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Viral Hemorrhagic Fevers of Animals Caused by Positive-Stranded RNA Viruses

  • Chapter
Global Virology I - Identifying and Investigating Viral Diseases

Abstract

The term “viral hemorrhagic fevers” (VHFs) can loosely be applied to many serious diseases of animals (including fish, who are incapable of a fever response). While VHFs of humans are caused by viruses, limited to only four to five families (i.e., Arenaviridae, Bunyaviridae, Filoviridae, Flaviviridae, and possibly Rhabdoviridae), VHFs of animals are caused by a much broader variety of viruses. Therefore, Chaps. 11–14 were grouped using the Baltimore classification, i.e., by genome type, as opposed to the classification supported by the International Committee on Taxonomy of Viruses. As one could guess, the largest number of VHFs in animals is caused by mononegaviruses, but some are caused by viruses that have positive-sense or double-stranded RNA genomes, and some even have DNA genomes. This chapter focuses on positive-stranded RNA viruses. However, the reader is encouraged to read all four chapters to get an idea of the breadth of disease mechanisms and natural histories of this fascinating group of viruses that have both direct and indirect effects on humans, as well as implications for larger societal issues, such as food security and ecological dynamics. At the end of each chapter, “honorable mention” is given to some serious viral diseases that may have incomplete hemorrhagic features in regard to the definition provided in the introduction to the first chapter of this series.

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References

  1. Childs T. X Disease of Cattle - Saskatchewan. Can J Comp Med Vet Sci. 1946;10(11):316–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  2. Ridpath JF, Neill JD, Vilcek S, Dubovi EJ, Carman S. Multiple outbreaks of severe acute BVDV in North America occurring between 1993 and 1995 linked to the same BVDV2 strain. Vet Microbiol. 2006;114(3–4):196–204.

    PubMed  Google Scholar 

  3. Carman S, van Dreumel T, Ridpath J, Hazlett M, Alves D, Dubovi E, et al. Severe acute bovine viral diarrhea in Ontario, 1993–1995. J Vet Diagn Invest. 1998;10(1):27–35.

    CAS  PubMed  Google Scholar 

  4. Rebhun WC, French TW, Perdrizet JA, Dubovi EJ, Dill SG, Karcher LF. Thrombocytopenia associated with acute bovine virus diarrhea infection in cattle. J Vet Intern Med. 1989;3(1):42–6.

    CAS  PubMed  Google Scholar 

  5. Pellerin C, van den Hurk J, Lecomte J, Tussen P. Identification of a new group of bovine viral diarrhea virus strains associated with severe outbreaks and high mortalities. Virology. 1994;203(2):260–8.

    CAS  PubMed  Google Scholar 

  6. Peterhans E, Bachofen C, Stalder H, Schweizer M. Cytopathic bovine viral diarrhea viruses (BVDV): emerging pestiviruses doomed to extinction. Vet Res. 2010;41(6):44.

    PubMed Central  PubMed  Google Scholar 

  7. Loken T, Nyberg O. Eradication of BVDV in cattle: the Norwegian project. Vet Rec. 2013;172(25):661.

    CAS  PubMed  Google Scholar 

  8. Ståhl K, Alenius S. BVDV control and eradication in Europe—an update.pdf. Jpn J Vet Res. 2012;60(Supplement):S31–9.

    Google Scholar 

  9. Duffell SJ, Sharp MW, Bates D. Financial loss resulting from BVD-MD virus infection in a dairy herd. Vet Rec. 1986;118(2):38–9.

    CAS  PubMed  Google Scholar 

  10. Houe H. Economic impact of BVDV infection in dairies. Biologicals. 2003;31(2):137–43.

    PubMed  Google Scholar 

  11. Houe H, Pedersen KM, Meyling A., editors. A computerized spread sheet model for calculating total annual national losses due to bovine viral diarrhea virus infection in dairy herds and sensitivity analysis of selected parameters. Second symposium on pestiviruses; 1993; Annecy, France: Fondation Marcel Merieux.

    Google Scholar 

  12. Baker JC, Houe H. Preface bovine viral diarrhea virus. Vet Clin North Am Food Anim Pract. 1995;11(3):xiii–xiv.

    Google Scholar 

  13. Williams ES, Barker IK. Infectious diseases of wild mammals. 3rd ed. Ames, IA: Iowa State University Press; 2001. viii, 558 p. p.

    Google Scholar 

  14. Haines DM, Clark EG, Dubovi E. Monoclonal antibody based immunohistochemical detection of bovine viral diarrhea virus in formalin fixed, paraffin embedded tissues. Vet Pathol. 1992;29(1):27–33.

    CAS  PubMed  Google Scholar 

  15. Odeon AC, Kelling CL, Marshall DJ, Estela ES, Dubovi EJ, Donis RO. Experimental infection of calves with bovine viral diarrhea virus genotype II (NY-93). J Vet Diagn Invest. 1999;11(3):221–8.

    CAS  PubMed  Google Scholar 

  16. Risalde MA, Molina V, Sanchez-Cordon PJ, Romero-Palomo F, Pedrera M, Bartolome G, et al. Pathogenic mechanisms implicated in the intravascular coagulation in the lungs of BVDV-infected calves challenged with BHV-1. Vet Res. 2013;44:20. (20):1–13.

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Corapi WV, Elliot RD, French TW, Arthur DG, Bezek DM, Dubovi EJ. Thrombocytopenia and hemorrhages in veal calves infected with bovine viral diarrhea virus. J Aml Vet Med Assoc. 1990;196(6):590–6.

    CAS  Google Scholar 

  18. Corapi WV, French TW, Dubovi E. Severe thrombocytopenia in young calves experimentally infected with noncytopathic bovine viral diarrhea virus. J Virol. 1989;63(9):3934–43.

    CAS  PubMed Central  PubMed  Google Scholar 

  19. Marshall DJ, Moxley RA, Kelling CL. Distribution of virus and viral antigen in specific pathogen-free calves following inoculation with noncytopathic bovine viral diarrhea virus. Vet Pathol. 1996;33(3):311–8.

    CAS  PubMed  Google Scholar 

  20. Walz PH, Bell TG, Steficek BA, Kaiser L, Maes RK, Baker JC. Experimental model of type II bovine viral diarrhea virus-induced thrombocytopenia in neonatal calves. J Vet Diagn Invest. 1999;11(6):505–14.

    CAS  PubMed  Google Scholar 

  21. Scruggs DW, Fleming SA, Maslin WR, Wayne GA. Osteopetrosis, anemia, thrombocytopenia, and marrow necrosis in beef calves naturally infected with bovine virus diarrhea virus. J Vet Diagn Invest. 1995;7(4):555–9.

    CAS  PubMed  Google Scholar 

  22. Bolin SR, Ridpath JF. Differences in virulence between two noncytopathic bovine viral diarrhea viruses in calves. Am J Vet Res. 1992;53(11):2157–63.

    CAS  PubMed  Google Scholar 

  23. Hamers C, Couvreur B, Dehan P, Letellier C, Lewalle P, Pastoret PP, et al. Differences in experimental virulence of bovine viral diarrhoea viral strains isolated from haemorrhagic syndromes. Vet J. 2000;160(3):250–8.

    CAS  PubMed  Google Scholar 

  24. Blanchard PC, Ridpath JF, Walker JB, Hietala SK. An outbreak of late-term abortions, premature births, and congenital deformities associated with a bovine viral diarrhea virus 1 subtype b that induces thrombocytopenia. J Vet Diagn Invest. 2010;22(1):128–31.

    PubMed  Google Scholar 

  25. Walz PH, Bell TG, Grooms DL, Kaiser L, Maes RK, Baker JC. Platelet aggregation responses and virus isolation from platelets in calves experimentally infected with type I or type II bovine viral diarrhea virus. Can J Vet Res. 2001;65:241–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  26. Olafson P, Mac CA, Fox FH. An apparently new transmissible disease of cattle. Cornell Vet. 1946;36:205–13.

    CAS  PubMed  Google Scholar 

  27. Bielefeldt Ohmann H, Ronsholt L, Bloch B. Demonstration of bovine viral diarrhoea virus in peripheral blood mononuclear cells of persistently infected, clinically normal cattle. J Gen Virol. 1987;68(Pt 7):1971–82.

    PubMed  Google Scholar 

  28. Bolin SR, McClurkin AW, Coria MF. Effects of bovine viral diarrhea virus on the percentages and absolute numbers of circulating B and T lymphocytes in cattle. Am J Vet Res. 1985;46(4):884–6.

