Skip to main content

Viral Hemorrhagic Fevers of Animals Caused by Double-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 will focus on double-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.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Maclachlan NJ, Guthrie AJ. Re-emergence of bluetongue, African horse sickness, and other orbivirus diseases. Vet Res. 2010;41(6):35.

    Article  PubMed Central  PubMed  Google Scholar 

  2. Mellor PS, Boorman J. The transmission and geographical spread of African horse sickness and bluetongue viruses. Ann Trop Med Parasitol. 1995;89(1):1–15.

    CAS  PubMed  Google Scholar 

  3. Rodriguez M, Hooghuis H, Castano M. African horse sickness in Spain. Vet Microbiol. 1992;33(1–4):129–42.

    Article  CAS  PubMed  Google Scholar 

  4. House JA. African horse sickness. Vet Clin North Am Equine Pract. 1993;9(2):355–64.

    CAS  PubMed  Google Scholar 

  5. Jupp PG, McIntosh BM, Nevill EM. A survey of the mosquito and Culicoides faunas at two localities in the Karoo region of South Africa with some observations of bionomics. Onderstepoort J Vet Res. 1980;47(1):1–6.

    CAS  PubMed  Google Scholar 

  6. Hopley R, Toth B. Focus on: African horse sickness. Vet Rec. 2013;173(1):13–4.

    Article  PubMed  Google Scholar 

  7. Thompson GM, Jess S, Murchie AK. A review of African horse sickness and its implications for Ireland. Ir Vet J. 2012;65(1):9.

    Article  PubMed Central  PubMed  Google Scholar 

  8. Guthrie AJ. African horse sickness. In: Sellon DC, Long MT, editors. Equine infectious diseases. St. Louis, MO: Saunders Elsevier; 2007. p. 164–71.

    Chapter  Google Scholar 

  9. Mellor PS, Hamblin C. African horse sickness. Vet Res. 2004;35(4):445–66.

    Article  PubMed  Google Scholar 

  10. Binepal VS, Wariru BN, Davies FG, Soi R, Olubayo R. An attempt to define the host range for African horse sickness virus (Orbivirus, Reoviridae) in east Africa, by a serological survey in some Equidae, Camelidae, Loxodontidae and Carnivore. Vet Microbiol. 1992;31(1):19–23.

    Article  CAS  PubMed  Google Scholar 

  11. Alexander KA, Kat PW, House J, House C, O'Brien SJ, Laurenson MK, et al. African horse sickness and African carnivores. Vet Microbiol. 1995;47(1–2):133–40.

    Article  CAS  PubMed  Google Scholar 

  12. Laegreid WW, Burrage TG, Stone-Marschat M, Skowronek A. Electron microscopic evidence for endothelial infection by African horsesickness virus. Vet Pathol. 1992;29(6):554–6.

    Article  CAS  PubMed  Google Scholar 

  13. von Teichman BF, Dungu B, Smit TK. In vivo cross-protection to African horse sickness Serotypes 5 and 9 after vaccination with serotypes 8 and 6. Vaccine. 2010;28(39):6505–17.

    Article  Google Scholar 

  14. Laegreid WW, Skowronek A, Stone-Marschat M, Burrage T. Characterization of virulence variants of African horsesickness virus. Virology. 1993;195(2):836–9.

    Article  CAS  PubMed  Google Scholar 

  15. Skowronek AJ, LaFranco L, Stone-Marschat MA, Burrage TG, Rebar AH, Laegreid WW. Clinical pathology and hemostatic abnormalities in experimental African horsesickness. Vet Pathol. 1995;32(2):112–21.

    Article  CAS  PubMed  Google Scholar 

  16. Brown CC, Meyer RF, Grubman MJ. Presence of African horse sickness virus in equine tissues, as determined by in situ hybridization. Vet Pathol. 1994;31(6):689–94.

    Article  CAS  PubMed  Google Scholar 

  17. Burrage TG, Laegreid WW. African horsesickness: pathogenesis and immunity. Comp Immunol Microbiol Infect Dis. 1994;17(3–4):275–85.

