1887
Research Open Access
Like 0

Abstract

Background

Highly pathogenic avian influenza (HPAI) H5Nx and human H1N1pdm2009 influenza viruses can infect cats. Infections in cats may result in viral adaptations or recombinant viruses, which may facilitate zoonotic transfer.

Aim

We aimed to investigate the presence of HPAI H5 clade 2.3.4.4 and H1 influenza viruses and antibodies to these viruses in domestic and rural stray cats in the Netherlands and factors associated with exposure.

Methods

Sera from stray and domestic cats, sampled 2020–2023, were analysed by ELISA and confirmed by hemagglutination inhibition assay (HAI) and pharyngeal swabs and lung tissue for influenza A virus by RT-qPCR.

Results

In 701 stray cats, 83 (11.8%; 95% confidence interval (CI): 9.5–14.5) sera were positive for HPAI H5 and 65 findings were confirmed. In HAI, two sera were positive for both HPAI H5 and H1. In 871 domestic cats, four (0.46%; 95% CI: 0.13–1.2) sera were HPAI H5 positive and none were confirmed but 40 (4.6%; 95% CI: 3.3–6.2) sera were seropositive for H1 and 26 were confirmed. Stray cats living in nature reserves (odds ratio (OR) = 5.4; 95% CI: 1.5–20.1) and older cats (OR = 3.8; 95% CI: 2.7–7.1) were more likely to be HPAI H5 seropositive. No influenza A virus was detected in 230 cats.

Conclusion

The higher HPAI H5 seroprevalence in stray cats compared with domestic cats suggests more frequent viral exposure, most likely due to foraging on wild birds. In contrast, exposure to H1 was more common in domestic cats compared with stray cats.

Loading

Article metrics loading...

/content/10.2807/1560-7917.ES.2024.29.44.2400326
2024-10-31
2024-11-01
http://instance.metastore.ingenta.com/content/10.2807/1560-7917.ES.2024.29.44.2400326
Loading
Loading full text...

Full text loading...

/deliver/fulltext/eurosurveillance/29/44/eurosurv-29-44-4.html?itemId=/content/10.2807/1560-7917.ES.2024.29.44.2400326&mimeType=html&fmt=ahah