    CAS  PubMed  Google Scholar 

  29. Reggiado C, Kaeberle ML. Detection of bacteremia in cattle inoculated with bovine viral diarrhea virus. Am J Vet Res. 1981;42(2):218–21.

    Google Scholar 

  30. Baker JC. The clinical manifestations of bovine viral diarrhea virus. Vet Clin North Am Food Anim Pract. 1995;11(3):425–45.

    CAS  PubMed  Google Scholar 

  31. Smirnova NP, Webb BT, Bielefeldt-Ohmann H, Van Campen H, Antoniazzi AQ, Morarie SE, et al. Development of fetal and placental innate immune responses during establishment of persistent infection with bovine viral diarrhea virus. Virus Res. 2012;167(2):329–36.

    CAS  PubMed  Google Scholar 

  32. Perdrizet JA, Rebhun WC, Dubovi E, Donis RO. Bovine virus diarrhea—an apparently new transmissible disease of cattle. Cornell Vet. 1986;77:46–74.

    Google Scholar 

  33. Friedgut O, Rotenberg D, Brenner J, Yehuda S, Paz R, Alpert N, et al. Description of the first acute bovine diarrhea virus-2 outbreak in Israel. Vet J. 2011;189(1):108–10.

    PubMed  Google Scholar 

  34. Yamini B, Poppenga RH, Emmett BW, Judge LJ. Dicoumarol (moldy sweet clover) toxicosis in a group of Holstein calves. J Vet Diagn Invest. 1995;7(3):420–2.

    CAS  PubMed  Google Scholar 

  35. Dubovi EJ. Laboratory diagnosis of bovine viral diarrhea virus. Biologicals. 2013;41(1):8–13.

    PubMed  Google Scholar 

  36. Van Campen H. Epidemiology and control of BVD in the U.S. Vet Microbiol. 2010;142(1–2):94–8.

    PubMed  Google Scholar 

  37. US Department of Agriculture, Animal and Plant Health Inspection Service. Beef 2007–08. Prevalence and Control of Bovine Viral Diarrhea Virus on U.S. Cow-calf, Operations, 2007–08. 2010. http://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy07/Dairy07_is_BVD.pdf. Accessed 30 Mar 2015.

  38. US Department of Agriculture, Animal and Plant Health Inspection Service. Bovine viral diarrhea (BVD) management practices and detection in bulk tank milk in the United States, 2007. Info Sheet 2008. http://www.aphis.usda.gov/animal_health/nahms/dairy/downloads/dairy07/Dairy07_is_BVD.pdf. Accessed 30 Mar 2015.

  39. US Department of Agriculture, Animal and Plant Health Inspection Service. Vaccine usage in U.S. feedlots. Info Sheet 2013. http://www.aphis.usda.gov/animal_health/nahms/feedlot/downloads/feedlot2011/Feed11_is_VaccineUsage.pdf. Accessed 30 Mar 2015.

  40. Giangaspero M, Vacirca G, Harasawa R, Mathias B, Panuccio A, De Giuli Morghen C, et al. Genotypes of pestivirus RNA detected in live virus vaccines for human use. J Vet Med Sci. 2001;63(7):723–33.

    CAS  PubMed  Google Scholar 

  41. Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA. Virus taxonomy, VIIIth report of the ICTV. London: Elsevier/Academic Press; 2005.

    Google Scholar 

  42. Pringle CR. Virus taxonomy–1999. The universal system of virus taxonomy, updated to include the new proposals ratified by the International Committee on Taxonomy of Viruses during 1998. Arch Virol. 1999;144(2):421–9.

    CAS  PubMed  Google Scholar 

  43. Horzinek MC. Pestivirus-taxonomic perspectives. Arch Virol Suppl. 1991;3:1–5.

    CAS  PubMed  Google Scholar 

  44. Wensvoort G. Topographical and functional mapping of epitopes of hog cholera virus with monoclonal antibodies. J Gen Microbiol. 1989;70:2865–76.

    Google Scholar 

  45. Meyers G, Thiel HJ. Molecular characterization of pestiviruses. Adv Virus Res. 1996;47:53–118.

    CAS  PubMed  Google Scholar 

  46. Hulst MM, Moormann RJ. Inhibition of pestivirus infection in cell culture by envelope proteins E(rns) and E2 of classical swine fever virus: E(rns) and E2 interact with different receptors. J Gen Virol. 1997;78(Pt 11):2779–87.

    CAS  PubMed  Google Scholar 

  47. Weiland F, Weiland E, Unger G, Saalmuller A, Thiel HJ. Localization of pestiviral envelope proteins E(rns) and E2 at the cell surface and on isolated particles. J Gen Virol. 1999;80(Pt 5):1157–65.

    CAS  PubMed  Google Scholar 

  48. Salmon DE. Hog cholera: its history, nature, and treatment. Washington, DC: U.S. Department of Agriculture, The Bureau of Animal Industry, 1889.

    Google Scholar 

  49. Greiser-Wilke I, Depner K, Fritzemeier J, Haas L, Moennig V. Application of a computer program for genetic typing of classical swine fever virus isolates from Germany. J Virol Methods. 1998;75(2):141–50.

    CAS  PubMed  Google Scholar 

  50. Meuwissen MP, Horst SH, Huirne RB, Dijkhuizen AA. A model to estimate the financial consequences of classical swine fever outbreaks: principles and outcomes. Prev Vet Med. 1999;42(3–4):249–70.

    CAS  PubMed  Google Scholar 

  51. Moennig V. Introduction to classical swine fever: virus, disease and control policy. Vet Microbiol. 2000;73(2–3):93–102.

    CAS  PubMed  Google Scholar 

  52. Wachendorfer G, Reinhold GE, Dingeldein W, Berger J, Lorenz J, Frost JW. [Analysis of the hog cholera outbreak in Hesse in 1971–1974]. Dtsch Tierarztl Wochenschr. 1978;85(4):113–20.

    Google Scholar 

  53. Krassnig R, Schuller W, Heinrich J, Werfring F, Kalaus P, Fruhwirth M. Isolation of the agent of European swine plague from imported frozen wild boar meat. Dtsch Tierarztl Wochenschr. 1995;102(1):56.

    CAS  PubMed  Google Scholar 

  54. Laddomada A, Patta C, Oggiano A, Caccia A, Ruiu A, Cossu P, et al. Epidemiology of classical swine fever in Sardinia: a serological survey of wild boar and comparison with African swine fever. Vet Rec. 1994;134(8):183–7.

    CAS  PubMed  Google Scholar 

  55. Artois M, Depner KR, Guberti V, Hars J, Rossi S, Rutili D. Classical swine fever (hog cholera) in wild boar in Europe. Rev Sci Tech. 2002;21(2):287–303.

    CAS  PubMed  Google Scholar 

  56. Brugh Jr M, Foster JW, Hayes FA. Studies on the comparative susceptibility of Wild European and domestic swine to hog cholera. Am J Vet Res. 1964;25:1124–7.

    PubMed  Google Scholar 

  57. Depner KR, Muller A, Gruber A, Rodriguez A, Bickhardt K, Liess B. Classical swine fever in wild boar (Sus scrofa)–experimental infections and viral persistence. Dtsch Tierarztl Wochenschr. 1995;102(10):381–4.

    CAS  PubMed  Google Scholar 

  58. Laddomada A. Incidence and control of CSF in wild boar in Europe. Vet Microbiol. 2000;73(2–3):121–30.

    CAS  PubMed  Google Scholar 

  59. de Smit AJ, Bouma A, Terpstra C, van Oirschot JT. Transmission of classical swine fever virus by artificial insemination. Vet Microbiol. 1999;67(4):239–49.

    PubMed  Google Scholar 

  60. Elbers AR, Stegeman A, Moser H, Ekker HM, Smak JA, Pluimers FH. The classical swine fever epidemic 1997–1998 in The Netherlands: descriptive epidemiology. Pre Vet Med. 1999;42(3–4):157–84.

    Google Scholar 

  61. Crauwels AP, Nielen M, Elbers AR, Stegeman JA, Tielen MJ. Neighbourhood infections of classical swine fever during the 1997–1998 epidemic in The Netherlands. Prev Vet Med. 2003;61(4):263–77.

    CAS  PubMed  Google Scholar 

  62. Laevens H, Koenen F, Deluyker H, de Kruif A. Experimental infection of slaughter pigs with classical swine fever virus: transmission of the virus, course of the disease and antibody response. Vet Rec. 1999;145(9):243–8.

