Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents
Identifieur interne : 001371 ( Pmc/Corpus ); précédent : 001370; suivant : 001372Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents
Auteurs : G. Kampf ; D. Todt ; S. Pfaender ; E. SteinmannSource :
- The Journal of Hospital Infection [ 0195-6701 ] ; 2020.
Abstract
Currently, the emergence of a novel human coronavirus, SARS-CoV-2, has become a global health concern causing severe respiratory tract infections in humans. Human-to-human transmissions have been described with incubation times between 2-10 days, facilitating its spread via droplets, contaminated hands or surfaces. We therefore reviewed the literature on all available information about the persistence of human and veterinary coronaviruses on inanimate surfaces as well as inactivation strategies with biocidal agents used for chemical disinfection, e.g. in healthcare facilities. The analysis of 22 studies reveals that human coronaviruses such as Severe Acute Respiratory Syndrome (SARS) coronavirus, Middle East Respiratory Syndrome (MERS) coronavirus or endemic human coronaviruses (HCoV) can persist on inanimate surfaces like metal, glass or plastic for up to 9 days, but can be efficiently inactivated by surface disinfection procedures with 62–71% ethanol, 0.5% hydrogen peroxide or 0.1% sodium hypochlorite within 1 minute. Other biocidal agents such as 0.05–0.2% benzalkonium chloride or 0.02% chlorhexidine digluconate are less effective. As no specific therapies are available for SARS-CoV-2, early containment and prevention of further spread will be crucial to stop the ongoing outbreak and to control this novel infectious thread.
Url:
DOI: 10.1016/j.jhin.2020.01.022
PubMed: 32035997
PubMed Central: 7132493
Links to Exploration step
PMC:7132493Le document en format XML
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<author><name sortKey="Kampf, G" sort="Kampf, G" uniqKey="Kampf G" first="G." last="Kampf">G. Kampf</name>
<affiliation><nlm:aff id="aff1">University Medicine Greifswald, Institute for Hygiene and Environmental Medicine, Ferdinand-Sauerbruch-Straße, 17475 Greifswald, Germany</nlm:aff>
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<author><name sortKey="Todt, D" sort="Todt, D" uniqKey="Todt D" first="D." last="Todt">D. Todt</name>
<affiliation><nlm:aff id="aff2">Department of Molecular and Medical Virology, Ruhr University Bochum, Universitätsstrasse 50, 44801 Bochum, Germany</nlm:aff>
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<author><name sortKey="Pfaender, S" sort="Pfaender, S" uniqKey="Pfaender S" first="S." last="Pfaender">S. Pfaender</name>
<affiliation><nlm:aff id="aff2">Department of Molecular and Medical Virology, Ruhr University Bochum, Universitätsstrasse 50, 44801 Bochum, Germany</nlm:aff>
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<author><name sortKey="Steinmann, E" sort="Steinmann, E" uniqKey="Steinmann E" first="E." last="Steinmann">E. Steinmann</name>
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<sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents</title>
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<front><div type="abstract" xml:lang="en"><title>Summary</title>
<p>Currently, the emergence of a novel human coronavirus, SARS-CoV-2, has become a global health concern causing severe respiratory tract infections in humans. Human-to-human transmissions have been described with incubation times between 2-10 days, facilitating its spread via droplets, contaminated hands or surfaces. We therefore reviewed the literature on all available information about the persistence of human and veterinary coronaviruses on inanimate surfaces as well as inactivation strategies with biocidal agents used for chemical disinfection, e.g. in healthcare facilities. The analysis of 22 studies reveals that human coronaviruses such as Severe Acute Respiratory Syndrome (SARS) coronavirus, Middle East Respiratory Syndrome (MERS) coronavirus or endemic human coronaviruses (HCoV) can persist on inanimate surfaces like metal, glass or plastic for up to 9 days, but can be efficiently inactivated by surface disinfection procedures with 62–71% ethanol, 0.5% hydrogen peroxide or 0.1% sodium hypochlorite within 1 minute. Other biocidal agents such as 0.05–0.2% benzalkonium chloride or 0.02% chlorhexidine digluconate are less effective. As no specific therapies are available for SARS-CoV-2, early containment and prevention of further spread will be crucial to stop the ongoing outbreak and to control this novel infectious thread.</p>
</div>
