JDR Vol.14 No.8 pp. 1105-1114
doi: 10.20965/jdr.2019.p1105


General Review on Hog Cholera (Classical Swine Fever), African Swine Fever, and Salmonella enterica Serovar Choleraesuis Infection

Sumio Shinoda*,†, Tamaki Mizuno**, and Shin-ichi Miyoshi**

*Collaborative Research Center of Okayama University for Infectious Diseases in India
1-1-1 Tsushima-naka, Kitaku, Okayama, Okayama 700-8530, Japan

Corresponding author

**Graduate School of Medicine, Dentistry and Pharmaceutical Sciences, Okayama University, Okayama, Japan

June 6, 2019
September 12, 2019
November 1, 2019
classical swine fever (CSF), African swine fever (ASF), Salmonella enterica serovar Choleraesuis, hog cholera

Classical swine fever (CSF, hog cholera) has reemerged in Japan after 26 years and affected domestic pigs and wild boars. CSF was reported in Gifu prefecture on September 2018. Approximately 90,000 breeding domestic pigs were sacrificed by farmers of Gifu and Aichi prefectures to prevent expansion of CSF outbreak. In mid September 2019, CSF outbreaks have occurred in 8 prefectures in central Japan. African swine fever (ASF) is another viral infectious disease that affects domestic pigs and wild boars, although the etiologic agent is different from that of CSF. Both CSF and ASF affect pig farmers because of their intense infectivity to domesticated pigs. Fortunately, the causative agents are not pathogenic to human. However, an enteric bacterium Salmonella enterica serovar Choleraesuis is pathogenic to pigs and humans. As Salmonella Choleraesuis causes food poisoning in humans, the infection is monitored by “Food Sanitation Law” in Japan. CSF, ASF, and Salmonella enterica serovar Choleraesuis salmonellosis are translated in Japanese as “ton-korera,” “afurika ton-korera,” and “buta-korera,” respectively, wherein “ton” and “buta” both mean pig or hog. Therefore the above Japanese words mean hog cholera.

