A Review of Asymptomatic and Subclinical Middle East Respiratory Syndrome Coronavirus Infections
Identifieur interne : 001319 ( Pmc/Corpus ); précédent : 001318; suivant : 001320A Review of Asymptomatic and Subclinical Middle East Respiratory Syndrome Coronavirus Infections
Auteurs : Rebecca Grant ; Mamunur Rahman Malik ; Amgad Elkholy ; Maria D. Van KerkhoveSource :
- Epidemiologic Reviews [ 0193-936X ] ; 2019.
Abstract
The epidemiology of Middle East respiratory syndrome coronavirus (MERS-CoV) since 2012 has been largely characterized by recurrent zoonotic spillover from dromedary camels followed by limited human-to-human transmission, predominantly in health-care settings. The full extent of infection of MERS-CoV is not clear, nor is the extent and/or role of asymptomatic infections in transmission. We conducted a review of molecular and serological investigations through PubMed and EMBASE from September 2012 to November 15, 2018, to measure subclinical or asymptomatic MERS-CoV infection within and outside of health-care settings. We performed retrospective analysis of laboratory-confirmed MERS-CoV infections reported to the World Health Organization to November 27, 2018, to summarize what is known about asymptomatic infections identified through national surveillance systems. We identified 23 studies reporting evidence of MERS-CoV infection outside of health-care settings, mainly of camel workers, with seroprevalence ranges of 0%–67% depending on the study location. We identified 20 studies in health-care settings of health-care worker (HCW) and family contacts, of which 11 documented molecular evidence of MERS-CoV infection among asymptomatic contacts. Since 2012, 298 laboratory-confirmed cases were reported as asymptomatic to the World Health Organization, 164 of whom were HCWs. The potential to transmit MERS-CoV to others has been demonstrated in viral-shedding studies of asymptomatic MERS infections. Our results highlight the possibility for onward transmission of MERS-CoV from asymptomatic individuals. Screening of HCW contacts of patients with confirmed MERS-CoV is currently recommended, but systematic screening of non-HCW contacts outside of health-care facilities should be encouraged.
Url:
DOI: 10.1093/epirev/mxz009
PubMed: 31781765
PubMed Central: 7108493
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">A Review of Asymptomatic and Subclinical Middle East Respiratory Syndrome Coronavirus Infections</title><author><name sortKey="Grant, Rebecca" sort="Grant, Rebecca" uniqKey="Grant R" first="Rebecca" last="Grant">Rebecca Grant</name><affiliation><nlm:aff id="aff1">Department of Infectious Hazard Management, WHO Health Emergencies Programme,<institution>World Health Organization</institution>, Geneva,<country country="CH">Switzerland</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Centre for Global Health,<institution>Institut Pasteur</institution>, Paris,<country country="FR">France</country></nlm:aff></affiliation></author><author><name sortKey="Malik, Mamunur Rahman" sort="Malik, Mamunur Rahman" uniqKey="Malik M" first="Mamunur Rahman" last="Malik">Mamunur Rahman Malik</name><affiliation><nlm:aff id="aff2">Infectious Hazard Management Unit, Department of Health Emergencies,<institution>World Health Organization Regional Office for the Eastern Mediterranean</institution>, Cairo,<country country="EG">Egypt</country></nlm:aff></affiliation></author><author><name sortKey="Elkholy, Amgad" sort="Elkholy, Amgad" uniqKey="Elkholy A" first="Amgad" last="Elkholy">Amgad Elkholy</name><affiliation><nlm:aff id="aff2">Infectious Hazard Management Unit, Department of Health Emergencies,<institution>World Health Organization Regional Office for the Eastern Mediterranean</institution>, Cairo,<country country="EG">Egypt</country></nlm:aff></affiliation></author><author><name sortKey="Van Kerkhove, Maria D" sort="Van Kerkhove, Maria D" uniqKey="Van Kerkhove M" first="Maria D" last="Van Kerkhove">Maria D. Van Kerkhove</name><affiliation><nlm:aff id="aff1">Department of Infectious Hazard Management, WHO Health Emergencies Programme,<institution>World Health Organization</institution>, Geneva,<country country="CH">Switzerland</country></nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">31781765</idno><idno type="pmc">7108493</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7108493</idno><idno type="RBID">PMC:7108493</idno><idno type="doi">10.1093/epirev/mxz009</idno><date when="2019">2019</date><idno type="wicri:Area/Pmc/Corpus">001319</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">001319</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">A Review of Asymptomatic and Subclinical Middle East Respiratory Syndrome Coronavirus Infections</title><author><name sortKey="Grant, Rebecca" sort="Grant, Rebecca" uniqKey="Grant R" first="Rebecca" last="Grant">Rebecca Grant</name><affiliation><nlm:aff id="aff1">Department of Infectious Hazard Management, WHO Health Emergencies Programme,<institution>World Health Organization</institution>, Geneva,<country country="CH">Switzerland</country></nlm:aff></affiliation><affiliation><nlm:aff id="aff3">Centre for Global Health,<institution>Institut Pasteur</institution>, Paris,<country country="FR">France</country></nlm:aff></affiliation></author><author><name sortKey="Malik, Mamunur Rahman" sort="Malik, Mamunur Rahman" uniqKey="Malik M" first="Mamunur Rahman" last="Malik">Mamunur Rahman Malik</name><affiliation><nlm:aff id="aff2">Infectious Hazard Management Unit, Department of Health Emergencies,<institution>World Health Organization Regional Office for the Eastern Mediterranean</institution>, Cairo,<country country="EG">Egypt</country></nlm:aff></affiliation></author><author><name sortKey="Elkholy, Amgad" sort="Elkholy, Amgad" uniqKey="Elkholy A" first="Amgad" last="Elkholy">Amgad Elkholy</name><affiliation><nlm:aff id="aff2">Infectious Hazard Management Unit, Department of Health Emergencies,<institution>World Health Organization Regional Office for the Eastern Mediterranean</institution>, Cairo,<country country="EG">Egypt</country></nlm:aff></affiliation></author><author><name sortKey="Van Kerkhove, Maria D" sort="Van Kerkhove, Maria D" uniqKey="Van Kerkhove M" first="Maria D" last="Van Kerkhove">Maria D. Van Kerkhove</name><affiliation><nlm:aff id="aff1">Department of Infectious Hazard Management, WHO Health Emergencies Programme,<institution>World Health Organization</institution>, Geneva,<country country="CH">Switzerland</country></nlm:aff></affiliation></author></analytic><series><title level="j">Epidemiologic Reviews</title><idno type="ISSN">0193-936X</idno><idno type="eISSN">1478-6729</idno><imprint><date when="2019">2019</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Abstract</title><p>The epidemiology of Middle East respiratory syndrome coronavirus (MERS-CoV) since 2012 has been largely characterized by recurrent zoonotic spillover from dromedary camels followed by limited human-to-human transmission, predominantly in health-care settings. The full extent of infection of MERS-CoV is not clear, nor is the extent and/or role of asymptomatic infections in transmission. We conducted a review of molecular and serological investigations through PubMed and EMBASE from September 2012 to November 15, 2018, to measure subclinical or asymptomatic MERS-CoV infection within and outside of health-care settings. We performed retrospective analysis of laboratory-confirmed MERS-CoV infections reported to the World Health Organization to November 27, 2018, to summarize what is known about asymptomatic infections identified through national surveillance systems. We identified 23 studies reporting evidence of MERS-CoV infection outside of health-care settings, mainly of camel workers, with seroprevalence ranges of 0%–67% depending on the study location. We identified 20 studies in health-care settings of health-care worker (HCW) and family contacts, of which 11 documented molecular evidence of MERS-CoV infection among asymptomatic contacts. Since 2012, 298 laboratory-confirmed cases were reported as asymptomatic to the World Health Organization, 164 of whom were HCWs. The potential to transmit MERS-CoV to others has been demonstrated in viral-shedding studies of asymptomatic MERS infections. Our results highlight the possibility for onward transmission of MERS-CoV from asymptomatic individuals. Screening of HCW contacts of patients with confirmed MERS-CoV is currently recommended, but systematic screening of non-HCW contacts outside of health-care facilities should be encouraged.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Zaki, Am" uniqKey="Zaki A">AM Zaki</name></author><author><name sortKey="Van Boheemen, S" uniqKey="Van Boheemen S">S van Boheemen</name></author><author><name sortKey="Bestebroer, Tm" uniqKey="Bestebroer T">TM Bestebroer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Hijawi, B" uniqKey="Hijawi B">B Hijawi</name></author><author><name sortKey="Abdallat, M" uniqKey="Abdallat M">M Abdallat</name></author><author><name sortKey="Sayaydeh, A" uniqKey="Sayaydeh A">A Sayaydeh</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Assiri, A" uniqKey="Assiri A">A Assiri</name></author><author><name sortKey="Mcgeer, A" 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Epidemiol Rev</journal-id><journal-id journal-id-type="iso-abbrev">Epidemiol Rev</journal-id><journal-id journal-id-type="publisher-id">epirev</journal-id><journal-title-group><journal-title>Epidemiologic Reviews</journal-title></journal-title-group><issn pub-type="ppub">0193-936X</issn><issn pub-type="epub">1478-6729</issn><publisher><publisher-name>Oxford University Press</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">31781765</article-id><article-id pub-id-type="pmc">7108493</article-id><article-id pub-id-type="doi">10.1093/epirev/mxz009</article-id><article-id pub-id-type="publisher-id">mxz009</article-id><article-categories><subj-group subj-group-type="heading"><subject>Review</subject></subj-group></article-categories><title-group><article-title>A Review of Asymptomatic and Subclinical Middle East Respiratory Syndrome Coronavirus Infections</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Grant</surname><given-names>Rebecca</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref ref-type="aff" rid="aff3">3</xref></contrib><contrib contrib-type="author"><name><surname>Malik</surname><given-names>Mamunur Rahman</given-names></name><xref ref-type="aff" rid="aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Elkholy</surname><given-names>Amgad</given-names></name><xref ref-type="aff" rid="aff2">2</xref></contrib><contrib contrib-type="author"><name><surname>Van Kerkhove</surname><given-names>Maria D</given-names></name><xref ref-type="aff" rid="aff1">1</xref><xref rid="cor1" ref-type="corresp"></xref><pmc-comment>vankerkhovem@who.int </pmc-comment>
