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Identification of Alpha and Beta Coronavirus in Wildlife Species in France: Bats, Rodents, Rabbits, and Hedgehogs

Identifieur interne : 000617 ( Pmc/Checkpoint ); précédent : 000616; suivant : 000618

Identification of Alpha and Beta Coronavirus in Wildlife Species in France: Bats, Rodents, Rabbits, and Hedgehogs

Auteurs : Elodie Monchatre-Leroy ; Franck Boué ; Jean-Marc Boucher ; Camille Renault ; François Moutou ; Meriadeg Ar Gouilh [France] ; Gérald Umhang

Source :

RBID : PMC:5744139

Abstract

Coronaviruses are closely monitored in the context of emerging diseases and, as illustrated with Severe Acute Respiratory Syndrome coronavirus (SARS-CoV) and Middle East Respiratory Syndrome-coronavirus (MERS-CoV), are known to cross the species barrier and eventually to move from wildlife to humans. Knowledge of the diversity of coronaviruses in wildlife is therefore essential to better understand and prevent emergence events. This study explored the presence of coronaviruses in four wild mammal orders in France: Bats, rodents, lagomorphs, and hedgehogs. Betacoronavirus and Alphacoronavirus genera were identified. The results obtained suggest the circulation of potentially evolving virus strains, with the potential to cross the species barrier.


Url:
DOI: 10.3390/v9120364
PubMed: 29186061
PubMed Central: 5744139


Affiliations:


Links toward previous steps (curation, corpus...)