References

  1. The World Organisation for Animal Health (WOAH). OIE terrestrial manual 2021. Avian influenza (including infection with high pathogenicity avian influenza viruses). Paris: WOAH; May 2021. Available from: https://www.woah.org/en/what-we-do/standards/codes-and-manuals/terrestrial-manual-online-access
  2. Food and Agriculture Organization of the United Nations (FAO). Ongoing avian influenza outbreaks in animals pose risk to humans. Rome: FAO; 12 Jul 2023. Available from: https://www.fao.org/animal-health/news-events/news/detail/ongoing-avian-influenza-outbreaks-in-animals-pose-risk-to-humans/en
  3. Guo H, de Vries E, McBride R, Dekkers J, Peng W, Bouwman KM, et al. Highly pathogenic influenza A(H5Nx) viruses with altered H5 receptor-binding specificity. Emerg Infect Dis. 2017;23(2):220-31.  https://doi.org/10.3201/eid2302.161072  PMID: 27869615 
  4. Agüero M, Monne I, Sánchez A, Zecchin B, Fusaro A, Ruano MJ, et al. Highly pathogenic avian influenza A(H5N1) virus infection in farmed minks, Spain, October 2022. Euro Surveill. 2023;28(3):2300001.  https://doi.org/10.2807/1560-7917.ES.2023.28.3.2300001  PMID: 36695488 
  5. Bordes L, Vreman S, Heutink R, Roose M, Venema S, Pritz-Verschuren SBE, et al. Highly pathogenic avian influenza H5N1 virus infections in wild red foxes (Vulpes vulpes) show neurotropism and adaptive virus mutations. Microbiol Spectr. 2023;11(1):e0286722.  https://doi.org/10.1128/spectrum.02867-22  PMID: 36688676 
  6. Rijks JM, Hesselink H, Lollinga P, Wesselman R, Prins P, Weesendorp E, et al. Highly pathogenic avian influenza A(H5N1) virus in wild red foxes, the Netherlands, 2021. Emerg Infect Dis. 2021;27(11):2960-2.  https://doi.org/10.3201/eid2711.211281  PMID: 34670656 
  7. Puryear W, Sawatzki K, Hill N, Foss A, Stone JJ, Doughty L, et al. Highly pathogenic avian influenza A(H5N1) virus outbreak in New England seals, United States. Emerg Infect Dis. 2023;29(4):786-91.  https://doi.org/10.3201/eid2904.221538  PMID: 36958010 
  8. Burrough ER, Magstadt DR, Petersen B, Timmermans SJ, Gauger PC, Zhang J, et al. Highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024. Emerg Infect Dis. 2024;30(7):1335-43.  https://doi.org/10.3201/eid3007.240508  PMID: 38683888 
  9. Chestakova IV, van der Linden A, Bellido Martin B, Caliendo V, Vuong O, Thewessen S, et al. High number of HPAI H5 virus infections and antibodies in wild carnivores in the Netherlands, 2020-2022. Emerg Microbes Infect. 2023;12(2):2270068.  https://doi.org/10.1080/22221751.2023.2270068  PMID: 37842795 
  10. Briand F-X, Souchaud F, Pierre I, Beven V, Hirchaud E, Hérault F, et al. Highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus in domestic cat, France, 2022. Emerg Infect Dis. 2023;29(8):1696-8.  https://doi.org/10.3201/eid2908.230188  PMID: 37379514 
  11. Moreno A, Bonfante F, Bortolami A, Cassaniti I, Caruana A, Cottini V, et al. Asymptomatic infection with clade 2.3.4.4b highly pathogenic avian influenza A(H5N1) in carnivore pets, Italy, April 2023. Euro Surveill. 2023;28(35):2300441.  https://doi.org/10.2807/1560-7917.ES.2023.28.35.2300441  PMID: 37650905 
  12. Sillman SJ, Drozd M, Loy D, Harris SP. Naturally occurring highly pathogenic avian influenza virus H5N1 clade 2.3.4.4b infection in three domestic cats in North America during 2023. J Comp Pathol. 2023;205:17-23.  https://doi.org/10.1016/j.jcpa.2023.07.001  PMID: 37586267 
  13. Rabalski L, Milewska A, Pohlmann A, Gackowska K, Lepionka T, Szczepaniak K, et al. Emergence and potential transmission route of avian influenza A (H5N1) virus in domestic cats in Poland, June 2023. Euro Surveill. 2023;28(31):2300390.  https://doi.org/10.2807/1560-7917.ES.2023.28.31.2300390  PMID: 37535471 
  14. Domańska-Blicharz K, Świętoń E, Świątalska A, Monne I, Fusaro A, Tarasiuk K, et al. Outbreak of highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus in cats, Poland, June to July 2023. Euro Surveill. 2023;28(31):2300366.  https://doi.org/10.2807/1560-7917.ES.2023.28.31.2300366  PMID: 37535474 
