Bovine Coronavirus Infection: Pathology and Interspecies Transmission
*Dairy Hygiene Research Division, Hokkaido Research Station, National Institute of Animal Health, 4 Hitsujigaoka, Toyohira, Sapporo, Hokkaido 062-0045, Japan
**United Graduate School of Veterinary Sciences, Gifu University, 1-1 Yanagido, Gifu 501-1193, Japan
Bovine diarrhea is one of the major diseases that cause major economic damage to farmers. There are many kinds of viral diseases that cause diarrhea in cattle. Among them, bovine coronavirus infection and bovine rotavirus infection are known as diseases that frequently occur throughout the world, and whose incidence and numbers of infected cattle are particularly large. Both viruses cause diarrhea in newborn calves, but bovine coronavirus (BCoV), lead to more economic damage because they also cause a type of diarrhea in adult cattle called winter dysentery (WD) and respiratory disease. However, since it is generally difficult to isolate coronaviruses from cultured cells, and these viruses have huge RNAs of about 30kb, research on coronaviruses, including genomic analysis, have not advanced sufficiently to cope with this problem. Recent reports have suggested that BCoV is able to overcome host range barriers with relative ease and even to transmit to humans. It has thus become necessary to consider their significance as zoonosis, even though much about the ecology of BCoV remains unknown. This paper will outline bovine coronavirus infection and describe BCoV characteristics that have been reported so far.
-  M. M. Lai, S. Perlman, and L. J. Anderson, “Coronaviridae,” in D. M. Knipe, P. M. Howley (Eds.), “Fields Virology,” 5th ed., Philadelphia, Lippincott Williams and Wilkins, p. 1305-1335, 2006.
-  D. A. Brian and R. S. Baric, “Coronavirus genome structure and replication,” Curr. Top Microbiol. Immunol., Vol.287, pp. 1-30, 2005.
-  International Committee on Taxonomy of Viruses: ICTV,
-  M. L. Ballesteros, C. M. Sanchez, and L. Enjuanes, “Two amino acid changes at the N-terminus of transmissible gastroenteritis coronavirus spike protein result in the loss of enteric tropism,” Virology, Vol.227, No.2, pp. 378-388, 1997.
-  J. K. Fazakerley, S. E. Parker, F. Bloom, and M. J. Buchmeier, “The V5A13.1 envelope glycoprotein deletion mutant of mouse hepatitis virus type-4 is neuroattenuated by its reduced rate of spread in the central nervous system,” Virology, Vol.187, No.1, pp. 178-188, 1992.
-  S. T. Hingley, J. L. Gombold, E. Lavi, and S. R. Weiss, “MHV-A59 fusion mutants are attenuated and display altered hepatotropism,” Virology, Vol.200, No.1, pp. 1-10, 1994.
-  B. Schultze, H. J. Gross, R. Brossmer, and G. Herrler, “The S protein of bovine coronavirus is a hemagglutinin recognizing 9-Oacetylated sialic acid as a receptor determinant,” J. Virol., Vol.65, No.11, pp. 6232-6237, 1991.
-  S. Takase-Yoden, T. Kikuchi, S. G. Siddell, and F. Taguchi, “Localization of major neutralizing epitopes on the S1 polypeptide of the murine coronavirus peplomer glycoprotein,” Virus Res., Vol.18, No.2-3, pp. 99-107, 1991.
-  D. Yoo and D. Deregt, “A single amino acid change within antigenic domain II of the spike protein of bovine coronavirus confers resistance to virus neutralization,” Clin. Diagn. Lab. Immunol., Vol.8, No.2, pp. 297-302, 2001.
-  C. A. Mebus, E. L. Stair, M. B. Rhodes, and M. J. Twiehaus, “Neonatal calf diarrhea: propagation, attenuation, and characteristics of a coronavirus-like agent,” Am. J. Vet. Res., Vol.34, No.2, pp. 145-150, 1973.
-  R. L. Sharpee, C. A. Mebus, and E. P. Bass, “Characterization of a calf diarrheal coronavirus,” Am. J. Vet. Res., Vol.37, No.9, pp. 1031-1041, 1976.
