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Colloids and Surfaces A: Physicochem. Eng. Aspects 444 (2014) 226– 231

Contents lists available at ScienceDirect

Colloids and Surfaces A: Physicochemical andEngineering Aspects

jo ur nal ho me p ag e: www.elsev ier .com/ locate /co lsur fa

reen synthesis of silver nanoparticles using tea leaf extractnd evaluation of their stability and antibacterial activity

ian Suna, Xiang Caia,b, Jiangwei Lia, Min Zhengb, Zuliang Chenb,c, Chang-Ping Yua,∗

Key Laboratory of Urban Environment and Health, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, ChinaSchool of Chemistry and Materials Science, Fujian Normal University, Fuzhou 350007, ChinaCentre for Environmental Risk Assessment and Remediation, University of South Australia, Mawson Lakes, SA 5095, Australia

i g h l i g h t s

A simple and green way was devel-oped to synthesize AgNPs using teaextract.The synthesized AgNPs was char-acterized by TEM, XRD, FT-IR, andICP-MS.Ag+ release from the synthesizedAgNPs was lower indicating the highstability.The synthesized AgNPs showed slightantibacterial activity against E. coli.

g r a p h i c a l a b s t r a c t

r t i c l e i n f o

rticle history:eceived 24 September 2013eceived in revised form0 December 2013ccepted 24 December 2013vailable online 7 January 2014

eywords:

a b s t r a c t

A simple, environmentally friendly and cost-effective method has been developed to synthesize silvernanoparticles (AgNPs) using tea leaf extract. We have studied the effects of the tea extract dosage, reactiontime and reaction temperature on the formation of AgNPs. The AgNPs were synthesized using silvernitrate and tea extract, and the reaction was carried out for 2 h at room temperature. The synthesizedAgNPs were characterized using transmission electron microscopy (TEM), X-ray diffraction (XRD), Fouriertransform infrared spectroscopy (FT-IR), thermogravimetric analyzer, and zeta potential analyzer. Thesynthesized AgNPs were nearly spherical, with the sizes ranging from 20 to 90 nm. FT-IR spectral analysis

reen synthesisilver nanoparticlesea leaf extractilver ion releasentibacterial effect

indicated the tea extract acted as the reducing and capping agents on the surface of AgNPs. Furthermore,the study of silver ion release from the tea extract synthesized AgNPs showed a good stability in terms oftime-dependent release of silver ions. In addition, the antibacterial activity of AgNPs was determined bymonitoring the growth curve and also by the Kirby-Bauer disk diffusion method. Due to the larger sizeand less silver ion release, the AgNPs synthesized by tea extract showed low antibacterial activity against

Escherichia coli.

. Introduction

In recent years, silver nanoparticles (AgNPs) have been widelysed in many consumer goods, such as medical devices, cleaning

gents, and clothing, due to its unique antimicrobial properties.enerally, the method for the AgNP preparation involves the reduc-

ion of silver ions in the solution or in high temperature in gaseous

∗ Corresponding author. Tel.: +86 592 6190768; fax: +86 592 6190768.E-mail address: cpyu@iue.ac.cn (C.-P. Yu).

927-7757/$ – see front matter © 2014 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.colsurfa.2013.12.065

© 2014 Elsevier B.V. All rights reserved.

environments [1]. However, the reducing reagents, such as sodiumborohydride, may increase the environmental toxicity or biologicalhazards [1,2]. Moreover, the capping agents like polyvinyl alcohol(PVA) or gelatin, have to be used to protect the AgNPs from aggre-gation. On the other hand, the high temperature may also increasethe cost. Hence, the development of a green synthesis of AgNP byusing environment-friendly solvents and nontoxic reagents is of

great interest.