Links to Exploration step

PMC:5744139

Le document en format XML

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<email>jean-marc.boucher@anses.fr</email>
(J.-M.B.);
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<nlm:aff id="af1-viruses-09-00364">ANSES, Laboratoire de la rage et de la faune sauvage, 54220 Nancy, France;
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<email>jean-marc.boucher@anses.fr</email>
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<title xml:lang="en" level="a" type="main">Identification of Alpha and Beta Coronavirus in Wildlife Species in France: Bats, Rodents, Rabbits, and Hedgehogs</title>
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<nlm:aff id="af1-viruses-09-00364">ANSES, Laboratoire de la rage et de la faune sauvage, 54220 Nancy, France;
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<email>camille.renault20@gmail.com</email>
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<email>jean-marc.boucher@anses.fr</email>
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<email>camille.renault20@gmail.com</email>
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<name sortKey="Renault, Camille" sort="Renault, Camille" uniqKey="Renault C" first="Camille" last="Renault">Camille Renault</name>
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<nlm:aff id="af1-viruses-09-00364">ANSES, Laboratoire de la rage et de la faune sauvage, 54220 Nancy, France;
<email>franck.boue@anses.fr</email>
(F.B.);
<email>jean-marc.boucher@anses.fr</email>
(J.-M.B.);
<email>camille.renault20@gmail.com</email>
(C.R.);
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<name sortKey="Moutou, Francois" sort="Moutou, Francois" uniqKey="Moutou F" first="François" last="Moutou">François Moutou</name>
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<name sortKey="Ar Gouilh, Meriadeg" sort="Ar Gouilh, Meriadeg" uniqKey="Ar Gouilh M" first="Meriadeg" last="Ar Gouilh">Meriadeg Ar Gouilh</name>
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<nlm:aff id="af3-viruses-09-00364">Université de Normandie, EA 2656, GRAM—Groupe de Recherche sur l’Adaptation Microbienne, UNICAEN/UNIROUEN, 14000 Caen, France;
<email>meriadeg.legouil@normandie-univ.fr</email>
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</affiliation>
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<nlm:aff id="af4-viruses-09-00364">Institut Pasteur, Infection et Epidemiologie, Unité Environnement et Risques Infectieux, 75015 Paris, France</nlm:aff>
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<name sortKey="Umhang, Gerald" sort="Umhang, Gerald" uniqKey="Umhang G" first="Gérald" last="Umhang">Gérald Umhang</name>
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<nlm:aff id="af1-viruses-09-00364">ANSES, Laboratoire de la rage et de la faune sauvage, 54220 Nancy, France;
<email>franck.boue@anses.fr</email>
(F.B.);
<email>jean-marc.boucher@anses.fr</email>
(J.-M.B.);
<email>camille.renault20@gmail.com</email>
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<email>gerald.umhang@anses.fr</email>
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<p>Coronaviruses are closely monitored in the context of emerging diseases and, as illustrated with Severe Acute Respiratory Syndrome coronavirus (SARS-CoV) and Middle East Respiratory Syndrome-coronavirus (MERS-CoV), are known to cross the species barrier and eventually to move from wildlife to humans. Knowledge of the diversity of coronaviruses in wildlife is therefore essential to better understand and prevent emergence events. This study explored the presence of coronaviruses in four wild mammal orders in France: Bats, rodents, lagomorphs, and hedgehogs.
<italic>Betacoronavirus</italic>
and
<italic>Alphacoronavirus</italic>
genera were identified. The results obtained suggest the circulation of potentially evolving virus strains, with the potential to cross the species barrier.</p>
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</TEI>
<pmc article-type="research-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">29186061</article-id>
<article-id pub-id-type="pmc">5744139</article-id>
<article-id pub-id-type="doi">10.3390/v9120364</article-id>
<article-id pub-id-type="publisher-id">viruses-09-00364</article-id>
<article-categories>
<subj-group subj-group-type="heading">
<subject>Article</subject>
</subj-group>
</article-categories>
<title-group>
<article-title>Identification of Alpha and Beta Coronavirus in Wildlife Species in France: Bats, Rodents, Rabbits, and Hedgehogs</article-title>
</title-group>
<contrib-group>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-3231-398X</contrib-id>
<name>
<surname>Monchatre-Leroy</surname>
<given-names>Elodie</given-names>
</name>
<xref ref-type="aff" rid="af1-viruses-09-00364">1</xref>
<xref rid="c1-viruses-09-00364" ref-type="corresp">*</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Boué</surname>
<given-names>Franck</given-names>
</name>
<xref ref-type="aff" rid="af1-viruses-09-00364">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Boucher</surname>
<given-names>Jean-Marc</given-names>
</name>
<xref ref-type="aff" rid="af1-viruses-09-00364">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Renault</surname>
<given-names>Camille</given-names>
</name>
<xref ref-type="aff" rid="af1-viruses-09-00364">1</xref>
</contrib>
<contrib contrib-type="author">
<name>
<surname>Moutou</surname>
<given-names>François</given-names>
</name>
<xref ref-type="aff" rid="af2-viruses-09-00364">2</xref>
</contrib>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0002-3672-9974</contrib-id>
<name>
<surname>Ar Gouilh</surname>
<given-names>Meriadeg</given-names>
</name>
<xref ref-type="aff" rid="af3-viruses-09-00364">3</xref>
<xref ref-type="aff" rid="af4-viruses-09-00364">4</xref>
</contrib>
<contrib contrib-type="author">
<contrib-id contrib-id-type="orcid" authenticated="true">https://orcid.org/0000-0001-6944-7474</contrib-id>
<name>
<surname>Umhang</surname>
<given-names>Gérald</given-names>
</name>
<xref ref-type="aff" rid="af1-viruses-09-00364">1</xref>
</contrib>
</contrib-group>
<aff id="af1-viruses-09-00364">
<label>1</label>
ANSES, Laboratoire de la rage et de la faune sauvage, 54220 Nancy, France;
<email>franck.boue@anses.fr</email>
