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Effects of gamma irradiation on physicochemical properties of heat-induced gel prepared with chicken salt-soluble proteins
Radiation Physics and Chemistry 106 (2015) 16–20
Contents lists available at ScienceDirect
Radiation Physics and Chemistry journal homepage: www.elsevier.com/locate/radphyschem
Effects of gamma irradiation on physicochemical properties of heat-induced gel prepared with chicken salt-soluble proteins Yun-Sang Choi a, Hyun-Wook Kim b, Ko-Eun Hwang b, Dong-Heon Song b, Tae-Jun Jeong b, Kwang-Wook Seo c, Young-Boong Kim a, Cheon-Jei Kim b,n a
Research Group of Convergence Technology, Korean Food Research Institute, Seongnam 463-746, Republic of Korea Department of Food Science and Biotechnology of Animal Resources, Konkuk University, Seoul 143-701, Republic of Korea c Food and Biological Resources Examination Division, Korean Intellectual Property Office, Daejeon 302-701, Republic of Korea b
H I G H L I G H T S
The effect of gamma irradiation on salt-soluble meat proteins was investigated. Gelling properties of salt-soluble protein affected by gamma irradiation. Gamma irradiation of meat products provides a basic resource processing technology.
art ic l e i nf o
a b s t r a c t
Article history: Received 23 December 2013 Accepted 30 June 2014 Available online 9 July 2014
The technological effects of gamma irradiation (0, 3, 7, and 10 kGy) on chicken salt-soluble meat proteins in a model system were investigated. There were no significant differences in protein, fat, and ash content, and sarcoplasmic protein solubility among all samples. The samples with increasing gamma irradiation levels had higher pH, lightness, yellowness, and apparent viscosity, whereas moisture content, water holding capacity, redness, myofibrillar protein solubility, total protein solubility, hardness, springiness, cohesiveness, gumminess, and chewiness were the highest in the unirradiated control. The result from meat products using gamma irradiation was intended to provide a basic resource processing technology. & 2014 Elsevier Ltd. All rights reserved.
Keywords: Gamma irradiation Heat-induced gel Chicken salt-soluble meat protein Model systems
1. Introduction In general gamma irradiation, unlike heat treatment, has been widely applied in medicine and biology in terms of its biological effects induced by the counter-intuitive switchover from low-dose stimulation to high-dose inhibition (Chung et al., 2006). Food irradiation technology has been confirmed as an effective method for the prevention of food spoilage as well as for the control of food pathogens, because the food technology is applied abundantly (Kim et al., 2014). Irradiation for meat and meat products is expected to prolong shelf life during storage. The World Health Organization (WHO) (1999) reported that irradiation up to 10 kGy is generally known to result in no change in the nutritional properties of food or in its safety. According to Jo et al. (1999), in irradiated meat and meat products, irradiation can have an effect on the acceleration of lipid oxidation, discoloration and the decline
n
Corresponding author. Tel.: þ 82 2 450 3684; fax: þ 82 2 444 6695. E-mail address: [email protected] (C.-J. Kim).
http://dx.doi.org/10.1016/j.radphyschem.2014.06.029 0969-806X/& 2014 Elsevier Ltd. All rights reserved.
of sensory characteristics, which can generate negative consumer responses. The gel formation of muscle proteins is the most important functional property of processed meat products (Wang et al., 1990). The muscle proteins, such as myofibrillar protein (saltsoluble), sarcoplasmic protein (water-soluble) and stroma protein (insoluble), undergo partial denaturation followed by an irreversible aggregation, which results in a three-dimensional network (Lanier et al., 2004). Total muscle protein is composed of approximately 30% myofibrillar proteins, in which the myofibrillar protein commonly results in gel formation due to the heat denaturation of the protein (Wang et al., 1990; Vega-Warner et al., 1999). The gel forms a stable tertiary structure due to a polymerization reaction between the protein molecules, depending on the moisture, salt, protein, pH, actomyosin solubility, and cooking methods (Yasui et al., 1982). Lee et al. (2000) reported the conformational changes of myosin by gamma irradiation. However, the effects of the heatinduced gelation properties of gamma-irradiated chicken saltsoluble protein are not known. Moreover, it is not understood whether the irradiated meat protein interacts with the salt-soluble meat proteins during gel network formation.
Y.-S. Choi et al. / Radiation Physics and Chemistry 106 (2015) 16–20
The objective of this study was to investigate the effect of gamma irradiation (0, 3, 7, and 10 kGy) on the proximate composition, water holding capacity, pH, color, protein solubility, apparent viscosity, and textural properties of heated-induced gel prepared with chicken salt-soluble protein in the model systems.
2. Materials and methods 2.1. Protein extraction Fresh chicken breast meat (broiler, Muscularis pectoralis major, 2 wk of age, approximately 1.5–2.0 kg live weight, moisture 74.95%, protein 22.58%, fat 1.09%, ash 1.31%) was purchased from a local processor. The reason for using chicken breast meat was due to its relatively low cost of production, low fat content, and high nutritional value. In addition, chicken meats are very popular among consumers and provide an excellent source of animal protein. The chicken meat was ground initially through an 8-mm plate, and then again ground through a 3-mm plate. The ground tissue was then placed in polyethylene bags, vacuum-packaged using a vacuum packaging system (FJ-500XL, Fujee Tech, Seoul, Korea) and stored at 0 1C until required for salt-soluble protein manufacture. The samples were allowed to equilibrate at 2 1C and the meat pH was determined with a pH meter (Model 340, Mettler-Toledo GmbH, Schwerzenbach, Switzerland) after mixing 10 g of ground muscle with 100 ml deionized–distilled water for 1 min. One part meat and two parts 0.58 M saline (0.49 M NaCl, 17.8 mM Na5P3O10, and 1 mM NaN3, pH 8.3, 2 1C) solution of the same ionic strength and pH were blended for 30 s in a blender. The slurry was kept at 2 1C for 1 h and then centrifuged (12,000g, 2 1C) for 1 h (Supra 25 K high speed refrigerated centrifuge, Hanil Science Industrial, Seoul, Korea). The protein extract was strained through three layers of cheesecloth (Camou et al., 1989). Protein concentrations of the meat solids and supernatant were determined by a nitrogen analyzer (Kjeltecs 2300Analyzer Unit, Foss Tecator AB, Höganas, Sweden). Nitrogen was converted to protein by multiplying by 6.25. Moisture and fat determinations were performed by AOAC (1995) methods.
