Literature DB >> 32614102

Using heat to kill SARS-CoV-2.

John P Abraham1, Brian D Plourde1, Lijing Cheng2.   

Abstract

The current coronavirus pandemic has reached global proportions and requires unparalleled collective and individual efforts to slow its spread. One critically important issue is the proper sterilization of physical objects that have been contaminated by the virus. Here, we review the currently existing literature on thermal inactivation of coronavirus (SARS-CoV-2) and present preliminary guideless on temperatures and exposure durations required to sterilize. We also compare these temperatures/exposure durations with potential household appliances that may be thought capable of performing sterilization.
© 2020 John Wiley & Sons, Ltd.

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Year:  2020        PMID: 32614102      PMCID: PMC7361064          DOI: 10.1002/rmv.2115

Source DB:  PubMed          Journal:  Rev Med Virol        ISSN: 1052-9276            Impact factor:   11.043


INTRODUCTION

As societies put themselves into voluntary or enforced isolation, large populations of people are experiencing reduced contact with others in public. When people venture into public, they are often donning masks (homemade or industrially produced) or other protective clothing. Upon returning to isolation, masks and other clothing should be treated as contaminated with virus. How should masks, clothing, and other items be treated? In many instances, simply setting items aside for a long enough period of time will kill the virus. However, the required durations are not known absolutely, and certainly depend on the type of surface. , , , , Some clothing types, for instance, are very capable of retaining moisture and consequently, this affects the survival of virus contained therein. The general consensus is that viruses can survive up to a few days in clothing. It is reasonable to expect a similar survival duration for viruses on/in protective face masks. That is, contaminated masks can be treated by merely setting them aside for some required duration until the viruses die. But to our best knowledge, there is no scientific study on the required duration, and any required duration would depend on the materials that form the mask. For instance, woven fibers differ from non‐woven polymeric filter media. Mask users can apply sanitizing chemicals (such as alcohol) but it is not clear whether this type of sanitizing would adversely affect the porous structure of masks and thereby make them less effective over time. Similarly, there is no current advice available for the use of heat to destroy SARS‐CoV‐2. Here, we summarize all the existing temperature/duration information for both SARS‐CoV‐2 and its sensitivity to heat. The summary is used to provide a reasonable recommendation for users to thermally destroy viruses on masks, clothing, or other objects.

Summary of the existing literature

An example of the state of knowledge on temperatures and coronavirus survival is provided by the CDC, which states: “Generally coronaviruses survive for shorter periods at higher temperatures and higher humidity than in cooler or dryer environments. However, we don't have direct data for this virus, nor do we have direct data for a temperature‐based cutoff for inactivation at this point. The necessary temperature would also be based on the materials of the surface, the environment, etc.”. But despite official statements such as the above, there is, in fact, some literature on the temperature and exposure durations that are required to inactivate SARS‐CoV‐2. In the following, a list of temperature/duration/inactivation rates is provided for coronavirus pathogens. In the listing, we report log reductions in viral load obtained from the references. In some studies, the heating protocol was such that no viral presence was detected afterwards. We have substituted an equivalent log reduction of 7 for these cases. Of course, the actual log reduction would be based on the sensitivity of the measurement instruments; however, for practical purposes, we consider a viral reduction of 7 or greater to be at or near total sterilization. In Table 1, we present this literature information. We note that there are differences in the strains and media in which the virus was cultivated. We also acknowledge that there are different thermal sensitivities for differing strains. It is further known that the media can affect the viral survival. For instance, media with protein content make the virus more resistant to heating. With this acknowledged, we opt to not provide separate analysis for different strains or media. Rather, our intent is to provide a single thermal recommendation that can be used to sterilize a broad range of materials.
TABLE 1

