The Bactericidal Effect of MA-T for Factitiously Contaminated and Used Masks

Ryuta Urakawa; Takekatsu Shibata; Motofumi Sogou; Kiyoto Takamori; Tsuyoshi Inoue; Kiyoshi Konishi; Takayoshi Sakai

doi:10.1248/bpb.b22-00046

Abstract

Matching transformation system (MA-T), an on-demand aqueous chlorine dioxide solution, is an excellent safety disinfectant, because chlorine dioxide is not detected during storage or before use. The production of chlorine dioxide in MA-T is induced by a catalytic reaction in the presence of target microorganisms. In this study, we investigated MA-T disinfection of masks as a reuse method to eliminate mask shortages. After spraying Escherichia coli on sterilized surgical mask, samples (factitiously contaminated masks) were treated with MA-T spraying or immersion, and the bactericidal efficacy was assessed by culturing. Used surgical masks were also sprayed with MA-T or were immersed in MA-T, and then were cultured to verify the bactericidal effect. The performance of N95 masks was assessed before and after application of MA-T. After spraying with MA-T, the numbers of bacteria of factitiously contaminated masks and used masks were drastically reduced compared with control samples (not applicable and p = 0.002, respectively). After MA-T immersion, the bacterial counts of both masks (factitiously contaminated masks and used masks) were significantly reduced (both p = 0.002). Taken together, the disinfection test on factitiously contaminated with E. coli and used surgical masks showed that masks can be disinfected by MA-T spray and sterilized by immersion, respectively. The N95 mask performance test after 30 min of immersion in MA-T showed that MA-T disinfected the mask without degrading the performance of the mask. In conclusion, MA-T is useful for the reuse of masks because of its decontamination effect and safety while maintaining the function of the mask.

INTRODUCTION

Coronavirus disease 2019 (COVID-19) pandemic caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) has led to a worldwide shortage of masks, gowns, face shields, and other personal protective equipment (PPE). The shortage of PPE is more serious in developing countries where medical systems are not functioning well.^1,2) Historically, the world has experienced a number of worldwide outbreaks of pestis, cholera, influenza or numerous infectious diseases such as typhoid, Ebola, SARS, and Middle East Respiratory Syndrome (MERS).^3,4) The history of infectious diseases is expected to repeat, and PPE will continue to be essential equipment for infectious prevention.

Infectious-protective clothing, especially masks, have commonly been single-use. In the wake of the SARS-CoV-2 pandemic, various methods for safe reuse have been tried, but no established method exists yet. The Centers for Disease Control and Prevention (CDC) reports that UV germicidal irradiation, vaporous hydrogen peroxide, and moist heat have been proposed as the most promising decontamination methods of N95 filtering facepiece respirators (FFRs).⁵⁾ However, because of concerns about impairment of mask performance and the lack of efficacy data against coronaviruses on the FFR, the report recommends an individual product approach or an individualized approach for each patient and treatment.

Aqueous chlorine dioxide solutions have long been known for their excellent disinfection effects^6,7) and have been used to disinfect tap water in Western countries. Cell membrane disruption is considered to be one of the mechanisms of reaction,^8,9) and denaturation of protein is another.^10,11) Due to its effectiveness against bacteria and viruses, it has been considered not only for drinking water and wastewater treatment, but also for environmental and food disinfection or medical applications.^12–16) Matching transformation system (MA-T) is an on-demand aqueous chlorine dioxide solution and exhibits a strong microbiocidal action. MA-T is a stable and excellent safety disinfectant, because chlorine dioxide is not detected in MA-T during storage or before use, and production of chlorine dioxide is induced by a catalytic action in the presence of targets of this disinfectant. MA-T only attacks live bacteria in the respiratory chain.¹⁷⁾ In a previous study, we proved that MA-T is effective against various microorganisms containing bacteria, fungi and viruses, and can be used safely in humans.¹⁸⁾ Furthermore, because MA-T does not evaporate nor ignite like ethanol, and it does not corrode metals, unlike treatments with other chlorine containing disinfectants, MA-T is expected to play an active role in the medical field.

