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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Asymptomatic Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infection: Extent and implications for infection control: A systematic review</title><author><name sortKey="Al Tawfiq, Jaffar A" sort="Al Tawfiq, Jaffar A" uniqKey="Al Tawfiq J" first="Jaffar A." last="Al-Tawfiq">Jaffar A. Al-Tawfiq</name><affiliation><nlm:aff id="aff1">Specialty Internal Medicine, Johns Hopkins Aramco Healthcare, Dhahran, Saudi Arabia</nlm:aff></affiliation><affiliation><nlm:aff id="aff2">Indiana University School of Medicine, Indianapolis, IN, USA</nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Johns Hopkins University School of Medicine, Baltimore, MD, USA</nlm:aff></affiliation></author><author><name sortKey="Gautret, Philippe" sort="Gautret, Philippe" uniqKey="Gautret P" first="Philippe" last="Gautret">Philippe Gautret</name><affiliation><nlm:aff id="aff4">Aix Marseille Univ, Institut de Recherche pour le Développement (IRD), Assistance Publique-Hôpitaux de Marseille (AP-HM), Service de Santé des Armées (SSA), Microbes Vecteurs Infections Tropicales et Méditerranéennes (VITROME), Institut Hospitalo-Universitaire-Méditerranée Infection (IHU-Méditerranée Infection), Marseille, France</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">30550839</idno><idno type="pmc">7110966</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7110966</idno><idno type="RBID">PMC:7110966</idno><idno type="doi">10.1016/j.tmaid.2018.12.003</idno><date when="2018">2018</date><idno type="wicri:Area/Pmc/Corpus">001415</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001415</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Asymptomatic Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infection: Extent and implications for infection control: A systematic review</title><author><name sortKey="Al Tawfiq, Jaffar A" sort="Al Tawfiq, Jaffar A" uniqKey="Al Tawfiq J" first="Jaffar A." last="Al-Tawfiq">Jaffar A. Al-Tawfiq</name><affiliation><nlm:aff id="aff1">Specialty Internal Medicine, Johns Hopkins Aramco Healthcare, Dhahran, Saudi Arabia</nlm:aff></affiliation><affiliation><nlm:aff id="aff2">Indiana University School of Medicine, Indianapolis, IN, USA</nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Johns Hopkins University School of Medicine, Baltimore, MD, USA</nlm:aff></affiliation></author><author><name sortKey="Gautret, Philippe" sort="Gautret, Philippe" uniqKey="Gautret P" first="Philippe" last="Gautret">Philippe Gautret</name><affiliation><nlm:aff id="aff4">Aix Marseille Univ, Institut de Recherche pour le Développement (IRD), Assistance Publique-Hôpitaux de Marseille (AP-HM), Service de Santé des Armées (SSA), Microbes Vecteurs Infections Tropicales et Méditerranéennes (VITROME), Institut Hospitalo-Universitaire-Méditerranée Infection (IHU-Méditerranée Infection), Marseille, France</nlm:aff></affiliation></author></analytic><series><title level="j">Travel Medicine and Infectious Disease</title><idno type="ISSN">1477-8939</idno><idno type="eISSN">1873-0442</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><sec><title>Background</title><p>The Middle East Respiratory Syndrome Coronavirus (MERS-CoV) emerged in 2012 and attracted an international attention as the virus caused multiple healthcare associated outbreaks. There are reports of the role of asymptomatic individuals in the transmission of MERS-CoV, however, the exact role is not known.</p></sec><sec><title>Method</title><p>The MEDLINE/PubMed and Scopus databases were searched for relevant papers published till August 2018 describing asymptomatic MERS-CoV infection.</p></sec><sec><title>Results</title><p>A total of 10 papers were retrieved and included in the final analysis and review. The extent of asymptomatic MERS infection had increased with change in the policy of testing asymptomatic contacts. In early cases in April 2012–October 2013, 12.5% were asymptomatic among 144 PCR laboratory-confirmed MERS-CoV cases while in 2014 the proportion rose to 25.1% among 255 confirmed cases. The proportion of asymptomatic cases reported among pediatric confirmed MERS-CoV cases were higher (41.9%–81.8%). Overall, the detection rate of MERS infection among asymptomatic contacts was 1-3.9% in studies included in this review. Asymptomatic individuals were less likely to have underlying condition compared to fatal cases. Of particular interest is that most of the identified pediatric cases were asymptomatic with no clear explanation.