Plasma-Synthesized Silver Nanoparticles on Electrospun Chitosan

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Plasma-Synthesized Silver Nanoparticles on Electrospun Chitosan Nanofiber Surfaces for Antibacterial Applications Dhyah Annur, Zhi-Kai Wang, Jiunn-Der Liao, and Changshu Kuo*

Downloaded by UNIV LAVAL on September 15, 2015 | http://pubs.acs.org Publication Date (Web): September 14, 2015 | doi: 10.1021/acs.biomac.5b00920

Department of Materials Science and Engineering, National Cheng Kung University, Tainan, 701-01, Taiwan ABSTRACT: Chitosan nanofibers have been electrospun with poly(ethylene oxide) and silver nitrate, as a coelectrospinning polymer and silver nanoparticle precursor, respectively. The average diameter of the as-spun chitosan nanofibers with up to 2 wt % silver nitrate loading was approximately 130 nm, and there was no evidence of bead formation or polymer agglomeration. Argon plasma was then applied for surface etching and synthesis of silver nanoparticles via precursor decomposition. Plasma surface bombardment induced nanoparticle formation primarily on the chitosan nanofiber surfaces, and the moderate surface plasma etching further encouraged maximum exposure of silver nanoparticles. UV−vis spectra showed the surface plasmon resonance signature of silver nanoparticles. The surface-immobilized nanoparticles were visualized by TEM and were found to have average particle diameters as small as 1.5 nm. Surface analysis by infrared spectroscopy and X-ray photoelectron spectroscopy confirmed the interactions between the silver nanoparticles and chitosan molecules, as well as the effect of plasma treatment on the nanofiber surfaces. Finally, a bacteria inhibition study revealed that the antibacterial activity of the electrospun chitosan nanofibers correspondingly increased with the plasma-synthesized silver nanoparticles.

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bead-free nanofiber formation with fiber diameters as small as hundreds of nanometers.16,17 New formulations of chitosan electrospinning solutions with additional ingredients allow secondary material modifications with certain functionalities. Alternatively, post treatments can also be used to achieve the desired surface modifications of the as-spun chitosan nanofibers.18 For example, the antibacterial activity of chitosan nanofibers can further be improved by the quaternization reaction of glucosamine units with alkyl halides, which generates the quaternary ammonium salt.19 Additionally, solution-based processes have been used to immobilize enzymes,11 dyes,20 and nanoparticles21,22 on the surfaces of chitosan nanofibers. Vapor-based surface cross-linking has also been demonstrated by the chemical vapor deposition of glutaraldehyde onto the electrospun chitosan fiber mats.23 The incorporation of silver nanoparticles in electrospun chitosan nanofibers has been shown to improve their antibacterial performance. This modification has been achieved by loading prefabricated silver nanoparticles into the electrospinning chitosan solution or by adding a silver precursor to the formulation and then performing the thermally induced synthesis of silver nanoparticles.24−26 However, the antibacterial performance of these silver nanoparticles is often restricted because they are uniformly distributed and mostly embedded below the nanofiber surface.27 To ensure the maximum exposure of silver nanoparticles, the reduction reaction of the precursor should be directed or confined to the nanofiber

INTRODUCTION Sustainable natural polysaccharides such as cellulose, chitin, chitosan, alginate, and starch are of interest for a number of biomedical and industrial applications.1 Inspired by nature, many of these biopolymers were constructed with lowdimensional morphologies of layers, fibers, or porous substances. Consequently, the large surface area of these lowdimensional materials fully exposes specific functionalities, while the structured-materials maintain robust geometries with desired mechanical strength. In recent years, a cost-effective and versatile technology known as polymer electrospinning has emerged for the fabrication of polymer-based nanofibers.2 Ambient and solution-based electrospinning processes are particularly applicable to biopolymers, which are generally vulnerable to high-temperature processes.3 Among the natural polysaccharides, chitosan, a deacetylated derivative of chitin, has attracted significant attention for electrospinning fabrication because of its abundant natural supply, biodegradability, biocompatibility, and low toxicity. Electrospun chitosan nanofibers have been developed for specific uses, such as metal chelating agents, 4,5 wound healing,6 tissue engineering scaffolds,7,8 antibacterial materials,8,9 and others.10−13 However, the fabrication of electrospun chitosan nanofibers has remained challenging due to hydrogen bonding interactions between polysaccharide chains, which lead to high crystallinity and poor solubility in common solvents.14 A high concentration of an acid, such as acetic acid, is typically formulated in the electrospinning solution to suppress chain-to-chain interactions and molecular agglomeration.15 Meanwhile, a coelectrospinning polymer, such as the water-soluble poly(ethylene oxide) or poly(vinyl alcohol), is added to further ensure uniform and © XXXX American Chemical Society

