Food Control 84 (2018) 312e320

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Food Control
journal homepage: www.elsevier.com/locate/foodcont

Antimicrobial and antioxidant efficiency of nanoemulsion-based

edible coating containing ginger (Zingiber officinale) essential oil and
its effect on safety and quality attributes of chicken breast fillets
Soheila Noori, Fariba Zeynali*, Hadi Almasi
Department of Food Science and Technology, Faculty of Agriculture, Urmia University, PO Box 57561-51818, Urmia, Iran

a r t i c l e i n f o a b s t r a c t

Article history: Nanoemulsion-based edible sodium caseinate coating containing ginger essential oil (GEO) (3 and 6% wt)
Received 26 April 2017 was applied onto chicken breast fillet to extend its shelf life. GC-MS analysis showed that the most
Received in revised form components of GEO were a-zingiberene (24.96%) and then b-sesquiphellandrene (12.74%). Comparison
26 July 2017
between conventional emulsion and nanoemulsion-based coatings was applied by particle size, poly-
Accepted 13 August 2017
dispersity index and z-potential analyses. Antibacterial potential of active coatings was more than their
Available online 16 August 2017
antioxidant activity and it was significantly (p < 0.05) increased when nanoemulsion was fabricated.
Nanoemulsion based edible coatings with 6% of GEO nanoemulsion caused to significant decrease of total
Keywords:
Chicken breast
aerobic psychrophilic bacteria of refrigerated chicken fillets during 12 days. The effect of GEO on TBARS
Edible coating levels of fillets was not significant. The lowest color difference and cooking loss were obtained for
Ginger essential oil nanoemulsion coated samples. The highest total acceptance was recorded for coated fillets with 6% of
Nanoemulsion GEO nanoemulsion during storage. Generally the GEO nanoemulsion was more effective than its con-
Shelf life extension ventional emulsion in extending the durability of chicken breast fillets.
© 2017 Elsevier Ltd. All rights reserved.
Chemical compounds studied in this article:
Glycerol PubChem CID: 753
Tween 80 PubChem CID: 5281955
Chloramphenicol PubChem CID: 5959
Gentamicin C1 PubChem CID: 72395
Methanol PubChem CID: 887
2,2-diphenyl-1- picrylhydrazyl (DPPH)
PubChem CID: 74358
2-thiobarbituric acid PubChem CID:
2723628

1. Introduction using novel preservation methods (Latou et al., 2014).

The consumption of poultry meat has increased over the last
decades due to the relatively low cost of production as compared to
meat products, low fat content, high nutritional value and distinct
flavor (Latou, Mexis, Badeka, Kontakos, & Kontominas, 2014).
However, high moisture and protein content and high pH value,
transform the poultry meat to a susceptible product for growth of
spoilage and pathogenic microorganisms (Kerry, O’Grady, & Hogan,
2006). Nowadays, a serious challenge for the poultry industry is the
shelf life extension of raw poultry meat. The short shelf life of the
chicken meat (approximately 4e5 days) reveals the necessity of
* Corresponding author.
E-mail address: f.zeynali@urmia.ac.ir (F. Zeynali).
Antimicrobial edible coating is one new approach to control
microbial growth and thus, improving safety and delaying spoilage
of meat, fish and poultry products (Umaraw & Verma, 2017).
Essential oils (EOs), are aromatic and volatile oily extracts obtained
from plant materials, including flowers, buds, roots, bark, and
leaves by means of expression, fermentation, extraction or steam
distillation. EOs are commonly utilized as flavoring agent in food-
stuffs. They are also known as a class of natural preservatives
because their strong antimicrobial and antioxidant properties have
been demonstrated in previous investigations (Jayasena & Jo, 2013).
Consumers’ growing concern over the safety of synthetic chemical
preservatives has led to the increase of tendency to the utilization
of EOs as antioxidant and antimicrobial agents in food industry
(Viuda-Martos et al., 2010).

