Subtype 12 Animals 1948 Chickens 146 Virulence 108

Evidence records

5 total
Experimental Infection
5 records · 2 evidence types
Evidence type
1 records
OVE7754
Key finding

In experimentally infected pheasants, H5N1-2021 showed faster systemic dissemination and higher tissue viral RNA levels than H5N8-2021, indicating greater pathogenicity.

Virus
Host
Location
Not specified
Supporting text

HPAIV systemic dissemination to multiple organs within pheasants was more rapid following infection with H5N1-2021 than H5N8-2021, with the former attaining generally higher viral RNA levels in tissues.

Method
experimental infection | tissue sampling | viral RNA quantification | comparison of systemic dissemination
Experimental system
controlled experimental infection of pheasants with HPAIV subtypes H5N1-2021 and H5N8-2021
Evidence type
4 records
OVE7755
Key finding

H5N8-2021 was successfully transmitted between pheasants in an intraspecies contact transmission experiment.

Virus
Host
Location
Not specified
Supporting text

Intraspecies transmission to contact pheasants was successful for both viruses and associated with viral environmental contamination.

Method
contact transmission experiment | environmental contamination assessment
Experimental system
intraspecies contact transmission model in pheasants
OVE7756
Key finding

H5N1-2021 was successfully transmitted between pheasants in an intraspecies contact transmission experiment.

Virus
Host
Location
Not specified
Supporting text

Intraspecies transmission to contact pheasants was successful for both viruses and associated with viral environmental contamination.

Method
contact transmission experiment | environmental contamination assessment
Experimental system
intraspecies contact transmission model in pheasants
OVE7758
Key finding

H5N1-2021 transmitted efficiently from infected pheasants to chickens and onward transmission to additional chicken contacts was achieved.

Virus
Host
Location
Not specified
Supporting text

Interspecies transmission to a first chicken-contact group was also efficient. However, further onward transmission to additional chicken contacts was only achieved with H5N1-2021.

Method
contact transmission experiment | sequential contact exposure
Experimental system
interspecies contact transmission model from pheasants to chickens with sequential chicken contact groups
OVE7757
Key finding

H5N8-2021 transmitted efficiently from infected pheasants to a first chicken-contact group, but onward transmission to additional chicken contacts was not achieved.

Virus
Host
Location
Not specified
Supporting text

Interspecies transmission to a first chicken-contact group was also efficient. However, further onward transmission to additional chicken contacts was only achieved with H5N1-2021.

Method
contact transmission experiment | sequential contact exposure
Experimental system
interspecies contact transmission model from pheasants to chickens with sequential chicken contact groups