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Food Hydrocolloids
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a r t i c l e i n f o a b s t r a c t
Article history: In this study, different concentrations of savory essential oil (0.5, 1, and 1.5%) were incorporated into
Received 25 February 2014 agar-based nanocomposite films as active packaging in order to evaluate their physical, mechanical, and
Accepted 25 September 2014 antimicrobial properties. X-ray diffractometry (XRD) and scanning electron microscopy (SEM) were
Available online 18 November 2014
performed to explain the structural properties and morphology of these films. Incorporation of savory
essential oil (SEO) into nanocomposite films decreased tensile strength and Young's modulus, but
Keywords:
increased the percent elongation at break. In addition, water solubility decreased when SEO was
Nanocomposite film
incorporated into the films, whereas it did not significantly affect water vapor permeability. The films
Agar
Savory essential oil
containing SEO were more effective against gram-positive bacteria (Listeria monocytogenes, Staphylo-
Antimicrobial activity coccus aureus and Bacillus cereus) than gram-negative bacteria (Escherichia coli). Results suggested that
Active packaging the agar-based nanocomposite films containing SEO can be used as active packaging for improving the
safety and shelf-life of foodstuff.
© 2014 Elsevier Ltd. All rights reserved.
1. Introduction Yu, Jin, Zhang, & Liu, 2008; Wu, Geng, Chang, Yu, & Ma, 2009).
Due to its thermoplastic, biocompatible, biodegradable, and mod-
In recent years, consumers greatly demand for the higher erate water resistance, agar has been tested as an alternative source
quality and longer shelf-life of foodstuff. One of the main ways for for petroleum plastic packaging materials (Rhim, 2011). However,
protecting foods and extending their shelf-life during storage and agar films have some poor physical, mechanical, and thermal
distribution is the usage of active packaging (Rhim, 2013). Various properties that are needed for food packaging applications (Rhim &
natural components have been utilized for the preparation of edible Ng, 2007). Nowadays, the application of nanotechnology to
films; but, among these materials, polysaccharides, because of their biopolymer films may open new possibilities for improving not
excellent mechanical and structural properties and poor barrier only their properties but also the cost-price efficiency (Espitia et al.,
capacity against moisture transfer, have been extensively used for 2012; Rhim & Ng, 2007). In this regard, different nanoparticles have
the development of biodegradable films (Phan, Debeaufort, Luu, & been used as the reinforcement for the preparation of nano-
Voilley, 2005). composite films, among which, cellulose nanowhiskers or cellulose
Agar (AG) is an unbranched polysaccharide extracted from the nanocrystals, owing to their high tensile strength and modulus,
marine algae of class Rhodophyceae such as Gelidium sp. and Gra- have attracted significant interest as potential nanoreinforcements
nez, Lo
cilaria sp. (Gime pez de Lacey, Pe
rez-Santín, Lo
pez-Caballero, during the last decade (George & Siddaramaiah, 2012). Because of
& Montero, 2013). The most important attribute of agar is its ability the reinforcement provided by the nanoparticles dispersed in the
to form hard gels at very low concentrations (0.04%); also, it has polymer matrix, nanocomposite-based films exhibit markedly
been broadly utilized as a gelling agent in processed foods, phar- improved mechanical, physical, thermal, and optical properties
maceutical products, cosmetics, biotechnology, and medicine (Li, compared to pure biopolymer-based films (Rhim & Ng, 2007).
Another strategy for improving the functionality of biopolymer-
based films in packaging is their activation using various types of
* Corresponding author. Tel.: þ98 122 6254986; fax: þ98 122 6253499. additives such as antimicrobials in order to extend the shelf-life of
E-mail address: rezai_ma@modares.ac.ir (M. Rezaei). foods (Quilaqueo-Gutie rrez, Echeverría, Ihl, Bifani, & Mauri, 2012).
http://dx.doi.org/10.1016/j.foodhyd.2014.09.037
0268-005X/© 2014 Elsevier Ltd. All rights reserved.