    CAS  PubMed  Google Scholar 

  63. Mintiens K, Laevens H, Dewulf J, Boelaert F, Verloo D, Koenen F. Risk analysis of the spread of classical swine fever virus through “neighbourhood infections” for different regions in Belgium. Prev Vet Med. 2003;60(1):27–36.

    CAS  PubMed  Google Scholar 

  64. Klinkenberg D, de Bree J, Laevens H, de Jong MC. Within- and between-pen transmission of classical swine fever virus: a new method to estimate the basic reproduction ratio from transmission experiments. Epidemiol Infect. 2002;128(2):293–9.

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Laevens H, Koenen F, Deluyker H, Berkvens D, de Kruif A. An experimental infection with classical swine fever virus in weaner pigs. I. Transmission of the virus, course of the disease, and antibody response. Vet Q. 1998;20(2):41–5.

    CAS  PubMed  Google Scholar 

  66. Dewulf J, Laevens H, Koenen F, Mintiens K, De Kruif A. An experimental infection with classical swine fever virus in pregnant sows: transmission of the virus, course of the disease, antibody response and effect on gestation. J Vet Med B Infect Dis Vet Public Health. 2001;48(8):583–91.

    CAS  PubMed  Google Scholar 

  67. Kaden V. The situation of classical swine fever in wild boars in the European community and selected aspects of disease transmission. Berl Munch Tierarztl Wochenschr. 1998;111(6):201–7.

    CAS  PubMed  Google Scholar 

  68. Kaden V, Renner C, Rothe A, Lange E, Hanel A, Gossger K. Evaluation of the oral immunisation of wild boar against classical swine fever in Baden-Wurttemberg. Berl Munch Tierarztl Wochenschr. 2003;116(9–10):362–7.

    PubMed  Google Scholar 

  69. Hughes RW, Gustafson DP. Some factors that may influence hog cholera transmission. Am J Vet Res. 1960;21:464–71.

    CAS  PubMed  Google Scholar 

  70. Dewulf J, Laevens H, Koenen F, Mintiens K, de Kruif A. Airborne transmission of classical swine fever virus under experimental conditions. Vet Rec. 2000;147(26):735–8.

    CAS  PubMed  Google Scholar 

  71. Gonzalez C, Pijoan C, Ciprian A, Correa P, Mendoza S. The effect of vaccination with the PAV-250 strain classical swine fever (CSF) virus on the airborne transmission of CSF virus. J Vet Med Sci. 2001;63(9):991–6.

    CAS  PubMed  Google Scholar 

  72. Moennig V, Greiser-Wilke I. Classical swine fever virus. In: Mahy BW, van Regenmortel MH, editors. Encyclopedia of virology. Academic Press, Waltham, MA; 2008. p. 525–32.

    Google Scholar 

  73. Weiss E, Teredesai A, Hoffmann R, Hoffmann-Fezer G. Volume distribution and ultrastructure of platelets in acute hog cholera. Thromb Diath Haemorrh. 1973;30(2):371–80.

    CAS  PubMed  Google Scholar 

  74. Knoetig SM, Summerfield A, Spagnuolo-Weaver M, McCullough KC. Immunopathogenesis of classical swine fever: role of monocytic cells. Immunology. 1999;97(2):359–66.

    CAS  PubMed Central  PubMed  Google Scholar 

  75. Summerfield A, Knotig SM, McCullough KC. Lymphocyte apoptosis during classical swine fever: implication of activation-induced cell death. J Virol. 1998;72(3):1853–61.

    CAS  PubMed Central  PubMed  Google Scholar 

  76. Summerfield A, Hofmann MA, McCullough KC. Low density blood granulocytic cells induced during classical swine fever are targets for virus infection. Vet Immunol Immunopathol. 1998;63(3):289–301.

    CAS  PubMed  Google Scholar 

  77. Summerfield A, Zingle K, Inumaru S, McCullough KC. Induction of apoptosis in bone marrow neutrophil-lineage cells by classical swine fever virus. J Gen Virol. 2001;82(6):1309–18.

    CAS  PubMed  Google Scholar 

  78. Summerfield A, McNeilly F, Walker I, Allan G, Knoetig SM, McCullough KC. Depletion of CD4(+) and CD8(high+) T-cells before the onset of viraemia during classical swine fever. Vet Immunol Immunopathol. 2001;78(1):3–19.

    CAS  PubMed  Google Scholar 

  79. Cheville NF, Mengeling WL. The pathogenesis of chronic hog cholera (swine fever). Histologic, immunofluorescent, and electron microscopic studies. Lab Invest. 1969;20(3):261–74.

    CAS  PubMed  Google Scholar 

  80. Ressang AA. Studies on the pathogenesis of hog cholera. II. Virus distribution in tissue and the morphology of the immune response. Zentralbl Veterinarmed B. 1973;20(4):272–88.

    CAS  PubMed  Google Scholar 

  81. Susa M, Konig M, Saalmuller A, Reddehase MJ, Thiel HJ. Pathogenesis of classical swine fever: B-lymphocyte deficiency caused by hog cholera virus. J Virol. 1992;66(2):1171–5.

    CAS  PubMed Central  PubMed  Google Scholar 

  82. Gomez-Villamandos JC, Ruiz-Villamor E, Bautista MJ, Quezada M, Sanchez CP, Salguero FJ, et al. Pathogenesis of classical swine fever: renal haemorrhages and erythrodiapedesis. J Comp Pathol. 2000;123(1):47–54.

    CAS  PubMed  Google Scholar 

  83. Heene D, Hoffmann-Fezer G, Muller-Berghaus G, Hoffmann R, Weiss E, Lasch HG. Coagulation disorders in acute hog cholera. Beitr Pathol. 1971;144(3):259–71.

    CAS  PubMed  Google Scholar 

  84. Trautwein G. Pathology and pathogenesis of the disease. In: Liess B, editor. Classical swine fever and related viral diseases. Boston, MA: Martinus Nijhoff Publishing; 1988. p. 27–54.

    Google Scholar 

  85. Ruggli N, Tratschin JD, Mittelholzer C, Hofmann MA. Nucleotide sequence of classical swine fever virus strain Alfort/187 and transcription of infectious RNA from stably cloned full-length cDNA. J Virol. 1996;70(6):3478–87.

    CAS  PubMed Central  PubMed  Google Scholar 

  86. Moormann RJ, van Gennip HG, Miedema GK, Hulst MM, van Rijn PA. Infectious RNA transcribed from an engineered full-length cDNA template of the genome of a pestivirus. J Virol. 1996;70(2):763–70.

    CAS  PubMed Central  PubMed  Google Scholar 

  87. Tratschin JD, Moser C, Ruggli N, Hofmann MA. Classical swine fever virus leader proteinase Npro is not required for viral replication in cell culture. J Virol. 1998;72(9):7681–4.

    CAS  PubMed Central  PubMed  Google Scholar 

  88. Meyers G, Saalmuller A, Buttner M. Mutations abrogating the RNase activity in glycoprotein E(rns) of the pestivirus classical swine fever virus lead to virus attenuation. J Virol. 1999;73(12):10224–35.

    CAS  PubMed Central  PubMed  Google Scholar 

  89. Van Gennip HG, Vlot AC, Hulst MM, De Smit AJ, Moormann RJ. Determinants of virulence of classical swine fever virus strain Brescia. J Virol. 2004;78(16):8812–23.

    PubMed Central  PubMed  Google Scholar 

  90. Risatti GR, Borca MV, Kutish GF, Lu Z, Holinka LG, French RA, et al. The E2 glycoprotein of classical swine fever virus is a virulence determinant in swine. J Virol. 2005;79(6):3787–96.

    CAS  PubMed Central  PubMed  Google Scholar 

  91. Ruggli N, Summerfield A, Fiebach AR, Guzylack-Piriou L, Bauhofer O, Lamm CG, et al. Classical swine fever virus can remain virulent after specific elimination of the interferon regulatory factor 3-degrading function of Npro. J Virol. 2009;83(2):817–29.

    CAS  PubMed Central  PubMed  Google Scholar 

  92. Summerfield A, Alves M, Ruggli N, de Bruin MG, McCullough KC. High IFN-alpha responses associated with depletion of lymphocytes and natural IFN-producing cells during classical swine fever. J Interferon Cytokine Res. 2006;26(4):248–55.

    CAS  PubMed  Google Scholar 

  93. Bauhofer O, Summerfield A, Sakoda Y, Tratschin JD, Hofmann MA, Ruggli N. Classical swine fever virus Npro interacts with interferon regulatory factor 3 and induces its proteasomal degradation. J Virol. 2007;81(7):3087–96.

