African swine fever in the Primorsky Krai: disease situation and molecular and biological properties of the isolate recovered from a wild boar long bone

It is necessary to continue the analysis of the situation and molecular and biological properties of the current African swine fever virus isolates, recovered in the Russian border territories to cover the following tasks: eradication of African swine fever; development of effective disease surveillance and control programs; search for promising genome markers for the vaccine development; implementation of the differentiation strategy between vaccinated and non-vaccinated animals; and clustering of the isolates. The post-hoc analysis of some ASF epidemiological data and comparative genetic analysis of isolates circulating in the Far East Federal District suggested the agent introduction and spread routes, as well as the seasonality of the infection occurrence in the Primorsky Krai. It was established, that two ASFV subgenotypes (IGR-I и IGR-II), differentiated by intergenic region I73R/I329L, circulated in the region under study during the first months post infection. Analysis of biological properties of ASFV/Primorsky 19/WB-6723 isolate recovered from the long bone of a dead wild boar in the Primorsky Krai suggested that the isolate is highly virulent, able to cause peracute to subacute disease and up to 100% mortality among infected animals. The incubation period and duration of the disease course in experimentally infected pigs were 4–6 and 3–5 days post infection, respectively. The ASFV genome was detected in blood samples collected from infected pigs on 5–8 days post infection by real-time polymerase chain reaction. Specific antibodies in blood samples were not detected. The need in further research of molecular and biological properties of current ASFV isolates was reaffirmed. To prevent the continuation of the epizooty and deterioration of the current situation the approaches to the disease surveillance and control need to be modified.

1. Gruzdev K. N., Igolkin A. S., Rakhmanov A. M., Shevtsov A. A. African swine fever in Russia: spread, clinical and anatomical manifestations. Veterinary Science Today. 2014; (4): 10–24. eLIBRARY ID: 22445544.

2. Beltran-Alcrudo D., Arias M., Gallardo C., Kramer S., Penrith M. L. African swine fever: Detection and diagnosis – A manual for veterinarians. FAO Animal Production and Health Manual No. 19. Rome: FAO; 2017. 88 p. Available at: https://www.fao.org/3/i7228e/i7228e.pdf.

3. Mazloum A., Igolkin A. S., Vlasova N. N., Romenskaya D. V. African swine fever virus: use of genetic markers in analysis of its routes of spread. Veterinary Science Today. 2019; (3): 3–14. DOI: 10.29326/2304-196X-2019-3-30-3-8.

4. European Food Safety Authority (EFSA), Desmecht D., Gerbier G., Gortázar Schmidt C., Grigaliuniene V., Helyes G., et al. Epidemiological analysis of African swine fever in the European Union (September 2019 to August 2020). EFSA J. 2021; 19 (5):e06572. DOI: 10.2903/j.efsa.2021.6572.

5. Sun E, Huang L., Zhang X., Zhang J., Shen D., Zhang Z., et al. Genotype I African swine fever viruses emerged in domestic pigs in China and caused chronic infection. Emerg. Microbes. Infect. 2021; 10 (1): 2183–2193. DOI: 10.1080/22221751.2021.1999779.

6. WOAH. Animal disease events. Available at: https://wahis.woah.org/#/report-management (date of access: 06.02.2022).

7. Terebova S. V., Koltun G. G., Podvalova V. V., Korotkova I. P. Risk analysis of the spread of african swine fever in Primorsky krai. Agrarnyi vestnik Primor’ya. 2020; 1 (17): 13–18. eLIBRARY ID: 42918095. (in Russ.)

8. Terebova S. V., Koltun G. G., Podvalova V. V., Korotkova I. P. Epizootii afrikanskoi chumy svinei v Primorskom krae. Problemy zootekhnii, veterinarii i biologii zhivotnykh na Dal’nem Vostoke = Problems of animal management, veterinary medicine and animal biology in the Far East: Proceedings. Responsible editor V. A. Gogulov. Blagoveshchensk: Far Eastern State Agrarian University; 2020; 27: 82–86. eLIBRARY ID: 43984373. (in Russ.)

9. Momot N. V., Kolina Yu. A., Kamliya I. L. New outbreaks of African swine fever in the wild. Bulletin of Altai State Agricultural University. 2020; 11 (193): 99–102. eLIBRARY ID: 44277338. (in Russ.)

10. Momot N. V., Kolina Yu. A., Kamliya I. L. Prevention and control of African swine fever. Scientific notes Kazan Bauman State Academy of Veterinary Medicine. 2021; 245 (1): 112–116. DOI: 10.31588/2413-4201-1883-245-1-112-116. (in Russ.)

11. Zakharova O. I., Titov I. A., Gogin A. E., Sevskikh T. A., Korennoy F. I., Kolbasov D. V., et al. African swine fever in the Russian Far East (2019–2020): Spatio-temporal analysis and implications for wild ungulates. Front. Vet. Sci. 2021; 8:723081. DOI: 10.3389/fvets.2021.723081.

