Accepted Manuscript

Facile synthesis of multifunctional Ag/Fe3O4-CS nanocomposites for antibacterial

and hyperthermic applications

Ngoan Thi Nguyen, Lam Dai Tran, Cuong Duc Nguyen, Loc Thai Nguyen, Cham Ba
Thi, Binh Hai Nguyen, Duong Ba Thi, Nam Hong Pham, Dzung Tuan Nguyen, Hoa
Thai Tran, Dien Gia Pham
PII: S1567-1739(15)30058-4
DOI: 10.1016/j.cap.2015.08.016
Reference: CAP 4056

To appear in: Current Applied Physics

Received Date: 25 April 2015

Revised Date: 10 August 2015
Accepted Date: 24 August 2015

Please cite this article as: N.T. Nguyen, L.D. Tran, C.D. Nguyen, L.T. Nguyen, C.B. Thi, B.H. Nguyen,
D.B. Thi, N.H. Pham, D.T. Nguyen, H.T. Tran, D.G. Pham, Facile synthesis of multifunctional Ag/Fe3O4-
CS nanocomposites for antibacterial and hyperthermic applications, Current Applied Physics (2015), doi:
10.1016/j.cap.2015.08.016.

This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to
our customers we are providing this early version of the manuscript. The manuscript will undergo
copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please
note that during the production process errors may be discovered which could affect the content, and all
legal disclaimers that apply to the journal pertain.
 ACCEPTED MANUSCRIPT
Highlighted

Facile synthesis of multifunctional Ag/Fe3O4-CS nanocomposites for

antibacterial and hyperthermic applications
Ngoan Thi Nguyen1, Lam Dai Tran2*,3, Cuong Duc Nguyen4, Loc Thai Nguyen5, Cham

Ba Thi1, Binh Hai Nguyen6, Duong Ba Thi1, Nam Hong Pham6, Dzung Tuan Nguyen7, Hoa

PT
Thai Tran4, Dien Gia Pham1**
1
Institute of Chemistry, Vietnam Academy of Science and Technology

RI
18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam
2
Graduate University of Science and Technology, Vietnam Academy of Science and Technology

SC
18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam
3
Duy Tan University, 182 Nguyen Van Linh, Da Nang, Vietnam
4

U
College of Sciences, Hue University, 77 Nguyen Hue, Hue City, Viet Nam
5
Food Engineering and Bioprocess Technology, Asian Institute of Technology, PO Box 4,
AN
KlongLuang, Pathumthani 12120, Bangkok, Thailand
6
Institute of Materials Science, Vietnam Academy of Science and Technology
M

18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam

7
Institute of Tropical Technology, Vietnam Academy of Science and Technology
D

18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam

TE

Corresponding author
*
Lam Dai Tran
Graduate University of Science and Technology, Vietnam Academy of Science and
EP

Technology
Phone: 84 4 37919090
Fax: 84 4 37919797
C

E-mail: tdlam@gust-edu.vast.vn
AC

**
Dien Gia Pham

Institute of Chemistry, Vietnam Academy of Science and Technology

Phone: 84 4 37564312
Fax: 84 4 38361283
 ACCEPTED MANUSCRIPT
Highlighted

Abstract

Nanocomposites containing two or more functional constituents are attractive candidates for

advanced nanomaterials. In this study, multifunctional Ag/Fe3O4-CS nanocomposites were

PT
successfully prepared, using chitosan as a stabilizing and cross-linking agent. The as-synthesized

nanocomposites were characterized by Transmission Electron Microscopy (TEM), Scanning

RI
Electron Microscopy (SEM), X-ray diffraction (XRD), Energy-dispersive X-ray spectroscopy

(EDS), UV-visible spectrophotometer (UV-Vis) and vibrating sample magnetometer (VSM). The

SC
results demonstrated that Ag/Fe3O4-CS composite nanoparticles (NPs) were composed of parent

U
components, Fe3O4 and Ag NPs, which were uniformly dispersed in the chitosan matrix. The hybrid
AN
NPs exhibited strong antibacterial property against Pseudomonas aeruginosa. With high

magnetization value (67 emu/g), the synthesized Ag/Fe3O4-CS composite can be easily separated or
M

recycled in potential biomedical applications. Furthermore, the results showed that the

multicomponent hybrid nanostructures appeared to be the promising material for local

D

hyperthermia, which can be used as thermoseeds for localized hyperthermia treatment of cancers.
TE

Keywords: Ag/Fe3O4-chitosan, nanocomposites, antibacterial activity, hyperthemia.