    Article  CAS  PubMed  Google Scholar 

  18. Castillo-Olivares J, Calvo-Pinilla E, Casanova I, Bachanek-Bankowska K, Chiam R, Maan S, et al. A modified vaccinia Ankara virus (MVA) vaccine expressing African horse sickness virus (AHSV) VP2 protects against AHSV challenge in an IFNAR −/− mouse model. PLoS One. 2011;6(1):e16503.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. El Garch H, Crafford JE, Amouyal P, Durand PY, Edlund Toulemonde C, Lemaitre L, et al. An African horse sickness virus serotype 4 recombinant canarypox virus vaccine elicits specific cell-mediated immune responses in horses. Vet Immunol Immunopathol. 2012;149(1–2):76–85.

    Article  PubMed  Google Scholar 

  20. Purse BV, Brown HE, Harrup L, Mertens PP, Rogers DJ. Invasion of bluetongue and other orbivirus infections into Europe: the role of biological and climatic processes. Rev Sci Tech. 2008;27(2):427–42.

    CAS  PubMed  Google Scholar 

  21. Coetzee P, Van Vuuren M, Stokstad M, Myrmel M, Venter EH. Bluetongue virus genetic and phenotypic diversity: towards identifying the molecular determinants that influence virulence and transmission potential. Vet Microbiol. 2012;161(1–2):1–12.

    Article  CAS  PubMed  Google Scholar 

  22. Bonneau KR, Mullens BA, MacLachlan NJ. Occurrence of genetic drift and founder effect during quasispecies evolution of the VP2 and NS3/NS3A genes of bluetongue virus upon passage between sheep, cattle, and Culicoides sonorensis. J Virol. 2001;75(17):8298–305.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Samal SK, el-Hussein A, Holbrook FR, Beaty BJ, Ramig RF. Mixed infection of Culicoides variipennis with bluetongue virus serotypes 10 and 17: evidence for high frequency reassortment in the vector. J Gen Virol. 1987;68(Pt 9):2319–29.

    Article  CAS  PubMed  Google Scholar 

  24. Samal SK, Livingston Jr CW, McConnell S, Ramig RF. Analysis of mixed infection of sheep with bluetongue virus serotypes 10 and 17: evidence for genetic reassortment in the vertebrate host. J Virol. 1987;61(4):1086–91.

    CAS  PubMed Central  PubMed  Google Scholar 

  25. Savini G, Afonso A, Mellor P, Aradaib I, Yadin H, Sanaa M, et al. Epizootic heamorragic disease. Res Vet Sci. 2011;91(1):1–17.

    Article  CAS  PubMed  Google Scholar 

  26. Schudel A, Wilson D, Pearson JE. Office international des epizooties international standards for bluetongue. Vet Ital. 2004;40(4):676–81.

    CAS  PubMed  Google Scholar 

  27. Tabachnick WJ. Culicoides variipennis and bluetongue-virus epidemiology in the United States. Annu Rev Entomol. 1996;41:23–43.

    Article  CAS  PubMed  Google Scholar 

  28. Maclachlan NJ. Bluetongue: history, global epidemiology, and pathogenesis. Prev Vet Med. 2011;102(2):107–11.

    Article  PubMed  Google Scholar 

  29. Gibbs EP, Greiner EC. The epidemiology of bluetongue. Comp Immunol Microbiol Infect Dis. 1994;17(3–4):207–20.

    Article  CAS  PubMed  Google Scholar 

  30. Tabachnick WJ. Culicoides and the global epidemiology of bluetongue virus infection. Vet Ital. 2004;40(3):144–50.

    CAS  PubMed  Google Scholar 

  31. Verwoerd DW, Erasmus BJ, editors. Bluetongue. 2nd ed. Cape Town, South Africa: Oxford Press; 2004.

    Google Scholar 

  32. Schwartz-Cornil I, Mertens PP, Contreras V, Hemati B, Pascale F, Breard E, et al. Bluetongue virus: virology, pathogenesis and immunity. Vet Res. 2008;39(5):46.

    Article  PubMed  Google Scholar 

  33. DeMaula CD, Leutenegger CM, Bonneau KR, MacLachlan NJ. The role of endothelial cell-derived inflammatory and vasoactive mediators in the pathogenesis of bluetongue. Virology. 2002;296(2):330–7.

