Letter www.acsami.org
Antisuperbug Cotton Fabric with Excellent Laundering Durability Ming Yu,†,‡ Ziqiang Wang,†,‡ Min Lv,§ Rongzhang Hao,⊥ Rongtao Zhao,⊥ Lihua Qi,⊥ Shima Liu,§ Chuhong Yu,‡ Bowu Zhang,‡ Chunhai Fan,§ and Jingye Li*,‡ ‡
CAS Center for Innovation in Advanced Nuclear Energy, Shanghai Institute of Applied Physics, and §CAS Key Lab of Interfacial Physics and Technology, Shanghai Institute of Applied PhysicsChinese Academy of Sciences, Shanghai 201800, P. R. China ⊥ Institute for Disease Control and Prevention, Academy of Military Medical Sciences, Beijing 100036, P. R. China S Supporting Information *
ABSTRACT: Multidrug-resistant superbugs are currently a severe threat to public health. Here, we report a novel kind of antisuperbug material prepared by irradiation induced graft polymerization of 1-butyl-3-vinyl imidazole chloride onto cotton fabric. The reduction of superbugs on this fabric is higher than 99.9%. Attributed to the strong covalent bonding between the graft chains and the cellulose macromolecules, the antisuperbug performance did not decrease even after 150 equiv of domestic laundering cycles. Covalent bonding also prevented the release of the antibacterial groups during application and guarantees the safety of the material, which was proved by animal skin irritation and acute oral toxicity tests.
KEYWORDS: antisuperbug cotton fabric, antibiotic resistance, radiation induced graft polymerization, laundering durability, covalent bonding
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major antibiotic-sensitive bacteria but allowing minor drugresistant bacteria to assume the dominant position. For example, methicillin-resistant Staphylococcus aureus (MRSA) and vancomycin-resistant Enterococci faecium (VREF) appeared soon after the application of these drugs.6,7 In 2010, a new gene, called “New Delhi metallo-β-lactamase 1 (NDM-1)”, was reported to have caused resistance to numerous antibiotics and could be transferred among bacteria, increasing the spread of resistance as well as the difficulties in their treatment.8 These antibacterial resistance issues have attracted the attention of health authorities all over the world.9,10 Stopping cross-infections, especially in hospitals and longterm care facilities where the environment is conducive for superbugs, is one prior issue.11 Important factors that should be considered beyond the patients themselves include the bioburden residue on the surfaces of materials used.12,13 Recently, a paper reported a significantly reduced bioburden using a copper alloy instead of ordinary metal parts in several hospitals due to the intrinsic broad-spectrum antibiotic activity of metallic copper.14 Patients’ clothings are also a suspected source of superbugs since there is a long time-window between sterilization cycles allowing superbugs to proliferate on clothes.15 There are two basic requirements for an antisuperbug fabric. First, the inhibiting agents should be attached firmly to the fabrics and should not be released into the environment,
uperbugs, defined as bacteria carrying resistance genes to many antibiotics, are becoming an increasingly serious threat to public health.1−3 Antibiotic resistance might be a direct result of the overuse of antibiotic drugs,4,5 eradicating Scheme 1. (a) Synthesis of Antisuperbug Cotton Fabric by Radiation Induced Graft Polymerization; (b) Antisuperbug Mechanism of Cotton-g-PBVIM
Received: June 23, 2016 Accepted: July 27, 2016 Published: July 27, 2016 © 2016 American Chemical Society
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DOI: 10.1021/acsami.6b07631 ACS Appl. Mater. Interfaces 2016, 8, 19866−19871
Letter
ACS Applied Materials & Interfaces
Figure 1. (a) Picture of the pristine cotton fabric and the cotton-g-PBVIM (DG = 14.8%). (b) Relationship between DG and the monomer concentration (absorbed dose = 30kGy). (c) FT-IR ATR spectra of the pristine cotton fabric and cotton-g-PBVIM (DG = 14.8%). SEM images (×2000) of (d) the pristine cotton fabric and (e) the cotton-g-PBVIM (DG = 14.8%).