C EP
AC
 ACCEPTED MANUSCRIPT
Highlighted

1. Introduction

Fabrication of NPs with desired properties through their surface modifications has attracted

growing attention in recent years [1]. Extensive efforts to date have shown that the advantages of

multicomponent hybrid nanostructures include (i) integration of different functionalities (ii) novel

PT
functions which are not available in single component materials or structures, (iii) enhancement of

properties and breaking the natural constraints of single phase materials [2, 3]. Many researches

RI
have investigated Fe3O4 composites or hybrids doped with noble or other transition metals as the

SC
formation of multicomponent nanostructures significantly broadened the properties and potential

application of Fe3O4 [4]. Although noble metals such as gold [5, 6], palladium [7, 8] and platinum

U
[9, 10] in Fe3O4 have excellent performance, their practical applications are restricted by the cost.
AN
Thus, attempts have been made to explore cheaper alternative metals which may have better

practical value. Magnetic materials and silver metal based bi-functional composites have been
M

extensively studied owing to their unique properties and applications [11, 12]. Individually, Fe3O4
D

and Ag NPs are classic nanomaterials and their properties as well as applications have been widely
TE

reported. Magnetic Fe3O4 NPs can be used in bioseparations, targeted drug delivery, magnetic

resonance imagining [13-16] and hyperthermia [17, 18] because of their biocompatibility, and low
EP

toxicity [19, 20]. On the other hand, silver NPs have long been known for their unique

physicochemical properties and broadly applied as catalysts, optical sensors, in electronics, optics,
C

and as bactericidal and therapeutic agents [21]. However, the applications Ag NPs, like other NPs,
AC

are usually hindered by the aggregation of particles which reduce their surface areas and eventually

their activity. Moreover, as the environmental hazards and negative effects of Ag NPs on human

beings have not been fully understood and evaluated, recovery or recycling of the used Ag NPs are

important [22]. The immobilization of Ag NPs on Fe3O4 surface was found to not only help improve

the dispersion of Ag NPs but also allow the facile recovery of the nanocomposites by magnetic
 ACCEPTED MANUSCRIPT
Highlighted

fields. The unique combination of surface properties of Ag NPs and magnetic properties of Fe3O4

lead to a great deal of potential applications in biological targeting, biological separation, high-

density magnetic recording, catalysis, and targeting therapy [23]. Therefore, many synthetic routes

of Ag-Fe3O4 NPs have been reported. Zhang et al. presented the one-pot synthesis of magnetically

PT
recoverable Ag-Fe3O4 nanocomposite in water-phase solution using AgNO3 and FeCl3 as precursors

and ethylene glycol as reductant [24]. Similarly, Zhu et al. fabricated Ag-Fe3O4 nanocomposites

RI
using ferrous chloride and silver nitrate as the iron and silver source in the presence of

SC
polyvinylpyrrolidone [25]. Chen et al. have used solvothermal method to synthesized Ag/Fe3O4

nanowire. Therein, Ag nanowire was prepared by a polyol synthesis route and the solvothermal

U
method was explored to load Fe3O4 on the silver nanowire [26]. Lopes et al. described the two-step
AN
chemical method to prepare Ag-Fe3O4 colloidal dimer NPs. The Ag NPs were prepared by heating a

mixture of C54H45NO3P3Ag, oleyamine, and oleic acid in phenyl-ether solution at 250 oC. After that,
M

the mixture including Ag colloidal NPs, Fe(acac)3, 1,2-hexadecanediol, oleic acid and oleyamine in
D

phenyl-ether was mixed and thermally processed to obtain Ag-Fe3O4 heterodimer NPs [27]. Li et al.
TE

reported the synthesis of Ag/Fe3O4 by electroless silver plating technique, using AgNO3 and

formaldehyde (methanal) on the surface of Fe3O4 NPs [28]. However, these methods have several
EP

intrinsic drawbacks, including the involvement of complicated chemical synthesis, high temperature

and pressure operation, the need of expensive surfactants. Therefore, it should be of particular
C

importance to explore facile, rapid, and low cost methods for preparing Ag-Fe3O4 NPs. Chitosan is a
AC

promising stabilizing and cross-linking agent in fabrication of Fe3O4/Ag NPs since it possesses

excellent properties such as availability, safety, non-toxicity, biocompatibility, biodegradability, low

immunogenicity, and antibacterial capacity [29]. Furthermore, few works have reported the

synthesis of Ag/Fe3O4-Chitosan (Ag/Fe3O4-CS) NPs as well as their application in antibacterial and

hyperthermia.
 ACCEPTED MANUSCRIPT
Highlighted

In this study, a facile method to prepare chitosan-based Ag/Fe3O4 nanocomposites (Ag/Fe3O4-

CS) at low temperature was proposed. The composite structure was formed via reduction of AgNO3

by NaBH4, in a suspension containing chitosan and Fe3O4. Structure, magnetic properties, and

composition of the nanocomposites were characterized. Furthermore, potential functionalities of the

PT
hybrid NPs such as antibacterial activity, magnetization and heating ability under external magnetic

field were also investigated.

RI
2. Materials and methods

SC
2.1. Materials

All of the chemicals were of analytical grade and used without further purification. Chitosan

U
was purchased from Tokyo Chemical Company Ltd. Other reagents such as FeCl2.4H2O,
AN
FeCl3.6H2O, NH4OH, CH3COOH, AgNO3, and NaBH4 were from Sigma Aldrich.

