LWT - Food Science and Technology xxx (xxxx) xxx

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LWT
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Encapsulation of fish oil by carrageenan and gum tragacanth as wall

materials and its application to the enrichment of chicken nuggets
Parastoo Pourashouri *, Bahareh Shabanpour , Sakineh Heydari , Sara Raeisi
Department of Seafood Science and Technology, Faculty of Fisheries and Environmental Sciences, Gorgan University of Agriculture Sciences and Natural Resources,
Gorgan, Iran

A R T I C L E I N F O A B S T R A C T

Keywords: Fish oil (FOL) and encapsulated fish oil by tragacanth (TRG) and carrageenan (CGN) were added to chicken
Carrageenan nuggets to evaluate the physicochemical, fatty acid profile and oxidative stability of pre-fried nuggets during
Fortification frozen storage. The panelists preferred fish oil addition as encapsulated (P < 0.05). The percentage of addition
Microcapsules
microcapsules (4–8%) was effective in acceptance of nuggets. The enriched samples by 4 g/100 g microcapsules
Fish oil
Tragacanth
were monitored by chemical and oxidative stability during storage. The CDs, TBARS and carbonyl values showed
significant differences during time of storage and between treatments (p < 0.05). At TRG and CGN treatments,
the EPA and DHA amount of the nuggets was significantly higher than control and FOL pre-fried samples.
Encapsulation of fish oil showed a protective effect against lipid and protein oxidation, and improved the
oxidative shelf life and the sensory characteristics of the enriched nuggets. The encapsulating of fish oil by
tragacanth was more effective in preserving the sensory characteristics.

1. Introduction
Fish and seafood are one of the main origins of PUFA (omega-3 fatty
acids such as EPA and DHA) which are important for human health
(Poyato, Ansorena, Berasategi, Navarro-Blasco, & Astiasarán, 2014).
Despite the general recommendations about using PUFA (omega-3), the
percentage of daily taken isn’t sufficient (Givens, 2015). Fortification of
foods with PUFA of marine origin, due to the role of bioactive com­
pounds in the prevention of certain diseases and health promotion, is an
important issue. Food traditions are changing in conformity with
human’s lifestyle which has been concentrated on time-saving; There­
fore, growing consumer demands for convenience and ready-to-eat
(RTE) products and like as pre-fried frozen ones which are one of the
major current attitudes and chicken nuggets are the most popular
(Jiménez-Martín, Pérez-Palacios, Carrascal, & Rojas, 2016). Today,
absorbing RTE products are progressively attainable in the market and
different sectors and the consumer’s expectations are for taste, flavor
and salutary effects (Sanjuás-Rey, Pourashouri, Barros-Velázquez, &
Aubourg, 2012). A strategic solution and potential method for higher
consumption of omega-3 fatty acids and make a healthier product for
concerned consumers could be enriching this type of products by fish oil
to reach the recommended level of these fatty acids in daily food diet
(80 mg of the sum of EPA and DHA per 100 g) (EU, 2010). In spite of all
the benefits of omega-3 fatty acids, one of the main challenges in
enriching with these compounds is their un-saturation and sensitivity to
oxidation which cause to reduce nutritional value (Shahidi & Zhong,
2010). In addition, the unpleasant smell of fish oil determines the sen­
sory characteristics of the product (Cho, Shim, & Park, 2003). Encap­
sulation is practicable in stabilizing highly unsaturated fatty acids and
masking the odor of fish oil and preserving the biological activity of the
nutrients (Kaushik, Dowling, Barrow, & Adhikari, 2015; Onwulata,
2013; Pourashouri et al., 2014); which active ingredients such as oils
and flavor ingredients in the walls material are bundled and produce
small capsules with numerous beneficial properties (Sauvant, Cansell,
Hadj Sassi, & Atgié, 2012; Velasco, Dobarganes, & Márquez-Ruiz, 2003).
The composition of wall material is one of the important parameters in
the encapsulation. The selected wall material should be able to preserve
core against oxygen, which increases the lifetime of the core (Gharsal­
laoui, Roudaut, Chambin, Voilley, & Saurel, 2007; Lim, Tan, Bakar, &
Ng, 2012).
Gums are polysaccharide polymers can be used as an emulsifier,
stabilizer, thickener due to their hydrocolloid attributes which have

* Corresponding author..
E-mail addresses: Pourashouri.p@gmail.com, pourashouri.p@gau.ac.ir (P. Pourashouri), b_shabanpour@yahoo.com (B. Shabanpour), s.heydari27@gmail.com
(S. Heydari), Sarah.Reisi69@gmail.com (S. Raeisi).

https://doi.org/10.1016/j.lwt.2020.110334
Received 25 May 2020; Received in revised form 1 October 2020; Accepted 3 October 2020
Available online 7 October 2020
0023-6438/© 2020 Elsevier Ltd. All rights reserved.

