1. CERAMICS
INTERNATIONAL
Available online at www.sciencedirect.com
Ceramics International 40 (2014) 7425–7430
Food-directed synthesis of cerium oxide nanoparticles and their
neurotoxicity effects
Majid Darroudia,b,n
, Seyed Javad Hoseinic
, Reza Kazemi Oskueec,d
, Hasan Ali Hosseinie
,
Leila Gholamib
, Sina Geraylif
a
Nuclear Medicine Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
b
Department of Modern Sciences and Technologies, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
c
Department of Medical Biotechnology, School of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
d
Targeted Drug Delivery Research Center, Mashhad University of Medical Sciences, Mashhad, Iran
e
Chemistry Department, Payame Noor University, 19395-4697 Tehran, Iran
f
Department of Biology, Faculty of Sciences, Ferdowsi University of Mashhad, Mashhad, Iran
Received 10 December 2013; received in revised form 21 December 2013; accepted 21 December 2013
Available online 14 January 2014
Abstract
The use of food-directed and natural products for the synthesis of different nanoparticles (e.g., metal and metal oxide) is of enormous interest to
modern nanoscience and nanotechnology. We have developed a facile and green chemistry method with bio-directed, and low cost materials for
the synthesis of cerium oxide nanoparticles (CeO2-NPs) using honey. In this method, the conversion of cerium cations into CeO2-NPs was
achieved via a sol–gel process in aqueous honey solutions. The synthesized CeO2-NPs were characterized by the following title: UV–vis
spectroscopy, field emission scanning electron microscopy (FESEM), Fourier transform infrared spectroscopy (FT-IR), thermogravimetric (TGA–
DTA) analysis, Energy dispersive spectrum (EDS), and powder X-ray diffraction (PXRD). Spherical CeO2-NPs were synthesized at different
calcination temperatures and FESEM imaging along with its corresponding particles size distribution indicated the formation of nanoparticles in
size of about 23 nm. The PXRD analysis revealed fluorite cubic structure for CeO2-NPs with preferential orientation at (111) reflection plane. In
vitro cytotoxicity studies on neuro2A cells, a dose dependent toxicity with non-toxic effect of a concentration below about 25 mg/mL was
illustrated. The synthesis of CeO2-NPs in aqueous honey solutions was found to be comparable to those obtained from conventional reduction
methods that uses hazardous materials proving to be an excellent alternative for the preparation of CeO2-NPs, using food and bio-derived
materials.
& 2013 Elsevier Ltd and Techna Group S.r.l. All rights reserved.
Keywords: A. Sol–gel processes; B. Electron microscopy; D. CeO2
1. Introduction
Cerium oxide nanoparticles (CeO2-NPs), as important rare-
earth oxide materials, have attracted enormous interest in
recent years due to its unique physicochemical properties that
are significantly different from those of bulk materials [1].
Nanocrystalline CeO2-NPs have been considered as a key
nanoscaled material for applications in catalysts [2], hydrogen
storage materials [3], fuel cells [4], polishing materials [5], gas
sensors [6], optical devices [7], ultraviolet absorbers [8], and
biomedical science fields [9,10]. Crystalline CeO2-NPs have
been synthesized by means of a variety of routes and
techniques, including solution precipitation [11], sonochemical
[12], hydrothermal [13], solvothermal [14], ball milling [15],
thermal decomposition [16], spray pyrolysis [17], thermal
hydrolysis [18], and sol–gel method [19–21]. However, the
utility of the mentioned methods suffers several drawbacks like
the use of high temperature and pressure, toxic reagents, long
reaction time, requirement of external additives as a specific
stabilizer, base and promoter during the reaction which limits
www.elsevier.com/locate/ceramint
0272-8842/$ - see front matter & 2013 Elsevier Ltd and Techna Group S.r.l. All rights reserved.
http://dx.doi.org/10.1016/j.ceramint.2013.12.089
n
Corresponding author at: Nuclear Medicine Research Center, Mashhad
University of Medical Sciences, Mashhad, Iran. Tel.: þ98 511 800 2286;
fax: þ98 511 800 2287.
E-mail addresses: majiddarroudi@gmail.com,
darroudim@mums.ac.ir (M. Darroudi).

