MEAT SCIENCE Meat Science 67 (2004) 643–649 www.elsevier.com/locate/meatsci Temperature abuse affects the quality of irradiated pork loins M.J. Zhu a, A. Mendonca b, D.U. Ahn b a,* a Department of Animal Science, Iowa State University, 2276 Kildee, Ames, IA 50011-3150, USA Department of Food Science and Human Nutrition, Iowa State University, 2312 Food Science Building, Ames, IA 50011-3150, USA Received 25 September 2003; accepted 9 January 2004 Abstract The influence of temperature abuse on the quality of irradiated pork loins was investigated. Pork loins were obtained directly from a local packing plant, sliced and vacuum-packaged. Pork loins were randomly separated into 3 groups, sliced, and assigned to receive 0, 1.5, or 2.5 kGy electron-beam irradiation. Then, each chop was further cut into three equal pieces and assigned to three temperature treatments: Trt I was placed in a refrigerator directly after irradiation; Trt II was left at room temperature for 3 h before refrigeration; and Trt III was exposed at room temperature for 1 h three consecutive days with intermittent storage at 4 °C between exposures. Before irradiation, each loin pieces were vacuum-packaged. Color, 2-thiobarbituric acid reactive substances (TBARS), and volatiles were measured after 0, 14, 28 and 42 days of storage, and water-holding capacity and sensory characteristics of the loins were measured after 0, 14 and 28 days of storage. Temperature abuse had no significant effect on color, oxidation, and volatiles of irradiated pork loins. However, temperature abuse improved water-holding capacity of meat, which could be caused by the accelerated hydrolysis of muscle proteins at higher temperature. Irradiation increased redness, sulfur contents in volatiles and offodor of pork loin. Off-odor and redness induced by irradiation sustained during storage. Among sulfur compounds, the content of dimethyl disulfide decreased gradually while the level of thiourea remained relatively constant. Irradiation also increased water loss, which might be related to the structural damage in membrane during irradiation. This study shows that temperature abuse has little effect on the quality of irradiated pork. Ó 2004 Elsevier Ltd. All rights reserved. Keywords: Pork loin; Water-holding capacity; Color; Volatiles; Temperature fluctuation; Irradiation 1. Introduction During large-scale distribution and handling of meat, especially in export of meat to foreign markets, there are numerous opportunities for meat to be temperature abused. These opportunities include loading and unloading of meat at shipping ports and subsequent transportation by trucks (refrigerated or unrefrigerated) to retail outlets where the meat has to be unloaded again and stacked for storage. Therefore, it is inevitable for meat products to be exposed to fluctuating temperatures during irradiation, transportation and subsequent storage, which may promote the growth of microorganism * Corresponding author. Tel.: +1-515-294-6595; fax: +1-515-2949143. E-mail address: duahn@iastate.edu (D.U. Ahn). 0309-1740/$ - see front matter Ó 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2004.01.005 including pathogens and accelerate quality changes in meat (Labuza & Fu, 1995). Reducing the incidence of foodborne pathogens and decreasing the numbers of microorganisms in meat products is a major objective of many meat processor in the United States. Irradiation is an attractive method to eliminate pathogens in meat products, but changes color and generates irradiation off-odor (Ahn, Jo, & Olson, 2000). In order to minimize quality change, low irradiation dosage is frequently used in meat processing. The bacteriocidal action of ionizing irradiation is largely linked to damage of bacterial DNA from the production of free radicals during the irradiation process some bacteria in meat products can repair the damage, and recover and proliferate during product transport and storage, especially during temperature abuse (Lee, Sebranek, Olson, & Dickson, 1996). Lucht, Blank, and Borsa (1998) demonstrated that a temperature of 14–22 °C is optimal for the recovery of irradiation-injured pathogens. 