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Effects of irradiation source and dose level on quality characteristics of processed meat products
Radiation Physics and Chemistry 130 (2017) 259–264
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Radiation Physics and Chemistry journal homepage: www.elsevier.com/locate/radphyschem
Effects of irradiation source and dose level on quality characteristics of processed meat products Youn-Kyung Ham a, Hyun-Wook Kim b, Ko-Eun Hwang a, Dong-Heon Song a, Yong-Jae Kim a, Yun-Sang Choi c, Beom-Seok Song d, Jong-Heum Park d, Cheon-Jei Kim a,n a
Department of Food science and Biotechnology of Animal Resources, Konkuk University, Seoul 143-701, Republic of Korea Meat Science and Muscle Biology Laboratory, Department of Animal Science, Purdue University, West Lafayette IN 47907, USA c Research Group of Convergence Technology, Korean Food Research Institute, Seongnam 463-746, Republic of Korea d Team for Radiation Food Science & Biotechnology, Advanced Radiation Technology Institute, Korea Atomic Energy Research Institute, Jeongeup 580-185, Republic of Korea b
H I G H L I G H T S
The effect of three irradiation source and dose level on meat products was studied. The redness was significantly influenced by irradiation sources and dose levels. Lipid oxidation, and microbial properties also affected by irradiation sources.
art ic l e i nf o
a b s t r a c t
Article history: Received 6 July 2016 Received in revised form 29 August 2016 Accepted 4 September 2016 Available online 5 September 2016
The effect of irradiation source (gamma-ray, electron-beam, and X-ray) and dose levels on the physicochemical, organoleptic and microbial properties of cooked beef patties and pork sausages was studied, during 10 days of storage at 30 71 °C. The processed meat products were irradiated at 0, 2.5, 5, 7.5, and 10 kGy by three different irradiation sources. The pH of cooked beef patties and pork sausages was unaffected by irradiation sources or their doses. The redness of beef patties linearly decreased with increasing dose level (P o0.05), obviously by e-beam irradiation compared to gamma-ray and X-ray (P o0.05). The redness of pork sausages was increased by gamma-ray irradiation, whereas it decreased by e-beam irradiation depending on absorbed dose level. No significant changes in overall acceptability were observed for pork sausages regardless of irradiation source (P4 0.05), while gamma-ray irradiated beef patties showed significantly decreased overall acceptability in a dose-dependent manner (Po 0.05). Lipid oxidation of samples was accelerated by irradiation depending on irradiation sources and dose levels during storage at 30 °C. E-beam reduced total aerobic bacteria of beef patties more effectively, while gamma-ray considerably decreased microbes in pork sausages as irradiation dose increased. The results of this study indicate that quality attributes of meat products, in particular color, lipid oxidation, and microbial properties are significantly influenced by the irradiation sources. & Published by Elsevier Ltd.
Keywords: Irradiation Beef patty Pork sausage X-ray Gamma-ray Electron-beam
1. Introduction Three irradiation sources, namely gamma-ray, electron-beam (e-beam), and X-ray approved for food irradiation by Codex Alimentarius Commission (2003), have been practically used to ensure microbial safety of meat and meat products even under unrefrigerated storage conditions (Roberts, 2014). With such evident advantage, it has been reported that irradiation could negatively
n
Corresponding author. E-mail address: [email protected] (C.-J. Kim).
http://dx.doi.org/10.1016/j.radphyschem.2016.09.010 0969-806X/& Published by Elsevier Ltd.
impact color, oxidative stability (particularly lipid oxidation), and sensory palatability, depending on the meat source, packaging methods, and irradiation conditions (Brewer, 2004). Gamma-ray and e-beam have been extensively used in not only commercial food sterilizing process but also scientific research determining quality changes in irradiated meat products (Lacroix and Ouattara, 2000). However, most consumers are still reluctant to purchase gamma-ray irradiated food due to their negative perceptions on the use of radioisotopes (Eustice and Bruhn, 2013). In terms of e-beam irradiation, the low penetration power of e-beam has been noted with locational variation in the irradiation effects on food
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system. (Miller, 2005). In this regard, X-ray irradiation has received a great attention as an effective means of food irradiation source with some advantages compared gamma-ray and e-beam. The major benefits of X-ray irradiation could be summarized as follows; 1) convenient operation of mechanical system, 2) higher productivity by reducing processing time, and 3) no generation of radioactive waste. In addition, the penetration power of X-ray irradiation is comparable to gamma-ray irradiation (Cleland and Stichelbaut, 2013). Thus, it has been anticipated that X-ray irradiation could be one of ways to considerably improve the negative perception of consumers on irradiated foods (Mitchell, 1994) and to overcome the technical limitations of e-beam irradiation. For these reasons, recent researches have evaluated the effects of the three irradiation sources on quality characteristics of several foods, for better application of food irradiation technology (Jung et al., 2015; Song et al., 2016). Although the effects of gamma-ray and e-beam irradiations on quality characteristics of meat products have been compared (López-González et al., 2000; Luchsinger et al., 1997; Park et al., 2010), there has been little information on the effects of the three irradiation sources on the quality characteristics of processed meat products at different absorbed dose levels. Therefore, the objective of this study was to evaluate the effects of irradiation source and dose levels on physicochemical, microbial and sensory properties of cooked beef patties and pork sausages.
2. Materials and methods 2.1. Sample preparation Cooked beef patties and pork sausages were manufactured according to the methods described by Kim et al. (2014b) and Lee et al. (2015), respectively. Beef patties were composed of 80% ground beef (M. semitendinosus), 15% pork back fat and 5% ice water. As additives, 1.2% nitrite picking salt (NaCl: sodium nitrite¼99.4:0.6), 0.05% sodium triphosphate, 1% sugar, 1% isolated soy protein, 0.1% pepper, 0.1% garlic powder, 0.1% ginger powder, 0.1% onion powder, 0.1% mixed spice (Nuremberg, Raps GmbH & Co., Kulmbach, Germany), and 0.05% L-ascorbic acid were added, based on total sample weight. Raw beef patties were cooked in a 15071 °C convention oven until the internal core temperature reached 7571 °C. Pork sausages were manufactured with 60% ground pork ham (M. biceps femoris, semitendinosus and semimembranosus), 20% pork back fat and 20% ice. The raw materials were emulsified with 1.2% nitrite picking salt, 0.3% sodium triphosphate, 0.5% sugar, 1% isolated soy protein, and 0.4% mixed spice (Bockwurst, Raps GmbH & Co., Kulmbach, Germany) in a bowl cutter. Meat batter was stuffed into collagen casing (#240, NIPPI Inc., Tokyo, Japan; approximately 25 mm diameter), and the pork sausages were cooked in a 75 71 °C smoke chamber for 40 min until the internal core temperature reached 72 71 °C. After cooling for 1 h, all cooked samples were individually vacuum-packaged with nylon/polyethylene bags (15 20 cm; thickness, 0.07 cm; 2 ml O2/m2/24 h at 0 °C) and stored in a 4 °C refrigerator for one day until irradiation process.
