key: cord-102833-hh4641o0
authors: Sarkis-Onofre, Rafael; Borges, Rafaela do Carmo; Demarco, Giulia; Dotto, Lara; Schwendicke, Falk; Demarco, Flávio Fernando
title: Decontamination of N95 respirators against SARS-CoV-2: a scoping review
date: 2020-11-13
journal: nan
DOI: 10.1016/j.jdent.2020.103534
sha: 
doc_id: 102833
cord_uid: hh4641o0

Objectives This scoping review aimed to map and compile the available evidence regarding the effectiveness of decontaminating N95 respirators against the novel coronavirus (SARS-CoV-2). Data We selected studies written in English assessing or discussing the decontamination strategies of N95 respirators against SARS-CoV-2. Two independent researchers performed the search and study screening. A descriptive analysis was carried out considering the study design of the included studies. Sources PubMed, SCOPUS, and Preprint platforms (bioRxiv and medRxiv). Study selection We included 55 reports from PubMed and SCOPUS. Nine articles were letters to the editors, 21 were in vitro studies, 16 were literature reviews, and 9 were classified as other study designs. We included 37 preprints. Two articles were letters to the editors, 24 were in vitro studies, 3 were literature reviews, and 8 were classified as other study designs. In general, vaporized hydrogen peroxide and ultraviolet irradiation were the strategies most cited and most promising. However, there is a lack of evidence and consensus related to the best method of N95 respirator decontamination. Conclusion The evidence regarding decontamination strategies of N95 respirators against SARS-CoV-2 remains scarce. Vaporized hydrogen peroxide and ultraviolet irradiation seem to be the current standard for N95 respirator decontamination. Clinical significance Vaporized hydrogen peroxide and ultraviolet irradiation appear to be the most promising methods for N95 respirator decontamination.

The novel coronavirus, termed SARS-CoV-2, has produced a social disruption globally, with severe consequences for the population's general health. There are more than 47 million confirmed cases at the present moment, with a cumulative number of deaths of over 1,215,000, according to the World Health Organization (WHO) (updated data can be accessed at https://www.worldometers.info/coronavirus/). Currently, vaccines are still under trial, and there are no effective drugs to treat this disease [1] .

Indeed, most of the available evidence supports the proposal that social distancing, wearing masks, and eye protection effectively prevent transmission [2] . Better hygiene (handwashing) and the use of sanitizers have also been found to reduce the spread of the disease (COVID-19) [1, 3, 4] .

WHO has recommended using masks, and governments have established face protection policies for public spaces [4] . The resulting increase in demand and a shortage of market availability have led to price increases for masks [5] [6] [7] [8] [9] . Health professionals are at high risk for infection with the new coronavirus, and a lack of adequate protective equipment during critical procedures in infected patients is increasing that risk considerably [10, 11] . In Brazil, for example, more nurses and nurse assistants have died due to COVID-19 than any other country [12] ; most of them have been infected during their work with infected patients, and in some situations, using home-made masks.

N95 respirators are a type of respirator mask used as facial protection by healthcare providers and are specifically advocated when performing aerosol-generating procedures [7, 13] . They present a hermetically sealed fit, and wearers do not breathe the surrounding air unfiltered. These respirators can filter over 95% of pollutant particles (>0.3 µm) in the air due to a higher electrostatic charge (which blocks the particles) and

have been suggested to be used to reduce the risk of SARS-CoV-2 spread [14] . These masks are intended for single use and, based on the manufacturer's instructions, they are heat sensitive and not designed to be sterilized; however, due to their high costs and limited availability [6, 13] , different methods to decontaminate N95 [5, 13, [15] [16] [17] [18] [19] respirators have been discussed to allow multiple usages. Other types of N95 respirator include a mask with a valve designed for people exposed to asbestos and dust.

Decontamination methods can be classified into chemical or physical treatment, dry heat, or moist heat [7] . Such approaches need to fulfill specific criteria: elimination of harmful pathogens; minimal damage to the facemask structure; low toxicity and costs; J o u r n a l P r e -p r o o f for the term "N95 AND Decontamination OR Disinfection" posted between "01 March 2020 and 10 August 2020" and considering the inclusion criteria reported previously.

