Highly potent silver-organoalkoxysilane antimicrobial porous nanomembrane
© Umar et al.; licensee Springer. 2013
Received: 2 November 2012
Accepted: 3 February 2013
Published: 10 April 2013
We used a simple electrospinning technique to fabricate a highly potent silver-organoalkoxysilane antimicrobial composite from AgNO3-polyvinylpyrrolidone (PVP)/3-aminopropyltrimethoxysilane (APTMS)/tetraethoxysilane (TEOS) solution. Spectroscopic and microscopic analyses of the composite showed that the fibers contain an organoalkoxysilane ‘skeleton,’ 0.18 molecules/nm2 surface amino groups, and highly dispersed and uniformly distributed silver nanoparticles (5 nm in size). Incorporation of organoalkoxysilanes is highly beneficial to the antimicrobial mat as (1) amino groups of APTMS are adhesive and biocidal to microorganisms, (2) polycondensation of APTMS and TEOS increases the membrane’s surface area by forming silicon bonds that stabilize fibers and form a composite mat with membranous structure and high porosity, and (3) the organoalkoxysilanes are also instrumental to the synthesis of the very small-sized and highly dispersed silver metal particles in the fiber mat. Antimicrobial property of the composite was evaluated by disk diffusion, minimum inhibition concentration (MIC), kinetic, and extended use assays on bacteria (Escherichia coli, Bacillus anthracis, Staphylococcus aureus, and Brucella suis), a fungus (Aspergillus niger), and the Newcastle disease virus. The membrane shows quick and sustained broad-spectrum antimicrobial activity. Only 0.3 mg of fibers is required to achieve MIC against all the test organisms. Bacteria are inhibited within 30 min of contact, and the fibers can be used repeatedly. The composite is silver efficient and environment friendly, and its membranous structure is suitable for many practical applications as in air filters, antimicrobial linen, coatings, bioadhesives, and biofilms.
KeywordsPolyvinylpyrrolidone (PVP) Silver Nanoparticles Antimicrobial Composite fibers
For the purpose of achieving higher antimicrobial functionality and circumventing the solubility problems associated with silver-based antimicrobial materials, duo- and multiaction-component composites harboring silver and its halides with other antimicrobial agents were fabricated [1–3]. Although these new materials showed a step forward in terms of antimicrobial effectiveness, some of them are of limited practical applications as they exist in powder form, and in some instances, fabrication procedures were cumbersome involving many steps . Hence, the need for fabrication of highly effective antimicrobial composites suitable for many practical applications is still a challenge. Both the ionic and metallic forms of silver are believed to have antimicrobial potency, though potency of metallic particles is considered superior. Antimicrobial activity of composites’ silver particles has a close relationship with the size and degree of dispersion of the particles. Generally, bigger silver particles are less effective compared to smaller particles, and aggregation of silver particles causes deterioration of antimicrobial activity in composite materials [5, 6]. High surface area-to-volume ratio of antimicrobial composites is also beneficial to the efficiency of incorporated antimicrobial agents and improves the overall antimicrobial activity of the composites . In this research, we used a simple electrospinning technique to prepare a highly potent silver-organoalkoxysilane antimicrobial fiber mat from AgNO3-polyvinylpyrrolidone (PVP)/3-aminopropyltrimethoxysilane (APTMS)/tetraethoxysilane (TEOS) solution. The technique allows fine-tuning and fabrication of fibrous composite from a viscous solution. Organoalkoxysilanes (APTMS and TEOS) were chosen because they are both liquids and easy to use in electrospinning. With electrospinning and organoalkoxysilanes, we were able to condition the fibrous composite with high surface area-to-volume ratio and monodispersed, small-sized silver particles. Moreover, in addition to silver particles, amino groups of APTMS also act as antimicrobial agent. Majority of reports on antimicrobial silver-nanofiber composites were conducted on two common bacterial strains: Escherichia coli and Staphylococcus aureus, and highly pathogenic bacteria like anthrax and brucella, and other microbial groups such as fungi and viruses are often avoided. We tend to have a comprehensive antimicrobial evaluation of the composite in this report. Hence, in addition to the common bacteria, pathogenic species (anthrax and brucella), a fungus (Aspergillus niger), and a virus (Newcastle disease virus) were also included as test organisms in this work.
