AFRICAN SWINE FEVER VIRUS: USE OF GENETIC MARKERS IN ANALYSIS OF ITS ROUTES OF SPREAD

At present no effective measures for specific prevention and treatment of African swine fever have been developed. The control strategy for the disease is designed for rapid diagnosis of infected animals with subsequent slaughter and decontamination (stamping out). The present review deals with current epidemic situation for African swine fever and examines features of the virus genomics and genetic differentiation of the isolates. The Russian Federation has been ASF-infected since 2007. Since that time the disease has been one of the key problems in pig farming of this country inflicting great economic losses, both directly and indirectly. The disease continues to spread. In January 2014 African swine fever was introduced to Lithuania, then pervaded Poland, Latvia, Estonia, Romania, Belgium and Moldova. Since 2018 the disease outbreaks have been reported in Asia (China, Vietnam, and Mongolia). Specific structure of the virus and long genome, encoding genes with unknown function, and circulation of 24 genotypes and 9 serotypes of the virus hinder the development of ASF vaccine. The article shows that the use of many specific genetic markers during determination of relationship and study of pathways of ASF virus global spread is the most accurate method.

1. Genetic variation among African swine fever genotype II viruses, eastern and central Europe. C. Gallardo, J. FernándezPinero, V. Pelayo [et al.]. Emerg. Infect. Dis. 2014; 20 (9): 1544–1547; DOI: 10.3201/eid2009.140554.

2. Analysis of changes in the genetic structure and biological properties of African swine fever virus in adaptation to continuous cell culture [Analiz izmenenij geneticheskoj struktury i biologicheskih svojstv virusa afrikanskoj chumy svinej pri adaptacii k perevivaemoj kul’ture kletok]. А. Mazloum, N. G. Zinyakov, А. S. Pershin [et al.]. Veterinary Science Today. 2018; 4: 21–25; DOI: 10.29326/2304-196X-2018-4-27-21-25 (in Russian).

3. Genome sequences derived from pig and dried blood pig feed samples provide important insights into the transmission of African swine fever virus in China in 2018. X. Wen, X. He, X. Zhang [et al.]. Emerg. Microbes Infect. 2019; 8 (1): 303–306; DOI: 10.1080/ 22221751.2019.1565915.

4. Analysis of monitoring study results of African swine fever virus DNA in 2017 [Analiz rezul’tatov monitoringovyh issledovanij po vyyavleniyu DNK virusa afrikanskoj chumy svinej, provedennyh v 2017 g.]. D. N. Fedoseyeva, Ye. V. Aronova, А. А. Varentzova [et al.]. Veterinary Science Today. 2018; 3: 21–25; DOI: 10.29326/2304- 196X-2018-3-26-21-25 (in Russian).

5. Genomic analysis of highly virulent Georgia 2007/1 isolate of African swine fever virus. D. A. Chapman, A. C. Darby, M. Da Silva [et al.]. Emerg. Infect. Dis. 2011; 17 (4): 599–605; DOI: 10.3201/ eid1704.101283.

6. Federal Service for Veterinary and Phytosanitary Surveillance (Rosselkhoznadzor) [Federal’naya sluzhba po veterinarnomu i fitosanitarnomu nadzoru (Rossel’hoznadzor)]. 2019. URL: https://www.fsvps.ru/fsvps-docs/ru/iac/asf/2019/08-12/03. pdf (in Russian).

7. Genotyping field strains of African swine fever virus by partial p72 gene characterization. A. D. Bastos, M. L. Penrith, C. Crucière [et al.]. Arch. Virol. 2003; 148 (4): 693–706; DOI: 10.1007/ s00705-002-0946-8.

8. African swine fever virus controls the host transcription and cellular machinery of protein synthesis. E. G. Sanchez, A. Quintas, M. Nogal [et al.]. Virus Res. 2013; 173 (1): 58–75; DOI: 10.1016/j. virusres.2012.10.025.

9. In vivo experimental studies of genotype II African swine fever virus (ASFV) isolates currently circulating in two Estonian counties. C. Gallardo, A. Soler, V. Delicado [et al.]. Proc. 10th Annual Meeting EPIZONE, 27–29 September 2016. Madrid, 2016: 81.

10. African swine fever virus eradication in Africa. M. L. Penrith, W. Vosloo, F. Jori, A. D. Bastos. Virus Res. 2013; 173 (1): 228–246; DOI: 10.1016/j.virusres.2012.10.011.

11. Molecular characterization of African swine fever virus (ASFV) isolates circulating in the Eastern European Union countries 2014–2016. R. Nieto, A. Soler, I. Nurmoja [et al.]. Proc. 10th Annual Meeting EPIZONE, 27–29 September 2016. Madrid, 2016: 164.

12. African swine fever virus include multiple mechanisms for the manipulation of interferon responses. S. Correia, S. Ventura, S. Goodbourn, R. М. E. Parkhouse. Cytokine. 2013; 63 (3): 256; DOI: 10.1016/j.cyto.2013.06.058.

