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Cited by 102Microbial infections and disease researchAnimal Virus Infections StudiesRespiratory viral infections research

Respiratory viruses identified in western Canadian beef cattle by metagenomic sequencing and their association with bovine respiratory disease

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Zhang, Maodong, Hill, Janet E., Fernando, Champika, Alexander, Trevor W., Timsit, Edouard, Meer, Frank, Huang, Yanyun·2019·Transboundary and Emerging Diseases
DOI 10.1111/tbed.13172PMC PMC7168561
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Abstract

Bovine respiratory disease (BRD) causes considerable economic losses in North America. The pathogenesis involves interactions between bacteria, viruses, environment and management factors. Primary viral infection can increase the risk of secondary fatal bacterial infection. The objective of this study was to use metagenomic sequencing to characterize the respiratory viromes of paired nasal swabs and tracheal washes from western Canadian feedlot cattle, with or without BRD. A total of 116 cattle (116 nasal swabs and 116 tracheal washes) were analysed. The presence of influenza D virus (IDV), bovine rhinitis A virus (BRAV), bovine rhinitis B virus (BRBV), bovine coronavirus (BCV) and bovine respiratory syncytial virus (BRSV) was associated with BRD. Agreement between identification of viruses in nasal swabs and tracheal washes was generally weak, indicating that sampling location may affect detection of infection. This study reported several viruses for the first time in Canada and provides a basis for further studies investigating candidate viruses important to the prevention of BRD.

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  • Viral agents such as BRSV, BHV-1, BVDV, influenza D virus, bovine rhinitis viruses, bovine coronaviruses, and parainfluenza-3 virus weaken immune defenses of calves, paving the way for bacterial infections that lead to serious respiratory issues.

    “Viral agents, such as bovine respiratory syncytial virus (BRSV), bovine herpesvirus 1 (BHV-1), bovine viral diarrhea virus (BVDV), influenza D virus, bovine rhinitis viruses, bovine coronaviruses, parainfluenza-3 virus, and others, further weaken the immune defenses of calves, paving the way for bacterial infections that lead to serious respiratory issues [13,47,48].”

    From Strategies for Bovine Respiratory Disease (BRD) Diagnosis and Prognosis: A Comprehensive Overview (2024) · cites this paper as [47]

    The Introduction (page unavailable) says viral infection can interfere with immune defenses and facilitate bacterial infection in the lower respiratory tract. It identifies several listed viruses as BRD pathogens, and the Statistical analyses section associates others with BRD. But the paper does not establish that every listed virus weakens calves’ immune defenses or causes secondary bacterial infection; the claim states that mechanism more definitively than the source does. (LLM, conf=0.85)

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Research works printed but not linked: 35

