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Combined effect of freeze chilling and MAP on quality parameters of raw chicken fillets
ARTICLE IN PRESS Food Microbiology 25 (2008) 575– 581
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Combined effect of freeze chilling and MAP on quality parameters of raw chicken fillets A. Patsias, A.V. Badeka, I.N. Savvaidis, M.G. Kontominas Laboratory of Food Chemistry and Microbiology, Department of Chemistry, University of Ioannina, Ioannina 45110, Greece
a r t i c l e in fo
abstract
Article history: Received 10 October 2007 Received in revised form 15 February 2008 Accepted 17 February 2008 Available online 2 March 2008
The effect of short-term frozen storage prior to thawing on the quality of freeze-chilled chicken fillets was investigated, as was the effect of modified atmosphere packaging (MAP). Four process treatments were used: (1) fresh chicken chilled at 4 1C without previous freezing, (2) freeze-chilled for 7 days and thawed at 4 1C, (3) chilled at 4 1C packaged under MAP (70% N2–30%CO2), and (4) packaged under MAP, freeze-chilled for 7 days and thawed at 4 1C. Microbiological, chemical and sensory analyses were conducted on samples for a period up to 15 days. Freeze-chilled fillets gave a lower total viable count (TVC) at a given sampling day than chilled fillets. MAP, as expected, delayed microbial growth. The Pseudomonads were the dominant microbial species in fillets under aerobic conditions. MAP reduced the populations of Pseudomonads by 2–4 log cfu/g. Lactic acid bacteria (LAB) and Enterobacteriaceae increased progressively for all treatments throughout storage. Yeasts and molds were inhibited by MAP and by freeze chilling. Total volatile basic nitrogen (TVB-N) values increased rapidly for the chilled fillets but remained significantly lower for the freezechilled and the MA-packaged samples. MAP and especially freeze chilling enhanced drip loss. MAP did not affect redness or yellowness of product while freeze chilling decreased product redness. Lightness was not affected by either MAP or freeze chilling. Based on taste, which proved to be the most sensitive sensory attribute, shelf life of product ranged from 6 to 7 days for all treatments leading to the conclusion that freeze chilling is a suitable technology for fresh chicken fillets enabling their distribution as a frozen product and upon subsequent thawing at their final destination, their retail display as chilled products. MAP in combination with freeze chilling had a negligible effect on product quality. & 2008 Published by Elsevier Ltd.
Keywords: Freeze chilling Modified atmosphere packaging Chicken fillets
1. Introduction Even though the effects of both chilling and freezing of foods are well documented (International Institute of Refrigeration, IIR, 1986), the effects of freeze chilling on quality of foods have only recently been systematically investigated (Guldager et al., 1998; Bøknaes et al., 2000; O’Leary et al., 2000; Martinsdottir and Magnusson, 2001; Emborg et al., 2002; Fagan et al., 2003; Redmond and Gormley, 2003; Redmond et al., 2004; Redmond et al., 2005). Freeze chilling involves initial freezing of a foodstuff with frozen storage being followed by thawing and distribution of the product at chill temperatures. Freeze chilling has already been commercially used at the retail level for chilled pre-packaged raw fish fillets which are replacing the traditional iced fish counter in supermarkets (Fagan et al., 2002). Freeze chilling offers a number of advantages over both frozen and chilled products such as (a)
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foodstuffs can be prepared in bulk, frozen and stored at deep freeze temperatures until required. Subsequently, a part or the whole batch of product can be thawed and further processed; (b) freeze chilling enables chilled foods to reach distant markets in the form of frozen product which is subsequently thawed at its final destination prior to retail display as a chilled food; (c) freeze chilling can reduce the level of product recalls enabling routine microbiological testing to be completed before the product is released from the manufacturing plant (Fagan et al., 2003). Work so far on freeze chilling has been limited to its application to fish (whiting, mackerel, salmon, Fagan et al., 2003; salmon and cod, Magnusson and Martinsdottir, 1995; Guldager et al., 1998; Bøknaes et al., 2000, 2001, 2002; Emborg et al., 2002), ready to eat meals such as lasagne (Redmond et al., 2005), steamed broccoli and instant mashed potatoes (O’Leary et al., 2000; Redmond et al., 2002) and cooked green beans and carrots (Redmond et al., 2004). Modified atmosphere packaging (MAP) has gained considerable popularity over the last decades as a modern non-thermal method of food preservation. The proper combination of gases
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(CO2, N2, and O2) in the headspace of food packs results in inhibition of spoilage microorganisms of perishable foods such as meat, fish and related products, developed under aerobic conditions and retention of their sensorial attributes (Davies, 1995). A minimum CO2 concentration of 20–30% is necessary to exhibit an inhibitory effect. (Stiles, 1991). An extended storage-life of poultry meat under low O2, high CO2 concentrations is observed because the spoilage caused by lactic acid bacteria (LAB) occurs later as compared to the spoilage caused by aerobic bacteria such as Pseudomonas spp. that prevail under aerobic conditions. In general, the defect caused by LAB is described as ‘‘souring’’, which is less offensive than the putrefaction that develops aerobically (Stiles, 1991). Microflora and spoilage pattern of chicken carcasses packaged under CO2 conditions are similar to those observed for red meat (Gill, 1986). Poultry meat is a very popular food commodity around the world and its consumption has increased over the last decades in many countries. Some of the reasons for its popularity are relatively low cost of production, low fat content, high nutritional value, distinct flavor and a variety of processed poultry products commercially available (Barbut, 2002). Poultry meat is a highly perishable food commodity providing an almost perfect medium for microbial growth (Jay, 1992) and it is thus of utmost importance for the poultry industry to develop new and effective methods of preservation to extend product shelf life (Chouliara et al., 2007, 2008). Given that no information exists in the literature on the application of either freeze chilling or the combination of freeze chilling and MAP to raw chicken meat, the objective of the present work was to investigate both the effect of short-sterm freeze chilling and the combined effect of freeze chilling and MAP on quality attributes of raw chicken breast fillets. A second objective was to determine product shelf life using above treatments.
