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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Evaluation of visual triage for screening of Middle East respiratory syndrome coronavirus patients</title><author><name sortKey="Alfaraj, S H" sort="Alfaraj, S H" uniqKey="Alfaraj S" first="S. H." last="Alfaraj">S. H. Alfaraj</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Al Tawfiq, J A" sort="Al Tawfiq, J A" uniqKey="Al Tawfiq J" first="J. A." last="Al-Tawfiq">J. A. Al-Tawfiq</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Gautret, P" sort="Gautret, P" uniqKey="Gautret P" first="P." last="Gautret">P. Gautret</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Alenazi, M G" sort="Alenazi, M G" uniqKey="Alenazi M" first="M. G." last="Alenazi">M. G. Alenazi</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Asiri, A Y" sort="Asiri, A Y" uniqKey="Asiri A" first="A. Y." last="Asiri">A. Y. Asiri</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Memish, Z A" sort="Memish, Z A" uniqKey="Memish Z" first="Z. A." last="Memish">Z. A. Memish</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">30224971</idno><idno type="pmc">6138856</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6138856</idno><idno type="RBID">PMC:6138856</idno><idno type="doi">10.1016/j.nmni.2018.08.008</idno><date when="2018">2018</date><idno type="wicri:Area/Pmc/Corpus">000F36</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000F36</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Evaluation of visual triage for screening of Middle East respiratory syndrome coronavirus patients</title><author><name sortKey="Alfaraj, S H" sort="Alfaraj, S H" uniqKey="Alfaraj S" first="S. H." last="Alfaraj">S. H. Alfaraj</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Al Tawfiq, J A" sort="Al Tawfiq, J A" uniqKey="Al Tawfiq J" first="J. A." last="Al-Tawfiq">J. A. Al-Tawfiq</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Gautret, P" sort="Gautret, P" uniqKey="Gautret P" first="P." last="Gautret">P. Gautret</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Alenazi, M G" sort="Alenazi, M G" uniqKey="Alenazi M" first="M. G." last="Alenazi">M. G. Alenazi</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Asiri, A Y" sort="Asiri, A Y" uniqKey="Asiri A" first="A. Y." last="Asiri">A. Y. Asiri</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Memish, Z A" sort="Memish, Z A" uniqKey="Memish Z" first="Z. A." last="Memish">Z. A. Memish</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author></analytic><series><title level="j">New Microbes and New Infections</title><idno type="eISSN">2052-2975</idno><imprint><date when="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The emergence of Middle East respiratory syndrome coronavirus (MERS-CoV) in September 2012 in Saudi Arabia had attracted the attention of the global health community. In 2017 the Saudi Ministry of Health released a visual triage system with scoring to alert healthcare workers in emergency departments (EDs) and haemodialysis units for the possibility of occurrence of MERS-CoV infection. We performed a retrospective analysis of this visual score to determine its sensitivity and specificity. The study included all cases from 2014 to 2017 in a MERS-CoV referral centre in Riyadh, Saudi Arabia. During the study period there were a total of 2435 suspected MERS cases. Of these, 1823 (75%) tested negative and the remaining 25% tested positive for MERS-CoV by PCR assay. The application of the visual triage score found a similar percentage of MERS-CoV and non–MERS-CoV patients, with each score from 0 to 11. The percentage of patients with a cutoff score of ≥4 was 75% in patients with MERS-CoV infection and 85% in patients without MERS-CoV infection (p 0.0001). The sensitivity and specificity of this cutoff score for MERS-CoV infection were 74.1% and 18.6%, respectively. The sensitivity and specificity of the scoring system were low, and further refinement of the score is needed for better prediction of MERS-CoV infection.