    Article  CAS  PubMed  Google Scholar 

  34. Drew CP, Gardner IA, Mayo CE, Matsuo E, Roy P, MacLachlan NJ. Bluetongue virus infection alters the impedance of monolayers of bovine endothelial cells as a result of cell death. Vet Immunol Immunopathol. 2010;136(1–2):108–15.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Letchworth GJ, Appleton JA. Passive protection of mice and sheep against bluetongue virus by a neutralizing monoclonal antibody. Infect Immun. 1983;39(1):208–12.

    PubMed Central  PubMed  Google Scholar 

  36. Barratt-Boyes SM, MacLachlan NJ. Dynamics of viral spread in bluetongue virus infected calves. Vet Microbiol. 1994;40(3–4):361–71.

    Article  CAS  PubMed  Google Scholar 

  37. Thorne ET, Williams ES, Spraker TR, Helms W, Segerstrom T. Bluetongue in free-ranging pronghorn antelope (Antilocapra americana) in Wyoming: 1976 and 1984. J Wildl Dis. 1988;24(1):113–9.

    Article  CAS  PubMed  Google Scholar 

  38. Beringer J, Hansen LP, Stallknecht DE. An epizootic of hemorrhagic disease in white-tailed deer in Missouri. J Wildl Dis. 2000;36(3):588–91.

    Article  CAS  PubMed  Google Scholar 

  39. Dal Pozzo F, Saegerman C, Thiry E. Bovine infection with bluetongue virus with special emphasis on European serotype 8. Vet J. 2009;182(2):142–51.

    Article  PubMed  Google Scholar 

  40. Osburn BI. The impact of bluetongue virus on reproduction. Comp Immunol Microbiol Infect Dis. 1994;17(3–4):189–96.

    Article  CAS  PubMed  Google Scholar 

  41. Wouda W, Peperkamp NH, Roumen MP, Muskens J, van Rijn A, Vellema P. Epizootic congenital hydranencephaly and abortion in cattle due to bluetongue virus serotype 8 in the Netherlands. Tijdschr Diergeneeskd. 2009;134(10):422–7.

    CAS  PubMed  Google Scholar 

  42. Baldet T, Delecolle JC, Cetre-Sossah C, Mathieu B, Meiswinkel R, Gerbier G. Indoor activity of Culicoides associated with livestock in the bluetongue virus (BTV) affected region of northern France during autumn 2006. Prev Vet Med. 2008;87(1–2):84–97.

    Article  CAS  PubMed  Google Scholar 

  43. White DM, Wilson WC, Blair CD, Beaty BJ. Studies on overwintering of bluetongue viruses in insects. J Gen Virol. 2005;86(Pt 2):453–62.

    Article  CAS  PubMed  Google Scholar 

  44. Bonneau KR, DeMaula CD, Mullens BA, MacLachlan NJ. Duration of viraemia infectious to Culicoides sonorensis in bluetongue virus-infected cattle and sheep. Vet Microbiol. 2002;88(2):115–25.

    Article  CAS  PubMed  Google Scholar 

  45. Niedbalski W. Bluetongue vaccines in Europe. Pol J Vet Sci. 2011;14(2):299–304.

    CAS  PubMed  Google Scholar 

  46. MacLachlan NJ, Conley AJ, Kennedy PC. Bluetongue and equine viral arteritis viruses as models of virus-induced fetal injury and abortion. Anim Reprod Sci. 2000;60–61:643–51.

    Article  PubMed  Google Scholar 

  47. Batten CA, Maan S, Shaw AE, Maan NS, Mertens PP. A European field strain of bluetongue virus derived from two parental vaccine strains by genome segment reassortment. Virus Res. 2008;137(1):56–63.

    Article  CAS  PubMed  Google Scholar 

  48. Roy P, Boyce M, Noad R. Prospects for improved bluetongue vaccines. Nat Rev Microbiol. 2009;7(2):120–8.

    Article  CAS  PubMed  Google Scholar 

  49. Inaba Y, Tanaka Y, Ishii S, Morimoto T, Sato K. Ibaraki virus, an agent of epizootic disease of cattle resembling bluetongue. IV. Physicochemical and serological properties of the virus. Jpn J Microbiol. 1970;14(5):351–60.

    Article  CAS  PubMed  Google Scholar 

  50. Omori T, Inaba Y, Morimoto T, Tanaka Y, Ishitani R. Ibaraki virus, an agent of epizootic disease of cattle resembling bluetongue. I. Epidemiologic, clinical and pathologic observations and experimental transmission to calves. Jpn J Microbiol. 1969;13(2):139–57.

