Transmission and Epidemiology of Bluetongue and Epizootic Hemorrhagic Disease in North America: Current Perspectives, Research Gaps, and Future Directions

Vector-Borne and Zoonotic Diseases

Volumn 15, Issue 6, 2015, Pages 348-363

  Ruder, Mark G ^a   Lysyk, Timothy J ^b   Stallknecht, David E ^c   Foil, Lane D ^d   Johnson, Donna J ^e   Chase, Christopher C ^f   Dargatz, David A ^g   Gibbs, E Paul J ^h  

^a USDA ARS   (United States)

^b LETHBRIDGE RESEARCH CENTRE   (Canada)

^c UNIVERSITY OF GEORGIA   (United States)

^d Louisiana State University AgCenter   (United States)

^e National Veterinary Services Laboratories   (United States)

^f SOUTH DAKOTA STATE UNIVERSITY   (United States)

^g CENTERS FOR EPIDEMIOLOGY AND ANIMAL HEALTH   (United States)

^h University of Florida College of Veterinary Medicine   (United States)

Author keywords

Bluetongue virus; Culicoides; Epidemiology; Epizootic hemorrhagic disease virus; Transmission; Vector

Indexed keywords

AFRICA; ALPACA; AMERICAN BISON; ARTHROPOD; ARTICLE; BIGHORN SHEEP; BLUETONGUE; BLUETONGUE ORBIVIRUS; CULICOIDES; DISEASE CARRIER; DISEASE DURATION; DOMESTIC CATTLE; DOMESTIC GOAT; DOMESTIC SHEEP; ENVIRONMENTAL TEMPERATURE; EPIDEMIC; EPIZOOTIC HEMORRHAGIC DISEASE; EUROPE; FREEZING; HUMAN; INCIDENCE; INFECTION RATE; MULE DEER; NONHUMAN; NORTH AMERICA; OVERWINTERING; PRIORITY JOURNAL; RUMINANT; SEROTYPE; UNITED STATES; VIREMIA; VIRUS LOAD; VIRUS TRANSMISSION; ANIMAL; CERATOPOGONIDAE; ORBIVIRUS; PHYSIOLOGY; REOVIRIDAE INFECTIONS; RESEARCH; SHEEP; STANDARDS; TRANSMISSION; VETERINARY; VIROLOGY;

ARTHROPODA; BLUETONGUE VIRUS; EPIZOOTIC HEMORRHAGIC DISEASE VIRUS; ORBIVIRUS; REOVIRIDAE;

ANIMALS; BLUETONGUE; BLUETONGUE VIRUS; CERATOPOGONIDAE; HEMORRHAGIC DISEASE VIRUS, EPIZOOTIC; INSECT VECTORS; NORTH AMERICA; REOVIRIDAE INFECTIONS; RESEARCH; RUMINANTS; SHEEP;

EID: 84931833571     PISSN: 15303667     EISSN: 15577759     Source Type: Journal    
DOI: 10.1089/vbz.2014.1703     Document Type: Article

References (155)

