Article pubs.acs.org/est
Particulate Respirators Functionalized with Silver Nanoparticles Showed Excellent Real-Time Antimicrobial Effects against Pathogens Clark Renjun Zheng,†,‡ Shuai Li,‡ Chengsong Ye,‡ Xinyang Li,∥ Chiqian Zhang,*,§ and Xin Yu*,‡ †
Brown University, Providence, Rhode Island 02912, United States Key Lab of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen, 361021, China ∥ College of Resources and Environment, University of Chinese Academy of Sciences, 19 A Yuquan Road, Beijing, 100049, China § Department of Civil and Environmental Engineering, University of Missouri, Columbia, Missouri 65211, United States ‡
S Supporting Information *
ABSTRACT: Particulate respirators designed to filtrate fine particulate matters usually do not possess antimicrobial functions. The current study aimed to functionalize particulate respirators with silver nanoparticles (nanosilver or AgNPs), which have excellent antimicrobial activities, utilizing a straightforward and effective method. We first enhanced the nanosilver-coating ability of nonwoven fabrics from a particulate respirator through surface modification by sodium oleate. The surfactant treatment significantly improved the fabrics’ water wet preference where the static water contact angles reduced from 122° to 56°. Both macroscopic agar-plate tests and microscopic scanning electron microscope (SEM) characterization revealed that nanosilver functionalized fabrics could effectively inhibit the growth of two model bacterial strains (i.e., Staphylococcus aureus and Pseudomonas aeruginosa). The coating of silver nanoparticles would not affect the main function of particulate respirators (i.e., filtration of fine air-borne particles). Nanosilver coated particulate respirators with excellent antimicrobial activities can provide real-time protection to people in regions with severe air pollution against air-borne pathogens.
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heat and damage the filter media, compromising the original function of particulate respirators.8 Engineered silver nanoparticles (nanosilver or AgNPs) have excellent and broad-spectrum antimicrobial activities and are good candidates that could functionalize particulate respirators. Silver ion release is the predominate antimicrobial mechanism of nanosilver where released Ag+ can strongly bind to important cellular components and efficiently inhibit vital cellular functions.10−16 In addition, nanosilver can generate reactive oxygen species (ROS) with the presence of oxygen.17−19 ROS are highly reactive and can strongly damage numerous cellular components such as proteins, lipids, and nucleic acids.20−26 Unlike antibiotics, it is not easy for microbes to develop resistance to nanosilver because it employs multiple antimicrobial mechanisms.27,28 On the other hand, many engineered nanoparticles have antimicrobial properties, but among them, nanosilver might be the most effective one.29,30 Furthermore, silver nanoparticles have relatively low cytotoxicity to mammalian cells.30,31
INTRODUCTION
Severe air pollution in China has raised great public concerns, and people choose to wear particulate respirators for selfprotection against fine air-borne particles such as PM2.5 (particulate matter with diameters less than 2.5 μm).1−4 High quality particulate respirators commercially available in China are expensive, and consumers hence tend to use them for an extended period of time. Extended use of respirators, however, may cause unexpected health problems, as fine particles intercepted by respirators’ filter media (nonwoven polymeric fabrics) frequently carry numerous types of air-borne bacteria.3,5 These bacteria, nurtured by human saliva, can remain viable on filter media for days and be inhaled due to reaerosolization by intense sneezing and coughing,6 posing unexpected threats to wearers’ health.7 Therefore, inactivation of airborne microbes accumulated on particulate respirators is indispensable to providing wearers better protection. Many methods have been exploited to kill airborne pathogens accumulated on respirators, including ethylene oxide oxidization, microwave steam exposure, microwave irradiation, and chlorination.8,9 While these methods can effectively kill the bacteria ex situ, they are unable to provide a real-time antimicrobial control while the respirators are being worn. In addition, microwave irradiation could generate extreme dry © XXXX American Chemical Society
Received: February 15, 2016 Revised: May 11, 2016 Accepted: June 6, 2016
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DOI: 10.1021/acs.est.6b00788 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