(F.B.);
<email>jean-marc.boucher@anses.fr</email>
(J.-M.B.);
<email>camille.renault20@gmail.com</email>
(C.R.);
<email>gerald.umhang@anses.fr</email>
(G.U.)</aff>
<aff id="af2-viruses-09-00364">
<label>2</label>
ANSES, ENVA, 94701 Maisons-Alfort, France;
<email>francoismoutou@orange.fr</email>
</aff>
<aff id="af3-viruses-09-00364">
<label>3</label>
Université de Normandie, EA 2656, GRAM—Groupe de Recherche sur l’Adaptation Microbienne, UNICAEN/UNIROUEN, 14000 Caen, France;
<email>meriadeg.legouil@normandie-univ.fr</email>
</aff>
<aff id="af4-viruses-09-00364">
<label>4</label>
Institut Pasteur, Infection et Epidemiologie, Unité Environnement et Risques Infectieux, 75015 Paris, France</aff>
<author-notes>
<corresp id="c1-viruses-09-00364">
<label>*</label>
Correspondence:
<email>elodie.monchatre-leroy@anses.fr</email>
; Tel.: +33-3-83-29-89-50</corresp>
</author-notes>
<pub-date pub-type="epub">
<day>29</day>
<month>11</month>
<year>2017</year>
</pub-date>
<pub-date pub-type="collection">
<month>12</month>
<year>2017</year>
</pub-date>
<volume>9</volume>
<issue>12</issue>
<elocation-id>364</elocation-id>
<history>
<date date-type="received">
<day>02</day>
<month>11</month>
<year>2017</year>
</date>
<date date-type="accepted">
<day>21</day>
<month>11</month>
<year>2017</year>
</date>
</history>
<permissions>
<copyright-statement>© 2017 by the authors.</copyright-statement>
<copyright-year>2017</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>Coronaviruses are closely monitored in the context of emerging diseases and, as illustrated with Severe Acute Respiratory Syndrome coronavirus (SARS-CoV) and Middle East Respiratory Syndrome-coronavirus (MERS-CoV), are known to cross the species barrier and eventually to move from wildlife to humans. Knowledge of the diversity of coronaviruses in wildlife is therefore essential to better understand and prevent emergence events. This study explored the presence of coronaviruses in four wild mammal orders in France: Bats, rodents, lagomorphs, and hedgehogs.
<italic>Betacoronavirus</italic>
and
<italic>Alphacoronavirus</italic>
genera were identified. The results obtained suggest the circulation of potentially evolving virus strains, with the potential to cross the species barrier.</p>
</abstract>
<kwd-group>
<kwd>coronavirus</kwd>
<kwd>wildlife</kwd>
<kwd>wild rabbits</kwd>
<kwd>hedgehogs</kwd>
<kwd>bats</kwd>
<kwd>rodents</kwd>
<kwd>France</kwd>
<kwd>genetic diversity</kwd>
</kwd-group>
</article-meta>
</front>
<floats-group>
<fig id="viruses-09-00364-f001" orientation="portrait" position="float">
<label>Figure 1</label>
<caption>
<p>Different types of collected samples by French administrative department (excluding French Guyana in South America).</p>
</caption>
<graphic xlink:href="viruses-09-00364-g001"></graphic>
</fig>
<fig id="viruses-09-00364-f002" orientation="portrait" position="float">
<label>Figure 2</label>
<caption>
<p>Bayesian phylogeny of 50 genetic sequences of viruses detected in the study with 127 representative sequences of the whole diversity of the group of
<italic>Coronavirinae</italic>
. Selected coronavirus RdRp sequences, including some extracted from full genomes, were aligned with original sequences from this study in SEAVIEW v4.6. [
<xref rid="B8-viruses-09-00364" ref-type="bibr">8</xref>
]. Statistical support (posterior probability) of nodes are depicted using a gradual color code of the tree, with green indicating significant posterior probability values (>0.95). Genbank identification numbers, strain names, and the main information are written in taxa labels. Taxa labels of
<italic>Alphacoronavirus</italic>
,
<italic>Betacoronavirus</italic>
and of the clade grouping
<italic>Gammacoronavirus</italic>
and
<italic>Deltacoronavirus</italic>
are in purple, blue, and orange, respectively. Viruses detected in this study are depicted in red (HE: Sequences from hedgehogs, R: Sequences from rodents, CS: Sequences from bats; and L: Sequences from rabbits).</p>
</caption>
<graphic xlink:href="viruses-09-00364-g002"></graphic>
</fig>
<table-wrap id="viruses-09-00364-t001" orientation="portrait" position="float">
<object-id pub-id-type="pii">viruses-09-00364-t001_Table 1</object-id>
<label>Table 1</label>
<caption>
<p>Species of analyzed bats by year and by positive sample.</p>
</caption>
<table frame="hsides" rules="groups">
<thead>
<tr>
<th rowspan="2" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" colspan="1">Species</th>
<th colspan="4" align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1">Number of Carcasses Total (Positive Samples)</th>
</tr>
<tr>
<th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2013</th>
<th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2014</th>
<th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">2015</th>
<th align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">total</th>
</tr>
</thead>
<tbody>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">Non-identified bats</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">4</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3</td>
<td align="center" valign="middle" rowspan="1" colspan="1">9</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Rhinolophus ferrumequinum</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Rhinolophus hipposideros</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">4</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">8</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Rhinolophus euryale</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Barbastella barbatellus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">4</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Myotis myotis</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Myotis blythii</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Myotis mystacinus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">4</td>
<td align="center" valign="middle" rowspan="1" colspan="1">5</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Myotis emarginatus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">11 (2)</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">13</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Myotis bechsteinii</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Myotis daubentonii</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Myotis nattereri</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1 (1)</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Myotis</italic>
