Identification of seropositive wild boars in Eurasia as a sign of possible formation of African swine fever-endemic areas (review)

   The continued spread of African swine fever (ASF) in Eurasia remains a global problem for the world pig industry. The disease is characterized by high mortality (up to 100 %) and acute course - domestic and wild animals die within the first two weeks after infection. However, active surveillance on ASF in Eastern Europe had been showing regular detection of seropositive susceptible animals, especially among wild boar populations which may indicate chronic, asymptomatic infection and even the survival of individual animals. At the same time, the persistence of the virus in the wild boar population creates constant risks of sporadic outbreaks of ASF in infected areas, and the infection can become endemic.

   The aim of the study was a systematic review of the available data on seroprevalence among wild boars in relation to the possible establishment of ASF endemicity in Eurasia.

   In these animals, there was a change in the dynamics of the disease, which is manifested by self-sustaining cycles of infection. Seropositive wild boars are being found in the Baltic countries, Hungary, Poland, Romania, Slovakia, and Russia. Seroprevalence rates among wild boars hunted in ASF-infected areas of European countries range from 0.3 to 3.8 %. In the Baltic countries, the number of seropositive samples from wild boars exceeds the number of samples positive for ASF virus in polymer chain reaction (PCR). A similar trend persists in those regions where the ASF virus has been present for a long time (Poland, Lithuania, Latvia, Estonia), which may indicate the endemic nature of ASF. In the Russian Federation, ASF-endemic territories in the wild have not yet been registered, although isolated cases of seropositive wild boars have been detected in some regions since 2013. In the future, in order to understand the dynamics of the disease in the wild, it is necessary to conduct a comprehensive diagnosis of the ASF virus genome and antibodies in wild boar samples, which eventually will allow choosing the right strategy to combat ASF.

1. Blome S., Franzke K., Beer M. African swine fever-A review of current knowledge. Virus Research. 2020;287:198099. https://doi.org/10.1016/j.virusres.2020.198099

2. EFSA Panel on Animal Health and Welfare, Nielsen S. S., Alvarez J., Bicout D. J., Calistri P., Canali E., Drewe J. A., Garin-Bastuji B., Gonzales Rojas J. L., Schmidt C., Herskin M., Michel V., Padalino B., Pasquali P., Roberts H. C., Spoolder H., Stahl K., Velarde A., Winckler C., Blome S., Boklund A., Bøtner A., Dhollander S., Rapagna C., Van der Stede Y., Miranda Chueca M. A. Scientific Opinion on the research priorities to fill knowledge gaps in wild boar management measures that could improve the control of African swine fever in wild boar populations. EFSA Journal. 2021;19(7):e06716. https://doi.org/10.2903/j.efsa.2021.6716

3. Ge S., Li J., Fan X., Liu F., Li L., Wang Q., Ren W., Bao J., Liu C., Wang H., Liu Y., Zhang Y., Xu T., Wu X., Wang Z. Molecular Characterization of African Swine Fever Virus, China. Emerging Infectious Diseases. 2018;24(11):2131-2133. https://doi.org/10.3201/eid2411.181274

4. Ayanwale A., Trapp S., Guabiraba R., Caballero I., Roesch F. New Insights in the Interplay Between African Swine Fever Virus and Innate Immunity and Its Impact on Viral Pathogeniciy. Frontiers Microbiology. 2022;13:958307. https://doi.org/10.3389/fmicb.2022.958307

5. Conan A., Kim Y., Yang D. A., Win T. T. Z., Nekouei O., Pfeiffer D. U. African Swine Fever Cross-border Risk Assessment Manual: South-East Asia. World Organisation for Animal Health (OIE) Sub-Regional Representation for South-East Asia. Bangkok, Thailand, 2022. 36 p. URL: https://rr-asia.woah.org/wp-content/uploads/2022/04/asf-risk-assessment-manual-update_31mar22.pdf

6. Loi F., Di Sabatino D., Baldi I., Rolesu S., Gervasi V., Guberti V., Cappai S. Estimation of R0 for the Spread of the First ASF Epidemic in Italy from Fresh Carcasses. Viruses. 2022;14(10):2240. https://doi.org/10.3390/v14102240

7. Cadenas-Fernández E., Sánchez-Vizcaíno J. M., Pintore A., Denurra D., Cherchi M., Jurado C., Vicente J., Barasona J. A. Free-Ranging Pig and Wild Boar Interactions in an Endemic Area of African Swine Fever. Frontiers in Veterinary Science. 2019;6:376. https://doi.org/10.3389/fvets.2019.00376

