Bovine torovirus (Breda virus) revisited

Abstract Bovine torovirus (BoTV) is a pleomorphic virus with a spike-bearing envelope and a linear, non-segmented, positive-sense single-stranded RNA genome. This kidney-shaped virus is associated with diarrhea in calves and apparently has a worldwide distribution. This review provides details of the history and taxonomy of BoTV since its discovery in 1979. Information about virion morphology and architecture, antigenic and biological properties, viral genome, protein composition, thermal and chemical stability, and pH and proteolytic enzymes resistance is also summarized. A major focus of this review is to postulate a possible epidemiological cycle for BoTV, based on epidemiological data obtained in our studies and other published data, and progressing from the newborn calf to the adult animal. The distribution, host range, pathogenesis, disease and clinical signs (under experimental and natural exposure), pathology, diagnosis, prevention, treatment and control of BoTV infections are also described. In addition, a discussion of the zoonotic implications of torovirus-like particles detected in patients with gastroenteritis that resemble and cross-react with BoTV is presented. Hopefully, the findings described here will alert others to the existence of BoTV in cattle and its contribution to the diarrheal disease complex. This review also highlights the need for continual vigilance for potential zoonotic viruses belonging to the order Nidovirales, such as the SARS coronavirus.

[1]  E. Koonin The phylogeny of RNA-dependent RNA polymerases of positive-strand RNA viruses. , 1991, The Journal of general virology.

[2]  I. Kiss,et al.  Torovirus detection in faecal specimens of calves and pigs in Hungary: short communication. , 2002, Acta veterinaria Hungarica.

[3]  Marian C. Horzinek New virus diseases: visible evolution , 1993, Australian veterinary journal.

[4]  G. N. Woode Breda Virus , 1990, Virus Infections of Ruminants.

[5]  M. Brinton,et al.  New Aspects of Positive-Strand Rna Viruses , 1990 .

[6]  Marian C. Horzinek,et al.  The Genome Organization of the Nidovirales: Similarities and Differences between Arteri-, Toro-, and Coronaviruses☆ , 1997, Seminars in Virology.

[7]  A. Gorbalenya,et al.  A comparative sequence analysis to revise the current taxonomy of the family Coronaviridae , 2003, Archives of Virology.

[8]  G. Beards,et al.  AN ENVELOPED VIRUS IN STOOLS OF CHILDREN AND ADULTS WITH GASTROENTERITIS THAT RESEMBLES THE BREDA VIRUS OF CALVES , 1984, The Lancet.

[9]  J. D. den Boon,et al.  Primary structure and post-translational processing of the berne virus peplomer protein☆ , 1990, Virology.

[10]  S. Martin,et al.  The association of titers to bovine coronavirus with treatment for bovine respiratory disease and weight gain in feedlot calves. , 1998, Canadian journal of veterinary research = Revue canadienne de recherche veterinaire.

[11]  V. Mathan,et al.  Prevalence of neutralising antibodies to Berne virus in animals and humans in Vellore, South India , 2005, Archives of Virology.

[12]  Marian C. Horzinek,et al.  A 3'-coterminal nested set of independently transcribed mRNAs is generated during Berne virus replication , 1990, Journal of virology.

[13]  E. Pérez,et al.  Infectious agents associated with diarrhoea of calves in the canton of Tilarán, Costa Rica , 1998, Preventive Veterinary Medicine.

[14]  L. Saif,et al.  Epidemiologic factors and isotype-specific antibody responses in serum and mucosal secretions of dairy calves with bovine coronavirus respiratory tract and enteric tract infections. , 1991, American journal of veterinary research.

[15]  L. Saif,et al.  Viral Diarrheas of Man and Animals , 1989 .

[16]  R. Glass,et al.  Enzyme-linked immunosorbent assay reactivity of torovirus-like particles in fecal specimens from humans with diarrhea , 1993, Journal of clinical microbiology.

[17]  L. Saif,et al.  Comparative studies on three isolates of Breda virus of calves. , 1985, American journal of veterinary research.

[18]  Marian C. Horzinek,et al.  Coronaviruses: structure and genome expression. , 1988, The Journal of general virology.

[19]  G. Beards,et al.  Detection of Breda virus antigen and antibody in humans and animals by enzyme immunoassay , 1987, Journal of clinical microbiology.

[20]  Marian C. Horzinek,et al.  Toroviruses: replication, evolution and comparison with other members of the coronavirus-like superfamily. , 1993, The Journal of general virology.

