Torovirus Pathogenesis and Immune Responses

Armando E. Hoet; Linda J. Saif

doi:10.1128/9781555815790.ch23

Chapter 23 : Torovirus Pathogenesis and Immune Responses

Authors: Armando E. Hoet¹, Linda J. Saif²

VIEW AFFILIATIONS HIDE AFFILIATIONS

Affiliations: 1: Department of Veterinary Preventive Medicine, College of Veterinary Medicine, The Ohio State University, Columbus, OH 43210; 2: Food Animal Health Research Program, Ohio Agricultural Research and Development Center, and Department of Veterinary Preventive Medicine, College of Veterinary Medicine, The Ohio State University, Wooster, OH 44691

Content Type: Monograph

Publication Year: 2008

Category: Viruses and Viral Pathogenesis

Book DOI: 10.1128/9781555815790

Chapter DOI: 10.1128/9781555815790.ch23

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:

Torovirus Pathogenesis and Immune Responses, Page 1 of 2

< Previous page | Next page > /docserver/preview/fulltext/10.1128/9781555815790/9781555814557_Chap23-1.gif /docserver/preview/fulltext/10.1128/9781555815790/9781555814557_Chap23-2.gif

Abstract:

Toroviruses are pleomorphic viruses with a peplomer-bearing envelope containing an elongated tubular nucleocapsid with helical symmetry. They contain a linear, nonsegmented, positive- and single-stranded polyadenylated RNA genome. Currently only four species are recognized as members of the Torovirus genus in the Coronaviridae family: equine torovirus (EToV), initially known as Berne virus; bovine torovirus (BToV), originally known as Breda virus; human torovirus (HToV); and porcine torovirus. Torovirus-like (TVL) particles have been detected in feces from other animal species, such as turkeys, dogs, and cats. In addition, antibodies against toroviruses are frequently detected in ungulates such as horses, sheep, goats, and pigs. This chapter provides a comprehensive review of torovirus pathogenesis and immune responses. A brief epidemiological background highlighting HToVs is also provided.

Citation: Hoet A, Saif L. 2008. Torovirus Pathogenesis and Immune Responses, p 351-359. In Perlman S, Gallagher T, Snijder E (ed), Nidoviruses. ASM Press, Washington, DC. doi: 10.1128/9781555815790.ch23

Key Concept Ranking

Small Intestine: 0.5403617
Humoral Immune Response: 0.523018
Nosocomial Diarrhea: 0.49321407
Bovine torovirus: 0.48249203
Large Intestine: 0.47650084

0.5403617

Highlighted Text: Show | Hide

Full text loading...

References

/content/book/10.1128/9781555815790.ch23

1. Ali, A., and, D. L. Reynolds. 1997. Stunting syndrome in Turkey poults: isolation and identification of the etiologic agent. Avian Dis. 41: 870– 881.

2. Ali, A., and, D. L. Reynolds. 2000. Characterization of the stunting syndrome agent: relatedness to known viruses. Avian Dis. 44: 45– 50.

3. Ali, A., and, D. L. Reynolds. 2003. Turkey torovirus infection, p. 332– 336. In Y. Saif,, H. J. Barnes,, J. R. Glisson,, A. M. Fadly,, L. R. McDougald,, and D. E. Sawyne (ed.), Disease of Poultry, 11th ed. Blackwell Publishing, Ames, IA.

4. Beards, G. M.,, D. W. G. Brown,, J. Green, and, T. H. Flewett. 1986. Preliminary characterization of torovirus-like particles of humans: comparison with Berne virus of horses and Breda virus of Calves. J. Med. Virol. 20: 67– 78.

5. Beards, G. M.,, J. Green,, C. Hall,, T. H. Flewett,, F. Lamouliatte, and, P. Du Pasquier. 1984. An enveloped virus in stools of children and adults with gastroenteritis that resembles the Breda virus of calves. Lancet i: 1050– 1052.

6. Brown, D. W. G.,, G. M. Beards, and, T. H. Flewett. 1987. Detection of Breda virus antigen and antibody in humans and animals by enzyme immunoassay. J. Clin. Microbiol. 25: 637– 640.

7. Brown, D. W. G.,, R. Selvakumar,, D. J. Daniel, and, V. I. Mathan. 1988. Prevalence of neutralizing antibodies to Berne virus in animals and humans in Vellore, South India. Arch. Virol. 98: 267– 269.