2. the purity of the final product. Therefore, seeking a facile route
for low-cost, large-scale, controlled growth of CeO2-NPs at
atmospheric pressure and lower temperatures is essential. The
sol–gel method has gained quite an interest among researchers
since it offers controlled consolidation, shape modulation,
patterning of the nanostructures and a low processing tem-
perature [22,23]. Recently, biomaterials have been used in the
synthesis of CeO2-NPs [10,20,21], due to their quality of being
biodegradable and bioabsorbable with degradation products
that are non-toxic.
Currently, honey has been used in the field of nanotechnol-
ogy to apply green chemistry rules and environmentally benign
synthesis of nanoparticles [24–26]. Honey is a sweet viscous
fluid which is produced from honeybees, and is mainly
composed of carbohydrates, enzymes, vitamins, minerals and
antioxidants [27]. Honey mediated biological synthesis has lots
of advantages over other types of biological methods, includ-
ing avoidance of elaborate processes such as drying plant
materials and the maintenance of cell cultures [26]. Here, we
demonstrated a sol–gel approach for the synthesis of ultrafine
CeO2-NPs that has the advantages of being a simple process,
bio-directed, easy to scale-up and of low cost. Cerium nitrate
was used as the cerium source at different calcination
temperatures and the synthesized samples were then character-
ized through FESEM, PXRD, TGA–DTA, FT-IR, EDS, and
UV–vis spectroscopy.
2. Materials and methods
2.1. Materials and reagents
All the materials used were of analytical grade and were
used without any purification. Cerium (III) nitrate hexahydrate
was purchased from Fluka (Germany) and honey was pur-
chased from the local market (Ghayour-Mobarhan Honey Co.,
Mashhad – Iran). All glassware used in the laboratory
experiments were cleaned with fresh solutions of HNO3/HCl
(3:1, v/v), washed thoroughly with doubly distilled water, and
dried before use. Double distilled water was used in all
experiments.
2.2. Synthesis of CeO2-NPs
To prepare 5.0 g of CeO2-NPs, 12.6 g of Ce(NO3)3 Á 6H2O
was dissolved in 30 ml of distilled water and then stirred for
30 min. Meanwhile, 25 g of honey was dissolved in 50 ml of
distilled water and stirred for 15 min at room temperature to
achieve a clear honey solution. Afterwards, the cerium nitrate
solution was added to the honey solution, and the container
was place in an oil bath with a temperature at 60 1C. Through
stirring for 6 h, a light yellow color resin was obtained and
divided into 4 parts to be individually heated at a rate of 4 1C/
min up to the respective temperatures of 200 (C1), 400 (C2),
600 (C3), and 800 1C (C4), then the products was maintained
for 2 h at the specified temperatures in air to obtain CeO2-NPs.
2.3. Characterization of CeO2-NPs
The prepared CeO2-NPs were characterized by PXRD (Philips,
X0
pert, Cu Kα), FTIR (ST-IRST-SIR spectrometer), TGA (Q600),
UV–vis (Evolution 300s
Thermo Fisher Scientific), EDX (Leo
1450VP), and FESEM (Carl Zeiss Supra 55VP).
2.4. Evaluation of neurotoxicity effect
The cytotoxicity of CeO2-NPs was evaluated by the method
using 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium
bromide (MTT) assay [28]. Briefly, neuro2A cells were seeded
at a density of 1 Â 104
cells per well in 96-well plates and
incubated for 24 h. Thereafter, the cells were treated with
various concentrations of nanoparticles in the presence of 10%
FBS. The calcined CeO2-NPs (C3) was suspended in a stock
solution at 5 μg/ml in a solution of dimethyl sulfoxide
(DMSO)/double distilled water. After 24 h of incubation,
20 μl of 5 mg/ml MTT in the PBS buffer was added to each
well, and the cells were further incubated for 4 h at 37 1C. The
medium containing unreacted dye was discarded, and 100 μl of
DMSO was added to dissolve the formazan crystal formed by
live cells. Optical absorbance was measured at 590 nm
(reference wavelength 630 nm) using a microplate reader
(Statfax-2100, Awareness Technology, USA), and cell viabi-
lity was expressed as a percent relative to untreated control
cells. Values of metabolic activity are presented as mean7SD
of triplicates.
