LWT - Food Science and Technology 77 (2017) 323e331

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LWT - Food Science and Technology

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

Antioxidant protection of cooked meatballs during frozen storage by

whey protein edible lms with phytochemicals from Laurus nobilis L.
and Salvia ofcinalis

vez b, Meltem Serdarog
lu c
Tolga Akcan a, *, Mario Este
a
b
c

Pamukkale University, Faculty of Engineering, Department of Food Engineering, Denizli, Turkey

ceres, Spain
IPROCAR Research Institute, University of Extremadura, 10003 Ca
_
Ege University, Faculty of Engineering, Department of Food Engineering, Izmir,
Turkey

a r t i c l e i n f o

a b s t r a c t

Article history:
Received 16 May 2016
Received in revised form
18 November 2016
Accepted 19 November 2016
Available online 27 November 2016

The aim of this study was to assess the effectiveness of whey protein isolate based edible lms (WPFs)
incorporated with natural antioxidant extracts (NAE) from laurel (LA, Laurus nobilis L.) or sage (SA, Salvia
ofcinalis.) on the oxidative stability of cooked meatballs during frozen storage at
18  C for 60 days. TBA
values of the meatballs with NAE-WPF were lower than the TBA values of the meatballs with WPF and
the control (C) group of samples. Higher antioxidant activity by LA-WPF than SA-WPF was determined
with a 2,20 -diphenyl-2-picrylhydrazyl radical-scavenging assay. Incorporation of NAE from LA or SA into
the edible lms (EFs) resulted in reduced para-Anisidine value (p-Av) (P < 0.05) in cooked meatballs.
Total phenolic compound content was higher in meatballs treated with NAE-WPF than in the C group
suggesting that these natural compounds contributed to the oxidative stability of frozen meatballs. This
study shows that the application of an antioxidant active packaging with LA or SA to meatballs is a
feasible and effective antioxidant strategy for retarding oxidative changes in cooked and subsequently
frozen comminuted meat products.
2016 Elsevier Ltd. All rights reserved.

Keywords:
Edible lms
Antioxidant activity
Laurel and sage
Pre-cooked meatball
Frozen storage

1. Introduction
With the increasing demand in convenience foods, ready-to-eat
(RTE) products have become a popular category in the meat industry. This demand has initiated the development of processing
and packaging methods that keep their fresh appearance and avor
as long as possible (Yingyuad et al., 2006). Pre-cooked meat
products are prone to lipid oxidation, which conduce to rapid
development of rancid or stale avor, expressed as warmed-over
avor (WOF), during frozen storage (Love, 1988; St Angelo et al.,
1987; Tims & Watts, 1958). Hence, it is necessary to control and
minimize the extent of lipid oxidation in meat products. Addition of
antioxidants is one of the accepted methods to retard lipid oxidation in processed meat products. Synthetic antioxidants such as
butylatedhydroxyanisole (BHA), butylatedhydroxytoluene (BHT)
and tert-butylhydroquinone (TBHQ) are widely used in industrial
processing to improve the quality and to prolong the shelf life of

* Corresponding author.
E-mail address: tolgaakcan@gmail.com (T. Akcan).
http://dx.doi.org/10.1016/j.lwt.2016.11.051
0023-6438/ 2016 Elsevier Ltd. All rights reserved.

food product. However, the use of such compounds has been

related to potential safety problems, which has restricted its
application in the food industry (Rojas & Brewer, 2008). The use of
spices and herbs as natural antioxidants is becoming of more
important for the food industry for protection of such products
(Andersen, Lauridsen, & Skibsted, 2003). Their effectiveness however depends on many several factors such as the dose and mode of
application (Shah, Bosco, & Mir, 2014). In this regard, the application of natural antioxidants to edible lms in pre-cooked meat
products is an innovative but poorly explored option that needs
further comprehension.
Many researchers have reported antioxidant effects of sage in

vez, Ramrez, Ventanas, & Cava, 2007;
meat products (Este

ska, Borowski, & Danowska-Oziewicz, 2001; Zhang, Lin,
Karpin
Leng, Huang, & Zhou, 2013). Sage (Salvia ofcinalis) is a variety of
aromatic herb which has been planted widely throughout much of
the world. It is not only used as raw material in the pharmaceutical
and cosmetic industries but also used to improve avors of foods
(Tepe, Sokmen, Akpulat, & Sokmen, 2006). Bioactive compounds,
such as carnosol, carnosic acid and rosmarinic acid, may account for
the antioxidant activity of sage. Some researchers have reported

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T. Akcan et al. / LWT - Food Science and Technology 77 (2017) 323e331

that sage, or sage extracts, can effectively retard lipid oxidation in

muscle foods (Fasseas, Mountzouris, Tarantilis, Polissiou, & Zervas,
2008; Mc Carthy, Kerry, Kerry, Lynch, & Buckley, 2001a; Tanabe,
Yoshida, & Tomita, 2002). Fasseas et al. (2008) noted that addition of SA essential oils (3%) to porcine ground meat samples in the
cooked state and to bovine ground meat samples in the raw state
signicantly reduced the antioxidant activity at the end of storage
at 4  C which agreed with our results. The studies by Mielnik, Olsen,
Vogt, Adeline, and Skrede (2006) also indicated that addition of
grape seed extract with high cafeic acid concentration. to cooked
turkey meats had higher antiradical scavenging activity as
compared to the control group. Hinneburg, Damien Dorman, and
Hiltunen (2006) studied the antioxidant activity of water extracts
of herbs and spices. They reported that extracts obtained from LA
displayed the highest antioxidant activity in the ABTS and DPPH
radical scavenging assays than the iron-chelating assay.
The plant named as Daphne was dened as Laurus nobilis by
Goodyer in 1655. Leaves of L. nobilis are also widely used as a spice,
antiseptic, insecticide and stomachic, and were used in the past to
treat rheumatism in European folk medicine. L. nobilis, commonly
known as bay, sweet bay and laurel, is an evergreen tree native to
the Mediterranean region especially in Turkey, Greece, Spain, Italy