644 M.J. Zhu et al. / Meat Science 67 (2004) 643–649 Our study showed that the temperature abuse greatly accelerated the growth of Listeria monocytogenesis in ready-to-eat turkey meat products (Bisha, Mendonca, Sebranek, & Dickson, 2003). Apart from the proliferation of microorganisms in meat, fluctuating temperature accelerates a number of enzymatic and chemical reactions that can influence the shelf life of irradiated meat. Exposure of meat to increased temperature conditions undoubtedly accelerates proteases activity to breakdown muscle protein into small molecular weight peptides, and long term storage of meat is often associated with extensive softening of meat and color change independent of microorganism (Gill, 1996; Tewari, Jayas, & Holley, 1999). Lipid oxidation may also be accelerated under the elevated temperature conditions. However, no information on quality changes in irradiated meat by temperature abuse is currently available. Since two most frequent temperature abuses are delay at room temperature after irradiation and temperature fluctuation during transporting products from one location to another, meats were treated with a 3-h exposure to room temperature after irradiation and 1 h per day for three consecutive days of exposure to room temperature to simulate temperature fluctuation conditions in industry. To avoid the quality changes caused by microbial growth, the pork loins used in this study were directly purchased from a local packing plant where loins were dissected under strict hygiene conditions. A great care was taken to avoid microbial contamination during transportation and further packing. The objective of this study was to determine the effect of temperature fluctuation on the quality of irradiated pork loins. 2. Materials and methods III) were exposed at room temperature for 1 h three consecutive days with intermittent storage at 4 °C between exposures. In each step of meat handling, care was taken to avoid microbial contamination. Loin pieces were vacuum-packaged individually in low oxygen-permeable bags (nylon/polyethylene, 9.3 mL O2 /m2 /24 h at 0 C; Koch, Kansas City, MO) before irradiation. The energy and power level used for irradiation were 10 MeV and 10 kW, respectively, and the average dose rate was 88.3 kGy/min. To confirm the target dose, 2 alanine dosimeters per cart were attached on the top and bottom surface of a sample. The alanine dosimeter was read using a 104 Electron Paramagnetic Resonance Instrument (Bruker Instruments Inc., Billerica, MA, USA). The range of actual dosage for 1.5 kGy was 1.414–1.810 kGy and the range for 2.5 kGy was 2.34–3.12 kGy. Color, volatiles and lipid oxidation were analyzed after 0, 14, 28 and 42 days of storage, and water-holding capacity and sensory characteristics were evaluated after 0, 14, and 28 days of storage. 2.2. Water-holding capacity Measurement of water-holding capacity was performed by centrifugation method (Bertram, Andersen, & Karlsson, 2001). Samples were cut parallel to the muscle fiber direction, which is about 2.0 cm long and 0.5 0.2 cm in cross-sectional area. The samples were weighed and placed in test tubes with a filter paper (Whatman No. 1) cushion. The tube was sealed with parafilm then centrifuged at 400g at 4 °C for 60 min. After centrifugation the sample were weighed again. Water-holding capacity was calculated as the percentage of the difference in weight before and after centrifugation. Two meat samples were taken from each loin piece and the average data was used for statistical analysis. 