Received: July 10, 2015 Revised: August 24, 2015

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DOI: 10.1021/acs.biomac.5b00920 Biomacromolecules XXXX, XXX, XXX−XXX

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Biomacromolecules

water rinses were then performed to remove the extra TPP crosslinking agent and residual silver nitrate. Nanofiber morphologies were determined by scanning electron microscopy (SEM, JSM-7000, JEOL). Average fiber diameters and diameter distributions were analyzed by 120 diameter counts obtained from three individual SEM images for each sample. Silver nanoparticles within chitosan nanofibers were examined by transmission electron microscopy (TEM, JEM-2100, JEOL). The reflectance UV− vis spectra were recorded by a UV−vis spectrometer (S-3150, Scinco) equipped with an integrating sphere. Infrared spectra were acquired using a Jasco 460 Fourier transform infrared spectrometer. XPS spectra were measured with a Physical Electronics PHI 1600 spectrometer (MgKα X-ray source operating at 400 W and 15 kV27 mA). The antibacterial activity of the chitosan nanofibers was evaluated by measuring the inhibition zone against Escherichia coli (E. coli).30 In this disk diffusion method, the bacteria were grown on sterilized agar medium containing nutrient broth (Merck). Chitosan nanofibers on square plastic grids were placed on the solidified agar medium and incubated at 37 °C for 24 h. The inhibition zones were recorded in all four directions for each chitosan sample.

surfaces. A solution-based reduction enables the surface functionalization of silver nanoparticles,28 but the leftover reactant residue presents a potential problem for subsequent bioapplications. In this work, an argon-plasma synthesis of silver nanoparticles was successfully demonstrated for the surface immobilization of silver nanoparticles without the use of additional chemical reagents. Argon plasma etching and nanofiber thinning also promoted the further accumulation and exposure of silver nanoparticles on the nanofiber surfaces. Fourier-transform infrared spectroscopy (FT-IR) and X-ray photoelectron spectroscopy (XPS) were used to characterize the surfaces of the electrospun chitosan nanofibers before and after the plasma treatment, and an association between the silver nanoparticles and the amino functional groups on chitosan was identified. Transmission electron microscopy (TEM) images confirmed that most of the silver nanoparticles were immobilized on the chitosan nanofiber surfaces. Antibacterial experiments also revealed that the bacteriainhibited zone proportionally increased with the argon plasma dosage and produced more silver nanoparticles on the nanofiber surfaces. These results demonstrated the surface immobilization of plasma-synthesized silver nanoparticles on electrospun chitosan nanofibers and the promising performance of these materials in antibacterial applications.

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RESULTS AND DISCUSSION To enable the consistent and bead-free production of fibers, the electrospinning of chitosan nanofibers was carefully optimized with respect to the acetic acid concentration and the electrospinning ejection rate, while the other electrospinning parameters were kept constant. The presence of acetic acid at a high concentration stabilized the chitosan molecules in the aqueous electrospinning solution by preventing chain-to-chain interactions. Electrospinning formulations with 0.6 wt % PEO coelectrospinning polymer, equivalent to 5 wt % PEO in the solidified polymer nanofibers, ensured a homogeneous nanofiber formation with no molecular agglomeration. Further electrospinning optimization relied on the manipulation of the solution charge density in the splitting polymer jets (i.e., the balance between the evenly distributed electrostatic charges and the solution surface tension), which was regulated via the ejection flow rate as controlled by the syringe pump. At a constant applied voltage of 18 kV, a reduction in the ejection flow rate led to increased electrostatic charges that overwhelmed the solution surface tension and prevented bead formation in the electrospun nanofibers. As shown in the nine SEM images of Figure 1, nanofibers were successfully electrospun from the C0 chitosan/PEO solutions and were optimized with a high acetic acid concentration (70 wt %) and an ejection flow rate as low as 18 μL/min. The SEM image of this optimum formulation (Figure 1g) reveals a uniform fiber average diameter of 136 nm with no trace of beads. In contrast, lower acetic acid concentrations and higher flow rates caused the formation of beads or polymer agglomeration. The addition of silver nitrate precursor at a relatively low concentration had a negligible effect on the electrospinning product. Figure 2 summarizes the SEM morphologies of the asspun chitosan/PEO nanofibers with and without AgNO3, using the same electrospinning conditions as the sample shown in Figure 1g. All four samples (C0, C05Ag, C10Ag, and C20Ag) had similar fiber diameters that ranged from 115 to 140 nm and comparable diameter distributions, with diameter standard deviations between 23 and 30 nm (details are listed in Table 1). Randomly deposited chitosan nanofibers had a typical opaque and white appearance (see the image of the as-spun C10Ag in Figure 3). Therefore, an integrating sphere was utilized to record the reflectance UV−vis spectra of these samples to avoid light scattering effects.29 As shown in Figure