</p></sec><sec><title>Conclusions</title><p>The proportion of asymptomatic MERS cases were detected with increasing frequency as the disease progressed overtime. Those patients were less likely to have comorbid disease and may contribute to the transmission of the virus.</p></sec></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Drosten, C" uniqKey="Drosten C">C. Drosten</name></author><author><name sortKey="Muth, D" uniqKey="Muth D">D. Muth</name></author><author><name sortKey="Corman, V M" uniqKey="Corman V">V.M. Corman</name></author><author><name sortKey="Hussain, R" uniqKey="Hussain R">R. Hussain</name></author><author><name sortKey="Al Masri, M" uniqKey="Al Masri M">M. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Travel Med Infect Dis</journal-id><journal-id journal-id-type="iso-abbrev">Travel Med Infect Dis</journal-id><journal-title-group><journal-title>Travel Medicine and Infectious Disease</journal-title></journal-title-group><issn pub-type="ppub">1477-8939</issn><issn pub-type="epub">1873-0442</issn><publisher><publisher-name>Elsevier Ltd.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">30550839</article-id><article-id pub-id-type="pmc">7110966</article-id><article-id pub-id-type="publisher-id">S1477-8939(18)30343-0</article-id><article-id pub-id-type="doi">10.1016/j.tmaid.2018.12.003</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Asymptomatic Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infection: Extent and implications for infection control: A systematic review</article-title></title-group><contrib-group><contrib contrib-type="author" id="au1"><name><surname>Al-Tawfiq</surname><given-names>Jaffar A.</given-names></name><email>jaffar.tawfiq@jhah.com</email><email>jaltawfi@yahoo.com</email><xref rid="aff1" ref-type="aff">a</xref><xref rid="aff2" ref-type="aff">b</xref><xref rid="aff3" ref-type="aff">c</xref><xref rid="cor1" ref-type="corresp">∗</xref></contrib><contrib contrib-type="author" id="au2"><name><surname>Gautret</surname><given-names>Philippe</given-names></name><xref rid="aff4" ref-type="aff">d</xref></contrib></contrib-group><aff id="aff1"><label>a</label>Specialty Internal Medicine, Johns Hopkins Aramco Healthcare, Dhahran, Saudi Arabia</aff><aff id="aff2"><label>b</label>Indiana University School of Medicine, Indianapolis, IN, USA</aff><aff id="aff3"><label>c</label>Johns Hopkins University School of Medicine, Baltimore, MD, USA</aff><aff id="aff4"><label>d</label>Aix Marseille Univ, Institut de Recherche pour le Développement (IRD), Assistance Publique-Hôpitaux de Marseille (AP-HM), Service de Santé des Armées (SSA), Microbes Vecteurs Infections Tropicales et Méditerranéennes (VITROME), Institut Hospitalo-Universitaire-Méditerranée Infection (IHU-Méditerranée Infection), Marseille, France</aff><author-notes><corresp id="cor1"><label>∗</label>Corresponding author. P.O. Box 76, Room A-428-2, Building 61, Dhahran Health Center, Saudi Aramco, Dhahran, 31311, Saudi Arabia. <email>jaffar.tawfiq@jhah.com</email><email>jaltawfi@yahoo.com</email></corresp></author-notes><pub-date pub-type="pmc-release"><day>11</day><month>12</month><year>2018</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub" iso-8601-date="2019-02-01"><season>January-February</season><year>2019</year></pub-date><pub-date pub-type="epub"><day>11</day><month>12</month><year>2018</year></pub-date><volume>27</volume><fpage>27</fpage><lpage>32</lpage><history><date date-type="received"><day>2</day><month>10</month><year>2018</year></date><date date-type="rev-recd"><day>7</day><month>12</month><year>2018</year></date><date date-type="accepted"><day>10</day><month>12</month><year>2018</year></date></history><permissions><copyright-statement>© 2018 Elsevier Ltd. All rights reserved.</copyright-statement><copyright-year>2018</copyright-year><copyright-holder>Elsevier Ltd</copyright-holder><license><license-p>Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.