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Effect of functional chitosan coating and gamma irradiation on the shelf-life of chicken meat during refrigerated storage
Author’s Accepted Manuscript Effect of functional chitosan coating and gamma irradiation on the shelf-life of chicken meat during refrigerated storage Parviz Hassanzadeh, Hossein Tajik, Seyed Mehdi Razavi Rohani, Mehran Moradi, Mohammad Hashemi, Javad Aliakbarlu www.elsevier.com/locate/radphyschem
PII: DOI: Reference:
S0969-806X(17)30421-8 http://dx.doi.org/10.1016/j.radphyschem.2017.06.014 RPC7572
To appear in: Radiation Physics and Chemistry Received date: 13 April 2017 Revised date: 10 June 2017 Accepted date: 18 June 2017 Cite this article as: Parviz Hassanzadeh, Hossein Tajik, Seyed Mehdi Razavi Rohani, Mehran Moradi, Mohammad Hashemi and Javad Aliakbarlu, Effect of functional chitosan coating and gamma irradiation on the shelf-life of chicken meat during refrigerated storage, Radiation Physics and Chemistry, http://dx.doi.org/10.1016/j.radphyschem.2017.06.014 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Effect of functional chitosan coating and gamma irradiation on the shelf-life of chicken meat during refrigerated storage
Parviz Hassanzadeha, Hossein Tajikb, Seyed Mehdi Razavi Rohanib, Mehran Moradib*, Mohammad Hashemic, Javad Aliakbarlub a
Department of Food Hygiene and Aquatic Disease, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, East Azarbaijan, Iran
b
Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, Urmia University, Urmia, West Azarbaijan, Iran
c
Department of Nutrition, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
[email protected] [email protected].
*
Correspondent: Tel.: +984431942633; fax +984432771926;
Abstract The present study was conducted to evaluate the combined effect of low-dose gamma irradiation (2.5 kGy) and chitosan edible coating (2%) containing grape seed extract (GSE) (0.1%) on the microbial, chemical and sensorial quality of chicken breast meat during 21 days of storage at 4 C. The samples were periodically analyzed for microbiological (aerobic mesophilic and psychrotrophic counts), chemical (TBA, pH, aw) and sensorial (odor, appearance, and overall acceptability) characteristics. Results indicated that irradiation and the active coating had significant (P < 0.05) effects on reduction of bacterial growth with at least a 14-day extension of shelf life. Results represented the protective effect of chitosan coating containing GSE against 1
induced lipid oxidation by irradiation. All chitosan-coated samples showed lower TBA and pH values than other treatments during storage, and no significant (P > 0.05) difference was observed due to irradiation in TBA values. Results also indicated that the application of chitosan coating significantly improved the sensorial quality of the samples, and none of the evaluated sensorial attributes was significantly affected by irradiation. Based on the results obtained in this study, the application of low-dose gamma irradiation and chitosan coating containing GSE was effective in preserving the quality of fresh chicken meats and is recommended in meat products. Keywords: Gamma irradiation; active packaging; grape seed extract; chicken meat; shelf life.
1. Introduction Chicken meat is a food commodity with a rich source of essential amino acids, minerals, vitamins and low lipid content. Moreover, it contains relatively high levels of polyunsaturated fatty acids. All of these specifications illustrate chicken meat as an excellent substrate for microbial spoilage and oxidative reactions (Raeisi et al., 2016). Nowadays researchers and poultry processing industries are focusing on developing new techniques to reduce microbial growth and oxidative reactions of meat in order to extend its shelf life and preserve its original quality (Bazargani-Gilani et al., 2015). The integration became popular in poultry meat due to the worldwide popularity of these products. Recently, research has been intensified on the application of natural preservatives in food due to safety issues and consumer demands (Alizadeh Sani et al., 2017), because they extend the shelf life of food without side effects resulting in increased tendency for their application by both producers and researchers (Farhangfar et al., 2011). Edible coatings and films prepared from natural sources encounter with a special attention since they have been proven as a carrier of food additives such as flavors, antimicrobials, antioxidants, and enzymes. This type of packaging could regulate the release of functional compounds into food and maintains high levels of additives on the surface of foods. This phenomenon has of great importance to increase the shelf life of foods of animal origin (Moradi et al., 2016). Chitosan, in form of coating or film, is widely used in food due to its bioactive characteristics such as antifungal, antibacterial and antioxidative activities (Bazargani-Gilani et al., 2015). It is a natural biopolymer, which is 2
industrially produced by four steps including demineralization, deproteinization, decoloration and deacetylation of chitins which mainly obtained from crab and shrimp shells (BazarganiGilani et al., 2015). Chitosan as a coating solution or film has been used in food by many researchers for active packaging carrying natural antioxidants and/or antimicrobials (Jasour et al., 2015; Moradi et al., 2011;Özdemir and Gökmen, 2017; Yu et al., 2017). By-products from herbals materials were gained strong attention as a dietary supplement and food additive. Grape seed extract (GSE) is a novel ingredient extracted from the grape seeds (Vitis vinifera). Their functional properties, antioxidant and antimicrobial, are due to
the higher amounts of
polyphenolic compounds (Perumalla and Hettiarachchy, 2011; Shah et al., 2014). Biological activity of GSE has been shown in various meats (Farhangfar et al., 2011). Gama irradiation in medium doses can be used to improve the microbial quality of chicken meat, ensures its safety and extend its shelf life with no adverse changes or deterioration. The food industry has given permission to use gamma irradiation (≤10 kGy) in food packaging and food processing sites (Chen et al., 2016). In previous studies, gamma irradiation has been used in order to extend shelf life of different kinds of meat, including minced camel meat (Al-Bachir and Zeinou, 2009), intermediate‐moisture meat (Rao et al., 2005), barbecued chicken (Fallah et al., 2010), game hen carcasses (Yoon, 2003), minced chicken meat (Abdeldaiem, 2014) and chicken meat (Javanmard et al., 2006). A literature review represented some studies on the effect of combinational use of gamma irradiation and active coatings on the shelf life extension of meat (Abdeldaiem, 2014; Kang et al., 2007; Lacroix et al., 2004; Rao et al., 2005), but to our knowledge, no study has been conducted on the combined effect of gamma irradiation and active coatings in chicken meat. The use of combined technologies is increasing, therefore the present study was conducted to determine the potential of gamma irradiation and chitosan active coatings containing GSE individually and in combination as a hurdle system, to improve the microbial, chemical and sensorial quality of fresh chicken meat during refrigerated at 4 C. 2. Materials and Methods 2.1.Meat preparation The chicken breast was obtained directly from AzarShahr slaughterhouse (Azarshar, Iran) on the day of the experiment and immediately transported to the laboratory at refrigerated temperature.
