Influenza A in Bovine Species: A Narrative Literature Review
Identifieur interne : 000E41 ( Pmc/Curation ); précédent : 000E40; suivant : 000E42Influenza A in Bovine Species: A Narrative Literature Review
Auteurs : Chithra C. Sreenivasan ; Milton Thomas ; Radhey S. Kaushik ; Dan Wang [États-Unis] ; Feng Li [États-Unis]Source :
- Viruses [ 1999-4915 ] ; 2019.
Abstract
It is quite intriguing that bovines were largely unaffected by influenza A, even though most of the domesticated and wild animals/birds at the human–animal interface succumbed to infection over the past few decades. Influenza A occurs on a very infrequent basis in bovine species and hence bovines were not considered to be susceptible hosts for influenza until the emergence of influenza D. This review describes a multifaceted chronological review of literature on influenza in cattle which comprises mainly of the natural infections/outbreaks, experimental studies, and pathological and seroepidemiological aspects of influenza A that have occurred in the past. The review also sheds light on the bovine models used in vitro and in vivo for influenza-related studies over recent years. Despite a few natural cases in the mid-twentieth century and seroprevalence of human, swine, and avian influenza viruses in bovines, the evolution and host adaptation of influenza A virus (IAV) in this species suffered a serious hindrance until the novel influenza D virus (IDV) emerged recently in cattle across the world. Supposedly, certain bovine host factors, particularly some serum components and secretory proteins, were reported to have anti-influenza properties, which could be an attributing factor for the resilient nature of bovines to IAV. Further studies are needed to identify the host-specific factors contributing to the differential pathogenetic mechanisms and disease progression of IAV in bovines compared to other susceptible mammalian hosts.
Url:
DOI: 10.3390/v11060561
PubMed: 31213032
PubMed Central: 6631717
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<series><title level="j">Viruses</title>
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<front><div type="abstract" xml:lang="en"><p>It is quite intriguing that bovines were largely unaffected by influenza A, even though most of the domesticated and wild animals/birds at the human–animal interface succumbed to infection over the past few decades. Influenza A occurs on a very infrequent basis in bovine species and hence bovines were not considered to be susceptible hosts for influenza until the emergence of influenza D. This review describes a multifaceted chronological review of literature on influenza in cattle which comprises mainly of the natural infections/outbreaks, experimental studies, and pathological and seroepidemiological aspects of influenza A that have occurred in the past. The review also sheds light on the bovine models used in vitro and in vivo for influenza-related studies over recent years. Despite a few natural cases in the mid-twentieth century and seroprevalence of human, swine, and avian influenza viruses in bovines, the evolution and host adaptation of influenza A virus (IAV) in this species suffered a serious hindrance until the novel influenza D virus (IDV) emerged recently in cattle across the world. Supposedly, certain bovine host factors, particularly some serum components and secretory proteins, were reported to have anti-influenza properties, which could be an attributing factor for the resilient nature of bovines to IAV. Further studies are needed to identify the host-specific factors contributing to the differential pathogenetic mechanisms and disease progression of IAV in bovines compared to other susceptible mammalian hosts.</p>
</div>
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<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Viruses</journal-id>
<journal-id journal-id-type="iso-abbrev">Viruses</journal-id>
<journal-id journal-id-type="publisher-id">viruses</journal-id>
<journal-title-group><journal-title>Viruses</journal-title>
</journal-title-group>
<issn pub-type="epub">1999-4915</issn>
<publisher><publisher-name>MDPI</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">31213032</article-id>
<article-id pub-id-type="pmc">6631717</article-id>
<article-id pub-id-type="doi">10.3390/v11060561</article-id>
<article-id pub-id-type="publisher-id">viruses-11-00561</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Review</subject>
</subj-group>
</article-categories>
<title-group><article-title>Influenza A in Bovine Species: A Narrative Literature Review</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Sreenivasan</surname>
<given-names>Chithra C.</given-names>
</name>
<xref ref-type="aff" rid="af1-viruses-11-00561">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Thomas</surname>
<given-names>Milton</given-names>
</name>
<xref ref-type="aff" rid="af2-viruses-11-00561">2</xref>
</contrib>
<contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0003-4204-9323</contrib-id>
<name><surname>Kaushik</surname>
<given-names>Radhey S.</given-names>
</name>
<xref ref-type="aff" rid="af1-viruses-11-00561">1</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Wang</surname>
<given-names>Dan</given-names>
</name>
<xref ref-type="aff" rid="af1-viruses-11-00561">1</xref>
<xref ref-type="aff" rid="af3-viruses-11-00561">3</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Li</surname>
<given-names>Feng</given-names>
</name>
<xref ref-type="aff" rid="af1-viruses-11-00561">1</xref>
<xref ref-type="aff" rid="af3-viruses-11-00561">3</xref>
<xref rid="c1-viruses-11-00561" ref-type="corresp">*</xref>
</contrib>
</contrib-group>
<aff id="af1-viruses-11-00561"><label>1</label>
Department of Biology and Microbiology, South Dakota State University, Brookings, SD 57007, USA;<email>chithra.sreenivasan@sdstate.edu</email>
(C.C.S.);<email>radhey.kaushik@sdstate.edu</email>
(R.S.K.);<email>dan.wang@sdstate.edu</email>
(D.W.)</aff>
<aff id="af2-viruses-11-00561"><label>2</label>
Department of Veterinary and Biomedical Sciences, South Dakota State University, Brookings, SD 57007, USA;<email>milton.thomas@sdstate.edu</email>
</aff>
<aff id="af3-viruses-11-00561"><label>3</label>
BioSystems Networks and Translational Research Center (BioSNTR), Brookings, SD 57007, USA</aff>