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Zaki, A M" uniqKey="Zaki A">A.M. Zaki</name></author><author><name sortKey="Van Boheemen, S" uniqKey="Van Boheemen S">S. van Boheemen</name></author><author><name sortKey="Bestebroer, T M" uniqKey="Bestebroer T">T.M. Bestebroer</name></author><author><name sortKey="Osterhaus, A D M E" uniqKey="Osterhaus A">A.D.M.E. Osterhaus</name></author><author><name sortKey="Fouchier, R A M" uniqKey="Fouchier R">R.A.M. Fouchier</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Al Tawfiq, J A" uniqKey="Al Tawfiq J">J.A. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">New Microbes New Infect</journal-id><journal-id journal-id-type="iso-abbrev">New Microbes New Infect</journal-id><journal-title-group><journal-title>New Microbes and New Infections</journal-title></journal-title-group><issn pub-type="epub">2052-2975</issn><publisher><publisher-name>The Author(s). Published by Elsevier Ltd.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">30224971</article-id><article-id pub-id-type="pmc">6138856</article-id><article-id pub-id-type="publisher-id">S2052-2975(18)30068-4</article-id><article-id pub-id-type="doi">10.1016/j.nmni.2018.08.008</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article</subject></subj-group></article-categories><title-group><article-title>Evaluation of visual triage for screening of Middle East respiratory syndrome coronavirus patients</article-title></title-group><contrib-group><contrib contrib-type="author" id="au1"><name><surname>Alfaraj</surname><given-names>S.H.</given-names></name><xref rid="aff1" ref-type="aff">1</xref><xref rid="aff7" ref-type="aff">7</xref></contrib><contrib contrib-type="author" id="au2"><name><surname>Al-Tawfiq</surname><given-names>J.A.</given-names></name><xref rid="aff6" ref-type="aff">6</xref><xref rid="aff8" ref-type="aff">8</xref><xref rid="aff9" ref-type="aff">9</xref></contrib><contrib contrib-type="author" id="au3"><name><surname>Gautret</surname><given-names>P.</given-names></name><xref rid="aff10" ref-type="aff">10</xref></contrib><contrib contrib-type="author" id="au4"><name><surname>Alenazi</surname><given-names>M.G.</given-names></name><xref rid="aff2" ref-type="aff">2</xref></contrib><contrib contrib-type="author" id="au5"><name><surname>Asiri</surname><given-names>A.Y.</given-names></name><xref rid="aff3" ref-type="aff">3</xref></contrib><contrib contrib-type="author" id="au6"><name><surname>Memish</surname><given-names>Z.A.</given-names></name><email>zmemish@yahoo.com</email><xref rid="aff5" ref-type="aff">5</xref><xref rid="aff4" ref-type="aff">4</xref><xref rid="cor1" ref-type="corresp">∗</xref></contrib></contrib-group><aff id="aff1"><label>1)</label>Corona Center, Infectious Diseases Division, Department of Pediatrics, Prince Mohammed Bin Abdulaziz Hospital, Ministry of Health, Saudi Arabia</aff><aff id="aff2"><label>2)</label>Pediatric Emergency Medicine, Emergency Department, Prince Mohammed Bin Abdulaziz Hospital, Ministry of Health, Saudi Arabia</aff><aff id="aff3"><label>3)</label>Critical Care Department, Prince Mohammed Bin Abdulaziz Hospital, Ministry of Health, Saudi Arabia</aff><aff id="aff4"><label>4)</label>Infectious Diseases Division, Department of Medicine, Prince Mohammed Bin Abdulaziz Hospital, Ministry of Health, Saudi Arabia</aff><aff id="aff5"><label>5)</label>College of Medicine, Alfaisal University, Riyadh, Saudi Arabia</aff><aff id="aff6"><label>6)</label>Johns Hopkins Aramco Healthcare, Dhahran, Saudi Arabia</aff><aff id="aff7"><label>7)</label>University of British Columbia, Vancouver, Canada</aff><aff id="aff8"><label>8)</label>Indiana University School of Medicine, Indianapolis, IN, USA</aff><aff id="aff9"><label>9)</label>Johns Hopkins University School of Medicine, Baltimore, MD, USA</aff><aff id="aff10"><label>10)</label>Aix-Marseille Université, Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE) UM63 CNRS 7278 IRD 198 INSERM U1095, Marseille, France</aff><author-notes><corresp id="cor1"><label>∗</label><bold>Corresponding author:</bold> Ziad A. Memish, College of Medicine, Alfaisal University, P.O. Box 54146, Riyadh 11514, Kingdom of Saudi Arabia. Tel.: +966-50-5483515; fax: +966-11-2616464. <email>zmemish@yahoo.com</email></corresp></author-notes><pub-date pub-type="pmc-release"><day>11</day><month>8</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"><month>11</month><year>2018</year></pub-date><pub-date pub-type="epub"><day>11</day><month>8</month><year>2018</year></pub-date><volume>26</volume><fpage>49</fpage><lpage>52</lpage><history><date