2.2. Gamma irradiation The vacuum-packaged ground chicken breast was irradiated at 0, 3, 7, and 10 kGy in a cobalt-60 irradiator (point source, AECL, IR-79, Nordion International, Canada) with source strength of 3.7 1012 kBq (100 kCi) in Advanced Radiation Technology Institute of Korea Atomic Energy Research Institute (Republic of Korea). The size of each packaged sample was 8 10 cm2, and the thickness was below 1 cm. Dosimetry was performed using 5 mm diameter alanine dosimeters (Bruker Instruments, Germany), and the actual dose was within 7 2.0% of the target dose. The gammairradiated chicken breast (IP) was transferred immediately to a 4 1C refrigerator and stored until gel preparation (for 1 day).
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2.4. Water holding capacity (WHC) Water holding capacity (WHC) was measured gravimetrically as described by Kocher and Foegeding (1993) using chicken meat heat-induced gels prepared from four formulations (0, 3, 7, and 10 kGy). Before thermal processing, the sealed tubes were centrifuged at 1000g for 15 min at 4 1C to remove air bubbles. Samples were equilibrated at 20 1C for 10 min in a water bath, heated to 90 1C at 1.75 1C/min and held at 90 1C for 20 min after which the resulting supernatant was decanted and weighed. The samples were then stored at 4 1C for 24 h. Gels were centrifuged (Supra 25 K high speed refrigerated centrifuge, Hanil Science Industrial, Seoul, Korea) at 1000g for 15 min at 4 1C. Weights of the centrifuge tubes and the moisture captured within, as well as the filters with the cooked gel, were measured for calculation of the moisture loss and the cooked gel weight. Water holding capacity (%) was expressed using the following formula: WHC ð%Þ ¼ ½1–ðML=CGÞ 100 ML is the weight of the moisture loss from the gel after centrifugation and CG is the weight of the cooked gel. Data reported represent mean values from three replicates. Each replicate consisted of three observations per treatment. 2.5. Proximate composition Compositional properties of the samples were determined using AOAC procedures (1995). Moisture content (950.46B, oven airdrying method) was determined by weight loss after 12 h of drying at 105 1C in a drying oven (SW-90D, Sang Woo Scientific Co., Bucheon, Korea). Fat content (960.69, ether extractable component) was determined by the Soxhlet method with a solvent extraction system (Soxtecs Avanti 2050 Auto System, Foss Tecator AB, Höganas, Sweden), and protein content (981.10) was determined by the Kjeldahl method with an automatic Kjeldahl nitrogen analyzer (Kjeltecs 2300Analyzer Unit, Foss Tecator AB, Höganas, Sweden). Ash content was determined according to AOAC method 920.153 (muffle furnace). 2.6. pH determination The pH values of each sample were measured in a homogenate prepared with 5 g of sample and distilled water (20 ml) using a pH meter (Model 340, Mettler-Toledo GmbH, Schwerzenbach, Switzerland). All determinations were performed in triplicate. 2.7. Color evaluation The color of each gel was determined using a colorimeter (Minolta Chroma meter CR-210, Minolta Co., Osaka, Japan; illuminate C, calibrated with a white plate, Ln ¼ þ97.83, an ¼ 0.43, bn ¼ þ1.98). Six measurements for each of five replicates were taken. Lightness (CIE Ln), redness (CIE an), and yellowness (CIE bn) values were recorded. 2.8. Protein solubility
2.3. Gel preparation Salt-soluble chicken meat protein solutions were diluted to 5% protein with a saline solution of the same pH (6.0) as that of the protein extract, and transferred to glass gelling tubes (dimension ¼ 20 mm). The sealed tubes were centrifuged at 800g for 15 min at 4 1C to remove air bubbles. The samples were equilibrated at 20 1C for 10 min in a water bath, heated to 90 1C at 1.75 1C/min and held at 90 1C for 20 min. After heating, the tubes were immersed in water overnight at 4 1C (McCord et al., 1998).
Protein solubility was utilized as an indicator of protein denaturation (Joo et al., 1999). Sarcoplasmic protein solubility was determined by dissolving 2 g of muscle powder in 20 ml of ice-cold 25 mM potassium phosphate buffer (pH 7.2). The heat-induced gel samples and buffer were homogenized on ice with a homogenizer (Model AM-7, Nihonseiki Kaisha Ltd., Tokyo, Japan) set at 1500 rpm, and were left to stand on a shaker at 4 1C overnight. The mixtures were centrifuged at 1500g for 20 min and the protein concentrations of the supernatants were determined using the biuret method (Gornall
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et al., 1949). Total protein solubility was determined by homogenizing 2 g of muscle powder in 20 ml of ice-cold 1.1 mol/l potassium iodide in a 100 mol/l phosphate buffer (pH7.2). The procedures for homogenization, shaking, centrifugation, and protein determination are described above. Myofibrillar protein solubility was obtained by determining the difference between the total and sarcoplasmic protein solubilities. 2.9. Apparent viscosity Each gel viscosity was measured in triplicate with a rotational viscometer (HAKKE Viscotesters 500, Thermo Elctron Corporation, Karlsruhe, Germany) set at 10 rpm. A standard cylinder sensor (SV-E) was positioned in a 50 ml plastic cup filled with gel and allowed to rotate under a constant shear rate at s 1 for 30 s before each reading was taken. Apparent viscosity values in centipoises were obtained. The temperature of each sample at the time (18 71 1C) of viscosity testing was also recorded (Park et al., 2004). 2.10. Texture profile analysis (TPA) The textural properties of irradiated chicken salt-soluble meat protein samples during thermal gelation were measured with a texture analyzer (TA-XT2i, Stable Micro Systems, Surrey, England) with 25 kg load cell. The center cores of heat-induced gel samples were cut (20 mm in diameter, 15 mm height) and compressed twice to 30% of their original height at constant cross-head speed of 2.0 mm/s. The conditions of texture analysis were as follows: pre-test speed 2.0 mm/s, post-test speed 5.0 mm/s, maximum load 2 kg, head speed 2.0 mm/s, distance 8.0 mm, force 10 g. The texture profile analysis (TPA) parameters, namely hardness [peak force on first compression (N)], springiness [ratio of the sample recovered after the first compression], cohesiveness [ratio of the active work done under the second force–displacement curve to that done under the first compression curve], gumminess [hardness cohesiveness], and chewiness [hardness cohesiveness springiness (N)], were computed (Bourne, 1978). 2.11. Statistical analysis The experiment was replicated three times, each with a new batch of irradiated chicken salt-soluble meat protein, and the data were analyzed using the general linear model (GLM) procedure of the SAS (2011) statistical package. Main factors included gamma irradiation level (0, 3, 7, and 10 kGy). When an interaction between factors was found significant (Po0.05), means were separated out by treatment groups. If the interaction was not significant, data were pooled to test the main effect using Duncan's multiple range test.
