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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Virucidal Activity of World Health Organization–Recommended Formulations Against Enveloped Viruses, Including Zika, Ebola, and Emerging Coronaviruses</title><author><name sortKey="Siddharta, Anindya" sort="Siddharta, Anindya" uniqKey="Siddharta A" first="Anindya" last="Siddharta">Anindya Siddharta</name><affiliation><nlm:aff id="AF0001"><institution>Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Hannover</institution>,</nlm:aff></affiliation></author><author><name sortKey="Pfaender, Stephanie" sort="Pfaender, Stephanie" uniqKey="Pfaender S" first="Stephanie" last="Pfaender">Stephanie Pfaender</name><affiliation><nlm:aff wicri:cut=", and" id="AF0005"><institution>Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty</institution></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="AF0007"><institution>Federal Department of Home Affairs, Institute of Virology and Immunology</institution>,<addr-line>Bern and Mittelhäusern</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Vielle, Nathalie Jane" sort="Vielle, Nathalie Jane" uniqKey="Vielle N" first="Nathalie Jane" last="Vielle">Nathalie Jane Vielle</name><affiliation><nlm:aff wicri:cut=", and" id="AF0005"><institution>Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty</institution></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut=", and" id="AF0006"><institution>Graduate School for Cellular and Biomedical Sciences, University of Bern</institution></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="AF0007"><institution>Federal Department of Home Affairs, Institute of Virology and Immunology</institution>,<addr-line>Bern and Mittelhäusern</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Dijkman, Ronald" sort="Dijkman, Ronald" uniqKey="Dijkman R" first="Ronald" last="Dijkman">Ronald Dijkman</name><affiliation><nlm:aff wicri:cut=", and" id="AF0005"><institution>Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty</institution></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="AF0007"><institution>Federal Department of Home Affairs, Institute of Virology and Immunology</institution>,<addr-line>Bern and Mittelhäusern</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Friesland, Martina" sort="Friesland, Martina" uniqKey="Friesland M" first="Martina" last="Friesland">Martina Friesland</name><affiliation><nlm:aff id="AF0001"><institution>Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Hannover</institution>,</nlm:aff></affiliation></author><author><name sortKey="Becker, Britta" sort="Becker, Britta" uniqKey="Becker B" first="Britta" last="Becker">Britta Becker</name><affiliation><nlm:aff id="AF0002"><institution>Dr Brill + Partner GmbH Institute for Hygiene and Microbiology</institution>,<addr-line>Bremen</addr-line>,</nlm:aff></affiliation></author><author><name sortKey="Yang, Jaewon" sort="Yang, Jaewon" uniqKey="Yang J" first="Jaewon" last="Yang">Jaewon Yang</name><affiliation><nlm:aff id="AF0008"><institution>Applied Molecular Virology, Institut Pasteur Korea</institution>,<addr-line>Seongnam, Gyeonggi-do</addr-line>,<country>South Korea</country></nlm:aff></affiliation></author><author><name sortKey="Engelmann, Michael" sort="Engelmann, Michael" uniqKey="Engelmann M" first="Michael" last="Engelmann">Michael Engelmann</name><affiliation><nlm:aff id="AF0001"><institution>Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Hannover</institution>,</nlm:aff></affiliation></author><author><name sortKey="Todt, Daniel" sort="Todt, Daniel" uniqKey="Todt D" first="Daniel" last="Todt">Daniel Todt</name><affiliation><nlm:aff id="AF0001"><institution>Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Hannover</institution>,</nlm:aff></affiliation></author><author><name sortKey="Windisch, Marc P" sort="Windisch, Marc P" uniqKey="Windisch M" first="Marc P." last="Windisch">Marc P. Windisch</name><affiliation><nlm:aff id="AF0008"><institution>Applied Molecular Virology, Institut Pasteur Korea</institution>,<addr-line>Seongnam, Gyeonggi-do</addr-line>,<country>South Korea</country></nlm:aff></affiliation></author><author><name sortKey="Brill, Florian H" sort="Brill, Florian H" uniqKey="Brill F" first="Florian H." last="Brill">Florian H. Brill</name><affiliation><nlm:aff id="AF0002"><institution>Dr Brill + Partner GmbH Institute for Hygiene and Microbiology</institution>,<addr-line>Bremen</addr-line>,</nlm:aff></affiliation></author><author><name sortKey="Steinmann, Joerg" sort="Steinmann, Joerg" uniqKey="Steinmann J" first="Joerg" last="Steinmann">Joerg Steinmann</name><affiliation><nlm:aff wicri:cut=", and" id="AF0003"><institution>Institute of Medical Microbiology, University Hospital Essen, University Duisburg-Essen</institution></nlm:aff></affiliation></author><author><name sortKey="Steinmann, Jochen" sort="Steinmann, Jochen" uniqKey="Steinmann J" first="Jochen" last="Steinmann">Jochen Steinmann</name><affiliation><nlm:aff id="AF0002"><institution>Dr Brill + Partner GmbH Institute for Hygiene and Microbiology</institution>,<addr-line>Bremen</addr-line>,</nlm:aff></affiliation></author><author><name sortKey="Becker, Stephan" sort="Becker, Stephan" uniqKey="Becker S" first="Stephan" last="Becker">Stephan Becker</name><affiliation><nlm:aff id="AF0004"><institution>Institute for Virology, Philipps University of Marburg</institution>,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Alves, Marco P" sort="Alves, Marco P" uniqKey="Alves M" first="Marco P." last="Alves">Marco P. Alves</name><affiliation><nlm:aff wicri:cut=", and" id="AF0005"><institution>Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty</institution></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="AF0007"><institution>Federal Department of Home Affairs, Institute of Virology and Immunology</institution>,<addr-line>Bern and Mittelhäusern</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Pietschmann, Thomas" sort="Pietschmann, Thomas" uniqKey="Pietschmann T" first="Thomas" last="Pietschmann">Thomas Pietschmann</name><affiliation><nlm:aff id="AF0001"><institution>Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Hannover</institution>,</nlm:aff></affiliation></author><author><name