<author-notes><corresp id="c1-viruses-11-00561"><label>*</label>
Correspondence: <email>feng.li@sdstate.edu</email>
; Tel.: +1-605-688-6036</corresp>
</author-notes>
<pub-date pub-type="epub"><day>17</day>
<month>6</month>
<year>2019</year>
</pub-date>
<pub-date pub-type="collection"><month>6</month>
<year>2019</year>
</pub-date>
<volume>11</volume>
<issue>6</issue>
<elocation-id>561</elocation-id>
<history><date date-type="received"><day>17</day>
<month>5</month>
<year>2019</year>
</date>
<date date-type="accepted"><day>14</day>
<month>6</month>
<year>2019</year>
</date>
</history>
<permissions><copyright-statement>© 2019 by the authors.</copyright-statement>
<copyright-year>2019</copyright-year>
<license license-type="open-access"><license-p>Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by/4.0/">http://creativecommons.org/licenses/by/4.0/</ext-link>
).</license-p>
</license>
</permissions>
<abstract><p>It is quite intriguing that bovines were largely unaffected by influenza A, even though most of the domesticated and wild animals/birds at the human–animal interface succumbed to infection over the past few decades. Influenza A occurs on a very infrequent basis in bovine species and hence bovines were not considered to be susceptible hosts for influenza until the emergence of influenza D. This review describes a multifaceted chronological review of literature on influenza in cattle which comprises mainly of the natural infections/outbreaks, experimental studies, and pathological and seroepidemiological aspects of influenza A that have occurred in the past. The review also sheds light on the bovine models used in vitro and in vivo for influenza-related studies over recent years. Despite a few natural cases in the mid-twentieth century and seroprevalence of human, swine, and avian influenza viruses in bovines, the evolution and host adaptation of influenza A virus (IAV) in this species suffered a serious hindrance until the novel influenza D virus (IDV) emerged recently in cattle across the world. Supposedly, certain bovine host factors, particularly some serum components and secretory proteins, were reported to have anti-influenza properties, which could be an attributing factor for the resilient nature of bovines to IAV. Further studies are needed to identify the host-specific factors contributing to the differential pathogenetic mechanisms and disease progression of IAV in bovines compared to other susceptible mammalian hosts.</p>
</abstract>
<kwd-group><kwd>ruminants</kwd>
<kwd>bovine</kwd>
<kwd>cattle outbreaks</kwd>
<kwd>Influenza A</kwd>
<kwd>host restriction</kwd>
<kwd>bovine cell cultures</kwd>
<kwd>bovine respiratory disease</kwd>
<kwd>bronchopneumonia</kwd>
<kwd>epizootic cough</kwd>
<kwd>seroprevalence</kwd>
<kwd>MDBK cells</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group><fig id="viruses-11-00561-f001" orientation="portrait" position="float"><label>Figure 1</label>
<caption><p>Schematic illustration of the literature search strategy. (<bold>A</bold>
) A literature search was conducted using different keyword combinations in the PubMed database. Initial screening was carried out by shortlisting articles that matched the title for topic relevance and the availability of the articles in full text or abstract as shown in the flow chart. (<bold>B</bold>
) Articles obtained after the keyword search were categorized based on their content as described in the pie chart. A comprehensive analyses of influenza A related studies in bovines represented by donut chart were conducted. Abbreviations used: Influenza A virus, IAV; Influenza B virus, IBV; Influenza C virus, ICV; Influenza D virus, IDV.</p>
</caption>
<graphic xlink:href="viruses-11-00561-g001"></graphic>
</fig>
<fig id="viruses-11-00561-f002" orientation="portrait" position="float"><label>Figure 2</label>
<caption><p>The host range for all four types (IAV, IBV, ICV, and IDV) of influenza viruses. The association of influenza disease in different mammalian species with reference to cattle (orange) is described separately. In each box, the bold black line represents active infection/disease; dotted black line represents the exposure without active infection/disease, as demonstrated by the serological evidence. A red dotted line in IAV indicates the possible source/routes of IAV infection (human, avian or swine) that can occur in bovines. Red blocked line indicates neither disease nor exposure. Vector graphic images used in the figure were taken from icon pool of the Microsoft Office and Freepik (<uri xlink:href="www.freepik.com">www.freepik.com</uri>
).</p>
</caption>
<graphic xlink:href="viruses-11-00561-g002"></graphic>
</fig>
<fig id="viruses-11-00561-f003" orientation="portrait" position="float"><label>Figure 3</label>
<caption><p>History timeline of the major influenza events in the past (<bold>A</bold>
) Known human influenza pandemics along with the important outbreaks/discoveries. All the pandemics with year and country of origin are indicated in “black” flag, black font, while the other outbreaks/epidemics/discoveries are indicated in “orange” flag, red font. (<bold>B</bold>
) influenza A incidences occurred in ruminants especially bovine species, were plotted based on the information from peer-reviewed articles. Only the natural infections/outbreaks and seroepidemiological studies reported in cattle in the past were included in the timeline. Experimental studies were excluded in this timeline. Illustrated major events included the major influenza outbreaks, cattle epizootics/respiratory disease with year and country of origin, and are represented by black triangle blocks, black font. Please note that both the timelines (A and B) have same dimensions starting with human pandemic as early as 1580 to 2013 H7N9 outbreaks and the timeframe of these cattle outbreaks/diseases (1889, 1893, 1914–1916, 1949, 1959–1960, 1971–1981, 1997–1999, 2005–2006) occurred almost concurrent to the human pandemic/outbreaks, which is indicative of the natural susceptibility of bovines to human influenza viruses. Most of the cattle influenza A isolates appeared to be related to human influenza A strains, with the HA glycoprotein similar to the prototypic human H2 and H3 subtypes.</p>
</caption>
