Clinical and Epidemiologic Characteristics of Spreaders of Middle East Respiratory Syndrome Coronavirus during the 2015 Outbreak in Korea
Identifieur interne : 000E70 ( Pmc/Corpus ); précédent : 000E69; suivant : 000E71Clinical and Epidemiologic Characteristics of Spreaders of Middle East Respiratory Syndrome Coronavirus during the 2015 Outbreak in Korea
Auteurs : Chang Kyung Kang ; Kyoung-Ho Song ; Pyoeng Gyun Choe ; Wan Beom Park ; Ji Hwan Bang ; Eu Suk Kim ; Sang Won Park ; Hong Bin Kim ; Nam Joong Kim ; Sung-Il Cho ; Jong-Koo Lee ; Myoung-Don OhSource :
- Journal of Korean Medical Science [ 1011-8934 ] ; 2017.
Abstract
Nosocomial transmission is an important characteristic of Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infection. Risk factors for transmission of MERS-CoV in healthcare settings are not well defined. During the Korean outbreak in 2015, 186 patients had laboratory-confirmed MERS-CoV infection. Those suspected as a source of viral transmission were categorized into the spreader groups (super-spreader [n = 5] and usual-spreader [n = 10]) and compared to the non-spreader group (n = 171). Body temperature of ≥ 38.5°C (adjusted odds ratio [aOR], 5.54; 95% confidence interval [CI], 1.38–22.30;
Url:
DOI: 10.3346/jkms.2017.32.5.744
PubMed: 28378546
PubMed Central: 5383605
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Clinical and Epidemiologic Characteristics of Spreaders of Middle East Respiratory Syndrome Coronavirus during the 2015 Outbreak in Korea</title><author><name sortKey="Kang, Chang Kyung" sort="Kang, Chang Kyung" uniqKey="Kang C" first="Chang Kyung" last="Kang">Chang Kyung Kang</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Song, Kyoung Ho" sort="Song, Kyoung Ho" uniqKey="Song K" first="Kyoung-Ho" last="Song">Kyoung-Ho Song</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Choe, Pyoeng Gyun" sort="Choe, Pyoeng Gyun" uniqKey="Choe P" first="Pyoeng Gyun" last="Choe">Pyoeng Gyun Choe</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Park, Wan Beom" sort="Park, Wan Beom" uniqKey="Park W" first="Wan Beom" last="Park">Wan Beom Park</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Bang, Ji Hwan" sort="Bang, Ji Hwan" uniqKey="Bang J" first="Ji Hwan" last="Bang">Ji Hwan Bang</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Kim, Eu Suk" sort="Kim, Eu Suk" uniqKey="Kim E" first="Eu Suk" last="Kim">Eu Suk Kim</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Park, Sang Won" sort="Park, Sang Won" uniqKey="Park S" first="Sang Won" last="Park">Sang Won Park</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Kim, Hong Bin" sort="Kim, Hong Bin" uniqKey="Kim H" first="Hong Bin" last="Kim">Hong Bin Kim</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Kim, Nam Joong" sort="Kim, Nam Joong" uniqKey="Kim N" first="Nam Joong" last="Kim">Nam Joong Kim</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Cho, Sung Il" sort="Cho, Sung Il" uniqKey="Cho S" first="Sung-Il" last="Cho">Sung-Il Cho</name><affiliation><nlm:aff id="A2">JW Lee Center for Global Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation><affiliation><nlm:aff id="A3">Graduate School of Public Health and Institute of Health and Environment, Seoul National University, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Lee, Jong Koo" sort="Lee, Jong Koo" uniqKey="Lee J" first="Jong-Koo" last="Lee">Jong-Koo Lee</name><affiliation><nlm:aff id="A2">JW Lee Center for Global Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation><affiliation><nlm:aff id="A3">Graduate School of Public Health and Institute of Health and Environment, Seoul National University, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Oh, Myoung Don" sort="Oh, Myoung Don" uniqKey="Oh M" first="Myoung-Don" last="Oh">Myoung-Don Oh</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation><affiliation><nlm:aff id="A2">JW Lee Center for Global Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">28378546</idno><idno type="pmc">5383605</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5383605</idno><idno type="RBID">PMC:5383605</idno><idno type="doi">10.3346/jkms.2017.32.5.744</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">000E70</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000E70</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Clinical and Epidemiologic Characteristics of Spreaders of Middle East Respiratory Syndrome Coronavirus during the 2015 Outbreak in Korea</title><author><name sortKey="Kang, Chang Kyung" sort="Kang, Chang Kyung" uniqKey="Kang C" first="Chang Kyung" last="Kang">Chang Kyung Kang</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Song, Kyoung Ho" sort="Song, Kyoung Ho" uniqKey="Song K" first="Kyoung-Ho" last="Song">Kyoung-Ho Song</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Choe, Pyoeng Gyun" sort="Choe, Pyoeng Gyun" uniqKey="Choe P" first="Pyoeng Gyun" last="Choe">Pyoeng Gyun Choe</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Park, Wan Beom" sort="Park, Wan Beom" uniqKey="Park W" first="Wan Beom" last="Park">Wan Beom Park</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Bang, Ji Hwan" sort="Bang, Ji Hwan" uniqKey="Bang J" first="Ji Hwan" last="Bang">Ji Hwan Bang</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Kim, Eu Suk" sort="Kim, Eu Suk" uniqKey="Kim E" first="Eu Suk" last="Kim">Eu Suk Kim</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Park, Sang Won" sort="Park, Sang Won" uniqKey="Park S" first="Sang Won" last="Park">Sang Won Park</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Kim, Hong Bin" sort="Kim, Hong Bin" uniqKey="Kim H" first="Hong Bin" last="Kim">Hong Bin Kim</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Kim, Nam Joong" sort="Kim, Nam Joong" uniqKey="Kim N" first="Nam Joong" last="Kim">Nam Joong Kim</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Cho, Sung Il" sort="Cho, Sung Il" uniqKey="Cho S" first="Sung-Il" last="Cho">Sung-Il Cho</name><affiliation><nlm:aff id="A2">JW Lee Center for Global Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation><affiliation><nlm:aff id="A3">Graduate School of Public Health and Institute of Health and Environment, Seoul National University, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Lee, Jong Koo" sort="Lee, Jong Koo" uniqKey="Lee J" first="Jong-Koo" last="Lee">Jong-Koo Lee</name><affiliation><nlm:aff id="A2">JW Lee Center for Global Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation><affiliation><nlm:aff id="A3">Graduate School of Public Health and Institute of Health and Environment, Seoul National University, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author><author><name sortKey="Oh, Myoung Don" sort="Oh, Myoung Don" uniqKey="Oh M" first="Myoung-Don" last="Oh">Myoung-Don Oh</name><affiliation><nlm:aff id="A1">Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation><affiliation><nlm:aff id="A2">JW Lee Center for Global Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</nlm:aff></affiliation></author></analytic><series><title level="j">Journal of Korean Medical Science</title><idno type="ISSN">1011-8934</idno><idno type="eISSN">1598-6357</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Nosocomial transmission is an important characteristic of Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infection. Risk factors for transmission of MERS-CoV in healthcare settings are not well defined. During the Korean outbreak in 2015, 186 patients had laboratory-confirmed MERS-CoV infection. Those suspected as a source of viral transmission were categorized into the spreader groups (super-spreader [n = 5] and usual-spreader [n = 10]) and compared to the non-spreader group (n = 171). Body temperature of ≥ 38.5°C (adjusted odds ratio [aOR], 5.54; 95% confidence interval [CI], 1.38–22.30; <italic>P</italic> = 0.016), pulmonary infiltration of ≥ 3 lung zones (aOR, 7.33; 95% CI, 1.93–27.79; <italic>P</italic> = 0.003), and a more nonisolated in-hospital days (aOR, 1.32 per 1 day; 95% CI, 1.09–1.60; <italic>P</italic> = 0.004) were significant risk factors in the spreader group. There was no different clinical factor between super-spreaders and usual-spreaders. Nonisolated in-hospital days was the only factor which tended to be higher in super-spreaders than usual-spreaders (Mean, 6.6 vs. 2.9 days; <italic>P</italic> = 0.061). Early active quarantine might help reducing the size of an outbreak.