Bioresource Technology 169 (2014) 277–283

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Bioresource Technology

journal homepage: www.elsevier .com/locate /bior tech

Exploring redox-mediating characteristics of textile dye-bearingmicrobial fuel cells: thionin and malachite green

http://dx.doi.org/10.1016/j.biortech.2014.06.0840960-8524/� 2014 Elsevier Ltd. All rights reserved.

⇑ Corresponding author. Tel.: +886 3 9317497; fax: +886 3 9357025.E-mail addresses: boryannchen@yahoo.com.tw, bychen@niu.edu.tw (B.-Y. Chen).

Bor-Yann Chen a,⇑, Bin Xu b, Lian-Jie Qin b, John Chi-Wei Lan c, Chung-Chuan Hsueh a

a Department of Chemical and Materials Engineering, National I-Lan University, I-Lan 26047, Taiwanb School of Environmental and Materials Engineering, Yan-Tai University, 264005, Chinac Biorefinery and Bioprocess Engineering Laboratory, Department of Chemical Engineering and Materials Science, Yuan Ze University, Taoyuan, Taiwan

h i g h l i g h t s

� Disclose textile dyes as mediators to dye removal and bioelectricity generation.� Unveil mediating characteristics of thionin and malachite green to MFCs.� Suggest stimulating strategy for MFCs-based wastewater decolorization.

a r t i c l e i n f o

Article history:Received 8 May 2014Received in revised form 21 June 2014Accepted 24 June 2014Available online 1 July 2014

Keywords:Redox mediatorsTextile dye decolorizationBioelectricity generationMicrobial fuel cells

a b s t r a c t

Prior studies indicated that biodecolorized intermediates of azo dyes could act as electron shuttles tostimulate wastewater decolorization and bioelectricity generation (WD&BG) in microbial fuel cells(MFCs). This study tended to explore whether non-azo textile dyes (i.e., thionin and malachite green)could also own such redox-mediating capabilities for WD&BG. Prior findings mentioned that AOH and/or ANH2 substitute-containing auxochrome compounds (e.g., 2-aminophenol and 1,2-dihydroxyben-zene) could effectively mediate electron transport in MFCs for simultaneous WD&BG. This work clearlysuggested that the presence of electron-mediating textile dyes (e.g., thionin and malachite green (MG))in MFCs is promising to stimulate color removal and bioelectricity generation. That is, using MFCs asoperation strategy for wastewater biodecolorization is economically promising in industrial applicationsdue to autocatalytic acceleration of electron-flux for WD&BG in MFCs.

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction

As one of biomass-based renewable energy, microbial fuel cells(MFCs) could simultaneously expedite wastewater bioremediation(e.g., reductive decolorization) and bioelectricity generation (Karraet al., 2013; Zhuang et al., 2012). Although dye biodecolorizationand bioelectricity generation are competitive to each other, colorremoval efficiency still significantly enhanced via exogenous regu-lation of electron flux in MFCs. As a matter of fact, considering elec-tron-transfer phenomena in MFCs, electrochemical characteristicsof microorganisms (Logan and Regan, 2006) inevitably influencedthe performance of bioelectricity production through at least threemechanisms: electron shuttling cell-secreting mediators (e.g.,phenazine, quinones), membrane-bound redox proteins (e.g., cyto-chromes as mobile electron carriers), and conductive pili (or nano-wires) (e.g., wired communities of Geobacter sulfurreducens,

Shewanella oneidensis) (Logan, 2008). However, in this work onlystimulation of electron-shuttling mediators could be manipulatedexogenously from the engineering perspectives. If such mediatorswere originated from the pollutant species as shown herein, thisstimulating approach would be much promising for practicalapplication.

Although most of textile dyes used in industry are azo dyes(>60% of world total), non azo dyes are still present in diverse tex-tile dye-bearing wastewater. Apparently, simultaneous degrada-tion of multiple species of textile dyes via simple and ecofriendlymethods is inevitably required for industrial applications. In fact,for sustainable dye bioremediation, reductive decolorization cou-pled with MFCs to enhance electron-transporting capabilities wasmentioned to be technically promising (Du et al., 2007; Solankiet al., 2013). Chen et al. (2010b, 2012) also revealed that electricityproduction could be improved with facilitation of decolorizedintermediates of azo dyes (e.g., phenyl methadiamine, 2-amino-phenol) as electron shuttles to augment electron flux for wastewa-ter decolorization and bioelectricity generation (WD&BG) in MFCs.