M. Atef et al. / Food Hydrocolloids 45 (2015) 150e157 151
Nowadays, there is a preference for the use of natural active anti- SEO was added to the mixture at 0.5, 1, and 1.5% concentrations and
microbials, instead of synthetics such as plant extracts, for the homogenized by Ultra-Turrax (Wiggen Hauser, D-500, Germany) at
purpose of food preservation. 7000 rpm for 2 min (Ojagh, Rezaei, Razavi, & Hosseini, 2010). In
Antibacterial activity of extracts and essential oils of herbs and order to remove the dissolved air, the solution was degassed by
species can be attributed to their high content of phenolic com- slow stirring. Then, it was cast into Petri dishes and dried in an oven
pounds (Alizadeh et al., 2010; Mihajilov-Krstev et al., 2009). Sat- (40 C) for 24 h. After the removal of excess water, the samples were
ureja hortensis (summer savory) belonging to the Lamiaceae family peeled off from the Petri dishes and stored in a closed reservoir
is an annual and aromatic herb that is widely distributed in many prior to characterization. All the films were preconditioned in the
parts of the world. Summer savory is most often used as a culinary desiccators containing saturated magnesium nitrate solution at
herb; but, it also has marked medicinal benefits. The whole herb, 25 C and 52.89% relative humidity prior to testing.
especially the flowering shoots, is antiseptic, aromatic, carminative,
digestive, expectorant, and stomachic (Hadian, Ebrahimi, & Salehi, 2.4. Characterization
2010). Composition of oils from S. hortensis has been also investi-
gated. Major components of savory are carvacrol (>55%), p-cymene 2.4.1. X-ray diffractometry (XRD)
(1.95% and 12.30%), and g-terpinene (0.71% and 20.94%). In addition XRD measurements were performed using Philips X'Pert MPD
to these compounds, smaller amounts of a-terpinene and terpinene diffractometer (Eindhoven, Netherlands) by Co Ka radiation and X-
have been determined (Tozlu et al., 2011). ray wavelength of 1.54 nm at 40 kV and 30 mA. Nanocomposite
So far, a vast number of studies have been published about the films were analyzed between 2q ¼ 5 and 40 with the angle size of
preparation of nanocomposite films; but, only a few studies 2q ¼ 0.02 at speed of 1 /min at room temperature.
(Abdollahi, Rezaei, & Farzi, 2012; Alboofetileh, Rezaei, Hosseini, &
Abdollahi, 2014; Tunc & Duman, 2011) have been performed on 2.4.2. Scanning electron microscopy (SEM) analysis
the characteristic of functional bionanocomposite films. Further- Scanning electron microscopy (Philips XL 30) was used to
more, to the best knowledge of the present authors, no compre- examine the surface of agar/cellulose nanocomposite films with
hensive research has studied the effect of savory essential oil (SEO) and without SEO. The pieces were cut from the films, held by an
concentrations on the properties of agar nanocomposites in the aluminum tape, and sputtered by gold in a BAL-TEC SCD 005 sputter
film form for food packaging. coater (BAL-TEC AG, Balzers, Liechtenstein). All the specimens were
Thus, the focus of the present study was to prepare functional examined by a scanning electron microscope (Philips, Eindhoven,
nanocomposite films from agar reinforced with cellulose nano- Netherlands) under high vacuum condition at the accelerating
particles and comprehensively evaluate the effect of SEO on the voltage of 20.0 kV.
properties of agar-based nanocomposite films such as physical,
mechanical, microstructure, and optical attributes as well as anti-
2.4.3. Film thickness
microbial activity against Listeria monocytogenes, Staphylococcus
Film thickness was measured by a manual digital micrometer
aureus, Bacillus cereus, and Escherichia coli bacteria.
(Mitutoyo, Mizonokuchi, Japan) with sensitivity of 0.001 mm, at 10
random positions for each film. The mean value was used in tensile
2. Materials and methods
strength and water vapor permeability calculations.