and France (Yalin, Anik, Sanda, & akir, 2007; Skerget
et al., 2005).
Also some researches have shown that laurel leaf extracts have an
antioxidant activity (El, Karagozlu, Karakaya, & Sahn, 2014;
Ferreira, Proena, Serralheiro, & Arajo, 2006; Unver, Arslan,
Ozcan, & Akbulut, 2009). On the contrary of sage, there are
limited studies about the effect of laurel leaves on the oxidative
stability of meat and products. Further to the potential antioxidant
protection of these natural sources of phenolic compounds, the
impact of the avors and color of these plants on the sensory
properties and acceptability of cooked meatballs is unknown. The
feasibility of certain antioxidant strategies involving the application
of natural antioxidants may not overlook the consumer acceptability of the nal product.
To control food contamination and quality loss, edible coating or
biodegradable packaging has been recently introduced in food
processing. Several applications for meat, poultry, and seafood have
been reviewed by Gennadios, Hanna, and Kurth (1997) with signicant emphasis on the reduction of lipid oxidation, weight loss,
moisture loss, microbial quality, and volatile avor loss. Selected
antioxidant compounds including plant extracts or essential oils
have been incorporated in edible lms and coatings to retard

n, & Roncale

s,
oxidation during the storage of meat (Camo, Beltra
2008; Coskun, Calikoglu, Emiroglu, & Candogan, 2014). Meat processing and storage, prior to consumption can have a signicant
effect on meat quality (Pokorny, Yanishlieva, & Gordon, 2001).
This research aims to determine the effectiveness of whey
protein-based antioxidant edible lms incorporated with extracts
from laurel (Laurus nobilis L.) and sage (Salvia ofcinalis.) on the
oxidative stability and sensory properties and consumer acceptability of cooked meatballs during frozen storage.
2. Material and methods
2.1. Materials
Whey protein isolate was obtained from Davisco Foods International Inc. (BiPRO, Le Sueur, MN, USA). Glycerol, NaOH were
purchased from Merck Co. (Darmstadt, Germany). All materials
were food grade.
2.2. Extracts production
Leaves of laurel (Laurus nobilis L.) and sage (Salvia ofcinalis.)

were provided from Defne Ds Ticaret ve Tarm rnleri A.S. (Izmir,

Turkey). The procedure for the extraction of bioactive compounds
from the plant materials was based on that previously reported by

vez (2014) with some modiCando, Morcuende, Utrera, and Este
cations as follows. Firstly, laurel and sage leaves were grounded by
using hammer mill (Brook Crompton, Series 2000, England) then
were screened (Prfsieb Jel 200, Germany) and particles which
have more than 650 mm particle size were used for the extraction
methods. 15 g screened leaves were weighed onto lter paper for
each sample then samples with papers were folded and put into jar.
This was followed by addition of 100 mL of a mixture of ethanol:
water (80:20, v/v). Each sample was heated in a shaking water bath
for 4 h at 40  C. The combined supernatants were then ltered
through a 0.45-mm Millipore nylon lter and evaporated in rotary
evaporator (IKA) until removed the alcoholic portions then stored
at
80  C.
2.3. Whey protein isolate-based lm preparation
The whey protein isolate based edible lms (WPF) were formed
with the modication of the method described by Seydim and
Sarikus (2006). Whey protein isolate (5% wt/vol) was dissolved in
distilled water, and glycerol (5% wt/vol) was added. The pH was
adjusted to 8.0 with 2 N NaOH. Then, solutions were heated to
90 2 C while being stirred continuously for 30 min and cooling to
room temperature. The lm solutions were ltered through a layer
of cheesecloth. We added extracts into lm solutions (vol/vol) then
ve groups of WPFs were manufactured: (1) control WPFs without
natural antioxidant extracts (NAEs) addition (WPC), (2) 2% LA extracts from Laurus nobilis L. incorporated WPFs (LA2-WPF), (3) 4%
LA extracts from Laurus nobilis L. incorporated WPFs (LA4-WPF), (4)
2% SA extracts from Salvia ofcinalis. incorporated WPFs (SA2-WPF)
and (5) 4% SA extracts from Salvia ofcinalis. incorporated WPFs
(SA4-WPF). These ve WPF solutions (15 mL) were cast on sterile
plastic Petri dishes (9 cm diameter) and dried overnight at 35  C
and 45 5% RH. Thereafter dried lms were peeled for further use.
Film thicknesses were measured with a Digimatic Mitutoyo
Micrometer (Mitutoyo Corporation, Kawasaki, Japan) to the nearest
0.001 mm. Measurements were taken at 10 random locations of the
lms. Average thicknesses for WPC, LA2-WPF, LA4-WPF, SA2-WPF
and SA4-WPF lms were 0.172 0.013, 0.224 0.012,
0.284 0.015, 0.235 0.016 and 0.295 0.011 mm (standard
error), respectively.
2.4. Meatball preparation and lm application
Beef as boneless rounds was obtained from the local butcher in
Izmir, Turkey. All subcutaneous fat and inter-muscular fat was
removed from the muscles and used as the fat source. Lean and fat
were ground through a 3.5 mm plate grinder. Ground lean and back
fat were weighed to produce a target fat content of about 20%,
hand-mixed for 20 min and shaped into 7 cm diameter (and height
of 1 cm) meatballs. This was followed by cooking in a pre-heated
180  C electric oven for approximately 30 min (Arelik,Turkey)
which was standardized for temperature using a surface thermocouple (to give an internal temperature of 72  C). Samples of
cooked meatballs were randomly divided into six groups: (1)
control without edible lm (EF) (C), (2) control coated with WPC,
(3) 2% LA extracts from Laurus nobilis L. incorporated WPFs (LA2WPF), (4) 4% LA extracts from Laurus nobilis L. incorporated WPFs
(LA4-WPF), (5) 2% SA extracts from Salvia ofcinalis L. incorporated
WPFs (SA2-WPF) and (6) 4% SA extracts from Salvia ofcinalis L.
incorporated WPFs (SA4-WPF).
Meatballs were placed in the Petri dishes with the previously
prepared WPFs. Meatballs were manually wrapped with the WPFs

