Chitosan coatings incorporated with propolis extract and Zataria multiflora Boiss oil for active packaging of chicken breast meat

International Journal of Biological Macromolecules 141 (2019) 401–409

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International Journal of Biological Macromolecules journal homepage: http://www.elsevier.com/locate/ijbiomac

Chitosan coatings incorporated with propolis extract and Zataria multiflora Boiss oil for active packaging of chicken breast meat Tooraj Mehdizadeh ⁎, Ali Mojaddar Langroodi Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, Urmia University, 1177 Urmia, Iran

a r t i c l e

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Article history: Received 5 August 2019 Received in revised form 28 August 2019 Accepted 31 August 2019 Available online 02 September 2019 Keywords: Chicken meat Chitosan Combination Propolis extract Zataria multiflora Boiss

a b s t r a c t The impact of dipping in combination of propolis extract (PE) and chitosan (CH) coating enriched with Zataria multiflora essential oil (ZEO) on chemical, microbial and organoleptic properties of poultry meat was determined at 4 °C. GC–MS analysis showed that the most components of PE were Dihydrochrysin (9.69%) and b- Pinostrobin (7.41%). The results of mesophilic total viable plate counts (TVC), lactic acid bacteria (LAB), Psychotropic bacteria and Pseudomonas spp. showed detectably lower (p b 0.05) microbial count in CH-PE 1%-Z 0.5% and CH-PE 1%-Z 1% samples at the last day of storage. The results of chemical characteristics (pH, total volatile base nitrogen (TVB-N), 2-thiobarbituric acid reactive substances (TBARS)) in all treated samples compared with the control, revealed that there is a synergistic effect between CH, PE and ZEO. In the sensorial assessment, treatments containing 1% PE- 0.5% ZEO and 1% PE- 1% ZEO were mostly acceptable by the sensory analyst. These results offer a successful approach that chitosan coating enriched with combination of ZEO and PE can be an improving method to reducing deterioration of fresh packed chicken meat. © 2019 Elsevier B.V. All rights reserved.

1. Introduction Chicken meat is an excellent origin of animal protein of low lipid content and the high biological value, which contains all the essential amino acids and unsaturated fatty acids required for human diet. Durability of chicken meat can be b3 days in optimum temperature. Thus, the meat industry is concentrated on techniques to develop the shelf life and the total acceptability of chicken meat [1]. Microbial population and lipid oxidation are two major factors of quality deterioration of durability of chicken meat and affect the health of the consumers. Accordingly, applying natural preservatives are an excellent approach to extend durability of sensitive food such as meat products [2]. Control of various pathogenic bacteria, such as mesophilic psychrotrophic, psychrophilic, and thermophilic, is complicated since these microorganisms are capable to survive in different storage situations [3]. Edible coatings are compound preserving food and enhance the meat products qualities. These biopolymers have acceptable influences and may be applied as a main ingredient for the new generation of packaging [4]. Chitosan is a nontoxic and non-polluting material with good barrier properties, as well as carrier of foods additives that applied in meat products because of their wide range antimicrobial and antioxidant activity [5]. Based on previous works, edible chitosan coating incorporating plant extracts and essential oils can reduce the number of

⁎ Corresponding author. E-mail address: [email protected] (T. Mehdizadeh).

https://doi.org/10.1016/j.ijbiomac.2019.08.267 0141-8130/© 2019 Elsevier B.V. All rights reserved.

bacteria during storage time [2]. Zataria multiflora Boiss is a genus of flowering herb in the Lamiaceae family that native to southwestern Asia, mainly in Iran. Two major ingredients of Z. multiflora are thymol and carvacrol that had been described to have antioxidant and antibacterial properties and categorized as Generally Recognized as Safe (GRAS) by the US Food and Drug Administration (FDA) [6]. Also, one of the major restrictions to apply of EOs in food industry is the durability of their odor, which could change the sensory characteristics. Z. multiflora, like thyme, is traditionally added as a flavoring agent (spice) and herbal additive to various foods such as meat and dairy products in Iran [7]. Therefore, the essential oil of this plant is one of the few herbal essential oils that can be used in the proper concentration without any adverse effect on the food product. According to studies, Z. multiflora essential oil has good antimicrobial effect even at low concentrations [8]. In addition, it seems that using natural herbs incorporated with other preservatives might increase efficiency and minimize the effect on organoleptic characteristics of meat [2]. Propolis is a substance that is gathered by bees from herbs and contains different chemical agents with biological function such as phenolic, polyphenols, aldehydes, ketones, alcohols, amino acids and quinones [1]. The antimicrobial activity (Silva et al. (2018), Payandan et al. (2016), Seibert et al. (2019), Al Naggar et al. (2016)) and antioxidant properties (Mouhoubi-Tafinine et al. (2016), Ozdal et al. (2019), Tiveron et al. (2016), Al Naggar et al. (2016), da Silva et al. (2018)) of propolis extract (PE) has been reported by many researchers [9–16]. Enhancing antimicrobial and antioxidant activities of CH coating by enriching with PE was revealed by Duman and Ozpolat (2015) [17].

