Susceptibility of Chikungunya Virus to Inactivation by Heat and Commercially and World Health Organization-Recommended Biocides
Identifieur interne : 000534 ( Pmc/Corpus ); précédent : 000533; suivant : 000535Susceptibility of Chikungunya Virus to Inactivation by Heat and Commercially and World Health Organization-Recommended Biocides
Auteurs : Sergej Franz ; Martina Friesland ; Vânia Passos ; Daniel Todt ; Graham Simmons ; Christine Goffinet ; Eike SteinmannSource :
- The Journal of Infectious Diseases [ 0022-1899 ] ; 2018.
Abstract
Despite increasing clinical relevance of Chikungunya virus (CHIKV) infection, caused by a rapidly emerging pathogen, recommended guidelines for its inactivation do not exist. In this study, we investigated the susceptibility of CHIKV to inactivation by heat and commercially available hand, surface, and World Health Organization-recommended disinfectants to define CHIKV prevention protocols for healthcare systems.
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DOI: 10.1093/infdis/jiy359
PubMed: 29917109
PubMed Central: 6151073
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Susceptibility of Chikungunya Virus to Inactivation by Heat and Commercially and World Health Organization-Recommended Biocides</title><author><name sortKey="Franz, Sergej" sort="Franz, Sergej" uniqKey="Franz S" first="Sergej" last="Franz">Sergej Franz</name><affiliation><nlm:aff id="AF0001">Institute of Experimental Virology, TWINCORE Centre for Experimental and Clinical Infection Research (a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research), Hannover, Germany</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">Institute of Experimental Virology, TWINCORE Centre for Experimental and Clinical Infection Research (a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research), Hannover, Germany</nlm:aff></affiliation></author><author><name sortKey="Passos, Vania" sort="Passos, Vania" uniqKey="Passos V" first="Vânia" last="Passos">Vânia Passos</name><affiliation><nlm:aff id="AF0001">Institute of Experimental Virology, TWINCORE Centre for Experimental and Clinical Infection Research (a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research), Hannover, Germany</nlm:aff></affiliation><affiliation><nlm:aff id="AF0002">Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Portugal</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">Institute of Experimental Virology, TWINCORE Centre for Experimental and Clinical Infection Research (a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research), Hannover, Germany</nlm:aff></affiliation><affiliation><nlm:aff id="AF0003">Department of Molecular and Medical Virology, Ruhr-University Bochum, Germany</nlm:aff></affiliation></author><author><name sortKey="Simmons, Graham" sort="Simmons, Graham" uniqKey="Simmons G" first="Graham" last="Simmons">Graham Simmons</name><affiliation><nlm:aff id="AF0004">Blood Systems Research Institute, San Francisco, California</nlm:aff></affiliation><affiliation><nlm:aff id="AF0005">Department of Laboratory Medicine, University of California, San Francisco</nlm:aff></affiliation></author><author><name sortKey="Goffinet, Christine" sort="Goffinet, Christine" uniqKey="Goffinet C" first="Christine" last="Goffinet">Christine Goffinet</name><affiliation><nlm:aff id="AF0001">Institute of Experimental Virology, TWINCORE Centre for Experimental and Clinical Infection Research (a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research), Hannover, Germany</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">Institute of Experimental Virology, TWINCORE Centre for Experimental and Clinical Infection Research (a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research), Hannover, Germany</nlm:aff></affiliation><affiliation><nlm:aff id="AF0003">Department of Molecular and Medical Virology, Ruhr-University Bochum, Germany</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">29917109</idno><idno type="pmc">6151073</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6151073</idno><idno type="RBID">PMC:6151073</idno><idno type="doi">10.1093/infdis/jiy359</idno><date when="2018">2018</date><idno type="wicri:Area/Pmc/Corpus">000534</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000534</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Susceptibility