    CAS  PubMed Central  PubMed  Google Scholar 

  94. Fiebach AR, Guzylack-Piriou L, Python S, Summerfield A, Ruggli N. Classical swine fever virus N(pro) limits type I interferon induction in plasmacytoid dendritic cells by interacting with interferon regulatory factor 7. J Virol. 2011;85(16):8002–11.

    CAS  PubMed Central  PubMed  Google Scholar 

  95. Doceul V, Charleston B, Crooke H, Reid E, Powell PP, Seago J. The Npro product of classical swine fever virus interacts with IkappaBalpha, the NF-kappaB inhibitor. J Gen Virol. 2008;89(Pt 8):1881–9.

    CAS  PubMed  Google Scholar 

  96. Durand SV, Hulst MM, de Wit AA, Mastebroek L, Loeffen WL. Activation and modulation of antiviral and apoptotic genes in pigs infected with classical swine fever viruses of high, moderate or low virulence. Arch Virol. 2009;154(9):1417–31.

    CAS  PubMed Central  PubMed  Google Scholar 

  97. Precausta P, Kato F, Brun A. Swine fever. Immunisation of piglets. Comp Immunol Microbiol Infect Dis. 1983;6(4):281–9.

    CAS  PubMed  Google Scholar 

  98. Terpstra C, Woortmeyer R, Barteling SJ. Development and properties of a cell culture produced vaccine for hog cholera based on the Chinese strain. Dtsch Tierarztl Wochenschr. 1990;97(2):77–9.

    CAS  PubMed  Google Scholar 

  99. Terpstra C, Kroese AH. Potency control of modified live viral vaccines for veterinary use. Vaccine. 1996;14(6):570–5.

    CAS  PubMed  Google Scholar 

  100. Konig M, Lengsfeld T, Pauly T, Stark R, Thiel HJ. Classical swine fever virus: independent induction of protective immunity by two structural glycoproteins. J Virol. 1995;69(10):6479–86.

    CAS  PubMed Central  PubMed  Google Scholar 

  101. Suradhat S, Intrakamhaeng M, Damrongwatanapokin S. The correlation of virus-specific interferon-gamma production and protection against classical swine fever virus infection. Vet Immunol Immunopathol. 2001;83(3–4):177–89.

    CAS  PubMed  Google Scholar 

  102. Suradhat S, Thanawongnuwech R, Poovorawan Y. Upregulation of IL-10 gene expression in porcine peripheral blood mononuclear cells by porcine reproductive and respiratory syndrome virus. J Gen Virol. 2003;84(Pt 2):453–9.

    CAS  PubMed  Google Scholar 

  103. Ceppi M, de Bruin MG, Seuberlich T, Balmelli C, Pascolo S, Ruggli N, et al. Identification of classical swine fever virus protein E2 as a target for cytotoxic T cells by using mRNA-transfected antigen-presenting cells. J Gen Virol. 2005;86(Pt 9):2525–34.

    CAS  PubMed  Google Scholar 

  104. Piriou L, Chevallier S, Hutet E, Charley B, Le Potier MF, Albina E. Humoral and cell-mediated immune responses of d/d histocompatible pigs against classical swine fever (CSF) virus. Vet Res. 2003;34(4):389–404.

    CAS  PubMed  Google Scholar 

  105. Rau H, Revets H, Balmelli C, McCullough KC, Summerfield A. Immunological properties of recombinant classical swine fever virus NS3 protein in vitro and in vivo. Vet Res. 2006;37(1):155–68.

    CAS  PubMed  Google Scholar 

  106. Suradhat S, Sada W, Buranapraditkun S, Damrongwatanapokin S. The kinetics of cytokine production and CD25 expression by porcine lymphocyte subpopulations following exposure to classical swine fever virus (CSFV). Vet Immunol Immunopathol. 2005;106(3–4):197–208.

    CAS  PubMed  Google Scholar 

  107. Pauly T, Elbers K, Konig M, Lengsfeld T, Saalmuller A, Thiel HJ. Classical swine fever virus-specific cytotoxic T lymphocytes and identification of a T cell epitope. J Gen Virol. 1995;76(Pt 12):3039–49.

    CAS  PubMed  Google Scholar 

  108. Graham SP, Everett HE, Johns HL, Haines FJ, La Rocca SA, Khatri M, et al. Characterisation of virus-specific peripheral blood cell cytokine responses following vaccination or infection with classical swine fever viruses. Vet Microbiol. 2010;142(1–2):34–40.

    CAS  PubMed  Google Scholar 

  109. Graham SP, Haines FJ, Johns HL, Sosan O, La Rocca SA, Lamp B, et al. Characterisation of vaccine-induced, broadly cross-reactive IFN-gamma secreting T cell responses that correlate with rapid protection against classical swine fever virus. Vaccine. 2012;30(17):2742–8.

    CAS  PubMed  Google Scholar 

  110. Pasick J. Classical swine fever. In: USAHA, editor. Foreign animal diseases. 7th ed. Boca Raton, FL: Boca Publications Group, Inc; 2008. p. 197–205.

    Google Scholar 

  111. Van Oirschot JT. Hog cholera. In: Barbara E. Straw, Sylvie D’Allaire, William L. Mengeling, Taylor DJ, editors. Diseases of swine. Iowa State University Press, Iowa: Wiley, John & Sons, Incorporated; 1999. p. 159–72.

    Google Scholar 

  112. Weesendorp E, Stegeman A, Loeffen W. Dynamics of virus excretion via different routes in pigs experimentally infected with classical swine fever virus strains of high, moderate or low virulence. Vet Microbiol. 2009;133(1–2):9–22.

    CAS  PubMed  Google Scholar 

  113. Lavazza A, Capucci L. Rabbit haemorrhagic disease. Manual of diagnostic tests and vaccines for terrestrial animals. 7th ed. Paris: Office Internationale des Épizooties; 2012.

    Google Scholar 

  114. Lowings JP, Paton DJ, Sands JJ, De Mia GM, Rutili D. Classical swine fever: genetic detection and analysis of differences between virus isolates. J Gen Virol. 1994;75(Pt 12):3461–8.

    CAS  PubMed  Google Scholar 

  115. Paton DJ, McGoldrick A, Greiser-Wilke I, Parchariyanon S, Song JY, Liou PP, et al. Genetic typing of classical swine fever virus. Vet Microbiol. 2000;73(2–3):137–57.

    CAS  PubMed  Google Scholar 

  116. Lowings P, Ibata G, Needham J, Paton D. Classical swine fever virus diversity and evolution. J Gen Virol. 1996;77(Pt 6):1311–21.

    CAS  PubMed  Google Scholar 

  117. Bjorklund H, Lowings P, Stadejek T, Vilcek S, Greiser-Wilke I, Paton D, et al. Phylogenetic comparison and molecular epidemiology of classical swine fever virus. Virus Genes. 1999;19(3):189–95.

    CAS  PubMed  Google Scholar 

  118. Widjojoatmodjo MN, van Gennip HG, de Smit AJ, Moormann RJ. Comparative sequence analysis of classical swine fever virus isolates from the epizootic in The Netherlands in 1997–1998. Vet Microbiol. 1999;66(4):291–9.

    CAS  PubMed  Google Scholar 

  119. Greiser-Wilke I, Fritzemeier J, Koenen F, Vanderhallen H, Rutili D, De Mia GM, et al. Molecular epidemiology of a large classical swine fever epidemic in the European Union in 1997–1998. Vet Microbiol. 2000;77(1–2):17–27.

    CAS  PubMed  Google Scholar 

  120. Baker JA, inventor; Armour & Co, assignee. Method of producing non-virulent strains of attenuated and stabilized hog cholera virus. US; 1961.

    Google Scholar 

  121. Terpstra C, Robijns KG. Experience with regional vaccination against swine fever in enzootic areas for limited periods using C-strain virus. Tijdschr Diergeneeskd. 1977;102(2):106–12.

    CAS  PubMed  Google Scholar 

  122. Dahle J, Liess B. Assessment of safety and protective value of a cell culture modified strain “C” vaccine of hog cholera/classical swine fever virus. Berl Munch Tierarztl Wochenschr. 1995;108(1):20–5.

    CAS  PubMed  Google Scholar 

  123. Hulst MM, Westra DF, Wensvoort G, Moormann RJ. Glycoprotein E1 of hog cholera virus expressed in insect cells protects swine from hog cholera. J Virol. 1993;67(9):5435–42.

    CAS  PubMed Central  PubMed  Google Scholar 

  124. van Rijn PA, van Gennip HG, Moormann RJ. An experimental marker vaccine and accompanying serological diagnostic test both based on envelope glycoprotein E2 of classical swine fever virus (CSFV). Vaccine. 1999;17(5):433–40.