List of exposure temperatures and durations for inactivating coronavirus strains

Temperature (°C, °F)Duration (minutes)Log reductionVirusReferences
56, 133105SARS‐CoV (Urbani strain) 9
56, 133206SARS‐CoV (Urbani strain) 9
65, 14936SARS‐CoV (Urbani strain) 9
75, 167157SARS‐CoV (Urbani strain) 9
55, 1311205Gastroenteritis coronavirus 10
56, 133607Canine coronavirus 11
65, 149407Canine coronavirus 11
75, 167157Canine coronavirus 11
56, 133505Canine coronavirus 11
65, 14955Canine coronavirus 11
75, 16745Canine coronavirus 11
56, 13330>5SARS CoV, FFM1 no protein 12
50, 122301.9SARS, CoV, FFM1 With 20% protein 12
60, 14030>5SARS CoV, FFM1 no protein 12
60, 14030>5SARS, CoV, FFM1 With 20% protein 12
56, 13355.8SARS CoV (Hanoi strain) 13
56, 133106.5SARS CoV (Hanoi strain) 13
56, 13330>6.4SARS CoV (Hanoi strain) 13
56, 133302–5SARS CoV (FFM1 strain) 13
56, 13320>4.3SARS CoV (Urbani strain) 13
60, 14030>5SARS CoV (FFM1 strain) 13
60, 14030>4SARS CoV (FFM1 strain) 13
60, 14060>4SARS CoV (FFM1 strain) 13
65, 14910>4.3SARS CoV (Urbani strain) 13
List of exposure temperatures and durations for inactivating coronavirus strains What is seen from these tabulations is that the independent studies are mutually reinforcing. The results from Table 1 can be used to formulate general guidelines for the public.

Recommendations for thermally destroying coronavirus

We provide a reasonable estimate for near complete thermal destruction of coronavirus. For temperatures above 65°C (149°F) is expected to cause near complete inactivation with exposures greater than 3 minutes. For temperatures between 55 and 60°C (131‐140°F) heating should last 5 minutes or more. However, for temperatures in the range 50‐55°C (122‐131°F) we recommend 20 minutes or longer of exposure. At these levels, we expect the viral concentration to be lowered by log 5‐7, near or below the detectable limit. Because of the seriousness of the current coronavirus infection, we suggest a reasonable safety factor can be obtained by increasing the above‐listed temperatures by 10°C (about 18 °F). Extensive research has confirmed that at least for living cells, the sensitivity of thermal destruction is very strongly linked to temperature. That is, small increases in temperature cause large increases in the death rate. As an example, for mammalian cells and other pathogens (bacteria, viruses, and protozoa) the death rate rises rapidly as temperature increases. , Another reason for using a safety factor is that the temperatures experienced by the virus during heating will not necessarily equal the temperature of the applied heat. Thermal inertia causes a heating lag that depends, in part, on the media being heated. With this conservative approach, the following become the recommendations: In order to kill COVID‐19, heat virus‐containing objects for: 3 minutes at temperature above 75°C (160°F). 5 minutes for temperatures above 65°C (149°F). 20 minutes for temperatures above 60°C (140°F). It should be noted that these findings agree with WHO guidelines which report a 4 log reduction of coronavirus for 56°C (133°F) with 15‐minute exposures and is consistent with information for killing other infectious agents. These recommendations are hotter than encountered in residential clothes dryers, clothes washing machines, and dish washers. For these appliances, temperatures are typically at or below 57°C (135°F). These temperatures are also much hotter than residential hot water (in the United States), for example, plumbing codes limit hot water to 49°C (120°F). Of course, since soap has some virucide characteristics, washing with soap is expected to inactivate viruses by nonthermal means.

CONFLICT OF INTEREST

The authors declare no conflicts of interest.
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1.  Coronavirus survival on healthcare personal protective equipment.

Authors:  Lisa Casanova; William A Rutala; David J Weber; Mark D Sobsey
Journal:  Infect Control Hosp Epidemiol       Date:  2010-05       Impact factor: 3.254

2.  Effects of air temperature and relative humidity on coronavirus survival on surfaces.

Authors:  Lisa M Casanova; Soyoung Jeon; William A Rutala; David J Weber; Mark D Sobsey
Journal:  Appl Environ Microbiol       Date:  2010-03-12       Impact factor: 4.792

3.  Thermal inactivation studies of a coronavirus, transmissible gastroenteritis virus.

Authors:  H Laude
Journal:  J Gen Virol       Date:  1981-10       Impact factor: 3.891

Review 4.  Persistence of coronaviruses on inanimate surfaces and their inactivation with biocidal agents.