Cite this article as:
S. Shinoda, T. Mizuno, and S. Miyoshi, “General Review on Hog Cholera (Classical Swine Fever), African Swine Fever, and Salmonella enterica Serovar Choleraesuis Infection,” J. Disaster Res., Vol.14, No.8, pp. 1105-1114, 2019.
Data files:
  1. [1] A. Postel, T. Nishi, K. Kameyama, D. Meyer, O. Suckstorff, K. Fukai, and P. Becher, “Reemergence of Classical Swine Fever, Japan, 2018,” Emerg. Infect. Dis., Vol.25, No.6, doi:10.3201/eid2506.181578, 2019.
  2. [2] World Organisation for Animal Health (OIE), “Information on aquatic and terrestrial animal diseases,” [accessed October 11, 2019]
  3. [3] V. R. Brown and S. N. Bevins, “A review of classical swine fever virus and routes of introduction into the United States and the potential for virus establishment,” Front Vet. Sci., Vol.5, No.31, doi:10.3389/fvets.2018.00031, 2018.
  4. [4] S. Blome, C. Staubach, J. Henke, J. Carlson, and M. Beer, “Classical Swine Fever – An Updated Review,” Viruses, Vol.9, No.4, doi:10.3390/v9040086, 2017.
  5. [5] D. Beltran-Alcrudo, J. R. Falco, E. Raizman, and K. Dietze, “Transboundary spread of pig diseases: the role of international trade and travel,” BMC Vet. Res., Vol.15, No.1, Article No.64, doi:10.1186/s12917-019-1800-5, 2019.
  6. [6] M. P. M. Meuwissen, S. H. Horst, R. B. M. Huirme, and A. A. Dijkhuizen, “A model to estimate the financial consequences of classical swine fever outbreaks: principles and outcomes,” Prev. Vet. Med., Vol.42, No.3-4, pp. 249-270, 1999.
  7. [7] D. Thompson, P. Muriel, D. Russel, P. Osborne, A. Bromley, M. Rowland, S. Creigh-Tyle, and C. Brown, “Economic costs of the foot and mouth disease outbreak in the United Kingdom in 2001,” Rev. Sci. Tech., Vol.21, No.3, pp. 675-687, 2002.
  8. [8] S. Farez and R. S. Morley, “Potential animal health hazards of pork and pork products,” Rev. Sci. Tech. Off. Int. Epiz., Vol.16, No.1, pp. 65-78, 1997.
  9. [9] S. Edwards, A. Fukusho, P.-C. Lefèvre, A. Lipowski, Z. Pejsak, P. Roehe, and J. Westergaard, “Classical swine fever: The global situation,” Vet. Microbiol., Vol.73, No.1-3, pp. 103-119, 2000.
  10. [10] E. Weiland, R. Ahl, R. Stark, F. Weiland, and H. J. Thiel, “A second envelope glycoprotein mediates neutralization of a pestivirus, hog cholera virus,“ J. Virol., Vol.66, No.6, pp. 3677-3682, 1992.
  11. [11] M. Iqbal, H. Flick-Smith, and J. W. McCauley, “Interactions of bovine viral diarrhoea virus glycoprotein Erns with cell surface glycosaminoglycans,” J. Gen. Virol., Vol.81, pp. 451-459, 2000.
  12. [12] M. M. Hulst, H. G. van Gennip, A. C. Vlot, E. Schooten, A. J. de Smit, and R. J. Moormann, “Interaction of classical swine fever virus with membrane-associated heparan sulfate: Role for virus replication in vivo and virulence,” J. Virol., Vol.75, No.20, pp. 9565-9595, 2001.
  13. [13] Z. Wang, Y. Nie, P. Wang, M. Ding, and H. Deng, “Characterization of classical swine fever virus entry by using pseudo typed viruses: E1 and E2 are sufficient to mediate viral entry,” Virol., Vol.330, No.1, pp. 332-341, 2004.
  14. [14] Z. Wu, Q. Wang, Q. Feng, Y. Liu, J. Teng, A. C. Yu, and J. Chen, “Correlation of the virulence of CSFV with evolutionary patterns of E2 glycoprotein,” Front. Biosci., Vol.1, pp. 204-220, 2010.
  15. [15] F. Tang, Z. Pan, and C. Zhang, “The selection pressure analysis of classical swine fever virus envelope protein genes Erns and E2,” Virus Res., Vol.131, No.2, pp. 132-135, 2008.
  16. [16] G. R. Risatti, L. G. Holinka, I. Fernandez Sainz, C. Carrillo, G. F. Kutish, Z. Lu, J. Zhu, D. L. Rock, and M. V. Borca, “Mutation in the carboxyl terminal region of E2 glycoprotein of classical swine fever virus are responsible for viral attenuation in swine,” Virol., Vol.364, No.2, pp. 371-382, 2007.