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</div1>
</back>
</TEI>
<pmc article-type="review-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">J Hosp Infect</journal-id>
<journal-id journal-id-type="iso-abbrev">J. Hosp. Infect</journal-id>
<journal-title-group><journal-title>The Journal of Hospital Infection</journal-title>
</journal-title-group>
<issn pub-type="ppub">0195-6701</issn>
<issn pub-type="epub">1532-2939</issn>
<publisher><publisher-name>The Healthcare Infection Society. Published by Elsevier Ltd.</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">32035997</article-id>
<article-id pub-id-type="pmc">7132493</article-id>
<article-id pub-id-type="publisher-id">S0195-6701(20)30046-3</article-id>
<article-id pub-id-type="doi">10.1016/j.jhin.2020.01.022</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Article</subject>
</subj-group>
</article-categories>
<title-group><article-title>Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents</article-title>
</title-group>
<contrib-group><contrib contrib-type="author" id="au1"><name><surname>Kampf</surname>
<given-names>G.</given-names>
</name>
<email>guenter.kampf@uni-greifswald.de</email>
<xref rid="aff1" ref-type="aff">a</xref>
<xref rid="cor1" ref-type="corresp">∗</xref>
</contrib>
<contrib contrib-type="author" id="au2"><name><surname>Todt</surname>
<given-names>D.</given-names>
</name>
<xref rid="aff2" ref-type="aff">b</xref>
</contrib>
<contrib contrib-type="author" id="au3"><name><surname>Pfaender</surname>
<given-names>S.</given-names>
</name>
<xref rid="aff2" ref-type="aff">b</xref>
</contrib>
<contrib contrib-type="author" id="au4"><name><surname>Steinmann</surname>
<given-names>E.</given-names>
</name>
<xref rid="aff2" ref-type="aff">b</xref>
</contrib>
</contrib-group>
<aff id="aff1"><label>a</label>
University Medicine Greifswald, Institute for Hygiene and Environmental Medicine, Ferdinand-Sauerbruch-Straße, 17475 Greifswald, Germany</aff>
<aff id="aff2"><label>b</label>
Department of Molecular and Medical Virology, Ruhr University Bochum, Universitätsstrasse 50, 44801 Bochum, Germany</aff>
<author-notes><corresp id="cor1"><label>∗</label>
Corresponding author. <email>guenter.kampf@uni-greifswald.de</email>
</corresp>
</author-notes>
<pub-date pub-type="pmc-release"><day>6</day>
<month>2</month>
<year>2020</year>
</pub-date>
<pmc-comment> PMC Release delay is 0 months and 0 days and was based on .</pmc-comment>
<pub-date pub-type="ppub"><month>3</month>
<year>2020</year>
</pub-date>
<pub-date pub-type="epub"><day>6</day>
<month>2</month>
<year>2020</year>
</pub-date>
<volume>104</volume>
<issue>3</issue>
<fpage>246</fpage>
<lpage>251</lpage>
<history><date date-type="received"><day>31</day>
<month>1</month>
<year>2020</year>
</date>
<date date-type="accepted"><day>31</day>
<month>1</month>
<year>2020</year>
</date>
</history>
<permissions><copyright-statement>© 2020 The Healthcare Infection Society. Published by Elsevier Ltd. All rights reserved.</copyright-statement>
<copyright-year>2020</copyright-year>
<copyright-holder>The Healthcare Infection Society</copyright-holder>
<license><license-p>Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.</license-p>
</license>
</permissions>
<abstract id="abs0010"><title>Summary</title>
<p>Currently, the emergence of a novel human coronavirus, SARS-CoV-2, has become a global health concern causing severe respiratory tract infections in humans. Human-to-human transmissions have been described with incubation times between 2-10 days, facilitating its spread via droplets, contaminated hands or surfaces. We therefore reviewed the literature on all available information about the persistence of human and veterinary coronaviruses on inanimate surfaces as well as inactivation strategies with biocidal agents used for chemical disinfection, e.g. in healthcare facilities. The analysis of 22 studies reveals that human coronaviruses such as Severe Acute Respiratory Syndrome (SARS) coronavirus, Middle East Respiratory Syndrome (MERS) coronavirus or endemic human coronaviruses (HCoV) can persist on inanimate surfaces like metal, glass or plastic for up to 9 days, but can be efficiently inactivated by surface disinfection procedures with 62–71% ethanol, 0.5% hydrogen peroxide or 0.1% sodium hypochlorite within 1 minute. Other biocidal agents such as 0.05–0.2% benzalkonium chloride or 0.02% chlorhexidine digluconate are less effective. As no specific therapies are available for SARS-CoV-2, early containment and prevention of further spread will be crucial to stop the ongoing outbreak and to control this novel infectious thread.</p>