</license-p></license></permissions><abstract id="abs0010"><sec><title>Background</title><p>The Middle East Respiratory Syndrome Coronavirus (MERS-CoV) emerged in 2012 and attracted an international attention as the virus caused multiple healthcare associated outbreaks. There are reports of the role of asymptomatic individuals in the transmission of MERS-CoV, however, the exact role is not known.</p></sec><sec><title>Method</title><p>The MEDLINE/PubMed and Scopus databases were searched for relevant papers published till August 2018 describing asymptomatic MERS-CoV infection.</p></sec><sec><title>Results</title><p>A total of 10 papers were retrieved and included in the final analysis and review. The extent of asymptomatic MERS infection had increased with change in the policy of testing asymptomatic contacts. In early cases in April 2012–October 2013, 12.5% were asymptomatic among 144 PCR laboratory-confirmed MERS-CoV cases while in 2014 the proportion rose to 25.1% among 255 confirmed cases. The proportion of asymptomatic cases reported among pediatric confirmed MERS-CoV cases were higher (41.9%–81.8%). Overall, the detection rate of MERS infection among asymptomatic contacts was 1-3.9% in studies included in this review. Asymptomatic individuals were less likely to have underlying condition compared to fatal cases. Of particular interest is that most of the identified pediatric cases were asymptomatic with no clear explanation.</p></sec><sec><title>Conclusions</title><p>The proportion of asymptomatic MERS cases were detected with increasing frequency as the disease progressed overtime. Those patients were less likely to have comorbid disease and may contribute to the transmission of the virus.</p></sec></abstract><kwd-group id="kwrds0010"><title>Keywords</title><kwd>Middle East Respiratory Syndrome Coronavirus</kwd><kwd>MERS</kwd><kwd>Healthcare associated outbreaks</kwd></kwd-group></article-meta></front><body><sec id="sec1"><label>1</label><title>Introduction</title><p id="p0010">The emergence of the Middle East Respiratory Syndrome Coronavirus (MERS-CoV) in 2012 had attracted an international attention as the virus had cause multiple healthcare associated outbreaks [<xref rid="bib1" ref-type="bibr">[1]</xref>, <xref rid="bib2" ref-type="bibr">[2]</xref>, <xref rid="bib3" ref-type="bibr">[3]</xref>, <xref rid="bib4" ref-type="bibr">[4]</xref>, <xref rid="bib5" ref-type="bibr">[5]</xref>, <xref rid="bib6" ref-type="bibr">[6]</xref>, <xref rid="bib7" ref-type="bibr">[7]</xref>, <xref rid="bib8" ref-type="bibr">[8]</xref>, <xref rid="bib9" ref-type="bibr">[9]</xref>, <xref rid="bib10" ref-type="bibr">[10]</xref>, <xref rid="bib11" ref-type="bibr">[11]</xref>, <xref rid="bib12" ref-type="bibr">[12]</xref>, <xref rid="bib13" ref-type="bibr">[13]</xref>, <xref rid="bib14" ref-type="bibr">[14]</xref>, <xref rid="bib15" ref-type="bibr">[15]</xref>, <xref rid="bib16" ref-type="bibr">[16]</xref>, <xref rid="bib17" ref-type="bibr">[17]</xref>, <xref rid="bib18" ref-type="bibr">[18]</xref>, <xref rid="bib19" ref-type="bibr">[19]</xref>, <xref rid="bib20" ref-type="bibr">[20]</xref>, <xref rid="bib21" ref-type="bibr">[21]</xref>] within the Kingdom of Saudi Arabia [<xref rid="bib1" ref-type="bibr">1</xref>,<xref rid="bib2" ref-type="bibr">2</xref>,<xref rid="bib6" ref-type="bibr">6</xref>,<xref rid="bib8" ref-type="bibr">8</xref>,<xref rid="bib9" ref-type="bibr">9</xref>,<xref rid="bib13" ref-type="bibr">13</xref>] and outside Saudi Arabia [<xref rid="bib4" ref-type="bibr">4</xref>,<xref rid="bib5" ref-type="bibr">5</xref>,<xref rid="bib22" ref-type="bibr">22</xref>,<xref rid="bib23" ref-type="bibr">23</xref>]. As of December 7, 2018, the World Health Organization reported 2267 laboratory-confirmed cases worldwide and at least 804 related deaths in 27 countries [<xref rid="bib24" ref-type="bibr">24</xref>]. Despite the increase in the number of cases, the actual incidence of MERS-CoV among hospitalized patients with community acquired pneumonia is low. In a longitudinal study from 2012 to 2016, a total of 2657 patients were screened for MERS-CoV and only 20 (0.74%) tested positive [<xref rid="bib25" ref-type="bibr">25</xref>]. The study showed that MERS-CoV was rare in admitted patients with community acquired pneumonia and influenza