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

G. Kampf; D. Todt; S. Pfaender; E. Steinmann

doi:10.1016/j.jhin.2020.01.022

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

G. Kampf^a^,^∗^,

Correspondence information about the author G. Kampf

Email the author G. Kampf

D. Todt^b

S. Pfaender^b

E. Steinmann^b

DOI: https://doi.org/10.1016/j.jhin.2020.01.022

Article Info

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:

Coronavirus, Persistence, Inanimate surfaces, Chemical inactivation, Biocidal agents, Disinfection

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) [1x[1]WHO. Coronavirus Disease 2019 (COVID-19). WHO, ; 2020 (Situation Report 23.)

Google Scholar See all References1]. Together with Severe Acute Respiratory Syndrome (SARS) coronavirus and Middle East Respiratory Syndrome (MERS) coronavirus [2x[2]de Wit, E., van Doremalen, N., Falzarano, D., and Munster, V.J. SARS and MERS: recent insights into emerging coronaviruses. Nat Rev Microbiol. 2016; 14: 523–534

Google Scholar See all References2], 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 [3x[3]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

Google Scholar See all References3]. 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 [4x[4]Otter, J.A., Donskey, C., Yezli, S., Douthwaite, S., Goldenberg, S.D., and 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

Google Scholar See all References4,5x[5]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

Google Scholar See all References5], emphasizing the importance of a detailed understanding of coronavirus persistence on inanimate surfaces [6x[6]Geller, C., Varbanov, M., and Duval, R.E. Human coronaviruses: insights into environmental resistance and its influence on the development of new antiseptic strategies. Viruses. 2012; 4: 3044–3068

Google Scholar See all References6]. Various types of biocidal agents such as hydrogen peroxide, alcohols, sodium hypochlorite or benzalkonium chloride are used worldwide for disinfection, mainly in healthcare settings [7x[7]Kampf, G. Antiseptic stewardship: biocide resistance and clinical implications. Springer International Publishing, Cham; 2018

Google Scholar See all References7]. 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 ITable I). In addition it was shown at room temperature that HCoV-229E persists better at 50% compared to 30% relative humidity [8x[8]Ijaz, M.K., Brunner, A.H., Sattar, S.A., Nair, R.C., and Johnson-Lussenburg, C.M. Survival characteristics of airborne human coronavirus 229E. J Gen Virol. 1985; 66: 2743–2748

Google Scholar See all References8].

