Hindawi

Journal of Food Processing and Preservation

Volume 2023, Article ID 8381828, 8 pages
https://doi.org/10.1155/2023/8381828

Research Article
The Effect of Chitosan and Rosemary Essential Oil on the Quality
Characteristics of Chicken Burgers during Storage

Pouya Farokhzad,1 Asiye Ahmadi Dastgerdi ,1 and Javad Tabatabeian Nimavard2

1
Department of Food Science and Technology, Ardestan Branch, Islamic Azad University, Ardestan, Iran
2
Department of Animal Science, Islamic Azad University, Ardestan Branch, Ardestan, Iran

Correspondence should be addressed to Asiye Ahmadi Dastgerdi; [email protected]

Received 1 January 2023; Revised 7 March 2023; Accepted 2 June 2023; Published 7 June 2023

Academic Editor: Fatih Oz

Copyright © 2023 Pouya Farokhzad et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is
properly cited.

In this study, the effects of chitosan film (1 and 2%) containing rosemary essential oil (1%) in free and nanoliposome forms were
investigated on the physicochemical, microbial, organoleptic, and oxidation characteristics of chicken burgers during storage (day
1, day 10, and day 20) at 4°C. The results showed that chitosan and rosemary essential oil decreased pH, total volatile basic
nitrogen compounds (TVB-N), and oxidation parameters (peroxide value and thiobarbituric acid) in the chicken burgers
(p < 0:05). Compared to the control group (C), the growth of mesophilic and psychrophilic bacteria, Enterobacteriaceae,
Pseudomonas, Staphylococcus aureus, and mold and yeast in all treated groups (E1, E2, CH1, CH2, CHE1, CHE2, CHE3, and
CHE4) was delayed during storage. The color and hardness of the chicken burger were affected significantly (p < 0:05).
Regarding sensory characteristics, the control group obtained the highest score. The CHE4 group (2% chitosan+rosemary
essential oil nanoliposomes) was the most effective treatment for controlling the microbial flora, slowing down some
physicochemical and sensory changes, and increasing the shelf life of chicken burgers (p < 0:05). As a result, chitosan coating
with rosemary essential oil nanoliposome can guarantee microbiological safety and is recommended for long-term storage of
chicken burgers during cold storage.

1. Introduction soluble substances and therefore can increase the shelf life
of meat products [3].
Meat and its products are sources of protein, energy, B vita- Chitosan (C6H11NO4) is a natural polysaccharide that
mins, minerals, and amino acids. They are very sensitive to has been found in the exoskeleton of crustaceans, fungal cell
microbial spoilage due to their nutrients and chemical (high walls, and other biological materials [4, 5]. It has antibacte-
water activity and natural pH) and physical characteristics. rial and antifungal properties that are suitable for food pres-
It is possible to grow different microorganisms, especially ervation and increases the quality and stability of the
psychrotroph and pathogenic microorganisms [1]. Chicken physical characteristics of the food by creating a semiperme-
meat and chicken burgers and industrial production of bur- able barrier to water vapor, oxygen, and carbon dioxide and
gers and other ready-to-eat foods are important. increases the shelf life of the product [6].
Due to the increase in food-borne diseases caused by Essential oils and extracts that are incorporated into the
various pathogenic microorganisms, new methods for meat edible coating and films have antimicrobial and antioxidant
preservation have been considered. Films and edible coat- activity. It has been claimed that essential oils are safe sec-
ing containing antimicrobial and antioxidant agents can ondary metabolites (GRAS) and are recognized as alterna-
increase the shelf life of meat products. Edible coating slows tives to synthetic additives which can control pathogenic
the release of antimicrobial and antioxidant agents into the and spoilage bacteria and increase the shelf life of food [7].
meat [2]. The polysaccharide, protein, and fat origin coatings Rosemary (Rosmarinus officinalis L.) which belongs to
act as a barrier against the transfer of moisture, gases, and Lamiaceae family is native to South Asia and Europe. Several
2 Journal of Food Processing and Preservation