of Chikungunya Virus to Inactivation by Heat and Commercially and World Health Organization-Recommended Biocides</title><author><name sortKey="Franz, Sergej" sort="Franz, Sergej" uniqKey="Franz S" first="Sergej" last="Franz">Sergej Franz</name><affiliation><nlm:aff id="AF0001">Institute of Experimental Virology, TWINCORE Centre for Experimental and Clinical Infection Research (a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research), Hannover, Germany</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">Institute of Experimental Virology, TWINCORE Centre for Experimental and Clinical Infection Research (a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research), Hannover, Germany</nlm:aff></affiliation></author><author><name sortKey="Passos, Vania" sort="Passos, Vania" uniqKey="Passos V" first="Vânia" last="Passos">Vânia Passos</name><affiliation><nlm:aff id="AF0001">Institute of Experimental Virology, TWINCORE Centre for Experimental and Clinical Infection Research (a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research), Hannover, Germany</nlm:aff></affiliation><affiliation><nlm:aff id="AF0002">Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Portugal</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">Institute of Experimental Virology, TWINCORE Centre for Experimental and Clinical Infection Research (a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research), Hannover, Germany</nlm:aff></affiliation><affiliation><nlm:aff id="AF0003">Department of Molecular and Medical Virology, Ruhr-University Bochum, Germany</nlm:aff></affiliation></author><author><name sortKey="Simmons, Graham" sort="Simmons, Graham" uniqKey="Simmons G" first="Graham" last="Simmons">Graham Simmons</name><affiliation><nlm:aff id="AF0004">Blood Systems Research Institute, San Francisco, California</nlm:aff></affiliation><affiliation><nlm:aff id="AF0005">Department of Laboratory Medicine, University of California, San Francisco</nlm:aff></affiliation></author><author><name sortKey="Goffinet, Christine" sort="Goffinet, Christine" uniqKey="Goffinet C" first="Christine" last="Goffinet">Christine Goffinet</name><affiliation><nlm:aff id="AF0001">Institute of Experimental Virology, TWINCORE Centre for Experimental and Clinical Infection Research (a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research), Hannover, Germany</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">Institute of Experimental Virology, TWINCORE Centre for Experimental and Clinical Infection Research (a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research), Hannover, Germany</nlm:aff></affiliation><affiliation><nlm:aff id="AF0003">Department of Molecular and Medical Virology, Ruhr-University Bochum, Germany</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="2018">2018</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><title>Abstract</title><p>Despite increasing clinical relevance of Chikungunya virus (CHIKV) infection, caused by a rapidly emerging pathogen, recommended guidelines for its inactivation do not exist. In this study, we investigated the susceptibility of CHIKV to inactivation by heat and commercially available hand, surface, and World Health Organization-recommended disinfectants to define CHIKV prevention protocols for healthcare systems.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Bessaud, M" uniqKey="Bessaud M">M Bessaud</name></author><author><name sortKey="Peyrefitte, Cn" uniqKey="Peyrefitte C">CN Peyrefitte</name></author><author><name sortKey="Pastorino, Ba" uniqKey="Pastorino B">BA Pastorino</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Gardner, J" uniqKey="Gardner J">J Gardner</name></author><author><name sortKey="Rudd, Pa" uniqKey="Rudd P">PA Rudd</name></author><author><name sortKey="Prow, Na" uniqKey="Prow N">NA Prow</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Morrison, Te" uniqKey="Morrison T">TE Morrison</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tsetsarkin, Ka" uniqKey="Tsetsarkin K">KA Tsetsarkin</name></author><author><name sortKey="Vanlandingham, Dl" uniqKey="Vanlandingham D">DL Vanlandingham</name></author><author><name sortKey="Mcgee, Ce" uniqKey="Mcgee C">CE McGee</name></author><author><name sortKey="Higgs, S" uniqKey="Higgs