1. Allison AB, Goekjian V, Potgieter A, Wilson W, 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; 91:430-439.
2. Allison AB, Holmes EC, Potgieter AC, Wright IM, et al. Segmental configuration and putative origin of the reassortant orbivirus, epizootic hemorrhagic disease virus serotype 6, strain Indiana. Virology 2012; 424:67-75.
3. Anbalagan S, Cooper E, Klumper P, Simonson R. Whole genome analysis of epizootic hemorrhagic disease virus identified limited genome constellations and preferrential reassortment. J Gen Virol 2014; 95:434-441.
4. Anthony S. Maan JS, Maan N, Kgosana L, et al. Genetic and phylogenetic analysis of the outer-coat proteins VP2 and VP5 of epizootic haemorrhagic disease virus (EHDV): Comparison of genetic and serological data to characterise the EHDV serogroup. Virus Res 2009; 145:200-210.
5. Aradaib IE, Sawyer MM, Osburn BI. Experimental epizootic hemorrhagic disease virus-infection in calves - virological and serologic studies. J Vet Diagn Invest 1994; 6:489-492.
6. Aradaib IE, Mederos RA, Osburn BI. Evaluation of epizootic hemorrhagic disease virus infection in sentinel calves from the San Joaquin Valley of California. Vet Res Commun 2005; 29:447-451.
7. Atchley WR. The Culicoides of New Mexico (Diptera: Ceratopogonidae). Kans Univ Sci Bull 1967; 46:937-1022.
8. Backx A, Heutink R, van Roaj E, van Rign P. Transplacental and oral transmission of wild-type bluetongue virus serotype 8 in cattle after experimental infection. Vet Microbiol 2009; 138:23-243.
9. Balasuriya U, Nadler S, Wilson W, Pritchard L, et al. The NS3 proteins of global strains of bluetongue virus evolve into regional topotypes through negative (purifying) selection. Vet Microbiol 2008; 126:91-100.
10. Baldwin CA, Mosier DA, Rogers SJ, Bragg CR. An outbreak of disease in cattle due to bluetongue virus. J Vet Diagn Invest 1991; 3:525-255.
11. Barber TL. Temporal appearance, geographic distribution, and species of origin of bluetongue virus serotypes in the United States. Am J Vet Res 1979; 40:1654-1656.
12. Becker ME, Reeves WK, Dejean SK, Emery MP et al. Detection of bluetongue virus RNA in field-collected Culicoides spp. (Diptera: Ceratopogonidae) following the discovery of bluetongue viruse serotype 1 in white-tailed deer and cattle in Louisiana. J Med Entomol 2010; 47:269-273.
13. Beringer J, Hansen LP, Stallknecht DE. An epizootic of hemorrhagic disease in white-tailed deer in Missouri. J Wildl Dis 2000; 36:588-591.
14. Berry BS, Magori K, Perofsky AC, Stallknecht DE, et al. Wetland cover dynamics drive hemorrhagic disease patterns in white-tailed deer in the United States. J Wildl Dis 2013; 49:501-509.
15. Blanton FS, Wirth WW. Arthropods of Florida and Neighboring Land Areas. Vol. 10. The Sand Flies (Culicoides) of Florida (Diptera: Ceratopogonidae). Florida Dept. of Agriculture and Consumer Services, Division of Plant Industry, 1979, 204 pp.
16. Bonneau K, DeMaula C, Mullens B, and MacLachlan N. Duration of viraemia infectious to Culicoides sonorensis in bluetongue virus-infected cattle and sheep. Vet Microbiol 2002; 88:115-125.
17. Bouwknegt C, van Rijn PA, Schipper JJ, Holzel D et al. Potential role of ticks as vectors of bluetongue virus. Exp Appl Acarol 2010; 52:183-192.
18. Boyer TC, Ward MP, Wallace RL, Zhou EM, et al. Exploratory spatial data analysis of regional seroprevalence of antibodies against epizootic hemorrhagic disease virus in cattle from Illinois and Indiana. Am J Vet Res 2008; 69:1286-1293.
19. Boyer TC, Ward MP, Singer RS. Climate, landscape, and the risk of Orbivirus exposure in cattle in Illinois and western Indiana. Am J Trop Med Hyg 2010; 83:789-794.
20. Bréard E, Sailleau C, Gourreau J, Zientara S, et al. Outbreak of epizootic haemorrhagic disease on the island of Réunion. Vet Rec 2004; 155:422-423.
21. Burgin LE, Gloster J, Sanders C, Mellor PS, et al. Investigating incursions of bluetongue virus using a model of long-distance Culicoides biting midge dispersal. Transbound Emerg Dis 2013; 60:263-272.