3. Results and discussion The water holding capacity of heat-induced gel prepared with irradiated chicken salt-soluble protein is presented in Table 1. The water holding capacity of heat-induced gel prepared with irradiated chicken salt-soluble protein decreased with increasing gamma irradiation levels (Po 0.05). The water holding capacity and moisture content were results of a similar trend. These results agree with those reported by Osburn and Keeton (2004), who reported that the increase in moisture content can be attributed to the large water holding capacity of the hydrocolloid gel. Further, Nakayama and Sato (1971) observed that an increased water holding capacity can be largely attributed to myosin; hence, the results of this study may be affected by the water holding capacity
of myosin denaturation. The compositional properties of heatinduced gel samples are not shown in the table. The moisture contents of irradiated heat-induced gels (85.43–87.61%) were lower in formulations with the irradiated sample than the control (88.86%) (P o0.05), and decreased with an increase in the irradiation levels (P o0.05). The protein (10.21–10.56%), fat (1.15–1.18%), and ash (2.61–2.78%) contents of heat-induced gel samples were not significantly different between formulations with the treated irradiation and the control (P 40.05). According to Liu et al. (2008), the heat-induced gel involves the association of myosin and the action chains produce a continuous three-dimensional network in which water is trapped. The results of the moisture content may be attributed to protein denaturation due to irradiation. Table 2 shows the pH and color values of heat-induced gel prepared with irradiated chicken salt-soluble meat protein. The pH of the unheated and heated gels increased with increasing treated irradiation levels (Po 0.05). Similar results were obtained by Al-Bachir et al. (2010) for the influence of gamma irradiation on the chemical properties of chicken kebab. Increasing irradiation of chicken kebab significantly increased the pH values. The pH of the heated gel was higher in the gel prepared with irradiated chicken salt-soluble protein compared to the unheated gel. The pH increased when the gel was heated because the basic R group of the amino acid was exposed during heating. The differences in lightness (Ln-value), redness (an-value), and yellowness (bn-value) of the heat-induced gel prepared with irradiated chicken saltsoluble meat protein were significant (Po 0.05) (Table 2). The lightness and yellowness of the all irradiated treatment samples were higher than those of control, and among the irradiated treatments increased with increasing gamma irradiation levels. On the other hand, redness was highest in the unheated and heated control (P o0.05). The solubilities of sarcoplasmic, myofibrillar, and total proteins in the heat-induced gel prepared with irradiated chicken saltsoluble meat protein are presented in Table 3. Generally meat proteins can be divided into three groups, sarcoplasmic protein (water-soluble), myofibrillar protein (salt-soluble), and stromal protein (insoluble), based on their solubility characteristics (Xiong, 1997). According to Wang et al. (1990) protein solubility profiles are effective indications of the degree of protein denaturation during processing, depending on the physicochemical factor. The sarcoplasmic proteins of all treatments containing the control samples were not significantly different (P4 0.05). Myofibrillar protein solubility and total protein solubility of heat-induced gels prepared with chicken salt-soluble protein were higher in treatment samples with irradiation than in the control (Po 0.05). Lee et al. (2000) report that protein solubility increases slightly for irradiated beef with dose, and their result is different from that in this study. According to Sayre and Briskey (1963), the sarcoplasmic and myofibrillar protein solubility in meats of widely different quality was generated by a careful control of the conditions. Further, high values of total protein and sarcoplasmic protein solubility are important for high quality processed meat products (Young et al., 2005). Normally, the gel structure was affected by the myofibrillar protein gels formed. The apparent viscosity value of the unheated gel prepared with irradiated chicken salt-soluble meat protein is presented in Fig. 1. The control and all the irradiated and unheated gel samples were found to show thixotropic behavior with apparent viscosity values which decreased with an increase in rotation time. The apparent viscosity values of the gel prepared with irradiated chicken saltsoluble protein were affected by the irradiation levels. The control unheated gel samples had the lowest maximum viscosity, whereas the treatment samples of unheated gels had increased viscosity with increasing irradiation levels. Ciesla et al. (2004) reported that
Y.-S. Choi et al. / Radiation Physics and Chemistry 106 (2015) 16–20
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Table 1 Effect of water holding capacity on heat-induced gel prepared irradiated chicken salt-soluble protein. Parameters
Gamma irradiation levels (kGy)
Water holding capacity (%)
0
3
7
10
85.41 71.08a
83.16 71.57b
79.81 7 1.05c
75.96 7 1.17d
All values are the mean7 standard deviation of three replicates. a–d
Means within a row with different letters are significantly different (Po 0.05).
Table 2 Effect of pH and color on heat-induced gel prepared with irradiated chicken salt-soluble protein. Parameters
Gamma irradiation levels (kGy) 0
Unheated
Heated
pH Ln-value an-value bn-value pH Ln-value an-value bn-value
3 d
6.22 70.04 46.3571.87d 0.11 70.12a 1.39 70.24d 6.6770.10c 78.41 70.50c 0.3370.12a 4.22 70.64c
7 c
10 b
6.40 7 0.02 59.357 1.39c 0.26 7 0.13b 1.89 7 0.34c 6.72 7 0.13b 81.76 7 1.08b 0.69 7 0.12b 4.47 7 0.38b
6.56 7 0.02a 64.817 0.85a 0.667 0.19d 3.167 1.70a 6.78 7 0.15a 83.83 7 1.57a 0.88 7 0.15b 5.05 7 0.55a
6.52 7 0.03 62.53 7 1.14b 0.54 7 0.06c 2.677 1.12b 6.767 0.17ab 82.767 0.55ab 0.85 7 0.03b 4.53 7 0.14b
All values are the mean7 standard deviation of three replicates. a–d
Means within a row with different letters are significantly different (Po 0.05).
Table 3 Effect of protein solubility on heat-induced gel prepared by irradiating chicken salt-soluble protein. Parameters
Sarcoplasmic protein solubility (mg/g) Myofibrillar protein solubility (mg/g) Total protein solubility (mg/g)
Gamma irradiation levels (kGy) 0
3
7
10
3.73 7 0.39 10.14 7 0.63a 13.87 7 0.65a
3.497 0.22 7.99 7 0.21b 11.487 0.52b
3.497 0.23 6.43 7 0.42b 9.92 7 0.51c
3.217 0.17 6.08 7 0.21b 9.29 7 0.21c
All values are the mean7 standard deviation of three replicates. a–c
Means within a row with different letters are significantly different (Po 0.05).