date-type="received"><day>16</day><month>6</month><year>2018</year></date><date date-type="rev-recd"><day>7</day><month>7</month><year>2018</year></date><date date-type="accepted"><day>3</day><month>8</month><year>2018</year></date></history><permissions><copyright-statement>© 2018 The Author(s)</copyright-statement><copyright-year>2018</copyright-year><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"><p>The emergence of Middle East respiratory syndrome coronavirus (MERS-CoV) in September 2012 in Saudi Arabia had attracted the attention of the global health community. In 2017 the Saudi Ministry of Health released a visual triage system with scoring to alert healthcare workers in emergency departments (EDs) and haemodialysis units for the possibility of occurrence of MERS-CoV infection. We performed a retrospective analysis of this visual score to determine its sensitivity and specificity. The study included all cases from 2014 to 2017 in a MERS-CoV referral centre in Riyadh, Saudi Arabia. During the study period there were a total of 2435 suspected MERS cases. Of these, 1823 (75%) tested negative and the remaining 25% tested positive for MERS-CoV by PCR assay. The application of the visual triage score found a similar percentage of MERS-CoV and non–MERS-CoV patients, with each score from 0 to 11. The percentage of patients with a cutoff score of ≥4 was 75% in patients with MERS-CoV infection and 85% in patients without MERS-CoV infection (p 0.0001). The sensitivity and specificity of this cutoff score for MERS-CoV infection were 74.1% and 18.6%, respectively. The sensitivity and specificity of the scoring system were low, and further refinement of the score is needed for better prediction of MERS-CoV infection.</p></abstract><kwd-group id="kwrds0010"><title>Keywords</title><kwd>Middle East respiratory syndrome coronavirus (MERS-CoV)</kwd><kwd>Saudi Arabia</kwd><kwd>Scoring</kwd><kwd>Visual triage</kwd></kwd-group></article-meta></front><body><sec id="sec1"><title>Introduction</title><p id="p0010">The first case of Middle East respiratory syndrome coronavirus (MERS-CoV) was described in 2012 from a hospitalized patient in a private hospital in the Kingdom of Saudi Arabia <xref rid="bib1" ref-type="bibr">[1]</xref>. The disease has attracted the attention of the global heath community because it carries a high fatality rate of 40% to 60% <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>. The high case fatality rate could be an overestimate because the exact numbers of asymptomatic and mild cases were not well defined. Recent estimates indicate an overall fatality rate of 35%. Over the 4 years since the virus's discovery, there have been multiple healthcare-associated outbreaks <xref rid="bib2" ref-type="bibr">[2]</xref>, <xref rid="bib3" ref-type="bibr">[3]</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>. The main reason for these outbreaks was the difficulties in early identification of MERS-CoV confirmed cases from influenza-like illness cases, leading to inappropriate application of infection control standards and quarantine. In an effort to facilitate this task, differentiation between MERS-CoV and non–MERS-CoV cases based on epidemiologic and clinical indicators was evaluated in few studies, but with no helpful findings <xref rid="bib16" ref-type="bibr">[16]</xref>, <xref rid="bib17" ref-type="bibr">[17]</xref>, <xref rid="bib18" ref-type="bibr">[18]</xref>. A case–control analysis identified some significant predictors in univariate but not in multivariate analysis <xref rid="bib16" ref-type="bibr">[16]</xref>. In other studies, presenting symptoms were not specific for MERS-CoV infection <xref rid="bib17" ref-type="bibr">[17]</xref>, <xref rid="bib18" ref-type="bibr">[18]</xref>.</p><p id="p0015">The Saudi Ministry of Health (MoH) developed and released a visual triage system to be used by all hospitals for the early identification of patients with acute respiratory illness in EDs, dialysis units and clinics <xref rid="bib19" ref-type="bibr">[19]</xref>. In this study, we retrospectively evaluated the performance of this visual acute respiratory illness triage system for the prediction of MERS-CoV infection.