DOI QR코드

DOI QR Code

African swine fever: Etiology, epidemiological status in Korea, and perspective on control

  • Yoo, Dongwan (Department of Pathobiology, College of Veterinary Medicine, University of Illinois-Urbana-Champaign) ;
  • Kim, Hyunil (Optipharm Inc.) ;
  • Lee, Joo Young (Choong Ang Vaccine Laboratories Co. (Ltd.)) ;
  • Yoo, Han Sang (Department of Infectious Diseases, College of Veterinary Medicine, Seoul National University)
  • Received : 2019.12.30
  • Accepted : 2020.02.19
  • Published : 2020.03.31

Abstract

African swine fever (ASF), caused by the ASF virus, a member of the Asfarviridae family, is one of the most important diseases in the swine industry due to its clinical and economic impacts. Since the first report of ASF a century ago, ample information has become available, but prevention and treatment measures are still inadequate. Two waves of epizootic outbreaks have occurred worldwide. While the first wave of the epizootic outbreak was controlled in most of the infected areas, the second wave is currently active in the European and Asian continents, causing severe economic losses to the pig industry. There are different patterns of spreading in the outbreaks between those in European and Asian countries. Prevention and control of ASF are very difficult due to the lack of available vaccines and effective therapeutic measures. However, recent outbreaks in South Korea have been successfully controlled on swine farms, although feral pigs are periodically being found to be positive for the ASF virus. Therefore, we would like to share our story regarding the preparation and application of control measures. The success in controlling ASF on farms in South Korea is largely due to the awareness and education of swine farmers and practitioners, the early detection of infected animals, the implementation of strict control policies by the government, and widespread sharing of information among stakeholders. Based on the experience gained from the outbreaks in South Korea, this review describes the current understanding of the ASF virus and its pathogenic mechanisms, epidemiology, and control.

Keywords

Acknowledgement

This study was supported by BK21 PLUS and Research Institute for Veterinary Science, Seoul National University, Republic of Korea, and Agriculture and Food Research Initiative (AFRI) Competitive Grants No. 2018-67015-28287 from the US Department of Agriculture National Institute of Food and Agriculture (USDA NIFA) to D.Y.

References

  1. Montgomery R. A form of swine fever occurring in British East Africa (Kenya Colony). J Comp Pathol 1921;34:159-191. https://doi.org/10.1016/S0368-1742(21)80031-4
  2. Plowright W, Parker J, Peirce MA. African swine fever virus in ticks (Ornithodoros moubata, murray) collected from animal burrows in Tanzania. Nature 1969;221:1071-1073. https://doi.org/10.1038/2211071a0
  3. Sanchez-Cordon PJ, Montoya M, Reis AL, Dixon LK. African swine fever: a re-emerging viral disease threatening the global pig industry. Vet J 2018;233:41-48. https://doi.org/10.1016/j.tvjl.2017.12.025
  4. Arias M, Jurado C, Gallardo C, Fernandez-Pinero J, Sanchez-Vizcaino JM. Gaps in African swine fever: analysis and priorities. Transbound Emerg Dis 2018;65 Suppl 1:235-247.
  5. Gallardo C, Nieto R, Soler A, Pelayo V, Fernandez-Pinero J, Markowska-Daniel I, Pridotkas G, Nurmoja I, Granta R, Simon A, Perez C, Martin E, Fernandez-Pacheco P, Arias M. Assessment of African fever diagnostic techniques as a response to the epidemic outbreak in Eastern European Union countries: how to improve surveillance and control programs. J Clin Microbiol 2015;53:2555-2565. https://doi.org/10.1128/JCM.00857-15
  6. Sanchez-Vizcaino JM, Arias M. African swine fever. In: Zimmerman JJ, Karriker LA, Ramirez A, Schwartz KJ, Stevenson GW (eds.). Disease of Swine. 10th ed. pp. 396-404, Wiley-Blackwell, Ames, 2012.
  7. Bellini S, Rutili D, Guberti V. Preventive measures aimed at minimizing the risk of African swine fever virus spread in pig farming systems. Acta Vet Scand 2016;58:82. https://doi.org/10.1186/s13028-016-0264-x
  8. Gabriel C, Blome S, Malogolovkin A, Parilov S, Kolbasov D, Teifke JP, Beer M. Characterization of African swine fever virus Caucasus isolate in European wild boars. Emerg Infect Dis 2011;17:2342-2345. https://doi.org/10.3201/eid1712.110430
  9. Blome S, Gabriel C, Dietze K, Breithaupt A, Beer M. High virulence of African swine fever virus Caucasus isolate in European wild boars of all ages. Emerg Infect Dis 2012;18:708.