PVP (K1300) was obtained from Aldrich (St. Louis, MO, USA), APTMS (97%) from Alfa Aesar (Ward Hill, MA, USA), and TEOS (98%) from J&K Chemica (Beijing, China). Ethanol (99.7%) and silver nitrate were available from Beijing Chemical Works (Beijing, China). Microbial culture media were purchased from Becton Dickenson (Franklin Lakes, NJ, USA). All reagents were used as received. E. coli JM109 was obtained from our laboratory, and S. aureus ATCC6358P and the fungus A. niger ATCC10864 were kind donations from Professors Zhang Peng and Zhang Shurong of the College of Life Science and Technology, Beijing University of Chemical Technology. Brucella suis strain 2 CVCC70-502 (China Veterinary Culture Collection 502), Bacillus anthracis (CVCC40-221), and Newcastle disease virus LaSota strain were obtained from China Institute of Veterinary Drug Control.
A 5 wt.% (relative to the weight of PVP) AgNO3 was dissolved in 11.3 g of ethanol followed by addition and dissolution of 2 g of PVP so that its concentration is kept at 15 wt.%. Electrospinning of the feed solution was made by adding in the following sequence AgNO3-PVP solution/APTMS/TEOS (v/v) 3:2:1 and was kept stirring for 30 min at room temperature. The feed solution was loaded into a plastic syringe equipped with a flat-tip stainless steel needle connected to a positive electrode with high voltage supply capable of generating up to 40 kV. The counter electrode was a flat aluminum foil placed 10 cm away from the needle’s tip. With a working voltage of 13 kV, jets of nanofibers were deposited on the foil, forming a white, shiny porous membrane. The as-spun fibers were left in air overnight for further hydrolysis of alkoxysilanes. Subsequently, the composite was aged by heating at 60°C and 90°C for 5 h each and at 120°C for 2 h. Positive experimental controls were fabricated from PVP/APTMS/TEOS (v/v) 3:2:1 without silver content and AgNO3-PVP/TEOS (v/v) 3:2 (with 5 wt.% AgNO3 relative to PVP) as described above.
Scanning electron microscopy (SEM) images of the fiber mat were recorded with Hitachi S-4700 (Chiyoda-ku, Japan). SEM acceleration voltage was 20 kV. The size and morphology of the products were studied by transmission electron microscopy (TEM; H-800) and high-resolution transmission electron microscopy (HR-TEM). Acceleration voltage for TEM was 200 kV. Fiber samples for TEM were made into powder and dispersed in acetone by ultrasonication, loaded on a carbon-coated copper grid, and then allowed to dry at room temperature before recording the micrographs. HR-TEM images were taken with JEOL JEM 2100 (Akishima-shi, Japan). Chemical identity of silver species in the composite was analyzed by X-ray photoelectron spectroscopy (XPS; Escalab 250, Thermo Fisher, Waltham, MA, USA). The X-ray excitation energy was 1,486 eV (Al Kα), and the spectra were recorded with a pass energy of 30 eV. The presence of organoalkoxysilanes was confirmed by nuclear magnetic resonance (NMR; Bruker TOPSPIN2.1, Madison, WI, USA). Density of the composite’s surface amino groups was obtained with a UV–vis spectrophotometer (UV-2450, Shimadzu, Kyoto, Japan), and silver ion release pattern was analyzed by inductively coupled plasma atomic emission spectroscopy (ICP/AES) with a sequential plasma spectrometer (ICPS-7500, Shimadzu).
Determination of surface amino group density
The total amount of accessible primary amino groups of the AgNO3-PVP/APTMS/TEOS composite was determined with a modified surface imine formation procedure of Zhao et al. . Pieces of the composite mat were carefully vacuum-dried at 343 K, sealed, and subjected to argon atmosphere. Then 30 mL of anhydrous ethanol containing 4-nitrobenzaldehyde (1 mg/mL) and catalytic amounts of acetic acid (0.75 μL) was added. The reaction was performed at 50°C for 3 h. The fibers were then washed with ethanol and sonicated in ethanol for 1 min before being vacuum-dried. Subsequently, the new imine-functionalized material was hydrolyzed in water (10 mL) containing acetic acid (0.25 μL) at 30°C for 1 h, and the regenerated imine concentration was determined by spectrophotometry at λ = 268.5 nm.