</p></sec><sec id="sec2"><title>Patients and methods</title><p id="p0020">Prince Mohammed bin Abdulaziz Hospital is a referral centre for MERS-CoV patients diagnosed in the central region based in Riyadh, Saudi Arabia. The visual triage form documents the institution, unit, healthcare worker involved in the triage with name and signature, and patient contact details (<xref rid="fig1" ref-type="fig">Fig. 1</xref>). It comprises nine items classified into two sections, with one related to the patient's symptoms and signs and presentation and the other section related to the patient's potential risk of exposure to MERS-CoV, each with a defined predetermined score (<xref rid="fig1" ref-type="fig">Fig. 1</xref>). The patient's symptoms include fever, cough, shortness of breath, nausea, vomiting or diarrhea, sore throat or runny nose and the presence of underlying conditions including diabetes mellitus, chronic renal failure, coronary artery disease or heart failure. Any patient scoring ≥4 will need isolation and assessment by a physician before ruling out MERS-CoV. All admitted patients from 1 April 2014 to December 2017 who were tested for MERS-CoV were included in this study. MERS-CoV testing was done using nasopharyngeal swabs as described previously <xref rid="bib4" ref-type="bibr">[4]</xref>. MERS-CoV diagnosis was based on positive real-time reverse-transcriptase PCR as described previously <xref rid="bib4" ref-type="bibr">[4]</xref>, <xref rid="bib16" ref-type="bibr">[16]</xref>, <xref rid="bib20" ref-type="bibr">[20]</xref>.<fig id="fig1"><label>Fig. 1</label><caption><p>Visual triage form showing two sections, one related to patient presenting symptoms and signs and one related to risk of exposure to MERS-CoV. CAD, coronary artery disease; DM, diabetes mellitus; MERS-CoV, Middle East respiratory syndrome coronavirus.</p></caption><alt-text id="alttext0010">Fig. 1</alt-text><graphic xlink:href="gr1_lrg"></graphic></fig></p><p id="p0025">We calculated the triage score for each patient on the basis of the scores from Saudi MoH <xref rid="bib19" ref-type="bibr">[19]</xref> using the identified signs and symptoms. The percentage of patients with the specified score was calculated and compared between those with and without MERS-CoV infection using a chi-square test.</p><p id="p0030">We then calculated the sensitivity and specificity of the scoring scale adopted for the identification of positive cases in relation to virus detection by real-time PCR. Sensitivity and specificity were calculated, for an original cutoff value of 4. We subsequently challenged the triage scoring by increasing the values of MERS-CoV potential exposure specific items 7 to 9 by giving 6 points for factor 7 instead of 3, 4 points for factor 8 instead of 2 and 2 for factor 9 instead of 1. We then calculated sensitivity and specificity in the same manner.</p></sec><sec id="sec3"><title>Results</title><p id="p0035">During the study period from 2014 to 2017, there was a total of 2435 suspected MERS-CoV cases. Of these, 1823 cases (75%) tested negative and the remaining 25% tested positive for MERS-CoV by PCR. The application of the visual triage score resulted in a similar percentage of MERS-CoV and non–MERS-CoV patients with each score from 0 to 11 (<xref rid="fig2" ref-type="fig">Fig. 2</xref>). The percentage of patients with a cutoff score of ≥4 was 75% in patients with MERS and 85% in patients without MERS (p 0.0001). The sensitivity and specificity of this cutoff score for MERS-CoV infection were 74.1% and 18.6%, respectively. Increasing the values of items 7 to 9 and recalculating the score, as indicated above, was not discriminative as well.<fig id="fig2"><label>Fig. 2</label><caption><p>Percentage of patients (<italic>y</italic>-axis) with specified score (<italic>x</italic>-axis) in those with (solid line) and without (dashed line) MERS-CoV infection. MERS-CoV, Middle East respiratory syndrome coronavirus.