1887

Journal of General Virology header logo

Volume 105, Issue 1

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

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 (). Two pheasant farms, affected separately by H5N8 and H5N1 subtypes, included adjacently housed red-legged partridges (), 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.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): clade 2.3.4.4b , H5N1 , H5N8 , high-pathogenicity avian influenza viruses (HPAIVs) , partridges and pheasants
Funding
This study was supported by the:
  • Danish Veterinary and Food Administration (Award xxxx)
    • Principle Award Recipient: LarsE Larsen
  • Defra (Award SE2213)
    • Principle Award Recipient: AshleyC Banyard
  • H2020 European Institute of Innovation and Technology (Award VetBioNet)
    • Principle Award Recipient: HughSimmons
© 2024 Crown copyright
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License. This article was made open access via a Publish and Read agreement between the Microbiology Society and the corresponding author’s institution.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001946
2024-01-30
2024-04-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/105/1/jgv001946.html?itemId=/content/journal/jgv/10.1099/jgv.0.001946&mimeType=html&fmt=ahah

References

  1. Alexander DJ. An overview of the epidemiology of avian influenza. Vaccine 2007; 25:5637–5644 [View Article] [PubMed]
     [Google Scholar]
  2. Webster RG, Laver WG, Air GM, Schild GC. Molecular mechanisms of variation in influenza viruses. Nature 1982; 296:115–121 [View Article] [PubMed]
     [Google Scholar]
  3. Lowen AC. Constraints, drivers, and implications of influenza A virus reassortment. Annu Rev Virol 2017; 4:105–121 [View Article] [PubMed]
     [Google Scholar]
  4. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol Rev 1992; 56:152–179 [View Article] [PubMed]
     [Google Scholar]
  5. Alexander DJ, Brown IH. History of highly pathogenic avian influenza. Rev Sci Tech OIE 2009; 28:19–38 [View Article]
     [Google Scholar]
  6. Smith GJD, Donis RO. World Health Organization/World Organisation for Animal Health/Food and Agriculture Organization (WHO/OIE/FAO) H5 Evolution Working Group Nomenclature updates resulting from the evolution of avian influenza A(H5) virus clades 2.1.3.2a, 2.2.1, and 2.3.4 during 2013-2014. Influenza Other Respir Viruses 2015; 9:271–276 [View Article] [PubMed]
     [Google Scholar]
  7. Nuñez IA, Ross TM. A review of H5Nx avian influenza viruses. Ther Adv Vaccines Immunother 2019; 7:2515135518821625 [View Article] [PubMed]
     [Google Scholar]
  8. Lee D-H, Bertran K, Kwon J-H, Swayne DE. Evolution, global spread, and pathogenicity of highly pathogenic avian influenza H5Nx clade 2.3.4.4. J Vet Sci 2017; 18:269 [View Article]
     [Google Scholar]
  9. Alarcon P, Brouwer A, Venkatesh D, Duncan D, Dovas CI et al. Comparison of 2016–17 and previous epizootics of highly pathogenic avian influenza H5 Guangdong lineage in Europe. Emerg Infect Dis 2018; 24:2270–2283 [View Article]
     [Google Scholar]
  10. Adlhoch C, Fusaro A, Kuiken T, Niqueux É, Staubach C et al. Avian influenza overview May - August 2020. EFSA J 2020; 18:e06270 [View Article] [PubMed]
     [Google Scholar]
  11. Poen MJ, Venkatesh D, Bestebroer TM, Vuong O, Scheuer RD et al. Co-circulation of genetically distinct highly pathogenic avian influenza A clade 2.3.4.4 (H5N6) viruses in wild waterfowl and poultry in Europe and East Asia, 2017-18. Virus Evol 2019; 5:vez004 [View Article] [PubMed]
     [Google Scholar]
  12. Byrne AMP, James J, Mollett BC, Meyer SM, Lewis T et al. Investigating the genetic diversity of H5 avian influenza viruses in the United Kingdom from 2020-2022. Microbiol Spectr 2023; 11:e0477622 [View Article] [PubMed]
     [Google Scholar]
  13. Adlhoch C, Fusaro A, Gonzales JL, Kuiken T, Marangon S et al. European food safety authority; European centre for disease prevention and control; European Union reference laboratory for avian influenza. EFSA Journal 2020 [View Article]
     [Google Scholar]
  14. Liang Y, Nissen JN, Krog JS, Breum SØ, Trebbien R et al. Novel clade 2.3.4.4b highly pathogenic avian influenza A H5N8 and H5N5 viruses in Denmark, 2020. Viruses 2021; 13:886 [View Article] [PubMed]
     [Google Scholar]
