Journal for Veterinary Medicine, Biotechnology and Biosafety

Volume 11, Issue 1, January 2025, Pages 22–29

ISSN 2411-3174 (print version) ISSN 2411-0388 (online version)

SEROLOGICAL STUDIES OF WILD BIRDS OF THE ORDER PASSERIFORMES IN UKRAINE FOR THE PRESENCE OF ANTIBODIES TO THE INFLUENZA A VIRUS

Popova A. O., Muzyka N. M.

National Scientific Center ‘Institute of Experimental and Clinical Veterinary Medicine’, Kharkiv, Ukraine, e-mail: anastasiyaolegovna1996@gmail.com

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Citation for print version: Popova, A. O. and Muzyka, N. M. (2025) ‘Serological studies of wild birds of the order Passeriformes in Ukraine for the presence of antibodies to the Influenza A virus’, Journal for Veterinary Medicine, Biotechnology and Biosafety, 11(1), pp. 22–29.

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Citation for online version: Popova, A. O. and Muzyka, N. M. (2025) ‘Serological studies of wild birds of the order Passeriformes in Ukraine for the presence of antibodies to the Influenza A virus’, Journal for Veterinary Medicine, Biotechnology and Biosafety, 11(1), pp. 22–29. DOI: 10.36016/JVMBBS-2025-11-1-4.

Summary. The influenza A virus is classified as a particularly dangerous infection that causes severe disease in birds, humans, and animals. Given the biological characteristics of the influenza virus, its ability to rapidly mutate, and its potential to cross the interspecies barrier, special attention is currently being paid to the study of the circulation of this pathogen among various natural hosts. Wild waterfowl are believed to be the main natural reservoir of the influenza A virus, while the role of birds of the Passeriformes order remains uncertain. Notably, wild birds of the order Passeriformes comprise 60% of the global avian population, underscoring their ecological significance. This order encompasses many species with diverse biological, ecological, and behavioral characteristics. Some Passeriformes species are stable synanthropes, able to coexist with humans and domestic animals in urban and natural habitats. Due to the peculiarities of nesting, feeding, and especially watering places, they can potentially play a role in transmission to other birds. The purpose of our research was to conduct serological monitoring in Ukraine among birds of the order Passeriformes, as they can also be potential carriers of the influenza virus, but this issue has not been sufficiently studied in Ukraine. In 2023–2024, biological samples were collected from 32 species of Passeriformes in 5 regions of Ukraine in the amount of 354 samples. Blood sera and egg yolks were tested in ELISA and hemagglutination inhibition test to H5 and H7 subtypes of influenza virus. Antibodies to the influenza A virus were found in blood samples from the blackbird (seroprevalence was 11.1%), the song thrush (20%), and the blackcap (100%). The titer of antibodies in the HIT was 1:16 to the H7 influenza virus subtype from the Blackbird. ELISA detected no antibodies to the influenza virus in the egg yolk extracts

Keywords: seroprevalence, virus circulation, ELISA, hemagglutination inhibition test

References:

Abdelwhab, E. M. and Mettenleiter, T. C. (2023) ‘Zoonotic animal influenza virus and potential mixing vessel hosts’, Viruses, 15(4), p. 980. doi: 10.3390/v15040980.

Arenas, A., Carranza, J., Perea, A., Miranda, A., Maldonado, A. and Hermoso, M. (1990) ‘Type A influenza viruses in birds in southern Spain: Serological survey by enzymelinked immunosorbent assay and haemagglutination inhibition tests’, Avian Pathology, 19(3), pp. 539–546. doi: 10.1080/03079459008418706.

Blachere, F. M., Lindsley, W. G., Weber, A. M., Beezhold, D. H., Thewlis, R. E., Mead, K. R. and Noti, J. D. (2018) ‘Detection of an avian lineage influenza A(H7N2) virus in air and surface samples at a New York City feline quarantine facility’, Influenza and Other Respiratory Viruses, 12(5), pp. 613–622. doi: 10.1111/irv.12572.

Cabrera-Gaytán, D. A. (2024) ‘Avian influenza: a latent challenge’ [Influenza aviar: un reto latente], Revista Médica del Instituto Mexicano del Seguro Social, 62(6), p. e6383. doi: 10.5281/zenodo.12668094. [in Spanish].

Fereidouni, S., Munoz, O., Von Dobschuetz, S. and De Nardi, M. (2016) ‘Influenza virus infection of marine mammals’, EcoHealth, 13(1), pp. 161–170. doi: 10.1007/s10393-014-0968-1.

Flynn, O., Gallagher, C., Mooney, J., Irvine, C., Ducatez, M., Hause, B., McGrath, G. and Ryan, E. (2018) ‘Influenza D virus in cattle, Ireland’, Emerging Infectious Diseases, 24(2), pp. 389–391. doi: 10.3201/eid2402.170759.

Fujimoto, Y., Usui, T., Ito, H., Ono, E. and Ito, T. (2015) ‘Susceptibility of wild passerines to subtype H5N1 highly pathogenic avian influenza viruses’, Avian Pathology, 44(4), pp. 243–247. doi: 10.1080/03079457.2015.1043235.