</p></div></front><back><div1 type="bibliography"><listBibl><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><author><name sortKey="Osterhaus, Ad" uniqKey="Osterhaus A">AD Osterhaus</name></author><author><name sortKey="Fouchier, Ra" uniqKey="Fouchier R">RA Fouchier</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Oh, Md" uniqKey="Oh M">MD Oh</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Chowell, G" uniqKey="Chowell G">G Chowell</name></author><author><name sortKey="Abdirizak, F" uniqKey="Abdirizak F">F Abdirizak</name></author><author><name sortKey="Lee, S" uniqKey="Lee S">S Lee</name></author><author><name sortKey="Lee, J" uniqKey="Lee J">J Lee</name></author><author><name sortKey="Jung, E" uniqKey="Jung E">E Jung</name></author><author><name sortKey="Nishiura, H" uniqKey="Nishiura H">H Nishiura</name></author><author><name sortKey="Viboud, C" uniqKey="Viboud C">C Viboud</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Oboho, Ik" uniqKey="Oboho I">IK Oboho</name></author><author><name sortKey="Tomczyk, Sm" uniqKey="Tomczyk S">SM Tomczyk</name></author><author><name sortKey="Al Asmari, Am" uniqKey="Al Asmari A">AM Al-Asmari</name></author><author><name sortKey="Banjar, Aa" uniqKey="Banjar A">AA Banjar</name></author><author><name sortKey="Al Mugti, H" uniqKey="Al Mugti H">H Al-Mugti</name></author><author><name sortKey="Aloraini, Ms" uniqKey="Aloraini M">MS Aloraini</name></author><author><name sortKey="Alkhaldi, Kz" uniqKey="Alkhaldi K">KZ Alkhaldi</name></author><author><name sortKey="Almohammadi, El" uniqKey="Almohammadi E">EL Almohammadi</name></author><author><name sortKey="Alraddadi, Bm" uniqKey="Alraddadi B">BM Alraddadi</name></author><author><name sortKey="Gerber, Si" uniqKey="Gerber S">SI Gerber</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Cho, Sy" uniqKey="Cho S">SY Cho</name></author><author><name sortKey="Kang, Jm" uniqKey="Kang J">JM Kang</name></author><author><name sortKey="Ha, Ye" uniqKey="Ha Y">YE Ha</name></author><author><name sortKey="Park, Ge" uniqKey="Park G">GE Park</name></author><author><name sortKey="Lee, Jy" uniqKey="Lee J">JY Lee</name></author><author><name sortKey="Ko, Jh" uniqKey="Ko J">JH Ko</name></author><author><name sortKey="Lee, Jy" uniqKey="Lee J">JY Lee</name></author><author><name sortKey="Kim, Jm" uniqKey="Kim J">JM Kim</name></author><author><name sortKey="Kang, Ci" uniqKey="Kang C">CI Kang</name></author><author><name sortKey="Jo, Ij" uniqKey="Jo I">IJ Jo</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Stein, Ra" uniqKey="Stein R">RA Stein</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Choi, Ws" uniqKey="Choi W">WS Choi</name></author><author><name sortKey="Kang, Ci" uniqKey="Kang C">CI Kang</name></author><author><name sortKey="Kim, Y" uniqKey="Kim Y">Y Kim</name></author><author><name sortKey="Choi, Jp" uniqKey="Choi J">JP Choi</name></author><author><name sortKey="Joh, Js" uniqKey="Joh J">JS Joh</name></author><author><name sortKey="Shin, Hs" uniqKey="Shin H">HS Shin</name></author><author><name sortKey="Kim, G" uniqKey="Kim G">G Kim</name></author><author><name sortKey="Peck, Kr" uniqKey="Peck K">KR Peck</name></author><author><name sortKey="Chung, Dr" uniqKey="Chung D">DR Chung</name></author><author><name sortKey="Kim, Ho" uniqKey="Kim H">HO Kim</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Min, Ck" uniqKey="Min C">CK Min</name></author><author><name sortKey="Cheon, S" uniqKey="Cheon S">S Cheon</name></author><author><name sortKey="Ha, Ny" uniqKey="Ha N">NY Ha</name></author><author><name sortKey="Sohn, Km" uniqKey="Sohn K">KM Sohn</name></author><author><name sortKey="Kim, Y" uniqKey="Kim Y">Y Kim</name></author><author><name sortKey="Aigerim, A" uniqKey="Aigerim A">A Aigerim</name></author><author><name sortKey="Shin, Hm" uniqKey="Shin H">HM Shin</name></author><author><name sortKey="Choi, Jy" uniqKey="Choi J">JY Choi</name></author><author><name sortKey="Inn, Ks" uniqKey="Inn K">KS Inn</name></author><author><name sortKey="Kim, Jh" uniqKey="Kim J">JH Kim</name></author></analytic></biblStruct><biblStruct></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Korean Med Sci</journal-id><journal-id journal-id-type="iso-abbrev">J. Korean Med. Sci</journal-id><journal-id journal-id-type="publisher-id">JKMS</journal-id><journal-title-group><journal-title>Journal of Korean Medical Science</journal-title></journal-title-group><issn pub-type="ppub">1011-8934</issn><issn pub-type="epub">1598-6357</issn><publisher><publisher-name>The Korean Academy of Medical Sciences</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28378546</article-id><article-id pub-id-type="pmc">5383605</article-id><article-id pub-id-type="doi">10.3346/jkms.2017.32.5.744</article-id><article-categories><subj-group subj-group-type="heading"><subject>Original Article</subject><subj-group subj-group-type="subheading"><subject>Infectious Diseases, Microbiology & Parasitology</subject></subj-group></subj-group></article-categories><title-group><article-title>Clinical and Epidemiologic Characteristics of Spreaders of Middle East Respiratory Syndrome Coronavirus during the 2015 Outbreak in Korea</article-title></title-group><contrib-group><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0003-1952-072X</contrib-id><name><surname>Kang</surname><given-names>Chang Kyung</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0002-4517-3840</contrib-id><name><surname>Song</surname><given-names>Kyoung-Ho</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0001-6794-7918</contrib-id><name><surname>Choe</surname><given-names>Pyoeng Gyun</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0003-0022-9625</contrib-id><name><surname>Park</surname><given-names>Wan Beom</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0002-7628-1182</contrib-id><name><surname>Bang</surname><given-names>Ji Hwan</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0001-7132-0157</contrib-id><name><surname>Kim</surname><given-names>Eu Suk</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0002-0550-1897</contrib-id><name><surname>Park</surname><given-names>Sang Won</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0001-6262-372X</contrib-id><name><surname>Kim</surname><given-names>Hong Bin</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0001-6793-9467</contrib-id><name><surname>Kim</surname><given-names>Nam Joong</given-names></name><xref ref-type="aff" rid="A1">1</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0003-4085-1494</contrib-id><name><surname>Cho</surname><given-names>Sung-il</given-names></name><xref ref-type="aff" rid="A2">2</xref><xref ref-type="aff" rid="A3">3</xref></contrib><contrib contrib-type="author"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0003-4833-1178</contrib-id><name><surname>Lee</surname><given-names>Jong-koo</given-names></name><xref ref-type="aff" rid="A2">2</xref><xref ref-type="aff" rid="A3">3</xref></contrib><contrib contrib-type="author" corresp="yes"><contrib-id contrib-id-type="orcid" authenticated="true">http://orcid.org/0000-0002-2344-7695</contrib-id><name><surname>Oh</surname><given-names>Myoung-don</given-names></name><xref ref-type="aff" rid="A1">1</xref><xref ref-type="aff" rid="A2">2</xref></contrib></contrib-group><aff id="A1"><label>1</label>Department of Internal Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</aff><aff id="A2"><label>2</label>JW Lee Center for Global Medicine, Seoul National University College of Medicine, Seoul,<country>Korea</country>.