8. Cavanagh, D. 1997. Nidovirales: a new order comprising Coronaviridae and Arteriviridae. Arch. Virol. 143: 629– 633.

9. Cavanagh, D.,, D. A. Brian,, M. A. Brinton,, L. Enjuanes,, K. V. Holmes,, M. C. Horzinek,, M. M. C. Lai,, H. Laude,, P. G. W. Plagemann,, S. G. Siddell,, W. J. M. Spaan,, F. Taguchi, and, P. J. Talbot. 1994. The Coronaviridae now comprises two genera, Coronavirus and Torovirus: report of the Coronaviridae Study Group, p. 255– 257. In H. Laude, and J. F. Vautherot (ed.), Coronaviruses: Molecular Biology and Virus-Host Interactions. Plenum Press, New York, NY.

10. Cavanagh, D., and, D. Brown. 1990. Coronaviruses and Their Diseases. Plenum Press, New York, NY.

11. Cho, K. J.,, A. E. Hoet,, S. C. Loerch,, T. E. Wittum, and, L. J. Saif. 2001. Evaluation of concurrent shedding of bovine coronavirus via the respiratory tract and enteric route in feedlot cattle. Am. J. Vet. Res. 62: 1436– 1441.

12. Chouljenko, V. N.,, X. Q. Lin,, J. Storz,, K. G. Kousoulas, and, A. E. Gorbalenya. 2001. Comparison of genomic and predicted amino acid sequences of respiratory and enteric bovine coronaviruses isolated from the same animal with fatal shipping pneumonia. J. Gen. Virol. 82: 2927– 2933.

13. Cornelissen,, L. A. H. M. 1999. What are toroviruses? p. 7–20. In L. A. H. M. Cornelissen (ed.), Molecular Characterization of Ungulate Toroviruses. Universiteit Utrecht, Utrecht, The Netherlands.

14. Cornelissen, L. A. H. M.,, P. A. M. van Woensel,, R. J. de Groot,, M. C. Horzinek,, N. Visser, and, H. F. Egberink. 1998. Cell culture-grown putative bovine respiratory torovirus identified as a coronavirus. Vet. Rec. 142: 683– 686.

15. Duckmanton, L.,, B. Luan,, J. Devenish,, R. Tellier, and, M. Petric. 1997. Characterization of torovirus from human fecal specimens. Virology 239: 158– 168

16. Duckmanton, L. M.,, S. Carman,, E. Nagy, and, M. Petric. 1998. Detection of bovine torovirus in fecal specimens of calves with diarrhea from Ontario farms. J. Clin. Microbiol. 36: 1266– 1270.

17. Durham, P. J. K.,, L. E. Hassard,, G. R. Norman, and, R. L. Yemen. 1989. Viruses and virus-like particles detected during examination of feces from calves and piglets with diarrhea. Can. Vet. J. 30: 876– 881.

18. Fagerland, J. A.,, J. F. L. Pohlenz, and, G. N. Woode. 1986. A morphological study of the replication of Breda virus (proposed family Toroviridae) in bovine intestinal cells. J. Gen. Virol. 67: 1293– 1304.

19. Finlaison, D. S. 1995. Faecal viruses of dogs—an electron microscope study. Vet. Microbiol. 46: 295– 305.

20. Hall, G. A. 1987. Comparative pathology of infection by novel diarrhoea viruses. Ciba Found. Symp. 128: 192– 217.

21. Haschek, B.,, D. Klein,, V. Benetka,, C. Herrera,, I. Sommerfeld-Stur,, S. Vilcek,, K. Moestl, and, G. M. Beards. 2006. Detection of bovine torovirus in neonatal calf diarrhea in Lower Austria and Styria (Austria). J. Vet. Med. B 53: 160– 165.

22. Hasoksuz, M. H.,, S. L. Lathrop,, K. L. Gadfield, and, L. J. Saif. 1999. Isolation of bovine respiratory coronaviruses from feed-lot cattle and comparison of their biological and antigenic properties with bovine enteric coronaviruses. Am. J. Vet. Res. 60: 1227– 1233.

23. Heckert, R. A.,, L. J. Saif,, K. H. Hoblet, and, A. G. Agnes. 1990. A longitudinal study of bovine coronavirus enteric and respiratory infections in dairy calves in two herds in Ohio. Vet. Microbiol. 22: 187– 201.