</abstract>
<kwd-group id="kwrds0010"><title>Keywords</title>
<kwd>Coronavirus</kwd>
<kwd>Persistence</kwd>
<kwd>Inanimate surfaces</kwd>
<kwd>Chemical inactivation</kwd>
<kwd>Biocidal agents</kwd>
<kwd>Disinfection</kwd>
</kwd-group>
</article-meta>
</front>
<body><sec id="sec1"><title>Introduction</title>
<p id="p0010">A novel coronavirus (SARS-CoV-2) has recently emerged from China with a total of 45171 confirmed cases of pneumonia (as of February 12, 2020) [<xref rid="bib1" ref-type="bibr">1</xref>
]. Together with Severe Acute Respiratory Syndrome (SARS) coronavirus and Middle East Respiratory Syndrome (MERS) coronavirus [<xref rid="bib2" ref-type="bibr">2</xref>
], this is the third highly pathogenic human coronavirus that has emerged in the last two decades. Person-to-person transmission has been described both in hospital and family settings [<xref rid="bib3" ref-type="bibr">3</xref>
]. It is therefore of utmost importance to prevent any further spread in the public and healthcare settings. Transmission of coronaviruses from contaminated dry surfaces has been postulated including self-inoculation of mucous membranes of the nose, eyes or mouth [<xref rid="bib4" ref-type="bibr">4</xref>
,<xref rid="bib5" ref-type="bibr">5</xref>
], emphasizing the importance of a detailed understanding of coronavirus persistence on inanimate surfaces [<xref rid="bib6" ref-type="bibr">6</xref>
]. Various types of biocidal agents such as hydrogen peroxide, alcohols, sodium hypochlorite or benzalkonium chloride are used worldwide for disinfection, mainly in healthcare settings [<xref rid="bib7" ref-type="bibr">7</xref>
]. The aim of the review was therefore to summarize all available data on the persistence of all coronaviruses including emerging SARS-CoV and MERS-CoV as well as veterinary coronaviruses such as transmissible gastroenteritis virus (TGEV), mouse hepatitis virus (MHV) and canine coronavirus (CCV) on different types of inanimate surfaces and on the efficacy of commonly used biocidal agents used in surface disinfectants against coronaviruses.</p>
</sec>
<sec id="sec2"><title>Method</title>
<p id="p0015">A Medline search has been done on January 28, 2020. The following terms were used, always in combination with “coronavirus”, “TGEV”, “MHV” or “CCV”: survival surface (88 / 10 / 25 / 0 hits), persistence surface (47 / 1 / 32 / 0 hits), persistence hand (8 / 0 / 3 / 0 hits), survival hand (22 / 0 / 3 / 1 hits), survival skin (8 / 0 / 0 / 1 hits), persistence skin (1 / 0 / 0 / 1 hit), virucidal (23 / 3 / 3 / 1 hits), chemical inactivation (33 / 0 / 6 / 1), suspension test (18 / 0 / 0 / 0 hits) and carrier test (17 / 4 / 0 / 0 hits). Publications were included and results were extracted given they provided original data on coronaviruses on persistence (surfaces, materials) and inactivation by biocidal agents used for disinfection (suspension tests, carrier tests, fumigation studies). Data with commercial products based on various different types of biocidal agents were excluded. Reviews were not included, but screened for any information within the scope of this review.</p>
</sec>
<sec id="sec3"><title>Results</title>
<sec id="sec3.1"><title>Persistence of coronavirus on inanimate surfaces</title>
<p id="p0020">Most data were described with the endemic human coronavirus strain (HCoV-) 229E. On different types of materials it can remain infectious for from 2 hours up to 9 days. A higher temperature such as 30°C or 40°C reduced the duration of persistence of highly pathogenic MERS-CoV, TGEV and MHV. However, at 4°C persistence of TGEV and MHV can be increased to ≥ 28 days. Few comparative data obtained with SARS-CoV indicate that persistence was longer with higher inocula (<xref rid="tbl1" ref-type="table">Table I</xref>
). In addition it was shown at room temperature that HCoV-229E persists better at 50% compared to 30% relative humidity [<xref rid="bib8" ref-type="bibr">8</xref>
].<table-wrap position="float" id="tbl1"><label>Table I</label>
<caption><p>Persistence of coronaviruses on different types of inanimate surfaces</p>
</caption>
<alt-text id="alttext0010">Table I</alt-text>
<table frame="hsides" rules="groups"><thead><tr><th>Type of surface</th>
<th>Virus</th>
<th>Strain / isolate</th>
<th>Inoculum (viral titer)</th>
<th>Temperature</th>
<th>Persistence</th>
<th>Reference</th>
</tr>
</thead>
<tbody><tr><td rowspan="4">Steel</td>
<td>MERS-CoV</td>
<td>Isolate HCoV-EMC/2012</td>
<td>10<sup>5</sup>
</td>
<td>20°C<break></break>
30°C</td>
<td>48 h<break></break>
8–24 h</td>
<td>[<xref rid="bib21" ref-type="bibr">21</xref>
