127 Journal of Food Protection, Vol. 77, No. 1, 2014, Pages 127–132 doi:10.4315/0362-028X.JFP-13-242 Copyright G, International Association for Food Protection
Research Note
Influence of Modified Atmosphere Packaging on Meat Quality Parameters of Turkey Breast Muscles INES BLACHA, CARSTEN KRISCHEK,*
AND
¨ NTER KLEIN GU
Institute of Food Quality and Food Safety, Foundation University of Veterinary Medicine, D-30173 Hannover, Germany MS 13-242: Received 14 June 2013/Accepted 3 September 2013
ABSTRACT Poultry meat is often stored in modified atmosphere packaging (MAP) or vacuum packaging to improve consumer acceptance and shelf life. The aim of this study was to determine how different packaging conditions influence meat quality. Therefore, in three independent experiments, turkey breast muscle cutlets were packaged either in vacuum or in different modified atmosphere mixtures (80% O2, 20% CO2 [MAP 1]; 80% N2, 20% CO2 [MAP 2]; and 20% O2, 20% CO2, 60% N2 [MAP 3]) and stored for 12 days at 3uC. Color, pH, electrical conductivity, total viable counts, and Pseudomonas species were determined on days 1, 4, 8, and 12 of storage. On the same days, samples were collected for analysis of thiobarbituric acid– reactive substance and total volatile basic nitrogen concentrations. Sensory parameters and liquid loss were determined on days 4, 8, and 12. Vacuum-packaged meat had the highest liquid loss and lowest sensory results. MAP 1–packaged meat showed the highest sensory, redness, and thiobarbituric acid–reactive substance values. MAP 2–packaged meat had lower sensory values. MAP 3–packaged meat had lower redness and sensory values, especially at the end of storage. The study showed an impact of the packaging condition on different quality parameters, with a small advantage for storage of turkey cutlets in high-oxygen packages.
A large amount of poultry meat is purchased in cut-up parts that can be prepared quickly at home, because time for cooking preparation plays an essential role in consumers’ buying behavior (10, 23). These products are more susceptible to deterioration, and indicators like microbiological quality or the amounts of total volatile basic nitrogen (TVB-N) or thiobarbituric acid–reactive substances (TBARS) could be used for spoilage analysis (6). Moreover, poultry meat is often stored in modified atmosphere packaging (MAP) with high oxygen concentrations (8). An important advantage of this MAP storage is the extended shelf life of meat due to reduction of spoilage (10). Furthermore, meat in MAP positively influences consumers’ decisions during self-service purchase due to its bright red appearance (5). However, highoxygen packaging is also associated with negative aspects like increased levels of lipid oxidation (11) and the risk of uncontrolled oxygen release in the packaging unit that may be accompanied with combustion/burst and oxygen toxicity (2). In contrast to that, oxygen-free storage increases the risk for growth of anaerobic bacteria, such as Clostridium species (15). As data about MAP storage-related alterations of highly processed products in poultry are few, the objective of the present study was the analysis of quality changes in sliced turkey pieces stored for up to 12 days in high-oxygen (80%), low-oxygen (20%) and oxygen-free MAP, as well as * Author for correspondence. Tel: z495118567617; Fax: z49511856827617; E-mail: [email protected].
in vacuum packaging. The analysis considered microbiological and physicochemical parameters to obtain a comprehensive picture regarding the shelf life and spoilage of meat. MATERIALS AND METHODS Meat sampling. On three different days, 72 cutlets were obtained from a slaughterhouse each day, cut from breast muscles of commercial fast-growing turkey toms (Aviagen Turkeys Ltd., Chester, UK) approximately 12 h after slaughter and transported to our laboratory at 3uC within 2 h. Twenty-four hours after slaughter (day 1), microbiological samples were taken to determine the initial microbial status of the turkey meat. Then, approximately 70-g samples were cut from each cutlet, homogenized with a Grindomix homogenizer (Typ GM200, Retsch, Haan, Germany) and frozen at 220uC for analysis of TBARS and TVB-N concentrations. Subsequently, the remaining cutlet pieces were weighed (101.6 ¡ 18.6 g) and pH and electrical conductivity (EC) values were determined. The meat was then randomly subdivided to the four different packaging methods. The cutlets were packaged in polypropylene trays (ES Plastic GmbH & Co. KG, Passau, Germany) in high-oxygen (80% O2, 20% CO2 [MAP 1]) and oxygen-free (80% N2, 20% CO2 [MAP 2]) atmospheres, as well as in low-oxygen (20% O2, 60% N2, 20% CO2 [MAP 3]) atmosphere or in vacuum. Each tray contained two cutlets and was sealed with a Multivac t100 packaging machine (Sepp Haggenmueller GmbH & Co. KG, Wolfertschwerden, Germany) using polyethylene-ethylene vinyl alcohol-polypropylene transparent layers with high impermeability to O2 and CO2 (permeability: O2, 1.5 cm3/m2 d [day] bar at 23uC and 35% relative humidity [RH]; CO2, 5.5 cm3/m2 d bar at 23uC and 35% RH; and
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N2, 1 cm3/m2 d bar at 23uC and 35% RH) (SUEDPACK GmbH & Co. KG, Ochsenhausen, Germany). After packaging, the lightness (L*) and redness (a*) values of the meat were determined, followed by storage of all packages in the dark at 3uC. On days 4, 8, and 12, the analysis of color was repeated. At the same time points, three packages for each packaging method were chosen for analysis and thereby excluded from further storage. After opening and immediate sensory testing, samples were collected from every cutlet for microbiological analysis, and liquid loss was estimated after weighing. Subsequently, EC and pH were determined and the remaining piece of cutlet was used for TBARS and TVB-N analyses. These samples were stored as described above. Gas mixture analysis. The oxygen (O2) and carbon dioxide (CO2) concentrations of the MAP were analyzed with a CheckMate 9900 O2/CO2 (PBI-Dansensor A/S, Ringsted, Denmark) by inserting the needle through a gas-tight septum (PBI Dansensor). After analysis, another septum was stuck onto the