was more common than MERS [<xref rid="bib25" ref-type="bibr">25</xref>]. The explanation for the increased number of cases is the occurrence of multiple outbreaks as the hallmark of MERS-CoV transmission [<xref rid="bib26" ref-type="bibr">26</xref>]. The main patterns of MERS-CoV transmissions are: sporadic community cases from presumed non-human exposure, family clusters resulting from contact with an infected family index case, and healthcare-acquired infections between patients and from patients to healthcare workers [<xref rid="bib5" ref-type="bibr">5</xref>]. In addition, there were multiple occasions of transmission within the same family and that travel associated transmission of MERS-CoV poses a concern [<xref rid="bib27" ref-type="bibr">27</xref>,<xref rid="bib28" ref-type="bibr">28</xref>].</p><p id="p0015">There are reports of the role of asymptomatic individuals in the transmission of MERS-CoV, however, the exact role is not known [<xref rid="bib26" ref-type="bibr">26</xref>]. Many viral infections are associated with asymptomatic, subclinical, or very mild symptoms. In the case of poliomyelitis, 95% of those infected remain asymptomatic, yet they are still capable of spreading the virus (CDC). In one study, asymptomatic rhinovirus infection was four times as common as symptomatic infection [<xref rid="bib29" ref-type="bibr">29</xref>]. Another study found asymptomatic carriage of influenza virus to be 5.2–35.5% [<xref rid="bib30" ref-type="bibr">30</xref>]. During the severe acute respiratory syndrome (SARS) outbreak, a study examined the rate of positive healthcare workers (HCWs) who were exposed to patients with SARS before infection control measures were applied [<xref rid="bib31" ref-type="bibr">31</xref>]. Asymptomatic SARS based on serology was 13% compared to severe disease in 82% and 4% of mild symptoms [<xref rid="bib31" ref-type="bibr">31</xref>]. In this article, we systematically review the available literature on the occurrence of asymptomatic MERS-CoV infection and shed light on the possible role of those in the transmission of the virus.</p><sec id="sec1.1"><label>1.1</label><title>Search strategy</title><p id="p0020">We searched MEDLINE and Scopus databases for articles in accordance with the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines (<ext-link ext-link-type="uri" xlink:href="http://www.prismastatement.org/" id="intref0010">http://www.prismastatement.org</ext-link>) [<xref rid="bib32" ref-type="bibr">32</xref>]. We included the following terms:<list list-type="simple" id="ulist0010"><list-item id="u0010"><p id="p0025">#1: “Middle East Respiratory Syndrome Coronavirus” OR “MERS” OR “MERS-CoV” OR “Novel Coronavirus”</p></list-item><list-item id="u0015"><p id="p0030">#2: “Asymptomatic”</p></list-item><list-item id="u0020"><p id="p0035"># 3: “transmission”</p></list-item><list-item id="u0025"><p id="p0040">#4: #1 AND #2 AND #3.</p></list-item></list></p><p id="p0045">Early in the course of the MERS outbreak, the term MERS was not yet coined and the term Novel Coronavirus was used. Thus, we also conducted a focused search to identify any missed relevant publications.</p><p id="p0050">We included articles describing transmission of MERS-CoV in animals and humans from asymptomatic infection.</p></sec></sec><sec id="sec2"><label>2</label><title>Results</title><p id="p0055">Initial screening of retrieved articles excluded articles which were: review articles, and those which did not include specific rates or cases of asymptomatic MERS-CoV infection. A total of 10 papers were retrieved and included in the final analysis and review (<xref rid="fig1" ref-type="fig">Fig. 1</xref>, <xref rid="tbl1" ref-type="table">Table 1</xref>) [<xref rid="bib6" ref-type="bibr">6</xref>,<xref rid="bib33" ref-type="bibr">[33]</xref>, <xref rid="bib34" ref-type="bibr">[34]</xref>, <xref rid="bib35" ref-type="bibr">[35]</xref>, <xref rid="bib36" ref-type="bibr">[36]</xref>, <xref rid="bib37" ref-type="bibr">[37]</xref>, <xref rid="bib38" ref-type="bibr">[38]</xref>, <xref rid="bib39" ref-type="bibr">[39]</xref>, <xref rid="bib40" ref-type="bibr">[40]</xref>, <xref rid="bib41" ref-type="bibr">[41]</xref>]. We included studies in humans describing the incidence of asymptomatic MERS [<xref rid="bib6" ref-type="bibr">6</xref>,<xref rid="bib33" ref-type="bibr">[33]</xref>, <xref rid="bib34" ref-type="bibr">[34]</xref>, <xref rid="bib35" ref-type="bibr">[35]</xref>, <xref rid="bib36" ref-type="bibr">[36]</xref>, <xref rid="bib37" ref-type="bibr">[37]</xref>, <xref rid="bib38" ref-type="bibr">[38]</xref>, <xref rid="bib39" ref-type="bibr">[39]</xref>, <xref rid="bib40" ref-type="bibr">[40]</xref>] and two additional studies in animals [<xref rid="bib42" ref-type="bibr">42</xref>,<xref rid="bib43" ref-type="bibr">43</xref>].