3. Results and discussion
In this section, we shall discuss the results of the synthesized
CeO2-NPs in aqueous honey solutions. In this study, we
attempted the fabrication of CeO2-NPs by using the sol–gel
method and honey as a greener capping and/or stabilizing
agent. The extensive number of carbohydrates, enzymes, and
vitamins containing hydroxyl and amine groups in the honey
matrix structure can facilitate the complexation of cerium
cations (Ce3 þ
) to an initial molecular matrix. This structure
enables honey to coat and stabilize cerium species and finally
CeO2-NPs while inhibiting their excessive aggregation or
crystal growth. As it is illustrated in Fig. 1, due to the
increased calcination temperature, the color of sol–gel derived
CeO2-NPs changed from black to lemon and finally to white.
The thermogravimetric and derivative analysis (TGA/DTA)
curves of the as-prepared gel in an aqueous honey environment
are presented in Fig. 2. The heating process was started at
about 20 1C, and then increased up to 800 1C along with a
temperature rate change of 10 1C/min. The first weight loss
between 20 and 160 1C is an initial mass loss of 37.4% (bends
of Ed1 and Ed2) attributable to the loss of adsorbed water and
crystal water, since gradual dehydration of cerium hydroxide
takes place in this temperature range. The second stage appears
at 160–355 1C (48.5%) is attributed to the decomposition of
chemically bound groups, which corresponds to bends of Ed3
and Ed4. In this case, it represents decomposition of honey
molecules to other organic compound(s). Further mass loss of
M. Darroudi et al. / Ceramics International 40 (2014) 7425–74307426

3. 8.2% (Ed5) takes place in the range of 355–400 1C, associated
with further oxidation of cerium components [29]. The total
mass loss of the sample is 94.1%. No weight loss between 400
and 800 1C was detected on the TGA curve, which indicates
the formation of CeO2-NPs as the stable product.
The typical UV–vis absorption peak of the C3 is represented
in Fig. 3. The C3 was dispersed in water with concentration of
0.1 wt% and had the solution used to perform the UV–vis
measurement. The spectrum revealed a characteristic absorp-
tion peak at wavelength of 314 nm for C3, which can be
assigned to the intrinsic band-gap absorption of CeO2-NPs due
to the electron transitions from the valence band to the
conduction band. In other words, the absorption of the charge
transfer transition from O2p to Ce4f in CeO2-NPs produces the
band at approximately 300 nm [30,31]. A common way to
obtain the band gap of the materials with a direct band gap
from the absorbance spectra is to get the first derivative of the
absorbance with respect to the photon energies. The band gap
can be estimated from the maximum in the derivative spectrum
at the lower energy sides [32,33]. The derivative of the
absorbance of the CeO2-NPs illustrated in the inset of Fig. 3,
which indicates a band-gap of 3.5 eV for the C3 and is higher
than the bulk experimental value (3.19 eV) [34]. For nanopar-
ticles with particle sizes down to a few nanometers, the band-
gap value is modified because of the quantum confinement
effect [35]. The good absorption of the CeO2-NPs in the UV
region proves the applicability of this product in such medical
application such as sun-screen protectors or antiseptic in
ointments.
The CeO2-NP is a kind of typical calcium fluoride (CaF2)
structure with space group Fm3m. Fig. 4 portraits the PXRD
patterns of calcined CeO2-NPs in different temperatures that
were synthesized in the honey substrate. The same crystalline
Fig. 1. Lab photo of honey-based synthesized CeO2-NPs at different calcina-
tion temperatures.
Fig. 2. TGA–DTA curves of initial resin from 20 to 800 1C.
Fig. 3. UV–vis spectrum and band gap estimation (inset) of C3.
Fig. 4. PXRD patterns of honey-based synthesized CeO2-NPs in air at
different temperatures.
