Highly pathogenic avian influenza in the world: vaccination strategies (review)

Avian influenza viruses are epidemiologically dangerous zoonotic pathogens that can cause high morbidity and mortality both in animals and in humans. Reassortment and antigenic shift in the genome of the avian influenza virus draw to a change in its properties: host range, virulence, and other factors. The natural reservoir of avian influenza is wild waterfowl, which can transmit the virus to poultry through the direct contact. The exchange of antigenic sites of viruses occurs over several months in the traditional wintering grounds of migratory birds. Avian influenza viruses with altered genes as a result of reassortment, circulating in wild migratory birds, carry epizootic threat of spread of the disease to the unharmed areas. In this review of highly pathogenic avian influenza there has been analyzed the epizootic situation and possible vaccination strategies that exist in the world. The spatial trend in the spread of highly pathogenic avian influenza in the constituent entities of the Russian Federation was determined using the GIS tool, Median Center in the working environment of the ArcGIS Pro software. Based on the review of selected literature, it has been established that vaccination itself is not considered a solution to the problem. Without monitoring systems, stringent biosecurity and population reduction in case of outbreaks, the control and eradication of the disease is impossible. The decision to vaccinate against avian influenza should be made on a case-by-case basis, weighing all the risks of further spread and mutation of the virus. All industrial poultry enterprises exporting the products must operate in a closed mode and be excepted from the list of vaccination.

1. Lycett S. J., Duchatel F., Digard P. A brief history of bird flu. Philos Trans R Soc Lond B Biol Scii. 2019;374(1775):20180257. DOI: https://doi.org/10.1098/rstb.2018.0257

2. Webster R. G., Bean W. J., Gorman O. T., Chambers T. M., Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol. Rev. 1992;56(1): 152-179. DOI: https://doi.org/10.1128/mr.56.1.152-179.1992

3. Chen R., Holmes E. C. Avian influenza virus exhibits rapid evolutionary dynamics. Mol. Biol. Evol. 2006;23(12):2336-2341. DOI: https://doi.org/10.1093/molbev/msl102

4. Vasin A. V., Temkina O. A., Egorov V. V., Klotchenko S. A., Plotnikova M. A., Kiselev O. I. Molecular mechanisms enhancing the proteome of influenza A viruses: an overview of recently discovered proteins. Virus Res. 2014;185:53-63. DOI: https://doi.org/10.1016/j.virusres.2014.03.015

5. Mehle A., Dugan V. G., Taubenberger J. K., Doudna J. A. Reassortment and Mutation of the Avian Influenza Virus Polymerase PA Subunit Overcome Species Barriers. J. Virol. 2012;86(3):1750-1757. DOI: https://doi.org/10.1128/JVI.06203-11

6. Fouchier R. A., Munster V., Wallensten A., Bestebroer T. M., Herfst S., Smith D., Rimmelzwaan G. F., Olsen B., Osterhaus A. D. Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from black-headed gulls. J. Virol. 2005;79(5):2814-2822. DOI: https://doi.org/10.1128/JVI.79.5.2814-2822.2005

7. Shi W., Gao G. F. Emerging H5N8 avian influenza viruses. Science. 2021;372(6544):784-786. DOI: https://doi.org/10.1126/science.abg6302

8. Pechenkina A. A. Avian influenza: history, pathogen, epidemiology. Vestnik sovremennykh issledovaniy. 2020;(5-1(35)):16-20. (In Russ.). URL: https://www.elibrary.ru/item.asp?id=43942410&

9. Sims L. D., Swayne D. E. Animal Influenza. 2nd ed. John Wiley & Sons, Inc.; Ames, IA, USA: 2016, Avian influenza control strategies. pp. 363-377. URL: https://www.wiley.com/en-us/Animal+Influenza%2C+2nd+Edition-p-9781118907467

10. Boni M. F., Galvani A. P., Wickelgren A. L., Malani A. Economic epidemiology of avian influenza on small-holder poultry farms. Theor Popul Biol. 2013;90:135-144. DOI: https://doi.org/10.1016/j.tpb.2013.10.001

11. Mehta K, Goneau L. W., Wong J., L’Huillier A. G., Gubbay J. B. Zoonotic Influenza and Human Health-Part 2: Clinical Features, Diagnosis, Treatment, and Prevention Strategies. Curr Infect Dis Rep. 2018;20(10):38. DOI: https://doi.org/10.1007/s11908-018-0643-8