[21]  K. Holmes Enteric infections with coronaviruses and toroviruses. , 2001, Novartis Foundation symposium.

[22]  J. D. den Boon,et al.  Another triple-spanning envelope protein among intracellularly budding RNA viruses: The torovirus E protein , 1991, Virology.

[23]  S. Zaki,et al.  Optimization of extraction and PCR amplification of RNA extracts from paraffin-embedded tissue in different fixatives , 1993, Journal of Virological Methods.

[24]  Marian C. Horzinek,et al.  cDNA probes for the diagnosis of bovine torovirus (Breda virus) infection , 1991, Journal of clinical microbiology.

[25]  D. Smith,et al.  Epidemiologic herd-level assessment of causative agents and risk factors for winter dysentery in dairy cattle. , 1998, American journal of veterinary research.

[26]  G. Woode Breda and Breda-like viruses: diagnosis, pathology and epidemiology. , 2007, Ciba Foundation symposium.

[27]  M. Koopmans,et al.  Diagnosis of torovirus infection , 1991, The Lancet.

[28]  J. Pohlenz,et al.  A morphological study of the replication of Breda virus (proposed family Toroviridae) in bovine intestinal cells. , 1986, The Journal of general virology.

[29]  Marian C. Horzinek,et al.  Characterization of Berne virus genomic and messenger RNAs. , 1988, The Journal of general virology.

[30]  S. Tzipori,et al.  The relative importance of enteric pathogens affecting neonates of domestic animals. , 1985, Advances in veterinary science and comparative medicine.

[31]  T. Flewett,et al.  Preliminary Characterisation of Torovirus‐Like Particles of Humans: Comparison With Berne Virus of Horses and Breda Virus of Calves , 1986, Journal of medical virology.

[32]  J. Pohlenz,et al.  [The significance of bredavirus as a diarrhea agent in calf herds in Lower Saxony]. , 1992, DTW. Deutsche tierarztliche Wochenschrift.

[33]  L. Saif,et al.  Isolation of bovine respiratory coronaviruses from feedlot cattle and comparison of their biological and antigenic properties with bovine enteric coronaviruses. , 1999, American journal of veterinary research.

[34]  E. Wang,et al.  Human Torovirus: A New Nosocomial Gastrointestinal Pathogen , 1998, The Journal of infectious diseases.

[35]  J. Whelan,et al.  Novel diarrhoea viruses , 1987 .

[36]  Deborah S. Finlaison Faecal viruses of dogs — an electron microscope study , 1995, Veterinary Microbiology.

[37]  C W Ward,et al.  Progress towards a higher taxonomy of viruses , 1993, Research in Virology.

[38]  D. Reynolds,et al.  The in vitro propagation of stunting syndrome agent. , 1998, Avian diseases.

[39]  Marian C. Horzinek,et al.  Purification and partial characterization of a new enveloped RNA virus (Berne virus). , 1983, The Journal of general virology.

[40]  M. Lai,et al.  Recommendations of the coronavirus study group for the nomenclature of the structural proteins, mRNAs, and genes of coronaviruses , 1990, Virology.

[41]  L. Saif,et al.  Comparison of ELISA and RT-PCR versus Immune Electron Microscopy for Detection of Bovine Torovirus (Breda Virus) in Calf Fecal Specimens , 2003, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[42]  B. Morein,et al.  Virus Infections in Ruminants , 1990 .

[43]  V. Chouljenko,et al.  Coronavirus and Pasteurella Infections in Bovine Shipping Fever Pneumonia and Evans' Criteria for Causation , 2000, Journal of Clinical Microbiology.

[44]  L. Saif,et al.  A longitudinal study of bovine coronavirus enteric and respiratory infections in dairy calves in two herds in Ohio☆ , 1990, Veterinary Microbiology.

[45]  D. Reynolds,et al.  Characterization of the stunting syndrome agent: relatedness to known viruses. , 2000, Avian diseases.

[46]  G. H. Frank,et al.  Isolation of respiratory bovine coronavirus, other cytocidal viruses, and Pasteurella spp from cattle involved in two natural outbreaks of shipping fever. , 2000, Journal of the American Veterinary Medical Association.

[47]  D. Cavanagh Nidovirales: a new order comprising Coronaviridae and Arteriviridae. , 1997, Archives of virology.

[48]  Marian C. Horzinek,et al.  Surface proteins of Breda virus. , 1986, American journal of veterinary research.

[49]  J. D. den Boon,et al.  Identification and primary structure of the gene encoding the Berne virus nucleocapsid protein. , 1989, The Journal of general virology.