278 B.-Y. Chen et al. / Bioresource Technology 169 (2014) 277–283

Watanabe et al. (2009) also suggested anthraquinone, phenazine,viologen, naphthoquinone and cobalamin as basic skeletons ofelectron shuttles; however, these compounds were evidentlychemical structure-complicated and diverse, unfortunately notstructure-associated to each other (Sun et al., 2013). Moreover,Rau et al. (2002) disclosed the effect of different quinoid electronshuttles (i.e., AOH substitute containing compounds) on anaerobicdye reduction. Prior studies (e.g., Chen et al., 2013a) also revealedthat such decolorized intermediates (i.e., aromatic amines- amino-group(s) containing aromatics) were also electrochemically activeredox mediators for dye decolorization. In fact, proposed mecha-nisms also explained why AOH and/or ANH2 substitute(s) couldown electron-mediating capabilities for reversible electron trans-port. For instance, disubstituted auxochromes containing hydroxyland/or amino group(s) (e.g., 1,2-diaminobenzene, catechol) (Chenet al., 2013b) were found to be redox mediators for WD&BG withperspectives of chemical structure.

This first-attempt study extended to explore whether non-azotextile dyes or derived intermediates can also act as redox media-tors in MFCs. For example, thionin is a strongly staining metachro-matic dye widely used for biological staining (Gong et al., 2008)and is well-known electron mediator for bioelectricity generation(Rahimnejad et al., 2012; Ho et al., 2011). Cyclic voltametric dataconfirmed that thionin improved redox potential in acclimatizedbiofilm as compared to mediator-absent cells. These indicated thatthionin has significant capability to enhance bioelectricity produc-tion from electrochemically active biofilm in MFCs (Lin et al.,2014). With thionin as a model mediator for comparison, this workchose a cationic triphenylmethane dye- malachite green (MG)which is popularly widely used in aquaculture industry to preventinfection. Biodecolorization of MG by various microorganisms (e.g.,bacterium – Kurthia sp.; Kocuria rosa, Sphingomonas sp.; Pseudomo-nas pseudomallei, Citrobacter sp.; yeast – Saccharomyces cerevisiae;fungus – Ischnoderma resinosum, Penicillium pinophilum) were men-tioned (Chen et al., 2009; Jasinska et al., 2012; Kalyani et al., 2009).In addition, some enzymes (e.g., laccase, MG reductase, NADH-DCPI reductase) from myriads of microbes have been extensivelyexplored in terms of MG-decolorizing capabilities (Jadhav et al.,2007). Chen et al. (2010c) also disclosed biodegradation mecha-nisms of MG and methyl violet B. Moreover, color removal and bio-electricity generation could both be associated with electrontransport. This study revealed that MG could play as an electron-mediating shuttle to facilitate electron-transfer capabilities, sug-gesting that the existence of MG could accelerate rates of powergeneration as well as dye decolorization. Stimulating effects ofdye-mediator (e.g., MG and thionin) would be automatically trig-gered, suggesting that using MFC as remediation strategy couldbe more technically appropriate for wastewater decolorization.However, due to non-quasi reversibility of MG such mediatingcapabilities would be gradually attenuated during batch-modewastewater decolorization in MFCs.

2. Experimental section

2.1. MFC construction

Membrane-free air cathode single-chamber MFCs using seedingstrains Proteus hauseri ZMd44, Klebsiella pneumoniae ZMd31 andAeromonas hydrophila NIU01 were constructed in cylindrical tubesmade by polymethyl methacrylate (PMMA) (cell sizingID = 54 mm, L = 95 mm) with the operating volume of ca. 220 mL.Porous carbon cloth (CeTech™) (without waterproofing or catalyst)with a projected area of ca. 22.9 cm2 (i.e., p � 2.72) on one sidewere used as anode electrodes. The air cathode sized almost iden-

tical to the anode consisted of a polytetrafluorethylene (PTFE) dif-fusion layer (CeTech™) on the air-facing side.

