Journal of the Association of Arab Universities for Basic and Applied Sciences (2017) 24, 101–106

University of Bahrain
Journal of the Association of Arab Universities for
Basic and Applied Sciences
www.elsevier.com/locate/jaaubas
www.sciencedirect.com

REVIEW ARTICLE

Antioxidant properties of dairy products fortified

with natural additives: A review
Modi A. Alenisan, Hanan H. Alqattan, Lojayn S. Tolbah, Amal B. Shori *

King Abdulaziz University, Faculty of Science, Department of Biological Sciences, Jeddah 21589, Saudi Arabia

Received 12 January 2017; revised 30 March 2017; accepted 5 May 2017

Available online 5 June 2017

KEYWORDS Abstract Antioxidant is a molecule that inhibits the oxidation of other molecules caused by free
Antioxidant activity; radicals. Antioxidant activity of a dairy food is important both for the shelf life of the product
Dairy foods; as well as for protection from oxidative damage in the human body. The objective of this work
Phenolics; was to demonstrate the effects of natural antioxidants (plant-based sources) against synthetic
Natural antioxidant antioxidants in dairy food.
Ó 2017 University of Bahrain. Publishing services by Elsevier B.V. This is an open access article under the
CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction limited resources and access to modern treatments (Marles

Natural products and health foods have to be given a lot of
interests for enhancing overall well-being, in the prevention
of diseases and also in the incorporation of health-promoting
substances into the diet as natural food additives. Newly, the
valorization of underutilized foods has more priority because
of their antioxidant potential (Marles and Farnsworth, 1994;
Prasad et al., 2012).
Consumers have more concerns and recommendations to
use natural antioxidants from food sources rather than syn-
thetic antioxidants which have been restricted because of their
toxic and carcinogenic effects (Zambonin et al., 2012; Abdel-
Hameed et al., 2014). Many epidemiological studies reported
that the frequent consumption of high natural antioxidant
containing foods could lower the incidences of particular types
of cancers, hypertension, diabetes, and cardiovascular diseases,
especially, in developing countries where most people have
* Corresponding author.
E-mail address: shori_7506@hotmail.com (A.B. Shori).
Peer review under responsibility of University of Bahrain.
http://dx.doi.org/10.1016/j.jaubas.2017.05.001
1815-3852 Ó 2017 University of Bahrain. Publishing services by Elsevier B.V.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).
and Farnsworth, 1994). Dairy products are one of the most
interesting and promising foods with regard to their potential
antioxidant activity, due to their wide diversity of antioxidant
molecules such as milk caseins and whey proteins (Pihlanto,
2006; Suetsuna et al., 2000). Furthermore, milk contains a
variety of antioxidant molecule traces i.e. low molecular
weight thiols (Niero et al., 2014, 2015), ascorbate (Nielsen
et al., 2001), tocopherol, retinol and carotenoids (Jensen and
Nielsen, 1996; Nozière et al., 2006).
Medicinal plants rich in natural antioxidants and phenolics
are progressively applied in dairy foods manufacturing to
improve nutritional and therapeutic properties (Shori and
Baba, 2011a,b; Karaaslan et al., 2011; Martins et al., 2014;
Bertolino et al., 2015). Natural plant-based antioxidants can
be used to control the excess formation of free radicals and
increase the antioxidant capability as well as replace synthetic
antioxidants with side effects like liver damage and carcinogen-
esis (Meenakshi et al., 2009). Therefore, this mini-review
focused on antioxidant activity of dairy products in which syn-
thetic and natural antioxidants were incorporated.
102
2. Antioxidant activity (AA) in dairy foods
Niero et al. (2016) reported that a high total antioxidant
activity was found for partially skimmed milk (29.31–
44.72 mmol l
1 TE, 22.65–41.43 mmol l
1 TE) in contrast to
whole milk (24.15–43.05 mmol l
1 TE, 19.44–39.80 mmol l
1 TE)
both for UHT and pasteurized samples (Table 1). As a
consequence of the skimming process, partially skimmed milk
was deprived of diverse lipophilic antioxidants (e.g. retinol,
tocopherol and carotenoids), milk soluble fraction, however,
contained other powerful antioxidant compounds (e.g. ascor-
bate, thiols, whet proteins) (Niero et al., 2016; Walstra et al.,
2005). In another study, Santos et al. (2013) stated that the
addition of grape residue silage in the diet cows in order to