T. Akcan et al. / LWT - Food Science and Technology 77 (2017) 323e331

so that the entire surface of samples was covered by the edible lm.
Samples were stored at
18 1  C for 60 days and sampling was
carried out at days 15, 30, 45 and 60 for further analyses. The selection of the storage time was made upon the recommendations
made by meat retailers and reliable industrial and scientic databases (Meat Safety, 2016). The sampling dates were selected to
identify the targeted span to justify the usage of these composites;
i.e., WPF NAE.
2.5. Antioxidant activity with 2, 2-diphenyl-2-picrylhydrazyl
radical-scavenging assay
2,2-Diphenyl-2-picrylhydrazyl (DPPH) radical-scavenging assay
was modied according to Fratianni et al. (2010). Meat was mixed
with methanol (1:10 w/v) and immediately homogenized for 1 h.
The mixture was centrifuged at 4  C for 10 min at 1500g (Nve,
Trkiye), and the supernatant was collected. 0.1 g of the samples
and 5 mL of 0.004% DPPH in methanol were added to a test tube.
The samples were kept at room temperature for 30 min with
constant mixing. The percent inhibition of free radical formation by
DPPH (D%) was calculated as follows: D% ([Ablank eA sample/
Ablank])  100, where Ablank is the absorbance of the control reaction (containing all reagents except the test compound) and A
sample is the absorbance of the test compound read (517 nm).
2.6. Total phenols content (TPC)

325

UVeVis spectrophotometer (A1). Para-anisidine reagent (1 mL) was

added to 5 mL of the mixture and held in dark for 10 min before
absorbance reading (A2) at 350 nm. The result was calculated as
Av 25  (1.2  A2eA1)  m
1, where m represents mass of
extracted lipid from meatball.
2.10. Thiobarbituric acid value
Lipid oxidation was measured by the 2-thiobarbituric acid (TBA)
extraction method of described Witte, Krause, and Bailey (1970) as
modied. TBA values were calculated by multiplying the absorbance by 94%, the recovery of the standard from meat, resulting in a
K value of 5.2. The TBA values were calculated as mg of malondialdehyde (MDA) per kg of sample.
2.11. Color measurement
Color was measured at the surface of cooked meatballs during
the storage at
18 1  C for 60 d. Five measurements were taken
from each formulation at days 15, 30., 45. and 60. Color Flex A601010-615 Manual Version 23 Hunter Lab spectrocolorimeter
equipped with the light source illuminant D65 (100 standard
observer) was used for measurement. Color coordinate values
(Commission Internationale de lEclairage-CIE L*lightness,
a*redness and b*yellowness) were recorded. Before each measurement the apparatus was standardized against a white plate.
2.12. Sensory analysis

The phenolic content measurements were performed in both

the extracts and the meat products using a modied FolineCicalteu

lez (2001). The
method of that described by Escarpa and Gonza
extracts were diluted (1:200) with ethanol and 0.5 mL aliquots
were used for the quantication of total phenolics. For meatballs,
0.5 g were leaved in 5 mL methanol overnight in the refrigerator.
Mixture of 0.5 mL of each extract or spectrophotometric standard,
2.5 mL of FolineCiocalteu reagent and 2 mL of 7.5% Na2CO3 were
introduced in a ask. After letting them react for 30 min, the solutions were measured at 760 nm. Results were expressed as milligrams of Gallic acid equivalent (GAE) per milliliter of extract.

An eleven-member panel evaluated the samples on days 15, 30,

45 and 60 after frozen storage. Samples were placed in white
polystyrene plates coded with random 3-digit numbers. Samples
were heated in a microwave oven (5 min and 700 W) immediately
before serving. An eight-point scale was used where 8 extremely
desirable, extremely juicy, intense in beef avor, extremely tender,
acceptable and 1 denoted extremely undesirable, extremely dry,
devoid of beef avor, tough and unacceptable. Water and bread
were served for cleaning the mouth between samples.

2.7. Peroxide value (PV)

2.13. Statistical analysis

Peroxide value (PV) was determined according to the standard

method of AOAC. (1995) in the lipid samples extracted, as described
earlier. The lipid sample (1 g) was dissolved in 30 mL of the 3:2
acetic acid: chloroform solution, followed by the addition of 0.5 mL
saturated KI solution and manual shaking for 1 min. After adding
30 mL distilled water, the sample was titrated with 0.1 N sodium
thiosulfate solution. The results were expressed as milliequivalents
(meq) of active oxygen per kilogram of lipid.

Two replications of the study were performed and measurements of all parameters were made in duplicate. Mean values for
measured parameters were calculated and compared by analysis of
variance using the SPSS software for windows (SPSS 21.0 for Windows; SPSS Inc. Chicago, IL, USA). Storage data values were analyzed
using two-way ANOVA with treatment and storage time as main
effects. Means were further compared using Duncan test. Statistical
signicance was identied at the 95% condence level (P < 0.05).
The average values were reported along with standard deviation
(Standard Deviation).