Please cite this article as: Parastoo Pourashouri, LWT - Food Science and Technology, https://doi.org/10.1016/j.lwt.2020.110334
P. Pourashouri et al.
good properties that enabled their application as wall materials for
encapsulation (Raeisi, Ojagh, Pourashouri, Salaün, & Quek, 2020).
Carrageenan is a thermally reacting material, low-priced and simple to
handle and gelation is actually simple (Rodrigues, Carvalho, Gomes, &
Reis, 2015). Tragacanth has good emulsifying characteristics and is
stable to acidity and heat which is usually applied in several foods
(Farahmandfar, Mohseni, & Asnaashari, 2017).
Various procedures of micro or nano-encapsulation have been
patented by some companies for utilization of different compounds in
foods or as dietary supplements (Rutz, Borges, Zambiazi, da Rosa, & da
Silva, 2016). There are several documents on the characteristics of fish
oil microcapsules (García-Moreno et al., 2018; Pourashouri et al., 2014).
However, few studies relating to the application of fish oil encapsulated
in foods have been published, e.g., application of microcapsules con­
taining fish oil in meat and poultry products (Jiménez-Martín et al.,
2016; Josquin, Linssen, & Houben, 2012; Solomando, Antequera, &
Perez-Palacios, 2020), dairy products (Jamshidi, Shabanpour, Poura­
shouri, & Raeisi, 2019; Kolanowski & Weiβbrodt, 2007), bread and
bakery products (Liu, Wallin, & Saldeen, 2001; Saldeen, Wallin, &
Marklinder, 1998; Umesha, Manohar, Indiramma, Akshitha, & Naidu,
2015). Therefore, the current research aimed to compare the use of
carrageenan and tragacanth, as the polysaccharide-encapsulant to
coating fish oil and introduce the microcapsules to chicken nuggets. The
different nuggets were analyzed for physiochemical, fatty acids and
sensory quality during frozen storage.
2. Materials and methods
2.1. Preparation of fish oil microcapsules
The encapsulation of fish oil was carried out according to Azarikia
and Abbasi (2016). Briefly, stock solutions (1% w/v) of tragacanth (T)
and carrageenan (C) as wall materials (Sigma- Aldrich Co., St Louis, MO,
USA) were prepared in water separately. For preparation of mixed
emulsion, Whey protein concentrate (WPC) solution, T and C stock
dispersions were mixed gently (120 min, room temperature) using a
magnetic stirrer (Fisher Vortex Genie 2, Scientific Industries, Inc.,
Bohemia, Czech Republic) to form WPI-T or WPI-C complexes (0.8:1%
w/w) and stable emulsion (creaming index = 0%) (Gu, Decker, & Julian
McClements, 2007). Then, fish oil (8%) (Cod liver oil, (Sigma-Aldrich
Co., St Louis, MO, USA)) was gradually added to prepared wall com­
plexes and was mixed at 400 rpm for 10 min. Pre-homogenization of the
samples were done at 4000 rpm for 3 min by a rotor-stator homogenizer
(Ultra-Turrax, T25, Digital IKA-Werke Stuttgart Staufen, Germany) and
the homogenized samples (10,000 rpm, 1 min) were sonicated (Soni­
cator 400,40 kHz, Iran) at amplitude of 100% for 4 min and finally the
frozen emulsions (− 80 ◦ C) were freeze-dried during 72 h (− 50 ◦ C, 12
Pa) (FreeZone 4.5 L, Labconco Corp., Kansas City, MO, USA).
2.1.1. Surface oil and entrapment efficiency (EE)
The powder (2.5 g) was blended with hexane (15 ml) (Fisher Vertex
Genie 2, Scientific Industries, Inc., Bohemia, Czech Republic); then the
mixture was centrifuged (8000 rpm-20 min) (Eppendorf centrifuge
5810 R, Germany). A rotary evaporator (IKA, Germany) was used to
evaporate the solvent at 70 ◦ C; finally, the solvent-free extract was dried
at 105 ◦ C. The amount of surface oil was calculated gravimetrically and
used for encapsulation efficiency (Chang & Nickerson, 2018).
2.1.2. Scanning electron microscopy of microcapsules
The scanning microscope (FESEM, MIRA3, TESCAN-XMU) in vac­
uum state were used for monitoring the morphology. The prepared
samples were imaged with different magnifications (10 kV).
2.1.3. Moisture and solubility
The moisture content of oil microcapsules were determined by the
method of AOAC (2002).
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2.1.4. Hygroscopicity
Approximately 0.5 g of each microcapsule was weighted in a petri-
dish and was kept in a desiccator filled with saturated NaCl solution
(75% RH) at 25 ◦ C. In a week, hygroscopicity of the weighed samples
were determined (Cai & Corke, 2000).
2.1.5. Color
The color of microencapsulated fish oil was measured using a
colorimeter (Chroma meter CR-210, Minolta, Tokyo, Japan); calibrated
with a standard ceramic tiles. Results were expressed by CIE color values
[L*(lightness), a*(-a green, + a red), b*(-b blue, + b yellow)].
2.2. Chicken nugget preparation
Chicken nuggets were produced according to Arshad et al. (2017).
The fresh chicken fillets were purchased from local market (Eros, Gor­
gan, Iran). Briefly, the chicken nuggets were prepared by minced meat
(Moulinex 320, Spain), onion, black pepper and salt. Then, all in­
gredients were mixed and further minced in kitchen food processor
(Moulinex, France) according to each formulation. The optimal per­
centage of fish oil microcapsules was calculated from encapsulation
efficiency of each powder and according to the requirements of DHA and
EPA (Jiménez-Martín et al., 2016) and sensory acceptance during
pre-treatments. In order to supply the required amount of DHA and EPA
(>80 mg DHA and EPA) in the nuggets according to the calculations at
least 4 g/100 g microcapsules was required to reach the accepted levels.
A pre-treatment was arranged by sensory panels to determine suitable
level from 4 to 8%; then the nuggets containing 4% microcapsules were
selected. Three batches of nuggets were made per each treatment:
control (Control) without fish oil, (1%) fish oil (FOL), and tragacanth
(TRG) and carrageenan (CGN) microcapsules. Then each treatment was
separately mixed and molded (4 × 4 × 1 cm). Pre-dust and battering
were done and nuggets were pre-fried in sunflower oil for 30 s at 180 ◦ C
(central temperature of the nuggets) and immediately removed from the
fryer. The excess of external oil was removed by paper towel. The
nuggets were separately packaged in polyethylene bags and were stored
at − 18 ◦ C for three months (Krokida, Oreopoulou, & Maroulis, 2000).
The chemical analyses of the nuggets were performed at 0, 30 and 90
days of frozen storage period and sensory evaluations were done at first
of storage period. All experiments were done in three repetitions.
2.2.1. Conjugated dienes (CDs)
The concentration of CDs was determined by extraction solution
(hexane/isopropanol) according to Juntachote, Berghofer, Siebenhandl,
and Bauer (2006). Firstly, a homogenized suspension of 0.5 g of nugget
in 5 ml of water was prepared. Then, 0.5 ml of suspension was added to
5 ml of extraction solution (3:1 (v/v)). The mixture was centrifuged
(3500 rpm, 5 min), and the absorbance was measured at 233 nm (Bio­
chrom, Libra s12, Cambridge, England). The amount of CDs was
expressed as μmole/mg of sample by calculation the molar extinction
coefficient of 25,200 M− 1 cm− 1.
2.2.2. Thiobarbituric acid reactive substances (TBARS)
The TBARS values of the nuggets were measured based on the re­
action of 2-thiobarbituric acid (TBARS, a chromogenic reagent) with
malondialdehyde (MDA) to find the secondary lipid oxidation of the
samples as described by Buege and Aust (1978). Five grams of minced
nugget was mixed with 25 ml of stock solution (0.0335 g TBA, tri­
chloroacetic acid 15%, and hydrochloric acid 0.25N) and it was heated