first one to prevent gas leakage through the injection site during further storage. The O2 and CO2 contents were analyzed on days 1, 6, and 12 in all packages of MAP 1, 2, and 3 opened on day 12 of storage. pH, EC, color, and liquid loss. pH was measured using a portable pH meter (Knick Portamess, Knick GmbH, Berlin, Germany) equipped with a glass electrode (InLab 427, MettlerToledo, Urdorf, Switzerland). The EC (mS/cm) was measured with a portable EC meter (LF Star, Mattha¨us GmbH, Nobitz, Germany). The L* and a* values were determined with a colorimeter (Minolta CR-400, Minolta GmbH, Langenhagen, Germany) through the transparent film. Prior to the color analysis, the packages were turned, thereby considering direct contact of the meat with the film during measurement. Each L* and a* value was an average of four determinations. For liquid loss analysis, cutlets were dried carefully using a cloth and reweighed. This weight, after adding 5 g (microbial sample weight), and the initial cutlet weight, determined on day 1, were used to calculate the percentage of liquid loss. Microbiology. On day 1, before packaging, 2 g of each cutlet was collected and six meat samples were pooled. On days 4, 8, and 12, 5 g per cutlet was removed from every package for microbiological analysis, and the two samples from the same package were pooled for analysis. The 12-g (day 1) and 10-g (days 4, 8, and 12) samples were transferred, respectively, to 100 or 120 ml of sterile saline solution with peptone (0.85% NaCl, 0.1% peptone) and homogenized (Seward Stomacher 400 circulator, Seward Ltd., West Sussex, UK) for 2 min 30 s. Dilutions were prepared extending from 1:101 (bacterial solution to saline solution and peptone) to 1:104 referring to expected bacterial growth results. The dilutions were spread in duplicate on two different media: plate count nutrient agar (Merck KGaA, Darmstadt, Germany) for analysis of total viable count (TVC) and Pseudomonas agar base CM559 with selective cetrimide-fucidin-cephalosporin supplement (SR0151, Oxoid Deutschland GmbH, Wesel, Germany) for quantitative analysis of all Pseudomonas species. The plate count nutrient agar plates were incubated for 72 h at 30uC, and the Pseudomonas agar plates for 48 h at 30uC. Counts were expressed as log CFU per gram of meat. TBARS. The TBARS content was determined according to the method of Popp et al. (19). All experiments were performed in triplicate. To calculate the TBARS content, a standard curve with
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malondialdehyde (Merck KGaA) in the range of 0 to 1.0 mg/ml was prepared. The results were expressed in milligrams of malondialdehyde per kilogram of sample. TVB-N. The TVB-N content was determined and calculated according to European Commission regulation (EC) no. 2074/2005 (9). A Vapodest (C. Gerhardt GmbH & Co. KG, Koenigswinter, Germany) was used for analysis. TVB-N was calculated by multiplying the volume of titrated hydrochloric acid by 2.8. The results were expressed in milligrams of TVB-N per 100 g of meat. Sensory analysis. On days 4, 8, and 12, a trained panel of three persons (two female and one male) evaluated the appearance and odor of the meat samples immediately after the packages were opened. Depending on the aberrations in quality, points from 1 (unsatisfactory, not acceptable) to 5 (very good, no aberration in quality) could be given for both categories. The appearance points were multiplied by 3 and summated with the odor results. The sum was divided by 10 (maximum sensory points, 2.0). Chemicals. All chemicals were purchased from Applichem GmbH, Darmstadt, Germany, unless otherwise indicated. Statistical analysis. The data were analyzed using Statistica 10.0 software (StatSoft, Hamburg, Germany) with ‘‘packaging variant’’ (vacuum, MAP 1, MAP 2, and MAP 3) as the independent variable. The Shapiro-Wilk test was used to ensure that the data were normally distributed. Normally distributed data were analyzed using analysis of variance and the Tukey post hoc test. Non-normally distributed data (liquid loss, TBARS, and sensory analysis) were analyzed with the Mann-Whitney U test. A probability error of 0.05 was taken into account.
RESULTS AND DISCUSSION The results of gas analysis are shown in Figure 1. Comparable (P . 0.05) O2 and CO2 concentrations were observed in high-oxygen-packaged meat (MAP 1) over the whole storage period. The O2 contents in the high-nitrogen packages (MAP 2) increased significantly (P # 0.05) between days 1 and 12, whereas the day 6 results were comparable to those of the other days. The CO2 concentrations decreased between days 1 and 6. The day 12 results were comparable to the carbon dioxide amounts on the other days. The low-oxygen packages (MAP 3) only showed significantly (P # 0.05) decreasing O2 contents between days 6 and 12. The CO2 contents were comparable on all storage days. Various results concerning changes of gas composition were observed in other studies. For example, Irkin et al. (12) observed a decrease in oxygen content and, hence, an increase in the percentage of carbon dioxide during storage of minced beef meat. Al-Nehlawi et al. (1) observed an initial decrease in CO2 concentration during storage of chicken drumsticks that was followed by comparable CO2 concentrations during the following days. For oxygen, no significant (P . 0.05) differences in head space composition were observed. During storage of pig longissimus muscle slices in modified atmosphere, Pfeiffer and Menner (18) observed an initial decrease of CO2 content followed by an increase in the CO2 percentage. Changes in gas composition within the MAP are influenced by factors like soluting of the CO2, consumption of the O2 by the respiratory
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FIGURE 1. Least squares means (LSM) and standard deviations of the oxygen (O2) and carbon dioxide (CO2) concentrations in the modified atmosphere packaging (MAP 1, 80% O2, 20% CO2; MAP 2, 80% N2, 20% CO2; MAP 3, 20% O2, 60% N2, 20% CO2) on days 1, 6, and 12 of storage. LSM with different letters between days within the same parameter and packaging variant differ significantly (P # 0.05).