</aff><aff id="A3"><label>3</label>Graduate School of Public Health and Institute of Health and Environment, Seoul National University, Seoul,<country>Korea</country>.</aff><author-notes><corresp>Address for Correspondence: Myoung-don Oh, MD, PhD. Department of Internal Medicine, Seoul National University College of Medicine, 101 Daehak-ro, Jongno-gu, Seoul 03080, Korea. <email>mdohmd@snu.ac.kr</email></corresp></author-notes><pub-date pub-type="ppub"><month>5</month><year>2017</year></pub-date><pub-date pub-type="epub"><day>17</day><month>3</month><year>2017</year></pub-date><volume>32</volume><issue>5</issue><fpage>744</fpage><lpage>749</lpage><history><date date-type="received"><day>27</day><month>12</month><year>2016</year></date><date date-type="accepted"><day>30</day><month>1</month><year>2017</year></date></history><permissions><copyright-statement>© 2017 The Korean Academy of Medical Sciences.</copyright-statement><copyright-year>2017</copyright-year><license license-type="open-access" xlink:href="https://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="https://creativecommons.org/licenses/by-nc/4.0/">https://creativecommons.org/licenses/by-nc/4.0/</ext-link>) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.</license-p></license></permissions><abstract><p>Nosocomial transmission is an important characteristic of Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infection. Risk factors for transmission of MERS-CoV in healthcare settings are not well defined. During the Korean outbreak in 2015, 186 patients had laboratory-confirmed MERS-CoV infection. Those suspected as a source of viral transmission were categorized into the spreader groups (super-spreader [n = 5] and usual-spreader [n = 10]) and compared to the non-spreader group (n = 171). Body temperature of ≥ 38.5°C (adjusted odds ratio [aOR], 5.54; 95% confidence interval [CI], 1.38–22.30; <italic>P</italic> = 0.016), pulmonary infiltration of ≥ 3 lung zones (aOR, 7.33; 95% CI, 1.93–27.79; <italic>P</italic> = 0.003), and a more nonisolated in-hospital days (aOR, 1.32 per 1 day; 95% CI, 1.09–1.60; <italic>P</italic> = 0.004) were significant risk factors in the spreader group. There was no different clinical factor between super-spreaders and usual-spreaders. Nonisolated in-hospital days was the only factor which tended to be higher in super-spreaders than usual-spreaders (Mean, 6.6 vs. 2.9 days; <italic>P</italic> = 0.061). Early active quarantine might help reducing the size of an outbreak.</p></abstract><abstract abstract-type="graphical"><title>Graphical Abstract</title><p><graphic xlink:href="jkms-32-744-abf001.jpg" position="float" orientation="portrait"></graphic></p></abstract><kwd-group kwd-group-type="author"><kwd>MERS-CoV</kwd><kwd>Outbreak</kwd><kwd>Hospital Infection</kwd><kwd>Infection Transmission</kwd><kwd>Korea</kwd></kwd-group><funding-group><award-group><funding-source country="KR"><institution-wrap><institution>Korea Health Industry Development Institute</institution><institution-id institution-id-type="CrossRef">http://dx.doi.org/10.13039/501100003710</institution-id></institution-wrap></funding-source><award-id>HI15C3227</award-id></award-group></funding-group></article-meta></front><body><sec sec-type="intro"><title>INTRODUCTION</title><p>Middle East respiratory syndrome coronavirus (MERS-CoV) is a novel beta-coronavirus first identified in Saudi Arabia in 2012 (<xref rid="B1" ref-type="bibr">1</xref>). It causes severe acute respiratory infection, with a mortality rate of 36% (<xref rid="B2" ref-type="bibr">2</xref>). Most MERS-CoV infections occur in the Middle East, although travel-associated MERS cases have been reported in 17 countries outside the Middle East. As of November 3, 2016, 27 countries reported 1,813 laboratory-confirmed cases of infection with MERS-CoV, including 645 deaths, to the World Health Organization (WHO) (<xref rid="B2" ref-type="bibr">2</xref>).</p><p>In the Korean outbreak of MERS-CoV in 2015, the first known patient was a businessman returning from the Middle East. The outbreak was amplified by super-spreading events at hospitals and movement of patients between hospitals. Spreading events occurred until late June 2015, more than a month after the index patient was identified, resulting in a total of 186 patients with MERS-CoV infection and 38 fatalities, which is the largest outbreak outside the Arabian Peninsula (<xref rid="B3" ref-type="bibr">3</xref><xref rid="B4" ref-type="bibr">4</xref>). During the outbreak, almost 17,000 individuals at epidemiologic risk were quarantined, and all laboratory-confirmed cases were admitted to hospitals for isolation.</p><p>Of MERS-CoV cases, 44%–100% of individual outbreaks were linked to hospitals (<xref rid="B5" ref-type="bibr">5</xref><xref rid="B6" ref-type="bibr">6</xref>) and a nosocomial outbreak of MERS-CoV may result in a large cluster of cases, the so called “super-spreading events (<xref rid="B6" ref-type="bibr">6</xref><xref rid="B7" ref-type="bibr">7</xref>).” However, it is not known whether the spreading events are attributable to host factors such as clinical manifestations or epidemiologic factors such as duration of the nonisolated period (<xref rid="B8" ref-type="bibr">8</xref>). To understand the transmission risk of MERS-CoV in healthcare settings, we assessed the clinical and epidemiologic characteristics of non-spreaders, spreaders, and super-spreaders during the Korean outbreak.</p></sec><sec sec-type="materials|methods"><title>MATERIALS AND METHODS</title><sec><title>Patients and data collection</title><p>All laboratory-confirmed cases were admitted to government-designated hospitals, regardless of the severity of their illness. They were discharged after the resolution of all clinical symptoms and when 2 consecutive daily sputum samples were negative for MERS-CoV by real-time reverse transcription polymerase chain reaction (rRT-PCR). Laboratory diagnoses were made according to the WHO guideline (<xref rid="B9" ref-type="bibr">9</xref>).</p><p>We reviewed the publically available epidemiologic database compiled by the Korea Centers for Disease Control and Prevention (<xref rid="B3" ref-type="bibr">3</xref>) and clinical database compiled by the Korean Society of Infectious Diseases (KSID) (<xref rid="B10" ref-type="bibr">10</xref>). Infectious disease specialists who had cared for MERS patients completed case record form which KSID developed. The clinical data included demographics, clinical features, and the results of the laboratory tests. Government daily reports and local Korean news reports on the MERS outbreak were also reviewed (<xref rid="B11" ref-type="bibr">11</xref>).</p></sec><sec><title>Definitions and subgroup analyses</title><p>A spreader was defined as an index patient who was suspected of causing a secondary infection of MERS-CoV. Super-spreaders and usual-spreaders were defined as those who transmitted MERS-CoV to 6 or more and those who transmitted to fewer than 6 individuals, respectively. Nonisolated in-hospital days were defined as the sum of calendar days of the patient's hospital stay before being effectively isolated. Chest radiographs at presentation were analyzed and the number of abnormal lung zones, which were arbitrarily divided into 6 areas, was counted.