sortKey="Eickmann, Markus" sort="Eickmann, Markus" uniqKey="Eickmann M" first="Markus" last="Eickmann">Markus Eickmann</name><affiliation><nlm:aff id="AF0004"><institution>Institute for Virology, Philipps University of Marburg</institution>,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Thiel, Volker" sort="Thiel, Volker" uniqKey="Thiel V" first="Volker" last="Thiel">Volker Thiel</name><affiliation><nlm:aff wicri:cut=", and" id="AF0005"><institution>Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty</institution></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="AF0007"><institution>Federal Department of Home Affairs, Institute of Virology and Immunology</institution>,<addr-line>Bern and Mittelhäusern</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Steinmann, Eike" sort="Steinmann, Eike" uniqKey="Steinmann E" first="Eike" last="Steinmann">Eike Steinmann</name><affiliation><nlm:aff id="AF0001"><institution>Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Hannover</institution>,</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">28453839</idno><idno type="pmc">5407053</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5407053</idno><idno type="RBID">PMC:5407053</idno><idno type="doi">10.1093/infdis/jix046</idno><date when="2017">2017</date><idno type="wicri:Area/Pmc/Corpus">000717</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000717</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Virucidal Activity of World Health Organization–Recommended Formulations Against Enveloped Viruses, Including Zika, Ebola, and Emerging Coronaviruses</title><author><name sortKey="Siddharta, Anindya" sort="Siddharta, Anindya" uniqKey="Siddharta A" first="Anindya" last="Siddharta">Anindya Siddharta</name><affiliation><nlm:aff id="AF0001"><institution>Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Hannover</institution>,</nlm:aff></affiliation></author><author><name sortKey="Pfaender, Stephanie" sort="Pfaender, Stephanie" uniqKey="Pfaender S" first="Stephanie" last="Pfaender">Stephanie Pfaender</name><affiliation><nlm:aff wicri:cut=", and" id="AF0005"><institution>Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty</institution></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="AF0007"><institution>Federal Department of Home Affairs, Institute of Virology and Immunology</institution>,<addr-line>Bern and Mittelhäusern</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Vielle, Nathalie Jane" sort="Vielle, Nathalie Jane" uniqKey="Vielle N" first="Nathalie Jane" last="Vielle">Nathalie Jane Vielle</name><affiliation><nlm:aff wicri:cut=", and" id="AF0005"><institution>Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty</institution></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut=", and" id="AF0006"><institution>Graduate School for Cellular and Biomedical Sciences, University of Bern</institution></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="AF0007"><institution>Federal Department of Home Affairs, Institute of Virology and Immunology</institution>,<addr-line>Bern and Mittelhäusern</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Dijkman, Ronald" sort="Dijkman, Ronald" uniqKey="Dijkman R" first="Ronald" last="Dijkman">Ronald Dijkman</name><affiliation><nlm:aff wicri:cut=", and" id="AF0005"><institution>Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty</institution></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="AF0007"><institution>Federal Department of Home Affairs, Institute of Virology and Immunology</institution>,<addr-line>Bern and Mittelhäusern</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Friesland, Martina" sort="Friesland, Martina" uniqKey="Friesland M" first="Martina" last="Friesland">Martina Friesland</name><affiliation><nlm:aff id="AF0001"><institution>Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Hannover</institution>,</nlm:aff></affiliation></author><author><name sortKey="Becker, Britta" sort="Becker, Britta" uniqKey="Becker B" first="Britta" last="Becker">Britta Becker</name><affiliation><nlm:aff id="AF0002"><institution>Dr Brill + Partner GmbH Institute for Hygiene and Microbiology</institution>,<addr-line>Bremen</addr-line>,</nlm:aff></affiliation></author><author><name sortKey="Yang, Jaewon" sort="Yang, Jaewon" uniqKey="Yang J" first="Jaewon" last="Yang">Jaewon Yang</name><affiliation><nlm:aff id="AF0008"><institution>Applied Molecular Virology, Institut Pasteur Korea</institution>,<addr-line>Seongnam, Gyeonggi-do</addr-line>,<country>South Korea</country></nlm:aff></affiliation></author><author><name sortKey="Engelmann, Michael" sort="Engelmann, Michael" uniqKey="Engelmann M" first="Michael" last="Engelmann">Michael Engelmann</name><affiliation><nlm:aff id="AF0001"><institution>Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Hannover</institution>,</nlm:aff></affiliation></author><author><name sortKey="Todt, Daniel" sort="Todt, Daniel" uniqKey="Todt D" first="Daniel" last="Todt">Daniel Todt</name><affiliation><nlm:aff id="AF0001"><institution>Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Hannover</institution>,</nlm:aff></affiliation></author><author><name sortKey="Windisch, Marc P" sort="Windisch, Marc P" uniqKey="Windisch M" first="Marc P." last="Windisch">Marc P. Windisch</name><affiliation><nlm:aff id="AF0008"><institution>Applied Molecular Virology, Institut Pasteur Korea</institution>,<addr-line>Seongnam, Gyeonggi-do</addr-line>,<country>South Korea</country></nlm:aff></affiliation></author><author><name sortKey="Brill, Florian H" sort="Brill, Florian H" uniqKey="Brill F" first="Florian H." last="Brill">Florian H. Brill</name><affiliation><nlm:aff id="AF0002"><institution>Dr Brill + Partner GmbH Institute for Hygiene and Microbiology</institution>,<addr-line>Bremen</addr-line>,</nlm:aff></affiliation></author><author><name sortKey="Steinmann, Joerg" sort="Steinmann, Joerg" uniqKey="Steinmann J" first="Joerg" last="Steinmann">Joerg Steinmann</name><affiliation><nlm:aff wicri:cut=", and" id="AF0003"><institution>Institute of Medical Microbiology, University Hospital Essen, University