Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents

Published:February 06, 2020DOI:https://doi.org/10.1016/j.jhin.2020.01.022

      Summary

      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.

      Keywords

      Introduction

      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) [
      • WHO
      Coronavirus Disease 2019 (COVID-19).
      ]. Together with Severe Acute Respiratory Syndrome (SARS) coronavirus and Middle East Respiratory Syndrome (MERS) coronavirus [
      • de Wit E.
      • van Doremalen N.
      • Falzarano D.
      • Munster V.J.
      SARS and MERS: recent insights into emerging coronaviruses.
      ], 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 [
      • Chan J.F.
      • Yuan S.
      • Kok K.H.
      • To K.K.
      • Chu H.
      • Yang J.
      • et al.
      A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: a study of a family cluster.
      ]. 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 [
      • Otter J.A.
      • Donskey C.
      • Yezli S.
      • Douthwaite S.
      • Goldenberg S.D.
      • Weber D.J.
      Transmission of SARS and MERS coronaviruses and influenza virus in healthcare settings: the possible role of dry surface contamination.
      ,
      • Dowell S.F.
      • Simmerman J.M.
      • Erdman D.D.
      • Wu J.S.
      • Chaovavanich A.
      • Javadi M.
      • et al.
      Severe acute respiratory syndrome coronavirus on hospital surfaces.
      ], emphasizing the importance of a detailed understanding of coronavirus persistence on inanimate surfaces [
      • Geller C.
      • Varbanov M.
      • Duval R.E.
      Human coronaviruses: insights into environmental resistance and its influence on the development of new antiseptic strategies.
      ]. Various types of biocidal agents such as hydrogen peroxide, alcohols, sodium hypochlorite or benzalkonium chloride are used worldwide for disinfection, mainly in healthcare settings [
      • Kampf G.
      Antiseptic stewardship: biocide resistance and clinical implications.
      ]. 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.

      Method

      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.

      Results

       Persistence of coronavirus on inanimate surfaces

      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 (Table I). In addition it was shown at room temperature that HCoV-229E persists better at 50% compared to 30% relative humidity [
      • Ijaz M.K.
      • Brunner A.H.
      • Sattar S.A.
      • Nair R.C.
      • Johnson-Lussenburg C.M.
      Survival characteristics of airborne human coronavirus 229E.
      ].
      Table IPersistence of coronaviruses on different types of inanimate surfaces
      Type of surfaceVirusStrain / isolateInoculum (viral titer)TemperaturePersistenceReference
      SteelMERS-CoVIsolate HCoV-EMC/201210520°C

      30°C
      48 h

      8–24 h
      [
      • van Doremalen N.
      • Bushmaker T.
      • Munster V.J.
      Stability of Middle East respiratory syndrome coronavirus (MERS-CoV) under different environmental conditions.
      ]
      TGEVUnknown1064°C

      20°C

      40°C
      ≥ 28 d

      3–28 d

      4–96 h
      [
      • Casanova L.M.
      • Jeon S.
      • Rutala W.A.
      • Weber D.J.
      • Sobsey M.D.
      Effects of air temperature and relative humidity on coronavirus survival on surfaces.
      ]
      MHVUnknown1064°C

      20°C

      40°C
      ≥ 28 d

      4–28 d

      4–96 h
      [
      • Casanova L.M.
      • Jeon S.
      • Rutala W.A.
      • Weber D.J.
      • Sobsey M.D.
      Effects of air temperature and relative humidity on coronavirus survival on surfaces.
      ]
      HCoVStrain 229E10321°C5 d[
      • Warnes S.L.
      • Little Z.R.
      • Keevil C.W.
      Human Coronavirus 229E Remains Infectious on Common Touch Surface Materials.
      ]
      AluminiumHCoVStrains 229E and OC435 x 10321°C2–8 h[
      • Sizun J.
      • Yu M.W.
      • Talbot P.J.
      Survival of human coronaviruses 229E and OC43 in suspension and after drying on surfaces: a possible source of hospital-acquired infections.
      ]
      MetalSARS-CoVStrain P9105RT5 d[
      • Duan S.M.
      • Zhao X.S.
      • Wen R.F.
      • Huang J.J.
      • Pi G.H.
      • Zhang S.X.
      • et al.
      Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation.
      ]
      WoodSARS-CoVStrain P9105RT4 d[
      • Duan S.M.
      • Zhao X.S.
      • Wen R.F.
      • Huang J.J.
      • Pi G.H.
      • Zhang S.X.
      • et al.
      Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation.
      ]
      PaperSARS-CoVStrain P9105RT4–5 d[
      • Duan S.M.
      • Zhao X.S.
      • Wen R.F.
      • Huang J.J.
      • Pi G.H.
      • Zhang S.X.
      • et al.
      Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation.
      ]
      SARS-CoVStrain GVU6109106