Table IPersistence of coronaviruses on different types of inanimate surfaces
Type of surface	Virus	Strain / isolate	Inoculum (viral titer)	Temperature	Persistence	Reference
Steel	MERS-CoV	Isolate HCoV-EMC/2012	10⁵	20°C 30°C	48 h 8–24 h	[21x[21]van Doremalen, N., Bushmaker, T., and Munster, V.J. Stability of Middle East respiratory syndrome coronavirus (MERS-CoV) under different environmental conditions. Euro Surveill. 2013; 18 Google Scholar See all References21]
	TGEV	Unknown	10⁶	4°C 20°C 40°C	≥ 28 d 3–28 d 4–96 h	[22x[22]Casanova, L.M., Jeon, S., Rutala, W.A., Weber, D.J., and Sobsey, M.D. Effects of air temperature and relative humidity on coronavirus survival on surfaces. Appl Environ Microbiol. 2010; 76: 2712–2717 Google Scholar See all References22]
	MHV	Unknown	10⁶	4°C 20°C 40°C	≥ 28 d 4–28 d 4–96 h	[22x[22]Casanova, L.M., Jeon, S., Rutala, W.A., Weber, D.J., and Sobsey, M.D. Effects of air temperature and relative humidity on coronavirus survival on surfaces. Appl Environ Microbiol. 2010; 76: 2712–2717 Google Scholar See all References22]
	HCoV	Strain 229E	10³	21°C	5 d	[23x[23]Warnes, S.L., Little, Z.R., and Keevil, C.W. Human Coronavirus 229E Remains Infectious on Common Touch Surface Materials. mBio. 2015; 6: e01697–15 Google Scholar See all References23]
Aluminium	HCoV	Strains 229E and OC43	5 x 10³	21°C	2–8 h	[24x[24]Sizun, J., Yu, M.W., and 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 Google Scholar See all References24]
Metal	SARS-CoV	Strain P9	10⁵	RT	5 d	[25x[25]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 Google Scholar See all References25]
Wood	SARS-CoV	Strain P9	10⁵	RT	4 d	[25x[25]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 Google Scholar See all References25]
Paper	SARS-CoV	Strain P9	10⁵	RT	4–5 d	[25x[25]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 Google Scholar See all References25]
Paper	SARS-CoV	Strain GVU6109	10⁶ 10⁵ 10⁴	RT	24 h 3 h < 5 min	[26x[26]Lai, M.Y., Cheng, P.K., and Lim, W.W. Survival of severe acute respiratory syndrome coronavirus. Clin Infect Dis. 2005; 41: e67–e71 Google Scholar See all References26]
Glass	SARS-CoV	Strain P9	10⁵	RT	4 d	[25x[25]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 Google Scholar See all References25]
Glass	HCoV	Strain 229E	10³	21°C	5 d	[23x[23]Warnes, S.L., Little, Z.R., and Keevil, C.W. Human Coronavirus 229E Remains Infectious on Common Touch Surface Materials. mBio. 2015; 6: e01697–15 Google Scholar See all References23]
Plastic	SARS-CoV	Strain HKU39849	10⁵	22°-25°C	≤ 5 d	[27x[27]Chan, K.H., Peiris, J.S., Lam, S.Y., Poon, L.L., Yuen, K.Y., and Seto, W.H. The Effects of Temperature and Relative Humidity on the Viability of the SARS Coronavirus. Adv Virol. 2011; : 734690 Google Scholar See all References27]
	MERS-CoV	Isolate HCoV-EMC/2012	10⁵	20°C 30°C	48 h 8–24 h	[21x[21]van Doremalen, N., Bushmaker, T., and Munster, V.J. Stability of Middle East respiratory syndrome coronavirus (MERS-CoV) under different environmental conditions. Euro Surveill. 2013; 18 Google Scholar See all References21]
	SARS-CoV	Strain P9	10⁵	RT	4 d	[25x[25]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 Google Scholar See all References25]
	SARS-CoV	Strain FFM1	10⁷	RT	6–9 d	[28x[28]Rabenau, H.F., Cinatl, J., Morgenstern, B., Bauer, G., Preiser, W., and Doerr, H.W. Stability and inactivation of SARS coronavirus. Med Microbiol Immunol. 2005; 194: 1–6 Google Scholar See all References28]
	HCoV	Strain 229E	10⁷	RT	2–6 d	[28x[28]Rabenau, H.F., Cinatl, J., Morgenstern, B., Bauer, G., Preiser, W., and Doerr, H.W. Stability and inactivation of SARS coronavirus. Med Microbiol Immunol. 2005; 194: 1–6 Google Scholar See all References28]
PVC	HCoV	Strain 229E	10³	21°C	5 d	[23x[23]Warnes, S.L., Little, Z.R., and Keevil, C.W. Human Coronavirus 229E Remains Infectious on Common Touch Surface Materials. mBio. 2015; 6: e01697–15 Google Scholar See all References23]
Silicon rubber	HCoV	Strain 229E	10³	21°C	5 d	[23x[23]Warnes, S.L., Little, Z.R., and Keevil, C.W. Human Coronavirus 229E Remains Infectious on Common Touch Surface Materials. mBio. 2015; 6: e01697–15 Google Scholar See all References23]
Surgical glove (latex)	HCoV	Strains 229E and OC43	5 x 10³	21°C	≤ 8 h	[24x[24]Sizun, J., Yu, M.W., and 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 Google Scholar See all References24]
Disposable gown	SARS-CoV	Strain GVU6109	10⁶ 10⁵ 10⁴	RT	2 d 24 h 1 h	[26x[26]Lai, M.Y., Cheng, P.K., and Lim, W.W. Survival of severe acute respiratory syndrome coronavirus. Clin Infect Dis. 2005; 41: e67–e71 Google Scholar See all References26]
Ceramic	HCoV	Strain 229E	10³	21°C	5 d	[23x[23]Warnes, S.L., Little, Z.R., and Keevil, C.W. Human Coronavirus 229E Remains Infectious on Common Touch Surface Materials. mBio. 2015; 6: e01697–15 Google Scholar See all References23]
Teflon	HCoV	Strain 229E	10³	21°C	5 d	[23x[23]Warnes, S.L., Little, Z.R., and Keevil, C.W. Human Coronavirus 229E Remains Infectious on Common Touch Surface Materials. mBio. 2015; 6: e01697–15 Google Scholar See all References23]