studies have been conducted to evaluate the antimicrobial 2.5. Chicken Burger Preparation. For burger preparation, the
and antioxidant activity of rosemary essential oil and chicken fillet was minced by a meat grinder. Then, all the
increase the shelf life of food [8–10]. Some studies on the ingredients (onion, 8% breadcrumbs, 2% spices, and 5% liq-
use of chitosan [1, 11–14] and rosemary [15–17] in meat uid oil) were added to the meat in a blender. After cutting
products were reported previously. burger pieces to 100 g (1 × 8 cm), the samples were placed
One of the most important challenges in using essential between two films and were divided into 9 groups. The first
oils in food is improving and increasing their stability in pro- group was the control (C) as without chitosan and rosemary
cessing and controlling their release. Therefore, it is better essential oil. The second and third groups were wrapped in
before using them in food and beverages in order to limit chitosan with a concentration of 1% and 2% (CH1 and
the aroma during processing and storage; they must be encap- CH2). The fourth and fifth groups were wrapped in 1%
sulated [11]. During this process, very small particles or drop- essential oil in free and nanoliposome forms (E1 and E2).
lets are coated. The surrounding compound is called the core The sixth and seventh groups were wrapped in 1% chitosan
material, active compound, internal phase, and secondary film containing 1% essential oil in free and nanoliposome
compound; the material that covers the wall is known as the forms (CHE1 and CHE2). The eighth and ninth groups were
wall matrix, external phase, and membrane [18]. wrapped in 2% chitosan film containing 1% essential oil in
Due to the release of compounds with different hydro- free and nanoliposome forms (CHE3 and CHE4). The sam-
philic properties, nanoliposomes can be a suitable system ples were stored in a refrigerator (4 ± 2:2°C) and tested for
for the microencapsulation of fat-soluble compounds such physicochemical, microbial, and sensory changes for 20 days
as essential oils [19]. Liposomes, which usually have sizes (day 0, day1, day 10, and day 20).
between 3 and 6 nm, can create particles with a larger diam-
eter by joining each other. Features such as low toxicity and 2.6. Chemical Analysis. Briefly, 5 g of sample was homoge-
biodegradability have caused liposomes to be considered as a nized with 45 ml of deionized distilled water for 1 min at
very suitable carrier in modern systems [20]. 100 rpm at room temperature, and pH was measured with
The purpose of this study was to study the effect of chito- a pH meter (Metrohm, Switzerland). Total volatile nitrogen
san and nanoliposomes of rosemary essential oil on the qual- compounds (TVB-N) were determined according to the pro-
itative properties of chicken burgers at 4°C during 20 days. cedures previously characterized [2, 12, 23].

2. Material and Methods 2.7. Oxidation Analysis. The peroxide value (PV) and thio-
barbituric acid (TBARS) were determined according to the
2.1. Materials. Freshly chicken meat was prepared from Sejzi AOCS Cd 8-53 and Cd19-90 methods, respectively [24–26].
slaughterhouse in Isfahan province, Iran. Rosemary (R. offi-
cinalis L.) was obtained from botanical herbarium (Isfahan, 2.8. Color Analysis. For L∗ evaluation, HunterLab (FMS Jan-
Iran). Chitosan with an acetylation degree of 75-80% and a sen GmbH & Co. KG, USA) was used at room tempera-
molecular weight of 500,000 Da was purchased from ture [27].
Sigma-Aldrich Company (UK, Iran). All chemicals and
microbial culture media were obtained from Merck 2.9. Microbial Analysis. 10 g of the chicken burger was
(Germany). homogenized with 90 ml of sterile normal saline, and after
the preparation of serial dilutions, the pour-plate method
2.2. Chitosan Solution Preparation. Briefly, 10 g of chitosan
was used for counting total mesophilic and psychrophilic
was mixed with 500 ml of acetic acid, and the solution was
bacteria in plate count agar (PCA) and was incubated at
stirred with a magnetic stirrer for two days [12].
35°C for 72 hours and 7°C for 10 days, respectively. The
2.3. Essential Oil Extraction. The essential oil of rosemary LAB was enumerated in MRS agar and incubated at 35°C
was extracted by a Clevenger (Ashk-e-Shisheh, Iran) for 3- for 72 h. For the Enterobacteriaceae count, violet red bile
4 h. The collected essential oil was dehydrated by sodium dextrose agar (VRBA) was used after incubation at 35°C
sulfate and kept in the dark in the refrigerator (4°C) until for 24 h. To count Staphylococcus aureus, the Baird-Parker
the experiments [21]. Agar (BPA) was used after incubation at 35°C for 48 h. For
counting mold and yeast, rose Bengal chloramphenicol agar
2.4. Essential Oil Nanoliposome Preparation. In the thin layer was used after incubation at 25°C for 3-5 days. The colonies
coating method, 77.126 mg of soy phosphatidylcholine, were reported as log CFU/g chicken burgers [28].
16.254 mg of cholesterol, 1.365 g of polyethylene glycol,
and 7 ml of rosemary essential oil were mixed in 15 ml of 2.10. Sensory Evaluation. Sensory characteristics such as
chloroform and then deposited as a thin solid layer in a taste, aroma, color, texture, smell, and overall acceptance
rotary evaporator at 40°C. Phosphate buffered saline solu- were evaluated based on a 5-point hedonic scale using 10
tion (PBS) was used to hydrate the dried layer. The liposome panelists on day 10 [23].
particles were broken using an ultrasonic bath (Model 300,
Pulse, Italy) and were passed through 0.45 and 0.25 μm fil- 2.11. Statistical Analysis. The microbial and physicochemical
ters, respectively. In order to separate the free essential oil, parameters (parametric data) were analyzed using one-way
the solution was placed in a dialysis bag, in PBS at 4°C for variance and the Duncan test using SPSS software (version
2 h [22]. 20). The Kruskal-Wallis test was used to analyze
Journal of Food Processing and Preservation 3