In this study, mask disinfection was tested on the hypothesis that masks can be safely reused after disinfection with MA-T.

MATERIALS AND METHODS

Disinfection Test Using MA-T Spray on Surgical Masks Contaminated with Escherichia coli

Surgical masks were divided into identical 3.5 × 5 cm sections. A drop of 100 µL of E. coli, prepared at 2.70 × 10⁸/mL was added to each piece. All pieces were then dried. The pieces of mask containing E. coli were disinfected by spraying with 0.5 mL of 100 ppm MA-T and allowed to stand for 15 min. Twelve pieces with the same treatment were prepared, 6 for bacteriological examination of the mask outside-surface and 6 for bacteriological examination of the whole mask, including both surfaces and the inside. The outer surface of the mask was then placed on the surface of a brain-heart infusion (BHI) agar plate and incubated in a 37 °C incubator for 24 h. For bacterial culture of the whole mask, the disinfected piece was immersed in 3 mL of physiological saline, and 300 µL of the contaminated saline was spread onto a BHI agar plate with a sterilized bacteria spreader and incubated for 24 h in a 37 °C incubator. As a control, physiological saline was sprayed on the factitiously contaminated mask instead of MA-T, and bacteria on the mask surface were cultured, which was repeated 6 times. Colony forming unit (CFU) on each BHI agar plate was examined after incubation.

Disinfection Test by MA-T Immersion of Surgical Masks Contaminated with E. coli

The 3.5 × 5 cm pieces of surgical mask were prepared and were factitiously contaminated with E. coli by the same procedure as the disinfection test using MA-T spray on surgical masks. Six pieces were immersed in 30 mL of 100 ppm MA-T and another 6 pieces were immersed in 30 mL of physiological saline for control, which were allowed to stand for 15 min. After the mask pieces were removed, the remaining solution was centrifuged at 9000 × g for 5 min, and the precipitates were suspended in 250 µL of phosphate buffered saline (PBS). The MA-T treated suspension (250 µL) was spread onto BHI agar plate with a sterilized bacteria spreader. The control suspension was diluted 10⁵-fold with physiological saline, and 250 µL of diluted suspension was spread onto a BHI agar plate. The obtained BHI agar plates were incubated for 24 h in a 37 °C incubator.

Disinfection Test Using MA-T Spray on Surgical Masks Used by Health Care Provider

Surgical masks which had been used in a clinical setting for 8 h by the same clinical laboratory technician who routinely performed bacteriological tests or blood sampling from patients were prepared. The masks were cut in six 3.5 × 5 cm pieces with sterilized scissors. The pieces were disinfected by spraying 0.5 mL of 100 ppm MA-T or sprayed with physiological saline for control, all of them were allowed to stand for 15 min. For bacterial culture on the outside-surface of the mask, 6 pieces were sprayed with MA-T and the other 6 pieces were sprayed with physiological saline. The outside-surface of mask was placed on the surface of BHI agar plate, and cultured in the incubator at 37 °C for 24 h. For bacterial culture of the whole mask including both surfaces and the inside, 6 pieces sprayed with MA-T and 6 pieces sprayed with physiological saline were immersed in 3 mL of physiological saline, and 1 mL of the resulting solution was spread onto a BHI agar plate with a sterilized bacteria spreader and incubated for 24 h in a 37 °C incubator.

Disinfection Test by MA-T Immersion of Surgical Masks Used by Health Care Provider

The same type of surgical mask used by the same medical provider as in the disinfection test above was prepared. The masks were cut in six 3.5 × 5 cm pieces with sterilized scissors. Six pieces were disinfected by immersing them in 30 mL of 100 ppm MA-T and the other 6 pieces were immersed in 30 mL of physiological saline, and allowed to stand for 15 min. After the mask pieces were removed, the remaining solution was centrifuged at 9000 × g for 5 min, and the precipitates were suspended in 250 µL of PBS. The obtained suspension was spread onto a BHI plate medium with a sterilized bacteria spreader and incubated for 24 h at 37 °C.