8. Pikalo J., Schoder M. E., Sehl J., Breithaupt A., Tignon M., Cay A. B., Gager A. M., Fischer M., Beer M., Blome S. The African swine fever virus isolate Belgium 2018/1 shows high virulence in European wild boar. Transboundary and emerging diseases. 2020;67(4):1654-1659. https://doi.org/10.1111/tbed.13503

9. Nurmoja I., Petrov A., Breidenstein C., Zani L., Forth J. H., Beer M., Kristian M., Viltrop A., Blome S. Biological characterization of African swine fever virus genotype II strains from north-eastern Estonia in European wild boar. Transboundary and Emerging Diseases. 2017;64(6):2034-2041. https://doi.org/10.1111/tbed.12614

10. 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. Transboundary and Emerging Diseases. 2019;66(3):1399-1404. https://doi.org/10.1111/tbed.13132

11. Gallardo C., Nurmoja I., Soler A., Delicado V., Simón A., Martin E., Perez C., Nieto R., Arias M. Evolution in Europe of African swine fever genotype II viruses from highly to moderately virulent. Veterinary microbiology. 2018;219:70-79. https://doi.org/10.1016/j.vetmic.2018.04.001

12. 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. Transboundary and Emerging Diseases. 2016;63(5):e436-e440. https://doi.org/10.1111/tbed.12304

13. Sun E., Huang L., Zhang X., Zhang J., Shen D., Zhang Z., Wang Z., Huo H., Wang W., Huangfu H., Wang W., Li F., Liu R., Sun J., Tian Z., Xia W., Guan Y., He X., Zhu Y., Zhao D., Bu Z. Genotype I African swine fever viruses emerged in domestic pigs in China and caused chronic infection. Emerging microbes & infections. 2021;10(1):2183-2193. https://doi.org/10.1080/22221751.2021.1999779

14. Pershin A., Shevchenko I., Igolkin A., Zhukov I., Mazloum A., Aronova E., Vlasova N., Shevtsov A. A long-term study of the biological properties of ASF virus isolates originating from various regions of the Russian Federation in 2013-2018. Veterinary Sciences. 2019;6(4):99. https://doi.org/10.3390/vetsci6040099

15. Beltrán-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: Food and Agriculture Organization of the United Nations (FAO). 2017. 104 p. URL: https://www.fao.org/3/i7228e/i7228e.pdf

16. European Food Safety Authority, Boklund A., Bøtner A., Chesnoiu V. T., Depner K., Desmecht D., Guberti V., Helyes G., Korytarova D., Linden A., Miteva A., More S., Olsevskis E., Ostojic S., Roberts H., Spiridon M., Ståhl K., Thulke H.-H., Vilija G., Viltrop A., Wallo R., Wozniakowski G., Abrahantes C. J., Dhollander S., Gogin A., Ivanciu C., Papanikolaou A., Villeta L. C. G., Gortázar Schmidt Ch. Epidemiological analyses of African swine fever in the European Union (November 2018 to October 2019). EFSA Journal. 2020;18(1):e05996. https://doi.org/10.2903/j.efsa.2020.5996

17. Schulz K., Conraths F. J., Blome S., Staubach C., Sauter-Louis C. African Swine Fever: Fast and Furious or Slow and Steady? Viruses. 2019;11(9):866. https://doi.org/10.3390/v11090866

18. Sánchez-Cordón P. J., Nunez A., Neimanis A., Wikström-Lassa E., Montoya M., Crooke H., Gavier-Widén D. African Swine Fever: Disease Dynamics in Wild Boar Experimentally Infected with ASFV Isolates Belonging to Genotype I and II. Viruses. 2019;11(9):852. https://doi.org/10.3390/v11090852

19. OIE Terrestrial Manual 2019. Chapter 3.8.1. African swine fever (infection with African swine fever virus). URL: https://www.oie.int/fileadmin/Home/fr/Health_standards/tahm/3.08.01_ASF.pdf

20. Danzetta M. L., Marenzoni M. L., Iannetti S., Tizzani P., Calistri P., Feliziani F. African Swine Fever: Lessons to Learn From Past Eradication Experiences. A Systematic Review. Frontiers in Veterinary Science. 2020;7:296. https://doi.org/10.3389/fvets.2020.00296

21. Shotin A. R., Mazloum A., Igolkin A. S., Shevchenko I. V., Elsukova A. A., Aronova E. V., Vlasova N. N. Alternative approaches to the diagnosis of African swine fever in the Russian Federation in 2017-2021. Voprosy virusologii = Problems of Virology. 2022;67(4):290-303. (In Russ.). https://doi.org/10.36233/0507-4088-112