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seem to be suitable to extend shelf life of chicken meat because of possible interaction between active components of PE and EO. Moreover, there is little, if any, published data in this area, Therefore, the purpose of this research were to survey the preservative impacts of chitosan coating incorporated with combination of Z. multiflora EO and alcoholic propolis extract on chicken meat during refrigeration in normal packaging.

Table 1 Results of major chemical compositions of Iranian propolis ethanolic extract. Compound name 1 2 3 4 5 6

Classification

%

Dihydrochrysin Pinostrobin Caryophyllene oxide chrysin caffeic acid Alfaxalone

Flavonoids Flavonoids Sesquiterpenes Flavonoids Aromatic acids Aliphatic hydrocarbons 7 1,3,8-trihydroxy-6-methylanthracene-9,10-dione Aromatic hydrocarbons 8 Caryophyllene oxide Sesquiterpenes 9 naringenin Flavonoids 10 Palmitic acid Fatty acids 11 1-Heptatriacotanol Alcohol 12 2-Amino-1-(3-hydroxy-4-methoxyphenyl) Aromatic ethanone hydrocarbons 13 5-Methylsalicylaldehyde Aldehydes 14 3,12-Oleandione Triterpenes

9.69 7.41 6.12 5.06 5.01 4.87

2. Material and methods

4.03

2.1. Preparation of PE and gas chromatography-mass spectrometry (GC– MS)

3.38 3.04 2.24 2.05 1.77

Natural propolis was gathered from four beehives. Ethanol extracted propolis was provided by extracting propolis (100 g) with ethanol (200 mL, 95%). The PE was filtered six times by Whatman No 2 filter paper. Then, the supernatant PE was evaporated in a rotary evaporator (Laborata 4003; Heidolph, Germany) and the PE was kept at 4 °C until test. The GC–MS analysis of PE was evaluated based on the procedure of Marriott, Shellie, & Cornwell (2001) [23].

1.45 1.12

Moreover, Synergistic antimicrobial and antioxidant effects by combining PE and chitosan against food spoilage microorganisms and lipid oxidation has been studied by Piedrahíta Márquez et al. (2019), Ebadi et al. (2019), Jonaidi Jafari et al. (2017) and Rollini et al. (2017) [18–21]. In another study, polylactic acid film containing ethanolic extract of propolis and Ziziphora clinopodioides EO covered with cellulose nanoparticles, increased the shelf life of minced beef [22]. A blend of chitosan coating in combination of Z. multiflora EO and alcoholic PE would

C

CH

CH-AL

CH-Z 0.5%

CH-Z 1%

2.2. Essential oil isolation Zataria multiflora Boiss was collected from Shiraz city, Iran. As described previously hydrodistilation of dried parts of herb was carried out in a Clevenger-type set for 3 h. Anhydrous sodium sulfate was used for drying ZEO and kept at 4 °C until test [23].

CH-PE 1%

CH-PE1%-z 0.5%

CH-PE1%-Z1%

9

a 7

Total vaible count

b

a

a

c

a

b

b

b

b

c

c

c c

6 5

aaa

a

8

c a a

a a

c

c

aa

d

d b

d

d b

e f

f

4

d

ee

e

3 2 1 0 0

4

8

12

16

Storage time (day) Fig. 1. Comparison of TVC values of various samples over the storage time. Without coating (C), chitosan (CH), chitosan with alcohol (CH-AL), chitosan with ZEO 0.5% (CH-Z 0.5%), chitosan with ZEO 1% (CH-Z 1%), chitosan with propolis extract 1% (CH-PE 1%), chitosan with propolis extract 1% and ZEO 0.5% (CH-PE 1%-Z 0.5%), chitosan with propolis extract 1% and ZEO 1% (CHPE 1%-Z 1%). *Different lower case letters in a column indicate significant differences between treatments; during storage time (days) in each treatment (p b 0.05).

