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Effect of an active packaging with citrus extract on lipid oxidation and sensory quality of cooked turkey meat
Meat Science 96 (2014) 1171–1176
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Effect of an active packaging with citrus extract on lipid oxidation and sensory quality of cooked turkey meat Claudia Contini a, Rocío Álvarez b, Michael O'Sullivan a, Denis P. Dowling c, Sean Óg Gargan c, Frank J. Monahan a,⁎ a b c
UCD School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland Agroforestry Science Department, University of Seville, Seville, Spain UCD School of Mechanical and Materials Engineering, University College Dublin, Belfield, Dublin 4, Ireland
a r t i c l e
i n f o
Article history: Received 14 June 2013 Received in revised form 19 September 2013 Accepted 4 November 2013 Keywords: Active packaging Citrus extract Lipid oxidation Turkey meat Sensory analysis
a b s t r a c t An antioxidant active packaging was prepared by coating a citrus extract, consisting of a mixture of carboxylic acids and flavanones, on polyethylene terephthalate trays. The effect of the packaging in reducing lipid oxidation in cooked turkey meat and on meat pH, colour characteristics and sensorial parameters was investigated. An untrained sensory panel evaluated the odour, taste, tenderness, juiciness and overall acceptability of the meat, using triangle, paired preference and quantitative response scale tests. A comparison between the antioxidant effects of the different components of the extract was also carried out. The packaging led to a significant reduction in lipid oxidation. After 2 days of refrigerated storage the sensory panel detected differences in odour and, after 4 days, rated the meat stored in the active packaging higher for tenderness and overall acceptability. Citric acid appeared to be the most important component of the extract with regard to its antioxidant potency. © 2013 Elsevier Ltd. All rights reserved.
1. Introduction Lipid oxidation represents one of the major causes of the progressive deterioration in the quality of meat products, limiting their storage shelf life. The deterioration in organoleptic characteristics, and the associated loss of nutritional value induced by the oxidative process, can be delayed by the addition of antioxidants. Natural substances with antioxidant activity have been widely studied as food preservatives; these include flavonoids, phenolic acids, organic acids and carotenoids, which can reduce lipid oxidation by scavenging free radicals, chelating metal ions or quenching oxygen radicals (Brewer, 2011; Murphy, Kerry, Buckley, & Gray, 1998; Nijveldt et al., 2001; Yanishlieva, Marinova, & Pokorný, 2006). Beneficial effects on the oxidative stability and organoleptic properties of food have been found for grape seed extract in cooked ground beef (Ahn, Grün, & Fernando, 2002), green tea and grape seed extract in beef patties (Bañón, Díaz, Rodríguez, Garrido, & Price, 2007), oregano essential oil in chicken breast meat (Chouliara, Karatapanis, Savvaidis, & Kontominas, 2007) and rosemary extract in beef (Lee, Decker, Faustman, & Mancini, 2005; McBride, Hogan, & Kerry, 2007). The inclusion of natural extracts with antioxidant activity within the packaging material can protect food from lipid oxidation, thus ⁎ Corresponding author. Tel.: +353 1 716 2842. E-mail address: [email protected] (F.J. Monahan). 0309-1740/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.meatsci.2013.11.007
increasing its shelf-life (Siripatrawan & Harte, 2010; Wessling, Nielsen, & Giacin, 2000). Active antioxidant packaging for meat products has been prepared with oregano and rosemary extracts (Camo, Beltrán, & Roncalés, 2008) and barley husk extract (Pereira de Abreu, Paseiro Losada, Maroto, & Cruz, 2010). Another natural antioxidant, obtained from citrus extract and containing carboxylic acids and flavonoids, has been used in our laboratory as a coating on a polyethylene terephthalate (PET) based active packaging for cooked meats. The antioxidant coated trays were shown to be effective in reducing lipid oxidation, as assessed by 2-thiobarbituric acid-reactive substances (TBARS) and hexanal content, in cooked turkey breast meat during refrigerated storage (Contini et al., 2012). Chemical methods can be suitable tools for the evaluation of the level of oxidation in meat (Laguerre, Lecomte, & Villeneuve, 2007) with, for example, the quantification of hexanal, a product of the oxidation of linoleic acid, being commonly used as indicator of lipid oxidation in meat (Gandemer, 2002). The perception of the quality of a product, however, also depends on sensory characteristics like palatability, colour, texture and flavour, which can be evaluated only through sensory analysis assessments (Nute, 2002). In the present study, a citrus extract based active packaging tray, suitable for cooked meat is evaluated for its antioxidant efficacy, using the TBARS assay. Its effect on the colour parameters of meat, was determined instrumentally, and its effect on sensorial characteristics was assessed using sensory panel tests. Furthermore, the contribution of the principal components of
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the citrus extract to the total antioxidant effect of the active packaging was evaluated. 2. Materials and methods 2.1. Reagents A dried citrus extract containing a mixture of flavanones and carboxylic acids was obtained from Citrox Ltd., Middlesbrough, England. Methanol (≥99%), citric acid (CA, ≥99%), naringin (NA, ≥95%), neohesperidin (NEO, ≥90%), salicylic acid (SA, ≥99%), thiobarbituric acid (TBA, 98%), 1,1,3,3-tetraethoxypropane (TEP, ≥96%) and acetic acid (≥98%) were purchased from Sigma-Aldrich Ltd., Dublin, Ireland. Recycled polyethylene terephthalate (PET) trays (100 × 150 × 25 mm) were supplied by Holfeld Plastic, Co. Wicklow, Ireland. A low density polyvinylchloride (PVC) catering film (thickness 7.0 μm; O2 transmission 2000 cm3 m−2 day−1 bar−1) was obtained from Western Plastic Ltd., Galway, Ireland. 2.2. Preparation of turkey meat and PET coated trays Turkey breast meat was supplied by IGWT Poultry Service Ltd. (Co. Monaghan, Ireland). The meat was cooked in an oven to an internal temperature of 73 °C using the procedure described in Contini et al. (2012), cut into 5 mm slices with a meat slicer (Medoc, Logroños, Spain) and subsequently cut into 3 g square (30 mm × 30 mm) pieces. The coated PET trays (PET-CIT) were prepared by spraying a 100 mg ml− 1 methanolic solution of citrus extract through a Teflon nebulizer mounted on a computer numerical control system cncGraf (Boenigh Electronics, Bonn, Germany), following the procedure described in Contini et al. (2012). The amount of the citrus extract coated on the tray surface, calculated gravimetrically, was 0.46 mg cm−2 (Contini, 2013). Nine pieces of meat were placed on each PET (control) and PET-CIT tray, overwrapped with PVC film and stored for 4 days at 4 °C. 2.3. Sensory evaluation To evaluate sensory quality differences between meat stored on PET and on PET-CIT trays, sensory evaluation of the cooked turkey meat was carried out using triangle, paired preference and quantitative response scale tests. Eighteen untrained panellists (students and staff of the School of Agriculture and Food Science at University College Dublin) were recruited. For each sensory test, the meat samples were put in white, opaque containers and coded using three-digit numbers chosen randomly for each test. The sensory analysis was performed at day 0, day 2 and day 4 of storage, for which meat was removed from trays and kept at room temperature for 30 min before being served to the panel. All sessions were carried out in a sensory analysis laboratory equipped with individual testing booths and controlled lighting to neutralize any possible differences in colour or appearance of the meat. A single turkey breast was used for each sensory test to avoid differences not related to the packaging. Each sensory test was repeated three times, using three different turkey breasts. The triangle test (ISO 4120: 2004) was carried on olfactory and taste parameters. Assessors were asked to smell and taste one different and two identical samples of meat in the same session and instructed to indicate the odd sample. Results were compared with tables of minimum number of correct responses required for significance (ISO 4120: 2004). The paired preference test (ASTM E2263, 2012) was used to determine an overall preference between meat stored on the PET and on the PET-CIT trays. For this, assessors were asked to smell and taste the two meat samples and forced to indicate which one they preferred. The presentation order, as well as the numbering of the samples, was randomized for each assessor. Results were compared with tables of the number of common responses needed for significance (ASTM E2263, 2012). In the quantitative response scale test (ISO 4121: 2003-
