Influenza C Virus in Cattle with Respiratory Disease, United States, 2016–2018
Identifieur interne : 000529 ( Pmc/Corpus ); précédent : 000528; suivant : 000530Influenza C Virus in Cattle with Respiratory Disease, United States, 2016–2018
Auteurs : Hewei Zhang ; Elizabeth Porter ; Molly Lohman ; Nanyan Lu ; Lalitha Peddireddi ; Gregg Hanzlicek ; Douglas Marthaler ; Xuming Liu ; Jianfa BaiSource :
- Emerging Infectious Diseases [ 1080-6040 ] ; 2018.
Abstract
We identified influenza C virus (ICV) in samples from US cattle with bovine respiratory disease through real-time PCR testing and sequencing. Bovine ICV isolates had high nucleotide identities (≈98%) with each other and were closely related to human ICV strains (≈95%). Further research is needed to determine bovine ICV’s zoonotic potential.
Url:
DOI: 10.3201/eid2410.180589
PubMed: 30226175
PubMed Central: 6154146
Links to Exploration step
PMC:6154146Le document en format XML
<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Influenza C Virus in Cattle with Respiratory Disease, United States, 2016–2018</title><author><name sortKey="Zhang, Hewei" sort="Zhang, Hewei" uniqKey="Zhang H" first="Hewei" last="Zhang">Hewei Zhang</name></author><author><name sortKey="Porter, Elizabeth" sort="Porter, Elizabeth" uniqKey="Porter E" first="Elizabeth" last="Porter">Elizabeth Porter</name></author><author><name sortKey="Lohman, Molly" sort="Lohman, Molly" uniqKey="Lohman M" first="Molly" last="Lohman">Molly Lohman</name></author><author><name sortKey="Lu, Nanyan" sort="Lu, Nanyan" uniqKey="Lu N" first="Nanyan" last="Lu">Nanyan Lu</name></author><author><name sortKey="Peddireddi, Lalitha" sort="Peddireddi, Lalitha" uniqKey="Peddireddi L" first="Lalitha" last="Peddireddi">Lalitha Peddireddi</name></author><author><name sortKey="Hanzlicek, Gregg" sort="Hanzlicek, Gregg" uniqKey="Hanzlicek G" first="Gregg" last="Hanzlicek">Gregg Hanzlicek</name></author><author><name sortKey="Marthaler, Douglas" sort="Marthaler, Douglas" uniqKey="Marthaler D" first="Douglas" last="Marthaler">Douglas Marthaler</name></author><author><name sortKey="Liu, Xuming" sort="Liu, Xuming" uniqKey="Liu X" first="Xuming" last="Liu">Xuming Liu</name></author><author><name sortKey="Bai, Jianfa" sort="Bai, Jianfa" uniqKey="Bai J" first="Jianfa" last="Bai">Jianfa Bai</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">30226175</idno><idno type="pmc">6154146</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6154146</idno><idno type="RBID">PMC:6154146</idno><idno type="doi">10.3201/eid2410.180589</idno><date when="2018">2018</date><idno type="wicri:Area/Pmc/Corpus">000529</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000529</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Influenza C Virus in Cattle with Respiratory Disease, United States, 2016–2018</title><author><name sortKey="Zhang, Hewei" sort="Zhang, Hewei" uniqKey="Zhang H" first="Hewei" last="Zhang">Hewei Zhang</name></author><author><name sortKey="Porter, Elizabeth" sort="Porter, Elizabeth" uniqKey="Porter E" first="Elizabeth" last="Porter">Elizabeth Porter</name></author><author><name sortKey="Lohman, Molly" sort="Lohman, Molly" uniqKey="Lohman M" first="Molly" last="Lohman">Molly Lohman</name></author><author><name sortKey="Lu, Nanyan" sort="Lu, Nanyan" uniqKey="Lu N" first="Nanyan" last="Lu">Nanyan Lu</name></author><author><name sortKey="Peddireddi, Lalitha" sort="Peddireddi, Lalitha" uniqKey="Peddireddi L" first="Lalitha" last="Peddireddi">Lalitha Peddireddi</name></author><author><name sortKey="Hanzlicek, Gregg" sort="Hanzlicek, Gregg" uniqKey="Hanzlicek G" first="Gregg" last="Hanzlicek">Gregg Hanzlicek</name></author><author><name sortKey="Marthaler, Douglas" sort="Marthaler, Douglas" uniqKey="Marthaler D" first="Douglas" last="Marthaler">Douglas Marthaler</name></author><author><name sortKey="Liu, Xuming" sort="Liu, Xuming" uniqKey="Liu X" first="Xuming" last="Liu">Xuming Liu</name></author><author><name sortKey="Bai, Jianfa" sort="Bai, Jianfa" uniqKey="Bai J" first="Jianfa" last="Bai">Jianfa Bai</name></author></analytic><series><title level="j">Emerging Infectious Diseases</title><idno type="ISSN">1080-6040</idno><idno type="eISSN">1080-6059</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>We identified influenza C virus (ICV) in samples from US cattle with bovine respiratory disease through real-time PCR testing and sequencing. Bovine ICV isolates had high nucleotide identities (≈98%) with each other and were closely related to human ICV strains (≈95%). Further research is needed to determine bovine ICV’s zoonotic potential.