Huang et al. described the AgNP synthesis using a leaf extract ofCinnamomum camphora, while the reduction was considered due tothe phenolics, terpenoids, polysaccharides and flavonoids present

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n the extract [3]. Moreover, the extracts of various plants, includingucalyptus hybrid [4], Syzygium cumini [5], Sesuvium portulacastrum6], Boswellia ovalifoliolata [7], Calotropis procera [8], Musa para-isiacal [9], Acalypha indica [10] were successfully used for AgNPynthesis. In addition, tea leaf extract was used for the AgNP synthe-is. Begum et al. reported the AgNP synthesized by the ethyl acetatextract of tea leaves [11]. Nadagouda et al. showed the synthesizedgNP with the size range of 20–60 nm [12]. However, the reac-

ion conditions, including the temperature or tea extract dosage,he synthesis mechanism, the AgNP stability, and the antibacterialctivity have not been fully investigated.

Previous studies showed that AgNPs would likely release silverons after entering the aquatic environment [13,14], which wouldeduce the stability of AgNPs. In addition, silver ions exhibitedifferent physiochemical properties and biological toxicity fromgNPs [13,15,16]. Therefore, understanding of the silver ion release

rom AgNPs is necessary. Liu et al. reported more than 10% (w/w)ilver ions were released from citrate coated AgNPs (2 mg/L) in their-saturated (8.3 mg/L) water at pH 5.6 after 24 h [14]. Lee’s studyndicated that the silver ion release kinetics followed first-orderinetics [15]. In addition, the release rates of silver ions were mainlyependent on the particle sizes, the environmental factors (e.g., dis-olved oxygen, pH, temperature) [13,17], and the capping agents18]. However, quantitative data on the silver ion release from thereen synthesized AgNPs are limited.

The present study attempts to fill the knowledge gap by inves-igating the synthesis, stability, and antimicrobial ability of AgNPsynthesized by tea extract. Tea extract solution was used as a reduc-ng and capping reagent for the AgNP synthesis, and distilled watererved as the reaction medium. The reaction conditions on theynthesis of AgNPs were studied. The obtained particles were ana-yzed by transmission electron microscopy (TEM), X-ray diffractionXRD), Fourier transform infrared (FT-IR) spectroscopy, thermo-ravimetric analyzer, and zeta potential analyzer to understand theorphology and capping of AgNPs. The AgNP stability was eval-

ated via the time-dependent release of silver ions from the teaxtract synthesized AgNPs. In addition, the antibacterial activity byea extract synthesized AgNPs was also investigated.

. Materials and methods

.1. Synthesis of AgNPs by tea extract

Tea leaves extract was used as a reducing agent for the AgNP syn-hesis. 16 g of dried green tea leaves (Richun Tea Company, Fujian)as added to 100 mL ultrapure water in 250 mL Erlenmeyer flask.

he mixer was boiled (5 min), cooled, filtered, and the filtrate wastored at 4 ◦C as the stock solution and was used within 1 week. Theotal organic carbon (TOC) content of tea extract analyzed by TOCnalyzer (TOC-VCPH, Shimadzu, Japan), was approximately 20 g/L.

The stock solution of tea extract was diluted to 1%, 5%, 10%, 25%,0% and 100% (v/v) as reducing and capping solution. 750 �L silveritrate (10 mM) was injected at the rate of one drop per secondo 14.25 mL tea extract working solution with vigorously stirring.he working solution was stirred (700 rpm) for 120 min at 25, 40nd 55 ◦C, respectively. AgNPs were concentrated and purified byentrifugal ultrafiltration (Millipore, Amicon Ultra-15 3k, USA), andinsed with Milli-Q water (Millipore, 18.2 M� cm, USA).

.2. Characterization of AgNPs

The morphology of AgNPs was determined by TEM at 100 kVHitachi H-7600, Japan). Samples were prepared by placing a dropf fresh suspension on the TEM copper grids, followed by sol-ent evaporation at room temperature overnight. The configuration

hem. Eng. Aspects 444 (2014) 226– 231 227

of AgNPs was determined by XRD (PANalytical, X’ Pert Pro,Netherlands), operated at a voltage of 40 kV and a current of 30 mAwith Cu K� radiation. Thermogravimetric analysis (TGA) of the teaextract synthesized AgNPs was conducted in nitrogen atmosphereon a thermogravimetric analyzer (TG 209 F3 Tarsus, Germany Net-zsch Instruments, Inc.) in the temperature range of 40–1000 ◦C ata scanning rate of 10 ◦C/min. Sample was prepared by adding 2 mLof tea extract synthesized AgNPs into petri dish and drying for 72 hin the freeze dryer. The zeta-potential (Malvern Instruments, Zeta-PALS, UK) of AgNPs produced by tea extract was analyzed in order torecognize the surface charge of AgNPs. In addition, the hydrate par-ticle size was also determined by Zetasizer (Malvern Instruments,ZetaPALS, UK).