2.1. Sample preparation 2.3. Color measurement Twelve pork loins fabricated under strict hygienic conditions were obtained directly from a local packing plant. Chops from three different loins were pooled and used as one replication. The upper portion of each loin was sliced into 2.5-cm thick chops for water-holding capacity measurement. The rest was sliced to 1.0-cmthick chops and the chops were used for color, volatiles and 2-thiobarbituric acid reactive substances (TBARS) assays. Chops within each replication were randomly separated into three groups, and each group was assigned to receive 0, 1.5, or 2.5 kGy electron-beam irradiation using a Linear Accelerator (Circe IIIR; Thomson CSF Linac, Saint-Aubin, France). Each chop within a group was further cut into three equal pieces to make three sub-groups: one sub-group were refrigerated (4 °C) immediately after irradiation (Trt I); another subgroup was kept at room temperature (22 °C) for 3 h before refrigeration (Trt II); and the last sub-group (Trt The surface color of sliced pork loins was measured in package using a Hunter LabScan Colorimeter (Hunter Laboratory, Inc., Reston, VA) that had been calibrated against black and white reference tiles covered with the same packaging materials as used for samples. The CIE L (lightness), a (redness), and b (yellowness) values were obtained using an illuminant A (light source). Two color readings were taken from each side of a sliced loin. 2.4. 2-Thiobarbituric acid reactive substances measurement Five grams of minced loin were weighed into a 40-mL test tube and homogenized with 50 lL butylated hydroxyanisole (7.2%) and 15 mL of deionized distilled water (DDW) using a Polytron homogenizer (Type PT M.J. Zhu et al. / Meat Science 67 (2004) 643–649 10/35, Brinkman Instruments Inc., Westbury NY, USA) for 15 s at high speed. One milliliter of the meat homogenate was transferred to a disposable test tube (13 100 mm) and then thiobarbituric acid/trichloroacetic acid (15 mM TBA/15% TCA, 2 mL) was added. The mixture was vortex mixed and incubated in a boiling water bath for 15 min to develop color. The sample was cooled in cold water for 10 min, mixed again using a vortex mixer, and centrifuged for 15 min at 2500g at 4 °C. The absorbance of the resulting supernatant solution was determined at 531 nm against a blank containing 1 mL of DDW and 2 mL of TBA/TCA solution. The amounts of TBARS were expressed as milligrams of malonaldehyde per kilogram of meat. 2.5. Volatiles analysis A purge-and-trap dynamic headspace GC/MS system was used to identify and quantify the volatiles compounds. Three grams of minced loin meat was put in a 40-mL sample vial and flushed with helium gas (99.999%). After capping with a Teflon-lined, openmouth cap, the vial was placed in a refrigerated (4 °C) sample tray. Samples were purged at 40 °C with helium gas (40 mL/min) for 11 min. Volatiles were trapped with a Tenax/charcoal/silica trap column at 20 °C, desorbed for 2 min at 220 °C, concentrated using a cryofocusing unit at –90 °C, then desorbed into a GC column for 60 s at 220 °C. An HP-624 column (15 m, 250 lm i.d., 1.4 lm nominal), an HP-1 column (60 m, 250 lm i.d., 0.25 lm nominal), and an HP-Wax column (7.5 m, 250 lm i.d., 0.25 lm nominal) were combined using zero-volume connectors and used for volatiles analysis. A ramped oven temperature was used: the initial oven temperature was set at 0 °C for 2.5 min, then increased to 10 °C at 5 °C/min, to 45 °C at 10 °C/min, to 110 °C at 20 °C/min, to 210 °C at 10 °C/min, and held for 2.5 min. Liquid nitrogen was used to cool the oven below ambient temperature. Helium was the carrier gas at constant pressure of 22 psi. A mass selective detector (MSD) was used to identify and quantify volatiles compounds in irradiated samples. The ionization potential of MS will be 70 eV, scan range was between 19.1 and 350 m=z. The identification of volatiles was achieved by comparing mass spectral data with those of the Wiley Library. The peak area was reported as the amount of volatiles released (Ahn, Jo, Du, Olson, & Nam, 2000). 2.6. Sensory evaluation sensory characteristics and was assigned a score ranging from 1 (none) to 9 (extremely strong), respectively. All samples were labeled with random three-digit numbers and presented randomly to panelists. 