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct></listBibl></div1></back></TEI><pmc article-type="brief-report"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Emerg Infect Dis</journal-id><journal-id journal-id-type="iso-abbrev">Emerging Infect. Dis</journal-id><journal-id journal-id-type="publisher-id">EID</journal-id><journal-title-group><journal-title>Emerging Infectious Diseases</journal-title></journal-title-group><issn pub-type="ppub">1080-6040</issn><issn pub-type="epub">1080-6059</issn><publisher><publisher-name>Centers for Disease Control and Prevention</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">30226175</article-id><article-id pub-id-type="pmc">6154146</article-id><article-id pub-id-type="publisher-id">18-0589</article-id><article-id pub-id-type="doi">10.3201/eid2410.180589</article-id><article-categories><subj-group subj-group-type="heading"><subject>Dispatch</subject></subj-group><subj-group subj-group-type="article-type"><subject>Dispatch</subject></subj-group><subj-group subj-group-type="TOC-title"><subject>Influenza C Virus in Cattle with Respiratory Disease, United States, 2016–2018</subject></subj-group></article-categories><title-group><article-title>Influenza C Virus in Cattle with Respiratory Disease, United States, 2016–2018</article-title><alt-title alt-title-type="running-head">Influenza C Virus in Cattle, United States</alt-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Zhang</surname><given-names>Hewei</given-names></name></contrib><contrib contrib-type="author"><name><surname>Porter</surname><given-names>Elizabeth</given-names></name></contrib><contrib contrib-type="author"><name><surname>Lohman</surname><given-names>Molly</given-names></name></contrib><contrib contrib-type="author"><name><surname>Lu</surname><given-names>Nanyan</given-names></name></contrib><contrib contrib-type="author"><name><surname>Peddireddi</surname><given-names>Lalitha</given-names></name></contrib><contrib contrib-type="author"><name><surname>Hanzlicek</surname><given-names>Gregg</given-names></name></contrib><contrib contrib-type="author"><name><surname>Marthaler</surname><given-names>Douglas</given-names></name></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Liu</surname><given-names>Xuming</given-names></name></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Bai</surname><given-names>Jianfa</given-names></name></contrib><aff id="aff1">Chinese Academy of Agricultural Sciences, Institute of Special Economic Animal and Plant Sciences, Changchun, China (H. Zhang);</aff><aff id="aff2">Kansas State University Veterinary Diagnostic Laboratory, Manhattan, Kansas, USA (H. Zhang, E. Porter, M. Lohman, N. Lu, L. Peddireddi, G. Hanzlicek, D. Marthaler, X. Liu, J. Bai)</aff></contrib-group><author-notes><corresp id="cor1">Address for correspondence: Jianfa Bai or Xuming Liu, Kansas State University, Veterinary Diagnostic Laboratory, College of Veterinary Medicine, 2005 Research Park Cir, Manhattan, KS 66502, USA; email: <email xlink:href="jbai@vet.ksu.edu">jbai@vet.ksu.edu</email> or <email xlink:href="xmliu@vet.ksu.edu">xmliu@vet.ksu.edu</email></corresp></author-notes><pub-date pub-type="ppub"><month>10</month><year>2018</year></pub-date><volume>24</volume><issue>10</issue><fpage>1926</fpage><lpage>1929</lpage><abstract><p>We identified influenza C virus (ICV) in samples from US cattle with bovine respiratory disease through real-time PCR testing and sequencing. Bovine ICV isolates had high nucleotide identities (≈98%) with each other and were closely related to human ICV strains (≈95%). Further research is needed to determine bovine ICV’s zoonotic potential.</p></abstract><kwd-group kwd-group-type="author"><title>Keywords: </title><kwd>influenza C virus</kwd><kwd>cattle</kwd><kwd>bovine respiratory disease</kwd><kwd>BRDC</kwd><kwd>bovine respiratory disease complex</kwd><kwd>United States</kwd><kwd>USA</kwd><kwd>Midwest</kwd><kwd>Oklahoma</kwd><kwd>Montana</kwd><kwd>Texas</kwd><kwd>Kansas</kwd><kwd>Missouri</kwd><kwd>Colorado</kwd><kwd>Nebraska</kwd><kwd>livestock</kwd><kwd>cows</kwd><kwd>zoonoses</kwd><kwd>respiratory infections</kwd><kwd>viruses</kwd><kwd>influenza virus</kwd><kwd>influenza</kwd></kwd-group></article-meta></front><body><p>Influenza viruses are contagious zoonotic pathogens that belong to the <italic>Orthomyxoviridae</italic> family, which consists of 4 genera: <italic>Alphainfluenzavirus</italic> (influenza A virus), <italic>Betainfluenzavirus</italic> (influenza B virus), <italic>Gammainfluenzavirus</italic> (influenza C virus [ICV]), and <italic>Deltainfluenzavirus</italic> (influenza D virus) (<xref rid="R1" ref-type="bibr"><italic>1</italic></xref>–<xref rid="R4" ref-type="bibr"><italic>4</italic></xref>). Classification of influenza viruses is based on the antigenic differences in the nucleoprotein and matrix protein and supported by intergenic homologies of 20%–30% and intragenic homologies >85% (<xref rid="R3" ref-type="bibr"><italic>3</italic></xref>).</p><p>The most common influenza pathogen is influenza A virus, which can infect humans, pigs, cattle, birds, as well as other animals (<xref rid="R2" ref-type="bibr"><italic>2</italic></xref>,<xref rid="R4" ref-type="bibr"><italic>4</italic></xref>). ICV was first identified in humans in 1947. This group of influenza viruses was initially thought to exclusively infect humans until isolates were identified in pigs in China (<xref rid="R5" ref-type="bibr"><italic>5</italic></xref>,<xref rid="R6" ref-type="bibr"><italic>6</italic></xref>) and Japan (<xref rid="R7" ref-type="bibr"><italic>7</italic></xref>). Antigenic and genetic analyses suggest that ICV might transmit between humans and pigs in nature (<xref rid="R8" ref-type="bibr"><italic>8</italic></xref>); however, interspecies transmission has not been confirmed experimentally. In 2011, an influenza C–like virus was identified in swine and cattle in the United States (<xref rid="R9" ref-type="bibr"><italic>9</italic></xref>); this virus was initially proposed to be an ICV subtype but was later identified as influenza D virus (<xref rid="R3" ref-type="bibr"><italic>3</italic></xref>) because the virus had ≈50% overall amino acid identity with human ICV strains, a level of divergence similar to that between influenza A and influenza B viruses.