</contrib></contrib-group><aff id="aff1"><label>1</label>Department of Infectious Hazard Management, WHO Health Emergencies Programme,<institution>World Health Organization</institution>, Geneva,<country country="CH">Switzerland</country></aff><aff id="aff2"><label>2</label>Infectious Hazard Management Unit, Department of Health Emergencies,<institution>World Health Organization Regional Office for the Eastern Mediterranean</institution>, Cairo,<country country="EG">Egypt</country></aff><aff id="aff3"><label>3</label>Centre for Global Health,<institution>Institut Pasteur</institution>, Paris,<country country="FR">France</country></aff><author-notes><corresp id="cor1">Correspondence to Maria D Van Kerkhove, PhD, Department of Infectious Hazards Management, Health Emergencies Program, World Health Organization, Avenue Appia 20, 1211 Geneva, Switzerland (e-mail: <email>vankerkhovem@who.int</email>)</corresp></author-notes><pub-date pub-type="epub" iso-8601-date="2019-11-29"><day>29</day><month>11</month><year>2019</year></pub-date><pub-date pub-type="pmc-release"><day>29</day><month>11</month><year>2019</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<elocation-id>mxz009</elocation-id><history><date date-type="received"><day>6</day><month>12</month><year>2018</year></date><date date-type="rev-recd"><day>2</day><month>4</month><year>2019</year></date><date date-type="accepted"><day>9</day><month>9</month><year>2019</year></date></history><permissions><copyright-statement>© The Author(s) 2019. Published by Oxford University Press on behalf of the Johns Hopkins Bloomberg School of Public Health.</copyright-statement><copyright-year>2019</copyright-year><license license-type="cc-by-nc" xlink:href="http://creativecommons.org/licenses/by-nc/4.0/"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc/4.0/">http://creativecommons.org/licenses/by-nc/4.0/</ext-link>), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com</license-p></license></permissions><self-uri xlink:href="mxz009.pdf"></self-uri><abstract><title>Abstract</title><p>The epidemiology of Middle East respiratory syndrome coronavirus (MERS-CoV) since 2012 has been largely characterized by recurrent zoonotic spillover from dromedary camels followed by limited human-to-human transmission, predominantly in health-care settings. The full extent of infection of MERS-CoV is not clear, nor is the extent and/or role of asymptomatic infections in transmission. We conducted a review of molecular and serological investigations through PubMed and EMBASE from September 2012 to November 15, 2018, to measure subclinical or asymptomatic MERS-CoV infection within and outside of health-care settings. We performed retrospective analysis of laboratory-confirmed MERS-CoV infections reported to the World Health Organization to November 27, 2018, to summarize what is known about asymptomatic infections identified through national surveillance systems. We identified 23 studies reporting evidence of MERS-CoV infection outside of health-care settings, mainly of camel workers, with seroprevalence ranges of 0%–67% depending on the study location. We identified 20 studies in health-care settings of health-care worker (HCW) and family contacts, of which 11 documented molecular evidence of MERS-CoV infection among asymptomatic contacts. Since 2012, 298 laboratory-confirmed cases were reported as asymptomatic to the World Health Organization, 164 of whom were HCWs. The potential to transmit MERS-CoV to others has been demonstrated in viral-shedding studies of asymptomatic MERS infections. Our results highlight the possibility for onward transmission of MERS-CoV from asymptomatic individuals. Screening of HCW contacts of patients with confirmed MERS-CoV is currently recommended, but systematic screening of non-HCW contacts outside of health-care facilities should be encouraged.</p></abstract><kwd-group><kwd>health-care workers</kwd><kwd>infection control</kwd><kwd>MERS-CoV</kwd><kwd>seroprevalence</kwd><kwd>subclinical infections</kwd></kwd-group><counts><page-count count="13"></page-count></counts><custom-meta-group><custom-meta><meta-name>edited-state</meta-name><meta-value>corrected-proof</meta-value></custom-meta><custom-meta><meta-name>article-lifecycle</meta-name><meta-value>PAP</meta-value></custom-meta></custom-meta-group></article-meta></front><body><sec id="sec1a"><title>Abbreviations</title><def-list list-content="abbreviations"><def-item><term id="term1-doi">HCW</term><def><p>health-care worker</p></def></def-item><def-item><term id="term2-doi">MERS-CoV</term><def><p>Middle East respiratory syndrome coronavirus</p></def></def-item><def-item><term id="term3-doi">PCR</term><def><p>polymerase chain reaction</p></def></def-item><def-item><term id="term4-doi">WHO</term><def><p>World Health Organization</p></def></def-item></def-list></sec><sec id="sec1"><title>INTRODUCTION</title><p>Since 2012, the epidemiology of cases of Middle East respiratory syndrome coronavirus (MERS-CoV) infection reported to the World Health Organization (WHO) has been characterized largely by recurrent zoonotic spillover from the known animal reservoir—dromedary camels—and human-to-human transmission in health-care settings (<xref rid="ref1" ref-type="bibr">1</xref>). Outbreaks in health-care settings on occasion have resulted in large outbreaks (<xref rid="ref2" ref-type="bibr">2–9</xref>). Of the 2,260 cases (including 803 deaths) reported to WHO, 83% of cases have been reported in the Kingdom of Saudi Arabia (<xref rid="ref10" ref-type="bibr">10</xref>).</p><p>The clinical presentation of MERS-CoV infection ranges from asymptomatic to severe respiratory illness, with approximately 35.5% of cases resulting in death (<xref rid="ref1" ref-type="bibr">1</xref>). The role of asymptomatic or subclinical infections in human-to-human transmission of MERS-CoV is not well understood, but there is evidence that laboratory-confirmed MERS-CoV infection in patients who are reported as asymptomatic may be transmitted to other individuals (<xref rid="ref11" ref-type="bibr">11</xref>).</p><p>For many novel infectious pathogens, surveillance initially focuses on individuals with disease who seek care at health-care facilities, which undoubtedly underestimates the true prevalence of infection, because it will not account for mild or asymptomatic infections not requiring medical care. Detailed outbreak investigations often include laboratory testing of close contacts and of health-care workers (HCWs), regardless of symptoms, and specialized serological investigations will include individuals thought to be at higher risk of infection, such as HCWs or those with occupational exposure to animal reservoirs. Estimates of the true prevalence of infection of high-risk pathogens are important to understand the populations required for vaccine candidates or specific therapeutic treatments as and when they become available. In addition, the role of subclinical or asymptomatic infection is critical in understanding chains of transmission missed by surveillance systems. For MERS-CoV, asymptomatic infection has been reported to WHO, but the possibility of transmission prior to symptom onset is critical for recommending effective infection prevention and control measures and for reducing secondary MERS-CoV transmission.</p><p>The role of asymptomatic infections in transmission of other respiratory viruses has been investigated previously. Highly pathogenic avian influenza H5N1 RNA, for example, has been detected by polymerase chain reaction (PCR) from asymptomatic family contacts of ill patients, suggesting the possibility for onward transmission, even in the absence of symptoms (<xref rid="ref12" ref-type="bibr">12–15</xref>). For severe acute respiratory syndrome CoV, limited transmission to close contacts before symptom onset or hospitalization has been found in transmission-risk studies outside health-care settings, whereas human-to-human transmission within health-care settings was higher, likely due to higher viral load in hospitalized patients and more frequent exposure to the virus among HCWs (<xref rid="ref16" ref-type="bibr">16–18</xref>).</p><p>Here, we have reviewed available evidence of the extent of subclinical and asymptomatic infection of MERS-CoV stratified by evaluating studies in which infection within and outside of health-care settings has been measured, and the potential role of onward human-to-human transmission from asymptomatic cases.