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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Exportations of Symptomatic Cases of MERS-CoV Infection to Countries
outside the Middle East</title>
<author><name sortKey="Carias, Cristina" sort="Carias, Cristina" uniqKey="Carias C" first="Cristina" last="Carias">Cristina Carias</name>
</author>
<author><name sortKey="O Agan, Justin J" sort="O Agan, Justin J" uniqKey="O Agan J" first="Justin J." last="O Agan">Justin J. O Agan</name>
</author>
<author><name sortKey="Jewett, Amy" sort="Jewett, Amy" uniqKey="Jewett A" first="Amy" last="Jewett">Amy Jewett</name>
</author>
<author><name sortKey="Gambhir, Manoj" sort="Gambhir, Manoj" uniqKey="Gambhir M" first="Manoj" last="Gambhir">Manoj Gambhir</name>
</author>
<author><name sortKey="Cohen, Nicole J" sort="Cohen, Nicole J" uniqKey="Cohen N" first="Nicole J." last="Cohen">Nicole J. Cohen</name>
</author>
<author><name sortKey="Haber, Yoni" sort="Haber, Yoni" uniqKey="Haber Y" first="Yoni" last="Haber">Yoni Haber</name>
</author>
<author><name sortKey="Pesik, Nicki" sort="Pesik, Nicki" uniqKey="Pesik N" first="Nicki" last="Pesik">Nicki Pesik</name>
</author>
<author><name sortKey="Swerdlow, David L" sort="Swerdlow, David L" uniqKey="Swerdlow D" first="David L." last="Swerdlow">David L. Swerdlow</name>
</author>
</titleStmt>
<publicationStmt><idno type="wicri:source">PMC</idno>
<idno type="pmid">27358972</idno>
<idno type="pmc">4806968</idno>
<idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4806968</idno>
<idno type="RBID">PMC:4806968</idno>
<idno type="doi">10.3201/eid2204.150976</idno>
<date when="2016">2016</date>
<idno type="wicri:Area/Pmc/Corpus">000064</idno>
<idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000064</idno>
</publicationStmt>
<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Exportations of Symptomatic Cases of MERS-CoV Infection to Countries
outside the Middle East</title>
<author><name sortKey="Carias, Cristina" sort="Carias, Cristina" uniqKey="Carias C" first="Cristina" last="Carias">Cristina Carias</name>
</author>
<author><name sortKey="O Agan, Justin J" sort="O Agan, Justin J" uniqKey="O Agan J" first="Justin J." last="O Agan">Justin J. O Agan</name>
</author>
<author><name sortKey="Jewett, Amy" sort="Jewett, Amy" uniqKey="Jewett A" first="Amy" last="Jewett">Amy Jewett</name>
</author>
<author><name sortKey="Gambhir, Manoj" sort="Gambhir, Manoj" uniqKey="Gambhir M" first="Manoj" last="Gambhir">Manoj Gambhir</name>
</author>
<author><name sortKey="Cohen, Nicole J" sort="Cohen, Nicole J" uniqKey="Cohen N" first="Nicole J." last="Cohen">Nicole J. Cohen</name>
</author>
<author><name sortKey="Haber, Yoni" sort="Haber, Yoni" uniqKey="Haber Y" first="Yoni" last="Haber">Yoni Haber</name>
</author>
<author><name sortKey="Pesik, Nicki" sort="Pesik, Nicki" uniqKey="Pesik N" first="Nicki" last="Pesik">Nicki Pesik</name>
</author>
<author><name sortKey="Swerdlow, David L" sort="Swerdlow, David L" uniqKey="Swerdlow D" first="David L." last="Swerdlow">David L. Swerdlow</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="2016">2016</date>
</imprint>
</series>
</biblStruct>
</sourceDesc>
</fileDesc>
<profileDesc><textClass></textClass>
</profileDesc>
</teiHeader>
<front><div type="abstract" xml:lang="en"><p>In 2012, an outbreak of infection with Middle East respiratory syndrome coronavirus
(MERS-CoV), was detected in the Arabian Peninsula. Modeling can produce estimates of
the expected annual number of symptomatic cases of MERS-CoV infection exported and
the likelihood of exportation from source countries in the Middle East to countries
outside the region.</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>
<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">27358972</article-id>
<article-id pub-id-type="pmc">4806968</article-id>
<article-id pub-id-type="publisher-id">15-0976</article-id>
<article-id pub-id-type="doi">10.3201/eid2204.150976</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>Exportations of Symptomatic Cases of MERS-CoV Infection to Countries outside the Middle East</subject>
</subj-group>
</article-categories>
<title-group><article-title>Exportations of Symptomatic Cases of MERS-CoV Infection to Countries
outside the Middle East</article-title>
<alt-title alt-title-type="running-head">Exportations of MERS-CoV outside the Middle
East</alt-title>
</title-group>
<contrib-group><contrib contrib-type="author" corresp="yes"><name><surname>Carias</surname>
<given-names>Cristina</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>O’Hagan</surname>
<given-names>Justin J.</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Jewett</surname>
<given-names>Amy</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Gambhir</surname>
<given-names>Manoj</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Cohen</surname>
<given-names>Nicole J.</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Haber</surname>
<given-names>Yoni</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Pesik</surname>
<given-names>Nicki</given-names>
</name>
</contrib>
<contrib contrib-type="author"><name><surname>Swerdlow</surname>