2.2. Preparation of Fe3O4 NPs and Fe3O4-CS NPs

M

Fe3O4 NPs were synthesized through the co-precipitation method, which was based on the
D

procedures described by Hong et al. [30] with significant modifications. In a typical synthesis, a
TE

mixture was prepared by adding 4 ml of FeCl3 (2 M) and 2 ml of FeCl2 (2 M) solutions to a flat

bottom beaker. The solution was vigorously stirred at 30°C for 45 min. Chemical precipitation was
EP

carried out at 30oC under vigorous stirring and covering of N2 gas by slow addition of 100 ml of

aqueous ammonia solution (1 M). As the solution was stirred for about 1 h, black Fe3O4 NPs
C

appeared and were separated by external magnet. The NPs were then rinsed by distilled water and
AC

ethanol until pH reached 7. For preparation Fe3O4-CS NPs, chitosan (1 g) in 100 mL of 1.0 wt%

acetic acid solution and 1 g the collected magnetic Fe3O4 NPs in 100 mL distilled water was added

into three-necked flask [31]. The mixture was treated with ultrasonic for 5 min and stirred for 20

min to produce a well dispersed suspension of Fe3O4-CS NPs (labeled as A solution).

2.3. Synthesis of Ag/Fe3O4-CS nanocomposites, and Ag-CS NPs

 ACCEPTED MANUSCRIPT
Highlighted

Fe3O4/Ag-CS nanocomposites were synthesized by adding 20 ml of 0.1 M AgNO3 solution

to 50 ml of A solution with vigorously stirred for 30 min. After heat-treating at 40oC, an excess

amount of NaBH4 (2 M) was slowly added. The mixture was vigorously stirred for 30 min to obtain

hybrid Fe3O4/Ag-CS nanocomposites. The hybrid composites were first separated by external

PT
magnet and washed several times with water to remove residual components. Then, they were

collected and sonically dispersed in DI water for about 5 min for further experiment and analyses.

RI
The Ag-CS NPs were prepared using slight modification of the synthesis process of

SC
Ag/Fe3O4-CS. In a typical experiment, a homogeneous solution (20 mL) of 0.1 M AgNO3 was

added to 50 mL of 1.0 wt% acetic acid solution containing chitosan (0.25 g) with vigorous stirring

U
for 30 min at 40 oC. After that, an excess amount of NaBH4 (2 M) was slowly added and the mixture
AN
was vigorously stirred for 30 min to obtain Ag-CS NPs.

2.4. Characterizations
M

The transmission electron microscopy (TEM, Hitachi 100C), and scanning electron
D

microscopy (SEM, Model JSM-5300LV) equipped with an energy dispersive X-ray spectroscopy
TE

(EDS) is used to examine the morphology and elemental analysis of Ag/Fe3O4-CS composites. The

phase structure is characterized by the X-ray diffraction (XRD, D8 Advance, Brucker, Germany).
EP

The UV-visible absorption behaviors of the samples were recorded, using a Beckman DU 520 UV-

Vis spectrophotometer. Magnetic properties of Fe3O4 and Fe3O4/Ag-CS NPs were characterized by
C

a vibrating sample magnetometer (VSM) with the physical property measurement system (DMS
AC

800, Quantum Design, Inc.). Saturation magnetization (Ms) and coercive field (Hc) were measured

at room temperature with the magnetic field ranging from -10000 to 10000 Oe. The heating

experiments of the Ag/Fe3O4-CS NPs in AC magnetic field were performed on a medium frequency

induction heating apparatus.

2.5. Antibacterial activity of the synthesized Ag/Fe3O4-CS nanocomposites

 ACCEPTED MANUSCRIPT
Highlighted

The antibacterial activity of samples were preliminarily tested by agar diffusion method,

using pathogenic bacteria strain, Pseudomonas aeruginosa (ATCC 15442) (American Type Culture

Collection). Mueller-Hinton Agar (Merck) was used as the growth medium. Wells with diameters of

8 mm were punched on the agar plates with the help of sterile tips. Approximately 2.5 mL of target

PT
bacterial strains (105 cfu/mL) was inoculated on the plates and then 50 µl of sample (200 ppm) per

well was loaded. After being incubated at 37oC for 24 hours, the diameter of the inhibition zones

RI
were determined.

SC
2.6. Hyperthermic test

In the present study, magnetic hyperthermia (MHT) of material was measured using an

U
induction heater (DM100, Zaragoza, Spain) with a single turn, 2.5 cm diameter coil operating at 236
AN
kHz. The sample was put into the applicator where an alternating magnetic field was generated.