      105

      104
      RT24 h

      3 h

      < 5 min
      [
      • Lai M.Y.
      • Cheng P.K.
      • Lim W.W.
      Survival of severe acute respiratory syndrome coronavirus.
      ]
      GlassSARS-CoVStrain P9105RT4 d[
      • Duan S.M.
      • Zhao X.S.
      • Wen R.F.
      • Huang J.J.
      • Pi G.H.
      • Zhang S.X.
      • et al.
      Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation.
      ]
      HCoVStrain 229E10321°C5 d[
      • Warnes S.L.
      • Little Z.R.
      • Keevil C.W.
      Human Coronavirus 229E Remains Infectious on Common Touch Surface Materials.
      ]
      PlasticSARS-CoVStrain HKU3984910522°-25°C≤ 5 d[
      • Chan K.H.
      • Peiris J.S.
      • Lam S.Y.
      • Poon L.L.
      • Yuen K.Y.
      • Seto W.H.
      The Effects of Temperature and Relative Humidity on the Viability of the SARS Coronavirus.
      ]
      MERS-CoVIsolate HCoV-EMC/201210520°C

      30°C
      48 h

      8–24 h
      [
      • van Doremalen N.
      • Bushmaker T.
      • Munster V.J.
      Stability of Middle East respiratory syndrome coronavirus (MERS-CoV) under different environmental conditions.
      ]
      SARS-CoVStrain P9105RT4 d[
      • Duan S.M.
      • Zhao X.S.
      • Wen R.F.
      • Huang J.J.
      • Pi G.H.
      • Zhang S.X.
      • et al.
      Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation.
      ]
      SARS-CoVStrain FFM1107RT6–9 d[
      • Rabenau H.F.
      • Cinatl J.
      • Morgenstern B.
      • Bauer G.
      • Preiser W.
      • Doerr H.W.
      Stability and inactivation of SARS coronavirus.
      ]
      HCoVStrain 229E107RT2–6 d[
      • Rabenau H.F.
      • Cinatl J.
      • Morgenstern B.
      • Bauer G.
      • Preiser W.
      • Doerr H.W.
      Stability and inactivation of SARS coronavirus.
      ]
      PVCHCoVStrain 229E10321°C5 d[
      • Warnes S.L.
      • Little Z.R.
      • Keevil C.W.
      Human Coronavirus 229E Remains Infectious on Common Touch Surface Materials.
      ]
      Silicon rubberHCoVStrain 229E10321°C5 d[
      • Warnes S.L.
      • Little Z.R.
      • Keevil C.W.
      Human Coronavirus 229E Remains Infectious on Common Touch Surface Materials.
      ]
      Surgical glove (latex)HCoVStrains 229E and OC435 x 10321°C≤ 8 h[
      • Sizun J.
      • Yu M.W.
      • Talbot P.J.
      Survival of human coronaviruses 229E and OC43 in suspension and after drying on surfaces: a possible source of hospital-acquired infections.
      ]
      Disposable gownSARS-CoVStrain GVU6109106

      105

      104
      RT2 d

      24 h

      1 h
      [
      • Lai M.Y.
      • Cheng P.K.
      • Lim W.W.
      Survival of severe acute respiratory syndrome coronavirus.
      ]
      CeramicHCoVStrain 229E10321°C5 d[
      • Warnes S.L.
      • Little Z.R.
      • Keevil C.W.
      Human Coronavirus 229E Remains Infectious on Common Touch Surface Materials.
      ]
      TeflonHCoVStrain 229E10321°C5 d[
      • Warnes S.L.
      • Little Z.R.
      • Keevil C.W.
      Human Coronavirus 229E Remains Infectious on Common Touch Surface Materials.
      ]
      MERS = Middle East Respiratory Syndrome; HCoV = human coronavirus; TGEV = transmissible gastroenteritis virus; MHV = mouse hepatitis virus; SARS = Severe Acute Respiratory Syndrome; RT = room temperature.