2.8. Conjugated diene (CD) value

Lipid (0.5 g) extracted from meatballs was dissolved in isooctane and absorbance was measured at 234 nm. The increase in
the absorbance for each 50 mg lipid was determined (IUPAC., 1992).
Results were reported as absorbance E1%
1cm , which was given by the

1
formula: E1%
234:
A

(C*d)
,
where
Al is the absorbance at
l
1cm
234 nm, C the concentration of the lipid solution in iso-octane (g
100 ml
1) and d is the length of the cell (cm).
2.9. Para-Anisidine value (p-Av)
Para-anisidine value was determined by IUPAC. (1987, pp.
143e144) method. Meatball lipid was dissolved in n-hexane and
the absorbance of the mixture was measured at 350 nm by a

3. Results and discussion

3.1. Total phenolics and antioxidant activity results
Results of the effect of edible lms and natural antioxidants on
DPPH and phenolic content of cooked meatballs are presented in
Table 1. DPPH (%D) ranged from 45.78 to 90.47%. The antioxidant
capacity of C, WPC, LA2-WPF, SA2-WPF and SA4-WPF samples
signicantly (P < 0.05) decreased during the storage time. The
antioxidant potential of meatball samples was signicantly
(P < 0.05) affected by the application of NAE-WPC. Especially LA2WPF and LA4-WPF groups had higher anti-radical activity than the
other samples during the entire assay. This antioxidant activity may

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T. Akcan et al. / LWT - Food Science and Technology 77 (2017) 323e331

Table 1
Antioxidant effects of edible lms containing laurel or sage extracts against DPPH radical (%D) and Total phenols content (mg GAE 100 g
1) values of cooked meatballs during
frozen storage.a
Storage Period (Day)
15
Treatment
C
WPC
LA2-WPF
LA4-WPF
SA2-WPF
SA4-WPF

62.04
62.28
89.60
90.47
71.67
79.96

Treatment
C
WPC
LA2-WPF
LA4-WPF
SA2-WPF
SA4-WPF

86.13 1.66fA
131.49 2.68eA
212.90 2.00bA
236.54 4.92aA
144.45 2.19dA
156.57 3.30cA

1.31dA
0.92dA
1.03aA
0.23aA
0.90cA
0.91bA

30

45

60

DPPH (%D)
56.55 1.05eB
57.64 0.70eB
84.16 0.95bB
87.16 1.32aA
66.29 0.76dB
71.82 2.04cB

50.25
54.31
77.02
81.87
60.76
66.79

Total Phenols
75.67 0.99fB
117.96 6.29eB
186.25 4.24bB
210.20 6.31aB
127.63 2.81dB
139.39 3.21cB

55.36 2.63fC
87.84 2.71eC
152.54 8.61bC
192.10 3.48aC
101.30 4.23dC
119.80 3.44cC

1.93fC
0.97eB
1.34bC
1.18aB
0.94dC
1.79cC

45.78
46.93
70.43
81.32
54.96
63.30

2.04eD
4.74eC
3.02bD
5.94aB
3.30dD
3.19cD

46.04 2.22dD
74.48 1.81cD
103.88 6.34bD
153.39 17.48aD
78.58 4.74cD
93.99 3.38bD

aee Treatments within the same storage condition with the same superscripts are not different.
AeC Storage conditions within the same treatment with the same superscripts are not different.
a
The mean standard error. C, control without EF; WPC, control WPFs without NAEs addition; LA2-WPF, 2% LA extracts incorporated WPFs; LA4-WPF, 4% LA extracts
incorporated WPFs; SA2-WPF, 2% SA extracts incorporated WPFs and SA4-WPF, 4% SA extracts.

be plausibly attributed to the presence of phenolics from the NAEs.

On the other hand. Kosar, Dorman, and Hiltunen (2005) reported
that methanolic extracts of LA and SA had DPPH radical-scavenging
activity, with SA possessing higher antioxidant activity. Although
few studies are available in the literature regarding the measurement of DPPH value in meat products, In this study, the presence of
phenolic compounds were determined in sage (63.49 0.95 mg
GAE 100 g
1) and laurel extracts (81.68 0.56 mg GAE 100 g
1).
Hinneburg et al. (2006) reported 92 mg GAE 100 g
1 in laurel ex
ska, Oszmian

ski, and Lamertracts while Matkowski, Zielin
Zarawska (2008) reported that total phenolic material content of
sage extracts was 62.2 mg GAE 100 g
1. These differences may
result from differences in the plant variety, time, temperature,
solvent, phenolic acid equivalent and extraction method
(Hinneburg et al., 2006; Pizzale, Bortolomeazzi, Vichi, beregger, &
Conte, 2002). Total phenolic content of meatball samples are shown
in Table 1. C and WPC groups resulted in lower (P < 0.05) total
phenolic content as compared to the other samples. The presence
of phenolic compounds in the meat samples without added plant
extracts may be attributed to the phenolic structures of aromatic

amino acids. The results clearly show that addition of the plant
extracts signicantly increased the TPC in treated samples. LA2WPF and LA4-WPF groups had higher phenolic contents than the
other groups during storage. These results show that WPF-NAE
groups had a signicant (P < 0.05) effect on meatball samples
during storage time. In studies regarding utilization of phenolic
compounds as antioxidants, it was concluded that as a result of the
usage of plant originated additives which have high amounts of
phenolic compounds in meat products, it is possible to maintain the
antioxidant activity at maximum level during shelf life. For
instance, curry, mint leaves (Biswas, Chatli, & Sahoo, 2012), avocado

vez, 2011)
(Rodrguez-Carpena, Morcuende, Andrade, Kylli, & Este
extracts and Echinacea angustifolia extract (Gallo, Ferracane, &
Naviglio, 2012) were efciently used to maintain the antioxidant
protection of the products during storage period.