E) the panellists were asked to smell and taste the meat stored on the PET and the PET-CIT trays and evaluate its juiciness, tenderness, flavour and overall acceptability. Each assessor evaluated these characteristics on a standard 9-point hedonic scale from 1 to 9, where 1 corresponded to extremely dry, extremely tough, extremely tasteless and extremely unsatisfactory and 9 corresponded to extremely juicy, extremely tender, extremely tasty and extremely satisfactory. 2.4. Lipid oxidation assay, pH determination and colour measurement in cooked turkey meat Lipid oxidation, pH and colour measurements on turkey meat stored on the PET and PET-CIT trays for 0, 2 and 4 days were made in parallel to the sensory analysis. Lipid oxidation was measured using the distillation method described by Tarlagdis, Watts, and Younathan (1960) and expressed as TBARS values in mg malonaldehyde kg−1 meat. A malonaldehyde standard curve was prepared using TEP. A Hanna pH meter HI120 (Leighton Buzzard, Belfordshire, England) was used to measure the pH of 1 g samples of meat homogenized in 9 ml of distilled water using an Ultra Turrax T25 (Janke & Kunkel IKA-Labortechnik). Surface meat colour was measured using a reflectance Minolta CR-400 colorimeter (Osaka, Japan) according to CIE (1986). The measurement was carried out under illuminant D65, 10° observer angles and following instrument calibration using a white tile. The chromaticity coordinates recorded were L* (Lightness), a* (redness) and b* (yellowness). The value for each of these parameters was calculated as the average of three measurements. 2.5. Preparation of turkey meat with added citrus extract compounds The antioxidant effect of the citrus extract constituents was evaluated by adding specific quantities of each, in methanolic (NA, NEO and SA) and aqueous (CA) solutions, directly to 3 g of cooked turkey meat ground through an OMAS mincer plate with 4 mm diameter holes (Varese, Italy). The specific quantities added corresponded to the amounts of each citrus extract component coated on the tray surface in contact with the meat, calculated in a previous experiment (Contini, 2013). The values calculated were: 345 μg g−1 meat for CA, 497 μg g−1 meat for SA, 20 μg g−1 meat for NA and 19 μg g−1 meat for NEO. The substances were added in the following combinations: NA, NEO, SA and CA (solutions with single components); NA + NEO, NA + CA, NA + SA, NEO + CA, NEO + SA and CA + SA (solutions with a combination of two components); NA + NEO + SA, NA + NEO + CA, NA + CA + SA and NEO + SA + CA (solutions with a combination of three components). The antioxidant activity of the different combinations of citrus extract components were compared to the values for meat stored without antioxidants (control) and those obtained with a solution of all the antioxidants (NA + NEO + CA + SA). Lipid oxidation was measured in all samples by the TBARS assay immediately (day 0) and after 2 and 4 days of storage at 4 °C. 2.6. Statistical analysis Three separate turkey breasts were used for each experiment and the results of the analysis were expressed as mean ± standard deviation of three repetitions. A one-way analysis of variance (ANOVA) and Tukey's post hoc test was performed to determine significant differences between the treatments, using SPSS (version 18) statistical software (IBM Inc. Chicago, IL, USA). 3. Results and discussion 3.1. Measurement of pH, oxidation levels and colour of meat Storage on PET-CIT trays affected the pH of meat, which was significantly lower (p b 0.01) in meat on the PET-CIT trays compared
C. Contini et al. / Meat Science 96 (2014) 1171–1176 Table 1 pH, TBARS (mg MDA kg−1 meat) and colour variables (L*, a*, b*) of cooked turkey meat stored on PET and PET-CIT trays at 4 °C and assessed at day 0, day 2 and day 4. x,y,zWithin each treatment, values with different letters are significantly different due to the storage a,b time. Within each storage time, values with different letters are significantly different due to the treatment. Analytical parameters
Meat samples
Day 0
pH
PET PET-CIT PET PET-CIT PET PET-CIT PET PET-CIT PET PET-CIT
6.27 5.98 1.14 0.72 75.74 74.96 4.24 4.18 8.17 11.20
mg MDA/kg meat L* a* b*
± ± ± ± ± ± ± ± ± ±
Day 2
Day 4
6.33 ± 0.38az 0.07bz 0.12az 6.10 ± 0.29az 0.06bx 4.67 ± 0.34by 0.37ax 2.02 ± 0.83ay 0.82az 75.76 ± 1.57bz 1.54az 73.54 ± 1.15az 0.52az 1.79 ± 0.47ay 0.47az 4.20 ± 0.63bz 0.36ay 9.28 ± 0.88az 0.91bz 10.00 ± 1.45az
6.06 5.89 6.29 2.85 76.31 76.34 1.96 2.84 10.07 10.50
± ± ± ± ± ± ± ± ± ±
0.10bz 0.07az 0.82bz 0.12az 1.16az 0.88az 1.34ay .22az 0.44az 0.87az
to meat on the PET trays at day 0 and day 4 (Table 1). Previous studies in our laboratory have shown that antioxidant components are released from the coating on the trays into the meat as soon as the meat comes in contact with the trays (Contini, 2013). The early release of citric and salicylic acid therefore most likely accounts for the lower pH value found throughout the storage period. Lipid oxidation values (TBARS) in meat stored on PET trays progressively increased from 1.14 ± 0.06 to 6.29 ± 0.82, with significantly higher values at day 2 compared to day 0 (p b 0.01) and at day 4 compared to day 2 (p b 0.01). This is in accordance with previous studies on the oxidation of cooked turkey meat (Caprioli, O'Sullivan, & Monahan, 2009; Mielnik, Olsen, Vogt, Adeline, & Skrede, 2006). Storage on PET-CIT trays led to a significant (p b 0.01) reduction in lipid oxidation, with TBARS values less than half those of samples stored on the control PET trays after 2 and 4 days of storage (Table 1). The results of the colorimetric analysis of the meat samples showed that differences in L* (lightness) values between treatments were only significant at day 2 (p b 0.05), with meat on the PET-CIT trays having a lower value than that on the PET trays. Other studies have also shown that the addition of citric acid or citrus extracts resulted in a decrease of meat lightness and suggested that this may be linked to the pigments contained in the citrus extract or to changes in water retention of meat induced by citrus extract components (Ke, Huang, Decker, & Hultin, 2009; Nicolalde, Stetzer, Tucker, McKeith, & Brewer, 2006). The analysis of a* (redness) values showed a decrease in redness during storage from 4.24 ± 0.52 to 1.79 ± 0.47 in control samples on PET, with significantly lower (p b 0.01) values at days 2 and 4 compared to day 0. The PET-CIT trays were effective in lowering the reduction in a* value of meat which did not change significantly with storage and was significantly higher compared to control at day 2 (p b 0.01). A rapid decrease of meat redness as a consequence of lipid oxidation has been well documented, as well as the retardation of such a reduction being cited as among the benefits offered by treatments with antioxidants (Yu, Scanlin, Wilson, & Schmidt, 2002). The b* (yellowness) values of meat stored on PET trays showed a trend opposite to that of the a* values, with a progressive increase in yellowness with storage time, resulting in significantly higher values at days 2 and 4 compared to day 0 (p b 0.01). The PET-CIT treatment led to significantly higher initial b* values compared to the control samples (p b 0.01), although values were not significantly different thereafter. The higher initial b* values of meat stored on the PET-CIT trays, likely relates to pigments in the citrus extract, rather than to an effect on lipid oxidation (Fernández-López, Zhi, Aleson-Carbonell, Pérez-Alvarez, & Kuri, 2005). However, another study showed that CA can also be responsible for an increase in the b* value of cooked turkey meat (Sammel & Claus, 2006).