EXPERIMENTAL SECTION

All reagents and solvents in this work were of analytical reagent grade and were used as received without further purification. Low molecular weight chitosan (Mv: 50 000−190 000, with 75−85% deacetylation) and poly(ethylene oxide) (PEO, Mv: 600 000) were obtained from Sigma-Aldrich. Acetic acid solvent and tripolyphosphate (TPP) crosslinking agent were also purchased from Sigma-Aldrich. Silver nitrate (AgNO3, 99.5%), which served as the silver nanoparticle precursor was purchased from Mallinckrodt. The electrospinning formulations and nanofiber diameters are summarized in Table 1.

Table 1. Electrospinning Formulations and Average Diameters of the Electrospun Fibers electrospinning formulations in 70% acetic acid aqueous solution sample number

chitosan (wt %)

PEO (wt %)

C0 C05Ag C10Ag C20Ag

5.4 5.4 5.4 5.4

0.6 0.6 0.6 0.6

electrospinning parameters

AgNO3 (wt %)

average diameter (asspun) (nm)

STD of diameter (asspun) (nm)

0 0.5 1.0 2.0

136.4 125.0 140.6 115.6

26.3 30.1 23.5 28.0

The electrospinning of chitosan/PEO nanofibers was performed using a previously reported apparatus and procedures.29 Briefly, a syringe pump was used to control the steady electrospinning flow rates. A high voltage source of 18 kV was attached to the ejection needle. As-spun chitosan/PEO nanofibers, with or without the silver nitrate, were deposited on a plastic grid that was positioned in front of a grounded electrode. The chitosan nanofiber samples collected on plastic grids were cut to a size of 2 cm × 2 cm and stored in a desiccator for future use. Plasma treatment was carried out on a PJ plasma reactor (ASTP Products, Inc.) using a RF power of 200 W, a chamber pressure of 200 mTorr, and an argon flow of 32 sccm. The water resistance of the plasma-treated chitosan nanofibers was further improved by dipping the samples into an aqueous TPP solution (4 wt %) for 1 h. This process generates the ionic cross-linking between phosphate groups of TPP and amino groups of chitosan.15 Several B


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Figure 1. SEM morphologies of as-spun chitosan nanofibers from the C0 formulation produced by electrospinning at varying ejection flow rates and acetic acid concentrations. (Scale bar: 1 μm).

Figure 2. SEM morphologies of electrospun chitosan nanofibers preloaded with varying amounts of silver nitrate. The insets show the nanofiber diameter distributions. (Scale bar: 1 μm).

3a,b, both as-spun C0 and C10Ag samples did not absorb in the visible wavelength range. After the argon plasma treatment, the light yellow appearance of the C10Ag sample indicated the presence of silver nanoparticles (see the other images of C10Ag samples in Figure 3). The reflectance UV−vis spectra of C10Ag samples with different argon plasma dosages (from 0 to 2 min) were also recorded and are shown in Figure 3a,b. The

absorption bands centered at approximately 410 nm (λmax) were attributed to the surface plasmon resonance (SPR) of the silver nanoparticles. Continuous argon plasma bombardment intensified the SPR signals and also caused the SPR to shift to approximately 422 nm. The intensified SPR signals (profile b′ in Figure 3) suggested an increase in the number of silver nanoparticles, while the SPR red-shift indicated nanoparticle C


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Figure 3. Insets (a) and (b) illustrate the reflectance UV−vis spectra of C0 and C10Ag chitosan nanofibers, respectively. C10Ag samples exhibited SPR intensity increase and SPR wavelength red shift with increasing plasma dosages, as well as the color change shown in the five inset images.