http://dx.doi.org/10.1016/j.foodcont.2017.08.015
0956-7135/© 2017 Elsevier Ltd. All rights reserved.
 S. Noori et al. / Food Control 84 (2018) 312e320
A variety of antimicrobial edible coatings containing EOs have
been developed for fresh poultry, red meat and fish products.
Studies on the effect of chitosan-based coating containing cinna-
mon EO on rainbow trout (Ojagh, Rezaei, Razavi, & Hosseini, 2010),
soy protein-based coating enriched with thyme and oregano EOs
on fresh ground beef patties (Emirog lu, Yemiş, Coşkun, &
Candog an, 2010), whey protein isolate (WPI)-based coating
loaded with oregano and clove EOs on chicken breast fillet
(Ferna ndez-Pan, Carrio  n-Granda, & Mate , 2014) and chitosan-
based coating incorporated with orange peel EO on deepwater
pink shrimp (Alparslan & Baygar, 2017) are examples for using of
EO activated edible coatings in meat industry.
However, adding EOs into edible coatings can increase the
opacity thus affecting the appearance of products. The main reason
of this effect is that the dispersion of EOs within aqueous-based
products is rather difficult due to their low-water solubility. Thus,
large particulate structures will be formed that causes to scatter
visible light. In addition, the volatile nature of EOs causes their
significant loss during coating process and storage (Ma et al., 2016).
More researches are focused on improving the properties of anti-
microbial coatings with EOs. Nanoemulsion-based colloidal sys-
tems are used to improve properties of EO loaded coating solutions.
Oil-in-water nanoemulsions consist on lipid nano droplets (be-
tween 10 and 100 nm diameter) dispersed in an aqueous solution
(McClements, 2011). The advantages of nanoemulsions are include:
more transparency, enhanced physicochemical properties, more
stability, masking the taste or smell of core material and thus lower
effect on organoleptic properties of food, improved biological ac-
tivity of EO by increasing the surface area allows using lower doses
of EO (McClements & Rao, 2011). Recently, some researches have
been reported on the using of active edible coating containing EO-
loaded nanoemulsions for shelf life extension of green beans (Donsì
et al., 2015; Severino et al., 2015, 2014), fresh-cut Fuji apples (Salvia-
Trujillo, Rojas-Graü, Soliva-Fortuny, & Martín-Belloso, 2015), fish
fillets (Wu et al., 2016) and low-fat cheese (Artiga-Artigas, Acevedo-
Fani, & Martín-Belloso, 2017).
Ginger, the root of the plant Zingiber officinale Rosc. is one of the
most commonly used spices around the world. The EOs of ginger
(GEO) have been reported to have strong antimicrobial, antifungal
and antioxidant activities (Singh et al., 2008; El-Baroty, Abd El-
Baky, Farag, & Saleh, 2010). The main chemical compounds of
GEO are a-zingiberene, camphene, ar-curcumene and b-sesqui-
phellandrene (Singh, Maurya, Catalan, & de Lampasona, 2005).
There are a few reports about the using of GEO in preparation of
active films (Atare s, Bonilla, & Chiralt, 2010a; Atare s, De Jesús,
Talens, & Chiralt, 2010b; Tongnuanchan, Benjakul, & Prodpran,
2013). But its direct addition to a food or application in the
formulation of an edible coating for real food commodities is not
yet reported. Sodium caseinate (SC) is a low cost and available
water-soluble biopolymer obtained by the acid precipitation of
casein, the main protein in cow’s milk (Audic & Chaufer, 2005). SC
has a good film forming ability due to the potential of formation of
hydrogen bonding, electrostatic interactions and hydrophobic
forces (McHugh & Krochta, 1994). SC-based edible coatings are
attractive for food applications due to their high nutritional quality,
excellent sensory properties, good transparency, high water vapor
and gas barrier properties and potential to provide food products
with adequate protection from their surroundings (Kristo,
Koutsoumanis, & Biliaderis, 2008).
The efficacy of various edible coatings on the shelf life of chicken
meat have been evaluated by a number of researchers (Ferna ndez-
Pan et al., 2014; Latou et al., 2014; Seol, Lim, Jang, Jo, & Lee, 2009),
however, no definite data exist on the application of SC-based
edible coating in chicken meat products. Moreover, despite of
approving the drastically elevated antioxidant and antimicrobial
313
activity of EOs as a result of nanoemulsion formation in the liter-
ature, to the best of our knowledge, there are no reports on the
preparation of GEO nanoemulsions-loaded edible coating. Addi-
tionally, any former study has not used GEO for preservation of
chicken meat. The objective of the present work was to study the
effect of SCbased edible coating containing GEO nanoemulsions to
extend the shelf-life of fresh chicken breast fillets stored at 4
C.
Chemical composition, antioxidative and antimicrobial behaviors
of GEO were determined. After that, the influence of edible coatings
formed from conventional emulsions compared with nano-
emulsions on the quality attributes of chicken fillet was assessed in
order to establish a possible enhancement of GEO functionality due
to the reduced droplet size.
2. Materials and methods
2.1. Materials
The mature and healthy rhizomes of ginger (Zingiber officinale)
were purchased from the local market of Urmia, Iran. Food-grade
and spray dried sodium caseinate (protein content > 80%) (ob-
tained from Caragum Parsian, Tehran, Iran) was used for the coating
formulations. Fresh chicken breast fillets were provided by a local
poultry processing plant (Morghe Khanegi Co., Urmia, Iran) within
one hour after slaughter in insulated polystyrene boxes on ice.
Glycerol, and other reagents used were of analytical grade and were
purchased from Merck (Darmstadt, Germany).
2.2. Extraction and identification of the ginger essential oil
The fresh ginger rhizomes were properly washed and thinly
grated and were subjected to hydrodistillation for 4 h in the glass
Clevenger-type tool according to the method recommended by the
European Pharmacopoeia (Singh et al., 2008). The obtained light
yellow colored oil with a pleasant odor, was dried over anhydrous
sodium sulfate and stored in sealed vials at 4
C for GC/MS analysis.
GC-MS analyses were carried out on an Aglient 8690N GC-MS
system (USA) equipped with HP-5MS capillary column (phenyl
methyl siloxane, 30 m  0.25 mm i.d  25 mm). Oven temperature
was held at 60
C for 5 min and then programmed to 250
C at a rate
of 3
C/min and kept constant at 250
C for 10 min. Injector and
detector temperature was adjusted to 260
C and helium was used
as carrier gas at a flow rate 1.5 ml/min. Ionization voltage of mass
spectrometer in the EI-mode was equal to 70 eV and ionization
source temperature was 250
C. The compounds were identified by
comparison of retention indices (RI, HP-5) with those reported in
the literature and by comparison of their mass spectra with the
Wiley GC/MS Library, Mainlib Library and Replib Library data
published mass spectra data (El-Baroty et al., 2010).
2.3. Preparation and characterization of nanoemulsion
2.3.1. Nanoemulsion preparation
GEO nanoemulsion was formulated according to the method of
Ghosh, Mukherjee, and Chandrasekaran (2013) with some modi-
fications. Non-ionic surfactant Tween80 (HLB ¼ 15) and distilled