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wettability needs to be altered from oil-wet to water-wet. To accomplish this, the middle layer was first removed from the particulate respirator and cut into samples measured approximately 2 cm in diameter. The samples were then immersed in 2.4 × 10−3 M sodium oleate overnight for surface modification. The surfactant-treated fabric samples were finally air-dried at room temperature after briefly being rinsed by D.I. water. Wettability of the fabric samples before and after surfactant treatment was examined by measuring water contact angles on the sample surface using a goniometer (KRUSS, DSA100, Germany) (Figure 1). The surface morphology of the samples was also characterized by field emission scanning electron microscope (FESEM, S-4800, Hitachi, Japan) (Figure S1). Coating AgNPs on Fabrics. Silver nanoparticles were coated in situ on the fabric surface by following previously reported AgNP synthesis procedures57,58 with minor modifications. Briefly, a 12.5 mL solution of 14 mM silver nitrate was gently mixed with 237.5 mL of 0.06 g/L PVA solution containing surfactant-treated fabric samples. Then, an aliquot of 1.25 mL 14 mM NaBH4 solution was added dropwise to this mixture under continuous stirring at 700 rpm. Particle size and morphology of AgNPs prepared following the same procedure but in the absence of fabrics were characterized by a transmission electron microscope (TEM, H-7650, Hitachi, Japan) (Figure S2). Figure S3 shows the size distribution of the freshly prepared nanosilver. X-ray photoelectron spectroscopy (XPS) measurement of AgNPs coated on the fabrics (Figure 2) was performed on a ESCALAB-MK II instrument (VG Co., United Kingdom), and both survey and high resolution spectra of Ag3d were collected and calibrated to the binding energy of C1s at 284.6 ev. Antimicrobial Tests. Cell cultures of P. aeruginosa PAO1 and S. aureus were cultivated in Lysogeny Broth (LB)-Miller (tryptone 10 g/L, yeast extract 5 g/L, and sodium chloride 10 g/L) at 37 °C for 8 h with shaking at 200 rpm to reach the stationary phase. The final cell cultures were both diluted to a cell density of 108 CFUs/mL. An aliquot of 100 μL cell culture was then spread onto an LB-Miller agar plate along a line crossing the center of the plate. The center of the line was then covered with either a AgNP-coated fabric sample or an uncoated fabric sample (control), both of which had been sterilized. The sterilization was carried out at 121 °C (103.4 kPa) for 15 min. Evidence has showed that such a sterilization process (autoclaving) would not affect the properties of silver nanoparticles.59 The agar plates were then incubated at 37 °C for 24 h to observe the antimicrobial efficiency of AgNPfunctionalized fabrics against the two bacterial strains. In addition to the macroscopic assessment of the inhibitive capabilities of AgNP-coated fabrics, their antimicrobial efficiency was also characterized microscopically by FESEM. Both AgNP-coated and the untreated fabric samples that had contacted P. aeruginosa PAO1 and S. aureus from the above agar-plate testes were collected, pretreated with glutaraldehyde, rinsed by alcohol, and dried before FESEM imaging.
Owing to the unique merits discussed above, nanosilver has been used as antimicrobial agents in a wide variety of consumer products such as medical dressings (e.g., burn dressings), medical devices (e.g., catheter), and antimicrobial/antiodor textiles (e.g., antiodor underwear).31−36 To the best of our knowledge, however, research related to the application of nanosilver to functionalize particulate respirators is rare. We speculated that coating silver nanoparticles on particulate respirators would augment the function of respirators by providing real-time control of microbial growth. We chose Pseudomonas aeruginosa PAO1 and Staphylococcus aureus as representative air-borne bacteria in the current study to examine the antimicrobial activities of surface coated fabrics. P. aeruginosa and S. aureus are common Gram-negative and Gram-positive pathogenic bacteria, respectively.37,38 P. aeruginosa is a common and important air-borne bacterium which can cause many serious diseases in human beings.39−42 For instance, it is a major reason for morbidity and mortality for individuals with cystic fibrosis (CF).43 Cough of patients with CF can generate aerosols with P. aeruginosa.44,45 Evidence showed that exposure to PM2.5 in young children with CF is associated with initial P. aeruginosa acquisition.46 Furthermore, P. aeruginosa has been detected on air-borne particles (outdoor air samples) during haze events in China.47 S. aureus is also an important air-borne pathogen that presents in indoor bioaerosols and has the potential to infect people via airborne transmission.48−53 As an example, S. aureus has presented on air-borne particles in hospital wards.54 In addition, both P. aeruginosa and S. aureus have been isolated from dust samples during dust storm events.55 As a result, we utilized P. aeruginosa and S. aureus in this study as model strains for an antimicrobial test due to their important roles as air-borne pathogens. This practice would yield a conclusive analysis of antibacterial efficacy of AgNP-coated respirators. The objectives of this study were to develop a straightforward and effective AgNP-coating method to functionalize particulate respirators and examine their antibacterial activities against two bacterial strains representing airborne bacteria, S. aureus and P. aeruginosa. Both macroscopic agar-plate tests and scanning electron microscope (SEM) microscopic characterization were used to assess the antibacterial capabilities of AgNP-functionalized fabrics in inhibiting the growth of the model bacterial strains.