Figure 4. SEM morphologies of C10Ag samples versus the plasma dosages (0, 0.5, 1, 1.5, and 2 min) (Scale bar: 500 nm). Image f illustrates the diameter reductions of the C10Ag and C0 samples upon the plasma etching.

enlargement during the plasma treatment.31 Profile a′ in Figure 3 shows the characterization for the C0 chitosan nanofibers without the addition of silver nitrate. In the absence of the silver nitrate precursor, argon plasma induced only surface etching of the chitosan/PEO nanofibers. In the absence of oxygen gas, the argon plasma process degraded the molecular bonding, and the formation of carbonized species contributed toward the low wavelength absorption in the UV−vis spectra in Figure 3a. The SEM images in Figure 4 show the fiber morphologies of the C10Ag samples after argon plasma treatment. High argon plasma dosages (up to 2 min) caused notable diameter reduction, but no evidence of nanofiber melting or deformation was observed. The lack of evidence of electrospun chitosan nanofiber overheating indicated moderate and controllable temperatures within the plasma reactor. With a 1.5 min plasma dosage, the average diameter of the chitosan nanofibers was

etched to 90 nm, which was an approximately 30% reduction compared with the diameter of the as-spun C10Ag nanofibers. The average plasma etching rate in these cases was approximately 12 nm/min. Further plasma bombardment of C10Ag samples for a total of 2 min resulted in etched chitosan nanofibers as thin as 80 ± 25 nm in diameter along with some broken fibers, as shown in the SEM image. Because thin fiber fragments were found to have fiber diameters near 65 nm (see Figure 4f), the broken fibers were presumably caused by the weak mechanical strength of the ultrathin chitosan nanofibers with etched fiber diameters less than 60 nm. In the absence of the silver nitrate precursor, the C0 sample revealed a similar fiber etching profile. Broken chitosan nanofibers were observed after 1.5 min of plasma treatment, where the diameters of these broken fibers were below 70 nm. Infrared spectroscopy and XPS analysis were employed for the surface characterization of the plasma-treated chitosan D


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Figure 5. FT-IR analysis of the (a) C0, (b) C0_2_min, (c) C10Ag, (d) C10Ag_1_min, and (e) C10Ag_2_min samples. The insets show zoomed-in and detailed spectra in three wavenumber regions.

Figure 6. C 1s (i), O 1s (ii), N 1s (iii), and Ag 3d (iv) XPS spectra from (a) C0, (b) C0_2_min, (c) C10Ag, (d) C10Ag_1_min, and (e) C10Ag_2_min samples.

cm−1. More characteristic bands indicative of chitosan were assigned to the amide I band at 1654 cm−1 (CO stretching in amide I band), the N−H bending centered at 1558 cm−1, the symmetric deformation of −CH3 at 1375 cm−1, the −CH2−

nanofibers. As shown in Figure 5, the as-spun chitosan/PEO nanofibers (sample C0, spectrum a) presented a broad band (3600−3000 cm−1) encompassing the stretching mode of OH and NH2 groups, followed by C−H stretching centered at 2900 E


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Figure 7. TEM images of (a) as-spun C10Ag, (a′) zoom-in of as-spun C10Ag, (b) C10Ag_1_min, (c) C10Ag_2_min, and (d) C10Ag_2_min samples at high magnification. (e) Diameter distribution of silver nanoparticles in C10Ag_2_min samples.

