Food Research International 137 (2020) 109353

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Food Research International

journal homepage: www.elsevier.com/locate/foodres

Review

Advantages of techniques to fortify food products with the benefits of fish oil T
a b,c d,e f,⁎
Aniseh Jamshidi , Hui Cao , Jianbo Xiao , Jesus Simal-Gandara
a
Department of Fisheries, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran
b
Guangdong-Macau Traditional Chinese Medicine Technology Industrial Park Development Co., Ltd, Hengqin New Area, Zhuhai 519031, China
c
School of Pharmacy, Chengdu University of Traditional Chinese Medicine, Chengdu 611137, China
d
International Institute of Dietary Nutrition and Safety, Jiangsu University, Zhenjiang 212013, China
e
Institute of Food Safety and Nutrition, Jinan University, Guangzhou, China
f
Nutrition and Bromatology Group, Department of Analytical Chemistry and Food Science, Faculty of Food Science and Technology, University of Vigo - Ourense Campus,
E-32004 Ourense, Spain

A R T I C LE I N FO A B S T R A C T

Keywords: Fish oil has been widely applied in fortified food products because of its special health benefits especially
Fish oil containing high unsaturated fatty acids mainly docosahexaenoic acid (DHA) and eicosapentaenoic acid (EPA).
Fortification Nowadays, there are various foods fortify with fish oil available in the market. The main challenge of for-
Functional food tification of food products with fish oil is its highly susceptible to oxidation and its influence on sensory attri-
Oxidation
butes during storage. The fortification methods such as direct addition through bulk fish oil, emulsion or mi-
Sensory attributes
croencapsulation could effectively improve the oxidative stability of fish oil and mask unpleasant fishy flavour in
fortified products. Therefore, this article provides a review of techniques, their advantages and limitations,
together with the effects of incorporating fish oil in foods products.

1. Introduction
Increasing consumer demand for functional foods that contains
specific ingredients has led to consumers looking for foods, which
capable influencing health benefits and body function besides meeting
basic nutrition needs. In the nutrition science, attention has been given
to design, fortification and production of functional foods using
bioactive and nutraceuticals compounds. In this regard, production of
functional foods has a growing market accompanied by investigation to
produce new products. Therefore, products that claimed higher health
benefits are more successful (Jiménez-Colmenero, 2013).
Various studies have shown the beneficial effects of fish oil on
human health (Botrel, de Barros Fernandes, Borges, & Yoshida, 2014;
Pourashouri et al., 2014). Fish oils are known as a rich source of the
long-chain polyunsaturated omega-3 (n-3) fatty acids, containing doc-
osahexaenoic acid (DHA; 22:6n-3) and eicosapentaenoic acid (EPA;
20:5n-3) (Pourashouri et al., 2014). From chemical aspect, fatty acids
composed of hydrocarbon chains accompanied by a carboxyl (–COOH)
and methyl (–CH3) groups at each ends. Fatty acids have various length,
location of double bonds, and degree of unsaturation. When the first
double bonds placed in third carbons from methyl end, the fatty acids
known as Omega-3 fatty acids (Ellulu et al., 2015).
The high content of n-3 fatty acids and beneficial effects on human
health (especially for heart, brain, and nervous system functions) ex-
isting in fish oil led to consider it as functional components. Hence, the
pharmaceutical and food industries have attentiveness to use the fish
oil. Using dietary fish oil is one of methods for providing daily re-
quirement for fatty acids. Incorporating of fish in various products is
other method to use fish oil in food industry and easier handle of fish
oils (water-insoluble, oxidative susceptibility). On the other hand, meet
the needs for fatty acids in areas with less access to fresh fish or for
people who are not interested in consuming fish can obtain through the
fortification of food products by fish oil.
One of limitation of application fish oil for human conception and in
food industry is high susceptible of n-3 fatty acids to oxidation. The
addition of fish oil for fortifying food is challenging could overcome by
adding various antioxidants (e.g., trans-cinnamaldehyde, clove, vitamin
C, vitamin E, polyphenol), applying nano-/micro-encapsulation tech-
nique and masking fishy taste using flavouring agent (Jo, Chun, Kwon,
Min, & Choi, 2015). Furthermore, sensory attributes and evaluation of
shelf-life of fortified products by fish oil are important points in this
field of study and should be taken into consideration.
This review discusses the specific possibilities of using fish oil in
food industry as functional food. The present article highlights the
benefits of fish oil for human health, limitation of fish oil in food ap-
plication, and techniques used for incorporating fish oil in food

⁎
Corresponding author.
E-mail address: jsimal@uvigo.es (J. Simal-Gandara).