Ottawa, Canada) at the Korea Atomic Energy Research Institute (Jeongeup, Korea) with source strength of approximately 11.1 PBq, at dose rate of 10 kGy/h. E-beam and X-ray irradiation were performed using an ELV-4 electron beam accelerator (10 MeV) and X-ray linear accelerator (7.5 MeV) at the EB-Tech Co. (Daejeon, Korea), respectively. E-beam and X-ray irradiation were performed with a beam current of 1 mA and dose rate of 2.9 kGy/s and 5 kGy/ h, respectively. For dosimetry of samples, alanine dosimeters (5 mm diameter; Bruker Instruments, Bremen, Germany) were attached to the top and bottom of the samples, respectively. Subsequent to irradiation, the absorbed dose was measured with an electron paramagnetic resonance analyzer in accordance with international standards (ISO/ASTM 51607, 2004). The dose uniformity ratios (min/max ratios) of all irradiation sources were less than 1.2 and the actual dose was within 75% of the target dose. After irradiation, the irradiated samples were analyzed for quality characteristics on the day and stored in a 30 71 °C incubator for 10 days, to determine changes in lipid oxidation stability and microbial properties under the accelerated storage condition (Park et al., 2010). 2.3. Analysis of quality characteristics The pH values of the samples were determined using an electronic pH meter (Model 340; Mettler-Toledo GmbH, Schwerzenbach, Switzerland) (Lee et al., 2015). The CIE a*(redness) of samples was measured using a colorimeter (Chroma Meter CR-210; Konica Minolta, Osaka, Japan) (Lee et al., 2015). The hardness of beef patties and pork sausages were measured using a texture analyzer (TA-XT2i, Stable Micro System Ltd., Godalming, Surrey, UK) in accordance with the method of Choi et al. (2015). The sensory evaluation for overall acceptability (1 ¼not acceptable and 10 ¼very acceptable) was conducted by 12 trained panels (Kim et al., 2014a); the sample preparation and evaluation procedure were followed by AMSA research guidelines (2015). Lipid oxidation of samples was determined at 0, 3, 7 and 10 days of storage according to the modified TBARS method of Tarladgis et al. (1960) described by Kim et al. (2014b). Total aerobic bacteria and coliform bacteria were determined at 0, 3, 7 and 10 days of storage, using plate count agar and 3 M-Petrifilm E. coli/coliform count plates, respectively (Kim et al., 2014a; AOAC International, 2005). All measurements were conducted in triplicate. 2.4. Statistical analysis Experimental design was a completely randomized design with three independent batches. Analysis of variance (ANOVA) was performed on all the variables measured using the general linear model (GLM) procedure with SPSS software (SPSS Inc., Chicago, IL, USA, 2008). When significant differences were found, Duncan's multiple-range test was used to compare mean values among treatments at a significance level of 95%. Furthermore, simple linear regression analysis for each ionizing source was conducted to determine the level of relationship between the irradiation dose and analyzed variables.
3. Results and discussion 2.2. Irradiation procedure 3.1. Physicochemical and sensory properties The vacuum-packaged beef patties (approximately 15 mm thickness) and pork sausages (approximately 25 mm thickness) were irradiated at five absorbed dose levels of 0 (control), 2.5, 5, 7.5 or 10 kGy using three irradiation sources under the ambient temperature of 22 72 °C. Gamma-ray irradiation was conducted in a cobalt-60 irradiator (100 kCi, AECL, IR-79, MDS Nordion Inc.,
The significances of main effects, irradiation source and absorbed dose level, and their interaction, on physicochemical and sensory properties of cooked beef patties and pork sausages are shown in Table 1. No interactions between those main effects on all measurements of cooked beef patties were found (P 40.05),
Y.-K. Ham et al. / Radiation Physics and Chemistry 130 (2017) 259–264
Table 1 Significance of main effects and their interaction on physicochemical and sensory properties of cooked beef patties and pork sausages. Main effects and their interaction Cooked beef patties Ionizing source effect (I) Irradiation dose effect (D) Interaction (I D) Cooked pork sausages Ionizing source effect (I) Irradiation dose effect (D) Interaction (I D)
pH CIE a* (redness)
Hardness Sensory acceptability
NS
***
NS
***
NS
***
NS
***
NS
NS
NS
NS
***
***
*
NS
***
***
NS
***
***
***
NS
NS
NS, non-significance. *
p o 0.05. p o 0.001.
***
whereas the pH and CIE a* (redness) of cooked pork sausages were influenced by their interaction (P o0.05). The effects of irradiation source and dose level on physicochemical and sensory properties of cooked beef patties and pork sausages are presented in Figs. 1 and 2, respectively. The pH of cooked beef patties was unaffected by both the irradiation source and the dose level (P 40.05; Table 1), whereas a significant interaction between those main effects on the pH value of cooked pork sausages was found. The pH value of cooked pork sausages irradiated with gamma-ray and e-beam decreased with increasing absorbed dose level (P o0.05; Fig. 2a). However, the pH difference in pork sausages irradiated within 0 and 10 kGy dose level was less than 0.1 units, which might be numerically too small to affect quality characteristics of processed meat products. Similarly, previous studies reported that a change in pH of irradiated meat products had little to no impacts on their quality attributes (Luchsinger et al., 1997; Badr and Mahmoud, 2011). Redness of cooked beef patties and pork sausages was affected by both irradiation source and dose level (P o0.001; Table 1). The redness of cooked beef patties linearly decreased with increasing irradiation dose level (Po0.05; Fig. 1b); in particular, a dramatic decrease in redness of beef patties was found at e-beam irradiation. Regarding the redness of cooked pork sausages (Fig. 2b), a significant interaction between those main effects was observed (P o0.001; Table 1).Gamma-ray irradiation above 5 kGy tended to increase redness of pork sausages, whereas e-beam irradiation decreased the redness of pork sausages (Po0.05). However, X-ray irradiation over 7.5 kGy had no significant effect on redness of pork sausages (P4 0.05). This result indicates that the redness of cooked pork sausages could be differently affected by irradiation source. In general, color of irradiated meat products varies depending on irradiation doses, animal species of raw meat, muscle type, packaging type, and myoglobin concentration (Nam and Ahn, 2003; Lee and Song, 2002). Myoglobin is a pigment protein responsible for the color of meat products, and it has been suggested that carbonmonoxymyoglobin could be associated with the formation of pink color in irradiated fresh pork and poultry meat (Nam and Ahn, 2003). However, there has been no available research on color changes in processed and cooked meat products after irradiation. When nitrite is added to processed meat products, in general, nitrosyl hemochrome is a primary pigment responsible for redness development (Suman and Joseph, 2013). Thus, the decreased redness in this current study might be related to the decomposition of nitrosyl hemochrome. As well as, free radicals generated by irradiation could induce alteration of the
261