</p><p>For subgroup analyses, we censored cases with symptom onset after June 7 after which stricter infection control measures were implemented by the government, such as public disclosure of the names of affected hospitals, organizing rapid response teams, and applying stronger surveillance and isolation policies (<xref rid="B12" ref-type="bibr">12</xref>). Healthcare workers were also censored in another subgroup analyses because many wore personal protective equipment, which could also confound the transmission risk.</p></sec><sec><title>Statistical analysis</title><p>Multivariate analyses in a forward stepwise manner were performed with <italic>P</italic> = 0.050 as the threshold for entering and removing variables. For all analyses, a 2-tailed <italic>P</italic> value of 0.05 was considered significant. Statistical analyses were performed with PASW for Windows (version 18 software package; SPSS, Inc., Chicago, IL, USA).</p></sec><sec><title>Ethics statement</title><p>The Institutional Review Board at the Seoul National University Hospital approved the study. The board waived the requirement for written consent (IRB registration number 1607-062-775).</p></sec></sec><sec sec-type="results"><title>RESULTS</title><sec><title>Baseline characteristics</title><p>Characteristics of 186 patients with laboratory-confirmed MERS-CoV infection are shown in <xref ref-type="table" rid="T1">Table 1</xref>. Of them, 15 patients (8.1%) transmitted MERS-CoV (the spreader group) to others, and 171 patients (91.9%) did not (the non-spreader group). Age, sex, and underlying diseases were not different between the 2 groups. Among the spreaders, 5 patients (33.3%) were super-spreaders, while 10 (66.7%) were usual-spreaders. Baseline characteristics of these 2 groups were not significantly different.</p><table-wrap id="T1" orientation="portrait" position="float"><label>Table 1</label><caption><title>Comparison of patient demographics and clinical parameters between non-spreaders and spreaders, or usual-spreaders and super-spreaders during the 2015 Korean outbreak of MERS-CoV</title></caption><alternatives><graphic xlink:href="jkms-32-744-i001"></graphic><table frame="hsides" rules="rows"><col width="36.6%" span="1"></col><col width="12.68%" span="1"></col><col width="12.68%" span="1"></col><col width="12.68%" span="1"></col><col width="12.68%" span="1"></col><col width="12.68%" span="1"></col><thead><tr><th valign="top" align="left" rowspan="2" colspan="1" style="background-color:rgb(200,199,223)">Characteristics</th><th valign="top" align="center" rowspan="2" colspan="1" style="background-color:rgb(200,199,223)">Non-spreader (n = 171)</th><th valign="top" align="center" rowspan="1" colspan="2" style="background-color:rgb(200,199,223)">Spreader (n = 15)</th><th valign="top" align="center" rowspan="1" colspan="2" style="background-color:rgb(200,199,223)"><italic>P</italic> value</th></tr><tr><th valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(200,199,223)">Usual-spreader (n = 10)</th><th valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(200,199,223)">Super-spreader (n = 5)</th><th valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(200,199,223)">Non-spreader vs. spreader</th><th valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(200,199,223)">Usual-spreader vs. super-spreader</th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">Patient characteristics</td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="right" rowspan="1" colspan="1"></td><td valign="top" align="right" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> Age, mean (± SD)</td><td valign="top" align="center" rowspan="1" colspan="1">54.4 (± 16.2)</td><td valign="top" align="center" rowspan="1" colspan="1">54.4 (± 18.0)</td><td valign="top" align="center" rowspan="1" colspan="1">50.6 (± 19.3)</td><td valign="top" align="right" rowspan="1" colspan="1">0.780</td><td valign="top" align="right" rowspan="1" colspan="1">0.689</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> Male</td><td valign="top" align="center" rowspan="1" colspan="1">99 (57.9)</td><td valign="top" align="center" rowspan="1" colspan="1">8 (80.0)</td><td valign="top" align="center" rowspan="1" colspan="1">4 (80.0)</td><td valign="top" align="right" rowspan="1" colspan="1">0.108</td><td valign="top" align="right" rowspan="1" colspan="1">1.000</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> Underlying diseases</td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="right" rowspan="1" colspan="1"></td><td valign="top" align="right" rowspan="1" colspan="1"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> DM</td><td valign="top" align="center" rowspan="1" colspan="1">33 (19.3)</td><td valign="top" align="center" rowspan="1" colspan="1">0 (0.0)</td><td valign="top" align="center" rowspan="1" colspan="1">1 (20.0)</td><td valign="top" align="right" rowspan="1" colspan="1">0.251</td><td valign="top" align="right" rowspan="1" colspan="1">1.000</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> Hypertension</td><td valign="top" align="center" rowspan="1" colspan="1">51 (29.8)</td><td valign="top" align="center" rowspan="1" colspan="1">3 (30.0)</td><td valign="top" align="center" rowspan="1" colspan="1">1 (20.0)</td><td valign="top" align="right" rowspan="1" colspan="1">0.797</td><td valign="top" align="right" rowspan="1" colspan="1">0.682</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> Chronic kidney diseases</td><td valign="top" align="center" rowspan="1" colspan="1">8 (4.7)</td><td valign="top" align="center" rowspan="1" colspan="1">1 (10.0)</td><td valign="top" align="center" rowspan="1" colspan="1">0 (0.0)</td><td valign="top" align="right" rowspan="1" colspan="1">0.732</td><td valign="top" align="right" rowspan="1" colspan="1">1.000</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> Chronic heart diseases</td><td valign="top" align="center" rowspan="1" colspan="1">15 (8.8)</td><td valign="top" align="center" rowspan="1" colspan="1">0 (0.0)</td><td valign="top" align="center" rowspan="1" colspan="1">0 (0.0)</td><td valign="top" align="right" rowspan="1" colspan="1">0.999</td><td valign="top" align="right" rowspan="1" colspan="1">NA</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> Chronic lung diseases</td><td valign="top" align="center" rowspan="1" colspan="1">17 (9.9)</td><td valign="top" align="center" rowspan="1" colspan="1">2 (20.0)</td><td valign="top" align="center" rowspan="1" colspan="1">0 (0.0)</td><td valign="top" align="right" rowspan="1" colspan="1">0.679</td><td valign="top" align="right" rowspan="1" colspan="1">0.999</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> Chronic liver diseases</td><td valign="top" align="center" rowspan="1" colspan="1">9 (5.3)</td><td valign="top" align="center" rowspan="1" colspan="1">1 (10.0)</td><td valign="top" align="center" rowspan="1" colspan="1">0 (0.0)</td><td valign="top" align="right" rowspan="1" colspan="1">0.818</td><td valign="top" align="right" rowspan="1" colspan="1">1.000</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">Clinical characteristics at presentation</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Signs and symptoms<sup>*</sup></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Fever (≥ 38.5℃)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">22 (13.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">5 (50.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">1 (20.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.009</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.280</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Systolic BP ≤ 90 mmHg</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">9 (5.3)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">2 (20.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0 (0.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.227</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.999</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Diastolic BP ≤ 60 mmHg</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">28 (16.6)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">3 (30.