1887

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.

Funding
This study was supported by the:
  • Defra (Award SE2213)
    • Principle Award Recipient: AshleyC Banyard
  • BBSRC (Award BB/X006204/1)
    • Principle Award Recipient: JoeJames
  • 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.0.001852
2023-05-11
2024-04-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/104/5/jgv001852.html?itemId=/content/journal/jgv/10.1099/jgv.0.001852&mimeType=html&fmt=ahah

References

  1. 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]
  2. Adlhoch C, Gossner C, Koch G, Brown I, Bouwstra R et al. Comparing introduction to Europe of highly pathogenic avian influenza viruses A(H5N8) in 2014 and A(H5N1) in 2005. Euro Surveill 2014; 19:20996 [View Article] [PubMed]
    [Google Scholar]
  3. Adlhoch C, Fusaro A, Gonzales JL, Kuiken T, Marangon S et al. Avian influenza overview March - June 2022. EFSA J 2022; 20:e07415 [View Article] [PubMed]
    [Google Scholar]
  4. Adlhoch C, Brouwer A, Kuiken T, Mulatti P, Smietanka K et al. Avian influenza overview February - May 2018. EFSA J 2018; 16:e05358 [View Article] [PubMed]
    [Google Scholar]
  5. Beerens N, Koch G, Heutink R, Harders F, Vries DPE et al. Novel highly pathogenic Avian influenza A(H5N6) virus in the Netherlands, December 2017. Emerg Infect Dis 2018; 24:770–773 [View Article] [PubMed]
    [Google Scholar]
  6. Śmietanka K, Świętoń E, Kozak E, Wyrostek K, Tarasiuk K et al. Highly pathogenic Avian influenza H5N8 in Poland in 2019-2020. J Vet Res 2020; 64:469–476 [View Article] [PubMed]
    [Google Scholar]
  7. Adlhoch C, Fusaro A, Gonzales JL, Kuiken T, Marangon S et al. Avian influenza overview February - May 2021. EFSA J 2021; 19:e06951 [View Article] [PubMed]
    [Google Scholar]
  8. Byrne AM, James J, Mollett BC, Meyer SM, Lewis T et al. Investigating the genetic diversity of H5 avian influenza in the UK 2020-2022. bioRxiv [View Article]
    [Google Scholar]
  9. Adlhoch C, Fusaro A, Gonzales JL, Kuiken T, Marangon S et al. Avian influenza overview June - September 2022. EFSA J 2022; 20:e07597 [View Article] [PubMed]
    [Google Scholar]
  10. 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]
  11. Banyard AC, Lean FZX, Robinson C, Howie F, Tyler G et al. Detection of highly pathogenic Avian influenza virus H5N1 clade 2.3.4.4b in great Skuas: a species of conservation concern in Great Britain. Viruses 2022; 14:212 [View Article] [PubMed]
    [Google Scholar]
  12. Adlhoch C, Fusaro A, Gonzales JL, Kuiken T, Marangon S et al. Avian influenza overview December 2021 - March 2022. EFSA J 2022; 20:e07289 [View Article] [PubMed]
    [Google Scholar]
  13. The Animal and Plant Health Agency (APHA) Updated Outbreak Assessment #34: The Animal and Plant Health Agency; 2022
  14. Floyd T, Banyard AC, Lean FZX, Byrne AMP, Fullick E et al. Encephalitis and death in wild mammals at a rehabilitation center after infection with highly pathogenic Avian influenza A(H5N8) virus, United Kingdom. Emerg Infect Dis 2021; 27:2856–2863 [View Article]
    [Google Scholar]
  15. Postel A, King J, Kaiser FK, Kennedy J, Lombardo MS et al. Infections with highly pathogenic Avian influenza A virus (HPAIV) H5N8 in harbor seals at the German North Sea coast, 2021. Emerg Microbes & Infect 2022; 11:725–729 [View Article]
    [Google Scholar]
  16. Puryear W, Sawatzki K, Hill N, Foss A, Stone JJ. Outbreak of highly pathogenic Avian influenza H5N1 in New England seals. Mol Biol [View Article]
    [Google Scholar]
  17. Rijks JM, Hesselink H, Lollinga P, Wesselman R, Prins P et al. Highly pathogenic Avian influenza A(H5N1) virus in Wild Red Foxes, the Netherlands, 2021. Emerg Infect Dis 2021; 27:2960–2962 [View Article]
    [Google Scholar]
  18. Oliver I, Roberts J, Brown CS, Byrne AM, Mellon D et al. A case of avian influenza A(H5N1) in England, January 2022. Euro Surveill 2022; 27:2200061 [View Article] [PubMed]
    [Google Scholar]
  19. 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]
  20. Pan American Health Organization PAHO issues alert on outbreaks of avian influenza in birds in ten countries of the Americas; 2023 https://www.paho.org/en/news/17-1-2023-paho-issues-alert-outbreaks-avian-influenza-birds-ten-countries-americas accessed 27 March 2023
  21. Falchieri M, Reid SM, Ross CS, James J, Byrne AMP et al. Shift in HPAI infection dynamics causes significant losses in seabird populations across Great Britain. Vet Rec 2022; 191:294–296 [View Article] [PubMed]
    [Google Scholar]
  22. 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]