  10. Penrith ML, Vosloo W. Review of African swine fever: transmission, spread and control. J S Afr Vet Assoc 2009;80:58-62. https://doi.org/10.4102/jsava.v80i2.172
  11. Costard S, Mur L, Lubroth J, Sanchez-Vizcaino JM, Pfeiffer DU. Epidemiology of African swine fever virus. Virus Res 2013;173:191-197. https://doi.org/10.1016/j.virusres.2012.10.030
  12. Yanez RJ, Rodriguez JM, Nogal ML, Yuste L, Enriquez C, Rodriguez JF, Vinuela E. Analysis of the complete nucleotide sequence of African swine fever virus. Virology 1995;208:249-278. https://doi.org/10.1006/viro.1995.1149
  13. Rodriguez JM, Moreno LT, Alejo A, Lacasta A, Rodriguez F, Salas ML. Genome sequence of African swine fever virus BA71, the virulent parental strain of the nonpathogenic and tissue-culture adapted BA71V. PLoS One 2015;10:e0142889. https://doi.org/10.1371/journal.pone.0142889
  14. Dixon LK, Chapman DA, Netherton CL, Upton C. African swine fever virus replication and genomics. Virus Res 2013;173:3-14. https://doi.org/10.1016/j.virusres.2012.10.020
  15. Almendral JM, Almazan F, Blasco R, Vinuela E. Multigene families in African swine fever virus: family 110. J Virol 1990;64:2064-2072. https://doi.org/10.1128/jvi.64.5.2064-2072.1990
  16. Gonzalez A, Calvo V, Almazan F, Almendral JM, Ramirez JC, de la Vega I, Blasco R, Vinuela E. Multigene families in African swine fever virus: family 360. J Virol 1990;64:2073-2081. https://doi.org/10.1128/jvi.64.5.2073-2081.1990
  17. Vydelingum S, Baylis SA, Bristow C, Smith GL, Dixon LK. Duplicated genes within the variable right end of the genome of a pathogenic isolate of African swine fever virus. J Gen Virol 1993;74:2125-2130. https://doi.org/10.1099/0022-1317-74-10-2125
  18. Almazan F, Rodriguez JM, Andres G, Perez R, Vinuela E, Rodriguez JF. Transcriptional analysis of multigene family 110 of African swine fever virus. J Virol 1992;66:6655-6667. https://doi.org/10.1128/jvi.66.11.6655-6667.1992
  19. Yozawa T, Kutish GF, Afonso CL, Lu Z, Rock DL. Two novel multigene families, 530 and 300, in the terminal variable regions of African swine fever virus genome. Virology 1994;202:997-1002. https://doi.org/10.1006/viro.1994.1426
  20. Galindo I, Cuesta-Geijo MA, Hlavova K, Munoz-Moreno R, Barrado-Gil L, Dominguez J, Alonso C. African swine fever virus infects macrophages, the natural host cells, via clathrin- and cholesteroldependent endocytosis. Virus Res 2015;200:45-55. https://doi.org/10.1016/j.virusres.2015.01.022
  21. Hernaez B, Guerra M, Salas ML, Andres G. African swine fever virus undergoes outer envelope disruption, capsid disassembly and inner envelope fusion before core release from multivesicular endosomes. PLoS Pathog 2016;12:e1005595. https://doi.org/10.1371/journal.ppat.1005595
  22. Sanchez EG, Quintas A, Perez-Nunez D, Nogal M, Barroso S, Carrascosa AL, Revilla Y. African swine fever virus uses macropinocytosis to enter host cells. PLoS Pathog 2012;8:e1002754. https://doi.org/10.1371/journal.ppat.1002754
  23. Sanchez EG, Perez-Nunez D, Revilla Y. Mechanisms of entry and endosomal pathway of African swine fever virus. Vaccines (Basel) 2017;5:42. https://doi.org/10.3390/vaccines5040042
  24. Sanchez-Torres C, Gomez-Puertas P, Gomez-del-Moral M, Alonso F, Escribano JM, Ezquerra A, Dominguez J. Expression of porcine CD163 on monocytes/macrophages correlates with permissiveness to African swine fever infection. Arch Virol 2003;148:2307-2323. https://doi.org/10.1007/s00705-003-0188-4