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">1 (20.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.329</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.682</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Respiratory rate > 24/min</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">21 (12.4)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">5 (50.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0 (0.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.034</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.999</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Cough</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">93 (55.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">9 (90.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">4 (80.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.031</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.598</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Sputum</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">63 (37.3)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">9 (90.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">2 (40.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.011</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.062</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Dyspnea</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">32 (18.9)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">6 (60.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">3 (60.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.001</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">1.000</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Myalgia</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">71 (42.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">5 (50.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">3 (60.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.399</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.715</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Headache</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">34 (20.1)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">1 (10.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">2 (40.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.991</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.199</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Diarrhea</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">32 (18.9)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">1 (10.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">2 (40.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.920</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.199</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Laboratory tests</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> WBC > 10,000 /μL or < 4,000 /μL<sup>†</sup></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">75 (46.6)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">4 (40.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">4 (80.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.617</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.165</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Platelet < 100,000 /μL<sup>†</sup></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">28 (17.4)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">3 (30.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">2 (40.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.140</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.699</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> CRP ≥ 3.0 mg/dL<sup>‡</sup></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">66 (43.4)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">8 (88.9)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">4 (80.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.008</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.653</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> BUN > 20 mg/dL<sup>§</sup></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">24 (15.4)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">4 (40.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0 (0.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.267</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.999</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Creatinine > 1.5 mg/dL<sup>§</sup></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">8 (5.1)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">1 (10.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0 (0.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.799</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">1.000</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> CXR abnormality in more than 3 lung zones<sup>∥</sup></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">17 (10.3)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">5 (50.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">2 (40.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">< 0.001</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.715</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Symptom onset to negative conversion, day, median (IQR)<sup>¶</sup></td><td valign="top" align="center" rowspan="1" colspan="1">17.0 (13.0–21.0)</td><td valign="top" align="center" rowspan="1" colspan="1">23.5 (17.8–28.3)</td><td valign="top" align="center" rowspan="1" colspan="1">32.0 (28.3–43.3)</td><td valign="top" align="right" rowspan="1" colspan="1">< 0.001</td><td valign="top" align="right" rowspan="1" colspan="1">0.129</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">Clinical outcomes</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"></td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Mechanical ventilation<sup>*</sup></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">36 (21.3)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">7 (70.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">2 (40.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.002</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.274</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Days from symptom onset to mechanical ventilation, (IQR)<sup>*</sup></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">10.0 (7.0–12.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">6.5 (5.5–8.8)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">10.5 (9.0–12.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.221</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.159</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Mortality</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">31 (18.1)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">4 (40.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">1 (20.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.162</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.447</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)"> Days from symptom onset to death, median (IQR)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">15.0 (12.0–21.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">9.0 (3.8–9.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">5.0 (5.0–5.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.032</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.504</td></tr></tbody></table></alternatives><table-wrap-foot><p>Data shown are number (%) not otherwise specified.