    Article  CAS  PubMed  Google Scholar 

  51. Biek R. Evolutionary dynamics and spatial genetic structure of epizootic hemorrhagic disease virus in the eastern United States. Infect Genet Evol. 2007;7(5):651–5.

    Article  CAS  PubMed  Google Scholar 

  52. Allison AB, Goekjian VH, Potgieter AC, Wilson WC, Johnson DJ, Mertens PP, et al. Detection of a novel reassortant epizootic hemorrhagic disease virus (EHDV) in the USA containing RNA segments derived from both exotic (EHDV-6) and endemic (EHDV-2) serotypes. J Gen Virol. 2010;91(Pt 2):430–9.

    Article  CAS  PubMed  Google Scholar 

  53. Shope RE, Macnamara LG, Mangold R. A virus-induced epizootic hemorrhagic disease of the virginia white-tailed deer (Odocoileus Virginianus). J Exp Med. 1960;111(2):155–70.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  54. Omori T, Inaba Y, Morimoto T, Tanaka Y, Kono M. Ibaraki virus, an agent of epizootic disease of cattle resembling bluetongue. II. Isolation of the virus in bovine cell culture. Jpn J Microbiol. 1969;13(2):159–68.

    Article  CAS  PubMed  Google Scholar 

  55. Yadin H, Brenner J, Bumbrov V, Oved Z, Stram Y, Klement E, et al. Epizootic haemorrhagic disease virus type 7 infection in cattle in Israel. Vet Rec. 2008;162(2):53–6.

    Article  CAS  PubMed  Google Scholar 

  56. Temizel EM, Yesilbag K, Batten C, Senturk S, Maan NS, Clement-Mertens PP, et al. Epizootic hemorrhagic disease in cattle, Western Turkey. Emerg Infect Dis. 2009;15(2):317–9.

    Article  PubMed Central  PubMed  Google Scholar 

  57. Batten CA, Edwards L, Bin-Tarif A, Henstock MR, Oura CA. Infection kinetics of epizootic haemorrhagic disease virus serotype 6 in Holstein-Friesian cattle. Vet Microbiol. 2011;154(1–2):23–8.

    Article  CAS  PubMed  Google Scholar 

  58. Kedmi M, Van Straten M, Ezra E, Galon N, Klement E. Assessment of the productivity effects associated with epizootic hemorrhagic disease in dairy herds. J Dairy Sci. 2010;93(6):2486–95.

    Article  CAS  PubMed  Google Scholar 

  59. McLaughlin BE, DeMaula CD, Wilson WC, Boyce WM, MacLachlan NJ. Replication of bluetongue virus and epizootic hemorrhagic disease virus in pulmonary artery endothelial cells obtained from cattle, sheep, and deer. Am J Vet Res. 2003;64(7):860–5.

    Article  PubMed  Google Scholar 

  60. Aradaib IE, Brewer AW, Osburn BI. Interaction of epizootic hemorrhagic disease virus with bovine erythrocytes in vitro: electron microscope study. Comp Immunol Microbiol Infect Dis. 1997;20(3):281–3.

    Article  CAS  PubMed  Google Scholar 

  61. Quist CF, Howerth EW, Stallknecht DE, Brown J, Pisell T, Nettles VF. Host defense responses associated with experimental hemorrhagic disease in white-tailed deer. J Wildl Dis. 1997;33(3):584–99.

    Article  CAS  PubMed  Google Scholar 

  62. Gaydos JK, Allison AB, Hanson BA, Yellin AS. Oral and fecal shedding of epizootic hemorrhagic disease virus, serotype 1 from experimentally infected white-tailed deer. J Wildl Dis. 2002;38(1):166–8.

    Article  PubMed  Google Scholar 

  63. Aradaib IE, Akita GY, Osburn BI. Detection of epizootic hemorrhagic disease virus serotypes 1 and 2 in cell culture and clinical samples using polymerase chain reaction. J Vet Diagn Invest. 1994;6(2):143–7.

    Article  CAS  PubMed  Google Scholar 

  64. Abdy MJ, Howerth EE, Stallknecht DE. Experimental infection of calves with epizootic hemorrhagic disease virus. Am J Vet Res. 1999;60(5):621–6.