activity of the meat or microorganisms, and permeation of the gases through the transparent layer (18). The pH values were comparable between the different packaging variants, except on day 4. At this time point, MAP 1–stored products showed significantly (P # 0.05) lower pH values than the products stored in MAP 3. The vacuum- and MAP 2–stored meat had pH values comparable to the MAP 1 and MAP 3 results (Table 1). The pH results mainly agree with those of Martı´nez et al. (13), who could not observe any pH differences during storage of fresh pork sausages in low- and high-oxygen packages or in oxygen-free packages. In contrast to that, Mastromatteo et al. (14) observed lower pH values for the low-oxygen variant than for the high-oxygen variant in poultry. A reason for this difference might be that, in the study of Mastromatteo et al. (14), the low-oxygen packages had
higher CO2 concentrations than the high-oxygen packages. If CO2 solutes in water, forming carbonic acid, pH values usually decrease. The turkey meat stored in the different packaging variants did not differ significantly in terms of EC, except on day 4. MAP 3 meat had significantly (P # 0.05) lower EC values than the MAP 1 and MAP 2 products. Vacuumpackaged turkey meat had EC results similar to those of MAP 1, 2, and 3 (Table 1). The EC values in our study could be related to the appropriate pH values, especially in MAP 1 and MAP 3. The faster pH decrease results in pronounced shrinkage and denaturation of the myofibrillar proteins, accompanied by accelerated release of water and electrolytes (22). This causes higher EC values of the low-pH meat (24). On days 4, 8, and 12, vacuum-packaged meat had significantly (P # 0.05) higher liquid loss values than the
TABLE 1. LSM and standard deviations of pH and EC results for turkey meat depending on packaging method and storage time a LSM ¡ SD Parameter
Day
Vacuum packaging
pH
4 8 12 4 8 12
5.75 5.72 5.72 7.79 8.12 8.81
EC
a
¡ ¡ ¡ ¡ ¡ ¡
0.06 0.08 0.06 0.72 0.73 0.7
AB
AB
MAP 1
5.71 5.73 5.73 8.07 8.47 8.87
¡ ¡ ¡ ¡ ¡ ¡
0.08 0.05 0.04 0.91 0.92 0.62
MAP 2 B
A
5.76 5.73 5.73 8.33 8.84 8.91
¡ ¡ ¡ ¡ ¡ ¡
0.09 0.06 0.09 0.69 0.97 0.88
MAP 3 AB
A
5.80 5.72 5.77 7.30 8.66 9.26
¡ ¡ ¡ ¡ ¡ ¡
0.13 0.08 0.12 1.04 0.98 0.46
A
B
LSM, least squares means; MAP 1, 80% O2, 20% CO2; MAP 2, 80% N2, 20% CO2; MAP 3, 20% O2, 60% N2, 20% CO2; EC, electrical conductivity in mS/cm. LSM with different letters within a row differ significantly (P # 0.05); n ~ 18 cutlets per packaging method.
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other packaging variants on days 1, 4, and 8 of storage. On days 1 and 4, the results for the vacuum, MAP 2, and MAP 3 turkey cutlets were comparable, but on day 8, the a* values of the MAP 3 meat had decreased significantly (P # 0.05) compared with the values for the other stored products. On day 12, the MAP 3 meat had significantly (P # 0.05) lower a* values than the otherwise-comparable a* results of the other packaging variants (Table 2). The higher L* values of MAP 1 meat than of vacuumstored products, as well as the difference between MAP 1 and MAP 3, are supported by the results of Go´mez and Lorenzo (11). However, Mastromatteo et al. (14) found no L* differences between vacuum-, high-oxygen-, and lowoxygen-packaged poultry patties. With regard to the a* results, the higher a* results in the high-oxygen packages presented here mainly agree with the data of Sante et al. (21) in turkey meat, especially the presented reduction of the a* in the oxygen-containing packages during further storage. In contrast to our study, Bingol and Ergun (4) found in ostrich meat comparable a* results for high- and low-oxygen packages up to day 5, followed by a decrease in the highoxygen-stored products. The TVCs of MAP 1 meat on day 4 were significantly (P # 0.05) lower than the TVCs of the vacuum and MAP 2 variants, whereas the MAP 3 meat showed values comparable to those of all other variants. On day 8, MAP 1–stored meat showed significantly (P # 0.05) lower TVCs than vacuum- and MAP 3–stored products, whereas the MAP 2 meat had values comparable to those of all other variants. On day 12, no significant TVC differences were found between all packaging variants (Fig. 3). Concerning the Pseudomonas species, no differences (P . 0.05) were observed between the different packaging variants on days 4, 8, and 12. The amounts of Pseudomonas species ranged between 2.86 log CFU/g (day 1) and 4.68 log CFU/g (day 12) (data not shown). Rajkumar et al. (20) also observed lower TVCs for turkey meat packaged in 80% O2 than for vacuum-stored products during advanced storage (days 14 and 21), and Coventry et al. (7) found lower TVCs in high-oxygen- than in high-nitrogen-packaged beef after 2 to 6 weeks. However,
FIGURE 2. Least squares means (LSM) and standard deviations (n ~ 18) for liquid loss of turkey meat depending on packaging variant and storage time. LSM with different letters on the same day differ significantly (P # 0.05).