</p><p>Although influenza viruses of other genera can infect cattle, the potential for ICV infection in cattle has not been previously investigated. The objective of this study was to determine if ICV can be found in specimens from cattle with bovine respiratory disease and, if so, determine the prevalence.</p><sec><title>The Study</title><p>Bovine respiratory disease complex (BRDC) is one of the most common causes of death in livestock in US feedlots and feedlots worldwide (<xref rid="R10" ref-type="bibr"><italic>10</italic></xref>). During October 2016–January 2018, we collected 1,525 samples (mainly nasal swab and lung tissue specimens) from cattle in the Midwest of the United States and submitted them to Kansas State Veterinary Diagnostic Laboratory (Manhattan, Kansas, USA) for BRDC diagnostic testing. We screened samples for ICV by real-time reverse transcription PCR, as well as for 10 other BRDC-associated pathogens (<italic>Mannheimia haemolytica</italic>, <italic>Pasteurella multocida</italic>, <italic>Histophilus somni</italic>, <italic>Bibersteinia trehalosi</italic>, <italic>Mycoplasma bovis</italic>, bovine viral diarrhea virus, bovine respiratory syncytial virus, bovine respiratory coronavirus, bovine herpesvirus 1, and influenza D virus; <xref ref-type="local-data" rid="SD1">Technical Appendix</xref>). We sequenced a 590-bp fragment of the matrix gene from 12 ICV-positive samples (GenBank accession nos. MH421865–73; <xref ref-type="local-data" rid="SD1">Technical Appendix</xref> Table) to confirm the PCR results and perform a phylogenetic analysis. We selected 1 isolate (C/bovine/Montana/12/2016) for complete genome sequencing (GenBank accession nos. MH348113–9).</p><p>Of 1,525 samples, 64 (4.20%) were positive for ICV: 38 samples with a cycle threshold (C<sub>t</sub>) <36 and 26 with a C<sub>t</sub> 36–39. The most common pathogens were bovine respiratory coronavirus (34.98%), <italic>M. bovis</italic> (32.27%), and <italic>M</italic>. <italic>haemolytica</italic> (17.04%). The remaining BRDC pathogens were present but less prevalent: <italic>P</italic>. <italic>multocida</italic> (13.42%), <italic>H. somni</italic> (12.58%), influenza D virus (11.93%), bovine respiratory syncytial virus (9.19%), bovine viral diarrhea virus (7.05%), <italic>B. trehalosi</italic> (3.47%), and bovine herpesvirus 1 (2.95%).</p><p>Co-infections with <underline>></underline>1 pathogen are common in BRDC cases. ICV-positive samples were also found to be positive for <underline>></underline>1 bovine respiratory disease pathogen (n = 12, <xref rid="T1" ref-type="table">Table 1</xref>), the most common being <italic>M. bovis</italic> (9/12), followed by <italic>H. somni</italic> (7/12), and <italic>M. haemolytica</italic> (6/12). Among the ICV-positive samples, ICV12 was strongly positive (C<sub>t</sub> 15.81); this sample was also positive for <italic>M. haemolytica</italic> and <italic>P. multocida</italic>, both bacterial pathogens commonly associated with secondary infections. Other BRDC pathogens associated with secondary infections (<italic>M. bovis</italic>, bovine viral diarrhea virus, and <italic>H. somni</italic>) were also detected in samples ICV4, ICV16, ICV18, and ICV20 (<xref rid="R11" ref-type="bibr"><italic>11</italic></xref>–<xref rid="R13" ref-type="bibr"><italic>13</italic></xref>). These results suggest that ICV is associated with bovine respiratory disease in cattle.</p><table-wrap id="T1" position="float"><label>Table 1</label><caption><title>Cycle thresholds for ICV and other bovine respiratory pathogens in 12 ICV strong positive samples from cattle with respiratory disease, United States, October 2016–January 2018*</title></caption><table frame="hsides" rules="groups"><col width="33" span="1"></col><col width="27" span="1"></col><col width="28" span="1"></col><col width="31" span="1"></col><col width="31" span="1"></col><col width="28" span="1"></col><col width="28" span="1"></col><col width="29" span="1"></col><col width="50" span="1"></col><col width="51" span="1"></col><col width="46" span="1"></col><col width="45" span="1"></col><col width="49" span="1"></col><thead><tr><th valign="bottom" align="left" scope="col" rowspan="1" colspan="1">ID no.</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">State</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">ICV</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">BVDV</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">BHV-1</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">BRSV</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">BCoV</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">IDV</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1"><italic>Mycoplasma bovis</italic></th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1"><italic>Mannheimia haemolytica</italic></th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1"><italic>Pasteurella multocida</italic></th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1"><italic>Histophilus somni</italic></th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1"><italic>Bibersteinia trehalosi</italic></th></tr></thead><tbody><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">ICV1†</td><td