Silver ion release rate
The concentration of silver ions released in phosphate-buffered saline (PBS; 5.4 g of sodium dihydrogen phosphate monohydrate and 8.66 g of anhydrous disodium hydrogen phosphate in 1 L of distilled water, pH 7.0) from AgNO3-PVP/APTMS/TEOS fibers was measured by ICP/AES . One gram of composite sample was incubated in 100 mL of PBS at room temperature, and 5-mL solutions recovered at various times up to 80 h were analyzed by ICP/AES. A commercial ICP standard solution containing 50 ± 0.1 ppm of Ag+ was used for calibration.
All the organisms but brucella were cultivated in sterilized Luria Bertani (LB) broths (1% tryptone, 0.5% yeast extract, and 1% NaCl) on a 200-rpm shaking incubator at 37°C. Plating was done on LB 1% agar plates. Brucella strain was cultivated under the conditions mentioned above in tryptic soy broth (peptone from casein 17.0 g/L, peptone from soymeal 3.0 g/L, d-(+)-glucose 2.5 g/L, sodium chloride 5.0 g/L, and dipotassium hydrogen phosphate 2.5 g/L), and plating was done on tryptic soy agar (peptone from casein 15.0 g/L, peptone from soymeal 5.0 g/L, sodium chloride 5.0 g/L, and agar-agar 15.0 g/L). Plates are poured and allowed to cool for 24 h to ensure that they are completely dry before use. A. niger was cultured at 30°C.
Evaluation of antimicrobial activity
Prior to the experiment, all materials were accordingly sterilized by autoclaving, UV irradiation, or filtration. Antimicrobial activity of the AgNO3-PVP/APTMS/TEOS mat was evaluated on gram-negative bacteria (B. anthracis and E. coli), gram-positive bacteria (S. aureus and B. suis), and a fungus (A. niger) by qualitative and quantitative methods.
Qualitative evaluation was performed with a modified Kirby-Bauer assay . A 6-mm-diameter rounded piece of the mat was placed on a LB agar growth plate seeded with 100 to 200 μL (approximate concentration of 5 × 107 cfu/mL) overnight cultures of microorganisms then incubated for 12 h. Antibacterial activity was identified and estimated by a clear zone of inhibition in the indicator lawn around the fiber samples. PVP/APTMS/TEOS and AgNO3-PVP/TEOS served as positive controls and a clean filter paper as negative control. Sizes of inhibition zones were measured and digital images of the plates captured.
For minimum inhibition concentration (MIC) test, the inoculum was prepared by growing each microorganism in a liquid medium until a level of approximately 5 × 107 cfu/mL was reached. Eight sterilized culture tubes were prepared, each containing 10 mL of fresh LB medium and 10 μL of microbial culture, and then 0, 0.3, 0.6, 0.9, 1.5, 3, and 6 mg of fiber mat pieces were, respectively, added into the tubes. The tubes were incubated for 24 h on a shaker, and then survival of bacteria was noted by visual inspection. To confirm whether the effect of the membrane was bacteriostatic or bacteriocidal, 100 μL was drawn from cultures that appeared to have little or no cell growth and then plated and incubated for 12 to 48 h for colony-forming unit (cfu) count. The composite MIC was calculated as the lowest concentration at which bacterial growth was inhibited. Quantity of active silver utilized by the MIC composite was analyzed by ICP/AES. All assays were carried out in triplicate.
Antimicrobial efficiency (kinetics) of AgNO3-PVP/APTMS/TEOS fibers was evaluated on E. coli by viable cell count method. Positive (PVP/APTMS/TEOS and AgNO3-PVP/TEOS) and negative (fiber-free E. coli suspension) controls were set up in this test. Composite pieces were incubated in a test tube containing 3 mL of 5 × 107 cfu/mL E. coli suspension with continuous shaking. A 50-μL solution was removed from the tube as a function of contact time (min) and plated on LB agar plates to determine the number of surviving colonies. The plates were cultivated for 24 h, and numbers of viable colonies were counted to establish a function of percentage reduction versus contact time in minutes. By comparing with counts obtained from the negative control, the difference in the number of colonies before and after addition of the antimicrobial mat was calculated .