<given-names>David L.</given-names>
</name>
</contrib>
<aff id="aff1">IHRC, Inc., Atlanta (C. Carias, J.J. O’Hagan);</aff>
<aff id="aff2">Centers for Disease Control and Prevention, Atlanta, Georgia, USA (C. Carias, J.J. O’Hagan, A. Jewett, M. Gambhir, N.J. Cohen, Y. Haber, N. Pesik, D.L. Swerdlow);</aff>
<aff id="aff3">Monash University, Melbourne, Victoria, Australia (M. Gambhir)</aff>
</contrib-group>
<author-notes><corresp id="cor1">Address for correspondence: Cristina Carias, Centers for Disease
Control and Prevention, 1600 Clifton Rd NE, Mailstop C18, Atlanta, GA 30329-4027,
USA; email: <email xlink:href="vnn9@cdc.gov">vnn9@cdc.gov</email>
</corresp>
</author-notes>
<pub-date pub-type="ppub"><month>4</month>
<year>2016</year>
</pub-date>
<volume>22</volume>
<issue>4</issue>
<fpage>723</fpage>
<lpage>725</lpage>
<abstract><p>In 2012, an outbreak of infection with Middle East respiratory syndrome coronavirus
(MERS-CoV), was detected in the Arabian Peninsula. Modeling can produce estimates of
the expected annual number of symptomatic cases of MERS-CoV infection exported and
the likelihood of exportation from source countries in the Middle East to countries
outside the region.</p>
</abstract>
<kwd-group kwd-group-type="author"><title>Keywords: </title>
<kwd>Middle East</kwd>
<kwd>coronavirus</kwd>
<kwd>exportations</kwd>
<kwd>Middle East respiratory syndrome coronavirus</kwd>
<kwd>MERS-CoV</kwd>
<kwd>travel</kwd>
<kwd>disease spread</kwd>
<kwd>viruses</kwd>
</kwd-group>
</article-meta>
</front>
<body><p>In September 2012, the first confirmed case of Middle East respiratory syndrome coronavirus
(MERS-CoV) infection was reported in the Kingdom of Saudi Arabia (KSA) (<xref rid="R1" ref-type="bibr"><italic>1</italic>
</xref>
). Approximately 900
laboratory-confirmed cases had been identified as of January 16, 2015; more than 300 (37%)
have resulted in death. Although KSA has reported >80% of cases, infections have been
confirmed in other Middle Eastern, European, North American, and, more recently, Asian
countries (<xref rid="R2" ref-type="bibr"><italic>2</italic>
</xref>
). Multiple
introductions from an animal reservoir have occurred (<xref rid="R3" ref-type="bibr"><italic>3</italic>
</xref>
), but human-to-human transmission of MERS-CoV has also
been documented among family members of case-patients and healthcare personnel who cared
for case-patients (<xref rid="R4" ref-type="bibr"><italic>4</italic>
</xref>
–<xref rid="R6" ref-type="bibr"><italic>6</italic>
</xref>
). More than a dozen cases have been
identified among travelers returning from the Middle East to their home countries; onward
transmission in destination countries also occurred (<xref rid="R7" ref-type="bibr"><italic>7</italic>
</xref>
,<xref rid="R8" ref-type="bibr"><italic>8</italic>
</xref>
).</p>
<sec><title>The Study</title>
<p>We calculated the expected annual number of exportations of symptomatic cases of
infection with MERS-CoV and the likelihood of exportation from the Middle Eastern
countries where additional cases have been detected (KSA, Jordan, Qatar, and the United
Arab Emirates [UAE], which we refer to as source countries) to countries outside the
Middle East. We defined exportation as the arrival of a person infected with MERS-CoV in
a country other than KSA, Jordan, Qatar, and UAE as a result of MERS-CoV infection in
those source countries and subsequent outbound travel (not including medical
evacuation). Because it is unclear whether MERS-CoV cases in Middle Eastern countries
other than the source countries resulted from importation or a local outbreak, those
countries were excluded from the analysis. Exportations can occur by visitors returning
to their home countries or source country residents traveling abroad. We produced
example calculations for destination countries outside the Middle East where exportation
of MERS-CoV infection cases has been confirmed (Algeria, Austria, France, Greece, Italy,
Malaysia, Netherlands, Tunisia, United Kingdom, and the United States) as of January 16,
2015 (<xref ref-type="table" rid="T1">Table 1</xref>
).</p>
<table-wrap id="T1" position="float"><label>Table 1</label>
<caption><title>Number of symptomatic cases of MERS-CoV infection and number of symptomatic
cases exported to countries outside the Middle East, overall and during January 1,
2013–January 16, 2015*</title>
</caption>
<table frame="hsides" rules="groups"><col width="122" span="1"></col>
<col width="114" span="1"></col>
<thead><tr><th valign="bottom" align="left" scope="col" rowspan="1" colspan="1">Region and country<hr></hr>
</th>
<th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">No. cases overall (no. cases Jan
1, 2013–Jan 16, 2015) <hr></hr>
</th>
</tr>
<tr><th colspan="2" valign="top" align="left" scope="colgroup" rowspan="1">Source
countries</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> KSA</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">831 (826)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> UAE</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">67 (67)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Jordan</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">9 (7)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Qatar<hr></hr>