  23. 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]
  24. 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]
  25. World Organisation for Animal Health (WOAH) Terrestrial Manual: Avian influenza (infection with avian influenza viruses); 2019 accessed 26 November 2019
  26. 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]
  27. World Organisation for Animal Health (WOAH) Terrestrial Manual: Chapter 3.3.4. Avian Influenza (Including infection with High Pathogenicity Avian Influenza Viruses); 2021
  28. 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]
  29. 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]
  30. James J, Slomka MJ, Reid SM, Thomas SS, Mahmood S et al. Proceedings paper-Avian diseases 10th AI symposium issue development and application of real-time PCR assays for specific detection of contemporary Avian influenza virus subtypes N5, N6, N7, N8, and N9. Avian Dis 2019; 63:209–218 [View Article] [PubMed]
    [Google Scholar]
  31. James J, Bhat S, Walsh SK, Karunarathna TK, Sadeyen J-R et al. The origin of internal genes contributes to the replication and transmission fitness of H7N9 Avian influenza virus. J Virol 2022; 96:e0129022 [View Article] [PubMed]
    [Google Scholar]
  32. Arnold ME, Slomka MJ, Breed AC, Hjulsager CK, Pritz-Verschuren S et al. Evaluation of ELISA and haemagglutination inhibition as screening tests in serosurveillance for H5/H7 avian influenza in commercial chicken flocks. Epidemiol Infect 2018; 146:306–313 [View Article] [PubMed]
    [Google Scholar]
  33. 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] [PubMed]
    [Google Scholar]
  34. Global Consortium for H5N8 and Related Influenza Viruses Role for migratory wild birds in the global spread of avian influenza H5N8. Science 2016; 354:213–217 [View Article] [PubMed]
    [Google Scholar]
  35. 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]
  36. Leyson C, Youk S-S, Smith D, Dimitrov K, Lee D-H 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]
  37. Seekings AH, Warren CJ, Thomas SS, Lean FZX, Selden D et al. Different outcomes of chicken infection with contemporary (2020) UK-origin H5N1 and H5N8 highly pathogenic avian influenza viruses (clade 2.3.4.4). In preperation 2023
    [Google Scholar]
  38. Aldous EW, Seekings JM, McNally A, Nili H, Fuller CM et al. Infection dynamics of highly pathogenic avian influenza and virulent avian paramyxovirus type 1 viruses in chickens, turkeys and ducks. Avian Pathology 2010; 39:265–273 [View Article]
    [Google Scholar]
  39. Swayne DE, Slemons RD. Using mean infectious dose of high- and low-pathogenicity avian influenza viruses originating from wild duck and poultry as one measure of infectivity and adaptation to poultry. Avian Dis 2008; 52:455–460 [View Article] [PubMed]
    [Google Scholar]
  40. Pantin-jackwook MJ, Swayne DE. Pathogenesis and pathobiology of avian influenza virus infection in birds. Rev Sci Tech OIE 2009; 28:113–136 [View Article]
    [Google Scholar]
  41. Department for Environment Food and Rural Affairs (DEFRA) Code of practice for the welfare of laying hens and pullets; 2018 https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/732227/code-of-practice-welfare-of-laying-hens-pullets.pdf accessed 27 March 2023
  42. Department for Environment Food and Rural Affairs (DEFRA) Code of practice for the welfare of meat chickens and meat breeding chickens; 2018 https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/694013/meat-chicken-code-march2018.pdf accessed 27 March 2023
  43. Department for Environment Food and Rural Affairs (DEFRA) Ducks (mallard and Pekin): welfare recommendations; 2019 https://www.gov.uk/government/publications/poultry-on-farm-welfare/ducks-mallard-and-pekin-welfare-recommendations accessed 1 December 2022
  44. Slomka M, Reid S, Byrne A, Coward V, Seekings J et al. Challenges posed by the demand for accurate and efficient laboratory confirmation of UK H5N1 (clade 2.3.4.4) highly pathogenic avian influenza virus poultry outbreaks during the continuing epizootic since 2021-2022. Viruses 2023
    [Google Scholar]
  45. Palya V, Tatár-Kis T, Walkóné Kovács E, Kiss I, Homonnay Z et al. Efficacy of a recombinant Turkey herpesvirus AI (H5) vaccine in preventing transmission of heterologous highly pathogenic H5N8 clade 2.3.4.4b challenge virus in commercial broilers and layer pullets. J Immunol Res 2018; 2018:3143189 [View Article] [PubMed]
    [Google Scholar]
  46. Reperant LA, van Amerongen G, van de Bildt MWG, Rimmelzwaan GF, Dobson AP et al. Highly pathogenic Avian influenza virus (H5N1) infection in red foxes fed infected bird carcasses. Emerg Infect Dis 2008; 14:1835–1841 [View Article]