Table 4 Effect of texture profile analysis on heat-induced gel prepared with irradiated chicken salt-soluble protein. Parameters
Hardness (N) Springiness Cohesiveness Gumminess (N) Chewiness (N)
Gamma irradiation levels (kGy) 0
3
7
10
1.007 0.07a 0.98 7 0.05a 0.60 7 0.11a 0.747 0.13a 0.65 7 0.13a
0.93 7 0.12b 0.95 7 0.06ab 0.517 0.09b 0.517 0.8b 0.52 7 0.06b
0.88 70.05c 0.92 70.03b 0.44 70.03c 0.41 70.04c 0.38 70.04c
0.747 0.08d 0.84 7 0.04c 0.43 7 0.02c 0.36 7 0.03d 0.30 7 0.02d
All values are the mean 7 standard deviation of three replicates. Fig. 1. Apparent viscosity of chicken salt-soluble protein heat-induced gels formulated with irradiation for 30 s: (□) 0 kGy gamma irradiation (unirradation); (■) 3 kGy gamma irradiation; (△) 7 kGy gamma irradiation; (▲) 10 kGy gamma irradiation.
the viscosity of milk protein at the same shear rate for the irradiated solutions was higher than that for the control, due to the increase in viscosity caused by the proteins cross-linking. Normally, high viscosity in the model system is not easily changed due to an increase in emulsion stability (Akats and Genccelep, 2006; Choi et al., 2010). The irradiation levels significantly affected the textural properties of the heat-induced gel prepared with irradiated chicken saltsoluble meat protein (Table 4). The unirradiated control had the
a–d Means within a row with different letters are significantly different (P o0.05).
highest hardness, springiness, cohesiveness, gumminess, and chewiness (P o0.05), whereas the hardness, springiness, cohesiveness, gumminess, and chewiness of the heat-induced gel tended to decrease with increasing irradiation levels. The decreasing textural properties were most likely due to the denaturation of chicken salt-soluble protein by gamma irradiation.
4. Conclusions The analysis of irradiated chicken salt-soluble protein gels demonstrated that the gamma irradiation significantly affects
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heat-induced gel water holding capacity, apparent viscosity, and textural properties. The reduced water holding capacity and textural properties and increased apparent viscosity were most likely due to the denaturation of chicken salt-soluble protein by gamma irradiation. These results suggest that gelling properties of chicken salt-soluble protein in the model systems can be affected by gamma irradiation. This study of chicken meat products using gamma irradiation was intended to provide a gelling property. Acknowledgement This study was supported by the National Research Foundation of Korea funded by Ministry of Science, ICT and Future Planning (2013M2A2A6043298). References Akats, N., Genccelep, H., 2006. Effect of starch type and its modifications on physicochemical properties of bologna-type sausage produced with sheep tail rat. Meat Sci. 74, 404–408. Al-Bachir, M., Farah, S., Othman, Y., 2010. Influence of gamma irradiation and storage on the microbial load, chemical and sensory quality of chicken kebab. Radiat. Phys. Chem. 79, 900–905. AOAC, 1995. 16th ed.Official Methods of Analysis of AOAC, Vol. 41. Association of Official Analytical Chemists, Washington, DC. Bourne, M.C., 1978. Texture profile analysis. Food Technol. 32, 62–66. Camou, J.P., Sebranek, J.G., Plson, D.G., 1989. Effect of heating rate and protein concentration on gel strength and water loss of muscle protein gels. J. Food Sci. 54, 850–854. Choi, Y.S., Choi, J.H., Han, D.J., Kim, H.Y., Lee, M.A., Kim, H.W., Lee, J.W., Chung, H.J., Kim, C.J., 2010. Optimization of replacing pork back fat with grape seed oil and rice bran fiber for reduced-fat meat emulsion systems. Meat Sci. 84, 212–218. Chung, B.Y., Lee, Y.B., Baek, M.H., Kim, J.H., Wi, S.G., Kim, J.S., 2006. Effects of lowdose gamma-irradiation on production of shikonin derivatives in callus cultures of Lithospermum erythrorhizon S. Radiat. Phys. Chem. 75, 1018–1023. Ciesla, K., Salmieri, S., Lacroix, M., Tien Le, C., 2004. Gamma irradiation influence on physical properties of milk proteins. Radiat. Phys. Chem. 71, 93–97. Gornall, A.G., Bardawill, C.J., David, M.M., 1949. Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 177, 751–766. Jo, C., Lee, J.I., Ahn, D.U., 1999. Lipid oxidation, color changes and volatiles production in irradiated pork sausage with different fat content and packaging during storage. Meat Sci. 51, 355–361.