3.2. PV
PV measured during frozen storage of the cooked meatball
samples are shown in Table 2. PV for all samples varied irregularly

Table 2
Antioxidant effects of edible lms containing laurel or sage extracts on changes in peroxide (meq O2 kg
1) and conjugated diene (absorbance E1%
1cm ) values of cooked meatballs
during frozen storage.a
Storage Period (Day)
15

30

45

Treatment
C
WPC
LA2-WPF
LA4-WPF
SA2-WPF
SA4-WPF

5.78
5.28
4.59
3.77
4.53
4.00

Peroxide value
7.14 1.59aAB
6.41 1.87abA
2.86 1.38cA
1.89 1.32cA
5.76 2.14abA
4.16 1.56bcA

7.84
8.29
3.37
2.58
6.19
4.20

Treatment
C
WPC
LA2-WPF
LA4-WPF
SA2-WPF
SA4-WPF

17.82 0.48aA
17.45 1.42aA
9.57 0.80bcB
8.49 2.29cAB
14.54 0.32bA
10.15 1.51bcB

CD value
18.51 0.21aA
16.69 0.15abA
8.59 2.03dB
7.01 1.58dB
14.78 0.89bA
12.00 2.10cAB

13.75
13.17
11.65
10.32
12.80
12.87

0.97aB
0.52abA
1.71abA
1.24bA
0.52abA
1.11abA

60

1.37aA
2.58aA
1.78bcA
1.73cA
2.00abA
1.03bcA

0.94aC
0.78aC
0.36bA
1.20cA
0.64abB
0.76abA

7.41
7.07
2.93
2.54
6.02
3.65

0.53aAB
1.98aA
1.15bA
1.35bA
1.50aA
0.97bA

15.71 0.41aB
14.83 0.54bB
10.06 0.39dAB
7.81 0.53eB
11.54 0.43cC
10.93 0.17cAB

aee Treatments within the same storage condition with the same superscripts are not different.
AeC Storage conditions within the same treatment with the same superscripts are not different.
a
The mean standard error. C, control without EF; WPC, control WPFs without NAEs addition; LA2-WPF, 2% LA extracts incorporated WPFs; LA4-WPF, 4% LA extracts
incorporated WPFs; SA2-WPF, 2% SA extracts incorporated WPFs and SA4-WPF, 4% SA extracts.

T. Akcan et al. / LWT - Food Science and Technology 77 (2017) 323e331

during storage. PV measures the amount of hydroperoxides formed

as primary oxidation products at the initial stages of lipid oxidative
reactions (Teets & Were, 2008). These peroxides are very reactive
and may propagate further oxidative reactions to lipids and also to

vez, 2011), hence, their assessment provides valuable
proteins (Este
scientic information. Similar to our results, increments in PV
during storage of holy basil and galangal added to cooked ground
pork and rosemary, myrtle, nettle and lemon balm extracts added
to beef patties were reported by Hassan and Swet Fan (2005) and
Akarpat, Turhan, and Ustun (2008), respectively. PVs show statistically signicant (P < 0.05) differences between groups during
storage. The addition of extracts had an effect on PVs as LA4-WPF
had lower oxidation values during storage (P < 0.05). Frozen storage had no effect on PVs of NAE-WPF groups compared to C group
(P < 0.05). These results indicate that NAE-WPF applications were
effective in controlling lipid oxidation during frozen storage of
meatballs. No reports have been found in the literature concerning
the effects of the edible lms with natural antioxidant extracts
incorporated (laurel and sage) on frozen cooked meat products
oxidation. According to our results, the application of the NAE-WPF
inhibited the early expressions of the oxidative damage to meat
lipids during frozen storage. In addition to the already antioxidant
protection likely provided by plant phenolics, the action of the WPF
as oxygen barriers may have also contributed to inhibit the formation of peroxides as these species require the presence of mo
vez, 2015). In this regard, the thickness of the
lecular oxygen (Este
lms could have had an impact and hence, contribute to isolate the
meat product from the surrounding oxygen. The higher thickness of
the WPF treated with the NAE, probably due to the inuence of the
natural extracts on the rheological properties of the protein lms,
may contribute to explaining the higher antioxidant protection in
these products. In agreement with our results, Akarpat et al. (2008)
reported that treating beef patties with rosemary, myrtle, nettle
and lemon balm extracts led to signicantly (P < 0.05) lower
peroxide values compared to control during frozen storage. Stuchell
and Krochta (1995) reported that acetylated monoglyceride coatings used alone or after applying whey protein isolate solution or
whey protein isolate powder on the sh surface reduced PVs. El
et al. (2014) found that the essential oils of L. nobilis obtained
from hydrodistillation had a remarkable inhibitory effect on the
linoleic acid peroxidation. In analyzed meatballs, after 60 days of
storage a varied and disproportional increase in the levels of both
PV and AV was observed. This may indicate that the rate of hydroperoxide decomposition was higher than the rate of formation
at that point of storage (Georgantelis, Blekas, Katikou, Ambrosiadis,
& Fletouris, 2007).
3.3. Conjugated diene (CD) value
Unsaturated fatty acid double bonds occur naturally as methylene incomplete systems. As meat begins to oxidize, the double
bonds of these fatty acids shift to create conjugated systems, which
can then be measured spectrophotometrically (Teets & Were,
2008).
The concentration of conjugated dienes (CD) signicantly
decreased for all treatments (Table 2). Occurrence of changes in
treatment groups was found to be statistically signicant during
storage time with the exception of SA4-WPF group (P < 0.05). NAEWPF groups had lower concentration of CD compared to C and WPC
groups (P < 0.05). Particularly LA4-WPF exhibited the lowest concentration of CD during storage time (P < 0.05). Also Juntachote,
Berghofer, Siebenhandl, and Bauer (2006) noted that treatments
of cooked ground pork with dried Galangal and Holy basil powders
and extracts increased the concentration of conjugated diene with
the exception of the sample treated with Holy basil extracts during