</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">11 (9)<hr></hr>
</th>
</tr>
<tr><th colspan="2" valign="top" align="left" scope="colgroup" rowspan="1">Other Middle Eastern
countries</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Iran</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">5 (5)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Oman</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">7 (7)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Kuwait</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">3 (3)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Lebanon</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (1)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Turkey</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (1)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Yemen<hr></hr>
</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (1)<hr></hr>
</th>
</tr>
<tr><th colspan="2" valign="top" align="left" scope="colgroup" rowspan="1">Countries outside
the Middle East</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Tunisia</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">3 (3)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> United Kingdom</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">3 (3)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Algeria</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">2 (2)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> France</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">2 (2)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Netherlands</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">2 (2)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Austria</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (1)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Italy</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (1)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Malaysia<hr></hr>
</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (1)<hr></hr>
</th>
</tr>
<tr><th valign="bottom" align="left" scope="col" rowspan="1" colspan="1">Source and destination
country<hr></hr>
</th>
<th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">No. cases exported<hr></hr>
</th>
</tr>
<tr><th colspan="2" valign="top" align="left" scope="colgroup" rowspan="1">KSA</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Algeria</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">2 (2)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Netherlands</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">2 (2)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> United States</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">2 (2)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Austria</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (1)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Greece</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (1)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Malaysia</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (1)</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> United Kingdom<hr></hr>
</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (1)<hr></hr>
</th>
</tr>
<tr><th colspan="2" valign="top" align="left" scope="colgroup" rowspan="1">Qatar</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Tunisia<hr></hr>
</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (1)<hr></hr>
</th>
</tr>
<tr><th colspan="2" valign="top" align="left" scope="colgroup" rowspan="1">UAE</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> France<hr></hr>
</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (1)<hr></hr>
</th>
</tr>
<tr><th colspan="2" valign="top" align="left" scope="colgroup" rowspan="1">Jordan</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1"> Italy</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (1)</th>
</tr>
</thead>
<tbody><tr><td rowspan="1" colspan="1"></td>
</tr>
</tbody>
</table>
<table-wrap-foot><p>*Based on World Health Organization case counts. MERS-CoV, Middle Eastern
respiratory syndrome coronavirus; KSA, Kingdom of Saudi Arabia; UAE, United Arab
Emirates.</p>
</table-wrap-foot>
</table-wrap>
<p>To calculate exportations, we used a simple multiplier model whereby MERS-CoV incidence
rates among source country residents were extrapolated to rates among visitors. In
particular, for each source country, the expected number of cases among travelers was
calculated by multiplying the infection rate among residents in the affected countries
(total number of cases divided by number of residents) by the number of travelers and
the days travelers spend, on average, in the affected countries (<xref rid="R9" ref-type="bibr"><italic>9</italic>
</xref>
). To calculate incidence rates in destination
countries, the number of symptomatic cases was considered to be 10 times greater than
the reported number of cases (<xref rid="R8" ref-type="bibr"><italic>8</italic>
</xref>
).