[50]  D. Reed,et al.  Studies with an unclassified virus isolated from diarrheic calves , 1982, Veterinary Microbiology.

[51]  L. Saif,et al.  Mucosal and systemic antibody responses to bovine coronavirus structural proteins in experimentally challenge-exposed calves fed low or high amounts of colostral antibodies. , 1991, American journal of veterinary research.

[52]  G. H. Gerdes,et al.  Breda virus-like particles in calves in South Africa. , 1992, Journal of the South African Veterinary Association.

[53]  P. Durham,et al.  Viruses and virus-like particles detected during examination of feces from calves and piglets with diarrhea. , 1989, The Canadian veterinary journal = La revue veterinaire canadienne.

[54]  E. Nagy,et al.  Detection of Bovine Torovirus in Fecal Specimens of Calves with Diarrhea from Ontario Farms , 1998, Journal of Clinical Microbiology.

[55]  J. D. den Boon,et al.  The polymerase gene of corona- and toroviruses: evidence for an evolutionary relationship. , 1990, Advances in experimental medicine and biology.

[56]  Marian C. Horzinek,et al.  Hemagglutinin-esterase, a novel structural protein of torovirus , 1997, Journal of virology.

[57]  L. Saif,et al.  Enteric and nasal shedding of bovine torovirus (Breda virus) in feedlot cattle. , 2002, American journal of veterinary research.

[58]  Marian C. Horzinek,et al.  Identification and Characterization of a Porcine Torovirus , 1998, Journal of Virology.

[59]  R. Glass,et al.  Association of torovirus with acute and persistent diarrhea in children. , 1997, The Pediatric infectious disease journal.

[60]  T. Brown,et al.  Coronaviruses and their Diseases , 1990, Advances in Experimental Medicine and Biology.

[61]  Marian C. Horzinek,et al.  Resistance of Berne virus to physical and chemical treatment , 1986, Veterinary Microbiology.

[62]  Marian C. Horzinek,et al.  The proposed family toroviridae: Agents of enteric infections , 1987, Archives of Virology.

[63]  Marian C. Horzinek,et al.  Toroviridae: a taxonomic proposal. , 2010, Zentralblatt fur Veterinarmedizin. Reihe B. Journal of veterinary medicine. Series B.

[64]  H. V. Van Kruiningen,et al.  A Serologic Investigation for Coronavirus and Breda Virus Antibody in Winter Dysentery of Dairy Cattle in the Northeastern United States , 1992, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[65]  A. Kapikian,et al.  Virus infections of the gastrointestinal tract. Infectious Diseases and Antimicrobial Agents. Vol. 3. , 1982 .

[66]  L. Saif,et al.  Detection of Bovine Torovirus and other Enteric Pathogens in Feces from Diarrhea Cases in Cattle , 2003, Journal of veterinary diagnostic investigation : official publication of the American Association of Veterinary Laboratory Diagnosticians, Inc.

[67]  Marian C. Horzinek,et al.  Morphogenesis of Berne virus (proposed family Toroviridae). , 1986, The Journal of general virology.

[68]  A. Gorbalenya,et al.  Comparison of genomic and predicted amino acid sequences of respiratory and enteric bovine coronaviruses isolated from the same animal with fatal shipping pneumonia. , 2001, The Journal of general virology.

[69]  J. D. den Boon,et al.  The carboxyl-terminal part of the putative Berne virus polymerase is expressed by ribosomal frameshifting and contains sequence motifs which indicate that toro- and coronaviruses are evolutionarily related. , 1990, Nucleic acids research.

[70]  Marian C. Horzinek,et al.  The Molecular Biology of Toroviruses , 1995 .

[71]  M. Lai,et al.  The Coronaviridae now comprises two genera, coronavirus and torovirus: report of the Coronaviridae Study Group. , 1993, Advances in experimental medicine and biology.

[72]  Marian C. Horzinek,et al.  Association of diarrhea in cattle with torovirus infections on farms. , 1991, American journal of veterinary research.

[73]  C. Richardson,et al.  The novel hemagglutinin-esterase genes of human torovirus and Breda virus , 1999, Virus Research.

[74]  R. Tellier,et al.  Characterization of torovirus from human fecal specimens. , 1997, Virology.

[75]  G. Anderson,et al.  Coronavirus isolation from nasal swab samples in cattle with signs of respiratory tract disease after shipping. , 1996, Journal of the American Veterinary Medical Association.