6.5
pH

5.5

4.5
0 1 10 20
Storage time (day)

C CHE1
E1 CHE2
E2 CHE3
CH1 CHE4
CH2
(a)
TVB-N
45

40

35
mg N/100 g burger

30

25

20

15

10

0
0 1 10 20
Storage time (day)

C CHE1
E1 CHE2
E2 CHE3
CH1 CHE4
CH2
(b)

Figure 1: Chemical characteristics of chicken burgers during 20 days.

nonparametric data (sensory parameters). The analyses were storage (p > 0:05). pH value of the control group was signif-
conducted in triplicate. icantly higher than the treated groups at the end of storage
(p < 0:05). pH increasing in different groups can be related
3. Results and Discussion to the activity of microorganisms and the accumulation of
volatile bases [2].
3.1. Chemical Characteristics. At days 0 and 4, pH value was At day 0, TVB-N was not significantly different (p > 0:05)
not significantly different in all groups (p > 0:05) in different groups (Figure 1(b)). The initial content of TVB-
(Figure 1(a)). pH value increased significantly during storage N in the studied groups was from 13.58 to 15.82 mg N/100 g
(p < 0:05). In the CHE1, CHE2, CHE3, and CHE4 groups, burger, which indicates the high quality of the burger.
the changes in pH were not significantly different during TVB-N increased significantly during storage (p < 0:05),
4 Journal of Food Processing and Preservation

8
PV
7

5
meq/Kg oil
4

0
0 1 10 20
Storage time (day)

C CHE1
E1 CHE2
E2 CHE3
CH1 CHE4
CH2

1.4
TBARS
1.2

1
mg MDA/kg oil

0.8

0.6

0.4

0.2

0
0 1 10 20
Storage time (day)

C CHE1
E1 CHE2
E2 CHE3
CH1 CHE4
CH2

Figure 2: Oxidation stability of chicken burgers during 20 days.

but this increase was slower in the treatment groups than the and nonprotein nitrogen compounds of meat and produce
control group. volatile nitrogen compounds [30]. Due to the inhibition of
The CHE3 and CHE4 groups were the most effective microbial activity, the TVB-N content in the treated groups
treatments for controlling pH and TVB-N changes in burger was lower than the control group [2, 3, 28].
samples. At day 10, TVB-N in the control sample reached Sarmast et al. [30] reported that chitosan-gelatin coating
92.30 mg N/100 g burger, which was higher than the stan- containing lemon essential oil reduced the rate of pH
dard limit (25 mg N/100 g burger). In all treated groups with increase in the salmon fillets during storage, thereby reduc-
chitosan and rosemary essential oil combination, TVB-N ing microbial growth. Shankar et al. [31] showed that coat-
content did not exceed the limit during 20 days of storage ing of fish fillets with alginate containing essential oils and
[29]. Proteolytic enzymes of microorganisms affect protein citrus extracts reduced pH during storage. Abdeldaie et al.
Journal of Food Processing and Preservation 5