Characteristics parameters such as amplitude (40-80 (Oe)) and time (0-1600s) were preset prior to
M

the experiments. During the test, temperature of the sample increased due to the interractions with
D

the magnetic field. The temperature rise versus time was recorded with a 0.1°C resolution.
TE

3. Results and discussion

3.1. Characterization
EP

The crystal structure of as-prepared Fe3O4, Fe3O4-CS, and Ag/Fe3O4-CS NPs were examined

via powder XRD measurement, and the data is shown in Fig. 1. XRD pattern of Fe3O4 and Fe3O4-
C

CS NPs exhibited typical Fe3O4 cubic structure, where all diffraction peaks are well indexed to the
AC

(220), (311), (400), (422), (511), and (440) planes (JCPDS No. 19-0629). The weaker diffraction

lines of Fe3O4-CS NPs indicate that Fe3O4 particles were successfully coated by amorphous CS;

however, CS coating did not change the crystal structure of Fe3O4. The formation of Ag and Fe3O4

NPs in Ag/Fe3O4-CS nanocomposites is also confirmed by powder XRD. Beside the presence of

diffraction peaks of cubic magnetite, the typical peaks of face-centered cubic silver (111), (20), and
 ACCEPTED MANUSCRIPT
Highlighted

(220) at 2θ = 38.1°, 44.32°, and 64.4° (JCPDS No. 87-720) can be also observed. The characteristic

diffraction peaks of the Fe3O4 NPs in Ag/Fe3O4-CS did not differ from that of the pristine Fe3O4

NPs and Fe3O4-CS sample, indicating that Ag loading procedure did not influence the crystal

structure of the Fe3O4 NPs.

PT
Fig. 1.

The morphology of Fe3O4-CS, Ag/Fe3O4-CS NPs, and Ag-CS NPs was characterized by

RI
SEM and TEM images (Fig. 2 A-E). It can be seen that the morphology of CS-coated magnetite

SC
NPs exhibit highly dispersed particles with a size of about 10 nm (Fig. 2 A, B). As SEM and TEM

images of Fe3O4-CS and Ag/Fe3O4-CS were compared, Ag NPs appeared on the magnetic CS with

U
larger particle sizes, ranging from 20 to 50 nm which were in agreement with TEM image of Ag
AN
NPs in Ag-CS nanocomposite (Fig. 2 E). In Fig. 2 D, Ag and Fe3O4 appear as black and grey

particles, respectively, because Ag has a higher electron density and allows fewer electrons to
M

transmit through [32]. Fig. 2 F shows the UV-visible absorption spectra of Ag-CS NPs and
D

Ag/Fe3O4-CS nanocomposites. Compared with the absorption peak around 420 nm of pure Ag NPs,
TE

the surface plasmon resonance peak of Ag/Fe3O4-CS nanocomposites is broadened and red-shifted

to 446 nm, suggesting a contacting of the Ag NPs with the metal oxide [33]. The red shift was
EP

attributed to the electron transfer across the Ag-Fe3O4 interface [34].

Fig. 2.
C

To further determine the composition of the nanocomposites, energy dispersive X-ray

AC

spectroscopy was performed on an individual particle (Fig. 3). The Fe, O, Ag and C are four main

elements found and indicate that the obtained nanocomposites was composed the target materials.

The amount of Ag and Fe in the Ag/Fe3O4-CS was 17.69% and 51.21%, respectively (Table S1).

The formation of the hybrid nanocomposites could be explained based on physical mixing of Ag

and Fe3O4 NPs and their bindings via chitosan matrix. In general, Ag and Fe3O4 NPs could be
 ACCEPTED MANUSCRIPT
Highlighted

attracted to each other due Vander Waals forces [35], induced by high surface energy of the

particles. On the other hands, chitosan matrix, acting as a binder or cross-linking agent, embeds both

Ag and Fe3O4 NPs, conducive to the formation of composite structure. Individual NPs and chitosan

could interact via electrostatic forces (Ag NPs) [36] or Van der Waals and acid-base interactions

PT
(Fe3O4) [37]. All the above data demonstrated that the Ag/Fe3O4-CS can be successfully achieved

by facile method.

RI
Fig. 3.

SC
The magnetic hysteresis curves of pristine Fe3O4 and Ag/Fe3O4-CS nanocomposites are

shown in Fig. 4. No coercivity or remanence could be observed for the two samples, suggesting that

U
Fe3O4 NPs and the hybrid nanocomposites have superparamagnetic properties. Both of them
AN
showed strong magnetization at room temperature. The saturation magnetization of Ag/Fe3O4-CS is