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3.2. Triangle test for the evaluation of odour and taste A triangle test was conducted to assess the perception of differences in odour and taste between the meat stored on PET and PET-CIT trays. The odour results showed that at day 0 only 5 out of 18 assessors correctly identified the samples, suggesting no significant differences were perceptible between meat stored on PET and PET-CIT trays (Table 2). However, the number of correct answers increased progressively with storage time to reach 11 correct answers out of 18 at day 4, which indicated a significant difference (p b 0.05) in odour between control meat and meat stored on the PET-CIT trays. Although the test did not reveal the nature of these odour differences, it likely relates to rancid odours produced by lipid oxidation, which is more pronounced in control meat. In fact, storage on the PET-CIT trays led to a signification reduction in TBARS levels of meat (Table 1), which has previously been correlated to a lower production of hexanal, an aldehyde associated with rancid odour (Brunton, Cronin, Monahan, & Durcan, 2000; Contini et al., 2012). Storage on the PET-CIT trays led to a reduction in lipid oxidation to TBARS values close to 2 mg MDA kg−1 of meat (Table 1), which is considered by some as a rancid flavour threshold in meat (Campo et al., 2006). Other studies have also reported that volatile aldehydes produced by lipid oxidation are largely responsible for the rancid odour of oxidized food (Fernando, Berg, & Grün, 2003; Jo, Ahn, & Byun, 2002), hence a lower content of such compounds could explain the differences in olfactory characteristics of meat observed using the triangle test. Previous studies also showed that, after 4 days, assessors in a panel test could perceive a less pronounced rancid odour in cooked turkey meat wrapped in caseinate/glycerol edible films as a result of the inhibition of lipid oxidation (Caprioli et al., 2009). Citrus extract coatings showed similar antioxidant effects on the odour of beef meat (Fernández-López et al., 2005). The results of the triangle test for meat taste indicated no significant difference in meat taste arising from storage on the two tray types (Table 2). A more pronounced difference in odour compared to the taste induced by oxidative degradation of fats can be explained by the low threshold of perception of the volatile aldehydes which therefore affect odours in meat at the earliest stage of their production (Mottram & Edwards, 2006).
3.3. Paired preference test A paired preference test was conducted to assess if one of the two meat samples had more acceptable sensory characteristics, expressed as generic preference, irrespective of the specific characteristics of the meat. The assessors were asked to express their preference on the odour and taste characteristics of the meat. Since a forced choice procedure was adopted, a sample was chosen even if the selection by the assessor was done randomly. It is worth noting that a preference is not an intrinsic attribute of the product, but rather a subjective measure relating to the respondents' affective or hedonic response (ASTM E2263, 2012). The meat stored on PET-CIT trays always received the highest number of preferences, with a statistically significant higher score (p b 0.05) at day 2, with 14 preferences out of 18 (Table 3).
Table 2 Sensory evaluation by triangle test of cooked turkey meat stored on PET and PET-CIT trays at 4 °C and assessed at day 0, day 2 and day 4. Results are expressed as correct answers/total answers. Sensory parameters
Day 0
Day 2
Day 4
Odour Taste
5/18 (ns) 5/18 (ns)
8/18 (ns) 5/18 (ns)
11/18 (p b 0.05) 6/18 (ns)
ns = not significant.
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Table 3 Sensory evaluation by paired preference test on the overall preference of cooked turkey meat stored on PET and PET-CIT trays at 4 °C and assessed at day 0, day 2 and day 4. Meat samples
Day 0
Day 2
Day 4
PET PET-CIT
7 11 (ns)
4 14 (p b 0.05)
7 11 (ns)
ns = not significant.
3.4. Quantitative response scale test on sensorial characteristics of meat The quantitative response scale test showed that the meat samples stored on the PET-CIT trays yielded numerically higher values for all four sensorial parameters assessed at all storage times, compared to the control samples on uncoated PET. For tenderness, the higher scores for meat stored on PET-CIT trays were statistically significant (p b 0.01) at day 4 (Table 4). This reflects two opposite trends with increase in storage time: a decrease in scores for meat stored on the PET trays and an increase in scores for meat stored on PET-CIT trays. A significant difference (p b 0.05) was found also for the overall acceptability of meat at day 4 of storage. The higher tenderness scores for meat stored on the PET-CIT trays may be related to the lower oxidation of meat. Lipid oxidation has been associated with a decrease in meat tenderness believed to be due to oxidation-induced cross-linking of proteins (Lund, Lametsch, Hviid, Jensen, & Skibsted, 2007; Xiong, Park, & Ooizumi, 2009). The higher tenderness score at day 4 might also be due to differences in pH value which were significantly lower in meat stored on PET-CIT trays at day 0 and day 4 compared to the control meat (Table 1). A relationship between pH and meat tenderness was also previously reported for beef meat, where the tenderness tended to decrease with an increase of pH from 5.5 to 6.1, followed by an increase at pH values above 6.1 (Villarroel, María, Sañudo, Olleta, & Gebresenbet, 2003) and was ascribed to changes in the structure of the muscle (Purchas & Aungsupakorn, 1993). The positive effect of the antioxidant active packaging on the tenderness of meat could therefore depend on the presence of organic acids contained in the citrus extract. The higher score at day 4 for overall acceptability of the meat is probably related to the tenderness, as highlighted by previous studies on sensory evaluation of meat, which found a high correlation between tenderness and overall acceptability (Thompson, 2002). Other studies have pointed out that in sensory tests overall preferences for meat are mostly driven by differences in tenderness and juiciness (Savell et al., 1987). 3.5. Direct addition of citrus extract components to meat The addition of single citrus extract components to minced meat provided an indication of the relative contribution of each of the components to the antioxidant activity of the packaging. The analysis at day 0 and day 2 showed a significant reduction in lipid oxidation (p b 0.01)
Table 4 Sensory evaluation by quantitative response scale test of cooked turkey meat stored on PET and PET-CIT trays at 4 °C and assessed at day 0, day 2 and day 4. a,bWithin each storage time, values with different letters are significantly different due to the treatment. zWithin each treatment, values did not differ significantly due to the storage time. Sensory parameters
Meat samples Day 0
Juiciness
PET PET-CIT PET PET-CIT PET PET-CIT PET PET-CIT
Tenderness Flavour Overall acceptability
4.72 5.72 5.33 5.39 5.11 5.94 5.56 6.06
± ± ± ± ± ± ± ±
Day 2 1.81az 1.60az 2.01az 1.88az 1.91az 1.31az 1.82az 1.70az
4.28 4.39 5.28 5.44 4.89 5.78 5.06 5.72
± ± ± ± ± ± ± ±
Day 4 1.81az 1.75az 1.81az 1.46az 1.88az 1.63az 1.83az 1.45az
4.06 4.67 4.44 6.06 5.11 5.61 5.17 6.06
± ± ± ± ± ± ± ±
1.92az 1.91az 2.04az 1.73bz 1.41az 1.65az 1.38az 1.31bz