]</td>
</tr>
<tr><td>TGEV</td>
<td>Unknown</td>
<td>10<sup>6</sup>
</td>
<td>4°C<break></break>
20°C<break></break>
40°C</td>
<td>≥ 28 d<break></break>
3–28 d<break></break>
4–96 h</td>
<td>[<xref rid="bib22" ref-type="bibr">22</xref>
]</td>
</tr>
<tr><td>MHV</td>
<td>Unknown</td>
<td>10<sup>6</sup>
</td>
<td>4°C<break></break>
20°C<break></break>
40°C</td>
<td>≥ 28 d<break></break>
4–28 d<break></break>
4–96 h</td>
<td>[<xref rid="bib22" ref-type="bibr">22</xref>
]</td>
</tr>
<tr><td>HCoV</td>
<td>Strain 229E</td>
<td>10<sup>3</sup>
</td>
<td>21°C</td>
<td>5 d</td>
<td>[<xref rid="bib23" ref-type="bibr">23</xref>
]</td>
</tr>
<tr><td>Aluminium</td>
<td>HCoV</td>
<td>Strains 229E and OC43</td>
<td>5 x 10<sup>3</sup>
</td>
<td>21°C</td>
<td>2–8 h</td>
<td>[<xref rid="bib24" ref-type="bibr">24</xref>
]</td>
</tr>
<tr><td>Metal</td>
<td>SARS-CoV</td>
<td>Strain P9</td>
<td>10<sup>5</sup>
</td>
<td>RT</td>
<td>5 d</td>
<td>[<xref rid="bib25" ref-type="bibr">25</xref>
]</td>
</tr>
<tr><td>Wood</td>
<td>SARS-CoV</td>
<td>Strain P9</td>
<td>10<sup>5</sup>
</td>
<td>RT</td>
<td>4 d</td>
<td>[<xref rid="bib25" ref-type="bibr">25</xref>
]</td>
</tr>
<tr><td rowspan="2">Paper</td>
<td>SARS-CoV</td>
<td>Strain P9</td>
<td>10<sup>5</sup>
</td>
<td>RT</td>
<td>4–5 d</td>
<td>[<xref rid="bib25" ref-type="bibr">25</xref>
]</td>
</tr>
<tr><td>SARS-CoV</td>
<td>Strain GVU6109</td>
<td>10<sup>6</sup>
<break></break>
10<sup>5</sup>
<break></break>
10<sup>4</sup>
</td>
<td>RT</td>
<td>24 h<break></break>
3 h<break></break>
< 5 min</td>
<td>[<xref rid="bib26" ref-type="bibr">26</xref>
]</td>
</tr>
<tr><td rowspan="2">Glass</td>
<td>SARS-CoV</td>
<td>Strain P9</td>
<td>10<sup>5</sup>
</td>
<td>RT</td>
<td>4 d</td>
<td>[<xref rid="bib25" ref-type="bibr">25</xref>
]</td>
</tr>
<tr><td>HCoV</td>
<td>Strain 229E</td>
<td>10<sup>3</sup>
</td>
<td>21°C</td>
<td>5 d</td>
<td>[<xref rid="bib23" ref-type="bibr">23</xref>
]</td>
</tr>
<tr><td rowspan="5">Plastic</td>
<td>SARS-CoV</td>
<td>Strain HKU39849</td>
<td>10<sup>5</sup>
</td>
<td>22°-25°C</td>
<td>≤ 5 d</td>
<td>[<xref rid="bib27" ref-type="bibr">27</xref>
]</td>
</tr>
<tr><td>MERS-CoV</td>
<td>Isolate HCoV-EMC/2012</td>
<td>10<sup>5</sup>
</td>
<td>20°C<break></break>
30°C</td>
<td>48 h<break></break>
8–24 h</td>
<td>[<xref rid="bib21" ref-type="bibr">21</xref>
]</td>
</tr>
<tr><td>SARS-CoV</td>
<td>Strain P9</td>
<td>10<sup>5</sup>
</td>
<td>RT</td>
<td>4 d</td>
<td>[<xref rid="bib25" ref-type="bibr">25</xref>
]</td>
</tr>
<tr><td>SARS-CoV</td>
<td>Strain FFM1</td>
<td>10<sup>7</sup>
</td>
<td>RT</td>
<td>6–9 d</td>
<td>[<xref rid="bib28" ref-type="bibr">28</xref>
]</td>
</tr>
<tr><td>HCoV</td>
<td>Strain 229E</td>
<td>10<sup>7</sup>
</td>
<td>RT</td>
<td>2–6 d</td>
<td>[<xref rid="bib28" ref-type="bibr">28</xref>
]</td>
</tr>
<tr><td>PVC</td>
<td>HCoV</td>
<td>Strain 229E</td>
<td>10<sup>3</sup>
</td>
<td>21°C</td>
<td>5 d</td>
<td>[<xref rid="bib23" ref-type="bibr">23</xref>
]</td>
</tr>
<tr><td>Silicon rubber</td>
<td>HCoV</td>
<td>Strain 229E</td>
<td>10<sup>3</sup>
</td>
<td>21°C</td>
<td>5 d</td>
<td>[<xref rid="bib23" ref-type="bibr">23</xref>
]</td>
</tr>
<tr><td>Surgical glove (latex)</td>
<td>HCoV</td>
<td>Strains 229E and OC43</td>
<td>5 x 10<sup>3</sup>
</td>
<td>21°C</td>
<td>≤ 8 h</td>
<td>[<xref rid="bib24" ref-type="bibr">24</xref>
]</td>
</tr>
<tr><td>Disposable gown</td>
<td>SARS-CoV</td>
<td>Strain GVU6109</td>
<td>10<sup>6</sup>
<break></break>
10<sup>5</sup>
<break></break>
10<sup>4</sup>
</td>
<td>RT</td>
<td>2 d<break></break>
24 h<break></break>
1 h</td>
<td>[<xref rid="bib26" ref-type="bibr">26</xref>
]</td>
</tr>
<tr><td>Ceramic</td>
<td>HCoV</td>
<td>Strain 229E</td>
<td>10<sup>3</sup>
</td>
<td>21°C</td>
<td>5 d</td>
<td>[<xref rid="bib23" ref-type="bibr">23</xref>
]</td>
</tr>
<tr><td>Teflon</td>
<td>HCoV</td>
<td>Strain 229E</td>
<td>10<sup>3</sup>
</td>
<td>21°C</td>
<td>5 d</td>
<td>[<xref rid="bib23" ref-type="bibr">23</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>MERS = Middle East Respiratory Syndrome; HCoV = human coronavirus; TGEV = transmissible gastroenteritis virus; MHV = mouse hepatitis virus; SARS = Severe Acute Respiratory Syndrome; RT = room temperature.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</p>
</sec>
<sec id="sec3.2"><title>Inactivation of coronaviruses by biocidal agents in suspension tests</title>
<p id="p0025">Ethanol (78–95%), 2-propanol (70–100%), the combination of 45% 2-propanol with 30% 1-propanol, glutardialdehyde (0.5–2.5%), formaldehyde (0.7–1%) and povidone iodine (0.23–7.5%) readily inactivated coronavirus infectivity by approximately 4 log<sub>10</sub>