Duisburg-Essen</institution></nlm:aff></affiliation></author><author><name sortKey="Steinmann, Jochen" sort="Steinmann, Jochen" uniqKey="Steinmann J" first="Jochen" last="Steinmann">Jochen Steinmann</name><affiliation><nlm:aff id="AF0002"><institution>Dr Brill + Partner GmbH Institute for Hygiene and Microbiology</institution>,<addr-line>Bremen</addr-line>,</nlm:aff></affiliation></author><author><name sortKey="Becker, Stephan" sort="Becker, Stephan" uniqKey="Becker S" first="Stephan" last="Becker">Stephan Becker</name><affiliation><nlm:aff id="AF0004"><institution>Institute for Virology, Philipps University of Marburg</institution>,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Alves, Marco P" sort="Alves, Marco P" uniqKey="Alves M" first="Marco P." last="Alves">Marco P. Alves</name><affiliation><nlm:aff wicri:cut=", and" id="AF0005"><institution>Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty</institution></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="AF0007"><institution>Federal Department of Home Affairs, Institute of Virology and Immunology</institution>,<addr-line>Bern and Mittelhäusern</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Pietschmann, Thomas" sort="Pietschmann, Thomas" uniqKey="Pietschmann T" first="Thomas" last="Pietschmann">Thomas Pietschmann</name><affiliation><nlm:aff id="AF0001"><institution>Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Hannover</institution>,</nlm:aff></affiliation></author><author><name sortKey="Eickmann, Markus" sort="Eickmann, Markus" uniqKey="Eickmann M" first="Markus" last="Eickmann">Markus Eickmann</name><affiliation><nlm:aff id="AF0004"><institution>Institute for Virology, Philipps University of Marburg</institution>,<country>Germany</country>;</nlm:aff></affiliation></author><author><name sortKey="Thiel, Volker" sort="Thiel, Volker" uniqKey="Thiel V" first="Volker" last="Thiel">Volker Thiel</name><affiliation><nlm:aff wicri:cut=", and" id="AF0005"><institution>Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty</institution></nlm:aff></affiliation><affiliation><nlm:aff wicri:cut="; and" id="AF0007"><institution>Federal Department of Home Affairs, Institute of Virology and Immunology</institution>,<addr-line>Bern and Mittelhäusern</addr-line>,<country>Switzerland</country></nlm:aff></affiliation></author><author><name sortKey="Steinmann, Eike" sort="Steinmann, Eike" uniqKey="Steinmann E" first="Eike" last="Steinmann">Eike Steinmann</name><affiliation><nlm:aff id="AF0001"><institution>Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Hannover</institution>,</nlm:aff></affiliation></author></analytic><series><title level="j">The Journal of Infectious Diseases</title><idno type="ISSN">0022-1899</idno><idno type="eISSN">1537-6613</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Abstract</title><p>The World Health Organization (WHO) published 2 alcohol-based formulations to be used in healthcare settings and for outbreak-associated infections, but inactivation efficacies of these products have not been determined against (re-)emerging viruses. In this study, we evaluated the virucidal activity of these WHO products in a comparative analysis. Zika virus (ZIKV), Ebola virus (EBOV), severe acute respiratory syndrome coronavirus (SARS-CoV), and Middle East respiratory syndrome coronavirus (MERS-CoV) as (re-)emerging viral pathogens and other enveloped viruses could be efficiently inactivated by both WHO formulations, implicating their use in healthcare systems and viral outbreak situations.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Osterholm, Mt" uniqKey="Osterholm M">MT Osterholm</name></author><author><name sortKey="Moore, Ka" uniqKey="Moore K">KA Moore</name></author><author><name sortKey="Kelley, Ns" uniqKey="Kelley N">NS Kelley</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Steinmann, J" uniqKey="Steinmann J">J Steinmann</name></author><author><name sortKey="Becker, B" uniqKey="Becker B">B Becker</name></author><author><name sortKey="Bischoff, B" uniqKey="Bischoff B">B Bischoff</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Suchomel, M" uniqKey="Suchomel M">M Suchomel</name></author><author><name sortKey="Rotter, M" uniqKey="Rotter M">M Rotter</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Suchomel, M" uniqKey="Suchomel M">M Suchomel</name></author><author><name sortKey="Kundi, M" uniqKey="Kundi M">M Kundi</name></author><author><name sortKey="Pittet, D" uniqKey="Pittet D">D Pittet</name></author><author><name sortKey="Rotter, Ml" uniqKey="Rotter M">ML Rotter</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Steinmann, J" uniqKey="Steinmann J">J Steinmann</name></author><author><name sortKey="Becker, B" uniqKey="Becker B">B Becker</name></author><author><name sortKey="Bischoff, B" uniqKey="Bischoff B">B Bischoff</name></author><author><name sortKey="Magulski, T" uniqKey="Magulski T">T Magulski</name></author><author><name sortKey="Steinmann, J" uniqKey="Steinmann J">J Steinmann</name></author><author><name sortKey="Steinmann, E" uniqKey="Steinmann E">E Steinmann</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pietschmann, T" uniqKey="Pietschmann T">T Pietschmann</name></author><author><name sortKey="Kaul, A" uniqKey="Kaul A">A Kaul</name></author><author><name sortKey="Koutsoudakis, G" uniqKey="Koutsoudakis G">G Koutsoudakis</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Eggers, M" uniqKey="Eggers M">M Eggers</name></author><author><name sortKey="Eickmann, M" uniqKey="Eickmann M">M Eickmann</name></author><author><name sortKey="Kowalski, K" uniqKey="Kowalski K">K Kowalski</name></author><author><name sortKey="Zorn, J" uniqKey="Zorn J">J Zorn</name></author><author><name sortKey="Reimer, K" uniqKey="Reimer K">K Reimer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Watt, A" uniqKey="Watt A">A Watt</name></author><author><name sortKey="Moukambi, F" uniqKey="Moukambi F">F Moukambi</name></author><author><name sortKey="Banadyga, L" uniqKey="Banadyga L">L Banadyga</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pfaender, S" uniqKey="Pfaender S">S Pfaender</name></author><author><name sortKey="Von Hahn, T" uniqKey="Von Hahn T">T von