67.5 emu/g, which is smaller than that of pure Fe3O4 (77.7 emu/g). The phenomenon could be due
M

to the incorporation of diamagnetic Ag and chitosan components in the nanostructures which dilutes
D

the magnetic response of the Fe3O4 component. The magnetization values of the nanocomposites in
TE

this study (67.5 emu/g) is higher than those of some works reported previously [12, 22, 36, 38],

indicating that the as-synthesized hybrid NPs could be used in prospective applications required the
EP

interactions of particles with external magnetic fields such as bioseparation, magnetic imaging or

hyperthermia treatment.
C

Fig. 4.
AC

3.2. Antibacterial tests

Silver, especially Ag NPs, has long been used in antibacterial materials. In this study,

antimicrobial properties of Fe3O4 NPs, Ag-CS NPs and Ag/Fe3O4-CS nanocomposites were tested

against P. aeruginosa, which is a common bacterium and one of the leading causes of nosocomial

infections worldwide [39] (Fig. 5). The results showed that pure Fe3O4 NPs have no antibacterial
 ACCEPTED MANUSCRIPT
Highlighted

activity. Ag/Fe3O4-CS nanocomposites exhibited better antibacterial effects against P. aeruginosa

than Ag-CS NPs, indicated by larger zone of inhibition (24 mm) than that of the Ag-CS NPs (14

mm). The antibacterial activity of Ag/Fe3O4-CS was attributed to the existence of the Ag NPs;

however, the bactericidal mechanism of Ag nanocomposites was still not clear and required further

PT
investigations. Kim et al. reported that the gelatin/Ag NP sponges exhibited efficient bactericidal

activity against both gram negative and positive bacteria, E. coli and S. aureus [40]. Davoodbasha

RI
et al. observed that the cellulose/Ag NP biocomposites showed a broad spectrum of antimicrobial

SC
activity toward various pathogens, being most effective against gram negative bacteria, and then

gram positive bacteria in the order C. albicans and A. parasiticus [41]. Bhupendra Chudasama et al

U
prepared bifunctional nanocomposite Fe3O4-Ag nanostructure then studied antimicrobial activity
AN
on both Gram negative (E. coli and P. vulgaris) and Gram positive (B. megaterium and S. aureus)

bacterial strains. The results showed that the effect of the nanocomposite on Gram negative strains
M

was found to be better than that observed for sole Ag NPs [42]. In another study, M. Kooti et al
D

have examined the antibacterial activity of the silver coated magnetic nanoparticles composite and
TE

compared the activity with that of AgNPs, bare magnetic nanoparticles and 5 five standard

antibacterial drugs, viz, Penicillin, Cefixime, Amoxicillin, Erythromycin and Streptomycin on

EP

B.subtilis and S. aureus (Gram positive); E coli and P.aeruginosa (Gram negative). It was found

that while all 5 screened drugs are not effective against Gram negative (E. coli and P. aeruginosa),
C

Ag@CoFe2O4 found to be effective [43].

AC

Further, these above results indicated that the antibacterial effect of Ag NPs is dependent on

size and shape of the particles and that will enhance the antibacterial ability by producing electronic

effects, which are defined as changes in the local electronic structure of the surface [44].

We can also speculate that Fe3O4 plays an additive role in the inhibitory effect of silver on

gram negative organisms [42, 43, 45]. Better antibacterial performance towards P. aeruginosa of
 ACCEPTED MANUSCRIPT
Highlighted

the Ag/Fe3O4-CS should be related to multicomponent hybrid nanostructures, in which more active

sites to damage bacterial membranes were provided. Furthermore, the Ag/Fe3O4-CS nanohybrids

are easily recycled and reusable due to its magnetic property. These results suggest that Ag/Fe3O4-

CS nanocomposites have the potential to be developed into a novel recyclable, antibacterial

PT
materials. Despite the main focus of this study was to develop a novel method for preparing

bifunctional Ag/Fe3O4-CS nanocomposite, however, the antibacterial effect of Ag/Fe3O4-CS

RI
against different types of bacteria still needs to be expanded in future studies to clearly understand

SC
bactericidal mechanism of composite Ag nanostructures.

Fig. 5.

U
3.3. The hyperthermic properties
AN
The heating efficacy of Ag/Fe3O4-CS suspension was investigated as additional

functionality. Fig. 6 A shows the time dependent heating curves of 1 mg/mL Ag/Fe3O4-CS under
M

external AC magnetic field. It has been observed that the temperature of samples increased as a
D

function time and reached saturation after 1200 s. With increasing magnetic field strengths (40–80

Oe), the maximum values of temperature were 31, 34, 36, 43, and 47 oC, respectively. The time-
TE

dependent temperature curve of four different concentrations of Ag/Fe3O4-CS nanocomposites

EP

exposed in AC magnetic field was also studied. As shown in Fig. 6 B, with the increasing

concentration of sample, the temperature rose rapidly. The temperature of the sample reached a
C

saturation temperature after a period of time with higher saturation time observed for higher
AC

concentration of the Ag/Fe3O4-CS nanocomposites. After 1200 s, the temperature of suspensions

containing Ag/Fe3O4-CS nanocomposites with concentration of 1 mg/mL is 47oC. Therein, the

heating of the cancer area containing the implanted thermoseeds to elevated temperatures of 41-46
o
C in an external AC magnetic field can kill tumor cells [46]. Therefore, the as-synthesized
 ACCEPTED MANUSCRIPT
Highlighted

multicomponent Ag/Fe3O4-CS hybrid NPs can be used as thermoseeds for localized hyperthermia

treatment of cancers.