water were used for preparation of nanoemulsion. Concentration of
GEO (5% v/v) and Tween80 (30% wt of GEO) were fixed for both of
emulsion and nanoemulsion formulations. Coarse emulsion was
prepared by gradually and continuous adding of GEO and surfactant
to water with shaking at 3000 rpm. Then, the coarse emulsion was
subjected to ultrasonic emulsification using a 20 kHz Sonicator
(OPTIMA, XL100K, Germany). The operation power was adjusted to
200 W and a sonotrode containing a piezoelectric crystal with a
probe diameter of 15 mm was applied. Sonicator probe was
314 S. Noori et al. / Food Control 84 (2018) 312e320
symmetrically dipped into coarse emulsion in depth of 25 mm, and
the sonication process was carried out for 5 min. The temperature
difference between initial coarse emulsions to final nanoemulsion
was less than 10
C. Then, the coarse emulsion and formulated
nanoemulsion were characterized in room temperature.
2.3.2. Measurement of particle size and z-potential
The DeBroukere mean diameter (D43) and polydispersity index
(PDI) of GEO emulsion and nanoemulsion were determined ac-
cording to the method of Hosseinnia, Alizadeh Khaledabad, and
Almasi (2017). Dynamic light scattering (DLS) technique employ-
ing a Zetasizer Nano-ZS (Malvern instruments, Worcestershire, UK)
was used. All measurements were carried out at 25
C. z-potential
of emulsion and nanoemulsion for determination the surface
charge of droplets was also measured at 25
C.
2.4. Preparation of coating solutions
The 4 g SC were dissolved in 100 ml distilled water and stirred at
a controlled temperature of 30
C and 1100 rpm for 3 h. 1.2 g (30%
wt of SC) glycerol was added as plasticizer. Then, GEO emulsion and
nanoemultion were added with constant stirring to reach final
concentration of GEO to 3 and 6% wt of SC. After 20 min stirring at
1100 rpm, the solutions were characterized and applied for coating
of chicken fillets.
2.5. Characterization of coating solutions
2.5.1. Antimicrobial activity
For determining the antimicrobial activity of coating solutions
containing GEO emulsion and nanoemulsion, an agar well diffusion
assay over two food pathogen microorganisms Listeria mono-
cytogenes (ATCC 19111), Salmonella typhimurium (ATTC 14028) was
carried out. The antimicrobial activity of coating solutions was
measured by paper disc method according to Seol et al. (2009). In
order to evaluate the stability of antimicrobial potential of active
coatings, in addition to fresh prepared coating solutions, this
experiment was carried out on coating solutions after 12 days of
storage at 4
C. Sterilized 8 mm diameter paper discs were placed
on the nutrient agar plates spread with pathogenic bacteria and
50 ml of coating solutions were dropped onto the paper discs
separately. Chloramphenicol and gentamicin antibiotics incorpo-
rated SC solutions (3% wt of SC) were also used as reference stan-
dards. The plates were then incubated at 37
C for 24 h.
Antimicrobial activity was evaluated by measuring the zone of in-
hibition against the tested microorganisms.
2.5.2. Antioxidant properties
The antioxidant activity of coating solutions was determined by
DPPH radical scavenging method as described by El-Baroty et al.
(2010) with some modifications. Different concentrations of
coating solutions (0.4e6.4 mg ml1) in 1 ml of methanol were
added to 25 ml of methanolic DPPH (100 mmol/L1) solution. The
mixtures were incubated in the dark at 25 ± 2
C for 30 min, then
the absorbance was measured at 517 nm against a blank (pure
methanol) by using a spectrophotometer (Unico, S 2100 SUV,
Dayton, NJ, USA). SC solution containing 3% wt of BHT was used as
reference standard. The coating solution concentration providing
50% inhibition (IC50) was calculated from a graph representing the
inhibition percentage against coating concentration. This test was
repeated after 12 days refrigerated storage of coating solutions in
order to assess the stability of their antioxidant potential.
2.6. Treatment of chicken fillets
Fresh chicken fillets were aseptically portioned into smaller
pieces weighing about 50 g. The prepared chicken fillets were
coated by dipping them into the prepared coating solutions for
2 min at room temperature, then drying for 2 min. The samples
coated with solutions containing 3 and 6% wt of GEO emulsion and
nanoemulsion were coded as SC-E3%, SC-E6%, SC-NE3% and SC-
NE6%, respectively. Pure SC solution was also used for coating
(SC). Moreover, a control sample coated with distilled water at
similar conditions was prepared (Control). All samples were placed
in polystyrene (PS) trays and wrapped with low density poly-
ethylene LDPE casing. The coated and control samples were kept
refrigerated at 4
C for 12 days. This storage time was selected ac-
cording to our pre-tests by evaluation of sensorial attributes and
microbial population of all treatments. Sampling was carried out on
days 1, 4, 8 and 12 of storage.
2.7. Chicken meat quality testing
2.7.1. Microbiological analyses
Counts of psychrophilic bacteria, molds and yeasts on chicken
fillets were determined during cold storage. Chicken fillet samples
(25 g) were transferred aseptically into individual stomacher bags
(Seward Medical, UK), containing 225 ml of sterile buffered pep-
tonewater (BPW) solution (0.1 g/100 ml) and homogenized in a
stomacher (Lab Blender 400, Seward Medical, UK) for 60 s. Serial
dilutions were made and 0.1 ml was spread over previously pre-
pared plate count agar (PCA) or chloramphenicol glucose agar
(CGA) and incubated at 4 ± 1
C for 10 days or for at 25 ± 1
C for 3
days for determination of psychrophilic bacteria and molds and
yeasts, respectively. Microbiological data were transformed into
logarithms of the number of colony-forming units (Log CFU/g).
2.7.2. Determination of thiobarbituric acid (TBA) value
Thiobarbituric acid reactive substances (TBARS) were deter-
mined as described by Song, Liu, Shen, You, and Luo (2011) using a
spectrophotometer (Unico, S 2100 SUV, Dayton, NJ, USA) at 532 nm.
TBARS content was expressed as mg of MDA/kg chicken meat.
2.7.3. Cooking loss measurements
The cooking loss was estimated as described by Barbanti and
Pasquini (2005). The percentage of weight loss relative to the
initial weight was calculated by weighing the samples after 1 h
cooking at water bath with temperature of 80
C.
2.7.4. Color properties
Color parameter values of fillets were determined by using a
Hunter Lab colorimeter (Minolta model CR-410, Japan). Color values
(L* (lightness), a* (red/green) and b* (yellow/blue)) of five random
points of each sample surface were determined and the average
values were used in calculation of total color difference (DE) ac-
cording to Eq. (1):
rffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
 2  2  2
DE ¼ L*  L*s þ a*  a*s þ b*  b*s (1)
where, L*s (55.66), a*s (1.89) and b*s (5.54) are color values of the
standard and fresh chicken fillet two hours after slaughter.
2.7.5. Sensory evaluation
Semi-trained 10 member panelists at department of food sci-
ence of Urmia University evaluated the total acceptance of samples
(Kilincceker, Dogan, & Kucukoner, 2009). All panelists had a back-
ground in meat evaluation and were selected based on their
 S. Noori et al. / Food Control 84 (2018) 312e320 315