12. Germeraad E. A., Sanders P., Hagenaars T. J., De Jong M. C. M., Beerens N., Gonzales J. L. Virus shedding of avian influenza in poultry: A systematic review and meta-analysis. Viruses. 2019;11(9):812. DOI: https://doi.org/10.3390/v11090812

13. Page M. J., McKenzie J. E., Bossuyt P. M., Boutron I., Hoffmann T. C., Mulrow C. D. et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ. 2021;372:n71. DOI: https://doi.org/10.1136/bmj.n71

14. Burt J. E., Barber G. Elementary Statistics for Geographers, Second Edition. Guilford Publications, 1996. 640 p.

15. Marchenko V. Yu., Susloparov I. M., Ignat’ev V. E., Gavrilova E. V., Maksyutov R. A., Ryzhikov A. B. Overview of the Situation on Highly Pathogenic Avian Influenza Virus H5 in Russia in 2016-2017. Problemy osobo opasnykh infektsiy = Problems of Particularly Dangerous Infections. 2018;(1):30-35. (In Russ.). DOI: https://doi.org/10.21055/0370-1069-2018-1-30-35

16. Marchenko V. Yu., Goncharova N. I., Tran T. N., Trinh K. S., Nguyen N. Q., Gavrilova E. V., Maksyutov R. A., Ryzhikov A. B. Overview of the Epizootiological Situation on Highly Pathogenic Avian Influenza Virus in Russia in 2019. Problemy osobo opasnykh infektsiy = Problems of Particularly Dangerous Infections. 2020;(2):31-37. (In Russ.). DOI: https://doi.org/10.21055/0370-1069-2020-2-31-37

17. Marchenko V. Yu., Goncharova N. I., Gavrilova E. V., Maksyutov R. A., Ryzhikov A. B. Overview of the Epizootiological Situation on Highly Pathogenic Avian Influenza in Russia in 2020. Problemy osobo opasnykh infektsiy = Problems of Particularly Dangerous Infections. 2021;(2):33-40. (In Russ.). DOI: https://doi.org/10.21055/0370-1069-2021-2-33-40

18. Lu L., Lycett S. J., Leigh Brown A. J. Reassortment patterns of avian influenza virus internal segments among different subtypes. BMC Evol Biol. 2014;14(1):1-16. DOI: https://doi.org/10.1186/1471-2148-14-16

19. Khan S. U., Gurley E. S., Gerloff N., Rahman M. Z., Simpson N., Rahman M., et al. Avian influenza surveillance in domestic waterfowl and environment of live bird markets in Bangladesh, 2007-2012. Sci Rep. 2018;8(1):9396. DOI: https://doi.org/10.1038/s41598-018-27515-w

20. Shin J., Kang S., Byeon H., Cho S. M., Kim S. Y., Chung Y. J., et al. Highly pathogenic H5N6 avian influenza virus subtype clade 2.3.4.4 indigenous in South Korea. Sci Rep. 2020;10(1):7241. DOI: https://doi.org/10.1038/s41598-020-64125-x

21. Araujo J., Petry M. V., Fabrizio T., Walker D., Ometto T., Thomazelli L.M., et al. Migratory birds in southern Brazil are a source of multiple avian influenza virus subtypes. Influenza Other Respi Viruses. 2018;12(2):220-231. DOI: https://doi.org/10.1111/irv.12519

22. Frolov A. V., Pankratov S. V., Rozhdestvenskaya T. N., Norkina S. N., Shestopalov A. M. Avian influenza. Specific prevention. Veterinariya i kormlenie. 2020;(7):64-66. (In Russ.). DOI: https://doi.org/10.30917/ATT-VK-1814-9588-2020-7-17

23. Irza V. N., Dzhavadov E. D., Petrova O. G. Avian flu. BIO. 2021;(2(245)):22-27. (In Russ.). URL: https://elibrary.ru/item.asp?id=46283984

24. Liu Lin-lin, Fang B., Yu X., Li X., Lei Ya-ke, Chen D. Strengthened Monitoring of H5 Avian Influenza Viruses in External Environment in Hubei, 2018. Curr Med Sci. 2020;40(1):63-68. DOI: https://doi.org/10.1007/s11596-020-2147-7