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Under an aseptic condition, the meat was cut and pre-weighed to 200-gram samples and kept in sterile polyethylene bags (Zipack™, Tehran, Iran) at 4 C until coating. 2.2.Preparation of GSE and chitosan coating solution Commercial GSE powder [extraction solvent: water, phenolics contents (gallic acid equivalents, dry basis) ≥ 90 g GAE/100 g], was provided kindly by Mega Natural Inc. (Madera, CA, USA). Medium molecular weight chitosan flakes (75-85% degree of deacetylation) was purchased from Sigma-Aldrich Company (St. Louis, MO, USA). Chitosan solution (20 g/L) was prepared by dissolving two grams of chitosan in 100 mL of 10 g L-1 acetic acid (Merck, Darmstadt, Germany) with constant agitation overnight at room temperature (Yingyuad, et al., 2006). Glycerol (Merck, Darmstadt, Germany) was added to the chitosan solution at 0.5 mL g-1. 2.3.Treatment of meat samples Meat samples were divided to six groups: (i) uncoated (control, C); (ii) uncoated+ irradiated (I); (iii) immersed in chitosan solution (CH); (iv) irradiated + immersed in chitosan solution (ICH); (v) immersed in chitosan solution containing 0.1% GSE (GCH) and (vi) irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH). Samples were immersed in 200 volumes of chitosan or chitosan+ GSE solution for 1 min and then drained and packed in sterile polyethylene bags. 2.4.Radiation treatment After coating, chitosan coated samples from groups I, ICH and IGCH, were immediately transferred under the refrigerated condition to Atomic Energy Organization of Iran located in Tehran, Iran and exposed to gamma radiation using a
60
Co radiation source (Gamma Cell 220
Nordion International Inc., Ontario, Canada) at a dose of 2.5 kGy. The absorbed doses were measured by alanine dosimeter. Samples were covered with crushed ice to keep them at 33 C during the irradiation process. After irradiation, samples were transported back to Urmia University and stored at 4 C for 21 days. Sampling for shelf-life evaluation was done at days 0, 3, 6, 9, 14 and 21 for all irradiated and non-irradiated meat samples. 2.5.Microbiological evaluation
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At each time, meat samples (25 g) were homogenized in 225 mL of sterile 0.1% peptone water (Merck, Darmstadt, Germany) for 1 min using stomacher (model 400, Seward Medical Ltd, London, U.K.). Decimal dilutions (1:10) in 0.1% peptone water solution were prepared and appropriate diluents were poured on plates of the following agars: Plate Count Agar (PCA, Merck, Darmstadt, Germany) for total mesophilic viable count (TMVC) incubated at 35 C for 24 h and PCA for total psychrotrophic viable count (TPVC) incubated at 7 C for 5-7 days. Results were expressed as log10 CFU g-1. 2.6.Chemical quality evaluation 2.6.1. Crude protein and fat measurement The samples were separately homogenized (IKA, T25 basic, Germany) and analyzed for crude protein and crude fat, according to AOAC methods (AOAC, 1990). 2.6.2. pH measurement Ten grams of sample was homogenized with 90 mL of distilled water for 30 s and pH value of the homogenate was measured using a pH-meter (pH-Meter E520, Metrohm Herisau, Switzerland). 2.6.3. Water activity measurement The water activities of all samples were measured at room temperature with a water activity meter (Novasina, ms1, Pfäffi- kon, Switzerland). 2.6.4. Lipid oxidation evaluation Lipid oxidation of each control and treated samples were performed by an extraction thiobarbituric acid (TBA) method as described by Pikul, et al. (1989) with minor modification. Each 10 g set of meat samples were individually homogenized in 35 mL of cold (4 C) extraction solution containing 4% perchloric acid (Merck, Darmstadt, Germany)
and 1 mL of BHA
(Merck, Darmstadt, Germany) (1 mg mL-1) at 13,500 rpm for 1 min. The preparation was mixed and filtered, then the filtrate was adjusted to 50 mL with 4% perchloric acid and 5 mL aliquot of the filtrate was added to 5 mL of TBA (Merck, Darmstadt, Germany) (0.02 M). The mixture was vortexed and then incubated in a 100 °C water bath for 60 min for color development. The absorbance at 532 nm was measured with a spectrophotometer (Novaspec II spectrophotometer 5
(Amersham Pharmacia Biotech Inc., Buckinghamshire, UK). The TBA values were expressed in units of mg malonaldehyde kg-1 (mg MDA kg -1) sample. 2.7.Sensorial evaluation Meat samples were evaluated by 6-member trained sensory panel participants from our department during days 0, 3, 6, 9, 14 and 21. The panelists were trained before their participation. Panelists evaluated odor, appearance and overall acceptability using a nine-point hedonic scale (9 = like extremely; 8 = like very much; 7 = like moderately; 6 = like slightly; 5 = neither like nor dislike; 4 = dislike slightly; 3 = dislike moderately; 2 = dislike very much; 1 = dislike extremely) (Ehsani et al., 2016). 2.8.Statistical analysis All experiments had three replications for each treatment and measurement. Data were expressed as mean ± SD. Significant differences were evaluated at P < 0.05 by analysis of variance (ANOVA) and Duncan's multiple range test using SPSS 13.0 (SPSS Inc., Chicago, IL, USA).
3. Results and discussion 3.1.Microbiological changes Both chitosan and GSE represent an antimicrobial and an antioxidants activity. GSE is one of the most powerful natural antioxidants, while in the case of antimicrobial activity, GSE is weaker than chitosan. The binary use of these two compounds enhance the effects of each of the two compounds (Moradi et al., 2011). Changes on TMVC and TPVC are shown in Tables 1 and 2. TMVC and TPVC values of all treatments significantly (P < 0.05) increased during the storage at 4 C and the highest increase rate was observed in control samples. TMVC and TPVC values of all treated samples were significantly lower than control revealing the inhibitory effect of treatments on the increase rate of TMVC and TPVC, and the highest and the lowest effects were observed in IGCH and CH samples, respectively. Irradiation reduced significantly the TMVC and TPVC level and showed a significant lower microorganisms level during storage as compared to the control (P<0.05). As it can be seen, non-irradiated samples including C, CH, and GCH, reached to the value of 7 log CFU g-1 (the limit of acceptability) on day 9, 14 and 21 of storage, respectively, however, I, ICH and IGCH samples never reached the limit of 6
acceptability value of TMVC till the end of storage time. Similar to thermal and chemical treatments, the type and the number of microorganisms found in the flora of food affect the efficiency of irradiation process, and then radiation efficacy is reduced by increasing the food microbial counts. Former studies reported similar results for the effect of irradiation (Al-Bachir and Zeinou, 2009; Fallah et al., 2010; Özden et al., 2007; Rahimi et al., 2013) and chitosan coatings (Duan et al., 2010; Gómez-Estaca et al., 2007; Kanatt et al., 2004) on the reduction of TMVC and TPVC values. Most phenolics of GSE have a more powerful effect on bacteria. It was previously proposed that GSE was more effective on gram-positive than gram-negative bacteria and some groups of spoilage bacteria, including gram-positive lactic acid bacteria, showed a high resistance into GSE (Moradi et al., 2011). The exact antimicrobial activity mechanism remains unclear, whereas it was demonstrated that epigallocatechin-3-gallate inhibit dihydrofolate reductase, the enzyme involved in folate metabolism and biosynthesis of some major biomolecules (Kao et al., 2010).