The quantification of AgNP stock suspensions was analyzed byinductively coupled plasma optical emission spectrometry (ICP-OES) (PerkinElmer Optima 7000 DV, USA) after nitric acid digestion.Silver concentrations in the solution were analyzed by inductivelycoupled plasma mass spectrometry (Agilent 7500cx, USA). The dis-solved silver ion was isolated by removing AgNPs using centrifugalultrafilter devices (Millipore Amicon Ultra-4 3 K, USA), subjectedto centrifugation for 30 min at 4000 rpm [14], whereas the totalsilver concentration was analyzed after nitric acid digestion. TheAgNP concentration was calculated by deducting dissolved silverion from total silver.

FT-IR spectroscopy measurements were carried out to identifythe functional groups which are bound distinctively on the AgNPsurface and involved in the synthesis of AgNPs. Samples for the FT-IR analysis were prepared by drying the tea extract taken beforeand after synthesis of AgNPs. Samples for FT-IR measurement wereprepared by mixing 1% (w/w) specimens with 100 mg of potas-sium bromide powder and pressing the mixture into a sheer slice.Hand-ground samples were measured by a FT-IR spectrometer (FT-IR Nicolet 5700, Thermo Corp. USA). The average of 9 scans wascollected for each measurement using a resolution of 2 cm−1.

2.3. Silver ion release test

The dissolution kinetics of AgNPs synthesized by the tea extractin air-saturated (8.2 mg O2/L) deionized water was investigated.PVA-coated, uncoated, and commercial AgNPs were also appliedfor comparison, for which the preparation processes are describedin supplementary information (SI). The AgNP stock suspension wasdiluted with deionized water to 1.0 mg/L. The initial pH values oftea extract AgNPs, PVA-coated AgNPs, uncoated AgNPs, and com-mercial AgNPs were 6.9, 6.8, 6.9, and 7.2, respectively. Silver ionrelease experiments were carried out in triplicate on dark shaker(120 rpm) at 28 ◦C.

2.4. Antibacterial susceptibility test

The antibacterial test was carried out via a growth inhibitionassay. Escherichia coli K12 strain MPAO1 (Coli Genetic Stock Center[CGSC; Yale University]) was grown on Luria-Bertani (LB) mediumat 37 ◦C for overnight. The cultures were diluted in fresh LB mediumto get an initial 0.05 absorbance at OD600. 150 �L of AgNPs solu-tion under target concentrations were pipetted into eight parallelwells of a 96-well microplate (8 replicates), and 150 �L of E. colicells were inoculated in each well. The final concentrations ofAgNPs were 50.0, 25.0, 12.5, 6.25, 3.12, 1.56, 0.78, 0.39, 0.195 mg/L,respectively. The absorbance was measured at OD600 through a 96-well microplate with a SpectraMax M5 Multi-detection Microplate

Reader (Molecular Devices Inc., USA) at predetermined time inter-vals.

In addition, the antimicrobial susceptibility test was also per-formed according to a modified Kirby-Bauer disk diffusion method

228 Q. Sun et al. / Colloids and Surfaces A: Physicochem. Eng. Aspects 444 (2014) 226– 231

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s described by Liu et al. [17]. Details of the experiment wereescribed in SI.