22. Carpenter S, Lunt HL, Arav D, Venter GJ, et al. Oral susceptibility to bluetongue virus of Culicoides (Diptera: Ceratopogonidae) from the United Kingdom. J Med Entomol 2006; 43:73-78.
23. Carpenter S, McArthur C, Selby R, Ward R, et al. Experimental infection studies of UK Culicoides species midges with blue-tongue virus serotypes 8 and 9. Vet Rec 2008; 163:589-592.
24. Chalmers GA, Vance HN, Mitchell GJ. An outbreak of hemorrhagic epizootic disease in wild ungulates in Alberta. J Wildl Dis 1964; 15:1-6.
25. Cheney IW, Larson MD, Mecham JO, Wilson WL. Geographical genetic variation in the gene encoding VP3 from Alberta isolate of epizootic hemorrhagic disease virus. Virus Res 1995; 36:279-286.
26. Cheney I, Yamakawa M, Roy P, Mecham J, et al. Molecular characterization of the segment 2 gene of epizootic hemorrhagic disease virus serotype 2: Gene sequence and genetic diversity. Virology 1996; 224:555-560.
27. th United States Animal Health Association. St. Louis, MO: United States Animal Health Association, 1981:522-537.
28. Downes JA. The Culicoides variipennis complex: A necessary re-alignment of nomenclature (Diptera: Ceratopogonidae). Can Entomol 1978; 110:63-69.
29. Drolet BS, Reister LM, Rigg TD, Nol P, et al. Experimental infection of white-tailed deer (Odocoileus virginianus) with northern European bluetongue virus serotype 8. Vet Microbiol 2013; 166:347-355.
30. th Annual Meeting of the United States Animal Health Association. Kansas City, MO: Richardson Communications Group, 2013:189.
31. Dulac GC, Dubuc C, Meyers DJ, Afshan A, et al. Incursion of bluetongue virus type 11 and epizootic hemorrhagic disease of deer type 2 for two consecutive years in the Okanagan Valley. Can Vet J 1989; 30:351.
32. Dulac GC, Sterritt WG, Dubac C, Afshar A, et al. Incursions of orbiviruses in Canada and their serologic monitoring in the native animal population between 1962 and 1991. In: Walton TE, Osburn BI, eds. Bluetongue, African Horse Sickness, and Related Orbiviruses: Proceedings of the Second International Symposium. Boca Raton, FL: CRC Press Inc., 1992:120-127.
33. European Food Safety Authority (EFSA) Panel on Animal Health and Welfare (AHAW). 2009. Scientific Opinion on Epizootic Hemorrhagic Disease. EFSA J 7:1418. [67 pp.]. doi:10.2903/j.efsa.2009.1418. Available at www.efsa.europa.eu/efsajournal
34. Favero C, Matos ACD, Campos FS, Cândido MV, et al. Epizootic hemorrhagic disease in Brocket deer, Brazil. Emerg Inf Dis 2013; 19:346.
35. Fischer JR, Hansen LP, Turk JR, Miller MA, et al. An epizootic of hemorrhagic disease in white-tailed deer (Odocoileus virginianus) in Missouri: Necropsy findings and population impact. J Wildl Dis 1995; 31:30-36.
36. Flacke GL, Yabsley MJ, Hanson BA, Stallknecht DE. Hemorrhagic disease in Kansas: Enzootic stability meets epizootic disease. J Wildl Dis 2004; 40:288-293.
37. Foster NM, Breckon RD, Luedke AJ, Jones RH, et al. Transmission of two strains for epizootic hemorrhagic disease virus in deer by Culicoides variipennis. J Wildl Dis 1977; 13:9-16.
38. Foster NM, Metcalf FE, Barber TL, Jones RH, et al. Bluetongue and epizootic hemorrhagic disease virus isolations from vertebrate and invertebrate hosts at common geographic sites. J Am Vet Med Assoc 1980; 176:116-118.
39. Gaydos JK, Allison AB, Hanson BA, Yellin SA, et al. Oral and fecal shedding of epizootic hemorrhagic disease virus, serotype 1 from experimentally infected white-tailed deer. J Wildl Dis 2002a; 38:166-168.
40. Gaydos JK, Davidson WR, Elvinger F, Howerth EW, et al. Cross-protection between epizootic hemorrhagic disease virus serotypes 1 and 2 in white-tailed deer. J Wildl Dis 2002b; 38:720-728.
41. Gaydos JK, Davidson WR, Elvinger F, Mead DG, et al. Innate resistance to epizootic hemorrhagic disease in white-tailed deer. J Wildl Dis 2002c; 38:713-719.
42. Gaydos JK, Stallknecht DE, Kavanaugh D, Olson RJ, et al. Dynamics of maternal antibodies to hemorrhagic disease viruses (Reoviridae: Orbivirus) in white-tailed deer. J Wildl Dis 2002d; 38:253-257.