MAP products. Turkey meat in MAP 1, 2, and 3 showed comparable liquid loss results on all days (Fig. 2). Rajkumar et al. (20) also observed higher liquid loss in vacuumpackaged turkey meat than in products stored in highoxygen atmosphere. The higher drip loss might be due to greater physical compression by the vacuum-packaging procedure (17). On day 1, the L* values were higher (P # 0.05) in the MAP 1 samples than in the other packages. The MAP 2 meat had significantly (P # 0.05) lower L* values than meat in the other packaging variants, whereas vacuum and MAP 3 products showed comparable L* values. On days 4 and 8, MAP 3 meat had the highest L* values, differing from meat in all other packaging variants. The results for the MAP 1 cutlets lay between the results of the other packaging variants, differing (P # 0.05) from all other variants on day 4 and from vacuum and MAP 3 meat on day 8. On days 4 and 8, the vacuum and MAP 2 products had comparable L* values. The L* values were determined to be comparable between all packaging variants on day 12 (Table 2). On all days, MAP 1 meat had the highest a* values, differing significantly (P # 0.05) from the results of the
TABLE 2. LSM and standard deviations of lightness and redness results of turkey meat, determined through the packaging film, depending on packaging method and storage time a LSM ¡ SD Parameter
Day
Vacuum packaging
L*
1 4 8 12 1 4 8 12
50.49 49.76 50.13 50.52 3.61 3.63 3.81 3.89
a*
a
¡ ¡ ¡ ¡ ¡ ¡ ¡ ¡
1.99 2.17 1.62 2.20 0.69 0.72 0.69 0.70
B C C
B B B A
MAP 1
51.19 50.99 51.22 51.48 4.65 4.97 4.60 4.26
¡ ¡ ¡ ¡ ¡ ¡ ¡ ¡
1.94 1.65 1.55 1.50 1.01 1.00 1.09 1.06
MAP 2 A B B
A A A A
49.40 49.95 50.45 51.14 3.77 3.90 4.10 4.12
¡ ¡ ¡ ¡ ¡ ¡ ¡ ¡
2.12 1.75 1.74 1.37 0.89 0.91 0.74 0.70
MAP 3 C C BC
B B B A
50.31 51.88 52.15 52.29 3.83 3.90 3.08 2.36
¡ ¡ ¡ ¡ ¡ ¡ ¡ ¡
1.79 1.72 1.87 3.56 0.97 0.79 1.12 1.42
B A A
B B C B
LSM, least squares means; MAP 1, 80% O2, 20% CO2; MAP 2, 80% N2, 20% CO2; MAP 3, 20% O2, 20% CO2, 60% N2; L*, lightness; a*, redness. LSM with different letters within a row differ significantly (P # 0.05). Numbers of cutlets per packaging method: days 1 and 4, n ~ 54; day 8, n ~ 36; day 12, n ~ 18.
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VACUUM AND MODIFIED ATMOSPHERE STORAGE OF TURKEY MEAT
FIGURE 3. Least squares means (LSM) and standard deviations (n ~ 9) for total viable counts (TVC) of turkey meat depending on packaging variant and storage time. LSM with different letters on the same day differ significantly (P # 0.05).
Mastromatteo et al. (14) found higher TVCs in highoxygen- than in low-oxygen- and vacuum-packaged poultry patties on days 6 and 8 of storage. The Pseudomonas species results presented here are mainly in accordance with those of Bingol and Ergun (4), who did not mention differences between low- and high-oxygenstored ostrich meat, and Coventry et al. (7), who mentioned maximal values of about 104 CFU/cm22 in nitrogenpackaged meat after 6 weeks of storage. However, Mastromatteo et al. (14) determined different Pseudomonas contents in vacuum-, low-oxygen-, and high-oxygenpackaged poultry patties. The high-oxygen packages had the highest values on days 3 to 8. Balamatsia et al. (3) observed lower values for vacuum-packaged than for lowoxygen-packaged broiler breast muscles. On days 4 and 12, MAP 1 meat had significantly (P # 0.05) higher TBARS results than all other packaging variants. On day 4, the vacuum-packaged meat had lower (P # 0.05) TBARS values than the MAP 3 products, whereas the MAP 2 results only differed (P # 0.05) from the MAP 1 values. Vacuum, MAP 2, and MAP 3 meat showed comparable values on day 12. On day 8, no significant differences were observed between all packaging variants (Fig. 4). The effect of intensified lipid oxidation due to higher oxygen concentration in the surrounding atmosphere has already been described (13). However, there are also reports in which no difference in TBARS values in packaging variants with various oxygen contents is stated (16). Considering the TVB-N concentrations of the meat, no significant (P . 0.05) effects of the different packaging variants could be ascertained in our study. The values ranged between 27.04 mg/100 g of meat (day 1) and 28.20 mg/100 g of meat (day 12) (data not shown). Fraqueza et al. (10) also did not find significant differences of TVB-N concentrations in turkey meat packaged with 50% CO2 or 50% N2, but they determined a positive correlation between TVB-N content and Pseudomonas species. However, Balamatsia et al. (3) found lower TVB-N values of MAP-stored than of vacuumstored chicken breasts and, in addition, observed a positive relation between microbial and TVB-N values.
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FIGURE 4. Least squares means (LSM) and standard deviations (n ~ 18) for thiobarbituric acid–reactive substances (TBARS) of turkey meat depending on packaging variant and storage time. LSM with different letters on the same day differ significantly (P # 0.05).
On all days (days 4, 8, and 12), MAP 1 meat showed significantly (P # 0.05) higher sensory values and, therefore, better appearance and odor results than all other variants. The vacuum, MAP 2, and MAP 3 stored meat had comparable results on day 4, but not during further storage. On day 8, vacuum-packaged meat showed significantly (P # 0.05) lower sensory results than the otherwise-comparable values of the MAP 2 and MAP 3 products, whereas on day 12, the values in MAP 3 meat dropped to the lowest sensory results, differing significantly (P # 0.05) from the MAP 2- but not the vacuum-packaged turkey cutlets (data not shown). Balamatsia et al. (3) showed during 15 days of storage that vacuum- in relation to low-oxygen-packaged chicken meat had worse sensory results at the end of storage and not at the beginning, as in the present study. In contrast to the present study, Rajkumar et al. (20) found better odor results in vacuum-packaged than in high-oxygen-stored turkey meat. In conclusion, in the present study, a high-oxygen atmosphere was advantageous for packaging, considering the different interests of consumers and food producers. Whereas the consumer is mainly influenced by color and other sensory aspects of meat, for food producers, shelf life is an important feature. High-oxygen-containing packages were rated better concerning consumers’ interests despite their higher TBARS values and had no disadvantages from the food producers’ point of view. The high-nitrogen variant might be an alternative, having satisfying results for most parameters, but provides a less-attractive appearance. ACKNOWLEDGMENTS This study was funded by the Ahrberg Foundation, Hannover, Germany. The authors gratefully acknowledge Bettina Engel-Abe´ and Manuela von Ahlen and all the people participating the time-consuming meat collections and analyses.