sp.</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Nyctalus noctula</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Nyctalus leisleri</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">9</td>
<td align="center" valign="middle" rowspan="1" colspan="1">4</td>
<td align="center" valign="middle" rowspan="1" colspan="1">15</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Plecotus austriacus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">4</td>
<td align="center" valign="middle" rowspan="1" colspan="1">4</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">10</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Plecotus auritus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3</td>
<td align="center" valign="middle" rowspan="1" colspan="1">4</td>
<td align="center" valign="middle" rowspan="1" colspan="1">8</td>
<td align="center" valign="middle" rowspan="1" colspan="1">15</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Pipistrellus pipistrellus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">42</td>
<td align="center" valign="middle" rowspan="1" colspan="1">127 (4)</td>
<td align="center" valign="middle" rowspan="1" colspan="1">78 (1)</td>
<td align="center" valign="middle" rowspan="1" colspan="1">247</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Pipistrellus kuhlii</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">9</td>
<td align="center" valign="middle" rowspan="1" colspan="1">20</td>
<td align="center" valign="middle" rowspan="1" colspan="1">11</td>
<td align="center" valign="middle" rowspan="1" colspan="1">40</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Pipistrellus nathusii</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">20</td>
<td align="center" valign="middle" rowspan="1" colspan="1">5</td>
<td align="center" valign="middle" rowspan="1" colspan="1">27</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Pipistrellus pygmaeus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">17</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3</td>
<td align="center" valign="middle" rowspan="1" colspan="1">23</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Pipistrellus</italic>
sp.</td>
<td align="center" valign="middle" rowspan="1" colspan="1">11</td>
<td align="center" valign="middle" rowspan="1" colspan="1">20 (2)</td>
<td align="center" valign="middle" rowspan="1" colspan="1">7</td>
<td align="center" valign="middle" rowspan="1" colspan="1">38</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Vespertilio murinus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">2</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Eptesicus serotinus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">7</td>
<td align="center" valign="middle" rowspan="1" colspan="1">11</td>
<td align="center" valign="middle" rowspan="1" colspan="1">8</td>
<td align="center" valign="middle" rowspan="1" colspan="1">26</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Eptesicus nilssonii</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Miniopterus schreibersii</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1 (1)</td>
<td align="center" valign="middle" rowspan="1" colspan="1">4 (1)</td>
<td align="center" valign="middle" rowspan="1" colspan="1">5</td>
</tr>
<tr>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">
<bold>Total</bold>
</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">113</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">243 (9)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">148 (3)</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">504 (12)</td>
</tr>
</tbody>
</table>
</table-wrap>
<table-wrap id="viruses-09-00364-t002" orientation="portrait" position="float">
<object-id pub-id-type="pii">viruses-09-00364-t002_Table 2</object-id>
<label>Table 2</label>
<caption>
<p>Number of samples and positive results for rodents per year and per area (NC: No capture program, NE: Not evaluable, [IC 95%]).</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">Year</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Species</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Bitche Infected/Total</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Forbach Infected/Total</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">La Petite Pierre Infected/Total</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Murbach Infected/Total</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Wissembourg Infected/Total</th>
<th align="center" valign="middle" style="border-top:solid thin;border-bottom:solid thin" rowspan="1" colspan="1">Prevalence by Species</th>
</tr>
</thead>
<tbody>
<tr>
<td rowspan="5" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">2014</td>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Apodemus</italic>
sp.</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">6/82</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/4</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(6/86) 6.98 [3.24; 14.40]</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Myodes glareolus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3/32</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/4</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(3/38) 7.89 [2.72; 20.80]</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Arvicola terrestris</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/16</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(0/16) 0 [0.00; 19.36]</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Microtus</italic>
sp.</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/3</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(0/3) 0 [0.00; 56.15]</td>
</tr>
<tr>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Total</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">9/114</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0/8</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0/2</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0/19</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td rowspan="5" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">2015</td>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Apodemus</italic>