-  D. A. Benfield and L. J. Saif, “Cell culture propagation of a coronavirus isolated from cows with winter dysentery,” J. Clin. Microbiol., Vol.28, No.6, pp. 1454-1457, 1990.
-  L. J. Saif, K. V. Brock, D. R. Redman, and E. M. Kohler, “Winter dysentery in dairy herds: electron microscopic and serological evidence for an association with coronavirus infection,” Vet. Rec., Vol.128, No.19, pp. 447-449, 1991.
-  M. Hasoksuz, S. L. Lathrop, K. L. Gadfield, and L. J. Saif, “Isolation of bovine respiratory coronaviruses from feedlot cattle and comparison of their biological and antigenic properties with bovine enteric coronaviruses,” Am. J. Vet. Res., Vol.60, No.10, pp. 1227-1233, 1999.
-  S. L. Lathrop, T. E.Wittum, K. V. Brock, S. C. Loerch, L. J. Perino, H. R. Bingham, F. T. McCollum, and L. J. Saif, “Association between infection of the respiratory tract attributable to bovine coronavirus and health and growth performance of cattle in feedlots,” Am. J. Vet. Res., Vol.61, No.9, pp. 1062-1066, 2000.
-  J. Storz, L. Stine, A. Liem, and G. A. Anderson, “Coronavirus isolation from nasal swab samples in cattle with signs of respiratory tract disease after shipping,” J. Am. Vet. Med. Assoc., Vol.208, No.9, pp. 1452-1455, 1996.
-  R. A. Heckert, L. J. Saif, K. H. Hoblet, and A. G. Agnes, “A longitudinal study of bovine coronavirus enteric and respiratory infections in dairy calves in two herds in Ohio,” Vet. Microbiol., Vol.22, No.2-3, pp. 187-201, 1990.
-  M. S. McNulty, D. G. Bryson, G. M. Allan, and E. F. Logan, “Coronavirus infection of the bovine respiratory tract,” Vet. Microbiol., Vol.9, No.5, pp. 425-434, 1984.
-  D. J. Reynolds, T. G. Debney, G. A. Hall, L. H. Thomas, and K. R. Parsons, “Studies on the relationship between coronaviruses from the intestinal and respiratory tracts of calves,” Arch. Virol., Vol.85, Nos.1-2, pp. 71-83, 1985.
-  L. H. Thomas, R. N. Gourlay, E. J. Stott, C. J. Howard, and J. C. Bridger, “A search for new microorganisms in calf pneumonia by the inoculation of gnotobiotic calves,” Res. Vet. Sci., Vol.33, No.2, pp. 170-182, 1982.
-  S. L. Lathrop, T. E. Wittum, S. C. Loerch, L. J. Perino, and L. J. Saif, “Antibody titers against bovine coronavirus and shedding of the virus via the respiratory tract in feedlot cattle,” Am. J. Vet. Res., Vol.61, No.9, pp. 1057-1061, 2000.
-  D. Rasschaert, M. Duarte, and H. Laude, “Porcine respiratory coronavirus differs from transmissible gastroenteritis virus by a few genomic deletions,” J. Gen. Virol., Vol.71, No.11, pp. 2599-2607, 1990.
-  R. D.Wesley, R. D.Woods, and A. K. Cheung, “Genetic analysis of porcine respiratory coronavirus, an attenuated variant of transmissible gastroenteritis virus,” J. Virol., Vol.65, No.6, pp. 3369-3373, 1991.
-  S. Bernard and H. Laude, “Site-specific alteration of transmissible gastroenteritis virus spike protein results in markedly reduced pathogenicity,” J. Gen. Virol., Vol.76, No.9, pp. 2235-2241, 1995.
-  C. Krempl, B. Schultze, H. Laude, and G. Herrler, “Point mutations in the S protein connect the sialic acid binding activity with the enteropathogenicity of transmissible gastroenteritis coronavirus,” J. Virol., Vol.71, No.4, pp. 3285-3287, 1997.
