Materials Science and Engineering C 36 (2014) 146–151

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Preparation, characterization, and antibacterial activity studies of silver-loaded poly(styrene-co-acrylic acid) nanocomposites Cunfeng Song a,b, Ying Chang a, Ling Cheng a, Yiting Xu a, Xiaoling Chen c,⁎, Long Zhang a, Lina Zhong a, Lizong Dai a,⁎ a b c

Department of Materials Science and Engineering, College of Materials, Xiamen University, Xiamen 361005, China Department of Chemistry, College of Chemistry and Chemical Engineering, Xiamen University, Xiamen 361005, China Department of Endodontics, Xiamen Stomatology Hospital, Teaching Hospital of Fujian Medical University, Xiamen 361003, China

a r t i c l e

i n f o

Article history: Received 4 June 2013 Received in revised form 24 October 2013 Accepted 28 November 2013 Available online 7 December 2013 Keywords: Antibacterial agent Soap-free emulsion polymerization Silver Nanocomposites

a b s t r a c t A simple method for preparing a new type of stable antibacterial agent was presented. Monodisperse poly(styreneco-acrylic acid) (PSA) nanospheres, serving as matrices, were synthesized via soap-free emulsion polymerization. Field-emission scanning electron microscopy micrographs indicated that PSA nanospheres have interesting surface microstructures and well-controlled particle size distributions. Silver-loaded poly(styrene-co-acrylic acid) (PSA/ Ag-NPs) nanocomposites were prepared in situ through interfacial reduction of silver nitrate with sodium borohydride, and further characterized by transmission electron microscopy and X-ray diffraction. Their effects on antibacterial activity including inhibition zone, minimum inhibitory concentration (MIC), minimum bactericidal concentration (MBC), and bactericidal kinetics were evaluated. In the tests, PSA/Ag-NPs nanocomposites showed excellent antibacterial activity against both gram-positive Staphylococcus aureus and gram-negative Escherichia coli. These nanocomposites are considered to have potential application in antibacterial coatings on biomedical devices to reduce nosocomial infection rates. © 2013 Elsevier B.V. All rights reserved.

1. Introduction Uses of biomedical devices are always associated with a risk of infection. Surface bacterial infestation to biomedical devices, such as catheters, dental materials, wound and burn dressings, and implants, could be resistant to immune defense mechanisms, and then result in serious infection [1]. The presence of antibacterial agents is an effective strategy to keep biomedical devices away from the infestation of detrimental bacteria. Antibacterial agents need to combine desirable attributes, for instance, excellent antibacterial activity, environmental safety, low toxicity, and ease of fabrication [2]. German obstetrician C. S. F. Crede introduced 1% silver nitrate solution as an eye solution for the prevention of Gonococcal ophthalmia neonatorum in 1884, which is perhaps the first scientifically documented medical use of silver [3,4]. From then on, silver is well known to have strong antibacterial effects, broad-spectrum biocidal activity, and low toxicity to mammalian cell. The mechanism of silver's antibacterial property may involve free silver ions (Ag+) uptake [5–7]. Firstly, due to the high affinity with thiol groups presented in the cysteine residues, Ag+ ions can interact with respiratory enzymes. This will lead to disruption of the mitochondrial respiratory chain [8]. Furthermore, the

⁎ Corresponding authors. Tel.: +86 592 2186178; fax: +86 592 2183937. E-mail addresses: [email protected] (X. Chen), [email protected] (L. Dai). 0928-4931/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.msec.2013.11.042

mitochondrial dysfunction interrupts ATP synthesis, and induces DNA damage. Finally, apoptosis may occur and program cell death [9]. In medical applications, silver in the form of nanoparticles is a promising alternative to silver salts and bulk metal, because salts may possess quick and uncontrolled silver release while the bulk metal is a sluggish and inefficient releasing system [10]. In order to prepare highly stable silver nanoparticle dispersions for practical purposes, inorganic matrices including silica glass [11], zeolite, apatite [12–14], zirconium phosphate [15,16], etc. are usually used to overcome unwanted agglomeration of the colloids. The sol–gel derived silica glass powders containing colloidal silver were reported to be used as antibacterial agents of composite resin for dental restoration [17]. Commercial silver-zeolites could serve as antibacterial agents against oral bacteria even under anaerobic conditions [18]. Recently, many researches focused on the preparation of polymeric matrices with silver nanoparticles as well as the studies of their antibacterial activity [19–24]. Varun Sambhy et al. presented a method of fabricating dual action antibacterial composites consisted of a cationic polymer matrix and embedded silver bromide nanoparticles [2]. Colloidal silver could also be deposited onto surface-functional porous poly(ethylene glycol dimethacrylate-co-acrylonitrile) microspheres, owing to the high affinity between silver and nitrile group on the surface of the microspheres [25]. In this paper, monodisperse nanospheres were served as polymeric matrices to prepare antibacterial agents for the first time. We synthesized poly(styrene-co-acrylic acid) (PSA) nanospheres via soap-free