43. Gaydos JK, Crum JM, Davidson WR, Cross SS, et al. Epizootiology of an epizootic hemorrhagic disease outbreak in West Virginia. J Wildl Dis 2004; 40:383-393.
44. Gerry AC, Mullens BA. Seasonal abundance and survivorship of Culicoides sonorensis (Diptera: Ceratopogonidae) at a Southern California dairy, with reference to potential blue-tongue virus transmission and persistence. J Med Entomol 2000; 37:675-688.
45. Gerry AC, Mullens BA, Maclachlan NJ, Mecham JO. Seasonal transmission of bluetongue virus by Culicoides sonorensis (Diptera: Ceratopogonidae) at a Southern California dairy and evaluation of vectorial capacity as a predictor of blue-tongue virus transmission. J Med Entomol 2001; 38:197-209.
46. Gibbs E, Lawman M. Infection of British deer and farm animals with epizootic haemorrhagic disease of deer virus. J Comp Pathol 1977; 87:335-343.
47. Gibbs E, Greiner E, Taylor W, Barber T, et al. Isolation of bluetongue virus serotype 2 from cattle in Florida: Serotype of bluetongue virus hitherto unrecognized in the Western Hemisphere. Am J Vet Res 1983; 44:2226.
48. Gibbs EPJ, Greiner EC. Bluetongue and epizootic hemorrhagic disease. In: Monath T, ed. Arboviruses: Epidemiology and Ecology, vol. 2. Boca Raton, FL: CRC Press Inc., 1989:39-70.
49. Gibbs EPJ, Greiner EC. The epidemiology of bluetongue. Comp Immunol Microbiol Infect Dis 1994; 17:207-220.
50. Gibbs EPJ, Homan EJ, Mo CL, Greiner EC, et al. Epidemiology of bluetongue viruses in the American tropics. Ann NY Acad Sci 1992; 653:243-250.
51. Gibbs EPJ, Tabachnick WJ, Holt TJ, Stallknecht DE. US concerns over bluetongue. Science 2008; 320:872-872.
52. Green AL, Dargatz DA, Schmidtmann ET, Herrero MV, et al. Risk factors associated with herd-level exposure of cattle in Nebraska, North Dakota, and South Dakota to bluetongue virus. Am. J Vet Res 2005; 66:853-860.
53. Hardy WT, Price DA. Soremuzzle of sheep. J Am Vet Med Assoc 1952; 120:23.
54. Hoff GL, Hoff DM. Bluetongue and epizootic hemorrhagic disease: A review of these diseases in non-domestic artiodactyles. J Zoo Wildl Med 1976; 7:26-30.
55. Hoff GL, Trainer DO. Experimental infection of North American elk with epizootic hemorrhagic disease virus 1. J Wildl Dis 1973; 9: 129-132.
56. Hoff GL, Trainer DO. Observations on bluetongue and epizootic hemorrhagic disease viruses in white-tailed deer: (1) distribution of virus in the blood (2) cross-challenge. J Wildl Dis 1974; 10:25-31.
57. Hoff GL, Trainer DO. Bluetongue and epizootic hemorrhagic disease viruses: Their relationship to wildlife species. Adv Vet Sci Comp Med 1978; 22:111-132.
58. Hofmann MA, Renzullo S, Mader M, Chaignat V, et al. Genetic characterization of toggenburg orbivirus, a new bluetongue virus, from goats, Switzerland. Emerg Inf Dis 2008; 14:1855-1861.
59. Holbrook FR, Tabachnick WJ, Schmidtmann ET, McKinnon CN, et al. Sympatry in the Culicoides variipennis complex (Diptera: Ceratopogonidae): Taxonomic reassessment. J Med Entomol 2000; 37:65-76.
60. House C, Shipman LD, Weybright G. Serological diagnosis of epizootic hemorrhagic disease in cattle in the USA with lesions suggestive of vesicular disease. Trop Vet Med 1998; 849:497-500.
61. rd ed. Ames, IA: Iowa State Press, 2001: 77-97.
62. Johnson DJ, Ostlund EN, Stallknecht DE, Goekjian VH, et al. First report of bluetongue virus serotype 1 isolated from a white-tailed deer in the United States. J Vet Diagn Invest 2006; 18:398-401.
63. Jones R, Luedke A. Epidemiological notes: Two bluetongue epizootics. Mosq News 1969.
64. Jones RH, Roughton RD, Foster NM, Bando BM. Culicoides, the vector of epizootic hemorrhagic disease in white-tailed deer in Kentucky in 1971. J Wildl Dis 1977; 13:2-8.
65. Jorgensen NM. The systematics, occurrence, and host preference of Culicoides (Diptera: Ceratopoginidae) in southeastern Washington. Melanderia 1969; 3:1-47.