(95 ◦ C − 10 min); in following samples were cooled in running water.
Then the samples were centrifuged (5500 rpm-20 min) and absorbance
was recorded (532 nm) and TBARS value of the samples was obtained by
standard curve (obtained from MDA standards).
2.2.3. Protein carbonyls
Protein oxidation in chicken nuggets was determined according to
P. Pourashouri et al.
the described method by Jiménez-Martín et al. (2016). The conversion
of protein carbonyls to 2, 4 dinitrophenylhydrazones (DNPH) is the base
of this method. The concentration of derivatives was spectrophotomet­
rically measured at 280 and 370 nm. In brief, minced meat (1:10 (w/v))
was mixed with sodium phosphate buffer (20 mM) containing NaCl (0.6
M; pH 6.5). Then, 1 ml of cold trichloroacetic acid (TCA; 10%) was
added to precipitation of protein (0.2 ml; two aliquot for protein and
carbonyl concentration) and centrifuged (5 min at 5000 rpm). One shot
was treated with 1 ml 2M HCl (protein concentration). To determine the
carbonyl concentration, the second pellet was mixed with 0.2% (w/v)
DNPH in 2 M HCl. Incubation was done for 1 h at 25 ◦ C in darkness and
samples were precipitated. The percolated samples washed with 1 ml of
ethanol:ethyl acetate (1:1, v/v); the washing was repeated until the
discoloration of ethanol/ethyl acetate extract to ensure the removal of
excess DNPH. The sediment was then stirred in 1.5 ml of buffer sodium
phosphate containing guanidine. The amount of carbonyls was
expressed as nanomoles of carbonyl per milligram of protein using an
absorption coefficient of 21.0 nM− 1 cm− 1 at 370 nm for protein
hydrazones.
2.2.4. Fatty acid profile
The fatty acid composition was measured (Metcalfe & Schmitz,
1961). Five ml of 2% methanolic extract was added to the extracted oil
by the method of Bligh and Dyer (1959). The vortexed samples were
incubated in a water bath (Memert, Germany; 100 ◦ C, 10 min). Then,
2.5 ml of BF3 solution was added to the tubes of samples and were
heated in water bath (3 min). The cooled mixture was then shaken by 1
ml of hexane and 1 ml of saturated salt (300 g of sodium chloride/liter of
distilled water). After the formation of two separate phases, the upper
phase was carefully separated and used for experiment. The capillary
column (25 m × 0.2 mm, film thickness, BPX70 SGE) was used to
examine and identify the fatty acids in the extracted oil by the gas
chromatography (Hewlett Packard 5890 series II, Ramsey, MN, USA).
2.2.5. Sensory evaluation
Sensory evaluations were carried by the hedonic test, using the nine-
point scale (Table 1), which was rated of “very bad” to “very good”
(Juntachote et al., 2006). The evaluation was performed in a part of the
laboratory space with white fluorescence light. The deep-fried Nuggets
were fried at 180 ◦ C for 4 min and were served in a white plastic dish
with numbered code. After evaluating each sample, small crackers and
water were ready to fresh the taste. Visual assessment, texture, taste,
flavor were assessed by thirty semi-trained university students with
different gender (25–29 years old, female and male) (Jiménez-Martín,
Gharsallaoui, Pérez-Palacios, Ruiz Carrascal, & Antequera Rojas, 2015).
2.3. Statistical analysis
Data were analyzed using IBM SPSS Statistics for Windows (Version
22.0., IBM Corp. Armonk, NY., USA). The experimental data were
analyzed by one or two-way analysis of variance in a completely ran­
domized design and Tukey test was used to the comparison of the mean
values (p < 0.05).
Table 1
Physicochemical characteristics of fish oil microcapsules.
Treatment Surface oil (%) EE (%) Moisture (%) Solubility (%)
b b b b
TRG 2.23 ± 0.56 68.73 ± 2.6 2.08 ± 0.03 60.10 ± 4.18
CGN 8.55 ± 1.26a 46.00 ± 5.12a 2.58 ± 0.06a 73.55 ± 9.30a
Different letters in each column indicate significant difference (P < 0.05).
FOL: fish oil; TRG: Encapsulated fish oil by tragacanth; CGN: Encapsulated fish oil by Carrageenan.
3
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3. Results and discussion
3.1. The microcapsules characteristics
3.1.1. Surface oil and EE
Significant differences were found between the physical character­
istics of the microcapsules (p < 0.05) (Table 1). It can be detected how
the CGN samples had higher surface oil (8.55%), solubility and hygro­
scopicity values than TRG microcapsules. The encapsulation matrix
composition was effective in higher loading efficiency; which could
apply a barrier protection effect against lipid oxidation of encapsulated
fish oil. The rapid formation and drying of the wall material can also
reduce non-encapsulated oil (Ogrodowska, Tańska, & Brandt, 2017).
Mehrad, Shabanpour, Jafari, and Pourashouri (2015) also reported high
amount (5%) of surface on encapsulated fish oil by mixture of carra­
geenan and maltodextrin. The TRG treatment showed higher encapsu­
lation efficiency (EE) (68.73%) than CGN samples (46%). It has been
shown that the combination of wall materials is often progress the
loading efficiency (Ogrodowska et al., 2017; Pourashouri et al., 2014).
The combination of tragacanth and whey protein as wall material
showed better oil coating than mixture of carrageenan and whey pro­
tein. Electrostatic bonding between whey protein and tragacanth on the
surface of the oil particles resulted in the formation of a thick layer due
to stable emulsions and also increased efficiency (Guzey & McClements,
2007).
3.1.2. Scanning electron microscopy of microcapsules
The outer morphology of the fish oil microcapsules was imaged by
SEM (Fig. 1). The morphological and microstructure parameters of
powders with other related parameters are substantial for stability,
function and reconstitution of microcapsules (Ogrodowska et al., 2017).
The CGN powders had more porosity and pore on the surface compared
to the TRG treatment. It could be a reason of the higher surface oil
(8.55%) in CGN treatment. The freeze-dried powders are irregular, light
weight, highly porous and heterogeneous than spray dried powders
(Yazicioglu, Sahin, & Sumnu, 2015). Xia et al. (2017) showed the
smooth surface of the freeze-dried particles increases the chance of
oxidative stability of the encapsulated oil; uniform surface reduces the
contact between oil and oxygen and will increase the stability of the
samples.
3.1.3. Moisture and solubility
Moisture content of the microcapsules obtained with different wall
combination by freeze-drying method was varied (p > 0.05) (Table 1).
The sample prepared by TRG had the lower moisture content (2.08%).
The moisture content is important for storage stability (Ogrodowska
et al., 2017). Karaca, Nickerson, and Low (2013) reported 2.80–3.23%
moisture content for lyophilized flaxseed oil with protein isolates as wall
material. Experimental results of different drying method by Ogro­
dowska et al. (2017) showed that powders of seed oil of pumpkin pre­
pared by freeze-drying had a lower moisture content (2.4%) compared
to spray-dried samples (3.10–4.14%). Table 1 shows the type of wall
(TRG and CGN) had a significant effect on the solubility of the produced
powders (p < 0.05). The lowest solubility was obtained in the powders
prepared by TRG (60.10%), while in the CGN it was higher (73.55%).
Mostly, oil microcapsules are applied for ease of processing, product
formulation and handling. The powders with suitable physical and
Hygroscopicity (%) L* a* b*
b a b
0.59 ± 0.04 92.16 ± 0.8 1.33 ± 0.26 12.03 ± 0.23b
4.29 ± 0.18a 84.7 ± 1.05b 4.7 ± 0.46a 24.03 ± 0.26a
P. Pourashouri et al. LWT xxx (xxxx) xxx