when CA was added to the meat (Fig. 1). The other components did not show antioxidant activity (with the exception of the NA + NEO + SA combination) up to day 2, with values similar to, or higher than, the control packaging. At day 4, inclusion of all individual components and combinations thereof led to a significant reduction in lipid oxidation compared to the control (p b 0.01). Again, CA showed the highest antioxidant activity, with TBARS value significantly lower (p b 0.01) than those of the other components added individually or in the various combinations. The higher efficacy of citric acid compared to the flavanones may be due to its higher (at least 17-fold) level of addition (see Section 2.5). At day 4, CA alone was most effective in retarding lipid oxidation, suggesting that some of the other components may actually compromise its antioxidant efficacy (e.g. CA vs combinations of CA with one or more of NA, NEO and SA). The antioxidant efficacy of CA most likely relates to its properties as a metal chelator, which permits it to bind pro-oxidant metals via its carbonyl or hydroxyl groups (Francis, Dodge, & Gillow, 1992). Although citrus extracts could differ in their composition, several studies have assessed their ability to delay lipid oxidation in meat (Ke et al., 2009; Lee et al., 2005). In addition to metal chelating, other mechanisms have been proposed for the antioxidant activity of CA, including its effect in breaking down preformed peroxides (Vareltzis, Hultin, & Autio, 2008). These studies have also pointed out that the antioxidant activity of CA does not relate to acidification which, on the contrary, would promote lipid oxidation. Fewer studies are available on the antioxidant activity of SA, the other major component of citrus extract. Salicylic acid is present in plants as a regulator of growth processes and inhibits degradation processes by stimulating antioxidant enzyme activity thus reducing free radical formation (Tareen, Abbasi, & Hafiz, 2012). The limited antioxidant effect found for SA is in agreement with the finding of Brettonet, Hewavitarana, DeJong, and Lanari (2010) which showed the ability of SA to reduce TBARS values of meat only in combination with other phenolic acids. In addition, in the present study, antioxidant enzyme activity in muscle would have been inactivated by the heat treatment, making any stimulating effect of SA on antioxidant enzymes redundant. Flavanones like NA and NEO are well known for their strong antioxidant activity as free radical scavengers (Nijveldt et al., 2001) and other flavonoids have already been used with success as active substances in antioxidant active packaging for food preservation (Chen, Lee, Zhu, & Yam, 2012). The relatively low contribution of NA and NEO to the total antioxidant effect of the packaging might therefore be due to their relative low level of occurrence in the citrus extract composition used herein, rather than a low effectiveness in reducing lipid oxidation processes per se.
4. Conclusion This study shows that antioxidant active packaging with citrus extract is effective in reducing the lipid oxidation of cooked turkey meat during storage and in maintaining its sensory characteristics, particularly tenderness and overall acceptability. The increase in tenderness could be due to reduction in lipid oxidation of meat stored in the active packaging and to lower pH values leading to modifications in the muscle structure. Citric acid was the main driver of antioxidant activity amongst the citrus extract components. These findings show that trays coated with citrus extract have potential to prolong the consumer acceptability of cooked meat products.
Acknowledgments This work was undertaken within the Precision Strategic Research Cluster supported by the Science Foundation Ireland grant 08/SRC/ I1411.
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Fig. 1. Effect of the direct addition of citrus extract components on lipid oxidation (TBARS values) in cooked minced meat stored at 4 °C and assessed at day 0, day 2 and day 4 of storage. a,b,c,d,e,f,gWithin each storage time, values with different letters are significantly different due to treatment (p b 0.01). x,y,zWithin each treatment, values with different letters are significantly different due to storage time (p b 0.05). CA, citric acid; NA, naringin; NEO, neohesperidin; SA, salicylic acid.
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International Standard ISO 4121: 2003(E) (2003). Sensory analysis — Guidelines for the use of quantitative response scales. Jo, C., Ahn, D. U., & Byun, M. W. (2002). Irradiation-induced oxidative changes and production of volatile compounds in sausages prepared with vitamin E-enriched commercial soybean oil. Food Chemistry, 76, 299–305. Ke, S., Huang, Y., Decker, E. A., & Hultin, H. O. (2009). Impact of citric acid on the tenderness, microstructure and oxidative stability of beef muscle. Meat Science, 82, 113–118. Laguerre, M., Lecomte, J., & Villeneuve, P. (2007). Evaluation of the ability of antioxidants to counteract lipid oxidation: Existing methods, new trends and challenges. Progress in Lipid Research, 46, 244–282. Lee, S., Decker, E. A., Faustman, C., & Mancini, R. A. (2005). The effects of antioxidant combinations on color and lipid oxidation in n−3 oil fortified ground beef patties. Meat Science, 70, 683–689. Lund, M. N., Lametsch, R., Hviid, M. S., Jensen, O. N., & Skibsted, L. H. (2007). High-oxygen packaging atmosphere influences protein oxidation and tenderness of porcine longissimus dorsi during chill storage. Meat Science, 77, 295–303. McBride, N. T. M., Hogan, S. A., & Kerry, J. P. (2007). Comparative addition of rosemary extract and additives on sensory and antioxidant properties of retail packaged beef. International Journal of Food Science and Technology, 42, 1201–1207. Mielnik, M. B., Olsen, E., Vogt, G., Adeline, D., & Skrede, G. (2006). Grape seed extract as antioxidant in cooked, cold stored turkey meat. Food Science and Technology, 39, 191–198. Mottram, D. S., & Edwards, R. A. (2006). The role of triglycerides and phospholipids in the aroma of cooked beef. Journal of the Science of Food and Agriculture, 34(5), 517–522. Murphy, A., Kerry, J. P., Buckley, J., & Gray, I. (1998). The antioxidative properties of rosemary oleoresin and inhibition of off-flavour in precooked roast beef slices. Journal of the Science and Food and Agriculture, 77(2), 235–243. Nicolalde, C., Stetzer, A. J., Tucker, E. M., McKeith, F. K., & Brewer, M. S. (2006). Antioxidant and modified atmosphere packaging prevention of discoloration in pork bones during retail display. Meat Science, 72, 713–718. Nijveldt, R. J., van Nood, E., van Hoorn, D. E. C., Boelens, P. G., van Norren, K., & van Leeuwen, P. A.M. (2001). Flavonoids: A review of probable mechanisms of action and potential applications. American Journal of Clinical Nutrition, 74, 418–425. Nute, G. R. (2002). Sensory analysis of meat. In J. P. Kerry, J. F. Kerry, & D. Ledward (Eds.), Meat processing: Improving quality (pp. 175–192). Cambridge: Woodhead Publishing. Pereira de Abreu, D. A., Paseiro Losada, P., Maroto, J., & Cruz, J. M. (2010). Evaluation of the effectiveness of a new active packaging film containing natural antioxidants (from barley husk) that retard lipid damage in frozen Atlantic salmon (Salmo salar L.). Food Research International, 43(5), 1277–1282. Purchas, R. W., & Aungsupakorn, R. (1993). Further investigations into the relationship between ultimate pH and tenderness for beef samples from bulls and steers. Meat Science, 34(2), 163–178. Sammel, L. M., & Claus, J. R. (2006). Citric acid and sodium citrate effects on pink color development of cooked ground turkey irradiated pre- and post-cooking. Meat Science, 72, 567–573. Savell, J. W., Branson, R. E., Cross, H. R., Stiffler, D.M., Wise, J. W., Griffin, D. B., & Smith, G. C. (1987). National consumer retail beef study: Palatability evaluations of beef loin steaks that differed in marbling. Journal of Food Science, 52(3), 517–519. Siripatrawan, U., & Harte, B. R. (2010). Physical properties and antioxidant activity of an active film from chitosan incorporated with green tea extract. Food Hydrocolloids, 24, 770–775.