12. Remyga S. G., Pershin A. S., Shevchenko I. V., Igolkin A. S., Shevtsov A. A. Clinical and post-mortem signs in European wild boars and domestic pigs infected with African swine fever virus. Veterinary Science Today. 2016; (3): 46–51. eLIBRARY ID: 27175029. (in Russ.)

13. Vlasov M. E., Sibgatullova A. K., Balyshev V. M. The course of disease in pigs infected with ASF virus isolates, obtained in different regions of the Russian Federation. Veterinariya. 2019; 4: 15–19. DOI: 10.30896/0042-4846.2019.22.4.15-19. (in Russ.)

14. Bolgova M. V., Morgounov Yu. P., Vasilyev A. P., Baluishev V. M. Biological characteristics of african swine fever virus isolates detected in the Russion Federation in 2012. Actual Questions of Veterinary Biology. 2013; 4 (20): 26–30. eLIBRARY ID: 20911850. (in Russ.)

15. Balyshev V., Vlasov M., Imatdinov A., Titov I., Morgunov S., Malogolovkin A. Biological properties and molecular genetic characteristics of the African swine fever virus, isolated in 2016–2017 in various regions of the Russian Federation. Rossiiskaia selskokhoziaistvennaia nauka. 2018; (4): 54–57. DOI: 10.31857/S250026270000536-4. (in Russ.)

16. Chernykh O. Yu., Krivonos R. A., Verhovsky O. A., Aliper T. I., Pershin A. S., Zhukov I. Yu., et al. Molecular and biological properties of the isolate Timashevsk 01/18. Veterinarian. 2019; 2: 15–22. DOI: 10.33632/1998-698X.2019-2-15-22. (in Russ.)

17. Pershin A., Shevchenko I., Igolkin A., Zhukov I., Mazloum A., Aronova E., et al. A long-term study of the biological properties of ASF virus isolates originating from various regions of the Russian Federation in 2013–2018. Vet. Sci. 2019; 6 (4):99. DOI: 10.3390/vetsci6040099.

18. Shevchenko I. V. Biological properties and whole genome sequencing of Russian ASFV isolates, recovered in 2013–2014: Author’s Abstract of Candidate of Biological Sciences’ Thesis. Vladimir; 2017. 23 p. Available at: https://viewer.rsl.ru/ru/rsl01006663342?page=1&rotate=0&theme=white. (in Russ.)

19. Zhukov I. Yu. Biological properties of African swine fever virus isolates and peculiarities of the disease course after experimental infection: Author’s Abstract of Candidate of Biological Sciences’ Thesis. Vladimir; 2018. 23 p. Available at: https://viewer.rsl.ru/ru/rsl01008706424?page=1&rotate=0&theme=white. (in Russ.)

20. Sibgatullova A. K., Vlasov M. E., Lunina D. A. Spatial-temporal characteristics of the results of genotyping of the I73R/I329L adjacent region of ASF virus isolates circulating in the territory of the Russian Federation. Veterinariya. 2021; 1: 29–32. DOI: 10.30896/0042-4846.2021.24.1.29-32. (in Russ.)

21. Vlasov M. E. Biological properties of African swine fever virus isolates recovered in different regions of the Russian Federation from wild boar and domestic pigs: Candidate of Veterinary Sciences’ Thesis. Volginsky; 2021. 149 p. (in Russ.)

22. Shevchenko I. V., Zhukov I. Yu., Pershin A. S., Remyga S. G., Shevtsov A. A., Igolkin A. S. Guidelines for bioassay procedure involving infection of pigs with African swine fever virus: approved by FGBI “ARRIAH” 28.12.2017 No. 77-17. Vladimir; 2017. 11 p. (in Russ.)

23. Guidelines for the assessment of clinical signs and post-mortem lesions after experimental infection with African swine fever virus: approved by Rosselkhoznadzor in 2017. MU 40-15. Vladimir: FGBI “ARRIAH”; 2017. 21 p. (in Russ.)

24. Pershin A. S., Komova Т. N., Shotin A. R., Zhukov I. Yu., Vlasova N. N., Shevchenko I. V., Igolkin A. S. Guidelines for detection of African swine fever virus antibodies with immunoperoxidase assay: approved by FGBI “ARRIAH” 26.12.2019 No. 106-19. Vladimir; 2020. 12 p. (in Russ.)

25. Mazloum A., van Schalkwyk A., Shotin A., Igolkin A., Shevchenko I., Gruzdev K. N., Vlasova N. Comparative analysis of full genome sequences of African swine fever virus isolates taken from wild boars in Russia in 2019. Pathogens. 2021; 10 (5):521. DOI: 10.3390/pathogens10050521.

26. Yang J., Tang K., Cao Z., Pfeiffer D. U., Zhao K., Zhang Q., Zeng D. D. Demand-driven spreading patterns of African swine fever in China. Chaos. 2021; 31 (6):061102. DOI: 10.1063/5.0053601.