myoglobin structure, and free radicals could be generated more rapidly under high dose rate (Lee and Song, 2002; López-González et al., 2000). Thus, generative difference in free radicals between different irradiation sources might be possibly involved in the change in redness of irradiated beef patties and pork sausages. Further studies determining the effect of different irradiation sources and dose levels on nitrosyl hemochrome stability and free radical generation would be warranted to clearly elucidate color changes in processed/cooked and irradiated meat products. Hardness of cooked beef patties and pork sausages was unaffected by irradiation (P 40.05; Figs. 1c and 2c), except for pork sausages irradiated with gamma-ray. As similar results, previous studies reported that irradiation did not affect the hardness of beef or pork patties (Park et al., 2010; Lee et al., 2005). No significant interactions between irradiation source and dose level on overall acceptability of cooked beef patties and pork sausages were found (Table 1). The overall acceptability of cooked beef patties consistently decreased with increasing dose level (P o0.05), regardless of irradiation sources. In particular, an obvious decrease in the overall acceptability was observed for beef patties irradiated with gamma-ray (Fig. 1d). Similarly, the overall acceptability of cooked pork sausages steadily decreased when absorbed dose level increased (Po 0.05; Fig. 2d); however, the change in overall acceptability of pork sausages was unaffected by different irradiation sources (P 40.05; Table 1). It has been well documented that the generation of radiolytic off-flavor and odor is a main reason for the decline in sensorial acceptability of irradiated meat products (Shin et al., 2014). According to López-gonzález et al. (2000), a noticeable “cardboardy” and “soured flavor” in beef patties was produced by gamma-ray rather than e-beam irradiation, which was also consistent with our finding. 3.2. Lipid oxidation To determine the effects of irradiation source and dose level on lipid oxidation, the 2-thiobarbituric reactive substances (TBARS) value of irradiated meat products was evaluated on 0, 3, 7 and 10 days of accelerated storage at 30 °C (Table 2). Significant interactions were found among irradiation source, dose level and storage period for extent of lipid oxidation in both cooked beef patties and pork sausages (P o0.05). In particular, gamma-ray irradiation significantly increased TBARS values of cooked beef patties compared to those irradiated with e-beam or X-ray (P o0.05). In terms of pork sausages, X-ray irradiation resulted in significantly higher TBARS values, followed by gamma-ray, and e-beam (Po0.05). Hydroxyl radicals generated by ionizing irradiation are known as a factor in accelerating lipid oxidation (Smith et al., 1960). As irradiation dose increased, TBARS values for cooked beef patties and pork sausages also significantly increased (P o0.05), regardless of irradiation source. Regarding cooked pork sausages, the irradiation source and dose level represented a significant interaction (P o0.05). Numerous previous studies have indicated that the acceleration of lipid oxidation in irradiated meat products depends upon irradiation dose levels (Song et al., 2009). In this regard, our finding indicates that the extent of lipid oxidation may be differently affected by different irradiation sources at identical dose. 3.3. Microbial properties The initial total aerobic bacteria (TAB) populations in cooked beef patties and pork sausages were below the detection limit for microbial analysis (o 1 Log CFU/g), regardless of irradiation source (Table 3). The growth of TAB in beef patties was significantly suppressed by irradiation until 7 days of storage. Non-irradiated control beef patties were considered as spoiled because of the inflated packaging pouch as a sign of gas production due to growth
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20.00
6.30
a)
6.20
CIE a* (redness)
pH value
6.10 6.00 5.90 5.80
18.00 17.00 16.00 15.00 14.00
5.70
13.00
5.60
12.00
5.50
11.00 0
b)
19.00
2.5
5
7.5
10
0
2.5
Irradiation dose (kGy) 2.00
10.00
Overall acceptability
Hardness (kg)
10
d)
9.00
1.60 1.40 1.20 1.00 0.80 0.60
8.00 7.00 6.00 5.00 4.00
0.40
3.00
0.20
2.00
0.00
7.5
Irradiation dose (kGy)
c)
1.80
5
0
2.5
5
7.5
10
1.00
0
2.5
5
7.5
10
Irradiation dose (kGy)
Irradiation dose (kGy)
Fig. 1. Changes in physicochemical and sensory properties of cooked beef patties irradiated with gamma-ray, electron-beam, and X-ray. Symbols represent the mean values of each treatment, and lines indicate the prediction model of regression analysis. Treatments: gamma-ray (■), e-beam (▲), X-ray (●). Gamma-ray prediction line (∙∙∙∙∙∙∙), e-beam prediction line (- - - -), X-ray prediction line (——). Sensory evaluation for overall acceptability was conducted as 1¼ not acceptable and 10¼ very acceptable.
of bacteria on 7 days of storage (Jo et al., 2003). At the 10th day of storage, e-beam irradiated beef patties had TAB counts under the detection limit, whereas gamma-ray 2.5 kGy and X-ray 2.5, 5 kGy irradiated samples showed 5.35, 7.17, and 6.39 Log CFU/g of TAB, respectively. These results indicate that e-beam irradiation might be more effective in improving microbial safety of cooked beef patties during storage, when compared to gamma-ray or X-ray irradiation. For cooked pork sausages, irradiation over 7.5 kGy showed significant reducing effect on TAB at day 3 (P o0.05), although TAB was recovered during accelerated storage in 10 kGy X-ray irradiated samples (3.71 Log CFU/g) on the same day. Throughout the 10 days of storage, gamma-ray irradiation was more effective at decreasing TAB population of pork sausages than other irradiation sources. E-beam irradiation also significantly reduced TAB in pork sausages, dose dependently, following gamma-ray. X-ray showed less effective sterilizing effect on the TAB in the samples during the storage. Cooked pork sausages irradiated with 10 kGy gamma-ray and e-beam had no detectable TAB until the end of the accelerated storage, whereas it seemed that X-ray irradiation up to 10 kGy was not enough to eliminate TAB in cooked pork sausages. These results showed that different bactericidal effect according to ionizing
sources in each type of meat product. X-ray irradiation effect against bacteria in foods is still controversial when compared to gamma-ray or e-beam irradiation. Shin et al. (2014) and Schilling et al. (2009) reported that X-ray irradiation showed similar effects to gamma-ray and e-beam on microbial properties of meat products, while Jung et al. (2015) observed more decreased bacteria population in e-beam irradiated red pepper compared to X-ray or gamma-ray irradiation ones. Meanwhile, Chung et al. (2000) reported that gamma-ray irradiation was more effective than e-beam irradiation in the destruction of P. fluorescens in beef patties. As mentioned above, inhibitory effects of irradiation on microbial growth in irradiated meat products could be different and affected by various characteristics of meat products (additives, meat source, initial microbial load and chemical/physical properties) as well as irradiation sources (Thayer et al., 1995; Jung et al., 2015; Song et al., 2016).
4. Conclusion Our results indicate that irradiation sources differently affected the quality attributes of processed meat products, in particular the
Y.-K. Ham et al. / Radiation Physics and Chemistry 130 (2017) 259–264
10.00
6.50
a)
6.45
8.00
CIE a* (redness)
6.35
pH value
b)
9.00
6.40
6.30 6.25 6.20
7.00 6.00 5.00 4.00 3.00 2.00
6.15 6.10
1.00 0
2.5
5
7.5
0.00
10
0
2.5
Irradiation dose (kGy) 0.60
10.00
c)
7.5
10
d)
9.00
Overall acceptability
Hardness (kg)
5
Irradiation dose (kGy)
0.50 0.40 0.30 0.20 0.10 0.00
263
8.00 7.00 6.00 5.00 4.00 3.00 2.00
0
2.5
5
7.5
1.00
10
0
Irradiation dose (kGy)
2.5
5
7.5
10
Irradiation dose (kGy)
Fig. 2. Changes in physicochemical and sensory properties of cooked pork sausages irradiated with gamma-ray, electron-beam, and X-ray. Symbols represent the mean values of each treatment, and lines indicate the prediction model of regression analysis. Treatments: gamma-ray (■), e-beam (▲), X-ray (●). Gamma-ray prediction line (∙∙∙∙∙∙∙), e-beam prediction line (- - - -)X-ray prediction line (——). Sensory evaluation for overall acceptability was conducted as 1¼ not acceptable and 10 ¼very acceptable.