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Tareen, M. J., Abbasi, N. A., & Hafiz, I. A. (2012). Postharvest application of salicylic acid enhanced antioxidant enzyme activity and maintained quality of peach cv. ‘Flordaking’ fruit during storage. Scientia Horticulturae, 142, 221–228. Tarlagdis, B. G., Watts, B.M., & Younathan, M. T. (1960). A distillation method for the quantitative determination of malonaldehyde in rancid food. The Journal of the American Oil Chemists' Society, 37, 44–48. Thompson, J. (2002). Managing meat tenderness. Meat Science, 62, 295–308. Vareltzis, P., Hultin, H. O., & Autio, W. R. (2008). Hemoglobin-mediated lipid oxidation of protein isolates obtained from cod and haddock white muscle as affected by citric acid, calcium chloride and pH. Food Chemistry, 108, 64–74. Villarroel, M., María, G. A., Sañudo, C., Olleta, J. L., & Gebresenbet, G. (2003). Effect of transport time on sensorial aspects of beef meat quality. Meat Science, 63, 353–357.
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Contents lists available at ScienceDirect
Meat Science journal homepage: www.elsevier.com/locate/meatsci
Effect of an active packaging with citrus extract on lipid oxidation and sensory quality of cooked turkey meat Claudia Contini a, Rocío Álvarez b, Michael O'Sullivan a, Denis P. Dowling c, Sean Óg Gargan c, Frank J. Monahan a,⁎ a b c
UCD School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland Agroforestry Science Department, University of Seville, Seville, Spain UCD School of Mechanical and Materials Engineering, University College Dublin, Belfield, Dublin 4, Ireland
a r t i c l e
i n f o
Article history: Received 14 June 2013 Received in revised form 19 September 2013 Accepted 4 November 2013 Keywords: Active packaging Citrus extract Lipid oxidation Turkey meat Sensory analysis
a b s t r a c t An antioxidant active packaging was prepared by coating a citrus extract, consisting of a mixture of carboxylic acids and flavanones, on polyethylene terephthalate trays. The effect of the packaging in reducing lipid oxidation in cooked turkey meat and on meat pH, colour characteristics and sensorial parameters was investigated. An untrained sensory panel evaluated the odour, taste, tenderness, juiciness and overall acceptability of the meat, using triangle, paired preference and quantitative response scale tests. A comparison between the antioxidant effects of the different components of the extract was also carried out. The packaging led to a significant reduction in lipid oxidation. After 2 days of refrigerated storage the sensory panel detected differences in odour and, after 4 days, rated the meat stored in the active packaging higher for tenderness and overall acceptability. Citric acid appeared to be the most important component of the extract with regard to its antioxidant potency. © 2013 Elsevier Ltd. All rights reserved.
1. Introduction Lipid oxidation represents one of the major causes of the progressive deterioration in the quality of meat products, limiting their storage shelf life. The deterioration in organoleptic characteristics, and the associated loss of nutritional value induced by the oxidative process, can be delayed by the addition of antioxidants. Natural substances with antioxidant activity have been widely studied as food preservatives; these include flavonoids, phenolic acids, organic acids and carotenoids, which can reduce lipid oxidation by scavenging free radicals, chelating metal ions or quenching oxygen radicals (Brewer, 2011; Murphy, Kerry, Buckley, & Gray, 1998; Nijveldt et al., 2001; Yanishlieva, Marinova, & Pokorný, 2006). Beneficial effects on the oxidative stability and organoleptic properties of food have been found for grape seed extract in cooked ground beef (Ahn, Grün, & Fernando, 2002), green tea and grape seed extract in beef patties (Bañón, Díaz, Rodríguez, Garrido, & Price, 2007), oregano essential oil in chicken breast meat (Chouliara, Karatapanis, Savvaidis, & Kontominas, 2007) and rosemary extract in beef (Lee, Decker, Faustman, & Mancini, 2005; McBride, Hogan, & Kerry, 2007). The inclusion of natural extracts with antioxidant activity within the packaging material can protect food from lipid oxidation, thus ⁎ Corresponding author. Tel.: +353 1 716 2842. E-mail address: [email protected] (F.J. Monahan). 0309-1740/$ – see front matter © 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.meatsci.2013.11.007
increasing its shelf-life (Siripatrawan & Harte, 2010; Wessling, Nielsen, & Giacin, 2000). Active antioxidant packaging for meat products has been prepared with oregano and rosemary extracts (Camo, Beltrán, & Roncalés, 2008) and barley husk extract (Pereira de Abreu, Paseiro Losada, Maroto, & Cruz, 2010). Another natural antioxidant, obtained from citrus extract and containing carboxylic acids and flavonoids, has been used in our laboratory as a coating on a polyethylene terephthalate (PET) based active packaging for cooked meats. The antioxidant coated trays were shown to be effective in reducing lipid oxidation, as assessed by 2-thiobarbituric acid-reactive substances (TBARS) and hexanal content, in cooked turkey breast meat during refrigerated storage (Contini et al., 2012). Chemical methods can be suitable tools for the evaluation of the level of oxidation in meat (Laguerre, Lecomte, & Villeneuve, 2007) with, for example, the quantification of hexanal, a product of the oxidation of linoleic acid, being commonly used as indicator of lipid oxidation in meat (Gandemer, 2002). The perception of the quality of a product, however, also depends on sensory characteristics like palatability, colour, texture and flavour, which can be evaluated only through sensory analysis assessments (Nute, 2002). In the present study, a citrus extract based active packaging tray, suitable for cooked meat is evaluated for its antioxidant efficacy, using the TBARS assay. Its effect on the colour parameters of meat, was determined instrumentally, and its effect on sensorial characteristics was assessed using sensory panel tests. Furthermore, the contribution of the principal components of