  25. Popescu L, Gaudreault NN, Whitworth KM, Murgia MV, Nietfeld JC, Mileham A, Samuel M, Wells KD, Prather RS, Rowland RR. Genetically edited pigs lacking CD163 show no resistance following infection with the African swine fever virus isolate, Georgia 2007/1. Virology 2017;501:102-106. https://doi.org/10.1016/j.virol.2016.11.012
  26. Carrascosa AL, Sastre I, Vinuela E. African swine fever virus attachment protein. J Virol 1991;65:2283-2289. https://doi.org/10.1128/jvi.65.5.2283-2289.1991
  27. Carrascosa AL, Saastre I, Gonzalez P, Vinuela E. Localization of the African swine fever virus attachment protein P12 in the virus particle by immunoelectron microscopy. Virology 1993;193:460-465. https://doi.org/10.1006/viro.1993.1146
  28. Angulo A, Alcami A, Vinuela E. Virus-host interactions in African swine fever: the attachment to cellular receptors. Arch Virol Suppl 1993;7:169-183. https://doi.org/10.1007/978-3-7091-9300-6_14
  29. Carrascosa AL, Sastre I, Vinuela E. Production and purification of recombinant African swine fever virus attachment protein p12. J Biotechnol 1995;40:73-86. https://doi.org/10.1016/0168-1656(95)00035-O
  30. Rojo G, Garcia-Beato R, Vinuela E, Salas ML, Salas J. Replication of African swine fever virus DNA in infected cells. Virology 1999;257:524-536. https://doi.org/10.1006/viro.1999.9704
  31. Galindo I, Alonso C. African swine fever virus: a review. Viruses 2017;9:103. https://doi.org/10.3390/v9050103
  32. Rodriguez JM, Salas ML, Vinuela E. Intermediate class of mRNAs in African swine fever virus. J Virol 1996;70:8584-8589. https://doi.org/10.1128/jvi.70.12.8584-8589.1996
  33. Lopez-Otin C, Simon-Mateo C, Martinez L, Vinuela E. Gly-Gly-X, a novel consensus sequence for the proteolytic processing of viral and cellular proteins. J Biol Chem 1989;264:9107-9110. https://doi.org/10.1016/S0021-9258(18)60496-X
  34. Simon-Mateo C, Andres G, Almazan F, Vinuela E. Proteolytic processing in African swine fever virus: evidence for a new structural polyprotein, pp62. J Virol 1997;71:5799-5804. https://doi.org/10.1128/jvi.71.8.5799-5804.1997
  35. Martinez-Pomares L, Simon-Mateo C, Lopez-Otin C, Vinuela E. Characterization of the African swine fever virus structural protein p14.5: a DNA binding protein. Virology 1997;229:201-211. https://doi.org/10.1006/viro.1996.8434
  36. Salas ML, Andres G. African swine fever virus morphogenesis. Virus Res 2013;173:29-41. https://doi.org/10.1016/j.virusres.2012.09.016
  37. Zsak L, Sur JH, Burrage TG, Neilan JG, Rock DL. African swine fever virus (Asfv) multigene families 360 and 530 genes promote infected macrophage survival. Sci World J 2001;1:97. https://doi.org/10.1100/tsw.2001.202
  38. Moore DM, Zsak L, Neilan JG, Lu Z, Rock DL. The African swine fever virus thymidine kinase gene is required for efficient replication in swine macrophages and for virulence in swine. J Virol 1998;72:10310-10315. https://doi.org/10.1128/jvi.72.12.10310-10315.1998
  39. Oliveros M, Garcia-Escudero R, Alejo A, Vinuela E, Salas ML, Salas J. African swine fever virus dUTPase is a highly specific enzyme required for efficient replication in swine macrophages. J Virol 1999;73:8934-8943. https://doi.org/10.1128/jvi.73.11.8934-8943.1999
  40. Salguero FJ, Sanchez-Cordon PJ, Sierra MA, Jover A, Nunez A, Gomez-Villamandos JC. Apoptosis of thymocytes in experimental African swine fever virus infection. Histol Histopathol 2004;19:77-84.