transfer its phenolic compounds to the milk exhibited antioxi-
dant activity of 44.6 mg GAE l
1. The addition of grape resi-
due was thought to decrease the oxidation of milk fat which
was enriched in unsaturated fatty acids due to dietary soybean
oil supplementation. In fact, the transfer of some phenolic
compounds to milk of dairy cows is low. For instance, ferulic
acid has a recovery rate of 0.02 g 100 g
1 of the administered
dosage (Soberon et al., 2012). Transferring high concentra-
tions of phenolics to milk is not preferred to inhibit lipid oxi-
dation (Sies and Stahl, 1995) as the suitable proportion
between concentrations of antioxidant compounds and those
of unsaturated fatty acids may be important (Granelli et al.,
1998).
Antioxidant activity in dairy products supplemented with
various plants is summarized in Table 1.
Shori (2013) studied the impact of soybean supplementa-
tion to improve the antioxidant and the viability of lactic acid
bacteria in cow- and camel-milk yogurts during refrigerated
storage. They observed that the antioxidant activity of Glycine
max L. (soybean) supplemented camel milk yogurt had the
highest antioxidant activity on day 7 of storage (67.59
± 1.4%) and reduced to 61.56 ± 1.4% on day 21 of storage
(p > 0.05) (Table 1). The antioxidant activity of soybean-
cow milk yogurt showed significant reduction during 21 days
of refrigerated storage to 35.29 ± 1.0%, while it was 58%
on 7 days. The addition of soybean into yogurts prepared from
either cow or camel milk enhances the viability of lactic acid
bacteria and antioxidant activity during refrigerated storage.
The antioxidant properties of soybean associated to isofla-
vones and polyphenolic compounds (Sroska and Cisowski,
2003; Kim et al., 2006; Slavin et al., 2009), as well as, milk pro-
tein proteolysis (Lourens-Hattingh and Viljoen, 2001) and
organic acids production (Correia et al., 2005).
The antioxidant activities in fresh camel milk yogurt (15.4
± 1.3%) were lower than cow milk yogurt (26.4 ± 0.7%). A
yogurt formation with the addition of Allium sativum signifi-
cantly increased the antioxidant activities in both cow milk
yogurt (37.9 ± 0.8%) and camel milk yogurt (26.1 ± 0.8%)
(Shori and Baba, 2011b). Allium sativum extracts were stated
to have the ability to scavenge different radicals
(Bhagyalakshmi et al., 2005; Pedraza-Chaverri et al., 2006)
via sulfur, phenolic, flavonoid, and terpenoid compounds pre-
sent in the mature garlic bulbs (Miller et al., 2000; Nuutila
et al., 2003; Bozin et al., 2008). The presence of Allium sativum
during milk fermentation affected antioxidant activities. The
antioxidant activities of cow milk yogurt decreased to
26–28% whereas camel milk yogurt increased to 49–65%
M.A. Alenisan et al.
during 7–21 days of storage (Shori and Baba, 2011b). Caleja
et al. (2016) reported that yogurts with the addition of Foenicu-
lum vulgare Mill. (fennel) and Matricaria recutita L. (chamo-
mile) decoctions had higher antioxidant activity than the
synthetic additive (potassium sorbate). Chamomile showed
the highest antioxidant activity, while fennel and the synthetic
additives showed a very similar antioxidant activity in yogurt
(Table 1). After seven days of storage, the potassium sorbate
(E202) lost considerable antioxidant capacity as well as the
natural product. The use of aqueous extracts produced from
plants enhanced the antioxidant activity of yogurts (Table 1),
and showed higher capacity than the synthetic additives
(E202).
O’Sullivan et al. (2014) investigated the effect of addition of
two common brown algae, namely Ascophyllum nodosum (AN)
(100% water and 80% ethanol extracts) and Fucus vesiculosus
(FV) (60% ethanol extract), on antioxidant potential of yogurt
at concentrations of 0.25 and 0.5%. The highest antioxidant
activities were detected in AN100 (0.5%) with 32% and
FV60e (0.5%) with 47%. The DPPH radical scavenging action
of all yogurts was comparable over the 28 day storage period.
All algal extract-enriched yogurt samples had significantly
higher DPPH radical scavenging activities compared to the
corresponding control (plain-yogurt) indicating that the algal
extracts were stable within yogurt.
El-Said et al. (2014) determined the antioxidant activities
[radical scavenging activity (RSA %), ABTS radical scaveng-
ing, total phenolic content (TPC) and total flavonoids content
(TFC)] of stirred-type yogurt fortified with 5%, 10%, 15%,
20%, 25%, 30% and 35% of the PPE, before and after inocu-