S">S Higgs</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Vanlandingham, Dl" uniqKey="Vanlandingham D">DL Vanlandingham</name></author><author><name sortKey="Tsetsarkin, K" uniqKey="Tsetsarkin K">K Tsetsarkin</name></author><author><name sortKey="Hong, C" uniqKey="Hong C">C Hong</name></author></analytic></biblStruct><biblStruct></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="Siddharta, A" uniqKey="Siddharta A">A Siddharta</name></author><author><name sortKey="Pfaender, S" uniqKey="Pfaender S">S Pfaender</name></author><author><name sortKey="Vielle, Nj" uniqKey="Vielle N">NJ Vielle</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="Huang, Yj" uniqKey="Huang Y">YJ Huang</name></author><author><name sortKey="Hsu, Ww" uniqKey="Hsu W">WW Hsu</name></author><author><name sortKey="Higgs, S" uniqKey="Higgs S">S Higgs</name></author><author><name sortKey="Vanlandingham, Dl" uniqKey="Vanlandingham D">DL Vanlandingham</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Pastorino, B" uniqKey="Pastorino B">B Pastorino</name></author><author><name sortKey="Baronti, C" uniqKey="Baronti C">C Baronti</name></author><author><name sortKey="Gould, Ea" uniqKey="Gould E">EA Gould</name></author><author><name sortKey="Charrel, Rn" uniqKey="Charrel R">RN Charrel</name></author><author><name sortKey="De Lamballerie, X" uniqKey="De Lamballerie X">X de Lamballerie</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">29917109</article-id><article-id pub-id-type="pmc">6151073</article-id><article-id pub-id-type="doi">10.1093/infdis/jiy359</article-id><article-id pub-id-type="publisher-id">jiy359</article-id><article-categories><subj-group subj-group-type="heading"><subject>Major Articles and Brief Reports</subject><subj-group subj-group-type="category-toc-heading"><subject>Viruses</subject></subj-group></subj-group></article-categories><title-group><article-title>Susceptibility of Chikungunya Virus to Inactivation by Heat and Commercially and World Health Organization-Recommended Biocides</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Franz</surname><given-names>Sergej</given-names></name><xref ref-type="aff" rid="AF0001">1</xref></contrib><contrib contrib-type="author"><name><surname>Friesland</surname><given-names>Martina</given-names></name><xref ref-type="aff" rid="AF0001">1</xref></contrib><contrib contrib-type="author"><name><surname>Passos</surname><given-names>Vânia</given-names></name><xref ref-type="aff" rid="AF0001">1</xref><xref ref-type="aff" rid="AF0002">2</xref></contrib><contrib contrib-type="author"><name><surname>Todt</surname><given-names>Daniel</given-names></name><xref ref-type="aff" rid="AF0001">1</xref><xref ref-type="aff" rid="AF0003">3</xref></contrib><contrib contrib-type="author"><name><surname>Simmons</surname><given-names>Graham</given-names></name><xref ref-type="aff" rid="AF0004">4</xref><xref ref-type="aff" rid="AF0005">5</xref></contrib><contrib contrib-type="author"><name><surname>Goffinet</surname><given-names>Christine</given-names></name><xref ref-type="aff" rid="AF0001">1</xref><xref ref-type="author-notes" rid="fn-0100"></xref><xref ref-type="corresp" rid="c1"></xref><pmc-comment>christine.goffinet@twincore.de </pmc-comment>
</contrib><contrib contrib-type="author"><name><surname>Steinmann</surname><given-names>Eike</given-names></name><xref ref-type="aff" rid="AF0001">1</xref><xref ref-type="aff" rid="AF0003">3</xref><xref ref-type="author-notes" rid="fn-0100"></xref></contrib></contrib-group><aff id="AF0001"><label>1</label>Institute of Experimental Virology, TWINCORE Centre for Experimental and Clinical Infection Research (a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research), Hannover, Germany</aff><aff id="AF0002"><label>2</label>Instituto de Ciências Biomédicas Abel Salazar, Universidade do Porto, Portugal</aff><aff id="AF0003"><label>3</label>Department of Molecular and Medical Virology, Ruhr-University Bochum, Germany</aff><aff id="AF0004"><label>4</label>Blood Systems Research Institute, San Francisco, California</aff><aff id="AF0005"><label>5</label>Department of Laboratory Medicine, University of California, San Francisco</aff><author-notes><fn id="fn-0100"><p>contributed equally.