  41. Salguero FJ, Sanchez-Cordon PJ, Nunez A, Fernandez de Marco M, Gomez-Villamandos JC. Proinflammatory cytokines induce lymphocyte apoptosis in acute African swine fever infection. J Comp Pathol 2005;132:289-302. https://doi.org/10.1016/j.jcpa.2004.11.004
  42. Hernaez B, Diaz-Gil G, Garcia-Gallo M, Ignacio Quetglas J, Rodriguez-Crespo I, Dixon L, Escribano JM, Alonso C. The African swine fever virus dynein-binding protein p54 induces infected cell apoptosis. FEBS Lett 2004;569:224-228. https://doi.org/10.1016/j.febslet.2004.06.001
  43. Hurtado C, Granja AG, Bustos MJ, Nogal ML, Gonzalez de Buitrago G, de Yebenes VG, Salas ML, Revilla Y, Carrascosa AL. The C-type lectin homologue gene (EP153R) of African swine fever virus inhibits apoptosis both in virus infection and in heterologous expression. Virology 2004;326:160-170. https://doi.org/10.1016/j.virol.2004.05.019
  44. Banjara S, Caria S, Dixon LK, Hinds MG, Kvansakul M. Structural insight into African swine fever virus A179L-mediated inhibition of apoptosis. J Virol 2017;91:e02228-16.
  45. Nogal ML, Gonzalez de Buitrago G, Rodriguez C, Cubelos B, Carrascosa AL, Salas ML, Revilla Y. African swine fever virus IAP homologue inhibits caspase activation and promotes cell survival in mammalian cells. J Virol 2001;75:2535-2543. https://doi.org/10.1128/JVI.75.6.2535-2543.2001
  46. Anderson EC, Hutchings GH, Mukarati N, Wilkinson PJ. African swine fever virus infection of the bushpig (Potamochoerus porcus) and its significance in the epidemiology of the disease. Vet Microbiol 1998;62:1-15. https://doi.org/10.1016/S0378-1135(98)00187-4
  47. Oura CA, Powell PP, Anderson E, Parkhouse RM. The pathogenesis of African swine fever in the resistant bushpig. J Gen Virol 1998;79:1439-1443. https://doi.org/10.1099/0022-1317-79-6-1439
  48. Zsak L, Caler E, Lu Z, Kutish GF, Neilan JG, Rock DL. A nonessential African swine fever virus gene UK is a significant virulence determinant in domestic swine. J Virol 1998;72:1028-1035. https://doi.org/10.1128/jvi.72.2.1028-1035.1998
  49. Sussman MD, Lu Z, Kutish G, Afonso CL, Roberts P, Rock DL. Identification of an African swine fever virus gene with similarity to a myeloid differentiation primary response gene and a neurovirulence-associated gene of herpes simplex virus. J Virol 1992;66:5586-5589. https://doi.org/10.1128/jvi.66.9.5586-5589.1992
  50. Afonso CL, Piccone ME, Zaffuto KM, Neilan J, Kutish GF, Lu Z, Balinsky CA, Gibb TR, Bean TJ, Zsak L, Rock DL. African swine fever virus multigene family 360 and 530 genes affect host interferon response. J Virol 2004;78:1858-1864. https://doi.org/10.1128/JVI.78.4.1858-1864.2004
  51. Kay-Jackson PC, Goatley LC, Cox L, Miskin JE, Parkhouse RM, Wienands J, Dixon LK. The CD2v protein of African swine fever virus interacts with the actin-binding adaptor protein SH3P7. J Gen Virol 2004;85:119-130. https://doi.org/10.1099/vir.0.19435-0
  52. Borca MV, Kutish GF, Afonso CL, Irusta P, Carrillo C, Brun A, Sussman M, Rock DL. An African swine fever virus gene with similarity to the T-lymphocyte surface antigen CD2 mediates hemadsorption. Virology 1994;199:463-468. https://doi.org/10.1006/viro.1994.1146
  53. Borca MV, Carrillo C, Zsak L, Laegreid WW, Kutish GF, Neilan JG, Burrage TG, Rock DL. Deletion of a CD2-like gene, 8-DR, from African swine fever virus affects viral infection in domestic swine. J Virol 1998;72:2881-2889. https://doi.org/10.1128/jvi.72.4.2881-2889.1998
  54. Boinas FS, Hutchings GH, Dixon LK, Wilkinson PJ. Characterization of pathogenic and non-pathogenic African swine fever virus isolates from Ornithodoros erraticus inhabiting pig premises in Portugal. J Gen Virol 2004;85:2177-2187. https://doi.org/10.1099/vir.0.80058-0
  55. Gallardo C, Soler A, Rodze I, Nieto R, Cano-Gomez 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;66:1399-1404. https://doi.org/10.1111/tbed.13132
  56. Burmakina G, Malogolovkin A, Tulman ER, Zsak L, Delhon G, Diel DG, Shobogorov NM, Morgunov YP, Morgunov SY, Kutish GF, Kolbasov D, Rock DL. African swine fever virus serotype-specific proteins are significant protective antigens for African swine fever. J Gen Virol 2016;97:1670-1675. https://doi.org/10.1099/jgv.0.000490
  57. Monteagudo PL, Lacasta A, Lopez E, Bosch L, Collado J, Pina-Pedrero S, Correa-Fiz F, Accensi F, Navas MJ, Vidal E, Bustos MJ, Rodriguez JM, Gallei A, Nikolin V, Salas ML, Rodriguez F. BA71 delta CD2: a new recombinant live attenuated African swine fever virus with cross-protective capabilities. J Virol 2017;91:e01058-17.