Hahn</name></author><author><name sortKey="Steinmann, J" uniqKey="Steinmann J">J Steinmann</name></author><author><name sortKey="Ciesek, S" uniqKey="Ciesek S">S Ciesek</name></author><author><name sortKey="Steinmann, E" uniqKey="Steinmann E">E Steinmann</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Muller, Ja" uniqKey="Muller J">JA Müller</name></author><author><name sortKey="Harms, M" uniqKey="Harms M">M Harms</name></author><author><name sortKey="Schubert, A" uniqKey="Schubert A">A Schubert</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ciesek, S" uniqKey="Ciesek S">S Ciesek</name></author><author><name sortKey="Friesland, M" uniqKey="Friesland M">M Friesland</name></author><author><name sortKey="Steinmann, J" uniqKey="Steinmann J">J Steinmann</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Rabenau, Hf" uniqKey="Rabenau H">HF Rabenau</name></author><author><name sortKey="Rapp, I" uniqKey="Rapp I">I Rapp</name></author><author><name sortKey="Steinmann, J" uniqKey="Steinmann J">J Steinmann</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Klein, M" uniqKey="Klein M">M Klein</name></author><author><name sortKey="Deforest, A" uniqKey="Deforest A">A Deforest</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="brief-report"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Infect Dis</journal-id><journal-id journal-id-type="iso-abbrev">J. Infect. Dis</journal-id><journal-id journal-id-type="publisher-id">jid</journal-id><journal-title-group><journal-title>The Journal of Infectious Diseases</journal-title></journal-title-group><issn pub-type="ppub">0022-1899</issn><issn pub-type="epub">1537-6613</issn><publisher><publisher-name>Oxford University Press</publisher-name><publisher-loc>US</publisher-loc></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">28453839</article-id><article-id pub-id-type="pmc">5407053</article-id><article-id pub-id-type="doi">10.1093/infdis/jix046</article-id><article-id pub-id-type="publisher-id">jix046</article-id><article-categories><subj-group subj-group-type="heading"><subject>Brief Report</subject></subj-group></article-categories><title-group><article-title>Virucidal Activity of World Health Organization–Recommended Formulations Against Enveloped Viruses, Including Zika, Ebola, and Emerging Coronaviruses</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Siddharta</surname><given-names>Anindya</given-names></name><xref ref-type="aff" rid="AF0001"><sup>1</sup></xref><xref ref-type="author-notes" rid="fn-002"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Pfaender</surname><given-names>Stephanie</given-names></name><xref ref-type="aff" rid="AF0005"><sup>5</sup></xref><xref ref-type="aff" rid="AF0007"><sup>7</sup></xref><xref ref-type="author-notes" rid="fn-002"><sup>a</sup></xref></contrib><contrib contrib-type="author"><name><surname>Vielle</surname><given-names>Nathalie Jane</given-names></name><xref ref-type="aff" rid="AF0005"><sup>5</sup></xref><xref ref-type="aff" rid="AF0006"><sup>6</sup></xref><xref ref-type="aff" rid="AF0007"><sup>7</sup></xref></contrib><contrib contrib-type="author"><name><surname>Dijkman</surname><given-names>Ronald</given-names></name><xref ref-type="aff" rid="AF0005"><sup>5</sup></xref><xref ref-type="aff" rid="AF0007"><sup>7</sup></xref></contrib><contrib contrib-type="author"><name><surname>Friesland</surname><given-names>Martina</given-names></name><xref ref-type="aff" rid="AF0001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Becker</surname><given-names>Britta</given-names></name><xref ref-type="aff" rid="AF0002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Yang</surname><given-names>Jaewon</given-names></name><xref ref-type="aff" rid="AF0008"><sup>8</sup></xref></contrib><contrib contrib-type="author"><name><surname>Engelmann</surname><given-names>Michael</given-names></name><xref ref-type="aff" rid="AF0001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Todt</surname><given-names>Daniel</given-names></name><xref ref-type="aff" rid="AF0001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Windisch</surname><given-names>Marc P.</given-names></name><xref ref-type="aff" rid="AF0008"><sup>8</sup></xref></contrib><contrib contrib-type="author"><name><surname>Brill</surname><given-names>Florian H.</given-names></name><xref ref-type="aff" rid="AF0002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Steinmann</surname><given-names>Joerg</given-names></name><xref ref-type="aff" rid="AF0003"><sup>3</sup></xref></contrib><contrib contrib-type="author"><name><surname>Steinmann</surname><given-names>Jochen</given-names></name><xref ref-type="aff" rid="AF0002"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>Becker</surname><given-names>Stephan</given-names></name><xref ref-type="aff" rid="AF0004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Alves</surname><given-names>Marco P.</given-names></name><xref ref-type="aff" rid="AF0005"><sup>5</sup></xref><xref ref-type="aff" rid="AF0007"><sup>7</sup></xref></contrib><contrib contrib-type="author"><name><surname>Pietschmann</surname><given-names>Thomas</given-names></name><xref ref-type="aff" rid="AF0001"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>Eickmann</surname><given-names>Markus</given-names></name><xref ref-type="aff" rid="AF0004"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>Thiel</surname><given-names>Volker</given-names></name><xref ref-type="aff" rid="AF0005"><sup>5</sup></xref><xref ref-type="aff" rid="AF0007"><sup>7</sup></xref></contrib><contrib contrib-type="author" corresp="yes"><name><surname>Steinmann</surname><given-names>Eike</given-names></name><xref ref-type="aff" rid="AF0001"><sup>1</sup></xref><pmc-comment>eike.steinmann@twincore.de </pmc-comment>