Table 2 Lipid oxidation (2-thiobarbituric acid reactive substances, TBARS) of cooked beef patties and pork sausages irradiated with gamma-ray, electron-beam, and X-ray during storage at 30 °C for 10 days. Storage period (days)
Control (0 kGy)
Gamma-ray (kGy)
E-beam (kGy)
SEM1
X-ray (kGy)
2.5
5
7.5
10
2.5
5
7.5
10
2.5
5
7.5
10
Cooked beef patties 0 3 7 10
0.28BCDa 0.29Ca 0.29Ca 0.24Eb
0.29BCD 0.31BCE 0.34AB 0.29D
0.31BCa 0.35ABa 0.36Aa 0.34Ba
0.32BCb 0.35ABa 0.36Aa 0.35Ba
0.45Aa 0.36Ab 0.35Ab 0.33BCb
0.28BCDa 0.31BCa 0.30Ca 0.31CDa
0.31BCa 0.31BCa 0.32ABCa 0.32BCDa
0.32BCa 0.33ABa 0.34ABa 0.35Ba
0.33Ba 0.32ABCa 0.35Aa 0.35Ba
0.25Db 0.30BCa 0.31BCa 0.32BCDa
0.27CDc 0.29Cbc 0.32ABCab 0.33BCa
0.31BCb 0.32ABCb 0.32ABCb 0.39Aa
0.31BCb 0.32ABCb 0.35ABab 0.39Aa
0.016 0.004 0.004 0.005
Cooked pork sausages 0 3 7 10
0.09Eb 0.21Ha –2 –
0.35Cb 0.55BCa – –
0.34Dd 0.55BCb 0.62BCa 0.39BCE
0.46Bb 0.59ABa 0.61BCa 0.37BCc
0.45BCE 0.58ABCb 0.64Ba 0.40Bd
0.21Db 0.28Ga 0.30Ea 0.28Ca
0.23Db 0.31FGa 0.34DEa 0.33BCa
0.30C 0.34EF 0.35D 0.32BCE
0.32C 0.36E 0.35D 0.34BCE
0.35Cc 0.45Db 0.58C 0.55Aa
0.44BCE 0.53Cb 0.64Ba 0.59Aab
0.46BCE 0.62Ab 0.70Aa 0.60Ab
0.54Ac 0.62Ab 0.71Aa 0.58Abc
0.014 0.019 0.021 0.017
A–H
Means that different letters within the same row were significantly different (po 0.05). Means that different letters within the same column were significantly different (po 0.05).
a–d
1 2
SEM: the standard error of the means. ‘–’ bar indicates no determination of total aerobic bacteria population when samples had obvious spoilage odor and slim layer.
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Table 3 Total aerobic bacteria (Log CFU/g) of cooked beef patties and pork sausages irradiated with gamma-ray, e-beam and X-ray during storage at 30 °C for 10 days. Storage period (days)
Control (0 kGy)
Gamma-ray (kGy)
E-beam (kGy)
SEMa
X-ray (kGy)
2.5
5
7.5
10
2.5
5
7.5
10
2.5
5
7.5
10
Cooked beef patties 0 3 7 10
NDb 5.89 –c –
ND ND ND 5.35
ND ND ND ND
ND ND ND ND
ND ND ND ND
ND ND ND ND
ND ND ND ND
ND ND ND ND
ND ND ND ND
ND ND ND 7.17
ND ND ND 6.39
ND ND ND ND
ND ND ND ND
0.000 0.500 0.000 0.557
Cooked pork sausages 0 3 7 10
ND 7.85 – –
ND 7.83 – –
ND 4.54 8.19 –
ND ND ND 4.60
ND ND ND ND
ND 7.55 7.97 –
ND 7.18 7.27 –
ND 3.10 6.20 6.77
ND ND ND ND
ND 7.86 – –
ND 6.89 – –
ND 6.39 7.87 –
ND 3.71 7.80 7.58
0.000 0.492 0.623 0.863
a b c
SEM: the standard error of the means. ND: not detected. ‘–’ the bar indicates no determination of total aerobic bacteria population when samples had obvious spoilage odor and slim layer.
oxidation-related characteristics (such as color and lipid oxidation). In addition, the irradiation effects could differ depending on the type of processed meat products. For better application of food irradiation technology, this current study suggests that further studies on the different effects of irradiation source on each type of processed meat products should be warranted while considering meat source, formulation and processing used for processed meat product manufacture.
Acknowledgments This research was supported by the Nuclear Research & Development Program of the Korea Science and Engineering Foundation Grant funded by the Government of the Republic of Korea (2012M2A2A6011320). The authors were also partially supported by the Brain Korea 21 Plus (BK 21 Plus) Project from the Ministry of Education and Human Resources.
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846–851. 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., 2014a. Effects of kimchi and smoking on quality characteristics and shelf life of cooked sausages prepared with irradiated pork. Meat Sci. 96, 548–553. Kim, H.W., Lee, S.Y., Hwang, K.E., Song, D.H., Kim, Y.J., Ham, Y.K., Lee, C.H., Choi, Y.S., Lee, J.W., Kim, C.J., 2014b. Effects of soy sauce and packaging method on volatile compounds and lipid oxidation of cooked irradiated beef patties. Radiat. Phys. Chem. 103, 209–212. Lacroix, M., Ouattara, B., 2000. Combined industrial processes with irradiation to assure innocuity and preservation of food products – a review. Food Res. Int. 33, 719–724. Lee, J.W., Park, K.S., Kim, J.G., Oh, S.H., Lee, Y.S., Kim, J.H., Byun, M.W., 2005. Combined effects of gamma irradiation and rosemary extract on the shelf-life of a ready-to-eat hamburger steak. Radiat. Phys. Chem. 72, 49–56. Lee, S.Y., Kim, H.W., Hwang, K.E., Song, D.H., Choi, M.S., Ham, Y.K., Choi, Y.S., Lee, J. W., Lee, S.K., Kim, C.J., 2015. Combined effect of Kimchi powder and onion peel extract on quality characteristics of emulsion sausages prepared with irradiated pork. Korean J. Food Sci. 35, 277–285. Lee, Y., Song, K.B., 2002. Effect of γ-irradiation on the molecular properties of myoglobin. J. Biochem. Mol. Biol. 35, 590–594. López-González, V., Murano, P.S., Brennan, R.E., Murano, E.A., 2000. Sensory evaluation of ground beef patties irradiated by gamma rays versus electron beam under various packaging conditions. J. Food Qual. 23, 195–204. Luchsinger, S.E., Kropf, D.H., García Zepeda, C.M., Hunt, M.C., Stroda, S.L., Mardsden, J.L., Kastner, C.L., 1997. Color and oxidative properties of irradiated ground beef patties. J. Muscle Foods 8, 445–464. Miller, R.B., 2005. Food irradiation using electron beams. In: Miller, R.B. (Ed.), Electronic Irradiation of Foods. Springer, New York, pp. 43–74. Mitchell, G.E., 1994. Irradiation preservation of meats. Food Aust. 46, 512–516. Nam, K.C., Ahn, D.U., 2003. Effects of irradiation on meat color. Food Sci. Biotechnol. 12, 198–205. Park, J.G., Yoon, Y., Park, J.N., Han, I.J., Song, B.S., Kim, J.H., Kim, W.G., Hwang, H.J., Han, S.B., Lee, J.W., 2010. Effects of gamma irradiation and electron beam irradiation on quality, sensory, and bacterial populations in beef sausage patties. Meat Sci. 85, 368–372. Roberts, P.B., 2014. Food irradiation is safe: half a century of studies. Radiat. Phys. Chem. 105, 78–82. Schilling, M.W., Yoon, Y., Todarskyy, O., Pham, A.J., Williams, R.C., Marshall, D.L., 2009. Effects of ionizing irradiation and hydrostatic pressure on Escherichia coli O157: H7 inactivation, chemical composition, and sensory acceptability of ground beef patties. Meat Sci. 81, 705–710. Shin, M.H., Lee, J.W., Yoon, Y.M., Kim, J.H., Moon, B.G., Kim, J.H., Song, B.S., 2014. Comparison of quality of bologna sausage manufactured by electron beam or X-ray irradiated ground pork. Korean J. Food Sci. Anim. 34, 464–471. Smith, N.L., Tinsley, I.J., Bubl, C.E., 1960. The thiobarbituric acid test in irradiation sterilized beef. Food Technol. 14, 317–320. Song, B.S., Park, J.G., Kim, W.G., Kim, J.H., Choi, J.I., Yoon, Y., Byun, M.W., Kim, C.J., Lee, J.W., 2009. Comparison of the quality of gamma ray- or electron beamirradiated minced pork and pork patties. Korean J. Food Sci. Anim 29, 194–202. Song, B.S., Lee, Y., Moon, B.G., Go, S.M., Park, J.H., Kim, J.K., Jung, K., Kim, D.H., Ryu, S. R., 2016. Comparison of bactericidal efficiency of 7.5 MeV X-rays, gamma-rays, and 10 MeV e-beams. Radiat. Phys. Chem. 125, 106–108. Suman, S.P., Joseph, P., 2013. Myoglobin chemistry and meat color. Annu. Rev. Food Sci. Technol. 4, 79–99. Tarladgis, B.G., Watts, B.M., Younathanm, M.T., Dugan, L., 1960. A distillation method for the quantitative determination of malonaldehyde in rancid foods. J. Am. Oil Chem. Soc. 37, 44–52. Thayer, D.W., Boyd, G., Fox, J.B., Lakritz, H., Hampson, J.W., 1995. Variations in radiation sensitivity of foodborne pathogens associated with suspending meat. J. Food Sci. 60, 63–67.