https://doi.org/10.1016/j.foodres.2020.109353
Received 16 January 2020; Received in revised form 20 May 2020; Accepted 24 May 2020
Available online 26 May 2020
0963-9969/ © 2020 Elsevier Ltd. All rights reserved.
A. Jamshidi, et al.
products. Furthermore, the fortified products using fish oil and effects
of incorporating of fish oil in food products discussed.
2. Benefits of fish oil for human health
Preventing of cardiovascular diseases, cancer (colon, breast, and
prostate), and Alzheimers disease have been reported through con-
sumption of fish oil (Boran, Karaçam, & Boran, 2006). Furthermore,
fatty acids of fish oil may have been considered to treat other diseases
including obesity, Type-2 diabetes, depression, non-alcoholic fatty liver
disease, and inflammation (Ellulu et al., 2015). Researches have shown
that besides the reducing risk of cardiovascular disease, omega-3 fatty
acids also improved heart rate, reduced the risk of heart attack, blood
pressure, blood lipid levels, and hardening of the arteries (Ellulu et al.,
2015). Kaul et al. (2008) reported that giving dietary polyunsaturated
fatty acids (fish, flaxseed, and hempseed) to 86 healthy volunteers
(male and female) during 12 weeks, resulted in increasing plasma levels
of DHA and EPA with fish oil supplementation, transiently increasing of
alpha linolenic acid with flaxseed oil supplementation, and non-chan-
ging the concentration of plasma fatty acid with hempseed oil supple-
mentation. In order to achieve cardiovascular health benefits, they
stated that consumption of two capsules (with any of these oils) might
not provide the expected result during 3 months’ period. In this regard,
Harris, Pottala, Sands, and Jones (2007) investigated the consumption
oily fish or taking fish oil capsules on cardiovascular health benefits in
healthy premenopausal women by consuming 485 mg EPA and DHA
through serving oily fish (salmon and albacore tuna) twice per week or
taking 1–2 capsules per day during 16 weeks. They suggested that the
effect of serving weekly oily fish or daily fish oil capsules containing
equal contents of EPA and DHA showed equally effect on the amounts
of n-3 fatty acids in blood lipids. On the other hand, given the benefits
of Omega-3 fatty acids such as decreased insulin resistance and trigly-
cerides, and increased HDL, the use of omega-3 fatty acids appears to be
appropriate in combination with weight loss programs (DeFina,
Marcoux, Devers, Cleaver, & Willis, 2010). Decreasing body fat mass by
using fish oil supplement have been reported in some studies, although
other studies have been shown no relation among weight loss and the
Omega-3 fatty acid consumption (DeFina et al., 2010).
Serving two to three times per week of seafood is recommended to
meet the advised level of fatty acids for pregnant women, children and
elderly people (Olsen & Secher, 2002). However, there are re-
commendations for different targets/effects of fatty acids consumption:
0.2–0.65 g/day to get general good health, 1 g/day to prevent myo-
cardial infarction, 2–4 g/day to reduce blood triglyceride (Kris-
Etherton, Harris, & Appel, 2002). In individuals who do not regularly
consume fish and seafood, the amounts of EPA and DHA fatty acids are
likely low. When individuals do not desire changing their lifestyles and
eating habits and consume more fish, they can achieve their needs to
EPA and DHA through the fortified foods or fish oil capsules. Without
changing dietary habits, individuals can achieve desired amounts of
fatty acids with consumption a single fish oil capsule per day, which
contain 1 g fish oil and supply about 0.3 g EPA and DHA per day (Calder
& Yaqoob, 2009). There are two strategies to supply fatty acids through
food fortification, which includes fortifying meat and dairy products
with fish oil, and to feed livestock with fatty acids resulted fortification
of milk, meat, and eggs with EPA and DHA. Food processing or storage,
and metabolic pathway in the animals limit the level of incorporation of
fish oil in food products or feeding livestock. Anyway, it is a good op-
tion to increase the fatty acids intake in individuals who do not interest
to change their eating habits (Calder & Yaqoob, 2009).
3. Fish oil limitation for food application
3.1. Oxidation
The high susceptibility to oxidative deterioration is one of the major
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Food Research International 137 (2020) 109353
issues related to fish oil n-3 fatty acids (Pourashouri et al., 2014). Au-
toxidation takes place in three stages. Initiation is the formation peroxyl
radicals followed by hydroperoxides from reaction of free radicals of
unsaturated fatty acids with oxygen). Propagation is due to peroxyl
radicals attacking more double bonds and forming a new free radical
and hydroperoxide. Finally, the termination is the formation of non-
reactive substances such as aldehydes, alcohols, acids, and ketones from
reaction free radicals with each other, the most important cause of
deterioration in quality (Boran et al., 2006). During photooxidation, UV
energy is absorbed by oil or food systems containing oil, moved to
higher energy state, and produced singlet oxygen, which attack un-
saturated fatty acids to produce peroxyl radicals and then hydroper-
oxides. The physical form of oil, temperature, and microcomponents in
the oil (such as hydroperoxides, free fatty acids, and pigments) were
influenced on extent of oxidative deterioration. (Boran et al., 2006).
Methods including peroxide value (PV), thiobarbituric acid (TBA), acid
value (AV) and unsaponifiable matter (USM) are commonly used for
evaluation and monitoring oxidative degradation of oils and food pro-
ducts containing oil during storage. The acceptability and quality of oils
for human consumption are limited in range of 8 meqO2/kg of oil of PV
and 7–8 mg malonaldehyde/kg of oil of TBA according to the regulatory
agencies (Huss, 1988).
Therefore, the protection of fish oil in order to make it more stable
during usage and storage is necessary. Beside the controlling environ-
mental conditions including inhibition of high temperature during
processing, prevention of exposure to light and oxygen, and storage at
or below 20 °C in the dark, the application of antioxidants has sig-
nificant effects on the protection of fish oil (Boran et al., 2006; Huss,
1988). The application of antioxidants including calcium disodium
ethylenediaminetetraacetate (EDTA) (Let, Jacobsen, Frankel, & Meyer,
2003), propyl gallate, citric acid ester (Let, Jacobsen, & Meyer, 2004),
α- and γ-tocopherol mixture, and ascorbyl palmitate (Let, Jacobsen,
Pham, & Meyer, 2005), in combination with rapeseed oil were in-
vestigated to protect milk product fortified with omega-3 fatty acids
from fish oil against oxidation. The results indicated that EDTA alone
did not showed antioxidant properties in the milk emulsions fortified
with fish oil and the addition of rapeseed oil containing natural toco-
pherols to fish oil was effective for inhibiting oxidation. The prediction
of oxidative stability of Kilka oil were evaluated by the artificial neural
network (ANN) and neuro-fuzzy inference system (ANFIS) modelling
with three inputs including antioxidant type (gallic acid and methyl
gallate as natural antioxidants), temperature (35, 45, and 55 ⁰C) and
concentration (0, 200, 400, 800 and 1600 mg L−1). The results in-
dicated that the best model which shown high sensitivity of oxidation
parameters specially the induction period on concentrations of methyl
gallate and gallic acid was ANFIS which showed the effects of anti-
oxidants on predict retard oil oxidation and enhance Kilka oil shelf-life
(Asnaashari, Farhoosh, & Farahmandfar, 2016). The effects of Spirulina
(Arthrospira platensis) (Golmakani, Moosavi-Nasab, Keramat, &
Mohammadi, 2018) and Ghure (unripe grape) marc (Golmakani,
Keramat, Moosavi-Nasab, & Moosavian, 2017) extracts on oxidation
stability of kilka (Clupeonella cultriventris caspia) oil were investigated
during 15 days at 60 °C in comparison with the effects of BHT and β-
carotene. The lower Totox, peroxide and p-anisidine values were ob-
served in kilka oils treated with Spirulina and Ghure compared with the
control group during storage.
Essential oils, which are aromatic oily liquids extracted from plants,
have emerged as natural antioxidants. These oils are obtained from
oregano, rosemary, clove, thyme, sage and mint and contained phe-
nolics, terpenes, and alcoholic compounds (Jayasena & Jo, 2013). The
induction period (IP), which showed the stability or shelf-life of edible
oils, of fish oil were prolonged after addition of basil (Ocimum basilicum
L.), thyme (Thymus serpyllum L.) and oregano (Origanum vulgare L.)
extracts under accelerated oxidation (80, 100 and 120 °C) (Šimat et al.,
2017). Antioxidant assay of mixtures of tocopherols, ascorbyl palmi-
tate, green tea catechins and rosemary extract on omega-3 fish oil was
A. Jamshidi, et al.
conducted and decreased lipid oxidation was reported 30% by ascorbyl
palmitate and rosemary mix and 40% by ascorbyl palmitate and toco-
pherol mix more than the effects of each single components. Further-
more, the addition of green tea extracts in combination with other
antioxidants showed synergistic influence and resulted in increase the
stability of n-3 fish oil (Moen, Stoknes, & Breivik, 2017). Oxidative
stability of essential oil and aqueous extract of ginger (Zingiber offici-
nale) in fish oil-in-water emulsion (5%) (Kumari, Venkateshwarlu,
Choukse, & Anandan, 2014), and stevia rebaudiana stem (SRS) on fish
oil of Yellowfin tuna (Thunnus albacares) (Yu et al., 2017), have also
been proposed the high protection of herbal extract and essential oils
against lipid oxidation of fish oils. In this regard, Mezza et al. (2018)
and Keramat, Golmakani, Aminlari, and Shekarforoush (2016) also
reported the antioxidant activity of Bunium persicum and Rosmarinus
officinalis essential oils on sunflower and olive oils, respectively.
Encapsulation is one of the most known techniques using for
coating, protecting against oxidation. There has been more interest
recently in designing emulsions than in enhancing the nutritive and
oxidative aspects of food fortified with fish oil (Jamshidi, Shabanpour,
Pourashouri, & Raeisi, 2018). Nielsen and Jacobsen (2009) fortified
energy bars with 5% fish oil through pre-emulsification of the fish oil
with sodium caseinate and reported higher oxidative stability in the
energy bars with addition 100–2000 ppm of the metal chelator ethy-
lenediaminetetraaceticacid (EDTA) to emulsified fish oil. The anti-
oxidant effects of medium chain triglycerides, lemon oil, and thyme oil
were investigated as carrier for fish oil in nanoemulsions and the results
showed a high impact on oxidative stability of fish oil nanoemulsions as
following order: thyme oil > lemon oil > MCT (Walker, Gumus,
Decker, & McClements, 2017). Adding palmitic acid (as solid lipid) and
quercetin (as antioxidant) for fish oil encapsulation were investigated in
a whey protein isolate (WPI) of nanoparticle emulsion and resulted in
improving physical properties and oxidative stability of emulsions
(Azizi, Li, Kaul, & Abbaspourrad, 2019). The oxidative stability of for-
tified cow milk and soy milk with fish oil incorporating rosemary ex-
tract was evaluated and the results showed that the effects of rosemary
extracts on lipid oxidation was higher in cow milk than the soy milk,
which indicated the role of food components on the fate of bioactive
antioxidant ingredients in a specific food product (Qiu, Jacobsen, &
Sørensen, 2018). The oxidative stability of shrimp and tuna salads
containing mayonnaise (with or without fish oil) were evaluated, and
the results proved that asparagus in fish oil fortified shrimp salad
showed antioxidation effects, as well as the spices in fish oil fortified
shrimp showed following antioxidation effects as following: or-
egano > rosemary > thyme (Sørensen, Nielsen, & Jacobsen, 2010).
Hermund et al. (2015) stated that the water extract from Fucus vesicu-
losus demonstrated lower oxidative deterioration in milk or mayonnaise
fortified with fish oil, which was related to high phenolic and car-
otenoid contents.
3.2. Sensory attributes
Sensory attributes are one of the most important parameters that
affects the marketability and acceptability of food products by con-
sumers. The reaction between carbonyl compounds and amine com-
pounds in food products resulted in browning reaction that produce
cooked flavour compounds (Shibamoto, 1996). In the oil rich food, such
as fish or fish oil, the oil ingredients have been important role in for-
mation of browning-flavour compounds as precursors of carbonyl
compounds. During the oxidation process, the carbonyl compounds and
free radicals that were made from degradation of polyunsaturated fatty
acids, reacted with amine compounds and produced a cooked flavour
(Lee, Macku, & Shibamoto, 1991). Several flavour volatile including
aldehydes and ketones are produced as a result of the oxidation and
breakdown of hydroperoxides generated during oxidation process. The
volatile compounds including 2,6-nonadienal, 4-heptenal, and 3,6-
nonadienal are responsible to unacceptable fishy flavour of EPA and
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Food Research International 137 (2020) 109353
DHA containing fish oils. Karahadian and Lindsay (1989) reported that
the developing green and cucumber flavours caused by 2,6-(trans, cis)-
nonadienal, 2-trans-hexenal and 1-cis-5-octadien-3-one compounds
during initially menhaden oil oxidation. By depletion 2,6-trans, cis-
nonadienal and decreasing the green flavour, the 4-cis-heptenal com-
pound appears which characterizing burnt flavour, following by
trans–cis-cis- and trans–trans–cis-2,4,7-decatrienal compounds result to
burnt/fishy or cod liver oil-like flavours which demonstrated oxidized
fish oil. The using of propyl gallate mixtures as an antioxidant in for-
tified mayonnaise with fish oil promoted the development of fishy and
rancid off flavours which related to volatile oxidation compounds in-
cluding 3-furaldehyde, 2,4-heptadienal, 2,4-decadienal and ethyl ben-
zene (Jacobsen et al., 1999).
Raymond (1994) stated that trimethylamine oxide (TMAO), which
is present in fish and fish oil, could form various amine compounds
during thermal degradation. So, the carbonyl compounds created from
lipids can be react with amines formed from TMAO and led to produce
flavour compounds. The efficacy of spray-drying on sensory attributes
of produced fish oil microcapsules using modified cellulose, skim milk
powder, and a mixture of fish gelatine and corn-starch was evaluated
during the storage in presence of air and under vacuum conditions. The
results demonstrated that undesirable odour attributes and peroxide
value were increased in fish oil powders stored in air and elimination of
the air improved the odour profile and stability of samples during
storage (Kolanowski, Jaworska, Weißbrodt, & Kunz, 2007). Addition of
strawberry flavour (8%) and antioxidants/pro-oxidant of citric acid,
vitamin K, iron, and EDTA into fortified drinking yoghurt with fish oil,
rapeseed oil, or a mixture of fish oil and rapeseed oil resulted in
masking fishy off-flavour; the volatiles did not increase and the rape-
seed oil did not reduce the peroxide values (Nielsen, Debnath, &
Jacobsen, 2007). The oxidative stability and sensory evaluation of en-
ergy bars fortified with microencapsulated fish oil powder or fish oil
emulsion were investigated and the results showed that in the emulsi-
fied fish oil samples, the protection methods with sodium caseinate
were similar to modified atmosphere, although the EDTA had more
protection. The sensory analysis showed that there were no differences
in fishy flavours in samples containing fish oil powder or fish oil
emulsion (Nielsen & Jacobsen, 2009).
4. Methods and techniques for incorporating fish oil in food
products
Foods products containing fish oil also can be considered as func-
tional food group because of preventing of several diseases and im-
proving the state of health (Jiménez-Martín, Gharsallaoui, Pérez-
Palacios, Carrascal, & Rojas, 2015). Despite the high health benefits of
fish oil, its application in the food industry limited by low solubility,
oxidation susceptibility, undesired fishy flavour and poor handling
properties. (Aghbashlo, Mobli, Madadlou, & Rafiee, 2013; Wang, Tian,
& Chen, 2011). Extensive studies have been done to overcome on these
limitations and various methods have been investigated to fortify food
products with fish oil. Direct addition of bulk fish oil, emulsification
and microencapsulation techniques are the most common methods used
for fortifying of food products with fish oil. In case of adding bulk fish
oil, incorporation flavouring compounds is necessary for masking the
undesired fishy flavour. It seems that among these methods, micro-
encapsulation, which including enclosed active compounds as a core
within the secondary materials as a wall, is more efficient for fortifying
food products with fish oil. In this case, fish oil can be converted from
liquid form to a powdered encapsulated form, which led to improve its
handling and flow properties. On the other hand, encapsulation can
protect fish oil against moisture, heat, light or oxidation (Jafari, As-
sadpoor, and Bhandari, 2008).
A. Jamshidi, et al.
4.1. Using bulk fish oil
Fortification with bulk fish oil is not suitable for any kind of food
products, so fats, and foods products containing flavouring compounds
that can masking unpleasant fishy taste are more appropriate
(Kolanowski and Laufenberg, 2006). There were not many new study
conducted on adding bulk fish oil directly to the food products and
more of researches were investigated the addition various antioxidant
compounds in food products fortified with bulk fish oil. The using of
antioxidants in fortifying food products with bulk fish oil was suggested
in order to prevent fish oil oxidation and reduce the levels of free ra-
dicals and lipid hydroperoxides which influenced the profile of volatiles
and developed unpleasant off-odours and off-flavours (Drusch, Groß, &
Schwarz, 2008). The combinations of effects of various antioxidants
including tocopherols (α-, γ- and/or δ-), rosmarinic acid, rosemary
extract rich in carnosic acid, lecithin, and citric acid were evaluated for
achieving the stability of bulk fish oil. The results showed that with
high concentration of γ- or δ -tocopherol and low in α-tocopherol, by
containing tocopherol-sparing synergists such as ascorbyl palmitate and
carnosic acid from rosemary extract and metal-chelating agents, such as
citric acid showed the higher efficiency in stabilisation of bulk fish oil
(Drusch et al., 2008).
Kolanowski and Laufenberg (2006) evaluated the fortification of
various market food products including soybean salad oil, milk, fla-
voured yogurt, orange drink, apple-beetroot juice, soft margarine, and
mix of butter and vegetable oil by adding fish oil. They are stated that
only salad oil and fat spreads were fortified up to 1.5% by fish oil, while
flavoured yoghurt was proposed at range up to 0.75% fish oil. In this
study, milk, orange drink and vegetable juices were not suitable for this
kind of fortification because of the accumulation of fish oil on their
surface, as well as needed to more flavours and sweeteners for masking
fishy taste. In contrast, Let et al. (2003) reported that fortification of
milk with fish oil (1.5% wt, highly unsaturated tuna oil and cod liver
oil) was possible and unpleasant fishy flavour could not be detected
specially in samples fortified with tuna oil. It could be related to the
emulsification process and present EDTA in order to increase oxidation
stability. In study of fortification of milk with milk fat (1.0% w/w), fish
oil (0.5% w/w) or fish oil:rapeseed oil mixture, Let et al. (2005) stated
that the fortified milk was showed acceptable sensory attributes but it
was necessary to application of a mixture of fish oil and rapeseed oil
with PV values below than 0.5 meq kg−1.
On the other hand, the lack of correlation between chemical oxi-
dation markers and sensorial attributed of panel response have been
reported in evaluation of different marine oils (Macfarlane, Salt, Birkin,
& Kendrick, 2001). This could be related to this fact that lipid hydro-
peroxides may not responsible for off-flavour formation (Frankel,
Huang, Prior, & Aeschbach, 1996). Chee et al. (2005) also stated that
fruit flavours (strawberry in milk or strawberry-banana in yogurt)
might be extremely useful in masking the slight fish flavour inherent in
even freshly prepared omega-3 PUFA emulsions.
In several studies, food products have been fortified with bulk fish
oil or algae oil which containing different antioxidants including ro-
semary extracts in bulk fish oil or oil-in-water emulsions and fish oil
emulsions (Frankel et al., 1996), and EDTA and gallic acid in mayon-
naise containing 16% fish oil and 64% rapeseed oil (Jacobsen et al.,
1999). It is claimed that the hydrophilic rosemary antioxidants oriented
in the air-oil interface and showed more protection in the bulk oil
systems than the oil in water emulsion systems which partitioning into
the water phase (Frankel et al., 1996). As Jacobsen et al. (1999) re-
ported using EDTA as antioxidant in mayonnaise containing 16% fish
oil and 64% rapeseed oil decreased the formation of free radicals, lipid
hydroperoxides, volatiles, and fishy and rancid off-flavours, but gallic
acid although reduced the formation of free radicals and lipid hydro-
peroxides but developed the oxidative flavours. Nielsen et al. (2007)
also fortified drinking yogurt with fish oil incorporating with citric acid
ester, vitamin K, and EDTA as antioxidants. They demonstrated that the