Calculations were made by using Excel (Microsoft Corporation, Redmond, Washington, USA).
The probability of exportation was calculated while assuming the number of exportations
was Poisson distributed, with the mean equal to the expected exportations (<xref ref-type="local-data" rid="SD1">Technical Appendix 1</xref>
, and <xref ref-type="local-data" rid="SD1">Technical Appendix 2</xref>
). </p>
<p>Expected annual exportations of symptomatic MERS-CoV infection cases among visitors to
the Middle East source countries were highest among visitors to KSA (<xref ref-type="table" rid="T2">Table 2</xref>
). For visitors returning from KSA, expected
exportations were higher among visitors returning to Algeria, where the number of
expected exportations was 1 (95% CI 0–5) and the likelihood of
<underline>></underline>
1 exportation was 58%; and Malaysia, where the number of
expected exportations was 1 (95% CI 0–5) and the likelihood of
<underline>></underline>
1 exportation was 47%.</p>
<table-wrap id="T2" position="float"><label>Table 2</label>
<caption><title>Estimated annual number of symptomatic cases of MERS-CoV infection exported
and likelihood of <underline>></underline>
1 exportation for countries outside
the Middle East among visitors to the source countries*</title>
</caption>
<table frame="hsides" rules="groups"><col width="80" span="1"></col>
<col width="136" span="1"></col>
<col width="84" span="1"></col>
<col width="90" span="1"></col>
<col width="90" span="1"></col>
<thead><tr><th rowspan="2" valign="bottom" align="left" scope="col" colspan="1">Country of
destination<hr></hr>
</th>
<th rowspan="2" valign="bottom" align="center" scope="col" colspan="1">Observed no.
symptomatic cases exported<hr></hr>
</th>
<th valign="bottom" colspan="3" align="center" scope="colgroup" rowspan="1">No. cases
exported from source countries (95% CI); % likelihood for
<underline>></underline>
1 exportation†<hr></hr>
</th>
</tr>
<tr><th valign="bottom" colspan="1" align="center" scope="colgroup" rowspan="1">Jordan<hr></hr>
</th>
<th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">KSA<hr></hr>
</th>
<th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">UAE<hr></hr>
</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">Algeria</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">2 from KSA</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (0–5); 58</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">NA</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">Austria</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 1</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">NA</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">France</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 from UAE</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 11</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 9</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">Italy</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 from Jordan</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 3</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 9</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">Greece</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 1</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">NA</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">Netherlands</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">2 from KSA</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 5</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 4</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">Malaysia</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 from KSA</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (0–5); 47</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">NA</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">Tunisia</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 from Qatar</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 19</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">NA</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">United Kingdom</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 from KSA</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 24</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 35</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">United States</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 1</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 27</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 31</th>
</tr>
</thead>
<tbody><tr><td rowspan="1" colspan="1"></td>
</tr>
</tbody>
</table>
<table-wrap-foot><p>*The incubation period considered was 5.5 days (95% CI 3.6–10.2 days)
(<xref rid="R8" ref-type="bibr"><italic>8</italic>
</xref>
). MERS-CoV, Middle
Eastern respiratory syndrome coronavirus; KSA, Kingdom of Saudi Arabia; UAE,
United Arab Emirates; NA, not available.
†Information on tourists to
Qatar was not available.</p>
</table-wrap-foot>
</table-wrap>
<p>Expected exportations among residents from the Middle East source countries traveling
abroad also were estimated to be higher for visitors from KSA (<xref ref-type="table" rid="T3">Table 3</xref>
). Expected exportations among residents in KSA visiting
abroad were highest for the United States, where the number of expected exportations was
1 (95% CI 0–5) and the likelihood of <underline>></underline>
1 exportation was
51%.</p>
<table-wrap id="T3" position="float"><label>Table 3</label>
<caption><title>Estimated annual number of symptomatic cases of MERS-CoV infection exported
and likelihood of <underline>></underline>
1 exportation for countries outside
the Middle East among source country residents traveling outside the Middle
East*</title>
</caption>
<table frame="hsides" rules="groups"><col width="82" span="1"></col>
<col width="99" span="1"></col>
<col width="74" span="1"></col>
<col width="75" span="1"></col>
<col width="74" span="1"></col>
<col width="75" span="1"></col>
<thead><tr><th rowspan="2" valign="bottom" align="left" scope="col" colspan="1">Country of
destination<hr></hr>
</th>
<th rowspan="2" valign="bottom" align="center" scope="col" colspan="1">Observed no.