  15. Global consortium for H5N8 and related influenza viruses Role for migratory wild birds in the global spread of avian influenza H5N8. Role for migratory wild birds in the global spread of avian influenza H5N8. Science 2016; 354:213–217 [View Article]
     [Google Scholar]
  16. Kim JK, Negovetich NJ, Forrest HL, Webster RG. Ducks: the “Trojan horses” of H5N1 influenza. Influenza Other Respir Viruses 2009; 3:121–128 [View Article] [PubMed]
     [Google Scholar]
  17. APHA (Animal and Plant Health Agency); Defra (Department for the Environment, Food and Rural Affairs). Poultry and other captive birds: registration rules and forms. Updated 6 June 2022; 2002 https://www.gov.uk/government/publications/poultry-including-game-birds-registration-rules-and-forms accessed 15 January 2024
  18. Madden JR. How many gamebirds are released in the UK each year?. Eur J Wildl Res 2021; 67:72 [View Article]
     [Google Scholar]
  19. Miljøministeriet Bekendtgørelse om udsætning af vildt, jagtmåder og jagtredskaber. Miljømin., Naturstyrelsen, j.nr. NST-300-00040; 2016 https://mst.dk/media/141642/3-bekendtgoerelse-om-udsaetninger.pdf accessed 18 August 2023
  20. Brookes SM, Mansfield KL, Reid SM, Coward V, Warren C et al. Incursion of H5N8 high pathogenicity avian influenza virus (HPAIV) into gamebirds in England. Epidemiol Infect 2022; 150: [View Article]
     [Google Scholar]
  21. Madden J, Sage R. Ecological Consequences of Gamebird Releasing and Management on Lowland Shoots in England: A Review by Rapid Evidence Assessment for Natural England and the British Association of Shooting and Conservation., Natural England Evidence Review. NEER016. Peterborough: Natural England; 2020
  22. Gortázar C, Acevedo P, Ruiz-Fons F, Vicente J. Disease risks and overabundance of game species. Eur J Wildl Res 2006; 52:81–87 [View Article]
     [Google Scholar]
  23. Bertran K, Dolz R, Majó N. Pathobiology of avian influenza virus infection in minor gallinaceous species: a review. Avian Pathology 2014; 43:9–25 [View Article]
     [Google Scholar]
  24. Bertran K, Lee D-H, Pantin-Jackwood MJ, Spackman E, Balzli C et al. Pathobiology of clade 2.3.4.4 H5Nx high-pathogenicity avian influenza virus infections in minor gallinaceous poultry supports early backyard flock introductions in the Western United States in 2014-2015. J Virol 2017; 91:e00960-17 [View Article] [PubMed]
     [Google Scholar]
  25. Slemons RD, Easterday BC. Host response differences among 5 avian species to an influenzavirus--A-turkey-Ontario-7732-66 (Hav5N?). Bull World Health Organ 1972; 47:521–525 [PubMed]
     [Google Scholar]
  26. Liang Y, Krog JS, Ryt-Hansen P, Pedersen AG, Kvisgaard LK et al. Molecular characterization of highly pathogenic avian influenza viruses H5N6 detected in Denmark in 2018-2019. Viruses 2021; 13:1052 [View Article] [PubMed]
     [Google Scholar]
  27. Liang Y, Hjulsager CK, Seekings AH, Warren CJ, Lean FZX et al. Pathogenesis and infection dynamics of high pathogenicity avian influenza virus (HPAIV) H5N6 (clade 2.3.4.4b) in pheasants and onward transmission to chickens. Virology 2022; 577:138–148 [View Article] [PubMed]
     [Google Scholar]
  28. APHA (Animal and Plant Health Agency) Highly pathogenic avian influenza (HPAI) in the UK, and Europe. Updated Outbreak Assessment. (1 March 2021) number #18; 2021 https://webarchive.nationalarchives.gov.uk/ukgwa/20210802175516/https://www.gov.uk/government/publications/avian-influenza-bird-flu-in-europe accessed 15 January 2024
  29. APHA (Animal and Plant Health Agency) Highly pathogenic avian influenza (HPAI) in the UK, and Europe. Updated Outbreak Assessment. (25 April 2022) #24; 2022 https://www.gov.uk/government/publications/avian-influenza-bird-flu-in-europe accessed 15 January 2024
  30. Slomka MJ, Reid SM, Byrne AMP, Coward VJ, Seekings J et al. Efficient and informative laboratory testing for rapid confirmation of H5N1 (Clade 2.3.4.4) high-pathogenicity avian influenza outbreaks in the United Kingdom. Viruses 2023; 15:1344 [View Article] [PubMed]
     [Google Scholar]
  31. Tammiranta N, Isomursu M, Fusaro A, Nylund M, Nokireki T et al. Highly pathogenic avian influenza A (H5N1) virus infections in wild carnivores connected to mass mortalities of pheasants in Finland. Infect Genet Evol 2023; 111:105423 [View Article] [PubMed]
     [Google Scholar]
  32. Liang Y, Boklund AE, Larsen LE, Breum SØ, Giese S et al. Transmission Routes of Clade 2.3.4.4b H5Nx High Pathogenicity Avian Influenza Viruses into Poultry in Denmark in 2020/2021 and 2021/2022. Manuscript in preparation.