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Fig. 1. FE-SEM micrographs and hydrodynamic size distributions of PSA nanospheres: AA/St: (a, b) 5 wt.%; (c, d) 10 wt.%; (e, f) 15 wt.%; (g, h) 25 wt.%.

emulsion polymerization. Using silver nitrate (AgNO3) as a precursor and sodium borohydride (NaBH4) as an oxidizing agent, silver nanoparticles were deposited onto the surfaces of PSA nanospheres. The obtained polymer/silver nanocomposites (PSA/Ag-NPs) are expected to have potential applications as antibacterial agents in biomedical devices. Preparation, characterization, and antibacterial activity of PSA/Ag-NPs

nanocomposites were studied and discussed in detail. The parameters of additives (antibacterial agents, antioxidant, wetting agents, etc.), such as size and content, play important roles in the final performance of materials [26–28]. Therefore, controlling the size of antibacterial agents, just as what we have done in this paper (through the control over the size of matrix), becomes meaningful.

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Fig. 2. FITR of PSA nanospheres.

Fig. 4. XRD of PSA/Ag-NPs nanocomposites.

2. Materials and methods

2.3. Characterization of PSA nanospheres and PSA/Ag-NPs nanocomposites

2.1. Preparation of monodisperse poly(styrene-co-acrylic acid) (PSA) nanospheres

The morphologies of PSA nanospheres and PSA/Ag-NPs nanocomposites were characterized via field-emission scanning electron microscopy (FE-SEM) (LEO1530, LEO, Germany) and transmission electron microscopy (TEM) (JEM-2100, JEOL, Japan). The hydrodynamic size of PSA nanospheres were analyzed by dynamic light scattering (DLS) using a Zetasizer (Mastersizer 2000, Malvern, UK). Fourier transform infrared spectrophotometry (FTIR) (Nicolet iS10, Thermo Nicolet, USA) was used to study the surface properties of PSA nanospheres. The phase characteristics of Ag in the nanocomposites were observed by selected area electron diffraction (SAED) (JEM-2100, JEOL, Japan) and Xray diffraction (XRD) (X'pert PRO, PANalytical B.V., Netherlands) measurement.

Monodisperse PSA nanospheres were prepared by soap-free emulsion polymerization of styrene (St) and acrylic acid (AA) in water according to the method as described in the literature [29,30]. Briefly, a certain amount of AA (0.1, 0.2, 0.3, and 0.5 g) and 45 mL of H2O were initially charged into a three-necked flask. After the feeding AA being fully dissolved, 2.0 g of styrene was added. The solution was vigorously stirred for 30 min at room temperature under nitrogenous atmosphere. 0.04 g of KPS, dissolved in 5 mL of H2O, was injected into the solution under stirring. Then the emulsion was heated to 75 °C and preserved for 12 h. The products were washed with ultrapure water extensively and dispersed in water finally.

2.2. Synthesis of PSA/Ag-NPs nanocomposites The fabrication of PSA/Ag-NPs nanocomposites was described as follows: 20 mL of aqueous PSA dispersion (0.3 mg/mL) was mixed with 0.5 mL of 10 mM AgNO3 in a 50 mL one-necked flask. The mixture dispersion was stirred for 5 h with a magnetic bar at room temperature. It was followed by adding 10 mM NaBH4 into the dispersion and continuously stirring in an ice water bath for another 2 h. The attached Ag+ ions were reduced by NaBH4, which led to the deposition of Ag nuclei and nanoparticles onto PSA surfaces. The resulting PSA/Ag-NPs nanocomposites were washed with ultrapure water several times and collected for the further examination.