</p></fn><corresp id="c1">Correspondence: C. Goffinet, PhD, Department of Experimental Virology, TWINCORE, Centre for Experimental and Clinical Infection Research, Feodor-Lynen-Strasse 7, 30625 Hannover, Germany (<email>christine.goffinet@twincore.de</email>).</corresp></author-notes><pub-date pub-type="ppub"><day>01</day><month>11</month><year>2018</year></pub-date><pub-date pub-type="epub" iso-8601-date="2018-06-15"><day>15</day><month>6</month><year>2018</year></pub-date><pub-date pub-type="pmc-release"><day>15</day><month>6</month><year>2018</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>218</volume><issue>9</issue><fpage>1507</fpage><lpage>1510</lpage><history><date date-type="received"><day>09</day><month>4</month><year>2018</year></date><date date-type="accepted"><day>12</day><month>6</month><year>2018</year></date></history><permissions><copyright-statement>© The Author(s) 2018. Published by Oxford University Press for the Infectious Diseases Society of America.</copyright-statement><copyright-year>2018</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="jiy359.pdf"></self-uri><abstract><title>Abstract</title><p>Despite increasing clinical relevance of Chikungunya virus (CHIKV) infection, caused by a rapidly emerging pathogen, recommended guidelines for its inactivation do not exist. In this study, we investigated the susceptibility of CHIKV to inactivation by heat and commercially available hand, surface, and World Health Organization-recommended disinfectants to define CHIKV prevention protocols for healthcare systems.</p></abstract><abstract abstract-type="teaser"><p>In this study, we characterized the stability of Chikungunya virus to heat inactivation and susceptibility to various commercially available hand- and surface- as well as WHO-recommended disinfectants to aid the development of appropriate disinfection and sanitization regimens.</p></abstract><kwd-group><kwd>Chikungunya virus</kwd><kwd>hand disinfection</kwd><kwd>heat inactivation</kwd><kwd>surface disinfection</kwd><kwd>World Health Organization</kwd></kwd-group><funding-group><award-group award-type="grant"><funding-source><named-content content-type="funder-name">Deutsche Forschungsgemeinschaft</named-content><named-content content-type="funder-identifier">10.13039/501100001659</named-content></funding-source><award-id>GO2153/3-1</award-id></award-group><award-group award-type="grant"><funding-source><named-content content-type="funder-name">Helmholtz Center for Infection Research</named-content></funding-source></award-group></funding-group><counts><page-count count="4"></page-count></counts></article-meta></front><body><p>Over the past decades, Chikungunya virus (CHIKV), an enveloped ribonucleic acid (RNA) virus, has spread globally. Although the virus has already been isolated in 1953, in-depth research has been limited since then and was primarily motivated by sporadic outbreaks like the French island La Reunion outbreak in 2005/2006 [<xref rid="CIT0001" ref-type="bibr">1</xref>]. Although CHIKV is mainly transmitted via bites of hematophagous arthropods such as mosquitoes (eg, <italic>Aedes aegypti</italic>), nonvector transmission through contaminated saliva has been reported in an experimental mouse model [<xref rid="CIT0002" ref-type="bibr">2</xref>]. Therefore, additional routes of viral transmission formally cannot be excluded. Infection with CHIKV often results in acute illness characterized by the classic triad of fever, arthralgia, and rash, and it can become chronic in a subset of patients. Recent outbreaks in Southeast Asia and South America [<xref rid="CIT0003" ref-type="bibr">3</xref>] as well as genetic adaptation to new vectors including <italic>Aedes albopictus</italic> [<xref rid="CIT0004" ref-type="bibr">4</xref>] justify the growing perception of CHIKV as a global health concern. However, guidelines on handling contamination and occupational exposure as well as confirmed procedures of virus inactivation and disinfection have not been established to date. In this study, we tested different inactivation methods using low-priced materials accessible to healthcare systems.</p><sec sec-type="methods" id="s1"><title>METHODS</title><sec id="s2"><title>Cells</title><p>BHK-21 cells and HEK293T cells were propagated in Dulbecco’s modified Eagle’s medium supplemented with 10% fetal calf serum, 100 units/mL penicillin, 100 µg/mL streptomycin, and 2 mM L-glutamine.