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MATERIALS AND METHODS Materials. Sodium borohydride (NaBH4), silver nitrate, poly(vinyl alcohol) (PVA), and sodium oleate were purchased from Sinopharm Chemical Reagent Co., Ltd. (Shanghai, China), and used without further purification. Particulate respirator 3M N95 (code: 8210VCN, 3M Company, U.S.A.) was selected and tested in this study because it is a National Institute for Occupational Safety and Health (NIOSH) approved respirator and has a high market share in China. P. aeruginosa PAO1 (ATCC 15692) and S. aureus (isolated from Jiulong River, Fujian, China) were used as the model bacterial strains to examine the antibacterial activities of AgNP-coated fabrics. Modification of Wettability of Fabric Surfaces and Characterization. Preliminary tests indicate that the original 3M N95 particulate respirator is hydrophobic, in agreement with its composition which consists mainly of nonwoven fabrics of polypropylene and polyester.56 In order to effectively coat silver nanoparticles on these nonwoven fabrics, their surface
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RESULTS AND DISCUSSION Characterization of the Respirator’s Fabric Fibers. Fabric fibers of the 3M N95 respirator were found entangled with each other (Figure S1a), a common feature of typical nonwoven fabrics. Diameters of fabric fibers covered a range of sizes from about 15 μm to as large as 340 μm, but most fibers had diameters within 15 to 30 μm (Figure S1b). B
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Figure 2. XPS spectra of (a) survey scan and (b) high-resolution scan of Ag3d for post AgNP coating fabrics treated by sodium oleate.
Respirator fabrics under the current study consist of 40% to 70% of polypropylene and 10% to 30% of polyester.56 These polymeric fabrics have low surface energy due to low surface density of polar functional groups, and hence they are hydrophobic in nature. In the current study, pretreatment of fabrics with sodium oleate, a nontoxic and environmentally friendly surfactant,61,62 has two functions. First, wetting reversal of the fabric surface can be achieved by orderly lining up the surfactants’ hydrophobic tails perpendicular to the fabric surface through hydrophobic interactions. Second, the exposed carboxylic functional groups complexed with silver ions can serve as in situ surface reaction sites for AgNP synthesis in the existence of externally added reductant (NaBH4). XPS analysis confirmed the formation of AgNPs on the fabrics. As presented in the survey spectra (Figure 2a), Ag3d peaks were easily distinguished. The high resolution spectra of Ag3d (Figure 2b) indicated two binding energies at 374.14 and 368.14 eV, corresponding to the signals of Ag3d3/2 and Ag3d5/2 of metallic silver, respectively.63 It has been reported that the binding energies of metallic Ag and Ag+ of Ag2O are located at 368.3 eV and 367.6 eV to 367.8 eV, respectively.64−66 In our research, the slight shift of the signal of AgNPs from 368.3 eV to 368.14 eV67 might be caused by oxidation of small amounts of metallic silver on the surface. The majority of AgNPs coated on fabrics, however, should still be in metallic silver form.
Figure 1. Static water contact angles on the middle-layer fabrics of 3M N95 particulate respirators: (a) Original fabrics before surfactant treatment (θa); (b) fabrics after surfactant treatment with sodium oleate (θb); and (c) fabrics after surfactant treatment and nanosilver coating (θc).