sensitivity and limit detection of taste and smell of very low con- in main chemical compounds of GEO identified in other references.
centrations of GEO. The attributes considered in the sensory eval- For example, Singh et al. (2008) identified geranial (25.9%) as the
uation were appearance and color, odor and elasticity. A five point major constituent in ginger oil, but it was detected in trace amount
descriptive hedonic scale, where 5 ¼ like extremely and 1 ¼ dislike (0.34%) in our study. Aggrawal, Walia, Dhingra, and Khambay
extremely was used. A score of 3 was taken as the lower limit of (2001) reported that the fresh rhizomes of ginger contained cur-
acceptability. cumene as the major constituent. These differences are may be due
to genetic, age and stage of maturity, weather conditions, soil
2.8. Statistical analysis composition, plant organs, distillation conditions and some other
factors (Rehman, Hanif, Mushtaq, & Al-Sadi, 2016).
All assays were performed in triplicate. Statistics on a
completely randomized design were performed with the analysis of 3.2. Emulsion and nanoemulsion characterization
variance (ANOVA) procedure in SPSS (Version 21, SPSS Inc., Chicago,
IL, USA) software. Duncan’s multiple range test (p < 0.05) was used Mean droplet size of the emulsion and nanoemulsion and their
to detect differences among mean values of chicken fillets’ prop- PDI and z-potential are shown in Fig. 1. The droplet size of con-
erties in all test intervals. ventional emulsion was 167.3 ± 1.5 nm and was decreased about
three times to 57.4 ± 2.7 nm when nanoemulsion was prepared.
3. Results and discussion Similar results were reported by Ghosh et al. (2013) for basil oil
nanoemulsion formulated using Tween80 and water by ultrasonic
3.1. Chemical composition of ginger essential oil emulsification method. While, Severino et al. (2015) prepared
carvacrol and bergamot, mandarin and lemon EOs loaded nano-
The production yield of essential oil was 1.1%. The EO extracted emulsions using Tween 20 and reported mean droplet sizes in the
from rhizomes of Z. officinale showed the presence of 67 compo- range of 133.4e176.4 nm. These differences with our results indi-
nents that the 30 major compounds are shown in Table 1. All of the cate that Tween 80 is favorable for oil-in-water emulsions due to its
identified chemical compounds represented 94.87% of total GEO. higher hydrophilicelipophilic balance (HLB-15) than other poly-
The major organic compound detected in the essential oil, was a- sorbates (Ghosh et al., 2013). Some other researchers fabricated
zingiberene by concentration of 24.96% of all identified compounds. nanoemulsions by incorporation of EOs in the biopolymer solutions
The other main identified compounds were b-sesquiphellandrene such as sodium alginate (Acevedo-Fani, Salvia-Trujillo, Rojas-Graü,
(12.74%), sesquisabinene hydrate (6.19%), camphene (5.90%), zin- & Martín-Belloso, 2015; Artiga-Artigas et al., 2017; Salvia-Trujillo
giberenol (4.26%), (E)-citral (3.93%), sabinene (3.75%), (E)-farnesene et al., 2015) and chitosan (Wu et al., 2016) prior to sonication
(3.73%), and italicene (3.21%). Our results are in good agreement process. All of these researchers reported larger droplet sizes (in
with the findings of Singh et al. (2005) and El-Baroty et al. (2010) range of 169e490 nm) than that obtained in this research
who reported that b-sesquiphellandrene and a-zingiberene are (57.4 nm). Also, two or more main intensity peaks, were observed
the main constituents of GEO. However, there are major differences in the mentioned researches due to the aggregation of biopolymers.
But droplet size distributions were detected as monodisperse in the
coarse emulsion and nanoemulsion prepared in this research. It
Table 1
Chemical composition of Zingiber officinale (rhizomes) essential oil.
could be concluded that the Tween 80 as a small molecule sur-
factant is comparatively effective in minimizing droplet diameter
Compounds Concentration Retention time
than biopolymers due to its rapid adsorption onto droplet surface
(Peak area %) (min)
(Qian & McClement, 2011). Formation of a dense and thick layer on
Alpha-pinene 0.85 4.58 the surface of EO droplets as a result of using biopolymers, causes to
Camphene 5.90 4.88
Sabinene 3.75 6.32
increase the diameter of obtained droplets.
Borneol 0.99 8.72 As shown in Fig. 1, the PDI was also decreased after nano-
Z-citral 2.84 10.40 emulsion fabrication. GEO nanoemulsion presented the higher in-
Geraniol 0.58 10.62 tensity peak at the 57 nm region indicating that most of the
E-citral 3.93 11.10
Thymol 0.88 11.37
b-Elemene 0.65 13.31
Bicyclo 0.81 14.13
Trans-beta-farnesene 0.78 14.57
1,8-Cineole 1.59 15.27
a-Zingiberene 24.96 15.92
a-farnesene 2.63 15.98
(E)-farnesene 3.73 16.07
b-bisabolene 1.96 16.12
b-sesquiphellandrene 12.74 16.49
Elemol 2.31 16.90
Nerolidol 1.51 17.07
Germacrene 0.5 17.11
Sesquisabinene hydrate 6.19 17.66
1H-cycloprop 1.72 17.83
Zingiberenol 4.26 18.18
Valencene 1.41 18.32
b-eudesmol 1.62 18.94
Epizonarene 1.31 18.97
Aromadendrene 0.91 19.17
Italicene 3.21 19.60
Farnesa 2.48 19.70
Octadecadienoic acid 0.87 25.69
Fig. 1. Particle size distribution of the GEO emulsion and nanoemulsions fabricated by
Total 94.87
ultrasonication method.
316 S. Noori et al. / Food Control 84 (2018) 312e320