13. Molecular epidemiology of African swine fever in East Africa. B. A. Lubisi, A. D. Bastos, R. M. Dwarka, W. Vosloo. Arch. Virol. 2005; 150 (12): 2439–2452; DOI: 10.1007/s00705-005-0602-1.

14. African swine fever virus isolate, Georgia, 2007. R. J. Rowlands, V. Michaud, L. Heath [et al.]. Emerg. Infect. Dis. 2008; 14 (12): 1870–1874; DOI: 10.3201/eid1412.080591.

15. Molecular epidemiology of African swine fever virus studied by analysis of four variable genome regions. R. J. Nix, C. Gallardo, G. Hutchings [et al.]. Arch. Virol. 2006; 151 (12): 2475–2494; DOI: 10.1007/s00705-006-0794-z.

16. African swine fever virus replication and genomics. L. K. Dixon, D. A. Chapman, C. L. Netherton, C. Upton. Virus Res. 2013; 173 (1): 3–14; DOI: 10.1016/j.virusres.2012.10.020.

17. Phylodynamics and evolutionary epidemiology of African swine fever p72-CVR genes in Eurasia and Africa. M. A. Alkhamis, C. Gallardo, C. Jurado [et al.]. PLoS ONE. 2018; 13 (2):e0192565; DOI: 10.1371/journal.pone.0192565.

18. African swine fever virus. EFSA Panel on Animal Health and Welfare (AHAW). EFSA J. 2015; 13 (7):4163; DOI: 10.2903/j. efsa.2015.4163.

19. Phylogenomic analysis of 11 complete African swine fever virus genome sequences. E. P. de Villiers, C. Gallardo, M. Arias [et al.]. Virology. 2010; 400 (1): 128–136; DOI: 10.1016/j. virol.2010.01.019.

20. An update on the epidemiology and pathology of African swine fever. J. M. Sánchez-Vizcaíno, L. Mur, J. C. Gomez-Villamandos, L. Carrasco. J. Comp. Pathol. 2015; 152 (1): 9–21; DOI: 10.1016/j. jcpa.2014.09.003.

21. Tandem repeat sequence in the intergenic region MGF 505 9R/10R is a new marker of the genetic variability among ASF Genotype II viruses. A. Elsukova, I. Shevchenko, A. Varentsova [et al.]. Proc. 10th Annual Meeting EPIZONE, 27–29 September 2016. Madrid, 2016: 78.

22. Assessment of African swine fever diagnostic techniques as a response to the epidemic outbreaks in Eastern European Union Countries: How to improve surveillance and control programs. C. Gallardo, R. Nieto, A. Soler [et al.]. J. Clin. Microbiol. 2015; 53 (8): 2555–2565; DOI: 10.1128/JCM.00857-15.

23. Variable and constant regions in African swine fever virus DNA. R. Blasco, M. Agüero, J. M. Almendral, E. Viñuela. Virology. 1989; 168 (2): 330–338; DOI: 10.1016/0042-6822(89)90273-0.

24. Attenuated and non-haemadsorbing (non-HAD) genotype II African swine fever virus (ASFV) isolated in Europe, Latvia 2017. C. Gallardo, A. Soler, I. Rodze [et al.]. Transbound. Emerg. Dis. 2019; 66 (3): 1399–1404; DOI: 10.1111/tbed.13132.

25. World Animal Health Information Database (WAHID Interface). OIE. 2018. URL: https://www.oie.int/wahis_2/public/wahid. php/Diseaseinformation/WI.

26. Blome S., Gabriel C., Beer M. Pathogenesis of African swine fever in domestic pigs and European wild boar. Virus Res. 2013; 173 (1): 122–130; DOI: 10.1016/j.virusres.2012.10.026.

27. Breese, Jr. S. S., De Boer C. J. Electron microscope observation of African swine fever virus in tissue culture cells. Virology. 1966; 28 (3): 420–428; DOI: 10.1016/0042-6822(66)90054-7.

28. Comparison of the genome sequences of non-pathogenic and pathogenic African swine fever virus isolates. D. A. Chapman, V. Tcherepanov, C. Upton, L. K. Dixon. J. Gen. Virol. 2008; 89 (Pt. 2): 397–408; DOI: 10.1099/vir.0.83343-0.

29. Course and transmission characteristics of oral low-dose infection of domestic pigs and European wild boar with a Caucasian African swine fever virus isolate. J. Pietschmann, C. Guinat, M. Beer [et al.]. Arch. Virol. 2015; 160 (7): 1657–1667; DOI: 10.1007/ s00705-015-2430-2.

30. Detection of African swine fever antibodies in experimental and field samples from the Russian Federation: implications for control. L. Mur, A. Igolkin, A. Varentsova [et al.]. Transbound. Emerg. Dis. 2016; 63 (5): 436–440; DOI: 10.1111/tbed.12304.

