key: cord-315637-7td617dm
authors: Rothe, M.; Rohm, E.; Mitchell, E.; Bedrosian, N.; Kelly, C.; String, G.; Lantagne, D. S.
title: A systematic review of mask disinfection and reuse for SARS-CoV-2
date: 2020-11-12
journal: nan
DOI: 10.1101/2020.11.11.20229880
sha: 
doc_id: 315637
cord_uid: 7td617dm

We conducted a systematic review of hygiene intervention effectiveness against SARS-CoV-2, including developing inclusion criteria, conducting the search, selecting articles for inclusion, and summarizing included articles. We reviewed 104,735 articles, and 109 articles meeting inclusion criteria were identified, with 33 additional articles identified from reference chaining. Herein, we describe results from 58 mask disinfection and reuse studies, where the majority of data were collected using N95 masks. Please note, no disinfection method consistently removed >3 log of virus irrespective of concentration, contact time, temperature, and humidity. However, results show it is possible to achieve >3 log reduction of SARS-CoV-2 using appropriate concentrations and contact times of chemical (ethanol, hydrogen peroxide, peracetic acid), radiation (PX-UV, UVGI), and thermal (autoclaving, heat) disinfection on N95 masks. N95 mask reuse and failure data indicate that hydrogen peroxide, heat, and UV-GI are promising for mask reuse, peracetic acid and PX-UV need more data, and autoclaving and ethanol lead to mask durability failures. Data on other mask types is limited. We thus recommend focusing guidelines and further research on the use of heat, hydrogen peroxide, and UVGI for N95 mask disinfection/reuse. All of these disinfection options could be investigated for use in LMIC and humanitarian contexts.

masks. N95 mask reuse and failure data indicate that hydrogen peroxide, heat, and UV-GI are promising 23 for mask reuse, peracetic acid and PX-UV need more data, and autoclaving and ethanol lead to mask 24 durability failures. Data on other mask types is limited. We thus recommend focusing guidelines and 25 further research on the use of heat, hydrogen peroxide, and UVGI for N95 mask disinfection/reuse. All of 26 these disinfection options could be investigated for use in LMIC and humanitarian contexts. Synopsis:

In resource-limited contexts, N95s are reused. We recommend using heat, hydrogen 34 peroxide, or UVGI to disinfect and reuse N95 masks. 35

In December 2019, novel coronavirus SARS-CoV-2 emerged into the human population, leading to a 37 worldwide pandemic. 1 Due to lack of medical counter-measures, measures to prevent SARS-CoV-2 38 transmission include physical distancing, masking, hand hygiene, and surface disinfection. 2 39

While SARS-CoV-2 has global impact, people living in low-and middle-income countries (LMIC) and 40 humanitarian contexts are particularly impacted by COVID-19. 3 SARS-CoV-2 transmission is enabled in 41 areas with overcrowded living situations, poor hygiene conditions, and lack of access to personal 42 protective equipment (PPE). 4 Moreover, refugees, displaced persons, and people in informal settlements 43 in LMIC are particularly vulnerable populations, due to living in crowded conditions with weakened 44 health systems and poor water and sanitation infrastructure. 5, 6 45

One hygiene intervention increasingly being used in SARS-CoV-2 contexts is cleaning and/or 46 disinfecting masks for reuse in resource-limited contexts. 7 Since December 2019, there has been an 47

In total, 92 individual mask disinfection tests were conducted across 32 studies 12, 13, 15, 18-20, 22-24, 27-31, 33, 36, 111 38, 40, 41, 43, 44, 47-49, 51, 56, 62-67 . The masks tested included: 75 tests with N95s (82%), 5 (5%) with cloth masks, 112 4 (4%) with surgical masks, three (3%) with KN95s, three (3%) with Tyvek, and 1 (1%) with a plastic 113 face shield and 1 (1%) unspecified. Please note 78 (85%) are considered respirators (N95s and KN95s). 114