valign="top" align="center" rowspan="1" colspan="1">TX</td><td valign="top" align="center" rowspan="1" colspan="1">29.95</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">36.77</td><td valign="top" align="center" rowspan="1" colspan="1">39.41</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">ICV2†</td><td valign="top" align="center" rowspan="1" colspan="1">OK</td><td valign="top" align="center" rowspan="1" colspan="1">23.92</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">24.25</td><td valign="top" align="center" rowspan="1" colspan="1">29.17</td><td valign="top" align="center" rowspan="1" colspan="1">31.30</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">31.32</td><td valign="top" align="center" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">ICV3†</td><td valign="top" align="center" rowspan="1" colspan="1">OK</td><td valign="top" align="center" rowspan="1" colspan="1">21.02</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">38.93</td><td valign="top" align="center" rowspan="1" colspan="1">27.00</td><td valign="top" align="center" rowspan="1" colspan="1">29.15</td><td valign="top" align="center" rowspan="1" colspan="1">31.40</td><td valign="top" align="center" rowspan="1" colspan="1">NT</td><td valign="top" align="center" rowspan="1" colspan="1">NT</td><td valign="top" align="center" rowspan="1" colspan="1">NT</td><td valign="top" align="center" rowspan="1" colspan="1">NT</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">ICV4‡</td><td valign="top" align="center" rowspan="1" colspan="1">OK</td><td valign="top" align="center" rowspan="1" colspan="1">29.98</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">24.54</td><td valign="top" align="center" rowspan="1" colspan="1">31.33</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">31.05</td><td valign="top" align="center" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">ICV5†</td><td valign="top" align="center" rowspan="1" colspan="1">MO</td><td valign="top" align="center" rowspan="1" colspan="1">24.47</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">34.98</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">30.12</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">28.00</td><td valign="top" align="center" rowspan="1" colspan="1">24.40</td><td valign="top" align="center" rowspan="1" colspan="1">34.00</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">ICV6†</td><td valign="top" align="center" rowspan="1" colspan="1">CO</td><td valign="top" align="center" rowspan="1" colspan="1">26.91</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">30.25</td><td valign="top" align="center" rowspan="1" colspan="1">32.78</td><td valign="top" align="center" rowspan="1" colspan="1">29.60</td><td valign="top" align="center" rowspan="1" colspan="1">30.00</td><td valign="top" align="center" rowspan="1" colspan="1">35.00</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">ICV12†</td><td valign="top" align="center" rowspan="1" colspan="1">MT</td><td valign="top" align="center" rowspan="1" colspan="1">15.81</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">22.87</td><td valign="top" align="center" rowspan="1" colspan="1">25.70</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">ICV16‡</td><td valign="top" align="center" rowspan="1" colspan="1">NE</td><td valign="top" align="center" rowspan="1" colspan="1">27.18</td><td valign="top" align="center" rowspan="1" colspan="1">16.44</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">28.47</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">ICV18†</td><td valign="top" align="center" rowspan="1" colspan="1">MN</td><td valign="top" align="center" rowspan="1" colspan="1">30.58</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">35.06</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">ICV20‡</td><td valign="top" align="center" rowspan="1" colspan="1">KS</td><td valign="top" align="center" rowspan="1" colspan="1">27.92</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">23.49</td><td valign="top" align="center" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">ICV21‡</td><td valign="top" align="center" rowspan="1" colspan="1">KS</td><td valign="top" align="center" rowspan="1" colspan="1">26.72</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">35.59</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">25.67</td><td valign="top" align="center" rowspan="1" colspan="1">30.95</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">28.47</td><td valign="top" align="center" rowspan="1" colspan="1">–</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">ICV22†</td><td valign="top" align="center" rowspan="1" colspan="1">MT</td><td valign="top" align="center" rowspan="1" colspan="1">25.08</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">20.24</td><td valign="top" align="center" rowspan="1" colspan="1">35.58</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">–</td><td valign="top" align="center" rowspan="1" colspan="1">35.64</td><td valign="top" align="center" rowspan="1" colspan="1">–</td></tr></tbody></table><table-wrap-foot><p>*BCoV, bovine respiratory corona virus; BHV-1, bovine herpesvirus 1; BRSV, bovine respiratory syncytial virus; BVDV, bovine viral diarrhea virus; ICV, influenza C virus; ID, identification; IDV, influenza D virus; NT, not tested (sample used up); –, negative.
†Nasal swab sample used in analysis.