66. Kedmi M, Van Straten M, Ezra E, Galon N, et al. Assessment of the productivity effects associated with epizootic hemorrhagic disease in dairy herds. J Dairy Sci 2010; 93:2486-2495.
67. Koumbati M, Mangana O, Nomikou K, Mellor P, et al. Duration of bluetongue viraemia and serological responses in experimentally infected European breeds of sheep and goats. Vet Microbiol 1999; 64:277-285.
68. Losson B, Mignon B, Paternostre J, Madder M, et al. Biting midges overwintering in Belgium. Vet Rec 2007; 160:451-452.
69. Luedke AJ, Jochim MM, Bowne JG. Preliminary bluetongue transmission with the sheep ked Melophagus ovinus (L.). Can J Comp Med Vet Sci 1965; 29:229-231.
70. Lysyk TJ, Danyk T. Effect of temperature on life-history parameters of adult Culicoides sonorensis (Diptera: Ceratopogonidae) in relation to geographic origin and vectorial capacity for bluetongue virus. J Med Entomol 2007; 44:741-751.
71. Maan S, Maan N, Samuel A, Rao S, et al. Analysis and phylogenetic comparisons of full-length VP2 genes of the 24 bluetongue virus serotypes. J Gen Virol 2007; 88:621-630.
72. th bluetongue virus serotype from Kuwait. PLoS One 2011; 6:e26147.
73. MacLachlan NJ, Zientara S, Stallknecht DE, Boone JD, et al. Phylogenetic comparison of the S10 genes of recent isolates of bluetongue virus from the United States and French Martinique Island. Virus Res 2007; 129:236-240.
74. Mayo CE, Gardner IA, Mullens BA, Barker CM, et al. Anthropogenic and meteorological factors influence vector abundance and prevalence of bluetongue virus infection of dairy cattle in California. Vet Microbiol 2012; 155:158-164.
75. Mayo CE, Mullens BA, Reisen WF, Osborne CJ, et al. Seasonal and interseasonal dynamics of bluetongue virus infection of dairy cattle and Culicoides sonorensis midges in northern California - implication for virus overwintereing in temperate zones. PLoS One 2014; 4:1-6.
76. McGowan B. An epidemic resembling soremuzzle or bluetongue in California sheep. Conell Vet 1953; 43:213.
77. Mecham JO, Stallknecht D, Wilson WC. The S7 gene and VP7 protein are highly conserved among temporally and geographically distinct American isolates of epizootic hemorrhagic disease virus. Virus Res 2003; 94: 129-133.
78. Menzies FD, McCullough SJ, McKeown IM, Foster JL, et al. Evidence for transplacental and contact transmission of bluetongue virus in cattle. Vet Rec 2008; 163:203-209.
79. Metcalf H, Luedke A, Jochim M. Epizootic hemorrhagic disease virus infection in cattle. In: Walton TE, Osburn BI, eds. Bluetongue, African Horse Sickness, and Related Orbiviruses: Proceedings of the Second International Symposium, Boca Raton, FL: CRC Press Inc., 1992:222-237.
80. Metcalf HE, Pearson JE, Klingsporn AL. Bluetongue in cattle: A serologic survey of slaughter cattle in the United States. Am J Vet Res 1981; 42:1057-1061.
81. Mertens PPC, Maan S, Samuel AR, Attoui H. 2005. Orbivirus: Reoviridae. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball LA, eds. Virus Taxonomy: VIIIth Report of the ICTV. London: Elsevier/Academic Press, 2005:466-483.
82. Miller MM, Brown J, Cornish T, Johnson G, et al. Investigation of a bluetongue disease epizootic caused by bluetongue virus serotype 17 in sheep in Wyoming. JAVMA 2010; 237:955-959.
83. Mullen GR, Haynes ME, Nusbaum KE. Potential vectors of bluetongue and epizootic hemorrhagic disease viruses of cattle and white-tailed deer in Alabama. Prog Clin Biol Res 1985a; 178:201-206.
84. Mullen GR, Jones RH, Braverman Y, Nusbaum KE. Laboratory infections of Culicoides debilipalpis and C. stellifer (Diptera: Ceratopogonidae) with bluetongue virus. Prog Clin Biol Res 1985b; 178:239-243.
85. Mullens BA, Dada CE. Spatial and seasonal distribution of potential vectors of hemorrhagic disease viruses to peninsular bighorn sheep in the Santa Rosa Mountains of southern California. J Wildl Dis 1992; 28:192-205.
86. Mullens BA, Gerry AC, Lysyk TJ, Schmidtmann ET. Environmental effects on vector competence and virogenesis of bluetongue virus in Culicoides: Interpreting laboratory data in a field context. Vet Ital 2004; 40:160-166.