    [Google Scholar]
  47. Bouma A, Claassen I, Natih K, Klinkenberg D, Donnelly CA et al. Estimation of transmission parameters of H5N1 avian influenza virus in chickens. PLOS Pathog 2009; 5:e1000281 [View Article] [PubMed]
    [Google Scholar]
  48. Killingley B, Nguyen-Van-Tam J. Routes of influenza transmission. Influenza Other Respir Viruses 2013; 7 Suppl 2:42–51 [View Article] [PubMed]
    [Google Scholar]
  49. James J, Byrne AMP, Goharriz H, Golding M, Cuesta JMA et al. Infectious droplet exposure is an inefficient route for SARS-CoV-2 infection in the ferret model. J Gen Virol 2022; 103:11 [View Article]
    [Google Scholar]
  50. Peacock THP, James J, Sealy JE, Iqbal M. A global perspective on H9N2 Avian influenza virus. Viruses 2019; 11:620 [View Article] [PubMed]
    [Google Scholar]
  51. Filaire F, Lebre L, Foret-Lucas C, Vergne T, Daniel P et al. Highly pathogenic Avian influenza A(H5N8) clade 2.3.4.4b virus in dust samples from poultry farms, France, 2021. Emerg Infect Dis 2022; 28:1446–1450 [View Article]
    [Google Scholar]
  52. Swayne DE. Epidemiology of avian influenza in agricultural and other man-made systems. Avian Influenza 200859–85 [View Article]
    [Google Scholar]
  53. Nikitin N, Petrova E, Trifonova E, Karpova O. Influenza virus aerosols in the air and their infectiousness. Adv Virol 2014; 2014:859090 [View Article] [PubMed]
    [Google Scholar]
  54. Beerens N, Germeraad EA, Venema S, Verheij E, Pritz-Verschuren SBE et al. Comparative pathogenicity and environmental transmission of recent highly pathogenic avian influenza H5 viruses. Emerg Microbes Infect 2021; 10:97–108 [View Article] [PubMed]
    [Google Scholar]
  55. Ahrens AK, Selinka HC, Mettenleiter TC, Beer M, Harder TC. Exploring surface water as a transmission medium of avian influenza viruses - systematic infection studies in mallards. Emerg Microbes Infect 2022; 11:1250–1261 [View Article] [PubMed]
    [Google Scholar]
  56. Department for Environment Food and Rural Affairs (DEFRA) Biosecurity and preventing welfare impacts in poultry and captive birds; 2022 https://www.gov.wales/sites/default/files/publications/2022-10/biosecurity-and-preventing-welfare-impacts-in-poultry-and-captive-birds-update.pdf accessed 27 March 2023
  57. Alexander DJ, Brown IH. History of highly pathogenic avian influenza. Revue Scientifique et Technique 2009; 28:19–38 [View Article]
    [Google Scholar]
  58. Swayne DE, Suarez DL, Sims LD. Influenza. Dis Poul 2020210–256 [View Article]
    [Google Scholar]
  59. 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]
  60. Grund C, Hoffmann D, Ulrich R, Naguib M, Schinköthe J et al. A novel European H5N8 influenza A virus has increased virulence in ducks but low zoonotic potential. Emerg Microbes Infect 2018; 7:132 [View Article] [PubMed]
    [Google Scholar]
  61. Bingham J, Green DJ, Lowther S, Klippel J, Burggraaf S et al. Infection studies with two highly pathogenic avian influenza strains (Vietnamese and Indonesian) in Pekin ducks (Anas platyrhynchos), with particular reference to clinical disease, tissue tropism and viral shedding. Avian Pathology 2009; 38:267–278 [View Article]
    [Google Scholar]
  62. Vigeveno RM, Poen MJ, Parker E, Holwerda M, de Haan K et al. Outbreak severity of highly pathogenic Avian influenza A(H5N8) viruses is inversely correlated to polymerase complex activity and interferon induction. J Virol 2020; 94:e00375-20 [View Article] [PubMed]
    [Google Scholar]
  63. Löndt BZ, Núñez A, Banks J, Alexander DJ, Russell C et al. The effect of age on the pathogenesis of a highly pathogenic avian influenza (HPAI) H5N1 virus in Pekin ducks (Anas platyrhynchos) infected experimentally. Influenza Other Respir Viruses 2010; 4:17–25 [View Article] [PubMed]
    [Google Scholar]
  64. Nagy ZA, Horváth E, Urbán Z. Antigen capture in chicken spleen during the primary immune response and relationship to phagocytic activity. Nat New Biol 1973; 242:241–244 [View Article] [PubMed]
    [Google Scholar]
  65. Parker CD, Irvine RM, Slomka MJ, Pavlidis T, Hesterberg U et al. Outbreak of Eurasian lineage H5N1 highly pathogenic avian influenza in turkeys in Great Britain in November 2007. Vet Rec 2014; 175:282 [View Article] [PubMed]
    [Google Scholar]
  66. 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]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001852
Loading
/content/journal/jgv/10.1099/jgv.0.001852
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
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