or more. (<xref rid="tbl2" ref-type="table">Table II</xref>
). Sodium hypochlorite required a minimal concentration of at least 0.21% to be effective. Hydrogen peroxide was effective with a concentration of 0.5% and an incubation time of 1 min. Data obtained with benzalkonium chloride at reasonable contact times were conflicting. Within 10 min a concentration of 0.2% revealed no efficacy against coronavirus whereas a concentration of 0.05% was quite effective. 0.02% chlorhexidine digluconate was basically ineffective (<xref rid="tbl2" ref-type="table">Table II</xref>
).<table-wrap position="float" id="tbl2"><label>Table II</label>
<caption><p>Inactivation of coronaviruses by different types of biocidal agents in suspension tests</p>
</caption>
<alt-text id="alttext0015">Table II</alt-text>
<table frame="hsides" rules="groups"><thead><tr><th>Biocidal agent</th>
<th>Concentration</th>
<th>Virus</th>
<th>Strain / isolate</th>
<th>Exposure time</th>
<th>Reduction of viral infectivity (log<sub>10</sub>
)</th>
<th>Reference</th>
</tr>
</thead>
<tbody><tr><td rowspan="7">Ethanol</td>
<td>95%</td>
<td>SARS-CoV</td>
<td>Isolate FFM-1</td>
<td>30 s</td>
<td align="char">≥ 5.5</td>
<td>[<xref rid="bib29" ref-type="bibr">29</xref>
]</td>
</tr>
<tr><td>85%</td>
<td>SARS-CoV</td>
<td>Isolate FFM-1</td>
<td>30 s</td>
<td align="char">≥ 5.5</td>
<td>[<xref rid="bib29" ref-type="bibr">29</xref>
]</td>
</tr>
<tr><td>80%</td>
<td>SARS-CoV</td>
<td>Isolate FFM-1</td>
<td>30 s</td>
<td align="char">≥ 4.3</td>
<td>[<xref rid="bib29" ref-type="bibr">29</xref>
]</td>
</tr>
<tr><td>80%</td>
<td>MERS-CoV</td>
<td>Strain EMC</td>
<td>30 s</td>
<td align="char">> 4.0</td>
<td>[<xref rid="bib14" ref-type="bibr">14</xref>
]</td>
</tr>
<tr><td>78%</td>
<td>SARS-CoV</td>
<td>Isolate FFM-1</td>
<td>30 s</td>
<td align="char">≥ 5.0</td>
<td>[<xref rid="bib28" ref-type="bibr">28</xref>
]</td>
</tr>
<tr><td>70%</td>
<td>MHV</td>
<td>Strains MHV-2 and MHV-N</td>
<td>10 min</td>
<td align="char">> 3.9</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td>70%</td>
<td>CCV</td>
<td>Strain I-71</td>
<td>10 min</td>
<td align="char">> 3.3</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td rowspan="6">2-Propanol</td>
<td>100%</td>
<td>SARS-CoV</td>
<td>Isolate FFM-1</td>
<td>30 s</td>
<td align="char">≥ 3.3</td>
<td>[<xref rid="bib28" ref-type="bibr">28</xref>
]</td>
</tr>
<tr><td>75%</td>
<td>SARS-CoV</td>
<td>Isolate FFM-1</td>
<td>30 s</td>
<td align="char">≥ 4.0</td>
<td>[<xref rid="bib14" ref-type="bibr">14</xref>
]</td>
</tr>
<tr><td>75%</td>
<td>MERS-CoV</td>
<td>Strain EMC</td>
<td>30 s</td>
<td align="char">≥ 4.0</td>
<td>[<xref rid="bib14" ref-type="bibr">14</xref>
]</td>
</tr>
<tr><td>70%</td>
<td>SARS-CoV</td>
<td>Isolate FFM-1</td>
<td>30 s</td>
<td align="char">≥ 3.3</td>
<td>[<xref rid="bib28" ref-type="bibr">28</xref>
]</td>
</tr>
<tr><td>50%</td>
<td>MHV</td>
<td>Strains MHV-2 and MHV-N</td>
<td>10 min</td>
<td align="char">> 3.7</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td>50%</td>
<td>CCV</td>
<td>Strain I-71</td>
<td>10 min</td>
<td align="char">> 3.7</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td rowspan="2">2-Propanol and 1-propanol</td>
<td rowspan="2">45% and 30%</td>
<td>SARS-CoV</td>
<td>Isolate FFM-1</td>
<td>30 s</td>
<td align="char">≥ 4.3</td>
<td>[<xref rid="bib29" ref-type="bibr">29</xref>
]</td>
</tr>
<tr><td>SARS-CoV</td>
<td>Isolate FFM-1</td>
<td>30 s</td>
<td align="char">≥ 2.8</td>
<td>[<xref rid="bib28" ref-type="bibr">28</xref>
]</td>
</tr>
<tr><td rowspan="4">Benzalkonium chloride</td>
<td>0.2%</td>
<td>HCoV</td>
<td>ATCC VR-759 (strain OC43)</td>
<td>10 min</td>
<td align="char">0.0</td>
<td>[<xref rid="bib31" ref-type="bibr">31</xref>
]</td>
</tr>
<tr><td>0.05%</td>
<td>MHV</td>
<td>Strains MHV-2 and MHV-N</td>
<td>10 min</td>
<td align="char">> 3.7</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td>0.05%</td>
<td>CCV</td>
<td>Strain I-71</td>
<td>10 min</td>
<td align="char">> 3.7</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td>0.00175%</td>
<td>CCV</td>
<td>Strain S378</td>
<td>3 d</td>
<td align="char">3.0</td>
<td>[<xref rid="bib32" ref-type="bibr">32</xref>
]</td>
</tr>
<tr><td>Didecyldimethyl ammonium chloride</td>
<td>0.0025%</td>
<td>CCV</td>
<td>Strain S378</td>
<td>3 d</td>
<td align="char">> 4.0</td>
<td>[<xref rid="bib32" ref-type="bibr">32</xref>
]</td>
</tr>
<tr><td rowspan="2">Chlorhexidine digluconate</td>
<td>0.02%</td>
<td>MHV</td>
<td>Strains MHV-2 and MHV-N</td>
<td>10 min</td>