    PubMed  Google Scholar 

  125. Beer M, Reimann I, Hoffmann B, Depner K. Novel marker vaccines against classical swine fever. Vaccine. 2007;25(30):5665–70.

    CAS  PubMed  Google Scholar 

  126. Dong XN, Wei K, Liu ZQ, Chen YH. Candidate peptide vaccine induced protection against classical swine fever virus. Vaccine. 2002;21(3–4):167–73.

    CAS  PubMed  Google Scholar 

  127. Dong XN, Chen Y, Wu Y, Chen YH. Candidate multi-peptide-vaccine against classical swine fever virus induced potent immunity with serological marker. Vaccine. 2005;23(28):3630–3.

    CAS  PubMed  Google Scholar 

  128. Dong XN, Chen YH. Candidate peptide-vaccines induced immunity against CSFV and identified sequential neutralizing determinants in antigenic domain A of glycoprotein E2. Vaccine. 2006;24(11):1906–13.

    CAS  PubMed  Google Scholar 

  129. Liu S, Tu C, Wang C, Yu X, Wu J, Guo S, et al. The protective immune response induced by B cell epitope of classical swine fever virus glycoprotein E2. J Virol Methods. 2006;134(1–2):125–9.

    CAS  PubMed  Google Scholar 

  130. Andrew ME, Morrissy CJ, Lenghaus C, Oke PG, Sproat KW, Hodgson AL, et al. Protection of pigs against classical swine fever with DNA-delivered gp55. Vaccine. 2000;18(18):1932–8.

    CAS  PubMed  Google Scholar 

  131. Andrew M, Morris K, Coupar B, Sproat K, Oke P, Bruce M, et al. Porcine interleukin-3 enhances DNA vaccination against classical swine fever. Vaccine. 2006;24(16):3241–7.

    CAS  PubMed  Google Scholar 

  132. Yu X, Tu C, Li H, Hu R, Chen C, Li Z, et al. DNA-mediated protection against classical swine fever virus. Vaccine. 2001;19(11–12):1520–5.

    CAS  PubMed  Google Scholar 

  133. Ganges L, Barrera M, Nunez JI, Blanco I, Frias MT, Rodriguez F, et al. A DNA vaccine expressing the E2 protein of classical swine fever virus elicits T cell responses that can prime for rapid antibody production and confer total protection upon viral challenge. Vaccine. 2005;23(28):3741–52.

    CAS  PubMed  Google Scholar 

  134. Wienhold D, Armengol E, Marquardt A, Marquardt C, Voigt H, Buttner M, et al. Immunomodulatory effect of plasmids co-expressing cytokines in classical swine fever virus subunit gp55/E2-DNA vaccination. Vet Res. 2005;36(4):571–87.

    CAS  PubMed  Google Scholar 

  135. van Zijl M, Wensvoort G, de Kluyver E, Hulst M, van der Gulden H, Gielkens A, et al. Live attenuated pseudorabies virus expressing envelope glycoprotein E1 of hog cholera virus protects swine against both pseudorabies and hog cholera. J Virol. 1991;65(5):2761–5.

    PubMed Central  PubMed  Google Scholar 

  136. Hooft van Iddekinge BJ, de Wind N, Wensvoort G, Kimman TG, Gielkens AL, Moormann RJ. Comparison of the protective efficacy of recombinant pseudorabies viruses against pseudorabies and classical swine fever in pigs; influence of different promoters on gene expression and on protection. Vaccine. 1996;14(1):6–12.

    CAS  PubMed  Google Scholar 

  137. Mulder WA, Priem J, Glazenburg KL, Wagenaar F, Gruys E, Gielkens AL, et al. Virulence and pathogenesis of non-virulent and virulent strains of pseudorabies virus expressing envelope glycoprotein E1 of hog cholera virus. J Gen Virol. 1994;75(Pt 1):117–24.

    CAS  PubMed  Google Scholar 

  138. Peeters B, Bienkowska-Szewczyk K, Hulst M, Gielkens A, Kimman T. Biologically safe, non-transmissible pseudorabies virus vector vaccine protects pigs against both Aujeszky’s disease and classical swine fever. J Gen Virol. 1997;78(Pt 12):3311–5.

    CAS  PubMed  Google Scholar 

  139. Hammond JM, McCoy RJ, Jansen ES, Morrissy CJ, Hodgson AL, Johnson MA. Vaccination with a single dose of a recombinant porcine adenovirus expressing the classical swine fever virus gp55 (E2) gene protects pigs against classical swine fever. Vaccine. 2000;18(11–12):1040–50.

    CAS  PubMed  Google Scholar 

  140. Hammond JM, Jansen ES, Morrissy CJ, Williamson MM, Hodgson AL, Johnson MA. Oral and sub-cutaneous vaccination of commercial pigs with a recombinant porcine adenovirus expressing the classical swine fever virus gp55 gene. Arch Virol. 2001;146(9):1787–93.

    CAS  PubMed  Google Scholar 

  141. Hammond JM, Jansen ES, Morrissy CJ, Hodgson AL, Johnson MA. Protection of pigs against ‘in contact’ challenge with classical swine fever following oral or subcutaneous vaccination with a recombinant porcine adenovirus. Virus Res. 2003;97(2):151–7.

    CAS  PubMed  Google Scholar 

  142. Hammond JM, Johnson MA. Porcine adenovirus as a delivery system for swine vaccines and immunotherapeutics. Vet J. 2005;169(1):17–27.

    CAS  PubMed  Google Scholar 

  143. Hahn J, Park SH, Song JY, An SH, Ahn BY. Construction of recombinant swinepox viruses and expression of the classical swine fever virus E2 protein. J Virol Methods. 2001;93(1–2):49–56.

    CAS  PubMed  Google Scholar 

  144. Voigt H, Merant C, Wienhold D, Braun A, Hutet E, Le Potier MF, et al. Efficient priming against classical swine fever with a safe glycoprotein E2 expressing Orf virus recombinant (ORFV VrV-E2). Vaccine. 2007;25(31):5915–26.

    CAS  PubMed  Google Scholar 

  145. Widjojoatmodjo MN, van Gennip HG, Bouma A, van Rijn PA, Moormann RJ. Classical swine fever virus E(rns) deletion mutants: trans-complementation and potential use as nontransmissible, modified, live-attenuated marker vaccines. J Virol. 2000;74(7):2973–80.

    CAS  PubMed Central  PubMed  Google Scholar 

  146. van Gennip HG, Bouma A, van Rijn PA, Widjojoatmodjo MN, Moormann RJ. Experimental non-transmissible marker vaccines for classical swine fever (CSF) by trans-complementation of E(rns) or E2 of CSFV. Vaccine. 2002;20(11–12):1544–56.

    PubMed  Google Scholar 

  147. Maurer R, Stettler P, Ruggli N, Hofmann MA, Tratschin JD. Oronasal vaccination with classical swine fever virus (CSFV) replicon particles with either partial or complete deletion of the E2 gene induces partial protection against lethal challenge with highly virulent CSFV. Vaccine. 2005;23(25):3318–28.

    CAS  PubMed  Google Scholar 

  148. Frey CF, Bauhofer O, Ruggli N, Summerfield A, Hofmann MA, Tratschin JD. Classical swine fever virus replicon particles lacking the Erns gene: a potential marker vaccine for intradermal application. Vet Res. 2006;37(5):655–70.

    CAS  PubMed  Google Scholar 

  149. Reimann I, Depner K, Trapp S, Beer M. An avirulent chimeric Pestivirus with altered cell tropism protects pigs against lethal infection with classical swine fever virus. Virology. 2004;322(1):143–57.

    CAS  PubMed  Google Scholar 

  150. Konig P, Blome S, Gabriel C, Reimann I, Beer M. Innocuousness and safety of classical swine fever marker vaccine candidate CP7_E2alf in non-target and target species. Vaccine. 2011;30(1):5–8.

    PubMed  Google Scholar 

  151. Risatti GR, Holinka LG, Lu Z, Kutish GF, Tulman ER, French RA, et al. Mutation of E1 glycoprotein of classical swine fever virus affects viral virulence in swine. Virology. 2005;343(1):116–27.

    CAS  PubMed  Google Scholar 

  152. Risatti GR, Holinka LG, Carrillo C, Kutish GF, Lu Z, Tulman ER, et al. Identification of a novel virulence determinant within the E2 structural glycoprotein of classical swine fever virus. Virology. 2006;355(1):94–101.