       Inactivation of coronaviruses by biocidal agents in suspension tests

      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 log10 or more. (Table II). 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 (Table II).
      Table IIInactivation of coronaviruses by different types of biocidal agents in suspension tests
      Biocidal agentConcentrationVirusStrain / isolateExposure timeReduction of viral infectivity (log10)Reference
      Ethanol95%SARS-CoVIsolate FFM-130 s≥ 5.5[
      • Rabenau H.F.
      • Kampf G.
      • Cinatl J.
      • Doerr H.W.
      Efficacy of various disinfectants against SARS coronavirus.
      ]
      85%SARS-CoVIsolate FFM-130 s≥ 5.5[
      • Rabenau H.F.
      • Kampf G.
      • Cinatl J.
      • Doerr H.W.
      Efficacy of various disinfectants against SARS coronavirus.
      ]
      80%SARS-CoVIsolate FFM-130 s≥ 4.3[
      • Rabenau H.F.
      • Kampf G.
      • Cinatl J.
      • Doerr H.W.
      Efficacy of various disinfectants against SARS coronavirus.
      ]
      80%MERS-CoVStrain EMC30 s> 4.0[
      • Siddharta A.
      • Pfaender S.
      • Vielle N.J.
      • Dijkman R.
      • Friesland M.
      • Becker B.
      • et al.
      Virucidal Activity of World Health Organization-Recommended Formulations Against Enveloped Viruses, Including Zika, Ebola, and Emerging Coronaviruses.
      ]
      78%SARS-CoVIsolate FFM-130 s≥ 5.0[
      • Rabenau H.F.
      • Cinatl J.
      • Morgenstern B.
      • Bauer G.
      • Preiser W.
      • Doerr H.W.
      Stability and inactivation of SARS coronavirus.
      ]
      70%MHVStrains MHV-2 and MHV-N10 min> 3.9[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      70%CCVStrain I-7110 min> 3.3[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      2-Propanol100%SARS-CoVIsolate FFM-130 s≥ 3.3[
      • Rabenau H.F.
      • Cinatl J.
      • Morgenstern B.
      • Bauer G.
      • Preiser W.
      • Doerr H.W.
      Stability and inactivation of SARS coronavirus.
      ]
      75%SARS-CoVIsolate FFM-130 s≥ 4.0[
      • Siddharta A.
      • Pfaender S.
      • Vielle N.J.
      • Dijkman R.
      • Friesland M.
      • Becker B.
      • et al.
      Virucidal Activity of World Health Organization-Recommended Formulations Against Enveloped Viruses, Including Zika, Ebola, and Emerging Coronaviruses.
      ]
      75%MERS-CoVStrain EMC30 s≥ 4.0[
      • Siddharta A.
      • Pfaender S.
      • Vielle N.J.
      • Dijkman R.
      • Friesland M.
      • Becker B.
      • et al.
      Virucidal Activity of World Health Organization-Recommended Formulations Against Enveloped Viruses, Including Zika, Ebola, and Emerging Coronaviruses.
      ]
      70%SARS-CoVIsolate FFM-130 s≥ 3.3[
      • Rabenau H.F.
      • Cinatl J.
      • Morgenstern B.
      • Bauer G.
      • Preiser W.
      • Doerr H.W.
      Stability and inactivation of SARS coronavirus.
      ]
      50%MHVStrains MHV-2 and MHV-N10 min> 3.7[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      50%CCVStrain I-7110 min> 3.7[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      2-Propanol and 1-propanol45% and 30%SARS-CoVIsolate FFM-130 s≥ 4.3[
      • Rabenau H.F.
      • Kampf G.
      • Cinatl J.
      • Doerr H.W.
      Efficacy of various disinfectants against SARS coronavirus.
      ]
      SARS-CoVIsolate FFM-130 s≥ 2.8[
      • Rabenau H.F.
      • Cinatl J.
      • Morgenstern B.
      • Bauer G.
      • Preiser W.
      • Doerr H.W.
      Stability and inactivation of SARS coronavirus.
      ]
      Benzalkonium chloride0.2%HCoVATCC VR-759 (strain OC43)10 min0.0[
      • Wood A.
      • Payne D.
      The action of three antiseptics/disinfectants against enveloped and non-enveloped viruses.
      ]
      0.05%MHVStrains MHV-2 and MHV-N10 min> 3.7[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      0.05%CCVStrain I-7110 min> 3.7[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      0.00175%CCVStrain S3783 d3.0[
      • Pratelli A.
      Action of disinfectants on canine coronavirus replication in vitro.
      ]
      Didecyldimethyl ammonium chloride0.0025%CCVStrain S3783 d> 4.0[
      • Pratelli A.
      Action of disinfectants on canine coronavirus replication in vitro.
      ]
      Chlorhexidine digluconate0.02%MHVStrains MHV-2 and MHV-N10 min0.7–0.8[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      0.02%CCVStrain I-7110 min0.3[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      Sodium hypochlorite0.21%MHVStrain MHV-130 s≥ 4.0[
