Reusing filtering facepiece respirators (FFRs) has been suggested as a strategy to conserve available supplies for home and healthcare environments during an influenza pandemic. For reuse to be possible, used FFRs must be decontaminated before redonning to reduce the risk of virus transmission; however, there are no approved methods for FFR decontamination. An effective method must reduce the microbial threat, maintain the function of the FFR, and present no residual chemical hazard. The method should be readily available, inexpensive and easily implemented by healthcare workers and the general public. Many of the general decontamination protocols used in healthcare and home settings are unable to address all of the desired qualities of an efficient FFR decontamination protocol. The goal of this study is to evaluate the use of two commercially available steam bags, marketed to the public for disinfecting infant feeding equipment, for FFR decontamination. The FFRs were decontaminated with microwave generated steam following the manufacturers' instructions then evaluated for water absorption and filtration efficiency for up to three steam exposures. Water absorption of the FFR was found to be model specific as FFRs constructed with hydrophilic materials absorbed more water. The steam had little effect on FFR performance as filtration efficiency of the treated FFRs remained above 95%. The decontamination efficacy of the steam bag was assessed using bacteriophage MS2 as a surrogate for a pathogenic virus. The tested steam bags were found to be 99.9% effective for inactivating MS2 on FFRs; however, more research is required to determine the effectiveness against respiratory pathogens.

One possibility of overcoming the problems posed by the lack of decontamination equipment and elaborate protocols is to use technology that is readily available and already used by the general public for other applications with similar requirements. Off-the-shelf microwave steam bags (MSBs) are one option that may be used in healthcare and home environments. These bags, typically used to decontaminate breast pump and infant feeding accessories, are available for purchase in many retail stores where infant associated goods are sold. The instructions are written for the general public and are based on the operation of a microwave oven, which are readily available in home and healthcare environments. The use of commercially available steam bags for FFR decontamination has not been investigated, although previous studies suggest that microwave generated steam decontamination is promising [3] , [5] , [6] , [12] , [13] . The goal of this study is to evaluate the use of two commercially available steam bags for FFR decontamination with specific considerations to FFR filtration performance, FFR water absorption, decontamination efficacy, ease of use, and logistic benefits.

Some of the previously examined methods, although promising in laboratory studies, may not be universally suited for both healthcare and home environments. Methods that require decontamination equipment such as UV lights, vaporous hydrogen peroxide generators, and moist heat incubators would be better suited for healthcare facilities where such disinfection equipment is more likely to be available. Home environments lack sophisticated decontamination technology, but have disinfectants such as bleach and peroxide; however, the use of these products for FFR decontamination would require customized procedures which may not be easily executed by the general public. Moreover, skin and inhalation health hazards from the use of chemically treated FFRs are a concern [8] , [11] . Healthcare professionals, including infection control practitioners, are better prepared to follow customized detailed disinfection procedures than the general public due to training and experience. The logistics of an FFR decontamination program also need to be considered. FFR decontamination in healthcare settings may occur as a batch process, whereby one or a few employees decontaminate all FFRs or as an individual process, whereby the individual user is responsible for decontaminating their own respirator. Each scenario requires a system to identify the FFR user (to avoid sharing of FFRs among users), to track the number of decontamination cycles for each FFR, and to provide a means to efficiently store the FFR between uses.

The potential reuse of National Institute for Occupational Safety and Health (NIOSH) -certified N95 filtering facepiece respirators (FFRs) has been suggested as a possible strategy to conserve available supplies for home and healthcare environments during an influenza pandemic [1] , [2] . Reuse of FFRs may result in a risk of contact transmission by touching a contaminated surface of the respirator followed by touching the eyes, nose, and/or mouth. Physical and chemical methods to remove or inactivate viruses on FFR surfaces have been previously examined [3] , [4] , [5] , [6] , [7] , [8] , [9] , [10] , [11] . These methods were evaluated for decontamination efficacy, effect on FFR filtration and fit, wearer safety (i.e. chemical residues and off-gassing) and processing cost as suggested in a report issued by the Institute of Medicine (IOM) [1] . The IOM report also recommended that simple decontamination methods should be evaluated for ease of implementation in home and healthcare settings.

Table 3 lists the CV values for the MS2 contamination of each FFR model. Five of the six data sets achieved the ASTM E2721-10 quality objective CV value of ≤40% [18] . The average decontamination efficacy resulting from the use of MSB X bags was greater than 99.9% (3 logs) for all three FFR models tested ( Table 3 ). The average decontamination efficacy for the Moldex model was greater than 99.99% or 4 logs. The MS2 challenge concentration for the Moldex models was more than 2 logs higher than the Kimberly Clark (7.1) or 3M 1860 (7.6). MSB Y bags achieved 99.9% reduction of MS2 for two FFR models while the results of the third model measured greater than or equal to 99.86%.