2.7. Statistical analysis A split-plot design was used in this study. Chops from different loins were first split into three irradiation dosages, and then individual chops were cut into three pieces and assigned to three temperature treatments. Data were processed by the general linear model (GLM) of statistical analysis system (SAS, 2000). The differences in the mean values were compared by the Tukey’s multiple range test, and mean values and standard error of the means (SEM) were reported (P < 0:05). 3. Results and discussion 3.1. Water-holding capacity Water-holding capacity is an important quality characteristic of pork loins. These results demonstrated that irradiation significantly increased the loss of water from loins (Table 1). For the control samples with no temperature abuse (Trt I), both irradiation at 1.5 and Table 1 Water-holding capacity influenced by irradiation and treatments of pork loins Characteristics Trt I Trt II Trt III 0 kGy 1.5 kGy 2.5 kGy 0 day 8.1b 11.3a 10.9a 8.9b 10.2a 10.0a – – – SEM 0.9 0.9 – 0 kGy 1.5 kGy 2.5 kGy 14 day 8.1bx 9.0ab 10.2ax 8.6x 10.0 9.9x 6.4y 8.6 6.8y 0.5 0.9 0.8 SEM 0.5 0.6 0.4 2.3 0 kGy 1.5 kGy 2.5 kGy 28 day 5.7b 6.4ab 8.0ax 7.4 6.9 6.2y 6.0 6.3 6.4y 0.6 0.7 0.4 SEM 0.6 0.6 0.6 x;y Twelve trained sensory panelists characterized the smell of irradiated loins under different temperature fluctuation. Panelists were trained to familiarize with irradiation odor, the scale to be used, and the range of intensities likely to be encountered during the study. A 9-point category scale was used to describe the 645 SEM 0.5 1.2 0.9 Means within a row with different superscript differ significantly ðP < 0:05Þ; n ¼ 4. a–c Means within a column with different superscript differ significantly (P < 0:05). Trt I, refrigerated immediately after irradiation; Trt II, kept at room temperature for 3 h before refrigerated storage; Trt III, were exposed at room temperature for 1 h at three consecutive days with intermittent storage at 4 °C between exposures. 646 M.J. Zhu et al. / Meat Science 67 (2004) 643–649 2.5 kGy significantly increased centrifugation loss compared to that of non-irradiated samples. This result is in agreement with a previous report about increased centrifugation loss and reduced water-holding capacity of pork chops after irradiation (Zhao & Sebranek, 1996). The mechanism for irradiation-induced centrifugation loss in pork loins is not clear, but two possible theories exist: (1) irradiation may damage the integrity of membrane structure of muscle fibers (Lakritz, Carroll, Jenkins, & Maerker, 1987) and (2) irradiation may denature the muscle proteins, thus lowering waterholding capacity (Lynch, Macfie, & Mead, 1991). After 14 days of refrigerated storage, samples from three consecutive days of exposure to room temperature (Trt III) had lower centrifugation loss than other treatments (Table 1). Since the meat used in this study is at postrigor stage, the water-holding capacity of meat is gradually improving during storage due to hydrolysis of muscle proteins. Therefore, the improved water-holding capacity observed in this study could be due to accelerated hydrolysis of proteins during temperature abuse, since high temperature increases protease activity (DeTable 2 Color a of pork loin effected by irradiation and treatments after storage Irradiation dose Trt I Trt II Trt III 0 kGy 1.5 kGy 2.5 kGy 0 day 13.0b 14.6a 15.2ay 13.2c 14.3b 15.6ax – – – SEM 0.4 0.2 – 0 kGy 1.5 kGy 2.5 kGy 14 day 12.8b 15.1ax 15.9a 12.6c 14.1by 16.8a 12.5c 14.5bxy 15.9a SEM 0.3 0.3 0.4 0 kGy 1.5 kGy 2.5 kGy 28 day 14.4b 15.5a 16.2a 14.6b 15.5a 15.9a 13.3b 16.1a 16.3a SEM 0.3 0.2 0.4 0 kGy 1.5 kGy 2.5 kGy 42 day – 14.9b 16.1a – 15.3 16.0 – 14.7b 16.3a SEM 0.3 0.4 0.2 a–c SEM 0.4 0.2 0.1 0.3 0.2 0.3 0.4 0.3 0.3 – 0.3 0.3 Means within a column with different superscript differ significantly ðP < 0:05Þ; n ¼ 4. x;y Means within a row with different superscript differ significantly ðP < 0:05Þ. Trt I, refrigerated immediately after irradiation; Trt II, kept at room temperature for 3 h before refrigerated storage; Trt III, were exposed at room temperature for 1 h at three consecutive days with intermittent storage at 4 °C between exposures. vine, Wahlgren, & Tornberg, 1999). During storage, water-holding capacity increased for all loins with various irradiation doses and temperature treatments (Table 1). This may also be due to the hydrolysis of muscle proteins during storage, a continuation of the postmortem changes in muscle (Koohmaraie, 1994). 