Disinfection methods were grouped into three categories: chemical disinfection, radiation disinfection, 115 and thermal disinfection. In total, 31 chemical disinfection tests were conducted (34% of tests), including 116 15 tests with various forms of hydrogen peroxide (aerosolized, gas plasma, ionized, vapor), ozone gas 117 (11), ethanol (2), peracetic acid with hydrogen peroxide (1), peracetic acid (1), and ethylene oxide (1). In 118 total, 18 radiation disinfection tests were conducted, including 15 with ultraviolet germicidal irradiation 119 (UVGI) and three with pulsed xenon UV (PX-UV). In total, 43 (47%) thermal disinfection tests were 120 conducted, including moist heat (17 samples), dry heat (14), steaming (5), microwave generated steam 121 (MGS) (5), autoclave (1), and heat (1). Please note disinfection efficacy was calculated using log 122 reductions, or if not available, in a "complete inactivation" binary metric as reported by study authors. 123

Of the 92 total tests, 21 were conducted with MS-2, 15 with SARS-CoV-2, 12 with IAV, 8 with Phi6, 8 124 with H1N1, 6 with PCRV, 6 with a mixture (MS2, Phi6, IAV, MHV), 3 with MHV, 3 with H5N1, 2 with 125 P22, and 1 each with Tulane virus, TGEV, Rotavirus, PPV, HCoV-229E, Canine parvovirus, BVDV, and 126

As can be seen, while the majority of data were collected on N95s, there was high variability in the 128 number of disinfectants tested against SARS-CoV-2 and surrogates used for testing. Limiting the results 129 to N95 masks only, there were 15 tests using SARS-CoV-2, 18 using MS2, eight using Phi6, eight using 130 H1N1, and six using IAV. 131

In the 15 SARS-CoV-2 N95 mask samples, eight were chemical (hydrogen peroxide 15, 29, 30, 36, 48 , ethanol 15, 132 29 , peracetic acid 30 ), four were radiation (PX-UV 13 , UVGI 15, 29, 31 ), and three were thermal (autoclave 30 , 133 . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 12, 2020. ; dry heat 29, 49 ). All applications of hydrogen peroxide (10-210 minute exposure), ethanol (spraying, 134 saturation), and 10% peracetic acid (60 minute exposure) achieved SARS-CoV-2 inactivation or >3 log 135 reduction. PX-UV and UVGI achieved >3 log reduction with ≥ 5 minute contact time. Dry 70°C heat for 136 50 minutes and autoclaving at 121°C for 15 minutes led to >5 and >6 log reduction, respectively. Please 137 note all methods tested achieved inactivation (binary) or >3 log reduction except for UVGI at 2 minutes 138 contact time. 139

In the 18 MS2 results 22, 23, 44, 56, 64, 66, 72 , UVGI for 1-10 minutes did not achieve >3 log reduction, nor did 140 70°C dry heat for 15-30 minutes. Steam for 10 seconds -15 minutes did achieve >3 log reduction. Moist 141 heat at 72-82°C for 30 minutes did achieve >6 log reductions when humidity was >25% or >50%. The 142 results from the eight H1N1 results 33, 38, 63, 65 were presented in log reduction ranges, not specific log 143 reductions, which precludes analysis herein. In the eight Phi6 results 27, 40, 56, 72 , moist heat at 72-82°C for 144 30 minutes achieved <6 or >6 log reduction but inaccurate humidity readings occlude results, 7% 145 aerosolized hydrogen peroxide had >6 log reductions with 30 minute exposure, and VHP at 16 146 gram/minute had >4 log after 30-40 minute exposure time; please note UVGI for one minute had only 1.5 147 log reduction. In the six IAV samples 41, 43, 56, 63 , ozone removed 1-2 log after 40 minute exposure to 20 148 ppm, and moist heat and MGS achieved >3 log reduction after 30 minutes exposure to 60-82C moist heat 149 for 30 minutes and 2 minute exposure to MGS. 150

Five tests were conducted on cloth masks 23, 41 , using ozone gas against IAV, and heat/steam against MS2. 151

Steaming for 15 minutes achieved >15 log reduction (the only method to achieve >3). Four tests were 152 conducted on surgical masks 24, 64 , using UVGI for 2 minutes, dry heat at 102°C for 60 minutes, VHP for 153 20 minutes, and MGS for 30 minutes; all achieved >3 log reduction. In three tests on Tyvek 41 , ozone gas 154 at 20 ppm for 40 minutes led to ~1-2 log reductions of IAV. On one face shield 67 , PX-UV reduced canine 155 parvovirus by >4 log with 5 minute exposure time. Studies noted radiation disinfection did not deactivate 156 viruses in a uniform manner due to the complex shapes of masks, thus masks should not be stacked if UV 157 disinfection is used. 158 . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 12, 2020. ;