</p><p>MERS-CoV = Middle East Respiratory Syndrome Coronavirus, SD = standard deviation, DM = diabetes mellitus, NA = not available, BP = blood pressure, WBC = white blood cell, CRP = C-reactive protein, BUN = blood urea nitrogen, CXR = chest X-ray, IQR = interquartile range.</p><p><sup>*</sup>Data were unavailable in 2 cases (1.1%); <sup>†</sup>Data were unavailable in 10 cases (5.4%); <sup>‡</sup>Data were unavailable in 20 cases (10.8%); <sup>§</sup>Data were unavailable in 15 cases (8.1%); <sup>∥</sup>Data were unavailable in 6 cases (3.2%); <sup>¶</sup>Data were unavailable in 43 cases (23.1%).</p></table-wrap-foot></table-wrap></sec><sec><title>Clinical characteristics</title><p>At presentation, patients in the spreader group were more likely than those in the non-spreader group to have a fever of ≥ 38.5°C (40.0% vs. 13.0%, <italic>P</italic> = 0.009) and a tachypnea of > 24 breaths per minute (33.3% vs. 12.4%, <italic>P</italic> = 0.034). They were also more likely to have lower respiratory manifestations such as cough, sputum, and dyspnea (86.7% vs. 55.0%, <italic>P</italic> = 0.031; 73.3% vs. 37.3%, <italic>P</italic> = 0.011; and 60.0% vs. 18.9%, <italic>P</italic> = 0.001, respectively).</p><p>On admission, elevated C-reactive protein (≥ 3.0 mg/dL) was the only laboratory parameter that was more common in the spreader than the non-spreader group (85.7% vs. 43.4%, <italic>P</italic> = 0.008). Infiltrates involving 3 or more lung zones on chest radiographs taken at presentation were more common in the spreader group than in the non-spreader group (46.7% vs. 10.3%, <italic>P</italic> < 0.001). The median days from the onset of illness to the negative conversion of sputum MERS-CoV by rRT-PCR were significantly different (27.0 vs. 17.0 days, <italic>P</italic> < 0.001).</p><p>Treatment with mechanical ventilation was required in 21.3% (36/169) of the non-spreader group and 60.0% (9/15) of the spreader group (<italic>P</italic> = 0.002). Deaths occurred in 18.1% (31/171) of the non-spreader group and 33.3% (5/15) of the spreader group (<italic>P</italic> = 0.162). Median days from symptom onset to death was significantly different (15.0 vs. 9.0 days, <italic>P</italic> = 0.032). Clinical parameters were not different between super-spreaders and usual-spreaders.</p></sec><sec><title>Epidemiologic characteristics</title><p>The course of disease spread could not be determined in 10 patients, including 5 with an unidentified source of infection and 5 with more than one possible scenario. Excluding the first imported case, the courses of disease spread could be determined in 175 patients. Of them, 173 were infected at healthcare facilities (12 hospitals, 3 clinics, and 2 ambulances). The disease was transmitted to 2 remaining patients in household settings. The date of symptom onset could not be determined in 5 patients, including 2 patients who were asymptomatic and 3 with an ambiguous onset of MERS-CoV symptoms during another illness.</p><p>Of the 15 spreaders, 5 and 8 cases were in the second- and third-chain of transmission, respectively (<xref ref-type="table" rid="T2">Table 2</xref>). Spreaders transmitted MERS-CoV from days 1 to 11 of their illness (median, 7 days; interquartile range [IQR], 5 to 8 days) (<xref ref-type="fig" rid="F1">Fig. 1A</xref>). The number of patients infected by each spreader ranged from 1 to 84 (IQR, 1 to 12).</p><table-wrap id="T2" orientation="portrait" position="float"><label>Table 2</label><caption><title>Comparison of epidemiologic characteristics between non-spreaders and spreaders, or usual-spreaders and super-spreaders during the 2015 Korean outbreak of MERS-CoV</title></caption><alternatives><graphic xlink:href="jkms-32-744-i002"></graphic><table frame="hsides" rules="rows"><col width="35.76%" span="1"></col><col width="11.39%" span="1"></col><col width="12.76%" span="1"></col><col width="12.76%" span="1"></col><col width="13.67%" span="1"></col><col width="13.67%" span="1"></col><thead><tr><th valign="top" align="left" rowspan="2" colspan="1" style="background-color:rgb(200,199,223)">Epidemiologic characteristics</th><th valign="top" align="center" rowspan="2" colspan="1" style="background-color:rgb(200,199,223)">Non-spreader (n = 171)</th><th valign="top" align="center" rowspan="1" colspan="2" style="background-color:rgb(200,199,223)">Spreader (n = 15)</th><th valign="top" align="center" rowspan="1" colspan="2" style="background-color:rgb(200,199,223)"><italic>P</italic> value</th></tr><tr><th valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(200,199,223)">Usual-spreader (n = 10)</th><th valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(200,199,223)">Super-spreader (n = 5)</th><th valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(200,199,223)">Non-spreader vs. spreader</th><th valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(200,199,223)">Usual-spreader vs. super-spreader</th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">Phase in chain of transmission</td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="center" rowspan="1" colspan="1"></td><td valign="top" align="right" rowspan="6" colspan="1">0.003</td><td valign="top" align="right" rowspan="6" colspan="1">0.058</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> Primary</td><td valign="top" align="center" rowspan="1" colspan="1">0 (0.0)</td><td valign="top" align="center" rowspan="1" colspan="1">0 (0.0)</td><td valign="top" align="center" rowspan="1" colspan="1">1 (20.0)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> Secondary</td><td valign="top" align="center" rowspan="1" colspan="1">25 (14.6)</td><td valign="top" align="center" rowspan="1" colspan="1">2 (22.2)</td><td valign="top" align="center" rowspan="1" colspan="1">3 (60.0)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> Tertiary</td><td valign="top" align="center" rowspan="1" colspan="1">116 (67.8)</td><td valign="top" align="center" rowspan="1" colspan="1">7 (77.8)</td><td valign="top" align="center" rowspan="1" colspan="1">1 (20.0)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> Quaternary</td><td valign="top" align="center" rowspan="1" colspan="1">23 (13.5)</td><td valign="top" align="center" rowspan="1" colspan="1">0 (0.0)</td><td valign="top" align="center" rowspan="1" colspan="1">0 (0.0)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1"> Undetermined</td><td valign="top" align="center" rowspan="1" colspan="1">7 (4.1)</td><td valign="top" align="center" rowspan="1" colspan="1">1 (10.0)</td><td valign="top" align="center" rowspan="1" colspan="1">0 (0.0)</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">Symptom onset after June 7<sup>*</sup></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">48 (28.9)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">3 (30.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0 (0.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.466</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.999</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Median incubation period, day, mean (± SD)<sup>†</sup></td><td valign="top" align="center" rowspan="1" colspan="1">7.4 (± 4.5)</td><td valign="top" align="center" rowspan="1" colspan="1">7.8 (± 2.6)</td><td valign="top" align="center" rowspan="1" colspan="1">8.0 (± 5.0)</td><td valign="top" align="right" rowspan="1" colspan="1">0.716</td><td valign="top" align="right" rowspan="1" colspan="1">0.905</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">Symptom onset to isolation, day, median (IQR)<sup>*</sup></td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">2.0 (1.0–6.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">5.0 (3.8–5.8)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">8.0 (4.0–9.