Fig. 1. SEM micrographs of the surface of (a) TRG, (b) CGN fish oil microcapsules. TRG: Encapsulated fish oil by tragacanth; CGN: Encapsulated fish oil by
Carrageenan.

functional characterization are applicable (Ogrodowska et al., 2017).

This difference in solubility can be attributed to the difference of the
formed bonds in the matrix of wall materials. The solubility of micro­
capsules is effective on release of core material (Cho et al., 2003).

3.1.4. Hygroscopicity
Hygroscopicity property is also known as capacity of water absorp­
tion of powders from medium with high humidity until equilibrium.
After the surface absorption, the powders become dense and form a
sticky mass (Ribeiro, Costa, & Afonso, 2016). As shown in Table .1,
hygroscopic percentage was higher in microcapsules by CGN (4.29%)
than TRG (0.59%). According to the results, tragacanth has the ability to
form good films with whey protein, which reduces the amount of
moisture absorption. The higher CGN hygroscopic value is probably
related to moisture content. Physical parameters of powders, such as
moisture content, solubility and hygroscopicity are substantial for sta­
bility and reconstitution of microcapsules, in which the wall combina­ Fig. 2. Conjugated dienes (CDs) of chicken nuggets containing fish oil and
tion and method of drying are determining parameters (Samborska, encapsulated fish oil during frozen storage. Blue histogram (control); Orange
2019). According to Molina, Clemente, Scapim, and Vagula (2014) more histogram (fish oil); Grey histogram (Encapsulated fish oil by tragacanth);
porosity and fine particles contain wider contact surfaces and more Yellow histogram (Encapsulated fish oil by Carrageenan). A− C Different letters
acting site. indicate significant differences between treatments at each storage time. a-c
Different letters indicate significant difference of each treatment during storage
(P < 0.05). (For interpretation of the references to color in this figure legend,
3.1.5. Color
the reader is referred to the Web version of this article.)
The color of microcapsules was evaluated by measuring of L*, a* and
b* values (Table 1). The color of the powders is important in acceptance
be related to a greater surface oil and lower encapsulation efficiency in
and addition to product formulation. In this study, the microcapsules
CGN. The TBARS in enriched treatments, by encapsulated fish oil (TRG
showed a red-yellow color (positive a* and b*), with high lightness
or CGN) show significant differences respect to control. The presence of
(L*:84.7–94.16). The TRG treatment showed higher lightness than the
the gums in the wall combination was effective in higher stability of the
CGN treatment; lower redness and yellowness was observed in TRG
fish oil. According to Jiménez-Martín et al. (2015), encapsulation of fish
treatment (p < 0.05). The difference in the color of the microcapsules
oil is suitable method for enriching frozen meat products. Salminen
can be assigned to the wall combination of powders. According to
(2013) showed that incorporating fish oil in emulsion form decreased
Ogrodowska et al. (2017), size of microcapsules and drying method is
the oxidation of the enriched sausage.
effective on the color index, in which spray-dried samples had higher
According to Huang, Xiong, Kong, Huang, and Li (2013), oxidation
lightness than freeze-dried.
has a significant effect on quality degradation during the processing and
maintenance of formulated meat products. Reducing the quality of
3.2. Pre-fried chicken nuggets characteristics during storage
oxidation meat products is generally associated with reduced color,
nutrient degradation, and probable configuration of toxic compounds
3.2.1. Oxidative stability
(Huang et al., 2013; Shahidi & Zhong, 2010). During frozen storage of
The change in the primary (CDs) and secondary (TBARS value) lipid
formulated meat products, the fats become oxidized, and the
oxidation-derived compounds of nuggets enriched by fish oil during
non-saturated fatty acids form hydroperoxides, which then degrade to
frozen storage was evaluated (Figs. 2 and 3). Analysis of the data of
secondary compounds, including malonaldehyde and other carbonyl
oxidation compounds showed that the effect of enrichment, type of wall
compounds, which causes an unpleasant smell (Ganhão, Estévez, &
material and storage time and their interactions were significant (P <
Morcuende, 2011). In minced meat, peroxidants are released from a
0.05). According to the results, the FOL samples showed higher CDs and
variety of broken cell organs, and the entry of air can also effect on the
TBARS values. At the end of storage, the nuggets containing encapsu­
oxidation process by reacting oxygen to meat composition. Besides, the
lated fish oil showed lower oxidation. CDs value in CGN was slightly
presence of metals such as iron and copper in meat enhances the rate of
higher than the determined for the TRG sample, which could probably