The search was undertaken using EndNote (EndNote X9, Thomson Reuters, New York, US). Two researchers independently identified relevant records by analyzing titles and abstracts for relevance according to the eligibility criteria. Retrieved records were classified as include, exclude, or uncertain. The full-text articles of the included and uncertain records were selected for further eligibility screening by the same two reviewers, again independently. Discrepancies in the screening of titles/abstracts and fulltext articles were resolved through a discussion. In case of disagreement, the opinion of a third reviewer was obtained. The study selection of published studies and preprint materials was carried out separately.

We created a form using Excel (Microsoft, Redmond, Washington, US), which was pilot tested by three reviewers to reach a consensus on what data to collect and how. Then, two reviewers extracted the data independently, and a third reviewer evaluated this process.

Five studies reported the process for N95 decontamination with vaporized hydrogen peroxide. Schwartz et al. (2020) described the process implemented at Duke University (US) and demonstrated that vaporized hydrogen peroxide is an efficacious decontamination method that does not cause physical or performance degradation of the masks [25] . Perkins et al. (2020) described the process implemented at the University of New Mexico (US) and reported on the low toxicity of their methods. The authors highlighted the importance of physically assessing masks after decontamination [61] . Grossman et al.

(2020) described decontamination using vaporized hydroperoxide employed by Washington University (US). They demonstrated that the entire process requires less than 24 hours and showed that it is important to create a workflow to achieve effective decontamination considering pre-processing steps, decontamination, and post-processing steps [60] . Jatta et al. (2020) presented the decontamination using vaporized hydrogen peroxide (59%) and demonstrated that this approach could be used safely without affecting mask performance [36] . Hankenson et al. (2020) described a process to develop a multiroom animal housing into a vaporized hydrogen peroxide center and found that this method can decontaminate a significant number of masks [34] .

Further studies evaluated this latter strategy combined with others or discussed its availability and feasibility. Cadnum et al. (2020) performed an in vitro study and compared the use of a high-level decontamination cabinet that generates aerosolized peracetic acid and hydrogen peroxide with ultraviolet C light and dry heat at 70 °C for 30 minutes. They demonstrated that aerosolized peracetic acid and hydrogen peroxide are useful for the decontamination of N95 respirators [5] . J o u r n a l P r e -p r o o f Kobayashi et al. (2020) assessed the authority recommendations in the Netherlands, the state governments in the US, the European Commission Directorate-General for Health and Consumers, and the European Medicines Agency regarding the use of vaporous hydrogen peroxide. They found that although this method seems to lead to acceptable decontamination while retaining mask integrity according to visual inspections, this type of decontamination is not available throughout all countries and institutions, and currently, no standard for its application exists [23] .

Ten reviews noted that vaporous hydrogen peroxide appears to be a highly promising method for N95 respirator decontamination [45, 47, [51] [52] [53] 55, 57, 58, 64] .

Hamzanzi et al. (2020) presented a prototype model for N95 respirator decontamination using ultraviolet germicidal irradiation that would allow decontamination of 18 to 27 masks in one process [22] . Kobayashi et al. (2020) assessed the authority recommendations on ultraviolet germicidal irradiation use and found that although this method is promising, it has not been standardized by any of the authorities so far [23] . Cadnum et al. (2020) demonstrated that ultraviolet C could reduce N95 respirator contamination, but efficacy varied with different mask types and locations on the respirator [5] . demonstrated that ultraviolet C light inactivated SARS-CoV-2 more slowly on N95 respirators than stainless steel, most likely due to its porous nature [32] . Simmons et al.

(2020) noted that a pulsed xenon ultraviolet system is promising for N95 respirator suggested using a hybrid method, including ultraviolet C and heat treatment, that can be extended to other infections agents [28] . highlighted that at least 1 J/cm2 of ultraviolet C applied to all surfaces is necessary to ensure N95 respirator decontamination. However, the authors emphasized that ultraviolet C decontamination has limitations, mainly because each mask type requires a specific irradiation dose to be reliably effective [24] .