  17. [17] G. R. Risatti, L. G. Holinka, I. Fernandez Sainz, C. Carrillo, Z. Lu, and M. V. Borca, “N-linked glycosylation status of classical swine fever virus strain Brescia E2 glycoprotein influences virulence in swine,” J. Virol., Vol.81, No.2, pp. 924-933, 2007.
  18. [18] I. Fernandez Sainz, L. G. Holinka, Z. Lu, G. R. Rizatti, and M. V. Borca, “Removal of a N-linked glycosylation site of classical swine fever virus strain Brescia Erns glycoprotein affects virulence in swine,” Virol., Vol.370, No.1, pp. 122-129, 2008.
  19. [19] D. Liang, I. F. Sainz, I. H. Ansari, L. H. Gil, V. Vassilev, and R. O. Donis, “The envelope glycoprotein E2 is a determinant of cell culture tropism in ruminant pestiviruses,” J. Gen. Virol., Vol.84, pp. 1269-1274, 2003.
  20. [20] F.-I. Wang, M.-C. Deng, Y.-L. Huang, and C.-Y. Chang, “Structures and Functions of pestivirus glycoproteins: not simply surface matters,” Viruses, Vol.7, No.7, pp. 3506-3529, doi:10.3390/v7072783, 2015.
  21. [21] M. König, T. Lengsfeld, T. Pauly, R. Stark, and H. J. Thiel, “Classical swine fever virus: Independent induction of protective immunity by two structural glycoproteins,” J. Virol., Vol.69, No.10, pp. 6479-6486, 1995.
  22. [22] H. Zhang, C. Leng, Z. Tian, C. Liu, J. Chen, Y. Bai, Z. Li, L. Xiang, H. Zhai, Q. Wang, J. Peng, T. An, Y. Kan, L. Yao, X. Yang, X. Cai, and G. Tong, “Complete genomic characteristics and pathogenic analysis of the newly emerged classical swine fever virus in China,” BMC Vet. Res., Vol.14, No.1, Article No.204, doi:10.1186/s12917-018-1504-2, 2018.
  23. [23] R. C. Laughlin, R. Madera, Y. Peres, B. R. Berquist, L. Wang, S. Buist, Y. Buakova, S. Palle, C. J. Chung, M. V. Rasmussen, E. Martel, D. A. Brake, J. G. Neilan, S. D. Lawhon, L. G. Adams, J. Shi, and S. Marcel, “Plant-made E2 glycoprotein single-dose vaccine protects pigs against classical swine fever,” Plant Biotechnol. J., Vol.17, No.2, pp. 410-420, 2019.
  24. [24] A. J. de Smit, H. G. P. van Gennip, G. K. W. Miedema, P. A. van Rijn, C. Terstra, and R. J. M. Moormann, “Recombinant classical swine fever (CSF) viruses derived from the Chinese vaccine strain (C-strain) of CSF virus retain their avirulent and immunogenic characteristics,” Vaccine, Vol.18, No.22, pp. 2351-2358, 2000.
  25. [25] V. Moennig, G. Floegel-Niesmann, and I. Greiser-Wilke, “Clinical signs and epidemiology of classical swine fever: a review of new knowledge,” Vet. J., Vol.165, No.1, pp. 11-20, 2003.
  26. [26] E. Weiland, R. Stark, B. Haas, T. Rümenapf, G. Meyers, and H. J. Thief, “Pestivirus glycoprotein which includes neutralizing antibodies from part of a disulfide-linked heterodimer,” J. Virol., Vol.64, No.8, pp. 3563-3569, 1990.
  27. [27] J. T. van Oirschot, “Vaccinology of classical swine fever: from lab to field,” Vet. Microbiol., Vol.96, No.4, pp. 367-384, 2003.
  28. [28] Y. Burakova, R. Madera, L. Wang, S. Buist, K. Lleellish, J. R. Schlup, and J. Shi, “Food-grade saponin extract as an emulsifier and immunostimulant in emulsion-based subunit vaccine for pigs,” J. Immunol. Res., Vol.2018, Article ID 8979838, doi:10.1155/2018/8979838, 2018.
  29. [29] S. Costard, B. Wieland, W. de Glanville, F. Jori, R. Rowlands, W. Vosloo et al., “African swine fever: how can global spread be prevented?,” Philos. Trans. R. Soc. Lond B. Biol. Sci., Vol.364, No.1530, pp. 2683-2696, 2009.
  30. [30] M. Juszkiewicz, M. Walczak, and G. Woźniakowski, “Characteristics of selected active substances used in disinfectants and their virucidal activity against ASFV,” J. Ved. Res., Vol.63, No.1, pp. 17-25, 2019.
  31. [31] R. E. Montgomery, “On a form of a swine fever occurring in British East Africa (Kenya Colony),” J. Comp. Pathol., Vol.34, pp. 159-191, 1921.