24. Heckert, R. A.,, L. J. Saif,, J. P. Mengel, and, G. W. Myers. 1991. Mucosal and systemic antibody responses to bovine corona-virus structural proteins in experimentally challenge-exposed calves fed low or high amounts of colostral antibodies. Am. J. Vet. Res. 52: 700– 708.

25. Heckert, R. A.,, L. J. Saif, and, G. W. Myers. 1991. Mucosal and systemic isotype specific antibody responses to bovine coronavirus structural proteins in naturally infected dairy calves. Am. J. Vet. Res. 52: 852– 857.

26. Heckert, R. A.,, L. J. Saif,, G. W. Myers, and, A. G. Agnes. 1991. Epidemiologic factors and isotype-specific antibody responses in serum and mucosal secretions of dairy calves with bovine coronavirus respiratory tract and enteric tract infections. Am. J. Vet. Res. 52: 845– 851.

27. Hoet, A. E.,, K. O. Cho,, K. O. Chang,, S. C. Loerch,, T. E. Wittum, and, L. J. Saif. 2002. Enteric and nasal shedding of bovine torovirus (Breda virus) in feedlot cattle. Am. J. Vet. Res. 63: 342– 348.

28. Hoet, A. E.,, P. R. Nielsen,, M. Hasoksuz,, C. Thomas,, T. E. Wittum, and, L. J. Saif. 2003. Detection of bovine torovirus and other enteric pathogens in feces from diarrhea cases in cattle. J. Vet. Diagn. Investig. 15: 205– 212.

29. Hoet, A. E., and, L. J. Saif. 2004. Bovine torovirus (Breda virus) revisited. Anim. Health Res. Rev. 5: 157– 171.

30. Hoet, A. E.,, J. Smiley,, C. Thomas,, P. R. Nielsen,, T. E. Wittum, and, L. J. Saif. 2003. Association of enteric shedding of bovine torovirus (Breda virus) and other enteropathogens with diarrhea in veal calves. Am. J. Vet. Res. 64: 485– 490.

31. Holmes, K. V. 2001. Enteric infections with coronaviruses and toroviruses. Novartis Found. Symp. 238: 258– 275.

32. Horzinek, M. C. 1999. Toroviruses (Coronaviridae), p. 1798– 1803. In A. Granoff, and R. Webster (ed.), Encyclopedia of Virology, 2nd ed. Academic Press, San Diego, CA.

33. Horzinek, M. C.,, T. H. Flewett,, L. J. Saif,, W. J. M. Spaan,, M. Weiss, and, G. N. Woode. 1987. A new family of vertebrate viruses: Toroviridae. Intervirology 27: 17– 24.

34. Horzinek, M. C., and, M. Weiss. 1984. Toroviridae: a taxonomic proposal. Zentbl. Vetmed. Reihe B 31: 649– 659.

35. Horzinek, M. C., and, M. Weiss. 1990. Toroviruses, p. 253– 262. In L. J. Saif, and K. W. Theil (ed.), Viral Diarrheas of Man and Animals. CRC Press, Boca Raton, FL.

36. Jamieson, F. B.,, E. E. L. Wang,, C. Bain,, J. Good,, L. M. Duckmanton, and, M. Petric. 1998. Human torovirus: a new nosocomial gastrointestinal pathogen. J. Infect. Dis. 178: 1263– 1269.

37. Kapil, S., and, S. M. Goyal. 1995. Bovine coronavirus-associated respiratory disease. Compend. Continuing Educ. Practi. Vet. 17: 1179– 1181.

38. Kluver, S. 1991. Electron microscopical and serological study of the occurrence of Breda torovirus, a cause of calf diarrhoea. Ph.D. thesis. Tierärztliche Hochschule, Hannover, Germany.

39. Koopmans, M.,, H. Cremers,, G. N. Woode, and, M. C. Horzinek. 1990. Breda virus (Toroviridae) infection and systemic antibody response in sentinel calves. Am. J. Vet. Res. 51: 1443– 1448.

40. Koopmans, M.,, S. Goosen,, A. Lima,, I. Mcauliffe,, J. Nataro,, L. Barret,, R. I. Glass, and, R. Guerrant. 1997. Association of torovirus with acute and persistent diarrhea in children. Pediatr. Infect. Dis. J. 16: 504– 507.