Please note no disinfection method consistently removed >3 log reduction of virus irrespective of 159 concentration, contact time, temperature, and humidity. However, results did show that it is possible to 160 achieve >3 log reduction of SARS-CoV-2 using appropriate concentrations and contact times of chemical 161 (ethanol, hydrogen peroxide, peracetic acid), radiation (PX-UV, UVGI), and thermal (autoclaving, heat) 162 disinfection. 163 164 165 . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 12, 2020. ; https://doi.org/10.1101/2020.11.11.20229880 doi: medRxiv preprint

Mask durability was assessed based on four criteria: filtration, fit, fiber resilience, and strap performance. 167

Disinfection cycles were also noted, and the maximum amount of cycles was determined when a failure 168 was recorded in any of the four criteria. 169

In total, 159 individual mask reuse tests were conducted in 42 studies 7, 12, 14-17, 19-22, 25-30, 32-37, 39, 42, 45-47, 49-55, 170 57-62, 64, 68 . The masks tested included: 114 tests with N95s (72%), an additional four tests with KN95s 171

(2.5%), seven tests with folded or molded or HKYZ N95s (4.4%), four tests with FFPs (2.5%), and two 172 tests with respirator fabric (1%). Thus a total of 131 tests (82%) were conducted with respirators. 173

Additionally, 11 tests were conducted with surgical masks (7%), five with nanofiber filter masks (3.1%), 174 four with procedure masks (2.5%), three with sterilization wrap (2%) and EX101 masks (2%), and one 175 (1%) with a cloth mask, and one (1%) unspecified. 176

Disinfection methods were grouped into three categories: chemical disinfection, radiation disinfection, 177 and thermal disinfection. In total, 65 chemical reuse tests were conducted (41% of tests), including 20 178 tests with forms of hydrogen peroxide, ethanol (20), isopropyl alcohol (7), bleach (5), ethylene oxide (5), 179 soap and water (3), ozone gas (3), peracetic acid (1), and household detergent (1). In total, 24 radiation 180 reuse tests were conducted (15%), including 15 with ultraviolet germicidal irradiation (UVGI), five with 181 gamma radiation, three with microwaves, and one with pulsed xenon UV (PX-UV). In total, 70 (44%) 182 thermal reuse tests were conducted, including dry heat (23 samples), autoclave (16), steam (10), moist 183 heat (9), microwave generated steam (6), heat (3), hot water soak (2), and boiling (1). 184

The majority of data were collected on N95s. Given the wide differences in test conditions, results are 185 summarized by disinfection agent for N95s only, for agents with >5 samples or those agents identified in 186 the disinfection efficacy section as achieving >3 log reduction of SARS-CoV-2, including ethanol, 187 hydrogen peroxide, peracetic acid, PX-UV, UVGI, autoclaving, and heat. 188 . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 12, 2020. ; https://doi.org/10. 1101 /2020 Autoclaving (n=14) 14, 30, 34, 42, 45, 55, 57, 59 and ethanol disinfection (n=14) 15-17, 29, 42, 45, 53, 58 led to failures 189 within two disinfection cycles in 12 and 13 tests, respectively. This indicates these methods cannot be 190 utilized for N95 reuse. 191

Steam (n=5) 16, 26, 42, 52 and moist heat (n=9) 7, 19, 28, 32, 45, 61, 62 had mixed results, with 3 failures in 1-5 cycles 192 (but two tests that lasted up to 1-10 cycles), 4 failures in 0-4 cycles (and four tests with no failure in 1-10 193 cycles and one not recorded), respectively. More research is indicated to understand these results. 194

Hydrogen peroxide disinfection (n=20) 15, 19, 27, 29, 30, 36, 45, 51, 57, [59] [60] [61] 68 , dry heat (n=19) 12, 16, 19, 21, 29, 33-35, 42, 45, 195 49, 50, 52, 54 , UVGI (n=13) 15, 16, 29, 35, 42, 45, 46, 52, [59] [60] [61] [62] , and ethylene oxide (n=5) CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this this version posted November 12, 2020. ; https://doi.org/10.1101/2020.11.11.20229880 doi: medRxiv preprint