View Table in HTML

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 IITable 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 IITable II).

Table IIInactivation of coronaviruses by different types of biocidal agents in suspension tests
Biocidal agent	Concentration	Virus	Strain / isolate	Exposure time	Reduction of viral infectivity (log₁₀)	Reference
Ethanol	95%	SARS-CoV	Isolate FFM-1	30 s	≥ 5.5	[29x[29]Rabenau, H.F., Kampf, G., Cinatl, J., and Doerr, H.W. Efficacy of various disinfectants against SARS coronavirus. J Hosp Infect. 2005; 61: 107–111 Google Scholar See all References29]
	85%	SARS-CoV	Isolate FFM-1	30 s	≥ 5.5	[29x[29]Rabenau, H.F., Kampf, G., Cinatl, J., and Doerr, H.W. Efficacy of various disinfectants against SARS coronavirus. J Hosp Infect. 2005; 61: 107–111 Google Scholar See all References29]
	80%	SARS-CoV	Isolate FFM-1	30 s	≥ 4.3	[29x[29]Rabenau, H.F., Kampf, G., Cinatl, J., and Doerr, H.W. Efficacy of various disinfectants against SARS coronavirus. J Hosp Infect. 2005; 61: 107–111 Google Scholar See all References29]
	80%	MERS-CoV	Strain EMC	30 s	> 4.0	[14x[14]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 Google Scholar See all References14]
	78%	SARS-CoV	Isolate FFM-1	30 s	≥ 5.0	[28x[28]Rabenau, H.F., Cinatl, J., Morgenstern, B., Bauer, G., Preiser, W., and Doerr, H.W. Stability and inactivation of SARS coronavirus. Med Microbiol Immunol. 2005; 194: 1–6 Google Scholar See all References28]
	70%	MHV	Strains MHV-2 and MHV-N	10 min	> 3.9	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
	70%	CCV	Strain I-71	10 min	> 3.3	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
2-Propanol	100%	SARS-CoV	Isolate FFM-1	30 s	≥ 3.3	[28x[28]Rabenau, H.F., Cinatl, J., Morgenstern, B., Bauer, G., Preiser, W., and Doerr, H.W. Stability and inactivation of SARS coronavirus. Med Microbiol Immunol. 2005; 194: 1–6 Google Scholar See all References28]
	75%	SARS-CoV	Isolate FFM-1	30 s	≥ 4.0	[14x[14]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 Google Scholar See all References14]
	75%	MERS-CoV	Strain EMC	30 s	≥ 4.0	[14x[14]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 Google Scholar See all References14]
	70%	SARS-CoV	Isolate FFM-1	30 s	≥ 3.3	[28x[28]Rabenau, H.F., Cinatl, J., Morgenstern, B., Bauer, G., Preiser, W., and Doerr, H.W. Stability and inactivation of SARS coronavirus. Med Microbiol Immunol. 2005; 194: 1–6 Google Scholar See all References28]
	50%	MHV	Strains MHV-2 and MHV-N	10 min	> 3.7	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
	50%	CCV	Strain I-71	10 min	> 3.7	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
2-Propanol and 1-propanol	45% and 30%	SARS-CoV	Isolate FFM-1	30 s	≥ 4.3	[29x[29]Rabenau, H.F., Kampf, G., Cinatl, J., and Doerr, H.W. Efficacy of various disinfectants against SARS coronavirus. J Hosp Infect. 2005; 61: 107–111 Google Scholar See all References29]
2-Propanol and 1-propanol	45% and 30%	SARS-CoV	Isolate FFM-1	30 s	≥ 2.8	[28x[28]Rabenau, H.F., Cinatl, J., Morgenstern, B., Bauer, G., Preiser, W., and Doerr, H.W. Stability and inactivation of SARS coronavirus. Med Microbiol Immunol. 2005; 194: 1–6 Google Scholar See all References28]
Benzalkonium chloride	0.2%	HCoV	ATCC VR-759 (strain OC43)	10 min	0.0	[31x[31]Wood, A. and Payne, D. The action of three antiseptics/disinfectants against enveloped and non-enveloped viruses. J Hosp Infect. 1998; 38: 283–295 Google Scholar See all References31]
	0.05%	MHV	Strains MHV-2 and MHV-N	10 min	> 3.7	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
	0.05%	CCV	Strain I-71	10 min	> 3.7	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
	0.00175%	CCV	Strain S378	3 d	3.0	[32x[32]Pratelli, A. Action of disinfectants on canine coronavirus replication in vitro. Zoonoses Publ Health. 2007; 54: 383–386 Google Scholar See all References32]
Didecyldimethyl ammonium chloride	0.0025%	CCV	Strain S378	3 d	> 4.0	[32x[32]Pratelli, A. Action of disinfectants on canine coronavirus replication in vitro. Zoonoses Publ Health. 2007; 54: 383–386 Google Scholar See all References32]
Chlorhexidine digluconate	0.02%	MHV	Strains MHV-2 and MHV-N	10 min	0.7–0.8	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
Chlorhexidine digluconate	0.02%	CCV	Strain I-71	10 min	0.3	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