lation with the traditional yoghurt starter. The antioxidant
activities (ABTS radical scavenging) of control before and
after addition of yogurt starter were 3.18 ± 0.03% and 1.91
± 0.01% respectively. In addition, the antioxidant activities
of yogurt with 35% of PPE before and after adding yogurt
starter were 14.01 ± 2.07% and 12.22 ± 1.89% respectively.
DPPH radical scavenging of control before adding yogurt star-
ter was 19.12 ± 1.56%, and 17.91 ± 1.54% after addition of
yogurt starter. This study indicated that, milk fermentation
with PPE reduced significantly the antioxidant activity of
yogurt.
Yogurt with the addition of Azadirachta indica showed
higher antioxidant effect compared to plain yogurt (53.1
± 5.0% and 35.9 ± 5.2%, respectively) after 28 days of stor-
age (Shori and Baba, 2011a). Azadirachta indica have antioxi-
dant properties due to the presence of high concentration of
vitamin C and riboflavin (Sithisarn et al., 2005; Madhi et al.,
2003; Atangwho et al., 2009). In addition, fermentation and
post-acidification products produced during storage such as
organic acid derivative and milk protein proteolysis could be
possible sources of DPPH inhibitors. (Lourens-Hattingh and
Viljoen, 2001; Correia et al., 2004). In the presence of Azadir-
achta indica yogurt showed higher antioxidant activity and this
is beneficial in two respects: firstly, reducing lipid oxidation
process in yogurt which might be responsible for unwanted
chemical compounds and formation of off-flavors (Berset
et al., 1994), and secondly, increasing dietary antioxidants
which prevent the progressive impairment of pancreatic beta-
cell function due to oxidative stress (Liu et al., 2005).
Marinho et al. (2015) compared the antioxidant activity of
cheese samples coated and uncoated with the rosemary leaves.
Activation energy (Ea) values indicated that the cheeses coated
 Antioxidant properties of dairy products
Table 1 Antioxidant activity in dairy products supplemented with natural additives (i.e. plant-based sources).
Samples Additives Extraction Method Antioxidant activity Storage Significant References
Time level
Raw milk Bronopol (as preservatives) Water 2,2’-Azino-Bis(3-Ethilbenzotiazolina-6 22.61– - – Niero et al.
Whole UHT milk - Sulfonic Acid) (ABTS assay) 38.39 lmol l
1 TE24.15– (2016)
Skimmed UHT milk - 43.05 lmol l
1 TE29.31–
Whole pasteurized - 44.72 lmol l
1 TE19.44–
milk - 39.80 lmol l
1 TE22.65–
Skimmed 41.43 lmol l
1 TE
pasteurized milk
Cow’s Milk Grape residue silage Pure methanol Reducing power (mg GAE l
1) 44.6 mg GAE l
1 - P < 0.05 Santos et al.
(2013)
Cow milk Plain Water (1,1-diphenyl-2-picrylhydrazyl radical 26.41 ± 07% 21 days P < 0.05 Shori (2013)
Camel milk Glycine max L. (Soybean). (DPPH) 61.76 ± 2.2%
15.44 ± 1.2%
53.16 ± 0.1%
Cow milk yogurt Plain Water (1,1-diphenyl-2-picrylhydrazyl radical 26.4 ± 0.7% 21 days P < 0.05 Shori and Baba
Camel milk yogurt Allium sativum (DPPH) 37.9 ± 0.8% (2011b)
15.4 ± 1.3%
26.1 ± 0.8%
Yogurt Plain Water Reducing power 32.4 ± 0.4 mg ml
1 (EC50) 14 days P < 0.001 Caleja et al.
Potassium sorbate (E202) (1,1-diphenyl-2-picrylhydrazyl radical 195 ± 5 mg ml
1 (EC50) (2016)
Foeniculum vulgare Mill. (DPPH) 29 ± 2 mg ml
1 (EC50)
(fennel) 111 ± 20 mg ml
1 (EC50)
Matricaria recutita L. 27 ± 1 mg ml
1 (EC50)
(chamomile) 94 ± 4 mg ml
1 (EC50)
16.4 ± 0.8 mg ml
1 (EC50)
45 ± 3 mg ml
1 (EC50)
Yogurt Plain Ethanol:Water (1,1-diphenyl-2-picrylhydrazyl radical 20% 28 days P < 0.05 O’Sullivan
Ascophyllum nodosum (0.5%) (DPPH) 32% et al. (2016)
Fucus vesiculosus (0.5%) 47%
Yogurt Plain Water Radical scavenging activity (RSA %) 19.12 ± 1.56 % (before)* - P < 0.05 El-Said et al.
Pomegranate peel extracts 2,20 -azino-bis (3-ethylbenzothiazoline-6- 17.91 ± 1.54 % (after)** (2014)
(PPE) sulfonic acid) (ABTS ) 3.18 ± 0.03 % (before)* 1.91
(before and after inoculation with the ± 0.01 % (after)**
starter) 53.41 ± 2.48 % (before)*
43.81 ± 2.54 % (after)**
14.01 ± 2.07 % (before)*
12.22 ± 1.89 % (after)**
Yogurt Plain Water (1,1-diphenyl-2-picrylhydrazyl radical 35.9 ± 5.2% 28 days P < 0.05 Shori and baba
Azadirachta indica (DPPH) 53.1 ± 5.0% (2011a)
Semi-hard cheese Coated with dehydrated Chloroform:ethanol Kinetic study (Ozawa’s 85.91 ± 2.07kJ mol_1 60 days P < 0.05 Marinho et al.
rosemary leaves (2:1 ml:ml), non-isothermal method) 59.05 ± 1.48kJ mol_1 (2015)
Uncoated
Cheese Green pink pepper Water (2,2-diphenyl-1-picrylhydrazyl)DPPH 21.7 ± 0.8 lg ml
1 (EC50) 30 days P > 0.05 Dannenberg
Mature pink pepper 23.5 ± 1.2 lg ml
1 (EC50) et al. (2016)
(Schinus terebinthifolius