      • Dellanno C.
      • Vega Q.
      • Boesenberg D.
      The antiviral action of common household disinfectants and antiseptics against murine hepatitis virus, a potential surrogate for SARS coronavirus.
      ]
      0.01%MHVStrains MHV-2 and MHV-N10 min2.3–2.8[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      0.01%CCVStrain I-7110 min1.1[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      0.001%MHVStrains MHV-2 and MHV-N10 min0.3–0.6[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      0.001%CCVStrain I-7110 min0.9[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      Hydrogen peroxide0.5%HCoVStrain 229E1 min> 4.0[
      • Omidbakhsh N.
      • Sattar S.A.
      Broad-spectrum microbicidal activity, toxicologic assessment, and materials compatibility of a new generation of accelerated hydrogen peroxide-based environmental surface disinfectant.
      ]
      Formaldehyde1%SARS-CoVIsolate FFM-12 min> 3.0[
      • Rabenau H.F.
      • Cinatl J.
      • Morgenstern B.
      • Bauer G.
      • Preiser W.
      • Doerr H.W.
      Stability and inactivation of SARS coronavirus.
      ]
      0.7%SARS-CoVIsolate FFM-12 min> 3.0[
      • Rabenau H.F.
      • Cinatl J.
      • Morgenstern B.
      • Bauer G.
      • Preiser W.
      • Doerr H.W.
      Stability and inactivation of SARS coronavirus.
      ]
      0.7%MHV10 min> 3.5[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      0.7%CCVStrain I-7110 min> 3.7[
      • Saknimit M.
      • Inatsuki I.
      • Sugiyama Y.
      • Yagami K.
      Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
      ]
      0.009%CCV24 h> 4.0[
      • Pratelli A.
      Canine coronavirus inactivation with physical and chemical agents.
      ]
      Glutardialdehyde2.5%SARS-CoVHanoi strain5 min> 4.0[
      • Kariwa H.
      • Fujii N.
      • Takashima I.
      Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents.
      ]
      0.5%SARS-CoVIsolate FFM-12 min> 4.0[
      • Rabenau H.F.
      • Cinatl J.
      • Morgenstern B.
      • Bauer G.
      • Preiser W.
      • Doerr H.W.
      Stability and inactivation of SARS coronavirus.
      ]
      Povidone iodine7.5%MERS-CoVIsolate HCoV-EMC/201215 s4.6[
      • Eggers M.
      • Eickmann M.
      • Zorn J.
      Rapid and Effective Virucidal Activity of Povidone-Iodine Products Against Middle East Respiratory Syndrome Coronavirus (MERS-CoV) and Modified Vaccinia Virus Ankara (MVA).
      ]
      4%MERS-CoVIsolate HCoV-EMC/201215 s5.0[
      • Eggers M.
      • Eickmann M.
      • Zorn J.
      Rapid and Effective Virucidal Activity of Povidone-Iodine Products Against Middle East Respiratory Syndrome Coronavirus (MERS-CoV) and Modified Vaccinia Virus Ankara (MVA).
      ]
      1%SARS-CoVHanoi strain1 min> 4.0[
      • Kariwa H.
      • Fujii N.
      • Takashima I.
      Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents.
      ]
      1%MERS-CoVIsolate HCoV-EMC/201215 s4.3[
      • Eggers M.
      • Eickmann M.
      • Zorn J.
      Rapid and Effective Virucidal Activity of Povidone-Iodine Products Against Middle East Respiratory Syndrome Coronavirus (MERS-CoV) and Modified Vaccinia Virus Ankara (MVA).
      ]
      0.47%SARS-CoVHanoi strain1 min3.8[
      • Kariwa H.
      • Fujii N.
      • Takashima I.
      Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents.
      ]
      0.25%SARS-CoVHanoi strain1 min> 4.0[
      • Kariwa H.
      • Fujii N.
      • Takashima I.
      Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents.
      ]
      0.23%SARS-CoVHanoi strain1 min> 4.0[
      • Kariwa H.
      • Fujii N.
      • Takashima I.
      Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents.
      ]
      0.23%SARS-CoVIsolate FFM-115 s≥ 4.4[
      • Eggers M.
      • Koburger-Janssen T.
      • Eickmann M.
      • Zorn J.
      In Vitro Bactericidal and Virucidal Efficacy of Povidone-Iodine Gargle/Mouthwash Against Respiratory and Oral Tract Pathogens.
      ]
      0.23%MERS-CoVIsolate HCoV-EMC/201215 s≥ 4.4[
      • Eggers M.
      • Koburger-Janssen T.
      • Eickmann M.
      • Zorn J.
      In Vitro Bactericidal and Virucidal Efficacy of Povidone-Iodine Gargle/Mouthwash Against Respiratory and Oral Tract Pathogens.
      ]
      SARS = Severe Acute Respiratory Syndrome; MERS = Middle East Respiratory Syndrome; MHV = mouse hepatitis virus; CCV = canine coronavirus; HCoV = human coronavirus.