even under standard laundry and sterilization procedures. Second, the antibacterial mechanism should differ from antibiotics to avoid developing additional or cross-resistance. Durable functionalized cotton fabrics can be prepared via the radiation-induced graft polymerization (RIGP) method, which utilizes radicals that are generated on the main chain of cellulose macromolecules under irradiation to initiate graft polymerization of the vinyl monomers. Because the functional graft chains are bonded covalently with the cellulose macromolecules, the functionalized cotton fabrics have excellent mechanical and thermal durability, which can maintain their properties after hundreds of normal laundering cycles, thousands of abrasion cycles, and steam ironing.16,17 In addition, the breathability of the resultant functional fabrics is comparable to that of pristine cotton fabrics since the woven structures are unchanged, which is important for the wearing comfort.18
Imidazolium salts (IMSs) are a large family of ionic liquids containing imidazole rings.19 Many N-substituted small imidazolium molecules have good antibacterial activity even to superbugs like MRSA.20 The antibacterial mechanism of IMSs and their polymeric derivatives is believed to involve the electrostatic interaction of the cationic portion with the negatively charged bacterial cell wall. In addition, their lipophilic N-substituted groups disturb cell membranes, resulting in leakage of intracellular substances and cell death. This mechanism is promising in terms of combating superbugs, because it is quite different from the interactions between antibiotics and bacteria. In the current study, a novel antisuperbug cotton fabric was created by RIGP of the 1-butyl-3-vinyl imidazole chloride (BVIM) onto cotton fabric, taking advantage of the physical interaction mechanism between graft chains and superbugs as illustrated in Scheme 1. In addition to antibacterial performance, the laundering durability and safety (i.e., skin irritation 19867
DOI: 10.1021/acsami.6b07631 ACS Appl. Mater. Interfaces 2016, 8, 19866−19871
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the stretching vibration of the imidazole ring,21 demonstrating the successful graft polymerization of BVIM onto the cotton fabric. SEM images of the pristine cotton fabric and cotton-gPBVIM are compared in Figure 1d, e. The integrated fibers structure is not affected after the graft polymerization, however, a gel-like layer stuck on the fibers surface of the cotton-gPBVIM was formed because of the accumulation of the graft chains. Cotton-g-PBVIM with DG of 14.8% was used to test the antibacterial properties because the softness and moisture permeability of the cotton fabric did not decrease under this DG (Figure S1). The broad-spectrum antibacterial properties of cotton-g- PBVIM was tested by measuring the inactivation efficiency to different Gram-positive and Gram-negative bacteria including E. coli, K. pneumoniae, S. aureus, E. faecium and A. calcoaceticus, according to different industry standards at different agencies (details are listed in the Supporting Information). For the reader’s convenience, the result is presented in the form of reduction ratio of the colony counts of the bacteria incubated on the cotton-g-PBVIM to that on the pristine cotton fabric. As presented in Figure 2a (calculated from data in Tables S1 and S2, images of bacteria colony are shown in Figures S2−S5), a strong and broad-spectrum antibacterial property of the cotton-g-PBVIM was demonstrated by the reduction of more than 99.9% of all bacteria after 18 or 24 h according to the standard’s requirements, regardless of the Gram-positive bacteria or of the Gram-negative bacteria with an additional outer membrane for protection. Especially, Acinetobacter sp. as a conditional pathogenic bacteria, which is difficult to kill with traditional antibacterial agents, was also eradicated which illustrated the effective antibacterial property of the IMS graft chains. Three superbugs, MRSA, VREF, and A. calcoaceticus carrying blaNDM-1 gene, were used in this study. MRSA is a S. aureus mutant that shows resistance to the penicillin, particularly methicillin, involving a drug resistance gene (mecA) that decreases the affinity of penicillin to the relevant proteins.22 Activation of the drug resistance gene in VREF is triggered by autophosphorylation of the VanR protein in the cell wall.23 As expected, the reduction to these superbugs inoculated onto cotton-g-PBVIM and cultured was also over 99.9%, comparable to their relatives (Figures S6 and S7). Remarkably, the complete kill of the A. calcoaceticus carrying blaNDM-1 as shown in Figure 2b, c, is the first report of an antibacterial textile that can inactivate superbugs carrying the NDM-1 gene that cause a dangerous multidrug resistance, to the best of our knowledge. The cellular structure of fungi differs from bacteria; however, the cell wall of fungi contains negatively charged phosphatidylethanolamine.24 Theoretically, IMS graft chains on cotton-gPBVIM should have activity against fungi, which is demonstrated by the inactivation efficacy over 99.9% to C. albicans (Figure S8). From the results given above, it is apparent that both bacteria, including superbugs, and fungi can be killed in contacting with cotton-g-PBVIM. The cell walls of the bacteria and fungi are negatively charged at physiological pH, therefore the positively charged graft chains can be attracted electrostatically to the cell wall, and the hydrophobic butyl groups can disturb this structure leading to the efflux of intracellular substances and finally killing the bacteria and fungi. Because negatively charged cell wall is the result of the natural requirement, mutations to resist the imidazolium group seem
Figure 2. (a) Reduction percentage of common bacteria, superbugs, and fungi cultured on cotton-g-PBVIM (DG = 14.8%) after period time (18 h according to ISO standard 20743 marked as #ISO or 24 h according to AATCC method 100−2012 marked as #A). The colony of A. calcoaceticus carrying blaNDM-1 gene cultured on (b) the pristine cotton fabric and (c) the cotton-g-PBVIM (DG = 14.8%). The SEM images (×50 000) of E. coli cultured for 30 min on (d) the pristine cotton fabric and (e) the cotton-g-PBVIM (DG = 14.8%).