In sum, eight reviews commented that ultraviolet germicidal irradiation is a highly promising strategy for N95 decontamination [45, 47, [50] [51] [52] [53] 57, 58] .

Different decontamination methods and protocols using heat have been discussed in the literature and found to be promising for N95 respirator decontamination.

The use of moist heat was cited in two letters [7, 13] , six in vitro studies [17, 27, 29, 31, 37, 38] , and two other study designs [66, 67] . Regarding the in vitro studies, Anderegg et al. (2020) demonstrated that moist heat is a scalable method; all masks passed the fit testing and maintained filtration efficiency after five cycles [27] . Bopp et al. (2020) noted that N95 respirators could resist up to three cycles of moist heat [29] . Daeschler et al. (2020) tested different humidity scenarios and found that it is possible to use 50% relative humidity for up to 10 cycles [31] . However, Pascoe et al. (2020) demonstrated that moist heat was effective only in some types of N95 respirators [38] .

The use of dry heat was cited in four in vitro studies [32, 37, 38, 43] , one review [46] , and one other study design [66] . Fischer et al. (2020) and Pascoe et al. (2020) demonstrated that the use of dry heat at 70 ºC is effective [32, 38] , but Fischer et al. (2020) highlighted that this approach is not recommended for more than two rounds [32] . Ou et al. (2020) compared dry and moist heat; dry heat was a better method for maintaining filtration efficiency and fit testing, but by adding moisture, the virus inactivation was higher [37]. Xiang et al. (2020) demonstrated the successful use of dry heat at 70 °C after 1, 2, and 3 hours for N95 respirator decontamination [43] . Other methods cited included the deposit of silver nanoparticles [68] .

Thirty-seven studies fulfilled the eligibility criteria from which the data were extracted ( Figure 1 ).

Tables 3 and 4 present the characteristics of the included studies. Related to the study design of included studies, two articles were letters to the editors explaining the results of in vitro studies [70, 71] , 24 were in vitro studies [16, , 3 were literature reviews [95] [96] [97] , and 8 were classified as other study designs [98] [99] [100] [101] [102] [103] [104] [105] . Details regarding preprint in vitro studies are presented in the Supplemental Material.

Related to the decontamination regimens tested or discussed, the use of vaporized hydrogen peroxide and ultraviolet irradiation were the regimens most cited. Vaporized hydrogen peroxide was cited in one letter [70] , 9 in vitro studies J o u r n a l P r e -p r o o f [74, 76, 78, 79, 81, 86, 87, 92, 93] , one review [95] , and two other study designs [98, 101] . The use of ultraviolet irradiation was cited in 8 in vitro studies [16, 72, 79, 80, 81, 89, 92, 93] , 3 reviews [95] [96] [97] and 5 other study designs [99, 100, 102104, 105] .

Seven in-vitro studies demonstrated that hydrogen peroxide is effective as a decontamination method of N95 respirators [75, 76, 78, 81, 86, 87, 93] . One review [95] showed that vaporous hydrogen peroxide has substantial potential for the decontamination of these respirators. Cramer et al. (2020) , in a qualitative study, supported the use of SteraMist iHP technology [98] , and Kenney et al. (2020) demonstrated in a letter the use of the BQ-50 system [70] .

Four in vitro studies [16, 72, 81, 89] demonstrated that ultraviolet C is effective as a decontamination method of N95 respirators. Two reviews showed that ultraviolet C light is one of the most promising decontamination [95, 96] . However, Tommey et al.

(2020) highlighted concerns about using this method due to incomplete penetration into deeper layers of the filter [97] . Five studies presented different devices to use ultraviolet C light as a decontamination method [99, 100, 102, 104, 105] .

Different decontamination methods and protocols using heat were discussed and demonstrated.

Moist heat was cited in 6 in vitro studies [73, 77, 80, 83, 91, 93] and one review.