-  V. N. Chouljenko, K. G. Kousoulas, X. Lin, and J. Storz, “Nucleotide and predicted amino acid sequences of all genes encoded by the 3’ genomic portion (9.5 kb) of respiratory bovine coronaviruses and comparisons among respiratory and enteric coronaviruses,” Virus Genes, Vol.17, No.1, pp. 33-42, 1998.
-  V. N. Chouljenko, X. Q. Lin, J. Storz, K. G. Kousoulas, and A. E. Gorbalenya, “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., Vol.82, No.12, pp. 2927-2933, 2001.
-  M. Hasoksuz, S. Sreevatsan, K. O. Cho, A. E. Hoet, and L. J. Saif, “Molecular analysis of the S1 subunit of the spike glycoprotein of respiratory and enteric bovine coronavirus isolates,” Virus Res., Vol.84, Nos.1-2, pp. 101-109, 2002.
-  J. H. Jeong, G. Y. Kim, S. S. Yoon, S. J. Park, Y. J. Kim, C. M. Sung, S. S. Shin, B. J. Lee, M. I. Kang, N. Y. Park, H. B. Koh, and K. O. Cho, “Molecular analysis of S gene of spike glycoprotein of winter dysentery bovine coronavirus circulated in Korea during 2002-2003,” Virus Res., Vol.108, Nos.1-2, pp. 207-212, 2005.
-  T. Kanno, S. Hatama, R. Ishihara, and I. Uchida, “Molecular analysis of the S glycoprotein gene of bovine coronaviruses isolated in Japan from 1999 to 2006,” J. Gen. Virol., Vol.88, No.4, pp. 1218-1224, 2007.
-  M. Hasoksuz, S. Lathrop, M. A. Al-dubaib, P. Lewis, and L. J. Saif, “Antigenic variation among bovine enteric coronaviruses (BECV) and bovine respiratory coronaviruses (BRCV) detected using monoclonal antibodies,” Arch. Virol., Vol.144, No.12, pp. 2441-2447, 1999.
-  H. Tsunemitsu, Z. R. el-Kanawati, D. R. Smith, H. H. Reed, and L. J. Saif, “Isolation of coronaviruses antigenically indistinguishable from bovine coronavirus from wild ruminants with diarrhea,” J. Clin. Microbiol., Vol.33, No.12, pp. 3264-3269, 1995.
-  L. J. Saif, D. R. Redman, P. D. Moorhead, and K.W. Theil, “Experimentally induced coronavirus infections in calves: viral replication in the respiratory and intestinal tracts,” Am. J. Vet. Res., Vol.47, No.7, pp. 1426-1432, 1986.
-  L. J. Saif and K. L. Smith, “Enteric viral infections of calves and passive immunity,” J. Dairy Sci., Vol.68, No.1, pp. 206-228, 1985.
-  C. J. Thomas, A. E. Hoet, S. Sreevatsan, T. E.Wittum, R. E. Briggs, G. C. Duff, and L. J. Saif, “Transmission of bovine coronavirus and serologic responses in feedlot calves under field conditions,” Am. J. Vet. Res., Vol.67, No.8, pp. 1412-1420, 2006.
-  S. J. Park, G. Y. Kim, H. E. Choy, Y. J. Hong, L. J. Saif, J. H. Jeong, S. I. Park, H. H. Kim, S. K. Kim, S. S. Shin, M. I. Kang, and K. O. Cho, “Dual enteric and respiratory tropisms of winter dysentery bovine coronavirus in calves,” Arch. Virol., Vol.152, No.10, pp. 1885-1900, 2007.
-  K. O. Cho, A. E. Hoet, S. C. Loerch, T. E. Wittum, and L. J. Saif, “Evaluation of concurrent shedding of bovine coronavirus via the respiratory tract and enteric route in feedlot cattle,” Am. J. Vet. Res., Vol.62, No.9, pp. 1436-1441, 2001.
-  C. F. Crouch, T. J. Raybould, and S. D. Acres, “Monoclonal antibody capture enzyme-linked immunosorbent assay for detection of bovine enteric coronavirus,” J. Clin. Microbiol., Vol.19, No.3, pp. 388-393, 1984.