2. Materials and methods 2.1. Sample preparation and treatment Chicken breast fillets (300 g/fillet) were prepared in a local poultry plant (Pindos SA, Ioannina, Greece) immediately after slaughter, packaged as described below and blast frozen at 40 1C for 3 h. Frozen samples were kept at this temperature for 7 days and allowed to thaw at refrigeration temperature (471 1C for 9 h) where they were kept for an additional period of 9 days (treatments 1 and 2) or 15 days (treatments 3 and 4). Four lots of samples were prepared: 1. chilled at 4 1C without previous freezing; 2. freeze-chilled and thawed as described above; 3. chilled at 4 1C and packaged under modified atmosphere (70% N2:30% CO2); 4. packaged under modified atmosphere (70% N2:30% CO2), freeze-chilled and thawed as described above.
(Ringsted). Fillets to be packaged aerobically were packaged in a polyethylene film, 75 mm in thickness, having an oxygen permeability of 4600 mL/(m2 day atm) at 60% RH/25 1C and a water vapor permeability of 1.75 g/(m2 day atm) at 100% RH/25 1C. 2.1.1. Sample analysis Samples 1 and 2 were tested at sampling days 0, 3, 5, 7, and 9 while samples 3 and 4 were tested at sampling days 0, 3, 5, 7, 9, 12, and 15. 2.2. Microbiological analyses The following groups of microflora were monitored: TVC, Pseudomonads, Enterobacteriaceae, LAB, yeasts and molds as well as Salmonella spp and Listeria monocytogenes. A sample (25 g) was removed aseptically using a scalpel and forceps from the chicken breast fillet, transferred to a stomacher bag (Seward Medical, UK), containing 225 ml of sterile quarterstrength Ringer’s solution, and homogenized using a stomacher (Lab Blender 400, Seward Medical) for 60 s at room temperature. For microbial enumeration, 0.1 mL samples of serial dilutions (1:10, diluent, quarter-strength Ringer’s solution) of chicken homogenates were spread on the surface of dry media. Total viable counts (TVC) were determined using plate count agar (PCA; Merck, Denmark, Germany), after incubation for 3 days at 30 1C. Pseudomonads were determined on cetrimide fusidin cephaloridine agar (oxoid supplemented with selective supplement SR 103, Oxoid, Basingstoke, UK) after incubation at 25 1C for 2 days (Mead and Adams, 1977). For members of the Enterobacteriaceae family, 1.0 mL sample was inoculated into 10 mL of molten (45 1C) violet red bile glucose agar (Oxoid). After setting, a 10 mL overlay of molten medium was added and incubated at 30 1C for 24 h. The large colonies with purple haloes were counted (Mossel et al., 1979). Lactic acid bacteria were determined on de Man Rogosa Sharpe medium (Oxoid) after incubation at 25 1C for 5 days. Yeasts and molds were enumerated using rose bengal chloroamphenicol agar (RBC; Merck) after incubation at 25 1C for 3 days in the dark. All plates were examined visually for typical colony types and morphological characteristics associated with each growth medium. In addition, the selectivity of each medium was checked routinely by Gram staining and microscopic examination of smears prepared from randomly selected colonies from all of the media. Salmonella was determined according to ISO6579, 2002. L. monocytogenes was determined according to ISO11290-1, 1996. 2.3. Chemical analysis The pH value was recorded using a Metrohm, model 691, pH meter. Chicken samples were thoroughly homogenized with 10 ml of distilled water and the homogenate used for pH determination. Total volatile basic nitrogen (TVB-N) was determined according to the method of Malle and Poumeyrol (1989). 2.4. Physical testing
Fillets to be packaged under modified atmosphere were placed in low-density polyethylene/polyamide/low-density polyethylene (LDPE/PA/LDPE) barrier pouches (1 fillet/pouch), 75 mm in thickness having an oxygen permeability of 52.2 mL/(m2 day atm) at 60% RH/25 1C and water vapor permeability of 2.4 g/(m2 day) at 100% RH/25 1C. Gas mixtures were prepared using a PBI-Dansensor model 9000 gas mixer (Ringsted, Denmark). Pouches were heatsealed using a BOSS model N48 vacuum sealer (Boss GmbH, Germany). Gas concentrations in packages were determined using a PBI, model Checkmate 9900 headspace analyzer instrument
Color determination was carried out on the surface of breast chicken meat using a Hunter Lab, model DP-9000, optical sensor colorimeter (Hunter Associates Laboratory, Reston, VA, USA) as described by Du et al. (2002). The quantity of drip released from fillets after storage was measured by removal of the product from the pre-weighed pouch and reweighing. Drip loss was expressed as a percentage of the initial weight of the packaged product (Kotzekidou and Bloukas, 1996).