symptomatic cases exported<hr></hr>
</th>
<th valign="bottom" colspan="4" align="center" scope="colgroup" rowspan="1">No. cases
exported from source countries (95% CI); % likelihood for
<underline>></underline>
1 exportation†<hr></hr>
</th>
</tr>
<tr><th valign="bottom" colspan="1" align="center" scope="colgroup" rowspan="1">Jordan<hr></hr>
</th>
<th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">KSA<hr></hr>
</th>
<th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">Qatar<hr></hr>
</th>
<th valign="bottom" align="center" scope="col" rowspan="1" colspan="1">UAE<hr></hr>
</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">Italy‡</th>
<th valign="middle" align="center" scope="col" rowspan="1" colspan="1">0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 1</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 18</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">NA</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 8</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">Malaysia§</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 33</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 1</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 2</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">Tunisia‡</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 2</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">United Kingdom§</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 35</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 3</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 25</th>
</tr>
<tr><th valign="top" align="left" scope="col" rowspan="1" colspan="1">United States§</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">2 from KSA</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 0</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">1 (0–5); 51</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 2</th>
<th valign="top" align="center" scope="col" rowspan="1" colspan="1">0 (0–4); 8</th>
</tr>
</thead>
<tbody><tr><td rowspan="1" colspan="1"></td>
</tr>
</tbody>
</table>
<table-wrap-foot><p>*The incubation period considered was 5.5 days (95% CI 3.6–10.2 days)
(<xref rid="R8" ref-type="bibr"><italic>8</italic>
</xref>
). MERS-CoV, Middle
Eastern respiratory syndrome coronavirus; KSA, Kingdom of Saudi Arabia; UAE,
United Arab Emirates; NA, not available.
†Information on Middle
Eastern visitors to France, Netherlands, and Greece was not available. Number of
Middle Eastern residents visiting Algeria and Austria was not available by country
of residence.
‡Number of Middle Eastern visitors traveling to Italy
and Tunisia corresponds to persons whose nationality is that of Middle Eastern
source countries.
§Number of Middle Eastern visitors traveling to
Malaysia, the United Kingdom, and the United States corresponds to residents in
the Middle East.</p>
</table-wrap-foot>
</table-wrap>
</sec>
<sec sec-type="conclusions"><title>Conclusions</title>
<p>More complex models have been developed to characterize exportations of infectious
disease cases via infectious travelers (<xref rid="R10" ref-type="bibr"><italic>10</italic>
</xref>
,<xref rid="R11" ref-type="bibr"><italic>11</italic>
</xref>
). The main advantage of our approach is its simplicity
and reproducibility within short timeframes. This model also complements previous work
on the risk for MERS-CoV exportation by global air travel, which attempted to quantify
travel volume to the affected areas and calculate exportations among Hajj pilgrims in
KSA (<xref rid="R12" ref-type="bibr"><italic>12</italic>
</xref>
,<xref rid="R13" ref-type="bibr"><italic>13</italic>
</xref>
). In our calculations, however, the visitor data
included persons traveling by air, land, and sea and distinguished between visitors to
the Middle East and persons from the Middle East traveling abroad over the period of 1
year. Unlike Khan et al. (<xref rid="R12" ref-type="bibr"><italic>12</italic>
</xref>
),
we accounted for the rate of infection in the source countries by calculating source
country–specific MERS-CoV incidence rates. Furthermore, by accounting for the
different travel volume of visitors to the Middle East compared with Middle East
residents traveling to non–Middle Eastern countries, we suggested the mode of
exportation (visitor to the Middle East vs. Middle East resident visiting abroad). For
Malaysia, estimated expected exportations were higher among visitors to source countries
than among source country residents visiting abroad, consistent with the number of
exportations detected by surveillance. However, the opposite was true for the United
States, where 2 source country residents were found to have MERS-CoV infection during
their US visit (<xref rid="R7" ref-type="bibr"><italic>7</italic>
</xref>
).</p>
<p>Our findings have limitations. The estimates are based on historical incidence data.