</contrib></contrib-group><aff id="AF0001"><label>1</label><institution>Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Hannover</institution>,</aff><aff id="AF0002"><label>2</label><institution>Dr Brill + Partner GmbH Institute for Hygiene and Microbiology</institution>,<addr-line>Bremen</addr-line>,</aff><aff id="AF0003"><label>3</label><institution>Institute of Medical Microbiology, University Hospital Essen, University Duisburg-Essen</institution>, and</aff><aff id="AF0004"><label>4</label><institution>Institute for Virology, Philipps University of Marburg</institution>,<country>Germany</country>;</aff><aff id="AF0005"><label>5</label><institution>Department of Infectious Diseases and Pathobiology, Vetsuisse Faculty</institution>, and</aff><aff id="AF0006"><label>6</label><institution>Graduate School for Cellular and Biomedical Sciences, University of Bern</institution>, and</aff><aff id="AF0007"><label>7</label><institution>Federal Department of Home Affairs, Institute of Virology and Immunology</institution>,<addr-line>Bern and Mittelhäusern</addr-line>,<country>Switzerland</country>; and</aff><aff id="AF0008"><label>8</label><institution>Applied Molecular Virology, Institut Pasteur Korea</institution>,<addr-line>Seongnam, Gyeonggi-do</addr-line>,<country>South Korea</country></aff><author-notes><fn id="fn-002"><label>a</label><p>A. S. and S. P. contributed equally to this work.</p></fn><fn id="fn-0001"><p>Correspondence: E. Steinmann, PhD, Institute of Experimental Virology, Twincore, Centre for Experimental and Clinical Infection Research, Feodor-Lynen-Straße 7-9, 30625 Hannover, Germany (<email>eike.steinmann@twincore.de</email>).</p></fn></author-notes><pub-date pub-type="ppub"><day>15</day><month>3</month><year>2017</year></pub-date><pub-date pub-type="epub" iso-8601-date="2017-02-01"><day>01</day><month>2</month><year>2017</year></pub-date><pub-date pub-type="pmc-release"><day>01</day><month>2</month><year>2017</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>215</volume><issue>6</issue><fpage>902</fpage><lpage>906</lpage><history><date date-type="received"><day>01</day><month>12</month><year>2016</year></date><date date-type="accepted"><day>15</day><month>2</month><year>2017</year></date></history><permissions><copyright-statement>© The Author 2017. Published by Oxford University Press for the Infectious Diseases Society of America.</copyright-statement><copyright-year>2017</copyright-year><license license-type="cc-by-nc-nd" xlink:href="http://creativecommons.org/licenses/by-nc-nd/4.0/"><license-p>This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs licence (<ext-link ext-link-type="uri" xlink:href="http://creativecommons.org/licenses/by-nc-nd/4.0/">http://creativecommons.org/licenses/by-nc-nd/4.0/</ext-link>), which permits non-commercial reproduction and distribution of the work, in any medium, provided the original work is not altered or transformed in any way, and that the work is properly cited. For commercial re-use, please contact journals.permissions@oup.com</license-p></license></permissions><self-uri xlink:href="jix046.pdf"></self-uri><abstract><title>Abstract</title><p>The World Health Organization (WHO) published 2 alcohol-based formulations to be used in healthcare settings and for outbreak-associated infections, but inactivation efficacies of these products have not been determined against (re-)emerging viruses. In this study, we evaluated the virucidal activity of these WHO products in a comparative analysis. Zika virus (ZIKV), Ebola virus (EBOV), severe acute respiratory syndrome coronavirus (SARS-CoV), and Middle East respiratory syndrome coronavirus (MERS-CoV) as (re-)emerging viral pathogens and other enveloped viruses could be efficiently inactivated by both WHO formulations, implicating their use in healthcare systems and viral outbreak situations.</p></abstract><kwd-group><kwd>Zika virus</kwd><kwd>Ebola virus</kwd><kwd>WHO</kwd><kwd>SARS</kwd><kwd>MERS.</kwd></kwd-group><funding-group><award-group award-type="grant"><funding-source><named-content content-type="funder-id">Helmholtz Centre for Infection Research</named-content></funding-source></award-group><award-group award-type="grant"><funding-source><named-content content-type="funder-id">National Research Foundation</named-content><named-content content-type="funder-identifier">http://dx.doi.org/10.13039/501100001321</named-content></funding-source></award-group><award-group award-type="grant"><funding-source><named-content content-type="funder-id">Korean government</named-content></funding-source><award-id>2014K1A4A7A01074644</award-id></award-group></funding-group><counts><page-count count="5"></page-count></counts></article-meta></front><body><p>Hygienic hand antisepsis is one of the most important measures in preventing healthcare- and outbreak-associated viral infections. To reduce the spread of infections, biocides with a proven virucidal efficacy should be readily available. The World Health Organization (WHO) proposed in its 2009 <italic>Guidelines on Hand Hygiene in Health Care</italic> the use of of 2 alcohol-based hand rubs (formulation I and formulation II) for surgical and hygiene hand disinfection in healthcare settings and to reduce the transmission of pathogens by hands [<xref rid="CIT0001" ref-type="bibr">1</xref>]. However, limited data exist on the efficacy of disinfectants, including the WHO formulations, against novel viruses that have emerged during recent outbreaks in different parts of the world. Most recently, Zika virus (ZIKV), a <italic>flavivirus</italic> that was discovered originally in Africa, has raised considerable international concern. In 2013, the largest and most complex outbreak of Ebola virus (EBOV), a <italic>filovirus</italic> that spreads mainly through contact with body fluids of symptomatic patients or contaminated surfaces, occurred in West Africa [<xref rid="CIT0002" ref-type="bibr">2</xref>]. One year previously in 2012, a novel <italic>Coronavirus</italic> (CoV) named Middle East respiratory syndrome (MERS) emerged, preceded by severe acute respiratory syndrome (SARS) in 2002/2003, with both viruses causing acute respiratory diseases in humans and displaying a high case-fatality rate.