Fig. 6.

4. Conclusion

PT
In summary, multifunctional Ag/Fe3O4-CS nanocomposites was successfully synthesized

through simple method and applied to antibacterial activity and local hyperthermia. The prepared

RI
Ag/Fe3O4-CS nanocomposites revealed good antibacterial activity, especially against P. aeruginosa

SC
(gram-negative bacteria) and it can be used as highly efficient separable and reusable materials,

under magnetic field, for inhibition of bacterial growth. Furthermore, the NPs hybrid will be useful

U
as good thermoseeds for localized hyperthermia treatment of cancers. The findings could contribute
AN
to the large scale synthesis of bi-functional Ag/Fe3O4-CS NPs for diverse applications.

Acknowledgments
M

This work was supported by the National Foundation for Science and Technology
D

Development (NAFOSTED), project code: 103.02-2011.57 (D.G.Pham). Financial support was also
TE

provided in part by IFS grant (N0 F/5022-1). Loc T. Nguyen was also funded by Asian Institute of

Technology (AIT) Research Initiation Grant (SERD-2014-1FB). The authors would like to express
EP

their sincere thanks to Prof. Dr. Sci. Nguyen Xuan Phuc for helpful discussion and support.

References
C

1. R. Mohammadi, E. Eidi, M. Ghavami, M. Z. Kassaee, J. Mol. Catal. A-Chem. 393 (2014) 309–
AC

316.

2. H. Zeng, S. Sun, Adv. Funct. Mater. 18 (2008) 391–400.

3. H. Wang, J. Shen, G. Cao, Z. Gai, K. Hong, P.R. Debata, P.B. and S. Zhou,, J. Mater. Chem. B. 1

(2013) 6225-6234.
 ACCEPTED MANUSCRIPT
Highlighted

4. M. E. F. Brollo1, R. L.-Ruiz, D. Muraca, S. J. A. Figueroa, K. R. Pirota, M. Knobel, Scientific

Reports 4 (2014) 1-6.

5. H. Yu, M. Chen, P. M. Rice, S. X. Wang, R. L. White, S. Sun, Nano Lett. 5 (2005) 379-382.

6. A. Mezni, I. Balti, A. Mlayah, N. Jouini, L. S. Smiri, J. Phys. Chem. C 117 (2013) 16166−16174.

PT
7. W. Sun, Q. Li, S. Gao, J. K. Shang, Appl. Catal. B-Environ. 125 (2012) 1-9.

8. T. Yao, Q. Zuo, H. Wang, J. Wu, B. Xin, F. Cui, T. Cui, J. Colloid. Interf. Sci. 450 (2015) 366–

RI
373.

SC
9. C. Wang, H. Daimon, S. Sun, Nano Lett. 9 (2009) 1493-1496.

10. D. Wu, H. Fan, Y. Li, Y. Zhang, H. Liang, Q. Wei, Biosens. Bioelectron. 46 (2013) 91–96.

U
11. D. Tang, R. Yuan, and Y. Chai, J. Phys. Chem. B110 (2006) 11640-11646.
AN
12. H. Xia, B. Cui, J. Zhou, L. Zhang, J. Zhang, X.Guo, H. Guo, Appl. Surf. Sci. 257 (2011) 9397-

9402.
M

13. A. K. Gupta, M. Gupta, Biomater. 26 (2005) 3995-4021.

D

14. J. Dobson, Drug Dev. Res. 67 (2006) 55-60.

TE

15. C. J. Sunderland, M. Steiert, J. E. Talmadge, A. M. Derfus, S. E. Barry, Drug Dev. Res. 67

(2006) 70-93.
EP

16. M. Arruebo, R. F.-Pacheco, M. R. Ibarra, J. Santamarıa, Nano Today 2 (2007) 22-32.

17. J. P. Fortin, C. Wilhelm, J. Servais, C. Menager, J. C. Bacri, F. Gazeau, J. Am. Chem. Soc. 129
C

(2007) 2628–2635.
AC

18. J. Giri, P. Pradhan, T. Sriharsha, D. Bahadur, J. Appl. Phys. 97 (2005) 10Q916.

19. J. Gao, H. Gu and B. Xu, Acc. Chem. Res. 42 (2009) 1097-1107.

20. R. R. Qiao, C. H. Yang, M. Y. Gao, J. Mater. Chem. 19 (2009) 6274-6293.

21. S. Prabhu, E. K.Poulose, Int. Nano Lett. (2012) 2:32.

22. M. Zhu, C. Wang, D. Meng, G. Diao, J. Mater. Chem. A. 1 (2013) 2118-2125.

 ACCEPTED MANUSCRIPT
Highlighted

23. C. H. Liu, Z. D. Zhou, X. Yu, B. Q. Lv, J. F. Mao, D. Xiao, Inorg. Mater. 44 (2008) 291-295.

24. D.-H. Zhang, G.-D. Li, J.-X. Li, J.-S. Chen, Chem. Commun. 29 (2008) 3414–3416.

25. S. Zhu, C. Fan, J. Wang, J. He, E. Liang, M. Chao, J. Colloid. Interf. Sci. 438 (2015) 116–121.

26. J. Chen, Y. Liu, G. Zhu, A. Yuan, Cryst. Res. Technol. 49 (2014) 309–314.

PT
27. G. Lopes, J. M. Vargas, S. K. Sharma, F Béron, K. R. Pirota, M. Knobel, C. Rettori, R. D.