  1. S Allander, T., Tammi, M. T., Eriksson, M., Bjerkner, A., Tiveljung-Lindell, A., & Andersson, B. (2005). Cloning of a human parvovirus by mo- lecular screening of respiratory tract samples. Proceedings of the National Academy of Sciences of the United States of America, 102, 12891-12896.
  2. Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics (Oxford, England), 30, 2114-2120. https://doi.org/10.1093/bioinformatics/btu170 · DOI · Paper page
  3. Bowland, S. L., & Shewen, P. E. (2000). Bovine respiratory disease: Commercial vaccines currently available in Canada. The Canadian Veterinary Journal, 41, 33-48.
  4. Brister, J. R., Ako-Adjei, D., Bao, Y., & Blinkova, O. (2015). NCBI viral ge- nomes resource. Nucleic Acids Research, 43, D571-577. https://doi. org/10.1093/nar/gku1207 · DOI
  5. Cibulski, S. P., Teixeira, T. F., Dos Santos, H. F., de Sales Lima, F. E., Scheffer, C. M., Varela, A. P., … Roehe, P. M. (2016). Ungulate copi- parvovirus 1 (bovine parvovirus 2): Characterization of a new gen- otype and associated viremia in different bovine age groups. Virus Genes, 52, 134-137. https://doi.org/10.1007/s11262-015-1266-x · DOI
  6. Cohen, J. (1960). A coefficient of agreement for nominal scales. Educational and Psychological Measurement, 20, 37-46. https://doi. org/10.1177/001316446002000104 · DOI · Paper page
  7. Cotmore, S. F., Agbandje-McKenna, M., Chiorini, J. A., Mukha, D. V., Pintel, D. J., Qiu, J., … Davison, A. J. (2014). The family parvoviri- dae. Archives of Virology, 159, 1239-1247. https://doi.org/10.1007/ s00705-013-1914-1 · DOI
  8. Edwards, T. A. (2010). Control methods for bovine respiratory disease for feedlot cattle. The Veterinary Clinics of North America Food Animal Practice, 26, 273-284. https://doi.org/10.1016/j.cvfa.2010.03.005 · DOI
  9. Ellis, J. A. (2009). Update on viral pathogenesis in BRD. Animal Health Research Reviews, 10, 149-153. https://doi.org/10.1017/ S146625230999020X · DOI
  10. Ferguson, L., Olivier, A. K., Genova, S., Epperson, W. B., Smith, D. R., Schneider, L., … Wan, X. F. (2016). Pathogenesis of influenza D virus in cattle. Journal of Virology, 90, 5636-5642. https://doi.org/10.1128/ JVI.03122-15 · DOI
  11. Flynn, O., Gallagher, C., Mooney, J., Irvine, C., Ducatez, M., Hause, B., … Ryan, E. (2018). Influenza D virus in cattle, Ireland. Emerging Infectious Diseases, 24, 389-391. https://doi.org/10.3201/eid2402.170759 · DOI
  12. Fulton, R. W. (2009). Bovine respiratory disease research (1983- 2009). Animal Health Research Reviews, 10, 131-139. https://doi. org/10.1017/S146625230999017X · DOI · Paper page
  13. Hause, B. M., Collin, E. A., Anderson, J., Hesse, R. A., & Anderson, G. (2015). Bovine rhinitis viruses are common in U.S. cattle with bo- vine respiratory disease. PloS One, 10, e0121998. https://doi. org/10.1371/journal.pone.0121998 · DOI
  14. Hause, B. M., Huntimer, L., Falkenberg, S., Henningson, J., Lechtenberg, K., & Halbur, T. (2017). An inactivated influenza D virus vaccine partially protects cattle from respiratory disease caused by homol- ogous challenge. Veterinary Microbiology, 199, 47-53. https://doi. org/10.1016/j.vetmic.2016.12.024 · DOI
  15. Hilton, W. M. (2014). BRD in 2014: Where have we been, where are we now, and where do we want to go? Animal Health Research Reviews, 15, 120-122. https://doi.org/10.1017/S1466252314000115 · DOI
  16. Landis, J. R., & Koch, G. G. (1977). The measurement of observer agree- ment for categorical data. Biometrics, 33, 159-174. https://doi. org/10.2307/2529310 · DOI · Paper page
  17. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., … Durbin, R. (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25, 2078-2079. https://doi.org/10.1093/ bioinformatics/btp352 · DOI · Paper page
  18. Mekata, H., Yamamoto, M., Hamabe, S., Tanaka, H., Omatsu, T., Mizutani, T., … Okabayashi, T. (2018). Molecular epidemiological survey and phylogenetic analysis of bovine influenza D virus in Japan. Transboundary and Emerging Diseases, 65, e355-e360. https://doi. org/10.1111/tbed.12765 · DOI
  19. Mitra, N., Cernicchiaro, N., Torres, S., Li, F., & Hause, B. M. (2016). Metagenomic characterization of the virome associated with bo- vine respiratory disease in feedlot cattle identified novel viruses and suggests an etiologic role for influenza D virus. The Journal of General Virology, 97, 1771-1784. https://doi.org/10.1099/ jgv.0.000492 · DOI
  20. Mosier, D. (2014). Review of BRD pathogenesis: The old and the new. Animal Health Research Reviews, 15, 166-168. https://doi. org/10.1017/S1466252314000176 · DOI
  21. Murray, G. M., O'Neill, R. G., More, S. J., McElroy, M. C., Earley, B., & Cassidy, J. P. (2016). Evolving views on bovine respiratory disease: An appraisal of selected key pathogens -Part 1. Veterinary Journal, 217, 95-102. https://doi.org/10.1016/j.tvjl.2016.09.012 · DOI
  22. Ng, T. F., Kondov, N. O., Deng, X., Van Eenennaam, A., Neibergs, H. L., & Delwart, E. (2015). A metagenomics and case-control study to identify viruses associated with bovine respiratory disease. Journal of Virology, 89, 5340-5349. https://doi.org/10.1128/JVI.00064-15 · DOI · Paper page
  23. Parker, J., & Chen, J. (2017). Application of next generation sequencing for the detection of human viral pathogens in clinical specimens. Journal of Clinical Virology, 86, 20-26. https://doi.org/10.1016/j. jcv.2016.11.010 · DOI
  24. Quast, M., Sreenivasan, C., Sexton, G., Nedland, H., Singrey, A., Fawcett, L., … Li, F. (2015). Serological evidence for the presence of influenza D virus in small ruminants. Veterinary Microbiology, 180, 281-285. https://doi.org/10.1016/j.vetmic.2015.09.005 · DOI
  25. Schmidt, M., Katano, H., Bossis, I., & Chiorini, J. A. (2004). Cloning and characterization of a bovine adeno-associated virus. Journal of Virology, 78, 6509-6516. https://doi.org/10.1128/ jvi.78.12.6509-6516.2004 · DOI
  26. Shan, T., Li, L., Simmonds, P., Wang, C., Moeser, A., & Delwart, E. (2011). The fecal virome of pigs on a high-density farm. Journal of Virology, 85, 11697-11708. https://doi.org/10.1128/JVI.05217-11 · DOI
  27. Snoeck, C. J., Oliva, J., Pauly, M., Losch, S., Wildschutz, F., Muller, C. P., … Ducatez, M. F. (2018). Influenza D virus circulation in cattle and swine, Luxembourg, 2012-2016. Emerging Infectious Diseases, 24, 1388-1389. https://doi.org/10.3201/eid2407.171937 · DOI
  28. Storz, J., Lin, X., Purdy, C. W., Chouljenko, V. N., Kousoulas, K. G., Enright, F. M., … Loan, R. W. (2000). Coronavirus and Pasteurella infections in bovine shipping fever pneumonia and Evans' criteria for causation. Journal of Clinical Microbiology, 38, 3291-3298.
  29. Su, S., Fu, X., Li, G., Kerlin, F., & Veit, M. (2017). Novel influenza D virus: Epidemiology, pathology, evolution and biological characteristics. Virulence, 8, 1580-1591. https://doi.org/10.1080/21505594.2017 · DOI
  30. Taylor, J. D., Fulton, R. W., Lehenbauer, T. W., Step, D. L., & Confer, A. W. (2010). The epidemiology of bovine respiratory disease: What is the evidence for predisposing factors? The Canadian Veterinary Journal, 51, 1095-1102.
  31. Timsit, E., Christensen, H., Bareille, N., Seegers, H., Bisgaard, M., & Assie, S. (2013). Transmission dynamics of Mannheimia haemolytica in newly- received beef bulls at fattening operations. Veterinary Microbiology, 161, 295-304. https://doi.org/10.1016/j.vetmic.2012.07.044 · DOI
  32. Timsit, E., Hallewell, J., Booker, C., Tison, N., Amat, S., & Alexander, T. W. (2017). Prevalence and antimicrobial susceptibility of Mannheimia haemolytica, Pasteurella multocida, and Histophilus somni isolated from the lower respiratory tract of healthy feedlot cattle and those diagnosed with bovine respiratory disease. Veterinary Microbiology, 208, 118-125. https://doi.org/10.1016/j.vetmic.2017.07.013 · DOI
  33. Timsit, E., Workentine, M., van der Meer, F., & Alexander, T. (2018). Distinct bacterial metacommunities inhabit the upper and lower re- spiratory tracts of healthy feedlot cattle and those diagnosed with bronchopneumonia. Veterinary Microbiology, 221, 105-113. https:// doi.org/10.1016/j.vetmic.2018.06.007 · DOI
  34. Zhang, H., Porter, E., Lohman, M., Lu, N., Peddireddi, L., Hanzlicek, G., … Bai, J. (2018). Influenza C virus in cattle with respiratory disease, United States, 2016-2018. Emerging Infectious Diseases, 24, 1926- 1929. https://doi.org/10.3201/eid2410.180589 · DOI
  35. Zhu, L., Xing, Z., Gai, X., Li, S., San, Z., & Wang, X. (2014). Identification of a novel enterovirus E isolates HY12 from cattle with severe re- spiratory and enteric diseases. PloS One, 9, e97730. https://doi. org/10.1371/journal.pone.0097730 · DOI