‡Lung sample used in analysis.</p></table-wrap-foot></table-wrap><p>We further evaluated 12 strong positive (C<sub>t</sub><31) samples by sequencing a 590-bp fragment of their matrix gene. Alignment of the partial matrix gene sequences indicated that the isolates in 3 samples (ICV2, ICV3, and ICV4) obtained from different cattle on the same farm in Oklahoma were identical. Because these 3 influenza viruses were most likely the same strain, the virus in just 1 sample (ICV2) was used for phylogenetic analysis. The matrix gene sequence in sample ICV5 from Missouri (GenBank accession no. MH421866) was identical to that in ICV6 from Colorado (GenBank accession no. MH421867).</p><p>Phylogenetic analysis indicated that the bovine ICV isolates are closely related to the porcine and human ICV isolates, and the bovine ICV isolates are more closely related to each other (<xref rid="T2" ref-type="table">Table 2</xref>; <xref ref-type="fig" rid="F1">Figure</xref>). The bovine ICV isolates’ partial matrix gene sequences shared high nucleotide identities (≈98%). For both partial matrix gene sequences and the whole genome sequence (7 segments), the nucleotide identity between bovine and human isolates was ≈95%. The full genome sequence of C/bovine/Montana/12/2016 from sample ICV12 had high nucleotide identity to C/Mississippi/80 (and several other human ICV strains), with an overall identity of 97.1%. Nucleotide identities between these 2 isolates were also high for each gene: 97.0% for polymerase basic 2, 97.7% for polymerase basic 1, 97.5% for polymerase 3, 96.2% for hemagglutininesterase, 96.8% for nucleoprotein, 96.8% for matrix, and 97.6% for nonstructural protein. The only porcine ICV isolate available was more closely related to human (≈98% identity) isolates than bovine (≈95% identity) isolates; the porcine ICV isolate had nearly the same identity that the human ICV isolates had among each other (<xref rid="T2" ref-type="table">Table 2</xref>).</p><table-wrap id="T2" position="float"><label>Table 2</label><caption><title>Average nucleotide identities among bovine, porcine, and human ICV strains, United States*</title></caption><table frame="hsides" rules="groups"><col width="124" span="1"></col><col width="65" span="1"></col><col width="70" span="1"></col><col width="71" span="1"></col><col width="80" span="1"></col><col width="70" span="1"></col><thead><tr><th valign="bottom" align="left" scope="col" rowspan="1" colspan="1">Gene sequence</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Bovine ICV, %</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Human ICV, %</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Bovine ICV vs. human ICV, %</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Bovine ICV vs. porcine ICV, %</th><th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Human ICV vs. porcine ICV, %</th></tr></thead><tbody><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">Matrix, partial</td><td valign="top" align="center" rowspan="1" colspan="1">98.43</td><td valign="top" align="center" rowspan="1" colspan="1">98.47</td><td valign="top" align="center" rowspan="1" colspan="1">95.54</td><td valign="top" align="center" rowspan="1" colspan="1">96.06</td><td valign="top" align="center" rowspan="1" colspan="1">98.84</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">Polymerase basic 2</td><td valign="top" align="center" rowspan="1" colspan="1">NA</td><td valign="top" align="center" rowspan="1" colspan="1">97.76</td><td valign="top" align="center" rowspan="1" colspan="1">94.97</td><td valign="top" align="center" rowspan="1" colspan="1">95.00</td><td valign="top" align="center" rowspan="1" colspan="1">98.34</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">Polymerase basic 1, full length</td><td valign="top" align="center" rowspan="1" colspan="1">NA</td><td valign="top" align="center" rowspan="1" colspan="1">97.59</td><td valign="top" align="center" rowspan="1" colspan="1">94.69</td><td valign="top" align="center" rowspan="1" colspan="1">94.70</td><td valign="top" align="center" rowspan="1" colspan="1">98.08</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">Polymerase 3</td><td valign="top" align="center" rowspan="1" colspan="1">NA</td><td valign="top" align="center" rowspan="1" colspan="1">97.79</td><td valign="top" align="center" rowspan="1" colspan="1">96.36</td><td valign="top" align="center" rowspan="1" colspan="1">95.50</td><td valign="top" align="center" rowspan="1" colspan="1">97.31</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">Hemagglutinin esterase</td><td valign="top" align="center" rowspan="1" colspan="1">NA</td><td valign="top" align="center" rowspan="1" colspan="1">95.44</td><td valign="top" align="center" rowspan="1" colspan="1">90.83</td><td valign="top" align="center" rowspan="1" colspan="1">91.10</td><td valign="top" align="center" rowspan="1" colspan="1">95.97</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">Nucleoprotein</td><td valign="top" align="center" rowspan="1" colspan="1">NA</td><td valign="top" align="center" rowspan="1" colspan="1">97.67</td><td valign="top" align="center" rowspan="1" colspan="1">95.48</td><td valign="top" align="center" rowspan="1" colspan="1">95.30</td><td valign="top" align="center" rowspan="1" colspan="1">97.85</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">Matrix, complete</td><td