Zysler, J. Phys. Chem. C 114 (2010) 10148–10152.

RI
28. S. Li, Z. Zhou, T. Zhang, G. Jiang, R. Su, J. Magn. Magn. Mater. 358-359 (2014) 27–31.

SC
29. Y. Wu, Y. Wang, G. Luo, Y. Dai, Bioresource Technol. 100 (2009) 3459–3464.

30. R. Y. Hong, J. H. Li, H. Z. Li, J. Ding, Y. Zheng, D. G. Wei, J. Magn. Magn. Mater. 320 (2008)

U
1605–1614.
AN
31. N. D. Cuong, T. T. Hoa, D. Q. Khieu, T. D. Lam, N. D. Hoa, N. V. Hieu, J. Alloys Compd. 523

(2012) 120–126.
M

32. L. Zhang, Y.-H. Dou, H.-C. Gu, J. Colloid. Interf. Sci. 297 (2006) 660–664.
D

33. C. Wang, H. Yin, S. Dai, S. Sun, Chem. Mater. 22 (2010) 3277–3282.

TE

34. H. Yu, M. Chen, P. M. Rice, S. X. Wang, R. L. White, S. H. Sun, Nano Lett. 5 (2005) 379–382.

35. D. Li, R. B. Kaner, J. Am. Chem. Soc. 128 (2006) 968-975.

EP

36. J. L. Arias, H. Reddy, P. Couvreur, J. Mater. Chem. 22 (2012) 7622-7632.

37. H. Huang, Q. Yuan, X. Yang, Colloid Surf. B: Biointer. 39 (2004) 31–37.

C

38. A. Amarjargal, L. D. Tijing, I. T. Im, C. S Kim, Chem. Eng. J. 226 (2013) 243–254.
AC

39. T. Strateva, D. Yordanov, J. Med. Microbiol. 58 (2009) 1133–1148.

40. S. C. Kim, S. M. Kim, G. J. Yoon, S. W. Nam, S. Y. Lee, J. W. Kim, Curr. Appl. Phys., 14,

(2014) S172-S179.

41. M. Davoodbasha, S.-Y. Lee, S.-C. Kim, J.-W. Kim, RSC Adv. 5 (2015) 35052–35060.
 ACCEPTED MANUSCRIPT
Highlighted

42. B. Chudasama, A.K. Vala, N. Andhariya, R. V. Mehta , R. V. Upadhyay, J. Nanopart Res., 12

(2010), 1677–1685.

43. M. Kooti, S. Saiahi, H. Motamedi, J. Magn. Magn. Mater., 333 (2013), 138–143.

44. C. Zhang, X. Wang, J. Sun, T. Koua, Z. Zhang, Cryst. Eng. Comm., 15 (2013) 3965-3973.

PT
45. D. Lee, R. E. Cohen, M. F. Rubner, Langmuir 21 (2005) 9651 9659.

46. D.-L. Zhao, X.-X. Wang, X.-W. Zeng, Q.-S. Xia, J.-T. Tang, J. Alloys Compd. 477 (2009) 739–

RI
743.

U SC
AN
M
D
TE
C EP
AC
 ACCEPTED MANUSCRIPT
Highlighted

<Figure captions>

Fig. 1. XRD pattern of Fe3O4, Fe3O4-CS, and Ag/Fe3O4-CS nanocomposites.

Fig. 2. SEM images of Fe3O4-CS NPs (A), and Ag/Fe3O4-CS nanocomposites (C); TEM images of

Fe3O4-CS NPs (B), Ag/Fe3O4-CS nanocomposites (D), and Ag- CS NPs (E); and UV-Vis absorption

PT
of Ag-CS NPs and Ag/Fe3O4-CS nanocomposite (F).

Fig. 3. Energy dispersive X-ray spectroscopy of the prepared Fe3O4/Ag-CS nanocomposites. The

RI
unit “count” refers to the number of X-rays received and processed by the detector.

SC
Fig. 4. Magnetization curves of Fe3O4 NPs and Fe3O4/Ag-CS nanocomposites

Fig. 5. Photograph of the antibacterial test results for Ag/Fe3O4-CS nanocomposites (1), Fe3O4 NPs

U
(2), and Ag-CS NPs (3) against P. aeruginosa.
AN
Fig. 6. Time-dependent temperature curves of Ag/Fe3O4-CS ferrofluid at different magnetic field

strengths (A), and at different Ag/Fe3O4-CS concentrations (B).