27. Gao L., Sun X., Yang H., Xu Q., Li J., Kang J., et al. Epidemic situation and control measures of African swine fever outbreaks in China 2018–2020. Transbound. Emerg. Dis. 2021; 68 (5): 2676–2686. DOI: 10.1111/tbed.13968.

28. Dixon L. K., Sun H., Roberts H. African swine fever. Antiviral Res. 2019; 165: 34–41. DOI: 10.1016/j.antiviral.2019.02.018.

29. You S., Liu T., Zhang M., Zhao X., Dong Y., Wu B., et al. African swine fever outbreaks in China led to gross domestic product and economic losses. Nat. Food. 2021; 2: 802–808. DOI: 10.1038/s43016-021-00362-1.

30. Rosselkhoznadzor. Zaregistrirovana vspyshka afrikanskoi chumy svinei v Primorskom krae = African swine fever outbreak reported in the Primorsky Krai. Available at: https://fsvps.gov.ru/fsvps/news/31380.html (date of access: 22.02.2022). (in Russ.)

31. Gallardo C., Sastre P., Rueda P., Gerilovych A. P., Kit M., Nurmoja I., Le Potier M. F. Methods for African swine fever diagnosis in clinical and en-vironmental samples. Chapter 5. In: Understanding and combatting African swine fever. A European perspective. Eds.: L. Iacolina, M.-L. Penrith, S. Bellini, E. Chenais, F. Jori, M. Montoya, et al. 2021; 141–160. DOI: 10.3920/978-90-8686-910-7_5.

32. EFSA (European Food Safety Authority), Cortiñas Abrahantes J., Gogin A., Richardson J., Gervelmeyer A. Epidemiological analyses on African swine fever in the Baltic countries and Poland. EFSA Journal. 2017; 15 (3):4732. DOI: 10.2903/j.efsa.2017.4732.

33. Petrova О. N., Korennoy F. I., Tatsenko Е. Е., Karaulov A. K., Gulenkin V. М. Prognoz po afrikanskoi chume svinei v Rossiiskoi Federatsii na 2018 god = African swine fever forecast in the Russian Federation for 2018. In: Infectious animal disease forecasting for 2018. Vladimir: FGBI “ARRIAH”; 2018; 56–92. (in Russ.)

34. Oganesyan A. S., Shibayev М. A., Baskakova N. Ye., Korennoy F. I., Karaulov A. К. African swine fever epidemic in 2007–2017. Part 1. Common trends for ASF in the Russian Federation and in Eurasia. Veterinary Science Today. 2018; (2): 18–25. DOI: 10.29326/2304-196X-2018-2-25-18-25.

35. Gervasi V., Marcon A., Bellini S., Guberti V. Evaluation of the efficiency of active and passive surveillance in the detection of African swine fever in wild boar. Vet. Sci. 2019; 7 (1):5. DOI: 10.3390/vetsci7010005.

36. Gallardo C., Fernández-Pinero J., Arias M. African swine fever (ASF) diagnosis, an essential tool in the epidemiological investigation. Virus Res. 2019; 271:197676. DOI: 10.1016/j.virusres.2019.197676.

37. Mur L., Igolkin A., Varentsova A., Pershin A., Remyga S., Shevchenko I., Zhukov I., Sánchez-Vizcaíno J. M. Detection of African Swine Fever Antibodies in Experimental and Field Samples from the Russian Federation: Implications for Control. Transbound. Emerg. Dis. 2016; 63 (5):e436-40. DOI: 10.1111/tbed.12304.

38. Gallardo C., Soler A., Rodze I., Nieto R., Cano-Gómez C., Fernandez- Pinero J., Arias M. Attenuated and non-haemadsorbing (non-HAD) genotype II African swine fever virus (ASFV) isolated in Europe, Latvia 2017. Transbound. Emerg. Dis. 2019; 66 (3): 1399–1404. DOI: 10.1111/tbed.13132.

39. Sun E., Zhang Z., Wang Z., He X., Zhang X., Wang L., et al. Emergence and prevalence of naturally occurring lower virulent African swine fever viruses in domestic pigs in China in 2020. Sci. China. Life Sci. 2021; 64 (5): 752–765. DOI: 10.1007/s11427-021-1904-4.

40. Nurmoja I., Petrov A., Breidenstein C., Zani L., Forth J. H., Beer M., et al. Biological characterization of African swine fever virus genotype II strains from north-eastern Estonia in European wild boar. Transbound. Emerg. Dis. 2017; 64 (6): 2034–2041. DOI: 10.1111/tbed.12614.

41. Fedoseyeva D. N., Aronova Ye. V., Varentsova A. A., Yelsukova A. A., Mazloum A., Sharypova D. V., et al. Analysis of monitoring studies on African swine fever virus DNA detection carried out in 2017. Veterinary Science Today. 2018; (3): 21–25. DOI: 10.29326/2304-196X-2018-3-26-21-25.