T. Mehdizadeh, A. Mojaddar Langroodi / International Journal of Biological Macromolecules 141 (2019) 401–409

2.3. Chicken breast fillet and coating preparation Skinned chicken breast fillets with proximate composition (fat (1.5%), moisture (72.2%), protein (1.6%) and ash (1.7%)) were prepared from a poultry processing slaughter plant (Morghe Salem Co., Urmia, Iran) and directly were transferred within 1 h after in insulated polystyrene trays under refrigeration conditions (4 °C). Samples (140–170 g, 1.5 cm of thickness) were individually prepared by sterile cutting equipment. A crab shell chitosan (2%) (Sigma-Aldrich Co., Germany) was dissolved in acetic acid (1%) and glycerol (0.75 mL/g). Then, PE and ZEO were mixed at different concentrations. After that, surfactant agent (Tween 80, Pub Chem Co., USA) was mixed to the ZEO-incorporated treatments. The chicken meat treatments were randomly divided into eight groups parts and coated based on these formulations: control, CH, CH-AL, CH-Z 0.5%, CH-Z 1%, CH-PE 1%, and CH-PE 1%- Z 0.5% and CH-PE 1%- Z 1%. Finally, chicken meat samples were immersed in prepared solution for 1–2 min. The samples were allowed to drain for 2 min under a biological safety cabinet and wrapped in low density polyethylene LDPE bags [24]. Three packages for each treatment were selected to be sampled on day 0, 4, 8, 12 and 16. 2.4. Microbiological determinations The microbiological determination was performed on days 0, 4, 8, 12, 16 of keeping time. Ten g of chicken treatments were mixed with 90 mL of peptone water (0.1%) (Sigma-Aldrich Co., Germany) and shacked for 2–3 min. Decimal serial dilution were used for mesophilic total viable plate counts (TVC, PCA, Merck, Darmstadt, Germany), on the plate count agar and kept at 30 °C for 2 days. Pseudomonas spp., were numbered on Pseudomonas agar enriched with cetrimide fusidin cephaloridine agar (CFC). Psychrotrophic bacteria were numbered on Plate Count Agar. Plates were kept at 25 °C (2 days) and 7 °C (10 days) for Pseudomonas and Psychrotrophic growth, respectively [25]. LAB were numbered on de Man Rogosa Sharpe (Sigma-Aldrich Co., Germany) agar and kept at 30 °C for 2 days. 2.5. Thiobarbituric acid value Thiobarbituric acid-reactive substance (TBARS) value tests were applied colorimetrically as described by Wrolstad et al. (2005) to evaluate the lipid oxidation in mg malonaldehyde per kg of sample [26]. 2.6. Total volatile nitrogen (TVN) A macro Kjeldahl method with a vapor distillation apparatus according on Goulas and Kontominas (2005) was applied. TVN was reported as mg/100 g of chicken breast [27]. 2.7. pH value The pH was determined in triplicate from 5 g chicken sample that had been homogenized for 30s in 25 mL distilled water at 13500 rpm. Then the pH was read using a digital pH meter (Model Approx. Rs 7000, Labline Stock Centre, India) that calibrated daily to pHs 4 and 7 [28]. 2.8. Sensory evaluation For this purpose, the sensory analysis was conducted in two stages; in the first stage, the analysis (taste) was only conducted in the first day by cooking the samples at 155 °C for 15 min. While in the second stage, the analysis was evaluated for, odor, color, texture and overall acceptability every four days during the storage days until the 16th day. Twenty trained analyzers were participated from university of Urmia (Department of Food hygiene & quality control) on the basis of their

403

experience in the sensory analysis. The scale points were: 1 (dislike extremely) to 9 (like extremely) [29]. 2.9. Statistical analysis All of the data are shown as the mean ± standard error. The data evaluated applying IBM SPSS Software 21. The whole experiment for each treatment was repeated in independent triplicate using duplicate samples each time and the means were reported. 3. Results and discussion Fourteen agents were evaluated in PE by GC–MS analysis outcomes reported that flavonoids (25.2%) was the major agent (Table 1). Researchers have reported various compounds in propolis analysis. For example, a study in Egypt The main compounds were 1-(2,4-dihydroxy-6methoxyphenyl)-3-phenylprop-2-en-1-one and Hexadecanoic acid [30]. In another study in Poland, glycerol esters of phenolic acids, as well as unusually high amounts of p-coumaric and ferulic acid and their benzyl esters, were detected [31]. The amount and the difference of the compounds is related to extraction method, soil type, drying plant method, season of growth and plant age [5]. Koo et al. (2000) concluded that PE is rich in flavonoids especially kaempferol and quercetin which have antioxidant and antibacterial characteristics [32]. 3.1. Microbiological analysis The outcomes for TVC, LAB, Pseudomonas spp., and Psychrotrophic bacteria number are presented in Figs. 1–4. The antibacterial characteristic of PE is revealed in many works [33,34]. The primary bacterial number indicated an ability antibacterial activity for PE and ZEO ingredients. The primary TVC number for chicken meat were at standard ranges (4.04–4.86 log CFU/g). The lowest microbial level at the last day of storage was reported in CH-Z 1% (5.3), CH-PE 1%-Z 0.5% (4.41) and CH-PE 1%-Z 1% (4.32) samples. Considering the value of 7 log CFU/g, which is the accepted limit of TVC value for fresh poultry meat, the combination of ZEO and PE with CH films was more effective in reducing the microbial growth of chicken breast fillets during storage [35]. Jonaidi Jafari et al. (2017) showed that chitosan edible coating containing 1% propolis extract could decrease number of aerobic mesophilic bacteria (7 log in the 12 days) [20]. The present results are in agreement with those of Bazargani-Gilani et al. (2015) who reported 10 or 15 days of shelf life extension of chicken breast meat after using pomegranate fruit juice and Zataria multiflora EO in coating chitosan solution [36]. The antibacterial action of PE is related to prevent cell division, destroy cell, causing the changes to membrane phospholipid and fatty acid value, and prohibit RNA and DNA synthesis [37]. The antimicrobial action of PE related to the chemical composition, solvent and dose [38]. ZEO has a major role by altering the active transport, cytoplasmic membrane integrity, coagulation of cell contents and electron flow [39]. The TVC showed that all groups containing ZEO and PE maintained acceptable microbial level during the storage time. The galangin, chrysin, quercetin, kaempferol, decreased the microbial growth in treatments enriched with PE. The antimicrobial synergy mechanism of these three combinations depends on the between the flavonoids, the phenolic acids in PE, ZEO and positively charged amino groups of chitosan [38]. In the current work, the initial psychrotrophic bacteria numbers were ranged from 3.21 log CFU/g, in CH-PE1%-Z 1% treatments, to 4.26 log CFU/g in control sample. Duman and Özpolat (2014) revealed that in control and PE (0.1%) treatments psychrotrophic bacteria number passed 6 log CFU/g, on 15th and 18th day, respectively and in the present study, it was on 16th storage day for control sample [17]. At the last day of work, psychrotrophic bacteria level reached 6.01, 5.66, 5.9, 5.81, 5.6, 4.9, 5.6, 3.91 and 3.22 log CFU/g in control, CH, CH-AL, CH-Z 0.5%, CH-Z 1%, CH-PE 1%, CH-PE1%-Z 0.5% and CH-PE1%-Z 1% treated samples, respectively.