</p><p>We previously evaluated the WHO formulations in a quantitative suspension test for chemical disinfectants and antiseptics in human medicine using different nonenveloped model viruses and observed that formulation I demonstrated a better activity than formulation II against these nonenveloped viruses [<xref rid="CIT0003" ref-type="bibr">3</xref>]. However, at that time neither formulation met the requirements for virucidal activity against poliovirus according to the European Guideline (EN14476) [<xref rid="CIT0003" ref-type="bibr">3</xref>] or for surgical hand treatment according to the European Norm (EN12971) [<xref rid="CIT0004" ref-type="bibr">4</xref>]. Since then, both WHO formulations have been modified with higher alcohol content and lower glycerol concentration and are now fulfilling the guideline requirements [<xref rid="CIT0005" ref-type="bibr">5</xref>, <xref rid="CIT0006" ref-type="bibr">6</xref>].</p><p>In this study, we evaluated for the first time the modified WHO-recommended alcohol-based formulations against different enveloped viruses, including emerging ZIKV, EBOV, SARS-CoV, and MERS-CoV and performed a comparative inactivation analysis of these emerging viruses and other important reference viruses.</p><sec id="s1"><title>MATERIAL AND METHODS</title><sec id="s2"><title>Cell Culture and Viral Strains</title><p>An overview of the viruses and cell culture systems used in this study is given in Supplementary Table 1. Hepatitis C virus (HCV) chimeric Jc1 virus was generated in the human hepatoma cell line (Huh7.5) as previously described [<xref rid="CIT0007" ref-type="bibr">7</xref>]. The African lineage ZIKV strain (MP1751), isolated in Uganda in 1962, was propagated by using Vero-B4 cells like MERS-CoV strain EMC and SARS-CoV strain Frankfurt 1. Bovine CoV (BcoV) was produced in the human glioblastoma astrocytoma cells U373, human influenza A virus (H1N1) was produced in Madin-Darby canine kidney epithelial cells (MDCK) and modified vaccinia Ankara strain (MVA) was produced in baby hamster kidney cells (BHK-21). Ebola virus was propagated in Vero E6 cells as previously described [<xref rid="CIT0008" ref-type="bibr">8</xref>]. Ebola virus–like particles encoding a luciferase were generated using 239T cells as previously reported [<xref rid="CIT0009" ref-type="bibr">9</xref>]. In general, cell lines were cultured in Dulbecco’s modified minimal essential medium or Eagle’s minimum essential medium supplemented with 10% fetal calf serum and other additions (Supplementary Table 1).</p></sec><sec id="s3"><title>Quantitative Suspension Test and Virus Titrations</title><p>One part by volume of the test virus suspension and 1 part by volume of the organic load were mixed with 8 parts by volume of 1 of the 2 WHO formulations at different concentrations. Additional information is provided in the Supplementary Data.</p></sec><sec id="s4"><title>Statistical Analyses</title><p>Concentrations at which the formulations reached the half maximal virus inactivation effective concentration (EC<sub>50</sub>) were determined using nonlinear regression using the robust fitting method on the normalized 50% tissue culture infectious dose (TCID<sub>50</sub>) data implemented in GraphPad Prism version 6.07 for Windows. The mean TCID<sub>50</sub> of 2 individual experiments and standard deviations of means were also calculated using GraphPad Prism. Significance of differences in mean EC<sub>50</sub> obtained for the viruses between WHO formulations I and II was tested using 2-tailed Wilcoxon matched-pairs signed rank test (<italic>P</italic> < .01).</p></sec></sec><sec id="s5"><title>RESULTS</title><sec id="s6"><title>Virucidal Activity of World Health Organization Formulations Against Hepatitis C Virus and Zika Virus</title><p>Hepatitis C virus and ZIKV both belong to the family of <italic>Flaviviridae</italic> (Supplementary Table 1) but are transmitted in the environment by different routes. Whereas HCV is a blood-borne virus [<xref rid="CIT0010" ref-type="bibr">10</xref>], transmission of ZIKV occurs mainly through mosquitos, with the most important and common vectors being the <italic>Aedes</italic> genus. However, other modes of transmission, including sexual transmission, have been reported. To determine the efficacy of WHO formulations I and II against HCV and ZIKV, we incubated the 2 viruses for 30 seconds with the formulations at final concentrations ranging from 10% to 80% (<xref ref-type="fig" rid="F1">Figure 1</xref>). In the case of HCV, viral titers started to decline at a concentration of 30% with WHO formulation II and 40% with WHO formulation I and were reduced to background levels at a concentration of 60% with WHO formulation I and at 40% with WHO formulation II, respectively (<xref ref-type="fig" rid="F1">Figure 1A</xref>). As depicted in <xref ref-type="fig" rid="F1">Figure 1B</xref>, a dose-dependent reduction of viral titers was also observed for ZIKV (<xref ref-type="fig" rid="F1">Figure 1B</xref>). Importantly, viral titers of 10<sup>6</sup> TCID<sub>50</sub>/mL in the control decreased to undetectable levels with WHO formulation I at a concentration of 40%, whereas a concentration of only 30% was required for complete inactivation with WHO forumulation II.</p><fig fig-type="figure" id="F1" orientation="portrait" position="float"><label>Figure 1.</label><caption><p>Virucidal activity of World Health Organization (WHO) formulations I and II against hepatitis C virus (HCV), Zika virus (ZIKV), Middle East respiratory syndrome coronavirus (MERS-CoV), and severe acute respiratory syndrome coronavirus (SARS-CoV). <italic>A</italic>, World Health Organization formulations I and II were tested for their efficacy in inactivating HCV. The biocide concentrations ranged from 0% to 80% with an exposure time of 30 seconds. For this inactivation assay, 1 part virus and 1 part organic load were mixed with 8 parts biocide. Residual infectivity was determined by a limiting dilution assay. Viral titers are displayed as 50% tissue culture infectious dose (TCID<sub>50</sub>) values. The cytotoxicity was calculated in analogy to the determination of virus titer (TCID<sub>50</sub>/mL) and is depicted as a dashed line. The means of 2 independent experiments with standard deviations are shown. Efficacy of WHO formulations I and II against ZIKV (<italic>B</italic>), MERS-CoV (<italic>C</italic>), and SARS-CoV (<italic>D</italic>) was addressed by a quantitative suspension assay as described for panel <italic>A</italic>. Abbreviation: nd, not detected.