[76]  Marian C. Horzinek Toroviruses--members of the coronavirus superfamily? , 1993, Archives of virology. Supplementum.

[77]  L. Saif,et al.  Evaluation of concurrent shedding of bovine coronavirus via the respiratory tract and enteric route in feedlot cattle. , 2001, American journal of veterinary research.

[78]  G. Hall Comparative pathology of infection by novel diarrhoea viruses. , 2007, Ciba Foundation symposium.

[79]  Marian C. Horzinek,et al.  The coronaviruslike superfamily. , 1993, Advances in experimental medicine and biology.

[80]  H. Laude,et al.  Coronaviruses : molecular biology and virus-host interactions , 1993 .

[81]  L. Saif,et al.  Association of enteric shedding of bovine torovirus (Breda virus) and other enteropathogens with diarrhea in veal calves. , 2003, American journal of veterinary research.

[82]  P. Middleton Viruses that multiply in the gut and cause endemic and epidemic gastroenteritis , 1996, Clinical and Diagnostic Virology.

[83]  L. Saif,et al.  Association between infection of the respiratory tract attributable to bovine coronavirus and health and growth performance of cattle in feedlots. , 2000, American journal of veterinary research.

[84]  N. Cheville,et al.  Cellular Lesions in Intestinal Mucosa of Gnotobiotic Calves Experimentally Infected with a New Unclassified Bovine Virus (Breda Virus) , 1984, Veterinary pathology.

[85]  J. Pohlenz,et al.  Astrovirus and Breda virus infections of dome cell epithelium of bovine ileum , 1984, Journal of clinical microbiology.

[86]  R. Tellier,et al.  Bovine torovirus: Sequencing of the structural genes and expression of the nucleocapsid protein of Breda virus , 1998, Virus Research.

[87]  G. Allan,et al.  Coronavirus infection of the bovine respiratory tract , 1984, Veterinary Microbiology.

[88]  Marian C. Horzinek,et al.  Berne virus is not 'coronavirus-like'. , 1984, The Journal of general virology.

[89]  L. Saif,et al.  Experimentally induced coronavirus infections in calves: viral replication in the respiratory and intestinal tracts. , 1986, American journal of veterinary research.

[90]  E. Vanopdenbosch,et al.  Breda virus associated with respiratory disease in calves , 1991, Veterinary Record.

[91]  E. Gray,et al.  Evidence of torovirus infection in diarrhoeic cattle , 1996, Veterinary Record.

[92]  R. Webster,et al.  Encyclopedia of virology , 1999 .

[93]  Marian C. Horzinek,et al.  Seroepidemiology of Breda virus in cattle using ELISA , 1989, Veterinary Microbiology.

[94]  Marian C. Horzinek,et al.  Phylogenetic and Evolutionary Relationships among Torovirus Field Variants: Evidence for Multiple Intertypic Recombination Events , 2003, Journal of Virology.

[95]  Marian C. Horzinek,et al.  Toroviridae: a proposed new family of enveloped RNA viruses. , 2007, Ciba Foundation symposium.

[96]  G. Hall,et al.  Studies on the relationship between coronaviruses from the intestinal and respiratory tracts of calves , 2005, Archives of Virology.

[97]  E. Vanopdenbosch,et al.  Prevalence of torovirus infections in Belgian cattle and their role in respiratory, digestive and reproductive disorders. , 1992 .

[98]  D. L. Hill,et al.  Virus-like particles in a positive case of canine parvovirus enteritis , 1984 .

[99]  Marian C. Horzinek,et al.  Toroviruses of Animals And Humans: A Review , 1994, Advances in Virus Research.

[100]  E. D. Chirnside Equine arteritis virus: An overview , 1992, British Veterinary Journal.

[101]  D. Reynolds,et al.  Stunting syndrome in turkey poults: isolation and identification of the etiologic agent. , 1997, Avian diseases.

[102]  M. Koopmans,et al.  The Pathogenesis of Torovirus Infections in Animals and Humans , 1995 .

[103]  Marian C. Horzinek,et al.  The peplomers of Berne virus. , 1986, The Journal of general virology.

[104]  J. Laporte,et al.  Studies on bovine breda virus , 1987, Veterinary Microbiology.

[105]  Y. L. Lin,et al.  Inhibition of Japanese encephalitis virus infection by nitric oxide: antiviral effect of nitric oxide on RNA virus replication , 1997, Journal of virology.

[106]  E. Peterhans,et al.  The haemagglutinating activity of Berne virus. , 1986, The Journal of general virology.