</p></sec><sec id="sec1ab"><title>METHODS</title><p>We conducted a literature search in PubMed and EMBASE databases for observational epidemiologic studies of laboratory-confirmed MERS-CoV infection using the following search terms: “MERS-CoV” or “MERS” AND “seroprevalence” or “prevalence” or ”serological” or “infection” or “asymptomatic.” Additional studies were identified through consultation with the WHO MERS technical network and in the bibliography of a related recently published review (<xref rid="ref19" ref-type="bibr">19</xref>). Publications in English dated before November 15, 2019, were considered, with no additional restrictions on year of publication. We assessed the titles and abstracts of identified studies to determine their eligibility for inclusion in the study. We stratified our analyses to evaluate subclinical and/or asymptomatic infection identified inside and outside health-care facilities. For descriptive analysis of WHO case-based data, we used the ggplot2 in R, version 3.4.2.0 (R Foundation for Statistical Computing, Vienna, Austria.).</p><p>For MERS-CoV infections studied outside health-care settings, we included studies in which evidence of MERS-CoV infection was reported, using molecular and/or serological methods in either individuals with occupational exposure to dromedary camels; familial, occupational, or social contacts of patients with confirmed MERS outside of health-care settings; the general population; or through national MERS surveillance records, when published. Eligible studies included reporting of the number of individuals tested and the number with molecular or serological evidence of MERS-CoV infection.</p><p>To evaluate MERS-CoV infections studied within health-care settings, we included studies in which the authors reported evidence of MERS-CoV infection, using molecular and/or serological methods among HCW and among non-HCW contacts (e.g., family contacts) of confirmed MERS cases treated in health care settings.</p><p>For each eligible study, we extracted information on the year of publication, the year biological samples were collected, the country in which the study was conducted, the number of individuals tested, characteristics of the individuals tested, and the total number of confirmed MERS-CoV infections by molecular or serological assay. Asymptomatic MERS-CoV infection was considered a laboratory-confirmed infection with no reported symptoms at the time of sampling.</p><p>In addition, we evaluated the symptomatic profile and place of reporting among laboratory-confirmed MERS-CoV infections reported to WHO from September 2012 to November 27, 2018. Within WHO databases, cases are classified as primary cases if they were reported as such by the reporting Member State; if direct or indirect contact with dromedary camels or dromedary products was reported in the case; and/or the exposures were under investigation without known contact with a patient with probable or confirmed MERS. Cases were classified as secondary cases due to human-to-human transmission if the patient reported recent direct contact with a patient known to have MERS-CoV infection and/or were identified as a household, occupational, or HCW contact of a patient known to have MERS-CoV infection.</p><fig id="f1" orientation="portrait" position="float"><label>Figure 1</label><caption><p> Flow diagram of selection of articles for the review of symptomatic and subclinical Middle East respiratory syndrome coronavirus (MERS-CoV) infections. Additional records identified through consultation with the World Health Organization MERS technical network and in the bibliography of a related review (<xref rid="ref19" ref-type="bibr">19</xref>).</p></caption><graphic xlink:href="mxz009f1"></graphic></fig></sec><sec id="sec2"><title>RESULTS</title><p>In total, we identified 43 studies in which MERS-CoV infections measured by serology and/or molecular testing were reported; 23 focused on individuals with exposures outside of health-care settings (<xref rid="ref4" ref-type="bibr">4</xref>, <xref rid="ref7" ref-type="bibr">7</xref>, <xref rid="ref11" ref-type="bibr">11</xref>, <xref rid="ref20" ref-type="bibr">20–39</xref>), and 20 focused on individuals with exposures inside health-care facilities (<xref rid="ref5" ref-type="bibr">5</xref>, <xref rid="ref7" ref-type="bibr">7</xref>, <xref rid="ref29" ref-type="bibr">29</xref>, <xref rid="ref32" ref-type="bibr">32</xref>, <xref rid="ref40" ref-type="bibr">40–54</xref>). The selection of identified and included studies is shown in <xref rid="f1" ref-type="fig">Figure 1</xref>.</p><p>The 23 studies in which MERS-CoV infections were measured by serology and/or molecular testing outside of health-care settings are described in <xref rid="TB1" ref-type="table">Table 1</xref>. The majority of studies focused on measuring seroprevalence of MERS-CoV in individuals with occupational exposure to dromedaries in the Middle East and Africa (<xref rid="ref20" ref-type="bibr">20–28</xref>).</p><p>In the largest seroprevalence study conducted to date, 0.1% seroprevalence was calculated among general population samples collected in 2012–2013, 2% seroprevalence among shepherds of dromedaries, and 4% seroprevalence among slaughterhouse workers (<xref rid="ref37" ref-type="bibr">37</xref>). Additional estimates of seroprevalence among occupational high-risk populations ranged from 0% to 67%, with seropositivity being detected in Kingdom of Saudi Arabia, Qatar, and Kenya, and from 0% to 54% among contacts of patients with confirmed MERS in household settings largely in countries of the Middle East. Within these studies, the majority of infections detected by serology appeared to be asymptomatic. Within these studies, a high proportion of seropositive camel workers reported no symptoms (80%–100% among seropositive individuals).</p><p>The 20 studies in which MERS-CoV infections were measured by serology and/or molecular testing within health-care settings are listed in <xref rid="TB2" ref-type="table">Table 2</xref> and include studies of HCWs and close contacts of patients with confirmed infection. The largest molecular and serological studies among HCWs were conducted among 1,695 and 1,169 HCWs in Kingdom of Saudi Arabia (<xref rid="ref32" ref-type="bibr">32</xref>) and the Republic of Korea (<xref rid="ref40" ref-type="bibr">40</xref>), respectively; the authors reported evidence of infection of 1% and 1.5%, respectively. Infection was more frequent among HCWs who did not use personal protective equipment when in contact with a patient with MERS (<xref rid="ref40" ref-type="bibr">40</xref>).</p><table-wrap id="TB1" orientation="portrait" position="float"><label>Table 1</label><caption><p>Evidence of Middle East Respiratory Syndrome Coronavirus Infection Outside Health-Care Settings, 2012–2018</p></caption><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col></colgroup><thead><tr><th align="center" rowspan="1" colspan="1"><bold>First Author, Year (Reference No.)</bold></th><th align="center" rowspan="1" colspan="1"><bold>Years of Study</bold></th><th align="center" rowspan="1" colspan="1"><bold>Location of Study</bold></th><th align="center" rowspan="1" colspan="1"><bold>No. of Subjects</bold></th><th align="center" rowspan="1" colspan="1"><bold>Description of Subjects</bold></th><th align="center" rowspan="1" colspan="1"><bold>Laboratory Results</bold></th><th align="center" rowspan="1" colspan="1"><bold>Evidence of Asymptomatic MERS-CoV Infection Among PCR/Serologically Positive Subjects</bold></th></tr></thead><tbody><tr><td align="center" colspan="7" rowspan="1"><italic>Occupational Exposure to Dromedaries</italic></td></tr><tr><td align="left" rowspan="1" colspan="1">Aburizaiza, 2014 (<xref rid="ref20" ref-type="bibr">20</xref>)</td><td align="left" rowspan="1" colspan="1">2012</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="center" rowspan="1" colspan="1">226</td><td align="left" rowspan="1" colspan="1">Slaughterhouse workers</td><td align="left" rowspan="1" colspan="1">0 (0%) had specific antibodies against MERS-CoV (immunofluorescence assay and neutralization)</td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Chu, 2014 (<xref rid="ref21" ref-type="bibr">21</xref>)</td><td align="left" rowspan="1" colspan="1">2013</td><td align="left" rowspan="1" colspan="1">Egypt</td><td align="center" rowspan="1" colspan="1">179</td><td align="left" rowspan="1" colspan="1">Camel abattoir workers</td><td align="left" rowspan="1" colspan="1">0 (0%) had serological evidence of MERS-CoV infection</td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Hemida, 2015 (<xref rid="ref22" ref-type="bibr">22</xref>)</td><td align="left" rowspan="1" colspan="1">2013–2014</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="center" rowspan="1" colspan="1">191</td><td align="left" rowspan="1" colspan="1">Occupational exposure to dromedary camels</td><td align="left" rowspan="1" colspan="1">0 (0%) had specific antibodies against MERS-CoV (ppNT)</td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Memish, 2015 (<xref rid="ref23" ref-type="bibr">23</xref>)</td><td align="left" rowspan="1" colspan="1">2012</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="center" rowspan="1" colspan="1">75</td><td align="left" rowspan="1" colspan="1">Direct contact with domestic animals, including camels</td><td align="left" rowspan="1" colspan="1">0 (0%) had specific antibodies against MERS-CoV (ppNT)</td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Reusken, 2015 (<xref rid="ref24" ref-type="bibr">24</xref>)</td><td align="left" rowspan="1" colspan="1">2013–2014</td><td align="left" rowspan="1" colspan="1">Qatar</td><td align="center" rowspan="1" colspan="1">294</td><td align="left" rowspan="1" colspan="1">Daily occupational contact with dromedary camels</td><td align="left" rowspan="1" colspan="1">10 (3.4%) had specific neutralizing antibodies against MERS-CoV (ELISA and PRNT<sub>90</sub>)</td><td align="left" rowspan="1" colspan="1">10 (100%) reported no severe health problems</td></tr><tr><td align="left" rowspan="1" colspan="1">Liljander, 2016 (<xref rid="ref25" ref-type="bibr">25</xref>)</td><td align="left" rowspan="1" colspan="1">2013–2014</td><td align="left" rowspan="1" colspan="1">Kenya</td><td align="center" rowspan="1" colspan="1">1,222</td><td