3.2. Color values and TBARS values As shown in Table 2, irradiated samples have higher redness (a value) than control samples, which is in agreement with the previous results (Ahn et al., 2000). Temperature abuse had no effect on the redness of pork loin. No significant changes in redness occurred during storage. As for lightness (L value) and yellowness (b value), no changes were observed for both temperature abuses and during storage (data not shown). Overall, the temperature fluctuations had no effect on the color values of irradiated pork loins. Temperature fluctuation, irradiation and storage had little influence on TBARS of pork loins (data not shown). Minimal irradiation and temperature fluctuation effects on TBARS were expected because the loin chops were vacuumed packaged. Table 3 Irradiation off-odor as influenced by irradiation and treatments of pork loins Irradiation dose Trt I Trt II Trt III 0 kGy 1.5 kGy 2.5 kGy 0 day 1.5b 5.7a 6.0a 1.4b 6.2a 7.0a – – – SEM 0.4 0.5 – 0 kGy 1.5 kGy 2.5 kGy 14 day 1.3b 6.9a 7.1a 1.5c 5.6b 7.6a 1.7b 6.8a 7.3a SEM 0.4 0.3 0.5 0 kGy 1.5 kGy 2.5 kGy 28 day 1.4c 6.2b 7.3a 1.2b 5.4a 6.3a 1.7b 4.7a 5.7a SEM 0.4 0.5 0.6 a;b SEM 0.3 0.6 0.6 0.3 0.4 0.5 0.4 0.5 0.6 Means within a row with different superscript differ significantly ðP < 0:05Þ; n ¼ 12. Trt I, refrigerated immediately after irradiation; Trt II, kept at room temperature for 3 h before refrigerated storage; Trt III, were exposed at room temperature for 1 h at three consecutive days with intermittent storage at 4 °C between exposures. Twelve trained sensory panelists characterized the smell of irradiated loins stored under different temperature conditions. A 9-point category scale was used to describe the sensory characteristics and was assigned a score ranging from 1 (none) to 9 (extremely strong), respectively. M.J. Zhu et al. / Meat Science 67 (2004) 643–649 50 45 40 35 30 25 20 15 10 5 0 Thiourea contentin volatiles of 0 kGy irradiated prok loins 10000 Trt 1 Trt 2 Trt 3 0 14 28 Thiourea content (x10 4) Ion counts (x10000) Dimethyl disulfide in volatiles of 0 kGy irradiated pork loins 42 Trt 1 8000 Trt 2 6000 Trt 3 4000 2000 0 -2000 0 Storage (days) trt1 7000 6000 5000 Trt 2 Trt 3 4000 3000 2000 2000 0 0 14 28 28 42 Thiourea content in volatiles of 2 kGy irradiated pork loins 30000 Thiourea content (x10 4) 9000 8000 14 Storage (day) Dimethyl disulfide in volatiles of 1.5 kGy irradiated pork loins Ion counts (x10000) 647 Trt 1 25000 Trt 2 20000 Trt 3 15000 10000 5000 0 42 0 Storage (days) 14 28 42 Storage (day) 20000 18000 16000 14000 12000 10000 8000 6000 4000 2000 0 Thiourea content involatiles of 3 kGy irradiated prokloins Trt 1 Trt 2 Trt 3 0 14 28 42 Storage (days) Fig. 1. Effects of temperature fluctuation and storage on dimethyl disulfide contents (104 counts) in volatiles of pork loins under different irradiation conditions. Trt I, pork loins were refrigerated (4 °C) immediately after irradiation; Trt II, irradiated pork loins were kept at room temperature (22 °C) for 3 h before refrigeration; Trt III, after irradiation, pork loins were exposed at room temperature for 1 h three consecutive days with intermittent storage at 4 °C between exposures. Pork chops were irradiated at 0, 1.5 or 2.5 kGy. Volatiles were analyzed after storage at 4 °C for 0, 14, 28, and 42 days. A purge-and-trap dynamic headspace GC/MS system was used to identify and quantify the volatiles compounds. A mass selective detector (MSD) was used to identify and quantify volatiles compounds in irradiated samples. The identification of volatiles was achieved by comparing mass spectral data with those of the Wiley Library. The peak area (104 ion counts) was reported as the amount of volatiles released (n ¼ 4). 