  33. APHA (Animal and Plant Health Agency) Gamebird keeping in Great Britain: General guidance. Updated August 2015; 2015 http://apha.defra.gov.uk/documents/surveillance/diseases/gamebirds-guidance.pdf accessed 15 January 2024
  34. Home Office Guidance on the operation of the Animals (Scientific Procedures) Act 1986 (ASPA); 2020 https://www.gov.uk/guidance/guidance-on-the-operation-of-the-animals-scientific-procedures-act-1986 accessed 15 January 2024
  35. Puranik A, Slomka MJ, Warren CJ, Thomas SS, Mahmood S et al. Transmission dynamics between infected waterfowl and terrestrial poultry: differences between the transmission and tropism of H5N8 highly pathogenic avian influenza virus (clade 2.3.4.4a) among ducks, chickens and turkeys. Virology 2020; 541:113–123 [View Article] [PubMed]
     [Google Scholar]
  36. WOAH (World Organisation for Animal Health) Avian Influenza (including infection with high pathogenicity avian influenza viruses): manual of diagnostic tests and vaccines for terrestrial animals, chapter 3.3.4; 2021 https://www.woah.org/fileadmin/Home/eng/Health_standards/tahm/3.03.04_AI.pdf accessed 15 January 2024
  37. Reed LJ, Muench H. A simple method of estimating fifty percent endpoints. Am J Epidemiol 1938; 27:493–497 [View Article]
     [Google Scholar]
  38. Slomka MJ, Puranik A, Mahmood S, Thomas SS, Seekings AH et al. Ducks are susceptible to infection with a range of doses of H5N8 highly pathogenic avian influenza virus (2016, clade 2.3.4.4b) and are largely resistant to virus-specific mortality, but efficiently transmit infection to contact turkeys. Avian Dis 2019; 63:172–180 [View Article] [PubMed]
     [Google Scholar]
  39. Slomka MJ, To TL, Tong HH, Coward VJ, Hanna A et al. Challenges for accurate and prompt molecular diagnosis of clades of highly pathogenic avian influenza H5N1 viruses emerging in Vietnam. Avian Pathol 2012; 41:177–193 [View Article] [PubMed]
     [Google Scholar]
  40. Seekings AH, Warren CJ, Thomas SS, Mahmood S, James J et al. Highly pathogenic avian influenza virus H5N6 (clade 2.3.4.4b) has a preferable host tropism for waterfowl reflected in its inefficient transmission to terrestrial poultry. Virology 2021; 559:74–85 [View Article] [PubMed]
     [Google Scholar]
  41. Slomka MJ, Pavlidis T, Coward VJ, Voermans J, Koch G et al. Validated realtime reverse transcriptase PCR methods for the diagnosis and pathotyping of Eurasian H7 avian influenza viruses. Influenza Other Respir Viruses 2009; 3:151–164 [View Article] [PubMed]
     [Google Scholar]
  42. Nagy A, Černíková L, Kunteová K, Dirbáková Z, Thomas SS et al. A universal RT-qPCR assay for “One Health” detection of influenza A viruses. PLoS One 2021; 16:e0244669 [View Article] [PubMed]
     [Google Scholar]
  43. Löndt BZ, Nunez A, Banks J, Nili H, Johnson LK et al. Pathogenesis of highly pathogenic avian influenza A/turkey/Turkey/1/2005 H5N1 in Pekin ducks (Anas platyrhynchos) infected experimentally. Avian Pathol 2008; 37:619–627 [View Article] [PubMed]
     [Google Scholar]
  44. Slomka MJ, Seekings AH, Mahmood S, Thomas S, Puranik A et al. Unexpected infection outcomes of China-origin H7N9 low pathogenicity avian influenza virus in turkeys. Sci Rep 2018; 8:7322 [View Article] [PubMed]
     [Google Scholar]
  45. James J, Billington E, Warren CJ, De Sliva D, Di Genova C et al. 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. J Gen Virol 2023; 104: [View Article] [PubMed]
     [Google Scholar]