Sodium hypochlorite	0.21%	MHV	Strain MHV-1	30 s	≥ 4.0	[33x[33]Dellanno, C., Vega, Q., and 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 Google Scholar See all References33]
	0.01%	MHV	Strains MHV-2 and MHV-N	10 min	2.3–2.8	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
	0.01%	CCV	Strain I-71	10 min	1.1	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
	0.001%	MHV	Strains MHV-2 and MHV-N	10 min	0.3–0.6	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
	0.001%	CCV	Strain I-71	10 min	0.9	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
Hydrogen peroxide	0.5%	HCoV	Strain 229E	1 min	> 4.0	[34x[34]Omidbakhsh, N. and 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 Google Scholar See all References34]
Formaldehyde	1%	SARS-CoV	Isolate FFM-1	2 min	> 3.0	[28x[28]Rabenau, H.F., Cinatl, J., Morgenstern, B., Bauer, G., Preiser, W., and Doerr, H.W. Stability and inactivation of SARS coronavirus. Med Microbiol Immunol. 2005; 194: 1–6 Google Scholar See all References28]
	0.7%	SARS-CoV	Isolate FFM-1	2 min	> 3.0	[28x[28]Rabenau, H.F., Cinatl, J., Morgenstern, B., Bauer, G., Preiser, W., and Doerr, H.W. Stability and inactivation of SARS coronavirus. Med Microbiol Immunol. 2005; 194: 1–6 Google Scholar See all References28]
	0.7%	MHV		10 min	> 3.5	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
	0.7%	CCV	Strain I-71	10 min	> 3.7	[30x[30]Saknimit, M., Inatsuki, I., Sugiyama, Y., and Yagami, K. Virucidal efficacy of physico-chemical treatments against coronaviruses and parvoviruses of laboratory animals. Jikken Dobutsu Exp Anim. 1988; 37: 341–345 Google Scholar See all References30]
	0.009%	CCV		24 h	> 4.0	[35x[35]Pratelli, A. Canine coronavirus inactivation with physical and chemical agents. Vet J (London, England : 1997). 2008; 177: 71–79 Google Scholar See all References35]
Glutardialdehyde	2.5%	SARS-CoV	Hanoi strain	5 min	> 4.0	[36x[36]Kariwa, H., Fujii, N., and Takashima, I. Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents. Dermatol (Basel, Switzerland). 2006; 212: 119–123 Google Scholar See all References36]
Glutardialdehyde	0.5%	SARS-CoV	Isolate FFM-1	2 min	> 4.0	[28x[28]Rabenau, H.F., Cinatl, J., Morgenstern, B., Bauer, G., Preiser, W., and Doerr, H.W. Stability and inactivation of SARS coronavirus. Med Microbiol Immunol. 2005; 194: 1–6 Google Scholar See all References28]
Povidone iodine	7.5%	MERS-CoV	Isolate HCoV-EMC/2012	15 s	4.6	[37x[37]Eggers, M., Eickmann, M., and 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 Google Scholar See all References37]
	4%	MERS-CoV	Isolate HCoV-EMC/2012	15 s	5.0	[37x[37]Eggers, M., Eickmann, M., and 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 Google Scholar See all References37]
	1%	SARS-CoV	Hanoi strain	1 min	> 4.0	[36x[36]Kariwa, H., Fujii, N., and Takashima, I. Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents. Dermatol (Basel, Switzerland). 2006; 212: 119–123 Google Scholar See all References36]
	1%	MERS-CoV	Isolate HCoV-EMC/2012	15 s	4.3	[37x[37]Eggers, M., Eickmann, M., and 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 Google Scholar See all References37]
	0.47%	SARS-CoV	Hanoi strain	1 min	3.8	[36x[36]Kariwa, H., Fujii, N., and Takashima, I. Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents. Dermatol (Basel, Switzerland). 2006; 212: 119–123 Google Scholar See all References36]
	0.25%	SARS-CoV	Hanoi strain	1 min	> 4.0	[36x[36]Kariwa, H., Fujii, N., and Takashima, I. Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents. Dermatol (Basel, Switzerland). 2006; 212: 119–123 Google Scholar See all References36]
	0.23%	SARS-CoV	Hanoi strain	1 min	> 4.0	[36x[36]Kariwa, H., Fujii, N., and Takashima, I. Inactivation of SARS coronavirus by means of povidone-iodine, physical conditions and chemical reagents. Dermatol (Basel, Switzerland). 2006; 212: 119–123 Google Scholar See all References36]
	0.23%	SARS-CoV	Isolate FFM-1	15 s	≥ 4.4	[38x[38]Eggers, M., Koburger-Janssen, T., Eickmann, M., and 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 Google Scholar See all References38]
	0.23%	MERS-CoV	Isolate HCoV-EMC/2012	15 s	≥ 4.4	[38x[38]Eggers, M., Koburger-Janssen, T., Eickmann, M., and 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 Google Scholar See all References38]