<fig id="fig1"><label>Fig. 1</label><caption><p>A flow diagram of the search strategy according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [<xref rid="bib32" ref-type="bibr">32</xref>].</p></caption><alt-text id="alttext0020">Fig. 1</alt-text><graphic xlink:href="gr1_lrg"></graphic></fig><table-wrap position="float" id="tbl1"><label>Table 1</label><caption><p>A summary of studies addressing asymptomatic MERS cases in Humans.</p></caption><alt-text id="alttext0025">Table 1</alt-text><table frame="hsides" rules="groups"><thead><tr><th>Study</th><th>Year</th><th>Setting</th><th>Method of diagnosis</th><th>Total number of confirmed MERS cases</th><th>Proportion of asymptomatic cases among confirmed cases (%)</th><th>Number of confirmed cases among asymptomatic screened contacts</th><th>Reference</th></tr></thead><tbody><tr><td align="left">1</td><td align="left">April 2012 to October 2013</td><td align="left">Laboratory-confirmed and probable MERS-CoV symptomatic cases from 9 countries</td><td align="left">PCR</td><td align="left">144</td><td align="left">18 (12.5%)</td><td align="left">–</td><td align="left">[<xref rid="bib33" ref-type="bibr">33</xref>]</td></tr><tr><td align="left">2</td><td align="left">December 2012 and August 2013</td><td align="left">Asymptomatic Saudi Arabian HCWs contacts (n = 520 screened)</td><td align="left">PCR</td><td align="left">4</td><td align="left">–</td><td align="left">4/520 (0.8%)</td><td align="left">[<xref rid="bib35" ref-type="bibr">35</xref>]</td></tr><tr><td align="left">3</td><td align="left">2015</td><td align="left">Asymptomatic South Korea HCWs contacts (n = 591 screened)</td><td align="left">PCR</td><td align="left">3</td><td align="left">–</td><td align="left">3/591 (0.5%)</td><td align="left">[<xref rid="bib34" ref-type="bibr">34</xref>]</td></tr><tr><td align="left">4</td><td align="left">2015</td><td align="left">South Korea HCWs (n = 574 screened) and non-HCWs contacts (n = 307 screened)</td><td align="left">Serology (ELISA/IFA/PRNT)</td><td align="left">1</td><td align="left">–</td><td align="left">0/574 HCWs 1/307 non-HCWs (0.3%) 1/1610 (0.06%)</td><td align="left">[<xref rid="bib36" ref-type="bibr">36</xref>]</td></tr><tr><td align="left">5</td><td align="left">January 1 through May 16, 2014</td><td align="left">Laboratory-confirmed cases reported to the Saudi Arabian Ministry of Health during the Jeddah Outbreak</td><td align="left">PCR</td><td align="left">255</td><td align="left">64 (25.1%) including 41 HCWs and 23 non-HCWs</td><td></td><td align="left">[<xref rid="bib6" ref-type="bibr">6</xref>]</td></tr><tr><td align="left">6</td><td align="left">June 4, 2013, to November 5, 2013</td><td align="left">Saudi Arabian household contacts (N = 280 screened)</td><td align="left">PCR or serology</td><td align="left">12</td><td align="left">11 (91.7%)</td><td align="left">Not available</td><td align="left">[<xref rid="bib37" ref-type="bibr">37</xref>]</td></tr><tr><td align="left">7</td><td align="left">September 1, 2012, to December 2, 2013</td><td align="left">Laboratory-confirmed pediatric cases reported to the Saudi Arabian Ministry of Health</td><td align="left">PCR</td><td align="left">11</td><td align="left">9 (81.8%)</td><td align="left">–</td><td align="left">[<xref rid="bib38" ref-type="bibr">38</xref>]</td></tr><tr><td align="left">8</td><td align="left">June 2012, to April 19, 2016</td><td align="left">Laboratory-confirmed pediatric cases reported to the Saudi Arabian Ministry of Health</td><td align="left">PCR</td><td align="left">31</td><td align="left">13 (41.9%)</td><td align="left">–</td><td align="left">[<xref rid="bib39" ref-type="bibr">39</xref>]</td></tr><tr><td align="left">9</td><td