60000 Thiourea content (x10 4) Ion counts (x10000) Dimethyl disulfide involatilesof 2.5 kGy irradiated porkloins Trt 1 50000 Trt 2 40000 Trt 3 30000 20000 10000 0 0 14 28 42 Storage (day) Fig. 2. Effects of temperature fluctuation during storage on thiourea content (104 counts) in irradiated pork loins. Trt I, pork loins were refrigerated (4 °C) immediately after irradiation; Trt II, irradiated pork loins were kept at room temperature (22 °C) for 3 h before refrigeration; Trt III, after irradiation, pork loins were exposed at room temperature for 1 h three consecutive days with intermittent storage at 4 °C between exposures. Pork chops were irradiated at 0, 1.5 or 2.5 kGy. Volatiles were analyzed after storage at 4 °C for 0, 14, 28, and 42 days. A purgeand-trap dynamic headspace GC/MS system was used to identify and quantify the volatiles compounds. A mass selective detector (MSD) was used to identify and quantify volatiles compounds in irradiated samples. The identification of volatiles was achieved by comparing mass spectral data with those of the Wiley Library. The peak area (104 ion counts) was reported as the amount of volatiles released (n ¼ 4). 648 M.J. Zhu et al. / Meat Science 67 (2004) 643–649 3.3. Sensory evaluation and volatiles analysis Irradiation induced strong off-odor (Table 3). After irradiation, off-odor intensity increased from around 1.5 points to above 5 points on a 9-point scale. This irradiation off-odor was a pungent, cooked corn like odor that has been reported in previous research (Ahn et al., 2000; Du, Hur, & Ahn, 2002). Temperature fluctuation and storage had no significant effect on irradiation off-odor (Table 3). Irradiation induces sulfur-containing volatiles, which are the main compounds for irradiation off-odor (Du et al., 2002; Kim, Nam, & Ahn, 2002). Dimethyl disulfide was almost undetectable in non-irradiated samples, but the amount of dimethyl disulfide dramatically increased after irradiation (Fig. 1). During storage, the content of dimethyl disulfide gradually reduced and became barely detectable after 28 days of storage (Fig. 1). This suggested that dimethyl disulfide might not be the only sulfur volatile contributing to irradiation offodor because strong irradiation off-odor was still apparent by sensory panelists after 28 days of storage (Table 3). However, no significant amounts of other sulfur volatiles were detected in this study. In another study, dimethyl disulfide content was shown constant in volatiles of irradiated vacuum-packaged pork during storage (Ahn, Nam, Du, & Jo, 2001). Irradiation odor seems to be more related to thiourea content in volatiles than other sulfur compounds (Fig. 2). After 42 days of storage, significant amounts of thiourea still remained in meat. This result was in agreement with the sensory data where a sulfur-like offodor was noted (Table 3). Thiourea content in volatiles enhanced greatly by irradiation, and increased slightly after 14 days refrigerated storage before decreasing at 42 days of storage (Fig. 2). There was no overall difference in thiourea content among different temperature fluctuation. Combining with sensory evaluation data, this result showed that temperature abuse did not influence the irradiation off-odor of pork loins. 4. Conclusion Mild temperature fluctuation had minor effect on color, oxidation, and volatiles of irradiated pork loins. However, temperature fluctuation improved waterholding capacity of meat. Irradiation increased redness, sulfur contents in volatiles and off-odor of pork loins. During storage, the content of dimethyl disulfide decreased gradually while the level of thiourea remained relatively constant. 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