</p></caption><alt-text id="alttext0015">Fig. 2</alt-text><graphic xlink:href="gr2_lrg"></graphic></fig></p></sec><sec id="sec4"><title>Discussion</title><p id="p0040">We retrospectively evaluated the proposed Saudi MoH triage scoring system for the screening of MERS-CoV patients. During the outbreak of severe acute respiratory syndrome, one hospital expanded the isolation criteria to include all patients with undifferentiated fever with or without respiratory symptoms or chest X-ray changes <xref rid="bib21" ref-type="bibr">[21]</xref>. Differentiating patients with MERS-CoV from other non–MERS-CoV patients has been a challenge for the healthcare workers in Saudi Arabia. There are no signs, symptoms, physical findings, specific laboratory or radiologic findings that can help healthcare workers identify MERS-CoV patients <xref rid="bib17" ref-type="bibr">[17]</xref>, <xref rid="bib18" ref-type="bibr">[18]</xref>, <xref rid="bib19" ref-type="bibr">[19]</xref>. This was made clear from recent MoH data, which showed that every year more than 50,000 patients suspected to be infected with MERS-CoV were tested kingdomwide, with a yield of 0.7% positivity <xref rid="bib22" ref-type="bibr">[22]</xref>. This calls for regular review of MERS-CoV case definition and a reevaluation of the visual triage scoring to ensure its accuracy and to avoid clogging isolation rooms and exhausting MoH financial resources by excessive testing of suspected MERS-CoV cases. In addition, it is important to have healthcare organizations ready to identify and isolate patients with suspected MERS-CoV. In a recent study evaluating the readiness of hospitals in the United States, 42 specific drills for patients with possible MERS-CoV infection were conducted in New York City <xref rid="bib23" ref-type="bibr">[23]</xref>. The drills revealed variable identification of potentially infectious patients and implementation of appropriate infection control measures <xref rid="bib23" ref-type="bibr">[23]</xref>.</p><p id="p0045">Rever-transcriptase PCR testing for MERS-CoV is the reference standard test for MERS-CoV, and in the Kingdom of Saudi Arabia, the MoH assigned five regional laboratories for testing all samples (Makkah, Madinah, Jeddah, Riyadh and Dammam). When samples are collected from the same city where a laboratory is located, it takes an average of a full day for the result, while samples from outside the city will take 1.5 days, and from one region to another, it will take 2 days. In the setting of crowded EDs, limited numbers of isolation rooms and the need to rapidly decide on contact tracing and intervention for contacts of positive patients, this time frame is potentially long.</p><p id="p0050">To address this concern and to avoid a huge backlog of patients in the ED, two strategies are needed. First, the case definition needs to be revised after careful review of available data to the MoH for 5 years. Second, we must invest in developing highly sensitive and specific point-of-care testing in EDs and haemodialysis units where the results will be available in 1 to 2 hours <xref rid="bib24" ref-type="bibr">[24]</xref>, <xref rid="bib25" ref-type="bibr">[25]</xref>, <xref rid="bib26" ref-type="bibr">[26]</xref>. Emerging diseases with regional and international implications need to be addressed in a consultative format involving all stakeholders locally, regionally and internationally.</p><p id="p0055">The current study, conducted on a large number of patients, showed that clinical scoring is not predictive of MERS infection. Our results are robust and confirm that MERS cannot be distinguished from other respiratory infections on the basis of risk factors and clinical features. Thus, all patients with nonspecific symptoms in a MERS-endemic area will have to be isolated until MERS can be ruled out by PCR testing. This strategy has important consequences in terms of public health, notably in order to limit the transmission of MERS in the healthcare setting. This is particularly relevant in countries where access to rapid diagnosis is scarce. Meanwhile, until point-of-care MERS-CoV testing is made available, triage of patients on the basis of the current MoH triage score should be revised to a robust scoring system.</p><p id="p0060">The current study has few limitations. This is a retrospective study, and thus the exact application of the findings on new cases might not be generalizable. The study was performed in a MERS-CoV referral centre, and the applicability of the findings to patients being seen in the ED therefore might not be accurate. 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