align="left" rowspan="1" colspan="1">Livestock handlers in Kenya</td><td align="left" rowspan="1" colspan="1">2 (0.2%) had confirmed serological evidence of MERS-CoV infection (recombinant ELISA, PRNT<sub>50</sub> and PRNT<sub>90</sub>)</td><td align="left" rowspan="1" colspan="1">2 (100%) reported no recent clinical symptoms, indication mild or subclinical infection</td></tr><tr><td align="left" rowspan="1" colspan="1">So, 2018 (<xref rid="ref26" ref-type="bibr">26</xref>)</td><td align="left" rowspan="1" colspan="1">2016</td><td align="left" rowspan="1" colspan="1">Nigeria</td><td align="center" rowspan="1" colspan="1">261</td><td align="left" rowspan="1" colspan="1">Abattoir workers with exposure to dromedaries</td><td align="left" rowspan="1" colspan="1">0 (0%) had specific neutralizing antibodies against MERS-CoV (ELISA and ppNT)</td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Alshukairi, 2018 (<xref rid="ref27" ref-type="bibr">27</xref>)</td><td align="left" rowspan="1" colspan="1">2018</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="center" rowspan="1" colspan="1">30</td><td align="left" rowspan="1" colspan="1">Camel herders, truck drivers, and handlers</td><td align="left" rowspan="1" colspan="1">20 (67%) seropositive for MERS-CoV infection (ELISA, PRNT<sub>50</sub> and MERS-CoV–specific T-cell response)</td><td align="left" rowspan="1" colspan="1">6 (20%) reported fever or cold in the previous 4 months</td></tr><tr><td align="left" rowspan="1" colspan="1">Zohaib, 2018 (<xref rid="ref28" ref-type="bibr">28</xref>)</td><td align="left" rowspan="1" colspan="1">2016–2017</td><td align="left" rowspan="1" colspan="1">Pakistan</td><td align="center" rowspan="1" colspan="1">840</td><td align="left" rowspan="1" colspan="1">Camel herders</td><td align="left" rowspan="1" colspan="1">0 (0%) had serological evidence of MERS-CoV infection (ELISA, PRNT<sub>50</sub>)</td><td rowspan="1" colspan="1"></td></tr><tr><td align="center" colspan="7" rowspan="1"><italic>Contacts of Patients Outside Health</italic>-<italic>Care Settings Who Had Confirmed MERS</italic></td></tr><tr><td align="left" rowspan="1" colspan="1">Health Protection Agency, 2013 (<xref rid="ref29" ref-type="bibr">29</xref>)</td><td align="left" rowspan="1" colspan="1">2013</td><td align="left" rowspan="1" colspan="1">United Kingdom</td><td align="center" rowspan="1" colspan="1">33</td><td align="left" rowspan="1" colspan="1">Close contacts of a confirmed case</td><td align="left" rowspan="1" colspan="1">2 (6%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">0 (0%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Assiri, 2013 (<xref rid="ref4" ref-type="bibr">4</xref>)</td><td align="left" rowspan="1" colspan="1">2013</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="center" rowspan="1" colspan="1">217</td><td align="left" rowspan="1" colspan="1">Household contacts of confirmed cases</td><td align="left" rowspan="1" colspan="1">5 (2%) had confirmed MERS-CoV infection (RT-PCR and viral load)</td><td align="left" rowspan="1" colspan="1">Not reported</td></tr><tr><td align="left" rowspan="1" colspan="1">Omrani, 2013 (<xref rid="ref30" ref-type="bibr">30</xref>)</td><td align="left" rowspan="1" colspan="1">2013</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="center" rowspan="1" colspan="1">10</td><td align="left" rowspan="1" colspan="1">Household contacts of confirmed cases</td><td align="left" rowspan="1" colspan="1">0 (0%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td rowspan="1" colspan="1"></td></tr><tr><td colspan="7" align="right" rowspan="1"><bold>Table continues</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">Mailles, 2013 (<xref rid="ref31" ref-type="bibr">31</xref>)</td><td align="left" rowspan="1" colspan="1">2013</td><td align="left" rowspan="1" colspan="1">France</td><td align="center" rowspan="1" colspan="1">162</td><td align="left" rowspan="1" colspan="1">Contacts of a confirmed case</td><td align="left" rowspan="1" colspan="1">1 (1%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">0 (0%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Memish, 2014 (<xref rid="ref32" ref-type="bibr">32</xref>)</td><td align="left" rowspan="1" colspan="1">2012–2014</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="center" rowspan="1" colspan="1">462</td><td align="left" rowspan="1" colspan="1">Family contacts of confirmed cases</td><td align="left" rowspan="1" colspan="1">10 (2%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">Not reported</td></tr><tr><td align="left" rowspan="1" colspan="1">Drosten, 2014 (<xref rid="ref11" ref-type="bibr">11</xref>)</td><td align="left" rowspan="1" colspan="1">2013</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="center" rowspan="1" colspan="1">280</td><td align="left" rowspan="1" colspan="1">Household contacts of confirmed cases</td><td align="left" rowspan="1" colspan="1">12 (4%) had laboratory evidence of secondary MERS transmission (RT-PCR, ELISA, recombinant immunofluorescence assay, PRNT<sub>50</sub>, PRNT<sub>90</sub>)</td><td align="left" rowspan="1" colspan="1">11 (92%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Arwady, 2016 (<xref rid="ref33" ref-type="bibr">33</xref>)</td><td align="left" rowspan="1" colspan="1">2014</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="center" rowspan="1" colspan="1">79</td><td align="left" rowspan="1" colspan="1">Relatives of patients infected with MERS-CoV</td><td align="left" rowspan="1" colspan="1">11 (14%) had molecular evidence of MERS-CoV infection (RT-PCR); 8 (10%) additional contacts had serological evidence of MERS-CoV infection (ELISA)</td><td align="left" rowspan="1" colspan="1">2 (11%) reported mild symptoms and 3 (16%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Plipat, 2017 (<xref rid="ref34" ref-type="bibr">34</xref>)</td><td align="left" rowspan="1" colspan="1">2015</td><td align="left" rowspan="1" colspan="1">Thailand</td><td align="center" rowspan="1" colspan="1">48</td><td align="left" rowspan="1" colspan="1">High-risk contacts of a confirmed case</td><td align="left" rowspan="1" colspan="1">0 (0%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Al Hosani, 2019 (<xref rid="ref35" ref-type="bibr">35</xref>)</td><td align="left" rowspan="1" colspan="1">2013–2018</td><td align="left" rowspan="1" colspan="1">United Arab Emirates</td><td align="center" rowspan="1" colspan="1">124</td><td align="left" rowspan="1" colspan="1">Case patients and household contacts of patients with MERS-CoV</td><td align="left" rowspan="1" colspan="1">13 (54%) cases had MERS-CoV antibodies; 0 (0%) household contacts had serological evidence of MERS-CoV infection (ELISA and microneutralization)</td><td align="left" rowspan="1" colspan="1">3 of 13 case patients (23%) were asymptomatic</td></tr><tr><td align="center" colspan="7" rowspan="1"><italic>General Population</italic></td></tr><tr><td align="left" rowspan="1" colspan="1">Gierer, 2013 (<xref rid="ref36" ref-type="bibr">36</xref>)</td><td align="left" rowspan="1" colspan="1">2010–2012</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="center" rowspan="1" colspan="1">268</td><td align="left" rowspan="1" colspan="1">Children hospitalized for lower respiratory tract infection and male blood donors</td><td align="left" rowspan="1" colspan="1">0 (0%) had specific neutralizing antibodies against MERS-CoV (lentiviral vector system)</td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Müller, 2015 (<xref rid="ref37" ref-type="bibr">37</xref>)</td><td align="left" rowspan="1" colspan="1">2012–2013</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="center" rowspan="1" colspan="1">10,009</td><td align="left" rowspan="1" colspan="1">Healthy individuals across all 13 provinces of KSA</td><td align="left" rowspan="1" colspan="1">15 (0.1%) had anti–MERS-CoV antibodies (recombinant ELISA, recombinant immunofluorescence assay, PRNT<sub>50</sub> and PRNT<sub>90</sub>)</td><td align="left" rowspan="1" colspan="1">Not reported</td></tr><tr><td align="left" rowspan="1" colspan="1">Munyua, 2017 (<xref rid="ref38" ref-type="bibr">38</xref>)</td><td align="left" rowspan="1" colspan="1">2013</td><td align="left" rowspan="1" colspan="1">Kenya</td><td align="center" rowspan="1" colspan="1">760</td><td align="left" rowspan="1" colspan="1">Households exposed to seropositive camels</td><td align="left" rowspan="1" colspan="1">0 (0%) had specific neutralizing antibodies against MERS-CoV (ELISA and PRNT<sub>50</sub>)</td><td rowspan="1" colspan="1"></td></tr><tr><td colspan="7" align="right" rowspan="1"><bold>Table continues</bold></td></tr><tr><td align="center" colspan="7" rowspan="1"><italic>Retrospective Review of National Surveillance Records</italic></td></tr><tr><td align="left" rowspan="1" colspan="1">Al Hosani, 2016 (<xref rid="ref7" ref-type="bibr">7</xref>)</td><td align="left" rowspan="1" colspan="1">2013–2014</td><td align="left" rowspan="1" colspan="1">United Arab Emirates</td><td align="center" rowspan="1" colspan="1">1,586</td><td align="left" rowspan="1" colspan="1">Case patients from surveillance records who were suspected to have MERS</td><td align="left" rowspan="1" colspan="1">65 (4%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">23 (35%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Saeed, 2017 (<xref rid="ref39" ref-type="bibr">39</xref>)</td><td align="left" rowspan="1" colspan="1">2015–2016</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="center" rowspan="1" colspan="1">57,363</td><td align="left" rowspan="1" colspan="1">Case patients suspected to have MERS</td><td align="left" rowspan="1" colspan="1">384 (1%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">19 (5%) were asymptomatic</td></tr></tbody></table><table-wrap-foot><p>Abbreviations: ELISA, enzyme-linked immunoassay; KSA, Kingdom of Saudi Arabia; MERS-CoV, Middle East respiratory syndrome coronavirus; PCR, polymerase chain reaction; ppNT, pseudoparticle neutralization test; PRNT<sub>50</sub>, 50% plaque reduction neutralization test; PRNT<sub>90</sub>, 90% plaque reduction neutralization test; RT-PCR, reverse transcriptase polymerase chain reaction.