wagging vibration in primary alcohols at 1341 cm−1, the amide III vibration due to the combination of NH deformation and C−N stretching at 1259 cm−1, the C−O stretching centered 1048 cm−1, and the out-of plane bendings of O−H and N−H groups at 720 cm−1.32,33 After argon plasma treatment, the FTIR spectrum (spectrum b) of the C0_2_min sample revealed no discernible differences compared with the as-spun sample (spectrum a). However, a detailed comparison between spectra a and b revealed a significant decrease in the −CH2− band at 1341 cm−1, while the −CH3 absorption band at 1375 cm−1 remained unchanged (see the inset III). This observation indicated that the primary alcohol groups (−CH2−OH) in the chitosan and chitin repeat units were more vulnerable to the argon plasma compared with the amide groups in the chitin units. Such plasma degradation of the primary alcohols also resulted in a slight absorption decrease for the C−H stretching at 2875 cm−1, as outlined in the inset I. Similar etching preferences for the primary alcohol group were also identified in the infrared spectra of chitosan samples containing the silver nitrate precursor. In addition, plasma-synthesized silver nanoparticles in the chitosan/PEO nanofibers were apparent in the infrared spectra. The as-spun C10Ag nanofibers had moderate N−H bending absorption at approximately 1558 cm−1 (see the inset II, spectrum c). In the presence of silver nanoparticles, this band noticeably evolved (spectra d and e), indicating an association between the N−H groups and the silver nanoparticles.34,35 The surface characteristics and interactions between the chitosan and silver nanoparticles were further investigated by XPS. As illustrated in Figure 6i, the C 1s spectrum of the chitosan/PEO nanofiber sample (sample C0) was fitted with three binding energies. Peak 1 at 287.4 eV was attributed to the amide (N−CO) and the acetal (O−C−O), and peak 3 at 284.3 eV was attributed to the CH3 of the acetyl group. Peak 2, centered at 285.9 eV, was assigned to other C−O groups from the polymers, including the primary alcohol group (−CH2− OH). After the argon plasma surface bombardment, both C0 and C10Ag samples showed a decline in peak 2, suggesting a loss of primary alcohol groups (−CH2−OH). This XPS result echoes the previous discussion of the −CH2− band decrease at

1341 cm−1 in the infrared spectrum analysis (the inset III of Figure 5). The O 1s spectra illustrated a predominant binding energy at 532.2 eV for all samples (Figure 6ii), while the broadening full width at half-maximum (fwhm) from 1.7 to 2.5 eV suggested the presence of divided oxygen species after the argon plasma bombardment. The N 1s binding energy for sample C0 (spectrum a in Figure 6iii) resolved two peaks at 398.7 and 400 eV, corresponding to amine and acetamide groups, respectively.36 Sample C10Ag (with silver nitrate) had identical N 1s characteristics as the C0 sample (spectra a and c in Figure 6iii) due to the relatively low concentration of the silver precursor and negligible interactions between the silver nitrate and chitosan.28 Plasma-treated samples with or without silver precursors (C0 and C10Ag) had an upper shift in the N 1s binding energy to 399.3 eV, indicating the presence of more electronegative substituents on the nitrogen atoms, including nitrogen to oxygen associations (N···O) and nitrogen associations with the silver nanoparticles (N···Ag). This observation was also suggested by the infrared spectra of the samples (inset II of Figure 5). The upper shift of the N 1s binding energy due to the presence of silver nanoparticles also agreed with the corresponding down shift in the Ag 3d binding energies to 367.1 and 373.1 eV (spectrum e in Figure 6iv) from the original values of 367.3 and 373.3 eV, respectively, in the asspun C10Ag nanofibers. The intensities of these two binding energies showed remarkable increases after 1 and 2 min argon plasma treatments. The silver/carbon atomic ratios estimated by the XPS analysis were both initially 0.024 but dramatically increased to approximately 0.047 and 0.115 for the C10Ag_1_min and C10Ag_2_min samples. Because the XPS penetration depth is limited to only tens of angstroms, the intensified Ag 3d peak suggested that the silver nanoparticles propagated and accumulated near the nanofiber surfaces upon the argon plasma bombardment. The distribution of surface-immobilized silver nanoparticles in the chitosan nanofibers was visualized by TEM. Prior to the plasma treatment, the as-spun C10Ag sample showed no trace of metallic nanoparticles (Figure 7a,a′). With the 1 min argon plasma dosage, immobilized silver nanoparticles were exclusively observed near the fiber surfaces in the C10Ag_1_min F


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Figure 8. Antibacterial inhibition zone measurements for C0, C10Ag, and C20Ag samples versus the argon plasma dosages. The inset shows an example of the inhibited-growth zones surrounding the nanofiber sample.