<td align="char">0.7–0.8</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td>0.02%</td>
<td>CCV</td>
<td>Strain I-71</td>
<td>10 min</td>
<td align="char">0.3</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td rowspan="5">Sodium hypochlorite</td>
<td>0.21%</td>
<td>MHV</td>
<td>Strain MHV-1</td>
<td>30 s</td>
<td align="char">≥ 4.0</td>
<td>[<xref rid="bib33" ref-type="bibr">33</xref>
]</td>
</tr>
<tr><td>0.01%</td>
<td>MHV</td>
<td>Strains MHV-2 and MHV-N</td>
<td>10 min</td>
<td align="char">2.3–2.8</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td>0.01%</td>
<td>CCV</td>
<td>Strain I-71</td>
<td>10 min</td>
<td align="char">1.1</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td>0.001%</td>
<td>MHV</td>
<td>Strains MHV-2 and MHV-N</td>
<td>10 min</td>
<td align="char">0.3–0.6</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td>0.001%</td>
<td>CCV</td>
<td>Strain I-71</td>
<td>10 min</td>
<td align="char">0.9</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td>Hydrogen peroxide</td>
<td>0.5%</td>
<td>HCoV</td>
<td>Strain 229E</td>
<td>1 min</td>
<td align="char">> 4.0</td>
<td>[<xref rid="bib34" ref-type="bibr">34</xref>
]</td>
</tr>
<tr><td rowspan="5">Formaldehyde</td>
<td>1%</td>
<td>SARS-CoV</td>
<td>Isolate FFM-1</td>
<td>2 min</td>
<td align="char">> 3.0</td>
<td>[<xref rid="bib28" ref-type="bibr">28</xref>
]</td>
</tr>
<tr><td>0.7%</td>
<td>SARS-CoV</td>
<td>Isolate FFM-1</td>
<td>2 min</td>
<td align="char">> 3.0</td>
<td>[<xref rid="bib28" ref-type="bibr">28</xref>
]</td>
</tr>
<tr><td>0.7%</td>
<td>MHV</td>
<td></td>
<td>10 min</td>
<td align="char">> 3.5</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td>0.7%</td>
<td>CCV</td>
<td>Strain I-71</td>
<td>10 min</td>
<td align="char">> 3.7</td>
<td>[<xref rid="bib30" ref-type="bibr">30</xref>
]</td>
</tr>
<tr><td>0.009%</td>
<td>CCV</td>
<td></td>
<td>24 h</td>
<td align="char">> 4.0</td>
<td>[<xref rid="bib35" ref-type="bibr">35</xref>
]</td>
</tr>
<tr><td rowspan="2">Glutardialdehyde</td>
<td>2.5%</td>
<td>SARS-CoV</td>
<td>Hanoi strain</td>
<td>5 min</td>
<td align="char">> 4.0</td>
<td>[<xref rid="bib36" ref-type="bibr">36</xref>
]</td>
</tr>
<tr><td>0.5%</td>
<td>SARS-CoV</td>
<td>Isolate FFM-1</td>
<td>2 min</td>
<td align="char">> 4.0</td>
<td>[<xref rid="bib28" ref-type="bibr">28</xref>
]</td>
</tr>
<tr><td rowspan="9">Povidone iodine</td>
<td>7.5%</td>
<td>MERS-CoV</td>
<td>Isolate HCoV-EMC/2012</td>
<td>15 s</td>
<td align="char">4.6</td>
<td>[<xref rid="bib37" ref-type="bibr">37</xref>
]</td>
</tr>
<tr><td>4%</td>
<td>MERS-CoV</td>
<td>Isolate HCoV-EMC/2012</td>
<td>15 s</td>
<td align="char">5.0</td>
<td>[<xref rid="bib37" ref-type="bibr">37</xref>
]</td>
</tr>
<tr><td>1%</td>
<td>SARS-CoV</td>
<td>Hanoi strain</td>
<td>1 min</td>
<td align="char">> 4.0</td>
<td>[<xref rid="bib36" ref-type="bibr">36</xref>
]</td>
</tr>
<tr><td>1%</td>
<td>MERS-CoV</td>
<td>Isolate HCoV-EMC/2012</td>
<td>15 s</td>
<td align="char">4.3</td>
<td>[<xref rid="bib37" ref-type="bibr">37</xref>
]</td>
</tr>
<tr><td>0.47%</td>
<td>SARS-CoV</td>
<td>Hanoi strain</td>
<td>1 min</td>
<td align="char">3.8</td>
<td>[<xref rid="bib36" ref-type="bibr">36</xref>
]</td>
</tr>
<tr><td>0.25%</td>
<td>SARS-CoV</td>
<td>Hanoi strain</td>
<td>1 min</td>
<td align="char">> 4.0</td>
<td>[<xref rid="bib36" ref-type="bibr">36</xref>
]</td>
</tr>
<tr><td>0.23%</td>
<td>SARS-CoV</td>
<td>Hanoi strain</td>
<td>1 min</td>
<td align="char">> 4.0</td>
<td>[<xref rid="bib36" ref-type="bibr">36</xref>
]</td>
</tr>
<tr><td>0.23%</td>
<td>SARS-CoV</td>
<td>Isolate FFM-1</td>
<td>15 s</td>
<td align="char">≥ 4.4</td>
<td>[<xref rid="bib38" ref-type="bibr">38</xref>
]</td>
</tr>
<tr><td>0.23%</td>
<td>MERS-CoV</td>
<td>Isolate HCoV-EMC/2012</td>
<td>15 s</td>
<td align="char">≥ 4.4</td>
<td>[<xref rid="bib38" ref-type="bibr">38</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>SARS = Severe Acute Respiratory Syndrome; MERS = Middle East Respiratory Syndrome; MHV = mouse hepatitis virus; CCV = canine coronavirus; HCoV = human coronavirus.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</p>
</sec>
<sec id="sec3.3"><title>Inactivation of coronaviruses by biocidal agents in carrier tests</title>
<p id="p0030">Ethanol at concentrations between 62% and 71% reduced coronavirus infectivity within 1 min exposure time by 2.0–4.0 log<sub>10</sub>
. Concentrations of 0.1–0.5% sodium hypochlorite and 2% glutardialdehyde were also quite effective with > 3.0 log<sub>10</sub>
reduction in viral titre. In contrast, 0.04% benzalkonium chloride, 0.06% sodium hypochlorite and 0.55% ortho-phtalaldehyde were less effective (<xref rid="tbl3" ref-type="table">Table III</xref>