valign="top" align="center" rowspan="1" colspan="1">NA</td><td valign="top" align="center" rowspan="1" colspan="1">98.33</td><td valign="top" align="center" rowspan="1" colspan="1">95.51</td><td valign="top" align="center" rowspan="1" colspan="1">95.80</td><td valign="top" align="center" rowspan="1" colspan="1">98.82</td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">Nonstructural protein<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">NA<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">98.32<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">95.67<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">95.80<hr></hr></td><td valign="top" align="center" rowspan="1" colspan="1">98.36<hr></hr></td></tr><tr><td valign="top" align="left" scope="row" rowspan="1" colspan="1">Entire genome</td><td valign="top" align="left" rowspan="1" colspan="1"></td><td valign="top" align="center" rowspan="1" colspan="1">97.56</td><td valign="top" align="center" rowspan="1" colspan="1">94.79</td><td valign="top" align="center" rowspan="1" colspan="1">94.74</td><td valign="top" align="center" rowspan="1" colspan="1">97.82</td></tr></tbody></table><table-wrap-foot><p>*ICV, influenza C virus; NA, not applicable.</p></table-wrap-foot></table-wrap><fig id="F1" fig-type="figure" position="float"><label>Figure</label><caption><p>Phylogenetic tree of 10 bovine ICV isolates compared with 1 porcine and 195 human ICV isolates (not labeled), United States. Some subtrees containing only human isolates were collapsed to decrease the size of the image. A representative taxon identification number for each collapsed subtree is shown with the number of taxa in the subtree in parentheses. The percentage of trees in which the associated taxa clustered together is shown above the branches. The tree with the highest log likelihood is shown. The tree is drawn to scale, with branch lengths in the same units as those of the evolutionary distances used to infer the phylogenetic tree. Scale bar indicates the relative distance of 0.005, which indicates a 0.5% sequence difference. ICV, influenza C virus.</p></caption><graphic xlink:href="18-0589-F"></graphic></fig><p>The phylogenetic tree of the partial matrix gene sequences (<xref ref-type="fig" rid="F1">Figure</xref>) further demonstrates the relationship between bovine and human ICV isolates. All bovine ICVs formed a separate clade on the phylogenetic tree, with a 99% bootstrap value. Of the 195 partial matrix gene sequences from human ICVs, the 10 corresponding sequences from bovine ICVs had the highest identities (average 96.70%) to those from C/Mississippi/80 (GenBank no. AB000720.1), C/Nara/82 (GenBank no. AB000723), and C/Kyoto/41/82 (GenBank no. AB000724) and the lowest identities (average 94.21%) to those from C/Yamagata/30/2014 (GenBank no. LC123874) and C/Yamagata/32/2014 (GenBank no. LC123875).</p></sec><sec sec-type="conclusions"><title>Conclusions</title><p>This study confirms the presence of ICV in US cattle with clinical signs of bovine respiratory disease. Although interspecies transmission of influenza viruses occurs between humans and other animals, we do not have data that indicates ICV is a zoonotic pathogen. However, the full genome sequence of C/bovine/Montana/12/2016 has 97.1% nucleotide identity with the human isolate C/Mississippi/80, which is within the range of average identities among human isolates. More detailed investigations are needed to confirm if ICV is involved in bovine respiratory disease, to characterize the relationship between bovine and human ICV strains, and to determine the zoonotic potential of bovine ICV isolates to cause human disease.</p></sec><sec sec-type="supplementary-material"><title></title><supplementary-material content-type="local-data" id="SD1"><caption><title>Technical Appendix</title><p>Description of methods used for PCR and phylogenetic analysis and bovine influenza C virus sequence information.</p></caption><media mimetype="application" mime-subtype="pdf" xlink:href="18-0589-Techapp-s1.pdf" xlink:type="simple" id="d35e934" position="anchor"></media></supplementary-material></sec></body><back><fn-group><fn fn-type="citation"><p><italic>Suggested citation for this article</italic>: Zhang H, Porter E, Lohman M, Lu N, Peddireddi L, Hanzlicek G, et al. Influenza C virus in cattle with respiratory disease, United States, 2016–2018. Emerg Infect Dis. 2018 Oct [<italic>date cited</italic>]. <ext-link ext-link-type="uri" xlink:href="https://doi.org/10.3201/eid2410.180589">https://doi.org/10.3201/eid2410.180589</ext-link></p></fn></fn-group><ack><p>Funding for this study was provided by the Kansas State Veterinary Diagnostic Laboratory and the Swine Health Information Center.</p></ack><bio id="d35e950"><p>Mr. Zhang is a joint doctoral student candidate at the Chinese Academy of Agricultural Sciences in Changchun, China, and Kansas State University in Manhattan, Kansas, USA. His research interests are the development and validation of molecular diagnostic assays for animal and zoonotic pathogens.