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the citrus extract to the total antioxidant effect of the active packaging was evaluated. 2. Materials and methods 2.1. Reagents A dried citrus extract containing a mixture of flavanones and carboxylic acids was obtained from Citrox Ltd., Middlesbrough, England. Methanol (≥99%), citric acid (CA, ≥99%), naringin (NA, ≥95%), neohesperidin (NEO, ≥90%), salicylic acid (SA, ≥99%), thiobarbituric acid (TBA, 98%), 1,1,3,3-tetraethoxypropane (TEP, ≥96%) and acetic acid (≥98%) were purchased from Sigma-Aldrich Ltd., Dublin, Ireland. Recycled polyethylene terephthalate (PET) trays (100 × 150 × 25 mm) were supplied by Holfeld Plastic, Co. Wicklow, Ireland. A low density polyvinylchloride (PVC) catering film (thickness 7.0 μm; O2 transmission 2000 cm3 m−2 day−1 bar−1) was obtained from Western Plastic Ltd., Galway, Ireland. 2.2. Preparation of turkey meat and PET coated trays Turkey breast meat was supplied by IGWT Poultry Service Ltd. (Co. Monaghan, Ireland). The meat was cooked in an oven to an internal temperature of 73 °C using the procedure described in Contini et al. (2012), cut into 5 mm slices with a meat slicer (Medoc, Logroños, Spain) and subsequently cut into 3 g square (30 mm × 30 mm) pieces. The coated PET trays (PET-CIT) were prepared by spraying a 100 mg ml− 1 methanolic solution of citrus extract through a Teflon nebulizer mounted on a computer numerical control system cncGraf (Boenigh Electronics, Bonn, Germany), following the procedure described in Contini et al. (2012). The amount of the citrus extract coated on the tray surface, calculated gravimetrically, was 0.46 mg cm−2 (Contini, 2013). Nine pieces of meat were placed on each PET (control) and PET-CIT tray, overwrapped with PVC film and stored for 4 days at 4 °C. 2.3. Sensory evaluation To evaluate sensory quality differences between meat stored on PET and on PET-CIT trays, sensory evaluation of the cooked turkey meat was carried out using triangle, paired preference and quantitative response scale tests. Eighteen untrained panellists (students and staff of the School of Agriculture and Food Science at University College Dublin) were recruited. For each sensory test, the meat samples were put in white, opaque containers and coded using three-digit numbers chosen randomly for each test. The sensory analysis was performed at day 0, day 2 and day 4 of storage, for which meat was removed from trays and kept at room temperature for 30 min before being served to the panel. All sessions were carried out in a sensory analysis laboratory equipped with individual testing booths and controlled lighting to neutralize any possible differences in colour or appearance of the meat. A single turkey breast was used for each sensory test to avoid differences not related to the packaging. Each sensory test was repeated three times, using three different turkey breasts. The triangle test (ISO 4120: 2004) was carried on olfactory and taste parameters. Assessors were asked to smell and taste one different and two identical samples of meat in the same session and instructed to indicate the odd sample. Results were compared with tables of minimum number of correct responses required for significance (ISO 4120: 2004). The paired preference test (ASTM E2263, 2012) was used to determine an overall preference between meat stored on the PET and on the PET-CIT trays. For this, assessors were asked to smell and taste the two meat samples and forced to indicate which one they preferred. The presentation order, as well as the numbering of the samples, was randomized for each assessor. Results were compared with tables of the number of common responses needed for significance (ASTM E2263, 2012). In the quantitative response scale test (ISO 4121: 2003-
E) the panellists were asked to smell and taste the meat stored on the PET and the PET-CIT trays and evaluate its juiciness, tenderness, flavour and overall acceptability. Each assessor evaluated these characteristics on a standard 9-point hedonic scale from 1 to 9, where 1 corresponded to extremely dry, extremely tough, extremely tasteless and extremely unsatisfactory and 9 corresponded to extremely juicy, extremely tender, extremely tasty and extremely satisfactory. 2.4. Lipid oxidation assay, pH determination and colour measurement in cooked turkey meat Lipid oxidation, pH and colour measurements on turkey meat stored on the PET and PET-CIT trays for 0, 2 and 4 days were made in parallel to the sensory analysis. Lipid oxidation was measured using the distillation method described by Tarlagdis, Watts, and Younathan (1960) and expressed as TBARS values in mg malonaldehyde kg−1 meat. A malonaldehyde standard curve was prepared using TEP. A Hanna pH meter HI120 (Leighton Buzzard, Belfordshire, England) was used to measure the pH of 1 g samples of meat homogenized in 9 ml of distilled water using an Ultra Turrax T25 (Janke & Kunkel IKA-Labortechnik). Surface meat colour was measured using a reflectance Minolta CR-400 colorimeter (Osaka, Japan) according to CIE (1986). The measurement was carried out under illuminant D65, 10° observer angles and following instrument calibration using a white tile. The chromaticity coordinates recorded were L* (Lightness), a* (redness) and b* (yellowness). The value for each of these parameters was calculated as the average of three measurements. 2.5. Preparation of turkey meat with added citrus extract compounds The antioxidant effect of the citrus extract constituents was evaluated by adding specific quantities of each, in methanolic (NA, NEO and SA) and aqueous (CA) solutions, directly to 3 g of cooked turkey meat ground through an OMAS mincer plate with 4 mm diameter holes (Varese, Italy). The specific quantities added corresponded to the amounts of each citrus extract component coated on the tray surface in contact with the meat, calculated in a previous experiment (Contini, 2013). The values calculated were: 345 μg g−1 meat for CA, 497 μg g−1 meat for SA, 20 μg g−1 meat for NA and 19 μg g−1 meat for NEO. The substances were added in the following combinations: NA, NEO, SA and CA (solutions with single components); NA + NEO, NA + CA, NA + SA, NEO + CA, NEO + SA and CA + SA (solutions with a combination of two components); NA + NEO + SA, NA + NEO + CA, NA + CA + SA and NEO + SA + CA (solutions with a combination of three components). The antioxidant activity of the different combinations of citrus extract components were compared to the values for meat stored without antioxidants (control) and those obtained with a solution of all the antioxidants (NA + NEO + CA + SA). Lipid oxidation was measured in all samples by the TBARS assay immediately (day 0) and after 2 and 4 days of storage at 4 °C. 2.6. Statistical analysis Three separate turkey breasts were used for each experiment and the results of the analysis were expressed as mean ± standard deviation of three repetitions. A one-way analysis of variance (ANOVA) and Tukey's post hoc test was performed to determine significant differences between the treatments, using SPSS (version 18) statistical software (IBM Inc. Chicago, IL, USA). 3. Results and discussion 3.1. Measurement of pH, oxidation levels and colour of meat Storage on PET-CIT trays affected the pH of meat, which was significantly lower (p b 0.01) in meat on the PET-CIT trays compared
C. Contini et al. / Meat Science 96 (2014) 1171–1176 Table 1 pH, TBARS (mg MDA kg−1 meat) and colour variables (L*, a*, b*) of cooked turkey meat stored on PET and PET-CIT trays at 4 °C and assessed at day 0, day 2 and day 4. x,y,zWithin each treatment, values with different letters are significantly different due to the storage a,b time. Within each storage time, values with different letters are significantly different due to the treatment. Analytical parameters
Meat samples
Day 0
pH
PET PET-CIT PET PET-CIT PET PET-CIT PET PET-CIT PET PET-CIT
6.27 5.98 1.14 0.72 75.74 74.96 4.24 4.18 8.17 11.20
mg MDA/kg meat L* a* b*
± ± ± ± ± ± ± ± ± ±
Day 2
Day 4