).<table-wrap position="float" id="tbl3"><label>Table III</label>
<caption><p>Inactivation of coronaviruses by different types of biocidal agents in carrier tests</p>
</caption>
<alt-text id="alttext0020">Table III</alt-text>
<table frame="hsides" rules="groups"><thead><tr><th>Biocidal agent</th>
<th>Concentration</th>
<th>Virus</th>
<th>Strain / isolate</th>
<th>Volume / material</th>
<th>Organic load</th>
<th>Exposure time</th>
<th>Reduction of viral infectivity (log<sub>10</sub>
)</th>
<th>Reference</th>
</tr>
</thead>
<tbody><tr><td rowspan="7">Ethanol</td>
<td>71%</td>
<td>TGEV</td>
<td>Unknown</td>
<td>50 μl / stainless steel</td>
<td>None</td>
<td>1 min</td>
<td align="char">3.5</td>
<td>[<xref rid="bib39" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td>71%</td>
<td>MHV</td>
<td>Unknown</td>
<td>50 μl / stainless steel</td>
<td>None</td>
<td>1 min</td>
<td align="char">2.0</td>
<td>[<xref rid="bib39" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td>70%</td>
<td>TGEV</td>
<td>Unknown</td>
<td>50 μl / stainless steel</td>
<td>None</td>
<td>1 min</td>
<td align="char">3.2</td>
<td>[<xref rid="bib39" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td>70%</td>
<td>MHV</td>
<td>Unknown</td>
<td>50 μl / stainless steel</td>
<td>None</td>
<td>1 min</td>
<td align="char">3.9</td>
<td>[<xref rid="bib39" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td>70%</td>
<td>HCoV</td>
<td>Strain 229E</td>
<td>20 μl / stainless steel</td>
<td>5% serum</td>
<td>1 min</td>
<td align="char">> 3.0</td>
<td>[<xref rid="bib40" ref-type="bibr">40</xref>
]</td>
</tr>
<tr><td>62%</td>
<td>TGEV</td>
<td>Unknown</td>
<td>50 μl / stainless steel</td>
<td>None</td>
<td>1 min</td>
<td align="char">4.0</td>
<td>[<xref rid="bib39" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td>62%</td>
<td>MHV</td>
<td>Unknown</td>
<td>50 μl / stainless steel</td>
<td>None</td>
<td>1 min</td>
<td align="char">2.7</td>
<td>[<xref rid="bib39" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td>Benzalkoniumchloride</td>
<td>0.04%</td>
<td>HCoV</td>
<td>Strain 229E</td>
<td>20 μl / stainless steel</td>
<td>5% serum</td>
<td>1 min</td>
<td align="char">< 3.0</td>
<td>[<xref rid="bib40" ref-type="bibr">40</xref>
]</td>
</tr>
<tr><td rowspan="5">Sodium hypochlorite</td>
<td>0.5%</td>
<td>HCoV</td>
<td>Strain 229E</td>
<td>20 μl / stainless steel</td>
<td>5% serum</td>
<td>1 min</td>
<td align="char">> 3.0</td>
<td>[<xref rid="bib40" ref-type="bibr">40</xref>
]</td>
</tr>
<tr><td>0.1%</td>
<td>HCoV</td>
<td>Strain 229E</td>
<td>20 μl / stainless steel</td>
<td>5% serum</td>
<td>1 min</td>
<td align="char">> 3.0</td>
<td>[<xref rid="bib40" ref-type="bibr">40</xref>
]</td>
</tr>
<tr><td>0.06%</td>
<td>TGEV</td>
<td>Unknown</td>
<td>50 μl / stainless steel</td>
<td>None</td>
<td>1 min</td>
<td align="char">0.4</td>
<td>[<xref rid="bib39" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td>0.06%</td>
<td>MHV</td>
<td>Unknown</td>
<td>50 μl / stainless steel</td>
<td>None</td>
<td>1 min</td>
<td align="char">0.6</td>
<td>[<xref rid="bib39" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td>0.01%</td>
<td>HCoV</td>
<td>Strain 229E</td>
<td>20 μl / stainless steel</td>
<td>5% serum</td>
<td>1 min</td>
<td align="char">< 3.0</td>
<td>[<xref rid="bib40" ref-type="bibr">40</xref>
]</td>
</tr>
<tr><td>Glutardialdehyde</td>
<td>2%</td>
<td>HCoV</td>
<td>Strain 229E</td>
<td>20 μl / stainless steel</td>
<td>5% serum</td>
<td>1 min</td>
<td align="char">> 3.0</td>
<td>[<xref rid="bib40" ref-type="bibr">40</xref>
]</td>
</tr>
<tr><td rowspan="2">Ortho-phtalaldehyde</td>
<td>0.55%</td>
<td>TGEV</td>
<td>Unknown</td>
<td>50 μl / stainless steel</td>
<td>None</td>
<td>1 min</td>
<td align="char">2.3</td>
<td>[<xref rid="bib39" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td>0.55%</td>
<td>MHV</td>
<td>Unknown</td>
<td>50 μl / stainless steel</td>
<td>None</td>
<td>1 min</td>
<td align="char">1.7</td>
<td>[<xref rid="bib39" ref-type="bibr">39</xref>
]</td>
</tr>
<tr><td>Hydrogen peroxide</td>
<td>Vapor of unknown concentration</td>
<td>TGEV</td>
<td>Purdue strain type 1</td>
<td>20 μl / stainless steel</td>
<td>None</td>
<td>2–3 h</td>
<td align="char">4.9–5.3*</td>
<td>[<xref rid="bib41" ref-type="bibr">41</xref>
]</td>
</tr>
</tbody>
</table>
<table-wrap-foot><fn><p>TGEV = transmissible gastroenteritis virus; MHV = mouse hepatitis virus; HCoV = human coronavirus; *depending on the volume of injected hydrogen peroxide.</p>
</fn>
</table-wrap-foot>
</table-wrap>
</p>
</sec>
</sec>