25. Verhagen J. H., Lexmond P., Vuong O., Schutten M., Guldemeester J., Osterhaus A. D. M. E., et. al. Discordant detection of avian influenza virus subtypes in time and space between poultry and wild birds; Towards improvement of surveillance programs. PLoS One. 2017;12(3):e0173470. DOI: https://doi.org/10.1371/journal.pone.0173470

26. Tarigan S., Wibowo M. H., Indriani R., Sumarningsih S., Artanto S., Idris S., et al. Field effectiveness of highly pathogenic avian influenza H5N1 vaccination in commercial layers in Indonesia. PLoS One. 2018;13(1):e0190947. DOI: https://doi.org/10.1371/journal.pone.0190947

27. Swayne D. E., Kapczynski D. R. Vaccines, vaccination and immunology for avian influenza viruses in poultry. In Avian influenza (D. E. Swayne, ed.). Blackwell, Ames, Iowa. 2008. Ch. 19. pp. 407-451. DOI: https://doi.org/10.1002/9780813818634.ch19

28. Marangon S., Capua I. Control of avian influenza in Italy: From stamping out to emergency and prophylactic vaccination. Dev Biol (Basel). 2006;124:109-115.

29. Hautefeuille C., Azzouguen B., Mouchel S., Dauphin G., Peyre M. Evaluation of vaccination strategies to control an avian influenza outbreak in French poultry production networks using EVACS tool. Prev Vet Med. 2020;184:105129. DOI: https://doi.org/10.1016/j.prevetmed.2020.105129

30. Swayne D. E., Pavade G., Hamilton K., Vailat B., Miyagishima K. Assessment of national strategies for control of high-pathogenicity avian influenza and low-pathogenicity notifiable avian influenza in poultry, with emphasis on vaccines and vaccination. OIE Rev Sci Tech. 2011;30(3):839-870. DOI: http://dx.doi.org/10.20506/rst.30.3.2081

31. Marangon S., Busani L., Capua I. Practicalities of the implementation of a vaccination campaign for avian influenza. Avian Dis. 2007;51(s1):297-303. DOI: https://doi.org/10.1637/7539-033006R.1

32. Sirawan A., Berry A., Badra R., El Bazzal B., Dabaja M., Kataya H., et al. Avian influenza surveillance at the human–animal interface in lebanon, 2017. East Mediterr Heal J. 2020;26(7):774-778. DOI: https://doi.org/10.26719/emhj.20.004

33. He F., Leyrer S., Kwang J. Strategies towards universal pandemic influenza vaccines. Expert Rev Vaccines. 2016;15(2):215-25. DOI: https://doi.org/10.1586/14760584.2016.1115352

34. Villanueva-Cabezas J. P., Coppo M. J. C., Durr P. A., McVernon J. Vaccine efficacy against Indonesian Highly Pathogenic Avian Influenza H5N1: systematic review and meta-analysis. Vaccine. 2017;35(37):4859-4869. DOI: https://doi.org/10.1016/j.vaccine.2017.07.059

35. Bruschke C., Brückner G., Vallat B. International standards and guidelines for vaccination of poultry against highly pathogenic avian influenza. Dev Biol (Basel). 2007;130:23-30.

36. Putri K., Wibowo M. H., Tarigan S., Wawegama N., Ignjatovic J, Noormohammadi A. H. Analysis of antibody response to an epitope in the haemagglutinin subunit 2 of avian influenza virus H5N1 for differentiation of infected and vaccinated chickens. Avian Pathol. 2020;49(2):161-170. DOI: https://doi.org/10.1080/03079457.2019.1694635

37. Wan Z., Cardenas G. S., Liu J., Santos J., Carnaccini S., Geiger G., et al. Alternative Strategy for a Quadrivalent Live Attenuated Influenza Virus Vaccine. J. Virol. 2018;92(21):e01025-18. DOI: https://doi.org/10.1128/JVI.01025-18

38. Tate M. D. Highly pathogenic avian H5N8 influenza viruses: should we be concerned? Virulence. 2018;9(1):20-21. DOI: https://doi.org/10.1080/21505594.2017.1386832

39. Horman W. S. J., Nguyen T. H. O., Kedzierska K., Bean A. G. D., Layton D. S. The drivers of pathology in zoonotic avian influenza: The interplay between host and pathogen. Front Immunol. 2018;9:1812. DOI: https://doi.org/10.3389/fimmu.2018.01812

40. Hasan N. H., Ignjatovic J., Peaston A., Hemmatzadeh F. Avian Influenza Virus and DIVA Strategies. Viral Immunol. 2016;29(4):198-211. DOI: https://doi.org/10.1089/vim.2015.0127

41. Capua I., Cattoli G., Marangon S. DIVA − A vaccination strategy enabling the detection of field exposure to avian influenza. Dev Biol (Basel). 2004;119:229-233.