Daescher et al (2020) demonstrated that moist heat could be used even after ten cycles, maintaining mask integrity [73] . Doshi et al (2020) presented a method using moist heat that could be scaled for low resources settings [77] . Liao et al. (2020) tested different disinfection methods; moist heat was found to be the most promising approach [80] .

The use of dry heat was cited in 5 in vitro studies [81, 83, 84, 94, 103] and one review [96] . Meisenhelder et al. (2020) showed that 95 °C dry heat could be used for 30 minutes and five cycles, maintaining mask properties [84] . Lensky et al (2020) proposed the use of industrial dryers to heat masks for 65 min at 80 °C and demonstrated that the masks maintained their properties after three cycles [103] .

Other methods cited included ozone [74, 82] and 70 0 ethanol [85, 92] . Dave et al (2020) . and Manning et al. (2020) demonstrated that ozone is effective as a disinfection method [74, 82] , and Manning et al. (2020) highlighted that this method did not degrade mask properties [82] . Nazeeri et al. (2020) showed that the use of a vacuum chamber is important after 70° ethanol treatment to recover filtering efficiency [85] .

This study discussed the evidence about the effectiveness of decontamination strategies of N95 respirators against the novel coronavirus. Our results demonstrate a lack of evidence and consensus related to the best method for N95 respirator decontamination.

However, vaporized hydrogen peroxide and ultraviolet irradiation were the regimens most cited and seemed to be the most promising methods for such decontamination.

Hydrogen peroxide vapor decontamination is common in different fields and facilities, including scientific, pharmaceutical, and medical ones. The method has low toxicity and uses the catalytic reduction of peroxide to oxygen and water [106] . However, it requires a specific room and equipment to achieve effective decontamination and, hence, is rather expensive. Ultraviolet irradiation is a decontamination method using ultraviolet light to inactivate microorganisms through RNA damage and cell function disruption [107] . This method has limitations due to different masks requiring a variety of irradiation dosages; a high dosage, in turn, could result in increased toxicity and mask structural damage. Moreover, this approach also needs specific equipment, limiting its availability.

Ideally, any decontamination method should eliminate all pathogens and maintain mask integrity and filter capacity at low toxicity and cost. Today, no one method fulfills these criteria, and the extended use of masks seems to be an appropriate, low-cost approach for overcoming the discussed availability limitations. Current recommendations consider mask-wearing periods between 4 and 40 hours [23] . Notably, additional protection, such as face shields and strict adherence to hand hygiene practices is necessary, particularly if extending mask-wearing periods [108] .

Outcomes such as mechanical integrity and performance of N95 respirators should be observed when assessing decontamination strategies of such respirators because decontamination may come at a price; decontaminated but ineffective masks are not useful and can even be dangerous. indicated that fit testing must be performed after decontamination, and if decontamination is achieved but the masks lose J o u r n a l P r e -p r o o f their integrity, further usage should be stopped [18] . Hence, both integrity and performance should be prioritized when implementing decontamination strategies, although not all included studies concomitantly tested decontamination and subsequent mask performance.

Our study presents some limitations. First, because this was a scoping review, we did not conduct a risk of bias/quality assessment of the included studies. Second, we included only studies in English. Third, the included studies present different designs and protocols, making it difficult to compare the results, particularly because many N95 respirator brands are available on the market, different regimens were tested, and individual scenarios of wearers (such as the influence of cosmetics or sunscreen use for ultraviolet decontamination) are difficult to test. Further, many studies presented severe limitations, including small sample size and poor quantitative data reporting. Fourth, we included articles discussing decontamination methods based on opinions rather than evidence, making it difficult to provide more general conclusions and recommendations, and we included preprint studies; however, these are preliminary reports of works that have not been certified by peer review results and should, therefore, be interpreted with caution. Finally, we included different reviews that could generate an overlap of papers; however, 34 preprint reports (not considering preprint reviews) were included, but they were not part of the 16 published reviews.

The global COVID-19 pandemic is still currently accelerating. The shortage of protective equipment, particularly for healthcare workers, indicates that more investigations for safely decontaminating N95 respirators are necessary. The availability and cost-effectiveness of decontamination should also be considered in future primary studies.