align="left">April 2014 to November 2016</td><td align="left">Laboratory-confirmed pediatric cases admitted to one Saudi Arabian Hospital</td><td align="left">PCR</td><td align="left">7</td><td align="left">3 (42.8%)</td><td align="left">–</td><td align="left">[<xref rid="bib40" ref-type="bibr">40</xref>]</td></tr><tr><td align="left">10</td><td align="left">June 2017 Outbreak</td><td align="left">Healthcare workers contacts at one hospital in Saudi Arabia</td><td align="left">PCR</td><td align="left">879</td><td align="left">15 (53%)</td><td align="left">–</td><td align="left">[<xref rid="bib41" ref-type="bibr">41</xref>]</td></tr></tbody></table></table-wrap></p><sec id="sec2.1"><label>2.1</label><title>Animal infection</title><p id="p0060">In a rabbit model of MERS-CoV infection, MERS-CoV was detected in the lungs without significant histopathological changes and no symptoms [<xref rid="bib42" ref-type="bibr">42</xref>]. In an evaluation of contacts of a positive dromedary camel, 2 (5.8%) of 34 dromedary contacts tested positive and were asymptomatic [<xref rid="bib43" ref-type="bibr">43</xref>].</p></sec><sec id="sec2.2"><label>2.2</label><title>Extent of asymptomatic MERS in humans</title><p id="p0065">The proportion of asymptomatic MERS probably remained unchanged, or even declined with implementation of personal protection measures; asymptomatic case identification increased by change in testing recommendations. This change had also resulted in the reduction of case-fatality rate from 65% mainly in severe cases to 44.5% in mixed population [<xref rid="bib44" ref-type="bibr">44</xref>]. This reduction was partially related to an increase in the rate of asymptomatic individuals from 0% to 28.6% in early reports [<xref rid="bib44" ref-type="bibr">44</xref>]. A summary of studies addressing asymptomatic MERS cases in Humans is shown in <xref rid="tbl1" ref-type="table">Table 1</xref>. In early cases from April 2012 to October 2013, there were 144 laboratory-confirmed MERS-CoV cases including 18 (12.5%) asymptomatic individuals [<xref rid="bib33" ref-type="bibr">33</xref>]. In one study from Saudi Arabia, 4 (0.8%) of 520 asymptomatic HCWs screened were positive [<xref rid="bib35" ref-type="bibr">35</xref>]. In South Korea, 3 (0.5%) of 591 asymptomatic HCWs were detected positive via PCR screening [<xref rid="bib34" ref-type="bibr">34</xref>]. In a recent study from Saudi Arabia, 17 out of 879 HCWs tested positive for MERS-CoV and 53% of them were asymptomatic by PCR [<xref rid="bib41" ref-type="bibr">41</xref>].</p><p id="p0070">In a seroepidemiologic survey conducted in South Korea, of 1610 asymptomatic HCWs and non-HCWs contacts only 1 non-HCW (0.06%) tested positive [<xref rid="bib36" ref-type="bibr">36</xref>]. Asymptomatic persons were identified in the Jeddah outbreak. There were 64 (25%) asymptomatic of 255 individual tested including 41 HCWs and 23 non-HCWs [<xref rid="bib6" ref-type="bibr">6</xref>]. In a total of 280 household contacts, 12 individuals were identified by PCR or serology of whom 11 (3.9%) were asymptomatic [<xref rid="bib37" ref-type="bibr">37</xref>]. Asymptomatic individuals were less likely to have underlying condition (42%) compared to 86% of fatal cases [<xref rid="bib45" ref-type="bibr">45</xref>]. However, serologic evaluation of contacts and patients may underestimate the extent of the disease as antibodies wane over time and is related to disease severity [<xref rid="bib46" ref-type="bibr">46</xref>]. Of particular interest is that most of the identified pediatric cases were asymptomatic with no clear explanation [<xref rid="bib38" ref-type="bibr">[38]</xref>, <xref rid="bib39" ref-type="bibr">[39]</xref>, <xref rid="bib40" ref-type="bibr">[40]</xref>,<xref rid="bib47" ref-type="bibr">47</xref>].</p><p id="p0075">Overall, the detection rate of MERS cases among asymptomatic contacts when screened was less than 1% in the available studies included in this review (<xref rid="tbl1" ref-type="table">Table 1</xref>). The proportion of asymptomatic cases among all confirmed cases, widely differed in the available reports. The differences between the study setting and the populations studied did not allow any reliable comparison. According to the last WHO update 21% of the 2228 cases confirmed MERS-CoV cases were reported to have no or mild symptoms while 46% had severe disease or died [<xref rid="bib48" ref-type="bibr">48</xref>].