  58. Salguero FJ, Ruiz-Villamor E, Bautista MJ, Sanchez-Cordon PJ, Carrasco L, Gomez-Villamandos JC. Changes in macrophages in spleen and lymph nodes during acute African swine fever: expression of cytokines. Vet Immunol Immunopathol 2002;90:11-22. https://doi.org/10.1016/S0165-2427(02)00225-8
  59. Revilla Y, Callejo M, Rodriguez JM, Culebras E, Nogal ML, Salas ML, Vinuela E, Fresno M. Inhibition of nuclear factor κB activation by a virus-encoded IκB-like protein. J Biol Chem 1998;273:5405-5411. https://doi.org/10.1074/jbc.273.9.5405
  60. Neilan JG, Lu Z, Kutish GF, Zsak L, Lewis TL, Rock DL. A conserved African swine fever virus IκB homolog, 5EL, is nonessential for growth in vitro and virulence in domestic swine. Virology 1997;235:377-385. https://doi.org/10.1006/viro.1997.8693
  61. Gomez-Villamandos JC, Bautista MJ, Sanchez-Cordon PJ, Carrasco L. Pathology of African swine fever: the role of monocyte-mediated protective immune response. Virus Res 2013;173:140-149. https://doi.org/10.1016/j.virusres.2013.01.017
  62. Sanchez-Vizcaino JM, Mur L, Gomez-Villamandos JC, Carrasco L. An update on the epidemiology and pathology of African swine fever. J Comp Pathol 2015;152:9-21. https://doi.org/10.1016/j.jcpa.2014.09.003
  63. Gallardo C, Soler A, Nieto R, Sanchez MA, Martins C, Pelayo V, Carrascosa A, Revilla Y, Simon A, Briones V, Sanchez-Vizcaino JM, Arias M. Experimental transmission of African swine fever (ASF) low virulent isolate NH/P68 by surviving pigs. Transbound Emerg Dis 2015;62:612-622. https://doi.org/10.1111/tbed.12431
  64. Kalenzi Atuhaire D, Ochwo S, Afayoa M, Norbert Mwiine F, Kokas I, Arinaitwe E, Ademun-Okurut RA, Boniface Okuni J, Nanteza A, Ayebazibwe C, Okedi L, Olaho-Mukani W, Ojok L. Epidemiological overview of African swine fever in Uganda (2001-2012). J Vet Med 2013;2013:949638. https://doi.org/10.1155/2013/949638
  65. Thomas LF, Bishop RP, Onzere C, Mcintosh MT, Lemire KA, de Glanville WA, Cook EA, Fevre EM. Evidence for the presence of African swine fever virus in an endemic region of western Kenya in the absence of any reported outbreak. BMC Vet Res 2016;12:192. https://doi.org/10.1186/s12917-016-0830-5
  66. Wardley RC, de M Andrade C, Black DN, de Castro Portugal FL, Enjuanes L, Hess WR, Mebus C, Ordas A, Rutili D, Sanchez Vizcaino J, Vigario JD, Wilkinson PJ, Moura Nunes JF, Thomson G. African swine fever virus. Brief review. Arch Virol 1983;76:73-90. https://doi.org/10.1007/BF01311692