Joo, S.T., Kauffman, R.G., Kim, B.C., Park, G.B., 1999. The relationship of sarcoplasmic and myofibrillar protein solubility to colour and water-holding capacity in porcine longissimus muscle. Meat Sci. 52, 291–297. Kim, H.W., Choi, J.H., Choi, Y.S., Kim, H.Y., Lee, M.A., Hwang, K.E., Song, D.H., Lee, J.W., Kim, C.J., 2014. Effects of kimchi and smoking on quality characteristics and shelf life of cooked sausages prepared with irradiated pork. Meat Sci. 96, 548–553. Kocher, P., Foegeding, E., 1993. Microcentrifuge-based method for measuring waterholding of protein gels. J. Food Sci. 58, 1040–1046. Lanier, T.C., Carvajal, P., Yongaswatdigul, J., 2004. Surimi gelation chemistry. In: Prak, J.W. (Ed.), Surimi and Surini Seafood, 2nd ed. Marcel Dekker, New York, pp. 451–470. Lee, J.W., Yook, H.S., Lee, K.H., Kim, J.H., Kim, W.J., Byun, M.W., 2000. Conformational changes of myosin by gamma irradiation. Radiat. Phys. Chem. 58, 271–277. Liu, R., Zhao, S.M., Xiong, S.B., Xie, B.J., Qin, L.H., 2008. Role of secondary structures in the gelation of porcine myosin at different pH values. Meat Sci. 80, 632–639. McCord, A., Smyth, A.B., O'Neill, E.E., 1998. Heat-induced gelation properties of saltsoluble muscle proteins as affected by non-meat proteins. J Food Sci. 63, 580–583. Nakayama, T., Sato, Y., 1971. Relationship between binding quality of meat and myofibrillar protein. J. Texture Stud. 2, 475–488. Osburn, W.N., Keeton, J.T., 2004. Evaluation of low-fat sausage containing desinewed lamb and konjac gel. Meat Sci. 68, 221–233. Park, S.Y., Wang, S.H., Chin, K.B., Kim, Y.D., 2004. Rheological properties of the mixture and heat-induced gel prepared from pork salt soluble protein in combined with soluble chitooligosaccharide and chitosan. Korean J. Food Sci. Technol. 36, 594–597. SAS, 2011. SAS User's Guide: Basic Statistical Analysis. Statistical Analysis Systems Institute, NC, USA. Sayre, R.N., Briskey, E.J., 1963. Protein solubility as influenced by physiological conditions in the muscle. J. Food Sci. 28, 675–679. Vega-Warner, V., Merkel, R.A., Smith, D.M., 1999. Composition, solubility and gel properties of salt soluble proteins from two bovine muscle types. Meat Sci. 51, 197–203. Wang, S.F., Smith, D.M., Steffe, J.F., 1990. Effect of pH on the dynamic rhelogical properties of chicken breast salt-soluble protein during heat-induced gelation. Poult. Sci. 69, 2220–2227. World Health Organization (WHO), 1999. High Dose Irradiation: Wholesomeness of Food Irradiated with Doses Above 10 kGy. WHO Technical Report Series 890, Geneva. Xiong, Y.L., 1997. Structure–function relationships of muscle proteins. In: Damodaran, S., Paraf, A. (Eds.), Food Proteins and Their Applications. Marcel Dekker, New York, pp. 341–392. Yasui, T., Ishioroshi, M., Samejima, K., 1982. Effect of actomyosin on heat-induced gelation of myosin. J. Agric. Biol. Chem. 46, 1049–1059. Young, O.A., Zhang, S.X., Farouk, M.M., Podmore, C., 2005. Effects of pH adjustment with phosphates on attributes and functionalities of normal and high pH beef. Meat Sci. 70, 133–139.
Contents lists available at ScienceDirect
Radiation Physics and Chemistry journal homepage: www.elsevier.com/locate/radphyschem
Effects of gamma irradiation on physicochemical properties of heat-induced gel prepared with chicken salt-soluble proteins Yun-Sang Choi a, Hyun-Wook Kim b, Ko-Eun Hwang b, Dong-Heon Song b, Tae-Jun Jeong b, Kwang-Wook Seo c, Young-Boong Kim a, Cheon-Jei Kim b,n a
Research Group of Convergence Technology, Korean Food Research Institute, Seongnam 463-746, Republic of Korea Department of Food Science and Biotechnology of Animal Resources, Konkuk University, Seoul 143-701, Republic of Korea c Food and Biological Resources Examination Division, Korean Intellectual Property Office, Daejeon 302-701, Republic of Korea b
H I G H L I G H T S
The effect of gamma irradiation on salt-soluble meat proteins was investigated. Gelling properties of salt-soluble protein affected by gamma irradiation. Gamma irradiation of meat products provides a basic resource processing technology.
art ic l e i nf o
a b s t r a c t
Article history: Received 23 December 2013 Accepted 30 June 2014 Available online 9 July 2014
The technological effects of gamma irradiation (0, 3, 7, and 10 kGy) on chicken salt-soluble meat proteins in a model system were investigated. There were no significant differences in protein, fat, and ash content, and sarcoplasmic protein solubility among all samples. The samples with increasing gamma irradiation levels had higher pH, lightness, yellowness, and apparent viscosity, whereas moisture content, water holding capacity, redness, myofibrillar protein solubility, total protein solubility, hardness, springiness, cohesiveness, gumminess, and chewiness were the highest in the unirradiated control. The result from meat products using gamma irradiation was intended to provide a basic resource processing technology. & 2014 Elsevier Ltd. All rights reserved.
Keywords: Gamma irradiation Heat-induced gel Chicken salt-soluble meat protein Model systems
1. Introduction In general gamma irradiation, unlike heat treatment, has been widely applied in medicine and biology in terms of its biological effects induced by the counter-intuitive switchover from low-dose stimulation to high-dose inhibition (Chung et al., 2006). Food irradiation technology has been confirmed as an effective method for the prevention of food spoilage as well as for the control of food pathogens, because the food technology is applied abundantly (Kim et al., 2014). Irradiation for meat and meat products is expected to prolong shelf life during storage. The World Health Organization (WHO) (1999) reported that irradiation up to 10 kGy is generally known to result in no change in the nutritional properties of food or in its safety. According to Jo et al. (1999), in irradiated meat and meat products, irradiation can have an effect on the acceleration of lipid oxidation, discoloration and the decline
n
Corresponding author. Tel.: þ 82 2 450 3684; fax: þ 82 2 444 6695. E-mail address: [email protected] (C.-J. Kim).
http://dx.doi.org/10.1016/j.radphyschem.2014.06.029 0969-806X/& 2014 Elsevier Ltd. All rights reserved.
of sensory characteristics, which can generate negative consumer responses. The gel formation of muscle proteins is the most important functional property of processed meat products (Wang et al., 1990). The muscle proteins, such as myofibrillar protein (saltsoluble), sarcoplasmic protein (water-soluble) and stroma protein (insoluble), undergo partial denaturation followed by an irreversible aggregation, which results in a three-dimensional network (Lanier et al., 2004). Total muscle protein is composed of approximately 30% myofibrillar proteins, in which the myofibrillar protein commonly results in gel formation due to the heat denaturation of the protein (Wang et al., 1990; Vega-Warner et al., 1999). The gel forms a stable tertiary structure due to a polymerization reaction between the protein molecules, depending on the moisture, salt, protein, pH, actomyosin solubility, and cooking methods (Yasui et al., 1982). Lee et al. (2000) reported the conformational changes of myosin by gamma irradiation. However, the effects of the heatinduced gelation properties of gamma-irradiated chicken saltsoluble protein are not known. Moreover, it is not understood whether the irradiated meat protein interacts with the salt-soluble meat proteins during gel network formation.
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The objective of this study was to investigate the effect of gamma irradiation (0, 3, 7, and 10 kGy) on the proximate composition, water holding capacity, pH, color, protein solubility, apparent viscosity, and textural properties of heated-induced gel prepared with chicken salt-soluble protein in the model systems.