87. Murphy MD, Howerth EW, MacLachlan NJ, Stallknecht DE. Genetic variation among epizootic hemorrhagic disease viruses in the southeastern United States: 1978-2001. Inf Gen Evol 2005; 5:157-165.
88. Murphy MD, Hanson BA, Howerth EW, Stallknecht DE. Molecular characterization of epizootic hemorrhagic disease virus serotype 1 associated with a 1999 epizootic in white-tailed deer in the eastern United States. J Wildl Dis 2006; 42:616-624.
89. Murray JO, Trainer DO. Bluetongue virus in North American elk. J Wildl Dis 1970; 6:144-148.
90. th North American Wildlife & Natural Resources Conference. Washington, DC: Wildlife Management Institute, 1992:499-516.
91. nd International Symposium. Boca Raton, FL: CRC Press Inc., 1992a:238-248.
92. Nettles VF, Davidson WR, Stallknecht DE. Surveillance for hemorrhagic disease in white-tailed deer and other wild ruminants, 1980-1989. In: Proceeding of the Annual Conference of the Southeastern Association of Fish and Wildlife Agencies. Montgomery, AK: 1992b; 46:138-146.
93. Odiawa G, Blue J, Tyler D, Shotts E. Bluetongue and epizootic hemorrhagic disease in ruminants in Georgia: Survey by serotest and virologic isolation. Am J Vet Res 1985; 46: 2193.
94. Ortega J, Crossley B, Dechant JE, Drew CP, et al. Fatal bluetongue virus infection in an alpaca (Vicugna pacos) in California. J Vet Diagn Invest 2010; 22:134-136.
95. Ostlund E, Moser K, Johnson D, Pearson J. Distribution of bluetongue in the United States of America, 1991-2002. Vet Ital 2004; 40:83-88.
96. th Annual Meeting of the United States Animal Health Association, Greensboro, NC: Richardson Communications Group, 2008:148-151.
97. th Annual Meeting of the United States Animal Health Association. Kansas City, MO: Richardson Communications Group, 2010:157-158.
98. Pare J, Geale DW, Koller-Jones M, Hooper-McGrevy K, et al. Serological status of Canadian cattle for brucellosis, anaplasmosis, and bluetongue in 2007-2008. Can Vet J 2012; 53:949-956.
99. Pearson J, Gustafson G, Shafer A, Alstad A, et al. Distribution of bluetongue in the United States. In: Walton TE, Osburn BI, eds. Bluetongue, African horse sickness, and related orbiviruses: Proceedings of the Second International Symposium. Boca Raton, FL: CRC Press Inc., 1992:128-139.
100. Pritchard L, Gould A, Wilson W, Thompson L, et al. Complete nucleotide sequence of RNA segment 3 of bluetongue virus serotype 2 (Ona-A). Phylogenetic analyses reveal the probable origin and relationship with other orbiviruses. Virus Res 1995; 35:247-261.
101. Purse BV, Mellor PS, Rogers DJ, Samuel AR, et al. Climate change and the recent emergence of bluetongue in Europe. Nat Rev Micro 2005; 3:171-181.
102. Pybus MJ, Ravi M, Pollock C. Epizootic hemorrhagic disease in Alberta, Canada. J Wildl Dis 2014; 50:720-722.
103. Quist CF, Howerth EW, Stallknecht DE, Brown J, et al. Host defense responses associated with experimental hemorrhagic disease in white-tailed deer. J Wildl Dis 1997; 33:584-599.
104. Richards R, MacLachlan N, Heidner H, Fuller F. Comparison of virologic and serologic responses of lambs and calves infected with bluetongue virus serotype 10. Vet Microbiol 1988; 18:233-242.
105. Robinson RM, Hailey TL, Livingston CW, Thomas JW. Bluetongue in the desert bighorn sheep. J Wildl Managem 1967; 31:165-168.
106. th Annual Meeting of the United States Animal Health Association. Greensboro, NC: Richardson Communications Group, 2012:191-193.
107. Roughton RD. An outbreak of a hemorrhagic disease in white-tailed deer in Kentucky. J Wildl Dis 1975; 11:177-186.
108. Ruder MG, Allison AB, Stallknecht DE, Mead DG, et al. Susceptibility of white-tailed deer (Odocoileus virginianus) to experimental infection with epizootic hemorrhagic disease virus serotype 7. J Wildl Dis 2012a: 48:676-685.
109. Ruder MG, Howerth EW, Stallknecht DE, Allison AB, et al. Vector competence of Culicoides sonorensis (Diptera: Ceratopogonidae) to epizootic hemorrhagic disease virus serotype 7. Parasit Vector 2012b; 5:1-8.