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C

CH

CH-AL

CH-Z 0.5%

CH-Z 1%

CH-PE 1%

CH-PE1%-Z 0.5%

CH-PE1%-Z1%

aa

a a a b

9 8

Psycotropic bacteria count

7 a

6 5 4

a a

a

a aa a b

b bb

bb

b b c

b b b

b c

cb

cc

d d

3

d

c e

d

e

e

2 1 0

0

4

8 Storage me (day)

12

16

Fig. 2. Comparison of psychrotrophic bacteria counts of various samples over the storage time. *Different lower case letters in a column indicate significant differences between treatments; during storage time (days) in each treatment (p b 0.05).

According on our outcomes, which indicated that mixing PE to chitosan coating decreased psychrotrophic bacterial population in our treatments. If the PE applied alone, after a while the amount of the PE is decreased which affected in low antibacterial impacts, but when the PE and CH applied together, it leads to stability of the PE properties for a significant period. This is due to the phenomenon that allowing the PE to hydrolyze the peptidoglycan layer surrounding the cytoplasmic membrane of bacteria, increasing the antibacterial effect of chitosan. [20]. In present study, on all days of storage, the groups treated with combination of ZEO and PE had significantly lower psychrotrophic bacterial counts (p N 0.05), which are in agreement with previous studies [22,40]. The variations of Pseudomonas spp. count in treated groups was similar to TVC and psychrotrophic values (Fig. 3). Pseudomonas spp. as microflora of chicken meat in refrigeration condition and with proteolysis properties are the most important group of microorganisms responsible for spoilage of fresh meat when their counts reach 7–8 log CFU/g [41]. The primary number of Pseudomonads was 4.51 and reached to 9.82 log CFU/g at the last day of keeping time. In addition, detectably lower Pseudomonads numbers (p b 0.05) were shown for CH-PE1%-Z 0.5% and CH-PE1%-Z1% treatments kept during the total storage at 4 °C. Pobiega et al. (2019) indicated that the strong antibacterial influence of chitosan incorporating PE and different EOs likely outcomes from the combination active ingredients of PE and ZEO [38]. The synergistic mechanism between EO and various extracts is not fully comprehended. It is reported that using of EO incorporated with PE have synergistic effect on bacteria inhibition by increasing the size and number of pores in cell structure [42]. Among all the groups in current research, CHPE1%-Z1% treatments was concluded to be the most useful in