22. De la Torre A., Bosch J., Iglesias I., Muoz M. J., Mur L., Martínez-López B., Martínez M., Sánchez-Vizcaíno J. M. Assessing the risk of African swine fever introduction into the European Union by wild boar. Transboundary and Emerging Diseases. 2015;62(3):272-279. https://doi.org/10.1111/tbed.12129

23. Vergne T., Gogin A., Pfeiffer D. U. Statistical exploration of local transmission routes for African swine fever in Pigs in the Russian Federation, 2007-2014. Transboundary and Emerging Diseases. 2017;64(2):504-512. https://doi.org/10.1111/tbed.12391

24. Frant M. P., Gal-Cisoń A., Bocian Ł., Ziętek-Barszcz A., Niemczuk K., Szczotka-Bochniarz A. African Swine Fever (ASF) Trend Analysis in Wild Boar in Poland (2014-2020). Animals (Basel). 2022;12(9):1170. https://doi.org/10.3390/ani12091170

25. Nurmoja I., Mõtus K., Kristian M., Niine T., Schulz K., Depner K., Viltrop A. Epidemiological analysis of the 2015-2017 African swine fever outbreaks in Estonia. Preventive Veterinary Medicine. 2020;181:104556. https://doi.org/10.1016/j.prevetmed.2018.10.001

26. Gogin A., Gerasimov V., Malogolovkin A., Kolbasov D. African swine fever in the North Caucasus region and the Russian Federation in years 2007-2012. Virus Research. 2013;173(1):198-203. https://doi.org/10.1016/j.virusres.2012.12.007

27. Sauter-Louis C., Conraths F. J., Probst C., Blohm U., Schulz K., Sehl J., Fischer M., Forth J. H., Zani L., Depner K., Mettenleiter T. C., Beer M., Blome S. African Swine Fever in Wild Boar in Europe - A Review. Viruses. 2021;13(9):1717. https://doi.org/10.3390/v13091717

28. Chenais E., Ståhl K., Guberti V., Depner K. Identification of Wild Boar-Habitat Epidemiologic Cycle in African Swine Fever Epizootic. Emerging Infectious Diseases. 2018;24(4):809-811. https://doi.org/10.3201/eid2404.172127

29. Gulyukin A. M., Belimenko V. V., Shabeykin A. A., Tsaregradskiy P. Yu., Patrikeev V. V. Epizootic situation on african swine fever in nature conservation areas. Veterinariya = Veterinary. 2022;(11):15. (In Russ.). https://doi.org/10.30896/0042-4846.2022.25.11.15-22

30. Halasa T., Boklund A., Bøtner A., Mortensen S., Kjær L. J. Simulation of transmission and persistence of African swine fever in wild boar in Denmark. Preventive Veterinary Medicine. 2019;167(1):68-79. https://doi.org/10.1016/j.prevetmed.2019.03.028

31. O'Neill X., White A., Ruiz-Fons F., Gortázar C. Modelling the transmission and persistence of African swine fever in wild boar in contrasting European scenarios. Scientific Reports. 2020;10:5895. https://doi.org/10.1038/s41598-020-62736-y

32. Lange M., Reichold A., Thulke H. Modelling advanced knowledge of African swine fever, resulting surveillance patterns at the population level and impact on reliable exit strategy definition. EFSA Journal. 2021;18(3):6429E. https://doi.org/10.2903/sp.efsa.2021.EN-6429

33. Gervasi V., Guberti V. African swine fever endemic persistence in wild boar populations: Key mechanisms explored through modelling. Transboundary and emerging diseases. 2021;68(5):2812-2825. https://doi.org/10.1111/tbed.14194

34. Franzoni G., Graham S. P., Giudici S. D., Bonelli P., Pilo G., Anfossi A. G., Pittau M., Nicolussi P. S., Laddomada A., Oggiano A. Characterization of the interaction of African swine fever virus with monocytes and derived macrophage subsets. Veterinary microbiology. 2017;198:88-98. https://doi.org/10.1016/j.vetmic.2016.12.010

35. Bastos A. D., Penrith M. L., Cruciere C., Edrich J., Hutchings G., Roger F., Couacy-Hymann E., Thomson G. R. Genotyping field strains of African swine fever virus by partial p72 gene characterisation. Archives of virology. 2003;148:693-706. https://doi.org/10.1007/s00705-002-0946-8