110. Sailleau C, Zanella G, Breard E, Viarouge C, et al. Co-circulation of bluetongue and epizootic haemorrhagic disease viruses in cattle in Reunion Island. Vet Microbiol 2012; 155:191-197.
111. Savini G, Afonso A, Mellor P, Aradaib I, et al. Epizootic haemorrhagic disease. Res Vet Sci 2011; 91:1-17.
112. Schmidtmann ET. Testing the relationship between dissolved salts and immature populations of the Culicoides variipennis complex (Diptera: Ceratopogonidae). Environ Entomol 2006; 35:1154-1160.
113. Schmidtmann ET, Bobian RJ, Belden RP. Soil chemistries define aquatic habitats with immature populations of the Culicoides variipennis complex (Diptera: Ceratopogonidae). J Med Entomol 2000; 37:768-773.
114. Schmidtmann ET, Herrero MV, Green AL, Dargatz DA, et al. Distribution of Culicoides sonorensis (Diptera: Ceratopogonidae) in Nebraska, South Dakota, and North Dakota: Clarifying the epidemiology of bluetongue disease in the northern Great Plains region of the United States. J Med Entomol 2011; 48:634-643.
115. Sellers RF, Maarouf AR. Trajectory analysis and bluetongue virus serotype 2 in Florida 1982. Can J Vet Res 1989; 53: 100-102.
116. Sellers RF, Maarouf AR. Possible introduction of epizootic hemorrhagic disease of deer virus (serotype2) and bluetongue virus (serotype 11) into British Columbia in 1987 and 1988 by infected Culicoides carried on the wind. Can J Vet Res 1991; 55:367-370.
117. Shapiro JL, Wiegers A, Dulac GC, Bouffard A, et al. A surevy of cattle for antibodies against bluetongue and epizootic hemorrhagic disease of deer viruses in British Columbia and southwestern Alberta in 1987. Can J Vet Res 1991; 55:203-204.
118. Shope RE, MacNamara LG, Mangold R. A virus-induced epizootic hemorrhagic disease of the Virginia white-tailed deer (Odocoileus virginianus). J Exp Med 1960; 111:155-170.
119. th Annual Meeting of the United States Animal Health Association, October 23-29, 2008, Greensboro, NC.
120. Singer RS, MacLachlan NJ, Carpenter TE. Maximal predicted duration of viremia in bluetongue virus-infected cattle. J Vet Diagn Invest 2001; 13:43-49.
121. Sleeman JM, Howell JE, Knox WM, Stenger PJ. Incidence of hemorrhagic disease in white-tailed deer is associated with winter and summer climatic conditions. EcoHealth 2009; 6:11-15.
122. Smith KE, Stallknecht DE. Culicoides (Diptera: Ceratopogonidae) collected during epizootics of hemorrhagic disease among captive white-tailed deer. J Med Entomol 1996; 33:507-510.
123. Smith KE, Stallknecht DE, Nettles VF. Experimental infection of Culicoides lahillei (Diptera: Ceratopogonidae) with epizootic hemorrhagic disease virus serotype 2 (Orbivirus: Reoviridae). J Med Entomol 1996a; 33:117-122.
124. Smith KE, Stallknecht DE, Sewell CT, Rollor EA, et al. Monitoring of Culicoides spp. at a site enzootic for hemorrhagic disease in white-tailed deer in Georgia, USA. J Wildl Dis 1996b; 32:627-642.
125. Stair EL, Robinson RM, Jones LP. Spontaneous bluetongue in Texas white-tailed deer. Pathologia Veterinaria 1968; 5:164-173.
126. Stallknecht DE, Howerth EW. Epidemiology of bluetongue and epizootic hemorrhagic disease in wildlife: Surveillance methods. Vet Ital 2004; 40:203-207.
127. Stallknecht DE, Luttrell MP, Smith KE, Nettles VF. Hemorrhagic disease in white-tailed deer in Texas: A case for enzootic stability. J Wildl Dis 1996; 32:695-700.
128. th North American Wildlife and Natural Resources Conference. 2002; 67:75-86.
129. Stallknecht DE, Allison AP, Park AW, Phillips JE, et al. Apparent increase in reported hemorrhagic disease in the midwest and northeast United States. J Wildl Dis 2015; in press. doi: http://dx.doi.org/10.7589/2013-12-330.
130. Stott JL, Else KC, McGowan B, Wilson LK. Epizootiology of bluetongue virus in the western United States. Proceedings of the Annual Meeting of the United States Animal Health Association 1981; 85:170-180.