prohibiting division of Pseudomonads in chicken meat treatments, resulting in a 2.81 log cycle reduce compared to control sample, likely carried out to the synergistic antimicrobial effect of CH, PE and ZEO. These results are in agreement with other studies that reported the reduction of Pseudomonas spp. in chicken meat treated with chitosan and EO [22,36,43]. LAB are facultative anaerobic bacteria that considered as a remarkable part of the chicken meat microflora. In current research, the primary LAB count of treatments ranged from 2.19 log CFU/g, in CH-PE1%-Z1% treatments, to 3.26 log CFU/g in controls. CH-PE1%-Z 0.5% and CH-PE1%-Z1% samples produced detectably lower (p b 0.05) LAB numbers (3.72 and 3.62 log, respectively) as compared to the control treatments. In addition, the growth design of LAB indicated that control was the highest at 16th day (7.51 log CFU/g), then CH sample (7.22 log CFU/g). Completely consistent with results of this study, Bazargani-Gilani et al. (2007) reported 1.5 log cycle decrease of LAB count after coating with chitosan containing pomegranate fruit juice and Zataria multiflora EO [36]. In another study, Jonaidi Jafari et al. (2018) revealed that the number of LAB was 7.7 log CFU/g at day 12 in control sample and 7.3 log CFU/g in CH sample, which is in good agreement with our findings [20]. Lopez-Caballero et al. (2005) showed that CH has no clear impact on decreasing the population of LAB [44]. Due to the outer membrane of gramnegative bacteria, various researcher reported the greater antimicrobial effect of propolis on gram-positive bacteria compared to gramnegative [9,45]. In addition, ferulic acid indicates antibacterial activity against some bacteria, and it possibly associates with to the bacteriostatic and bactericidal activity of PE. Ethanol did not indicate any preventing impact against the evaluated bacteria showing the antimicrobial impact was due to the PE [18].

T. Mehdizadeh, A. Mojaddar Langroodi / International Journal of Biological Macromolecules 141 (2019) 401–409

C

CH

CH-AL

CH-Z 0.5%

CH-Z 1%

10

CH-PE 1%

Pseudomonas count

a

7

b b c

6

4

a

b b

8

a

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b

a

b b bb

c de

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dd d

a aa

aa

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CH-PE1%-Z1%

aa a

aaa

9

5

CH-PE1%-z 0.5%

405

e

a cc

3 2 1 0

0

4

8 Storage me (day)

12

16

Fig. 3. Comparison of Pseudomonas spp. counts of various samples over the storage time. *Different lower case letters in a column indicate significant differences between treatments; during storage time (days) in each treatment (p b 0.05).

3.2. Assessment of pH value Alterations in pH of chicken treatments at refrigerated temperature are presented in Fig. 5. The primary pH of poultry meat (pH 5.7–6) was according on the outcomes of a past research [36]. The pH values of all groups exceeded during the keeping time, by action of microbial or endogenous enzymes like lipase and protease that cause an exceed in trimethylamine and ammonia in examination [36]. The pH values of the CH-Z 1%, CH-PE1%-Z 0.5% and CH-PE1%-Z 1% treatments were consistently lower than that of the others during whole storage period. The increase of pH has a negative impact on the sample condition mostly in organoleptic properties such as color, odor and texture. According to the result of pH value, it can be highlighted that combination treatments (CH-PE1%-Z 0.5% and CH-PE1%-Z 1%) showed higher antimicrobial activity compared to samples treated with chitosan, PE or ZEO alone. Therefore, the significantly (p b 0.05) high microbial growth rate of the control, CH and CH-AL fillets during storage could be associated with their higher pH. These results are in agreement with the findings of Berizi et al. (2018) and Vaithiyanathan, et al. (2011) that showed chitosan in combination with natural preservatives could notably decrease pH value in food model system and chicken meat respectively [46,47]. 3.3. TBARS evaluation The impacts of chitosan coating enriched with PE and ZEO on TBARS treatments are presented in Table 2. In current study, secondary products of lipid oxidation, as determined by TBARS values were elevated for all samples during the keeping time. The initial TBA level in the control treatment was 0.16 mg of MDA/kg of chicken meat, which exceeded

to 2.21 mg at the end of keeping time. After day four, the TBARS formation in the samples treated by ZEO and PE alone and in combination with ZEO, were significantly lower than CH, CH-AL as well as the control group (p b 0.05). Noori et al. (2018) applied nanoemulsion-based edible sodium caseinate coating containing ginger essential oil (GEO) (3 and 6% wt) onto chicken breast fillet. There were no significant differences between the treatments, and TBARS values of all samples up to day of 8 were recorded around 0.02 mg MDA.kg −1 [48]. In contrast, according on present research Jonaidi Jafari et al. (2018) reported that samples treated by CH and PE had less increase of TBARS compare to other samples until 12th day [20]. This change could be due to flavonoid and phenolic ingredients of PE and the impact of these agents on lipid oxidation. Kumazawa et al. (2004) revealed that the antioxidative activity of PE is related to α-tocopherol [49]. The chicken breast fillets coated with CH had lower TBARS value than control during storage except for day zero (p b 0.05). This may have occurred due to the chelating effect of CH with metal ions or the low oxygen availableness on the fillet surface [3]. In confirmation of this, some works showed that chitosan coating has significantly good impacts on decreasing TBARS value [50,51]. Furthermore, antioxidant activity of PE was indicated in the work of Siripatrawan, et al. (2016) which is in according on current work [45]. The antioxidant activity of ZEO in active film and coating has been reported in previous studies [2,36,52]. As expected, chitosan edible coating incorporating combination of ZEO and PE prolonged the shelf life of chicken breast fillet by its antioxidative activity. 3.4. Total volatile nitrogen (TVN) Alterations in TVN level of chicken meat samples are presented in Fig. 6. Iran Veterinary Organization reported that the passable level for