In the second phase of testing, the triplicate samples for each of the FFR models, 3M 1870, Kimberly-Clark PFR95, and Moldex 2200, passed the filtration efficiency testing after three cycles of decontamination using both steam bag brands ( Table 2 ). For the MSB X bags, the filtration efficiencies of the experimental models were statistically similar to the controls for both the 3M 1870 (p = 0.19) and the Moldex 2200 (p = 0.40), while the treated Kimberly-Clark PFR95 models were statistically different from the controls (p = 0.01). MSB Y bags produced statistically similar results for the control and treated samples for each model; 3M 1870 (p = 0.19) Moldex 2200 (p = 0.40) and Kimberly-Clark PFR95 (p = 0.42). The results for drying of the FFRs were similar for 30 min compared to the 60 min drying time ( Tables 1 and 2 ). All models from the second phase of testing were included in the third phase of testing.

Table 1 lists the water absorption/retention and filtration efficiency of all FFR models after one cycle of steam bag decontamination using the MSB X bags. All of the six FFR models (one sample per model) surpassed the filtration efficiency requirements of 95%. The absorption values for models 3M 1860, 3M 8210 and the Cardinal Health N95 were roughly an order of magnitude higher than the values for 3M 1870, Kimberly-Clark PFR95, and Moldex 2200. The models 3M 1860, 3M 8210 and the Cardinal Health N95 remained wet after the 60 min drying period and were eliminated from further testing.

Discussion

Commercially available MSBs offer intrinsic benefits for FFR decontamination in home and healthcare settings. The steam bags, constructed for the purpose of disinfection (baby bottles and breast pumps), are readily available for purchase. The instructions for use are clearly provided on the side of the bags (Fig. 1). Simple, well-illustrated decontamination instructions are important for users with limited experience in disinfection and sterilization. For the MSB X bags, the instructions are included in an approximate 8” ×4” panel and are accompanied by step-by-step photographs. MSB Y bags include use instruction in three languages, English, Spanish, and French. The instructions are written for a range of microwave powers (500–1100W+), providing versatility for multiple microwave models. The steam bag can provide a dual function of storage and decontamination. A used FFR can be stored in the bag and decontaminated when use is required. Defined areas on the bag for the user's name and a checkbox indicating the number of uses provides a method for inventory accounting.

Steam sterilization, by the use of autoclaves, is routinely used in the processing of medical equipment. Autoclaves produce high pressure saturated steam and are effective at inactivating microorganisms including spores [20]. Unfortunately, autoclaving is highly destructive process for some FFR models [9]. Atmospheric applications of steam, such as the use of MSBs, are less destructive on FFRs but are less effective in inactivating microorganisms. Furthermore, the disinfecting ability of steam bags is not well characterized. Labeling on the steam bags or the steam bag packaging claims that “steam kills 99.9% of most harmful bacteria and germs”. The steam bags repeatedly produced a 3 log or 99.9% reduction in MS2 for the three FFR models tested in this study (Table 3). FFR decontamination using microwave generated steam has been examined previously, although without the use of a steam bag. Fisher et al., 2009, demonstrated a greater than 4 log, or 99.99%, reduction of MS2 virus after a 45 s treatment [3]. This study was performed on small FFR coupons contaminated with MS2-containing droplet nuclei in the same model microwave used in this current investigation. Fisher et al. (2010) examined cyclic MS2 contamination and decontamination of FFRs with microwave generated steam [5]. The findings in that study suggest that protective residues (proteins, respiratory secretions, cellular debris, etc.), which are a component of infectious aerosols, have less of an effect on the decontamination efficacy of steam compared to other decontamination methods. Heimbuch et al. studied the use of microwave generated steam on the inactivation of H1N1 deposited on FFRs as aerosols and droplets [6]. The microwave generated steam yielded a >4-log reduction of viable H1N1 virus for all FFR tested. In 93% of the experiments, the virus was reduced to levels below the limit of detection of the method. The presence of some viable virus on the FFRs was speculated to be “due to non-uniform distribution of steam over the entire surface of the FFR”. Heimbuch et al. further speculated that “optimization of the water reservoir holder will likely minimize or eliminate this issue”. The steam bags, used in this study, provide a defined volume for the entrapment of steam and, therefore, a more uniform application.

The FFR filtration performance for the three cycle treatments was within acceptable levels of the selection criterion for each FFR model treated in each steam bag brand. Bergman et al. reported similar results with no deleterious effect of microwave generated steam on the filtration performance of three surgical and three particulate N95 FFRs [12]. Moreover Bergman et al. and Viscusi et al. found fit of the FFR models used in their investigations to be unaffected by the use of microwave generated steam [12], [21]. Although the steam bags used in this study differs from the vessel used to house the FFRs in the Viscusi and Bergman studies, the results are promising.