2. Materials and methods 2.1. Protein extraction Fresh chicken breast meat (broiler, Muscularis pectoralis major, 2 wk of age, approximately 1.5–2.0 kg live weight, moisture 74.95%, protein 22.58%, fat 1.09%, ash 1.31%) was purchased from a local processor. The reason for using chicken breast meat was due to its relatively low cost of production, low fat content, and high nutritional value. In addition, chicken meats are very popular among consumers and provide an excellent source of animal protein. The chicken meat was ground initially through an 8-mm plate, and then again ground through a 3-mm plate. The ground tissue was then placed in polyethylene bags, vacuum-packaged using a vacuum packaging system (FJ-500XL, Fujee Tech, Seoul, Korea) and stored at 0 1C until required for salt-soluble protein manufacture. The samples were allowed to equilibrate at 2 1C and the meat pH was determined with a pH meter (Model 340, Mettler-Toledo GmbH, Schwerzenbach, Switzerland) after mixing 10 g of ground muscle with 100 ml deionized–distilled water for 1 min. One part meat and two parts 0.58 M saline (0.49 M NaCl, 17.8 mM Na5P3O10, and 1 mM NaN3, pH 8.3, 2 1C) solution of the same ionic strength and pH were blended for 30 s in a blender. The slurry was kept at 2 1C for 1 h and then centrifuged (12,000g, 2 1C) for 1 h (Supra 25 K high speed refrigerated centrifuge, Hanil Science Industrial, Seoul, Korea). The protein extract was strained through three layers of cheesecloth (Camou et al., 1989). Protein concentrations of the meat solids and supernatant were determined by a nitrogen analyzer (Kjeltecs 2300Analyzer Unit, Foss Tecator AB, Höganas, Sweden). Nitrogen was converted to protein by multiplying by 6.25. Moisture and fat determinations were performed by AOAC (1995) methods.
2.2. Gamma irradiation The vacuum-packaged ground chicken breast was irradiated at 0, 3, 7, and 10 kGy in a cobalt-60 irradiator (point source, AECL, IR-79, Nordion International, Canada) with source strength of 3.7 1012 kBq (100 kCi) in Advanced Radiation Technology Institute of Korea Atomic Energy Research Institute (Republic of Korea). The size of each packaged sample was 8 10 cm2, and the thickness was below 1 cm. Dosimetry was performed using 5 mm diameter alanine dosimeters (Bruker Instruments, Germany), and the actual dose was within 7 2.0% of the target dose. The gammairradiated chicken breast (IP) was transferred immediately to a 4 1C refrigerator and stored until gel preparation (for 1 day).
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2.4. Water holding capacity (WHC) Water holding capacity (WHC) was measured gravimetrically as described by Kocher and Foegeding (1993) using chicken meat heat-induced gels prepared from four formulations (0, 3, 7, and 10 kGy). Before thermal processing, the sealed tubes were centrifuged at 1000g for 15 min at 4 1C to remove air bubbles. Samples were equilibrated at 20 1C for 10 min in a water bath, heated to 90 1C at 1.75 1C/min and held at 90 1C for 20 min after which the resulting supernatant was decanted and weighed. The samples were then stored at 4 1C for 24 h. Gels were centrifuged (Supra 25 K high speed refrigerated centrifuge, Hanil Science Industrial, Seoul, Korea) at 1000g for 15 min at 4 1C. Weights of the centrifuge tubes and the moisture captured within, as well as the filters with the cooked gel, were measured for calculation of the moisture loss and the cooked gel weight. Water holding capacity (%) was expressed using the following formula: WHC ð%Þ ¼ ½1–ðML=CGÞ 100 ML is the weight of the moisture loss from the gel after centrifugation and CG is the weight of the cooked gel. Data reported represent mean values from three replicates. Each replicate consisted of three observations per treatment. 2.5. Proximate composition Compositional properties of the samples were determined using AOAC procedures (1995). Moisture content (950.46B, oven airdrying method) was determined by weight loss after 12 h of drying at 105 1C in a drying oven (SW-90D, Sang Woo Scientific Co., Bucheon, Korea). Fat content (960.69, ether extractable component) was determined by the Soxhlet method with a solvent extraction system (Soxtecs Avanti 2050 Auto System, Foss Tecator AB, Höganas, Sweden), and protein content (981.10) was determined by the Kjeldahl method with an automatic Kjeldahl nitrogen analyzer (Kjeltecs 2300Analyzer Unit, Foss Tecator AB, Höganas, Sweden). Ash content was determined according to AOAC method 920.153 (muffle furnace). 2.6. pH determination The pH values of each sample were measured in a homogenate prepared with 5 g of sample and distilled water (20 ml) using a pH meter (Model 340, Mettler-Toledo GmbH, Schwerzenbach, Switzerland). All determinations were performed in triplicate. 2.7. Color evaluation The color of each gel was determined using a colorimeter (Minolta Chroma meter CR-210, Minolta Co., Osaka, Japan; illuminate C, calibrated with a white plate, Ln ¼ þ97.83, an ¼ 0.43, bn ¼ þ1.98). Six measurements for each of five replicates were taken. Lightness (CIE Ln), redness (CIE an), and yellowness (CIE bn) values were recorded. 2.8. Protein solubility
2.3. Gel preparation Salt-soluble chicken meat protein solutions were diluted to 5% protein with a saline solution of the same pH (6.0) as that of the protein extract, and transferred to glass gelling tubes (dimension ¼ 20 mm). The sealed tubes were centrifuged at 800g for 15 min at 4 1C to remove air bubbles. The samples were equilibrated at 20 1C for 10 min in a water bath, heated to 90 1C at 1.75 1C/min and held at 90 1C for 20 min. After heating, the tubes were immersed in water overnight at 4 1C (McCord et al., 1998).