Contents lists available at ScienceDirect
Radiation Physics and Chemistry journal homepage: www.elsevier.com/locate/radphyschem
Effects of irradiation source and dose level on quality characteristics of processed meat products Youn-Kyung Ham a, Hyun-Wook Kim b, Ko-Eun Hwang a, Dong-Heon Song a, Yong-Jae Kim a, Yun-Sang Choi c, Beom-Seok Song d, Jong-Heum Park d, Cheon-Jei Kim a,n a
Department of Food science and Biotechnology of Animal Resources, Konkuk University, Seoul 143-701, Republic of Korea Meat Science and Muscle Biology Laboratory, Department of Animal Science, Purdue University, West Lafayette IN 47907, USA c Research Group of Convergence Technology, Korean Food Research Institute, Seongnam 463-746, Republic of Korea d Team for Radiation Food Science & Biotechnology, Advanced Radiation Technology Institute, Korea Atomic Energy Research Institute, Jeongeup 580-185, Republic of Korea b
H I G H L I G H T S
The effect of three irradiation source and dose level on meat products was studied. The redness was significantly influenced by irradiation sources and dose levels. Lipid oxidation, and microbial properties also affected by irradiation sources.
art ic l e i nf o
a b s t r a c t
Article history: Received 6 July 2016 Received in revised form 29 August 2016 Accepted 4 September 2016 Available online 5 September 2016
The effect of irradiation source (gamma-ray, electron-beam, and X-ray) and dose levels on the physicochemical, organoleptic and microbial properties of cooked beef patties and pork sausages was studied, during 10 days of storage at 30 71 °C. The processed meat products were irradiated at 0, 2.5, 5, 7.5, and 10 kGy by three different irradiation sources. The pH of cooked beef patties and pork sausages was unaffected by irradiation sources or their doses. The redness of beef patties linearly decreased with increasing dose level (P o0.05), obviously by e-beam irradiation compared to gamma-ray and X-ray (P o0.05). The redness of pork sausages was increased by gamma-ray irradiation, whereas it decreased by e-beam irradiation depending on absorbed dose level. No significant changes in overall acceptability were observed for pork sausages regardless of irradiation source (P4 0.05), while gamma-ray irradiated beef patties showed significantly decreased overall acceptability in a dose-dependent manner (Po 0.05). Lipid oxidation of samples was accelerated by irradiation depending on irradiation sources and dose levels during storage at 30 °C. E-beam reduced total aerobic bacteria of beef patties more effectively, while gamma-ray considerably decreased microbes in pork sausages as irradiation dose increased. The results of this study indicate that quality attributes of meat products, in particular color, lipid oxidation, and microbial properties are significantly influenced by the irradiation sources. & Published by Elsevier Ltd.
Keywords: Irradiation Beef patty Pork sausage X-ray Gamma-ray Electron-beam
1. Introduction Three irradiation sources, namely gamma-ray, electron-beam (e-beam), and X-ray approved for food irradiation by Codex Alimentarius Commission (2003), have been practically used to ensure microbial safety of meat and meat products even under unrefrigerated storage conditions (Roberts, 2014). With such evident advantage, it has been reported that irradiation could negatively
n
Corresponding author. E-mail address: [email protected] (C.-J. Kim).
http://dx.doi.org/10.1016/j.radphyschem.2016.09.010 0969-806X/& Published by Elsevier Ltd.
impact color, oxidative stability (particularly lipid oxidation), and sensory palatability, depending on the meat source, packaging methods, and irradiation conditions (Brewer, 2004). Gamma-ray and e-beam have been extensively used in not only commercial food sterilizing process but also scientific research determining quality changes in irradiated meat products (Lacroix and Ouattara, 2000). However, most consumers are still reluctant to purchase gamma-ray irradiated food due to their negative perceptions on the use of radioisotopes (Eustice and Bruhn, 2013). In terms of e-beam irradiation, the low penetration power of e-beam has been noted with locational variation in the irradiation effects on food
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system. (Miller, 2005). In this regard, X-ray irradiation has received a great attention as an effective means of food irradiation source with some advantages compared gamma-ray and e-beam. The major benefits of X-ray irradiation could be summarized as follows; 1) convenient operation of mechanical system, 2) higher productivity by reducing processing time, and 3) no generation of radioactive waste. In addition, the penetration power of X-ray irradiation is comparable to gamma-ray irradiation (Cleland and Stichelbaut, 2013). Thus, it has been anticipated that X-ray irradiation could be one of ways to considerably improve the negative perception of consumers on irradiated foods (Mitchell, 1994) and to overcome the technical limitations of e-beam irradiation. For these reasons, recent researches have evaluated the effects of the three irradiation sources on quality characteristics of several foods, for better application of food irradiation technology (Jung et al., 2015; Song et al., 2016). Although the effects of gamma-ray and e-beam irradiations on quality characteristics of meat products have been compared (López-González et al., 2000; Luchsinger et al., 1997; Park et al., 2010), there has been little information on the effects of the three irradiation sources on the quality characteristics of processed meat products at different absorbed dose levels. Therefore, the objective of this study was to evaluate the effects of irradiation source and dose levels on physicochemical, microbial and sensory properties of cooked beef patties and pork sausages.