Surfactant Treatment of Respirator Fabrics and AgNP Coating. Surface wettability of fabrics before and after surfactant treatment was assessed by measuring the static water contact angle on the fabric surface. Figure 1 shows representative contact angle images of fabrics before (θa) and after (θb) surfactant treatment, and post in situ coating of AgNPs (θc). θa, θb, and θc were 122° ± 6°, 56° ± 5°, and 45° ± 4°, respectively, suggesting that wetting reversal of fabrics was achieved by surfactant modification. In a similar study to improve the wetting preference of polypropylene fibers, a twostage sequential treatment with dioctadecyldimethylammonium bromide (DODAB) and a soybean protein shifted the contact angle of samples from 128° to almost 0°.60 C
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Figure 3. Macroscopic examination of antimicrobial capability of AgNP-fabrics against P. aeruginosa PAO1 and S. aureus by evaluating the growth statuses of bacteria incubated on an agar plate covered with fabrics with different treatments: (a) P. aeruginosa PAO1 on agar plate with an untreated fabric sample; (b) S. aureus with an untreated fabric sample; (c) P. aeruginosa PAO1 with a AgNP-coated fabric sample; and (d) S. aureus with a AgNP-coated fabric sample.
Macroscopic Examination of Antimicrobial Capability of AgNP-Fabrics. Antimicrobial efficiency of AgNP-fabrics against the two selected bacterial strains was assessed by examining the bacterial growth track, a vertical path of bacterial lawn formed on the agar plates after 24-h incubation upon inoculation. Figure 3a,b shows the results of negative controls for P. aeruginosa PAO1 and S. aureus, respectively, using untreated fabrics. Both bacterial growth tracks were unaffected in the presence of original fabrics, showing visible growth for both P. aeruginosa PAO1 and S. aureus underneath the untreated fabrics. By contrast, bacterial growths for both pathogens were strongly inhibited by AgNP-coated fabrics (Figure 3c,d) placed across the center of each path, leaving broken tracks of bacterial growth and apparent inhibition zones for both cases. The above macroscopic antibacterial tests indicate that, contrasted with untreated respirator fabrics, AgNP-coated fabrics can effectively inhibit bacterial growth of both model strains P. aeruginosa PAO1 (Gram-negative) and S. aureus (Gram-positive) selected in this study. As AgNP-coated fabrics demonstrated effective inhibitive effects toward P. aeruginosa PAO1 and S. aureus, which can be traced in various environmental media including air,55 it is promising that these modified fabrics would show potential antibacterial capabilities against other air-borne pathogens. Microscopic Characterization of Antimicrobial Capability of AgNP-Fabrics. Antimicrobial efficiency of treated and untreated fabrics was also examined microscopically by characterizing these fabrics post the agar-plate test (Figure 4).
We screened many different parts of the nanosilver-coated fabrics post-antimicrobial test and found that attachment of cells onto most parts was minimal. For instance, in the image zone scanned by FESEM, only few S. aureus cells were detected on the AgNP-coated fabric (Figure 4a). A similar pattern was observed for the AgNP-coated fabric sample against P. aeruginosa PAO1 (Figure 4c). Those few bacterial cells remaining on the surface of the AgNP-coated fabric fibers might be the inoculated bacteria that had been previously spread on the agar plates. In agreement with previous studies,68−71 we observed cell debris on fibers of nanosilvercoated fabrics post-antimicrobial test (Figure 4a,c). This observation indicates that many cells were disrupted or destructed due to the strong antimicrobial activities of nanosilver, as no growth of bacteria colonies was observed in the corresponding FESEM images. By contrast, under the same magnification, FESEM images show that both S. aureus and P. aeruginosa PAO1 cells grew well on the untreated fabric, with a large number of cells attached to fabric fibers (Figure 4b,d). The contrast between bacterial growth patterns on untreated and AgNP-coated fabrics, as detected by FESEM (Figure 4), clearly demonstrated that AgNP-functionalized fabrics had strong antimicrobial efficacy against both P. aeruginosa PAO1 and S. aureus. In conclusion, results of FESEM scannning and macrospopic agar-plate exmination are in good agreement with each other that nanosilver-coated fabrics had good antimicrobial activities. Potential Applications of Nanosilver-Coated Particulate Respirators. Nanosilver-functionalized particulate resD
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Figure 4. Growth status of bacteria on respirator fabrics post-agar-plate tests as revealed by FESEM: (a) S. aureus on AgNP-coated fabric fibers; (b) S. aureus on untreated fabric fibers; (c) P. aeruginosa PAO1 on AgNP-coated fabric fibers; and (d) P. aeruginosa PAO1 on untreated fabric fibers.