Han, Y., Hou, G., Jiang, W., Han, C., Liu, S., Chen, Jie, Li, J., Zhang, P., Huang, B., Liu, Y. and Chen, Jiming (2012) ‘A survey of Avian influenza in tree sparrows in China in 2011’, PLoS One, 7(4), p. e33092. doi: 10.1371/journal.pone.0033092.

Hatta, M., Zhong, G., Gao, Y., Nakajima, N., Fan, S., Chiba, S., Deering, K. M., Ito, M., Imai, M., Kiso, M., Nakatsu, S., Lopes, T. J., Thompson, A. J., McBride, R., Suarez, D. L., Macken, C. A., Sugita, S., Neumann, G., Hasegawa, H., Paulson, J. C., Toohey-Kurth, K. L. and Kawaoka, Y. (2018) ‘Characterization of a Feline influenza A(H7N2) virus’, Emerging Infectious Diseases, 24(1), pp. 75–86. doi: 10.3201/eid2401.171240.

Horimoto, T., Hiono, T., Mekata, H., Odagiri, T., Lei, Z., Kobayashi, T., Norimine, J., Inoshima, Y., Hikono, H., Murakami, K., Sato, R., Murakami, H., Sakaguchi, M., Ishii, K., Ando, T., Otomaru, K., Ozawa, M., Sakoda, Y. and Murakami, S. (2016) ‘Nationwide distribution of Bovine influenza D virus infection in Japan’, PLoS One, 11(9), p. e0163828. doi: 10.1371/journal.pone.0163828.

Jöstl, N., Weidinger, P., Lussy, H., Bailey, T. A., Joseph, S., McKeown, S., O’Donovan, D., Li, X. and Nowotny, N. (2023) ‘Antibody prevalence to Avian influenza virus subtypes H5, H7 and H9 in falcons, captive and wild birds, United Arab Emirates, 2003–2006’, Veterinary Medicine and Science, 9(4), pp. 1890–1900. doi: 10.1002/vms3.1156.

Kawaoka, Y. and Neumann, G. (2012) ‘Influenza viruses: An introduction’, in Kawaoka, Y. and Neumann, G. (eds.) Influenza Virus: Methods and Protocols. Totowa, NJ: Humana Press (Methods in Molecular Biology, 865), pp. 1–9. doi: 10.1007/978-1-61779-621-0_1.

Lee, C. T., Slavinski, S., Schiff, C., Merlino, M., Daskalakis, D., Liu, D., Rakeman, J. L., Misener, M., Thompson, C., Leung, Y. L., Varma, J. K., Fry, A., Havers, F., Davis, T., Newbury, S., Layton, M., For the Influenza A(H7N2) Response Team (2017) ‘Outbreak of Influenza A(H7N2) among cats in an animal shelter with cat-to-human transmission—New York City, 2016’, Clinical Infectious Diseases, 65(11), pp. 1927–1929. doi: 10.1093/cid/cix668.

Leibler, J. H., Abdelgadir, A., Seidel, J., White, R. F., Johnson, W. E., Reynolds, S. J., Gray, G. C. and Schaeffer, J. W. (2023) ‘Influenza D virus exposure among US cattle workers: A call for surveillance’, Zoonoses and Public Health, 70(2), pp. 166–170. doi: 10.1111/zph.13008.

Liu, R., Sheng, Z., Huang, C., Wang, D. and Li, F. (2020) ‘Influenza D virus’, Current Opinion in Virology, 44, pp. 154–161. doi: 10.1016/j.coviro.2020.08.004.

Malekian, M., Shagholian, J. and Hosseinpour, Z. (2021) ‘Pathogen presence in wild birds inhabiting landfills in Central Iran’, EcoHealth, 18(1), pp. 76–83. doi: 10.1007/s10393-021-01516-0.

Marinova-Petkova, A., Laplante, J., Jang, Y., Lynch, B., Zanders, N., Rodriguez, M., Jones, J., Thor, S., Hodges, E., De La Cruz, J. A., Belser, J., Yang, H., Carney, P., Shu, B., Berman, L., Stark, T., Barnes, J., Havers, F., Yang, P., Trock, S. C., Fry, A., Gubareva, L., Bresee, J. S., Stevens, J., Daskalakis, D., Liu, D., Lee, C. T., Torchetti, M. K., Newbury, S., Cigel, F., Toohey-Kurth, K., St. George, K., Wentworth, D. E., Lindstrom, S. and Davis, C. T. (2017) ‘Avian Influenza A(H7N2) virus in human exposed to sick cats, New York, USA, 2016’, Emerging Infectious Diseases, 23(12), pp. 2046–2049. doi: 10.3201/eid2312.170798.

Morishita, T. Y., Aye, P. P., Ley, E. C. and Harr, B. S. (1999) ‘Survey of pathogens and blood parasites in free-living passerines’, Avian Diseases, 43(3), pp. 549–552. PMID: 10494426.