4
P. Pourashouri et al. LWT xxx (xxxx) xxx

Fig. 3. TBAS of chicken nuggets containing fish oil and encapsulated fish oil
during frozen storage. Blue histogram (control); Orange histogram (fish oil);
Grey histogram (Encapsulated fish oil by tragacanth); Yellow histogram
(Encapsulated fish oil by Carrageenan). A-C Different letters indicate significant
differences between treatments at each storage time. a-c Different letters indi­
cate significant difference of each treatment during storage. (For interpretation
of the references to color in this figure legend, the reader is referred to the Web
version of this article.)
oxidation and free radicals formation (Huang et al., 2013). Therefore, in
enriched meat products by PUFA, the oxidation should be monitored.
3.2.2. Protein carbonyls
The changes in carbonyl content (PCs) in nuggets during frozen
storage were also evaluated (Fig. 4). PCs is considered an indicator for
protein oxidation (Jiménez-Martín et al., 2016). The oxidation of amino
acids can produce carbonyl derivatives (Serpen, Gökmen, & Fogliano,
2012; Sohaib et al., 2017). The minced meat has greater contact with
oxygen than the cut and chopped meat, so it is more prone to oxidation.
The several factors in meat such as metal catalysts, pH, temperature, and
phenolic compounds increase the probability of PCs formation (M.
Al-Hijazeen, Mendonca, Lee, & Ahn, 2018; Estévez, 2011). Generally,
higher PCs would indicate higher oxidation. Regardless of the type of
added microcapsules, the value of PCs increased with frozen storage
time. At the end of storage, PCs increased to 10.69 (μmol/mg protein)
for enriched nuggets with fish oil and to 8.07 and 9.10 (μmol/mg pro­
tein) for nuggets incorporated with encapsulated fish oil (TRG and
CGN). According to the results, the addition of fish oil (FOL) alone
increased the rate of PCs. The reduction observed in the PCs of the
encapsulated oil with different wall material is mainly related to the
surface oil and morphology of microcapsules. This difference between
fish oil and encapsulated oil can be due to the formation of more fatty
acid oxidation compounds in this treatment than microcapsule con­
taining treatments. Other studies have also reported similar increase of
carbonyls during frozen storage of meat products enriched with omega-3
(Baron, KjÆrsgård, Jessen, & Jacobsen, 2007; Botsoglou, Govaris,
Ambrosiadis, Fletouris, & Botsoglou, 2014; Jiménez-Martín et al., 2016;
Soyer, Özalp, Dalmış, & Bilgin, 2010). The formation of more free rad­
icals can increase the oxidation of protein in the meat product
(Jiménez-Martín et al., 2016). As a result of this study, microcapsule
formulations can also play an important role in protecting of protein
oxidation. According to the Marwan Al-Hijazeen, Lee, Mendonca, and
Ahn (2016), the addition of essential oil of specific plants diminished the
amount of carbonyls in frozen chicken meat. Therefore, natural anti­
oxidant or other protection methods are needed for enriched products by
omega-3.
3.2.3. Fatty acid composition
The major fatty acids in raw and pre-fried chicken nuggets contain­
ing fish oil and encapsulated fish oil at the beginning and end of the
storage period are displayed in Tables 2 and 3. In control nugget, C18:1
and C18:2 were the most abundant MUFA and PUFA, respectively. Ac­
cording the results, fatty acid composition of batches was affected by the
addition of fish oil. The raw nuggets incorporated with the bulk and
encapsulated fish oil showed the highest content of EPA and DHA; which
are commonly applied as indicators for oil quality (Vasile, Romero,
Judis, & Mazzobre, 2019). In relation to the type of microcapsules, the
TRG microcapsules showed slightly more protection during storage (p <
0.05). The amount of EPA and DHA was increased of 0.05 mg/g sample
in control to 2.01–2.04 mg/g in enriched treatments. The highest
amounts of PUFA and ω3 were observed in these treatments (Table 2).
Table 2
Fatty acids profile (mg/g sample) on raw chicken nuggets containing fish oil and
encapsulated fish oil.
Co FO TRG CGN