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2.5. Sensory evaluation At all sampling days, samples destined for sensory evaluation were frozen. Chicken breast samples (ca. 100 g) were cooked in a microwave oven at high power (700 W) for 4 min including time of defrosting. An untrained panel of 17 judges experienced in chicken evaluation was used for sensory analysis. Panelists were asked to evaluate taste and odor of cooked samples. Along with the test samples, the panelists were presented with a freshly thawed chicken sample, stored at 40 1C throughout the experiment, this serving as the reference sample. Acceptability of odor and taste was estimated using a scale ranging from 9 to 0, with 9 corresponding to the most liked sample and 0 corresponding to the least liked sample. A score of 5 was taken as the lower limit of acceptability. 2.6. Statistical analysis Experiments were replicated twice on different occasions with different chicken samples. Analyses were run in triplicate for each replicate (n ¼ 2 3). Microbiological data were transformed into logarithms of the number of colony forming units (cfu/g) and were subjected to analysis of variance (ANOVA). Trial results were analyzed as 4 treatments 6 replicates. Means and standard deviations were calculated and when F values were significant at the Po0.05 level, mean differences were separated by the least significant difference (LSD) procedure.
3. Results and discussion 3.1. Microbiological analyses TVC values for the four different treatments as a function of storage time are shown in Fig. 1A. Initial TVC values in the range of 4.3–4.6 log cfu/g are indicative of good quality chicken meat. These values are in excellent agreement with those of Balamatsia et al. (2006) (4.29 log cfu/g) for chicken breast fillets, Chouliara et al. (2007, 2008) (4.28 log cfu/g) for chopped chicken breast meat and Chouliara et al. (2007, 2008) (4.3 log cfu/g) for chunks of chicken breast meat but significantly lower than those of Kakouri and Nychas (1994) (6.74 log cfu/ml) for chicken breast fillet most probably owed to cross contamination during preparation. Chilled fillets reached 7 log cfu/g, related to the upper microbiological limit for fresh poultry meat, as defined by the ICMFS (1986) after 5–6 days while freeze-chilled fillets reached the same value after approximately 8 days of storage. In turn, chilled fillets under MAP reached a TVC of 7 log cfu/g after approximately 10 and 12 days, respectively. It was anticipated that freeze chilling would produce a higher TVC as freezing opens up product structure resulting in more drip than chilling alone (Fagan et al., 2003). However, present data did not support this postulation as freeze-chilled fillets gave a lower TVC (Po0.05) at a given sampling day than chilled fillets. MAP, as expected, delayed microbial growth as a large portion of the spoilage microflora of chicken meat, mainly pseudomonads, are aerobic being inhibited by high CO2 concentrations (Farber, 1991). This statement is supported by data in Fig. 1B. Fagan et al. (2003) reported statistically insignificant differences between TVC for chilled and freeze-chilled whiting fillets (5.54 log cfu/g vs. 5.24 log cfu/g) and mackerel fillets (5.34 log cfu/g vs. 5.14 log cfu/g) after 3 days of storage. Similarly, statistically insignificantly differences between chilled and freeze-chilled salmon portions (7.36 log cfu/g vs. 7.56 log cfu/g) were reported after 5 days of storage at 4 1C. In contrast O’Leary et al. (2000),
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reported a higher TVC for freeze-chilled than chilled steamed salmon (3.62 log cfu/g vs. 2.68 log cfu/g) after 5 days of refrigerated storage. Similarly, Redmond et al. (2005) reported a higher TVC for freeze-chilled as compared to chilled beef lasagne (4.03 s, 1.95 log cfu/g) after 7 days of storage at 4 1C. The Pseudomonads (Fig. 1B) were the dominant microbial species in chicken fillets under aerobic packaging conditions. Interestingly, freeze chilling gave a lower (Po0.05) count of Pseudomonads than chilled samples by approximately 0.5–1.5 log cfu/g throughout storage. As mentioned previously, this was not anticipated given the effect of freezing on meat structure. Significantly lower (Po0.05) counts of Pseudomonads by approximately 2–4 log cfu/g of MA-packaged samples as compared to air-packaged samples were recorded throughout the entire storage period. Such a trend was anticipated given the strictly aerobic nature of Pseudomonads (Balamatsia et al., 2007; Chouliara et al., 2007, 2008). After 9 days of storage, freeze-chilled samples under MAP gave a lower Pseudomonads count (Po0.05) than chilled samples under MAP by approximately 1 log cfu/g. This difference remained until day 15 of storage. The reason for such a behavior is not clear requiring further investigation. Above results with regard to the effect of MAP are in good agreement with those of Skandamis and Nychas (2002) who reported a reduction of 3 log cfu/ml in beef stored under MAP after 6 days of storage at 5 1C as compared to control samples. Of the facultative anaerobic bacterial species, LAB constituted a part of the natural microflora of raw chicken meat stored both in air and under MAP (Fig. 1C). Initial (day 0) LAB counts determined were between 3.7 and 4 log cfu/g, increasing progressively with storage time attaining final counts of ca. 6.6 and 7.5 log cfu/g for freeze-chilled and chilled samples stored in air and ca. 6.1 and 7.4 log cfu/g for freeze-chilled and chilled samples stored under MAP, respectively. The behavior exhibited by LAB was fully anticipated given the fact that LAB are facultative anaerobic and are able to grow both in the presence and absence of oxygen. Patsias et al. (2006) reported a small reduction of about 1.7 log cfu/g in LAB populations in pre-cooked chicken products after 12 days of storage at 4 1C under MAP as compared to airpackaged pre-cooked samples. Skandamis and Nychas (2002) reported rapid growth of LAB in beef under MAP at 5 1C with no differences compared to air-packaged samples. Enterobacteriaceae, a large group of facultatively anaerobic bacteria, used as hygiene indicators, were found in low numbers (day 0) and progressively