2.1. Materials
2.4.4. Film solubility in water
To determine the percentage solubility of the films in water, the
Food grade agar, Glycerol, and Tween 80 were obtained from
procedure proposed by Tunc et al. (2007) was used. At first, the
Merck Co. Germany. Savory essential oil (S. hortensis) supplied from
specimens (4 cm 4 cm) were dried at 105 C for 24 h to measure
Barij Co. (Kashan, Iran) and stored in dark container at 4 C until
initial dry matter (Wi). Then, the dried nanocomposite films were
used. For antimicrobial assays, Brain Heart Infusion Broth (BHI) and
immersed in 50 mL of distilled water for 24 h at room temperature.
Tryptic Soy Agar (TSA) were purchased from Quelab, Canada.
At the end of 24 h, the unsolubilized films were filtered using a
Whatman No. 1 filter paper. The remaining pieces of the samples
2.2. Bacterial strains and maintenance
after immersion were dried at 105 C for 24 h to the constant final
dry weight (Wf). Values of water solubility (%) were determined in
All the stock cultures such as L. monocytogenes (PTCC 1298), E.
triplicate for each treatment and calculated using the following
coli (PTCC 1330), B. cereus (PTCC 1154), and S. aureus (PTCC 25923)
equation:
were obtained from Persian Type Culture Collection (Tehran, Iran).
All the strains were reserved in Brain Heart Infusion Broth (BHI) .
with the supplement of 30% glycerol and stored at 20 C until use.
Solubility in water % ¼ Wi Wf 100 Wi (1)
Subculturing was performed on a monthly basis to preserve bac-
terial viability. 2.4.5. Water vapor permeability (WVP)
WVP values of the nanocomposite films were determined using
2.3. Preparation of antimicrobial films a modified ASTM method E96-92, as described by Rhim (2011). The
samples were cut into circles and sealed on top of the permeation
Agar film solution was prepared by dissolving 1.5 g of AG in cells containing 10 cc of distilled water (100% RH; 2.337 103 Pa
100 mL of distilled water under vigorous mixing at 95 C for 30 min. vapor pressure at 20 C). Then, the cells were stored in a desiccator
Glycerol was used as a plasticizer at 33% content based on dry agar containing silica gel to provide constant RH at 20 C. Afterward, the
film (Tian, Xu, Yang, & Guo, 2011). In order to reduce aggregation amount of water vapor transferred through the films was measured
and good dispersion of nanoparticles, the suspension of nano- using weight loss of the cell for the period of 8 h. WVP (1010 g/
crystalline cellulose (NCC) was sonicated for 5 min, then dispersed ms Pa) of the films was measured by the following equation:
in the agar solution and stirred by a magnetic stirrer for 2 h. Af-
terwards, Tween 80, as an emulsifier, was added to the film solution
at the level of 0.2% of essential oil. After stirring at 50 C for 30 min, WVP ¼ W$X=A$t$DP (2)
152 M. Atef et al. / Food Hydrocolloids 45 (2015) 150e157
Where W is weight gain of the cell (g), X is average film thickness qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
*
(m), and A, t, and DP are area of exposed film (m2), time (s) and
2 2
Cab ¼ a* þ b* (6)
differential of partial water vapor pressure (Pa), respectively.
Average value of three replicates for each sample was also obtained.
b*
h*ab ¼ 180 þ arctg When a < 0 (7)
a*
2.4.6. Water contact angle (CA) measurement
Light barrier properties of the film samples were measured by
Contact angle measurements of water on the surface of nano-
scanning the samples at wavelengths between 200 and 800 nm
composite films were carried out using a PG-X goniometer (Model
using a UVevisible spectrophotometer. Also, the opacity of the
PG-X, Switzerland). A water drop (5 mL) was placed on the film
agar-based nanocomposite films (with the dimension of 1 4 cm)
surface with the dimensions of 2 cm 5 cm using a microsyringe at
was evaluated by measuring absorbance at 600 nm using a UV/VIS
room temperature. Reported values were the averages of five rep-
spectrophotometer (Model UNIC 4802 UV/VIS Double Beam, China)
licates observed on different spots of the samples.