</p></bio><ref-list><title>References</title><ref id="R1"><label>1. </label><mixed-citation publication-type="journal"><string-name><surname>King</surname><given-names>AMQ</given-names></string-name>, <string-name><surname>Lefkowitz</surname><given-names>EJ</given-names></string-name>, <string-name><surname>Mushegian</surname><given-names>AR</given-names></string-name>, <string-name><surname>Adams</surname><given-names>MJ</given-names></string-name>, <string-name><surname>Dutilh</surname><given-names>BE</given-names></string-name>, <string-name><surname>Gorbalenya</surname><given-names>AE</given-names></string-name>, <etal>et al.</etal><article-title>Changes to taxonomy and the International Code of Virus Classification and Nomenclature ratified by the International Committee on Taxonomy of Viruses (2018).</article-title><source>Arch Virol</source>. <year>2018</year>;<volume>163</volume>:<fpage>2601</fpage>–<lpage>31</lpage>. <pub-id pub-id-type="doi">10.1007/s00705-018-3847-1</pub-id><pub-id pub-id-type="pmid">29754305</pub-id></mixed-citation></ref><ref id="R2"><label>2. </label><mixed-citation publication-type="webpage"><string-name><surname>Spickler</surname><given-names>AR</given-names></string-name>. Influenza. Flu, grippe, avian influenza, grippe aviaire, fowl plaque, swine influenza, hog flu, pig flu, equine influenza, canine influenza. <year>2016</year> [cited 2018 Mar 8]. <ext-link ext-link-type="uri" xlink:href="http://www.cfsph.iastate.edu/Factsheets/pdfs/influenza.pdf">http://www.cfsph.iastate.edu/Factsheets/pdfs/influenza.pdf</ext-link></mixed-citation></ref><ref id="R3"><label>3. </label><mixed-citation publication-type="journal"><string-name><surname>Hause</surname><given-names>BM</given-names></string-name>, <string-name><surname>Collin</surname><given-names>EA</given-names></string-name>, <string-name><surname>Liu</surname><given-names>R</given-names></string-name>, <string-name><surname>Huang</surname><given-names>B</given-names></string-name>, <string-name><surname>Sheng</surname><given-names>Z</given-names></string-name>, <string-name><surname>Lu</surname><given-names>W</given-names></string-name>, <etal>et al.</etal><article-title>Characterization of a novel influenza virus in cattle and Swine: proposal for a new genus in the <italic>Orthomyxoviridae</italic> family.</article-title><source>MBio</source>. <year>2014</year>;<volume>5</volume>:<fpage>e00031</fpage>–<lpage>14</lpage>. <pub-id pub-id-type="doi">10.1128/mBio.00031-14</pub-id><pub-id pub-id-type="pmid">24595369</pub-id></mixed-citation></ref><ref id="R4"><label>4. </label><mixed-citation publication-type="journal"><string-name><surname>Vemula</surname><given-names>SV</given-names></string-name>, <string-name><surname>Zhao</surname><given-names>J</given-names></string-name>, <string-name><surname>Liu</surname><given-names>J</given-names></string-name>, <string-name><surname>Wang</surname><given-names>X</given-names></string-name>, <string-name><surname>Biswas</surname><given-names>S</given-names></string-name>, <string-name><surname>Hewlett</surname><given-names>I</given-names></string-name>. <article-title>Current approaches for diagnosis of influenza virus infections in humans.</article-title><source>Viruses</source>. <year>2016</year>;<volume>8</volume>:<fpage>96</fpage>. <pub-id pub-id-type="doi">10.3390/v8040096</pub-id><pub-id pub-id-type="pmid">27077877</pub-id></mixed-citation></ref><ref id="R5"><label>5. </label><mixed-citation publication-type="journal"><string-name><surname>Guo</surname><given-names>YJ</given-names></string-name>, <string-name><surname>Jin</surname><given-names>FG</given-names></string-name>, <string-name><surname>Wang</surname><given-names>P</given-names></string-name>, <string-name><surname>Wang</surname><given-names>M</given-names></string-name>, <string-name><surname>Zhu</surname><given-names>JM</given-names></string-name>. <article-title>Isolation of influenza C virus from pigs and experimental infection of pigs with influenza C virus.</article-title><source>J Gen Virol</source>. <year>1983</year>;<volume>64</volume>:<fpage>177</fpage>–<lpage>82</lpage>. <pub-id pub-id-type="doi">10.1099/0022-1317-64-1-177</pub-id><pub-id pub-id-type="pmid">6296296</pub-id></mixed-citation></ref><ref id="R6"><label>6. </label><mixed-citation publication-type="journal"><string-name><surname>Yuanji</surname><given-names>G</given-names></string-name>, <string-name><surname>Desselberger</surname><given-names>U</given-names></string-name>. <article-title>Genome analysis of influenza C viruses isolated in 1981/82 from pigs in China.</article-title><source>J Gen Virol</source>. <year>1984</year>;<volume>65</volume>:<fpage>1857</fpage>–<lpage>72</lpage>. <pub-id pub-id-type="doi">10.1099/0022-1317-65-11-1857</pub-id><pub-id pub-id-type="pmid">6502138</pub-id></mixed-citation></ref><ref id="R7"><label>7. </label><mixed-citation publication-type="journal"><string-name><surname>Yamaoka</surname><given-names>M</given-names></string-name>, <string-name><surname>Hotta</surname><given-names>H</given-names></string-name>, <string-name><surname>Itoh</surname><given-names>M</given-names></string-name>, <string-name><surname>Homma</surname><given-names>M</given-names></string-name>. <article-title>Prevalence of antibody to influenza C virus among pigs in Hyogo Prefecture, Japan.