103
Raddi)
(continued on next page)
 104 M.A. Alenisan et al.

with the rosemary leaves (85.91 ± 2.07 kJ mol
1) were more

The simulated digestion system was comprised of two sections, including gastric and intestinal digestion, with pH values of 1.2 and 6.8, respectively. Accordingly, there were two digestive fluids
prepared; simulated gastric fluid using NaCl, HCl, purified porcine pepsin and deionized water; and simulated intestinal fluid using monobasic potassium phosphate, sodium hydroxide, potassium
resistant to the oxidation process than uncoated cheese sam-

Rashidinejad

Rashidinejad
et al. (2016)

et al. (2014)
ple (59.05 ± 1.48 kJ mol
1) after 1440 h of ripening. Madsen
References

and Bertelsen (1995) stated that the antioxidant activity of

rosemary was referred to the existence of phenolic diterpenes,
such as carnosol and carnosic acid, and also to its capacity to
donate electrons to free radicals and break the chain reaction.
Significant

P < 0.05
P  0.05

In another study conducted by Dannenberg et al. (2016),

both essential oils of green pink pepper (GEO) and mature
level

pink pepper (MEO) demonstrated antioxidant activity, as

the concentration of free radical DPPH decreased in cheese.
Storage

90 days

90 days

The EC50 (concentration of EO desired to minimize the initial

Time

concentration of the free radical DPPH by 50%) were 21.7

± 0.8 lg ml
1 for GEO and 23.5 ± 1.2 lg ml
1 for MEO.
However, the statistical analysis showed no significant differ-
8.2 mmol kg
1(1000 ppm)

ence in the antioxidant activity of this two EO. MEO showed

13 mmol kg
1(1000 ppm)

activity versus the formation of primary oxidative com-

Antioxidant activity

240 Teq, mmol g
1

190 Teq, mmol g
1

pounds (e.g. peroxides) of the lipid peroxidation process that

215 mmol TE g
1

110 mmol TE g
1

105 mmol TE g
1

extends the shelf life of the products by preserving sensory

14.5 mmol kg
1

4.8 mmol kg
1

5 mmol kg
1

features for a longer period of time being in agreement with

(1000 ppm)

(1000 ppm)

Olmedo et al. (2008, 2009).