sp.</td>
<td align="center" valign="middle" rowspan="1" colspan="1">8/64</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1/38</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(9/104) 8.65 [4.62; 15.63]</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Myodes glareolus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1/7</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/17</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1/15</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(2/39) 5.13 [1.42; 16.89]</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Arvicola terrestris</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/18</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(0/18) 0 [0.00; 17.59]</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Microtus</italic>
sp.</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/6</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(0/6) 0 [0.00; 39.30]</td>
</tr>
<tr>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Total</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">9/77</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">1/55</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">1/17</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0/18</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td rowspan="5" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">2016</td>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Apodemus</italic>
sp.</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1/4</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/11</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(1/16) 6.25 [1.11; 28.33]</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Myodes glareolus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/2</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(0/3) 0 [0.00; 56.15]</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Arvicola terrestris</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(0/1) 0 [0.00; 79.35]</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Microtus</italic>
sp.</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" rowspan="1" colspan="1">NE</td>
</tr>
<tr>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">Total</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">1/6</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0/12</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">0/2</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">NC</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
</tr>
<tr>
<td rowspan="5" align="center" valign="middle" style="border-bottom:solid thin" colspan="1">
<bold>Total from 2014 to 2016</bold>
</td>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Apodemus</italic>
sp.</td>
<td align="center" valign="middle" rowspan="1" colspan="1">9/68</td>
<td align="center" valign="middle" rowspan="1" colspan="1">6/82</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1/53</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/3</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(16/206) 7.77 [4.84; 12.24]</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Myodes glareolus</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1/9</td>
<td align="center" valign="middle" rowspan="1" colspan="1">3/32</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/21</td>
<td align="center" valign="middle" rowspan="1" colspan="1">1/18</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(5/80) 6.25 [2.70; 13.81]</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Arvicola terrestris</italic>
</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/1</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/34</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(0/35) 0 [0.00; 9.89]</td>
</tr>
<tr>
<td align="left" valign="middle" rowspan="1" colspan="1">
<italic>Microtus</italic>
sp.</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/6</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/0</td>
<td align="center" valign="middle" rowspan="1" colspan="1">0/3</td>
<td align="center" valign="middle" rowspan="1" colspan="1">(0/9) 0 [0.00; 29.91]</td>
</tr>
<tr>
<td align="left" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">
<bold>Total</bold>
</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">
<bold>10/83</bold>
</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">
<bold>9/114</bold>
</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">
<bold>1/75</bold>
</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">
<bold>1/21</bold>
</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1">
<bold>0/37</bold>
</td>
<td align="center" valign="middle" style="border-bottom:solid thin" rowspan="1" colspan="1"></td>
</tr>
</tbody>
</table>
</table-wrap>
</floats-group>
</pmc>
<affiliations>
<list>
<country>
<li>France</li>
</country>
<region>
<li>Île-de-France</li>
</region>
<settlement>
<li>Paris</li>
</settlement>
</list>
<tree>
<noCountry>
<name sortKey="Boucher, Jean Marc" sort="Boucher, Jean Marc" uniqKey="Boucher J" first="Jean-Marc" last="Boucher">Jean-Marc Boucher</name>
<name sortKey="Boue, Franck" sort="Boue, Franck" uniqKey="Boue F" first="Franck" last="Boué">Franck Boué</name>
<name sortKey="Monchatre Leroy, Elodie" sort="Monchatre Leroy, Elodie" uniqKey="Monchatre Leroy E" first="Elodie" last="Monchatre-Leroy">Elodie Monchatre-Leroy</name>
<name sortKey="Moutou, Francois" sort="Moutou, Francois" uniqKey="Moutou F" first="François" last="Moutou">François Moutou</name>
<name sortKey="Renault, Camille" sort="Renault, Camille" uniqKey="Renault C" first="Camille" last="Renault">Camille Renault</name>
<name sortKey="Umhang, Gerald" sort="Umhang, Gerald" uniqKey="Umhang G" first="Gérald" last="Umhang">Gérald Umhang</name>
</noCountry>
<country name="France">
<region name="Île-de-France">
<name sortKey="Ar Gouilh, Meriadeg" sort="Ar Gouilh, Meriadeg" uniqKey="Ar Gouilh M" first="Meriadeg" last="Ar Gouilh">Meriadeg Ar Gouilh</name>
</region>
</country>
</tree>
</affiliations>
</record>

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