42. Cabral L. A. DIVA strategy for avian influenza. Aust Vet J. 2015;93(1-2):N2-N24. DOI: https://doi.org/10.1111/avj.143

43. Suarez D. L. DIVA vaccination strategies for avian influenza virus. Avian Dis. 2012;56(4sl):836-844. DOI: https://doi.org/10.1637/10207-041512-Review.1

44. Borisov A. V., Borisov V. V., Irza V. N., Rakhmanov A. M. Scientific and legal groundwork for measures aimed at control of highly pathogenic avian influenza. Trudy Federal'nogo tsentra okhrany zdorov'ya zhivotnykh. 2007;5:83-93 (In Russ.). URL: https://www.elibrary.ru/item.asp?id=14454048

45. Tikhonova Z. V. Problems and the prospect for the preventive maintenance of epizootic disease of the influenza of birds (literary survey). Veterinarnaya praktika. 2007;2(37):10-16. (In Russ.). URL: https://www.elibrary.ru/item.asp?id=12501993

46. Allison A. B., Ballard J. R., Tesh R. B., Brown J. D., Ruder M. G., Keel M. K., et al. Cyclic Avian Mass Mortality in the Northeastern United States Is Associated with a Novel Orthomyxovirus. J Virol. 2015;89(2):1389. DOI: https://doi.org/10.1128/JVI.02019-14

47. Chen H. H5N1 avian influenza in China. Sci China, Ser C Life Sci. 2009;52(5):419-427. DOI: https://doi.org/10.1007/s11427-009-0068-6

48. Huynh H. T. T., Truong L. T., Meeyam T., Le H. T., Punyapornwithaya V. Individual and flock immunity responses of naïve ducks on smallholder farms after vaccination with H5N1 Avian Influenza vaccine: a study in a province of the Mekong Delta, Vietnam. PeerJ. 2019;7(1):e6268. DOI: https://doi.org/10.7717/peerj.6268

49. Sun Z., Wang J., Huang Z. Assessment of China’s H5N1 routine vaccination strategy. Sci Rep. 2017;7:46441 DOI: https://doi.org/10.1038/srep46441

50. Sayedahmed E. E., Elkashif A., Alhashimi M., Sambhara S., Mittal S. K. Adenoviral vector-based vaccine platforms for developing the next generation of influenza vaccines. Vaccines. 2020;8(4):574. DOI: https://doi.org/10.3390/vaccines8040574

51. Forster P. Ten years on: Generating innovative responses to avian influenza. Ecohealth. 2014;11(1):15-21. DOI: https://doi.org/10.1007/s10393-013-0887-6

52. Pramuwidyatama M. G., Hogeveen H., Saatkamp H. W. A systematic evaluation of measures against highly pathogenic avian influenza (HPAI) in Indonesia. Front Vet Sci. 2019;(6):33. DOI: https://doi.org/10.3389/fvets.2019.00033

53. Dalla Pozza M., Ceolin C., Marangon S. Emergency Response Following Suspicion of an Avian Influenza Outbreak. Zoonoses Public Health. 2008;55(1):50-53. DOI: https://doi.org/10.1111/j.1863-2378.2007.01083.x

54. Volkov M. High and low pathogenic avian flu. Zhivotnovodstvo Rossii. 2021;(6):17-22. (In Russ.). DOI: https://doi.org/10.25701/ZZR.2021.97.56.003

55. Zhou S., Tian H., Wu X., Xu B., Yang J., Chan K. K. Y., et al. Genetic evidence for avian influenza H5N1 viral transmission along the black sea-mediterranean flyway. J Gen Virol. 2016;97(9):2129-2134. DOI: https://doi.org/10.1099/jgv.0.000534

56. Kostina L. V., Zaberezhnyy A. D., Grebennikova T. V., Antipova N. V., Aliper T. I., Nepoklonov E. A. Vaccines against avian influenza in poultry. Voprosy virusologii = Problems of Virology. 2017;62(2):53-60. (In Russ.). DOI: https://doi.org/10.18821/0507-4088-2017-62-2-53-60