2.2. Cyclic voltammetric determination

Cyclic voltammetry of candidate mediators (e.g., thionin, mala-chite green) was performed using an electrochemical workstation(Jiehan 5600, Taiwan) at 10 mV s�1 scan rate. The working, coun-ter, and reference electrodes were a glassy carbon electrode(0.07 cm2), platinum electrode (6.08 cm2), and a Hg/Hg2Cl2 elec-trode filled with saturated KCl(aq), respectively. The glassy carbonelectrode (GCE, ID = 3 mm; model CHI104, CH Instruments Inc.,USA) was successively polished with 0.05 lm alumina polish andthen rinsed with 0.5 M H2SO4 and deionized water before use.The experiments were performed in phosphate buffer solutions(PBS; pH = 7.0) at 0.1 M and the solutions were purged with nitro-gen for 15 min prior to analysis. The scanning rate was 10 mV s�1

over the range from 0.4 to �0.6 V. The redox potentials recordedas Hg/Hg2Cl2 reference electrode were corrected by 0.241 V (i.e.,E0 of Hg/Hg2Cl2) to the standard hydrogen electrode (SHE).

2.3. Electrochemical measurements

(a) Electrochemical impedance spectroscopy (EIS) (HIOKI 3522-50, Japan) measurement was conducted on steady-state open cir-cuit potential distributed with an amplitude of 10 mV at the fre-quency range of 104–5 � 10�3 Hz. Collected data were analyzedusing the software for Nyquist plot (Zview 2.6b, Jiehan Tech.). (b)Regarding power generation measurement, cell voltage was auto-matically measured (set at one data point per minute) using a dataacquisition system (DAS 5020; Jiehan Technology Corporation)through external resistance Rout = 1 KX for comparison with priorresults (Chen et al., 2010a). The power densities (P) and currentdensities (I) of MFCs were determined using linear sweep voltam-metry (LSV) measurement and the corresponding voltages wererecorded using a multimeter. Note that all MFCs were operatedin the mode of membrane-less single chamber at 25 �C.

2.4. Bioelectro-kinetics analysis – Tafel plot

Tafel plot was employed to obtain kinetic parameters for MFC

model (Raman and Lan, 2012) via Tafel equation ln ii0

� �¼ ðbÞ Fg

RT,

where i0 is exchange current density, i is the electrode current den-sity (mA m�2), b is the electron transfer coefficient or oxidativeTafel slope, R is the ideal gas constant (8.31 J mol�1 K�1), F is theFaraday constant (96,456 C mol�1 e�), T is the absolute tempera-ture (K) and finally g is the activation over potential. The Tafelequation provides a relationship between the current and the overpotential during the oxidation or reduction reaction of an elec-trode, where anode was kept as the working electrode, Ag/AgClas the reference electrode, and the cathode as the counter elec-trode (Mohan et al., 2012). The ZMd44-seeded MFC supplementedwith fresh MG (40 mg L�1) and diazo dye RBu160 (200 mg L�1)were tested by scan range from �0.65 V to 0.05 V which are opencircuit voltage (OCV)-dependent.

3. Results and discussion

3.1. Cyclic voltammetric evaluation

To determine whether non-azo dyes- thionin and MG owncapability to enhance bioelectricity generation in MFCs, cyclic vol-tammograms (CVs) of both compounds were conducted for feasi-bility study (Figs. 1A and 1B). As shown in Fig. 1A, cyclicvoltammetric profiles indicated that thionin and fresh MG could

E/V (vs. Hg/Hg2Cl2)

-.8 -.6 -.4 -.2 0.0 .2 .4 .6

I/µ A

-6

-4

-2

0

2

4

0.1 mM MG

0.1M PBS(Blank)

0.1 mM Thionin

Fig. 1A. Cyclic voltammograms for the redox processes of thionin, malachite green(MG) in 0.1 M phosphate-buffered solution (PBS) at pH 7.0 (scan rate = 10 mV s�1).

E/V (vs.Hg2Cl2)

-.8 -.6 -.4 -.2 0.0 .2 .4 .6

I/µA

-6

-4

-2

0

2

1st cycle 5th cycle 20th cycle 50th cycle 100th cycle

Fig. 1B. Cyclic voltammograms for the redox processes of malachite green (MG) in0.1 M phosphate-buffered solution (PBS) at pH 7.0 (scan rate = 10 mV s�1), wheredifferent CV profiles indicated 1st, 5th, 20th, 50th and 100th cycle-scan results.