Mask Performance Test before and after MA-T Processing

The tests were conducted at the Technology Institution of Industrial Safety (Saitama, Japan) in accordance with the standard for dust masks.¹⁹⁾ The following tests were conducted on unused N95 masks which were untreated with MA-T and unused N95 masks immersed in 150 ppm MA-T for 30 min.

(1) Inspiratory Resistance Test

The pressure difference between the inside and outside of a dust mask attached to a micro-manometer (130-1Kp-DGR; Sayama Corporation, Tokyo, Japan) was measured when air was passed through it at a flow rate of 40 L per minute.

(2) Particle Filtration Efficiency (PFE) Test

Air containing sodium chloride was passed through the inside of a mask attached to a dust respirator testing apparatus (AP-9000-AP632; Sibata Scientific Technology Ltd., Japan) at a flow rate of 85 L per minute, and the concentration of sodium chloride before and after passing through the mask was continuously measured by a sodium chloride concentration analyzer using the scattered light method until the sodium chloride supplied to the filtration media reached 100 mg. The air containing sodium chloride had a median size distribution of sodium chloride particles between 0.06 and 0.1 µm, a geometric standard deviation (S.D.) of 1.8 or less, a sodium chloride concentration of 50 mg or less per m³, and a variation of plus or minus 15% or less. The particle filtration efficiency was calculated from the following formula.

NaCl particle mass concentration (mg/m³) = (D1) × K-value/1000
D1: Upstream Detector Count (CPM)
D2: Downstream Detector Count (CPM)
Blank value: (D1/D2) Sensitivity ratio of the detector
K-value: mass conversion count {(µg/m³)/(CPM)}

Statistical Analysis

Mann–Whitney’s U test was performed for comparisons of bacteria numbers between control samples and samples disinfected by MA-T. The significance level of all statistical test results was evaluated at two-sided alpha level of 0.05. The statistical analysis was performed by SPSS ver.26

RESULTS

The results of disinfection test using MA-T spray on surgical masks factitiously contaminated with E. coli are shown in Table 1. When the bacteria on the mask surface were cultured on the BHI agar plate and CFU was determined, the mean number of bacterial colony was 53.2 with S.D. of 49.4. For the whole mask, the mean number of CFU was 168 with S.D. of 173, after 10-fold multiplying the actual colony number on the agar plate. An image of agar plates is shown in Supplementary Fig. S1 (C, D; representative 2 of 6 plates were only shown). The number of bacterial CFU in control was incalculably high (Supplementary Figs. S1A, B). Because the applied bacterial CFU is 2.70 × 10⁷ (log₁₀CFU = 7.43) and CFU of MA-T treated-whole mask is 168 (log₁₀CFU = 2.23), the log₁₀ reduction of CFU of whole mask is 5.2 with treatment of MA-T spraying.

Table 1. Disinfection Test Using MA-T Spray on Surgical Masks Contaminated with E. coli (N = 6)

Part of mask	Sample number						Mean (S.D.)
Part of mask	No.1	No.2	No.3	No.4	No.5	No.6	Mean (S.D.)
Surface^a⁾	4	5	35	70	71	134	53.2 (49.4)
Whole^b⁾	40	70	90	140	160	510	168 (173)

a) Values showed numbers of bacterial colony on each BHI agar plate. b) Values showed 10-fold numbers of bacterial colony on BHI agar plate, because 300 µL of 3 mL was spread onto agar plate as indicated in “Disinfection test using MA-T spray on surgical masks contaminated with Escherichia coli” of Materials and Methods. The number of CFU in control was incalculably high as shown in Supplementary Figs. S1A and B.

The results of disinfection test by MA-T immersion of surgical masks contaminated with E. coli are shown in Table 2. With physiological saline immersion, the mean number of CFU was 2.53 × 10⁷ with S.D. of 0.63 × 10⁷, while all the number of bacteria after MA-T immersion was 0 (or 1>, p = 0.002). Because the control CFU is 2.53 × 10⁷ (log₁₀CFU = 7.40) and CFU of MA-T immersion-mask is less than 1 (log₁₀CFU < 0), The log₁₀ reduction of CFU of whole mask is >7.40 with treatment of MA-T immersion.