C14:0 0.13 ± 0.00b 0.45 ± 0.01a 0.44 ± 0.00a 0.45 + 0.02a

C16:0 5.21 ± 0.34 5.69 ± 0.05 5.63 ± 0.01 5.70 ± 0.06
C17:0 Ndb 0.09 ± 0.41a 0.09 ± 0.01a 0.09 + 0.00a
C18:0 2.12 ± 0.10 2.04 ± 0.05 1.94 ± 0.03 1.94 ± 0.04
C14:1 0.03 ± 0.00a 0.02 ± 0.00b 0.02 ± 0.00 0.02 ± 0.00b
C16:1 1.10 ± 0.02c 1.43 ± 0.01ab 1.31 ± 0.00b 1.46 ± 0.05a
C17:1 Ndb 0.08 ± 0.00a 0.08 ± 0.00a 0.077 ± 0.01a
C18:1 6.74 ± 0.01b 7.31 + 0.00a 7.19 ± 0.09a 7.29 + 0.02a
C22:1 0.12 ± 0.00a 0.10 ± 0.00bc 0.09 ± 0.00c 0.11 ± 0.00ab
C20:1n 0.03 ± 0.00b 0.16 ± 0.00a 0.16 ± 0.00a 0.16 ± 0.02a
C18:2n6 3.68 ± 0.08 3.47 ± 0.00 3.68 ± 0.14 3.72 ± 0.00
C18:3n6 Ndb 0.05 ± 0.01a 0.05 ± 0.00a 0.05 ± 0.01a
C18:3n3 0.02 ± 0.00b 0.80 ± 0.01a 0.79 ± 0.00a 0.78 ± 0.01a
C20:3n6 0.04 ± 0.00a 0.03 ± 0.01a 0.03 ± 0.00a 0.04 ± 0.00a
C20:3n3 0.04 ± 0.00c 0.41 ± 0.03b 0.43 ± 0.02a 0.41 ± 0.01b
C20:4n6 0.49 ± 0.00c 1.00 ± 0.01ab 1.01 ± 0.00a 1.00 ± 0.00b
C20:5n3 0.01 ± 0.00b 1.16 ± 0.01a 1.17 ± 0.00a 1.16 ± 0.01a
C22:6n3 0.03 ± 0.00b 0.85 ± 0.02a 0.86 ± 0.00a 0.86 ± 0.01a
C22:4n6 0.19 ± 0.03 0.18 ± 0.00 0.18 ± 0.00 0.20 ± 0.00
SFA 7.48 ± 0.23b 8.28 ± 0.00a 8.12 ± 0.07a 8.20 ± 0.12a
Fig. 4. Protein Carbonyls content of chicken nuggets containing fish oil and MUFA 8.03 ± 0.01c 9.12 ± 0.02a 8.87 ± 0.08b 9.14 ± 0.04a
encapsulated fish oil during frozen storage. Blue histogram (control); Orange PUFA 4.53 ± 0.03b 7.99 ± 0.01a 8.23 ± 0.14a 8.26 ± 0.01a
EPA + DHA 0.05 ± 0.01c 2.01 ± 0.00b 2.04 ± 0.00a 2.02 ± 0.00ab
histogram (fish oil); Grey histogram (Encapsulated fish oil by tragacanth);
ω3/ω6 0.02 ± 0.00b 0.68 ± 0.05a 0.63 ± 0.06a 0.64 ± 0.05a
Yellow histogram (Encapsulated fish oil by Carrageenan). A− C Different letters
indicate significant differences between treatments at each storage time. a-c Different small letters show significant difference between treatments. Nd = not
Different letters indicate significant difference of each treatment during storage. detected.
(For interpretation of the references to color in this figure legend, the reader is FOL: fish oil; TRG: Encapsulated fish oil by tragacanth; CGN: Encapsulated fish
referred to the Web version of this article.) oil by Carrageenan.

5
P. Pourashouri et al. LWT xxx (xxxx) xxx

Table 3 Table 3 (continued )