</p></table-wrap-foot></table-wrap><table-wrap id="TB2" orientation="portrait" position="float"><label>Table 2</label><caption><p>Evidence of Middle East Respiratory Syndrome Coronavirus Infection in Health-Care Settings, 2012–2018</p></caption><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col></colgroup><thead><tr><th align="center" rowspan="1" colspan="1"><bold>First Author, Year (Reference No.)</bold></th><th align="center" rowspan="1" colspan="1"><bold>Years of Study</bold></th><th align="center" rowspan="1" colspan="1"><bold>Location of Study</bold></th><th align="center" rowspan="1" colspan="1"><bold>No. of Individuals Tested</bold></th><th align="center" rowspan="1" colspan="1"><bold>Description of Subjects</bold></th><th align="center" rowspan="1" colspan="1"><bold>Laboratory Results</bold></th><th align="center" rowspan="1" colspan="1"><bold>Evidence of Asymptomatic MERS-CoV Infection Among PCR/Serologically Positive Subjects</bold></th></tr></thead><tbody><tr><td align="center" colspan="7" rowspan="1"><italic>HCW Contacts of Patients With Confirmed MERS-CoV</italic></td></tr><tr><td align="left" rowspan="1" colspan="1">Health Protection Agency, 2013 (<xref rid="ref29" ref-type="bibr">29</xref>)</td><td align="left" rowspan="1" colspan="1">2013</td><td align="left" rowspan="1" colspan="1">United Kingdom</td><td align="left" rowspan="1" colspan="1">59</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">0 transmission (RT-PCR)</td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Memish, 2014 (<xref rid="ref32" ref-type="bibr">32</xref>)</td><td align="left" rowspan="1" colspan="1">2012–2013</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="left" rowspan="1" colspan="1">1,695</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">19 (1%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">2 (11%) were asymptomatic; 5 (26%) had mild infection</td></tr><tr><td align="left" rowspan="1" colspan="1">Kim, 2016 (<xref rid="ref40" ref-type="bibr">40</xref>)</td><td align="left" rowspan="1" colspan="1">2015</td><td align="left" rowspan="1" colspan="1">ROK</td><td align="left" rowspan="1" colspan="1">1,169</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">17 (1%) had evidence of MERS-CoV infection, higher among HCWs who did not use PPE (ELISA and indirect immunofluorescence test)</td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Cho, 2016 (<xref rid="ref41" ref-type="bibr">41</xref>)</td><td align="left" rowspan="1" colspan="1">2015</td><td align="left" rowspan="1" colspan="1">ROK</td><td align="left" rowspan="1" colspan="1">218</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">8 (4%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Park, 2016 (<xref rid="ref42" ref-type="bibr">42</xref>)</td><td align="left" rowspan="1" colspan="1">2015</td><td align="left" rowspan="1" colspan="1">ROK</td><td align="left" rowspan="1" colspan="1">519</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">3 (1%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">3 (100%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Hastings, 2016 (<xref rid="ref43" ref-type="bibr">43</xref>)</td><td align="left" rowspan="1" colspan="1">2014</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="left" rowspan="1" colspan="1">16</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">14 (88%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">13 (81%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Moon, 2017 (<xref rid="ref44" ref-type="bibr">44</xref>)</td><td align="left" rowspan="1" colspan="1">2015</td><td align="left" rowspan="1" colspan="1">ROK</td><td align="left" rowspan="1" colspan="1">82</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">0 transmission from asymptomatic HCWs (RT-PCR and ELISA)</td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1">Alfaraj, 2019 (<xref rid="ref45" ref-type="bibr">45</xref>)</td><td align="left" rowspan="1" colspan="1">2015</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="left" rowspan="1" colspan="1">153</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">7 (5%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">5 (71%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Amer, 2018 (<xref rid="ref46" ref-type="bibr">46</xref>)</td><td align="left" rowspan="1" colspan="1">2017</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="left" rowspan="1" colspan="1">879</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">17 (2%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">17 (100%) were asymptomatic or had mild disease</td></tr><tr><td align="left" rowspan="1" colspan="1">Amer, 2018 (<xref rid="ref47" ref-type="bibr">47</xref>)</td><td align="left" rowspan="1" colspan="1">2017</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="left" rowspan="1" colspan="1">107</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">9 (8%) positive for MERS-CoV (RT-PCR)</td><td rowspan="1" colspan="1"></td></tr><tr><td align="center" colspan="7" rowspan="1"><italic>Asymptomatic Infection Among Infected HCWs</italic></td></tr><tr><td align="left" rowspan="1" colspan="1">Alshukairi, 2016 (<xref rid="ref48" ref-type="bibr">48</xref>)</td><td align="left" rowspan="1" colspan="1">2014–2016</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="left" rowspan="1" colspan="1">NR</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">18 had molecular and serological evidence of MERS-CoV infection (RT-PCR, ELISA, IFA)</td><td align="left" rowspan="1" colspan="1">6 (33%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Assiri, 2016 (<xref rid="ref49" ref-type="bibr">49</xref>)</td><td align="left" rowspan="1" colspan="1">2014–2015</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="left" rowspan="1" colspan="1">NR</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">7 had molecular and serological evidence of MERS-CoV infection (RT-PCR, ELISA, IFA, MT)</td><td align="left" rowspan="1" colspan="1">4 (57%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Balkhy, 2016 (<xref rid="ref50" ref-type="bibr">50</xref>)</td><td align="left" rowspan="1" colspan="1">2015</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="left" rowspan="1" colspan="1">NR</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">43 had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">25 (58%) were asymptomatic</td></tr><tr><td colspan="7" align="right" rowspan="1"><bold>Table continues</bold></td></tr><tr><td align="left" rowspan="1" colspan="1">Al Hosani, 2016 (<xref rid="ref7" ref-type="bibr">7</xref>)</td><td align="left" rowspan="1" colspan="1">2013–2014</td><td align="left" rowspan="1" colspan="1">United Arab Emirates</td><td align="left" rowspan="1" colspan="1">NR</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">31 had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">12 (39%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Alenazi, 2017 (<xref rid="ref51" ref-type="bibr">51</xref>)</td><td align="left" rowspan="1" colspan="1">2015</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="left" rowspan="1" colspan="1">NR</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">43 had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">18 (42%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">2018<xref rid="tblfn1" ref-type="table-fn"><sup>a</sup></xref></td><td align="left" rowspan="1" colspan="1">2012–2018</td><td align="left" rowspan="1" colspan="1">Global</td><td align="left" rowspan="1" colspan="1">NR</td><td align="left" rowspan="1" colspan="1">HCW</td><td align="left" rowspan="1" colspan="1">389 had laboratory-confirmed MERS-CoV infection</td><td align="left" rowspan="1" colspan="1">94 (24%) were asymptomatic</td></tr><tr><td align="center" colspan="7" rowspan="1"><italic>MERS-CoV Infection in Health-Care Settings Among Non–HCWs</italic></td></tr><tr><td align="left" rowspan="1" colspan="1">Al-Abdallat, 2014 (<xref rid="ref5" ref-type="bibr">5</xref>)</td><td align="left" rowspan="1" colspan="1">2012–2013</td><td align="left" rowspan="1" colspan="1">Jordan</td><td align="left" rowspan="1" colspan="1">124</td><td align="left" rowspan="1" colspan="1">Contacts identified during MERS outbreak</td><td align="left" rowspan="1" colspan="1">9 (7%) had serological evidence of MERS-CoV infection (ELISA, IFA, MT)</td><td align="left" rowspan="1" colspan="1">0 (0%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Cho, 2016 (<xref rid="ref41" ref-type="bibr">41</xref>)</td><td align="left" rowspan="1" colspan="1">2015</td><td align="left" rowspan="1" colspan="1">ROK</td><td align="left" rowspan="1" colspan="1">675</td><td align="left" rowspan="1" colspan="1">Patients in hospital, contacts of patients infected with MERS-CoV</td><td align="left" rowspan="1" colspan="1">33 (5%) had molecular evidence of MERS-CoV infection (RT-PCR)</td><td rowspan="1" colspan="1"></td></tr><tr><td align="center" colspan="7" rowspan="1"><italic>Extent of Asymptomatic Infection Among Laboratory-Confirmed MERS Cases</italic></td></tr><tr><td align="left" rowspan="1" colspan="1">Oboho, 2015 (<xref rid="ref52" ref-type="bibr">52</xref>)</td><td align="left" rowspan="1" colspan="1">2014</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="left" rowspan="1" colspan="1">NR</td><td align="left" rowspan="1" colspan="1">Confirmed MERS-CoV infection</td><td align="left" rowspan="1" colspan="1">255 had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">64 (25%) patients were asymptomatic, although 26 patients interviewed reported at least 1 symptom consistent with respiratory illness</td></tr><tr><td