</p></caption><graphic xlink:href="jix04601"></graphic></fig></sec><sec id="s7"><title>Susceptibility of Bovine Coronoavirus, Middle East Respiratory Syndrom Coronavirus, and Severe Acute Respiratory Syndrome Coronoavirus to World Health Organization Formulations</title><p>Next, we investigated the susceptibility of emerging respiratory CoVs against the WHO formulations in the same experimental suspension assay setup. As reference for CoVs, which can be cultivated under lower biosafety levels, we included BCoV that naturally infects cattle. As depicted in Supplementary Figure 1<italic>A</italic>, WHO formulation II at a 30% concentration was sufficient to completely inactivate BCoV, whereas for WHO formulation I higher concentrations of at least 40% were required (Supplementary Figure 1<italic>A</italic>). Similar inactivation profiles could be observed for MERS-CoV (<xref rid="F1" ref-type="fig">Figure 1C</xref>) and SARS-CoV (<xref rid="F1" ref-type="fig">Figure 1D</xref>), demonstrating a high susceptibility of these emerging CoVs to WHO formulations. Furthermore, these results implicate BCoV as a valid surrogate virus for inactivation studies with MERS-CoV and SARS-CoV.</p></sec><sec id="s8"><title>Virucidal Activity of World Health Organization Formulations Against Ebola Virus, Human Influenza A Virus, and Modified Vaccinia Ankara Strain</title><p>Work with infectious EBOV is restricted to biosafety level 4 laboratories, significantly limiting studies with these viruses. In 2014, Watt et al reported a novel life cycle modelling approach for EBOV, which can be performed at biosafety level 2 laboratories [<xref rid="CIT0009" ref-type="bibr">9</xref>]. Inactivation of these transcription- and replication-competent virus-like particles (trVLPs) with WHO formulations showed a dose-dependent reduction of trVLP reporter activity with increasing WHO formulation I and II concentrations (<xref ref-type="fig" rid="F2">Figure 2A</xref>). Next, we tested full infectious EBOV cultured at biosafety level 4 for its susceptibility to WHO formulations for potential usage in outbreak situations. Interestingly, viral titers of 10<sup>7</sup> TCID<sub>50</sub>/mL in the control were reduced to background levels at concentrations of 40% with WHO formulation II and 60% with WHO formulation I, showing again a superior virucidal activity of WHO formulation II compared with WHO formulation I (<xref ref-type="fig" rid="F2">Figure 2B</xref>). We also included the influenza A virus H1N1 in these inactivation experiments because of its importance in causing viral respiratory epidemics and pandemics. H1N1 could be inactivated at concentrations of 60% with WHO formulation I and 40% with WHO formulation II (Supplementary Figure 1<italic>B</italic>). Furthermore, MVA was studied for its susceptibility to WHO formulations because it is the chosen test virus for all enveloped viruses in the European Guideline. In line with EBOV and H1N1, similar inactivation profiles could be observed with increasing WHO formulation I and II concentrations (Supplementary Figure 1<italic>C</italic>).</p><fig fig-type="figure" id="F2" orientation="portrait" position="float"><label>Figure 2.</label><caption><p>Effect of World Health Organization formulations I and II against Ebola virus (EBOV) and comparative viral susceptibility analysis. World Health Organization formulations I and II were tested for their efficacy in inactivating EBOV transcription- and replication-competent virus-like particles (trVLPs) (<italic>A</italic>) and EBOV (<italic>B</italic>). The biocide concentrations ranged from 0% to 80% with an exposure time of 30 seconds. For this inactivation assay, 1 part virus and 1 part organic load were mixed with 8 parts of biocide. For determination of the EBOV trVLP infectivity, luciferase activity was measured 72 hours later. For EBOV, residual infectivity was determined by a limiting dilution assay. Viral titers are displayed as 50% tissue culture infectious dose (TCID<sub>50</sub>) values. The cytotoxicity was calculated in analogy to the determination of virus titer (TCID<sub>50</sub>/mL) and is depicted as a dashed line. The means of 2 independent experiments with standard deviations are shown. Normalized values of percentage inactivation of viral infectivity (<italic>y</italic>-axis) were plotted against WHO formulations I (<italic>C</italic>) or II (<italic>D</italic>) in dose-response curves (<italic>x</italic>-axis, log representation). Viruses are listed in each panel and are ranked from the most to the least stable. Normalization and nonlinear regression calculation of all data were performed using GraphPad Prism version 6.07 for Windows. Abbreviation: nd, not detected.</p></caption><graphic xlink:href="jix04602"></graphic></fig></sec><sec id="s9"><title>Comparative Inactivation Profiles for World Health Organization Formulations Against Enveloped Viruses</title><p>Based on the obtained virucidal activities of the WHO formulations against the different enveloped viruses, we next analyzed the inactivation profiles in a comparative analysis (<xref rid="F2" ref-type="fig">Figure 2C</xref> and 2D). The most susceptible viruses to the WHO formulation I were the bovine and emerging CoVs (BCoV, SARS-CoV, MERS-CoV) and ZIKV (<xref rid="F2" ref-type="fig">Figure 2C</xref>). With a shift to increasing WHO forumation I concentration, the more stable viruses included the full infectious EBOV (trVLPs excluded in this analysis) and HCV (<xref rid="F2" ref-type="fig">Figure 2C</xref>). The highest alcohol-based concentrations of WHO formulation I (>40%) were required for H1N1 and MVA, which displayed nearly identical inactivation response curves (<xref rid="F2" ref-type="fig">Figure 2C</xref>). The results for the isopropanol-based WHO formulation II are depicted in <xref rid="F2" ref-type="fig">Figure 2D</xref>; it demonstrated a similar pattern of susceptibility for the different enveloped viruses with an obvious shift toward lower concentrations (<xref rid="F2" ref-type="fig">Figure 2D</xref>). The CoVs and ZIKV showed the highest susceptibility to WHO formulation II, whereas HCV, EBOV, H1N1 and MVA demonstrated a more resistant inactivation profile (<xref rid="F2" ref-type="fig">Figure 2D</xref>). To also directly compare the performance of the 2 WHO formulations, we determined the concentrations at which the products reached the EC<sub>50</sub> (Supplementary Figure 2). World Health Organization formulation II showed a significantly higher virucidal activity against the different viruses compared with WHO formulation I (<italic>P</italic> = .008). In summary, CoVs and ZIKV showed the highest susceptibility to WHO formulations. Ebola virus and HCV were observed to be less susceptible than the CoVs, whereas H1N1 and MVA were the most stable viruses. In addition, WHO formulation II demonstrated a higher virucidal effect compared with WHO formulation I.