droplets had very small diameters after sonication. PDI was recor-
ded as 0.222 ± 0.032 for GEO nanoemulsion and was increased to
0.584 ± 0.056 when conventional emulsion was prepared. The
narrow intensity peak and the lower PDI of nanoemulsion
approved the efficiency of ultrasonication method in formation of a
uniformly size distributed nanoemulsion. Tang, Manickam, Wei,
and Nashiru (2012) reported that the lower ultrasonic frequency
and amplitude cause to decrease the PDI of aspirin loaded nano-
emulsions obtained by ultrasound emulsification method.
The z-potential values of GEO emulsion and nanoemulsion are
also presented in Fig. 1 z-potential determines the surface charge at
the interface of the droplets governed by the charge of surfactants
adsorbed around them, which can be of anionic, cationic or non-
ionic nature. Emulsions and nanoemulsions prepared in this
study contained a non-ionic surfactant (Tween 80); then, one
would expect an electrical charge close to zero. However, a negative
z-potential was recorded for both of them. GEO nanoemulsion
showed a larger z-potential (18.70 ± 1.32 mV) in comparison to
conventional emulsion (4.09 ± 1.00 mV). Acevedo-Fani et al.
(2015) also showed a negative charge on the surface of Tween 80
emulsified nanoemulsions containing sage EO and attributed that
to the presence of ionizable groups in EO. When emulsions are
exposed to sever mechanical stresses such as ultrasonication, it
might causes the releasing free hydroxyl and carboxyl groups from
chemical compositions of EO that move toward the surface of
droplets and are available to bind with water (Chen, Gao, Yang, &
Gao, 2013). These deprotonated alcohols (R-O-) or carboxylic
acids (R-COO-) contribute to increase the negative charge in the
interface of the droplets after ultrasonication process.
If the absolute value of z-potential is between 30 and 60 mV, the
nanoemulsion system is stable (Haghju, Beigzadeh, Almasi, &
Hamishehkar, 2016). The absolute z-potential values of emulsions
and nanoemulsions in this study were lower than 30 mV. Therefore,
electrostatic repulsion among droplets is not enough to stabilize
the prepared nanoemulsion and electrostatic mechanisms have no
Fig. 2. Antibacterial activity of SC-based edible coatings containing GEO emulsion and
considerable effect on its stabilization. All of researches that nanoemulsions and two antibiotics against S. typhimurium (A) and L. monocytogenes
fabricated EO nanoemulsions stabilized by biopolymers, reported (B). Data shown are the means ± standard deviation. Means with different letters are
higher z-potential values in comparison to the results of this significantly different (P < 0.05).
research. For example, þ57.33 mV and 71 mV were reported for z-
potential of chitosan (Wu et al., 2016) and sodium alginate (Salvia-
Trujillo et al., 2015) stabilized EO nanoemulsions. Therefore, it diffusion of bioactive compounds of essential oil through agar gel
should be acknowledged that, although the droplet size and PDI resulted significantly (p < 0.05) greater inhibition zones around the
were increased by using biopolymers instead of low molecular coating solutions (8.66 ± 0.94 mm and 10.33 ± 0.93 mm for
weight surfactants, however the increasing of the z-potential cau- S. typhimurium and L. monocytogenes bacteria, respectively). By
ses to more electrostatic repulsion and more stabilization of increasing GEO content to 6%, the antimicrobial activity against
biopolymer emulsified nanoemulsions. It should be noted that, the L. monocytogenes was increased significantly (p < 0.05) but it was
Tween 80 emulsified emulsion and nanoemulsion were added to not significant for S. typhimurium (p > 0.05). High antimicrobial
the SC solution at the next step. Thus, it could help to more stabilize properties of GEO loaded SC solutions are mainly related to phenol
of droplets by partial substitution of SC chains with Tween 80 diterpenes and sesquiterpenes especially a-zingiberene, b-sesqui-
molecules. However, more experiments are needed for proving this phellandrene and zingiberenol which high amount of these com-
hypothesis. As Atares et al. (2010a) approved that the SC has a good pounds are present in GEO (Calo, Crandall, O’Bryan, & Ricke, 2015).
emulsifying ability on ginger and cinnamon EOs. The incorporation of GEO into the nanoemulsion system caused
to a significant increase in antimicrobial activity. Inhibition zones
3.3. Characterization of coating solutions against both of bacteria were significantly (p < 0.05) increased by
addition of GEO in the nanoemulsion forms instead of conventional
3.3.1. Antimicrobial activity emulsion. For example, when 6% of GEO was used as nanoemulsion
The effectiveness of edible coatings in inhibiting S. typhimurium form in the formulation of coating solution, about 57% and 39%
(A) and L. monocytogenes (B) is shown in Fig. 2. The SC solution increment in antimicrobial potential was observed against
containing 3% Gentamicin exhibited the highest antimicrobial ac- S. typhimurium and L. monocytogenes respectively. From the data it
tivity against both of bacteria. Pure SC showed a slight antimicrobial is clear that the antibacterial effects of GEO nanoemulsions is better
activity against tested bacteria which is likely due to sulfhydryl and than chloramphenicol for the tested bacterial strains. Weiss,
amide groups in its side chains. Antimicrobial activity of pure SC Takhistov, and McClements (2006) suggested that a reduction in
solution was not recorded at day of 12 because it was completely the EO droplet size by nanoemulsion formation would allow anti-
putrefied due to the microbial growth in it. When 3% of GEO in the microbial compounds to penetrate faster in the bacterial cell thus,
form of conventional emulsion was incorporated into SC solution, the higher and faster antimicrobial behavior is observed. Salvia-
 S. Noori et al. / Food Control 84 (2018) 312e320
Trujillo et al. (2015) reported similar results when compared the
antimicrobial activity of lemongrass EO incorporated nano-
emulsions and conventional emulsions.
As can be seen in Fig. 2, the antimicrobial activity of the both of
emulsion and nanoemulsion was decreased significantly (p < 0.05)
during storage period. However, no reduction was observed for
synthetic antibiotics after 12 days. This could be attributed to the