    CAS  PubMed  Google Scholar 

  153. Holinka LG, Fernandez-Sainz I, O’Donnell V, Prarat MV, Gladue DP, Lu Z, et al. Development of a live attenuated antigenic marker classical swine fever vaccine. Virology. 2009;384(1):106–13.

    CAS  PubMed  Google Scholar 

  154. Cooke BD. Rabbit haemorrhagic disease: field epidemiology and the management of wild rabbit populations. Rev Sci Tech. 2002;21:347–58.

    CAS  PubMed  Google Scholar 

  155. Capucci L, Scicluna MT, Lavazza A. Diagnosis of viral haemorrhagic disease of rabbits and the European brown hare syndrome. Rev Sci Tech. 1991;10:347–70.

    CAS  PubMed  Google Scholar 

  156. Green KY, Ando T, Balayan MS, Berke T, Clarke IN, Estes MK, et al. Taxonomy of the caliciviruses. J Infect Dis. 2000;181 Suppl 2:S322–30.

    PubMed  Google Scholar 

  157. Meyers G, Wirblich C, Thiel HJ. Genomic and subgenomic RNAs of rabbit haemorrhagic disease virus are both protein-linked and packaged into particles. Virology. 1991;184:677–86.

    CAS  PubMed  Google Scholar 

  158. Meyers G, Wirblich C, Thiel HJ. Rabbit haemorrhagic disease virus—molecular cloning and nucleotide sequencing of a Calicivirus genome. Virology. 1991;184:664–76.

    CAS  PubMed  Google Scholar 

  159. Wirblich C, Meyers G, Ohlinger VF, Capucci L, Eskens U, Haas B, et al. European brown hare syndrome virus: relationship to rabbit hemorrhagic disease virus and other caliciviruses. J Virol. 1994;68:5164–73.

    CAS  PubMed Central  PubMed  Google Scholar 

  160. Meyers G, Wirblich C, Thiel HJ, Thumfart JO. Rabbit hemorrhagic disease virus: genome organization and polyprotein processing of a Calicivirus studied after transient expression of DNA constructs. Virology. 2000;276:349–63.

    CAS  PubMed  Google Scholar 

  161. Le Gall Reculé G, Zwinglestein F, Fages MP, Bertagnoli S, Gelfi J, Aubineau J, et al. Characterisation of a non-pathogenic and non-protective infectious rabbit lagovirus related to RHDV. Virology. 2011;410:395–402.

    PubMed  Google Scholar 

  162. Capucci L, Fusi P, Lavazza A, Pacciarini ML, Rossi C. Detection and preliminary characterization of a new calicivirus related to rabbit haemorrhagic disease virus but non pathogenic. J Virol. 1996;70:8614–23.

    CAS  PubMed Central  PubMed  Google Scholar 

  163. Forrester NL, Trout RC, Gould EA. Benign circulation of rabbit haemorrhagic disease virus on Lambay Island, Eire. Virology. 2007;358:18–22.

    CAS  PubMed  Google Scholar 

  164. Strive T, Wright JD, Robinson AJ. Identification and partial characterisation of a new lagovirus in Australian wild rabbits. Virology. 2009;384:97–105.

    CAS  PubMed  Google Scholar 

  165. Strive T, Wright J, Kovaliski J, Botti G, Capucci L. The non-pathogenic Australian lagovirus RCV-A1 causes a prolonged infection and elicits partial cross-protection to rabbit haemorrhagic disease virus. Virology. 2010;398:125–34.

    CAS  PubMed  Google Scholar 

  166. Hoehn M, Kerr PJ, Strive T. In situ hybridisation assay for localisation of rabbit calicivirus Australia-1 (RCV-A1) in European rabbit (Oryctolagus cuniculus) tissues. J Virol Methods. 2013;188:148–52.

    CAS  PubMed  Google Scholar 

  167. Kerr PJ, Kitchen A, Holmes EC. Origin and phylodynamics of rabbit hemorrhagic disease virus. J Virol. 2009;83:12129–38.

    CAS  PubMed Central  PubMed  Google Scholar 

  168. Forrester NL, Trout RC, Turner SL, Kelly D, Boag B, Moss S, et al. Unravelling the paradox of rabbit haemorrhagic disease virus emergence, using phylogenetic analysis; possible implications for rabbit conservation strategies. Biol Conserv. 2006;131:296–306.

    Google Scholar 

  169. Kinnear M, Linde CC. Capsid gene divergence in rabbit hemorrhagic disease virus. J Gen Virol. 2010;91:174–81.

    CAS  PubMed  Google Scholar 

  170. Bergin IL, Wise AG, Bolin SR, Mullaney TP, Kiupel M, Maes RK. Novel calicivirus identified in rabbits, Michigan, USA. Emerg Infect Dis. 2009;15:1955–62.

    CAS  PubMed Central  PubMed  Google Scholar 

  171. Le Gall RG, Zwinglestein F, Boucher S, Le Normand B, Plassiart G, Portejoie Y, et al. Detection of a new variant of rabbit haemorrhagic disease virus in France. Vet Rec. 2011;168:137–8.

    Google Scholar 

  172. Dalton KP, Nicieza I, Balseiro A, Muguerza MA, Rossell JM, Casais R, et al. Variant rabbit haemorrhagic disease virus in young rabbits in Spain. Emerg Infect Dis. 2012;18:2009–12.

    PubMed Central  PubMed  Google Scholar 

  173. Frölich K, Kujawski OE, Rudolph M, Ronsholt L, Speck S. European brown hare syndrome virus in free-ranging European brown hares from Argentina. J Wildl Dis. 2003;39:121–4.

    PubMed  Google Scholar 

  174. McIntosh MT, Behan SC, Mohamed FW, Lu Z, Moran KE, Burrage TG, et al. A pandemic strain of calicivirus threatens rabbit industries in the Americas. Virol J. 2007;4:96.

    PubMed Central  PubMed  Google Scholar 

  175. Farnos O, Rodrıguez D, Valdes O, Chiong M, Parra F, Toledo JR, et al. Molecular and antigenic characterization of rabbit hemorrhagic disease virus isolated in Cuba indicates a distinct antigenic subtype. Arch Virol. 2007;152:1215–21.

    CAS  PubMed  Google Scholar 

  176. Villafuerte R, Calvete C, Blanco JC, Lucientes J. Incidence of viral haemorrhagic disease in wild rabbit populations in Spain. Mammalia. 1995;59:651–9.

    Google Scholar 

  177. Delibes-Mateos M, Delibes M, Ferreras P, Villafuerte R. Key role of European rabbits in the conservation of the Western Mediterranean basin hotspot. Conserv Biol. 2008;22:1106–17.

    PubMed  Google Scholar 

  178. Cooke BD, Fenner F. Rabbit haemorrhagic disease and the biological control of wild rabbits, Oryctolagus cuniculus, in Australia and New Zealand. Wildl Res. 2002;29:689–706.

    Google Scholar 

  179. Cooke BD. Rabbits: manageable environmental pests or participants in new Australian ecosystems? Wildl Res. 2012;39:279–89.

    Google Scholar 

  180. Cooke BD, Chudleigh P, Simpson S, Saunders G. The economic benefits of the biological control of rabbits in Australia, 1950–2011. Aust Econ Hist Rev. 2013;53:1–17.

    Google Scholar 

  181. Kerr PJ. Myxomatosis in Australia and Europe: a model for emerging infectious diseases. Antiviral Res. 2012;93:387–415.

    CAS  PubMed  Google Scholar 

  182. Elsworth PG, Kovaliski J, Cooke BD. Rabbit haemorrhagic disease: are Australian rabbits (Oryctolagus cuniculus) evolving resistance to infection with Czech CAPM 351 RHDV? Epidemiol Infect. 2012;140:1972–81.

    CAS  PubMed  Google Scholar 

  183. Nystrom K, Le Gall Reculé G, Grassi P, Abrantes J, Ruvoën-Clouet N, Le Moullac-Vaidye B, et al. Histo-blood group antigens act as attachment factors of rabbit hemorrhagic disease virus infection in a virus strain-dependent manner. PLoS Pathog. 2011;7:e1002188.

    CAS  PubMed Central  PubMed  Google Scholar 

  184. Gregg DA, House C, Meyer R, Berninger M. Viral haemorrhagic disease of rabbits in Mexico: epidemiology and viral characterization. Rev Sci Tech. 1991;10:435–51.

    CAS  PubMed  Google Scholar 

  185. Gavier-Widén D, Mörner T. Descriptive epizootilogical study of European brown hare syndrome in Sweden. J Wildl Dis. 1993;29:15–20.