41. Koopmans, M.,, A. Herrewegh, and, M. C. Horzinek. 1991. Diagnosis of torovirus infection. Lancet 337: 859. (Letter.)

42. Koopmans, M., and, M. C. Horzinek. 1994. Toroviruses of animals and humans: a review. Adv. Virus Res. 43: 233– 273.

43. Koopmans, M., and, M. C. Horzinek. 1995. The pathogenesis of torovirus infections in animals and humans, p. 403– 413. In S. G. Siddell (ed.), The Coronaviridae. Plenum Press, New York, NY.

44. Koopmans, M.,, M. Petric,, R. I. Glass, and, S. S. Monroe. 1993. Enzyme-linked immunosorbent assay reactivity of torovirus-like particles in fecal specimens from humans with diarrhea. J. Clin. Microbiol. 31: 2738– 2744.

45. Koopmans, M.,, E. J. Snijder, and, M. C. Horzinek. 1991. cDNA probes for the diagnosis of bovine torovirus (Breda virus) infection. J. Clin. Microbiol. 29: 493– 497.

46. Koopmans, M.,, U. Van Den Boom,, G. N. Woode, and, M. C. Horzinek. 1989. Seroepidemiology of Breda virus in cattle using ELISA. Vet. Microbiol. 19: 233– 243.

47. Koopmans, M.,, L. van Wuijckhuise-Sjouke,, Y. H. Schukken,, H. Cremers, and, M. C. Horzinek. 1991. Association of diarrhea in cattle with torovirus infections on farms. Am. J. Vet. Res. 52: 1769– 1773.

48. Krishnan, T., and, T. N. Naik. 1997. Electronmicroscopic evidence of torovirus like particles in children with diarrhoea. Indian J. Med. Res. 105: 108– 110.

49. Kroneman, A.,, L. A. H. M. Cornelissen,, M. C. Horzinek,, R. J. de Groot, and, H. F. Egberink. 1998. Identification and characterization of a porcine torovirus. J. Virol. 72: 3507– 3511.

50. Lacombe, D.,, F. Lamouliatte,, C. Billeaud, and, B. Sandler. 1988. Virus Breda et entéropathie hémorragique, Rappel á propos d’une observation. Arch. Fr. Pediatr. 45: 442.

51. Lamouliatte, F.,, P. Du Pasquier,, F. Rossi,, J. Laporte, and, J. P. Loze. 1987. Studies on bovine Breda virus. Vet. Microbiol. 15: 261– 278.

52. Lathrop, S. L.,, T. E. Wittum,, K. V. Brock,, S. C. Loerch,, L. J. Perino,, H. R. Bingham,, F. T. McCollum, and, L. J. Saif. 2000. Association between infection of the respiratory tract attributed to bovine coronavirus and health and growth performance of cattle in feedlots. Am. J. Vet. Res. 61: 1062– 1066.

53. Liebler, E. M.,, S. Kluver,, J. F. Pohlenz, and, M. Koopmans. 1992. The significance of bredavirus as a diarrhea agent in calf herds in Lower Saxony. Dtsch. Tieraerztl. Wochenschr. 99: 195– 200.

54. Lin, X. Q.,, K. L. O’Reilly,, J. Storz,, C. W. Purdy, and, R. W. Loan. 2000. Antibody responses to respiratory coronavirus infections of cattle during shipping fever pathogenesis. Arch. Virol. 145: 2335– 2349.

55. Lodha, A.,, N. De Silva,, M. Petric, and, A. M. Moore. 2005. Human torovirus: a new virus associated with neonatal necrotizing enterocolitis. Acta Paediatr. 94: 1085– 1088.

56. Martin, S. W.,, E. Nagy,, P. E. Shewen, and, R. J. Harland. 1998. The association of titers to bovine coronavirus with treatment for bovine respiratory disease and weight gain in feedlot calves. Can. J. Vet. Res. 62: 257– 261.

57. Matiz, K.,, S. Kecskeméti,, I. Kiss,, Z. Adám,, J. Tanyi, and, B. Nagy. 2002. Torovirus detection in faecal specimens of calves and pigs in Hungary: short communication. Acta Vet. Hung. 50: 293– 296.

58. McNulty, M. S.,, D. G. Bryson,, G. M. Allan, and, E. F. Logan. 1984. Coronavirus infection of the bovine respiratory tract. Vet. Microbiol. 9: 425– 434.