physical and chemical instability of phenolic compounds of GEO
and their degradation affected by environmental factors (e.g. oxy-
gen, light, moisture, temperature, pH) (Rehman et al., 2016). By
comparing of data it is clear that the decreasing of antimicrobial
activity over time in nanoemulsion loaded solutions is lower than
those containing conventional emulsions. For example, the
decreasing of antimicrobial activity of SC-E6% sample against
L. monocytogenes was about 26% after 12 days of storage. But it was
calculated as about 15% when similar concentration of GEO was
used in the form of nanoemulsion. It demonstrates that nano-
encapsulation of GEO in the form of nanoemulsion, is an efficient
method for protecting and increasing the stability of its bioactive
compounds. Donsì, Annunziata, Sessa, and Ferrari (2011) reported
that the physical and chemical stability of D-limonene is increased
by encapsulation into nanoemulsions.
One another important result concluded from Fig. 2 is that the
antimicrobial activity of antibiotics and GEO emulsions and nano-
emulsions on Gram-positive bacterium (L. monocytogenes) is more
than Gram-negative one (S. typhimurium). One of the main reasons
for higher resistance of S. typhimurium is the structural differences
in the bacterial membrane. The cell wall of Gram-negative bacteria
is more complex due to the presence of an outer membrane, which
is composed mainly of lipopolysaccharide, in addition to a thin
peptidoglycan layer. Thus, the outer membrane of Gram-negative
bacteria acts as a permeability barrier, so that the absorption of
reactive oxygen species (ROS) and bioactive compounds into the
cell is reduced (Russell, 2003). In confirmation of our results,
Sayyad and Chaudhari (2010) reported that the antimicrobial ac-
tivity of GEO against Gram-positive bacteria is more drastically
higher than Gram-negative bacteria.
3.3.2. Antioxidant activity
DPPH scavenging potential of active coating solutions was
measured and compared with BHT. Fig. 3 shows the IC50 of the
coating solutions. The highest scavenging activity was shown by 3%
Fig. 3. Antioxidant activity of SC-based edible coatings containing GEO emulsion and
nanoemulsions and BHT. Data shown are the means ± standard deviation. Means with
different letters are significantly different (P < 0.05).
317
BHT loaded SC solution with IC50 of 0.68 mg ml1. Pure SC solution
had the lowest antioxidant activity (IC50 of 4.43 mg ml1). The
scavenging mechanism of SC may be related to the fact that free
radicals can react with the side chains of amino acids especially
residual free amino (NH2) groups to form stable macromolecule
radicals (Jime nez, Sanchez-Gonz alez, Desobry, Chiralt, & Arab
Tehrany, 2014). Antioxidant activity of SC solution was increased
by adding of GEO. But the increasing of GEO concentration had no
significant effect on IC50 values (p > 0.05). Generally, a weak anti-
oxidant activity is reported for GEO in literature. El-Baroty et al.
(2010) compared the antioxidant potential of GEO, cinnamon EO
(CEO), BHA, BHT and a-tocopherol (a-TOC). In agreement with our
results, according to their report the order of antioxidant activity
was as follows: GEO < a-TOC < BHA¼CEO < BHT. Singh et al. (2005)
also reported that the antioxidant activity of the oleoresins of
ginger is more than its EO. Summarizing these results, it may be
concluded that the GEO, rich in a-zingiberene, possesses strong
antimicrobial activity and weak antioxidant potential.
As shown in Fig. 3, the antioxidant activity of coating solutions
was increased by incorporation of GEO nanoemulsions. At the
concentration of 6%, the IC50 values of conventional emulsion and
nanoemulsion loaded samples at the first day of analysis were
recorded as 2.97 and 2.21 mg ml1, respectively. Droplet size
reduction due to formation of nanoemulsion causes to increase
specific surface of GEO and thus a fast and efficient free radical
absorption would be achieved. There is not any previous research
on the effect of nanoencapsulation on antioxidant activity of EOs to
compare with our results and this is the first report on this subject.
The decreased antioxidant activity by significant increasing of
IC50 values at 12th day revealed again the instability of GEO
bioactive compounds. Such reduction was not observed for SC-BHT
and pure SC samples. However, formation of nanoemulsion
decreased the degradation of GEO components. The percent of IC50
increasing for sample of SC-E6% from day 1 to day 12 was about
25%. But, it was increased about 13% for SC-NE6% sample that was
not statistically significant (p > 0.05) with first day. This is due to
the size reduction and formation of a thicker SC layer on the surface
of smaller EO droplets in nanoemulsion (Donsì et al., 2011). The
enhanced antimicrobial and antioxidant activities of nano-
emulsions over conventional emulsions and their increased sta-
bility would allow reducing the concentration to be incorporated in
foods and active coating or packaging.
3.4. Chicken meat quality attributes
3.4.1. Microbial analysis
Changes in aerobic psychrophilic flora of the uncoated and
coated chicken fillets are presented in Fig. 4A. The counts of psy-
chrophilic bacteria were increased with the storage time especially
for the control sample. The uncoated control sample had the
highest growth rate of psychrophilic bacteria that demonstrates the
necessity of using an additional treatment to increase the shelf life
of chicken meat. The uncoated and pure SC coated samples were
completely spoiled and putrefied at day 8 and withdrawn from the
experiments course. The microbial growth in fillets coated with 6%
GEO emulsion was lower than those coated with 3% of it. The mi-
crobial population was reduced from 5.76 Log CFU.g1 to 4.59 Log
CFU.g1 at 12th day of storage when the content of GEO emulsion
was increased from 3 to 6%. Although nanoemulsion loaded coat-
ings resulted more effective in slowing down the bacterial growth,
but it was not enough to stop it. In general, the most effective in-
hibition of psychrophilic bacteria was obtained for fillets coated by
the GEO nanoemulsion in the concentration of 6%.
The growth of molds and yeast exhibited similar trends during
storage (Fig. 4B). The highest slope of increment in population of
318 S. Noori et al. / Food Control 84 (2018) 312e320