increased to approximately 6.5 log cfu/g in the air-chilled samples after day 9 of storage. In contrast, in freeze-chilled and MA-packaged samples, the population of Enterobacteriaceae remained below or equal to 5.5 log cfu/g throughout the entire storage period. Thus, both freeze chilling and MAP partly inhibited the growth of Enterobacteriaceae. MAP further inhibited Enterobacteriaceae, which reached a population of 3.6 and 5.2 log cfu/g after 15 days of storage for the freezechilled and chilled sample under MAP, respectively. Present results with regard to the effect of MAP are in agreement with those of Chouliara et al. (2007, 2008) who reported a 2–3 log cfu/g reduction of Enterobacteriaceae under various MAP conditions after 6 days of storage at 4 1C. Lastly, most yeasts and molds, aerobic in nature, increased from an initial value of 2.9–3.0 to 6.3 log cfu/g in the chilled airpackaged samples (Fig. 1E). They were, however, substantially inhibited by MAP reaching populations between 3 and 3.6 log cfu/g after 15 days of storage. Interestingly, yeasts and molds were also inhibited by freeze chilling reaching a population of 3.8–3.9 log cfu/g on day 9 of storage. With regard to MAP, present results are in general agreement with those of Balamatsia et al. (2007) who reported a decrease in yeasts by 3.1–4.1 log cfu/g for chicken
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Fig. 1. (A) Changes in total viable counts of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.17–0.55). (B) Changes in Pseudomonas spp. of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.11–0.61). (C) Changes in lactic acid bacteria of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.12–0.48). (D) Changes in Enterobacteriaceae of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freezechilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.08–0.44). (E) Changes in yeasts and molds of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.09–0.42).
breast fillets under MAP and VP as compared to air-packaged samples stored at 4 1C. A lower reduction effect of MAP on yeasts (0.5–1.0 log cfu/g) was reported by Chouliara et al. (2007, 2008) for chilled chicken breast meat after 6 days of storage at 4 1C. Neither Salmonella spp. or L. monocytogenes were detected in samples.
3.2. Chemical changes Differences in pH between chilled and freeze-chilled samples were not statistically significant (P40.05); pH values ranging between 5.9 and 6.1. Results were somewhat different for MA-packaged samples where statistically significant differences in pH were recorded after day 7 of storage. pH values varied
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between 6.1 and 5.6 for both chilled and freeze-chilled samples stored under MAP which was attributed to the production of lactic acid through LAB metabolism and CO2 dissolution in the aqueous phase of the chicken muscle (Farber, 1991). Present pH values, with regard to the effect of MAP, are in excellent agreement with those of Chouliara et al. (2007, 2008) who reported pH values between 5.9 and 6.4 for air and MA-packaged chopped chicken breast meat stored for 25 days at 4 1C. Results for TVB-N are shown in Fig. 2. The initial TVB-N value of 12 mg/100 g increased sharply in the chilled sample stored in air resulting in high TVB-N values (49 g/100 g) after 9 day of storage. The proposed upper limit of 30 mg/100 g (Bynn et al., 2003) as indicator of meat freshness for pork was exceeded between day 4 and 5 of storage for the chilled sample giving a reasonably good correlation of TVB-N with microbiological data (TVC). In contrast, the freeze-chilled sample stored in air and both the MA-packaged samples gave TVB-N values lower or equal to 25 mg/100 g throughout storage rendering TVB-N an unfit indicator of freeze-chilled chicken meat quality. Present TVB-N values are in general agreement with those of Balamatsia et al. (2006, 2007) who reported TVB-N values in the range of 54.5 mg/100 g for air-packaged chicken breast fillets after 15 days of storage at 4 1C. With regard to the effect of freeze chilling on TVB-N values, Fagan et al. (2003) did not observe statistically significant differences between chilled and freeze-chilled whiting and mackerel fillets after 3 days of storage and salmon portions after 5 days of storage.
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Table 1 Effect of freeze chilling and MAP on % drip loss of chicken breast fillets stored at 4 1C Storage time (days)
Chilled in Chilled under air MAP
Freeze-chilled in air
Freeze-chilled under MAP
0 9 15
0 3.970.2 –
12.070.5 11.570.6 –
11.570.8 – 10.670.5
0 – 5.870.3
Table 2 Effect of freeze chilling and MAP on color parameters of chicken breast fillets stored at 4 1C Storage time (days)
Chilled in Chilled under air MAP
Freeze-chilled in air
Freeze-chilled under MAP
L*-value 0 9 15
51.771.4 56.371.8 –
51.772.0 – 57.871.6
52.771.1 57.371.9 –
52.772.1 – 60.272.8
a*-value 0 9 15
3.970.1 3.970.2 3.270.2 – – 3.470.1
2.970.1 2.670.1 –
2.970.2 – 2.570.1
b*-value 0 9 15
12.670.3 12.670.4 12.970.2 – – 12.170.3
12.270.2 12.670.1 –
12.270.3 – 12.070.2
3.3. Physical testing The effect of specific treatment on % drip loss is shown in Table 1. Drip loss varied between 0% and 3.9% for the chilled product, and between 0% and 5.8% for the chilled product under MAP after 9 days of storage. MAP seemed to enhance moisture loss in the product possibly by decreasing the water holding capacity of proteins through pH drop due to CO2 dissolution in the aqueous phase of the product. As expected, drip loss in the freezechilled and the chilled under MAP product showed a different pattern starting from an initial high value of 11–12% on day 0 (immediately after thawing) attributed to the thawing process and retaining this range of values after 15 days of storage. Obviously, the effect of MAP was negligible as compared to the strong effect of freezing/thawing on drip loss. Present drip loss values are in general agreement with those of Fagan et al. (2003) who reported drip loss values for chilled and freeze-chilled
TVB N (mg/100g)
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Fig. 2. Changes in TVB-N values of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.33–2.1).