3.2.Chemical changes Protein and fat contents of the control samples were analyzed on the first day of study and results were 20.56 and 1.36 %, respectively. The lowest and the highest aw values of the treatments during storage were 0.96 and 0.98, respectively, without any significant (P > 0.05) changes among treatments during storage (Table 3). The pH changes of chicken meat samples during storage are shown in Table 4. The average pH value of the samples was 5.6 on the first day of storage which increased in all treatments during storage. The pH values of all treated samples were significantly lower than control (P<0.05). All coated samples (CH, ICH. IGCH) had significantly lower pH values than non-coated samples (C and I), indicating the causative effect of chitosan coating on the constancy of pH value during storage. It can be due to acidic properties of chitosan solution and prevention of microbial growth on the surface of the samples. Former studies reported that chitosan coating application in chicken meat samples could stabilize the pH value of them during storage and chitosan coated samples had lower pH values than others as well (Duan et al., 2010; Fan et al., 2009; Yingyuad et al., 2006). Table 5, represents the correlation between TMVC values and pH values of the treatments during storage. As showed, there was a significant (P < 0.05) association between TMVC values and pH values of the 7
samples. Chitosan-coated samples had lower correlation coefficient than non-coated samples and the lowest coefficient was observed in CH samples indicating control of microbial growth and pH elevation by chitosan coating application. The effects of radiation on chemical characteristics of the meat are influenced by radiation dose, type, and composition of meat, keeping temperature, gaseous composition of packaging and microbial load of meat (Lee et al., 2006). According to Al-Bachir and Zeinou (2009), lipid oxidation of meat is initiated soon after slaughtering and develop to unacceptable levels during storage. Results of TBARS values of chicken meat treated with gamma irradiation and chitosan coatings during 21 days of storage period are shown in Table 6. Results showed that over the storage period at 4 C, malondialdehyde (MDA) values increased in all treated samples. The highest and the lowest TBARS values were observed in I (1.95 mg MDA kg -1) and GCH (0.085 mg MDA kg -1) samples, respectively. Irradiation increased TBARS values of the samples during storage, due to the generation of free radicals by ionizing radiation which induces lipid peroxidation, however, the difference was not significant (P > 0.05) when compared to control. Other researchers reported the same results for the effects of irradiation on lipid oxidation as well (Javanmard et al., 2006; Kwon et al., 2008). Regarding TBARS values of irradiated samples (I, ICH and IGCH), IGCH samples showed lower values compared to I samples during 21 days of storage (P<0.05), represents the protective effect of chitosan coating containing GSE against induced lipid oxidation by irradiation. These results may be rationalized considering the possible synergistic activity among polyphenols of GSE and chitosan that is applied on meat. GSE is reported as potent antioxidant compounds owning scavenging activities against free radical and Schiff-base metal complexes as well as synergistic activity with another antioxidant (Perumalla and Hettiarachchy, 2011). The antioxidant activity of GSE is contributed to polyphenolic compounds including gallic acid, monomeric flavan-3-ols catechin, epicatechin, gallocatechin, epigallocatechin and epicatechin 3-O-gallate, as well as more highly polymerized procyanidin (Gibis et al., 2013). During the storage, an increment in lipid oxidation of samples containing GSE is possibly related to the development of phenolic aldehydes due to degradation of some phenolic compounds of phenolic-rich agents (Moradi et al., 2011). Results also indicated that chitosan coating could inhibit the increase rate of MDA values of treated samples during storage compared to control. A significant difference (P<0.05) was observed between CH and C samples during the first 3 days of storage and between GCH and C 8
samples up to the end of storage time. Yingyuad et al. (2006) reported that chitosan coating could effectively preserve refrigerated grilled pork against lipid oxidation which was completely consistent with results of the present study. It was also reported that the antioxidant activity of chitosan increased upon irradiation (25 kGy) without significant effects on its antimicrobial property (Kanatt et al., 2004). The authors showed that irradiated chitosan had antioxidant activity 27-fold greater than the non-irradiated chitosan. When chitosan was irradiated at a dose higher than 40 kGy, no further increase in its antioxidant activity was recorded. The increase in reducing power upon irradiation indicated enhanced antioxidant activity that can be exploited for radiation-processed food in reducing radiation-induced lipid peroxidation. 3.3.Sensorial changes Changes in sensorial attributes are one of the main reason of shelf life reduction of meat products, that can be due to microbial growth and lipid oxidation resulting in the production of adverse metabolites and reduction of sensorial properties (Brannan and Mah, 2007; Kwon et al., 2008). The sensory evaluation results of chicken meat samples during days 0, 3, 6, 9, 14 and 21 are given in Figure 1. The sensory scores (odor and color and overall acceptability) of control and treated samples declined during storage, while they were acceptable, although, sensory evaluation of control samples was not performed on 9th and 14th days of storage period due to the presence of spoilage signs. Results indicated that irradiation decreased sensory scores (especially odor attribute) when compared to other samples, however, it was not statistically significant (P > 0.05). Other work performed by Abu-Tarboush et al. (1997) demonstrated that irradiation at a dose between 2.5 and 10 kGy had a slight effect on the sensory quality (appearance, odor, taste, and texture) on both raw and cooked chicken meat. Several sulfurs containing compounds especially dimethyl trisulfide are produced in irradiated chicken meat samples (Kim et al., 2002), which might affect sensorial attributes of irradiated samples in the present study. According to sensory results, irradiation could preserve the quality of fresh chicken meats for 5 days and extend their shelf life until the end of the storage period (day 21). Similar results were obtained by other researchers who reported approximately two weeks shelf life extension in irradiated chicken meat samples (Javanmard et al., 2006). Results also indicated a higher sensorial scores in chitosan coated samples, indicating the effects of chitosan coating on preserving sensory characteristics of chicken meat which were in line with results of former studies (Kanatt et al., 9
2008; Rao et al., 2005; Yingyuad et al., 2006). The type of food and chitosan determines the effect of chitosan coating on sensorial attributes of food. A more recent work showed that chitosan coating did not affect the sensorial quality of ready-to-cook meat in terms of changes in appearance and any off-flavor (Kanatt et al., 203). As seen in figure 1, the addition of GSE to coating did not significantly impact consumer preference (P > 0.05). The highest sensorial scores were observed in IGCH samples during storage that may be due to functional properties of chitosan and GSE. It can highlight the effects of irradiation and chitosan coating incorporated with GSE on preserving sensorial characteristics of fresh chicken meats. At the end of the storage, all chitosan or chitosan-GSE coated samples were accepted by sensory members with good scores, while the bacterial loads in the same days were above to the limited level. This phenomenon may be due to the unique activity of chitosan coating on meat, which masks some deteriorative signs, including off-flavour and off-odour development as well as textural and sensory defects (Jasour et al., 2015). 4. Conclusion Results of the present study indicated that quality of fresh chicken meats preserved in all treated samples resulting in a notable shelf life enhancement as compared to the control. According to our results, the shelf life of control samples was 7 days during refrigeration and was extended to 14 days in CH and GCH samples and up to the end of storage (21 days) in I, ICH and IGCH samples. Based on the obtained results, IGCH samples had the best microbial, chemical and sensorial characteristics during storage among all treatments. Therefore, low-dose gamma irradiation, as well as chitosan coating containing GSE, can be practically applied to preserve the quality of chicken meats and producers and consumers would avail the benefits of natural bioactive compounds as well as shelf life extended products. Conflict of interest Authors declare no conflict of interest.