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Research Note
Influence of Modified Atmosphere Packaging on Meat Quality Parameters of Turkey Breast Muscles INES BLACHA, CARSTEN KRISCHEK,*
AND
¨ NTER KLEIN GU
Institute of Food Quality and Food Safety, Foundation University of Veterinary Medicine, D-30173 Hannover, Germany MS 13-242: Received 14 June 2013/Accepted 3 September 2013
ABSTRACT Poultry meat is often stored in modified atmosphere packaging (MAP) or vacuum packaging to improve consumer acceptance and shelf life. The aim of this study was to determine how different packaging conditions influence meat quality. Therefore, in three independent experiments, turkey breast muscle cutlets were packaged either in vacuum or in different modified atmosphere mixtures (80% O2, 20% CO2 [MAP 1]; 80% N2, 20% CO2 [MAP 2]; and 20% O2, 20% CO2, 60% N2 [MAP 3]) and stored for 12 days at 3uC. Color, pH, electrical conductivity, total viable counts, and Pseudomonas species were determined on days 1, 4, 8, and 12 of storage. On the same days, samples were collected for analysis of thiobarbituric acid– reactive substance and total volatile basic nitrogen concentrations. Sensory parameters and liquid loss were determined on days 4, 8, and 12. Vacuum-packaged meat had the highest liquid loss and lowest sensory results. MAP 1–packaged meat showed the highest sensory, redness, and thiobarbituric acid–reactive substance values. MAP 2–packaged meat had lower sensory values. MAP 3–packaged meat had lower redness and sensory values, especially at the end of storage. The study showed an impact of the packaging condition on different quality parameters, with a small advantage for storage of turkey cutlets in high-oxygen packages.
A large amount of poultry meat is purchased in cut-up parts that can be prepared quickly at home, because time for cooking preparation plays an essential role in consumers’ buying behavior (10, 23). These products are more susceptible to deterioration, and indicators like microbiological quality or the amounts of total volatile basic nitrogen (TVB-N) or thiobarbituric acid–reactive substances (TBARS) could be used for spoilage analysis (6). Moreover, poultry meat is often stored in modified atmosphere packaging (MAP) with high oxygen concentrations (8). An important advantage of this MAP storage is the extended shelf life of meat due to reduction of spoilage (10). Furthermore, meat in MAP positively influences consumers’ decisions during self-service purchase due to its bright red appearance (5). However, highoxygen packaging is also associated with negative aspects like increased levels of lipid oxidation (11) and the risk of uncontrolled oxygen release in the packaging unit that may be accompanied with combustion/burst and oxygen toxicity (2). In contrast to that, oxygen-free storage increases the risk for growth of anaerobic bacteria, such as Clostridium species (15). As data about MAP storage-related alterations of highly processed products in poultry are few, the objective of the present study was the analysis of quality changes in sliced turkey pieces stored for up to 12 days in high-oxygen (80%), low-oxygen (20%) and oxygen-free MAP, as well as * Author for correspondence. Tel: z495118567617; Fax: z49511856827617; E-mail: [email protected].
in vacuum packaging. The analysis considered microbiological and physicochemical parameters to obtain a comprehensive picture regarding the shelf life and spoilage of meat. MATERIALS AND METHODS Meat sampling. On three different days, 72 cutlets were obtained from a slaughterhouse each day, cut from breast muscles of commercial fast-growing turkey toms (Aviagen Turkeys Ltd., Chester, UK) approximately 12 h after slaughter and transported to our laboratory at 3uC within 2 h. Twenty-four hours after slaughter (day 1), microbiological samples were taken to determine the initial microbial status of the turkey meat. Then, approximately 70-g samples were cut from each cutlet, homogenized with a Grindomix homogenizer (Typ GM200, Retsch, Haan, Germany) and frozen at 220uC for analysis of TBARS and TVB-N concentrations. Subsequently, the remaining cutlet pieces were weighed (101.6 ¡ 18.6 g) and pH and electrical conductivity (EC) values were determined. The meat was then randomly subdivided to the four different packaging methods. The cutlets were packaged in polypropylene trays (ES Plastic GmbH & Co. KG, Passau, Germany) in high-oxygen (80% O2, 20% CO2 [MAP 1]) and oxygen-free (80% N2, 20% CO2 [MAP 2]) atmospheres, as well as in low-oxygen (20% O2, 60% N2, 20% CO2 [MAP 3]) atmosphere or in vacuum. Each tray contained two cutlets and was sealed with a Multivac t100 packaging machine (Sepp Haggenmueller GmbH & Co. KG, Wolfertschwerden, Germany) using polyethylene-ethylene vinyl alcohol-polypropylene transparent layers with high impermeability to O2 and CO2 (permeability: O2, 1.5 cm3/m2 d [day] bar at 23uC and 35% relative humidity [RH]; CO2, 5.5 cm3/m2 d bar at 23uC and 35% RH; and
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N2, 1 cm3/m2 d bar at 23uC and 35% RH) (SUEDPACK GmbH & Co. KG, Ochsenhausen, Germany). After packaging, the lightness (L*) and redness (a*) values of the meat were determined, followed by storage of all packages in the dark at 3uC. On days 4, 8, and 12, the analysis of color was repeated. At the same time points, three packages for each packaging method were chosen for analysis and thereby excluded from further storage. After opening and immediate sensory testing, samples were collected from every cutlet for microbiological analysis, and liquid loss was estimated after weighing. Subsequently, EC and pH were determined and the remaining piece of cutlet was used for TBARS and TVB-N analyses. These samples were stored as described above. Gas mixture analysis. The oxygen (O2) and carbon dioxide (CO2) concentrations of the MAP were analyzed with a CheckMate 9900 O2/CO2 (PBI-Dansensor A/S, Ringsted, Denmark) by inserting the needle through a gas-tight septum (PBI Dansensor). After analysis, another septum was stuck onto the first one to prevent gas leakage through the injection