Fatty acids profile (mg/g sample) on pre-fried chicken nuggets containing fish Storage Co FO TRG CGN
oil and encapsulated fish oil during frozen storage. (month)
Storage Co FO TRG CGN C20:3n6 0 0.04 ± 0.03 ± 0.03 ± 0.04 ±
(month) 0.00Aa 0.00Aa 0.00Aa 0.00Aa
C14:0 0 0.30 ± 0.41 ± 0.45 ± 0.47 ± 3 NdBc NdBc 0.02 ± 0.01 ±
0.00b 0.00a 0.03a 0.04a 0.00Ba 0.00Bb
3 0.36 ± 0.56 ± 0.51 ± 0.51 ± C20:3n3 0 0.03 ± 0.40 ± 0.42 ± 0.42 ±
0.10b 0.02a 0.08a 0.09a 0.00Ac 0.00Ab 0.00Aa 0.00Aa
C16:0 0 10.80 ± 10.03 ± 10.03 ± 11.13 ± 3 0.01 ± 0.27 ± 0.39 ± 0.37 ±
0.01b 0.00c 0.00c 0.06a 0.00Bc 0.01Bb 0.01Ba 0.01Ba
3 11.14 ± 10.48 ± 10.52 ± 10.55 ± C20:4n6 0 0.39 ± 0.96 ± 1.03 ± 0.97 ±
0.11a 0.03b 0.08b 0.13b 0.00b 0.01a 0.02a 0.01a
C17:0 0 Ndb 0.09 ± 0.08 ± 0.11 ± 3 0.38 ± 0.95 ± 0.99 ± 0.95 ±
0.00Aa 0.00a 0.00a 0.00c 0.01b 0.01a 0.00b
3 Ndb 0.01 ± 0.05 ± 0.04 ± C20:5n3 0 0.008 ± 1.03 ± 1.16 ± 1.135 ±
0.00Ba 0.00a 0.00a 0.00c 0.01b 0.00a 0.01a
C18:0 0 1.31 ± 1.86 ± 2.13 ± 2.09 ± 3 Ndc 0.96 ± 1.15 ± 1.09 ±
0.01c 0.04b 0.00a 0.05a 0.02b 0.00a 0.01a
3 1.46 ± 2.36 ± 2.26 ± 2.32 ± C22:6n3 0 0.03 ± 0.73 ± 0.81 ± 0.76 ±
0.02b 0.30a 0.00ab 0.06ab 0.00Ad 0.00c 0.00a 0.00b
C20:0 0 0.29 ± 0.27 ± 0.27 ± 0.28 ± 3 NdBc 0.66 ± 0.80 ± 0.72 ±
0.00a 0.00b 0.00b 0.00ab 0.03b 0.00a 0.02ab
3 0.29 ± 0.28 ± 0.25 ± 0.31 ± C22:4n6 0 0.18 ± 0.18 ± 0.18 ± 0.18 ±
0.00a 0.00a 0.00b 0.01a 0.00a 0.00a 0.00a 0.00a
C22:0 0 0.74 ± 0.72 ± 0.71 ± 0.73 ± 3 0.17 ± 0.17 ± 0.17 ± 0.17 ±
0.00Ba 0.02a 0.00a 0.00a 0.00a 0.00a 0.01a 0.00a
3 0.90 ± 0.71 ± 0.76 ± 0.74 ± SFA 0 13.46 ± 13.39 ± 13.70 ± 14.82 ±
0.03Aa 0.00b 0.03b 0.01b 0.02 Abc 0.47 Bc 0.04Ab 0.06Aa
C14:1 0 0.02 ± 0.02 ± 0.02 ± 0.02 ± 3 14.16 ± 14.41 ± 14.36 ± 14.48 ±
0.00a 0.00a 0.00a 0.00a 0.07Aa 0.29 Aa 0.03Aa 0.00Aa
3 0.02 ± 0.01 ± 0.02 ± 0.01 ± MUFA 0 45.60 ± 45.51 ± 43.41 ± 41.77 ±
0.00a 0.00b 0.00a 0.00b 1.19a 0.82Aa 0.25ab 0.07b
C16:1 0 0.82 ± 1.23 ± 1.20 ± 1.22 ± 3 42.51 ± 41.96 ± 41.68 ± 40.33 ±
0.01b 0.01Ba 0.00a 0.01a 0.31a 0.14Bab 0.40ab 0.54b
3 0.69 ± 2.44 ± 1.24 ± 1.28 ± PUFA 0 75.36 ± 74.29 ± 70.78 ± 68.97 ±
0.06c 0.16Aa 0.00b 0.02b 0.00a 0.03b 0.13c 0.02d
C17:1 0 Ndb 0.08 ± 0.07 ± 0.07 ± 3 75.32 ± 74.12 ± 69.92 ± 68.74 ±
0.01a 0.00a 0.00a 0.10a 0.24a 0.69b 0.10b
3 Ndb 0.09 ± 0.08 ± 0.08 ± EPA + 0 0.04 ± 1.77 ± 1.98 ± 1.90 ±
0.00a 0.00a 0.00a DHA 0.00d 0.01c 0.00a 0.02b
C18:1 0 9.86 ± 11.66 ± 9.87 ± 8.21 ± 3 Ndc 1.63 ± 1.96 ± 1.81 ±
0.10b 0.45Aa 0.10b 0.09Ac 0.06b 0.01a 0.04ab
3 9.67 ± 10.92 ± 9.70 ± 7.94 ±
a-c Different letters indicate significant differences between treatments.
0.00b 0.01Ba 0.07b 0.04Bc A− B
Different letters indicate significant differences due storage time.
C18:1cis9 0 34.58 ± 32.08 ± 31.98 ± 32.00 ±
0.50Aa 0.35Ab 0.15b 0.01b Nd = not detected; FOL: fish oil; TRG: Encapsulated fish oil by tragacanth; CGN:
3 31.69 ± 27.86 ± 30.30 ± 30.72 ± Encapsulated fish oil by Carrageenan.
0.29Ba 0.09Bb 0.46a 0.45a
C22:1 0 0.10 ± 0.09 ± 0.09 ± 0.08 ±
The pre-frying oil, process and heat was effective on the fatty acids
0.00a 0.00ab 0.00ab 0.00b
3 0.25 ± 0.14 ± 0.09 ± 0.09 ±
composition of the nugget; which arachidic acid (C20:0), docosanoic
0.05a 0.02ab 0.01b 0.00b acid (C22:0), oleic acid (18:1cis-9) and Linolelaidic acid (C18:2trans)
C20:1n 0 0.19 ± 0.32 ± 0.15 ± 0.15 ± have been added to fatty acid profile belonging to the culinary fat. A
0.00b 0.00a 0.00c 0.00c similar result was obtained by Miranda et al. (2010), who reported
3 0.17 ± 0.28 ± 0.24 ± 0.18 ±
changes in the fatty acid profile of pre-fried tuna pasties and ham nug­
0.00b 0.02a 0.03ab 0.01b
C18:2n6 0 72.53 ± 67.83 ± 63.88 ± 62.31 ± gets due to frying oil. Pre-frying in olive oil decreased the proportion of
0.00a 0.00b 0.00c 0.00d SFA and increased the ratio of MUFA in the products, whiles when
3 72.58 ± 67.97 ± 63.19 ± 62.34 ± sunflower oil was used, the ratio of PUFA in fried products increased. In
0.01a 0.06b 0.66c 0.09c the current study, after pre-frying, significant decrease in EPA-DHA
C18:2 trns 0 0.85 ± 0.86 ± 0.83 ± 0.87 ±
0.00a 0.03a 0.01a 0.00a
content was found in all batches and it was more evident in fish oil
3 0.93 ± 0.91 ± 0.85 ± 0.85 ± batch. The encapsulation of fish oil improved the protection of EPA and
0.00a 0.01ab 0.00bc 0.02c DHA. Moreover, it improved the nutritional value and stabilized the
C18:3 cis 0 1.25 ± 1.16 ± 1.35 ± 1.22 ± fatty acids in frozen pre-fried nuggets. The fatty acids such as amount of
0.00b 0.00c 0.00a 0.00b
C20: 3n3 decreased in greater intensity in FOL batch after three months
3 1.22 ± 1.21 ± 1.29 ± 1.20 ±
0.08b 0.09b 0.03a 0.01b of storage. This may indicate the efficiency of wall materials at micro­
C18:3n6 0 Ndd 0.29 ± 0.24 ± 0.26 ± capsules tested in this study to protect the fatty acids of the encapsulated
0.00Aa 0.00Ac 0.00Ab fish oil to oxidation during the pre-frying and storage. Solomando et al.
3 Ndb 0.24 ± 0.23 ± 0.23 ± (2020) showed similar results in enriched sausages by multilayer fish oil
0.00Ba 0.00Ba 0.00Ba
C18:3n3 0 0.02 ± 0.77 ± 0.79 ± 0.78 ±
microcapsules; which incorporating monolayer microcapsules
0.00Ab 0.00Aa 0.00Aa 0.00Aa decreased the EPA and DHA values after 4 months of frozen storage. The
3 0.01 ± 0.73 ± 0.77 ± 0.76 ± ω3/ω6 ratio increased in the nuggets with fish oil to control; Similar to
0.00Bc 0.00Bb 0.00Ba 0.00Ba the observation of Jiménez-Martín et al. (2014). Regardless of the wall
material type, the oil encapsulation decreased quality loss of fatty acid