. Results and discussion

.1. Effect of the tea extract dosage

The effects of the initial concentrations of the tea extract on thegNPs productivity were studied at 25 ◦C. The stock solution of teaxtract was diluted to 1%, 5%, 10%, 25%, 50% and 100% (v/v) andas used as working solution, with the TOC of 1.0, 2.0, 5.0, 10.1,

nd 20.2 g/L, respectively. The formation of AgNPs was indicatedy the appearance of signature brown color of the solution (SI Fig.1). To understand the formation of AgNPs, the total silver con-entrations and silver ion concentrations were analyzed. As shownn Fig. 1A the production efficiencies of AgNPs were 99.1%, 99.7%,9.9%, 99.8%, 94.6%, and 95.3% (w/w) with 1%, 5%, 10%, 25%, 50%, and00% (v/v) tea extract, respectively. The production efficiencies ofgNPs were all above 94% (w/w), while the highest AgNP produc-

ion efficiency was achieved with 5% (v/v) tea extract. In addition,he zeta potential is shown in Fig. 1B. Generally, a suspension thatxhibits an absolute zeta potential less than 20 mV is considerednstable and will result in precipitation of particles from solution19], whereas the absolute zeta potential higher than 20 mV is sta-le [20]. In this study, zeta potentials of AgNPs were −20.7 and21.3 mV with 1% and 5% (v/v) tea extracts, respectively, indicat-

ng the stability of AgNP suspensions. The zeta potentials of AgNPsncreased as the tea extract concentrations increased, and reached12.0 and −11.3 mV with 50% and 100% (v/v) tea extract, indicating

he instability of AgNP suspensions at high tea extract concentra-ion. Therefore, 5% (v/v) tea extract was chosen in the followingtudy.

.2. Effect of temperature on AgNP synthesis

The effect of temperature on the AgNPs formation was investi-ated at 25, 40, and 55 ◦C with 5% (v/v) tea extract. The previoustudy of AgNP synthesis by Pulicaria glutinosa extract showed thegNP production was enhanced by increasing temperature [21].ur results showed that the increase in temperature had no sig-ificant effect on the production efficiencies of AgNPs (data nothown), and this difference may be due to the production efficiency

n the present study was already 99.7% (w/w) at 25 ◦C and had littlepace to improve. However, the average hydrate particle sizes ofgNPs were 91, 129, and 175 nm at 25, 40, and 55 ◦C, respectively

Fig. 2A). The increase of AgNP size with the increasing temperature

Tea extract dil ute rates

efficiencies (A) and zeta potential (B) (±standard error).

was in accordance with the previous study [1,21,22]. This is prob-ably due to the reaction rates of AgNP synthesis increased as thetemperature increased, consequently, the particle sizes increased[22].

3.3. Characterization of tea extract synthesized AgNPs

TEM was employed to characterize the size, shape and mor-phology of the synthesized AgNPs. The TEM images of AgNPssynthesized by 5% (v/v) diluted tea extract (1 g/L TOC) are shown inFig. 2B–D. The morphology of AgNPs is nearly spherical. AgNP sizesranged from 20 to 90 nm. The difference in the particle size by TEMand in situ dynamic light scattering techniques may be due to theaggregation during the sample preparation [14].

The XRD pattern of the dried silver nanoparticles is shown inFig. 3. The XRD peaks at 2� degree of 38.1, 44.3, 64.4 and 77.4 can beattributed to the (1 1 1), (2 0 0), (2 2 0), and (3 1 1) crystalline planesof the face centered cubic crystalline structure of metallic silver(JCPDS file No. 01-071-4613). Besides, the peak near 31.9 impliedthe possible existence of Ag2O [17,23].

FT-IR spectroscopy was used to characterize and identify thechemical composition of the AgNP surface. The FT-IR spectra ofcontrol dried tea extract (before reaction without AgNO3) and syn-thesized AgNPs (after reaction with AgNO3) are shown in Fig. 4.Both of them showed a shift in peaks: 3420–3371 (due to N–Hstretching, amides), 2931–2925 (due to C–H stretching, alkanes),1383–1371 (characteristic of hydroxyl groups, phenolic hydroxyl),1051–1044 cm−1 (due to C-stretching, ether groups). In addition,the synthesized AgNPs showed other peaks at 1695, 1452, 1241,and 926 cm−1 related to alkene groups (C C stretching), tertiaryammonium ions, poly phenols, aliphatic amines (C–N stretch-ing vibrations), and alkene groups (C–H stretching), respectively.The FT-IR analysis indicated the involvement of amides, carboxyl,amino groups and poly phenols in the synthesized AgNPs. It is wellknown that there are tea polyphenols, protein, and amino acid intea. The organic compounds in tea extract could attribute to thereduction of AgNO3 and the stabilization of AgNPs by the surfacebound by the organic compounds [24]. Similar observations werenoticed in the green synthesis of AgNPs using plant extract [25,26].The synthesis of AgNPs was demonstrated by the tea polyphenol(Baicao Co. China) of 5.0 mg/L (TEM image is shown in SI Fig. S2),which supported AgNPs could be synthesized by the reduction of

silver ion via tea polyphenols.