<graphic xlink:href="viruses-11-00561-g003"></graphic>
</fig>
<table-wrap id="viruses-11-00561-t001" orientation="portrait" position="float"><object-id pub-id-type="pii">viruses-11-00561-t001_Table 1</object-id>
<label>Table 1</label>
<caption><p>Natural and experimental cases of influenza A associated with ruminant species.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Description</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Year</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Ref.</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1"><bold>Natural infection</bold>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1"></td>
<td align="center" valign="middle" rowspan="1" colspan="1"></td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Influenza outbreak in Japan</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1951</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B76-viruses-11-00561" ref-type="bibr">76</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Incidence, level of influenza, and adeno virus antibodies in domestic animal species</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1969</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B25-viruses-11-00561" ref-type="bibr">25</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Antigenic characteristics of influenza viruses from domestic animals and birds (USSR)</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1973</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B89-viruses-11-00561" ref-type="bibr">89</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Influenza outbreak in cattle</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1973</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B90-viruses-11-00561" ref-type="bibr">90</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Isolation of influenza A strains from cattle</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1973</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B46-viruses-11-00561" ref-type="bibr">46</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Study of cattle influenza</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1976</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B92-viruses-11-00561" ref-type="bibr">92</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Influenza in cattle</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1977</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B91-viruses-11-00561" ref-type="bibr">91</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Hong Kong influenza A strains in calves</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1977</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B48-viruses-11-00561" ref-type="bibr">48</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Pathological anatomical examination of the lung from bovine influenza</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1977</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B94-viruses-11-00561" ref-type="bibr">94</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Influenza of cattle</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1978</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B93-viruses-11-00561" ref-type="bibr">93</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Unexplained sporadic milk drop in cows</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1997</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B95-viruses-11-00561" ref-type="bibr">95</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Bovine influenza</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1998</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B97-viruses-11-00561" ref-type="bibr">97</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Influenza A in dairy cows with sporadic milk syndrome</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1999</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B98-viruses-11-00561" ref-type="bibr">98</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Evidence of antibodies in sera/nasal samples against human influenza viruses from 17 outbreaks of respiratory disease with milk drop syndrome and diarrhea in cattle in 1998–1999</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2002</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B99-viruses-11-00561" ref-type="bibr">99</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Wild animals as a reservoir for different bacterial and viral diseases including avian influenza</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2002</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B102-viruses-11-00561" ref-type="bibr">102</xref>
]</td>
</tr>
<tr><td colspan="3" align="center" valign="middle" rowspan="1"><bold>Experimental infection</bold>
</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Experimental infection of bovines with human influenza virus </td>
<td align="center" valign="middle" rowspan="1" colspan="1">1954</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B26-viruses-11-00561" ref-type="bibr">26</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Experimental inoculation of calves with influenza virus A/csf/Udmurtiia/116/73</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1977</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B27-viruses-11-00561" ref-type="bibr">27</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Experimental infection of influenza in yak and presence of H3N2 antibodies</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1974</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B103-viruses-11-00561" ref-type="bibr">103</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant vaccinia virus expressing HA in cattle, sheep, and poultry</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1986</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B104-viruses-11-00561" ref-type="bibr">104</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Intranasal inoculation of calves with live swine influenza virus </td>