Acknowledgments
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The authors are grateful to the Faculty of Veterinary Medicine, Urmia University (Urmia, Iran) for financial support.
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Figure captions: Figure 1: The diagrams of descriptive sensory analysis of meat during refrigerated storage at days 0, 3, 6, 9, 14 and 21. A: odor, B: color and C: Overall acceptability. Treatments: Control, uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated + immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH).
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Figure 1
Table 1. Changes in total mesophilic bacteria count (log CFU g-1) of chicken meat samples during storage at 4 °C (M±SD).
Storage time (days) Treatment C I CH ICH GCH IGCH
0
3 A
3.65±0.20 2.07±0.14D 3.24±0.27B 2.02±0.10D 2.72±0.16C 1.47±0.19E
6 A
4.25±0.20 2.65±0.25C 3.75±0.41B 2.28±0.17D 3.39±0.24B 1.90±0.19D
9 A
5.54±0.28 3.38±0.10D 4.60±0.26B 3.07±0.17D 4.15±0.22C 2.61±0.34E
*
A
7.35±0.23 4.25±0.13C 5.56±0.25B 4.11±0.22C 5.33±0.18B 3.55±0.25D
14
21
* 5.57±0.20B 6.73±0.27A 5.26±0.28B 6.61±0.29A 4.62±0.28C
* 6.95±0.30A 7.95±0.31B 6.74±0.24B 7.59±0.44B 6.13±0.27B
Not analyzed due to development of visible spoilage signs. Treatments: Control (C), uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated + immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH). Different letters for each time indicate a statistically significant difference (P < 0.05).
17
Table 2. Changes in psychrotrophic count (log CFU g-1) of chicken meat samples during storage at 4 °C (M±SD). Storage time (days) Treatment C I CH ICH GCH IGCH
0
3 B
4.20±0.20 2.65±0.16D 4.10±0.15A 2.26±0.19F 3.50±0.21C 2.36±0.21E
6 A
4.73±0.32 3.20±0.25D 4.56±0.21B 2.84±0.15E 4.16±0.23C 2.55±0.17F
9 A
6.11±0.26 3.85±0.25D 5.01±0.17B 3.57±0.23E 4.70±0.19C 3.05±0.19F
A
7.68±0.32 4.70±0.22C 5.87±0.34B 4.61±0.17C 5.84±0.24B 4.14±0.25D
14
21
* 5.59±0.28B 7.01±0.26A 5.70±0.23C 6.90±0.38A 5.17±0.18D
* 7.10±0.18B 8.16±0.29A 6.95±0.36C 7.99±0.34A 6.80±0.31C
*
Not analyzed due to development of visible spoilage signs. Treatments: Control (C), uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated + immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH). Different letters for each time indicate a statistically significant difference (P < 0.05).
Table 3. Changes in pH values of chicken meat samples during storage at 4 °C (M±SD).
Storage time (days) Treatment C I CH ICH GCH IGCH
0
3
6
9
14
21
5.7±0.05AB 5.8±0.05A 5.6±0.05B 5.7±0.05AB 5.6±0.10B 5.7±0.05AB
5.8±0.05A 5.8±0.05A 5.5±0.05C 5.6±0.05B 5.6±0.05B 5.6±0.05B
6.0±0.10A 5.8±0.05B 5.6±0.05C 5.6±0.05C 5.7±0.10BC 5.7±0.05BC
6.3±0.05A 6.0±0.10B 5.7±0.05C 5.7±0.05C 5.7±0.10C 5.8±0.10C
* 6.5±0.05A 5.7±0.10B 5.8±0.10B 5.8±0.05B 5.8±0.05B
* 6.7±0.10A 6.1±0.10C 6.2±0.10C 6.2±0.10BC 6.3±0.10B
*
Not analyzed due to development of visible spoilage signs. Treatments: Control (C), uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated + immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH). Different letters for each time indicate a statistically significant difference (P < 0.05).
18
Table 4. Correlation between total mesophilic bacteria count and pH values of chicken meat samples during storage at 4 °C (M±SD).
Treatment C I CH ICH GCH IGCH
Correlation coefficient 0.98 0.95 0.69 0.82 0.72 0.86
Significance 0.0001 0.0001 0.0045 0.0001 0.0024 0.0001
Treatments: Control (C), uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated + immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH).
Table 5. Changes in aw values of chicken meat samples during storage at 4 °C (M±SD).
Storage time (days) Treatment C I CH ICH GCH IGCH
0
3
6
9
14
21
0.97±0.01 0.96±0.01 0.97±0.01 0.96±0.01 0.96±0.02 0.97±0.02
0.96±0.01 0.97±0.01 0.96±0.01 0.97±0.02 0.97±0.01 0.96±0.01
0.97±0.01 0.97±0.02 0.97±0.02 0.96±0.02 0.98±0.01 0.96±0.01
0.97±0.02 0.97±0.01 0.97±0.01 0.97±0.01 0.97±0.01 0.97±0.01
* 0.97±0.01 0.97±0.02 0.97±0.01 0.97±0.01 0.97±0.02
* 0.97±0.02 0.97±0.01 0.98±0.01 0.97±0.01 0.98±0.01
*
Not analyzed due to development of visible spoilage signs. Same superscript letters indicate no significant difference within a column (P >0.05). Treatments: Control (C), uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated +
19
immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH).
Table 6. Changes in thiobarbituric acid reactive substances values (mg MDA kg -1) of chicken meat samples during storage at 4 °C (M±SD)
Storage time (days) Treatment
0
3
C I CH ICH GCH IGCH
0.32±0.06AB 0.35±0.08A 0.18±0.07CD 0.30±0.07ABC 0.08±0.01D 0.21±0.06BCD
0.40±0.06AB 0.47±0.16A 0.24±0.09CD 0.42±0.03A 0.11±0.05D 0.27±0.07BC
6
9
0.49±0.08BC 0.61±0.16ABC 0.69±0.17A 0.90±0.25A C 0.35±0.10 0.47±0.11CD 0.64±0.08AB 0.87±0.15AB 0.16±0.04D 0.23±0.07D C 0.41±0.09 0.54±0.16BCD
14
21
* 1.28±.28A 0.66±0.09B 1.11±0.19A 0.31±0.06C 0.79±0.16B
* 1.95±0.18A 0.90±0.12C 1.73±0.12AB 0.39±0.21D 1.31±0.34B
*
Not analyzed due to development of visible spoilage signs. Treatments: Control (C), uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated + immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH). Different letters for each time indicate a statistically significant difference (P < 0.05).
Highlights Keeping quality of chicken meat were ensured with irradiation and active packaging. GSE incorporation into chitosan coating decreased lipid oxidation. Chitosan or chitosan- GSE coated samples were accepted by sensory members. Combined preservation activity achieved with active coating and irradiation.