The capping organic groups on the surface of tea extract synthe-sized AgNPs was further confirmed by TGA. Fig. 5 shows the TGAcurve with three weight losses. The first weight loss was observed at

Q. Sun et al. / Colloids and Surfaces A: Physicochem. Eng. Aspects 444 (2014) 226– 231 229

and T

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Fig. 2. The average hydrate particle sizes (±standard error) (A),

round 100 ◦C due to the loss of adsorbed water. The second weightoss, which accounted for 19% of the total AgNPs weight, appearedt 180–380 ◦C. The degradation of organic compounds, includingerulic acid, ascorbic acid, and quercetins, might cause the weightoss [27]. The combustion of carbohydrates and the less condensedtructures of the lignin molecules would also cause the weight loss

28]. In addition, the degradation or glycosylation of the catechins

ight contribute to the weight loss [29]. There is a steady weightoss appeared at 380–1000 ◦C, which accounted for 19% of the total

eight loss. This was probably due to the thermal degradation of

ig. 3. XRD pattern of 5% (v/v) tea extract synthesized silver nanoparticles AgNPs.

EM image of AgNPs formed at 25 ◦C (B), 40 ◦C (C), and 55 ◦C (D).

resistant aromatic structures and the decomposition of biogenicsalt, such as carbonates [28]. Data from TGA indicated the contentof tea component estimated from the weight loss was 39% of thetea extract synthesized AgNPs.

3.4. Release of silver ion

Since the silver ion release is an important behavior of AgNPs,the characterization of silver ion release is necessary to under-stand the environmental fate of synthesized AgNPs. In this study,

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230 Q. Sun et al. / Colloids and Surfaces A: Physicoc

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Fig. 5. TGA curve of tea extract synthesized AgNPs.

ime-dependent release of silver ion from the tea extract synthe-ized AgNPs was measured using centrifugal ultrafiltration andCP-MS. For comparison, the silver ion releases by AgNPs pre-ared by other processes, including PVA-coated AgNPs, uncoatedgNPs, and commercial AgNPs, were also tested. Fig. 6 shows time-esolved concentrations of silver ion released from the AgNPs.he released silver ion concentrations of tea extract synthesizedgNPs was 6.73 �g/L at 2 h, and was increased to 8.94 �g/L at4 h, while the released silver ion concentrations of commercialgNPs, PVA-coated AgNPs, and uncoated AgNPs at 24 h were 28.3,5.2, 83.2 �g/L, respectively. The lowest silver ion release rate waschieved by tea extract synthesized AgNPs. The reason for thiss because the surface of AgNPs might be sufficiently covered byhe groups from the tea extract, including the amides, carboxyl,henols, etc., as shown in Fig. 4. These functional groups might

nhibit the dissolution of AgNPs by oxygen to release silver ions30]. In addition, the released silver ions could be reduced to AgNPsue to the reducing capacity of tea extract. Furthermore, TEMnalysis showed the average sizes of the tea extract synthesized,VA-coated, uncoated, and commercial AgNPs were 45, 12, 15, and0 nm, respectively. Previous study showed the silver ion releasingate decreased with an increased particle size [14].

AgNPs could keep release silver ions in the aquatic environment.n the present study, the release rates of silver ions were 2.8%, 3.5%,

nd 8.3% (w/w) at pH around 7 in the presence of dissolved oxygenfter 24 h for commercial AgNPs, PVA-coated AgNPs, and uncoatedgNPs, respectively. In comparison, the release rate of silver ions

rom AgNPs synthesized by tea extract was less than 0.9% (w/w). The

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Fig. 6. Silver ion release kinetics by different AgNPs (±standard error).

hem. Eng. Aspects 444 (2014) 226– 231

lower ion release rate of tea extract synthesized AgNPs indicated agood stability and the probably longer preservation time. In addi-tion, AgNPs is known to show the antibacterial activity, which tosome extent is through the release of silver ions [31]. Therefore, theantimicrobial activity of tea extract synthesized AgNPs is expectedto be less than that of other AgNPs.