327

the rst 3 days of storage and then decreased till the end of storage.
Georgantelis et al. (2007) reported that conjugated diene values of
beef burgers treated with rosemary extract led to lower values
when compared to control at the end of frozen storage period (day
180). CD hydroperoxides are expected to decompose to secondary
products that have not the ability of UV light absorption or cause
reduction in absorptivity. In the present study, this was observed.
~ a-Ramos and Xiong (2003) reported that
Similar to our results, Pen
addition of nonhydrolyzed and hydrolyzed whey protein isolates to
cooked pork patties decreased concentration of conjugated dienes
for all treatments at end of the storage time (day 7). It is worth
mentioning that whey proteins and their hydrolysates have also
been reported to display antioxidant properties (Liu, Xiong, &
Buttereld, 2000). It is hence, likely that WPC may have also
contributed to inhibit lipid oxidation by radical scavenging mechanisms. This extent, however, requires further conrmation in the
present conditions.
3.4. P-Anisidine value (p-Av)
The effect of processing on the oxidation of the lipids in meatballs was evaluated using diverse oxidation parameters. One of
them is p-anisidine which is used for the aldehydes (secondary
products) generated from the breakdown of peroxides. Table 3 reports the data obtained with these determinations. The p-anisidine
value was similar (P > 0.05) between C, WPC and SA2-WPF groups
at day 15. On the contrary LA2-WPF, LA4-WPF and SA4-WPF groups
had signicantly (p < 0.05) lower p-anisidine value at day 15 than
the other treatments. It is shown that laurel extract has been
effective on p-anisidine value which is in good agreement with the
previous measurements, already described. Storage period had a
signicant (P < 0.05) inuence on p-anisidine values of cooked
meatballs. Similar to our results, Kobus-Cisowska, Flaczyk,

ska, and Kmiecik (2014) reported that addition of ginkgo
Rudzin
biloba leaves extracts had a signicant effect on the inhibition of
the p-anisidine values of cooked pork meatballs. Regarding the
cooked samples, the heat treatment caused a decrease in the
amount of peroxides, which were transformed into secondary
oxidation products. This resulted in an increase of the p-anisidine
value. Rodriguez-Estrada, Penazzi, Caboni, Bertacco, and Lercker
(1997) reported that the cooked hamburgers registered a signicant rise in the p-anisidine values regard to that of the raw meat.
3.5. TBA
The antioxidant effects of treatments, as measured by TBA, over
60 days of frozen storage are shown in Table 3. TBA values were
signicantly (P < 0.05) lower for all treatments compared to those
for the control during the frozen storage. Similar to p-AV, the lowest
TBA value occurred in the LA4-WPF group at 15 day (P < 0.05). NAEWPF groups were the most effective (P < 0.05) at reducing the
values of TBA. Also compared to control, WPC group had signicantly lower (P < 0.05) TBA values during storage which emphasizes the potential role of the protein lms as antioxidants thorough
a likely oxygen barrier mechanism and plausible radical scavenging
actions. This result indicates that lipid oxidation was effectively
retarded by WPFs and NAE-incorporated WPFs during frozen
storage time.
Soy protein-based edible lms containing essential oils of
oregano and thyme applied on ground beef patties had insignicant TBARS value as compared to controls (Coskun et al., 2014).

ri, Saucier, and Lacroix (2004) noted that
Oussalah, Caillet, Salmie
milk protein-based edible lms containing 1% essential oil of
oregano and pimento applied on beef muscle slices resulted in
either higher or statistically insignicant, which disagreed with our

328

T. Akcan et al. / LWT - Food Science and Technology 77 (2017) 323e331

Table 3
Antioxidant effects of edible lms containing laurel or sage extracts on changes in para-anisidine (Av) and TBA (mg MDA kg
1) values of cooked meatballs during refrigerated
storage.a
Storage Period (Day)
15

30

45

60
19.32 1.29aA
17.65 0.79bA
11.00 0.25dA
9.69 0.30eA
14.52 0.46cA
10.77 0.66dA

Treatment
C
WPC
LA2-WPF
LA4-WPF
SA2-WPF
SA4-WPF

3.68
3.55
2.38
2.16
3.37
2.65

0.06aD
0.29aD
0.32bcD
0.41cD
0.19aD
0.21bD

p-AV
10.89 0.60aC
9.71 0.51bC
5.11 0.72dC
4.94 0.85dC
7.10 0.59cC
5.65 0.87dC

14.13 0.40aB
13.68 0.32aB
6.61 0.57dB
6.77 0.86dB
10.27 0.17bB
7.87 0.19cB

Treatment
C
WPC
LA2-WPF
LA4-WPF
SA2-WPF
SA4-WPF

0.38
0.33
0.21
0.15
0.27
0.21

0.03aD
0.05bD
0.02dD
0.02eB
0.03cB
0.02dB

TBA
0.70
0.44
0.28
0.23
0.34
0.26

0.81
0.59
0.33
0.36
0.36
0.34

0.04aC
0.06bC
0.03cdC
0.03dB
0.03cAB
0.06cdAB

0.02aB
0.10bB
0.04cB
0.09cA
0.10cAB
0.17cAB

0.90
0.76
0.42
0.42
0.41
0.41

0.04aA
0.04bA
0.02cA
0.10cA
0.07cA
0.16cA

aee Treatments within the same storage condition with the same superscripts are not different.
AeC Storage conditions within the same treatment with the same superscripts are not different.
a
The mean standard error. C, control without EF; WPC, control WPFs without NAEs addition; LA2-WPF, 2% LA extracts incorporated WPFs; LA4-WPF, 4% LA extracts
incorporated WPFs; SA2-WPF, 2% SA extracts incorporated WPFs and SA4-WPF, 4% SA extracts.