Table 2. Disinfection Test by MA-T Immersion of Surgical Masks Contaminated with E. coli (N = 6)

Treatment	Sample number						Mean (S.D.)	p
Treatment	No.1	No.2	No.3	No.4	No.5	No.6	Mean (S.D.)	p
Control ^a⁾	1.83 × 10⁷	1.97 × 10⁷	2.30 × 10⁷	2.57 × 10⁷	3.12 × 10⁷	3.41 × 10⁷	2.53 × 10⁷ (0.63 × 10⁷)	0.002
MA-T ^b⁾	0	0	0	0	0	0	0

p-Value was a result of Mann–Whitney’s U test. a) Values showed 10⁵-fold numbers of bacterial colony on BHI agar plate, because 10⁵-diluted suspension was spread onto agar plate as indicated in “Disinfection test by MA-T immersion of surgical masks contaminated with E. coli” of Materials and Methods. Consequently, the actual mean value of colony number was 253. b) The actual values of 6 samples were 0, which means less than 1 (1 >), and we did not indicated S.D.

Table 3 shows the results of disinfection test using MA-T spray on surgical masks used by health care provider. After spraying MA-T onto used masks, no bacteria were detected on the surface of the masks (1>), while a mean of 21.2 CFU with S.D. of 19.4 (p = 0.002) was detected on the control masks. An image of representative of the BHI agar plate is shown in Supplementary Fig. S2. For the whole mask, a mean of 5 CFU with S.D. of 3.6 was detected after spraying MA-T, compared to a mean of 236 bacteria with S.D. of 156 in the control, which was a significant decrease (p = 0.002).

Table 3. Disinfection Test Using MA-T Spray on Surgical Masks Used by Health Care Provider (N = 6)

Part of mask	Treatment	Sample number						Mean (S.D.)	p
Part of mask	Treatment	No.1	No.2	No.3	No.4	No.5	No.6	Mean (S.D.)	p
Surface	Control	2	11	13	17	27	57	21.2 (19.4)	0.002
Surface	MA-T ^b⁾	0	0	0	0	0	0	0
Whole ^a⁾	Control	72	75	189	288	312	477	236 (156)	0.002
Whole ^a⁾	MA-T	0	3	3	6	9	9	5 (3.6)

p-Values were results of Mann–Whitney’s U test. a) Values showed 3-fold numbers of bacterial colony on BHI agar plate, because 1 mL of 3 mL was spread onto agar plate as indicated in “Disinfection test using MA-T spray on surgical masks used by health care provider” of Materials and Methods. b) The actual values of 6 samples were 0, which means less than 1 (1 >), and we did not indicate S.D.

Table 4 is the results of disinfection test by MA-T immersion of surgical masks used by health care provider. No bacteria (1>) were detected after immersion with MA-T, while a mean of 295 bacterial colony with S.D. of 181 (p = 0.002) was detected on the control pieces.

Table 4. Disinfection Test by MA-T Immersion of Surgical Masks Used by Health Care Provider (N = 6)

Treatment	Sample number						Mean (S.D.)	p
Treatment	No.1	No.2	No.3	No.4	No.5	No.6	Mean (S.D.)	p
Control	88	174	216	262	489	543	295 (181)	0.002
MA-T ^a)	0	0	0	0	0	0	0

p-Value was a result of Mann–Whitney’s U test. a) The actual values of 6 samples were 0, which means less than 1 (1 >), and we did not indicated S.D.

The results of mask performance test before and after MA-T processing are shown in Table 5 and Supplementary Fig. S3. Unused and MA-T untreated N95 showed only a small increase in inspiratory resistance with the cumulative particle supply, and the filtration efficiency remained above 99%. Masks immersed in 150 ppm MA-T for 30 min had a slight increase in inspiratory resistance with cumulative particle supply. Though the collection efficiency was slightly inferior to that of N95 untreated with MA-T, it was above 95%.