59. Middleton, P. J. 1996. Viruses that multiply in the gut and cause endemic and epidemic gastroenteritis. Clin. Diagn. Virol. 6: 93– 101.

60. Muir, P.,, D. A. Harbour,, T. J. Gruffydd-Jones,, P. E. Howard,, C. D. Hopper,, E. A. D. Gruffydd-Jones,, H. M. Broadhead,, C. M. Clarke, and, M. E. Jones. 1990. A clinical and microbiological study of cats with protruding nictitating membranes and diarrhoea: isolation of a novel virus. Vet. Rec. 127: 324– 330.

61. Pérez, E.,, A. Kummeling,, M. M. H. Janssen,, C. Jiménez,, R. Alvarado,, M. Caballero,, P. Donado, and, R. H. Dwinger. 1998. Infectious agents associated with diarrhoea of calves in the canton of Tilarán, Costa Rica. Prev. Vet. Med. 33: 195– 205.

62. Pohlenz, J. F.,, G. N. Woode,, N. F. Cheville,, A. H. Mokresh, and, K. A. Mohammed. 1982. Morphologic lesions in the intestinal mucosa of newborn calves reproduced by unclassified virus (“Breda-virus”), p. 252– 254. In Proceedings of 12th World Congress on Cattle Diseases.

63. Pohlenz, J. F. L.,, N. F. Cheville,, G. N. Woode, and, A. H. Mokresh. 1984. Cellular lesions in intestinal mucosa of gnoto-biotic calves experimentally infected with a new unclassified bovine virus (Breda virus). Vet. Pathol. 21: 407– 417.

64. Reynolds, D. J.,, T. G. Debney,, G. A. Hall,, L. H. Thomas, and, K. R. Parsons. 1985. Studies on the relationship between coronaviruses from the intestinal and respiratory tracts of calves. Arch. Virol. 85: 71– 83.

65. Saif, L. J.,, D. R. Redman,, P. D. Moorhead, and, K. W. Theil. 1986. Experimentally induced coronavirus infections in calves: viral replication in the respiratory and intestinal tract. Am. J. Vet. Res. 47: 1426– 1432.

66. Saif, L. J.,, D. R. Redman,, K. W. Theil,, P. D. Moorhead, and, C. K. Smith. 1981. Studies on an enteric “Breda” virus in calves, abstr. 62, p. 42. In 62nd Annu. Meet. Conf. Res. Workers Anim. Diagn.

67. Scott, A. C.,, M. J. Chaplin,, M. J. Stack, and, L. J. Lund. 1987. Porcine torovirus? Vet. Rec. 120: 583.

68. Scott, F. M. M.,, A. Holliman,, G. W. Jones,, E. W. Gray, and, J. Fitton. 1996. Evidence of torovirus infection in diarrhoeic cattle. Vet. Rec. 138: 284– 285.

69. Snijder, E. J.,, J. Ederveen,, W. J. M. Spaan,, M. Weis, and, M. C. Horzinek. 1988. Characterization of Berne virus genomic and messenger RNAs. J. Gen. Virol. 69: 2135– 2144.

70. Snijder, E. J., and, M. C. Horzinek. 1993. Toroviruses: replication, evolution and comparison with other members of the coronavirus-like superfamily. J. Gen. Virol. 74: 2305– 2316.

71. Snijder, E. J., and, M. C. Horzinek. 1995. The molecular biology of toroviruses, p. 219– 238. In S. G. Siddell (ed.), The Coronaviridae. Plenum Press, New York, NY.

72. Snijder, E. J.,, M. C. Horzinek, and, W. J. M. Spaan. 1994. The coronaviruslike superfamily, p. 235– 244. In H. Laude, and J. F. Vautherot (ed.), Coronaviruses: Molecular Biology and Virus-Host Interactions. Plenum Press, New York, NY.

73. Storz, J.,, C. W. Purdy,, L.-X. Qing,, M. Burrell,, R. E. Truax,, R. E. Briggs,, G. H. Frank, and, R. W. Loan. 2000. Isolation of respiratory bovine coronavirus, other cytocidal viruses, and Pasteurella spp. from cattle involved in two natural outbreaks of shipping fever. J. Am. Vet. Med. Assoc. 216: 1599– 1604.