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T. Mehdizadeh, A. Mojaddar Langroodi / International Journal of Biological Macromolecules 141 (2019) 401–409

C

CH

CH-AL

CH-Z 0.5%

CH-Z 1%

CH-PE 1%

CH-PE1%-z 0.5%

CH-PE1%-Z1%

10 9

Lactic acid bacteria count

8

a

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Fig. 4. Comparison of lactic acid bacteria counts of various samples over the storage time. *Different lower case letters in a column indicate significant differences between treatments; during storage time (days) in each treatment (p b 0.05).

sample, time factor has negative effect on TVN and its value reached 25 mg/100 g in day 8 and 46.9 mg/100 g at the 16th day. In the CH treated sample, this level changed to 25.2 in day 12 which is in passable

TVN is 28 mg/100 g [36]. In the current work the initial TVN were between 8.3 and 9.8 mg/100 g for control and treated chicken meat, showing that passable situation for fresh chicken meat applied. In control

6.8

C

CH

CH-AL

CH-Z 0.5%

CH-Z 1%

CH-PE 1%

CH-PE1%-Z 0.5%

CH-PE 1%-Z 1% a b

6.6 6.4 6.2

a

a

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b b b

a

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a a a

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b b c

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5.8

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6 pH

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5.6 5.4 5.2 5 0

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8 Storage me (days)

12

16

Fig. 5. Changes in pH values of chicken meat samples during refrigerated storage. *Different lower case letters in a column indicate significant differences between treatments; during storage time (days) in each treatment (p b 0.05).

T. Mehdizadeh, A. Mojaddar Langroodi / International Journal of Biological Macromolecules 141 (2019) 401–409

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Table 2 Changes in TBARS value (mg MDA/kg) of chicken meat during refrigerated storage. Treatment

Storage time (day)

C CH CH-AL CH-Z 0.5% CH-Z 1% CH-PE 1% CH-PE1%-Z 0.5% CH-PE1%-Z 1%

0

4

8

12

16

0.16 ± 0.04Aa 0.16 ± 0.06 Aa 0.16 ± 0.06 Aa 0.16 ± 0.05 Aa 0.16 ± 0.07 Aa 0.16 ± 0.03 Aa 0.16 ± 0.08 Aa 0.16 ± 0.06 Aa

0.64 ± 0.05 Ba 0.34 ± 0.02 Bb 0.31 ± 0.02 Bc 0.26 ± 0.05 bc 0.27 ± 0.06 bc 0.25 ± 0.03 Bc 0.24 ± 0.02 Bc 0.25 ± 0.03 Bc

0.97 ± 0.06 Ca 0.51 ± 0.04 Cb 0.49 ± 0.03 Cd 0.38 ± 0.04 Ec 0.35 ± 0.02 Ce 0.33 ± 0.01Ce 0.29 ± 0.02Cf 0.27 ± 0.03Cf

1.81 ± 0.07 Da 0.99 ± 0.08 Db 0.59 ± 0.05 Dc 0.48 ± 0.03 Dd 0.44 ± 0.04 Dd 0.42 ± 0.03Dd 0.32 ± 0.05De 0.31 ± 0.02De

2.21 ± 0.09 Ea 1.076 ± 0.07 Eb 1.22 ± 0.06 Ec 0.78 ± 0.09 Ed 0.76 ± 0.02 Dd 0.72 ± 0.02 Ed 0.58 ± 0.04 Ee 0.59 ± 0.04 Ee

Treatments: Without coating (C), chitosan (CH), chitosan with alcohol (CH-AL), chitosan with ZEO 0.5% (CH-Z 0.5%), chitosan with ZEO 1% (CH-Z 1%), chitosan with propolis extract 1% (CH-PE 1%), chitosan with propolis extract 1% and ZEO 0.5 (CH-PE 1%-Z 0.5%), chitosan with propolis extract 1% and ZEO 1% (CH-PE 1%-Z 1%). Different uppercase letters in the same row and lowercase letters in the same column indicate significant differences (p b 0.05).

level, but in day 16 the value passed this value. In the CH incorporated with ZEO treatment, TVN increased to 27.2 mg/100 g, which is more than the standard level. Increasing the concentration of ZEO enriched with PE decreased the level of TVN value during keeping time by reducing the initial numbers of the spoilage bacteria. In all treatments incorporated with PE, TVN value remained lower throughout the work. There was a significant positive correlation between the TVN and pH, as increase in volatile amine lead to increase of pH, which is revealed in this study. Mojaddar Langroodi et al. (2018) demonstrated that CH alone and incorporated with other compounds could detectably reduce TVN formation [2]. This can be by preventing in microbial population and lipid oxidation to separate TVN from amine agents [20]. PE had a detectable effect on TVN in the present research, which was in agreement with results reported by Fuat Gulhan et al. (2012) and Jonaidi Jafari et al. (2017) [20,53].