  15. Lee K, Yeom M, Vu TTH, Do HQ, Na W, Lee M, et al. Characterization of highly pathogenic avian influenza A (H5N1) viruses isolated from cats in South Korea, 2023. Emerg Microbes Infect. 2024;13(1):2290835.  https://doi.org/10.1080/22221751.2023.2290835  PMID: 38044871 
  16. Klopfleisch R, Wolf PU, Uhl W, Gerst S, Harder T, Starick E, et al. Distribution of lesions and antigen of highly pathogenic avian influenza virus A/Swan/Germany/R65/06 (H5N1) in domestic cats after presumptive infection by wild birds. Vet Pathol. 2007;44(3):261-8.  https://doi.org/10.1354/vp.44-3-261  PMID: 17491066 
  17. Siegers JY, Ferreri L, Eggink D, Veldhuis Kroeze EJB, Te Velthuis AJW, van de Bildt M, et al. Evolution of highly pathogenic H5N1 influenza A virus in the central nervous system of ferrets. PLoS Pathog. 2023;19(3):e1011214.  https://doi.org/10.1371/journal.ppat.1011214  PMID: 36897923 
  18. Leschnik M, Weikel J, Möstl K, Revilla-Fernández S, Wodak E, Bagó Z, et al. Subclinical infection with avian influenza A (H5N1) virus in cats. Emerg Infect Dis. 2007;13(2):243-7.  https://doi.org/10.3201/eid1302.060608  PMID: 17479886 
  19. Zhao S, Schuurman N, Tieke M, Quist B, Zwinkels S, van Kuppeveld FJM, et al. Serological screening of influenza A virus antibodies in cats and dogs indicates frequent infection with different subtypes. J Clin Microbiol. 2020;58(11):e01689-20.  https://doi.org/10.1128/JCM.01689-20  PMID: 32878956 
  20. Kuiken T, Rimmelzwaan G, van Riel D, van Amerongen G, Baars M, Fouchier R, et al. Avian H5N1 influenza in cats. Science. 2004;306(5694):241.  https://doi.org/10.1126/science.1102287  PMID: 15345779 
  21. Rimmelzwaan GF, van Riel D, Baars M, Bestebroer TM, van Amerongen G, Fouchier RAM, et al. Influenza A virus (H5N1) infection in cats causes systemic disease with potential novel routes of virus spread within and between hosts. Am J Pathol. 2006;168(1):176-83, quiz 364.  https://doi.org/10.2353/ajpath.2006.050466  PMID: 16400021 
  22. Hatta M, Zhong G, Gao Y, Nakajima N, Fan S, Chiba S, et al. Characterization of a feline influenza A(H7N2) virus. Emerg Infect Dis. 2018;24(1):75-86.  https://doi.org/10.3201/eid2401.171240  PMID: 29260686 
  23. Shen H-X, Li X, Yang D-Q, Ju H-B, Ge F-F, Wang J, et al. Phylogenetic analysis and evolutionary dynamics of H3N2 canine and feline influenza virus strains from 2006 to 2019. J Med Virol. 2021;93(6):3496-507.  https://doi.org/10.1002/jmv.26767  PMID: 33386745 
  24. van den Brand JMA, Stittelaar KJ, van Amerongen G, van de Bildt MWG, Leijten LME, Kuiken T, et al. Experimental pandemic (H1N1) 2009 virus infection of cats. Emerg Infect Dis. 2010;16(11):1745-7.  https://doi.org/10.3201/eid1611.100845  PMID: 21029533 
  25. Fiorentini L, Taddei R, Moreno A, Gelmetti D, Barbieri I, De Marco MA, et al. Influenza A pandemic (H1N1) 2009 virus outbreak in a cat colony in Italy. Zoonoses Public Health. 2011;58(8):573-81.  https://doi.org/10.1111/j.1863-2378.2011.01406.x  PMID: 21824359 
  26. Löhr CV, DeBess EE, Baker RJ, Hiett SL, Hoffman KA, Murdoch VJ, et al. Pathology and viral antigen distribution of lethal pneumonia in domestic cats due to pandemic (H1N1) 2009 influenza A virus. Vet Pathol. 2010;47(3):378-86.  https://doi.org/10.1177/0300985810368393  PMID: 20382823 
  27. Duijvestijn MBHM, Schuurman NNMP, Vernooij JCM, van Leeuwen MAJM, Bosch B-J, van den Brand JMA, et al. Serological survey of retrovirus and coronavirus infections, including SARS-CoV-2, in rural stray cats in the Netherlands, 2020-2022. Viruses. 2023;15(7):1531.  https://doi.org/10.3390/v15071531  PMID: 37515217 
  28. World Health Organization (WHO). Genetic and antigenic characteristics of zoonotic influenza A viruses and development of candidate vaccine viruses for pandemic preparedness. Geneve: WHO; Sep 2023. Available from: https://cdn.who.int/media/docs/default-source/influenza/who-influenza-recommendations/vcm-southern-hemisphere-recommendation-2024/202309_zoonotic_vaccinvirusupdate.pdf?sfvrsn=e78676a0_5