20
PII: DOI: Reference:
S0969-806X(17)30421-8 http://dx.doi.org/10.1016/j.radphyschem.2017.06.014 RPC7572
To appear in: Radiation Physics and Chemistry Received date: 13 April 2017 Revised date: 10 June 2017 Accepted date: 18 June 2017 Cite this article as: Parviz Hassanzadeh, Hossein Tajik, Seyed Mehdi Razavi Rohani, Mehran Moradi, Mohammad Hashemi and Javad Aliakbarlu, Effect of functional chitosan coating and gamma irradiation on the shelf-life of chicken meat during refrigerated storage, Radiation Physics and Chemistry, http://dx.doi.org/10.1016/j.radphyschem.2017.06.014 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Effect of functional chitosan coating and gamma irradiation on the shelf-life of chicken meat during refrigerated storage
Parviz Hassanzadeha, Hossein Tajikb, Seyed Mehdi Razavi Rohanib, Mehran Moradib*, Mohammad Hashemic, Javad Aliakbarlub a
Department of Food Hygiene and Aquatic Disease, Faculty of Veterinary Medicine, University of Tabriz, Tabriz, East Azarbaijan, Iran
b
Department of Food Hygiene and Quality Control, Faculty of Veterinary Medicine, Urmia University, Urmia, West Azarbaijan, Iran
c
Department of Nutrition, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran
[email protected] [email protected].
*
Correspondent: Tel.: +984431942633; fax +984432771926;
Abstract The present study was conducted to evaluate the combined effect of low-dose gamma irradiation (2.5 kGy) and chitosan edible coating (2%) containing grape seed extract (GSE) (0.1%) on the microbial, chemical and sensorial quality of chicken breast meat during 21 days of storage at 4 C. The samples were periodically analyzed for microbiological (aerobic mesophilic and psychrotrophic counts), chemical (TBA, pH, aw) and sensorial (odor, appearance, and overall acceptability) characteristics. Results indicated that irradiation and the active coating had significant (P < 0.05) effects on reduction of bacterial growth with at least a 14-day extension of shelf life. Results represented the protective effect of chitosan coating containing GSE against 1
induced lipid oxidation by irradiation. All chitosan-coated samples showed lower TBA and pH values than other treatments during storage, and no significant (P > 0.05) difference was observed due to irradiation in TBA values. Results also indicated that the application of chitosan coating significantly improved the sensorial quality of the samples, and none of the evaluated sensorial attributes was significantly affected by irradiation. Based on the results obtained in this study, the application of low-dose gamma irradiation and chitosan coating containing GSE was effective in preserving the quality of fresh chicken meats and is recommended in meat products. Keywords: Gamma irradiation; active packaging; grape seed extract; chicken meat; shelf life.
1. Introduction Chicken meat is a food commodity with a rich source of essential amino acids, minerals, vitamins and low lipid content. Moreover, it contains relatively high levels of polyunsaturated fatty acids. All of these specifications illustrate chicken meat as an excellent substrate for microbial spoilage and oxidative reactions (Raeisi et al., 2016). Nowadays researchers and poultry processing industries are focusing on developing new techniques to reduce microbial growth and oxidative reactions of meat in order to extend its shelf life and preserve its original quality (Bazargani-Gilani et al., 2015). The integration became popular in poultry meat due to the worldwide popularity of these products. Recently, research has been intensified on the application of natural preservatives in food due to safety issues and consumer demands (Alizadeh Sani et al., 2017), because they extend the shelf life of food without side effects resulting in increased tendency for their application by both producers and researchers (Farhangfar et al., 2011). Edible coatings and films prepared from natural sources encounter with a special attention since they have been proven as a carrier of food additives such as flavors, antimicrobials, antioxidants, and enzymes. This type of packaging could regulate the release of functional compounds into food and maintains high levels of additives on the surface of foods. This phenomenon has of great importance to increase the shelf life of foods of animal origin (Moradi et al., 2016). Chitosan, in form of coating or film, is widely used in food due to its bioactive characteristics such as antifungal, antibacterial and antioxidative activities (Bazargani-Gilani et al., 2015). It is a natural biopolymer, which is 2
industrially produced by four steps including demineralization, deproteinization, decoloration and deacetylation of chitins which mainly obtained from crab and shrimp shells (BazarganiGilani et al., 2015). Chitosan as a coating solution or film has been used in food by many researchers for active packaging carrying natural antioxidants and/or antimicrobials (Jasour et al., 2015; Moradi et al., 2011;Özdemir and Gökmen, 2017; Yu et al., 2017). By-products from herbals materials were gained strong attention as a dietary supplement and food additive. Grape seed extract (GSE) is a novel ingredient extracted from the grape seeds (Vitis vinifera). Their functional properties, antioxidant and antimicrobial, are due to
the higher amounts of
polyphenolic compounds (Perumalla and Hettiarachchy, 2011; Shah et al., 2014). Biological activity of GSE has been shown in various meats (Farhangfar et al., 2011). Gama irradiation in medium doses can be used to improve the microbial quality of chicken meat, ensures its safety and extend its shelf life with no adverse changes or deterioration. The food industry has given permission to use gamma irradiation (≤10 kGy) in food packaging and food processing sites (Chen et al., 2016). In previous studies, gamma irradiation has been used in order to extend shelf life of different kinds of meat, including minced camel meat (Al-Bachir and Zeinou, 2009), intermediate‐moisture meat (Rao et al., 2005), barbecued chicken (Fallah et al., 2010), game hen carcasses (Yoon, 2003), minced chicken meat (Abdeldaiem, 2014) and chicken meat (Javanmard et al., 2006). A literature review represented some studies on the effect of combinational use of gamma irradiation and active coatings on the shelf life extension of meat (Abdeldaiem, 2014; Kang et al., 2007; Lacroix et al., 2004; Rao et al., 2005), but to our knowledge, no study has been conducted on the combined effect of gamma irradiation and active coatings in chicken meat. The use of combined technologies is increasing, therefore the present study was conducted to determine the potential of gamma irradiation and chitosan active coatings containing GSE individually and in combination as a hurdle system, to improve the microbial, chemical and sensorial quality of fresh chicken meat during refrigerated at 4 C. 2. Materials and Methods 2.1.Meat preparation The chicken breast was obtained directly from AzarShahr slaughterhouse (Azarshar, Iran) on the day of the experiment and immediately transported to the laboratory at refrigerated temperature.