M
D
TE
C EP
AC
 ACCEPTED MANUSCRIPT
Fig. 1.

(311)
@Fe O

T(440)
Fe 3O34 4
@Fe
Fe 3O O-CS
34 4
-CS

C R(511)
IP
@Ag/Fe
Ag/Fe 3O
O4-CS
3 4-CS
(200)

(400)

S(422)
Intensity (a.u.)

U
AN
M
(200) D
E P (111)
TE

(220)
C
AC

30 40 50 60 70
2θ (deg.)
 (B)
ACCEPTED MANUSCRIPT

PT
RI
SC
(D)

U
AN
M
D
TE
EP

2.5
C

(F)
AC

2.0
Absorbance

1.5

1.0 Ag/Fe3O4-CS

0.5
Ag-CS
0.0
320 420 520 620 7
Wavelength (nm)
 ACCEPTED MANUSCRIPT
Fig. 3.

1600 EDX spectrum of Fe3O4/Ag nanocomposite

Fe
1400
O

PT
1200

RI
1000
counts

SC
800 Ag

Fe U
AN
600

400 Ag
M

C Fe
D

200
TE

0
EP

0 1 2 3 4 5 6 7 8 9 1
Energy (keV)
C
AC
 ACCEPTED MANUSCRIPT
Fig. 4.
80 Ag/Fe3O4-CS
Fe3O4
60
Magnetization (emu/g)

40

PT
20

RI
0

SC
-20

-40

U
AN
-60

-80
M

-10000 -5000 0 5000 10000

D

Magnetic field (Oe)

TE
C EP
AC
 ACCEPTED MANUSCRIPT
Fig. 5.

P. aeruginosa

PT
1

RI
2

U SC
3
AN
M
D
TE
EP
C
AC
 ACCEPTED MANUSCRIPT

Fig. 6.
60 60
80 Oe (A) 1 mg/ml (B)
70 Oe 55 55 0.7 mg/ml
60 Oe
50 Oe 0.5 mg/ml

PT
50 50 0.3 mg/ml
40 Oe

Temperature ( C)
o
45 45

RI
40 40

SC
35 35

30 30

25
U 25
AN
200 400 600 800 1000 1200 1400 1600 0 200 400 600 800 1000 1200 1400
Time (s) Time (s)
M
D
TE
C EP
AC
 ACCEPTED MANUSCRIPT
> A facile method to prepare bi-funtional Ag/Fe3O4-CS nanocomposites.

>The antibacterial and hyperthermic properties of Ag/Fe3O4-CS hybrid nanoparticles.

> Potential application of bi-funtional Ag/Fe3O4-CS nanocomposites for antibacterial activity and
localized hyperthermic cancerous treatment.

PT
RI
U SC
AN
M
D
TE
C EP
AC
 ACCEPTED MANUSCRIPT

Electronic Supplementary information (ESI) for

PT
Facile synthesis of multifunctional Ag/Fe3O4-CS nanocomposites

RI
for antibacterial and hyperthermic applications

U SC
Ngoan Thi Nguyen1, Lam Dai Tran2*,3, Cuong Duc Nguyen4, Loc Thai Nguyen5, Cham Ba Thi1, Binh Hai Nguyen6,
Duong Ba Thi1, Nam Hong Pham6, Dzung Tuan Nguyen7, Hoa Thai Tran4, Dien Gia Pham1**

AN
1Institute of Chemistry, Vietnam Academy of Science and Technology

M
18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam
2Graduate University of Science and Technology, Vietnam Academy of Science and Technology

D
18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam

TE
3Duy Tan University, 182 Nguyen Van Linh, Da Nang, Vietnam
4College of Sciences, Hue University, 77 Nguyen Hue, Hue City, Viet Nam
EP
5Food Engineering and Bioprocess Technology, Asian Institute of Technology, PO Box 4, KlongLuang, Pathumthani

12120, Bangkok, Thailand

6Institute of Materials Science, Vietnam Academy of Science and Technology
C

18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam

AC

7Institute of Tropical Technology, Vietnam Academy of Science and Technology

18 Hoang Quoc Viet, Cau Giay, Hanoi, Vietnam

 ACCEPTED MANUSCRIPT

Table S1. Major elemental components of A/Fe3O4-CS analyzed by EDX

Element Energy (keV) Mass (%) Atom (%) Error (%)

PT
C K* 0.277 3.28 8.92 0.09

RI
SC
NK 0.392 0.42 1.25 0.67

OK 0.525 26.42 52.70 0.33

U
AN
Na K* 1.041 0.50 0.92 0.47

M
Si K* 1.739 0.21 0.43 0.24

D
P K* 2.013 0.17 0.27 0.21

S K* 3.307
TE 0.10 0.14 0.16
EP
Fe K 6.398 51.21 30.00 0.55
C

Ag L 2.983 17.69 5.37 0.47

AC