6.33 ± 0.38az 0.07bz 0.12az 6.10 ± 0.29az 0.06bx 4.67 ± 0.34by 0.37ax 2.02 ± 0.83ay 0.82az 75.76 ± 1.57bz 1.54az 73.54 ± 1.15az 0.52az 1.79 ± 0.47ay 0.47az 4.20 ± 0.63bz 0.36ay 9.28 ± 0.88az 0.91bz 10.00 ± 1.45az
6.06 5.89 6.29 2.85 76.31 76.34 1.96 2.84 10.07 10.50
± ± ± ± ± ± ± ± ± ±
0.10bz 0.07az 0.82bz 0.12az 1.16az 0.88az 1.34ay .22az 0.44az 0.87az
to meat on the PET trays at day 0 and day 4 (Table 1). Previous studies in our laboratory have shown that antioxidant components are released from the coating on the trays into the meat as soon as the meat comes in contact with the trays (Contini, 2013). The early release of citric and salicylic acid therefore most likely accounts for the lower pH value found throughout the storage period. Lipid oxidation values (TBARS) in meat stored on PET trays progressively increased from 1.14 ± 0.06 to 6.29 ± 0.82, with significantly higher values at day 2 compared to day 0 (p b 0.01) and at day 4 compared to day 2 (p b 0.01). This is in accordance with previous studies on the oxidation of cooked turkey meat (Caprioli, O'Sullivan, & Monahan, 2009; Mielnik, Olsen, Vogt, Adeline, & Skrede, 2006). Storage on PET-CIT trays led to a significant (p b 0.01) reduction in lipid oxidation, with TBARS values less than half those of samples stored on the control PET trays after 2 and 4 days of storage (Table 1). The results of the colorimetric analysis of the meat samples showed that differences in L* (lightness) values between treatments were only significant at day 2 (p b 0.05), with meat on the PET-CIT trays having a lower value than that on the PET trays. Other studies have also shown that the addition of citric acid or citrus extracts resulted in a decrease of meat lightness and suggested that this may be linked to the pigments contained in the citrus extract or to changes in water retention of meat induced by citrus extract components (Ke, Huang, Decker, & Hultin, 2009; Nicolalde, Stetzer, Tucker, McKeith, & Brewer, 2006). The analysis of a* (redness) values showed a decrease in redness during storage from 4.24 ± 0.52 to 1.79 ± 0.47 in control samples on PET, with significantly lower (p b 0.01) values at days 2 and 4 compared to day 0. The PET-CIT trays were effective in lowering the reduction in a* value of meat which did not change significantly with storage and was significantly higher compared to control at day 2 (p b 0.01). A rapid decrease of meat redness as a consequence of lipid oxidation has been well documented, as well as the retardation of such a reduction being cited as among the benefits offered by treatments with antioxidants (Yu, Scanlin, Wilson, & Schmidt, 2002). The b* (yellowness) values of meat stored on PET trays showed a trend opposite to that of the a* values, with a progressive increase in yellowness with storage time, resulting in significantly higher values at days 2 and 4 compared to day 0 (p b 0.01). The PET-CIT treatment led to significantly higher initial b* values compared to the control samples (p b 0.01), although values were not significantly different thereafter. The higher initial b* values of meat stored on the PET-CIT trays, likely relates to pigments in the citrus extract, rather than to an effect on lipid oxidation (Fernández-López, Zhi, Aleson-Carbonell, Pérez-Alvarez, & Kuri, 2005). However, another study showed that CA can also be responsible for an increase in the b* value of cooked turkey meat (Sammel & Claus, 2006).
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3.2. Triangle test for the evaluation of odour and taste A triangle test was conducted to assess the perception of differences in odour and taste between the meat stored on PET and PET-CIT trays. The odour results showed that at day 0 only 5 out of 18 assessors correctly identified the samples, suggesting no significant differences were perceptible between meat stored on PET and PET-CIT trays (Table 2). However, the number of correct answers increased progressively with storage time to reach 11 correct answers out of 18 at day 4, which indicated a significant difference (p b 0.05) in odour between control meat and meat stored on the PET-CIT trays. Although the test did not reveal the nature of these odour differences, it likely relates to rancid odours produced by lipid oxidation, which is more pronounced in control meat. In fact, storage on the PET-CIT trays led to a signification reduction in TBARS levels of meat (Table 1), which has previously been correlated to a lower production of hexanal, an aldehyde associated with rancid odour (Brunton, Cronin, Monahan, & Durcan, 2000; Contini et al., 2012). Storage on the PET-CIT trays led to a reduction in lipid oxidation to TBARS values close to 2 mg MDA kg−1 of meat (Table 1), which is considered by some as a rancid flavour threshold in meat (Campo et al., 2006). Other studies have also reported that volatile aldehydes produced by lipid oxidation are largely responsible for the rancid odour of oxidized food (Fernando, Berg, & Grün, 2003; Jo, Ahn, & Byun, 2002), hence a lower content of such compounds could explain the differences in olfactory characteristics of meat observed using the triangle test. Previous studies also showed that, after 4 days, assessors in a panel test could perceive a less pronounced rancid odour in cooked turkey meat wrapped in caseinate/glycerol edible films as a result of the inhibition of lipid oxidation (Caprioli et al., 2009). Citrus extract coatings showed similar antioxidant effects on the odour of beef meat (Fernández-López et al., 2005). The results of the triangle test for meat taste indicated no significant difference in meat taste arising from storage on the two tray types (Table 2). A more pronounced difference in odour compared to the taste induced by oxidative degradation of fats can be explained by the low threshold of perception of the volatile aldehydes which therefore affect odours in meat at the earliest stage of their production (Mottram & Edwards, 2006).
3.3. Paired preference test A paired preference test was conducted to assess if one of the two meat samples had more acceptable sensory characteristics, expressed as generic preference, irrespective of the specific characteristics of the meat. The assessors were asked to express their preference on the odour and taste characteristics of the meat. Since a forced choice procedure was adopted, a sample was chosen even if the selection by the assessor was done randomly. It is worth noting that a preference is not an intrinsic attribute of the product, but rather a subjective measure relating to the respondents' affective or hedonic response (ASTM E2263, 2012). The meat stored on PET-CIT trays always received the highest number of preferences, with a statistically significant higher score (p b 0.05) at day 2, with 14 preferences out of 18 (Table 3).
Table 2 Sensory evaluation by triangle test of cooked turkey meat stored on PET and PET-CIT trays at 4 °C and assessed at day 0, day 2 and day 4. Results are expressed as correct answers/total answers. Sensory parameters
Day 0
Day 2
Day 4
Odour Taste
5/18 (ns) 5/18 (ns)
8/18 (ns) 5/18 (ns)
11/18 (p b 0.05) 6/18 (ns)
ns = not significant.