  67. EFSA Panel on Animal Health and Welfare (AHAW). Scientific opinion on African swine fever. EFSA J 2010;8:1556.
  68. Botija CS. African swine fever. New developments. Rev Sci Tech Off Int Epiz 1982;1:1065-1094.
  69. Mur L, Boadella M, Martinez-Lopez B, Gallardo C, Gortazar C, Sanchez-Vizcaino JM. Monitoring of African swine fever in the wild boar population of the most recent endemic area of Spain. Transbound Emerg Dis 2012;59:526-531. https://doi.org/10.1111/j.1865-1682.2012.01308.x
  70. Beltran-Alcrudo D, Lubroth J, Depner K, De La Rocque S. African swine fever in the Caucasus. FAO Empres Watch 2008:1-8.
  71. 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 Res 2013;173:198-203. https://doi.org/10.1016/j.virusres.2012.12.007
  72. Kolbasov D, Titov I, Tsybanov S, Gogin A, Malogolovkin A. African swine fever virus, Siberia, Russia, 2017. Emerg Infect Dis 2018;24:796-798. https://doi.org/10.3201/eid2404.171238
  73. Zhou X, Li N, Luo Y, Liu Y, Miao F, Chen T, Zhang S, Cao P, Li X, Tian K, Qiu HJ, Hu R. Emergence of African swine fever in China. Transbound Emerg Dis 2018;65:1482-1484. https://doi.org/10.1111/tbed.12989
  74. Feng Y, Zhao T, Nguyen T, Inui K, Ma Y, Nguyen TH, Nguyen VC, Liu D, Bui QA, To LT, Wang C, Tian K, Gao GF. Porcine respiratory and reproductive syndrome virus variants, Vietnam and China, 2007. Emerg Infect Dis 2008;14:1774-1776. https://doi.org/10.3201/eid1411.071676
  75. Vui DT, Tung N, Inui K, Slater S, Nilubol D. Complete genome sequence of porcine epidemic diarrhea virus in Vietnam. Genome Announc 2014;2:e00753-14.
  76. Wang WH, Lin CY, Chang Ishcol MR, Urbina AN, Assavalapsakul W, Thitithanyanont A, Lu PL, Chen YH, Wang SF. Detection of African swine fever virus in pork products brought to Taiwan by travellers. Emerg Microbes Infect 2019;8:1000-1002. https://doi.org/10.1080/22221751.2019.1636615
  77. Kim HJ, Cho KH, Lee SK, Kim DY, Nah JJ, Kim HJ, Kim HJ, Hwang JY, Sohn HJ, Choi JG, Kang HE, Kim YJ. Outbreak of African swine fever in South Korea, 2019. Transbound Emerg Dis 2020;67:473-475. https://doi.org/10.1111/tbed.13483
  78. Kim HJ, Lee MJ, Lee SK, Kim DY, Seo SJ, Kang HE, Nam HM. African swine fever virus in pork brought into South Korea by travelers from China, August 2018. Emerg Infect Dis 2019;25:1231-1233. https://doi.org/10.3201/eid2506.181684
  79. Gaudreault NN, Richt JA. Subunit vaccine approaches for African swine fever virus. Vaccines (Basel) 2019;7:56. https://doi.org/10.3390/vaccines7020056
  80. Sanchez EG, Perez-Nunez D, Revilla Y. Development of vaccines against African swine fever virus. Virus Res 2019;265:150-155. https://doi.org/10.1016/j.virusres.2019.03.022
  81. Teklue T, Sun Y, Abld M, Luo Y, Qiu HJ. Current status and evolving approaches to African swine fever vaccine development. Transbound Emerg Dis 2020;67:529-542. https://doi.org/10.1111/tbed.13364
  82. Tlaxca JL, Ellis S, Remmele RL Jr. Live attenuated and inactivated viral vaccine formulation and nasal delivery: potential and challenges. Adv Drug Deliv Rev 2015;93:56-78. https://doi.org/10.1016/j.addr.2014.10.002
  83. Leitao A, Cartaxeiro C, Coelho R, Cruz B, Parkhouse RM, Portugal FC, Vigario JD, Martins CL. The non-haemadsorbing African swine fever virus isolate ASFV/NH/P68 provides a model for defining the protective anti-virus immune response. J Gen Virol 2001;82:513-523. https://doi.org/10.1099/0022-1317-82-3-513
  84. Plotkin SA. Vaccines: the fourth century. Clin Vaccine Immunol 2009;16:1709-1719. https://doi.org/10.1128/CVI.00290-09
  85. Blome S, Gabriel C, Beer M. Modern adjuvants do not enhance the efficacy of an inactivated African swine fever virus vaccine preparation. Vaccine 2014;32:3879-3882. https://doi.org/10.1016/j.vaccine.2014.05.051
  86. Borca MV, Irusta P, Carrillo C, Afonso CL, Burrage T, Rock DL. African swine fever virus structural protein p72 contains a conformational neutralizing epitope. Virology 1994;201:413-418. https://doi.org/10.1006/viro.1994.1311
  87. Ruiz Gonzalvo F, Carnero ME, Caballero C, Martinez J. Inhibition of African swine fever infection in the presence of immune sera in vivo and in vitro. Am J Vet Res 1986;47:1249-1252.