View Table in HTML

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 IIITable III).

Table IIIInactivation of coronaviruses by different types of biocidal agents in carrier tests
Biocidal agent	Concentration	Virus	Strain / isolate	Volume / material	Organic load	Exposure time	Reduction of viral infectivity (log₁₀)	Reference
Ethanol	71%	TGEV	Unknown	50 μl / stainless steel	None	1 min	3.5	[39x[39]Hulkower, R.L., Casanova, L.M., Rutala, W.A., Weber, D.J., and Sobsey, M.D. Inactivation of surrogate coronaviruses on hard surfaces by health care germicides. Am J Infect Control. 2011; 39: 401–407 Google Scholar See all References39]
	71%	MHV	Unknown	50 μl / stainless steel	None	1 min	2.0	[39x[39]Hulkower, R.L., Casanova, L.M., Rutala, W.A., Weber, D.J., and Sobsey, M.D. Inactivation of surrogate coronaviruses on hard surfaces by health care germicides. Am J Infect Control. 2011; 39: 401–407 Google Scholar See all References39]
	70%	TGEV	Unknown	50 μl / stainless steel	None	1 min	3.2	[39x[39]Hulkower, R.L., Casanova, L.M., Rutala, W.A., Weber, D.J., and Sobsey, M.D. Inactivation of surrogate coronaviruses on hard surfaces by health care germicides. Am J Infect Control. 2011; 39: 401–407 Google Scholar See all References39]
	70%	MHV	Unknown	50 μl / stainless steel	None	1 min	3.9	[39x[39]Hulkower, R.L., Casanova, L.M., Rutala, W.A., Weber, D.J., and Sobsey, M.D. Inactivation of surrogate coronaviruses on hard surfaces by health care germicides. Am J Infect Control. 2011; 39: 401–407 Google Scholar See all References39]
	70%	HCoV	Strain 229E	20 μl / stainless steel	5% serum	1 min	> 3.0	[40x[40]Sattar, S.A., Springthorpe, V.S., Karim, Y., and Loro, P. Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses. Epidemiol Infect. 1989; 102: 493–505 Google Scholar See all References40]
	62%	TGEV	Unknown	50 μl / stainless steel	None	1 min	4.0	[39x[39]Hulkower, R.L., Casanova, L.M., Rutala, W.A., Weber, D.J., and Sobsey, M.D. Inactivation of surrogate coronaviruses on hard surfaces by health care germicides. Am J Infect Control. 2011; 39: 401–407 Google Scholar See all References39]
	62%	MHV	Unknown	50 μl / stainless steel	None	1 min	2.7	[39x[39]Hulkower, R.L., Casanova, L.M., Rutala, W.A., Weber, D.J., and Sobsey, M.D. Inactivation of surrogate coronaviruses on hard surfaces by health care germicides. Am J Infect Control. 2011; 39: 401–407 Google Scholar See all References39]
Benzalkoniumchloride	0.04%	HCoV	Strain 229E	20 μl / stainless steel	5% serum	1 min	< 3.0	[40x[40]Sattar, S.A., Springthorpe, V.S., Karim, Y., and Loro, P. Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses. Epidemiol Infect. 1989; 102: 493–505 Google Scholar See all References40]