and acute oral toxicity) of the antisuperbug cotton fabric were also validated. The functional cotton fabric, named as cotton-g-PBVIM in the following, was prepared via RIGP method and then exacted with hot-water to remove the residue monomer and homopolymer thoroughly. The color of the cotton-g-PBVIM with a degree of grafting (DG) of 14.8% turned to light yellow from white (Figure 1a) because of the conjugation effect of the imidazole rings in the graft chains. Figure 1b shows the linear increasing dependence relationship of DG on the monomer concentration because more BVIM was graft polymerized at higher concentrations, which enabled us to easily control the amount of DG. The chemical structure of the cotton fabrics was measured by FT-IR attenuated total reflection (ATR) spectroscopy analysis as given in Figure 1c. Compared to the spectrum of the pristine cotton fabric, a new band at 1576 cm−1 appeared on the spectrum of cotton-g-PBVIM resulted from 19868
DOI: 10.1021/acsami.6b07631 ACS Appl. Mater. Interfaces 2016, 8, 19866−19871
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Figure 3. (a) Set-up of the accelerated laundering test according to AATCC Test method 61−2006 2A. (b) After 30 accelerated laundering cycles, the reduction percentage of common bacteria, superbugs, and fungi cultured on cotton-g-PBVIM (DG = 14.8%) after period time 24 h according to AATCC method 100−2012. (c) The FT-IR ATR spectra and (d) the XPS spectra of the cotton-g-PBVIM (DG = 14.8%) before and after 30 accelerated laundering cycles.
can kill certain drug-resistant bacteria, such as MRSA, mainly by immobilizing copper, silver or TiO2 nanoparticles, their durability is rarely mentioned.27−29 If there is no strong connections between antibacterial nanoparticles and textiles, the nanoparticles are easily released during the application, which is not only lowering the antibacterial properties of the textiles but also suspect to do harm to the human body and environment. The covalent bonding between the graft chains and the cellulose macromolecules promising the imidazolium groups will firmly attached to the cotton fabric during the application, guaranteeing excellent laundering durability and safety. The inactivation efficacy of cotton-g-PBVIM after 30 cycles of accelerated laundering (setup as Figure 3a, details are in the Experimental Section in the Supporting Information, 30 cycles of accelerated laundering equal to 150 domestic laundering episodes) to E. coli, S. aureus, MRSA, VREF and C. albicans, was still higher than 99.9%, almost unchanged as compared to the value of the one as-prepared in Figure 3b (calculated from the data in Table S3). This excellent laundering durability result is consistent with our previous studies, which means the covalent bonds are strong enough to survive the mechanical rubbing and detergent effect in laundering, this was confirmed by the FT-IR ATR spectroscopy and X-ray photoelectron spectroscopy (XPS) analyses presented in Figure 3c, d. The element contents analysis yielded the same results, where the change of N element
unlikely. From the SEM images in Figure 2d, e, it can be found that E. coli exposed to pristine cotton fabric maintained their cellular integrity after 30 min, whereas E. coli exposed to cottong-PBVIM lost their cellular integrity, indicating cell damage and death.25 Cell membrane lysis is consistent with the mechanism discussed in this work. The reason for the outstanding antisuperbug efficiency of the functionalized cotton fabric is that the effect occurs external to the body and the antibacterial groups are covalently bonded, thus the composition of the antibacterial groups is not limited compared to drugs used in vivo. Vancomycin, for example, is often used to cure patients infected with MRSA; its minimum inhibitory concentration is 2 mg/L, and its concentration in blood should be controlled below 20 mg/L to avoid toxicity,26 meaning the concentration of the functional antibacterial group is about 1 × 10−5 mol/kg in vivo. However, the content of the imidazolium groups on cotton-g-PBVIM with DG of 14.8% calculated here is 0.6 mol/kg. The concentration of the antibacterial groups to bacteria on cotton-g-PBVIM is 4−5 orders of magnitude higher than that of antibiotics used to kill bacteria in vivo. To this effect, almost all bacteria on cotton-gPBVIM were killed and the rare survivor would have no opportunity to mutate. Laundering durability is another key factor for the commercial application of the antisuperbug cotton fabric. Although there are many reports on antibacterial textiles that 19869