3.5. Sensory evaluation All samples were analyzed based on 9-point hedonic scale, and the score of 7 or more considered acceptable. Alterations in organoleptic properties of treatments during keeping time are shown in Table 3. According to results of fillet cooking in day zero, addition of PE and ZEO, especially at concentrations higher than 1%, partially affects the taste and reduces its score in terms of analyzers. There was no significant difference between CH-PE 1% and CH-PE 1%-Z 0.5% (p N 0.05). As the results of color parameter during storage, Addition of propolis had a negative effect on the color of the samples, but with increasing storage

time over the days, there was a significant difference (p b 0.05) between them with the decrease in the score of the uncoated and CH treatments. In odor parameter, the initial scores of the treatments were altered by PE and ZEO but in the last day of test, the changes of all organoleptic factors in samples treated with ZEO and PE was detectable in compare to the control group (p b 0.05) (Table 3). On the first day in this investigation, no significant difference exists between treatments group except CH-Z 1% with regard to the texture scores given by the panel members (p N 0.05). The scores of all the treatments were decreased with storage time, which probably originated from protein break down. However, the rate of this decrease in PE and ZEO coated treatments was lower than other samples. The outcomes of overall acceptability demonstrated that the CH-PE1%, CH PE1%Z0.5% and CH-PE1%-Z1% treatments had satisfactory score (7˂) factors until the last day of storage. The higher score belonged to CH-PE1%Z1% sample. This may have happened due to the controlling of microbial spoilage. Kanatt et al. (2008) demonstrated that CH had no unpleasant impact on meat [54]. Also, Jo, Lee, Lee, and Byun (2001) indicated that chitosan has a significant good influence on color factor in sausage [55]. This is consistent with previous findings on the use of natural compounds in chitosan coating in such products as chicken breast [24], and chicken kebab [43].

4. Conclusion The current research indicates that chitosan enriched with PE and ZEO had a high antibacterial and antioxidant impact against some

45

C

40

CH

TVN(mg/100g)

35 30

CH+AL

25

CH+Z 0.5%

20 CH+Z 1%

15 10

CH+PE1%

5

CH+PE1%+Z 0.5%

0 0

4

8

12

16

CH+PE1%+Z 1%

Storage me (days) Fig. 6. Comparison of mean total volatile base nitrogen (TVB-N) content in various samples during refrigeration.

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T. Mehdizadeh, A. Mojaddar Langroodi / International Journal of Biological Macromolecules 141 (2019) 401–409

Table 3 Changes in sensory attributes of chicken meat during refrigerated storage. Treatment

Storage time (day) 0

4

8

12

16

Taste C CH CH-AL CH-Z0.5% CH-Z1% CH-PE 1% CH-PE1%-Z0.5% CH-PE1%-Z1%

8.4 ± 0.41ab 8.5 ± 0.69a 8.7 ± 0.41a 9 ± 0.72b 7.7 ± 0.51c 8.2 ± 0.32abc 8.1 ± 0.53abc 7.8 ± 0.39c

– – – – – –

– – – – – –

– – – – – –

– – – – – –

Color C CH CH-AL CH-Z0.5% CH-Z1% CH-PE1% CH-PE1%-Z0.5% CH-PE1%-Z1%

8.6 ± 0.67a 7.2 ± 0.67ab 6.8 ± 0.73bc 6.6 ± 0.63bc 6.3 ± 0.94cd 4.9 ± 0.66d 4.5 ± 0.59d 4.5 ± 0.78d

6.3 ± 1.03ab 6.4 ± 1.21a 5.9 ± 1.12ab 5.9 ± 1.13ab 5.3 ± 0.76ab 5.1 ± 0.24b 4.9 ± 0.42b 4.8 ± 0.67b

5.6 ± 0.32ab 5.9 ± 1.12a 5.4 ± 0.17abc 5.5 ± 0.36abc 5.1 ± 0.54bc 4.6 ± 0.84c 4.5 ± 0.32c 4.2 ± 0.56c

4.2 ± 0.32b 5.3 ± 0.13a 5.6 ± 0.34a 5.6 ± 1.05a 4.8 ± 0.49ab 4.6 ± 0.74ab 4.3 ± 0.69ab 4.1 ± 0.41ab

1.4 ± 0.67c 2.1 ± 1.33c 3.7 ± 0.26b 5.1 ± 0.34a 4.7 ± 0.18ab 4.5 ± 1.17ab 4.2 ± 0.62ab 4.1 ± 0.85ab

Odor C CH CH-AL CH-Z0.5% CH-Z1% CH-PE 1% CH-PE1%-Z0.5% CH-PE1%-Z 1%

8.8 ± 0.58a 8.8 ± 0.37a 8.7 ± 0.61a 8.6 ± 0.38a 7.8 ± 0.44b 8.1 ± 0.37b 8.3 ± 0.64b 8.1 ± 0.49b