B.-Y. Chen et al. / Bioresource Technology 169 (2014) 277–283 279

possibly perform such redox-mediating characteristics as electronshuttles. As known, electron shuttles (ESs) can mediate electrontransfer in quasi-reversibility for augmentation of electron flux infuel cells. In addition, the current is controlled by both the chargetransfer and mass transport (Watanabe et al., 2009; Kazuya et al.,2009; Van der Zee and Cervantes, 2009). Regarding capabilities ofelectron-shuttling, the appearance of the voltammogram of candi-date mediator(s) strongly depends upon the location of standardpotentials, E0

1 andE02Þ, and the difference between them

ðDE0 ¼ E02 � E0

1Þ (Bard and Faulkner, 2009). In fact, with identicalscan conditions, the difference of redox potential of MG was appar-ently larger than that of thionin, suggesting that intact MG shouldbe more electrochemically active electron shuttle for bioelectricitygeneration. However, as time went by after some scan cycles, suchcapabilities of redox mediators for MG gradually attenuated (i.e.,decreases in DE0 after different cycles of scan tests, as shown inFig. 1B), suggesting that non-quasi reversible conversion of MGto less electrochemically active chemicals(s) may be taking place(e.g., leuco form of MG or derived intermediates) (Chen et al.,2010c). This finding also suggested that if MG is present in indus-

trial wastewater bearing with myriads of textile dyes, bacterialdecolorization rate could be enhanced due to automatic stimula-tion of MG triggered as a redox mediator for color removal.

Regarding minor redox peaks shown in Figs. 1A and 1B (Bardand Faulkner, 2009), even identical material was used for CV scan,slightly different shapes of CV cumes (e.g., some minor redoxpeaks) might still appear. In fact, such minor peaks were depen-dent upon modes of scan tests. However, major redox peaks asshown herein were still remained identical. That is, scan ratewould not change the characteristics of redox mediator(s) to betested; therefore, minor peaks shown in CV profiles may be consid-ered as ‘‘noises’’ and attenuation of major redox peaks was inevita-bly due to non-quasi reversibility of shuttled MG.

3.2. Power generation analysis

To reveal whether the compound thionin and MG could act asexogenous electron-shuttling mediators, comparative analysisupon power density-curves based on polarization data of MFCssupplemented with thionin and MG was also conducted (Table 1).As a matter of fact, when 40 mg L�1 thionin was supplemented toK. pneumoniae ZMd31-seeded MFC, the power-generating effi-ciency increased from 29.63 ± 1.28 to 45.97 ± 2.12 mW m�2 (ca.155% increase). For 40 mg L�1 fresh MG supplemented to ZMd31-seeded MFC, the power-generating efficiency increased from29.63 ± 1.28 to 67.38 ± 1.87 mW m�2 (ca. 227% increase). Regard-ing P. hauseri ZMd44-seeded MFC, the power-generating efficiencyincreased from 21.82 ± 1.41 to 38.84 ± 1.85 mW m�2 (ca. 178%increase) when 40 mg L�1 thionin was supplemented. Moreover,for 40 mg L�1 fresh MG supplemented, the power-generating effi-ciency increased from 21.82 ± 1.41 to 50.04 ± 2.28 mW m�2 (ca.229% increase). In addition, for A. hydrophila NIU01-seeded MFC,the power-generating efficiency increased from 28.28 ± 0.93 to40.87 ± 1.53 mW m�2 (ca. 144% increase) when 40 mg L�1 thioninwas supplemented. Moreover, for 40 mg L�1 fresh MG supple-mented, the power-generating efficiency increased from28.28 ± 0.93 to 58.86 ± 1.88 mW m�2 (208% increase; Fig. 2A).Moreover, experiments at least in duplicate (e.g., replicate (I) and(II) in Fig. 2A) were implemented to confirm such stimulating char-acteristics of thionin and MG. These all clearly pointed out thatredox mediator-thionin and intact MG could effectively stimulateelectrochemically functioning anodic biofilm in MFC to have excel-lent efficiencies of electricity generation. Apparently, compared tothionin, intact MG seemed to be more promising to be an electron-shuttling mediator to enhance power generation as disclosed in CVprofiles (Fig. 1A). However, as CV profiles (Fig. 1B) indicated, onceelectron transfer is triggered to be taken place for decolorization,MG irreversibly converted to less electrochemically active inter-mediates. This led to gradual decreases in stimulation of power-generating capabilities (i.e., different times after supplementation;Fig. 2B). Of course, when batch mode of MFC operation is selectedfor treatment of MG and textile dyes-bearing wastewater,enhancement upon color removal due to MG stimulation wouldbe progressively declined. That is, continuous mode of operationwould be more promising as fresh MG would be continuouslyfed into the system to have maximal stimulation of MG as a redoxmediator to color removal.