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Food Research International 137 (2020) 109353
fortified yogurt with fish oil was very stable compared to yogurts
containing rapeseed oil or a mixture of rapeseed oil and fish oil during
storage for 29 days, as well as the antioxidative effects of EDTA and pro-
oxidative effects of vitamin K were indicated.
4.2. Emulsions
The most common step for formation microcapsules of fish oil is
producing of an emulsion. The nonpolar fish oil droplets can be dis-
persed in aqueous systems through emulsification using a surface-active
carrier. For fortifying food products, emulsions of fish oil were able to
use directly (in meat systems or beverages) or prepared into micro-
capsules/powdered by remove the solvent (water) from the system
(Drusch, 2012). Fish oil, in its emulsified form, was added during
production of mortadella (Cáceres, García, & Selgas, 2008), various
other meat products (Lee, Faustman, Djordjevic, Faraji, & Decker,
2006), energy bars (Hermund et al., 2015; Horn, Nielsen, & Jacobsen,
2009; Nielsen & Jacobsen, 2009) or pan bread (Serna-Saldivar, Zorrilla,
De La Parra, Stagnitti, & Abril, 2006).
Recently, emulsion based delivery systems showed an increasing
interest as an appropriate technology for incorporating and protecting
lipids in food products (Salminen, Herrmann, & Weiss, 2013). Poyato
et al. (2013). There are different types of emulsion delivery systems
including solid lipid particles, filled hydrogel particles and conven-
tional, multiple and multilayer emulsions (McClements, 2010). Some
studies reported using emulsion delivery systems as fat substitute to
improve the nutritional quality and healthier lipid profiles of food
products (Berasategi, Barriuso, Ansorena, & Astiasaran, 2012; García-
Iñiguez de Ciriano et al., 2010). As emulsions are thermodynamically
unstable, different strategies used to overcome on the instability factors
of emulsions such as creaming, coalescence, Ostwald ripening, and
aggregation. Emulsion characteristics plays a key role in stability of
microencapsulated fish oil. For example, Jafari, Assadpoor, He, and
Bhandari (2008) used different emulsifying systems to investigate the
emulsion size of fish oil droplets and reported that smaller droplet size
produced higher encapsulation efficiency.
Using methods including low pressure by membrane emulsification,
high pressure by high-pressure homogenizer, de-agglomeration to form
nano-sized particles by ultrasonication, and microencapsulation by
microfluidization techniques led to force fish oil droplets dispersed into
a continuous aqueous phase, which resulted in microcapsules with high
encapsulation efficiency, loading capacity and strong protection against
fish oil oxidation (Chatterjee & Judeh, 2016). Various techniques in-
cluding spray-drying, freeze-drying, spray-granulation or extrusion
have been used to convert the emulsion into microcapsules. In order to
reinforce the microcapsule structure, solidification of emulsions also
can be carried out by adding a cross-linking reagent (e.g. transgluta-
minase), or coacervating with oppositely charged polysaccharides be-
fore applying the drying method (Drusch, 2012). Three processing
steps, needed to apply these techniques for producing fish oil micro-
capsules, are included: (a) emulsification, (b) high pressure homo-
genizer (Jamshidi, Antequera, Solomando, and Perez-Palacios, 2019) or
ultrasonic atomization (Chatterjee & Judeh, 2016), followed by, (c)
freeze or spray-drying. The three steps of coacervation, membrane
emulsification followed by freeze-drying also applied for micro-
encapsulation of fish oil and resulted in microcapsules with high
loading capacity (Chatterjee & Judeh, 2016).
Several emulsions have been developed as delivery systems to en-
capsulate fish oil including conventional emulsions (O/W), micro/na-
noemulsions, multilayer emulsions (using layer-by-layer deposition
technology), double emulsions, and filled hydrogel beads (Gudipati,
Sandra, McClements, & Decker, 2010). Jo, Kwon, Min, and Choi (2015)
developed multi-layered fish oil emulsions using Tween 20 (1.25%),
chitosan (0.1%), and low methoxyl pectin (0.2%) as primary, sec-
ondary, and tertiary layers, respectively, and reported higher oxidation
stability and lower fish off-flavours in all multi-layered emulsions
A. Jamshidi, et al.
comparing with O/W emulsions containing a single layer. The double
emulsion and gelled emulsion discussed in this section as emulsion-
based delivery systems for fish oil.
4.2.1. Double emulsion
Double emulsions consist of initial simple water in oil emulsion
(W1/O) dispersed into outer continuous aqueous phase (W2) (Freire,
Bou, Cofrades, Solas, & Jiménez-Colmenero, 2016). The water-in-oil-in-
water (W/O/W) and oil-in-water-in-oil emulsions (O/W/O) are two
kinds of double emulsions, but W/O/W is the most common using form
of double emulsions and O/W/O could also be applied in specific ap-
plications (Jiménez-Colmenero, 2013).
As simple (O/W or W/O) emulsion delivery system did not show
sufficient satisfactory performance in protecting encapsulation in-
gredients against chemical degradation or controlled release, there are
a rising interest to use other delivery systems which demonstrated more
advantages than simple emulsions (Andrade, Wright, & Corredig,
2018). Using double emulsions in food applications demonstrated some
advantages such as mask flavours, prevent oxidation, improve sensory
attributes, and control release of ingredients. Regarding to the fat
content in functional foods, double emulsions act as improve qualitative
and quantitative of fat through reducing the fat content and providing
healthier fatty acid profiles (Freire et al., 2016). In this sense, Freire
et al. (2016) reported using double emulsions as fat substitutes in meat
products in order to improve fat quality. Moreover, W/O/W double
emulsions could be used in order to deliver hydrophilic and hydro-
phobic ingredient in the same system (Sagalowicz & Leser, 2010).
The main challenge of application of double emulsions in food
products is its thermodynamic instability. The instability factors of
double emulsions such as swelling or shrinkage of the inner droplets,
flocculation, and coalescence, resulted in phase separation through
releasing the inner aqueous droplets in the outer aqueous phase
(Dickinson, 2011). Although two different emulsifiers (lipophilic for W/
O and hydrophilic for W/O/W) are necessitated to reduce interfacial
tension of oil and water, well-designed double emulsion phases have
also been offered to increase double emulsions stability (Andrade et al.,
2018). In this sense, addition of WPI, starch or gelatine in order to
gelation of inner queues phase has been increase stability and en-
capsulation efficiency of double emulsions (Iancu, Chevalie, Popa, &
Hamaide, 2009; O'Regan & Mulvihill, 2010). The application of am-
phiphilic macromolecules and stabilizers including as proteins and
carbohydrates in order to improve double emulsion stability have been
also reported in literatures (Jamshidi et al., 2018; Poyato et al., 2013).
The most used lipophilic emulsifier for stabilising of W/O phase in
double emulsion is anonionic emulsifier of Polyglycerolpolyricinoleate
(PGPR), although it has GRAS status (generally recognised as safe)
leading interest to reduce its content in food. Jiménez-Colmenero
(2013) reviewed using hybrids of natural polymers in double emulsion
stability and application of double emulsion in functional food, re-
spectively.
4.2.2. Gelled emulsion
Gelled emulsion is an emulsion with a gel-like network structure
and solid-like mechanical properties (Serdaroğlu & Öztürk, 2017). The
most common method for preparing gelled emulsion is including ad-
dition of oil phase to aqueous phase containing hydrocolloids such as
carrageenan and alginate as gelling agents. In the next step, the emul-
sions cooled down to room temperature for allowing the hydrocolloid
to polymerize and then kept overnight under refrigeration (Alejandre,
Poyato, Ansorena, & Astiasarán, 2016). Gelled emulsion could be
helped reformulation processes of different meat products by mi-
micking hardness and water holding capacity in comparing to oil in
water emulsions (Poyato et al., 2013).
The application of simple and double gelled emulsion in food pro-
ducts have been described in the literature, although there were few
reported in developing of gelled double emulsions. Reducing fat,
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providing healthier fatty acid profile, and encapsulating hydrophilic
and lipophilic bioactive compounds could be achieved by using gelled
double emulsions for food applications Freire et al. (2016). Although
gelled emulsions showed more kinetically stability than simple emul-
sions, but higher energy also needed for the homogenization process of
gelled emulsions (Picone, Bueno, Michelon, & Cunha, 2017). Two steps
procedure have been used to prepare gelled double emulsions. At first
step, a double emulsion in liquid form is prepared and then by gelling
continuous phase at second step, is transformed into gelled emulsion
using thermal, enzymatic or chemical procedures (Dickinson, 2011;
Jiménez-Colmenero, 2013). Several hydrocolloids (pectin, alginate,
gellan gum, etc.) were applied in outer aqueous phase of double
emulsions to assist gelling in order to form the gelled emulsions
(Dickinson, 2011; Jiménez-Colmenero, 2013; Picone et al., 2017) in
combination with gelatine and microbial transglutaminase followed by
achieving the solid like properties at room temperature (Flaiz et al.,
2016).
Gelation rate is the most important step in production gelled
emulsions which defined the mechanical properties and resistance of
microcapsules to stress conditions during storage, ingestion and diges-
tion. (Picone & Cunha, 2011). Therefore, during the formation of gel
must ensure that the gelled emulsions are formed earlier than emulsion
flocculation and droplet coalescence. Considering that gelation can be
promoted using slow decrease in pH, it is important to know the ge-
lation rate of the aqueous phase leads to a more organized structure
and, thus, stronger and more deformable gels (Picone et al., 2017).
4.3. Encapsulation
Microencapsulation is a unique technique that has been used to coat
or entrap sensitive ingredients as core material within another one as
wall materials that consists a protective shell or wall (Pourashouri et al.,
2014). Protecting of core materials from adverse effects of environ-
mental conditions (light, moisture, and oxygen), controlling release of
ingredients at a particular time and location, masking of an off-flavours
taste or odours, modifying of the physical attributes and handling
properties by converting liquids to solids form, and improving oxidative
stability are intended to be achieved by microencapsulation (Piacentini,
Giorno, Dragosavac, Vladisavljević, & Holdich, 2013). There are many
encapsulation technique such as physical processes including spray-
drying, spray-chilling/coating, freeze-drying, extrusion or fluidised bed
coating, chemical processes including molecular inclusion, and physi-
cochemical techniques including single- or multi-core complex coa-
cervation and liposome entrapment (Kralovec, Zhang, Zhang, &
Barrow, 2012).
Selecting the core and wall material, designing formulation of
emulsion (ratio of core to wall), and selecting the suitable encapsulation
technology involved to produce fish oil microencapsulation. Higher
encapsulation efficiency and oxidative stability during storage revealed
a good microencapsulation system for fish oil microcapsules (Kaushik,
Dowling, Barrow, & Adhikari, 2015). Since, each drying technology and
coating materials had some advantages and disadvantages, so, through
a careful examination, designing an emulsion and selecting each drying
methods resulted in fish oil microcapsules with higher quality (Anwar &
Kunz, 2011). In this section, various microencapsulation technologies
are discussed with emphasis on fish oil microencapsulation.
4.3.1. Spray-drying
Microencapsulation of fish oil by spray-drying is the most frequently
used method which applied various carbohydrates, gums, proteins, and
synthetic polymers in aqueous phase of O/W emulsions (Anwar and
Kunz, 2011; Serfert, Drusch, Schwarz, 2009; Jafari et al., 2008;
Czerniak, Kubiak, Białas, & Jankowski, 2015). The basic process of
spray-drying involves dissolving the core material in a dispersion of the
wall material, producing an emulsion, pumping of the emulsion within
atomised chamber, atomising the emulsion into heated air, dehydrating
A. Jamshidi, et al.
the droplets and producing microcapsules (Anwar & Kunz, 2011). De-
pending on the characteristics of the core and wall materials, attributes
of the infeed emulsion, and operating conditions of the spray-drying,
the microcapsules size could be vary from 10–50 µm at the fine end to
2–3 mm at the large end (Nedovic, Kalusevic, Manojlovic, Levic, &
Bugarski, 2011). The inlet and outlet temperatures, airflow and hu-
midity, and powder particle size are the most important operating
conditions affecting the quality of spray-dried microcapsules. The
quality of spray-dried microcapsule is quite dependent on the spray-
dryer operating parameters and properties and the composition of the
feed emulsion.
However, high application of spray-dryer has been reported because
of its low cost, flexible, easy to scale-up and using available equipment,
there are some disadvantages of this method have been stated in some
literates. According to the short drying times, it was stated that using
spray-drying is useful for encapsulating heat-sensitive ingredients such
as fish oil. Although the short drying times and the high rate eva-
poration of water kept the core temperature below 100 °C during sur-
face film solidification (Jafari et al., 2008), the application of high air
temperature during drying the emulsions by spray-drying resulted in
producing microcapsules with a porous structure. Therefore, non-en-
capsulated oils presented on the surface or in the porous structures of
the microcapsules promoted the system to form peroxides and develop
unpleasant off-flavour (Anwar & Kunz, 2011; Kolanowski et al., 2007).
On the other hand, the high temperature used in spray-drying
leading to increase the oxidation during process and caused chemical
and sensory deterioration of fish oil. The low oil loading level, high
surface oil, and particle reaction and inflation during drying process are
other limitations of using spray-drying for fish oil encapsulation (Keogh
et al., 2001). In addition to select and design wall materials, using
methods in the emulsification process which is influenced the stability
of feed emulsions and the encapsulation efficiency plays an important
role in retention of fish oil and overcome on this throwback of spray-
drying. Additional stabilisation and oil loading was achieved through
using a casein-based Maillard reaction product (Kosaraju, Weerakkody,
& Augustin, 2009).
So using methods that manufacture small emulsion droplets exhibit
higher encapsulated oil and lower surface oil leading to increase oxi-
dative stability of microcapsules (Kaushik et al., 2015). In this regard,
application of microfluidizer during emulsion preparation led to de-
crease the droplet size and increase the encapsulation efficiency com-
paring with using ultrasonication (Jafari et al., 2008).
Aghbashlo et al., 2013 used mini-spray dryer with different drying
air temperatures (140, 160, and 180 ⁰C) to produce fish oil micro-
capsules with various simple and complex wall materials (skim milk
powder, whey protein concentrate, WPI, 80% WPI + 20% milk protein
concentrate, and 80% WPI + 20% sodium caseinate). They found that
by increasing the inlet drying air temperature, higher encapsulation
efficiency, peroxide value, and particle size were obtained. In addition,
presence of disaccharide lactose in the composition of skim milk
powder led to increase encapsulation efficiency and decrease peroxide
value. The higher the inlet drying air temperature, the higher was the
encapsulation efficiency, peroxide value, and particle size and the lower
was the residual moisture content and bulk density (Aghbashlo et al.,
2013). It has also been reported lower hydroperoxide content of mi-
croencapsulated fish oil at lower inlet/outlet temperatures than higher
drying air temperatures (Serfert, Drusch, & Schwarz, 2009; Tonon,
Grosso, & Hubinger, 2011).
Hence, application of complex coacervation, Maillard reaction and
further crosslinking of polymers using protein–carbohydrate conjugates
changed physical properties of the wall and can help in stabilising and
protecting of fish oil microcapsules against post spray-drying oxidation
(Kaushik et al., 2015). Recently, the fish oil microcapsules were opti-
mised using soy protein isolate and inulin as wall materials and the
results showed 61% yield and 94% encapsulation efficiency using small
amounts of inulin (inulin:SPI = 0.4) and fish oil (20%) and the
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Food Research International 137 (2020) 109353
microcapsules retained more than 81% oil when the cross-linking with
transglutaminase were applied (Rios-Mera et al., 2019). Chen,
McGillivray, Wen, Zhong, and Quek (2013) used milk proteins (whey
protein isolate and sodium caseinate in a ratio of 4:1) as wall material
to encapsulate three lipophilic bioactive components (fish oil, phytos-
terols and limonene) and compared with those containing only fish oil
by spray-dryer. The good microcapsules were achieved in 4:1 ratio of
wall to core and at 170 C and 70 C inlet and outlet temperature, re-
spectively. In addition, the microcapsules containing lipophilic bioac-
tive components had higher EPA and DHA retention and better flavour/
odour profile than the fish oil microcapsules. Some good reviews on
microencapsulation by spray-drying technique have published by Jafari
et al. (2008), and Encina, Vergara, Giménez, Oyarzún-Ampuero, and
Robert (2016).
4.3.2. Freeze-drying
Freeze-drying or lyophilisation is a dehydration process at low
temperature. The product frizzed at first step followed by lowering
pressure and removing the ice by sublimation at next step. Using the
low temperatures and removing the oxygen in freeze-drying process
lead to a high quality product with lower oxidation (Kaushik et al.,
2015). Although this technique is more suitable for microencapsulation
of very heat sensitive ingredients, such as fish oil, it is more costly and
less rapid process for dehydrating for example than spray-drying. Chen,
Zhong, Wen, McGillivray, and Quek (2013) encapsulated fish oil con-
taining phytosterol ester and limonene in whey protein isolate and
soluble corn fibre wall materials by spray- and freeze-drying. It was
found that higher retention of volatile fraction and lower surface oil
was obtained in spray-drying microcapsules and the higher oxidative
stability was achieved in freeze-drying microcapsules at the first of
storage, but generally, there were not significant differences between
the spray- and freeze-drying in protection the core materials.
Moreover, microcapsules obtained by freeze dryer had porous
structure that accelerates the oxidation during storage and increases its
transport and storage costs (Kaushik et al., 2015). On the other hand, it
could require to crush and screen (mesh size 2) to obtain microcapsules
from flakes according to the wall materials (Hosseini, Ghorbani, Jafari,
& Mahoonak, 2019). As Heinzelmann, Franke, Valesco, and Marquez-
Ruiz (2000) and Anwar and Kunz (2011) reported highly porous
structures and short shelf-life of freeze dried fish oil microcapsules due
to the easy access of oxygen to the interior of such microcapsules.
Hence, using freeze-drying technique for encapsulation of fish oil is an
expensive process and needs to overcome the porosity issues in the
structure of the final powder (Gouin, 2004; Kaushik et al., 2015). The
effect of different wall material on microencapsulation of fish oil by
freeze-drying were investigated in various study. In this regard the ef-
fect of maltodextrin, sodium caseinate, Hasani, Rad, Hosseini, and
Noghabi (2015) have investigated WPC and modified starch (Hi-Cap
100TM) on kilka oil (Clupeonella cultriventris caspia) and the higher
encapsulation efficiency were observed in maltodextrin: modified
starch: WPC combination.
In addition with freezing parameters (freezing rate and tempera-
tures), the carbohydrate selection affected the shelf-life and oxidative
stability of freeze-dried of fish oil microcapsules as a second en-
capsulating agent. In this regard, Jamshidi et al. (2018) used complexes
of WPC with inulin and fucoidan in order to encapsulate fish protein
hydrolysate and fish oil using double emulsion (W/O/W) and freeze
dryer. They obtained higher oxidative stability microcapsules in a
combined wall material matrix of WPC and fucoidan. In a similar study,
Zhang et al. (2015) used Maillard reaction products of conjugated be-
tween soy protein isolate and hydrolysed soy protein isolate (at dif-
ferent hydrolysis time at 120, 180, 103, 240, 270, and 300 min) with
maltodextrin to encapsulate fish oil by freeze-drying. By increasing the
hydrolysis time, the microencapsulation efficiency was increased and
favourable oxidative stability and structure were found in micro-
capsules coated by protein isolate and hydrolysed soy protein isolate
A. Jamshidi, et al.
and maltodextrin conjugates (270 min). Heinzelmann, Franke, Velasco,
and Marquez-Ruiz (2000) investigated various process parameters in-
cluding wall material, homogenisation pressure, freezing rate and in-
itial temperature of freeze-drying on oxidative stability of fish oil mi-
croencapsulated by sodium caseinate and lactose using freeze dryer.