  29. de Vries RP, de Vries E, Moore KS, Rigter A, Rottier PJM, de Haan CAM. Only two residues are responsible for the dramatic difference in receptor binding between swine and new pandemic H1 hemagglutinin. J Biol Chem. 2011;286(7):5868-75.  https://doi.org/10.1074/jbc.M110.193557  PMID: 21173148 
  30. Koel BF, van der Vliet S, Burke DF, Bestebroer TM, Bharoto EE, Yasa IWW, et al. Antigenic variation of clade 2.1 H5N1 virus is determined by a few amino acid substitutions immediately adjacent to the receptor binding site. MBio. 2014;5(3):e01070-14.  https://doi.org/10.1128/mBio.01070-14  PMID: 24917596 
  31. Munster VJ, Baas C, Lexmond P, Bestebroer TM, Guldemeester J, Beyer WEP, et al. Practical considerations for high-throughput influenza A virus surveillance studies of wild birds by use of molecular diagnostic tests. J Clin Microbiol. 2009;47(3):666-73.  https://doi.org/10.1128/JCM.01625-08  PMID: 19109483 
  32. Ende MVD, Strijkstra A, Dias E, Smit C. Spatial ecology and prey choice of tagged feral cats on the island of Schiermonnikoog, 2017. Lutra. 2017;60(2):73-91.
  33. Villanueva-Saz S, Martínez M, Rueda P, Pérez MD, Lacasta D, Marteles D, et al. Serological exposure to influenza A in cats from an area with wild birds positive for avian influenza. Zoonoses Public Health. 2024;71(3):324-30.  https://doi.org/10.1111/zph.13085  PMID: 37872888 
  34. Vahlenkamp TW, Teifke JP, Harder TC, Beer M, Mettenleiter TC. Systemic influenza virus H5N1 infection in cats after gastrointestinal exposure. Influenza Other Respir Viruses. 2010;4(6):379-86.  https://doi.org/10.1111/j.1750-2659.2010.00173.x  PMID: 20958932 
  35. Reperant LA, van de Bildt MW, van Amerongen G, Leijten LM, Watson S, Palser A, et al. Marked endotheliotropism of highly pathogenic avian influenza virus H5N1 following intestinal inoculation in cats. J Virol. 2012;86(2):1158-65.  https://doi.org/10.1128/JVI.06375-11  PMID: 22090101 
  36. Kim HM, Park EH, Yum J, Kim HS, Seo SH. Greater virulence of highly pathogenic H5N1 influenza virus in cats than in dogs. Arch Virol. 2015;160(1):305-13.  https://doi.org/10.1007/s00705-014-2284-z  PMID: 25416494 
  37. Vahlenkamp TW, Harder TC, Giese M, Lin F, Teifke JP, Klopfleisch R, et al. Protection of cats against lethal influenza H5N1 challenge infection. J Gen Virol. 2008;89(Pt 4):968-74.  https://doi.org/10.1099/vir.0.83552-0  PMID: 18343838 
  38. Driskell EA, Jones CA, Berghaus RD, Stallknecht DE, Howerth EW, Tompkins SM. Domestic cats are susceptible to infection with low pathogenic avian influenza viruses from shorebirds. Vet Pathol. 2013;50(1):39-45.  https://doi.org/10.1177/0300985812452578  PMID: 22732359 
  39. Chestakova IV, van der Linden A, Bellido Martin B, Caliendo V, Vuong O, Thewessen S, et al. High number of HPAI H5 virus infections and antibodies in wild carnivores in the Netherlands, 2020-2022. Emerg Microbes Infect. 2023;12(2):2270068.  https://doi.org/10.1080/22221751.2023.2270068  PMID: 37842795 
  40. Ellebedy AH, Krammer F, Li G-M, Miller MS, Chiu C, Wrammert J, et al. Induction of broadly cross-reactive antibody responses to the influenza HA stem region following H5N1 vaccination in humans. Proc Natl Acad Sci USA. 2014;111(36):13133-8.  https://doi.org/10.1073/pnas.1414070111  PMID: 25157133 
  41. Guthmiller JJ, Han J, Utset HA, Li L, Lan LY-L, Henry C, et al. Broadly neutralizing antibodies target a haemagglutinin anchor epitope. Nature. 2022;602(7896):314-20.  https://doi.org/10.1038/s41586-021-04356-8  PMID: 34942633 
  42. National Institute for Public Health and the Environment (RIVM). Feiten en cijfers griep. [Flu facts and figures]. Bilthoven: RIVM; 27 Sep 2024. Available from: https://www.rivm.nl/griep-griepprik/feiten-en-cijfers
/content/10.2807/1560-7917.ES.2024.29.44.2400326
Loading

Data & Media loading...

Supplementary data

Submit comment
Close
Comment moderation successfully completed
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