results. A similar positive effect of sage or sage extracts in meat

systems has been reported by others. Sage reduced TBARS values in
raw and cooked pork patties (Mc Carthy, Kerry, Kerry, Lynch, &
Buckley, 2001b) during storage at 4  C as well as in fresh and
frozen pork patties (Mc Carthy et al., 2001a). Addition of 3% (w/w)
sage essential oil efciently inhibited lipid oxidation in raw pork

vez et al.
and in cooked bovine meat (Fasseas et al., 2008). Este
(2007) showed that 0.1% essential oil from sage was more effec^te

during 90 days
tive in inhibiting the generation of MDA in liver pa
of storage at 4  C than 0.02% BHT. Also addition of 0.05, 0.10 and
0.15% (w/w) sage in Chinese sausage had lower TBA values as
compared with controls (Zhang et al., 2013). Tanabe et al. (2002)
reported that TBA values of the pork homogenate treated with
0.001 mL liquid extracts of 15 herb and spice samples (i.e. ginger,
cinnamon, clove, bay, sage, rosemary, thyme, savory, oregano,
parsley, sansho, allspice, cumin, nutmeg or caraway) were signicantly lower than the control. Our results are in agreement with
these previous results, indicating that sage and laurel can be used
as a natural antioxidant addition for edible lms which used for
inhibition of oxidation in meat products. The compounds in sage
showing the greatest antioxidant activity have been identied as
carnosol, rosmarinic acid and carnosic acid followed by caffeic acid,
rosmanol, rosmadial, genkwanin and cirsimaritin (Cuvelier,
Richard, & Berset, 1996). Politeo, Juki

c, and Milos (2007) noted
that eugenol and methyl eugenol which are components of
L. nobilis considered as the main contributors to the antioxidant
activity of laurel.
3.6. Instrumental color
Mean values for color components (L*, a* and b*) of meatballs
are shown in Table 4. LA2-WPF, LA4-WPF and SA4-WPF groups
displayed the lowest L* values (P < 0.05) during storage. Similar to
the lightening effect of edible lms on cooked meatballs observed
in the present study, Coskun et al. (2014) revealed that ground beef
treated with oregano essential oil incorporated in edible lms and
stored at 4  C for 12 days had higher L* value toward the end of
storage compared with control samples. Accordingly our results,
Zhang et al. (2013) reported that chinese sausage treated with 0.15%
sage and stored at 4  C for 21 days had lower L* value toward the
end of storage compared with control samples. The lower L* values

of LA2-WPF, LA4-WPF and SA4-WPF groups may have resulted from

the presence of pigmented materials which comes from the plant
itself, such as chlorophylls (Li-wen et al., 2012). Also Coskun et al.
(2014) investigated the effect of soy based edible lms incorporated with oregano essential oils on ground beef patties and they
found that incorporated lm had higher L* values as compared to
control.
The red-brownish color of cooked meats is mainly determined
by the presence of denatured-globin hemochromes formed as a
result of high temperatures (Fox, 1994). Redness of samples from
groups except LA4-WPF (P < 0.05) was not affected by the storage
time. At end of the storage, samples coated with NAE added EFs had
highest a* values compared with C and WPC groups (Table 4).
Especially LA4-WPF group had the highest a* values which means
that the concentration of NAEs had an inhibition effect on oxidation
of myoglobin. Mc Carthy et al. (2001a) reported that SA extract
resulted in lower a* values when applied to patties manufactured
from previously frozen pork as compared with the control over 6~o, Este

vez, Kylli, Heinonen, and
day refrigerated storage. Ganha
Morcuende (2010) reported that the decrease of redness was
signicantly affected by the addition of fruit extracts. Coskun et al.
(2014) pointed out that ground beef patties coated with thyme and
oregano essential oils added soy protein based EFs had lower a*
values compared with control groups and coated with soy protein
based EF without essential oils groups at 8 and 12 days of storage.
On the other side, Camo et al. (2008) stated that oregano extracts
containing active packaging material applied on fresh lamb steaks
resulted in higher a* values than did the control, and were effective
in delaying color loss during 13 days of refrigerated storage.
Yellowness (b* values) of all EF applied samples tended to increase over the storage period, while there was no signicant
change in b* value of the LA2-WPF, LA4-WPF and SA2-WPF groups
during frozen storage (P < 0.05) (Table 4). SA4-WPF and LA4-WPF
groups had higher b* values at end of storage (P < 0.05). Unlike L*
values, LA2-WPF, LA4-WPF and SA4-WPF groups had highest b*
values which may have resulted from the presence of pigmented
materials which comes from the plant itself, such as chlorophylls
nal, Babaoglu, and Karakaya (2014) reported that b* values of sage
essential oil added minced beef had increased compared with
control.