    PubMed  Google Scholar 

  186. Puggioni G, Cavadini P, Maestrale C, Scivoli R, Botti G, Ligios C, et al. The new French 2010 rabbit hemorrhagic disease virus causes an RHD-like disease in the Sardinian Cape hare (Lepus capensis mediterraneus). Vet Res. 2013;44(1):96.

    PubMed Central  PubMed  Google Scholar 

  187. McColl KA, Merchant JC, Hardy J, Cooke BD, Robinson A, Westbury HA. Evidence for insect transmission of rabbit haemorrhagic disease virus. Epidemiol Infect. 2002;129:655–33.

    CAS  PubMed Central  PubMed  Google Scholar 

  188. Asgari S, Hardy JRE, Sinclair RG, Cooke BD. Field evidence for mechanical transmission of rabbit haemorrhagic disease virus (RHDV) by flies (Diptera: Calliphoridae) among wild rabbits in Australia. Virus Res. 1998;54:123–32.

    CAS  PubMed  Google Scholar 

  189. Lenghaus C, Westbury H, Collins B, Ratnamohan N, Morrissy C. Overview of the RHD project in the Australian Animal Health Laboratory. In: Munro RK, Williams RT, editors. Rabbit haemorrhagic disease: issues in assessment for biological control. Canberra: Bureau of Resource Sciences; 1994. p. 104–29.

    Google Scholar 

  190. Henning J, Meers J, Davies PR, Morris RS. Survival of rabbit haemorrhagic disease virus (RHDV) in the environment. Epidemiol Infect. 2005;133:719–30.

    CAS  PubMed Central  PubMed  Google Scholar 

  191. White PJ, Norman RA, Hudson PJ. Epidemiological consequences of a pathogen having both virulent and avirulent modes of transmission: the case of rabbit haemorrhagic disease virus. Epidemiol Infect. 2002;129:665–77.

    CAS  PubMed Central  PubMed  Google Scholar 

  192. White PJ, Trout RC, Moss SR, Desai A, Armesto M, Forrester NL, et al. Epidemiology of rabbit haemorrhagic disease virus in the United Kingdom: evidence for seasonal transmission by both virulent and avirulent modes of infection. Epidemiol Infect. 2004;132:555–67.

    CAS  PubMed Central  PubMed  Google Scholar 

  193. Gall A, Hoffmann B, Teifke JP, Lange B, Schirrmeier H. Persistence of viral RNA in rabbits which overcome an experimental RHDV infection detected by a highly sensitive multiplex real-time RT-PCR. Vet Microbiol. 2007;120:17–32.

    CAS  PubMed  Google Scholar 

  194. Shien JH, Shieh HK, Lee LH. Experimental infections of rabbits with rabbit haemorrhagic disease virus monitored by polymerase chain reaction. Res Vet Sci. 2000;68:255–9.

    CAS  PubMed  Google Scholar 

  195. Kovaliski J, Sinclair R, Mutze G, Peacock D, Strive T, Abrantes J, et al. Molecular epidemiology of rabbit haemorrhagic disease virus in Australia: when one became many. Mol Ecol. 2013;23:408–20.

    Google Scholar 

  196. Ruvoën-Clouet N, Ganière JP, André-Fontaine G, Blanchard D, Le Pendu J. Binding of rabbit haemorrhagic disease virus to antigens of the ABH histo-blood group family. J Virol. 2000;74:11950–4.

    PubMed Central  PubMed  Google Scholar 

  197. Wang X, Xu F, Liu J, Gao B, Liu Y, Zhai Y, et al. Atomic model of rabbit hemorrhagic disease virus by cryo-electron microscopy and crystallography. PLoS Pathog. 2013;9:e1003132.

    CAS  PubMed Central  PubMed  Google Scholar 

  198. Mikami O, Park JH, Kimura T, Ochial K, Itakura C. Hepatic lesions in young rabbits experimentally infected with rabbit haemorrhagic disease virus. Res Vet Sci. 1999;66:237–42.

    CAS  PubMed  Google Scholar 

  199. Ferreira PG, Costa-E-Silva A, Oliveira MJR, Monteiro E, Cunha EM, Águas AP. Severe leukopenia and liver biochemistry changes in adult rabbits after calicivirus infection. Res Vet Sci. 2006;80:218–25.

    CAS  PubMed  Google Scholar 

  200. Gelmetti D, Grieco V, Rossi C, Capucci L, Lavazza A. Detection of rabbit haemorrhagic disease virus (RHDV) by in situ hybridisation with a digoxigenin labelled RNA probe. J Virol Methods. 1998;72:219–26.

    CAS  PubMed  Google Scholar 

  201. Prieto JM, Fernandez F, Alvarez V, Espi A, García-Marín JF, Alvarez M, et al. Immunohistochemical localisation of rabbit haemorrhagic disease virus VP-60 antigen in early infection of young and adult rabbits. Res Vet Sci. 2000;68:181–7.

    CAS  PubMed  Google Scholar 

  202. Fuchs A, Weissenböck H. Comparative histopathological study of rabbit haemorrhagic disease (RHD) and European brown hare syndrome (EBHS). J Comp Pathol. 1992;107:103–13.

    CAS  PubMed  Google Scholar 

  203. Tuñón MJ, Sanchez-Campos S, Garcia-Ferreras J, Álvarez M, Jorquera F, Gonzalez-Gallego J. Rabbit hemorrhagic viral disease: characterization of a new animal model of fulminant liver failure. J Lab Clin Med. 2003;141:272–8.

    PubMed  Google Scholar 

  204. Kimura T, Mitsui I, Okada Y, Furuya T, Ochiai K, Umemura T, et al. Distribution of rabbit haemorrhagic disease virus RNA in experimentally infected rabbits. J Comp Pathol. 2001;124:134–41.

    CAS  PubMed  Google Scholar 

  205. Chen S-Y, Chou C-C, Liu C-I, Shien J-H. Impairment of renal function and electrolyte balance in rabbit haemorrhagic disease. J Vet Med Sci. 2008;70:951–8.

    PubMed  Google Scholar 

  206. Teifke JP, Reimann I, Schirrmeier H. Subacute liver necrosis after experimental infection with rabbit haemorrhagic disease virus (RHDV). J Comp Pathol. 2002;126:231–4.

    CAS  PubMed  Google Scholar 

  207. Robinson AJ, So PTM, Muller WJ, Cooke BD, Capucci L. Statistical models for the effect of age and maternal antibodies on the development of rabbit haemorrhagic disease in Australian wild rabbits. Wildl Res. 2002;29:663–71.

    Google Scholar 

  208. Chen S-Y, Shien J-H, H-K OOI. Hyperlipidemia in rabbit hemorrhagic disease. Exp Anim. 2008;57:479–83.

    CAS  PubMed  Google Scholar 

  209. Cooke BD, Robinson AJ, Merchant JC, Nardin A, Capucci L. Use of ELISAs in field studies of rabbit haemorrhagic disease (RHD) in Australia. Epidemiol Infect. 2000;124:563–76.

    CAS  PubMed Central  PubMed  Google Scholar 

  210. Robinson AJ, Kirkland PD, Forrester RI, Capucci L, Cooke BD, Philbey AW. Serological evidence for the presence of a calicivirus in Australian wild rabbits, Oryctolagus cuniculus, before the introduction of rabbit haemorrhagic disease virus (RHDV): its potential influence on the specificity of a competitive ELISA for RHDV. Wildl Res. 2002;29:655–2.

    Google Scholar 

  211. Liu J, Kerr PJ, Strive T. A sensitive and specific blocking ELISA for the detection of rabbit calicivirus RCV-A1 antibodies. Virol J. 2012;9:182.

    PubMed Central  PubMed  Google Scholar 

  212. Liu J, Kerr PJ, Wright JD, Strive T. Serological assays to discriminate rabbit haemorrhagic disease virus from Australian non-pathogenic rabbit calicivirus. Vet Microbiol. 2012;157:345–54.

    PubMed  Google Scholar 

  213. Capucci L, Fallacara F, Grazioli S, Lavazza A, Pacciarini ML, Brocchi E. A further step in the evolution of rabbit hemorrhagic disease virus: the appearance of the first consistent antigenic variant. Virus Res. 1998;58:115–26.

    CAS  PubMed  Google Scholar 

  214. Schirrmeier H, Reimann I, Köllner B, Granzow H. Pathogenic, antigenic and molecular properties of rabbit haemorrhagic disease virus (RHDV) isolated from vaccinated rabbits: detection and characterization of antigenic variants. Arch Virol. 1999;144:719–35.