  88. Zsak L, Onisk DV, Afonso CL, Rock DL. Virulent African swine fever virus isolates are neutralized by swine immune serum and by monoclonal antibodies recognizing a 72-kDa viral protein. Virology 1993;196:596-602. https://doi.org/10.1006/viro.1993.1515
  89. Gomez-Puertas P, Oviedo JM, Rodriguez F, Coll J, Escribano JM. Neutralization susceptibility of African swine fever virus is dependent on the phospholipid composition of viral particles. Virology 1997;228:180-189. https://doi.org/10.1006/viro.1996.8391
  90. Borca MV, Carrillo C, Zsak L, Laegreid WW, Kutish GF, Neilan JG, Burrage TG, Rock DL. Deletion of a CD2-like gene, 8-DR, from African swine fever virus affects viral infection in domestic swine. J Virol 1998;72:2881-2889. https://doi.org/10.1128/jvi.72.4.2881-2889.1998
  91. Alonso F, Dominguez J, Vinuela E, Revilla Y. African swine fever virus-specific cytotoxic T lymphocytes recognize the 32 kDa immediate early protein (vp32). Virus Res 1997;49:123-130. https://doi.org/10.1016/S0168-1702(97)01459-7
  92. Leitao A, Malur A, Cornelis P, Martins CL. Identification of a 25-aminoacid sequence from the major African swine fever virus structural protein VP72 recognised by porcine cytotoxic T lymphocytes using a lipoprotein based expression system. J Virol Methods 1998;75:113-119. https://doi.org/10.1016/S0166-0934(98)00105-0
  93. Gomez-Puertas P, Rodriguez F, Oviedo JM, Ramiro-Ibanez F, Ruiz-Gonzalvo F, Alonso C, Escribano JM. Neutralizing antibodies to different proteins of African swine fever virus inhibit both virus attachment and internalization. J Virol 1996;70:5689-5694. https://doi.org/10.1128/jvi.70.8.5689-5694.1996
  94. Gomez-Puertas P, Rodriguez F, Oviedo JM, Brun A, Alonso C, Escribano JM. The African swine fever virus proteins p54 and p30 are involved in two distinct steps of virus attachment and both contribute to the antibody-mediated protective immune response. Virology 1998;243:461-471. https://doi.org/10.1006/viro.1998.9068
  95. Barderas MG, Rodriguez F, Gomez-Puertas P, Aviles M, Beitia F, Alonso C, Escribano JM. Antigenic and immunogenic properties of a chimera of two immunodominant African swine fever virus proteins. Arch Virol 2001;146:1681-1691. https://doi.org/10.1007/s007050170056
  96. Neilan JG, Zsak L, Lu Z, Burrage TG, Kutish GF, Rock DL. Neutralizing antibodies to African swine fever virus proteins p30, p54, and p72 are not sufficient for antibody-mediated protection. Virology 2004;319:337-342. https://doi.org/10.1016/j.virol.2003.11.011
  97. Oura CA, Denyer MS, Takamatsu H, Parkhouse RM. In vivo depletion of CD8+ T lymphocytes abrogates protective immunity to African swine fever virus. J Gen Virol 2005;86:2445-2450. https://doi.org/10.1099/vir.0.81038-0
  98. Argilaguet JM, Perez-Martin E, Lopez S, Goethe M, Escribano JM, Giesow K, Keil GM, Rodriguez F. BacMam immunization partially protects pigs against sublethal challenge with African swine fever virus. Antiviral Res 2013;98:61-65. https://doi.org/10.1016/j.antiviral.2013.02.005