  46. Lee HK, Tang JW-T, Kong DH-L, Koay ES-C. Simplified large-scale sanger genome sequencing for influenza A/H3N2 virus. PLoS One 2013; 8:e64785 [View Article] [PubMed]
     [Google Scholar]
  47. Shepard SS, Meno S, Bahl J, Wilson MM, Barnes J et al. Viral deep sequencing needs an adaptive approach: IRMA, the iterative refinement meta-assembler. BMC Genomics 2016; 17:801 [View Article] [PubMed]
     [Google Scholar]
  48. Pohlmann A, King J, Fusaro A, Zecchin B, Banyard AC et al. Has epizootic become enzootic? Evidence for a fundamental change in the infection dynamics of highly pathogenic avian influenza in Europe, 2021. mBio 2022; 13:e0060922 [View Article] [PubMed]
     [Google Scholar]
  49. Seekings AH, Warren CJ, Thomas SS, Lean FZX, Selden D et al. Different outcomes of chicken infection with UK-origin H5N1-2020 and H5N8-2020 high-pathogenicity avian influenza viruses (clade 2.3.4.4b). Viruses 2023; 15:1909 [View Article] [PubMed]
     [Google Scholar]
  50. Lean FZX, Núñez A, Banyard AC, Reid SM, Brown IH et al. Gross pathology associated with highly pathogenic avian influenza H5N8 and H5N1 in naturally infected birds in the UK (2020-2021). Vet Rec 2022; 190:e731 [View Article] [PubMed]
     [Google Scholar]
  51. Lean FZX, Vitores AG, Reid SM, Banyard AC, Brown IH et al. Gross pathology of high pathogenicity avian influenza virus H5N1 2021-2022 epizootic in naturally infected birds in the United Kingdom. One Health 2022; 14:100392 [View Article] [PubMed]
     [Google Scholar]
  52. Perkins LEL, Swayne DE. Pathobiology of A/chicken/Hong Kong/220/97 (H5N1) avian influenza virus in seven gallinaceous species. Vet Pathol 2001; 38:149–164 [View Article] [PubMed]
     [Google Scholar]
  53. Leyson C, Youk SS, Smith D, Dimitrov K, Lee DH et al. Pathogenicity and genomic changes of a 2016 European H5N8 highly pathogenic avian influenza virus (clade 2.3.4.4) in experimentally infected mallards and chickens. Virology 2019; 537:172–185 [View Article] [PubMed]
     [Google Scholar]
  54. Animal and Plant Health Agency Avian influenza in wild birds; 2023 https://www.gov.uk/government/publications/avian-influenza-in-wild-birds accessed 15 January 2024
  55. Animal and Plant Health Agency Highly Pathogenic Avian Influenza H5N1 outbreaks in Great Britain: United Kingdom October 2021 to September 2022. n.d https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/1166985/Highly_Pathogenic_Avian_Influenza_H5N1_outbreaks_in_Great_Britain_2021_to_2022.pdf accessed 15 January 2024
  56. Pan American Health Organization (PAHO) PAHO Issues Alert on Outbreaks of Avian Influenza in Birds in Ten Countries of the Americas (17 January 2023). n.d https://www.paho.org/en/news/17-1-2023-paho-issues-alert-outbreaks-avianinfluenza-birds-ten-countries-americas accessed 15 January 2024
  57. Caliendo V, Lewis NS, Pohlmann A, Baillie SR, Banyard AC et al. Transatlantic spread of highly pathogenic avian influenza H5N1 by wild birds from Europe to North America in 2021. Sci Rep 2022; 12:11729 [View Article] [PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001946
Loading
Transmission dynamics and pathogenesis differ between pheasants and partridges infected with clade 2.3.4.4b H5N8 and H5N1 high-pathogenicity avian influenza viruses
J. Gen. Virol. 105, 001946 (2024); https://doi.org/10.1099/jgv.0.001946
/content/journal/jgv/10.1099/jgv.0.001946
/content/journal/jgv/10.1099/jgv.0.001946
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error