whiting (1% vs. 6%) and mackerel (2% vs. 4%) fillets after 3 days of storage and for salmon portions (1.7% vs. 3.2%) after 5 days of storage at 4 1C. They are also in agreement with that of Redmond et al. (2005), who reported centrifugal drip losses of 3.4% vs. 1.56% for freeze-chilled and chilled beef lasagne after 7 days of storage at 4 1C. These authors reported no effect of MAP on drip loss in the freeze-chilled product in accordance to our findings. Higher values of drip loss reported in the present study as compared to those reported for fish are probably justified by the higher final pH of fish (6.2–6.6) as compared to that of chicken (5.6–5.8) at which poultry proteins lose more moisture due to denaturation and aggregation occurring close to their isoelectric point (Lawrie, 1979). In fish, due to a higher final pH, the water holding capacity of the fish muscle suffers less moisture loss and thus drip loss is limited. The effect of specific treatment on color of chicken breast fillets is shown in Table 2. MAP did not affect the redness (a-value) or yellowness (b-value) for the chicken samples while freeze chilling resulted in decreased product redness. With regard to the effect of MAP, present trend of a- and b-values trend is in agreement with that found by Chouliara et al. (2007, 2008) who reported a-values between 3.3 and 5.3 and b-values between 9.2 and 11.4 for chicken breast fillets stored aerobically and under MAP at 4 1C. Lightness (L*-values) increased with time ranging between 51.7 and 60.2 but both MAP and freeze chilling did not affect (Po0.05) this color parameter. Similarly, Ahn and Lee (2004) reported no changes in L*- and a*-values for both aerobically and vacuumpackaged turkey breast meat during 15 days of storage. However, they reported an increase in b*-values in aerobically packaged samples. Such a trend was not observed in the present study. With regard to the effect of freeze chilling, Fagan et al. (2003) reported no differences in both L*- and a*-values between chilled and freeze-chilled whiting and mackerel fillets and only a small increase in yellowness (b-values). Regarding salmon fillets, they reported a slight decrease only in product lightness as compared to the chilled product. O’Leary et al. (2000) reported no significant
ARTICLE IN PRESS A. Patsias et al. / Food Microbiology 25 (2008) 575–581
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Fig. 3. (A) Changes in odor scores of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.14–0.69). (B) Changes in taste cores of chicken breast fillets stored at 4 1C chilled aerobically packaged (~), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.13–0.71).
changes in color parameters of freeze-chilled as compared to chilled salmon portions. Finally, Redmond et al. (2005) reported a brighter color (L*/b*) for freeze-chilled as compared to chilled lasagne.
3.4. Sensory evaluation The effect of specific treatment on sensory attributes (odor and taste) is shown in Fig. 3A and B. Scores for odor (Fig. 3A) showed a pattern of decreasing acceptability with storage time. Until day 3 of storage all four treatments received high scores between 8.4 and 8.8 beyond which odor scores for the chilled samples decreased at a higher rate than the rest of the samples. The limit of acceptability (score of 5) was reached after 8 days for the chilled product 9 days for the chilled MA-packaged product and 8–9 days for both the freeze-chilled products. Respective data for taste are given in Fig. 3B. Taste proved to be a more sensitive sensory attribute for the evaluation of chicken breast fillets with initial scores for the chilled product being higher (8.4–8.7) than those of the freeze-chilled product (7.8–8.0). Until day 3 of storage, all treatments received a similar taste score between 7.6 and 8.0. The limit of acceptability was reached after 6–7 days for the freeze-chilled sample under MAP, after 7 days for the chilled in air sample and after 6–7 days for the chilled sample under MAP and the freeze-chilled sample. MAP did not substantially affect both odor and taste of the product. Jiang and Lee (1985) found no statistically significant differences in preference or acceptability scores between chilled and freeze-chilled salmon portions.
Similarly, Fagan et al. (2003) found no statistical differences in odor scores between chilled and freeze-chilled whiting and mackerel fillets stored for 3 days at 4 1C. However, odor scores were higher for chilled salmon portions as compared to freezechilled counterparts (odor score 5.6 vs. 3.6) after 5 days at 4 1C. Taste scores were similar for all three fish products (chilled and freeze-chilled samples). Finally, Redmond et al. (2005) did not observe differences in sensory acceptability of beef lasagne between chilled and freeze-chilled product stored for 7 days at 4 1C. Sensory data (taste data being the most sensitive) correlate reasonably well with microbiological (TVC) for chilled and chilled under MAP samples. Correlation was poor for the two freezechilled samples. Based primarily on sensory data, it is suggested that the use of freeze chilling did not extend the shelf life of chicken breast fillets but provided the advantage of short-term frozen storage (40 1C, 7 days in the present study) enabling ‘‘chilled’’ products to reach foreign markets more easily. MAP did not substantially affect shelf life of freeze-chilled product. Lastly, an issue that should be addressed is that of freezechilled product safety as the thawed product has a more open structure (due to freezing damage) which along with the excess free moisture (drip loss) could enhance pathogens’ growth during the subsequent chilling phase. In addition freezing does not kill all the bacteria (Forsythe and Hayes, 1998), and psychrophiles will preferentially grow during subsequent chilling. It is, therefore, obligatory to follow the guidelines for chilled foods (Inst., Food Sci. and Tech., 1990) rather than for frozen during the manufacture, distribution, thawing and retailing of freeze-chilled products.