3
Under an aseptic condition, the meat was cut and pre-weighed to 200-gram samples and kept in sterile polyethylene bags (Zipack™, Tehran, Iran) at 4 C until coating. 2.2.Preparation of GSE and chitosan coating solution Commercial GSE powder [extraction solvent: water, phenolics contents (gallic acid equivalents, dry basis) ≥ 90 g GAE/100 g], was provided kindly by Mega Natural Inc. (Madera, CA, USA). Medium molecular weight chitosan flakes (75-85% degree of deacetylation) was purchased from Sigma-Aldrich Company (St. Louis, MO, USA). Chitosan solution (20 g/L) was prepared by dissolving two grams of chitosan in 100 mL of 10 g L-1 acetic acid (Merck, Darmstadt, Germany) with constant agitation overnight at room temperature (Yingyuad, et al., 2006). Glycerol (Merck, Darmstadt, Germany) was added to the chitosan solution at 0.5 mL g-1. 2.3.Treatment of meat samples Meat samples were divided to six groups: (i) uncoated (control, C); (ii) uncoated+ irradiated (I); (iii) immersed in chitosan solution (CH); (iv) irradiated + immersed in chitosan solution (ICH); (v) immersed in chitosan solution containing 0.1% GSE (GCH) and (vi) irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH). Samples were immersed in 200 volumes of chitosan or chitosan+ GSE solution for 1 min and then drained and packed in sterile polyethylene bags. 2.4.Radiation treatment After coating, chitosan coated samples from groups I, ICH and IGCH, were immediately transferred under the refrigerated condition to Atomic Energy Organization of Iran located in Tehran, Iran and exposed to gamma radiation using a
60
Co radiation source (Gamma Cell 220
Nordion International Inc., Ontario, Canada) at a dose of 2.5 kGy. The absorbed doses were measured by alanine dosimeter. Samples were covered with crushed ice to keep them at 33 C during the irradiation process. After irradiation, samples were transported back to Urmia University and stored at 4 C for 21 days. Sampling for shelf-life evaluation was done at days 0, 3, 6, 9, 14 and 21 for all irradiated and non-irradiated meat samples. 2.5.Microbiological evaluation
4
At each time, meat samples (25 g) were homogenized in 225 mL of sterile 0.1% peptone water (Merck, Darmstadt, Germany) for 1 min using stomacher (model 400, Seward Medical Ltd, London, U.K.). Decimal dilutions (1:10) in 0.1% peptone water solution were prepared and appropriate diluents were poured on plates of the following agars: Plate Count Agar (PCA, Merck, Darmstadt, Germany) for total mesophilic viable count (TMVC) incubated at 35 C for 24 h and PCA for total psychrotrophic viable count (TPVC) incubated at 7 C for 5-7 days. Results were expressed as log10 CFU g-1. 2.6.Chemical quality evaluation 2.6.1. Crude protein and fat measurement The samples were separately homogenized (IKA, T25 basic, Germany) and analyzed for crude protein and crude fat, according to AOAC methods (AOAC, 1990). 2.6.2. pH measurement Ten grams of sample was homogenized with 90 mL of distilled water for 30 s and pH value of the homogenate was measured using a pH-meter (pH-Meter E520, Metrohm Herisau, Switzerland). 2.6.3. Water activity measurement The water activities of all samples were measured at room temperature with a water activity meter (Novasina, ms1, Pfäffi- kon, Switzerland). 2.6.4. Lipid oxidation evaluation Lipid oxidation of each control and treated samples were performed by an extraction thiobarbituric acid (TBA) method as described by Pikul, et al. (1989) with minor modification. Each 10 g set of meat samples were individually homogenized in 35 mL of cold (4 C) extraction solution containing 4% perchloric acid (Merck, Darmstadt, Germany)
and 1 mL of BHA
(Merck, Darmstadt, Germany) (1 mg mL-1) at 13,500 rpm for 1 min. The preparation was mixed and filtered, then the filtrate was adjusted to 50 mL with 4% perchloric acid and 5 mL aliquot of the filtrate was added to 5 mL of TBA (Merck, Darmstadt, Germany) (0.02 M). The mixture was vortexed and then incubated in a 100 °C water bath for 60 min for color development. The absorbance at 532 nm was measured with a spectrophotometer (Novaspec II spectrophotometer 5
(Amersham Pharmacia Biotech Inc., Buckinghamshire, UK). The TBA values were expressed in units of mg malonaldehyde kg-1 (mg MDA kg -1) sample. 2.7.Sensorial evaluation Meat samples were evaluated by 6-member trained sensory panel participants from our department during days 0, 3, 6, 9, 14 and 21. The panelists were trained before their participation. Panelists evaluated odor, appearance and overall acceptability using a nine-point hedonic scale (9 = like extremely; 8 = like very much; 7 = like moderately; 6 = like slightly; 5 = neither like nor dislike; 4 = dislike slightly; 3 = dislike moderately; 2 = dislike very much; 1 = dislike extremely) (Ehsani et al., 2016). 2.8.Statistical analysis All experiments had three replications for each treatment and measurement. Data were expressed as mean ± SD. Significant differences were evaluated at P < 0.05 by analysis of variance (ANOVA) and Duncan's multiple range test using SPSS 13.0 (SPSS Inc., Chicago, IL, USA).
3. Results and discussion 3.1.Microbiological changes Both chitosan and GSE represent an antimicrobial and an antioxidants activity. GSE is one of the most powerful natural antioxidants, while in the case of antimicrobial activity, GSE is weaker than chitosan. The binary use of these two compounds enhance the effects of each of the two compounds (Moradi et al., 2011). Changes on TMVC and TPVC are shown in Tables 1 and 2. TMVC and TPVC values of all treatments significantly (P < 0.05) increased during the storage at 4 C and the highest increase rate was observed in control samples. TMVC and TPVC values of all treated samples were significantly lower than control revealing the inhibitory effect of treatments on the increase rate of TMVC and TPVC, and the highest and the lowest effects were observed in IGCH and CH samples, respectively. Irradiation reduced significantly the TMVC and TPVC level and showed a significant lower microorganisms level during storage as compared to the control (P<0.05). As it can be seen, non-irradiated samples including C, CH, and GCH, reached to the value of 7 log CFU g-1 (the limit of acceptability) on day 9, 14 and 21 of storage, respectively, however, I, ICH and IGCH samples never reached the limit of 6
acceptability value of TMVC till the end of storage time. Similar to thermal and chemical treatments, the type and the number of microorganisms found in the flora of food affect the efficiency of irradiation process, and then radiation efficacy is reduced by increasing the food microbial counts. Former studies reported similar results for the effect of irradiation (Al-Bachir and Zeinou, 2009; Fallah et al., 2010; Özden et al., 2007; Rahimi et al., 2013) and chitosan coatings (Duan et al., 2010; Gómez-Estaca et al., 2007; Kanatt et al., 2004) on the reduction of TMVC and TPVC values. Most phenolics of GSE have a more powerful effect on bacteria. It was previously proposed that GSE was more effective on gram-positive than gram-negative bacteria and some groups of spoilage bacteria, including gram-positive lactic acid bacteria, showed a high resistance into GSE (Moradi et al., 2011). The exact antimicrobial activity mechanism remains unclear, whereas it was demonstrated that epigallocatechin-3-gallate inhibit dihydrofolate reductase, the enzyme involved in folate metabolism and biosynthesis of some major biomolecules (Kao et al., 2010).