2.4. Antibacterial assays 2.4.1. Bacterial culture Gram-positive Staphylococcus aureus (S. aureus, CMCC 26003) and gram-negative Escherichia coli (E. coli, CMCC 44103) were cultured in LB broth at 37 °C overnight until the optical density of culture medium reached 2.0 at 600 nm, which indicated the content of bacteria approximately reached 109 CUF/mL. 2.4.2. Inhibition zone test Freshly grown bacteria were diluted by LB broth to an approximate concentration of 2 × 107 CUF/mL of S. aureus or E. coli. 100 μL of this stock solution was plated on LB agar plate. 20 μL of PSA nanospheres, PSA/Ag-NPs nanocomposites and control solutions was respectively impregnated onto paper discs (6 mm diameter). The paper discs were

Fig. 3. TEM micrographs: (a) PSA nanospheres (AA/St: 15 wt.%); (b) PSA/Ag-NPs nanocomposites; The inset is SAED of PSA/Ag-NPs nanocomposites.

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Table 2 MIC test of various concentrations of PSA/Ag-NPs nanocomposites against S. aureus and E. coil.a Concentrations of PSA/Ag-NPs (μg/mL)

S. aureus

E. coil

12.5 25 50 100 200 1000

+ − − − − −

+ + − − − −

a

Fig. 5. Inhibition zones (1. Control; 2. PSA nanoparticles (AA/St: 15 wt.%); 3. 100 μg/mL; 4. 200 μg/mL of PSA/Ag-NPs nanocomposites) in the LB agar dishes inoculated with different bacteria: (a) S. aureus; (b) E. coil.

“+” for bacteria growth, “−” for no bacteria growth.

3. Results and discussions 3.1. Characterization of PSA nanospheres and PSA/Ag-NPs nanocomposites

placed on surface of the inoculated agar plates and incubated at 37 °C for 24 h. Colonies were visualized and images of the plates were captured [31–33]. A vernier caliper with an error of 0.1 mm was used to measure the size of inhibition zone.

2.4.3. Minimum inhibitory concentration (MIC) test PSA/Ag-NPs nanocomposites, at concentrations of 12.5, 25, 50, 100, 200, 1000 μg/mL, were added to the test tubes with the bacterial suspension which contained approximately 2 × 105 CUF/mL of S. aureus or E. coli. The MIC was measured using a LB medium broth microdilution method [34,35] at the concentration of which no bacterial growth was observed in the test tube after it was incubated at 37 °C for 24 h.

2.4.4. Minimum bactericidal concentration (MBC) test MBC is defined as the minimum concentration (μg/mL) of an antibacterial agent at which 99.9% of bacteria are killed [36]. An appropriate volume of a solution containing approximately 2 × 105 CUF/mL of S. aureus or E. coli in LB broth was added to sterile glass tubes. PSA nanosphere and PSA/Ag-NPs nanocomposites were tested in triplicate respectively at final concentrations of 50, 100, 200, 1000 μg/mL. The tubes were incubated at 37 °C with shaking at 250 rpm for 24 h. 100 μL aliquots taken from the tubes were plated on LB agar plates. The plates were incubated at 37 °C for 24 h, and then bacterial colonies were counted.

2.4.5. Bactericidal kinetics test The effect of PSA/Ag-NPs nanocomposites on the bacteria-growth kinetics in liquid media was studied. 10 mL of a solution containing approximately 2 × 105 CUF/mL of S. aureus or E. coli in LB broth was added to sterile glass tubes. Then these tubes were kept in an incubated shaker at 37 °C. When LB-strains broths were added to the tubes, the initial time was set as zero. 10 μL aliquots were withdrawn from each tube at certain time intervals. The solution was diluted 10 times. After that, 100 μL of the diluted solution was plated on LB agar plates. The plates were incubated at 37 °C for 24 h, and then bacterial colonies were counted [37].

Table 1 Correlation of the size of inhibition zone with various concentrations of PSA/Ag-NPs nanocomposites.a Concentrations of PSA/Ag-NPs Inhibition zone of S. aureus Inhibition zone of E. coli (μg/mL) (mm) (mm) 100 200 a

7.6 9.1

Size of inhibition zone ≥7 mm is effective.