Based on their result, no relation found between the microencapsula-
tion efficiency and oil particle, and the fast freezing in liquid nitrogen
affected more on the shelf life microcapsules.
4.3.3. Spray-chilling/coating
Spray-chilling technique is a fat-based system that the core disperses
into a liquefied coating material, and then sprayed through an atomiser
nozzle into a cool environment. Exchanging the heat between the
molten material and cold air, leading to solidify the core and form
particles (Okuro, de Matos Junior, & Favaro-Trindade, 2013). Gen-
erally, fat components are used as wall materials in spray chilling
technology to be solidify at cooling temperature step and immobilize
the core material.
Acting as a good barrier to moisture, simply application and scale
up, using low temperature, low-cost operation, controlled release
during thermal processing, and produce material with great solubility
in oil are the most advantages of using spray-chilling for micro-
encapsulation (Anwar & Kunz, 2011; Fadini et al., 2018; Okuro et al.,
2013). Using the lower drying temperature (50 to 70 ⁰C) to eliminate
water from the emulsion leads to increase the oxidative stability
(Anwar, Weissbrodt, & Kunz, 2010).
The spray-chilling is more suitable for protecting water-soluble
material than sensitive oil material. Therefore, this method could be
used as a secondary method for providing additional coating around the
fish oil microcapsules and improving microencapsulation stability
(Kaushik et al., 2015).
Few articles investigated the fish oil microcapsules obtained by
spray-chilling technique. Initially, Anwar et al. (2010) applied spray-
chilling followed by film coating with a fluid bed equipment to in-
vestigate stability of fish oil microcapsules. Fish oil microcapsules (with
various ratios of EPA and DHA) were produced using soluble soybean
polysaccharide and maltodextrin using spray-chilling, then the ob-
tained microcapsules were coated by hydroxypropyl betacyclodextrin
(15% film coating). They stated that using spray-chilling process pro-
duces more stable microcapsules in comparison with spray-chilling
followed by film coating because ineffective film forming by hydro-
xypropyl betacyclodextrin, however, spray-chilling were good method
for protecting fish oil microcapsules from oxidation. In the other study,
Anwar and Kunz (2011) investigated the superiority of the spray-chil-
ling process compared to spray- and freeze-drying for producing fish oil
microcapsules in different wall materials (maltodextrin, soybean so-
luble polysaccharide, hydroxypropyl betacyclodextrin and modified
starch). They obtained the most stable microcapsules with a mixture of
soybean soluble polysaccharide and modified starch and spray-chilling
technique that contained very low propanal. After five weeks storage,
the oxidative stability of produced microcapsules were as followed:
spray-chilling > spray-drying > freeze-drying.
In an earlier publication, Fadini et al. (2018) used the combination
of spray-drying and spray-chilling in order to encapsulation of fish oil
and sacha inchi oil. At first, different wall materials (skimmed milk
powder, acacia gum, and a mixture of acacia gum and grape juice) used
for encapsulating oils by spray-dryer, then a second shell were formed
surrounding the obtained microcapsules (1:1:1 ratio of wall materials
composition) using a mixture of vegetable fat and hydrogenated palm
oil by spray-chilling. They stated that using combination of micro-
encapsulation technique leading to mask oil taste, provide sufficient
amount of PUFAs, and increase the microcapsules application in func-
tional products. Fadini et al. (2019) also obtained double-shell micro-
capsules containing fish oil in order to investigate the effects of dif-
ferent hydrogenated palm oil and vegetable fat ratio in spray-chilling
on fish oil microcapsules produced by spray-dryer. The 40/60 or 50/50
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ratio of lipid matrixes showed lower loosing of eicosapentaenoic acid
and docosahexaenoic acid (between 1.68 and 28.68%) and equivalent
of encapsulation efficiency between 98.3 and 71.32%.
4.3.4. Coacervation
The microencapsulation by coacervation is consist of forming cross-
linked or agglomerated of oppositely charged polymers using pH-shift,
which incorporated core material as thick wall. Formation complex
coacervation is start with adding the core material (fish oil) to a warm
gelatine solution (8–11 w/w % at 50 °C), emulsification of this aqueous,
adding polysaccharides along with dilution water, and following with
adjusting the pH below the isoelectric point of protein to start elec-
trostatic interactions and form agglomerates. At next step, the aqueous
system cooled down (to 4–7 °C, below the gelling temperature), so the
polymer rich phase deposited around the oil droplets. Then, the cross-
linking agent added to happen wall hardening and obtain hard micro-
capsules (Piacentini et al., 2013; Wang, Adhikari, & Barrow, 2014).
Different dehydrating drying methods are using for complex coa-
cervation filtering the coacervates included drying in alcohol or by
adding silica, and also using spray- and freeze-drying which yielded an
acceptable and higher quality product (Piacentini et al., 2013). The pH
and protein/polyphosphate ratio are critical in complex coacervation
process as the charge balance, charge density and intensity of interac-
tions between polymers varies with pH levels (Patrick & Ntsama, 2014;
Wang et al., 2014).
The higher encapsulation efficiency, higher particle loading, lower
surface oil, controlled release of core material, heat resistant properties,
and produce thicker wall are the advantages of coacervation comparing
to other encapsulation methods. For example the higher loading oil
(60%) and the lower surface oil (0.1%) obtained by coacervation have
been reported in comparison with the amounts of loading oil (30%) and
surface oil (0.2–1%) obtained by spray-dryer (Kralovec et al., 2012).
During agglomeration, thicker wall could be formed leading to improve
oxidative stability of microcapsules during producing, application, and
storage. Wang, Vongsvivut, Adhikari, and Barrow (2015) reported high
encapsulation efficiency (99.82%), low surface oil (0.09 ± 0.01%),
and a high encapsulation yield (98.56%) in multi-core microcapsules of
tuna oil produced by crosslinking gelatine–sodium hexametaphosphate
with transglutaminase followed by freeze-drying.
In addition, with the burst release effect, aggregation and con-
glutination problems, selection effective wall material is a limitation of
these method since, gelatine is the primary protein formed a thick outer
shell in microencapsulation by complex coacervation (Wang et al.,
2014; Yang et al., 2014). Besides the gum Arabic, which is the most
compounds used in combination with gelatine for forming complex
coacervation, application of the different anionic polymers such as so-
dium dodecyl sulphate (SDS) (Li, Wu, Chen, & Wang, 2009), pectin
(Saravanan & Rao, 2010) acacia gum (Tamjidi, Nasirpour, & Shahedi,
2013), SDS/NaCMC (Patrick & Ntsama, 2014), sodium alginate,
CaCO_3, chitosan, Span-80 (Min, Jian-dong, Zhi-qiang, & Hong-yu,
2015) and chitosan (Kang, Dai, & Kim, 2012; Yang et al., 2014) have
been also reported in the literature. As Tamjidi et al. (2013) stated the
composition of wall formula demonstrated significant effects on mi-
croencapsulation efficiency, oil content of microcapsules, and particles
size, so by increasing wall materials and decreasing fish oil, the ME and
OCM increase but later decrease. Increasing FO in formulas causes an
increase in microcapsules size. Tuna oil were encapsulated using com-
plex coacervation method by myofibrillar protein (extracted from Cte-
nopharyngodon idellus) and κ- or λ-carrageenan (Bakry, Huang, Zhai, &
Huang, 2019). The optimum formulation was 4:1 ratio of myofibrillar
protein to carrageenan (κ- or λ-carrageenan) and pH 5.0, and the
complex coacervate microcapsules showed higher moisture content,
solubility, and oxidative stability, and lower hygroscopicity and wett-
ability. Patrick and Ntsama (2014) optimised the microencapsulation of
fish oil according to concentration of wall material, core to wall ratio,
and the pH, using complex coacervation of gelatine/SDS/NaCMC as
A. Jamshidi, et al.
wall material and reported optimum microencapsulation efficiency of
75.2 ± 0.73% and 53.2 ± 0.39% obtained by spray-drying and freeze
drying, respectively. The complex coacervation technology has been
studied extensively and reviewed by Aloys et al. (2016).
4.3.5. Extrusion or fluidised bed coating
Extrusion is another technology for fish oil microencapsulation
consisting of the addition of active compound as core material to the
dissolution of a hydrocolloid followed by extruding the mixture through
a syringe to form droplets. In this method, pressure used to force
mixture of biopolymer containing core material to pass through nozzle
into a hardening bath (Kaushik et al., 2015; Rodríguez, Martín, Ruiz, &
Clares, 2016).
The advantages of extrusion are producing less porous particles,
using mild pressure and temperature conditions, totally enclosing the
core material by the wall material, and washing any core from the
outside (Kaushik et al., 2015; Serfert et al., 2009). The high cost tech-
nology (almost twice that of spray-drying) and producing high shear
forces which resulted in lower stability of fish oil are more dis-
advantages of extrusion technology (Gouin, 2004).
There are various extrusion-based process including prilling, elec-
trostatic field, rotating disk, and co-extrusion process. The prilling is
extruded the mixture using pulsation of the jet or vibration of the nozzle
in a controlled way contrary with rotating disk which applied multi-
nozzle system. In the electrostatic field method, electrostatic forces at
the needle tip leading to form small droplets disrupt the liquid surface.
A nozzle with concentric holes placed on the outer circumference of a
rotating cylinder is used in the co-extrusion or centrifugal extrusion
(Joye & McClements, 2014; Rodríguez et al., 2016). Gouin, 2004 stated
that the particle size of co-extrusion which is quite commonly used in
microencapsulation processes, is 500–1000 m and too high for using in
many food products since particles above about 100 m impact mouth
feel. Ying et al. (2016) extruded gelatine-based dough (47%, 60% or
70%w/w total solids) containing fish oil microcapsules to produce ta-
blets containing 35% w/w oil and reported lower oil leakage from ta-
blets obtained from extrudates of dough with 47% w/w total solids and
pre-conditioned at 35 °C. Wu, Zhang, Xue, Xue, and Wang (2017) used
electro-coextrusion to produce core shell beads by alginates with dif-
ferent M/G (70.4%, 79.4%, and 88.0%), to encapsulate fish oil in an
acidic solution, the core shell beads were marginal shrinkage and
leakage lower fish oil although the dense hydrogel network protect the
fish oil against acidic environment. Since core shell improved the oxi-
dative stability of fish oil in an acidic solution, this study provides new
protective method to prevent oxidation of fish oil especially in acidic
medium foods.
4.3.6. Molecular inclusion or interfacial polymerisation
Molecular inclusion or interfacial polymerisation is generally ob-
tained by using cyclodextrins (CDs) as the encapsulating agents, which
is a nanoencapsulation process on a molecular scale. CDs are a family of
naturally cyclic oligosaccharides consisting of six, seven or eight glu-
cose subunits joined by α-1,4 glycosidic bonds in a cylinder-shaped.
CDs are derived from starch and divided to α-, β- and γ-cyclodextrins, in
which β- cyclodextrin is usually used (Pagington, 1986.). The hydro-
philic exterior and hydrophobic interior cavity of CDs structure makes
it suitable to encapsulate nonpolar molecules such as fish oil through a
hydrophobic interaction into polar internal cavity (Fang & Bhandari,
2010).
The solubility, temperature, pH, molecular weight and chemical
nature of core materials are affected the encapsulation efficiency of
CDs, so the small molecules with higher hydrophobicity more attached
to the CDs (Fang & Bhandari, 2010; Haiyee, Yahya, Rashid, & Hashim,
2016). The fish oil as a hydrophobic compound can be solubilized in the
hydrophobic cavity due to its hydrophobic portions (Seo, Min, & Choi,
2010).
The low toxicity, protection the functional materials, control release
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of guest material, mask unpleasant flavours and odours, prolong the
shelf-life (Nuchuchua et al., 2009). As well, using CDs for fish oil en-
capsulation decrease the oxygen accessibility and increase the oxidative
stability of unsaturated fish oil (Hădărugă et al., 2017). Coprecipitation,
cogrinding by slurry, dump, paste, and kneading, coevaporation, spray-
drying, freeze-drying and sealed-heating are various methods of CD
complexation (Kfoury, Auezova, Greige-Gerges, & Fourmentin, 2015).
The inclusion complex of Atlantic salmon oil (Salmo salar L.) with β-
cyclodextrin (β-CD) were prepared at a host–guest ratio of 1:1 and 3:1
using ethanol–water mixture and kneading methods (Hădărugă et al.,
2017). The inclusion compound was confirmed by thermogravimetry,
differential scanning calorimetry (DSC), and Karl Fischer titration (KFT)
analysis methods. Haiyee et al. (2016) extracted the fish oil from vis-
cera of catfish oil (Clarias batrachus) and encapsulate it by inclusion
complex with β–cyclodextrin using co-precipitation and kneading
methods in comparing with physical mixture and reported smaller in
crystal sizes and different morphology in inclusion complex obtained
compared to physical mixture. Konrádsdóttir, Geirsson, Halldórsson,
Halldórsson, and Loftsson (2014) stated only α-cyclodextrin and γ-cy-
clodextrin were able to stabilize cod-liver oil which confirmed by
confocal imaging. The cod-liver oil/γ-CD (3:1 M ratio) was lyophilized
and divided in three groups at different conditions during 1, 2, 4, 12
and 84 weeks against pure cod-liver oil as control. The results indicated
that γ-CD delays oxidative degradation in presence oxygen, but it does
not increase the stability of cod-liver oil under anaerobic conditions.
Choi, Ruktanonchai, Min, Chun, and Soottitantawat (2010) used β-cy-
clodextrin (water-soluble polymer) and polycaprolactone (water-in-
soluble polymer) to encapsulate fish oil and then determined the oxi-
dative stability of lyophilised microcapsules at different storage
temperatures, as well, the release behaviour of produced fish oil com-
plexes in deionised water, NaCl solution and fish sauce was in-
vestigated. Fish oil loaded β-cyclodextrin (10:20 ratio b-CD:FO w:w)
demonstrated better characteristic, encapsulation efficiency (84.1%),
and fish oil loading (62.7%), and also slower release in deionised water
and NaCl (15% and 25%) than in fish sauce.
4.3.7. Liposome
A liposome is a spherical bilayer vesicle of lipid that are prepared by
dispersions of polar lipids such as phospholipids in aqueous media
(Kaushik et al., 2015). Liposomes can be applied for encapsulating
(with sizes in the nanometre to micrometre range) both hydrophilic and
lipophilic molecules and can be formed in uni-lamellar or multi-la-
mellar structures. In order to encapsulate fish oil using liposome, fish
oil dissolved in phospholipids (with or without emulsifier) followed by
adding water and homogenized (sonication) and finally dried to pro-
duce powders (Rasti, Jinap, Mozafari, & Yazid, 2012; Vélez, Perotti,
Zanel, Hynes, & Gennaro, 2017).
Although encapsulating fish oil using liposome is stable against
oxidation, high biocompatibility and versatility, targeted to specific
locations, and can also be protected against environment conditions
(pH, temperature, ionic strength), but their application is limited for
encapsulating of fish oil because the process is costly/the high cost and
sometimes low stability (Gouin, 2004; Kaushik et al., 2015). The phy-
sicochemical properties of membranes including the nature of its
components, the size, surface charge, and lipid organization are re-
vealed the suitability of liposome formulation. On the other hand,
Sekhon (2010) stated that the concentration and type of phospholipids,
preparation method, nature of the encapsulated ingredients, and ionic
lipids are affected the liposomes.
Rasti et al. (2012) compared conventional rotary evaporation
method (using organic solvents) with Mozafari method (without using
organic solvents) to investigate the oxidative stability of freshly and
stored liposomal (> 200 nm) and nanoliposomal (50–200 nm) systems
containing polyunsaturated fatty acids. They found that decrease the
liposomes size, increase the surface charge, physical and oxidative
stability of liposomal PUFAs and the higher physicochemical stability
A. Jamshidi, et al.
Fig. 1. Different techniques for incorporating fish oil in food products.
observed in liposomes prepared by the Mozafari method but during
10 months of storage (4 °C in the dark) various method did not influ-
ence on the physicochemical stability of liposomes. Wang, Lv, Lu, Jiang,
and Lin (2015) studied the characteristics and stability of uncoated li-
posomes and carboxymethylchitosan-coated liposomes (CM-L) con-
taining fish oil (extracted from Nile tilapia viscera) and reported that
the carboxymethylchitosan-coating increased the mean diameter of li-
posomes and carboxymethylchitosan-coated liposomes were more
stable than uncoated liposomes during storage at 25 °C. Ojagh and
Hasani (2018) used nano-liposomes of fish oil to fortify bread with
nanoencapsulated fish oil (0.0 as control, and 5%, w/w) and reported
high encapsulation efficiency (90.12 ± 0.27%) and a good oxidative
stability of nano-liposomes of fish oil during 25 days storage in re-
frigerated. As well, fortified bread with nano-liposomes of fish oil
showed higher loaf volume of bread and had no negative effects on the
textural quality and sensory acceptability.
4.3.8. Advantages and disadvantages
Different technique of incorporating fish oil in food products has
been shown in Fig. 1. There are various studies on the application of
different wall materials (Gan, Cheng, & Easa, 2008), various emulsion
conditions (Jamshidi, Shabanpour, Pourashouri, & Raeisi, 2019;
Klinkesorn, Sophanodora, Chinachoti, Decker, & McClements, 2005),
and the effect of drying methods (Anwar & Kunz, 2011; Kralovec et al.,
2012; Shabanpour, Mehrdad, Pourashouri, & Jafari, 2018) on the ob-
tained fish oil microcapsules with high quality. As shown in Table 1, the
application of various wall materials has obtained considerable atten-
tion to produce high-quality fish oil microcapsules with high oxidative
stability. In addition, with the previous methods mentioned in fish oil
encapsulation, application of other methods such as encapsulation in
yeast cell as a natural micro-vesicles (Czerniak et al., 2015), using
spray-nozzles (Legako & Dunford, 2010), vacuum oven (at 40 °C for
24 h) (Liao, Luo, Zhao, & Wang, 2012), and Maillard cross-links (Gan
et al., 2008) have also been reported.
Spray-drying is the most common encapsulation technique used in
food industry. Spray-drying is an economical and flexible process that
applied available equipment to produce microcapsules with good
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Food Research International 137 (2020) 109353
quality (Botrel et al., 2014; Jafari et al., 2008; Yu et al., 2017). How-
ever, microcapsules obtained by spray-dryer process showed large
particle size, low oil loading, high surface oil, and low shelf-life because
of rapid oxidation of surface oil that leads to deterioration of sensory
quality (Chatterjee & Judeh, 2016). In Table 2, the advantages and
disadvantages of various encapsulation methods using for fish oil en-
capsulation are compared with spray-drying since it is the most
common method using to encapsulate fish oil.
5. Fortified products using fish oil
Fortification of food products with fish oil is an accepted practice by
consumers and food industries and aims to enhance the nutritional
value with healthy eating and diets. Fortification of food with fish oil
provide a functional products act as preventing of cardiovascular dis-
eases, cancer and autoimmune and inflammatory diseases (Jiménez-
Colmenero, 2013). Using fish oil in food fortification is challenge be-
cause of its highly susceptible to oxidation and its affecting on sensory
attributes of fortified food products. Regarding the effect of fish oil on
sensory attributes, a maximum limit should be applied to prevent af-
fecting sensory characteristics. The adding fish oil in range 1.0–60.0 g/
kg food product, using packaging for fortified food to prevent oxygen
and light penetration, and preventing of exposure to strong heat could
be applied to overcome on limitation of using fish oil in fortification
food products depending on the food type (Kolanowski & Laufenberg,
2006).
In an effort to increase fatty acids intakes, fortification of various
food products such as meat, milk and bread products have been ex-
amined using fish oil. Fortification of other products such as drinks
were also reported, since Habibi, Keramat, Hojjatoleslamy, and Tamjidi
(2017) prepared fish oil microcapsules using complex coacervates of
gelatine–gum Arabic (ratio 1:1) to fortify pomegranate juice. They re-
ported increasing turbidity and lightness of fortified pomegranate juice
and possibility of fortified pomegranate juice with fish oil micro-
capsules up to 100 mg long-chain n-3 PUFAs per litre. Enriching live-
stock feed with fish oil which most recently methods to fortify meat and
meat products with fish oil, was not discussed in the current article. The
A. Jamshidi, et al. Food Research International 137 (2020) 109353