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Use of good manufacturing practices (GMP) and hazard analysis of critical control point (HACCP) should be complementary guidelines during these processes. In addition, routine checks for all potential pathogens should also be made to ensure product safety. Particular attention should be also focused on the thawing step and careful temperature control should be exercised (Fagan et al., 2003). In the use of poultry fillets, tempering can be achieved by transferring packages from the supermarket deep freezer to the chilled retail display cabinets in the evening time, while the thawed product will be obtained the following morning. With respect to labeling, it is desirable for reasons of consumer information to label the product as ‘‘previously frozen’’ given that freeze-chilled meat products cannot be domestically refrozen. An expiration date must also be used and such a label must be attached at the beginning of the thawing stage.
4. Conclusions Chicken breast fillets are a suitable product for freeze chilling. Products stored at 40 1C for 7 days followed by thawing and storage for 6–7 days at 4 1C were still found sensorily acceptable. Modified atmosphere packaging had a small impact on quality of freeze-chilled chicken breast fillets.
Acknowledgment The authors would like to thank Pindos S.A., Ioannina, Greece, for providing chicken samples. References Ahn, D.U., Lee, E.J., 2004. Mechanisms and prevention of off-odor production and color changes in irradiated meat. In: Komolprasert, V., Morehouse, K.M. (Eds.), Irradiation of Food and Packaging. Recent Developments, ACS Symposium Series 875, pp. 43–76. Balamatsia, C.C., Rogga, K., Badeka, A., Kontominas, M.G., Savvaidis, I.N., 2006. Effect of low dose irradiation on microbiological, chemical and sensory characteristics of chicken meat stored aerobically at 4 1C. J. Food Prot. 69, 1125–1133. Balamatsia, C.C., Patsias, A., Kontominas, M.G., Savvaidis, I.N., 2007. Possible role of volatile amines as quality indicating metabolites in MAP packaged chicken fillets: correlation with microbiological and sensory attributes. Food Chem. 104, 1622–1628. Barbut, S., 2002. Poultry Products Processing. An Industry Guide. CRC Press, London. Bøknaes, N., Østerberg, C., Nielsen, J., Dalgaard, P., 2000. Influence of freshness and frozen storage temperature on quality of thawed cod fillets stored in modified atmosphere packaging. Leban. Wiss. und. Technol. 33, 244–248. Bøknaes, N., Østerberg, C., Sorensen, R., Nielsen, J., Dalgaard, P., 2001. Effects of technological parameters and fishing ground on quality attributes of thawed, chilled cod fillets stored in MAP. Leban. Wiss. und. Technol. 34, 513–520. Bøknaes, N., Jensen, K.N., Guldager, H.S., Østerberg, C., Nielsen, J., Dalgaard, P., 2002. Thawed chilled Barents sea cod fillets in MAP—application of multivariate data analysis to select key parameters in good manufacturing practice. Leban. Wiss. und. Technol. 35, 436–443. Byun, J.S., Min, J.S., Kim, I.S., Kim, J.W., Chung, M.S., Lee, M., 2003. Comparison of indicators of microbial quality of meat during aerobic cold storage. J. Food Prot. 66, 1733–1737. Chouliara, E., Karatapanis, A., Savvaidis, I.N., Kontominas, M.G., 2007. Combined effect of oregano essential oil and modified atmosphere packaging on shelf life extension of fresh chicken breast meat stored at 4 1C. Food Microbiol. 24, 607–617. Chouliara, E., Badeka, A., Savvaidis, I., Kontominas, M.G., 2008. Combined effect of irradiation and modified atmosphere packaging on shelf life extension of chicken breast meat: microbiological, chemical and sensory changes. Eur. Food Res. Technol. 226, 877–888.