2. Materials and methods 2.1. Sample preparation Cooked beef patties and pork sausages were manufactured according to the methods described by Kim et al. (2014b) and Lee et al. (2015), respectively. Beef patties were composed of 80% ground beef (M. semitendinosus), 15% pork back fat and 5% ice water. As additives, 1.2% nitrite picking salt (NaCl: sodium nitrite¼99.4:0.6), 0.05% sodium triphosphate, 1% sugar, 1% isolated soy protein, 0.1% pepper, 0.1% garlic powder, 0.1% ginger powder, 0.1% onion powder, 0.1% mixed spice (Nuremberg, Raps GmbH & Co., Kulmbach, Germany), and 0.05% L-ascorbic acid were added, based on total sample weight. Raw beef patties were cooked in a 15071 °C convention oven until the internal core temperature reached 7571 °C. Pork sausages were manufactured with 60% ground pork ham (M. biceps femoris, semitendinosus and semimembranosus), 20% pork back fat and 20% ice. The raw materials were emulsified with 1.2% nitrite picking salt, 0.3% sodium triphosphate, 0.5% sugar, 1% isolated soy protein, and 0.4% mixed spice (Bockwurst, Raps GmbH & Co., Kulmbach, Germany) in a bowl cutter. Meat batter was stuffed into collagen casing (#240, NIPPI Inc., Tokyo, Japan; approximately 25 mm diameter), and the pork sausages were cooked in a 75 71 °C smoke chamber for 40 min until the internal core temperature reached 72 71 °C. After cooling for 1 h, all cooked samples were individually vacuum-packaged with nylon/polyethylene bags (15 20 cm; thickness, 0.07 cm; 2 ml O2/m2/24 h at 0 °C) and stored in a 4 °C refrigerator for one day until irradiation process.
Ottawa, Canada) at the Korea Atomic Energy Research Institute (Jeongeup, Korea) with source strength of approximately 11.1 PBq, at dose rate of 10 kGy/h. E-beam and X-ray irradiation were performed using an ELV-4 electron beam accelerator (10 MeV) and X-ray linear accelerator (7.5 MeV) at the EB-Tech Co. (Daejeon, Korea), respectively. E-beam and X-ray irradiation were performed with a beam current of 1 mA and dose rate of 2.9 kGy/s and 5 kGy/ h, respectively. For dosimetry of samples, alanine dosimeters (5 mm diameter; Bruker Instruments, Bremen, Germany) were attached to the top and bottom of the samples, respectively. Subsequent to irradiation, the absorbed dose was measured with an electron paramagnetic resonance analyzer in accordance with international standards (ISO/ASTM 51607, 2004). The dose uniformity ratios (min/max ratios) of all irradiation sources were less than 1.2 and the actual dose was within 75% of the target dose. After irradiation, the irradiated samples were analyzed for quality characteristics on the day and stored in a 30 71 °C incubator for 10 days, to determine changes in lipid oxidation stability and microbial properties under the accelerated storage condition (Park et al., 2010). 2.3. Analysis of quality characteristics The pH values of the samples were determined using an electronic pH meter (Model 340; Mettler-Toledo GmbH, Schwerzenbach, Switzerland) (Lee et al., 2015). The CIE a*(redness) of samples was measured using a colorimeter (Chroma Meter CR-210; Konica Minolta, Osaka, Japan) (Lee et al., 2015). The hardness of beef patties and pork sausages were measured using a texture analyzer (TA-XT2i, Stable Micro System Ltd., Godalming, Surrey, UK) in accordance with the method of Choi et al. (2015). The sensory evaluation for overall acceptability (1 ¼not acceptable and 10 ¼very acceptable) was conducted by 12 trained panels (Kim et al., 2014a); the sample preparation and evaluation procedure were followed by AMSA research guidelines (2015). Lipid oxidation of samples was determined at 0, 3, 7 and 10 days of storage according to the modified TBARS method of Tarladgis et al. (1960) described by Kim et al. (2014b). Total aerobic bacteria and coliform bacteria were determined at 0, 3, 7 and 10 days of storage, using plate count agar and 3 M-Petrifilm E. coli/coliform count plates, respectively (Kim et al., 2014a; AOAC International, 2005). All measurements were conducted in triplicate. 2.4. Statistical analysis Experimental design was a completely randomized design with three independent batches. Analysis of variance (ANOVA) was performed on all the variables measured using the general linear model (GLM) procedure with SPSS software (SPSS Inc., Chicago, IL, USA, 2008). When significant differences were found, Duncan's multiple-range test was used to compare mean values among treatments at a significance level of 95%. Furthermore, simple linear regression analysis for each ionizing source was conducted to determine the level of relationship between the irradiation dose and analyzed variables.
3. Results and discussion 2.2. Irradiation procedure 3.1. Physicochemical and sensory properties The vacuum-packaged beef patties (approximately 15 mm thickness) and pork sausages (approximately 25 mm thickness) were irradiated at five absorbed dose levels of 0 (control), 2.5, 5, 7.5 or 10 kGy using three irradiation sources under the ambient temperature of 22 72 °C. Gamma-ray irradiation was conducted in a cobalt-60 irradiator (100 kCi, AECL, IR-79, MDS Nordion Inc.,
The significances of main effects, irradiation source and absorbed dose level, and their interaction, on physicochemical and sensory properties of cooked beef patties and pork sausages are shown in Table 1. No interactions between those main effects on all measurements of cooked beef patties were found (P 40.05),
Y.-K. Ham et al. / Radiation Physics and Chemistry 130 (2017) 259–264
Table 1 Significance of main effects and their interaction on physicochemical and sensory properties of cooked beef patties and pork sausages. Main effects and their interaction Cooked beef patties Ionizing source effect (I) Irradiation dose effect (D) Interaction (I D) Cooked pork sausages Ionizing source effect (I) Irradiation dose effect (D) Interaction (I D)
pH CIE a* (redness)
Hardness Sensory acceptability
NS
***
NS
***
NS
***
NS
***
NS
NS
NS
NS
***
***
*
NS
***
***
NS
***
***
***
NS
NS
NS, non-significance. *
p o 0.05. p o 0.001.