-  J. K. Collins, C. A. Riegel, J. D. Olson, and A. Fountain, “Shedding of enteric coronavirus in adult cattle,” Am. J. Vet. Res., Vol.48, No.3, pp. 361-365, 1987.
-  Y. Hoshino and F.W. Scott, “Coronavirus-like particles in the feces of normal cats,” Arch. Virol., Vol.63, No.2, pp. 147-152, 1980.
-  N. R. Underdahl, C. A. Mebus, and A. Torres-Medina, “Recovery of transmissible gastroenteritis virus from chronically infected experimental pigs,” Am. J. Vet. Res., Vol.36, No.10, pp. 1473-1476, 1975.
-  F. P. Williams, Jr., “Astrovirus-like, coronavirus-like, and parvovirus-like particles detected in the diarrheal stools of beagle pups,” Arch. Virol., Vol.66, No.3, pp. 215-226, 1980.
-  S. L. Schoenthaler and S. Kapil, “Development and applications of a bovine coronavirus antigen detection enzyme-linked immunosorbent assay,” Clin. Diagn. Lab. Immunol., Vol.6, No.1, pp. 130-132, 1999.
-  M. R. Rekik and S. Dea, “Comparative sequence analysis of a polymorphic region of the spike glycoprotein S1 subunit of enteric bovine coronavirus isolates,” Arch. Virol., Vol.135, Nos.3-4, pp. 319-331, 1994.
-  P. E. Brandao, F. Gregori, L. J. Richtzenhain, C. A. Rosales, L. Y. Villarreal, and J. A. Jerez, “Molecular analysis of Brazilian strains of bovine coronavirus (BCoV) reveals a deletion within the hypervariable region of the S1 subunit of the spike glycoprotein also found in human coronavirus OC43,” Arch. Virol., Vol.151, No.9, pp. 1735-1748, 2006.
-  C. K. Ko, M. I. Kang, G. K. Lim, G. Y. Kim, S. S. Yoon, J. T. Park, C. Jeong, S. H. Park, S. J. Park, Y. J. Kim, J. H. Jeong, S. K. Kim, S. I. Park, H. H. Kim, K. Y. Kim, and K. O. Cho, “Molecular characterization of HE, M, and E genes of winter dysentery bovine coronavirus circulated in Korea during 2002-2003,” Virus Genes, Vol.32, No.2, pp. 129-136, 2006.
-  L. Liu, S. Hagglund, M. Hakhverdyan, S. Alenius, L. E. Larsen, and S. Belak, “Molecular epidemiology of bovine coronavirus on the basis of comparative analyses of the S gene,” J. Clin. Microbiol., Vol.44, No.3, pp. 957-960, 2006.
-  S. J. Park, G. K. Lim, S. I. Park, H. H. Kim, H. B. Koh, and K. O. Cho, “Detection and molecular characterization of calf diarrhoea bovine coronaviruses circulating in South Korea during 2004-2005,” Zoonoses Public Health, Vol.54, Nos.6-7, pp. 223-230, 2007.
-  T. Kanno, T. Kamiyoshi, R. Ishihara, S. Hatama, and I. Uchida, “Phylogenetic studies of bovine coronaviruses isolated in Japan,” J. Vet. Med. Sci., Vol.71, No.1, pp. 83-86, 2009.
-  M. Hasoksuz, K. Alekseev, A. Vlasova, X. Zhang, D. Spiro, R. Halpin, S.Wang, E. Ghedin, and L. J. Saif, “Biologic, antigenic, and full-length genomic characterization of a bovine-like coronavirus isolated from a giraffe,” J. Virol., Vol.81, No.10, pp. 4981-4990, 2007.
-  F. Majhdi, H. C. Minocha, and S. Kapil, “Isolation and characterization of a coronavirus from elk calves with diarrhea,” J. Clin. Microbiol., Vol.35, No.11, pp. 2937-2942, 1997.