Our overall goal was to complete a systematic review of transmission pathways of SARS-CoV-2 that 206 could be interrupted with WASH interventions, with a focus on LMIC and humanitarian contexts. After 207 completing title, abstract, and full-text review of 104,735 articles, 109 articles meeting inclusion criteria 208 were identified, with 33 additional articles identified from reference chaining. Information on surface 209 disinfection has been published separately 8 ; herein we described results from 58 mask disinfection and 210 reuse summaries. 211

We identified a large amount of data on mask disinfection and reuse, although much was not comparable 212 as many studies lacked specificity on methods, and tested a wide range of conditions on a small number 213 of samples. This led to data from multiple articles summarized to generate themes. Overall, when 214 comparing the list of efficacious disinfectants (ethanol, hydrogen peroxide, peracetic acid, PX-UV, 215 UVGI, autoclaving, and heat) with the reuse information (hydrogen peroxide, heat, and UV-GI promising, 216 peracetic acid and PX-UV need more information, and autoclaving and ethanol lead to failures), it is 217 recommended to focus guidelines and future research on the use of heat, hydrogen peroxide, and UVGI. 218

For radiation, non-uniform distribution across N95 masks was noted, when can be managed by rotation 219 and ensuring no shadowing by straps/other masks 16 . All of these options could be investigated for use in 220 LMIC and humanitarian contexts. Further research is recommended on non-N95 masks, as there is a lack 221 of research on cloth masks in particular. 222

Limitations to this work include that pre-prints were included in review, bias was not assessed beyond 223 noting pre-print percentage, and after completing the review we (based on information available) 224 determined to focus this sub-paper on mask disinfection and reuse. Additionally, there is likely more 225 relevant data published after the final download date of July 10, 2020. We plan to update this review for a 226 second publication in early-mid 2021. We do not feel these limitations impact the results presented 227

herein. Please note all extracted data is available in an Excel file in Supplementary Information for open-228 access use. 229 . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 12, 2020. ; https://doi.org/10. 1101 /2020 In summary, while SARS-CoV-2 has had a global impact, people living in LMIC are disproportionately 230 impacted due to inability to adapt recommended safety measures, lack of resources, and underlying health 231 conditions. We identified that no disinfection method consistently removed >3 log reduction of SARS-232

CoV-2 virus irrespective of concentration, contact time, temperature, and humidity. However, results did 233

show that it is possible to achieve >3 log reduction of SARS-CoV-2 using appropriate concentrations and 234 contact times of chemical (ethanol, hydrogen peroxide, peracetic acid), radiation (PX-UV, UVGI), and 235 thermal (autoclaving, heat) disinfection, and that hydrogen peroxide, heat, and UV-GI have promise to 236 allow mask reuse without mask failures. Further research on mask disinfection and reuse -on a range of 237 masks -is needed to develop evidence-based recommendations to protect people by ensuring safety of 238 PPE in contexts where masks are re-used. 239 240 . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 12, 2020. ; https://doi.org/10.1101 https://doi.org/10. /2020 CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 12, 2020. ; https://doi.org/10.1101 https://doi.org/10. /2020 CoV-2 Inoculated N95 Respirators. medRxiv 2020, 2020.05.31.20118588. 352 . CC-BY-ND 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) preprint

The copyright holder for this this version posted November 12, 2020. ; https://doi.org/10. 1101 /2020 

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Dry Heat 289 as a Decontamination Method for N95 Respirator Reuse

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Applying Heat and 353 Humidity using Stove Boiled Water for Decontamination of N95 Respirators in Low Resource 354 Settings

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Enveloped Virus Inactivation on Personal Protective Equipment by 382 Exposure to Ozone

Feasibility of 384 Reusing Surgical Mask Under Different Disinfection Treatments

Efficacy of 388 moist heat decontamination against various pathogens for the reuse of N95 respirators in the 389 COVID-19 emergency

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Dry heat and microwave-generated steam protocols for 416 the rapid decontamination of respiratory personal protective equipment in response to COVID-417 19-related shortages

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437 Humidity and deposition solution play a critical role in virus inactivation by heat treatment on 438 N95 respirators

N95 440 Reprocessing by Low Temperature Sterilization with 59% Vaporized Hydrogen Peroxide during 441 the 2020 COVID-19 Pandemic

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