Table 5. Performance Test before and after MA-T Treatment of N95 Mask Inspiratory Resistance Test

	Inspiratory resistance test		Particle filtration efficiency test
	Air flow (L/min)	Inspiratory resistance (Pa)	Value	Filtration efficiency (%)	Inspiratory resistance (Pa)	Cumulative particle supply (mg)
Untreated N95	40	22	Initial	99.45	46	2.46
			Minimum	99.36	72	68.17
Disinfected N95 with MA-T	40	23	Initial	97.53	46	2.41
			Minimum	96.94	51	16.87

DISCUSSION

COVID-19 is caused by SARS-CoV-2, which is reported to enter the cell mainly via the angiotensin-converting enzyme 2 (ACE-2) as a receptor.²⁰⁾ ACE-2 was found to be present in the ductal epithelium of the salivary glands and several other tissues.²¹⁾ This fact reinforces the possibility of salivary gland and oral infection. Therefore, it is very important to wear PPEs properly to prevent contamination from saliva. Masks have long been used in order to prevent infection, but in recent years their effectiveness has been reevaluated. Consequently, masks have been proven to be particularly effective against infectious diseases that are spread by droplets and aerosols. The filtering function of the mask prevents the wearer from splashing droplets and prevents bacteria and viruses from entering from outside. It is known that the most contaminated area after wearing a mask is the outer surface of the mask. Considering contact infection through this area, disinfection of the outer surface is the most important priority when reusing a mask.

The largest amount of chlorine-related chemical compounds contained in MA-T is chlorite ion. The amount of chlorite ion of MA-T remains stable for several years at room temperature, and chlorine dioxide is not detected during storage. Joint FAO/WHO Expert Committee on Food Additives (JECFA) has set acceptable daily intake (ADI) for chlorite ions at 0.03 mg/kg body weight per day.²²⁾ Also, WHO guidelines for drinking-water quality established a provisional health-based guideline value of 0.7 mg/L for chlorite in drinking-water.²³⁾ This means that the 100 or 150 ppm MA-T used in this study is safe for humans. When there is a target for disinfection such as microorganisms, chlorite ion transfer to minimum required chlorine dioxide as a disinfectant is caused by catalytic action of Lewis acid. In addition, MA-T safety and efficacy against bacteria, fungi, and viruses have already been demonstrated in our previous studies, and it has been found to be sufficiently effective against SARS-CoV-2 and various microorganisms.¹⁸⁾ MA-T is currently available on the market under A2Care (MA-T: 100 ppm) and BACT-¹O₂ (MA-T: 150 ppm), and is used as a sanitizer and deodorant in airplanes and hotels in Japan. So far there are no reports of health hazards for MA-T. Therefore, we conceived of the use of MA-T for mask reuse.

In this study, we first conducted a disinfection test of MA-T using surgical masks contaminated with E. coli, because E. coli had a high minimum inhibitory concentration (MIC) among various bacteria and was considered to be representative of antimicrobial activity against other bacteria.¹⁸⁾ While the number of bacterial CFU in the control was immeasurably high, the mask sprayed with MA-T showed drastically-reduced numbers of CFU on the mask surface and throughout the mask, but it was impossible to reduce the number to zero. Also, the numbers of CFU had a lot of variation in the 6 samples. It is inferred that MA-T is not exposed to the folds of the mask and that the water repellency of the nonwoven fabric makes it difficult for MA-T to penetrate into the mask. On the other hand, no bacteria were detected at all in the contaminated masks when disinfected by immersion in MA-T. These results suggest that masks can be disinfected by MA-T spray and sterilized by immersion. In the disinfection test of used surgical masks, MA-T spray was able to reduce the bacteria on the mask surface to zero, and significantly reduced the bacteria in the whole mask. The surface of the mask could be sterilized because masks that are in regular use do not contain many bacteria, unlike masks that have been intentionally contaminated. In assuming infection from hands that have touched the surface of the mask, spraying MA-T is enough to disinfect the mask to prevent infection. It should be noted that the reason for the large variation in the controls in Table 3 may be due to the environment and behavior of the medical staff who used the masks. Also, the large variation in whole mask disinfected by MA-T may be due to the mask folds and the water repellency of the nonwoven fabric. When used masks were immersed in MA-T, no bacteria could be detected and sterilization was possible. The N95 mask immersed in 150 ppm MA-T for 30 min showed only a slight increase in inspiratory resistance with cumulative particle supply, which was almost the same increase as untreated N95. The PFE of processed N95 was constantly above 95%, which was slightly lower than that of untreated MA-T N95. In this test, N95 mask was immersed in 150 ppm MA-T for 30 min, and it is presumed that the mask performance will be further assured when we immerse 15 min in 100 ppm MA-T used in the disinfection test. These results suggest that MA-T can be used for disinfection and sterilization of masks without impairing mask performance, unlike disinfection with ethanol.^24,25)