AgNO3-PVP/APTMS/TEOS mat was soaked in water for 3 h, and then 10−6 Newcastle disease virus (LaSota strain) was incubated with the composite fibers for another 1 h. A set of five chicken embryos (11 days old) were prepared, and each was inoculated with 0.2 mL of the composite-incubated viral suspension, then placed at 37°C for 120 h. Similar experiments were set up with a suspension of pure Newcastle disease virus as the negative control.
Permanence of antimicrobial activity was investigated on the AgNO3-PVP/APTMS/TEOS fiber mat by using some pieces to repeatedly kill E. coli in 3-mL LB of 5 × 107 cfu/mL. After each bacterial killing, the LB is carefully decanted and a fresh E. coli suspension added to the fiber samples. Aliquots from these cultures were plated on LB agar for cfu count to determine the number of surviving cells.
Results and discussion
The density of the composite’s surface amino groups as estimated by surface imine formation procedure  was 0.18 molecules/nm2. About 0.00079% of the total amino groups added to the feed solution are available as surface amino groups while 99.99921% is locked up within the composite’s body. The locked up amino groups become gradually exposed for antimicrobial action as the composite dissolves and worn out in the course of application. These results along with the observations made from NMR analyses confirm that amino groups are an integral part of the fibers. The pattern of silver ion release  from AgNO3-PVP/APTMS/TEOS fibers is illustrated in Figure 2d. The rapid buildup of high initial concentration of silver ions in the first 24 h followed by a steady and slow increase in concentration confers the fiber mat with quick and long-lasting antimicrobial activity.
In the MIC test, the nanofiber mat sample weighing 0.3 mg provides the MIC for all the microorganisms under test. This MIC value is lower than those reported on other highly effective antimicrobial composite materials, such as the multiaction fibrous membrane containing apatite/Ag/AgBr/TiO2 and the dual-action AgBr/polymer composite  which achieved MIC at relatively high nanofiber concentrations of 0.6 mg and above. Not only our composite has a lower MIC value, but it is also silver efficient as the 0.3-mg fiber sample releases only 0.22 μg/mL of active silver to totally inhibit the microorganisms. This MIC silver concentration is much lower than the 37.65, 40, and 50 μg/mL [1, 4, 6] documented by other researchers. Attainment of this enhanced antimicrobial effectiveness with such small amount of nanofibers and active silver highlights the benefits of organoalkoxysilane functionalization and the advantages AgNO3-PVP/APTMS/TEOS has over previously reported antimicrobial composites. It is also important to note that both the qualitative and MIC test results attested to the composite’s broad-spectrum antimicrobial property on various groups of organisms.
From the results of kinetic studies presented on Figure 3f, AgNO3-PVP/APTMS/TEOS fibers show the fastest killing rate compared to positive controls. No bacterial growth was detected after 30 min of contact with AgNO3-PVP/APTMS/TEOS which means that the incubated cells have been inhibited and completely killed by the antimicrobial effect of the fibers. AgNO3-PVP/TEOS takes about 100 min to eradicate 99.67% of the incubated bacteria, while PVP/APTMS/TEOS reduces bacteria to 95.30%. As with the disc assay, results of kinetic tests also highlighted that all the composites are antimicrobials and AgNO3-PVP/APTMS/TEOS has stronger antimicrobial property than either of the two positive controls, further stressing the notion that synergy between silver and organoalkoxysilanes produces a composite with superior antimicrobial property. Moreover, in comparison to the previously reported composite materials which required 40 min, 50 min, and 24 h [1, 12, 17] to completely inhibit microorganisms, it is clear that AgNO3-PVP/APTMS/TEOS has better antimicrobial efficiency.
According to the results of antiviral analyses, only two out of the five fetuses inoculated with AgNO3-PVP/APTMS/TEOS-incubated viral suspension were infected, suggesting that the composite reduces viral infection capability by 60%. All the fetuses in the negative control were infected.