align="left" rowspan="1" colspan="1">Assiri, 2016 (<xref rid="ref49" ref-type="bibr">49</xref>)</td><td align="left" rowspan="1" colspan="1">2014–2015</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="left" rowspan="1" colspan="1">NR</td><td align="left" rowspan="1" colspan="1">Confirmed MERS-CoV infection</td><td align="left" rowspan="1" colspan="1">38 had molecular and serological evidence of MERS-CoV infection (RT-PCR, ELISA, IFA, MT)</td><td align="left" rowspan="1" colspan="1">2 (5%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Alenazi, 2017 (<xref rid="ref51" ref-type="bibr">51</xref>)</td><td align="left" rowspan="1" colspan="1">2015</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="left" rowspan="1" colspan="1">NR</td><td align="left" rowspan="1" colspan="1">Patient contacts in hospital</td><td align="left" rowspan="1" colspan="1">61 had molecular evidence of MERS-CoV infection (RT-PCR)</td><td align="left" rowspan="1" colspan="1">3 (5%) were asymptomatic</td></tr><tr><td align="left" rowspan="1" colspan="1">Zhao, 2017 (<xref rid="ref53" ref-type="bibr">53</xref>)</td><td align="left" rowspan="1" colspan="1">2015</td><td align="left" rowspan="1" colspan="1">KSA</td><td align="left" rowspan="1" colspan="1">NR</td><td align="left" rowspan="1" colspan="1">MERS survivors</td><td align="left" rowspan="1" colspan="1">18 had molecular and serological evidence of MERS-CoV infection (RT-PCR, ELISA, IFA, MT, PRNT<sub>50</sub>, and MERS-CoV–specific T-cell response)</td><td align="left" rowspan="1" colspan="1">3 (17%) were asymptomatic; patients with higher PRNT<sub>50</sub> and T-cell responses had longer stays in the intensive care unit</td></tr><tr><td align="left" rowspan="1" colspan="1">Payne, 2018 (<xref rid="ref54" ref-type="bibr">54</xref>)</td><td align="left" rowspan="1" colspan="1">2015–2016</td><td align="left" rowspan="1" colspan="1">Jordan</td><td align="left" rowspan="1" colspan="1">NR</td><td align="left" rowspan="1" colspan="1">Patient-contacts in hospital</td><td align="left" rowspan="1" colspan="1">16 had laboratory-confirmed MERS-CoV infection (RT-PCR, ELISA, MT)</td><td align="left" rowspan="1" colspan="1">3 (19%) were asymptomatic</td></tr></tbody></table><table-wrap-foot><p>Abbreviations: ELISA, enzyme-linked immunoassay; HCW, health-care worker; IFA, immunofluorescence assay; KSA, Kingdom of Saudi Arabia; MERS-CoV, Middle East respiratory syndrome coronavirus; MT, microneutralization assay; NR, not reported; PPE, personal protective equipment; PRNT, plaque reduction neutralization test; ROK, Republic of Korea; RT-PCR, reverse transcriptase polymerase chain reaction.</p><fn id="tblfn1"><p><sup>a</sup> World Health Organization, unpublished data, 2018.</p></fn></table-wrap-foot></table-wrap><p>Since 2012, 298 of the 2,274 laboratory-confirmed cases (13.1%) reported to WHO have been reported as asymptomatic at the time of reporting, 164 of these patients were HCWs. The demographic characteristics and clinical presentation of primary and secondary cases of MERS-CoV infection are listed in <xref rid="TB3" ref-type="table">Table 3</xref>. There were significantly more asymptomatic cases reported among secondary cases (n = 266 of 1,094; 24.3%) than among primary cases (n = 9 of 642 (1.4%); <italic>P</italic> < 0.001). Overall, no deaths were reported among patients with asymptomatic infections. <xref rid="f2" ref-type="fig">Figure 2</xref> shows the epidemic curve of MERS-CoV infections reported to WHO stratified by HCWs and non-HCWs. Of the 414 MERS-CoV infections among HCWs that were reported to WHO, 164 (39.6%) were reported to be asymptomatic.</p><table-wrap id="TB3" orientation="portrait" position="float"><label>Table 3</label><caption><p>Description of Characteristics of Middle East Respiratory Syndrome Coronavirus Infection Reported to World Health Organization from September 2012 to November 27, 2018</p></caption><table frame="hsides" rules="groups"><colgroup span="1"><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col><col align="left" span="1"></col></colgroup><thead><tr><th rowspan="1" colspan="1"></th><th colspan="6" align="center" rowspan="1"><bold>Reported Source of Infection</bold></th></tr><tr><th align="center" rowspan="1" colspan="1"><bold>MERS Case Characteristic</bold></th><th colspan="2" align="center" rowspan="1"><bold>Outside Health-Care Setting</bold></th><th colspan="2" align="center" rowspan="1"><bold>Within in Health-Care Setting</bold></th><th colspan="2" align="center" rowspan="1"><bold>Not Known at the Time of Reporting to WHO</bold></th></tr><tr><th rowspan="1" colspan="1"></th><th align="center" rowspan="1" colspan="1"><bold>No.</bold></th><th align="center" rowspan="1" colspan="1"><bold>%</bold></th><th align="center" rowspan="1" colspan="1"><bold>No.</bold></th><th align="center" rowspan="1" colspan="1"><bold>%</bold></th><th align="center" rowspan="1" colspan="1"><bold>No.</bold></th><th align="center" rowspan="1" colspan="1"><bold>%</bold></th></tr></thead><tbody><tr><td align="left" rowspan="1" colspan="1">Case classification</td><td align="center" rowspan="1" colspan="1">764</td><td rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1">826</td><td rowspan="1" colspan="1"></td><td align="center" rowspan="1" colspan="1">681</td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> Primary case<xref rid="tblfn2" ref-type="table-fn"><sup>a</sup></xref></td><td align="center" rowspan="1" colspan="1">561</td><td align="center" rowspan="1" colspan="1">73.4</td><td align="center" rowspan="1" colspan="1">2</td><td align="center" rowspan="1" colspan="1">0.2</td><td align="center" rowspan="1" colspan="1">79</td><td align="center" rowspan="1" colspan="1">11.6</td></tr><tr><td align="left" rowspan="1" colspan="1"> Secondary case<xref rid="tblfn3" ref-type="table-fn"><sup>b</sup></xref></td><td align="center" rowspan="1" colspan="1">193</td><td align="center" rowspan="1" colspan="1">25.3</td><td align="center" rowspan="1" colspan="1">816</td><td align="center" rowspan="1" colspan="1">98.8</td><td align="center" rowspan="1" colspan="1">85</td><td align="center" rowspan="1" colspan="1">12.5</td></tr><tr><td align="left" rowspan="1" colspan="1"> Unknown at the time of reporting</td><td align="center" rowspan="1" colspan="1">10</td><td align="center" rowspan="1" colspan="1">1.3</td><td align="center" rowspan="1" colspan="1">8</td><td align="center" rowspan="1" colspan="1">1.0</td><td align="center" rowspan="1" colspan="1">517</td><td align="center" rowspan="1" colspan="1">75.9</td></tr><tr><td align="left" rowspan="1" colspan="1">Primary MERS-CoV infection<xref rid="tblfn2" ref-type="table-fn"><sup>a</sup></xref></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> Age, years<xref rid="tblfn4" ref-type="table-fn"><sup>c</sup></xref></td><td align="center" colspan="2" rowspan="1">55.9 (45.0–69.0)</td><td align="center" colspan="2" rowspan="1">47.0 (39.0–55.0)</td><td align="center" colspan="2" rowspan="1">57.8 (46.0–72.0)</td></tr><tr><td align="left" rowspan="1" colspan="1"> Sex</td><td colspan="2" rowspan="1"></td><td colspan="2" rowspan="1"></td><td colspan="2" rowspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> Male</td><td align="center" rowspan="1" colspan="1">459</td><td align="center" rowspan="1" colspan="1">81.8</td><td align="center" rowspan="1" colspan="1">2</td><td align="center" rowspan="1" colspan="1">100</td><td align="center" rowspan="1" colspan="1">72</td><td align="center" rowspan="1" colspan="1">91.1</td></tr><tr><td align="left" rowspan="1" colspan="1"> Female</td><td align="center" rowspan="1" colspan="1">102</td><td align="center" rowspan="1" colspan="1">18.2</td><td align="center" rowspan="1" colspan="1">0</td><td align="center" rowspan="1" colspan="1">0</td><td align="center" rowspan="1" colspan="1">5</td><td align="center" rowspan="1" colspan="1">6.3</td></tr><tr><td align="left" rowspan="1" colspan="1"> Comorbidity</td><td colspan="2" rowspan="1"></td><td colspan="2" rowspan="1"></td><td colspan="2" rowspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> Any</td><td align="center" rowspan="1" colspan="1">316</td><td align="center" rowspan="1" colspan="1">56.3</td><td align="center" rowspan="1" colspan="1">1</td><td align="center" rowspan="1" colspan="1">50</td><td align="center" rowspan="1" colspan="1">17</td><td align="center" rowspan="1" colspan="1">21.5</td></tr><tr><td align="left" rowspan="1" colspan="1"> None</td><td align="center" rowspan="1" colspan="1">62</td><td align="center" rowspan="1" colspan="1">11.1</td><td align="center" rowspan="1" colspan="1">0</td><td align="center" rowspan="1" colspan="1">0</td><td align="center" rowspan="1" colspan="1">3</td><td align="center" rowspan="1" colspan="1">3.8</td></tr><tr><td align="left" rowspan="1" colspan="1"> Not reported</td><td align="center" rowspan="1" colspan="1">183</td><td align="center" rowspan="1" colspan="1">32.6</td><td align="center" rowspan="1" colspan="1">1</td><td align="center" rowspan="1" colspan="1">50</td><td align="center" rowspan="1" colspan="1">59</td><td align="center" rowspan="1" colspan="1">74.7</td></tr><tr><td align="left" rowspan="1" colspan="1"> Clinical presentation</td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> Asymptomatic</td><td align="center" rowspan="1" colspan="1">7</td><td align="center" rowspan="1" colspan="1">1.2</td><td align="center" rowspan="1" colspan="1">0</td><td align="center" rowspan="1" colspan="1">0</td><td align="center" rowspan="1" colspan="1">2</td><td align="center" rowspan="1" colspan="1">2.5</td></tr><tr><td align="left" rowspan="1" colspan="1"> Symptomatic</td><td align="center" rowspan="1" colspan="1">521</td><td align="center" rowspan="1" colspan="1">92.9</td><td align="center" rowspan="1" colspan="1">2</td><td align="center" rowspan="1" colspan="1">100</td><td align="center" rowspan="1" colspan="1">65</td><td