  32. [32] M. C. Niederwerder, A. M. M. Stoian, R. R. R. Rowland, S. S. Dritz, V. Pettrovan, L. A. Constance, J. T. Gerbhardt, M. Olcha, C. K. Jones, J. C. Woodworth, Y. Fang, J. Liang, and T. J. Hefley, “Infectious dose of African swine fever virus when consumed naturally in liquid or feed,” Emerg. Infect. Dis., Vol.25, No.5, pp. 891-897. 2019.
  33. [33] A. Gogin, V. Gerasimov, A. Malogolovkin, and D. Kolbasov, “African swine fever in the North Caucasus region and the Russian Federation in years 2007-2012,” Virus Res., Vol.173, No.1, pp. 198-203, 2013.
  34. [34] X. Zhou, N. Li, Y. Luo, Y. Liu, F. Miao, T. Chen, S. Zhang, P. Cao, X. Li, K. Tian, H. J. Qiu, and R. Hu, “Emergence of African swine fever in China, 2018,” Transbound Emerg. Dis., Vol.65, No.6, pp. 1482-1484, 2018.
  35. [35] World Organisation for Animal Health (OIE), “African Swine Fever,” [accessed October 11, 2019]
  36. [36] A. Sanchez-Vizcaino, “Reserios del virus de la peste porcina Africana, Investigacion del virus la P.P.A en los artropodos mediante la prueba de la hemoadsorcio,” Bull. Off. Int. Epizoot., Vol.60, pp. 895-899, 1963.
  37. [37] J. M. Sánchez-Vizcaíno, L. Mur, and B. Martínez-López, “African swine fever: an epidemiological update,” Transbound Emerg. Dis., Vol.59, No.51, pp. 27-35, doi:10.1111/j.1865-1682.2011.01293.x, 2012.
  38. [38] J. M. Sánchez-Vizcaíno, L. Mur, and B. Martínez-López, “African-swine fever (ASF): five years around Europe,” Vet. Miorobiol., Vol.165, No.1-2, pp. 45-50, 2013.
  39. [39] N. Mazur-Panasiuk, G. Woźniakowski, and K. Niermczuk, “The first complete genomic sequences of African swine fever virus isolated in Poland,” Nature, Sci. Rep., No.9, Article No.4556, doi:10.1038/s41598-018-36823-0, 2019.
  40. [40] V. R. Brown and S. N. Bevins, “A review of African swine fever and the potential for introduction into the United States and the possibility of subsequent establishment in feral swine and native ticks,” Front. Vet. Sci., Vol.5, No.11, doi:10.3389/fvets.2018.00011, 2018.
  41. [41] K. Sugiura and T. Haga, “A rapid risk assessment of African swine fever introduction and spread in Japan based on expert opinions,” J. Vet. Med. Sci., Vol.80, No.11, pp. 1743-1746, 2018.
  42. [42] J. Galinso and C. Alonso, “African swine fever virus: a review,” Viruses, Vol.9, No.5, Article No.103, doi:10.3390/v9050103, 2017.
  43. [43] A. Lacasta, M. Ballester, P. L. Monteagudo, J. M. Rodgríguez, M. L. Salas, F. Accensi, S. Pina-Pedrero, A. Bensaid, J. Argrilaguet, S. López-Sorta, E. Hutet, M. F. Le Potier, and F. Rodríquez, “Expression library immunization can confer protection against lethal challenge with African swine fever virus,” J. Virol., Vol.88, No.22, pp. 13322-13332, 2014.
  44. [44] A. L. Reis, C. C. Abrams, L. C. Goatley, C. Netherton, D. G. Chapman, P. Sanchez-Cordon, and L. K. Dixon, “Detection of African swine fever virus interferon inhibitors from the genome of a virulent isolate reduces virulence in domestic pigs and induces a protective response,” Vaccine, Vol.34, No.39, pp. 4698-4705, 2016.
  45. [45] T. Ezaki, “Report on Salmonella nomenclature of Judicial Commission during IUMS general meeting in Paris,” J. Antibacterial. Antifungal. Agents Jpn., Vol.76, No.10, pp. 839-841, 2002 (in Japanese).
  46. [46] T. Ezaki, Y. Kawamura, and E. Yabuuchi, “Recognition of nomenclatural standing of Salmonella typhi (Approved Lists 1980), Salmonella enteritidis (Approved Lists 1980) and Salmonella typhimurium (Approved Lists 1980), and conservation of the specific epithets enteritidis and typhimurioum. Request for an opinion,” Int. J. Syst. Evol. Microbiol., Vol.50, No.2, pp. 945-947, 2000.