3.2.Chemical changes Protein and fat contents of the control samples were analyzed on the first day of study and results were 20.56 and 1.36 %, respectively. The lowest and the highest aw values of the treatments during storage were 0.96 and 0.98, respectively, without any significant (P > 0.05) changes among treatments during storage (Table 3). The pH changes of chicken meat samples during storage are shown in Table 4. The average pH value of the samples was 5.6 on the first day of storage which increased in all treatments during storage. The pH values of all treated samples were significantly lower than control (P<0.05). All coated samples (CH, ICH. IGCH) had significantly lower pH values than non-coated samples (C and I), indicating the causative effect of chitosan coating on the constancy of pH value during storage. It can be due to acidic properties of chitosan solution and prevention of microbial growth on the surface of the samples. Former studies reported that chitosan coating application in chicken meat samples could stabilize the pH value of them during storage and chitosan coated samples had lower pH values than others as well (Duan et al., 2010; Fan et al., 2009; Yingyuad et al., 2006). Table 5, represents the correlation between TMVC values and pH values of the treatments during storage. As showed, there was a significant (P < 0.05) association between TMVC values and pH values of the 7
samples. Chitosan-coated samples had lower correlation coefficient than non-coated samples and the lowest coefficient was observed in CH samples indicating control of microbial growth and pH elevation by chitosan coating application. The effects of radiation on chemical characteristics of the meat are influenced by radiation dose, type, and composition of meat, keeping temperature, gaseous composition of packaging and microbial load of meat (Lee et al., 2006). According to Al-Bachir and Zeinou (2009), lipid oxidation of meat is initiated soon after slaughtering and develop to unacceptable levels during storage. Results of TBARS values of chicken meat treated with gamma irradiation and chitosan coatings during 21 days of storage period are shown in Table 6. Results showed that over the storage period at 4 C, malondialdehyde (MDA) values increased in all treated samples. The highest and the lowest TBARS values were observed in I (1.95 mg MDA kg -1) and GCH (0.085 mg MDA kg -1) samples, respectively. Irradiation increased TBARS values of the samples during storage, due to the generation of free radicals by ionizing radiation which induces lipid peroxidation, however, the difference was not significant (P > 0.05) when compared to control. Other researchers reported the same results for the effects of irradiation on lipid oxidation as well (Javanmard et al., 2006; Kwon et al., 2008). Regarding TBARS values of irradiated samples (I, ICH and IGCH), IGCH samples showed lower values compared to I samples during 21 days of storage (P<0.05), represents the protective effect of chitosan coating containing GSE against induced lipid oxidation by irradiation. These results may be rationalized considering the possible synergistic activity among polyphenols of GSE and chitosan that is applied on meat. GSE is reported as potent antioxidant compounds owning scavenging activities against free radical and Schiff-base metal complexes as well as synergistic activity with another antioxidant (Perumalla and Hettiarachchy, 2011). The antioxidant activity of GSE is contributed to polyphenolic compounds including gallic acid, monomeric flavan-3-ols catechin, epicatechin, gallocatechin, epigallocatechin and epicatechin 3-O-gallate, as well as more highly polymerized procyanidin (Gibis et al., 2013). During the storage, an increment in lipid oxidation of samples containing GSE is possibly related to the development of phenolic aldehydes due to degradation of some phenolic compounds of phenolic-rich agents (Moradi et al., 2011). Results also indicated that chitosan coating could inhibit the increase rate of MDA values of treated samples during storage compared to control. A significant difference (P<0.05) was observed between CH and C samples during the first 3 days of storage and between GCH and C 8
samples up to the end of storage time. Yingyuad et al. (2006) reported that chitosan coating could effectively preserve refrigerated grilled pork against lipid oxidation which was completely consistent with results of the present study. It was also reported that the antioxidant activity of chitosan increased upon irradiation (25 kGy) without significant effects on its antimicrobial property (Kanatt et al., 2004). The authors showed that irradiated chitosan had antioxidant activity 27-fold greater than the non-irradiated chitosan. When chitosan was irradiated at a dose higher than 40 kGy, no further increase in its antioxidant activity was recorded. The increase in reducing power upon irradiation indicated enhanced antioxidant activity that can be exploited for radiation-processed food in reducing radiation-induced lipid peroxidation. 3.3.Sensorial changes Changes in sensorial attributes are one of the main reason of shelf life reduction of meat products, that can be due to microbial growth and lipid oxidation resulting in the production of adverse metabolites and reduction of sensorial properties (Brannan and Mah, 2007; Kwon et al., 2008). The sensory evaluation results of chicken meat samples during days 0, 3, 6, 9, 14 and 21 are given in Figure 1. The sensory scores (odor and color and overall acceptability) of control and treated samples declined during storage, while they were acceptable, although, sensory evaluation of control samples was not performed on 9th and 14th days of storage period due to the presence of spoilage signs. Results indicated that irradiation decreased sensory scores (especially odor attribute) when compared to other samples, however, it was not statistically significant (P > 0.05). Other work performed by Abu-Tarboush et al. (1997) demonstrated that irradiation at a dose between 2.5 and 10 kGy had a slight effect on the sensory quality (appearance, odor, taste, and texture) on both raw and cooked chicken meat. Several sulfurs containing compounds especially dimethyl trisulfide are produced in irradiated chicken meat samples (Kim et al., 2002), which might affect sensorial attributes of irradiated samples in the present study. According to sensory results, irradiation could preserve the quality of fresh chicken meats for 5 days and extend their shelf life until the end of the storage period (day 21). Similar results were obtained by other researchers who reported approximately two weeks shelf life extension in irradiated chicken meat samples (Javanmard et al., 2006). Results also indicated a higher sensorial scores in chitosan coated samples, indicating the effects of chitosan coating on preserving sensory characteristics of chicken meat which were in line with results of former studies (Kanatt et al., 9
2008; Rao et al., 2005; Yingyuad et al., 2006). The type of food and chitosan determines the effect of chitosan coating on sensorial attributes of food. A more recent work showed that chitosan coating did not affect the sensorial quality of ready-to-cook meat in terms of changes in appearance and any off-flavor (Kanatt et al., 203). As seen in figure 1, the addition of GSE to coating did not significantly impact consumer preference (P > 0.05). The highest sensorial scores were observed in IGCH samples during storage that may be due to functional properties of chitosan and GSE. It can highlight the effects of irradiation and chitosan coating incorporated with GSE on preserving sensorial characteristics of fresh chicken meats. At the end of the storage, all chitosan or chitosan-GSE coated samples were accepted by sensory members with good scores, while the bacterial loads in the same days were above to the limited level. This phenomenon may be due to the unique activity of chitosan coating on meat, which masks some deteriorative signs, including off-flavour and off-odour development as well as textural and sensory defects (Jasour et al., 2015). 4. Conclusion Results of the present study indicated that quality of fresh chicken meats preserved in all treated samples resulting in a notable shelf life enhancement as compared to the control. According to our results, the shelf life of control samples was 7 days during refrigeration and was extended to 14 days in CH and GCH samples and up to the end of storage (21 days) in I, ICH and IGCH samples. Based on the obtained results, IGCH samples had the best microbial, chemical and sensorial characteristics during storage among all treatments. Therefore, low-dose gamma irradiation, as well as chitosan coating containing GSE, can be practically applied to preserve the quality of chicken meats and producers and consumers would avail the benefits of natural bioactive compounds as well as shelf life extended products. Conflict of interest Authors declare no conflict of interest.