<td align="center" valign="middle" rowspan="1" colspan="1">1987</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B105-viruses-11-00561" ref-type="bibr">105</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Experimental inoculation of a cat derived highly pathogenic avian influenza virus in calves</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2008</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B106-viruses-11-00561" ref-type="bibr">106</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Experimental inoculation of highly pathogenic avian influenza virus H5N1 in cattle egrets </td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2011</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B107-viruses-11-00561" ref-type="bibr">107</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>Articles in non-English languages*.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="viruses-11-00561-t002" orientation="portrait" position="float"><object-id pub-id-type="pii">viruses-11-00561-t002_Table 2</object-id>
<label>Table 2</label>
<caption><p>Serosurveillance studies of influenza A associated with ruminant species in the past.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Description</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Year</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Ref.</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Influenza A and B specific antibodies in domestic and wild animals</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1965</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B118-viruses-11-00561" ref-type="bibr">118</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Serological study in Ottawa based on immunoprecipitation test found influenza A antibodies in sheep and goat among 14 species tested</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1975</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B119-viruses-11-00561" ref-type="bibr">119</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Serosurveillance of swine H1N1 in cattle and swine in Great Britain</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1978</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B120-viruses-11-00561" ref-type="bibr">120</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Serological screening of influenza B and C in cattle, horses and other animals in Japan</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1978</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B56-viruses-11-00561" ref-type="bibr">56</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Serological evidence of influenza A in cattle in Japan</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1978</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B111-viruses-11-00561" ref-type="bibr">111</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Influenza-specific antibodies not detected in indigenous and non-indigenous sheep breeds of Northern Ireland</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1984</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B121-viruses-11-00561" ref-type="bibr">121</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Influenza in ruminants: a review with information regarding viruses isolated from the cattle</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1984</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B47-viruses-11-00561" ref-type="bibr">47</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Single radial hemolysis to measure influenza antibody in cattle serum </td>
<td align="center" valign="middle" rowspan="1" colspan="1">1986</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B123-viruses-11-00561" ref-type="bibr">123</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Swine influenza virus as a component in the respiratory disease complex in calves</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1986</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B122-viruses-11-00561" ref-type="bibr">122</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Presence of influenza A specific antibodies in cattle with respiratory disease and reduced milk yield</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1998</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B96-viruses-11-00561" ref-type="bibr">96</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Vaccination study of foot and mouth disease and influenza in cattle and sheep</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1998</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B125-viruses-11-00561" ref-type="bibr">125</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Influenza A antibodies associated with an acute reduction in milk yield in cattle in Britain</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2008</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B100-viruses-11-00561" ref-type="bibr">100</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Serosurveillance study of avian influenza H5N1 in cattle, buffaloes, sheep, goat, and other animals in Egypt</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2013</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B124-viruses-11-00561" ref-type="bibr">124</xref>
]</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="viruses-11-00561-t003" orientation="portrait" position="float"><object-id pub-id-type="pii">viruses-11-00561-t003_Table 3</object-id>
<label>Table 3</label>
<caption><p>Utility of bovine cell/tissue cultures for influenza A studies in the past.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Description</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Year</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Ref.