nanoparticles can effectively inhibit the growth of two model strains (i.e., P. aeruginosa PAO1 and S. aureus) that are traced in typical air pollution.55 It is expected that the developed coating method would have only a minimal impact on the major function of respirators in filtering air-borne particulate matter, as the treating process does not significantly affect the 3-D matrixes of the nonwoven fabrics. It is thus promising that incorporation of this simple AgNP coating process to future manufacturing processes would endow particulate respirators an additional capability in real-time control of air-borne pathogens, without compromising their major function. Further studies, however, need to be conducted to examine the AgNP-coated respirators’ in situ antimicrobial properties against simulated air streams or bioaerosols bearing more complex matrices of field air-borne pathogens. We argue that surfactant treatment and subsequent nanosilver coating would not affect the main function (i.e., filtration) of the respirators in that the physical structure of fabric samples did not change after nanosilver coating (Figure 4 and Figure S1). This assumption should be tested in the future to clarify whether the antimicrobial surface coating can affect the filtration performance of respirators. In addition, we only detected the antimicrobial activities of nanosilver-coated respirators against two model bacterial strains. Different pathogens would have different susceptibilities toward nanosilver. More research should be conducted to examine the effectiveness of nanosilver-coated respirators in controlling the (re)growth of different air-borne pathogens. Furthermore, even though AgNPs have non- or low-cytotoxicity against mammalian cells,30,31 it is still a concern whether the coated fabric would
pirators with real-time antimicrobial activities would have many potential applications. Fine air-borne particulate matter such as PM2.5 and PM10 is an important part of air pollution and has caused huge health concerns. Air-borne particulate matter is often associated with microorganisms, some of which might be pathogenic.5,72 For instance, one study revealed that PM10 pollutants in Beijing during a recent haze event contained more than 1300 inhalable microorganism species including pathogens.3 Because of health concerns, many individuals resort to wearing particulate respirators as a passive defense against fine particulate matter in polluted air. Particulate respirators available in the market, however, generally do not provide antimicrobial functions or might even serve as suitable substrates supporting bacterial growth. Particulate respirators with surface nanosilver coating showed good inhibitory effects on bacterial growth in this study. They can provide efficient and real-time antimicrobial protection to individuals who use particulate respirators during air pollution events. On the other hand, people in clinical settings such as medical doctors and nurses might have high chances to be infected by air-borne pathogens. Nanosilver-coated particulate respirators could also provide more protection to people associated with clinical settings. Environmental Implications and Future Work. The current study developed an effective and environmentally friendly method to coat silver nanoparticles on typical nonwoven fabrics of particulate respirators, using a representative commercially available product as an example. Both macroscopic and microscopic tests revealed that surface modification of the respirator’s nonwoven fabrics with silver E
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release AgNPs and exhibit adverse health effects. Consequently, whether AgNPs can be aerosolized and inhaled during breathing should be tested. Nanosilver-coated respirators might be washed and reused by users. Nanosilver coated textiles would release nanosilver during washing into sewage.34,35 Nanosilver release during washing would not only affect the antimicrobial activities of nanosilver-coated respirators but also have potential adverse effects on an aquatic ecosystem. Thus, potential nanosilver release from AgNPcoated respirators during washing needs to be further identified.
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ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.est.6b00788. FESEM images of the middle-layer fabric fibers from the untreated 3M N95 particulate respirator (Figure S1), TEM images of freshly prepared silver nanoparticles (Figure S2), and size distribution of freshly fabricated nanosilver (Figure S3) (PDF)
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AUTHOR INFORMATION
Corresponding Authors
*(X.Y.) Phone & Fax: +86-592-6190780. E-mail: yuxinsky@ icloud.com. *(C.Z.) Phone: +01-573-239-2887. E-mail: czxr9@mail. missouri.edu (co-corresponding author). Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS Financial supports for this study from the National Natural Science Foundation of China (51278482 and 51078343) and the National High-Tech R&D (863) Program of China (2012AA062607) are greatly acknowledged. We thank graduate students Mr. Chunming Wang, Mr. Song Gong, and Ms. Lu Lv at the Institute of Urban Environment, Chinese Academy of Sciences, for their experimental assistance. We also extend our thanks to graduate student Ms. Jiao Li at the University of Chinese Academy of Sciences for her assistance in XPS data analysis.
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DOI: 10.1021/acs.est.6b00788 Environ. Sci. Technol. XXXX, XXX, XXX−XXX