  47. [47] E. Yabuuchi and T. Ezaki, “Arguments against the replacement of type species of the genus Salmonella from Salmonella cholelaesuis to ‘Salmonella enterica’ and the creation of the term ‘neotype species,’ and for conservation of Salmonella choleraesuis,” Int. J. Syst. Evol. Microbiol., Vol.50, No.4, pp. 1693-1694, 2000.
  48. [48] Judicial Commission of the International Committee on Systematics of Prokaryotes, “The type species of the genus Salmonella Lignieres 1900 is Salmonella enterica (ex Kauffmann and Edwards 1952) Le Minor and Popoff 1987, with type strain LT2T, and conservation of the epithet enterica in Salmonella enterica over all earlier epithets that may be applied to this species. Opinion 80,” Int. J. Syst. Evol. Microbiol., Vol.55, No.1, pp. 519-520, 2005.
  49. [49] C.-L. Chen, L.-H. Su, R. P. Janapatla, C.-Y. Lin, and C.-H. Chiu, “Genetic analysis of virulence and antimicrobial-resistan plasimid pOU7519 in Salmonella enterica serovar Choleraesuis,” J. Microbiol. Immunol. Infect., doi:10.1016/j.jmii.2017.11.004, 2019.
  50. [50] R. Sugimoto, H. Suzuki, T. Nei, A. Tashiro, Y. Washio, K. Sonobe, Y. Nakamura, N. Wakayama, S. Inai, and H. Izumiya, “Neck abscess due to Salmonella Choleraesuis: case study and literature review,” J. Med. Microbiol. Case Reports, Vol.4, doi:10.1099/jmmcr.0.005109, 2017.
  51. [51] T. Whistler, P. Sapchookul, D. W. McCormick, O. Sangwichian, P. Jorakate, S. Makprasert, A. Jatapai, S. Naorat, U. Surin, S. Koosakunwat, S. Supcharassaeng, B. Piralam, M. Mikoleit, H. C. Baggett, J. Rhodes, and C. J. Gregory, “Epidemiology and antimicrobial resistance of invasive non-typhoidal Salmonellosis in rural Thailand from 2006-2014,” PLOS Neglect. Trop. Dis., Vol.12, No.8, e0006718, doi:10.1371/journal.pntd.0006718, 2018.
  52. [52] H. Herikstad, Y. Motarjemi, and R. V. Tauxe, “Salmonella surveillance: a global survey of public health serotyping,” Epidemiol. Infect., Vol.129, No.1, pp. 1-8, 2002.
  53. [53] A. M. Sy, J. Sandhu, and T. Lenox, “Salmonella enterica serotype Choleraesuis infection of the knee and femur in a nonbacteremic diabetic patient,” Case Rep. Infect. Dis., Vol.2013, Article ID 506157, doi:10.1155/2013/506157, 2013.
  54. [54] L. Zhu, X. Zhao, Q. Yin, X. Liu, X. Chen, C. Huang, and X. Suo, “Mucosal IgA and IFN-γ+ CD8 T cell immunity are important in the efficacy of live Salmonella enterica serovar Choleraesuis vaccines,” Nature, Sci. Rep., No.7, Article No.46408, doi:10.1038/srep46408, 2017.
  55. [55] X. Zhao, Q. Dai, D. Zhu, M. Liu, S. Chen, K. Sun, Q. Yang, Y. Wu, Q. Kong, and R. Jia, “Recombinant attenuated Salmonella Typhimurium with heterologous expression of the Salmonella Choleraesuis O-polysaccharide: high immunogenicity and protection,” Nature, Sci. Rep., No.7, Article No.7127, doi:10.1038/s41598-017-07689-5, 2017.
  56. [56] G. L. Alborali, J. Ruggeri, M. Pesciaroli, N. Martinelli, B. Chirullo, S. Ammendola, A. Battistoni, M. C. Ossiprandi, A. Corradi, and P. Pasquali, “Prime-boost vaccination with attenuated Salmonella Typhimurium ΔznuABC and inactivated Salmonella Choleraesuis is protective against Salmonella Choleraesuis challenge infection in piglets,” BMC Vet. Res., Vol.13, No.284, doi:10.1186/s12917-017-1202-5, 2017.
  57. [57] M. Matayoshi, T. Kitano, T. Sasaki, and M. Nakamura, “Resistance phenotypes and genotypes among multiple-antimicrobial-resistant Salmonella enterica subspecies enterica serovar Choleraesuis strains isolated between 2008 and 2012 from slaughter pigs in Okinawa Prefecture, Japan,” J. Vet. Med. Sci., Vol.77, No.6, pp. 705-710, 2015.

*This site is desgined based on HTML5 and CSS3 for modern browsers, e.g. Chrome, Firefox, Safari, Edge, IE9,10,11, Opera.

Last updated on Dec. 05, 2019