       Inactivation of coronaviruses by biocidal agents in carrier tests

      Ethanol at concentrations between 62% and 71% reduced coronavirus infectivity within 1 min exposure time by 2.0–4.0 log10. Concentrations of 0.1–0.5% sodium hypochlorite and 2% glutardialdehyde were also quite effective with > 3.0 log10 reduction in viral titre. In contrast, 0.04% benzalkonium chloride, 0.06% sodium hypochlorite and 0.55% ortho-phtalaldehyde were less effective (Table III).
      Table IIIInactivation of coronaviruses by different types of biocidal agents in carrier tests
      Biocidal agentConcentrationVirusStrain / isolateVolume / materialOrganic loadExposure timeReduction of viral infectivity (log10)Reference
      Ethanol71%TGEVUnknown50 μl / stainless steelNone1 min3.5[
      • Hulkower R.L.
      • Casanova L.M.
      • Rutala W.A.
      • Weber D.J.
      • Sobsey M.D.
      Inactivation of surrogate coronaviruses on hard surfaces by health care germicides.
      ]
      71%MHVUnknown50 μl / stainless steelNone1 min2.0[
      • Hulkower R.L.
      • Casanova L.M.
      • Rutala W.A.
      • Weber D.J.
      • Sobsey M.D.
      Inactivation of surrogate coronaviruses on hard surfaces by health care germicides.
      ]
      70%TGEVUnknown50 μl / stainless steelNone1 min3.2[
      • Hulkower R.L.
      • Casanova L.M.
      • Rutala W.A.
      • Weber D.J.
      • Sobsey M.D.
      Inactivation of surrogate coronaviruses on hard surfaces by health care germicides.
      ]
      70%MHVUnknown50 μl / stainless steelNone1 min3.9[
      • Hulkower R.L.
      • Casanova L.M.
      • Rutala W.A.
      • Weber D.J.
      • Sobsey M.D.
      Inactivation of surrogate coronaviruses on hard surfaces by health care germicides.
      ]
      70%HCoVStrain 229E20 μl / stainless steel5% serum1 min> 3.0[
      • Sattar S.A.
      • Springthorpe V.S.
      • Karim Y.
      • Loro P.
      Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses.
      ]
      62%TGEVUnknown50 μl / stainless steelNone1 min4.0[
      • Hulkower R.L.
      • Casanova L.M.
      • Rutala W.A.
      • Weber D.J.
      • Sobsey M.D.
      Inactivation of surrogate coronaviruses on hard surfaces by health care germicides.
      ]
      62%MHVUnknown50 μl / stainless steelNone1 min2.7[
      • Hulkower R.L.
      • Casanova L.M.
      • Rutala W.A.
      • Weber D.J.
      • Sobsey M.D.
      Inactivation of surrogate coronaviruses on hard surfaces by health care germicides.
      ]
      Benzalkoniumchloride0.04%HCoVStrain 229E20 μl / stainless steel5% serum1 min< 3.0[
      • Sattar S.A.
      • Springthorpe V.S.
      • Karim Y.
      • Loro P.
      Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses.
      ]
      Sodium hypochlorite0.5%HCoVStrain 229E20 μl / stainless steel5% serum1 min> 3.0[
      • Sattar S.A.
      • Springthorpe V.S.
      • Karim Y.
      • Loro P.
      Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses.
      ]
      0.1%HCoVStrain 229E20 μl / stainless steel5% serum1 min> 3.0[
      • Sattar S.A.
      • Springthorpe V.S.
      • Karim Y.
      • Loro P.
      Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses.
      ]
      0.06%TGEVUnknown50 μl / stainless steelNone1 min0.4[
      • Hulkower R.L.
      • Casanova L.M.
      • Rutala W.A.
      • Weber D.J.
      • Sobsey M.D.
      Inactivation of surrogate coronaviruses on hard surfaces by health care germicides.
      ]
      0.06%MHVUnknown50 μl / stainless steelNone1 min0.6[
      • Hulkower R.L.
      • Casanova L.M.
      • Rutala W.A.
      • Weber D.J.
      • Sobsey M.D.
      Inactivation of surrogate coronaviruses on hard surfaces by health care germicides.
      ]
      0.01%HCoVStrain 229E20 μl / stainless steel5% serum1 min< 3.0[
      • Sattar S.A.
      • Springthorpe V.S.
      • Karim Y.
      • Loro P.
      Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses.
      ]
      Glutardialdehyde2%HCoVStrain 229E20 μl / stainless steel5% serum1 min> 3.0[
      • Sattar S.A.
      • Springthorpe V.S.
      • Karim Y.
      • Loro P.
      Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses.
      ]
      Ortho-phtalaldehyde0.55%TGEVUnknown50 μl / stainless steelNone1 min2.3[
      • Hulkower R.L.
      • Casanova L.M.
      • Rutala W.A.
      • Weber D.J.
      • Sobsey M.D.
      Inactivation of surrogate coronaviruses on hard surfaces by health care germicides.
      ]
      0.55%MHVUnknown50 μl / stainless steelNone1 min1.7[
      • Hulkower R.L.
      • Casanova L.M.
      • Rutala W.A.
      • Weber D.J.
      • Sobsey M.D.
      Inactivation of surrogate coronaviruses on hard surfaces by health care germicides.
      ]
      Hydrogen peroxideVapor of unknown concentrationTGEVPurdue strain type 120 μl / stainless steelNone2–3 h4.9–5.3*[
      • Goyal S.M.
      • Chander Y.
      • Yezli S.
      • Otter J.A.
      Evaluating the virucidal efficacy of hydrogen peroxide vapour.
      ]
      TGEV = transmissible gastroenteritis virus; MHV = mouse hepatitis virus; HCoV = human coronavirus; *depending on the volume of injected hydrogen peroxide.