align="center" rowspan="1" colspan="1">82.3</td></tr><tr><td align="left" rowspan="1" colspan="1"> Not reported</td><td align="center" rowspan="1" colspan="1">33</td><td align="center" rowspan="1" colspan="1">5.9</td><td align="center" rowspan="1" colspan="1">0</td><td align="center" rowspan="1" colspan="1">0</td><td align="center" rowspan="1" colspan="1">12</td><td align="center" rowspan="1" colspan="1">15.2</td></tr><tr><td align="left" rowspan="1" colspan="1"> Outcome</td><td colspan="2" rowspan="1"></td><td colspan="2" rowspan="1"></td><td colspan="2" rowspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> Survived</td><td align="center" rowspan="1" colspan="1">167</td><td align="center" rowspan="1" colspan="1">29.8</td><td align="center" rowspan="1" colspan="1">1</td><td align="center" rowspan="1" colspan="1">50</td><td align="center" rowspan="1" colspan="1">14</td><td align="center" rowspan="1" colspan="1">17.7</td></tr><tr><td align="left" rowspan="1" colspan="1"> Died</td><td align="center" rowspan="1" colspan="1">277</td><td align="center" rowspan="1" colspan="1">49.4</td><td align="center" rowspan="1" colspan="1">0</td><td align="center" rowspan="1" colspan="1">0</td><td align="center" rowspan="1" colspan="1">32</td><td align="center" rowspan="1" colspan="1">40.5</td></tr><tr><td align="left" rowspan="1" colspan="1"> Not reported</td><td align="center" rowspan="1" colspan="1">117</td><td align="center" rowspan="1" colspan="1">20.8</td><td align="center" rowspan="1" colspan="1">1</td><td align="center" rowspan="1" colspan="1">50</td><td align="center" rowspan="1" colspan="1">33</td><td align="center" rowspan="1" colspan="1">41.8</td></tr><tr><td align="left" rowspan="1" colspan="1">Secondary MERS-CoV infection<xref rid="tblfn3" ref-type="table-fn"><sup>b</sup></xref></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td><td rowspan="1" colspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> Age, years<xref rid="tblfn4" ref-type="table-fn"><sup>c</sup></xref></td><td align="center" colspan="2" rowspan="1">40.7 (27.0–54.0)</td><td align="center" colspan="2" rowspan="1">49.3 (34.0–62.0)</td><td align="center" colspan="2" rowspan="1">42.7 (28.0–54.0)</td></tr><tr><td align="left" rowspan="1" colspan="1"> Sex</td><td colspan="2" rowspan="1"></td><td colspan="2" rowspan="1"></td><td colspan="2" rowspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> Male</td><td align="center" rowspan="1" colspan="1">124</td><td align="center" rowspan="1" colspan="1">64.2</td><td align="center" rowspan="1" colspan="1">451</td><td align="center" rowspan="1" colspan="1">55.3</td><td align="center" rowspan="1" colspan="1">51</td><td align="center" rowspan="1" colspan="1">60</td></tr><tr><td align="left" rowspan="1" colspan="1"> Female</td><td align="center" rowspan="1" colspan="1">69</td><td align="center" rowspan="1" colspan="1">35.8</td><td align="center" rowspan="1" colspan="1">365</td><td align="center" rowspan="1" colspan="1">44.7</td><td align="center" rowspan="1" colspan="1">34</td><td align="center" rowspan="1" colspan="1">40</td></tr><tr><td align="left" rowspan="1" colspan="1"> Comorbidity</td><td colspan="2" rowspan="1"></td><td colspan="2" rowspan="1"></td><td colspan="2" rowspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> Any</td><td align="center" rowspan="1" colspan="1">47</td><td align="center" rowspan="1" colspan="1">24.4</td><td align="center" rowspan="1" colspan="1">281</td><td align="center" rowspan="1" colspan="1">34.4</td><td align="center" rowspan="1" colspan="1">13</td><td align="center" rowspan="1" colspan="1">15.3</td></tr><tr><td align="left" rowspan="1" colspan="1"> None</td><td align="center" rowspan="1" colspan="1">43</td><td align="center" rowspan="1" colspan="1">22.3</td><td align="center" rowspan="1" colspan="1">104</td><td align="center" rowspan="1" colspan="1">12.7</td><td align="center" rowspan="1" colspan="1">10</td><td align="center" rowspan="1" colspan="1">11.8</td></tr><tr><td align="left" rowspan="1" colspan="1"> Not reported</td><td align="center" rowspan="1" colspan="1">103</td><td align="center" rowspan="1" colspan="1">53.4</td><td align="center" rowspan="1" colspan="1">431</td><td align="center" rowspan="1" colspan="1">52.8</td><td align="center" rowspan="1" colspan="1">62</td><td align="center" rowspan="1" colspan="1">72.9</td></tr><tr><td align="left" colspan="3" rowspan="1"> Clinical presentation</td><td colspan="2" rowspan="1"></td><td colspan="2" rowspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> Asymptomatic</td><td align="center" rowspan="1" colspan="1">74</td><td align="center" rowspan="1" colspan="1">38.3</td><td align="center" rowspan="1" colspan="1">180</td><td align="center" rowspan="1" colspan="1">22.1</td><td align="center" rowspan="1" colspan="1">12</td><td align="center" rowspan="1" colspan="1">14.1</td></tr><tr><td align="left" rowspan="1" colspan="1"> Symptomatic</td><td align="center" rowspan="1" colspan="1">103</td><td align="center" rowspan="1" colspan="1">53.4</td><td align="center" rowspan="1" colspan="1">482</td><td align="center" rowspan="1" colspan="1">59.1</td><td align="center" rowspan="1" colspan="1">51</td><td align="center" rowspan="1" colspan="1">60</td></tr><tr><td align="left" rowspan="1" colspan="1"> Not reported</td><td align="center" rowspan="1" colspan="1">16</td><td align="center" rowspan="1" colspan="1">8.3</td><td align="center" rowspan="1" colspan="1">154</td><td align="center" rowspan="1" colspan="1">18.9</td><td align="center" rowspan="1" colspan="1">22</td><td align="center" rowspan="1" colspan="1">25.9</td></tr><tr><td align="left" rowspan="1" colspan="1"> Outcome</td><td colspan="2" rowspan="1"></td><td colspan="2" rowspan="1"></td><td colspan="2" rowspan="1"></td></tr><tr><td align="left" rowspan="1" colspan="1"> Survived</td><td align="center" rowspan="1" colspan="1">127</td><td align="center" rowspan="1" colspan="1">65.8</td><td align="center" rowspan="1" colspan="1">337</td><td align="center" rowspan="1" colspan="1">41.3</td><td align="center" rowspan="1" colspan="1">28</td><td align="center" rowspan="1" colspan="1">32.9</td></tr><tr><td align="left" rowspan="1" colspan="1"> Died</td><td align="center" rowspan="1" colspan="1">27</td><td align="center" rowspan="1" colspan="1">14.0</td><td align="center" rowspan="1" colspan="1">248</td><td align="center" rowspan="1" colspan="1">30.4</td><td align="center" rowspan="1" colspan="1">20</td><td align="center" rowspan="1" colspan="1">23.5</td></tr><tr><td align="left" rowspan="1" colspan="1"> Not reported</td><td align="center" rowspan="1" colspan="1">39</td><td align="center" rowspan="1" colspan="1">20.2</td><td align="center" rowspan="1" colspan="1">231</td><td align="center" rowspan="1" colspan="1">28.3</td><td align="center" rowspan="1" colspan="1">37</td><td align="center" rowspan="1" colspan="1">43.5</td></tr></tbody></table><table-wrap-foot><p>Abbreviations: IQR, interquartile range; MERS-CoV, Middle East respiratory syndrome coronavirus; WHO, World Health Organization.</p><fn id="tblfn2"><p><sup>a</sup> Primary infection: reported direct or indirect contact with dromedary camels, no contact with a probable or confirmed MERS-CoV infected human case, no prior health care facility contact (<italic>n</italic> = 642).</p></fn><fn id="tblfn3"><p><sup>b</sup> Secondary infection: direct epidemiologic link to a human MERS infection (<italic>n</italic> = 1,094).</p></fn><fn id="tblfn4"><p><sup>c</sup> Values are expressed as mean (interquartile range).</p></fn></table-wrap-foot></table-wrap><sec id="sec3"><title>Evidence of human-to-human transmission from an asymptomatic infection</title><p>We found 4 studies that documented the duration of viral shedding from asymptomatic or mildly symptomatic individuals (<xref rid="ref55" ref-type="bibr">55–58</xref>). Among asymptomatic, PCR-positive MERS-CoV infections, positive reverse transcriptase (RT)-PCR results were reported from the day of initial testing for as long as 28–42 days (<xref rid="ref55" ref-type="bibr">55–58</xref>).</p><p>We found 1 study in which molecular and serological evidence of possible secondary transmission from asymptomatic individuals was reported (<xref rid="ref11" ref-type="bibr">11</xref>). The study was conducted as part of an investigation of 12 household contacts, in whom upper respiratory tract samples from 7 were PCR positive and an additional 5 samples were seropositive using recombinant immunofluorescence or plaque reduction neutralization test (<xref rid="ref11" ref-type="bibr">11</xref>). Eleven of these 12 individuals reported no symptoms at the time of sampling; this information, combined with epidemiologic data, indicated these people could have been involved in asymptomatic transmission within households.</p><p>We found 9 studies that described molecular evidence of MERS-CoV infection among asymptomatic individuals in health-care settings (<xref rid="ref7" ref-type="bibr">7</xref>, <xref rid="ref32" ref-type="bibr">32</xref>, <xref rid="ref42" ref-type="bibr">42</xref>, <xref rid="ref43" ref-type="bibr">43</xref>, <xref rid="ref45" ref-type="bibr">45</xref>, <xref rid="ref46" ref-type="bibr">46</xref>, <xref rid="ref50" ref-type="bibr">50</xref>, <xref rid="ref51" ref-type="bibr">51</xref>, <xref rid="ref53" ref-type="bibr">53</xref>). Infectivity of an asymptomatic HCW infected with MERS-CoV was investigated in 1 study, but no evidence was found of secondary transmission to 82 HCWs with contact to the HCW with MERS-CoV infection (<xref rid="ref44" ref-type="bibr">44</xref>).</p><fig id="f2" orientation="portrait" position="float"><label>Figure 2</label><caption><p> Epidemic curve of laboratory-confirmed Middle East respiratory syndrome coronavirus infections among A) health-care workers and B) non–health-care workers and outcome reported to the World Health Organization from 2012 to November 27, 2018.