Sodium hypochlorite	0.5%	HCoV	Strain 229E	20 μl / stainless steel	5% serum	1 min	> 3.0	[40x[40]Sattar, S.A., Springthorpe, V.S., Karim, Y., and Loro, P. Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses. Epidemiol Infect. 1989; 102: 493–505 Google Scholar See all References40]
	0.1%	HCoV	Strain 229E	20 μl / stainless steel	5% serum	1 min	> 3.0	[40x[40]Sattar, S.A., Springthorpe, V.S., Karim, Y., and Loro, P. Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses. Epidemiol Infect. 1989; 102: 493–505 Google Scholar See all References40]
	0.06%	TGEV	Unknown	50 μl / stainless steel	None	1 min	0.4	[39x[39]Hulkower, R.L., Casanova, L.M., Rutala, W.A., Weber, D.J., and Sobsey, M.D. Inactivation of surrogate coronaviruses on hard surfaces by health care germicides. Am J Infect Control. 2011; 39: 401–407 Google Scholar See all References39]
	0.06%	MHV	Unknown	50 μl / stainless steel	None	1 min	0.6	[39x[39]Hulkower, R.L., Casanova, L.M., Rutala, W.A., Weber, D.J., and Sobsey, M.D. Inactivation of surrogate coronaviruses on hard surfaces by health care germicides. Am J Infect Control. 2011; 39: 401–407 Google Scholar See all References39]
	0.01%	HCoV	Strain 229E	20 μl / stainless steel	5% serum	1 min	< 3.0	[40x[40]Sattar, S.A., Springthorpe, V.S., Karim, Y., and Loro, P. Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses. Epidemiol Infect. 1989; 102: 493–505 Google Scholar See all References40]
Glutardialdehyde	2%	HCoV	Strain 229E	20 μl / stainless steel	5% serum	1 min	> 3.0	[40x[40]Sattar, S.A., Springthorpe, V.S., Karim, Y., and Loro, P. Chemical disinfection of non-porous inanimate surfaces experimentally contaminated with four human pathogenic viruses. Epidemiol Infect. 1989; 102: 493–505 Google Scholar See all References40]
Ortho-phtalaldehyde	0.55%	TGEV	Unknown	50 μl / stainless steel	None	1 min	2.3	[39x[39]Hulkower, R.L., Casanova, L.M., Rutala, W.A., Weber, D.J., and Sobsey, M.D. Inactivation of surrogate coronaviruses on hard surfaces by health care germicides. Am J Infect Control. 2011; 39: 401–407 Google Scholar See all References39]
Ortho-phtalaldehyde	0.55%	MHV	Unknown	50 μl / stainless steel	None	1 min	1.7	[39x[39]Hulkower, R.L., Casanova, L.M., Rutala, W.A., Weber, D.J., and Sobsey, M.D. Inactivation of surrogate coronaviruses on hard surfaces by health care germicides. Am J Infect Control. 2011; 39: 401–407 Google Scholar See all References39]
Hydrogen peroxide	Vapor of unknown concentration	TGEV	Purdue strain type 1	20 μl / stainless steel	None	2–3 h	4.9–5.3*	[41x[41]Goyal, S.M., Chander, Y., Yezli, S., and Otter, J.A. Evaluating the virucidal efficacy of hydrogen peroxide vapour. J Hosp Infect. 2014; 86: 255–259 Google Scholar See all References41]