      Discussion

      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 [
      • Bean B.
      • Moore B.M.
      • Sterner B.
      • Peterson L.R.
      • Gerding D.N.
      • Balfour H.H.
      Survival of influenza viruses an environmental surfaces.
      ]. The transfer efficiency was lower (1.5%) with parainfluenza virus 3 and a 5 s contact between the surface and the hands [
      • Ansari S.A.
      • Springthorpe V.S.
      • Sattar S.A.
      • Rivard S.
      • Rahman M.
      Potential role of hands in the spread of respiratory viral infections: studies with human parainfluenza virus 3 and rhinovirus 14.
      ]. 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%) [
      • Kwok Y.L.
      • Gralton J.
      • McLaws M.L.
      Face touching: a frequent habit that has implications for hand hygiene.
      ]. 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.” [
      • WHO
      Infection prevention and control during health care when novel coronavirus (nCoV) infection is suspected.
      ] The typical use of bleach is at a dilution of 1:100 of 5% sodium hypochlorite resulting in a final concentration of 0.05% [
      • WHO. Annex G
      Use of disinfectants: alcohol and bleach. Infection prevention and control of epidemic-and pandemic-prone acute respiratory infections in health care.
      ]. Our summarized data with coronaviruses suggest that a concentration of 0.1% is effective in 1 min (Table III). 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 [
      • WHO. Annex G
      Use of disinfectants: alcohol and bleach. Infection prevention and control of epidemic-and pandemic-prone acute respiratory infections in health care.
      ].
      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 [
      • Siddharta A.
      • Pfaender S.
      • Vielle N.J.
      • Dijkman R.
      • Friesland M.
      • Becker B.
      • et al.
      Virucidal Activity of World Health Organization-Recommended Formulations Against Enveloped Viruses, Including Zika, Ebola, and Emerging Coronaviruses.
      ]. 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 [
      • Yen M.Y.
      • Lu Y.C.
      • Huang P.H.
      • Chen C.M.
      • Chen Y.C.
      • Lin Y.E.
      Quantitative evaluation of infection control models in the prevention of nosocomial transmission of SARS virus to healthcare workers: implication to nosocomial viral infection control for healthcare workers.
      ]. Compliance with hand hygiene can be significantly higher in an outbreak situation but is likely to remain an obstacle especially among physicians [
      • Alshammari M.
      • Reynolds K.A.
      • Verhougstraete M.
      • O'Rourke M.K.
      Comparison of perceived and observed hand hygiene compliance in healthcare workers in MERS-CoV endemic regions.
      ,
      • Al-Tawfiq J.A.
      • Abdrabalnabi R.
      • Taher A.
      • Mathew S.
      • Rahman K.A.
      Infection control influence of Middle East respiratory syndrome coronavirus: A hospital-based analysis.
      ,
      • Wong T.W.
      • Tam W.W.
      Handwashing practice and the use of personal protective equipment among medical students after the SARS epidemic in Hong Kong.
      ]. Transmission in healthcare settings can be successfully prevented when appropriate measures are consistently performed [
      • Wiboonchutikul S.
      • Manosuthi W.
      • Likanonsakul S.
      • Sangsajja C.
      • Kongsanan P.
      • Nitiyanontakij R.
      • et al.
      Lack of transmission among healthcare workers in contact with a case of Middle East respiratory syndrome coronavirus infection in Thailand.
      ,
      • Ki H.K.
      • Han S.K.
      • Son J.S.
      • Park S.O.
      Risk of transmission via medical employees and importance of routine infection-prevention policy in a nosocomial outbreak of Middle East respiratory syndrome (MERS): a descriptive analysis from a tertiary care hospital in South Korea.
      ].

      Conclusions

      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.

      Conflict of interest statement

      None declared.

      Funding Sources

      None.