</p></sec><sec id="s3"><title>Virus</title><p>We used the West African molecular clone strain 37997 coexpressing the green fluorescent protein as a reporter of infectivity [<xref rid="CIT0005" ref-type="bibr">5</xref>]. Infectious virus was generated by electroporation of full-length viral RNA into BHK-21 cells. Forty-eight hours posttransfection, at the peak of producer cell cytopathicity, virus particles were separated from cellular debris by filtration of the virus-containing supernatant through membranes with a pore size of 0.45 µm and stored in aliquots at −80°C before evaluation of the viral titer on HEK293T cells by flow cytometry. For this study, titers of the viral stocks ranged from 2.7 × 10<sup>6</sup> to 8.2 × 10<sup>7</sup> infectious units/mL.</p></sec><sec id="s4"><title>Statistics</title><p>Differences of means of 3 independent repetitions were tested for significance applying repeated measures 1-way analysis of variance followed by Dunnett’s multiple comparison testing using GraphPad Prism for Windows, version 7.04 (GraphPad Software, La Jolla, CA; <ext-link ext-link-type="uri" xlink:href="http://www.graphpad.com">www.graphpad.com</ext-link>).</p></sec></sec><sec id="s5"><title>RESULTS</title><p>To investigate the thermal stability of CHIKV, 9 parts cell culture medium was prewarmed to defined temperatures between 35 and 70°C while shaking at 500 rpm. Then, 1 part CHIKV was added to the medium and incubated for 1 and 5 minutes, respectively. Virus suspensions were cooled down to 4°C, serially diluted 8 times in 1:10 steps, and used for inoculation of HEK293T cells to determine the 50% tissue culture infective dose (TCID<sub>50</sub>/mL) by scoring the amounts of wells displaying green fluorescent protein 24 hours postinfection. Although incubation at temperatures up to 45°C for 5 minutes failed to modulate viral infectivity, CHIKV displayed a partial (<1 log) loss of infectivity upon heating at 50 and 55°C for 5 minutes and was fully inactivated upon heating at 70°C for 5 minutes (<xref ref-type="fig" rid="F1">Figure 1A</xref>). The z-value for CHIKV, representing the thermal death time with the conditions used in our assay, was 5.17. For chemical inactivation of CHIKV, no data or specific recommendations in case of occupational exposure exist so far. Alcohol-based disinfectants are routinely used for the decontamination of solutions, surfaces, skin, or wounds that were exposed to enveloped viruses. To evaluate the susceptibility of CHIKV to inactivation by biocides, we exposed the virus to different alcohols and commercially available alcohol-containing hand disinfectants (<xref ref-type="supplementary-material" rid="sup1">Supplementary Table 1</xref>). Specifically, 1 part virus suspension was mixed with 1 part organic load (0.3% bovine serum albumin [BSA] as interfering substance) and 8 parts disinfection solution of different concentrations. After an incubation time of 30 seconds, samples were serially diluted and the TCID<sub>50</sub>/mL values were determined as described above. Cytotoxic effects were monitored by microscopic analysis for altered density and morphology of the cellular monolayer and were quantified analogous to the TCID<sub>50</sub>/mL of the virus infectivity and was also verified by MTT assays. Strikingly, full inactivation by 1-propanol and 2-propanol was achieved at concentrations of 20% and 30%, respectively, whereas the fully effective concentration of ethanol was 40% (<xref ref-type="fig" rid="F1">Figure 1B</xref>). In line with this observation, Sterillium classic pure and Manorapid Synergy, containing high concentrations of propanol, were more effective in disinfecting CHIKV than Desderman pure, a mainly ethanol-based hand disinfectant (<xref ref-type="fig" rid="F1">Figure 1C</xref>). To simulate surface disinfection, we established an experimental system to test the stability on inanimate surfaces. Metal carriers providing a smooth surface were used on which virus suspension was applied. The ability of disinfectants to inactivate potentially residual infectivity of the dried virus was then monitored. The coated virus was covered with commercial surface disinfectants, and their virucidal activities