31. Dixon L. K. Molecular cloning and restriction enzyme mapping of an African swine fever virus isolate from Malawi. J. Gen. Virol. 1988; 69 (Pt. 7): Р. 1683–1694; DOI: 10.1099/0022-1317-69-7-1683.

32. Enhanced discrimination of African swine fever virus isolates through nucleotide sequencing of the p54, p72, and pB602L (CVR) genes. C. Gallardo, D. M. Mwaengo, J. M. Macharia [et al.]. Virus Genes. 2009; 38 (1): 85–95; DOI: 10.1007/s11262- 008-0293-2.

33. Genetic characterization of African swine fever virus isolates from soft ticks at the wildlife/domestic interface in Mozambique and identification of a novel genotype. C. J. Quembo, F. Jori, W. Vosloo, L. Heath. Transbound. Emerg. Dis. 2018; 65 (2): 420–431; DOI: 10.1111/tbed.12700.

34. Genetic characterization of African swine fever viruses from a 2008 outbreak in Tanzania. G. Misinzo, J. Magambo, J. Masambu [et al.]. Transbound. Emerg. Dis. 2011; 58 (1): 86–92; DOI: 10.1111/j.1865-1682.2010.01177.x.

35. Genetic characterization of circulating African swine fever viruses in Nigeria (2007–2015). P. D. Luka, J. E. Achenbach, F. N. Mwiine [et al.]. Transbound. Emerg. Dis. 2017; 64: 1598–1609; DOI: 10.1111/tbed.12553.

36. Genetic variation among African swine fever genotype II viruses, eastern and central Europe. C. Gallardo, J. FernándezPinero, V. Pelayo [et al.]. Emerg. Infect. Dis. 2014; 20 (9): 1544–1547; DOI: 10.3201/eid2009.140554.

37. Genome sequences derived from pig and dried blood pig feed samples provide important insights into the transmission of African swine fever virus in China in 2018. X. Wen, X. He, X. Zhang [et al.]. Emerg. Microbes Infect. 2019; 8 (1): 303–306; DOI: 10.1080/ 22221751.2019.1565915.

38. Genomic analysis of highly virulent Georgia 2007/1 isolate of African swine fever virus. D. A. Chapman, A. C. Darby, M. Da Silva [et al.]. Emerg. Infect. Dis. 2011; 17 (4): 599–605; DOI: 10.3201/ eid1704.101283.

39. Genotyping field strains of African swine fever virus by partial p72 gene characterization. A. D. Bastos, M. L. Penrith, C. Crucière [et al.]. Arch. Virol. 2003; 148 (4): 693–706; DOI: 10.1007/ s00705-002-0946-8.

40. In vivo experimental studies of genotype II African swine fever virus (ASFV) isolates currently circulating in two Estonian counties. C. Gallardo, A. Soler, V. Delicado [et al.]. Proc. 10th Annual Meeting EPIZONE, 27–29 September 2016. Madrid, 2016: 81.

41. Molecular characterization of African swine fever virus (ASFV) isolates circulating in the Eastern European Union countries 2014–2016. R. Nieto, A. Soler, I. Nurmoja [et al.]. Proc. 10th Annual Meeting EPIZONE, 27–29 September 2016. Madrid, 2016: 164.

42. Molecular epidemiology of African swine fever in East Africa. B. A. Lubisi, A. D. Bastos, R. M. Dwarka, W. Vosloo. Arch. Virol. 2005; 150 (12): 2439–2452; DOI: 10.1007/s00705-005-0602-1.

43. Molecular epidemiology of African swine fever virus studied by analysis of four variable genome regions. R. J. Nix, C. Gallardo, G. Hutchings [et al.]. Arch. Virol. 2006; 151 (12): 2475–2494; DOI: 10.1007/s00705-006-0794-z.

44. Phylodynamics and evolutionary epidemiology of African swine fever p72-CVR genes in Eurasia and Africa. M. A. Alkhamis, C. Gallardo, C. Jurado [et al.]. PLoS ONE. 2018; 13 (2):e0192565; DOI: 10.1371/journal.pone.0192565.

45. Phylogenomic analysis of 11 complete African swine fever virus genome sequences. E. P. de Villiers, C. Gallardo, M. Arias [et al.]. Virology. 2010; 400 (1): 128–136; DOI: 10.1016/j. virol.2010.01.019.

46. Tandem repeat sequence in the intergenic region MGF 505 9R/10R is a new marker of the genetic variability among ASF Genotype II viruses. A. Elsukova, I. Shevchenko, A. Varentsova [et al.]. Proc. 10th Annual Meeting EPIZONE, 27–29 September 2016. Madrid, 2016: 78.

47. Variable and constant regions in African swine fever virus DNA. R. Blasco, M. Agüero, J. M. Almendral, E. Viñuela. Virology. 1989; 168 (2): 330–338; DOI: 10.1016/0042-6822(89)90273-0.

48. World Animal Health Information Database (WAHID Interface). OIE. 2018. URL: https://www.oie.int/wahis_2/public/wahid. php/Diseaseinformation/WI.