The evidence supporting appropriate decontamination strategies of N95 respirators against the novel coronavirus remains scarce. Vaporized hydrogen peroxide and ultraviolet irradiation are the current standard for these respirators. However, cleaning is an essential step prior to decontamination, and decontamination methods should be followed by fit testing. Further, the extended use of masks appears to be an effective, low-cost approach to overcome the global shortage of N95 respirators. The study discussed about fittesting performance collected for the different respirator models treated with UVGI.

The data of this study strongly indicates that to protect the safety of the N95 respirator user, fit-testing after decontamination must be done each time a new model is introduced to a healthcare system. This has significant safety implications as varied decontamination methods are being used by different institutions. 

The study talks about a quality assurance (QA) step, after complete aeration, to ensure both qualitative and quantitative degradation has not occurred, ensuring that there was no physical or erformance degradation. Also, a standardized quantitative fit testing was preformed to ensure the integrity of the respirators is maintained over many decontamination cycles. In addition, we validated the efficacy of the decontamination process by using 9 individual 6-log biological indicators (Geobacillus stearothermophilus spores).

Using hydrogen peroxide vapor is a proven method of decontamination. Authors believe that decontamination of N95 respirators with hydrogen peroxide vapor is one such solution that affords us better ability to protect our health care workers as we continue to tackle this monumental issue. 

The study shows that overall, strategies involving the use of UVGI, ethylene oxide, dry oven heating and hydrogen peroxide vapour may be most promising for preservation of mask function and integrity. Decontamination with UVGI, moist heat incubation and microwave-generated steam does not appear to significantly affect N95 respirator fit or comfort. Until application of these methods has been adequately investigated in the hospital setting, their safety and effectiveness in the particular context of the SARS-CoV-2 outbreak is unknown. 

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. 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.

To synthesize existing data on the effectiveness of ultraviolet germicidal irradiation for N95 FFR decontamination Ultraviolet germicidal irradiation -

The authors findings suggest that further work in this area (or translation to a clinical setting) should use a cumulative UV-C dose of 40,000 J/m2 or greater, and confirm appropriate mask fit following decontamination. To outline a procedure by which PPE may be decontaminated using ultraviolet radiation in biosafety cabinets and discuss the dose ranges needed for effective decontamination of critical PPE. Furthermore, discuss the obstacles to this approach including the possibility that the UV radiation levels vary within biosafety cabinets.

Determining if ultraviolet lights used in biosafety cabinets could be temporarily repurposed for ultraviolet germicidal irradiation decontamination to preserve a dwindling supply of PPE Ultraviolet germicidal irradiation SARS-CoV-2 SARS-CoV-2 Measurements of ultraviolet radiation fluence using a ultraviolet radiation meter and variance.

Authors recognize that institutions will require robust quality control processes to guarantee the efficacy of any implemented decontamination protocol. They also recognize that in certain situations such institutional resources may not be available; while we subscribe to the general principle that some degree of decontamination is preferable to re-use without decontamination. Daeschler et al. 2020 To investigate whether thermal disinfection at 70°C for 60 min inactivates pathogens, including SARS-CoV-2, while maintaining critical N95 respirator protective properties for multiple cycles of disinfection and re-use in a realworld setting Authors found that one cycle of treatment with all modalities was effective in decontamination and was associated with no structural or functional deterioration. Kumar et al. 2020 (2) In this context, three types of masks, which are being used most of the countries, include N95, nonwoven fabric masks (often called as surgical mask) and self-made two-ply cotton masks are tested for filtering efficiency (before and after sterilisation) with and without gamma sterilisation. Comparison of filtering efficiency of the current work and with the results available in the literature for N95 masks,and testing in accordance with two breath condition (normal and during sneezing) is highlighted. however, the filtration efficiencies stayed within a certain range after 60 minutes of heat treatment rather than a steady rise.

Authors evaluates the virucidal activity of hydrogen peroxide vapor using a BQ- 50 Hydrogen peroxide vapor reprocessing may ease shortages and provide a higher filtration crisis alternative to non-NIOSH masks.