were determined by a TCID<sub>50</sub> assay. Specifically, 9 parts of virus suspension were mixed with 1 part organic load of 0.3% BSA. Fifty microliters of this solution were pipetted onto the middle of a metal disc. After 60-minute incubation at room temperature, the dried suspension was challenged for 1 minute with 100 µL of individual surface disinfectants. We chose surface disinfectants differing in their chemical composition. Bacillol AF represents an alcohol-based disinfectant, whereas Descosept spezial contains a quarternary ammonium compound and Perform belongs to the oxygen releasing agents. Subsequently, the carrier was transferred into a tube containing 900 µL 4°C cold cell culture medium and 0.5 grams of glass beads (diameter of 0.25–0.5 mm). The glass beads were added because they help in the complete recovery of all non-inactivated virus. The virus was reconstituted into the medium by vortexing the carrier-containing tube for 1 minute. Infectivity of the treated virus suspension was determined as TCID<sub>50</sub>/mL in HEK293T. Although CHIKV infectivity was surprisingly resistant to air-drying, the 3 tested surface disinfectants (Bacillol AF, Descosept spezial, and 0.5% Perform) shared the ability to fully inactivate dried virus at concentrations recommended by the manufactures (<xref ref-type="fig" rid="F1">Figure 1D</xref>). To verify that the susceptibility of the HEK293T target cells for the virus infection were not negatively influenced with the treatment by the product test solution, an interference control was performed.</p><fig fig-type="figure" id="F1" orientation="portrait" position="float"><label>Figure 1.</label><caption><p>Thermostability of Chikungunya virus (CHIKV) and its susceptibility to inactivation by commercially available disinfectants. Sensitivity of CHIKV to indicated temperatures and virucidal efficacies of disinfectants in solution and on surfaces were evaluated by determining 50% tissue culture infective dose (TCID<sub>50</sub>/mL). The limit of detection is indicated as a dashed line. Cytotoxic effects are displayed as white bars and were calculated analogous to virus infectivity by monitoring alterations of density and morphology in the cell culture monolayer. Values for cytotoxicity beneath the limit of detection are not displayed. (A) Infectivity of CHIKV after incubation at indicated temperatures for 1 or 5 minutes. Virucidal effect of alcohols (B) and hand disinfectants (C) after a 30-second treatment in solution. (D) Treatment of dried CHIKV on metal discs for 1 minute with commercial surface disinfectants. The graphs show the mean of 3 independent experiments with standard error. *, <italic>P</italic> < .05; **, <italic>P</italic> < .01. Abbreviations: LOD, limit of detection; n.d., not detected.</p></caption><graphic xlink:href="jiy35901"></graphic></fig><p>As a cost-effective alternative to commercial disinfectants, the World Health Organization (WHO) recommended 2 alcohol-based hand rubs in 2009 [<xref rid="CIT0006" ref-type="bibr">6</xref>]. In this study, we tested the anti-CHIKV effect of different concentrations of hand rub WHO formulations I and II (<xref ref-type="supplementary-material" rid="sup1">Supplementary Table 1</xref>), which meet the requirements of the European Guideline (EN14476) [<xref rid="CIT0007" ref-type="bibr">7</xref>] for antiviral activity against poliovirus and the European Norm (EN12971) [<xref rid="CIT0008" ref-type="bibr">8</xref>] for surgical hand treatment. The WHO formulation II, a propanol-based disinfectant, exerted a stronger antiviral effect than the ethanol-based WHO formulation I (<xref ref-type="fig" rid="F2">Figure 2A</xref> and <xref ref-type="fig" rid="F2">B</xref>). Of note, CHIKV displayed a higher degree of resistance to inactivation by the WHO formulations I and II than other currently emerging viruses (<xref ref-type="fig" rid="F2">Figure 2C</xref> and <xref ref-type="fig" rid="F2">D</xref>) including Ebola virus, Middle East respiratory syndrome coronavirus, and Zika virus [<xref rid="CIT0009" ref-type="bibr">9</xref>]. However, CHIKV was less stable than Modified Vaccinia virus Ankara virus, which serves as a gold standard for enveloped viruses in chemical inactivation assays [<xref rid="CIT0010" ref-type="bibr">10</xref>].