In repeated applications against E. coli, AgNO3-PVP/APTMS/TEOS shows cfu reductions of 98.0%, 99.6%, 99.0%, 99.0%, 99.3%, and 99.6% during the first, second, third, fourth, fifth, and sixth rounds of applications, respectively. The results suggest that the fiber mat has inherent antimicrobial property. Despite the repeated applications, the fibers’ ability to kill bacteria remains almost unchanged.
Functionalization with organoalkoxysilanes improves the antimicrobial effectiveness of AgNO3-PVP/APTMS/TEOS in a number of ways. First, organoalkoxysilanes aided in the synthesis of the very small-sized and highly dispersed silver nanoparticles in the mat; the two conditions are believed to enhance antimicrobial potency of composite silver particles [1, 6]. Silver ions kill bacteria by creating holes and leakage in the cell , by deactivation of cellular proteins, and by causing shrinkage of cytoplasmic membrane and cellular response that permanently condenses DNA . Second, APTMS equips the composite with surface amino groups to make the fibers adhesive and biocidal to microbial cells. Amino groups kill bacteria by capturing them and disrupting cellular functions  and by displacement of cations responsible for cell surface stability and integrity . Furthermore, the synergistic antibacterial effect between the fibers' embedded silver and the surface amino groups and the surface amino groups greatly benefits the composite’s biocidal efficiency. By capturing bacteria, the surface amino groups could effectively decrease the distance between silver species and bacteria and facilitates the release of active silver into bacteria. Also, adhesiveness of amino groups may suppress bacteria by restricting their freedom of movement and confining them to one place. Third, the increased surface area formed by the membranous structure and porosity of the composite is also a critical factor for the high antimicrobial action of AgNO3-PVP/APTMS/TEOS. Availability of antimicrobial silver is not limited to the silver species in solution, but also those silver on fiber mat surfaces. The increased surface area therefore offers advantage of improving antimicrobial potency of active silver species over the conventional use of powder/aqueous silver ions. Both the porous structures and PVP content of fibers aid in water movement and leaching of silver from the composite mat. Moreover, the inherent ability of PVP to absorb and retain water makes the composite suitable for potential application in wound dressing where wound hydration and absorption of exudates are needed.
The robustness of the electrospinning technique allows us to functionalize a silver-based composite with organoalkoxysilanes and fine tune the overall physical and chemical properties of the composite for improved antimicrobial potency and efficiency. Incorporation of organoalkoxysilanes improves the composite’s antimicrobial property as (1) hydrolytic polycondensation reaction of APTMS and TEOS creates silicon linkages to stabilize fibers and form a membranous mat of high porosity and surface area, (2) the silanes prevent aggregation of the synthesized silver particles, thereby facilitating the fabrication of very small-sized and highly dispersed silver metal particles in the composite, and in addition, (3) APTMS armed the composite fibers with amino groups to capture and kill microorganisms. Compared to other reported antimicrobial fibers, our composite shows superior antimicrobial performances. Test results also support the idea of dual-action mechanism of the fiber’s antimicrobial activity. The composite containing both silver and organoalkoxysilanes shows superior antimicrobial activity than those containing only silver or organoalkoxysilanes, thanks to the synergistic effect between various components of the composite. Further investigations showed that the fibers have inherent antimicrobial property and can be used repeatedly. The porous mat is biocidal to bacteria, fungus, and virus and may find applications in air filters, fabric linen for clothing, wound dressing, coatings, bioadhesives, and biofilms.
SU is a Ph.D. student at Beijing University of Chemical Technology, Beijing, China. YL is Master’s degree student at Beijing University of Chemical Technology, Beijing, China. YW is a Ph.D. student at Tsinghua University, Beijing, China. GL is a professor at Tsinghua University, Beijing, China. JD is a researcher at China Institute of Veterinary Drug Control, Beijing, China. RX is a Ph.D. student at Beijing University of Chemical Technology, Beijing China. JC is a professor at Beijing University of Chemical Technology, Beijing, China.
We acknowledge the support of Professors Yang Xiaoping, Zhang Liqun, and Liu Li of the School of Material Sciences, Professors Zhang Peng and Zhang Shurong of the School of Life Sciences, all from Beijing University of Chemical Technology, and Professor Jiang Taozhen from China Institute of Veterinary Drug Control, Department of Virology.
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