Protein solubility was utilized as an indicator of protein denaturation (Joo et al., 1999). Sarcoplasmic protein solubility was determined by dissolving 2 g of muscle powder in 20 ml of ice-cold 25 mM potassium phosphate buffer (pH 7.2). The heat-induced gel samples and buffer were homogenized on ice with a homogenizer (Model AM-7, Nihonseiki Kaisha Ltd., Tokyo, Japan) set at 1500 rpm, and were left to stand on a shaker at 4 1C overnight. The mixtures were centrifuged at 1500g for 20 min and the protein concentrations of the supernatants were determined using the biuret method (Gornall
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et al., 1949). Total protein solubility was determined by homogenizing 2 g of muscle powder in 20 ml of ice-cold 1.1 mol/l potassium iodide in a 100 mol/l phosphate buffer (pH7.2). The procedures for homogenization, shaking, centrifugation, and protein determination are described above. Myofibrillar protein solubility was obtained by determining the difference between the total and sarcoplasmic protein solubilities. 2.9. Apparent viscosity Each gel viscosity was measured in triplicate with a rotational viscometer (HAKKE Viscotesters 500, Thermo Elctron Corporation, Karlsruhe, Germany) set at 10 rpm. A standard cylinder sensor (SV-E) was positioned in a 50 ml plastic cup filled with gel and allowed to rotate under a constant shear rate at s 1 for 30 s before each reading was taken. Apparent viscosity values in centipoises were obtained. The temperature of each sample at the time (18 71 1C) of viscosity testing was also recorded (Park et al., 2004). 2.10. Texture profile analysis (TPA) The textural properties of irradiated chicken salt-soluble meat protein samples during thermal gelation were measured with a texture analyzer (TA-XT2i, Stable Micro Systems, Surrey, England) with 25 kg load cell. The center cores of heat-induced gel samples were cut (20 mm in diameter, 15 mm height) and compressed twice to 30% of their original height at constant cross-head speed of 2.0 mm/s. The conditions of texture analysis were as follows: pre-test speed 2.0 mm/s, post-test speed 5.0 mm/s, maximum load 2 kg, head speed 2.0 mm/s, distance 8.0 mm, force 10 g. The texture profile analysis (TPA) parameters, namely hardness [peak force on first compression (N)], springiness [ratio of the sample recovered after the first compression], cohesiveness [ratio of the active work done under the second force–displacement curve to that done under the first compression curve], gumminess [hardness cohesiveness], and chewiness [hardness cohesiveness springiness (N)], were computed (Bourne, 1978). 2.11. Statistical analysis The experiment was replicated three times, each with a new batch of irradiated chicken salt-soluble meat protein, and the data were analyzed using the general linear model (GLM) procedure of the SAS (2011) statistical package. Main factors included gamma irradiation level (0, 3, 7, and 10 kGy). When an interaction between factors was found significant (Po0.05), means were separated out by treatment groups. If the interaction was not significant, data were pooled to test the main effect using Duncan's multiple range test.
3. Results and discussion The water holding capacity of heat-induced gel prepared with irradiated chicken salt-soluble protein is presented in Table 1. The water holding capacity of heat-induced gel prepared with irradiated chicken salt-soluble protein decreased with increasing gamma irradiation levels (Po 0.05). The water holding capacity and moisture content were results of a similar trend. These results agree with those reported by Osburn and Keeton (2004), who reported that the increase in moisture content can be attributed to the large water holding capacity of the hydrocolloid gel. Further, Nakayama and Sato (1971) observed that an increased water holding capacity can be largely attributed to myosin; hence, the results of this study may be affected by the water holding capacity
of myosin denaturation. The compositional properties of heatinduced gel samples are not shown in the table. The moisture contents of irradiated heat-induced gels (85.43–87.61%) were lower in formulations with the irradiated sample than the control (88.86%) (P o0.05), and decreased with an increase in the irradiation levels (P o0.05). The protein (10.21–10.56%), fat (1.15–1.18%), and ash (2.61–2.78%) contents of heat-induced gel samples were not significantly different between formulations with the treated irradiation and the control (P 40.05). According to Liu et al. (2008), the heat-induced gel involves the association of myosin and the action chains produce a continuous three-dimensional network in which water is trapped. The results of the moisture content may be attributed to protein denaturation due to irradiation. Table 2 shows the pH and color values of heat-induced gel prepared with irradiated chicken salt-soluble meat protein. The pH of the unheated and heated gels increased with increasing treated irradiation levels (Po 0.05). Similar results were obtained by Al-Bachir et al. (2010) for the influence of gamma irradiation on the chemical properties of chicken kebab. Increasing irradiation of chicken kebab significantly increased the pH values. The pH of the heated gel was higher in the gel prepared with irradiated chicken salt-soluble protein compared to the unheated gel. The pH increased when the gel was heated because the basic R group of the amino acid was exposed during heating. The differences in lightness (Ln-value), redness (an-value), and yellowness (bn-value) of the heat-induced gel prepared with irradiated chicken saltsoluble meat protein were significant (Po 0.05) (Table 2). The lightness and yellowness of the all irradiated treatment samples were higher than those of control, and among the irradiated treatments increased with increasing gamma irradiation levels. On the other hand, redness was highest in the unheated and heated control (P o0.05). The solubilities of sarcoplasmic, myofibrillar, and total proteins in the heat-induced gel prepared with irradiated chicken saltsoluble meat protein are presented in Table 3. Generally meat proteins can be divided into three groups, sarcoplasmic protein (water-soluble), myofibrillar protein (salt-soluble), and stromal protein (insoluble), based on their solubility characteristics (Xiong, 1997). According to Wang et al. (1990) protein solubility profiles are effective indications of the degree of protein denaturation during processing, depending on the physicochemical factor. The sarcoplasmic proteins of all treatments containing the control samples were not significantly different (P4 0.05). Myofibrillar protein solubility and total protein solubility of heat-induced gels prepared with chicken salt-soluble protein were higher in treatment samples with irradiation than in the control (Po 0.05). Lee et al. (2000) report that protein solubility increases slightly for irradiated beef with dose, and their result is different from that in this study. According to Sayre and Briskey (1963), the sarcoplasmic and myofibrillar protein solubility in meats of widely different quality was generated by a careful control of the conditions. Further, high values of total protein and sarcoplasmic protein solubility are important for high quality processed meat products (Young et al., 2005). Normally, the gel structure was affected by the myofibrillar protein gels formed. The apparent viscosity value of the unheated gel prepared with irradiated chicken salt-soluble meat protein is presented in Fig. 1. The control and all the irradiated and unheated gel samples were found to show thixotropic behavior with apparent viscosity values which decreased with an increase in rotation time. The apparent viscosity values of the gel prepared with irradiated chicken saltsoluble protein were affected by the irradiation levels. The control unheated gel samples had the lowest maximum viscosity, whereas the treatment samples of unheated gels had increased viscosity with increasing irradiation levels. Ciesla et al. (2004) reported that
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Table 1 Effect of water holding capacity on heat-induced gel prepared irradiated chicken salt-soluble protein. Parameters
Gamma irradiation levels (kGy)
Water holding capacity (%)
0
3
7
10
85.41 71.08a
83.16 71.57b
79.81 7 1.05c
75.96 7 1.17d
All values are the mean7 standard deviation of three replicates. a–d
Means within a row with different letters are significantly different (Po 0.05).