site during further storage. The O2 and CO2 contents were analyzed on days 1, 6, and 12 in all packages of MAP 1, 2, and 3 opened on day 12 of storage. pH, EC, color, and liquid loss. pH was measured using a portable pH meter (Knick Portamess, Knick GmbH, Berlin, Germany) equipped with a glass electrode (InLab 427, MettlerToledo, Urdorf, Switzerland). The EC (mS/cm) was measured with a portable EC meter (LF Star, Mattha¨us GmbH, Nobitz, Germany). The L* and a* values were determined with a colorimeter (Minolta CR-400, Minolta GmbH, Langenhagen, Germany) through the transparent film. Prior to the color analysis, the packages were turned, thereby considering direct contact of the meat with the film during measurement. Each L* and a* value was an average of four determinations. For liquid loss analysis, cutlets were dried carefully using a cloth and reweighed. This weight, after adding 5 g (microbial sample weight), and the initial cutlet weight, determined on day 1, were used to calculate the percentage of liquid loss. Microbiology. On day 1, before packaging, 2 g of each cutlet was collected and six meat samples were pooled. On days 4, 8, and 12, 5 g per cutlet was removed from every package for microbiological analysis, and the two samples from the same package were pooled for analysis. The 12-g (day 1) and 10-g (days 4, 8, and 12) samples were transferred, respectively, to 100 or 120 ml of sterile saline solution with peptone (0.85% NaCl, 0.1% peptone) and homogenized (Seward Stomacher 400 circulator, Seward Ltd., West Sussex, UK) for 2 min 30 s. Dilutions were prepared extending from 1:101 (bacterial solution to saline solution and peptone) to 1:104 referring to expected bacterial growth results. The dilutions were spread in duplicate on two different media: plate count nutrient agar (Merck KGaA, Darmstadt, Germany) for analysis of total viable count (TVC) and Pseudomonas agar base CM559 with selective cetrimide-fucidin-cephalosporin supplement (SR0151, Oxoid Deutschland GmbH, Wesel, Germany) for quantitative analysis of all Pseudomonas species. The plate count nutrient agar plates were incubated for 72 h at 30uC, and the Pseudomonas agar plates for 48 h at 30uC. Counts were expressed as log CFU per gram of meat. TBARS. The TBARS content was determined according to the method of Popp et al. (19). All experiments were performed in triplicate. To calculate the TBARS content, a standard curve with
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malondialdehyde (Merck KGaA) in the range of 0 to 1.0 mg/ml was prepared. The results were expressed in milligrams of malondialdehyde per kilogram of sample. TVB-N. The TVB-N content was determined and calculated according to European Commission regulation (EC) no. 2074/2005 (9). A Vapodest (C. Gerhardt GmbH & Co. KG, Koenigswinter, Germany) was used for analysis. TVB-N was calculated by multiplying the volume of titrated hydrochloric acid by 2.8. The results were expressed in milligrams of TVB-N per 100 g of meat. Sensory analysis. On days 4, 8, and 12, a trained panel of three persons (two female and one male) evaluated the appearance and odor of the meat samples immediately after the packages were opened. Depending on the aberrations in quality, points from 1 (unsatisfactory, not acceptable) to 5 (very good, no aberration in quality) could be given for both categories. The appearance points were multiplied by 3 and summated with the odor results. The sum was divided by 10 (maximum sensory points, 2.0). Chemicals. All chemicals were purchased from Applichem GmbH, Darmstadt, Germany, unless otherwise indicated. Statistical analysis. The data were analyzed using Statistica 10.0 software (StatSoft, Hamburg, Germany) with ‘‘packaging variant’’ (vacuum, MAP 1, MAP 2, and MAP 3) as the independent variable. The Shapiro-Wilk test was used to ensure that the data were normally distributed. Normally distributed data were analyzed using analysis of variance and the Tukey post hoc test. Non-normally distributed data (liquid loss, TBARS, and sensory analysis) were analyzed with the Mann-Whitney U test. A probability error of 0.05 was taken into account.
RESULTS AND DISCUSSION The results of gas analysis are shown in Figure 1. Comparable (P . 0.05) O2 and CO2 concentrations were observed in high-oxygen-packaged meat (MAP 1) over the whole storage period. The O2 contents in the high-nitrogen packages (MAP 2) increased significantly (P # 0.05) between days 1 and 12, whereas the day 6 results were comparable to those of the other days. The CO2 concentrations decreased between days 1 and 6. The day 12 results were comparable to the carbon dioxide amounts on the other days. The low-oxygen packages (MAP 3) only showed significantly (P # 0.05) decreasing O2 contents between days 6 and 12. The CO2 contents were comparable on all storage days. Various results concerning changes of gas composition were observed in other studies. For example, Irkin et al. (12) observed a decrease in oxygen content and, hence, an increase in the percentage of carbon dioxide during storage of minced beef meat. Al-Nehlawi et al. (1) observed an initial decrease in CO2 concentration during storage of chicken drumsticks that was followed by comparable CO2 concentrations during the following days. For oxygen, no significant (P . 0.05) differences in head space composition were observed. During storage of pig longissimus muscle slices in modified atmosphere, Pfeiffer and Menner (18) observed an initial decrease of CO2 content followed by an increase in the CO2 percentage. Changes in gas composition within the MAP are influenced by factors like soluting of the CO2, consumption of the O2 by the respiratory
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FIGURE 1. Least squares means (LSM) and standard deviations of the oxygen (O2) and carbon dioxide (CO2) concentrations in the modified atmosphere packaging (MAP 1, 80% O2, 20% CO2; MAP 2, 80% N2, 20% CO2; MAP 3, 20% O2, 60% N2, 20% CO2) on days 1, 6, and 12 of storage. LSM with different letters between days within the same parameter and packaging variant differ significantly (P # 0.05).