</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Studies on the cellular enzymes and their role in the cytopathic effect of influenza in cell cultures</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1967</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B181-viruses-11-00561" ref-type="bibr">181</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Replication of WSN influenza virus in high titers in MDBK cell line at high and low multiplicity of infection</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1969</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B144-viruses-11-00561" ref-type="bibr">144</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Adaptation of the influenza virus in calf kidney cell cultures</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1969</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B182-viruses-11-00561" ref-type="bibr">182</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Study of infective and incomplete influenza virions grown in MDBK and HeLa cells</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1970</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B145-viruses-11-00561" ref-type="bibr">145</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Calf serum suppressed plaque formation of many influenza virus strains in different cell lines</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1970</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B183-viruses-11-00561" ref-type="bibr">183</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Influenza B virus propagation in bovine fetal kidney cell cultures: incomplete virus formation</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1970</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B148-viruses-11-00561" ref-type="bibr">148</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Influenza B virus forms plaque in primary calf kidney cells</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1971</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B156-viruses-11-00561" ref-type="bibr">156</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Interaction of swine influenza and bovine mycoplasma in bovine tracheal cultures</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1971</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B177-viruses-11-00561" ref-type="bibr">177</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Influenza virus adaptation (A2 (Hong Kong) 68) in calf kidney cell cultures</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1972</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B184-viruses-11-00561" ref-type="bibr">184</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Use of bovine kidney cells for the propagation of <italic>ts</italic>
recombinant viruses</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1972</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B173-viruses-11-00561" ref-type="bibr">173</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Use of primary bovine kidney cells at 25 °C for growing low temperature adapted vaccine virus</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1973</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B174-viruses-11-00561" ref-type="bibr">174</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Influenza virions grown in Madin–Darby Bovine Kidney (MDBK) cells without calf serum have more uncleaved HA especially in the early phase indicating that HA cleavage is both host cell and strain dependent</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1973</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B166-viruses-11-00561" ref-type="bibr">166</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Influenza virus grown in MDBK cells in the presence of medium containing 2% calf serum caused cleavage of HA polypeptide, to HA1 and HA2 unlike serum-free medium due to the plasminogen component in the sera</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1973</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B167-viruses-11-00561" ref-type="bibr">167</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Use of bovine kidney and trachea organ cultures for influenza for studying the virus reactogenic and immunogenic properties</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1975</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B178-viruses-11-00561" ref-type="bibr">178</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Study of the polypeptide composition of incomplete influenza viruses propagated in MDBK cells</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1975</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B185-viruses-11-00561" ref-type="bibr">185</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Use of lung and trachea organ cultures from bovine and other species for the influenza studies</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1976</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B176-viruses-11-00561" ref-type="bibr">176</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Use of bovine embryo kidney cells, roller cultures for high titer influenza virus propagation</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">1977</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B157-viruses-11-00561" ref-type="bibr">157</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>Articles in non-English languages*.</p>
</fn>
</table-wrap-foot>
</table-wrap>
<table-wrap id="viruses-11-00561-t004" orientation="portrait" position="float"><object-id pub-id-type="pii">viruses-11-00561-t004_Table 4</object-id>
<label>Table 4</label>
<caption><p>Summary of major bovine host antiviral factors and their interactions with influenza.</p>
</caption>
<table frame="hsides" rules="groups"><thead><tr><th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Description</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Year</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Ref.</th>
</tr>
</thead>
<tbody><tr><td align="center" valign="middle" rowspan="1" colspan="1">Inhibition of influenza virus hemagglutination by cow’s milk</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1949</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B189-viruses-11-00561" ref-type="bibr">189</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Inhibition of influenza virus hemagglutination by bovine amniotic fluid factor </td>
<td align="center" valign="middle" rowspan="1" colspan="1">1954</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B193-viruses-11-00561" ref-type="bibr">193</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Mucoprotein from bovine submaxillary glands with restricted hemagglutination inhibition activity against influenza virus </td>
<td align="center" valign="middle" rowspan="1" colspan="1">1955</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B192-viruses-11-00561" ref-type="bibr">192</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Influenza virus inhibitor in human and cow milk </td>