according to the method by Alboofetileh, Rezaei, Hosseini, and
Abdollahi (2013). Opacity of the samples was calculated using the
2.4.7. Swelling index following equation:
Kinetic test of swelling was evaluated by periodically measuring
weight increase of the sample films according to the method by Opacity ¼ Abs600 =X (8)
Lavorgna, Piscitelli, Mangiacapra, and Buonocore (2010). Film
specimens with the dimension of 2 2 cm were put into a desic- Where Abs600 is a value of absorbance at 600 nm and X is the film
cator (containing silica gel) for one week and weighed. Then, the thickness (mm).
samples were immersed in the closed beakers containing 50 mL of
distilled water and stored at room temperature. Before each time of 2.5. Microbiological analysis
weighing, the surface of all the film samples was dried by a filter
paper in order to remove the surface adsorbed water and weighing 2.5.1. Evaluation of antimicrobial activity of essential oil,
was continued until reaching the equilibrium state at the selected nanocomposite films, and film solutions
times. Swelling of the films was calculated using the following For this purpose, 10 ml of 106 (CFU)/ml of each bacterial strain (L.
equation: monocytogenes, S. aureus, B. cereus, and E. coli) was spread on tryptic
soy agar (TSA) by steel swab, which was cultured for 24 h in brain
Swelling ð%Þ ¼ ðWeight of wet film Weight of dry filmÞ heart infusion broth (Quelab, Canada) at 37 C (108 CFU/ml). 40 ml of
100=Weight of dry film (3) SEO for well test (6 mm diameter) and sterile filter paper discs
(6 mm in diameter, Whatman no.1) impregnated with 10 ml of
essential oil were used for disc diffusion. For disc diffusion and
2.4.8. Visco analyzer vapor-phase diffusion methods, circular pieces of different films
A Brookfield digital viscometer (Model LVDV-II þ P, USA) with (1.5 cm in diameter) were placed on the surface of TSA and on the
SC4-31 spindle was used to determine the rheological characteristic lids of TSA plates, respectively. Also, for determining the antimi-
of agar-based nanocomposite suspension containing various con- crobial activity of the film solutions, 40 ml of different film-forming
centrations of savory essential oil at the speeds of 6, 10, 12, 20, 30, solutions was added to TSA wells (6 mm in diameter). All the plates
50, 60, and 100 rpm before casting. Measurement was carried out in were incubated at 37 C for 24 h. After incubation, the microbial
about 15 mL of the film solution at 50 C. growth and inhibition degree of essential oil were illustrated as
follows: þþþ: totally inhibited; þþ: partially inhibited; þ: slightly
inhibited; -: no inhibition (Go mez-Estaca, Lo pez de Lacey, Lo pez-
2.4.9. Mechanical properties of the films
Caballero, Go mez-Guille n, & Montero, 2010). Also, the inhibition
Tensile strength (TS), Young's modulus (YM), and elongation at
break (E%) of the nanocomposite films were evaluated by a Uni- zones surrounding the film areas were reported for disc diffusion
versal Testing Machine (Model TVT-300Xp, Perten, Sweden). (Ojagh et al., 2010); but, for vapor-phase diffusion, the whole zone
Measurements were performed according to ASTM standard area was measured as “zone of inhibition” according to Lo'pez-
Caballero, Go'mez-Guille n, Pe'rez-Mateos, and Montero (2005).
method D 882-02 (ASTM, 2002). The film samples were prepared in
rectangular pieces (2.54 cm 10 cm) and their thickness was
measured at 10 points. The films were then stretched with 50 mm 2.6. Statistical analysis
of initial grip separation and 5 mm min1 of cross-head speed.
Mechanical properties of the samples were also measured for five Analysis of variance (ANOVA) followed by Duncan's multiple
times and average of the results was calculated. range test was used to determine any significant differences among
the treatments at 95% confidence level (p 0.05) and all the data
were reported in the form of mean ± SD.