Table 1
Application of various wall materials for encapsulating fish oil using different methods.
Encapsulation Wall materials composition Efficient wall material Reference
method

Spray-drying Fish gelatine, chitosan, combination of gelatine and chitosan, and a Mixture of gelatine and maltodextrin with MTGase Pourashouri et al. (2014)
mixture of microbial transglutaminase (MTGase) with maltodextrin chitosan with maltodextrin was insufficient
Novel cress seed mucilage/chitosan (CSM/CS) hydrogels Optimum processing conditions were CSM/CS Kavousi, Fathi, and Goli
volume ratio of 48:52 (2017)
Barley protein (Hordein and Glutelin) for microencapsulation of fish 15% protein and a 1.0 oil/protein ratio, optimum Wang et al. (2011)
oil tween 20 (1 g tween/100 g fish oil) inlet temperature of 150 °C
4 wall materials including skim milk powder (SMP), 70% 70% SMP + 30% lactose and 70% SMP + 30% Aghbashlo et al. (2013)
SMP + 30%maltodextrin, 70% SMP + 30% lactose, 70% SMP + 30% sucrose
sucrose
Freeze drying Gelatine, sodium Hexametaphosphate (SHMP) Using complex coacervation is suitable for Wang et al. (2015)
Tuna oil containing various ingredients (0.07% RP, 0.001% stabilizing multiple bioactive lipophilic ingredients
cholecalciferol, 0.8% α-tocopherol, 0.004% vitamin K2, 0.05%
coenzyme Q10 or 0.05% curcumin, w/w),
Isolated soy protein, using O/W/O double emulsification and A CIWE (primary O/W emulsion) prepared with Cho, Shim, and Park (2003)
subsequent enzymatic gelation method, using microbial 10% ISP was stable without any emulsifier
transglutaminase cross-linked proteins
Soy protein isolate/gum Arabic, (SPI:GA) and the concentration of The trials carried out with 1.5:1.0 SPI:GA, 1.0:1.0
the reticulating agent (TG) wall: core and 6.0 UA of TG/g and 1.5:1.0
SPI:GA, 2.0:1.0 wall: core and 10.0 UA of TG/g
presented approximately 25 g and 22 g of EPA þ
DHA n 100 g of microcapsules, respectively
Whey powder and sodium caseinate (4:1) using ultrasonication in Sonication treatment of 380 W for 3 min Hosseini et al. (2019)
different powers (180–380 W) and times (1–3 min)
Tuna oil in lecithin (primary emulsions) or by lecithin–chitosan Lecithin–chitosan membranes with corn syrup solids Klinkesorn et al. (2005)
(secondary emulsions) and absence and presence of corn syrup solids
(a carbohydrate)
Optimisation of encapsulation of fish protein hydrolysate and fish oil Using one pass high-pressure homogenization at Jamshidi, Antequera,
within a complex of whey protein concentrate and inulin using W1/O and three passes at W1/O/W2 to produce Solomando, and Perez-
double emulsion and high pressure homogenizer stable emulsion Palacios (2019)
Coacervation Gelatine solution and gum Arabic Results suggested the use of The best conditions of experiment were with 25% Alavi Talab, Ardjmand,
glutaraldehyde as the crosslinking agent instead of formaldehyde can glutaraldehyde at 1000 rpm of stirring speed. Motalebi, and Pourgholam
caused the Microcapsules become spherical shape, smooth surface (2010)
with no obvious dents and narrower particle size distribution
Soy protein isolate (SPI) and inulin Inulin (inulin:SPI = 0.4) and fish oil (20%) Rios-Mera et al. (2019)
Whey protein isolate 11 (WPI)-gum Arabic (GA) The optimum pH and WPI-to-GA ratio for complex Eratte, Wang, Dowling,
Followed by spray- and freeze-drying coacervation was found to be 3.75 and 3:1 by spray- Barrow, and Adhikari
drying (2014)