M. Darroudi et al. / Ceramics International 40 (2014) 7425–7430 7427

4. structure for all samples was observed. All of the detectable
Bragg0
s peaks with Miller indices (111), (200), (220), (311),
(222), (400), (331), (420), and (422) can be indexed as the
fluorite cubic structure (JCPDS #00-043-1002). The full width
at half maxima for all the peaks of the samples were broader
due to the combined effect of small crystal dimension and
associated relatively higher crystal lattice strain and defects
[36]. The broadening of the PXRD peaks also indicates that the
crystallite sizes of obtained CeO2-NPs are below 50 nm,
according to the literature [37] and this result impresses that
the size of the obtained samples are small, as confirmed by the
FESEM images of C3 in different magnifications (Fig. 5). After
the as-prepared CeO2-NPs was calcined from 200 to 800 1C
for 2 h, PXRD peaks become sharper with increasing calcina-
tion temperatures and FWHM decreased, indicating that the
crystallinity of CeO2-NPs are accelerated by the calcination
process. No peaks from possible intermediate phases, such as
Ce(OH)4/Ce(OH)3 was detected in PXRD patterns for the
prepared CeO2-NPs in different calcination temperatures,
indicating that the final samples were pure. Fig. 5 illustrates
Fig. 5. FESEM images at different magnification (A: 5, B: 50, and C: 130 K Â ) of C3.
Fig. 6. The Energy dispersive spectrum of C3.
M. Darroudi et al. / Ceramics International 40 (2014) 7425–74307428

5. the FESEM images of C3 in high magnifications. It is evident
from the images that obtained CeO2-NPs were small in size
($23 nm) and uniform in shape. The elemental composition
of the C3 was investigated by energy dispersive spectroscopy
(EDS) taken during FESEM analyses and is displayed in
Fig. 6. The EDS result shows cerium and oxygen atoms in the
specimen in a ratio close to 1:2 indicating the presence of
CeO2 in the sample.
Fig. 7 shows FT-IR spectral features of CeO2-NPs (C3). Strong
intense bands at 3408, 2922, 2850, 2372, 2343 cm–1
and below
700 cm–1
were observed. The intense bands at 3408 and
1611 cm–1
correspond to the ν(O–H) mode of (H-bonded) water
molecules and δ(OH), respectively [38]. Residual water and
hydroxyl groups are usually detected in the as-prepared CeO2-
NPs and further heat treatment is necessary for their elimination.
The FT-IR spectra of CeO2-NPs in the 1300–400 cm–1
region
have shown vibrations at 516 cm–1
, which is a characteristic
phonon mode for cubic cerium oxide [39]. The peak correspond-
ing to the Ce–O stretching is observed at 420 cm–1
and the bands
at 1054 and 1350 cm–1
are due to ν(Ce–O–Ce) vibration [40].
The band at 1078 cm–1
is assigned to the first overtone of the
fundamental vibration [39] at $520 cm–1
. The FT-IR spectrum
of the CeO2-NPs also exhibits a band below 700 cm–1
which is
due to the δ(Ce–O–C) mode [41]. The hydroxylation and
deprotonation of metal ions can be accelerated by raising the
solution temperature or pressure [42]. A sharp band at 1384 cm–1
is indicative of N¼O stretching vibration. This peak indicates
traces of nitrate [43].
The results of in vitro cytotoxicity studies, ranging from 0 to
100 μg/mL, after 24 h of incubation with different concentra-
tions of nanoparticles, are represented in Fig. 8. As the results
showed, for concentration above 25 μg/mL the metabolic
activity was decreased in a concentration dependent manner
meaning that metabolic activity started to decrease from 25 μg/
mL and reached its maximal decreasing in 100 μg/mL.
4. Conclusion
A food-directed, facile, eco-friendly and economically
feasible synthetic method has been applied for the synthesis
of CeO2-NPs via sol–gel route by using aqueous honey
solutions. From PXRD results, it was observed that all the
calcinations of CeO2-NPs at different temperatures exhibited
the high purity with the calcium fluoride (CaF2) structure. The
typical band gap was estimated from UV–vis spectrum and
was obtained to be about 3.5 eV and is higher than the bulk
experimental value. This method is interesting to apply and
extend the green chemistry rules in the preparation of
nanoparticles such as simple and low cost synthesis in a
normal atmosphere without any special physical conditions. It
is expected that these nanoparticles have the potential applica-
tions in different fields especially medicinal applications such
as cosmetics, sun-screen protectors, and as antiseptic in
ointments.
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