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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 [9x[9]Bean, B., Moore, B.M., Sterner, B., Peterson, L.R., Gerding, D.N., and Balfour, H.H. Survival of influenza viruses an environmental surfaces. J Infect Dis. 1982; 146: 47–51

Google Scholar See all References9]. The transfer efficiency was lower (1.5%) with parainfluenza virus 3 and a 5 s contact between the surface and the hands [10x[10]Ansari, S.A., Springthorpe, V.S., Sattar, S.A., Rivard, S., and 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

Google Scholar See all References10]. 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%) [11x[11]Kwok, Y.L., Gralton, J., and McLaws, M.L. Face touching: a frequent habit that has implications for hand hygiene. Am J Infect Contr. 2015; 43: 112–114

Google Scholar See all References11]. 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.” [12x[12]WHO. Infection prevention and control during health care when novel coronavirus (nCoV) infection is suspected. WHO, ; 2020 (Interim guidance. 25 January 2020)

Google Scholar See all References12] The typical use of bleach is at a dilution of 1:100 of 5% sodium hypochlorite resulting in a final concentration of 0.05% [13x[13]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, Geneva; 2014: 65–66

Google Scholar See all References13]. Our summarized data with coronaviruses suggest that a concentration of 0.1% is effective in 1 min (Table IIITable 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 [13x[13]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, Geneva; 2014: 65–66

Google Scholar See all References13].

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 [14x[14]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

Google Scholar See all References14]. 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 [15x[15]Yen, M.Y., Lu, Y.C., Huang, P.H., Chen, C.M., Chen, Y.C., and 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

Google Scholar See all References15]. Compliance with hand hygiene can be significantly higher in an outbreak situation but is likely to remain an obstacle especially among physicians [16x[16]Alshammari, M., Reynolds, K.A., Verhougstraete, M., and 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

Google Scholar See all References, 17x[17]Al-Tawfiq, J.A., Abdrabalnabi, R., Taher, A., Mathew, S., and Rahman, K.A. Infection control influence of Middle East respiratory syndrome coronavirus: A hospital-based analysis. Am J Infect Contr. 2019; 47: 431–434

Google Scholar See all References, 18x[18]Wong, T.W. and 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

Google Scholar See all References]. Transmission in healthcare settings can be successfully prevented when appropriate measures are consistently performed [19x[19]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

Google Scholar See all References19,20x[20]Ki, H.K., Han, S.K., Son, J.S., and 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

Google Scholar See all References20].

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.

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

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Article Info

Article Outline

Summary

Keywords:

Introduction

Method

Results

Persistence of coronavirus on inanimate surfaces

Inactivation of coronaviruses by biocidal agents in suspension tests

Inactivation of coronaviruses by biocidal agents in carrier tests

Discussion

Conclusions

Conflict of interest statement

Funding Sources

References

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