</p><fig fig-type="figure" id="F2" orientation="portrait" position="float"><label>Figure 2.</label><caption><p>Virucidal effects of World Health Organization formulations I and II (WHO I and II) on Chikungunya virus (CHIKV) infectivity and comparison of stability to other enveloped viruses. The disinfecting potential of WHO formulations I and II in solution assayed to determine the 50% tissue culture infective dose (TCID<sub>50</sub>/mL). The dashed line indicates the limit of detection. Cytotoxicity was determined equivalently to virus infectivity by observing potential disruptions in the cell culture monolayer and is presented as white bars. Infectivity of CHIKV after treatment with WHO formulations I and II in solution for 30 seconds (A and B) and comparison of its stability with other emerging enveloped viruses (C and D). The graphs show the mean of 3 independent experiments with standard error. Abbreviations: EboV, Ebola virus; LOD, limit of detection; MERS, Middle East respiratory syndrome corona virus; MVA, Modified Vaccinia Virus Ankara; n.d., not detected; ZikaV, Zika virus.</p></caption><graphic xlink:href="jiy35902"></graphic></fig></sec><sec id="s6"><title>DISCUSSION</title><p>In this study, we provide a profile of the sensitivity of CHIKV against heat-mediated inactivation and chemical disinfection. Heat inactivation of CHIKV has been partially addressed in the context of serum inactivation at 56°C for 30 minutes as a first-step preparation for plaque reduction neutralization tests [<xref rid="CIT0011" ref-type="bibr">11</xref>]. However, no systematic analysis of CHIKV’s thermosensitivity is available. We show that CHIKV is sensitive to increasing temperatures and can be safely and quickly inactivated when treated at temperatures above 70°C for at least 1 minute. Furthermore, we demonstrate a superior virucidal effect of propanol-based disinfectants over ethanol-based solutions. The resistance of CHIKV to short-term drying is consistent with results for freeze-dried virus [<xref rid="CIT0012" ref-type="bibr">12</xref>]. This finding underlines the necessity to probe existing antiviral disinfection protocols against emerging viral pathogens because this property could pose a potential risk for nonvector transmission of the virus.</p></sec><sec id="s7"><title>CONCLUSIONS</title><p>According to our results, all tested surface disinfectants were capable of inactivating CHIKV on a metal surface. More importantly, CHIKV was efficiently inactivated by both WHO-recommended formulations, validating their utility in the context of healthcare systems and CHIKV outbreak situations.</p></sec><sec sec-type="supplementary-material" id="s8"><title>Supplementary Data</title><p>Supplementary materials are available at <italic>The Journal of Infectious Diseases</italic> online. Consisting of data provided by the authors to benefit the reader, the posted materials are not copyedited and are the sole responsibility of the authors, so questions or comments should be addressed to the corresponding author.</p><supplementary-material content-type="local-data" id="sup1"><label>Supplementary Methods</label><media xlink:href="jiy359_suppl_supplementary_methods.pdf"><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>Author contributions.</italic></bold> S. F., C. G., and E. S. designed the study. S. F. performed all of the experiments. M. F. and V. P contributed to experiments. S. F., D. T, C. G., and E. S. analyzed the data. S. F., C. G., and E. S. wrote the article. S. F., D. T., and E. S. prepared the figures. M. F., G. S., and E. S. provided essential tools.</p><p><bold><italic>Financial support.</italic></bold> This work was funded by Deutsche Forschungsgemeinschaft (German-African Cooperation Projects in Infectiology, grant GO2153/3-1; to C. G.). The Helmholtz Center for Infection Research provided funding to C. G. and E. S. S. F. and V. P. are supported by the Infection Biology International PhD Program of Hannover Biomedical Research School. V. P. is supported by the GABBA PhD Program.</p><p><bold><italic>Potential conflicts of interest.</italic></bold> All authors: No reported conflicts of interest. All authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. 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