of nano-droplets with bacteria cells, yields a quantum-size effect

and increases the antimicrobial activity of EOs (Wu et al., 2016).

3.4.2. TBARS index

The change in secondary products of lipid oxidation, as deter-
mined by TBARS measurements was not significantly different
between the treatments and studied times. TBARS values of all
samples up to day of 8 were recorded around 0.02 mg MDA.kg1
(data are not shown). Just for uncoated and pure SC coated sample,
its amount was increased to 0.04 mg kg1 at 8th day of analysis.
Lastly, at the end of storage period (day of 12) the TBARS index of all
the GEO coated samples reached to 0.06 mg kg1 and there was no
significant different (p > 0.05) between emulsion and nano-
emulsion coated samples. As it mentioned earlier, the antioxidant
potential of GEO is weaker than its antimicrobial activity. So it was
predictable that the active coatings containing GEO would not have
any distinct effect on lipid oxidation of chicken fillets.

3.4.3. Cooking loss

Fig. 4. Effect of the edible coatings containing GEO emulsion and nanoemulsion on the
microbial growth (Log CFU/g) of psychrophilic bacteria (A) and molds and yeast (B) in
chicken breast fillets during storage at 4
C. Data shown are the means ± standard
deviation. Different lowercase letters show significantly different (p < 0.05) between
all samples and different uppercase letters show significantly different (p < 0.05) be-
tween times for each sample.
molds and yeast was observed for uncoated sample. Pure SC coated
fillets had also higher counts of molds and yeast during storage. It
could be attributed to an increased availability of protein (SC) or
carbohydrate (glycerol) sources for microbial growth.
The pronounced growth of molds and yeast was started after 4th
day in the coated samples with GEO emulsions and nanoemulsions.
The lowest growth of molds and yeast was observed for sample of
SC-NE6%.
Similar results were reported for comparison the effect of EO
emulsions and nanoemulsions on the microbial quality of low-fat
cheese (Artiga-Artigas et al., 2017), silver pomfret fish (Wu et al.,
2016) and fresh-cut Fuji apples (Salvia-Trujillo et al., 2015). There
are many studies on the antibacterial activity of EOs against path-
ogenic bacteria (Calo et al., 2015). The major active ingredients of
EOs are phenols, monoterpenes, sesquiterpenes and aldehydes.
These oxygenated bioactive compounds of EOs could disrupt and
penetrate the lipid structure of the bacteria cell membrane and
Cooking loss is an important factor affecting the appearance and
acceptance of chicken meat. Table 2 shows the cooking loss of the
coated samples after cooking. As it is clear, the change in the
cooking loss of the all samples was increased significantly (p < 0.05)
by increasing storage time. This increment was higher for control
and pure SC coated samples rather than active coated samples. The
cooking loss was increased about 32% for control sample from day
of 1 to 8th day. But increment of about 16% was recorded for SC-E3%
sample at a same storage period. Moreover, as it is deduced from
Table 2, the cooking loss of the active coated samples is significantly
(p < 0.05) lower than that of control and SC coated samples in each
experiment time. It should be considered that a major part of
weight loss is due to the moisture extraction. In the control and
pure SC coated samples, the concentration of water on the matrix
surface is higher, so it is easily exuded during cooking, causing a
greater loss of weight. However, GEO coated samples are resistant
against mass transport due to the partial hydrophobicity of the
surface of fillets. In agreement with our results, Artiga-Artigas et al.
(2017) showed a drastic reduced water loss in low-fat cheese pieces
after coating with sodium alginate solution containing oregano EO.
In spite of a significant effect of GEO on decreasing the cooking
loss of chicken fillets, the effect of GEO concentration and form of
the loaded GEO (emulsion or nanoemulsion) on the cooking loss in
each storage time was not significant (p > 0.05). It may be attrib-
uted to the thermal deformation of nanoemulsions or partially
degradation of GEO compounds induced by high temperatures of
cooking process.
Table 2
Cooking loss of chicken breasts coated with SC based coatings containing GEO
emulsion and nanoemulsion during storage at 4
C. Data shown are the
means ± standard deviation.
Samples Storage time (day)
1 4 8 12