50 Aa
Ba Ca
45 Ab Da Da Ea
BbBc Fa Ga Ha
Ac Cb Cb Db Eb
40 Gc Ec Dc Fb Gc Hb Fb Hb Gb
Hc
35
30
25
L⁎

20
15
10
5
0
C E1 E2 CH1 CH2 CHE1 CHE2 CHE3 CHE4
Treatments

Day 0
Day 10
Day 20

Figure 3: L∗ analysis of chicken burgers during 20 days. The mean ± SD (standard deviation) with different letters differs significantly
(p < 0:05).

[32] found that calcium caseinate film containing rosemary and reduce color degradation and increase the shelf life of
essential oil reduces TVB-N in carp fillets during cold meat products [13].
storage. Zhang et al. [36] showed that edible coating based on
chitosan and bamboo vinegar increased L∗ value in pork.
The color of the coated nuggets with rosemary and licorice
3.2. Oxidation Characteristics. As seen in Figure 2, at the
increased during storage [16].
beginning of the experiments (day 0), the peroxide value
(PV) and TBARS do not show a significant difference
3.4. Microbial Characteristics. The results of microbial anal-
(p > 0:05) but in all chicken burgers increased significantly
yses for chicken burger samples are shown in Figure 4. At
during storage (p < 0:05).
the beginning of the experiment (day 0), no significant dif-
PV represents the first oxidation products, and TBARS
ference was observed between the number of mesophilic,
represents the secondary oxidation products. At the end of
psychrophilic bacteria, Pseudomonas, Enterobacteriaceae,
storage, PV and TBARS in the control sample were signifi-
Staphylococcus aureus, and mold and yeast in different
cantly higher than other treatments (p < 0:05) and reached
groups (p > 0:05). During the storage period, the number
to 7.03 meq/kg oil and 0.93 mg MDA/kg oil, respectively.
of mesophilic and psychrophilic bacteria increased signifi-
The results indicate that coating with chitosan and rose-
cantly in all groups (p < 0:05). At day 20, the number of
mary essential oil (free/nanoliposome) has been able to reduce
mesophilic and psychrophilic bacteria was significantly
oxidation in chicken burgers. Rosemary essential oil contains
higher in the control group than in the treated groups
phenolic compounds and flavonoids that have strong antioxi-
(p < 0:05). In relation to the number of psychrophilic bacte-
dant activity [15, 16]. The antioxidant activity of rosemary has
ria, a similar trend was observed.
been proven in many studies [17, 33, 34]. Also, chitosan cre-
At day 10, the number of mesophilic, psychrophilic bac-
ates a barrier that covers the surface of the chicken burger
teria, Pseudomonas, Enterobacteriaceae, Staphylococcus
and therefore removes oxygen from it and reduces the oxida-
aureus, and mold and yeast increased significantly
tion of lipids in the chicken burger [12].
(p > 0:05). The highest microbial count was observed in the
Hassanzadeh et al. [35] reported a decrease in TBARS
control group, and the lowest count was observed in the
levels in chitosan-coated chicken breasts containing grape
CHE1, CHE2, CHE3, and CHE4 groups (p < 0:05).
seed extract. They showed a delay in increasing total volatile
The samples containing nanoliposomes of essential oil
nitrogen and lipid oxidation in coated lamb.
performed better than the samples containing free essential
oil, which can be attributed to the gradual release of essential
3.3. L∗ Analysis. Figure 3 shows the brightness of chicken oil during storage. The best sample for controlling the bacte-
burgers during 20 days. The control sample had the highest ria in burger samples was the CHE4 group, because the low-
L∗ (lightness). The brightness of all samples decreased sig- est number of bacteria was found in this group. According to
nificantly with time (p < 0:05). the national standard of Iran, the permissible limit of meso-
Meat pigment is deoxymyoglobin (purple-red color). In philic bacteria in burger is 6 log CFU/g of burger [29], and in
the presence of O2, oxymyoglobin (MbO2) is formed in a the control sample at day 10, the number of mesophilic bac-
bright red color. Edible coatings reduce the oxygen level teria was higher than the standard limit. Thus, the control
6 Journal of Food Processing and Preservation