      References

        • WHO
        Coronavirus Disease 2019 (COVID-19).
        WHO, 2020 (Situation Report 23.)
        • de Wit E.
        • van Doremalen N.
        • Falzarano D.
        • Munster V.J.
        SARS and MERS: recent insights into emerging coronaviruses.
        Nat Rev Microbiol. 2016; 14: 523-534
        • Chan J.F.
        • Yuan S.
        • Kok K.H.
        • To K.K.
        • Chu H.
        • Yang J.
        • et al.
        A familial cluster of pneumonia associated with the 2019 novel coronavirus indicating person-to-person transmission: a study of a family cluster.
        Lancet. 2020; https://doi.org/10.1016/s0140-6736(20)30154-9
        • Otter J.A.
        • Donskey C.
        • Yezli S.
        • Douthwaite S.
        • Goldenberg S.D.
        • Weber D.J.
        Transmission of SARS and MERS coronaviruses and influenza virus in healthcare settings: the possible role of dry surface contamination.
        J Hosp Infect. 2016; 92: 235-250
        • Dowell S.F.
        • Simmerman J.M.
        • Erdman D.D.
        • Wu J.S.
        • Chaovavanich A.
        • Javadi M.
        • et al.
        Severe acute respiratory syndrome coronavirus on hospital surfaces.
        Clin Infect Dis. 2004; 39: 652-657
        • Geller C.
        • Varbanov M.
        • Duval R.E.
        Human coronaviruses: insights into environmental resistance and its influence on the development of new antiseptic strategies.
        Viruses. 2012; 4: 3044-3068
        • Kampf G.
        Antiseptic stewardship: biocide resistance and clinical implications.
        Springer International Publishing, Cham2018
        • Ijaz M.K.
        • Brunner A.H.
        • Sattar S.A.
        • Nair R.C.
        • Johnson-Lussenburg C.M.
        Survival characteristics of airborne human coronavirus 229E.
        J Gen Virol. 1985; 66: 2743-2748
        • Bean B.
        • Moore B.M.
        • Sterner B.
        • Peterson L.R.
        • Gerding D.N.
        • Balfour H.H.
        Survival of influenza viruses an environmental surfaces.
        J Infect Dis. 1982; 146: 47-51
        • Ansari S.A.
        • Springthorpe V.S.
        • Sattar S.A.
        • Rivard S.
        • Rahman M.
        Potential role of hands in the spread of respiratory viral infections: studies with human parainfluenza virus 3 and rhinovirus 14.
        J Clin Microbiol. 1991; 29: 2115-2119
        • Kwok Y.L.
        • Gralton J.
        • McLaws M.L.
        Face touching: a frequent habit that has implications for hand hygiene.
        Am J Infect Contr. 2015; 43: 112-114
        • WHO
        Infection prevention and control during health care when novel coronavirus (nCoV) infection is suspected.
        WHO, 2020 (Interim guidance. 25 January 2020)
        • WHO. Annex G
        Use of disinfectants: alcohol and bleach. Infection prevention and control of epidemic-and pandemic-prone acute respiratory infections in health care.
        WHO, Geneva2014: 65-66
        • Siddharta A.
        • Pfaender S.
        • Vielle N.J.
        • Dijkman R.
        • Friesland M.
        • Becker B.
        • et al.
        Virucidal Activity of World Health Organization-Recommended Formulations Against Enveloped Viruses, Including Zika, Ebola, and Emerging Coronaviruses.
        J Infect Dis. 2017; 215: 902-906
        • Yen M.Y.
        • Lu Y.C.
        • Huang P.H.
        • Chen C.M.
        • Chen Y.C.
        • Lin Y.E.
        Quantitative evaluation of infection control models in the prevention of nosocomial transmission of SARS virus to healthcare workers: implication to nosocomial viral infection control for healthcare workers.
        Scand J Infect Dis. 2010; 42: 510-515
        • Alshammari M.
        • Reynolds K.A.
        • Verhougstraete M.
        • O'Rourke M.K.
        Comparison of perceived and observed hand hygiene compliance in healthcare workers in MERS-CoV endemic regions.
        Healthcare (Basel, Switzerland). 2018; 6: 122
        • Al-Tawfiq J.A.
        • Abdrabalnabi R.
        • Taher A.
        • Mathew S.
        • Rahman K.A.
        Infection control influence of Middle East respiratory syndrome coronavirus: A hospital-based analysis.
        Am J Infect Contr. 2019; 47: 431-434
        • Wong T.W.
        • Tam W.W.
        Handwashing practice and the use of personal protective equipment among medical students after the SARS epidemic in Hong Kong.
        Am J Infect Contr. 2005; 33: 580-586
        • Wiboonchutikul S.
        • Manosuthi W.
        • Likanonsakul S.
        • Sangsajja C.
        • Kongsanan P.
        • Nitiyanontakij R.
        • et al.
        Lack of transmission among healthcare workers in contact with a case of Middle East respiratory syndrome coronavirus infection in Thailand.
        Antimicrob Resist Infect Control. 2016; 5: 21
        • Ki H.K.
        • Han S.K.
        • Son J.S.
        • Park S.O.