    CAS  PubMed  Google Scholar 

  65. Gaydos JK, Davidson WR, Elvinger F, Howerth EW, Murphy M, Stallknecht DE. Cross-protection between epizootic hemorrhagic disease virus serotypes 1 and 2 in white-tailed deer. J Wildl Dis. 2002;38(4):720–8.

    Article  PubMed  Google Scholar 

  66. Flacke GL, Yabsley MJ, Hanson BA, Stallknecht DE. Hemorrhagic disease in Kansas: enzootic stability meets epizootic disease. J Wildl Dis. 2004;40(2):288–93.

    Article  PubMed  Google Scholar 

  67. Ohashi S, Yoshida K, Watanabe Y, Tsuda T. Identification and PCR-restriction fragment length polymorphism analysis of a variant of the Ibaraki virus from naturally infected cattle and aborted fetuses in Japan. J Clin Microbiol. 1999;37(12):3800–3.

    CAS  PubMed Central  PubMed  Google Scholar 

  68. Gaydos JK, Crum JM, Davidson WR, Cross SS, Owen SF, Stallknecht DE. Epizootiology of an epizootic hemorrhagic disease outbreak in West Virginia. J Wildl Dis. 2004;40(3):383–93.

    Article  PubMed  Google Scholar 

  69. Wechsler SJ, McHolland LE. Susceptibilities of 14 cell lines to bluetongue virus infection. J Clin Microbiol. 1988;26(11):2324–7.

    CAS  PubMed Central  PubMed  Google Scholar 

  70. Aradaib IE, Smith WL, Osburn BI, Cullor JS. A multiplex PCR for simultaneous detection and differentiation of North American serotypes of bluetongue and epizootic hemorrhagic disease viruses. Comp Immunol Microbiol Infect Dis. 2003;26(2):77–87.

    Article  PubMed  Google Scholar 

  71. Wilson WC, Hindson BJ, O’Hearn ES, Hall S, Tellgren-Roth C, Torres C, et al. A multiplex real-time reverse transcription polymerase chain reaction assay for detection and differentiation of bluetongue virus and epizootic hemorrhagic disease virus serogroups. J Vet Diagn Invest. 2009;21(6):760–70.

    Article  PubMed  Google Scholar 

  72. Clavijo A, Sun F, Lester T, Jasperson DC, Wilson WC. An improved real-time polymerase chain reaction for the simultaneous detection of all serotypes of Epizootic hemorrhagic disease virus. J Vet Diagn Invest. 2010;22(4):588–93.

    Article  PubMed  Google Scholar 

  73. Maan NS, Maan S, Nomikou K, Johnson DJ, El Harrak M, Madani H, Yadin H, Incoglu S, Yesilbag K, Allison AB, Stallknecht DE, Batten C, Anthony SJ, Mertens PP. RT-PCR assays for seven serotypes of epizootic haemorrhagic disease virus & their use to type strains from the Mediterranean region and North America. PLoS One. 2010;5(9). pii: e12782. doi: 10.1371/journal.pone.0012782.

  74. Stallknecht DE, Kellogg ML, Blue JL, Pearson JE. Antibodies to bluetongue and epizootic hemorrhagic disease viruses in a barrier island white-tailed deer population. J Wildl Dis. 1991;27(4):668–74.

    Article  CAS  PubMed  Google Scholar 

  75. Mecham JO, Wilson WC. Antigen capture competitive enzyme-linked immunosorbent assays using baculovirus-expressed antigens for diagnosis of bluetongue virus and epizootic hemorrhagic disease virus. J Clin Microbiol. 2004;42(2):518–23.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  76. Thevasagayam JA, Wellby MP, Mertens PP, Burroughs JN, Anderson J. Detection and differentiation of epizootic haemorrhagic disease of deer and bluetongue viruses by serogroup-specific sandwich ELISA. J Virol Methods. 1996;56(1):49–57.

    Article  CAS  PubMed  Google Scholar 

Download references

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 or of the institutions, and/or the 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.

Author information

Authors and Affiliations

Authors

Corresponding author

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

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this chapter

Cite this chapter

Miller, M., Lagreid, W., Kuhn, J.H., Lewis, C.E., Loiacono, C.M., White, D. (2015). Viral Hemorrhagic Fevers of Animals Caused by Double-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_13

Download citation

Publish with us

Policies and ethics