Inactivation of coronaviruses by heat

Sir

The global spread of COVID-19 has resulted in a huge demand for personal protective equipment including face masks [1]. Even some hospitals face a substantial shortage of suitable face masks (e.g. FFP masks or N95 masks) resulting in an evaluation of various procedures to reprocess them for a limited re-use. Although they are classified as single use products the question was raised if a thermal disinfection may be effective to reduce coronaviruses. That is why published data were reviewed to find out which temperature and exposure time is necessary for inactivation of coronaviruses.

A Medline search has been done on 20^th March 2020. The following terms were used, always in combination with “coronavirus”: heat inactivation (17 hits), heat disinfection (5 hits), heat inactivate (5 hits), heat kill (1 hit), thermal inactivation (6 hits), thermal disinfection (2 hits), thermal inactivate (3 hits) and thermal kill (0 hits). Publications were included and results were extracted given they provided original data on human (Severe Acute Respiratory Syndrome [SARS] coronavirus and Middle East Respiratory Syndrome [MERS] coronavirus) or zoonotic coronaviruses (Transmissible Gastroenteritis Virus [TGEV], Mouse Hepatitis Virus [MHV] and Porcine Epidemic Diarrhoea Virus [PEDV]) and their inactivation by various temperatures used for thermal disinfection. Reviews were not included but screened for any information within the scope of this review.

A total of 10 studies with original data were found. Overall a thermal disinfection at 60°C for 30 min, 65°C for 15 min and 80°C for 1 min was effective to strongly reduce coronavirus infectivity by at least 4 log₁₀ (Table 1 ).

Table I.

Heat inactivation of coronaviruses in test tube suspensions

Temperature	Virus	Strain/isolate	Exposure time	Reduction of viral infectivity (log10)	Reference
4°C	SARS-CoV	Strain FFM-1	30 min	0.0	[4]
4°C	PEDV	Strain CV777	2 h	0.0	[5]
25°C	MERS-CoV	Strain Hu/France–FRA2_130569/2013 (FRA2)	2 h	0.0	[6]
31°C	TGEV	Strain D52	80 min	0.7	[7]
35°C	TGEV	Strain D52	80 min	1.2	[7]
39°C	TGEV	Strain D52	80 min	3.0	[7]
40°C	MHV	Strains MHV-2 and MHV-N	30 min	0.3	[8]
40°C	PEDV	Strain CV777	2 h 75 min#	1.0 4.7	[5]
43°C	TGEV	Strain D52	50 min	3.8	[7]
44°C	PEDV	Strain CV777	2 h 45 min#	1.5 4.7	[5]
44°C	PEDV	Strain CV777	10 min	0.3	[9]
47°C	TGEV	Strain D52	20 min	4.2	[7]
48°C	PEDV	Strain CV777	2 h 15 min#	4.7 4.7	[5]
48°C	PEDV	Strain CV777	10 min	1.0–1.7	[9]
51°C	TGEV	Strain D52	5 min	4.4	[7]
55°C	TGEV	Strain D52	2 min	4.6	[7]
56°C	MERS-CoV	Strain Hu/France–FRA2_130569/2013 (FRA2)	30 s 15 min 30 min	0.1–0.9 ≥ 4.6 ≥ 4.3	[6]
56°C	SARS-CoV	Strain Hanoi	5 min 10 min 30 min	5.8 6.4 > 6.4	[10]
56°C	SARS-CoV	Strain FFM-1	30 min	1.9–5.0	[4]
56°C	SARS-CoV	Strain Urbani	20 min	≥ 4.3	[11]
60°C	MHV	Strains MHV-2 and MHV-N	1 min 5 min 15 min 30 min	2.6–2.9 3.6–3.9 > 3.9 > 3.9	[8]
60°C	SARS-CoV	Strain FFM-1	30 min	≥ 5.0	[4]
60°C	SARS-CoV	Strain FFM-1	30 min 60 min	≥ 4.0∗ ≥ 4.0	[12]
65°C	SARS-CoV	Strain Urbani	15 min	≥ 4.3∗∗	[11]
65°C	MERS-CoV	Strain Hu/France–FRA2_130569/2013 (FRA2)	30 s 15 min 30 min	0.9–3.6 ≥ 4.9 ≥ 4.9	[6]
65°C	SARS-CoV	Strain Urbani	10 min	≥ 4.3	[11]
65°C	MHV	Not described	15 min	≥ 6.0	[13]
80°C	MHV	Strains MHV-2 and MHV-N	1 min	> 3.9	[8]

^∗Not with anti-thrombin III as organic load;

^∗∗One outlier at 25 min with 3.6 log₁₀ explained by the authors with an experimental error;

^#In porcine plasma.

The effect of heat is explained by thermal aggregation of the SARS-CoV membrane protein [2]. It was shown that the nucleocapsid protein of SARS-CoV is completely denatured in 10 min at 55°C [3]. Health care providers may now have an idea what parameter for thermal disinfection may be effective in case of a lack of supply of appropriate face masks. One limitation is that all data described here were obtained with coronaviruses in suspension. That is why it may be possible that the results on dry surfaces may be different but this appears to be unlikely. Our data do not allow to evaluate if the function of a face mask remains unchanged after heat treatment. If thermal disinfection is used for the re-use of masks all institutions should evaluate the effect on their own masks in use, as different brands of masks and different specifications (e.g. with or without cellulose) will react individually towards a combination of time and heat. Easy tests to do are “fitting” and “water-resistance”. In addition, the numbers of re-uses should be traced (mark at the side of mask per cycle) and its effects examined.

Conflict of interest statement

None declared.