6
P. Pourashouri et al.
and keeps its value during frozen storage. Other investigations also
informed similar results of the increase PUFA in different enriched
chicken and meat products by gelled fish oil emulsion (Poyato et al.,
2014), salmon and flaxseed oil (Sell, Beamer, Jaczynski, & Matak, 2015)
and fish oil microcapsules (Solomando et al., 2020).
3.2.4. Color chicken nuggets
There was changes in color of treatments and storage time (p < 0.05)
(Fig. 5). The color values of samples showed that method of incorpo­
rating fish oil affected color indexes (p < 0.05). Regardless of the wall
material, at the initial the lightness of encapsulated samples (TRG and
CGN) was statistically higher than control and FOL samples and the L*
values decreased in TRG treatment with storage. But then, differences in
a* and b* values between FOL and other treatments were observed. The
yellowness of the nuggets decreased significantly in FOL and control
treatments and this change in TRG and CGN was lower. Sell et al. (2015)
reported the increasing of lightness with incorporation of salmon and
flaxseed oil to surimi, which lipid droplet diffused light and increased
the L* value. Poyato et al. (2014) observed that the brightness of the
enriched sausage was higher in gelled fish oil emulsion than control.
According to the changes in pigments, lipid oxidation could be catalyzed
and generated free radicals change the color of products (Hwang et al.,
2013). Overall, regardless of the treatments, there were variations in
Fig. 5. Color parameters of chicken nuggets enriched with omega-3 fatty acids;
A: Lightness, B: redness, C: yellowness; Blue histogram (Day 0); Orange histo­
gram (Day 30); Grey histogram (Day 90). A− C Different letters indicate signif­
icant differences between treatments at each storage time. a-c Different letters
indicate significant differences in each treatment during storage. (For inter­
pretation of the references to color in this figure legend, the reader is referred to
the Web version of this article.)
7
LWT xxx (xxxx) xxx
color parameters.
3.2.5. Sensory evaluation
The data of sensory attributes of nuggets containing fish oil and
encapsulated fish oil are shown in Fig. 6 (A and B). The evaluation was
conducted before eating (crust homogeneity, color and structure, odor,
fishy and rancid) and during eating (texture, crustiness, oiliness, juici­
ness, hardness, taste, flavor and fish odor) the nuggets. To select the
optimal percentage of microcapsules the primary evaluations were done
by addition of 4–8% powder to products (data not shown). The primary
sensory evaluation revealed that fortification up to 4 g/100 g had odor
acceptance; which it was approved by the evaluators. The scores of
sensory attributes before eating viz., homogeneity of the crust color and
structure, odor, fishy and rancid revealed that there was immense
variation in the results with odor and fishy (P < 0.05). The CGN and TRG
treatments awarded higher acceptance scores compared to FOL treat­
ment. Concerning fish odor, the results of the sensory evaluation were
consistent with the scores of during eating which more odor was
detected in fish oil treatment.
During eating, organoleptic parameters showed a significant differ­
ence (p < 0.05) in the flavor and fishy odor of the nuggets; the difference
of FOL treatment was detectable by the sensory panel in comparison of
other batches. The FOL nuggets got numerically lower points than the
encapsulated ones. The fish oil addition in nuggets did not significantly
affect the hardness, juiciness, oiliness and texture. The results showed
Fig. 6. Sensory parameter of chicken nuggets enriched with omega-3 fatty
acids A) before eating, B) During eating. Blue histogram (control); Orange
histogram (fish oil); Grey histogram (Encapsulated fish oil by tragacanth);
Yellow histogram (Encapsulated fish oil by Carrageenan). . (For interpretation
of the references to color in this figure legend, the reader is referred to the Web
version of this article.)
P. Pourashouri et al.
that encapsulation of fish oil with suitable coating material could pre­
serve the sensory quality characteristics. To enrichment of products, the
formulation, process and cooking methods can affect the sensory quality
(Jiménez-Martín et al., 2015, 2016). However, it is worthwhile to
mention that most of evaluators scored the TRG treatments like as
control. Overall, addition of fish oil in microcapsule form could not ef­
fect on the sensory properties of the product. This is compatible with
results of Sell et al. (2015), which surimi fortified with different sources
of fatty acid (flaxseed and fish oil) did not showed significant ranking
between the samples. Ghelichi, Shabanpour, and Pourashouri (2018)
stated that emulsified carp roe oil decreased fishy odor in fish sausages.
4. Conclusion
In this study, chicken nuggets were enriched with fish oil and
microcapsulated oil during frozen storage. The nugget samples (1% fish
oil) showed higher TBARS and CD values than enriched nugget samples
by encapsulated fish oil (TRG and CGN (5%)). The sensory evaluation of
TRG and CGN nuggets showed no difference when compared to control
nuggets. All the fortified nuggets by fish oil microcapsules indicated
good acceptability. At first, addition of free and encapsulated fish oil
increased the EPA and DHA contents in chicken nuggets and the
encapsulated oil showed more efficiency to preserve EPA and DHA
during storage. The pre-fried nuggets showed suitable fatty acid profile
and encapsulation of fish oil maintains fatty acid properties during
frozen storage. Therefore, these findings provided the overview of the
characteristics of functional chicken nuggets fortified with TRG and
CGN and proved the suitability of this method and wall material to the
encapsulation of fish oils and delivery through chicken nuggets.
Author declaration
We wish to confirm that there are no known conflicts of interest
associated with this publication.
CRediT authorship contribution statement
Parastoo Pourashouri: Conceptualization, Methodology, Supervi­
sion. Bahareh Shabanpour: Data curation, Methodology. Sakineh
Heydari: Resources, Investigation, Visualization, Writing - original
draft. Sara Raeisi: Investigation.
Declaration of competing interest
None.
Acknowledgment
This work was supported by the Gorgan University of Agricultural
Science & Natural Resources [grant number 94-336-10].
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.lwt.2020.110334.
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