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Davies, A.R., 1995. Advances in modified-atmosphere packaging. In: Gould, G.W. (Ed.), New Methods of Food preservation. Blackie Academic and Professional, London, pp. 304–320. Du, M., Hur, S.J., Ahn, D.U., 2002. Raw meat packaging and storage affect the color and odor of irradiated breast fillets after cooking. Meat Sci. 61, 49–54. Emborg, J., Laursen, B.G., Rathjen, T., Dalgaard, P., 2002. Microbial spoilage and formation of biogenic amines in fresh and thawed modified atmospherepacked salmon (Salmo salar) at 2 1C. J. Appl. Microbiol. 92, 750–798. Fagan, J.D., Gormley, T.R., Mhuircheartaigh, M.U., 2002. Freeze-chill technology for raw whiting and mackerel fillets. Farm Food 12, 14–17. Fagan, J.D., Gormley, T.R., Mhuircheartaigh, M.U., 2003. Effect of freeze-chilling, in comparison with fresh, chilling and freezing on some quality parameters if raw whiting, mackerel and salmon portions. Leban. Wiss. und. Technol. 36, 647–655. Farber, J.M., 1991. Microbiological aspects of modified atmosphere packaging technology. J. Food Prot. 54, 58–70. Forsythe, S.J., Hayes, P.R., 1998. Food spoilage. In: Forsythe, S.J., Hayes, P.R. (Eds.), Food Hygiene, Microbiology and HACCP, third ed. Aspen Publications, Gaithersburg, pp. 86–149. Gill, C.O., 1986. The control of microbial spoilage in fresh meats. In: Pearson, A.M., Dutson, T.R. (Eds.), Advances in Meat Research: Meat Poultry Microbiology. MacMillan, London, pp. 49–88. Guldager, H.S., Bøknaes, N., Østerberg, C., Nielsen, J., Dalgaard, P., 1998. Thawed cod fillets spoil less rapidly than unfrozen fillets stored under MAP at 2 1C. J. Food Prot. 61, 1129–1136. Institute of Food Science and Technology, 1990. Guidelines for the Handling of Chilled Foods, second ed., UK. International Commission on Microbiological Specifications for Foods (ICMSF), 1986. In: Microorganisms in Foods. Sampling for Microbiological Analysis: Principles and Scientific Applications, vol. 2, second ed. University of Toronto Press, Toronto, pp. 181–196. International Institute of Refrigeration (IIR), 1986. ISO11290-1, 1996. Microbiology of food and animal feeding stuffs. Horizontal method of the detection and enumeration of Listeria monocytogenes. Part 1: Detection method. ISO6579, 2002. Microbiology of food and animal feeding stuffs. Horizontal method for the detection of Salmonella spp. Jay, J.M., 1992. Modern Food Microbiology, fifth ed. Chapman & Hall, New York. Jiang, S.I., Lee, T.C., 1985. Changes in free aminoacids and protein denaturation of fish muscle during frozen storage. J. Agric. Food Chem. 38, 839–894. Kakouri, A., Nychas, G.J.E., 1994. Storage of poultry meat and MAP of VP: possible role of microbial metabolites as indicators of spoilage. J. Appl. Bacteriol. 16, 163–173. Kotzekidou, P., Bloukas, J.G., 1996. Effect of protective cultures and packaging film permeability on shelf-life of sliced vacuum-packed cooked ham. Meat Sci. 42, 333–345. Lawrie, R.A., 1979. Meat Science, third ed. Pergamon Press, Oxford, UK, pp. 312–321. Magnusson, H., Martinsdottir, E., 1995. Storage quality of fresh and frozen-thawed fish in ice. J. Food Sci. 60, 273–278. Malle, P., Poumeyrol, M., 1989. A new chemical criterion for the quality of fish: trimethylamine/total volatile basic nitrogen. J. Food Prot. 50, 419–423. Martinsdottir, E., Magnusson, H., 2001. Keeping quality of sea-frozen thawed cod fillets on ice. J. Food Sci. 66, 1402–1408. Mead, G.C., Adams, BW., 1977. Selective medium for rapid isolation of Pseudomonads associated with poultry meat spoilage. Br. Poult. Sci. 18, 661–670. Mossel, D.A.A., Eelderink, L., Koopmans, M., Rossen, F.V., 1979. Influence of carbon source, bile salts and incubation temperature on recovery of Enterobacteriaceae from foods using MacConkey-type agars. J. Food Prot. 42, 470–475. O’Leary, E., Gormley, T.R., Batler, F., Shilton, N., 2000. The effect of freeze-chilling on the quality of ready meal components. Leban. Wiss. und. Technol. 33, 217–224. Patsias, A., Chouliara, I., Badeka, A., Savvaidis, I.N., Kontominas, M.G., 2006. Shelf life of a chilled precooked chicken product stored in air and under modified atmospheres: microbiological, chemical and sensory attributes. Food Microbiol. 23, 423–429. Redmond, G.A., Gormley, T.R., 2003. Freeze-chilling ready meals. Food Eng. Ingredients 28, 36–39. Redmond, G.A., Butler, F., Gormley, T.R., 2002. The effect of freezing conditions on the quality of freeze-chilled reconstituted mashed potato. Leban. Wiss. und. Technol. 35, 201–204. Redmond, G.A., Gormley, T.R., Butler, F., 2004. The effect of short and long term freeze-chilling on the quality of cooked beans and carrots. Innov. Food Sci. Emerg. Technol. 5, 65–72. Redmond, G.H., Gormley, T.R., Butler, F., 2005. Effect of short and long term frozen storage with MAP on the quality of freeze-chilled lasagne. Leban. Wiss. und. Technol. 38, 81–87. Skandamis, P., Nychas, G.J.E., 2002. Preservation of fresh meat with active and modified atmosphere packaging conditions. Int. J. Food Microbiol. 79, 35–45. Stiles, M.E., 1991. Scientific principles of controlled/modified atmosphere packaging. In: Ooraikul, B., Stiles, M.E. (Eds.), Modified Atmosphere Packaging of Food. Ellis Horwood Ltd., Chichester, UK pp. 18–25 and 118–147.