<sec id="sec4"><title>Discussion</title>
<p id="p0035">Human coronaviruses can remain infectious on inanimate surfaces at room temperature for up to 9 days. At a temperature of 30°C or more the duration of persistence is shorter. Veterinary coronaviruses have been shown to persist even longer for 28 d. Contamination of frequent touch surfaces in healthcare settings are therefore a potential source of viral transmission. Data on the transmissibility of coronaviruses from contaminated surfaces to hands were not found. However, it could be shown with influenza A virus that a contact of 5 s can transfer 31.6% of the viral load to the hands [<xref rid="bib9" ref-type="bibr">9</xref>
]. The transfer efficiency was lower (1.5%) with parainfluenza virus 3 and a 5 s contact between the surface and the hands [<xref rid="bib10" ref-type="bibr">10</xref>
]. In an observational study, it was described that students touch their face with their own hands on average 23 times per h, with contact mostly to the skin (56%), followed by mouth (36%), nose (31%) and eyes (31%) [<xref rid="bib11" ref-type="bibr">11</xref>
]. Although the viral load of coronaviruses on inanimate surfaces is not known during an outbreak situation it seem plausible to reduce the viral load on surfaces by disinfection, especially of frequently touched surfaces in the immediate patient surrounding where the highest viral load can be expected. The WHO recommends “to ensure that environmental cleaning and disinfection procedures are followed consistently and correctly. Thoroughly cleaning environmental surfaces with water and detergent and applying commonly used hospital-level disinfectants (such as sodium hypochlorite) are effective and sufficient procedures.” [<xref rid="bib12" ref-type="bibr">12</xref>
] The typical use of bleach is at a dilution of 1:100 of 5% sodium hypochlorite resulting in a final concentration of 0.05% [<xref rid="bib13" ref-type="bibr">13</xref>
]. Our summarized data with coronaviruses suggest that a concentration of 0.1% is effective in 1 min (<xref rid="tbl3" ref-type="table">Table III</xref>
). That is why it seems appropriate to recommend a dilution 1:50 of standard bleach in the coronavirus setting. For the disinfection of small surfaces ethanol (62–71%; carrier tests) revealed a similar efficacy against coronavirus. A concentration of 70% ethanol is also recommended by the WHO for disinfecting small surfaces [<xref rid="bib13" ref-type="bibr">13</xref>
].</p>
<p id="p0040">No data were found to describe the frequency of hands becoming contaminated with coronavirus, or the viral load on hands either, after patient contact or after touching contaminated surfaces. The WHO recommends to preferably apply alcohol-based hand rubs for the decontamination of hands, e.g. after removing gloves. Two WHO recommended formulations (based on 80% ethanol or 75% 2-propanol) have been evaluated in suspension tests against SARS-CoV and MERS-CoV, and both were described to be very effective [<xref rid="bib14" ref-type="bibr">14</xref>
]. No in vitro data were found on the efficacy of hand washing against coronavirus contaminations on hands. In Taiwan, however, it was described that installing hand wash stations in the emergency department was the only infection control measure which was significantly associated with the protection from healthcare workers from acquiring the SARS-CoV, indicating that hand hygiene can have a protective effect [<xref rid="bib15" ref-type="bibr">15</xref>
]. Compliance with hand hygiene can be significantly higher in an outbreak situation but is likely to remain an obstacle especially among physicians [<xref rid="bib16" ref-type="bibr">[16]</xref>
, <xref rid="bib17" ref-type="bibr">[17]</xref>
, <xref rid="bib18" ref-type="bibr">[18]</xref>
]. Transmission in healthcare settings can be successfully prevented when appropriate measures are consistently performed [<xref rid="bib19" ref-type="bibr">19</xref>
,<xref rid="bib20" ref-type="bibr">20</xref>
].</p>
</sec>
<sec id="sec5"><title>Conclusions</title>
<p id="p0045">Human coronaviruses can remain infectious on inanimate surfaces for up to 9 days. Surface disinfection with 0.1% sodium hypochlorite or 62–71% ethanol significantly reduces coronavirus infectivity on surfaces within 1 min exposure time. We expect a similar effect against the SARS-CoV-2.</p>
</sec>
<sec id="sec6"><title>Conflict of interest statement</title>
<p id="p0050">None declared.</p>
</sec>
<sec id="sec7"><title>Funding Sources</title>
<p id="p0080">None.</p>
</sec>
</body>
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