The use of a steam bag has some limitations for FFR decontamination. The steam bags do not compartmentalize the water reservoir and sample location. The FFR is placed directly into the water in the reservoir, which produces the potential for water absorption by the FFR material. Water absorbency is important as a saturated FFR would require an extended drying period before reuse is possible. An extended drying period is counterproductive to increasing FFR supply in the event of shortages due to high demand. The potential to use the steam bags for FFR decontamination will likely be FFR model specific, as demonstrated by the water absorption data in this study (Tables 1 and 2). The absorption characteristics were also independent of the FFR classification as a particulate or surgical mask, which suggests simplification of determining decontamination potential is unlikely. These findings are supported by the results discussed in Viscusi et al. 2009, where differences in the hydrophobicity of FFR models, individual layers of FFRs, and even differences between the surfaces of a given layer were confirmed [8]. In fact, the FFR models eliminated after the first phase of testing were found to contain at least one hydrophilic layer, whereas the models proceeding to the second phase of testing were constructed entirely of hydrophobic materials [8], [22].

The decontamination procedure and demonstrated efficacy of the MSBs are not in alignment with current FDA guidelines and requirements for the reuse of single use medical devices [20], [23], [24]. However, government recommendations for FFR reuse are complicated; CDC and NIOSH recommendations have permitted reuse (i.e., multiple donnings of a previous worn FFR) without decontamination in some unique situations such treating TB patients and in emergency situations when supplies are limited (e.g., during the 2009–10 novel H1N1 influenza pandemic) [25], [26]. Furthermore, many FFR models used in healthcare (including 3 in this study) and nearly half of those models in the U.S. Strategic National Stockpile are not currently regulated by FDA as they are not being marketed as medical devices. Currently, NIOSH respirator certification does not include provisions for FFR decontamination and reuse. Decontamination of NIOSH certified FFRs for purposes of reuse is not recommended in the workplace, primarily because of concerns that decontamination would degrade the performance of the respirator. Thus, the results of this study should be viewed from the context of informing future government, public health, and infection control recommendations in an emergency, rather than as recommending changes to routine practice.

A cleaning procedure was not included as part of this study; however, it was previously demonstrated that soil load accumulation may not significantly impact microwave generated steam decontamination of FFRs [5]. Likewise, a high level disinfection, which eliminates all microorganisms except for a small number of bacterial spores, was not achieved with the use of the steam bags. Initial virus titers between 107 and 1010 pfu/FFR were reduced by 99.9%; leaving roughly 104 to 106 pfu/FFR. The titer of viable MS2 remaining on the respirator can present major health hazard concerns. However, the number of viable MS2 applied to the respirators (7–10 log 10 pfu) greatly exceeds the expected contamination levels of in-use scenarios.

In healthcare and home environments alike, the performance of the steam, and microwave ovens, may demonstrate some variability. It should be noted that the microwave used in this study was rated at 1100 W by the manufacturer, but was experimentally determined to function at 750 W previously [9]. It is possible that applying a longer treatment time, indicated by the steam bag instructions for a 750 W microwave, would produce increased decontamination efficacy. However, this introduces another level of complexity as it is possible that microwave performance in homes and healthcare settings may not be consistent with manufacturer ratings. It is possible that some of the steam bags may demonstrate inconsistent behavior. In this limited investigation, the steam bags were monitored for failures in the seams and zip lock seals after decontaminations with no discernable failures. The consistent decontamination performance of the steam bags supports the observation of maintained structural integrity during the steam procedure. However, care must be taken not to generalize this finding beyond the scope of this study.

More studies are required before the use of steam bags can be considered for FFR decontamination for the purpose of reuse. In general, reuse requires a higher degree of rigor than single use applications. Commonly used in the evaluation of medical devices, an ultrastructural analysis of the decontaminated FFRs may help to address concerns and knowledge gaps associated with FFR reuse. Quality control assessments of the steam bags and microwave ovens should be performed to investigate the utility of the steam bag decontamination procedure. Likewise, implementing MSB decontamination of FFRs in home and healthcare settings would present quality control issues which should be investigated for each environment. The use of MS2, a nonenveloped virus, in this study does not accurately reflect the potential efficacy of the steam bag against enveloped viruses including 2009 H1N1. In general, enveloped viruses are more susceptible to decontamination due to the fragile lipid coat. Testing the steam bags against other microbes can assist discerning the steam bags' potential. FFRs decontaminated using the steam bags should be fit tested to ascertain if any changes to FFR shape and fit occurred as a result of the steam process, although previous research with microwave generated steam suggests that this is unlikely.