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.057</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.267</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Nonisolated in-hospital days, median (IQR)</td><td valign="top" align="center" rowspan="1" colspan="1">0.0 (0.0–2.0)</td><td valign="top" align="center" rowspan="1" colspan="1">2.0 (0.8–4.5)</td><td valign="top" align="center" rowspan="1" colspan="1">7.0 (4.0–9.0)</td><td valign="top" align="right" rowspan="1" colspan="1">< 0.001</td><td valign="top" align="right" rowspan="1" colspan="1">0.061</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">Nonisolated in-hospital days ≥ 2 day</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">54 (31.6)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">6 (60.0)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">5 (100.0)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.003</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.999</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Symptom onset to diagnosis, day, mean (± SD)<sup>*</sup></td><td valign="top" align="center" rowspan="1" colspan="1">6.5 (± 3.9)</td><td valign="top" align="center" rowspan="1" colspan="1">7.5 (± 2.6)</td><td valign="top" align="center" rowspan="1" colspan="1">8.8 (± 3.4)</td><td valign="top" align="right" rowspan="1" colspan="1">0.178</td><td valign="top" align="right" rowspan="1" colspan="1">0.400</td></tr></tbody></table></alternatives><table-wrap-foot><p>Data shown are number (%) not otherwise specified.</p><p>MERS-CoV = Middle East Respiratory Syndrome Coronavirus, SD = standard deviation, IQR = interquartile range.</p><p><sup>*</sup>Data were unavailable in 5 cases (2.7%); <sup>†</sup>Data were unavailable in 7 cases (3.8%).</p></table-wrap-foot></table-wrap><fig id="F1" fig-type="figure" orientation="portrait" position="float"><label>Fig. 1</label><caption><p>Epidemiologic characteristics of 2015 Korean MERS-CoV outbreak. (<bold>A</bold>) Cumulative number of infected patients according to day of illness of each spreader. When infected patients were exposed to a spreader for more than one day, the number of infected patients was equally divided by the duration (day) of exposure. Different colors denote infections transmitted by different spreaders. Note that the 5 super-spreaders transmitted the virus to 92% (161/175) of all cases. (<bold>B</bold>) Nonisolated in-hospital days according to the date of symptom onset of each patient. Two spreaders transmitted MERS-CoV to healthcare workers despite the fact that they had been isolated before their symptom onset. (<bold>C</bold>) Days from symptom onset to diagnosis according to the date of symptom onset of each patient.</p><p>MERS-CoV = Middle East Respiratory Syndrome Coronavirus.</p></caption><graphic xlink:href="jkms-32-744-g001"></graphic></fig><p>The median duration of incubation was not different between the spreader and non-spreader groups. Median nonisolated in-hospital days were 4 and 0 days in the spreader and non-spreader groups, respectively (IQR, 1 to 7 vs. 0 to 2 days, <italic>P</italic> < 0.001).</p><p>Nonisolated in-hospital days were significantly different among the non-spreader, usual-spreader, and super-spreader groups (<xref ref-type="fig" rid="F2">Fig. 2A</xref>). Nonisolated in-hospital days of spreaders were also positively associated with the total number of infected patients, and the number of infected patients per spreader (R<sup>2</sup> = 0.520 and 0.625; <italic>P</italic> = 0.068 and 0.034, respectively) (<xref ref-type="fig" rid="F2">Fig. 2B</xref>).</p><fig id="F2" fig-type="figure" orientation="portrait" position="float"><label>Fig. 2</label><caption><p>Contribution of nonisolated in-hospital days to spreading events. (<bold>A</bold>) Nonisolated in-hospital days in non-spreader, usual-spreader, and super-spreader groups. Dashed lines denote median values at each group. Data points at 0 are shown at different level for clarity. (<bold>B</bold>) Number of spreaders (S) and infected patients (I), and I/S ratio according to nonisolated in-hospital days of spreaders. There were positive correlation between nonisolated in-hospital days of spreaders and I (red broken line) or I/S ratio (green broken line).</p></caption><graphic xlink:href="jkms-32-744-g002"></graphic></fig><p>Epidemiologic characteristics of super-spreaders and usual-spreaders were not different. However, nonisolated in-hospital days tended to be higher in the super-spreader group (median, 2.0 vs. 7.0 days, <italic>P</italic> = 0.061). The median number of nonisolated in-hospital days was 1 day in patients who developed symptoms before June 7 and 0 days in patients who developed symptoms after that date (IQR, 0 to 3 vs. 0 to 1 day, <italic>P</italic> = 0.001) (<xref ref-type="fig" rid="F1">Fig. 1B</xref>, <xref ref-type="supplementary-material" rid="S1">Supplementary Table 1</xref>). Days from symptom onset to diagnosis were also significantly different between these groups (mean, 7.5 vs. 4.6, <italic>P</italic> < 0.001) (<xref ref-type="fig" rid="F1">Fig. 1C</xref>, <xref ref-type="supplementary-material" rid="S1">Supplementary Table 1</xref>).</p></sec><sec><title>Risk factors for transmission</title><p>In multivariate analysis, fever (≥ 38.5°C) (adjusted odds ratio [aOR], 5.54; 95% confidence interval [CI], 1.38–22.30; <italic>P</italic> = 0.016), chest infiltrates in more than 3 lung zones (aOR, 7.33; 95% CI, 1.93–27.79; <italic>P</italic> = 0.003), and a longer nonisolated in-hospital day (aOR, 1.32 per 1 day; 95% CI, 1.09–1.60; <italic>P</italic> = 0.004) were independently associated with the spreader group vs. the non-spreader group (<xref ref-type="table" rid="T3">Table 3</xref>). Further inclusion of other variables did not result in additional significance.</p><table-wrap id="T3" orientation="portrait" position="float"><label>Table 3</label><caption><title>Forward stepwise multivariate analysis for risk factors for transmission of MERS-CoV</title></caption><alternatives><graphic xlink:href="jkms-32-744-i003"></graphic><table frame="hsides" rules="rows"><col width="27.5%" span="1"></col><col width="18.13%" span="1"></col><col width="18.13%" span="1"></col><col width="18.13%" span="1"></col><col width="18.13%" span="1"></col><thead><tr><th valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(200,199,223)">Variables</th><th valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(200,199,223)">Non-spreader (n = 171)</th><th valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(200,199,223)">Spreader (n = 15)</th><th valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(200,199,223)">aOR (95% CI)</th><th valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(200,199,223)"><italic>P</italic> value</th></tr></thead><tbody><tr><td valign="top" align="left" rowspan="1" colspan="1">Fever (≥ 38.5℃)</td><td valign="top" align="center" rowspan="1" colspan="1">22 (13.0)</td><td valign="top" align="center" rowspan="1" colspan="1">6 (40.0)</td><td valign="top" align="center" rowspan="1" colspan="1">5.54 (1.38–22.30)</td><td valign="top" align="right" rowspan="1" colspan="1">0.016</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">CXR abnormality in more than 3 lung zones</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">17 (10.3)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">7 (46.7)</td><td valign="top" align="center" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">7.33 (1.93–27.79)</td><td valign="top" align="right" rowspan="1" colspan="1" style="background-color:rgb(225,224,237)">0.003</td></tr><tr><td valign="top" align="left" rowspan="1" colspan="1">Nonisolated in-hospital days, median (IQR)</td><td valign="top" align="center" rowspan="1" colspan="1">0.0 (0.0–2.0)</td><td valign="top" align="center" rowspan="1" colspan="1">4.0 (1.0–7.0)</td><td valign="top" align="center" rowspan="1" colspan="1">1.32 (1.09–1.60)</td><td valign="top" align="right" rowspan="1" colspan="1">0.004</td></tr></tbody></table></alternatives><table-wrap-foot><p>Data shown are number (%).