3.3. Electrochemical impedance evaluation

To disclose how thionin and MG could play as electron-shut-tling mediators in MFCs, electrochemical impedance spectroscopy(EIS) measurements were also carried out to compare the resis-tance characteristics before and after supplementation of thioninand MG to MFCs (Fig. 3). According to Katz and Willner (2003),Nyquist plots were implemented for (A) ZMd31-seeded, (B)

Table 1List of data of power generation for three MFCs (unit: mW m�2).

MFC condition Blank Thionin (40 mg L�1) MG (40 mg L�1)

I II Avg I II Avg I II Avg

ZMd31 28.34 30.91 29.63 ± 1.28 43.85 48.09 45.97 ± 2.12 65.50 69.25 67.38 ± 1.87ZMd44 20.41 23.23 21.82 ± 1.41 36.99 40.69 38.84 ± 1.85 47.76 52.62 50.04 ± 2.28NIU01 27.35 29.21 28.28 ± 0.93 39.34 42.40 40.87 ± 1.53 56.98 60.74 58.86 ± 1.88

I, II and Avg denoted minimal, maximal and average values of tests in replicate.

Fig. 2A. Power density and polarization curves of ZMd31-seeded, ZMd44-seededand NIU01-seeded MFC bearing 40 mg L�1 supplemented thionin and malachitegreen (MG) (Blank is MFC without mediator supplementation) (I, II denotedreplicate 1 and 2, respectively).

Fig. 2B. Gradually attenuated profiles of power density and polarization curves of(A) ZMd31-seeded, (B) ZMd44-seeded and (C) NIU01-seeded MFC supplement with40 mg L�1 fresh malachite green (MG) for t = 0, 0.5, 1 h after supplementation (I, IIdenoted replicate 1 and 2, respectively; arrows indicated time increases after MGsupplementation).

280 B.-Y. Chen et al. / Bioresource Technology 169 (2014) 277–283

ZMd44-seeded, (C) NIU01-seeded MFCs with supplementation ofthionin and fresh MG at 40 mg L�1. Apparently, total internal resis-tance Rin (i.e., R = Relec + Rkin + Rdiff) and Rkin + Rdiff (i.e., kinetic anddiffusion resistance) (Sharma and Li, 2010) gradually decreased

Fig. 3. Nyquist plots of electrochemical impedance spectra by (A) ZMd31-seeded,(B) ZMd44-seeded, (C) NIU01-seeded MFCs bearing supplemented concentration atzero (Blank), thionin (40 mg L�1) and malachite green (MG) (40 mg L�1) (I:electrolyte resistance; II: kinetic and diffusion resistance).

Table 2List of critical parameters of EIS for three MFCs.

MFC condition Relec (Ohm) Rkin + Rdiff (Ohm) Total Rin (Ohm)

ZMd31 12.59 450.53 463.12ZMd31 & Thionin 14.55 389.29 403.84ZMd31 & MG 14.73 310.75 325.48

ZMd44 54.59 329.69 384.25ZMd44 & Thionin 38.34 251.28 289.62ZMd44 & MG 42.38 211.86 254.24

NIU01 16.36 421.77 435.13NIU01 & Thionin 15.91 303.65 319.56NIU01 & MG 13.46 242.61 256.07

Relec: electrolyte resistance (Ohm).Rkin + Rdiff: kinetic and diffusion resistance (Ohm) (II).Rin: internal resistance (Ohm).

Potential / V

-.7 -.6 -.5 -.4 -.3 -.2 -.1 0.0 .1

ln(I

/A m

A m

-2)

-10

-8

-6

-4

-2

0

2

Blankt=0 mint=30 mint=60 min

Fig. 4A. Tafel plot for ZMd44-seeded MFC with supplementation of malachite green(MG, 40 mg L�1) and RBu160 (200 mg L�1). The scan range is from ca. �0.65 V to0.05 V and Blank is MFC without mediator supplementation, t = 0, 30 and 60 minrepresent 0, 30 and 60 min after MG supplementation, respectively.