Authors:  G Kampf; D Todt; S Pfaender; E Steinmann
Journal:  J Hosp Infect       Date:  2020-02-06       Impact factor: 3.926

5.  Virus transfer from personal protective equipment to healthcare employees' skin and clothing.

Authors:  Lisa Casanova; Edie Alfano-Sobsey; William A Rutala; David J Weber; Mark Sobsey
Journal:  Emerg Infect Dis       Date:  2008-08       Impact factor: 6.883

Review 6.  Using heat to kill SARS-CoV-2.

Authors:  John P Abraham; Brian D Plourde; Lijing Cheng
Journal:  Rev Med Virol       Date:  2020-07-02       Impact factor: 11.043

Review 7.  Transmission of SARS and MERS coronaviruses and influenza virus in healthcare settings: the possible role of dry surface contamination.

Authors:  J A Otter; C Donskey; S Yezli; S Douthwaite; S D Goldenberg; D J Weber
Journal:  J Hosp Infect       Date:  2015-10-03       Impact factor: 3.926

8.  Canine coronavirus inactivation with physical and chemical agents.

Authors:  Annamaria Pratelli
Journal:  Vet J       Date:  2007-05-21       Impact factor: 2.688

9.  Inactivation of coronaviruses by heat.

Authors:  G Kampf; A Voss; S Scheithauer
Journal:  J Hosp Infect       Date:  2020-03-31       Impact factor: 3.926

10.  Stability and inactivation of SARS coronavirus.

Authors:  H F Rabenau; J Cinatl; B Morgenstern; G Bauer; W Preiser; H W Doerr
Journal:  Med Microbiol Immunol       Date:  2005-01       Impact factor: 3.402

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1.  A Methodology for Remote Microwave Sterilization Applicable to the Coronavirus and Other Pathogens Using Retrodirective Antenna Arrays.

Authors:  Konstantinos Kossenas; Symon K Podilchak; Davide Comite; Pascual D Hilario Re; George Goussetis; Sumanth K Pavuluri; Samantha J Griffiths; Robert J Chadwick; Chao Guo; Nico Bruns; Christine Tait-Burkard; Jurgen G Haas; Marc P Y Desmulliez
Journal:  IEEE J Electromagn RF Microw Med Biol       Date:  2021-05-03

2.  Quantifying pathogen infection risks from household laundry practices.

Authors:  Kelly A Reynolds; Marc P Verhougstraete; Kristina D Mena; Syed A Sattar; Elizabeth A Scott; Charles P Gerba
Journal:  J Appl Microbiol       Date:  2021-09-18       Impact factor: 4.059

Review 3.  Loop-Mediated Isothermal Amplification Detection of SARS-CoV-2 and Myriad Other Applications.

Authors:  Keith J M Moore; Jeremy Cahill; Guy Aidelberg; Rachel Aronoff; Ali Bektaş; Daniela Bezdan; Daniel J Butler; Sridar V Chittur; Martin Codyre; Fernan Federici; Nathan A Tanner; Scott W Tighe; Randy True; Sarah B Ware; Anne L Wyllie; Evan E Afshin; Andres Bendesky; Connie B Chang; Richard Dela Rosa; Eran Elhaik; David Erickson; Andrew S Goldsborough; George Grills; Kathrin Hadasch; Andrew Hayden; Seong-Young Her; Julie A Karl; Chang Hee Kim; Alison J Kriegel; Thomas Kunstman; Zeph Landau; Kevin Land; Bradley W Langhorst; Ariel B Lindner; Benjamin E Mayer; Lee A McLaughlin; Matthew T McLaughlin; Jenny Molloy; Christopher Mozsary; Jerry L Nadler; Melinee D'Silva; David Ng; David H O'Connor; Jerry E Ongerth; Olayinka Osuolale; Ana Pinharanda; Dennis Plenker; Ravi Ranjan; Michael Rosbash; Assaf Rotem; Jacob Segarra; Stephan Schürer; Scott Sherrill-Mix; Helena Solo-Gabriele; Shaina To; Merly C Vogt; Albert D Yu; Christopher E Mason
Journal:  J Biomol Tech       Date:  2021-09