activity of the meat or microorganisms, and permeation of the gases through the transparent layer (18). The pH values were comparable between the different packaging variants, except on day 4. At this time point, MAP 1–stored products showed significantly (P # 0.05) lower pH values than the products stored in MAP 3. The vacuum- and MAP 2–stored meat had pH values comparable to the MAP 1 and MAP 3 results (Table 1). The pH results mainly agree with those of Martı´nez et al. (13), who could not observe any pH differences during storage of fresh pork sausages in low- and high-oxygen packages or in oxygen-free packages. In contrast to that, Mastromatteo et al. (14) observed lower pH values for the low-oxygen variant than for the high-oxygen variant in poultry. A reason for this difference might be that, in the study of Mastromatteo et al. (14), the low-oxygen packages had
higher CO2 concentrations than the high-oxygen packages. If CO2 solutes in water, forming carbonic acid, pH values usually decrease. The turkey meat stored in the different packaging variants did not differ significantly in terms of EC, except on day 4. MAP 3 meat had significantly (P # 0.05) lower EC values than the MAP 1 and MAP 2 products. Vacuumpackaged turkey meat had EC results similar to those of MAP 1, 2, and 3 (Table 1). The EC values in our study could be related to the appropriate pH values, especially in MAP 1 and MAP 3. The faster pH decrease results in pronounced shrinkage and denaturation of the myofibrillar proteins, accompanied by accelerated release of water and electrolytes (22). This causes higher EC values of the low-pH meat (24). On days 4, 8, and 12, vacuum-packaged meat had significantly (P # 0.05) higher liquid loss values than the
TABLE 1. LSM and standard deviations of pH and EC results for turkey meat depending on packaging method and storage time a LSM ¡ SD Parameter
Day
Vacuum packaging
pH
4 8 12 4 8 12
5.75 5.72 5.72 7.79 8.12 8.81
EC
a
¡ ¡ ¡ ¡ ¡ ¡
0.06 0.08 0.06 0.72 0.73 0.7
AB
AB
MAP 1
5.71 5.73 5.73 8.07 8.47 8.87
¡ ¡ ¡ ¡ ¡ ¡
0.08 0.05 0.04 0.91 0.92 0.62
MAP 2 B
A
5.76 5.73 5.73 8.33 8.84 8.91
¡ ¡ ¡ ¡ ¡ ¡
0.09 0.06 0.09 0.69 0.97 0.88
MAP 3 AB
A
5.80 5.72 5.77 7.30 8.66 9.26
¡ ¡ ¡ ¡ ¡ ¡
0.13 0.08 0.12 1.04 0.98 0.46
A
B
LSM, least squares means; MAP 1, 80% O2, 20% CO2; MAP 2, 80% N2, 20% CO2; MAP 3, 20% O2, 60% N2, 20% CO2; EC, electrical conductivity in mS/cm. LSM with different letters within a row differ significantly (P # 0.05); n ~ 18 cutlets per packaging method.
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other packaging variants on days 1, 4, and 8 of storage. On days 1 and 4, the results for the vacuum, MAP 2, and MAP 3 turkey cutlets were comparable, but on day 8, the a* values of the MAP 3 meat had decreased significantly (P # 0.05) compared with the values for the other stored products. On day 12, the MAP 3 meat had significantly (P # 0.05) lower a* values than the otherwise-comparable a* results of the other packaging variants (Table 2). The higher L* values of MAP 1 meat than of vacuumstored products, as well as the difference between MAP 1 and MAP 3, are supported by the results of Go´mez and Lorenzo (11). However, Mastromatteo et al. (14) found no L* differences between vacuum-, high-oxygen-, and lowoxygen-packaged poultry patties. With regard to the a* results, the higher a* results in the high-oxygen packages presented here mainly agree with the data of Sante et al. (21) in turkey meat, especially the presented reduction of the a* in the oxygen-containing packages during further storage. In contrast to our study, Bingol and Ergun (4) found in ostrich meat comparable a* results for high- and low-oxygen packages up to day 5, followed by a decrease in the highoxygen-stored products. The TVCs of MAP 1 meat on day 4 were significantly (P # 0.05) lower than the TVCs of the vacuum and MAP 2 variants, whereas the MAP 3 meat showed values comparable to those of all other variants. On day 8, MAP 1–stored meat showed significantly (P # 0.05) lower TVCs than vacuum- and MAP 3–stored products, whereas the MAP 2 meat had values comparable to those of all other variants. On day 12, no significant TVC differences were found between all packaging variants (Fig. 3). Concerning the Pseudomonas species, no differences (P . 0.05) were observed between the different packaging variants on days 4, 8, and 12. The amounts of Pseudomonas species ranged between 2.86 log CFU/g (day 1) and 4.68 log CFU/g (day 12) (data not shown). Rajkumar et al. (20) also observed lower TVCs for turkey meat packaged in 80% O2 than for vacuum-stored products during advanced storage (days 14 and 21), and Coventry et al. (7) found lower TVCs in high-oxygen- than in high-nitrogen-packaged beef after 2 to 6 weeks. However,
FIGURE 2. Least squares means (LSM) and standard deviations (n ~ 18) for liquid loss of turkey meat depending on packaging variant and storage time. LSM with different letters on the same day differ significantly (P # 0.05).