A recent study by Rashidinejad et al. (2016) showed that
the fortification of full-fat cheese with free green tea extract
(GTE) significantly raised the antioxidant activities of the
cheese on day 0 and as well as over ripening. However, some
unexpected outcomes were observed. For instance, there was
Oxygen radical absorbance capacity
Ferric reducing antioxidant power

no significant difference in the FRAP values for cheeses for-

tified with 500 ppm GTE after 30 and 90 days
(11.3 mmol kg
1 and 11 mmol kg
1 respectively). The FRAP
values of the GTE-fortified cheese with a concentration of
1000 ppm (13 mmol kg
1) on day 90 were significantly less
than on day 30 (14.5 mmol kg
1). Similarly, the addition of
250 ppm GTE did not increase the FRAP value
(8.2 mmol kg
1) of full-fat cheeses on day 90. At all three dif-
(ORAC)
(FRAP)
Method

ferent points of ripening (days 0, 30, and 90) the FRAP values
ORAC
FRAP

for cheese fortified with 500 ppm GTE (9.8, 11.3,

11 mmol kg
1, respectively) were significantly (p  0.05) less
than cheese fortified with 1000 ppm GTE (12, 14.8,
intestinal fluid (SIF)

13 mmol kg
1, respectively). GTE used in the current study

digestion model***
By a simulated

contains numerous catechins, fundamentally epigallocatechin

By Simulated

gallate (EGCG), epicatechin gallate (ECG), and epigallocate-

Extraction

chin (EGC), along with others such as C and (-) epicatechin

(EC). The existence of gallated catechins that have a higher
affinity to connect with milk proteins explain unexpected
FRAP values (Ferruzzi and Green, 2006). Although, a high
Control (neither catechin nor

concentration of GTE added to the cheese significantly

Control with polyethylene

(p  0.05) increased oxygen radical absorbance capacity

phosphate, pancreatin and porcine bile extracts.
Green tea extract (GTE)

(ORAC) values, but there was no significant difference

polyethylene glycol)

(p > 0.05) on day 90 between the plain cheese and cheeses

fortified with minimal concentrations of GTE (e.g.
Without GTE

250 ppm), as also noted for FRAP antioxidant activity.

Before adding yogurt starter.
Additives

Withal, variations were found to be significant when the sam-

Catechin

After adding yogurt starter.

glycol

ples for day 0 and 30 were estimated. Similar to the FRAP

results, there were no significant differences detected between
Table 1 (continued)

ORAC values gained from full-fat digested cheese with free

GTE on day 30 and day 90. ORAC results could be referred
to incomplete degradation of catechins, indicating less con-
Low-fat Cheese
Full-fat cheese

stancy through the storage of cheese or under simulated gas-

trointestinal digestion environments (Rashidinejad et al.,
Samples

2016).
In 2014, Rashidinejad et al. demonstrated that the cheese
**
***
*

prepared from milk fortified with catechin had a higher

Antioxidant properties of dairy products
FRAP value (14.5 mmol kg
1) than non-fortified cheeses
(5 mmol kg
1, 4.8 mmol kg
1), both instantly after cheese pro-
duction and during the 90-day of ripening. There were no sig-
nificant differences in FRAP values between cheese containing
polyethylene glycol (PEG) and cheese with no PEG on days 0
and 90 of the ripening period, but there were on day 30. The
existence of polyethylene glycol could pick up surface active
properties based on the molecular weight, in addition to rais-
ing the solubility of phenolics in water, while the effect on
antioxidant activity is still unclear (Thaipong et al., 2006;
Wojdylo et al., 2007). The rate of FRAP antioxidant activity
increased with the concentration of fortified catechin on 30
and 90 days of ripening, cheese that fortified with 500 mg kg
1
of catechin had a much higher FRAP value compared to the
control or the other two fortified cheeses (Rashidinejad
et al., 2014). Subsequently, fortified phenolic catechin has an
important role in increasing the antioxidant activity of FRAP
than the phenolic compounds of endogenous milk that justifies
the reasons for the cheese fortified with phenolics in the current
study. The existence of milk proteins may influence the activity
of polyphenols, like catechin, through digestion (Jobstl et al.,
2004; Bae et al., 2009; Xiao et al., 2011). Therefore, significant
differences (p < 0.05) in ORAC values were noted between the
controls (with polyethylene glycol (105 mmol TE g
1), without
polyethylene glycol or catechin (110 mmol TE g
1), and
catechin-fortified cheeses (215 mmol TE g
1) after 90 days of
ripening.
3. Conclusion
The addition of plant-based antioxidants in dairy food has met
acceptance for the retardation of oxidation in dairy products.
Also, natural antioxidants used to prolong the shelf life of the
products as well as have fewer side effects than synthetic
antioxidants to the human body. Future studies are needed
to determine a variety of the plant antioxidant molecules and
their use in dairy food.
Conflict of interest
The authors have no conflict of interest.
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