36. Gallardo C., Mwaengo D. M., Macharia J. M., Arias M., Taracha E. A., Soler A., Okoth E., Martín E., Kasiti J., Bishop R. P. Enhanced discrimination of African swine fever virus isolates through nucleotide sequencing of the p54, p72, and pB602L (CVR) genes. Virus genes. 2009;38:85-95. https://doi.org/10.1007/s11262-008-0293-2

37. Sereda A. D., Kazakova A. S., Imatdinov A. R., Kolbasov D. V. Humoral and cell immune mechanisms under African swine fever. Sel'skokhozyaystvennaya biologiya = Agricultural Biology. 2015;50(6):709-718. (In Russ.). https://doi.org/10.15389/agrobiology.2015.6.709eng

38. Petrov A., Forth J., Zani L., Beer M., Blome S. No evidence for long‐term carrier status of pigs after African swine fever virus infection. Transboundary and emerging diseases. 2018;65(5):1318-1328. https://doi.org/10.1111/tbed.12881

39. Walczak M., Wasiak M., Dudek K., Kycko A., Szacawa E., Olech M., Woźniakowski G., Szczotka-Bochniarz A. Blood Counts, Biochemical Parameters, Inflammatory, and Immune Responses in Pigs Infected Experimentally with the African Swine Fever Virus Isolate Pol18_28298_O111. Viruses. 2021;13(3):521. https://doi.org/10.3390/v13030521

40. Lai D. C., Oh T., Nguyen H. T., Do D. T. The study of antigen carrying and lesions observed in pigs that survived post African swine fever virus infection. Tropical Animal Health and Production. 2022;54:264. https://doi.org/10.1007/s11250-022-03229-0

41. European Food Safety Authority (EFSA), Desmecht D., Gerbier G., Gortázar Schmidt Ch., Grigaliuniene V., Helyes G., Kantere M., Korytarova D., Linden A., Miteva A., Neghirla I., Olsevskis E., Ostojic S., Petit T., Staubach Ch., Thulke H.-H., Viltrop A., Richard W., Wozniakowski G., Cortiñas J. A., Broglia A., Dhollander S., Lima E., Papaniko-laou A., Van der Stede Y., Ståhl K. Scientific Opinion on the epidemiological analysis of African swine fever in the European Union (September 2019 to August 2020). EFSA Journal. 2021;19(5):e06572. https://doi.org/10.2903/j.efsa.2021.6572

42. EFSA Panel on Animal Health and Welfare. African swine fever. EFSA Journal. 2015;13(7):4163. https://doi.org/10.2903/j.efsa.2015.4163

43. European Food Safety Authority, Cortinas 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. https://doi.org/10.2903/j.efsa.2017.4732

44. European Food Safety Authority, Boklund A., Cay B., Depner K., Foldi Z., Guberti V., Masiulis M., Miteva A., More S., Olsevskis E., Satran P., Spiridon M., Stahl K., Thulke H.-H., Viltrop A., Wozniakowski G., Broglia A., Cortinas Abrahantes J., Dhollander S., Gogin A., Verdonck F., Amato L., Papanikolaou A., Gortazar C. Scientific report on the epidemiological analyses of African swine fever in the European Union (November 2017 until November 2018). EFSA Journal. 2018;16(11):e05494. https://doi.org/10.2903/j.efsa.2018.5494

45. European Food Safety Authority, Banos J. V., Boklund A., Gogin A., Gortazar C., Guberti V., Helyes G., Kantere M., Korytarova D., Linden A., Masiulis M., Miteva A., Neghirla I., Olsevskis E., Ostojic S., Petr S., Staubach C., Thulke H.-H., Viltrop A., Wozniakowski G., Broglia A., Abrahantes Cortinas J., Dhollander S., Mur L., Papanikolaou A., Van der Stede Y., Zancanaro G., Stahl K. Scientific report on the epidemiological analyses of African swine fever in the European Union. EFSA Journal 2022;20(5):e07290. https://doi.org/10.2903/j.efsa.2022.7290

46. Gallardo C., Soler A., Nieto R., Sánchez M. A., Martins C., Pelayo V., Carrascosa A., Revilla Y., Simón A., Briones V., Sánchez-Vizcaíno J. M., Arias M. Experimental Transmission of African Swine Fever (ASF) Low Virulent Isolate NH/P68 by Surviving Pigs. Transboundary and Emerging Diseases. 2015;62(6):612-622. https://doi.org/10.1111/tbed.12431