    CAS  PubMed  Google Scholar 

  215. Le Gall-Recule G, Lavazza A, Marchandeau S, Bertagnoli S, Zwingelstein F, Cavadini P, et al. Emergence of a new lagovirus related to rabbit haemorrhagic disease virus. Vet Res. 2013;44(1):81.

    PubMed Central  PubMed  Google Scholar 

  216. Wang X, Hao H, Qiu L, Dang R, Du E, Zhang S, et al. Phylogenetic analysis of rabbit haemorrhagic disease virus in China and the antigenic variation of new strains. Arch Virol. 2012;157:1523–30.

    CAS  PubMed  Google Scholar 

  217. Angulo E, Bárcena J. Towards a unique and transmissible vaccine against myxomatosis and rabbit haemorrhagic disease for rabbit populations. Wildl Res. 2007;34:567–77.

    CAS  Google Scholar 

  218. Abrantes J, van der Loo W, Le Pendu J, Esteves PJ. Rabbit haemorrhagic disease (RHD) and rabbit haemorrhagic disease virus (RHDV): a review. Vet Res. 2012;43:12.

    PubMed Central  PubMed  Google Scholar 

  219. Mutze G, Sinclair R, Peacock D, Kovaliski J, Capucci L. Does a benign calicivirus reduce the effectiveness of rabbit haemorrhagic disease virus (RHDV) in Australia? Experimental evidence from field releases of RHDV on bait. Wildl Res. 2010;37:311–9.

    Google Scholar 

  220. Matson DO. Release of RHD virus in Australia. Science. 1996;273:16–7.

    CAS  PubMed  Google Scholar 

  221. Smith AW. Release of RHD virus in Australia. Science. 1996;273:17–8.

    CAS  PubMed  Google Scholar 

  222. Snijder EJ, Meulenberg J. The molecular biology of arteriviruses. J Gen Virol. 1998;79(5):961–79.

    CAS  PubMed  Google Scholar 

  223. Lauck M, Hyeroba D, Tumukunde A, Weny G, Lank SM, Chapman CA, et al. Novel, divergent simian hemorrhagic fever viruses in a wild Ugandan red colobus monkey discovered using direct pyrosequencing. PLoS One. 2011;6(4):e19056.

    CAS  PubMed Central  PubMed  Google Scholar 

  224. Tauraso NM, Shelokov A, Palmer AE, Allen AM. Simian hemorrhagic fever. III. Isolation and characterization of a viral agent. Am J Trop Med Hyg. 1968;17(3):422–31.

    CAS  PubMed  Google Scholar 

  225. Allen AM, Palmer AE, Tauraso NM, Shelokov A. Simian hemorrhagic fever. II. Studies in pathology. Am J Trop Med Hyg. 1968;17(3):413–21.

    CAS  PubMed  Google Scholar 

  226. Palmer AE, Allen AM, Tauraso NM, Shelokov A. Simian hemorrhagic fever. I. Clinical and epizootiologic aspects of an outbreak among quarantined monkeys. Am J Trop Med Hyg. 1968;17(3):404–12.

    CAS  PubMed  Google Scholar 

  227. Lauck M, Sibley SD, Hyeroba D, Tumukunde A, Weny G, Chapman CA, et al. Exceptional simian hemorrhagic fever virus diversity in a wild African primate community. J Virol. 2013;87(1):688–91.

    CAS  PubMed Central  PubMed  Google Scholar 

  228. Lapin B, Shevtsova Z. On the identity of two simian hemorrhagic fever virus strains (Sukhumi and NIH). Zeitschrift fur Versuchstierkunde. 1970;13(1):21–3.

    Google Scholar 

  229. Shevtsova Z, Krylova R. A comparative study of 2 strains of simian hemorrhagic fever virus]. Vopr Virusol. 1971;16(6):686.

    CAS  PubMed  Google Scholar 

  230. Tauraso NM, Shelokov A, Allen AM, Palmer AE, Aulisio CG. Epizootic of simian haemorrhagic fever. Nature. 1968;218:876–7.

    Google Scholar 

  231. Gravell M, London W, Leon M, Palmer A, Hamilton R, editors. Differences among isolates of simian hemorrhagic fever (SHF) virus. Proc Soc Exp Biol Med. 1986;181(1):112–9.

    Google Scholar 

  232. London WT. Epizootiology, transmission and approach to prevention of fatal simian haemorrhagic fever in rhesus monkeys. 1977;268(5618):344–5.

    Google Scholar 

  233. Renquist D. Outbreak of simian hemorrhagic fever. J Med Primatol. 1989;19(1):77–9.

    Google Scholar 

  234. Dalgard DW, Hardy RJ, Pearson SL, Pucak GJ, Quander RV, Zack PM, et al. Combined simian hemorrhagic fever and Ebola virus infection in cynomolgus monkeys. Lab Anim Sci. 1992;42(2):152–7.

    CAS  PubMed  Google Scholar 

  235. Plagemann PG, Moennig V. Lactate dehydrogenase-elevating virus, equine arteritis virus, and simian hemorrhagic fever virus: a new group of positive-strand RNA viruses. Adv Virus Res. 1992;41:99–192.

    CAS  PubMed  Google Scholar 

  236. Godeny E, De Vries A, Wang X, Smith S, De Groot R. Identification of the leader-body junctions for the viral subgenomic mRNAs and organization of the simian hemorrhagic fever virus genome: evidence for gene duplication during arterivirus evolution. J Virol. 1998;72(1):862–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  237. Gravell M, London WT, Leon ME, Palmer AE, Hamilton RS. Differences among isolates of simian hemorrhagic fever (SHF) virus. Proc Soc Exp Biol Med. 1986;181(1):112–9.

    CAS  PubMed  Google Scholar 

  238. Gravell M, London WT, Rodriguez M, Palmer AE, Hamilton RS. Simian haemorrhagic fever (SHF): new virus isolate from a chronically infected patas monkey. J Gen Virol. 1980;51(Pt 1):99–106.

    CAS  PubMed  Google Scholar 

  239. Johnson RF, Dodd LE, Yellayi S, Gu W, Cann JA, Jett C, et al. Simian hemorrhagic fever virus infection of rhesus macaques as a model of viral hemorrhagic fever: clinical characterization and risk factors for severe disease. Virology. 2011;421(2):129–40.

    CAS  PubMed Central  PubMed  Google Scholar 

  240. Pedersen NC, Elliott JB, Glasgow A, Poland A, Keel K. An isolated epizootic of hemorrhagic-like fever in cats caused by a novel and highly virulent strain of feline calicivirus. Vet Microbiol. 2000;73(4):281–300.

    CAS  PubMed  Google Scholar 

  241. Pesavento PA, MacLachlan NJ, Dillard-Telm L, Grant CK, Hurley KF. Pathologic, immunohistochemical, and electron microscopic findings in naturally occurring virulent systemic feline calicivirus infection in cats. Vet Pathol. 2004;41(3):257–63.

    CAS  PubMed  Google Scholar 

  242. Pesavento PA, Stokol T, Liu H, van der List DA, Gaffney PM, Parker JS. Distribution of the feline calicivirus receptor junctional adhesion molecule a in feline tissues. Vet Pathol. 2011;48(2):361–8.

    CAS  PubMed  Google Scholar 

  243. United States Animal Health Association. Foreign animal diseases. 7th ed. Boca Raton, FL: Boca Publications Group, Inc.; 2008.

    Google Scholar 

  244. Monath TP. Treatment of yellow fever. Antiviral Res. 2008;78(1):116–24.

    CAS  PubMed  Google Scholar 

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Acknowledgments

The authors have no conflict of interests. We thank Laura Bollinger (IRF-Frederick) for technical writing services. The content of this publication does not necessarily reflect the views or policies of the US Department of Health and Human Services, the US Department of Agriculture and/or of the institutions and companies affiliated with the authors. JHK performed this work as an employee of Tunnell Government Services, Inc., a subcontractor to Battelle Memorial Institute under its prime contract with NIAID, under Contract No. HHSN272200700016I.

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Correspondence to David White D.V.M., Ph.D., D.A.C.V.M. .

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Van Campen, H. et al. (2015). Viral Hemorrhagic Fevers of Animals Caused by Positive-Stranded RNA Viruses. In: Shapshak, P., Sinnott, J., Somboonwit, C., Kuhn, J. (eds) Global Virology I - Identifying and Investigating Viral Diseases. Springer, New York, NY. https://doi.org/10.1007/978-1-4939-2410-3_14

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