7.1 8.4

Monodisperse poly(styrene-co-acrylic acid) nanospheres were synthesized by soap-free emulsion polymerization. Fig. 1 showed FE-SEM micrographs and hydrodynamic size distribution of PSA nanospheres prepared with different amount of AA. These results indicated that these nanospheres have interesting surface microstructures. There were many smart bulgings, which were uniformly distributed on the surface of the nanospheres. Due to these bulgings, the increased surface area could effectively improve the absorption of Ag+. From Fig. 1, wellcontrolled particle size distributions could also been observed. The mean size of PSA (AA/St: 5, 10, 15, 25 wt.%) were ca. 424.1 ± 9.9, 315.4 ± 8.2, 289.9 ± 5.9, and 282.1 ± 5.6 nm, respectively. The particle size of PSA nanospheres was inversely proportional to the feed AA amount. To explain this phenomenon, a hypothesis was proposed that the presence of higher amount of ionic functional emulsifying monomer caused the larger number of formed primary particles, whereas the quantities of St used in all formulations were constant [38]. FTIR spectroscopy was used to study the surface properties of PSA nanospheres. Fig. 2 displayed FTIR spectra of PSA nanospheres. In the spectrum, several characteristic peaks were detected. The peaks at 1601 cm−1 arose from C_C skeletal vibration of St, and the peaks at around 1709 cm−1 corresponded to C_O stretching vibration of carboxyl groups from AA. PSA (AA/St: 15 wt.%) was chosen to prepare PSA/Ag-NPs nanocomposites. TEM micrographs of PSA nanospheres and PSA/Ag-NPs nanocomposites were shown in Fig. 3. From the micrographs, the core– shell structure of PSA nanospheres (Fig. 3a) and PSA covered with Ag nanoparticles (Fig. 3b) could be seen clearly. In the SAED, as shown in the inset, rings were indexed according to the reflections of (111), (200), (220), and (311) crystalline planes of cubic phase of Ag (JCPDS card No. 04-0783), which confirmed that Ag was successfully deposited [39]. Besides, the XRD pattern also provided evidence of the welldefined Ag crystallization. As shown in Fig. 4, sharp peaks at 2θ = 38.1° (111), 44.3° (200), 64.4° (220), and 77.3° (311) were observed. 3.2. Antibacterial studies PSA/Ag-NPs nanocomposites exhibited antibacterial activity in the test of inhibition zone. As for S. aureus and E. coli, a zone directly around PSA/Ag-NPs coated paper disc could be viewed, whereas there was no clear zone around PSA coated paper disc and the control, as presented in Fig. 5. Bare PSA nanospheres (AA/St: 15 wt.%), with the concentration up to 1000 μg/mL, had not yet shown antibacterial activity against either the bacteria. This indicated that the growth inhibition was caused by Ag nanoparticles rather than PSA nanospheres. The bactericidal action of PSA/Ag-NPs nanocomposites caused the release of Ag+ irons and its diffusion into the agar layer, which blocked the growth of bacterial colonies in the agar medium [40]. The sizes of the inhibition zones for PSA/Ag-NPs nanocomposites were measured and listed in Table 1.

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Fig. 6. MBC test of different bacteria with PSA nanoparticles (AA/St: 15 wt.%) and various concentrations of PSA/Ag-NPs nanocomposites: (a) S. aureus and (b) E. coil.

With the increasing concentration of PSA/Ag-NPs nanocomposites, the inhibition zone became wide. As shown in Table 2, the MIC value of PSA/Ag-NPs nanocomposites against E. coli was 50 μg/mL, however, that value against S. aureus was only 25 μg/mL. As is well known, a lower MIC value corresponds to a higher antibacterial effectiveness [41–43]. Hence, the bacteriostatic effect for S. aureus was more noticeable than that for E. coli. The presence of PSA/Ag-NPs nanocomposites on the LB agar plates was able to kill the both types of the bacteria (Fig. 6). However, for PSA nanospheres (AA/St: 15 wt.%), uncontrollable bacterial proliferation was shown. It is obvious that, comparing with PSA/Ag-NPs nanocomposites, PSA nanospheres (AA/St: 15 wt.%) were ineffective for both types of the bacteria, even at 1000 μg/mL. E. coli was completely killed when the LB agar plates contained 200 μg/mL PSA/Ag-NPs nanocomposites. PSA/Ag-NPs nanocomposites showed an antibacterial activity against S. aureus at a much lower MBC value (100 μg/mL). One reason might be that the anionic surface of PSA/Ag-NPs nanocomposites increased their association with the positive charged bacterial surface. This reason was consistent with another report [44], which demonstrated cationic PEI-coated Ag@MESs were more effective in slowing the growth of gram-negative E. coli. Furthermore, the kinetics of antibacterial activity of PSA/Ag-NPs nanocomposites against S. aureus and E. coli were investigated, as