2.4.10. Color, light transmission, and opacity measurements
Lightness (L), redness (a), and yellowness (b) color system was
3. Results and discussion
used to evaluate the color of films by a colorimeter (BYK Gardner,
USA). Measurements were performed on white standard back-
3.1. X-ray diffractometry (XRD)
grounds (L* ¼ 94.41, a* ¼ 0.78, b* ¼ 0.51) and color difference (DE),
whiteness index (WI), chroma (Cab * ), and hue (h* ) were calculated
ab XRD spectra of the agar/cellulose nanocomposite films with and
using the following equations:
without essential oil are presented in Fig. 1. As can be seen from
qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi XRD graph, pure agar film showed two characteristic crystallinity
2 2 2
DE ¼ ðL* LÞ þ ða* aÞ þ ðb* bÞ (4) peaks at 2q ¼ 11.27 and 23.01 which was also observed in the
nanocomposites. When NCC incorporated in the agar matrix, a new
qffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi angle of diffraction peak was generated at 2q ¼ 26.27. This dif-
2
WI ¼ 100 ð100 L* Þ þ a*2 þ b*2 (5) fractograms suggested that NCC reinforced agar films as well as the
M. Atef et al. / Food Hydrocolloids 45 (2015) 150e157 153
Fig. 2. Scanning electron microscopic images of surface of agar/cellulose nanocomposite films: (a) Control, (b) agar/cellulose nanocomposite with 0.5% (v/v) SEO, (c) agar/cellulose
nanocomposite with 1% (v/v) SEO and (d) agar/cellulose nanocomposite with 1.5% (v/v) SEO.
154 M. Atef et al. / Food Hydrocolloids 45 (2015) 150e157
Table 1
Physical and mechanical properties of agar-based nanocomposite films with SEO.
Control 0.073 ± 0.00 29.68 ± 1.30b 1.60 ± 0.01c 55.76 ± 4.20b 31.21 ± 0.80a 51.73 ± 2.27a 62.00 ± 2.79c
SEO 0.5% 0.088 ± 0.01 29.67 ± 1.97b 1.53 ± 0.13c 62.99 ± 3.72a 28.26 ± 0.82b 46.17 ± 2.83b 66.13 ± 0.65b
SEO 1% 0.089 ± 0.01 24.80 ± 2.84ab 1.82 ± 0.12b 57.02 ± 2.45b 28.13 ± 1.64b 49.38 ± 3.08ab 72.87 ± 2.61a
SEO 1.5% 0.107 ± 0.00 23.54 ± 3.96a 2.34 ± 0.13a 46.50 ± 4.24c 20.38 ± 1.67c 51.67 ± 4.87a 69.35 ± 1.45ab
Values within each column with different letters are significantly different (p < 0.05).
Table 2
Color parameters of nanocomposite films with SEO.
Control 90.30 ± 0.21a 1.10 ± 0.04a 5.00 ± 0.16d 6.10 ± 0.26c 89.03 ± 0.25a 5.12 ± 0.15d 178.65 ± 0.01a
SEO 0.5% 88.60 ± 0.32ab 1.17 ± 0.12b 7.68 ± 0.38c 9.24 ± 0.40b 86.20 ± 0.37b 7.77 ± 0.38c 178.58 ± 0.01a
SEO 1% 88.85 ± 0.06a 1.33 ± 0.06a 8.54 ± 0.05b 9.78 ± 0.02b 85.89 ± 0.02b 8.65 ± 0.06b 178.58 ± 0.01a
SEO 1.5% 88.09 ± 0.50b 1.64 ± 0.03b 10.66 ± 0.78a 11.99 ± 0.92a 83.93 ± 0.88c 10.79 ± 0.77a 178.58 ± 0.01a
Means (n ¼ 3) with different letters within the same column indicate significant differences (p < 0.05).
Fig. 5. Effect of SEO on (a) opacity and (b) light transmission of agar/cellulose nanocomposite films.
156 M. Atef et al. / Food Hydrocolloids 45 (2015) 150e157
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