DOI: 10.1021/acsami.6b07631 ACS Appl. Mater. Interfaces 2016, 8, 19866−19871
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Figure 4. Animal skin irritation results according to ISO 10993.10−2010 standard. The images are rabbits’ back contacting cotton-g-PBVIM with DG of 14.8% (in the circles marked with red-dotted lines) and negative control (in the circles marked with blue-dotted lines) at 0, 1, 24, 48, and 72 h.
this study. The advantages lie in the following points. First, the fabric was shown to indeed effectively inhibit bacteria together with their antibiotic resistant mutants so-called superbugs and fungi with a reduction higher than 99.9%, demonstrating a broad-spectrum and efficient antimicrobial property. Second, covalent bonding assures that the graft chains are integrated with the cellulose macromolecules, leading to the effective maintenance of antibacterial property after 150 equivalent laundering cycles. Last, the covalent bonding prevents the graft chains from being released into the environment during their application, guaranteeing the safety of the cotton-g-PIMS fabrics, which is supported by negative results from the skin irritation and acute oral toxicity tests. Overall, the encouraging results of the current study, especially the ability to eradicate superbugs carrying the NDM-1 gene, made a first step toward the future tests in hospitals.
content of cotton-g-PBVIM was very small (from 3.56 to 3.66%) after laundering. According to standards on the safety evaluation of antibacterial textiles, animal skin irritation and acute oral toxicity are two requisite tests. Cotton-g-PBVIM samples and untreated control cotton fabrics were applied directly to the back skin of male rabbits as illustrated in Figure S8 according to the ISO 10993.10−2010 standard. After 24, 48, and 72 h, neither erythema nor edema was found (Figure 4). The primary irritation index of cotton-g-PBVIM is 0 (Tables S4 and S5). The acute oral toxicity test was conducted based on GB 15193.3−2014. Usually, the antibacterial finishing agent is used to evaluate the toxicity of antibacterial fabric prepared via finishing method.30 However, in this study, the antisuperbug cotton fabric was prepared by grafting method and the monomer BVIM can not be used to evaluate the toxicity of cotton-g-PBVIM directly, because the toxicity of monomer may be quite different to that of its polymer form. Cotton-g-PBVIM was immersed in water and extracted at 60 °C for 2 h, then the extracted solution was administered orally to 10 male and 10 female mice. The mice were observed every 2 days for 2 weeks and no toxic symptoms were found, nor did any of the mice die by the end of the 2 weeks observation period (Table S6). No pathological changes were found in the surviving mice. The absence of any dermal or acute oral toxicity can be attributed to the strong covalent bonds ensuring that the PBVIM grafting chains are permanently immobilized on the cotton fabric and there is no release of IMS groups during the use of these fabrics. These results reveal the safety of cotton-g-PBVIM. In conclusion, an antibacterial cotton fabric named cotton-gPBVIM was successfully prepared by graft polymerization in
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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/acsami.6b07631. Experimental details, data and images of the colony count of various bacteria cultured on the control sample and the cotton-g-PBVIM with the DG of 14.8%, antibacterial performance cotton-g-PBVIM after 30 accelerated laundering cycles, primary irritation index of animal skin irritation tests, results of acute oral toxicity tests (PDF) 19870
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AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Author Contributions †
M.Y. and Z.Q.W. contributed equally to this work.
Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS This work was financially supported by the National Natural Science Foundation of China (51473183 and 11475246). REFERENCES
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