</p></sec><sec id="sec2.3"><label>2.3</label><title>Asymptomatic travelers</title><p id="p0080">Imported MERS-CoV cases were treated in healthcare settings. More than 20 travel-related MERS-CoV had occurred as summarized previously [<xref rid="bib28" ref-type="bibr">28</xref>]. However, there were no reported asymptomatic cases. Travel related MERS-CoV occurred infrequently among pilgrims performing Umrah [<xref rid="bib28" ref-type="bibr">28</xref>,<xref rid="bib49" ref-type="bibr">49</xref>].</p></sec></sec><sec id="sec3"><label>3</label><title>Discussion</title><sec id="sec3.1"><label>3.1</label><title>Role of asymptomatic individuals in MERS-CoV infection</title><p id="p0085">The role of asymptomatic individuals was evaluated in a family cluster [<xref rid="bib50" ref-type="bibr">50</xref>]. The index case in that study was thought to have acquired MERS infection from an unrecognized mild or asymptomatic case [<xref rid="bib50" ref-type="bibr">50</xref>]. However, the link was not established in this case. One study suggested the possible transmission of MERS from an asymptomatic individual. The index case of a family cluster acquired infection 14 days after hospitalization suggesting that the infection occurred from an asymptomatic person [<xref rid="bib50" ref-type="bibr">50</xref>]. This is based on an incubation period of 7–10 days. In the South Korea outbreak, 82 contacts of an asymptomatic or mild MERS-CoV infection were tested by RT-PCR and serology and all of them were negative [<xref rid="bib51" ref-type="bibr">51</xref>]. In a study from Abu Dhabi, of 34 case-patients, 91% were asymptomatic with no evidence of transmission [<xref rid="bib52" ref-type="bibr">52</xref>]. In another study, most of the cases were either asymptomatic or mildly symptomatic [<xref rid="bib53" ref-type="bibr">53</xref>]. MERS-CoV was cultured from a patient with mild respiratory symptoms confirming the ability of such patients to transmit MERS-CoV [<xref rid="bib54" ref-type="bibr">54</xref>].</p><p id="p0090">The role of asymptomatic travelers in the potential transmission of the infection to household contacts is a concern. However, so far no such event had been reported. The risk of MERS-CoV infection seems to be low in travelers [<xref rid="bib49" ref-type="bibr">49</xref>], and there were multiple cases described in travelers [<xref rid="bib28" ref-type="bibr">28</xref>]. The risk of MERS-CoV was evaluated in a mathematical study and the model included all Middle East countries with reported locally acquired cases, and 41% of the travel-imported cases outside the Middle East were in the top ten countries [<xref rid="bib55" ref-type="bibr">55</xref>]. Although, India was the most at-risk country, there had been no reported cases from this country.</p><p id="p0095">The initial 2012 Hajj season started few weeks after the first case of MERS-CoV infection was reported [<xref rid="bib56" ref-type="bibr">56</xref>]. However, there were no reported cases among pilgrims in 2012 [<xref rid="bib57" ref-type="bibr">[57]</xref>, <xref rid="bib58" ref-type="bibr">[58]</xref>, <xref rid="bib59" ref-type="bibr">[59]</xref>, <xref rid="bib60" ref-type="bibr">[60]</xref>]. Thus, the Saudi Ministry of Health utilized the MERS-CoV case definition for monitoring any occurrence of the disease during Hajj for early detection of cases among pilgrims [<xref rid="bib61" ref-type="bibr">61</xref>]. An enhanced surveillance system was established for the detection of MERS-CoV cases. The disease remains limited to the Middle East with the exception of sporadic travel associated infections and the large outbreak in South Korea [<xref rid="bib22" ref-type="bibr">22</xref>,<xref rid="bib28" ref-type="bibr">28</xref>,<xref rid="bib62" ref-type="bibr">62</xref>,<xref rid="bib63" ref-type="bibr">63</xref>]. In one study conducted September 2012–October 2013, 77 travelers from the Middle East met the possible case definition for MERS and two of them tested positive for MERS [<xref rid="bib28" ref-type="bibr">28</xref>]. In a small study of 14 retuning Pilgrims, all patients were hospitalized for respiratory symptoms and none of them tested positive for MERS-CoV in Marseille France in October 2013 [<xref rid="bib64" ref-type="bibr">64</xref>]. Furthermore, nasopharyngeal swabs were collected from suspected cases and all samples tested negative for MERS-COV [<xref rid="bib56" ref-type="bibr">56</xref>]. Another small study of 7 Pilgrims in 2014 in Austria, none had MERS-CoV [<xref rid="bib65" ref-type="bibr">65</xref>].