***
whereas the pH and CIE a* (redness) of cooked pork sausages were influenced by their interaction (P o0.05). The effects of irradiation source and dose level on physicochemical and sensory properties of cooked beef patties and pork sausages are presented in Figs. 1 and 2, respectively. The pH of cooked beef patties was unaffected by both the irradiation source and the dose level (P 40.05; Table 1), whereas a significant interaction between those main effects on the pH value of cooked pork sausages was found. The pH value of cooked pork sausages irradiated with gamma-ray and e-beam decreased with increasing absorbed dose level (P o0.05; Fig. 2a). However, the pH difference in pork sausages irradiated within 0 and 10 kGy dose level was less than 0.1 units, which might be numerically too small to affect quality characteristics of processed meat products. Similarly, previous studies reported that a change in pH of irradiated meat products had little to no impacts on their quality attributes (Luchsinger et al., 1997; Badr and Mahmoud, 2011). Redness of cooked beef patties and pork sausages was affected by both irradiation source and dose level (P o0.001; Table 1). The redness of cooked beef patties linearly decreased with increasing irradiation dose level (Po0.05; Fig. 1b); in particular, a dramatic decrease in redness of beef patties was found at e-beam irradiation. Regarding the redness of cooked pork sausages (Fig. 2b), a significant interaction between those main effects was observed (P o0.001; Table 1).Gamma-ray irradiation above 5 kGy tended to increase redness of pork sausages, whereas e-beam irradiation decreased the redness of pork sausages (Po0.05). However, X-ray irradiation over 7.5 kGy had no significant effect on redness of pork sausages (P4 0.05). This result indicates that the redness of cooked pork sausages could be differently affected by irradiation source. In general, color of irradiated meat products varies depending on irradiation doses, animal species of raw meat, muscle type, packaging type, and myoglobin concentration (Nam and Ahn, 2003; Lee and Song, 2002). Myoglobin is a pigment protein responsible for the color of meat products, and it has been suggested that carbonmonoxymyoglobin could be associated with the formation of pink color in irradiated fresh pork and poultry meat (Nam and Ahn, 2003). However, there has been no available research on color changes in processed and cooked meat products after irradiation. When nitrite is added to processed meat products, in general, nitrosyl hemochrome is a primary pigment responsible for redness development (Suman and Joseph, 2013). Thus, the decreased redness in this current study might be related to the decomposition of nitrosyl hemochrome. As well as, free radicals generated by irradiation could induce alteration of the
261
myoglobin structure, and free radicals could be generated more rapidly under high dose rate (Lee and Song, 2002; López-González et al., 2000). Thus, generative difference in free radicals between different irradiation sources might be possibly involved in the change in redness of irradiated beef patties and pork sausages. Further studies determining the effect of different irradiation sources and dose levels on nitrosyl hemochrome stability and free radical generation would be warranted to clearly elucidate color changes in processed/cooked and irradiated meat products. Hardness of cooked beef patties and pork sausages was unaffected by irradiation (P 40.05; Figs. 1c and 2c), except for pork sausages irradiated with gamma-ray. As similar results, previous studies reported that irradiation did not affect the hardness of beef or pork patties (Park et al., 2010; Lee et al., 2005). No significant interactions between irradiation source and dose level on overall acceptability of cooked beef patties and pork sausages were found (Table 1). The overall acceptability of cooked beef patties consistently decreased with increasing dose level (P o0.05), regardless of irradiation sources. In particular, an obvious decrease in the overall acceptability was observed for beef patties irradiated with gamma-ray (Fig. 1d). Similarly, the overall acceptability of cooked pork sausages steadily decreased when absorbed dose level increased (Po 0.05; Fig. 2d); however, the change in overall acceptability of pork sausages was unaffected by different irradiation sources (P 40.05; Table 1). It has been well documented that the generation of radiolytic off-flavor and odor is a main reason for the decline in sensorial acceptability of irradiated meat products (Shin et al., 2014). According to López-gonzález et al. (2000), a noticeable “cardboardy” and “soured flavor” in beef patties was produced by gamma-ray rather than e-beam irradiation, which was also consistent with our finding. 3.2. Lipid oxidation To determine the effects of irradiation source and dose level on lipid oxidation, the 2-thiobarbituric reactive substances (TBARS) value of irradiated meat products was evaluated on 0, 3, 7 and 10 days of accelerated storage at 30 °C (Table 2). Significant interactions were found among irradiation source, dose level and storage period for extent of lipid oxidation in both cooked beef patties and pork sausages (P o0.05). In particular, gamma-ray irradiation significantly increased TBARS values of cooked beef patties compared to those irradiated with e-beam or X-ray (P o0.05). In terms of pork sausages, X-ray irradiation resulted in significantly higher TBARS values, followed by gamma-ray, and e-beam (Po0.05). Hydroxyl radicals generated by ionizing irradiation are known as a factor in accelerating lipid oxidation (Smith et al., 1960). As irradiation dose increased, TBARS values for cooked beef patties and pork sausages also significantly increased (P o0.05), regardless of irradiation source. Regarding cooked pork sausages, the irradiation source and dose level represented a significant interaction (P o0.05). Numerous previous studies have indicated that the acceleration of lipid oxidation in irradiated meat products depends upon irradiation dose levels (Song et al., 2009). In this regard, our finding indicates that the extent of lipid oxidation may be differently affected by different irradiation sources at identical dose. 3.3. Microbial properties The initial total aerobic bacteria (TAB) populations in cooked beef patties and pork sausages were below the detection limit for microbial analysis (o 1 Log CFU/g), regardless of irradiation source (Table 3). The growth of TAB in beef patties was significantly suppressed by irradiation until 7 days of storage. Non-irradiated control beef patties were considered as spoiled because of the inflated packaging pouch as a sign of gas production due to growth
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20.00
6.30
a)
6.20
CIE a* (redness)
pH value
6.10 6.00 5.90 5.80
18.00 17.00 16.00 15.00 14.00
5.70
13.00
5.60
12.00
5.50
11.00 0
b)
19.00
2.5
5
7.5
10
0
2.5
Irradiation dose (kGy) 2.00
10.00
Overall acceptability
Hardness (kg)
10
d)
9.00
1.60 1.40 1.20 1.00 0.80 0.60
8.00 7.00 6.00 5.00 4.00
0.40
3.00
0.20
2.00
0.00
7.5
Irradiation dose (kGy)
c)
1.80
5
0
2.5
5
7.5
10
1.00
0
2.5
5
7.5
10
Irradiation dose (kGy)
Irradiation dose (kGy)
Fig. 1. Changes in physicochemical and sensory properties of cooked beef patties irradiated with gamma-ray, electron-beam, and X-ray. Symbols represent the mean values of each treatment, and lines indicate the prediction model of regression analysis. Treatments: gamma-ray (■), e-beam (▲), X-ray (●). Gamma-ray prediction line (∙∙∙∙∙∙∙), e-beam prediction line (- - - -), X-ray prediction line (——). Sensory evaluation for overall acceptability was conducted as 1¼ not acceptable and 10¼ very acceptable.