Neumann, G., Treanor, J. J. and Kawaoka, Y. (2021) ‘Orthomyxoviruses’, in Howley, P. M. and Knipe, D. M. (eds.) Fields Virology. Vol. 1: Emerging Viruses. 7th ed. Philadelphia: Lippincott Willams and Wilkins, pp. 886–949. ISBN: 9781975112547. Available at: https://www.wolterskluwer.com/en/solutions/ovid/fields-virology--emerging-viruses-12601.

Peterson, A. T., Bush, S. E., Spackman, E., Swayne, D. E. and Ip, H. S. (2008) ‘Influenza A virus infections in land birds, People’s Republic of China’, Emerging Infectious Diseases, 14(10), pp. 1644–1646. doi: 10.3201/eid1410.080169.

Puryear, W., Sawatzki, K., Hill, N., Foss, A., Stone, J. J., Doughty, L., Walk, D., Gilbert, K., Murray, M., Cox, E., Patel, P., Mertz, Z., Ellis, S., Taylor, J., Fauquier, D., Smith, A., DiGiovanni, R. A., Van De Guchte, A., Gonzalez-Reiche, A. S., Khalil, Z., Van Bakel, H., Torchetti, M. K., Lantz, K., Lenoch, J. B. and Runstadler, J. (2023) ‘Highly pathogenic avian influenza A(H5N1) virus outbreak in New England seals, United States’, Emerging Infectious Diseases, 29(4), pp. 786–791. doi: 10.3201/eid2904.221538.

Root, J. J., Ellis, J. W. and Shriner, S. A. (2022) ‘Strength in numbers: Avian influenza A virus transmission to poultry from a flocking passerine’, Transboundary and Emerging Diseases, 69(4), pp. e1153–e1159. doi: 10.1111/tbed.14397.

Schnebel, B., Dierschke, V., Rautenschlein, S. and Ryll, M. (2005) ‘No detection of Avian influenza A viruses of the subtypes H5 and H7 and isolation of lentogenic Avian paramyxovirus serotype 1 in passerine birds during stopover in the year 2001 on the island Helgoland (North Sea)’, DTW. Deutsche Tierarztliche Wochenschrift, 112(12), pp. 456–460. PMID: 16425631.

Slusher, M. J., Wilcox, B. R., Lutrell, M. P., Poulson, R. L., Brown, J. D., Yabsley, M. J. and Stallknecht, D. E. (2014) ‘Are passerine birds reservoirs for Influenza a viruses?’, Journal of Wildlife Diseases, 50(4), pp. 792–809. doi: 10.7589/2014-02-043.

Spackman, E. (ed.) (2020) Animal Influenza Virus: Methods and Protocols. 3rd ed. New York, NY: Springer (Methods in Molecular Biology, 2123). doi: 10.1007/978-1-0716-0346-8.

Stehnii, B. T. and Muzyka, D. V. (2004) Method for Extracting Yolks of Avian Eggs for Immunologic Analysis [Sposib oderzhannia ekstraktu zhovtkiv yaiets dykykh ptakhiv dlia vykorystannia v imunobiolohichnykh reaktsiiakh]. Patent no. UA 70248 A. Available at: https://sis.nipo.gov.ua/en/search/detail/380805. [in Ukrainian].

Thorsson, E., Zohari, S., Roos, A., Banihashem, F., Bröjer, C. and Neimanis, A. (2023) ‘Highly pathogenic avian influenza A(H5N1) virus in a harbor porpoise, Sweden’, Emerging Infectious Diseases, 29(4), pp. 852–855. doi: 10.3201/eid2904.221426.

Tumpey, T. M., Basler, C. F., Aguilar, P. V., Zeng, H., Solórzano, A., Swayne, D. E., Cox, N. J., Katz, J. M., Taubenberger, J. K., Palese, P. and García-Sastre, A. (2005) ‘Characterization of the reconstructed 1918 Spanish influenza pandemic virus’, Science, 310(5745), pp. 77–80. doi: 10.1126/science.1119392.

Wasik, B. R., Voorhees, I. E. H. and Parrish, C. R. (2021) ‘Canine and feline influenza’, Cold Spring Harbor Perspectives in Medicine, 11(1), p. a038562. doi: 10.1101/cshperspect.a038562.

Williams, S. M., Dufour-Zavala, L., Jackwood, M. W., Lee, M. D., Lupiani, B., Reed, W. M., Spackman, E. and Woolcock, P. R. (2016) A Laboratory Manual for the Isolation, Identification, and Characterization of Avian Pathogens. 6th ed. Athens, GA: American Association of Avian Pathologists. ISBN 9780978916374.

Williams, R. A. J., Sánchez-Llatas, C. J., Doménech, A., Madrid, R., Fandiño, S., Cea-Callejo, P., Gomez-Lucia, E. and Benítez, L. (2023) ‘Emerging and novel viruses in passerine birds’, Microorganisms, 11(9), p. 2355. doi: 10.3390/microorganisms11092355.

Zhang, Z. and Lei, Z. (2024) ‘The alarming situation of Highly pathogenic avian influenza viruses in 2019–2023’, Global Medical Genetics, 11(03), pp. 200–213. doi: 10.1055/s-0044-1788039.