</p><p id="p0100">Mathematical models estimated the risk of MERS-CoV among pilgrims to be 1–7 cases per Hajj, and 3–10 per Umrah per year [<xref rid="bib66" ref-type="bibr">66</xref>]. It was estimated that 6.2 pilgrims may develop MERS-CoV symptoms during the Hajj, and 4 pilgrims may become infected and return home before symptoms development [<xref rid="bib67" ref-type="bibr">67</xref>]. However, systematic screening of pilgrims for MERS-CoV showed no positive cases [<xref rid="bib59" ref-type="bibr">59</xref>,<xref rid="bib65" ref-type="bibr">65</xref>,<xref rid="bib68" ref-type="bibr">[68]</xref>, <xref rid="bib69" ref-type="bibr">[69]</xref>, <xref rid="bib70" ref-type="bibr">[70]</xref>, <xref rid="bib71" ref-type="bibr">[71]</xref>, <xref rid="bib72" ref-type="bibr">[72]</xref>, <xref rid="bib73" ref-type="bibr">[73]</xref>, <xref rid="bib74" ref-type="bibr">[74]</xref>, <xref rid="bib75" ref-type="bibr">[75]</xref>, <xref rid="bib76" ref-type="bibr">[76]</xref>, <xref rid="bib77" ref-type="bibr">[77]</xref>, <xref rid="bib78" ref-type="bibr">[78]</xref>, <xref rid="bib79" ref-type="bibr">[79]</xref>, <xref rid="bib80" ref-type="bibr">[80]</xref>, <xref rid="bib81" ref-type="bibr">[81]</xref>]. Systematic surveillance of returning Pilgrims was done in several studies in Egypt, Iran, France, Ghana, Iran and Saudi Arabia [<xref rid="bib64" ref-type="bibr">64</xref>,<xref rid="bib68" ref-type="bibr">68</xref>,<xref rid="bib71" ref-type="bibr">71</xref>,<xref rid="bib72" ref-type="bibr">72</xref>]. Few studies examined MERS-CoV among symptomatic pilgrims and none was positive for MERS-CoV) [<xref rid="bib56" ref-type="bibr">56</xref>,<xref rid="bib59" ref-type="bibr">59</xref>,<xref rid="bib65" ref-type="bibr">65</xref>,<xref rid="bib81" ref-type="bibr">81</xref>]. There had been an extensive surveillance of MERS-CoV among pilgrims and only 4 cases have been linked to Umrah (Mini-Hajj) [<xref rid="bib82" ref-type="bibr">[82]</xref>, <xref rid="bib83" ref-type="bibr">[83]</xref>, <xref rid="bib84" ref-type="bibr">[84]</xref>, <xref rid="bib85" ref-type="bibr">[85]</xref>, <xref rid="bib86" ref-type="bibr">[86]</xref>].</p></sec><sec id="sec3.2"><label>3.2</label><title>Infection control implications</title><p id="p0105">The occurrence of asymptomatic infection of MERS and the possibility of transmission to other individuals is of particular importance for healthcare settings and for travelers. These RT-PCR positive persons with mild or no symptoms are usually identified when conducting laboratory screening tests as part of active case monitoring or contact investigations. Asymptomatic health care workers may contribute to healthcare associated transmission and asymptomatic travelers may potentially transmit the infection to household contacts. The WHO recommends the isolation of asymptomatic PCR-positive individuals and daily follow up for the occurrence of symptoms. Those individuals should be tested at least weekly and HCWs should not return to work until two consecutive upper respiratory tract samples are RT-PCR negative [<xref rid="bib87" ref-type="bibr">87</xref>]. In a study of severe cases and those with mild disease, the latter group cleared MERS-CoV at an earlier time than patients with severe disease whereby on day 12, 30% of mild cases and 76% of severe cases were positive for MERS-CoV by PCR [<xref rid="bib88" ref-type="bibr">88</xref>]. Another study reported prolonged nasal virus RNA detection (more than 5 weeks) from one asymptomatic RT-PCR positive health-care worker [<xref rid="bib89" ref-type="bibr">89</xref>].</p><p id="p0110">In conclusion, the proportion of asymptomatic MERS cases were detected with increasing frequency as the disease progressed overtime. 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