of bacteria on 7 days of storage (Jo et al., 2003). At the 10th day of storage, e-beam irradiated beef patties had TAB counts under the detection limit, whereas gamma-ray 2.5 kGy and X-ray 2.5, 5 kGy irradiated samples showed 5.35, 7.17, and 6.39 Log CFU/g of TAB, respectively. These results indicate that e-beam irradiation might be more effective in improving microbial safety of cooked beef patties during storage, when compared to gamma-ray or X-ray irradiation. For cooked pork sausages, irradiation over 7.5 kGy showed significant reducing effect on TAB at day 3 (P o0.05), although TAB was recovered during accelerated storage in 10 kGy X-ray irradiated samples (3.71 Log CFU/g) on the same day. Throughout the 10 days of storage, gamma-ray irradiation was more effective at decreasing TAB population of pork sausages than other irradiation sources. E-beam irradiation also significantly reduced TAB in pork sausages, dose dependently, following gamma-ray. X-ray showed less effective sterilizing effect on the TAB in the samples during the storage. Cooked pork sausages irradiated with 10 kGy gamma-ray and e-beam had no detectable TAB until the end of the accelerated storage, whereas it seemed that X-ray irradiation up to 10 kGy was not enough to eliminate TAB in cooked pork sausages. These results showed that different bactericidal effect according to ionizing
sources in each type of meat product. X-ray irradiation effect against bacteria in foods is still controversial when compared to gamma-ray or e-beam irradiation. Shin et al. (2014) and Schilling et al. (2009) reported that X-ray irradiation showed similar effects to gamma-ray and e-beam on microbial properties of meat products, while Jung et al. (2015) observed more decreased bacteria population in e-beam irradiated red pepper compared to X-ray or gamma-ray irradiation ones. Meanwhile, Chung et al. (2000) reported that gamma-ray irradiation was more effective than e-beam irradiation in the destruction of P. fluorescens in beef patties. As mentioned above, inhibitory effects of irradiation on microbial growth in irradiated meat products could be different and affected by various characteristics of meat products (additives, meat source, initial microbial load and chemical/physical properties) as well as irradiation sources (Thayer et al., 1995; Jung et al., 2015; Song et al., 2016).
4. Conclusion Our results indicate that irradiation sources differently affected the quality attributes of processed meat products, in particular the
Y.-K. Ham et al. / Radiation Physics and Chemistry 130 (2017) 259–264
10.00
6.50
a)
6.45
8.00
CIE a* (redness)
6.35
pH value
b)
9.00
6.40
6.30 6.25 6.20
7.00 6.00 5.00 4.00 3.00 2.00
6.15 6.10
1.00 0
2.5
5
7.5
0.00
10
0
2.5
Irradiation dose (kGy) 0.60
10.00
c)
7.5
10
d)
9.00
Overall acceptability
Hardness (kg)
5
Irradiation dose (kGy)
0.50 0.40 0.30 0.20 0.10 0.00
263
8.00 7.00 6.00 5.00 4.00 3.00 2.00
0
2.5
5
7.5
1.00
10
0
Irradiation dose (kGy)
2.5
5
7.5
10
Irradiation dose (kGy)
Fig. 2. Changes in physicochemical and sensory properties of cooked pork sausages irradiated with gamma-ray, electron-beam, and X-ray. Symbols represent the mean values of each treatment, and lines indicate the prediction model of regression analysis. Treatments: gamma-ray (■), e-beam (▲), X-ray (●). Gamma-ray prediction line (∙∙∙∙∙∙∙), e-beam prediction line (- - - -)X-ray prediction line (——). Sensory evaluation for overall acceptability was conducted as 1¼ not acceptable and 10 ¼very acceptable.
Table 2 Lipid oxidation (2-thiobarbituric acid reactive substances, TBARS) of cooked beef patties and pork sausages irradiated with gamma-ray, electron-beam, and X-ray during storage at 30 °C for 10 days. Storage period (days)
Control (0 kGy)
Gamma-ray (kGy)
E-beam (kGy)
SEM1
X-ray (kGy)
2.5
5
7.5
10
2.5
5
7.5
10
2.5
5
7.5
10
Cooked beef patties 0 3 7 10
0.28BCDa 0.29Ca 0.29Ca 0.24Eb
0.29BCD 0.31BCE 0.34AB 0.29D
0.31BCa 0.35ABa 0.36Aa 0.34Ba
0.32BCb 0.35ABa 0.36Aa 0.35Ba
0.45Aa 0.36Ab 0.35Ab 0.33BCb
0.28BCDa 0.31BCa 0.30Ca 0.31CDa
0.31BCa 0.31BCa 0.32ABCa 0.32BCDa
0.32BCa 0.33ABa 0.34ABa 0.35Ba
0.33Ba 0.32ABCa 0.35Aa 0.35Ba
0.25Db 0.30BCa 0.31BCa 0.32BCDa
0.27CDc 0.29Cbc 0.32ABCab 0.33BCa
0.31BCb 0.32ABCb 0.32ABCb 0.39Aa
0.31BCb 0.32ABCb 0.35ABab 0.39Aa
0.016 0.004 0.004 0.005
Cooked pork sausages 0 3 7 10
0.09Eb 0.21Ha –2 –
0.35Cb 0.55BCa – –
0.34Dd 0.55BCb 0.62BCa 0.39BCE
0.46Bb 0.59ABa 0.61BCa 0.37BCc
0.45BCE 0.58ABCb 0.64Ba 0.40Bd
0.21Db 0.28Ga 0.30Ea 0.28Ca
0.23Db 0.31FGa 0.34DEa 0.33BCa
0.30C 0.34EF 0.35D 0.32BCE
0.32C 0.36E 0.35D 0.34BCE
0.35Cc 0.45Db 0.58C 0.55Aa
0.44BCE 0.53Cb 0.64Ba 0.59Aab
0.46BCE 0.62Ab 0.70Aa 0.60Ab
0.54Ac 0.62Ab 0.71Aa 0.58Abc
0.014 0.019 0.021 0.017
A–H
Means that different letters within the same row were significantly different (po 0.05). Means that different letters within the same column were significantly different (po 0.05).
a–d
1 2
SEM: the standard error of the means. ‘–’ bar indicates no determination of total aerobic bacteria population when samples had obvious spoilage odor and slim layer.
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Table 3 Total aerobic bacteria (Log CFU/g) of cooked beef patties and pork sausages irradiated with gamma-ray, e-beam and X-ray during storage at 30 °C for 10 days. Storage period (days)
Control (0 kGy)
Gamma-ray (kGy)
E-beam (kGy)
SEMa
X-ray (kGy)
2.5
5
7.5
10
2.5
5
7.5
10
2.5
5
7.5
10
Cooked beef patties 0 3 7 10
NDb 5.89 –c –
ND ND ND 5.35
ND ND ND ND
ND ND ND ND
ND ND ND ND
ND ND ND ND
ND ND ND ND
ND ND ND ND
ND ND ND ND
ND ND ND 7.17
ND ND ND 6.39
ND ND ND ND
ND ND ND ND
0.000 0.500 0.000 0.557
Cooked pork sausages 0 3 7 10
ND 7.85 – –
ND 7.83 – –
ND 4.54 8.19 –
ND ND ND 4.60
ND ND ND ND
ND 7.55 7.97 –
ND 7.18 7.27 –
ND 3.10 6.20 6.77
ND ND ND ND
ND 7.86 – –
ND 6.89 – –
ND 6.39 7.87 –
ND 3.71 7.80 7.58
0.000 0.492 0.623 0.863
a b c
SEM: the standard error of the means. ND: not detected. ‘–’ the bar indicates no determination of total aerobic bacteria population when samples had obvious spoilage odor and slim layer.
oxidation-related characteristics (such as color and lipid oxidation). In addition, the irradiation effects could differ depending on the type of processed meat products. For better application of food irradiation technology, this current study suggests that further studies on the different effects of irradiation source on each type of processed meat products should be warranted while considering meat source, formulation and processing used for processed meat product manufacture.
Acknowledgments This research was supported by the Nuclear Research & Development Program of the Korea Science and Engineering Foundation Grant funded by the Government of the Republic of Korea (2012M2A2A6011320). The authors were also partially supported by the Brain Korea 21 Plus (BK 21 Plus) Project from the Ministry of Education and Human Resources.
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