</p></sec></sec><sec id="s10"><title>DISCUSSION</title><p>The WHO has recommended 2 formulations in <italic>Guidelines on Hand Hygiene in Health Care</italic>, a document proposing the use of cheap alcohol-based hand rubs to reduce the transmission of pathogens [<xref rid="CIT0001" ref-type="bibr">1</xref>]. We aimed in this study to analyze the virucidal efficacies of these products, particularly against emerging or re-emerging viruses that caused severe epidemics in the recent past [<xref rid="CIT0002" ref-type="bibr">2</xref>]. Importantly, both WHO formulations inactivated all tested viruses, including ZIKV, EBOV, and emerging CoVs, in a suspension test with 30-second exposure time, implicating the usability of these formulations in viral outbreak situations. In the case of ZIKV, specific viral inactivation data are lacking, and consequently disinfection guidelines are based on data obtained from other members of the <italic>flaviviruses</italic>. So far, 1 recent study by Müller et al reported that ZIKV was inactivated by classical inactivation methods including ultraviolet light [<xref rid="CIT0011" ref-type="bibr">11</xref>]. Zika virus was readily reduced in viral titers by the WHO formulations, similar to the other member of the family of <italic>Flaviviridae</italic>, HCV. These findings are supported by earlier analyses of the environmental stability and inactivation profiles of HCV, which showed strong virucidal effects of the main WHO formulation ingredients ethanol and isopropanol [<xref rid="CIT0012" ref-type="bibr">12</xref>]. For EBOV, limited data on the efficacy of virucidal products are available because these viruses require high biosafety level laboratories. The Centers for Disease Control and Prevention advises “suitable disinfectant solutions include 0.5% sodium hypochloride as well as 2% glutaraldehyde and phenolic disinfectants (0.5–3%)” for EBOV inactivation [<xref rid="CIT0013" ref-type="bibr">13</xref>]. The comparative inactivation analyses of all viruses tested revealed that the CoVs, in particular SARS-CoV, were the most susceptible viruses to WHO formulation treatment. The degree of susceptibility of the different viruses to the WHO formulation likely depends on the specific surface properties of the lipophilic envelope of the respective virus. We could show by a comparative inactivation analysis that H1N1 and MVA showed the highest stability against alcohol-based inactivation, with higher concentrations of WHO formulation I and II being required compared with CoVs, ZIKV, and EBOV. These results confirm MVA as the model surrogate virus for all enveloped viruses for testing chemical disinfectants and antiseptics in human medicine [<xref rid="CIT0008" ref-type="bibr">8</xref>]. When testing nonenveloped viruses like noro-, polio-, or adenovirus, a far higher level of resistance to both WHO formulations was observed, probably due to the more hydrophilic character of these viruses [<xref rid="CIT0003" ref-type="bibr">3</xref>, <xref rid="CIT0006" ref-type="bibr">6</xref>]. Interestingly, WHO formulation I was superior compared with WHO formulation II in inactivating these nonenveloped viruses, whereas in this study the opposite effect occurred, with WHO formulation II showing a higher virucidal activity against enveloped viruses. This discrepancy can be explained by the presence of the virus envelope, which likely renders enveloped viruses more susceptible to the isopropanol-based WHO formulation II compared with the ethanol-based WHO formulation I [<xref rid="CIT0014" ref-type="bibr">14</xref>]. Furthermore, isopropanol has 1 more carbon than ethanol, giving it greater lipophilic properties and higher virucidal activities against lipophilic viruses [<xref rid="CIT0015" ref-type="bibr">15</xref>].</p><p>In conclusion, WHO-recommended alcohol-based formulations were validated with different enveloped viruses. A strong virucidal effect against emerging pathogens, including ZIKV, EBOV, SARS-CoV, and MERS-CoV, could be demonstrated, implicating the usability of these WHO formulations in healthcare and outbreak-associated viral infections.</p></sec><sec sec-type="supplementary-material"><title>Supplementary Material</title><supplementary-material content-type="local-data" id="sup1"><label>Supplementary Data</label><media xlink:href="jix046_Supplementary_Data.zip"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material></sec></body><back><notes id="n1"><title>Notes</title><p><bold><italic>Acknowledgments.</italic></bold> We are grateful to Takaji Wakita and Jens Bukh for JFH1 and HCV isolates, to Charles Rice for Huh7.5 cells and the E9E10 monoclonal antibody, and to Thomas Hoenen for providing the EBOV trVLP system. We would like to thank Beatrice Zumkehr and Katharina Kowalski for technical assistance. Moreover, we thank all members of the Institute of Experimental Virology, Twincore, for helpful suggestions and discussions.</p><p><bold><italic>Financial support.</italic></bold> E. S. was supported by the Helmholtz Centre for Infection Research. M. P. W. and J. Y. were supported by a National Research Foundation of Korea grant funded by the Korean government (2014K1A4A7A01074644), Gyeonggi-do, KISTI, and the Institute Pasteur Ebola Task Force.</p><p><bold><italic>Potential conflicts of interest.</italic></bold> All authors: No reported conflicts. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. 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