</article-title><source>J Gen Virol</source>. <year>1991</year>;<volume>72</volume>:<fpage>711</fpage>–<lpage>4</lpage>. <pub-id pub-id-type="doi">10.1099/0022-1317-72-3-711</pub-id><pub-id pub-id-type="pmid">1848603</pub-id></mixed-citation></ref><ref id="R8"><label>8. </label><mixed-citation publication-type="journal"><string-name><surname>Kimura</surname><given-names>H</given-names></string-name>, <string-name><surname>Abiko</surname><given-names>C</given-names></string-name>, <string-name><surname>Peng</surname><given-names>G</given-names></string-name>, <string-name><surname>Muraki</surname><given-names>Y</given-names></string-name>, <string-name><surname>Sugawara</surname><given-names>K</given-names></string-name>, <string-name><surname>Hongo</surname><given-names>S</given-names></string-name>, <etal>et al.</etal><article-title>Interspecies transmission of influenza C virus between humans and pigs.</article-title><source>Virus Res</source>. <year>1997</year>;<volume>48</volume>:<fpage>71</fpage>–<lpage>9</lpage>. <pub-id pub-id-type="doi">10.1016/S0168-1702(96)01427-X</pub-id><pub-id pub-id-type="pmid">9140195</pub-id></mixed-citation></ref><ref id="R9"><label>9. </label><mixed-citation publication-type="journal"><string-name><surname>Hause</surname><given-names>BM</given-names></string-name>, <string-name><surname>Ducatez</surname><given-names>M</given-names></string-name>, <string-name><surname>Collin</surname><given-names>EA</given-names></string-name>, <string-name><surname>Ran</surname><given-names>Z</given-names></string-name>, <string-name><surname>Liu</surname><given-names>R</given-names></string-name>, <string-name><surname>Sheng</surname><given-names>Z</given-names></string-name>, <etal>et al.</etal><article-title>Isolation of a novel swine influenza virus from Oklahoma in 2011 which is distantly related to human influenza C viruses.</article-title><source>PLoS Pathog</source>. <year>2013</year>;<volume>9</volume>:<fpage>e1003176</fpage>. <pub-id pub-id-type="doi">10.1371/journal.ppat.1003176</pub-id><pub-id pub-id-type="pmid">23408893</pub-id></mixed-citation></ref><ref id="R10"><label>10. </label><mixed-citation publication-type="webpage"><collab>US Department of Agriculture</collab>. Cattle and calves nonpredator death loss in the United States, <year>2010</year> 2011 [cited 2018 Mar 8]. <ext-link ext-link-type="uri" xlink:href="https://www.aphis.usda.gov/animal_health/nahms/general/downloads/cattle_calves_nonpred_2010.pdf">https://www.aphis.usda.gov/animal_health/nahms/general/downloads/cattle_calves_nonpred_2010.pdf</ext-link></mixed-citation></ref><ref id="R11"><label>11. </label><mixed-citation publication-type="journal"><string-name><surname>Gabinaitiene</surname><given-names>A</given-names></string-name>, <string-name><surname>Siugzdaite</surname><given-names>J</given-names></string-name>, <string-name><surname>Zilinskas</surname><given-names>H</given-names></string-name>, <string-name><surname>Siugzda</surname><given-names>R</given-names></string-name>, <string-name><surname>Petkevicius</surname><given-names>S</given-names></string-name>. <article-title><italic>Mycoplasma bovis</italic> and bacterial pathogens in the bovine respiratory tract.</article-title><source>Vet Med (Praha)</source>. <year>2011</year>;<volume>56</volume>:<fpage>28</fpage>–<lpage>34</lpage>. <pub-id pub-id-type="doi">10.17221/1572-VETMED</pub-id></mixed-citation></ref><ref id="R12"><label>12. </label><mixed-citation publication-type="journal"><string-name><surname>Bielefeldt-Ohmann</surname><given-names>H</given-names></string-name>. <article-title>The pathologies of bovine viral diarrhea virus infection. A window on the pathogenesis.</article-title><source>Vet Clin North Am Food Anim Pract</source>. <year>1995</year>;<volume>11</volume>:<fpage>447</fpage>–<lpage>76</lpage>. <pub-id pub-id-type="doi">10.1016/S0749-0720(15)30461-8</pub-id><pub-id pub-id-type="pmid">8581857</pub-id></mixed-citation></ref><ref id="R13"><label>13. </label><mixed-citation publication-type="journal"><string-name><surname>Basqueira</surname><given-names>NS</given-names></string-name>, <string-name><surname>Martin</surname><given-names>CC</given-names></string-name>, <string-name><surname>dos Reis Costa</surname><given-names>JF</given-names></string-name>, <string-name><surname>Okuda</surname><given-names>LH</given-names></string-name>, <string-name><surname>Pituco</surname><given-names>ME</given-names></string-name>, <string-name><surname>Batista</surname><given-names>CF</given-names></string-name>, <etal>et al.</etal><article-title>Bovine respiratory disease (BRD) complex as a signal for bovine viral diarrhea virus (BVDV) presence in the herd.</article-title><source>Acta Sci Vet</source>. <year>2017</year>;<volume>45</volume>:<fpage>1434</fpage>.</mixed-citation></ref></ref-list></back></pmc></record>Pour manipuler ce document sous Unix (Dilib)
EXPLOR_STEP=$WICRI_ROOT/Wicri/Sante/explor/CovidV2/Data/Pmc/Corpus
HfdSelect -h $EXPLOR_STEP/biblio.hfd -nk 000529 | SxmlIndent | more
Ou
HfdSelect -h $EXPLOR_AREA/Data/Pmc/Corpus/biblio.hfd -nk 000529 | SxmlIndent | more
Pour mettre un lien sur cette page dans le réseau Wicri
{{Explor lien
|wiki= Wicri/Sante
|area= CovidV2
|flux= Pmc
|étape= Corpus
|type= RBID
|clé= PMC:6154146
|texte= Influenza C Virus in Cattle with Respiratory Disease, United States, 2016–2018
}}
Pour générer des pages wiki
HfdIndexSelect -h $EXPLOR_AREA/Data/Pmc/Corpus/RBID.i -Sk "pubmed:30226175" \
| HfdSelect -Kh $EXPLOR_AREA/Data/Pmc/Corpus/biblio.hfd \
| NlmPubMed2Wicri -a CovidV2
| This area was generated with Dilib version V0.6.33. |  |