131. Stott JL, Osburn BI, Alexander L. Ornithodoros coriaceus (pajaroello tick) as a vector of bluetongue virus. Am J Vet Res 1985; 46:1197-1199.
132. Tabachnick WJ. Culicoides variipennis and bluetongue virus epidemiology in the United States. Ann Rev Entomol 1996; 41:23-43.
133. Tabachnick WJ. Culicoides and the global epidemiology of bluetongue virus infection. Vet Ital 2004; 40:145-150.
134. Tanya V, Greiner E, Gibbs E. Evaluation of Culicoides insignis (Diptera: Ceratopogonidae) as a vector of bluetongue virus. Vet Microbiol 1992; 32:1-14.
135. Temizel EM, Yesilbag K, Batten C, Senturk S, et al. Epizootic hemorrhagic disease in cattle, Western Turkey. Emerg Inf Dis 2009; 15:317-319.
136. Tessaro SV, Clavijo A. Duration of bluetongue viremia in experimentally infected American bison. J Wildl Dis 2001; 37:722-729.
137. Thomas FC. Hemorrhagic disease. In: Davidson WR, ed. Diseases and Parasites of White-Tailed Deer. Tallahassee, FL: Tall Timbers Research Station, 1981:87-96.
138. Thomas FC, Trainer DO. Bluetongue virus in white-tailed deer. Am J Vet Res 1970; 30:271-278.
139. Thorne ET, Williams ES, Spraker TR, Helms W, et al. Bluetongue in free-ranging pronghorn antelope (Antilocapra americana) in Wyoming: 1976 and 1984. J Wildl Dis 1988; 24:113-119.
140. USDA National Agricultural Statistics Service (NASS), 2012 Census of Agriculture, United States Summary and State Data. Volume 1, Geographic Area Series Part 51, May 2014, 695 pp. Available at www.agcensus.usda.gov/Publications/2012/Full-Report/Volume-1,-Chapter-1-US/usv1.pdf
141. Van Campen H, Davis C, Flinchum JD, Bishop JV, et al. Epizootic hemorrhagic disease in yaks (Bos grunniens). J Vet Diag Invest 2013; 25:443-446.
142. Van Donkersgoed J, Gertonson A, Bridges M, Raths D, et al. Prevalence of antibodies to Bluetongue virus and Anaplasma marginale in Montana yearling cattle entering Alberta feedlots: Fall 2001. Can Vet J 2004; 45:486-492.
143. Van Donkersgoed J, Linfield TFT, Bridges M, Raths D, et al. Prevalence of antibodies to serotypes of Bluetongue virus and Anaplasma marginale in Montana feeder cattle: 2002-2003. Can Vet J 2006; 47:692-694.
144. Walton TE. The history of bluetongue and a current global overview. Vet Ital 2004; 40:31-38.
145. Walton TE, Barber TL, Jones RH, Luedke AJ. Epidemiology of bluetongue virus: Transmission cycle, vectors, and serotypic distribution in the Americas. Prev Vet Med 1984; 2:379-388.
146. Wilson A, Darpel K, Mellor PS. Where does bluetongue virus sleep in the winter? PLoS Biol 2008; 6:e210. DOI: 10.1037/journal.pbio.0060210.
147. Wilson W, Ma HC, Venter E, Van Djik A, et al. Phylogenetic relationships of bluetongue viruses based on gene S7. Virus Res 2000; 67:141-151.
148. Wilson WC, Mecham JO, Schmidtmann E, Sanchez CJ et al. Current status of bluetongue virus in the Americas. In: Mellor P, Baylis M, Mertens P, eds. Bluetongue. London, UK: Elsevier Ltd, 2009:197-221.
149. Wirth WW, Jones RH. The North American subspecies of Culicoides variipennis Diptera: Heleidae). United States Department of Agriculture Technical Bulletin 1957: no. 1170.
150. Wirth W, Morris C. The taxonomic complex, Culicoides variipennis. Prog Clin Biol Res 1985; 178:165-175.
151. Work TM, Jessup DA, Sawyer MM. Experimental bluetongue and epizootic hemorrhagic disease virus infection in California black-tailed deer. J Wildl Dis 1992; 28:623-628.
152. World Health Organization. Arboviruses and human disease. Report of a WHO scientific group. WHO Technical Report Series. 1967; 369:1-84.
153. Worwa G, Hilbe M, Ehrensperger F, Chaignat V, et al. Experimental transplacental infection of sheep with bluetongue virus serotype 8. Vet Rec 2009; 164:499-500.
154. Xu B, Madden M, Stallknecht DE, Hodler TW, et al. Spatialtemporal model of haemorrhagic disease in white-tailed deer in south-east USA, 1983 to 2000. Vet Rec 2012; 170: 288-288.
155. Yadin H, Brenner J, Bumbrov V, Oved Z, et al. Epizootic haemorrhagic disease virus type 7 infection in cattle in Israel. Vet Rec 2008; 162:53-56.