Demonstrate that an atmosphericpressure plasma generated by the microwave oven can decontaminate the respirator.

Tulane virus in artificial saliva and Geobacillus stearothermophilus spores.

The plasma species generated in this manner are capable of decontamination in 30 seconds and anyone with a microwave oven and a few simple household items can create a N-95 respirator decontamination unit for emergency use. --There is considerable discrepancy to the extent that no single reprocessing method is supported by all the guidance documents. The intervention with most support is vaporised hydrogen peroxide, though one document cautions about chemical residues and another indicates it has only been tested with some of the respirator models in common use. Similarly, ultraviolet germicidal irradiation receives both cautious support and concerns about inadequate decontamination because of incomplete penetration into deeper layers of the filter. Moist heat is cited as promising, though there are concerns when steam is microwave-generated where there may be uneven heating and where the metal nose band may generate sparks. Findings based on the article reporting

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The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. 

Authors support the use of the SteraMist Ionized hydrogen peroxide technology as a sterilization method for reuse of N95 masks, including many of the most commonly used models, following pretreatment with an Ionized hydrogen peroxide handheld delivery device. Gilbert et al. 2020 To document procedures to build a similar type of UVGI irradiation platform with off-the-shelf components from the hardware store and UVGI bulbs sold online or from biosafety cabinets (class I, II, or III) that are ubiquitously found throughout academic research and industrial centers around the world.

---The system presented is scalable and can be created for less than 50 US dollars, on site, at the point of need, and leverages resources that are currently untapped and sitting unused in public and private research facilities.

Authors review the available literature concerning use of germicidal ultraviolet-C (UV-C) light to decontaminate N95 masks and proposed a practical method for repeated point-of-use decontamination, using commercially-available UV-C crosslinker boxes from molecular biology laboratories or a simple low-cost, custom-designed and fabricated device to expose each side of the mask to 800-1200 mJ/cm2 of UV-C.Authos reviewed the efficacy of UV-C decontamination for N95s, considering factors such as UV transmittance to different layers of the mask, viral sensitivity to UV-C, and potential photodegradation of masks. They also presented the Local UV Box, a practical, low-cost device for smallscale UV-C decontamination of N95 masks. This device assures that a consistent dose of UV-C is applied to the masks, enabling reliable decontamination and repeated reuse without substantial mask photodegradation.A multidisciplinary pragmatic study was conducted to evaluate the use of an ultrasonic room highlevel disinfection system (HLDS) that generates aerosolized peracetic acid (PAA) and hydrogen peroxide for decontamination of large numbers of N95 respirators.Ultrasonic room highlevel disinfection system that generates aerosolized peracetic acid and hydrogen peroxide Bacteriophage MS2 and Geobacillus stearothermophilus sporesand Geobacillus stearothermophilu s spores CFU or PFU Authors found that a ultrasonic room highlevel disinfection system that generates aerosolized peracetic acid was effective for the decontamination of N95 respirators with a short cycle time. No adverse effects on filtration efficiency, structural integrity, or strap elasticity were detected after 5 treatment cycles. The ultrasonic room highlevel disinfection system that generates aerosolized peracetic acid system provides a rapidly scalable solution for hospitals requiring in-hospital disinfection of N95 respirators.

To present the Synchronous UV Decontamination System (SUDS), a novel device for rapidly deployable, point-of-care decontamination using UV-C germicidal irradiation.

---Authors designed a compact, easy-to-use device . This short decontamination time should enable care-providers to incorporate decontamination of FFR into a normal donning and doffing routine following patient encounters. Lensky et al. 2020 Authors propose a dry-heat decontamination method, using industrial dryers as the heat source.Dry-heat ---The data-driven protocol outlined passes the important tests of temperature stability and repeatability on a single machine.

To present a locally-implemented ultraviolet-C germicidal irradiation (UVGI)-based FFR decontamination pathway, utilizing a home-built UVGI array assembled entirely with previously existing components available.

---Herein authors have devised a methodology that leveraged local resources and supplies to execute a local robust, datadriven, replicable UVGI-based decontamination process.