4.  Effect of ambient temperature on respiratory tract cells exposed to SARS-CoV-2 viral mimicking nanospheres-An experimental study.

Authors:  Sachin Kumar; Alexandra Paul; Sayantan Chatterjee; Sabine Pütz; Natasha Nehra; Daniel S Wang; Arsalan Nisar; Christian M Jennings; Sapun H Parekh
Journal:  Biointerphases       Date:  2021-01-28       Impact factor: 2.456

5.  Thermal inactivation scaling applied for SARS-CoV-2.

Authors:  Shahar Seifer; Michael Elbaum
Journal:  Biophys J       Date:  2020-11-28       Impact factor: 4.033

6.  Decontamination and re-use of surgical masks and respirators during the COVID-19 pandemic.

Authors:  Marina Farrel Côrtes; Evelyn Patricia Sanchez Espinoza; Saidy Liceth Vásconez Noguera; Aline Alves Silva; Marion Elke Sielfeld Araya de Medeiros; Lucy Santos Villas Boas; Noely Evangelista Ferreira; Tania Regina Tozetto-Mendoza; Fernando Gonçalves Morais; Rayana Santiago de Queiroz; Adriana Coracini Tonacio de Proenca; Thais Guimaraes; Ana Rubia Guedes; Leila Suemi Harima Letaif; Amanda Cardoso Montal; Maria Cassia Mendes-Correa; Vanderley M John; Anna S Levin; Silvia Figueiredo Costa
Journal:  Int J Infect Dis       Date:  2020-12-24       Impact factor: 3.623

7.  Can shellfish be used to monitor SARS-CoV-2 in the coastal environment?

Authors:  Marion Desdouits; Jean-Côme Piquet; Candice Wacrenier; Cécile Le Mennec; Sylvain Parnaudeau; Sarah Jousse; Sophie Rocq; Lionel Bigault; Maud Contrant; Pascal Garry; Fabienne Chavanon; Raoul Gabellec; Laure Lamort; Luc Lebrun; Patrik Le Gall; Claire Meteigner; Anne Schmitt; Jean Luc Seugnet; Ophélie Serais; Cécile Peltier; Céline Bressolette-Bodin; Yannick Blanchard; Françoise S Le Guyader
Journal:  Sci Total Environ       Date:  2021-03-08       Impact factor: 7.963

Review 8.  The viability of SARS-CoV-2 on solid surfaces.

Authors:  Mohsen Hosseini; Saeed Behzadinasab; Zachary Benmamoun; William A Ducker
Journal:  Curr Opin Colloid Interface Sci       Date:  2021-06-16       Impact factor: 6.448

9.  Diverse high-affinity DNA aptamers for wild-type and B.1.1.7 SARS-CoV-2 spike proteins from a pre-structured DNA library.

Authors:  Jiuxing Li; Zijie Zhang; Jimmy Gu; Hannah D Stacey; Jann C Ang; Alfredo Capretta; Carlos D M Filipe; Karen L Mossman; Cynthia Balion; Bruno J Salena; Deborah Yamamura; Leyla Soleymani; Matthew S Miller; John D Brennan; Yingfu Li
Journal:  Nucleic Acids Res       Date:  2021-07-21       Impact factor: 16.971

Review 10.  Using heat to kill SARS-CoV-2.

Authors:  John P Abraham; Brian D Plourde; Lijing Cheng
Journal:  Rev Med Virol       Date:  2020-07-02       Impact factor: 11.043

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