20
19 Total mesophilic bacteria Taste
18

Log CFU/g burger

17
16
15
14
5
13
12
11
10
9
8
7
4
6
5
4
3
2
1
0
3
0 1 10 20
Storage time (day) 2
C CHE1
Odor Color
E1 CHE2 1
E2 CHE3
CH1 CHE4
CH2 0
16
15 Total psychrotrophic bacteria
Log CFU/g burger

14
13
12
11
10
9
8
7
6
5
4
3
2
1
0
0 1 10 20 Overall
Storage time (day)
Texture
acceptability
C CHE1
E1 CHE2
E2 CHE3
C CHE1
CH1 CHE4 E1 CHE2
CH2
4
E2 CHE3
Pseudomonas
CH1 CHE4
Log CFU/g burger

3
CH2
2

1 Figure 5: Sensory characteristics of chicken burgers.

0
0 1 10 20
Storage time (day)
C CHE1
In general, the microbial growth decreased with the
E1
E2
CHE2
CHE3
addition of rosemary essential oil and chitosan, which is
CH1
CH2
CHE4 attributed to the antimicrobial properties of rosemary essen-
5 Staphylococcus aureus tial oil [15, 16] and chitosan [11, 30, 35, 36]. The essential
oils destroy the cytoplasmic membrane of microorganisms
Log CFU/g burger

4
3
and cause cell death [2]. The antimicrobial property of chi-
2
1
tosan is attributed to its polycationic properties that break
0 the cell membrane, but it may be due to its chelating behav-
0 1 10 20
Storage time (day)
ior, water-binding properties, and inhibition of mRNA syn-
C CHE1 thesis [37].
E1 CHE2
E2 CHE3 Hasani-Javanmardi et al. [28] showed that nanoemul-
CH1 CHE4
CH2 sions of safflower oil and cumin essential oil reduced meso-
6 Coliform philic and psychrophilic bacteria, Enterobacteriaceae, and
Log CFU/g burger

5
4
lactic acid bacteria in lamb meat. Lacroix et al. [38] found
3 that the edible coating based on whey protein isolate casein-
2
1
ate reduced the number of mesophilic bacteria in minced
0 meat during refrigeration. Hassanzadeh et al. [35] reported
0 1 10 20
C CHE1 similar results regarding chicken breast coated with chitosan
E1
E2
CHE2
CHE3
and grape seed extract. Dini et al. [2] showed that composite
CH1
CH2
CHE4 films based on chitosan and cumin nanoemulsion essential
6 Mold & yeast oil reduced the mesophilic and psychrophile bacteria in beef.
Abdeldaiem et al. [32] did not detect Enterobacteriaceae in
Log CFU/g burger

carp fillets coated with calcium caseinate film containing

4
3
2 rosemary essential oil.
1
0
Similar results have been reported by Fallah et al. [39],
0 1 10
Storage time (day)
20
Pabast et al. [14], and Zhang et al. [40].
C CHE1
E1 CHE2
E2 CHE3
CH1 CHE4 3.5. Sensory Characteristics. Figure 5 shows the sensory eval-
CH2
uation of chicken burgers on day 10. In terms of color, there
Figure 4: Microbial characteristics of chicken burgers during 20 is no significant difference between the groups (p < 0:05). In
days. terms of taste and texture, the CHE4 group got the lowest
score. From the point of view of smell, the E1 and E2 groups
sample was acceptable for less than 10 days. In the CHE1, received the highest points. In the control samples, the E1,
CHE2, CHE3, and CHE4 groups, the number of mesophilic and E2 groups had the highest overall acceptance, and the
bacteria did not exceed the standard limit during storage. lowest overall acceptance was related to the CHE4 group.
Journal of Food Processing and Preservation 7

Rosemary essential oil contains many volatile com- Journal of Agricultural and Food Chemistry, vol. 52, no. 11,
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[15] M. R. Manhani, M. A. Nicoletti, C. A. Da Silva Barretto et al.,
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