        Risk of transmission via medical employees and importance of routine infection-prevention policy in a nosocomial outbreak of Middle East respiratory syndrome (MERS): a descriptive analysis from a tertiary care hospital in South Korea.
        BMC Pulm Med. 2019; 19: 190
        • van Doremalen N.
        • Bushmaker T.
        • Munster V.J.
        Stability of Middle East respiratory syndrome coronavirus (MERS-CoV) under different environmental conditions.
        Euro Surveill. 2013; 18
        • Casanova L.M.
        • Jeon S.
        • Rutala W.A.
        • Weber D.J.
        • Sobsey M.D.
        Effects of air temperature and relative humidity on coronavirus survival on surfaces.
        Appl Environ Microbiol. 2010; 76: 2712-2717
        • Warnes S.L.
        • Little Z.R.
        • Keevil C.W.
        Human Coronavirus 229E Remains Infectious on Common Touch Surface Materials.
        mBio. 2015; 6: e01697-15
        • Sizun J.
        • Yu M.W.
        • Talbot P.J.
        Survival of human coronaviruses 229E and OC43 in suspension and after drying on surfaces: a possible source of hospital-acquired infections.
        J Hosp Infect. 2000; 46: 55-60
        • Duan S.M.
        • Zhao X.S.
        • Wen R.F.
        • Huang J.J.
        • Pi G.H.
        • Zhang S.X.
        • et al.
        Stability of SARS coronavirus in human specimens and environment and its sensitivity to heating and UV irradiation.
        Biomed Environ Sci. 2003; 16: 246-255
        • Lai M.Y.
        • Cheng P.K.
        • Lim W.W.
        Survival of severe acute respiratory syndrome coronavirus.
        Clin Infect Dis. 2005; 41: e67-e71
        • Chan K.H.
        • Peiris J.S.
        • Lam S.Y.
        • Poon L.L.
        • Yuen K.Y.
        • Seto W.H.
        The Effects of Temperature and Relative Humidity on the Viability of the SARS Coronavirus.
        Adv Virol. 2011; : 734690
        • Rabenau H.F.
        • Cinatl J.
        • Morgenstern B.
        • Bauer G.
        • Preiser W.
        • Doerr H.W.
        Stability and inactivation of SARS coronavirus.
        Med Microbiol Immunol. 2005; 194: 1-6
        • Rabenau H.F.
        • Kampf G.
        • Cinatl J.
        • Doerr H.W.
        Efficacy of various disinfectants against SARS coronavirus.
        J Hosp Infect. 2005; 61: 107-111
        • Saknimit M.
        • Inatsuki I.
        • Sugiyama Y.
        • Yagami K.
        Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals.
        Jikken Dobutsu Exp Anim. 1988; 37: 341-345
        • Wood A.
        • Payne D.
        The action of three antiseptics/disinfectants against enveloped and non-enveloped viruses.
        J Hosp Infect. 1998; 38: 283-295
        • Pratelli A.
        Action of disinfectants on canine coronavirus replication in vitro.
        Zoonoses Publ Health. 2007; 54: 383-386
        • Dellanno C.
        • Vega Q.
        • Boesenberg D.
        The antiviral action of common household disinfectants and antiseptics against murine hepatitis virus, a potential surrogate for SARS coronavirus.
        Am J Infect Control. 2009; 37: 649-652
        • Omidbakhsh N.
        • Sattar S.A.
        Broad-spectrum microbicidal activity, toxicologic assessment, and materials compatibility of a new generation of accelerated hydrogen peroxide-based environmental surface disinfectant.
        Am J Infect Control. 2006; 34: 251-257
        • Pratelli A.
        Canine coronavirus inactivation with physical and chemical agents.
        Vet J (London, England : 1997). 2008; 177: 71-79
        • Kariwa H.
        • Fujii N.
        • Takashima I.
        Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents.
        Dermatol (Basel, Switzerland). 2006; 212: 119-123
        • Eggers M.
        • Eickmann M.
        • Zorn J.
        Rapid and Effective Virucidal Activity of Povidone-Iodine Products Against Middle East Respiratory Syndrome Coronavirus (MERS-CoV) and Modified Vaccinia Virus Ankara (MVA).
        Infect Dis Ther. 2015; 4: 491-501
        • Eggers M.
        • Koburger-Janssen T.
        • Eickmann M.
        • Zorn J.
        In Vitro Bactericidal and Virucidal Efficacy of Povidone-Iodine Gargle/Mouthwash Against Respiratory and Oral Tract Pathogens.
        Infect Dis Ther. 2018; 7: 249-259
        • Hulkower R.L.
        • Casanova L.M.
        • Rutala W.A.
        • Weber D.J.
        • Sobsey M.D.
        Inactivation of surrogate coronaviruses on hard surfaces by health care germicides.
        Am J Infect Control. 2011; 39: 401-407
        • Sattar S.A.
        • Springthorpe V.S.
        • Karim Y.
        • Loro P.
        Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses.
        Epidemiol Infect. 1989; 102: 493-505
        • Goyal S.M.
        • Chander Y.
        • Yezli S.
        • Otter J.A.
        Evaluating the virucidal efficacy of hydrogen peroxide vapour.
        J Hosp Infect. 2014; 86: 255-259

      Linked Article