fish oil fortification range, and the amounts of consumption of fortified Economic Research Service, 2005), consumption of 77.06 kg/annum or
products, need to be significantly higher to access recommendations to 211 g (7.4 oz)/day is recommended based on the quantity of EPA and
meet the needs of fatty acids (Kitessa, Gulati, Simos, Ashes, & Scott, DHA (Cox, Evans, & Lease, 2011).
2004). Different fortified food products with fish oil would increase the
intake of EPA and DHA through the diet at sensory acceptable levels
(Kolanowski and Laufenberg, 2006). According to the USA data (USDA/

Table 2
The advantages and disadvantages of various fish-oil microencapsulation methods compared with spray-drying.
Encapsulation Advantage Disadvantage Reference
method

Freeze-drying Using low temperature, carried out under vacuum, and Produce more microcapsules porous due to the Legako and Dunford (2010),
absence of oxygen sublimation, more costly and less rapid process for Eratte et al. (2014)
dehydrating
Spray-chilling Using low temperature, simply application and scale up, Applied as a secondary method for providing additional Fadini et al. (2018), Okuro et al.
low-cost operation, controlled release during thermal coating around the fish oil microcapsules in order to (2013), Anwar and Kunz (2011),
processing, produce material with great solubility in oil improving microencapsulation stability Anwar et al. (2010)
Coacervation Low surface oil, high oil content, high stability, excellent The burst release effect, aggregation and conglutination Tamjidi et al. (2012), Chatterjee
controlled release, heat resistant properties, higher particle problems, and selection effective wall material and Judeh (2016), Yang et al.
loading, and produce thicker wall (2014)
Extrusion Producing less porous particles, using mild pressure and The high cost technology (almost twice that of spray- Serfert et al. (2009), Kaushik
temperature conditions, totally enclosing the core material drying) and producing high shear forces leads to lower et al. (2015), Gouin (2004)
by the wall material, and washing any core from the outside stability
Molecular inclusion Control release of guest material, mask unpleasant flavours Nuchuchua et al. (2009), Seo
and odours, prolong the shelf-life, decrease the oxygen et al. (2010), Hădărugă et al.
accessibility and increase the oxidative stability (2017)
Liposome Stable microcapsules against the oxidation, high The high cost and sometimes low stability Gouin (2004), Kaushik et al.
biocompatibility and versatility, targeted to specific (2015)
locations, and can also be protected against environment
conditions (pH, temperature, ionic strength),