3.5. Antibacterial activity

The antibacterial activity of AgNPs against E. coli was investi-gated. Silver ion was found to be the most toxic species to inhibit thegrowth of E. coli. The E. coli growth was completely inhibited withthe silver ion concentration at or higher than 1.56 mg/L. The inhibi-tion concentrations were 12.5 and 25.0 mg/L for PVA-coated AgNPsand uncoated AgNPs, respectively. Whereas the tea extract synthe-sized AgNPs and commercial AgNPs did not show E. coli growthinhibition even at 50.0 mg/L.

Similar results were observed by the Kirby-Bauer disk diffu-sion method. As shown in Fig. S3, the biggest inhibition zones areobserved for silver ion (5 mm). PVA-coated and uncoated AgNPsalso showed clear antimicrobial activity with inhibition zone diam-eter of 1.2–1.5 mm. However, tea extract synthesized AgNPs alongwith commercial AgNPs showed little antibacterial activity withinhibition zone diameter of 0.5–0.8 mm.

It is not surprising for the best antimicrobial activity of sil-ver ion, since the good antibacterial activity of silver ions hasbeen reported [17,32]. Previous studies indicated the antibacterialactivity of AgNPs by attachment to the bacterial cell wall, or the for-mation of free radicals [33,34]. In addition, the silver ions releasedfrom AgNPs may play a vital role of the antibacterial activity dueto the interaction of silver ion with the thiol groups of enzymes[35]. As shown in Fig. 6, the silver ion release rate of the tea extractsynthesized AgNPs was lower due to the functional groups on thesurface of AgNPs or the reducing capacity of tea extract. This mightresult in the lower antibacterial activity of tea extract synthesizedAgNPs. On the other hand, smaller NPs were found to be moretoxic due to the easier uptake and larger surface area [36,37]. Fur-thermore, the potential for the silver ion releasing also increasedwith a decreasing AgNP size [38]. Therefore, the toxicity of AgNPswas found to be size and ion release rate dependent [37]. The lessantibacterial activity of the tea extract synthesized AgNPs might bedue to the larger size and less silver ion release.

4. Conclusions

The present study described a green and simple way to syn-thetize AgNPs by tea extract. AgNPs were characterized by TEM,XRD, TGA and FT-IR. The synthesized AgNPs was crystalline struc-ture, 20–90 nm in size, with functional groups from the tea extractcapped on the surface. The conditions such as the dosage of the teaextract and reaction temperature showed an effect on the produc-tion efficiency and formation rate of AgNPs. The silver ion releasefrom the tea extract synthesized AgNPs was lower compared tothe PVA-coated AgNPs, uncoated AgNPs, and commercial AgNPs,which highlight a good stability due to the functional groups fromthe tea extract capped on the AgNPs. However, due to the largersize and less silver ion release, the biosynthesized AgNPs showedslight antibacterial activity against E. coli.

Acknowledgements

We appreciate Dr. Sikandar I. Mulla for editing the manuscript.This work was supported by the Natural Science Foundation ofFujian Province, China (2011J05035), the National Science Founda-tion of China (41201490), Science and Technology Innovation and

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ollaboration Team Project of the Chinese Academy of Sciences,echnology Foundation for Selected Overseas Chinese Scholar ofOHRSS, China, Technology Planning Project of Xiamen, China

3502Z20120012), the Special Program for Key Basic Research ofhe Ministry of Science and Technology, China (2010CB434802),nd the CAS/SAFEA International Partnership Program for Creativeesearch Teams (KZCX2-YW-T08). The authors do not have anyonflict of interest to declare.

ppendix A. Supplementary data

Supplementary data associated with this article can beound, in the online version, at http://dx.doi.org/10.1016/j.colsurfa.013.12.065.

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