exposure time, both samples demonstrated increased inhibition zone sizes to 0.36 and 0.48 mm, respectively. When treated with 1.5 min of argon plasma, the C10Ag and C20 Ag samples had the maximum antibacterial activity and inhibited bacterial growth up to a distance of 0.78 mm. Further argon plasma treatment up to 2 min resulted in a slight decline in the inhibition zone to approximately 0.65 mm on average, presumably due to the overetching and breaking of the chitosan nanofibers, as shown in the previous morphology analysis. The remarkable improvement in antibacterial inhibition indicated that plasma-synthesized silver nanoparticles with maximum exposure on the surfaces of electrospun chitosan nanofibers can be adopted as candidates for water filtration and antibacterial applications.

sample (Figure 7b). These nanoparticles underwent further diameter growth upon another 1 min dose of plasma (Figure 7c). The average diameter of the silver nanoparticles in the C10Ag_2_min sample was found to be approximately 1.5 nm (Figure 7d,e). It was estimated that the complete reduction of all silver nitrate in the electrospun chitosan nanofibers formed surface-immobilized 1.5 nm silver nanoparticles with an average particle spacing as small as 0.5 nm, which obviously disagreed with the TEM image. Nevertheless, a similar estimation of the silver nitrate precursors in the plasma-etched outer layer, i.e., the 20 nm thick sheath, gave an average silver nanoparticle spacing to approximately 1.6 nm, which matched the TEM observation shown in Figure 7d. These results indicate that the synthesis of the surface-immobilized silver nanoparticles was primarily dependent on the decomposition of the silver nitrate located in the plasma-etched outer layer. During the short plasma exposure time, any outward migration of the precursor from the core to the nanofiber surface was negligible. The antibacterial performances of chitosan nanofibers with and without surface-immobilized silver nanoparticles were investigated by the disk diffusion method using E. coli as the model bacteria. All nanofibers were collected on plastic grids and cut to a size of 2 cm × 2 cm for the antibacterial experiments. The sizes of the inhibited-growth zones surrounding the nanofiber samples were measured in all four directions (see the example shown in Figure 8). These results for the C0, C10Ag, and C20Ag samples are summarized in Figure 8 as a function of the plasma dosage. In the absence of silver ions and silver nanoparticles, all C0 chitosan nanofibers before and after the argon plasma treatments had inadequate antibacterial activity, with nearly no zone of inhibition. With the addition of the silver precursor, the as-spun C10Ag and C20Ag nanofibers displayed inhibited-growth zones of 0.25 and 0.37 mm lengths on average, indicating moderate antibacterial activity from the Ag+ ion itself. In a separate experiment, the asspun C10Ag nanofibers prior to the plasma treatments were rinsed with water several times to remove the silver nitrate precursor. The resulting chitosan nanofibers showed low antibacterial performance, similar to the as-spun C0 sample. Inhibition zone improvements were observed in the silver nanoparticle-immobilized C10Ag and C20Ag nanofibers after the argon plasma bombardment. For the 0.5 and 1 min plasma

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CONCLUSION

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AUTHOR INFORMATION

Chitosan nanofibers with average diameters of approximately 130 nm were successfully electrospun from chitosan/PEO acetic acid solutions. The silver nitrate that was preloaded in the chitosan nanofibers subsequently decomposed to silver nanoparticles via argon plasma treatment. This solid-state synthetic approach produced surface-immobilized silver nanoparticles in the absence of additional chemical reagents and also facilitated maximum exposure on the nanofiber surfaces. Material characterizations revealed the effect of the argon plasma bombardment and the interactions between the silver nanoparticles and the amino groups of chitosan. TEM examination confirmed that plasma-synthesized silver nanoparticles with an average diameter of 1.5 nm were mostly positioned on the nanofiber surfaces. Antibacterial performance assays based on bacterial inhibition zone measurements indicated a strong correspondence with the plasma dosages and the resulting surface-immobilized silver nanoparticles.

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest. G


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ACKNOWLEDGMENTS The authors are grateful for the financial support from the Ministry of Science and Technology of Taiwan (NSC 1022923-E-006-004-MY3 and NSC 101-2218-E-006-016-) and for the helpful discussions with Prof. Tzong-Yow Tsai at National Cheng Kung University.


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Plasma-Synthesized Silver Nanoparticles on Electrospun Chitosan

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