<td align="center" valign="middle" rowspan="1" colspan="1">1960</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B226-viruses-11-00561" ref-type="bibr">226</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Beta inhibitors in bovine serum</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1963</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B227-viruses-11-00561" ref-type="bibr">227</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Use of sera from different species of animals to study periodate induced hemagglutination inhibitor</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1968</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B207-viruses-11-00561" ref-type="bibr">207</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Influenza A2/Hong Kong strains were sensitive to periodate-resistant inhibitors in normal bovine serum</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1971</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B206-viruses-11-00561" ref-type="bibr">206</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Serum inhibitors of hemagglutination</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1972</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B228-viruses-11-00561" ref-type="bibr">228</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Serum inhibitors of hemagglutination of A2/Hong Kong strains </td>
<td align="center" valign="middle" rowspan="1" colspan="1">1972</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B229-viruses-11-00561" ref-type="bibr">229</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Characterization of non-specific inhibitors of hemagglutination of influenza A virus in the sera of different species of animals and birds</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1977</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B208-viruses-11-00561" ref-type="bibr">208</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">*Serum inhibitors of cattle and influenza virus persistence in Madin–Darby Swine Kidney (MDSK) cells</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1980</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B230-viruses-11-00561" ref-type="bibr">230</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Conglutinin as bovine serum beta inhibitor of influenza virus hemagglutination and infectivity of H1 and H3 subtypes</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1992</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B212-viruses-11-00561" ref-type="bibr">212</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Isolation of influenza virus inhibitor, conglutinin </td>
<td align="center" valign="middle" rowspan="1" colspan="1">1992</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B214-viruses-11-00561" ref-type="bibr">214</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Opsonizing activity of conglutinin against influenza A virus </td>
<td align="center" valign="middle" rowspan="1" colspan="1">1993</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B213-viruses-11-00561" ref-type="bibr">213</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant bovine conglutinin deficient in N-terminal and collagenous domains and its activity against influenza virus</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1996</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B211-viruses-11-00561" ref-type="bibr">211</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Bovine collectins and its antiviral activity against rota virus </td>
<td align="center" valign="middle" rowspan="1" colspan="1">1998</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B216-viruses-11-00561" ref-type="bibr">216</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">CL-43, bovine serum collectin, and its antiviral activity by inhibiting the hemagglutination activity of influenza A virus </td>
<td align="center" valign="middle" rowspan="1" colspan="1">2002</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B231-viruses-11-00561" ref-type="bibr">231</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Bovine collectins_Conglutinin, CL-43, and CL-46</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2006</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B218-viruses-11-00561" ref-type="bibr">218</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Recombinant trimeric neck and carbohydrate recognition domains (NCRD) of bovine conglutinin and CL-46 demonstrated a higher level of intrinsic antiviral activity against influenza A virus </td>
<td align="center" valign="middle" rowspan="1" colspan="1">2010</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B217-viruses-11-00561" ref-type="bibr">217</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Aprotinin, a natural polypeptide of bovine lung origin can inhibit the HA cleavage of pdmH1N1 and its replication in different host systems</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2011</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B219-viruses-11-00561" ref-type="bibr">219</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Bovine colostrum can enhance natural killer cell activity and thus boosts the immune response against influenza in a mouse model</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2014</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B196-viruses-11-00561" ref-type="bibr">196</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" rowspan="1" colspan="1">Peptide inhibitors derived from lactoferrin C-lobe possess broad anti-influenza activity and prevented influenza hemagglutination and infection</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2012, 2017</td>
<td align="center" valign="middle" rowspan="1" colspan="1">[<xref rid="B199-viruses-11-00561" ref-type="bibr">199</xref>
,<xref rid="B203-viruses-11-00561" ref-type="bibr">203</xref>
]</td>
</tr>
<tr><td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Bovine lactoferrin interferes with the fusion of HA glycoprotein and thus inhibits influenza A infection</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2019</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">[<xref rid="B204-viruses-11-00561" ref-type="bibr">204</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>Articles in non-English languages*.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</floats-group>
</pmc>
</record>
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