damage the enzyme systems of the microorganism (Donsì, Control 34.31 ± 2.36aC
38.91 ± 1.07aB
45.16 ± 0.97aA
e
Annunziata, Vincensi, & Ferrari, 2012). In agreement with our re- SC 34.00 ± 1.32aC 37.12 ± 1.43aB 43.21 ± 1.45aA e
SC-E3% 31.18 ± 1.00bD 33.45 ± 1.65bcC 36.21 ± 0.38cB 38.56 ± 1.22aA
sults, in all of the above mentioned researches, the nanoemulsions
SC-E6% 30.54 ± 0.85bC 32.76 ± 0.67cB 36.67 ± 1.11bcA 38.11 ± 1.34aA
exhibited a better effect on the preservation of foods compared to SC-NE3% 30.00 ± 1.05bC 34.21 ± 0.43bB 38.79 ± 0.48bA 39.00 ± 0.34aA
the emulsions. Donsì et al. (2011) proposed that the encapsulation SC-NE6% 31.66 ± 0.63abC 32.89 ± 1.09bcC 37.87 ± 1.63bB 40.87 ± 0.32aA
of bioactive compounds in nanoemulsion formulation enhances of
Mean values with different lowercase letters indicate significant differences
transport mechanisms through the cell membrane of the target (p < 0.05) within a column.
microorganisms. In fact, the larger surface area and higher affinity Mean values with different uppercase letters indicate significant differences
(p < 0.05) within a raw.
 S. Noori et al. / Food Control 84 (2018) 312e320 319

Table 3 the pure SC coated sample was not acceptable (score 2). Sticky
Total color difference (DE) of chicken breasts coated with SC based coatings con- surface and unpleasant appearance of SC coating was the reason of
taining GEO emulsion and nanoemulsion during storage at 4
C. Data shown are the
means ± standard deviation.
this lower score. But the adding of GEO was lessen these defects.
The scores of all the samples were decreased with storage time.
Samples Storage time (day) However, the rate of this decrease in GEO coated samples was lower
1 4 8 12 than uncoated or SC coated fillets. Also, when the GEO nano-
Control e 2.74 ± 0.34bB 6.96 ± 0.76aA e emulsion was used in the formulation of coating, the scores was
SC 1.57 ± 0.11cC 2.94 ± 0.21bB 3.65 ± 0.56bA e significantly (p < 0.05) higher than those incorporated with con-
SC-E3% 0.86 ± 0.10dD 2.13 ± 0.23bC 2.91 ± 0.65bcA 3.45 ± 0.32bA ventional emulsion. At the end of storage period, the SC-NE6%
SC-E6% 3.01 ± 0.05aB 5.59 ± 0.37aA 3.52 ± 0.56bB 2.57 ± 0.21cB
sample obtained the highest score. The presence of GEO in the
SC-NE3% 0.57 ± 0.07dD 1.90 ± 0.54bC 3.95 ± 0.23bB 5.00 ± 0.07aA
SC-NE6% 2.48 ± 0.23bA 2.78 ± 0.11bA 2.33 ± 0.43cA 2.40 ± 0.54cA surface of the coated samples produced a distinct but acceptable
pleasant odor, well received by the panelists. This effect was pro-
Mean values with different lowercase letters indicate significant differences
(p < 0.05) within a column.
nounced for samples coated with nanoemulsion. Because it formed
Mean values with different uppercase letters indicate significant differences a more homogeneous solution; and therefore, a shiny surface on
(p < 0.05) within a raw. the fillets. On the other hand, it was declared previously that the
rate of microbial growth was diminished by decreasing the size of
GEO droplets. Therefore, the odor and appearance of nanoemulsion
3.4.4. Color properties coated samples were also better due to the controlling of microbial
Color and appearance features are considered as the most spoilage.
influential factor in marketability of meat and poultry by the
customer. Total color difference (DE) is a parameter that shows the 4. Conclusions
color difference of the meat at different times for ideal and fresh
meat. Table 3 shows that DE values of the coated chicken breasts The preparation, characterization and application of sodium
with fresh uncoated sample. caseinate-based edible coating containing ginger EO nanoemulsion
The passage of time has significant effect on the values of DE, was carried out. Ultrasonication was an effective method for
and it was increased significantly in all of the samples (p < 0.05). preparation of GEO nanoemulsion with decreasing of droplet size to
The highest DE was recorded for control sample at day 8 (6.96). about 57 nm. It was shown that the nanoemulsion-loaded coating
The effect of GEO on color properties of the fillets depends on solution has strong antimicrobial activity comparable to genta-
the GEO concentration and the type of emulsion (conventional or micin antibiotic. But its antioxidant potential was weaker than
nanoemulsion). DE values of active coated samples were increased antimicrobial activity. Nanoemulsion-based edible coating con-
significantly by increasing of GEO concentration. SC solution had a taining 6% of GEO nanoemulsion increased the shelf-life of chicken
slight milky white color with high transparency but GEO was bright breast by significant decreasing of total aerobic psychrophilic bac-
yellow in color. Consequently, addition of GEO increased the DE teria and molds and yeasts. By considering lower antioxidant ac-
values of coated sample. Another interesting result was that the DE tivity of GEO, the edible coatings have not a significant effect on
of nanoemulsion coated samples was significantly lower than TBARS values of fillets. Color difference with fresh chicken fillets for
conventional loaded samples at same dosage of GEO. By addition of the samples coated by GEO nanoemulsions was lower than those
GEO and Tween 80 to SC solution, the emulsion is formed and coated with conventional emulsions. The application of GEO on
caused to high turbidity blocking effect and increasing of opacity chicken meat was pleasant and nanoemulsion coated samples
that causes to increase the DE. However, by fabrication of nano- achieved the highest total acceptance during storage. The results of
emulsion, the GEO was dispersed more homogenously and size of this study confirmed the potential utility of the GEO nanoemulsion
droplets was reduced thus the light transmittance was increased. incorporated SC coatings for improving the shelf life of raw poultry
The positive effect on visual characteristics is one of the major meat.
benefits of nanoemulsions in food applications.
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