This research has four limitations. The first is low efficacy of chlorine dioxide against spores. Some bacteria belonged in genus Clostridium and genus Bacillus, such as Bacillus anthracis, Bacillus cereus, Clostridium botulinum, Clostridium difficile, and Clostridium perfringens can be causative agents of enteritis and food poisoning. Because MA-T, like other chlorinated agents, has low effectiveness against spore-forming bacteria, MA-T should not be used to disinfect feces or vomit from patients affected by such bacteria, or PPE used in such patient care. Second, the types of masks we tested are limited. It is possible that N95 or surgical masks from manufacturers other than those used in this study may give different results. However, the disinfecting effect of MA-T is clear from previous studies, and exposure of MA-T to bacteria is the key to its bactericidal action. Therefore, we believe that masks can be reused by spraying MA-T in normal use and by immersion in MA-T when sterilization is required. It is desirable to conduct similar tests in the future with products from different manufacturers. The third limitation is lack of performance testing of surgical masks disinfected by MA-T. It would certainly give us good information of reuse by conduct mask performance test on surgical masks. In this study, we focused on N95 masks, which are the most important in terms of performance and suffer the most from shortage in the medical field. It is desirable to conduct performance tests for surgical masks in the future. The last limitation is that the bacteria used in the test are limited or not identified. In the disinfection tests on factitiously contaminated masks, we used only E. coli. The similar tests for other opportunistic pathogens such as Staphylococcus aureus, Enterococcus faecalis, Acinetobacter baumannii, and Pseudomonas aeruginosa will provide further advantage to use MA-T for mask disinfection. In the disinfection tests on used masks, we did not identify the species of bacteria because the medium used in this study is capable of cultivating many kinds of bacteria, and our previous study have shown that MA-T is effective against many kinds of microorganisms. In order to get a clear understanding of the disinfection effect of MA-T, we think it would be useful to conduct identification tests of bacteria on used masks in the future.

The shortage of masks triggered by COVID-19 resulted in a failure to meet the demand of various groups including health care workers, and masks became difficult to obtain. In addition, the price of masks increased sharply, putting pressure on the budgets of hospitals and ordinary households. Demand for reuse of masks, which used to be used once and then disposed, is expected to increase in the future, due to the need to conserve energy, resources, and other environmental considerations. The results of this study suggest that MA-T may be a key drug to solve these problems.

In conclusion, the hypothesis of this study --- that the disinfection of masks by MA-T allows for reuse --- was strongly supported. Disinfection by MA-T immersion has the potential to be applied not only to masks, but also to lab coats, protective clothing, linens, etc., and we hope to see further research on the disinfection and reuse of these items. We also expect that MA-T will be used to address PPE shortages caused by new infectious diseases and PPE shortages in developing countries and other countries with dysfunctional healthcare systems.

Acknowledgments

This work was supported by Grant No. JPMJOP1861 of Program on Open Innovation Platform with Enterprises, Research Institute and Academia (OPERA) in Japan Science and Technology Agency (JST). The URL of JST OPERA is https://www.jst.go.jp/opera/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflict of Interest

Takekatsu Shibata is a director of Acenet Inc. that manufactures the MA-T. Kiyoto Takamori has stock in Acenet Inc. and he is a director of Acenet Inc. The other authors declare no conflict of interest.

Supplementary Materials

This article contains supplementary materials.

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