7.4 ± 0.36c 8.1 ± 0.47ab 8.1 ± 0.81ab 8.3 ± 0.48a 7.6 ± 0.55bc 7.8 ± 0.43abc 7.7 ± 0.37bc 7.6 ± 0.36bc

6.1 ± 0.21c 8.1 ± 0.58ab 7.9 ± 0.42ab 8.3 ± 0.84a 7.6 ± 0.59b 7.7 ± 0.22ab 7.7 ± 0.46ab 7.6 ± 0.57ab

4.4 ± 0.46d 6.3 ± 0.74c 6.6 ± 0.55bc 7 ± 0ab 7.2 ± 0.23ab 7.4 ± 0.59a 7.6 ± 0.43a 7.6 ± 0.59a

1.6 ± 0.73d 5.2 ± 0.65c 6.1 ± 0.93b 6.8 ± 0.25a 6.1 ± 0.52b 6.7 ± 0.54ab 6.9 ± 0.37ab 7.0 ± 0.0a

Texture C CH CH-AL CH-Z 0.5% CH-Z1% CH-PE1% CH-PE1%-Z0.5% CH-PE1%-Z1%

9.0 ± 0.0a 8.8 ± 0.33a 8.5 ± 0.59a 8.5 ± 0.72a 8.1 ± 0.36b 8.9 ± 0.81a 8.9 ± 0.67a 9.0 ± 0.0a

8.4 ± 0.72a 8.6 ± 0.49a 8.4 ± 0.13a 8.4 ± 0.37a 8 ± 0.56a 8.7 ± 0.55a 8.7 ± 0.34a 8.8 ± 0.26a

6.6 ± 0.31c 8.2 ± 0.58ab 8.2 ± 0.49ab 8.3 ± 0.48ab 7.6 ± 0.36b 8.6 ± 0.36a 8.6 ± 0.82a 8.7 ± 0.47a

4.4 ± 0.94d 5.7 ± 0.54c 7.9 ± 0.52ab 8.2 ± 0.47a 7.2 ± 0.75b 8.2 ± 1.11a 8.4 ± 0.36a 8.5 ± 0.35a

1.6 ± 0.72d 1.3 ± 0.22d 4.9 ± 0.68c 5.8 ± 0.23bc 7.7 ± 0.47a 6.9 ± 0.49b 7.8 ± 0.12a 8.2 ± 0.26a

Overall acceptability C CH CH-AL CH-Z0.5% CH-Z1% CH-PE1% CH PE1%-Z0.5% CH-PE1%-Z1%

7.2 ± 0.46d 8.1 ± 0.38bc 8.7 ± 0.76ab 8.8 ± 0.92a 8.2 ± 0.36abc 8.1 ± 0.48c 8.1 ± 0.21bc 8.2 ± 0.44abc

5.2 ± 0.87c 8.1 ± 0.81b 8.7 ± 0.69a 8.7 ± 0.51a 8.1 ± 0.81b 8.1 ± 0.87b 8.1 ± 0.32b 8.2 ± 0.31c

3.8 ± 0.67c 5.3 ± 0.63b 6.8 ± 0.82a 7.1 ± 0.99a 7.2 ± 1.15a 7.3 ± 0.94a 7.5 ± 0.56a 7.6 ± 0.48a

1.6 ± 0.36d 4.9 ± 0.68c 6.2 ± 0.21b 6.6 ± 0.18ab 7.1 ± 0.34a 7.2 ± 0.69a 7.3 ± 0.38a 7.4 ± 0.59a

1.4 ± 0.48e 4.7 ± 0.84d 6.2 ± 0.73c 6.3 ± 0.78bc 6.9 ± 0.63ab 7.1 ± 0.81a 7.2 ± 0.31a 7.3 ± 0.69a

Treatments: Without coating (C), chitosan (CH), chitosan with alcohol (CH-AL), chitosan with ZEO 0.5% (CH-Z 0.5%), chitosan with ZEO 1% (CH-Z 1%), chitosan with propolis extract 1% (CH-PE 1%), chitosan with propolis extract 1% and ZEO 0.5 (CH-PE 1%-Z 0.5%), chitosan with propolis extract 1% and ZEO 1% (CH-PE 1%-Z 1%). Different uppercase letters in the same row and lowercase letters in the same column indicate significant differences (p b 0.05).

bacteria and can enhance the chemical characteristic and show acceptable organoleptic characteristics such as color, odor, texture, taste and total acceptability in chicken breast meat. Despite many complications about organoleptic factor of samples incorporated with combination of CH and PE, CH and propolis can be applied to retard the oxidation reactions and spoilage. Accordingly, CH-PE1%-Z 1% indicated the best prohibition impact on the microbial and oxidative activity in chicken meat. This combination has been shown to extend the shelf life of chicken breast meat approximately 16 days and may be have the potential to be used as active packaging material. Acknowledgements This study was funded by the Faculty of Veterinary Medicine, Urmia University, Urmia, Iran.

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