MAP products. Turkey meat in MAP 1, 2, and 3 showed comparable liquid loss results on all days (Fig. 2). Rajkumar et al. (20) also observed higher liquid loss in vacuumpackaged turkey meat than in products stored in highoxygen atmosphere. The higher drip loss might be due to greater physical compression by the vacuum-packaging procedure (17). On day 1, the L* values were higher (P # 0.05) in the MAP 1 samples than in the other packages. The MAP 2 meat had significantly (P # 0.05) lower L* values than meat in the other packaging variants, whereas vacuum and MAP 3 products showed comparable L* values. On days 4 and 8, MAP 3 meat had the highest L* values, differing from meat in all other packaging variants. The results for the MAP 1 cutlets lay between the results of the other packaging variants, differing (P # 0.05) from all other variants on day 4 and from vacuum and MAP 3 meat on day 8. On days 4 and 8, the vacuum and MAP 2 products had comparable L* values. The L* values were determined to be comparable between all packaging variants on day 12 (Table 2). On all days, MAP 1 meat had the highest a* values, differing significantly (P # 0.05) from the results of the
TABLE 2. LSM and standard deviations of lightness and redness results of turkey meat, determined through the packaging film, depending on packaging method and storage time a LSM ¡ SD Parameter
Day
Vacuum packaging
L*
1 4 8 12 1 4 8 12
50.49 49.76 50.13 50.52 3.61 3.63 3.81 3.89
a*
a
¡ ¡ ¡ ¡ ¡ ¡ ¡ ¡
1.99 2.17 1.62 2.20 0.69 0.72 0.69 0.70
B C C
B B B A
MAP 1
51.19 50.99 51.22 51.48 4.65 4.97 4.60 4.26
¡ ¡ ¡ ¡ ¡ ¡ ¡ ¡
1.94 1.65 1.55 1.50 1.01 1.00 1.09 1.06
MAP 2 A B B
A A A A
49.40 49.95 50.45 51.14 3.77 3.90 4.10 4.12
¡ ¡ ¡ ¡ ¡ ¡ ¡ ¡
2.12 1.75 1.74 1.37 0.89 0.91 0.74 0.70
MAP 3 C C BC
B B B A
50.31 51.88 52.15 52.29 3.83 3.90 3.08 2.36
¡ ¡ ¡ ¡ ¡ ¡ ¡ ¡
1.79 1.72 1.87 3.56 0.97 0.79 1.12 1.42
B A A
B B C B
LSM, least squares means; MAP 1, 80% O2, 20% CO2; MAP 2, 80% N2, 20% CO2; MAP 3, 20% O2, 20% CO2, 60% N2; L*, lightness; a*, redness. LSM with different letters within a row differ significantly (P # 0.05). Numbers of cutlets per packaging method: days 1 and 4, n ~ 54; day 8, n ~ 36; day 12, n ~ 18.
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FIGURE 3. Least squares means (LSM) and standard deviations (n ~ 9) for total viable counts (TVC) of turkey meat depending on packaging variant and storage time. LSM with different letters on the same day differ significantly (P # 0.05).
Mastromatteo et al. (14) found higher TVCs in highoxygen- than in low-oxygen- and vacuum-packaged poultry patties on days 6 and 8 of storage. The Pseudomonas species results presented here are mainly in accordance with those of Bingol and Ergun (4), who did not mention differences between low- and high-oxygenstored ostrich meat, and Coventry et al. (7), who mentioned maximal values of about 104 CFU/cm22 in nitrogenpackaged meat after 6 weeks of storage. However, Mastromatteo et al. (14) determined different Pseudomonas contents in vacuum-, low-oxygen-, and high-oxygenpackaged poultry patties. The high-oxygen packages had the highest values on days 3 to 8. Balamatsia et al. (3) observed lower values for vacuum-packaged than for lowoxygen-packaged broiler breast muscles. On days 4 and 12, MAP 1 meat had significantly (P # 0.05) higher TBARS results than all other packaging variants. On day 4, the vacuum-packaged meat had lower (P # 0.05) TBARS values than the MAP 3 products, whereas the MAP 2 results only differed (P # 0.05) from the MAP 1 values. Vacuum, MAP 2, and MAP 3 meat showed comparable values on day 12. On day 8, no significant differences were observed between all packaging variants (Fig. 4). The effect of intensified lipid oxidation due to higher oxygen concentration in the surrounding atmosphere has already been described (13). However, there are also reports in which no difference in TBARS values in packaging variants with various oxygen contents is stated (16). Considering the TVB-N concentrations of the meat, no significant (P . 0.05) effects of the different packaging variants could be ascertained in our study. The values ranged between 27.04 mg/100 g of meat (day 1) and 28.20 mg/100 g of meat (day 12) (data not shown). Fraqueza et al. (10) also did not find significant differences of TVB-N concentrations in turkey meat packaged with 50% CO2 or 50% N2, but they determined a positive correlation between TVB-N content and Pseudomonas species. However, Balamatsia et al. (3) found lower TVB-N values of MAP-stored than of vacuumstored chicken breasts and, in addition, observed a positive relation between microbial and TVB-N values.
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FIGURE 4. Least squares means (LSM) and standard deviations (n ~ 18) for thiobarbituric acid–reactive substances (TBARS) of turkey meat depending on packaging variant and storage time. LSM with different letters on the same day differ significantly (P # 0.05).
On all days (days 4, 8, and 12), MAP 1 meat showed significantly (P # 0.05) higher sensory values and, therefore, better appearance and odor results than all other variants. The vacuum, MAP 2, and MAP 3 stored meat had comparable results on day 4, but not during further storage. On day 8, vacuum-packaged meat showed significantly (P # 0.05) lower sensory results than the otherwise-comparable values of the MAP 2 and MAP 3 products, whereas on day 12, the values in MAP 3 meat dropped to the lowest sensory results, differing significantly (P # 0.05) from the MAP 2- but not the vacuum-packaged turkey cutlets (data not shown). Balamatsia et al. (3) showed during 15 days of storage that vacuum- in relation to low-oxygen-packaged chicken meat had worse sensory results at the end of storage and not at the beginning, as in the present study. In contrast to the present study, Rajkumar et al. (20) found better odor results in vacuum-packaged than in high-oxygen-stored turkey meat. In conclusion, in the present study, a high-oxygen atmosphere was advantageous for packaging, considering the different interests of consumers and food producers. Whereas the consumer is mainly influenced by color and other sensory aspects of meat, for food producers, shelf life is an important feature. High-oxygen-containing packages were rated better concerning consumers’ interests despite their higher TBARS values and had no disadvantages from the food producers’ point of view. The high-nitrogen variant might be an alternative, having satisfying results for most parameters, but provides a less-attractive appearance. ACKNOWLEDGMENTS This study was funded by the Ahrberg Foundation, Hannover, Germany. The authors gratefully acknowledge Bettina Engel-Abe´ and Manuela von Ahlen and all the people participating the time-consuming meat collections and analyses.
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