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A. Jamshidi, et al. Food Research International 137 (2020) 109353

5.1. Meat products
The fortification process affected the textural of fortified products.
The more fish oil amounts used in the products led to the softer mouth-
feel which enhancing the sensory attributes (Cáceres et al., 2008). This
structure seems to be related to good binding properties in gels resulted
from protein–protein interaction (Delgado-Pando, Cofrades, Ruiz-
Capillas, & Jiménez-Colmenero, 2010a). Cáceres et al. (2008) stated
that the fat plays more important role than the amount of fish oil in-
corporated in relation to textural properties of fortified products. Its
role depends on the kind of products (hamburger, fresh, cooked or
fermented sausage, etc.), ingredient attributes, and breakdown level of
raw materials during product manufacture (Delgado-Pando, Cofrades,
Ruiz-Capillas, Teresa Solas, & Jiménez-Colmenero, 2010b). Using oil-
in-water fish emulsions as fat substitutes leading to select formulations
with special mechanical, nutritional, and textural properties, which
resulted in producing particular meat products and offering opportu-
nities to develop new products. Increasing the hardness, consistency
cohesiveness and adhesiveness of texture of bologna-type sausage also
reported by using proteins in wall materials and the role of covering
particles of fat by protein (Holt & Roginski, 2001).
Reducing fat content and improving fatty acid profile are the most
commonly purpose to fortify meat and meat products using fish oil.
Table 3 presented some studies that fortified meat products with fish oil
according to their main purpose and obtained results. Although the
emulsified meat products are popular as a ready to eat products, but
containing high fat content in these kind of products led to consider
reformulation these products through partially substitution of fat by
emulsion or microcapsules of fish oil (Sousa et al., 2017).
Jiménez-Colmenero (2013) were reformulated dry fermented sau-
sage by substitution of pork back fat using oil combination (olive, lin-
seed and fish oils) in aim of reducing fat content and improving fatty
acid profile. They reported reduced fat content, saturated fatty acid
content, and hardness, and increased polyunsaturated fatty acids and
cohesiveness.
The healthiest oil combination were prepared using mixture of ve-
getable oils (olive and linseed) and fish oils, in order to design a lipid
material containing a good balance of ne6/ne3 PUFA and PUFA/SFA
ratios, lower amounts of SFA, and higher amounts of MUFA and PUFA
as pork back fat substitute in frankfurters and pate (Delgado-Pando
et al., 2010; Delgado-Pando, Cofrades, Rodriguez-Salas, & Jiménez-
Colmenero, 2011). Jiménez-Martín et al. (2015) were fortified pre-fried
chicken nuggets with bulk fish oil, and microencapsulated fish oil, and
stated that fortified chicken nuggets with microcapsules were protected
lipid and protein against oxidation and preserved the sensory quality,
especially during the first month of storage comparing with pre-fried
chicken nuggets fortified with bulk fish oil. Regarding to produce
Frankfurter sausages with better lipid composition, Dominguez,
Pateiro, Sichetti Munekata, Bastianello Campagnol, and Lorenzo
(2017a) considered partial substitutes of pork back fat by micro-
encapsulated fish oil, unencapsulated olive, and fish oil mixture. They
reported that even though the fat and energy values were reduced in
Frankfurter sausages containing microcapsules, the lipid oxidation in-
creased. The Frankfurter sausages containing microcapsules showed
higher TBARS values and volatile compounds comparing with the
control and Frankfurter containing sausages unencapsulated olive and
fish oil mixture.
5.2. Dairy products
Since the milk and milk products are extensively consumed by
people of different age and have a critical role in nutritional factors,
using these products are potentially attractive method to increase fatty
acid contents using fish oil/to fortify these products as a delivery ve-
hicle for fatty acid using fish oil (Goyal et al., 2016). Oleic acid, linoleic
acid and α-linolenic acid (21–30%, 2–2.5% and 1–1.3% of total fat,
respectively) are consisted more than 95% of unsaturated fatty acids in
milk fat (Kaur, Basu, & Shivhare, 2015). The beneficial health claimed
of unsaturated fatty acids led to increase efforts to incorporated fatty
acids in various products such as milk and milk products. Fortification
of milk and milk products with fish oil led to highest content of poly-
unsaturated fatty acids specially EPA and DHA, which is considering as
health promoting fatty acids. In addition, fish oil is highly sensitive to
oxidation and development of volatile oxidation products negatively
influence the flavour and sensory characteristics of dairy products. The
amounts of incorporating fish oil before affecting the sensory attributes
of some dairy products are shown in Table 4.
Various studies have fortified different dairy products, such as milk
and yogurt (Jamshidi et al., 2018; Liu et al., 2016; McCowen et al.,
2010), cheese and cream cheeses (Calligaris et al., 2013; Horn et al.,
2012), low-fat ice cream (Andajani, Purnomo, & Radiati, 2015;
Mahrous & Abd-El-Salam, 2014), and low-calorie spreadable fats (soft
margarine and mix of butter and vegetable oil) (Kolanowski, Swiderski,
Lis, & Berger, 2001), by emulsion or microcapsules of fish oil. Directly
adding fish oil (which usually leads to a fishy odour and taste in result
of oxidation of these fatty acids), using a stabilized pre-emulsion of fish
oil (with only gentle agitation), and microencapsulation of fish oil are
different methods using to fortify dairy products. In pre-emulsion
method, fish oil could be added late in the process so the contact with
prooxidative compounds will minimize and the stability increase. Many
authors have successfully incorporated microencapsulated fish oil to
yogurt (Estrada, Boeneke, Bechtel, & Sathivel, 2011; Liu et al., 2016;
Tamjidi, Nasirpour, & Shahedi, 2012). Let, Jacobsen, and Meyer (2007)
have been fortified milk and yogurt with fish oil and reported that
fortified yogurt demonstrated lower level of fishy off-flavour and higher
oxidative stability than fortified milk with fish oil.

Table 3
Fortified meat products with fish oil.
Main purpose Oil Results Reference

Produce reduced-energy and reduced-fat
bologna sausages, enriched with ω-3
and Melissa officinalis extract
Produce Salami with a higher ω-3 fatty acid
content
Produce pork liver pâté fortified with ω-3
fatty acids
Produce Dutch-type salami
Produce of liver pâté
Linseed oil and algae oil
Used fish oil extract
A mixture of olive oil (443.9 g kg − 1),
linseed oil (378.7 g kg − 1) and fish oil
(177.4 g kg − 1)
Linseed oil and encapsulated fish oil or
canola and flaxseed pre-emulsified oil
Fish oil (with high content of n-3 long
chain fatty acids)
−1 −1
Fortified sausages with 850 kcal kg , 36gkg Berasategi et al. (2014)
fat, 6 g kg−1 ALA, 4.4 g kg−1
DHA and a ω-6:ω-3 ratio of 0.4, without
negative effects on sensory quality.
Muguerza, Ansorena, and
Astiasarán (2004)
A higher increase of the ω-3 family, as well as Delgado-Pando, Cofrades,
lower lipid stability to oxidation Rodríguez-Salas, and Jiménez-
Colmenero (2011)
Pelser, Linssen, Legger, and
Houben (2007)
Fortified pâté with lower SFA and higher PUFA Dominguez, Pateiro, Agregán,
contents, decreasing hardness and gumminess by et al. (2017)
increasing fish oil addition