Thus, they are especially applicable for periods in which the incidence of the disease
remains stable. For outbreaks characterized by a highly transmissible pathogen, the
model might severely underestimate exportations if incidence rates are not projected to
the period for which exportations are calculated. In addition, our small multiplier only
took into account exportations of symptomatic cases. Given that most of the detected
exportations resulted in hospitalization of the infected case-patient, the number of
exportations calculated here likely refers to exportations of severe symptomatic cases.
Recent results from a serologic survey performed during December 2012–December
2013 indicate that there might be as many as 44,951 (95% CI 26,971–71,922)
persons infected with MERS-CoV in KSA (<xref rid="R14" ref-type="bibr"><italic>14</italic>
</xref>
). During that period, there were 125 reported
confirmed cases; thus, the ratio of asymptomatic to reported cases might be much higher,
possibly in the hundreds. This finding suggests that exportations of asymptomatic cases
might be several orders of magnitude higher than those of severe symptomatic cases.</p>
<p>The upper bound of exportations for the countries least likely to receive symptomatic
case importations was 4, suggesting that small numbers of importations are largely
stochastic events. Although every country is at risk, as illustrated by the recent
outbreak of MERS-CoV infections in South Korea that was triggered by just 1 importation
(<xref rid="R15" ref-type="bibr"><italic>15</italic>
</xref>
), our model can be used
to assess risk level. Combined with other indicators, our model can help determine the
level of additional public health measures (e.g., border screenings) required for
infectious diseases threats from abroad.</p>
<p>No exportations of symptomatic cases were detected in some of the top travel volume
countries for trips originating in KSA, Jordan, UAE, and Qatar. Travel volume to Egypt,
India, and Pakistan was several times higher than that for other countries where
MERS-CoV has been detected. However, only 1 case of MERS-CoV infection has been detected
in Egypt (in a KSA resident) (<ext-link ext-link-type="uri" xlink:href="http://www.who.int/csr/don/2014_05_01_mers">http://www.who.int/csr/don/2014_05_01_mers</ext-link>
), and no MERS-CoV cases have
been detected in India or Pakistan. This finding suggests that MERS-CoV introductions
may have already occurred in these countries but have not been detected.</p>
<p>In summary, by adapting a simple model of disease spread, we estimated the expected
number of MERS-CoV symptomatic case exportations during a 1-year period among visitors
to the Middle East and visitors from KSA, Jordan, Qatar, and UAE to non–Middle
Eastern countries where case exportations have occurred. Our estimations suggest that
the risk for repeated exportations of severe symptomatic MERS-CoV cases is low, although
the number of asymptomatic case exportations might be higher.</p>
</sec>
<sec sec-type="supplementary-material"><title></title>
<supplementary-material content-type="local-data" id="SD1"><caption><title>Technical Appendix 1</title>
<p>Methods for calculating exportations of cases of Middle East respiratory syndrome
coronavirus (MERS-CoV) infection.</p>
</caption>
<media mimetype="application" mime-subtype="pdf" xlink:href="15-0976-Techapp-s1.pdf" xlink:type="simple" id="d36e749" position="anchor"></media>
</supplementary-material>
<supplementary-material content-type="local-data" id="SD2"><caption><title>Technical Appendix 2</title>
<p>Index on estimating spread of Middle East respiratory syndrome coronavirus
(MERS-CoV) infection by travel.</p>
</caption>
<media mimetype="application" mime-subtype="excel" xlink:href="15-0976-Techapp-s2.xlsx" xlink:type="simple" id="d36e756" position="anchor"></media>
</supplementary-material>
</sec>
</body>
<back><fn-group><fn fn-type="citation"><p><italic>Suggested citation for this article</italic>
: Carias C, O’Hagan JJ,
Jewett A, Gambhir M, Cohen NJ, Haber Y, et al. Exportations of symptomatic cases of
MERS-CoV infection to countries outside the Middle East. Emerg Infect Dis. 2016 Apr
[<italic>date cited</italic>
]. <ext-link ext-link-type="uri" xlink:href="http://dx.doi.org/10.3201/eid2204.150976">http://dx.doi.org/10.3201/eid2204.150976</ext-link>
</p>
</fn>
</fn-group>
<bio id="d36e769"><p>Dr. Carias is a modeler in the National Center for Emerging and Zoonotic Infectious
Diseases at the Centers for Disease Control and Prevention. She is interested in using
economic and infectious disease models to assist decision making in public health.</p>
</bio>
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