</p><p>MERS-CoV = Middle East Respiratory Syndrome Coronavirus, aOR = adjusted odds ratio, CI = confidence interval, CXR = chest X-ray, IQR = interquartile range.</p></table-wrap-foot></table-wrap><p>When we censored the data on symptom onset after June 7 or unknown onset (n = 56), dyspnea (aOR, 4.38; 95% CI, 1.13–16.90; <italic>P</italic> = 0.032), and a more nonisolated in-hospital days (aOR, 1.31 per 1 day; 95% CI, 1.07–1.60; <italic>P</italic> = 0.009) were associated with the spreader group (<xref ref-type="supplementary-material" rid="S2">Supplementary Tables 2</xref> and <xref ref-type="supplementary-material" rid="S3">3</xref>).</p><p>When healthcare workers were censored (n = 39), chest X-ray abnormalities in more than 3 lung zones (aOR, 4.97; 95% CI, 1.28–19.35; <italic>P</italic> = 0.021), and a more nonisolated in-hospital days (aOR, 5.63 per 1 day; 95% CI, 1.10–28.75; <italic>P</italic> = 0.038) were associated with the spreader groups (<xref ref-type="supplementary-material" rid="S4">Supplementary Tables 4</xref> and <xref ref-type="supplementary-material" rid="S5">5</xref>).</p></sec></sec><sec sec-type="discussion"><title>DISCUSSION</title><p>Hospital outbreaks were the defining characteristic of the Korean MERS-CoV outbreak in 2015. In this study, spreaders more frequently had high fever, more extensive infiltrates on chest radiographs, and a longer time to negative conversion of MERS-CoV rRT-PCR than non-spreaders, all suggesting more severe pneumonia. The spreader group had a significantly longer duration of nonisolated in-hospital days than the non-spreader groups.</p><p>Clinical parameters did not differ between super-spreaders and usual-spreaders, whereas nonisolated in-hospital days were substantially different between these 2 groups. These data suggest that large hospital outbreaks or super-spreading events may not be attributable to clinical manifestations, but to delay in isolation.</p><p>Spreaders transmitted MERS-CoV between days 1 and 11 of their illness. Of note, even a 1- or 2-day delay in isolating patients led secondary infections, with a peak of cumulative number on the seventh day of illness. These findings imply that MERS-CoV could be transmitted frequently during the early course of the disease. A recent virus shedding study showed that MERS-CoV titers in sputum samples were around 10<sup>8</sup> copies per milliliter as early as 3 days after symptom onset, while the viral shedding kinetics of the SARS-CoV infection was an inverted V shape, with its sharp peak around day 10 (<xref rid="B13" ref-type="bibr">13</xref>). These findings suggest that control of a MERS-CoV outbreak would be more difficult than that of a SARS-CoV outbreak. Considering that the shortest incubation period of MERS-CoV infection is 2 days and that patients may transmit the disease with a high viral load even in the early course of their illness, early detection and isolation of patients is imperative to control an outbreak of MERS-CoV.</p><p>A standard approach to control an outbreak begins with identifying all exposed individuals and assessing them for close contact, followed by quarantine. However, this approach is labor-intensive and time-consuming, especially when many individuals are exposed. Moreover, identification of all exposed individuals is difficult, because many, such as visitors and family members, may not be registered with hospitals. Indeed, 43.2% of the patients in Korea during the 2015 outbreak had not been identified as exposed individuals and were not monitored (<xref rid="B14" ref-type="bibr">14</xref>). Our experience suggests that quarantining all exposed individuals first, followed by an assessment of and monitoring of their close contacts may shorten the delay in isolating MERS patients, especially in healthcare settings.</p><p>Days of nonisolated in-hospital stay and symptom onset to diagnosis were significantly longer in patients who developed symptoms before June 7 than in patients who did after that date. The last super-spreader developed symptoms on June 5, and no additional super-spreading events occurred after June 7. All advocate the necessity of early adoption of an aggressive isolation policy.</p><p>Since this was an analysis of a single outbreak, it should be interpreted with caution. Additionally, although we analyzed the severity of symptom or chest infiltrations and time to negative conversion of MERS-CoV rRT-PCR, lack of each patient's serial viral load titers limited a direct evaluation of the degree of viral shedding, which could be another limitation.</p><p>In conclusion, high fever, more extensive chest infiltrates, and delay in isolation were associated with the transmission of MERS-CoV. Nonisolated in-hospital days were the only parameter that tended to be associated with super-spreaders compared with usual-spreaders. Early active quarantine might help control a future outbreak of MERS.</p></sec></body><back><fn-group><fn fn-type="supported-by"><p><bold>Funding:</bold> This work was supported by a grant from the Korean Healthcare Technology R & D Project through the Korea Health Industry Development Institute (KHIDI), funded by the Ministry of Health and Welfare, Korea (Grant No. HI15C3227).</p></fn><fn fn-type="COI-statement"><p><bold>DISCLOSURE:</bold> The authors have no potential conflicts of interest to disclose.</p></fn><fn fn-type="con"><p><bold>AUTHOR CONTRIBUTION:</bold> Conceptualization: Oh MD. Data curation: Kang CK, Choe PG. Investigation: Kang CK, Song KH, Choe PG, Park WB, Bang JH, Kim ES, Park SW, Kim HB, Kim NJ, Cho SI, Lee JK, Oh MD. Writing - original draft: Kang CK, Oh MD. 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mime-subtype="pdf" xlink:href="jkms-32-744-s001.pdf" orientation="portrait" id="d35e1865" position="anchor"></media></supplementary-material><supplementary-material content-type="local-data" id="S2"><caption><title>Supplementary Table 2</title><p>Comparison of clinical features and epidemiologic characteristics between the non-spreaders and the spreaders during the 2015 Korean outbreak of MERS-CoV, after censoring patients who had developed symptoms later than June 7 or unknown symptom onset (n = 56)</p></caption><media mimetype="application" mime-subtype="pdf" xlink:href="jkms-32-744-s002.pdf" orientation="portrait" id="d35e1872" position="anchor"></media></supplementary-material><supplementary-material content-type="local-data" id="S3"><caption><title>Supplementary Table 3</title><p>Forward stepwise multivariate analysis for risk factors for spreader of MERS-CoV, after censoring patients who had developed their symptom later than June 7</p></caption><media mimetype="application" mime-subtype="pdf" xlink:href="jkms-32-744-s003.pdf" orientation="portrait" id="d35e1879" position="anchor"></media></supplementary-material><supplementary-material content-type="local-data" id="S4"><caption><title>Supplementary Table 4</title><p>Clinical features and epidemiologic characteristics in non-spreaders, usual-spreaders, and super-spreaders during the 2015 Korean outbreak of MERS-CoV, after censoring healthcare workers (n = 39)</p></caption><media mimetype="application" mime-subtype="pdf" xlink:href="jkms-32-744-s004.pdf" orientation="portrait" id="d35e1886" position="anchor"></media></supplementary-material><supplementary-material content-type="local-data" id="S5"><caption><title>Supplementary Table 5</title><p>Forward stepwise multivariate analysis for risk factors for spreader of MERS-CoV, after censoring healthcare workers</p></caption><media mimetype="application" mime-subtype="pdf" xlink:href="jkms-32-744-s005.pdf" orientation="portrait" id="d35e1893" 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