Table 2 Effect of pH and color on heat-induced gel prepared with irradiated chicken salt-soluble protein. Parameters
Gamma irradiation levels (kGy) 0
Unheated
Heated
pH Ln-value an-value bn-value pH Ln-value an-value bn-value
3 d
6.22 70.04 46.3571.87d 0.11 70.12a 1.39 70.24d 6.6770.10c 78.41 70.50c 0.3370.12a 4.22 70.64c
7 c
10 b
6.40 7 0.02 59.357 1.39c 0.26 7 0.13b 1.89 7 0.34c 6.72 7 0.13b 81.76 7 1.08b 0.69 7 0.12b 4.47 7 0.38b
6.56 7 0.02a 64.817 0.85a 0.667 0.19d 3.167 1.70a 6.78 7 0.15a 83.83 7 1.57a 0.88 7 0.15b 5.05 7 0.55a
6.52 7 0.03 62.53 7 1.14b 0.54 7 0.06c 2.677 1.12b 6.767 0.17ab 82.767 0.55ab 0.85 7 0.03b 4.53 7 0.14b
All values are the mean7 standard deviation of three replicates. a–d
Means within a row with different letters are significantly different (Po 0.05).
Table 3 Effect of protein solubility on heat-induced gel prepared by irradiating chicken salt-soluble protein. Parameters
Sarcoplasmic protein solubility (mg/g) Myofibrillar protein solubility (mg/g) Total protein solubility (mg/g)
Gamma irradiation levels (kGy) 0
3
7
10
3.73 7 0.39 10.14 7 0.63a 13.87 7 0.65a
3.497 0.22 7.99 7 0.21b 11.487 0.52b
3.497 0.23 6.43 7 0.42b 9.92 7 0.51c
3.217 0.17 6.08 7 0.21b 9.29 7 0.21c
All values are the mean7 standard deviation of three replicates. a–c
Means within a row with different letters are significantly different (Po 0.05).
Table 4 Effect of texture profile analysis on heat-induced gel prepared with irradiated chicken salt-soluble protein. Parameters
Hardness (N) Springiness Cohesiveness Gumminess (N) Chewiness (N)
Gamma irradiation levels (kGy) 0
3
7
10
1.007 0.07a 0.98 7 0.05a 0.60 7 0.11a 0.747 0.13a 0.65 7 0.13a
0.93 7 0.12b 0.95 7 0.06ab 0.517 0.09b 0.517 0.8b 0.52 7 0.06b
0.88 70.05c 0.92 70.03b 0.44 70.03c 0.41 70.04c 0.38 70.04c
0.747 0.08d 0.84 7 0.04c 0.43 7 0.02c 0.36 7 0.03d 0.30 7 0.02d
All values are the mean 7 standard deviation of three replicates. Fig. 1. Apparent viscosity of chicken salt-soluble protein heat-induced gels formulated with irradiation for 30 s: (□) 0 kGy gamma irradiation (unirradation); (■) 3 kGy gamma irradiation; (△) 7 kGy gamma irradiation; (▲) 10 kGy gamma irradiation.
the viscosity of milk protein at the same shear rate for the irradiated solutions was higher than that for the control, due to the increase in viscosity caused by the proteins cross-linking. Normally, high viscosity in the model system is not easily changed due to an increase in emulsion stability (Akats and Genccelep, 2006; Choi et al., 2010). The irradiation levels significantly affected the textural properties of the heat-induced gel prepared with irradiated chicken saltsoluble meat protein (Table 4). The unirradiated control had the
a–d Means within a row with different letters are significantly different (P o0.05).
highest hardness, springiness, cohesiveness, gumminess, and chewiness (P o0.05), whereas the hardness, springiness, cohesiveness, gumminess, and chewiness of the heat-induced gel tended to decrease with increasing irradiation levels. The decreasing textural properties were most likely due to the denaturation of chicken salt-soluble protein by gamma irradiation.
4. Conclusions The analysis of irradiated chicken salt-soluble protein gels demonstrated that the gamma irradiation significantly affects
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heat-induced gel water holding capacity, apparent viscosity, and textural properties. The reduced water holding capacity and textural properties and increased apparent viscosity were most likely due to the denaturation of chicken salt-soluble protein by gamma irradiation. These results suggest that gelling properties of chicken salt-soluble protein in the model systems can be affected by gamma irradiation. This study of chicken meat products using gamma irradiation was intended to provide a gelling property. Acknowledgement This study was supported by the National Research Foundation of Korea funded by Ministry of Science, ICT and Future Planning (2013M2A2A6043298). References Akats, N., Genccelep, H., 2006. Effect of starch type and its modifications on physicochemical properties of bologna-type sausage produced with sheep tail rat. Meat Sci. 74, 404–408. Al-Bachir, M., Farah, S., Othman, Y., 2010. Influence of gamma irradiation and storage on the microbial load, chemical and sensory quality of chicken kebab. Radiat. Phys. Chem. 79, 900–905. AOAC, 1995. 16th ed.Official Methods of Analysis of AOAC, Vol. 41. Association of Official Analytical Chemists, Washington, DC. Bourne, M.C., 1978. Texture profile analysis. Food Technol. 32, 62–66. Camou, J.P., Sebranek, J.G., Plson, D.G., 1989. Effect of heating rate and protein concentration on gel strength and water loss of muscle protein gels. J. Food Sci. 54, 850–854. Choi, Y.S., Choi, J.H., Han, D.J., Kim, H.Y., Lee, M.A., Kim, H.W., Lee, J.W., Chung, H.J., Kim, C.J., 2010. Optimization of replacing pork back fat with grape seed oil and rice bran fiber for reduced-fat meat emulsion systems. Meat Sci. 84, 212–218. Chung, B.Y., Lee, Y.B., Baek, M.H., Kim, J.H., Wi, S.G., Kim, J.S., 2006. Effects of lowdose gamma-irradiation on production of shikonin derivatives in callus cultures of Lithospermum erythrorhizon S. Radiat. Phys. Chem. 75, 1018–1023. Ciesla, K., Salmieri, S., Lacroix, M., Tien Le, C., 2004. Gamma irradiation influence on physical properties of milk proteins. Radiat. Phys. Chem. 71, 93–97. Gornall, A.G., Bardawill, C.J., David, M.M., 1949. Determination of serum proteins by means of the biuret reaction. J. Biol. Chem. 177, 751–766. Jo, C., Lee, J.I., Ahn, D.U., 1999. Lipid oxidation, color changes and volatiles production in irradiated pork sausage with different fat content and packaging during storage. Meat Sci. 51, 355–361.
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