Overpotential / V

.1 .2 .3 .4 .5 .6 .7 .8

ln(I

/A m

A m

-2)

-10

-8

-6

-4

-2

0

2

Blank

t=0 min t=30 min

t=60 min

Fig. 4B. Anodic Tafel plot transformed from data shown in Fig. 4A.

B.-Y. Chen et al. / Bioresource Technology 169 (2014) 277–283 281

with appropriate supplementation of thionin and MG (Table 2).Moreover, this higher electron transfer efficiency was likelyresulted from the increased flux of electron transfer mediated bythionin and MG from microbes to electrode and proteomicallyexpressed microbes in biofilms on the anode (Fig. 3 and Table 2).These all pointed out that both thionin and MG could play a crucialrole to be electron shuttles to skyrocket efficiencies of bioelectric-ity-generation in MFC as anticipated (Zhang et al., 2010; Chenet al., 2012).

3.4. Bioelectro-kinetics analysis – Tafel plot

As the candidate mediators MG and thionin are both textiledyes, to conduct dye-decolorizing experiments inevitably encoun-ter interferences of second dye during data measurement. To

Table 3Summary table for kinetic analysis via Tafel plot.

Operation condition Tafel-slope polarization range (V) Linear regression Slope b r2

Blank 0.244–0.314 y = 11.03x � 4.196 11.03 0.2758 0.9947t = 0 0.326–0.386 y = 12.45x � 6.683 12.45 0.3113 0.9953t = 30 min 0.298–0.358 y = 11.32x � 5.496 11.32 0.2830 0.9973t = 60 min 0.288–0.348 y = 11.09x � 5.126 11.09 0.2773 0.9969

282 B.-Y. Chen et al. / Bioresource Technology 169 (2014) 277–283

resolve such problems for testing whether textile dyes couldenhance reductive decolorization, Tafel plot analysis suggestedby Mohan et al. (2012, 2013) was adopted to reveal dye-decoloriz-ing capabilities of candidate bacteria. Tafel-plot analyses were car-ried out to determine the exchange current density (i0) value,electron-transfer coefficient (b) and activation over potential (g).The values obtained from these analyses (Figs. 4A and 4B) are sum-marized in Table 3. As indicated in the Table 3, the value of b sig-nificantly increased after the supplementation of MG, revealingthat electron transfer significantly accelerated. However, valuesof b decreased with time after supplementation due to irreversibleattenuation of the electron-shuttling capability of MG as discussedin Figs. 1A and 2B. Approx. 60 min after MG addition, the electron-mediating characteristics appreciably reduced to be nearly identi-cal (i.e., bt = 60 min = 0.2773 and bBlank = 0.2758). Note that higheroxidation slope (i.e., larger b) indicated the requirement of higheractivation energy that makes oxidation less favorable, suggestinghigher electron-transfer capability (Mohan et al., 2013). This find-ing implied that stimulating effects of dye-mediator (e.g., MG andthionin) could be automatically triggered in textile dye-bearingwastewater treatment. That is to say, using MFC as remediationstrategy could be more technically appropriate for wastewaterdecolorization.

4. Conclusion

This study revealed that some biodecolorized intermediates(e.g., thionin and MG) could act as electron-shuttling mediator(s)to enhance capabilities of reductive decolorization and bioelectric-ity generation. Although fresh MG could perform excellent elec-tron-mediating characteristics than thionin, the gradually-attenuated shuttling capability of MG still limited its feasibilityfor practical uses. That is, continuous operation of dye-treatingMFCs for redox mediation is the most promising for wastewaterbiodecolorization.

Acknowledgements

The authors sincerely appreciate financial support (NSC 102-2221-E-197-016-MY3) from Taiwan’s National Science Councilfor the project of Microbial Fuel Cell (MFC)sdg conducted in Bio-chemical Engineering Lab, NIU. This study was completed as partof cooperative achievements for Academic Exchange Programbetween Yan-Tai University (China) and National I-Lan University(Taiwan) in 2013–2014.

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