shown in Fig. 7. Colony-forming of aliquot corresponded to the number of live bacteria in each suspension at the time of withdrawing aliquot. Thus, a plot of colony-forming units (CFU/mL) of strains versus time was constructed. As shown in Fig. 7, all the curves dropped steeply at the initial stage, which meant that the initial bactericidal efficiency of PSA/Ag-NPs nanocomposites was high [2]. In the case of S. aureus, when the concentration of PSA/Ag-NPs reached 100 μg/mL, all the initially inoculated bacteria were sterilized within 390 min. The concentration was increased to 200 μg/mL, the sterilizing time was shortened to 180 min. However, all the initially inoculated E. coli were killed within 390 min only if the concentration of PSA/Ag-NPs reached 200 μg/mL. PSA/Ag-NPs nanocomposites, which resulted in a remarkable decrease in the number of bacteria, performed a higher bactericidal efficiency against S. aureus than against E. coli at a lower equivalent concentration. However, increasing the concentration of PSA/Ag-NPs nanocomposites accelerated the elimination of both the two bacteria. Commercial nanocrystalline silver-coated dressings (Acticoat™) were reported to reduce infection in wound therapy [45,46]. In the above experiments, PSA/Ag-NPs nanocomposites exhibited significant antibacterial effects and broad-spectrum biocidal activity. Therefore, PSA/Ag-NPs nanocomposites are expected to develop antibacterial coatings on biomedical devices, which are broadly used in medical treating processes.

Fig. 7. Kinetics of antibacterial activity of PSA/Ag-NPs nanocomposites against different bacteria: (a) S. aureus; (b) E. coil.

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4. Conclusions Monodisperse poly(styrene-co-acrylic acid) (PSA) nanospheres, serving as matrices, were synthesized via soap-free emulsion polymerization. FE-SEM micrographs indicated that PSA nanospheres have interesting surface microstructures and well-controlled particle size distributions. Their silver nanocomposites (PSA/Ag-NPs) were prepared in situ through controlled interfacial reduction. The merits of the matrix can help us to control the size of the nanocomposites. Structural studies and XRD analysis clearly revealed the formation of Ag nanoparticles on the PSA matrices. The antibacterial activity of PSA/Ag-NPs nanocomposites against Gram-positive S. aureus and gram-negative E. coli was studied. Due to their excellent antibacterial activity, these nanocomposites are desirable to own potential application in developing antibacterial coatings on biomedical devices, such as wound and burn dressings, catheters, and temporary implants. Acknowledgments This work was financially supported by the Special Program for Key Research of Chinese National Basic Research Program (2011CB612303); the Nation Natural Science Foundation of China (51173153, U1205113) and Xiamen Science and Technology Committee (No. 3502Z20120015). Authors are also grateful to Fujian Provincial Key Laboratory of Fire Retardant Materials. References [1] V.M. Ragaseema, S. Unnikrishnan, V. Kalliyana Krishnan, L.K. Krishnan, Biomaterials 33 (2012) 3083–3092. [2] V. Sambhy, M.M. MacBride, B.R. Peterson, A. Sen, J. Am. Chem. Soc. 128 (2006) 9798–9808. [3] X. Chen, H.J. Schluesener, Toxicol. Lett. 176 (2008) 1–12. [4] S. Silver, L.T. Phung, G. Silver, J. Ind. Microbiol. Biotechnol. 33 (2006) 627–634. [5] C. Marambio-Jones, E.M.V. Hoek, J. Nanoparticle Res. 12 (2010) 1531–1551. [6] L. Bo, W. Yang, M. Chen, J. Gao, Q. Xue, Chem. Biodivers. 6 (2009) 111–116. [7] S. Bajpai, M. Bajpai, L. Sharma, Des. Monomers Polym. 14 (2011) 383–394. [8] P. AshaRani, G. Low Kah Mun, M.P. Hande, S. Valiyaveettil, ACS Nano. 3 (2008) 279–290. [9] Y.H. Hsin, C.F. Chen, S. Huang, T.S. Shih, P.S. Lai, P.J. Chueh, Toxicol. Lett. 179 (2008) 130–139. [10] G. Vertelov, Y.A. Krutyakov, O. Efremenkova, A.Y. Olenin, G. Lisichkin, Nanotechnology 19 (2008) 355707. [11] M. Kawashita, S. Tsuneyama, F. Miyaji, T. Kokubo, H. Kozuka, K. Yamamoto, Biomaterials 21 (2000) 393–398. [12] T. Syafiuddin, T. Igarashi, H. Shimomura, H. Hisamitsu, N. Goto, J. Showa Univ. Dent. Soc. 13 (1993) 443–449.

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Preparation, characterization, and antibacterial activity studies of silver-loaded poly(styrene-co-acrylic acid) nanocomposites.

A simple method for preparing a new type of stable antibacterial agent was presented. Monodisperse poly(styrene-co-acrylic acid) (PSA) nanospheres, se...
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