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Table 3 Sensory evaluation by paired preference test on the overall preference of cooked turkey meat stored on PET and PET-CIT trays at 4 °C and assessed at day 0, day 2 and day 4. Meat samples
Day 0
Day 2
Day 4
PET PET-CIT
7 11 (ns)
4 14 (p b 0.05)
7 11 (ns)
ns = not significant.
3.4. Quantitative response scale test on sensorial characteristics of meat The quantitative response scale test showed that the meat samples stored on the PET-CIT trays yielded numerically higher values for all four sensorial parameters assessed at all storage times, compared to the control samples on uncoated PET. For tenderness, the higher scores for meat stored on PET-CIT trays were statistically significant (p b 0.01) at day 4 (Table 4). This reflects two opposite trends with increase in storage time: a decrease in scores for meat stored on the PET trays and an increase in scores for meat stored on PET-CIT trays. A significant difference (p b 0.05) was found also for the overall acceptability of meat at day 4 of storage. The higher tenderness scores for meat stored on the PET-CIT trays may be related to the lower oxidation of meat. Lipid oxidation has been associated with a decrease in meat tenderness believed to be due to oxidation-induced cross-linking of proteins (Lund, Lametsch, Hviid, Jensen, & Skibsted, 2007; Xiong, Park, & Ooizumi, 2009). The higher tenderness score at day 4 might also be due to differences in pH value which were significantly lower in meat stored on PET-CIT trays at day 0 and day 4 compared to the control meat (Table 1). A relationship between pH and meat tenderness was also previously reported for beef meat, where the tenderness tended to decrease with an increase of pH from 5.5 to 6.1, followed by an increase at pH values above 6.1 (Villarroel, María, Sañudo, Olleta, & Gebresenbet, 2003) and was ascribed to changes in the structure of the muscle (Purchas & Aungsupakorn, 1993). The positive effect of the antioxidant active packaging on the tenderness of meat could therefore depend on the presence of organic acids contained in the citrus extract. The higher score at day 4 for overall acceptability of the meat is probably related to the tenderness, as highlighted by previous studies on sensory evaluation of meat, which found a high correlation between tenderness and overall acceptability (Thompson, 2002). Other studies have pointed out that in sensory tests overall preferences for meat are mostly driven by differences in tenderness and juiciness (Savell et al., 1987). 3.5. Direct addition of citrus extract components to meat The addition of single citrus extract components to minced meat provided an indication of the relative contribution of each of the components to the antioxidant activity of the packaging. The analysis at day 0 and day 2 showed a significant reduction in lipid oxidation (p b 0.01)
Table 4 Sensory evaluation by quantitative response scale test of cooked turkey meat stored on PET and PET-CIT trays at 4 °C and assessed at day 0, day 2 and day 4. a,bWithin each storage time, values with different letters are significantly different due to the treatment. zWithin each treatment, values did not differ significantly due to the storage time. Sensory parameters
Meat samples Day 0
Juiciness
PET PET-CIT PET PET-CIT PET PET-CIT PET PET-CIT
Tenderness Flavour Overall acceptability
4.72 5.72 5.33 5.39 5.11 5.94 5.56 6.06
± ± ± ± ± ± ± ±
Day 2 1.81az 1.60az 2.01az 1.88az 1.91az 1.31az 1.82az 1.70az
4.28 4.39 5.28 5.44 4.89 5.78 5.06 5.72
± ± ± ± ± ± ± ±
Day 4 1.81az 1.75az 1.81az 1.46az 1.88az 1.63az 1.83az 1.45az
4.06 4.67 4.44 6.06 5.11 5.61 5.17 6.06
± ± ± ± ± ± ± ±
1.92az 1.91az 2.04az 1.73bz 1.41az 1.65az 1.38az 1.31bz
when CA was added to the meat (Fig. 1). The other components did not show antioxidant activity (with the exception of the NA + NEO + SA combination) up to day 2, with values similar to, or higher than, the control packaging. At day 4, inclusion of all individual components and combinations thereof led to a significant reduction in lipid oxidation compared to the control (p b 0.01). Again, CA showed the highest antioxidant activity, with TBARS value significantly lower (p b 0.01) than those of the other components added individually or in the various combinations. The higher efficacy of citric acid compared to the flavanones may be due to its higher (at least 17-fold) level of addition (see Section 2.5). At day 4, CA alone was most effective in retarding lipid oxidation, suggesting that some of the other components may actually compromise its antioxidant efficacy (e.g. CA vs combinations of CA with one or more of NA, NEO and SA). The antioxidant efficacy of CA most likely relates to its properties as a metal chelator, which permits it to bind pro-oxidant metals via its carbonyl or hydroxyl groups (Francis, Dodge, & Gillow, 1992). Although citrus extracts could differ in their composition, several studies have assessed their ability to delay lipid oxidation in meat (Ke et al., 2009; Lee et al., 2005). In addition to metal chelating, other mechanisms have been proposed for the antioxidant activity of CA, including its effect in breaking down preformed peroxides (Vareltzis, Hultin, & Autio, 2008). These studies have also pointed out that the antioxidant activity of CA does not relate to acidification which, on the contrary, would promote lipid oxidation. Fewer studies are available on the antioxidant activity of SA, the other major component of citrus extract. Salicylic acid is present in plants as a regulator of growth processes and inhibits degradation processes by stimulating antioxidant enzyme activity thus reducing free radical formation (Tareen, Abbasi, & Hafiz, 2012). The limited antioxidant effect found for SA is in agreement with the finding of Brettonet, Hewavitarana, DeJong, and Lanari (2010) which showed the ability of SA to reduce TBARS values of meat only in combination with other phenolic acids. In addition, in the present study, antioxidant enzyme activity in muscle would have been inactivated by the heat treatment, making any stimulating effect of SA on antioxidant enzymes redundant. Flavanones like NA and NEO are well known for their strong antioxidant activity as free radical scavengers (Nijveldt et al., 2001) and other flavonoids have already been used with success as active substances in antioxidant active packaging for food preservation (Chen, Lee, Zhu, & Yam, 2012). The relatively low contribution of NA and NEO to the total antioxidant effect of the packaging might therefore be due to their relative low level of occurrence in the citrus extract composition used herein, rather than a low effectiveness in reducing lipid oxidation processes per se.
4. Conclusion This study shows that antioxidant active packaging with citrus extract is effective in reducing the lipid oxidation of cooked turkey meat during storage and in maintaining its sensory characteristics, particularly tenderness and overall acceptability. The increase in tenderness could be due to reduction in lipid oxidation of meat stored in the active packaging and to lower pH values leading to modifications in the muscle structure. Citric acid was the main driver of antioxidant activity amongst the citrus extract components. These findings show that trays coated with citrus extract have potential to prolong the consumer acceptability of cooked meat products.
Acknowledgments This work was undertaken within the Precision Strategic Research Cluster supported by the Science Foundation Ireland grant 08/SRC/ I1411.
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Fig. 1. Effect of the direct addition of citrus extract components on lipid oxidation (TBARS values) in cooked minced meat stored at 4 °C and assessed at day 0, day 2 and day 4 of storage. a,b,c,d,e,f,gWithin each storage time, values with different letters are significantly different due to treatment (p b 0.01). x,y,zWithin each treatment, values with different letters are significantly different due to storage time (p b 0.05). CA, citric acid; NA, naringin; NEO, neohesperidin; SA, salicylic acid.
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