Cited by

Sorted by citations

Authors
Zhang, M., Hill, J. E., Fernando, C., Alexander, T. W., Timsit, E., Meer, F., & Huang, Y.
Affiliations
  • University of Saskatchewan (CA)
  • Agriculture and Agri-Food Canada (CA)
  • University of Calgary (CA)
Corresponding author
Huang, Yanyun
ORCID
Venue
Transboundary and Emerging Diseases
Publisher
Wiley
Published
2019-04-09
Volume
66
Issue
3
Pages
1379-1386
ISSN
  • 1865-1674 (ISSN-L)
  • 1865-1682
DOI
10.1111/tbed.13172
PMC
PMC7168561
OpenAlex
W2921794314
Cited by
102
References
2
Citations by year
2026: 14 · 2025: 6 · 2024: 19 · 2023: 18 · 2022: 12 · 2021: 12 · 2020: 14 · 2019: 7
FWCI
8.28
Type
journal article
Language
en
Open access
Licence
Locations
  • Transboundary and Emerging Diseases (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • China Scholarship Council
  • Alberta Livestock and Meat Agency
Topics
  • Life Sciences › Immunology and Microbiology › Microbiology › Microbial infections and disease research
  • Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Virus Infections Studies
  • Health Sciences › Medicine › Epidemiology › Respiratory viral infections research
Keywords
bovine respiratory disease, respiratory viruses, virome, feedlot cattle, influenza D virus, bovine coronavirus, bovine respiratory syncytial virus, nasal swabs, tracheal wash, sampling sites
MeSH terms
Animals, Canada, Cattle, Cattle Diseases, Aphthovirus, Respiratory Tract Infections, RNA Virus Infections, RNA Viruses, Genome, Viral, Coronavirus, Bovine, Respiratory Syncytial Virus, Bovine, Thogotovirus, Metagenomics

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