74. Storz, J.,, L.-X. Qing,, C. W. Purdy,, V. N. Chouljenko,, K. G. Kousoulas,, F. M. Enright,, W. C. Gilmore,, R. E. Briggs, and, R. W. Loan. 2000. Coronavirus and Pasteurella infections in bovine shipping fever pneumonia and Evans’ criteria for causation. J. Clin. Microbiol. 38: 3291– 3297.

75. Storz, J.,, L. Stine,, A. Liem, and, G. A. Anderson. 1996. Coronavirus isolation from nasal swab samples in cattle with signs of respiratory tract disease after shipping. J. Am. Vet. Med. Assoc. 208: 1452– 1455.

76. Tellier, R., and, M. Petric. 1993. Human torovirus—purification from faeces, abstr. W24–4, p. 47. In IXth International Congress of Virology.

77. Thomas, C. J.,, A. E. Hoet,, S. Sreevatsan,, T. E. Wittum,, R. E. Briggs, and, L. J. Saif. 2006. Transmission of bovine corona-virus and serologic responses in feedlot calves under field conditions. Am. J. Vet. Res. 67: 1412– 1420.

78. Vanopdenbosch, E.,, G. Wellemans,, G. Charlier, and, K. Petroff. 1992. Bovine torovirus: cell culture propagation of a respiratory isolate and some epidemiological data. Vlaams Diergeneeskd. Tijdschr. 61: 45– 49.

79. Vanopdenbosch, E.,, G. Wellemans,, J. Oudewater, and, K. Petroff. 1992. Prevalence of torovirus infections in Belgian cattle and their role in respiratory, digestive and reproductive disorders. Vlaams Diergeneeskd. Tijdschr. 61: 187– 191.

80. Vanopdenbosch, E.,, G. Wellemans, and, K. Petroff. 1991. Breda virus associated with respiratory disease in calves. Vet. Rec. 129: 203.

81. Vorster, J. H., and, G. H. Gerdes. 1993. Breda virus-like particles in calves in South Africa. J. S. Afr. Vet. Assoc. 64: 58.

82. Weiss, M., and, M. C. Horzinek. 1987. The proposed family Toroviridae: agents of enteric infections. Arch. Virol. 92: 1– 15.

83. Weiss, M.,, F. Steck, and, M. C. Horzinek. 1983. Purification and partial characterization of a new enveloped RNA virus (Berne virus). J. Gen. Virol. 64: 1849– 1858.

84. Weiss, M.,, F. Steck,, R. Kaderli, and, M. C. Horzinek. 1984. Antibodies to Berne virus in horses and other animals. Vet. Microbiol. 9: 523– 531.

85. Woode, G. N. 1987. Breda and Breda-like viruses: diagnosis, pathology and epidemiology. Ciba Found. Symp. 128: 175– 191.

86. Woode, G. N. 1990. Breda virus, p. 311– 316. In Z. Dinter, and B. Morein (ed.), Virus Infections of Ruminants, 3rd ed. Elsevier Science Publishers B.V., Amsterdam, The Netherlands.

87. Woode, G. N. 1982. Etiology of enteric viral infections of calves: pathological and clinical aspects, p. 201– 208. In Proceedings of 12th World Congress on Cattle Diseases.

88. Woode, G. N. 1994. The Toroviruses: bovine (Breda virus) and equine (Berne virus) and the Torovirus-like agents of humans and animals, p. 581– 602. In A. Z. Kapikian (ed.), Viral Infections of the Gastrointestinal Tract, 2nd ed. Marcel Dekker, New York, NY.

89. Woode, G. N.,, J. F. L. Pohlenz,, N. E. Kelso-Gourley, and, J. A. Fagerland. 1984. Astrovirus and Breda virus infections of dome cell epithelium of bovine ileum. J. Clin. Microbiol. 19: 623– 630.

90. Woode, G. N.,, D. E. Reed,, P. L. Runnels,, M. A. Herrig, and, H. T. Hill. 1982. Studies with an unclassified virus isolated from diarrheic calves. Vet. Microbiol. 7: 221– 240.

91. Woode, G. N.,, L. J. Saif,, M. Quesada,, N. J. Winand,, J. F. L. Pohlenz, and, N. K. Gourley. 1985. Comparative studies on three isolates of Breda virus of calves. Am. J. Vet. Res. 46: 1003– 1010.