</p></caption><graphic xlink:href="mxz009f2"></graphic></fig></sec></sec><sec id="sec4"><title>DISCUSSION</title><p>In this review, we found 43 studies in which molecular and/or serological evidence of MERS-CoV infection was reported. Outside of health-care settings, the evidence of MERS-CoV infection has largely been focused on individuals with occupational exposure to dromedaries. The results to date are heterogenous, and although attempts have been made to evaluate MERS-CoV genetic diversity (<xref rid="ref59" ref-type="bibr">59</xref>, <xref rid="ref60" ref-type="bibr">60</xref>), the differences in seroprevalence results to date likely reflect differences in the selection and characteristics of dromedary herds and humans tested. The available evidence of the MERS-CoV epidemiologic and genetic characteristics does not suggest there are differences in the virus’s ability to infect humans. Evidence supports that individuals with occupational exposure to dromedaries have higher rates of seroprevalence compared with household contacts of patients with confirmed MERS-CoV infection, likely reflecting more intense, unprotected exposures to MERS-CoV through dromedary secretions (<xref rid="ref61" ref-type="bibr">61</xref>). That these individuals have subclinical infection and do not develop disease is likely because those with occupational exposure tend to be younger and healthier, without underlying high-risk conditions such as hypertension, diabetes, and renal failure. Variations in the seroprevalence rates by study are also likely due to variations in methodologies, including the timing of sample collection, serologic assays used, and interpretation of assay results.</p><p>Although the majority of human MERS-CoV infections have been reported to WHO from countries in the Arabian Peninsula, particularly Kingdom of Saudi Arabia, there is increasing evidence of infection in dromedary camels in herds throughout Africa and South Asia (<xref rid="ref62" ref-type="bibr">62</xref>). Additional serological and molecular epidemiology studies at the dromedary-human interface using a standardized approach and consistent methodology, in the Arabian Peninsula and in Africa and South Asia, are needed to further understand this observed heterogeneity—that is, whether the observed differences in evidence of infection outside health-care settings may be attributable to genetic variation of the virus across different geographic regions and/or to factors and behaviors in human populations in these regions, which may change the susceptibility to infection. WHO is currently supporting studies underway in several countries in the Middle East, Africa, and South Asia in which the extent of infection in occupationally exposed persons is being evaluated . The results of such studies can contribute to better understanding the geographic reach of MERS-CoV in dromedaries and humans.</p><p>Within health-care settings, the detection of asymptomatic, PCR-positive infection has been reported to WHO from affected member states and also documented in 10 published studies. Although onward transmission was not investigated in those studies, the researchers did capture evidence of RNA shedding, which suggests human-to-human transmission is possible from individuals with no signs or symptoms of infection. This is supported by evidence documenting duration of viral shedding beyond 3 weeks in patients with subclinical MERS-CoV infection (<xref rid="ref55" ref-type="bibr">55–58</xref>).</p><p>At the same time, the evidence for acute, asymptomatic MERS-CoV infection described in this review does not represent the full extent of subclinical infection. Asymptomatic contacts clear the virus more quickly than do symptomatic patients (<xref rid="ref58" ref-type="bibr">58</xref>) and antibody titers in the former are likely to be lower, if they seroconvert at all, than in infected patients exhibiting symptoms (<xref rid="ref63" ref-type="bibr">63</xref>). Timely and repeated biological specimen collection is needed to capture viral shedding and antibody kinetics of symptomatic and asymptomatic contacts (<xref rid="ref11" ref-type="bibr">11</xref>). This can be achieved if all high-risk contacts of patients with confirmed MERS-CoV infection are identified during an outbreak and then tested using molecular and serologic laboratory assays, regardless of whether the individual exhibits symptoms. In outbreak settings, without the inclusion of testing of all contacts, the identification of chains of transmission may be incomplete.</p><p>Indeed, the latest WHO surveillance guidelines recommend that all contacts of patients with laboratory-confirmed MERS outside of health care facilities should be placed under active surveillance for 14 days after the last exposure to the confirmed case and that any contacts with symptoms of respiratory illness should be tested for MERS-CoV infection (<xref rid="ref64" ref-type="bibr">64</xref>). If feasible, we recommend that follow-up should include molecular testing, regardless of the development of symptoms. In addition, studies conducted of high-risk workers, which have typically only included serologic testing, should also include molecular testing of upper respiratory samples in an attempt to capture viral carriage.</p><p>Despite these limitations in our current knowledge, the findings of our review reinforce the evidence that HCWs are more likely to be at risk of MERS-CoV infection due to close unprotected contact with patients with MERS patients prior to their diagnosis, particularly when aerosolizing procedures are performed. Because HCWs tend to be younger and healthier than patients in whom severe MERS develops, HCWs have fewer symptoms, if any, and present a silent risk of human-to-human transmission to others. Among HCW contacts, detailed studies of viral shedding and immune response of asymptomatic, PCR-positive MERS-CoV infections are urgently needed and should be conducted when outbreaks occur and enhanced surveillance is put in place by government and hospital officials.</p><p>Surveillance and testing for MERS-CoV have improved substantially since the virus was first discovered in 2012. In affected countries, visual respiratory triage systems before a patient enters the emergency department have been introduced; some emergency departments in affected countries have been restructured for enhanced triage of patients with respiratory symptoms; trainings specific to infection prevention and control of respiratory pathogens have been introduced and reintroduced in high-risk areas and hospitals with high turnover of HCWs; and audits of hospitals for compliance to specific infection prevention and control measures are regularly performed (<xref rid="ref6" ref-type="bibr">6</xref>). In addition, the systematic testing of HCWs, extending beyond nurses and doctors to include reception staff, cleaners, technicians, and so forth, regardless of the development of symptoms, as required by the latest infection prevention and control guidelines for HCWs by WHO and Kingdom of Saudi Arabia, for example, has detected subclinical and asymptomatic infections that likely would have gone undetected in past outbreaks. Asymptomatic infections may have played a role in extensive secondary transmission in health-care settings before the latest guidelines were introduced, and the impact of such policies may be reflected in the lower peaks on the global MERS-CoV epidemic curve since 2016. Without this level of contact follow-up in community settings, the extent of asymptomatic infections in the community will remain unknown.</p><p>Screening of HCWs with exposure to patients infected with MERS-CoV may be feasible for preventing human-to-human transmission in health-care settings, and appears to be effective in Kingdom of Saudi Arabia and other affected countries in which this infection prevention and control measure has been introduced. Screening of non-HCW contacts in health-care settings should also be encouraged. Outside health-care settings, the feasibility of screening may be reduced, particularly given the difficulty in detecting asymptomatic infections. Therefore, transmission of MERS-CoV outside health-care settings should be expected to continue until zoonotic spillover from dromedaries can be interrupted.</p></sec></body><back><ack id="mxz009-ack"><title>ACKNOWLEDGMENTS</title><p>Author affiliations: Centre for Global Health, Institut Pasteur, Paris, France (Rebecca Grant); Department of Infectious Hazard Management, Health Emergencies Program, World Health Organization, Geneva, Switzerland (Rebecca Grant, Maria D. Van Kerkhove); and Infectious Hazard Management Unit, Department of Health Emergencies, World Health Organization Regional Office for the Eastern Mediterranean, Cairo, Egypt (Mamunur Rahman Malik, Amgad Elkholy).</p><p>We thank public health and animal health workers in affected and at-risk member states for their continuous work in identifying Middle East respiratory (MERS-CoV) syndrome coronavirus infections in humans and animals.</p><p>Conflict of interest: none declared.</p></ack><ref-list id="bib1"><title>REFERENCES</title><ref id="ref1"><label>1.</label><mixed-citation publication-type="book"><person-group person-group-type="author"><collab>World Health Organization</collab></person-group><source><italic toggle="yes">WHO MERS Global Summary and Assessment of Risk: August 2018</italic></source>. <publisher-loc>Geneva, Switzerland</publisher-loc>:
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|texte= A Review of Asymptomatic and Subclinical Middle East Respiratory Syndrome Coronavirus Infections
}}
Pour générer des pages wiki
HfdIndexSelect -h $EXPLOR_AREA/Data/Pmc/Corpus/RBID.i -Sk "pubmed:31781765" \
| HfdSelect -Kh $EXPLOR_AREA/Data/Pmc/Corpus/biblio.hfd \
| NlmPubMed2Wicri -a MersV1
| This area was generated with Dilib version V0.6.33. |  |