T. Akcan et al. / LWT - Food Science and Technology 77 (2017) 323e331

329

Table 4
Instrumental CIE lightness (L*), redness (a*) and yellowness (b*) values of cooked meatballs coated with antioxidant edible lms during frozen storage.a
Storage Period (Day)
15

30

Treatment
C
WPC
LA2-WPF
LA4-WPF
SA2-WPF
SA4-WPF

39.19
41.08
37.37
31.09
33.80
29.41

Treatment
C
WPC
LA2-WPF
LA4-WPF
SA2-WPF
SA4-WPF

7.06 0.83bA
4.95 0.56cAB
7.68 0.53bA
10.64 1.16aA
6.87 0.33bA
7.69 0.97bA

Treatment
C
WPC
LA2-WPF
LA4-WPF
SA2-WPF
SA4-WPF

12.95
11.30
15.66
18.81
17.90
16.45

1.95abA
3.12aA
1.83bB
2.27cdB
2.28cA
2.55dB

0.46dAB
1.04eAB
0.61cA
1.48aA
0.22abA
1.72bcB

45

L*
39.58
42.53
41.59
35.56
34.23
36.87
a*
6.82
4.71
7.46
9.10
7.07
6.81

b*
14.09
10.70
15.74
18.64
18.57
17.71

2.10aA
0.97aA
1.59aA
1.75cA
1.39cA
3.06bcA

1.17aA
1.27aA
1.95bB
1.34cB
2.88bA
1.71cB

7.09 0.73bA
5.15 0.26cAB
7.23 0.54bA
11.35 0.98aA
6.76 0.58bA
7.39 0.15bA

0.71bA
0.24cA
1.04bA
1.14aB
0.89bA
0.67bA

39.84
41.15
36.94
30.26
35.68
31.08

60

1.12bA
1.19cB
1.22bA
1.06aA
1.40aA
0.69aB

13.61
12.20
15.34
19.66
18.45
19.82

1.18cAB
0.69dA
1.13bA
0.23aA
0.86aA
0.98aA

39.52
41.04
38.26
33.29
35.49
31.04

1.76aA
2.78aA
2.19abB
2.09cdAB
1.14bcA
3.01 dB

7.04 0.26bA
5.41 0.50cA
6.92 0.85bA
11.23 0.41aA
7.19 1.59bA
7.53 0.52bA
12.52
11.83
14.97
19.69
16.72
20.19

0.79dB
0.49dAB
1.19cA
0.71aA
1.97bA
0.26aA

aee Treatments within the same storage condition with the same superscripts are not different.
AeC Storage conditions within the same treatment with the same superscripts are not different.
a
The mean standard error. C, control without EF; WPC, control WPFs without NAEs addition; LA2-WPF, 2% LA extracts incorporated WPFs; LA4-WPF, 4% LA extracts
incorporated WPFs; SA2-WPF, 2% SA extracts incorporated WPFs and SA4-WPF, 4% SA extracts.

3.7. Sensory analysis

C group had higher sensory scores and overall acceptability than
EFs groups during frozen storage (P < 0.05). SA4-WPF had the
lowest overall acceptability scores (4.95) during storage period.
WPC had lower appearance and avor scores than the other groups
during frozen storage (P < 0.05). Therefore, these results suggest
that WPC decreased the sensory quality and overall acceptability of
meat balls but the addition of NAE improved some parameters such
as appearance and avor scores. However, it is obvious that the
increasing amount of extracts had adverse effect on sensory

characteristics of the cooked meatballs although those meatballs

still scored as acceptable. Chi, Zivanovic, and Peneld (2006) reported that avor scores for bologna slices with the application of
chitosan lms prepared with oregano essential oil decreased with
increasing concentration of essential oil in the lm formulation.
Coskun et al. (2014) suggested that oregano and thyme essential
oils incorporation into the soy based EFs resulted in an adverse
effect on sensory characteristics of the ground beef patties. As
generally expected sensory analyses scores declined during the
frozen storage (Fig. 1). Reason of the declining scores of EFs group
has been associated to edible lm treatment which is

Fig. 1. Sensory evaluation scores for cooked meatballs coated with antoxidant edible lms during frozen storage. C, control without EF; WPC, control WPFs without NAEs addition;
LA2-WPF, 2% LA extracts incorporated WPFs; LA4-WPF, 4% LA extracts incorporated WPFs; SA2-WPF, 2% SA extracts incorporated WPFs and SA4-WPF, 4% SA extracts. Each point
represents the mean value standard error. For each sensory attribute between groups, bars having common letters are not different.

330

T. Akcan et al. / LWT - Food Science and Technology 77 (2017) 323e331

unconventional treatment for the customers. Considering the

present results, oxidation phenomena may not be behind the
sensory scores and acceptability values and other factors may be
involved as the impact of the pigments and avors naturally present in the plant sources. The presence of unexpected sensory traits
(color/avor) in beef meatballs may contribute to the lower sensory
scores received by the treated samples.
4. Conclusions
LA and SA, when incorporated into whey protein based EFs,
resulted in lower peroxide and CD value, particularly at later periods of frozen storage, with signicant effect on TBA and p-anisidine value, indicating that antioxidant EF application on cooked
meatballs surface may control lipid oxidation and lipid hydrolysis.
It was concluded that extracts of these plants could be successfully
added to edible lms to function as natural antioxidants. The results support that the use of whey protein e laurel and sage NAE
lms as packaging material may have potential to extent the shelf
life of oxidation-susceptible products such as cooked meatballs.
The antioxidant effect of phenolic compounds naturally present in
the extracts may also be joined to the oxygen barrier effect and
further antioxidant protection of the WPF. As promising as these
results are additional research will be required to improve the
acceptability and sensory properties of the meatballs treated with
NAE edible lms. Further research could investigate the combined
application of laurel and sage in different meat products as well as
the use of different quantities to those used in this study for optimization of the antioxidative effects.
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