11
A. Jamshidi, et al.
Table 4
The amounts of incorporating fish oil before affecting the sensory attributes of dairy products.
Product Fortification levels
Spreadable fresh cheese (Philadelphia type) 15 g fish oil per kg
Non-flavoured semi-solid processed fresh low-fat cheese 3 g fish oil per kg
(110 g fat/kg)
Non-flavoured processed cheese (320 g fat/kg) 40 g fish oil per kg
Soft goat cheese 127 mg EPA + DHA per 28 g serving
Strawberry yogurt Omega-3 fatty acid content from 1.76% to 7.50% of the total fatty acids and the
EPA and DHA contents from undetectable to 2.9% and 2.37%
Unflavoured drinkable yogurt and a drinkable yogurt 2 and 3 g/kg of fish oil addition to a 2% fat
flavoured with strawberry
By providing carbohydrate, protein, fat, vitamin, calcium and
phosphor, yogurt plays an important role in nutrition and easy diges-
tible dairy product of daily diet in all ages (Turkmen, Senel, & Akal,
2019). Many nutraceutical effects including enhanced digestion and
immune systems and reduced serum cholesterol could be obtained by
consuming yogurt. Nowadays, production low-fat yogurt is achieving
more interest since it contains less calories while including the majority
of nutraceutical nutrients (Liu et al., 2016). On the other hand, de-
creasing the fat led to unbalanced yogurt flavour, because milk fat plays
a role of carrier for fat-soluble flavours, and influences the texture of
yogurt (Liu et al., 2016). Zhong, Yang, Cao, Liu, and Qin (2018) in-
vestigated the addition of fish oil/-oryzanol nanoemulsion onto yogurt
and found lower acidity, syneresis, and peroxide value in fortified yo-
gurt and increase of retention fish oil with closer sensory attributes
scores to control yogurt. The most common sensory attributes relating
to yogurt texture are viscosity and smoothness. Addition of nutrients or
microcapsules directly to the milk before cheese processing is the easier
method to produce fortified cheese. The effective fortification of the
nutrient and microcapsules in the cheese could be achieved only by
gaining a stable symbiosis between the aqueous and the added oil
phases (Calligaris et al., 2013). Studies reported that various dairy
products fortified with fish oil could be shown differ oxidative stability,
in this regard, spreadable fresh cheese containing 15 g fish oil/kg
showed up to 5 weeks shelf-life before the sensory quality decreased
(Horn et al., 2012).
Hejazian, Takami, and Shendi (2016) reported that unpleasant
odour and fishy taste of Kilka fish oil could be masked through mi-
croencapsulation and these microcapsules can be used to fortify cheese
in order to increase the nutritional value of fortified cheese. They mixed
Kilka oil with milk at 1% and 2% followed by spray-dried then added to
cheese at 5% level. There were no differences between sensory attri-
butes of fortified cheese with 1% and 2% Kilka oil, but in comparing
with the control, fortified cheese demonstrated higher fatty acids con-
tent and lower sensory acceptability. Moghadam, Pourahmad,
Mortazavi, Davoodi, and Azizinezhad (2019) added nanoencapsulated
of fish oil into probiotic-fermented milk and reported increasing via-
bility of Lactobacillus plantarum and EPA and DHA content and de-
creasing peroxide value, without negatively effect on overall accep-
tance of low fat probiotic fermented milk. Turkmen et al. (2019)
fortified blackberry yoghurt with odourless fish oil at different levels
(0.3%, 0.5% and 1.0%) and found that blackberry fruit yoghurt samples
containing 0.3% and 0.5% fish oil were acceptable by the panellists and
the higher peroxide values were observed in fortified samples com-
paring with the control. Ghorbanzade, Jafari, Akhavan, and Hadavi
(2017) applied Nano-liposome to nanoencapsulate fish oil in order to
fortify yogurt and investigate its characteristics during three weeks’
storage at 4 °C. They found that the amounts of acidity, syneresis and
peroxide value of fortified yogurt decreased, the DHA and EPA contents
increased, and the sensory characteristics of fortified yogurt were
closed to the control.
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Food Research International 137 (2020) 109353
Reference
Horn et al. (2012)
Horn et al. (2012)
Horn et al. (2012)
Hughes, Brian Perkins, Calder, and
Skonberg (2012)
Estrada et al. (2011)
Kolanowski and Weiβbrodt (2007)
5.3. Bakery products
Deficiency of protein, essential fatty acids and minerals of bread,
leads to consider it as a good option for fortifying with fish oil because
of low price, daily consumed by the whole population, and high market
availability product (de Conto, Oliveira, Martin, Chang, & Steel, 2012).
Using encapsulation of fish oil to fortify bread led to enhance nutri-
tional point of view and stability of fatty acids in bread (Rahaie,
Gharibzahedi, Razavi, & Jafari, 2014).
The high temperature during baking bread could be degraded EPA
and DHA followed by formation volatile secondary oxidation products,
generation unpleasant off-flavours, and reduce of palatability in fish oil
fortified breads (Henna Lu & Norziah, 2011). Nevertheless, the for-
tification bread with microencapsulated fish oil increases DHA fatty
acid, Henna Lu and Norziah (2011), but also the fortification bread with
fish oil negatively affected its palatability and the panellist were able to
distinguish the fishy flavour between fortified bread and the control.
By application fish oil microcapsules, the weight and volume of
bread increased and decrease respectively resulting increase the
amounts of microcapsules which related to increase the loaf density and
decrease the gluten concentration of formulation, so the loaf expansion
were decrease by increasing the amounts of microcapsules. Increasing
the amounts of microcapsules led to increase the hardness and decrease
the rate of drying during baking of bread, which negatively affected the
crumb porosity making the loaves harder (Gökmen et al., 2011).
Gökmen et al. (2011) stated that using nanoencapsulated oil could re-
duce the risk of acrylamide formation in bread which lipid oxidation
can promote formation it. In addition, increasing the microcapsules in
dough of bread reduced the formation of acrylamide and hydro-
xymethyl furfural in breads. It has been reported by many researchers
that the addition of surfactants and emulsifiers such as lecithin im-
proves the making properties and quality of breads (Serna-Saldivar
et al., 2006).
Feeding with bread containing microencapsulated tuna oil during
three weeks, led to increase Docosapentaenoic acid, EPA, DHA, total n-
3 PUFA in plasma proportions, and DHA and total n-3 PUFA in plasma
phospholipid fractions in the chronic study (Yep et al., 2002). Serna-
Saldivar et al. (2006) fortified pan bread using oil emulsions and mi-
croencapsulated obtained from different sources of fatty acids (algae,
fish and flax oils) and reported that fortified bread containing flax oil or
microencapsulated alga oil showed lower volume and higher density
than the other treatments and the bread containing alga oils had the
poorest texture lowest sensory acceptability. The fortified bread with
fish oil was well preferred during first days but least accepted after
13 days. Henna Lu and Norziah (2011) substituted shortening with
microencapsulated n-3 PUFA and found that microencapsulated n-3
PUFA were stable after baking and storage, as well as, these substitute
did not influence volume and quality of the bread showing an accep-
table palatability after 3-day storage.
Cereals and cereal bars fortified in ranges from 2000 to 5343 mg per
55 g serving (one cup) for cereals. The cereals containing EPA and DHA
A. Jamshidi, et al.
cannot be identified (Kaur et al., 2015). Horn et al. (2009) investigated
the influences of caffeic acid, ascorbyl palmitate, and tocopherol as
antioxidant on oxidative stability of energy bars fortified with fish oil
and reported that effectiveness of these antioxidant are related to their
different localisations and mechanisms of action, as c-tocopherol
showed best antioxidative effect. Hermund et al. (2015) also found less
oxidation products by application extracts of Fucus vesiculosus in
granola bars fortified with fish oil emulsion and stated that.
6. Effects of incorporating fish oil in food products
6.1. Enhanced of fatty acid profiles
Fish oil known as the main dietary source of n-3 PUFA. According to
the World Health Organization (WHO Study Group, 2003), ISSFAL
(International Society for the Study of Fatty acids and Lipids), and FDA
(Food and Drug Administration, 2000) recommendations, the adequate
intake of EPA and DHA from the regular consumption of fish or pro-
ducts fortified with fish oil is required to provide 200–500 mg per week,
0.65 g/day (minimum 0.22 g/day), and should not exceed 3.0 g/day
intake of EPA and DHA, respectively (Cáceres et al., 2008). The high
proportions of PUFA are necessarily healthy when there is a balance in
the n-6/n-3 ratio, so fish oil that provided high amounts of n-3 fatty
acids could be a good substitute to replace fat in fortified products as
functional products (Dominguez, Pateiro, Agregán, & Lorenzo, 2017b).
Regarding to recommendations for optimal intake of fatty acids to
prevent chronic disorders, dietary fat intake contain of total diet energy
(15–30%), < 10% saturated fatty acids, 6–10% polyunsaturated fatty
acids, 10–15% monounsaturated fatty acids, and < 1% trans fatty acids
(Delgado-Pando et al., 2010a, 2010b).
Healthier lipid reformulation in fortified products could be provided
by fat substitution with other fat with characteristics closer to health
recommendations such as lower proportions of SFA and higher pro-
portions of MUFAs and PUFA, and a good ratios of n-6/n-3 PUFA (< 4)
and PUFA/SFA (> 0.4). Since excessive quantity of n-6 PUFA and very
high n-6/n-3 PUFA ratios advanced some pathogenesis such as CVD,
cancer, arteriosclerosis, ischaemic heart disease, and inflammatory and
autoimmune diseases (Hathwar, Rai, Modi, & Narayan, 2012). Among
the various fat, fish oil is considered as a good source of n-3 PUFA
(35%), maximum long chain (33%), with high levels of EPA and DHA
acids and is cholesterol-free (Delgado-Pando et al., 2010a, 2010b).
There also are plant fats such as olive, linseed, canola, etc. which
have been substituted by fat of meat reformulation products. Various
meat products have been produced from olive, high-oleic acid sun-
flower, linseed (flaxseed), soybean, peanut, palm, fish etc. in order to
improve the nutritional quality (Kolanowski & Laufenberg, 2006). In
some literatures, a unique combination of fats (olive, linseed and fish
oils) was applied to gain lipid material with a fatty acid composition in
line with health recommendations containing low proportion of SFA
(less than 16%) and the proportion of those fatty acids which increased
the risk of cardiovascular disease (Delgado-Pando et al., 2010a;
Jiménez-Colmenero, 2013). Delgado-Pando et al. (2010b) designed a
healthy lipid composition using olive, linseed and fish oils (44.39,
37.87 and 17.74%, respectively), to obtain a healthier lipid formulation
containing a low proportion of SFA, high proportions of MUFA and
PUFA, and a balanced n-6/n-3 PUFA and PUFA/SFA ratios in line with
health recommendations.
Based on the European Commission Regulation, a ‘‘high omega 3
fatty acids’’ has been claimed when the product includes a minimum of
80 mg of the sum of EPA and DHA per 100 g of product. Dominguez,
Pateiro, Sichetti Munekata, Bastianello Campagnol, and Lorenzo
(2017), Dominguez, Pateiro, Agregán, and Lorenzo (2017) used olive
and fish oil mixture to produce functional frankfurter sausages with
claiming high in omega 3 fatty acids. They reported containing of
50.4 mg of EPA and 168.6 mg of DHA per 100 g of product in sausages
fortified with microencapsulated fish oil and 107.9 mg of EPA and
13
Food Research International 137 (2020) 109353
400.2 mg of DHA per 100 g of product in sausages fortified with un-
encapsulated olive and fish oil mixture.
The fish oil composition such as fatty acid content, cholesterol level,
etc. is depend on fish species and inherent compounds of fatty acids in
fish portions, as fish oil extracted from fish liver leads to increase
cholesterol content in fortified pâté even the PUFA content increased
and MUFA and SFA contents decreased comparing to the control
(Dominguez, Pateiro, Agregán, et al., 2017). Jiménez-Colmenero
(2013) stated that fortified dry fermented sausage with partial sub-
stitute pork back fat with healthier oil combination (olive, linseed and
fish oils) stabilized in a konjac matrix increased the proportion of cal-
ories from PUFA and reduced those provided by SFA and MUFA, in
addition with very remarkable decrease in the ne6/ne3 ratio.
6.2. Sensory characteristic and shelf-life
In fortified products, distinguished volatile compounds could be
almost derived from spices (terpenes) and lipid oxidation (Aldehydes).
Aldehydes and terpenes were the groups more abundant in sausages
(Dominguez, Pateiro, Sichetti Munekata, et al., 2017) and chicken
nuggets (Jiménez-Martín et al., 2015). Dominguez, Pateiro, Sichetti
Munekata, et al. (2017) and Josquin, Linssen, and Houben (2012), re-
ported three aldehyde included hexanal, heptanal, and pentanal were
detected from lipid oxidation of sausage and Frankfurt sausages pre-
pared with partial substitute of back fat by fish oil.
Jiménez-Colmenero (2013) stated that changes of sensory char-
acteristics of fortified sausages is related to the fat reduction, which
resulted decreasing the appearance and flavour of dry fermented sau-
sage. Decreeing juiciness of fortified sausages is also could be related to
the higher water binding of wall materials (konjac in their study) than
muscle structure, which led to release of lower fluids during chewing,
resulted in reducing juiciness. On the other hand, fat reduction in ad-
dition with presence of oil-in-water matrix make softer structures in
meat products and the firmness decreased. The appearance of bread
was affected by incorporating microencapsulate n-3, as de Conto et al.
(2012) reported the correlation between the colour and appearance of
fortified bread so, lower lightness and higher colour saturation, the
lower was the appearance.
The most important role of microencapsulation systems is protec-
tion of sensitive materials specially lipids from oxidation. Its effec-
tiveness to protect the core material against oxidation determined by
wall material characteristics and the encapsulation process (Wang
et al., 2014). In this regard, crosslinking process seems to be an effective
methods to produce stronger wall protective against oxidation. The
addition of transglutaminase resulted in inter- and intra-molecular
isopeptide bonds with gelatine molecules by cross-linking glutamine
and lysine amino acids residues (Kashiwagi et al., 2002). However, it
should be noted here that this crosslinking process only provide in-
solubility but no additional oxidative stability to microcapsules
(p > 0.05).
There are various reports regarding sensory attributes of fortified
food products with fish oil. The sensory characteristics could be nega-
tively affected by development fish oil fishy off-flavour and suscept-
ibility to oxidative deterioration during storage. According to the
Rognlien, Duncan, O’Keefe, and Eigel (2012) study, using low levels of
fresh fish oil (0.5% wt/wt) or butter oil (0.5% wt/wt) in fortified yogurt
without flavouring agents could not be distinguished/differentiated by
panellists. There were no differences in appearance and texture scores
between the fortified yogurt with fish oil and the control in Tamjidi
et al. (2012) study. Nevertheless, sensory attributes (aroma, flavour,
and overall acceptance) of fortified yogurt had lower scores than the
control, although the sensory attributes were improved by applying
diluted limejuice in fortified yogurt; however, the scores were still
lower than the control yogurt. Kolanowski and Weißbrodt (2007) stated
that higher fortification of unflavoured drinkable yogurt without and
with strawberry by 2 and 3 g/kg fish oil respectively, did not adversely
A. Jamshidi, et al.
influenced on overall sensory. Both Kolanowski and Weißbrodt (2007)
and Chee et al. (2005) reported that that flavouring agents such as
strawberry could help to mask the developing off-flavours due to fish oil
fortification.
7. Conclusions and outlook
Fortification of food with fish oil provide functional products pre-
venting cardiovascular diseases, cancer, and autoimmune and in-
flammatory diseases. The high susceptibility to oxidative deterioration
is one of the major issues related to fish oil Omega-3 fatty acids and
functional products fortified with fish oil. Extensive studies have been
done to overcome on these limitations and various methods have been
investigated to fortify food products with fish oil. Direct addition of
bulk fish oil, emulsification, and microencapsulation techniques are the
most common methods used for fortifying of food products with fish oil.
The application of antioxidants and microencapsulation technique have
significant effects on the protection of fortified products with fish oil in
addition with controlling environmental conditions. Hence volatile
compounds, which produced during oxidation of fish oil, create the
undesirable flavour and odours of the oil, further research is needed for
acceptable functional foods containing fish oil in terms of sensory
characteristics and shelf-life.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
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