-  C. K. Cebra, D. E. Mattson, R. J. Baker, R. J. Sonn, and P. L. Dearing, “Potential pathogens in feces from unweaned llamas and alpacas with diarrhea,” J. Am. Vet. Med. Assoc., Vol.223, No.12, pp. 1806-1808, 2003.
-  K. P. Alekseev, A. N. Vlasova, K. Jung, M. Hasoksuz, X. Zhang, R. Halpin, S. Wang, E. Ghedin, D. Spiro, and L. J. Saif, “Bovine-like coronaviruses isolated from four species of captive wild ruminants are homologous to bovine coronaviruses, based on complete genomic sequences,” J. Virol., Vol.82, No.24, pp. 12422-12431, 2008.
-  L. Jin, C. K. Cebra, R. J. Baker, D. E. Mattson, S. A. Cohen, D. E. Alvarado, and G. F. Rohrmann, “Analysis of the genome sequence of an alpaca coronavirus,” Virology, Vol.365, No.1, pp. 198-203, 2007.
-  N. Decaro, V. Martella, G. Elia, M. Campolo, V. Mari, C. Desario, M. S. Lucente, A. Lorusso, G. Greco, M. Corrente, M. Tempesta, and C. Buonavoglia, “Biological and genetic analysis of a bovine-like coronavirus isolated from water buffalo (Bubalus bubalis) calves,” Virology, Vol.370, No.1, pp. 213-222, 2008.
-  L. Vijgen, E. Keyaerts, E. Moes, I. Thoelen, E. Wollants, P. Lemey, A. M. Vandamme, and M. Van Ranst, “Complete genomic sequence of human coronavirus OC43: molecular clock analysis suggests a relatively recent zoonotic coronavirus transmission event,” J. Virol., Vol.79, No.3, pp. 1595-1604, 2005.
-  L. Vijgen, E. Keyaerts, P. Lemey, P. Maes, K. Van Reeth, H. Nauwynck, M. Pensaert, and M. Van Ranst, “Evolutionary history of the closely related group 2 coronaviruses: porcine hemagglutinating encephalomyelitis virus, bovine coronavirus, and human coronavirus OC43,” J. Virol., Vol.80, No.14, pp. 7270-7274, 2006.
-  X. M. Zhang, W. Herbst, K. G. Kousoulas, and J. Storz, “Biological and genetic characterization of a hemagglutinating coronavirus isolated from a diarrhoeic child,” J. Med. Virol., Vol.44, No.2, pp. 152-161, 1994.
-  K. Erles, C. Toomey, H. W. Brooks, and J. Brownlie, “Detection of a group 2 coronavirus in dogs with canine infectious respiratory disease,” Virology, Vol.310, No.2, pp. 216-223, 2003.
-  T. Kaneshima, T. Hohdatsu, K. Satoh, T. Takano, K. Motokawa, and H. Koyama, “The prevalence of a group 2 coronavirus in dogs in Japan,” J. Vet. Med. Sci., Vol.68, No.1, pp. 21-25, 2006.
-  S. L. Priestnall, J. Brownlie, E. J. Dubovi, and K. Erles, “Serological prevalence of canine respiratory coronavirus,” Vet. Microbiol., Vol.115, Nos.1-3, pp. 43-53, 2006.
-  T. Kaneshima, T. Hohdatsu, R. Hagino, S. Hosoya, Y. Nojiri, M. Murata, T. Takano, M. Tanabe, H. Tsunemitsu, and H. Koyama, “The infectivity and pathogenicity of a group 2 bovine coronavirus in pups,” J. Vet. Med. Sci., Vol.69, No.3, pp. 301-303, 2007.
-  K. Erles, K. B. Shiu, and J. Brownlie, “Isolation and sequence analysis of canine respiratory coronavirus,” Virus Res., Vol.124, Nos.1-2, pp. 78-87, 2007.
-  M. M. Ismail, K. O. Cho, L. A.Ward, L. J. Saif, and Y.M. Saif, “Experimental bovine coronavirus in turkey poults and young chickens,” Avian Dis., Vol.45, No.1, pp. 157-163, 2001.
This article is published under a Creative Commons Attribution-NoDerivatives 4.0 Internationa License.