Acknowledgments
10
The authors are grateful to the Faculty of Veterinary Medicine, Urmia University (Urmia, Iran) for financial support.
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Figure captions: Figure 1: The diagrams of descriptive sensory analysis of meat during refrigerated storage at days 0, 3, 6, 9, 14 and 21. A: odor, B: color and C: Overall acceptability. Treatments: Control, uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated + immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH).
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Figure 1
Table 1. Changes in total mesophilic bacteria count (log CFU g-1) of chicken meat samples during storage at 4 °C (M±SD).
Storage time (days) Treatment C I CH ICH GCH IGCH
0
3 A
3.65±0.20 2.07±0.14D 3.24±0.27B 2.02±0.10D 2.72±0.16C 1.47±0.19E
6 A
4.25±0.20 2.65±0.25C 3.75±0.41B 2.28±0.17D 3.39±0.24B 1.90±0.19D
9 A
5.54±0.28 3.38±0.10D 4.60±0.26B 3.07±0.17D 4.15±0.22C 2.61±0.34E
*
A
7.35±0.23 4.25±0.13C 5.56±0.25B 4.11±0.22C 5.33±0.18B 3.55±0.25D
14
21
* 5.57±0.20B 6.73±0.27A 5.26±0.28B 6.61±0.29A 4.62±0.28C
* 6.95±0.30A 7.95±0.31B 6.74±0.24B 7.59±0.44B 6.13±0.27B
Not analyzed due to development of visible spoilage signs. Treatments: Control (C), uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated + immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH). Different letters for each time indicate a statistically significant difference (P < 0.05).
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Table 2. Changes in psychrotrophic count (log CFU g-1) of chicken meat samples during storage at 4 °C (M±SD). Storage time (days) Treatment C I CH ICH GCH IGCH
0
3 B
4.20±0.20 2.65±0.16D 4.10±0.15A 2.26±0.19F 3.50±0.21C 2.36±0.21E
6 A
4.73±0.32 3.20±0.25D 4.56±0.21B 2.84±0.15E 4.16±0.23C 2.55±0.17F
9 A
6.11±0.26 3.85±0.25D 5.01±0.17B 3.57±0.23E 4.70±0.19C 3.05±0.19F
A
7.68±0.32 4.70±0.22C 5.87±0.34B 4.61±0.17C 5.84±0.24B 4.14±0.25D
14
21
* 5.59±0.28B 7.01±0.26A 5.70±0.23C 6.90±0.38A 5.17±0.18D
* 7.10±0.18B 8.16±0.29A 6.95±0.36C 7.99±0.34A 6.80±0.31C
*
Not analyzed due to development of visible spoilage signs. Treatments: Control (C), uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated + immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH). Different letters for each time indicate a statistically significant difference (P < 0.05).
Table 3. Changes in pH values of chicken meat samples during storage at 4 °C (M±SD).
Storage time (days) Treatment C I CH ICH GCH IGCH
0
3
6
9
14
21
5.7±0.05AB 5.8±0.05A 5.6±0.05B 5.7±0.05AB 5.6±0.10B 5.7±0.05AB
5.8±0.05A 5.8±0.05A 5.5±0.05C 5.6±0.05B 5.6±0.05B 5.6±0.05B
6.0±0.10A 5.8±0.05B 5.6±0.05C 5.6±0.05C 5.7±0.10BC 5.7±0.05BC
6.3±0.05A 6.0±0.10B 5.7±0.05C 5.7±0.05C 5.7±0.10C 5.8±0.10C
* 6.5±0.05A 5.7±0.10B 5.8±0.10B 5.8±0.05B 5.8±0.05B
* 6.7±0.10A 6.1±0.10C 6.2±0.10C 6.2±0.10BC 6.3±0.10B
*
Not analyzed due to development of visible spoilage signs. Treatments: Control (C), uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated + immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH). Different letters for each time indicate a statistically significant difference (P < 0.05).
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Table 4. Correlation between total mesophilic bacteria count and pH values of chicken meat samples during storage at 4 °C (M±SD).
Treatment C I CH ICH GCH IGCH
Correlation coefficient 0.98 0.95 0.69 0.82 0.72 0.86
Significance 0.0001 0.0001 0.0045 0.0001 0.0024 0.0001
Treatments: Control (C), uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated + immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH).
Table 5. Changes in aw values of chicken meat samples during storage at 4 °C (M±SD).
Storage time (days) Treatment C I CH ICH GCH IGCH
0
3
6
9
14
21
0.97±0.01 0.96±0.01 0.97±0.01 0.96±0.01 0.96±0.02 0.97±0.02
0.96±0.01 0.97±0.01 0.96±0.01 0.97±0.02 0.97±0.01 0.96±0.01
0.97±0.01 0.97±0.02 0.97±0.02 0.96±0.02 0.98±0.01 0.96±0.01
0.97±0.02 0.97±0.01 0.97±0.01 0.97±0.01 0.97±0.01 0.97±0.01
* 0.97±0.01 0.97±0.02 0.97±0.01 0.97±0.01 0.97±0.02
* 0.97±0.02 0.97±0.01 0.98±0.01 0.97±0.01 0.98±0.01
*
Not analyzed due to development of visible spoilage signs. Same superscript letters indicate no significant difference within a column (P >0.05). Treatments: Control (C), uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated +
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immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH).
Table 6. Changes in thiobarbituric acid reactive substances values (mg MDA kg -1) of chicken meat samples during storage at 4 °C (M±SD)
Storage time (days) Treatment
0
3
C I CH ICH GCH IGCH
0.32±0.06AB 0.35±0.08A 0.18±0.07CD 0.30±0.07ABC 0.08±0.01D 0.21±0.06BCD
0.40±0.06AB 0.47±0.16A 0.24±0.09CD 0.42±0.03A 0.11±0.05D 0.27±0.07BC
6
9
0.49±0.08BC 0.61±0.16ABC 0.69±0.17A 0.90±0.25A C 0.35±0.10 0.47±0.11CD 0.64±0.08AB 0.87±0.15AB 0.16±0.04D 0.23±0.07D C 0.41±0.09 0.54±0.16BCD
14
21
* 1.28±.28A 0.66±0.09B 1.11±0.19A 0.31±0.06C 0.79±0.16B
* 1.95±0.18A 0.90±0.12C 1.73±0.12AB 0.39±0.21D 1.31±0.34B
*
Not analyzed due to development of visible spoilage signs. Treatments: Control (C), uncoated+ irradiated (I); immersed in chitosan solution (CH); irradiated + immersed in chitosan solution (ICH); immersed in chitosan solution containing 0.1% GSE (GCH) and irradiated + immersed in chitosan solution containing 0.1% GSE (IGCH). Different letters for each time indicate a statistically significant difference (P < 0.05).
Highlights Keeping quality of chicken meat were ensured with irradiation and active packaging. GSE incorporation into chitosan coating decreased lipid oxidation. Chitosan or chitosan- GSE coated samples were accepted by sensory members. Combined preservation activity achieved with active coating and irradiation.
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