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Combined effect of freeze chilling and MAP on quality parameters of raw chicken fillets A. Patsias, A.V. Badeka, I.N. Savvaidis, M.G. Kontominas Laboratory of Food Chemistry and Microbiology, Department of Chemistry, University of Ioannina, Ioannina 45110, Greece
a r t i c l e in fo
abstract
Article history: Received 10 October 2007 Received in revised form 15 February 2008 Accepted 17 February 2008 Available online 2 March 2008
The effect of short-term frozen storage prior to thawing on the quality of freeze-chilled chicken fillets was investigated, as was the effect of modified atmosphere packaging (MAP). Four process treatments were used: (1) fresh chicken chilled at 4 1C without previous freezing, (2) freeze-chilled for 7 days and thawed at 4 1C, (3) chilled at 4 1C packaged under MAP (70% N2–30%CO2), and (4) packaged under MAP, freeze-chilled for 7 days and thawed at 4 1C. Microbiological, chemical and sensory analyses were conducted on samples for a period up to 15 days. Freeze-chilled fillets gave a lower total viable count (TVC) at a given sampling day than chilled fillets. MAP, as expected, delayed microbial growth. The Pseudomonads were the dominant microbial species in fillets under aerobic conditions. MAP reduced the populations of Pseudomonads by 2–4 log cfu/g. Lactic acid bacteria (LAB) and Enterobacteriaceae increased progressively for all treatments throughout storage. Yeasts and molds were inhibited by MAP and by freeze chilling. Total volatile basic nitrogen (TVB-N) values increased rapidly for the chilled fillets but remained significantly lower for the freezechilled and the MA-packaged samples. MAP and especially freeze chilling enhanced drip loss. MAP did not affect redness or yellowness of product while freeze chilling decreased product redness. Lightness was not affected by either MAP or freeze chilling. Based on taste, which proved to be the most sensitive sensory attribute, shelf life of product ranged from 6 to 7 days for all treatments leading to the conclusion that freeze chilling is a suitable technology for fresh chicken fillets enabling their distribution as a frozen product and upon subsequent thawing at their final destination, their retail display as chilled products. MAP in combination with freeze chilling had a negligible effect on product quality. & 2008 Published by Elsevier Ltd.
Keywords: Freeze chilling Modified atmosphere packaging Chicken fillets
1. Introduction Even though the effects of both chilling and freezing of foods are well documented (International Institute of Refrigeration, IIR, 1986), the effects of freeze chilling on quality of foods have only recently been systematically investigated (Guldager et al., 1998; Bøknaes et al., 2000; O’Leary et al., 2000; Martinsdottir and Magnusson, 2001; Emborg et al., 2002; Fagan et al., 2003; Redmond and Gormley, 2003; Redmond et al., 2004; Redmond et al., 2005). Freeze chilling involves initial freezing of a foodstuff with frozen storage being followed by thawing and distribution of the product at chill temperatures. Freeze chilling has already been commercially used at the retail level for chilled pre-packaged raw fish fillets which are replacing the traditional iced fish counter in supermarkets (Fagan et al., 2002). Freeze chilling offers a number of advantages over both frozen and chilled products such as (a)
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E-mail address: [email protected] (M.G. Kontominas). 0740-0020/$ - see front matter & 2008 Published by Elsevier Ltd. doi:10.1016/j.fm.2008.02.008
foodstuffs can be prepared in bulk, frozen and stored at deep freeze temperatures until required. Subsequently, a part or the whole batch of product can be thawed and further processed; (b) freeze chilling enables chilled foods to reach distant markets in the form of frozen product which is subsequently thawed at its final destination prior to retail display as a chilled food; (c) freeze chilling can reduce the level of product recalls enabling routine microbiological testing to be completed before the product is released from the manufacturing plant (Fagan et al., 2003). Work so far on freeze chilling has been limited to its application to fish (whiting, mackerel, salmon, Fagan et al., 2003; salmon and cod, Magnusson and Martinsdottir, 1995; Guldager et al., 1998; Bøknaes et al., 2000, 2001, 2002; Emborg et al., 2002), ready to eat meals such as lasagne (Redmond et al., 2005), steamed broccoli and instant mashed potatoes (O’Leary et al., 2000; Redmond et al., 2002) and cooked green beans and carrots (Redmond et al., 2004). Modified atmosphere packaging (MAP) has gained considerable popularity over the last decades as a modern non-thermal method of food preservation. The proper combination of gases
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(CO2, N2, and O2) in the headspace of food packs results in inhibition of spoilage microorganisms of perishable foods such as meat, fish and related products, developed under aerobic conditions and retention of their sensorial attributes (Davies, 1995). A minimum CO2 concentration of 20–30% is necessary to exhibit an inhibitory effect. (Stiles, 1991). An extended storage-life of poultry meat under low O2, high CO2 concentrations is observed because the spoilage caused by lactic acid bacteria (LAB) occurs later as compared to the spoilage caused by aerobic bacteria such as Pseudomonas spp. that prevail under aerobic conditions. In general, the defect caused by LAB is described as ‘‘souring’’, which is less offensive than the putrefaction that develops aerobically (Stiles, 1991). Microflora and spoilage pattern of chicken carcasses packaged under CO2 conditions are similar to those observed for red meat (Gill, 1986). Poultry meat is a very popular food commodity around the world and its consumption has increased over the last decades in many countries. Some of the reasons for its popularity are relatively low cost of production, low fat content, high nutritional value, distinct flavor and a variety of processed poultry products commercially available (Barbut, 2002). Poultry meat is a highly perishable food commodity providing an almost perfect medium for microbial growth (Jay, 1992) and it is thus of utmost importance for the poultry industry to develop new and effective methods of preservation to extend product shelf life (Chouliara et al., 2007, 2008). Given that no information exists in the literature on the application of either freeze chilling or the combination of freeze chilling and MAP to raw chicken meat, the objective of the present work was to investigate both the effect of short-sterm freeze chilling and the combined effect of freeze chilling and MAP on quality attributes of raw chicken breast fillets. A second objective was to determine product shelf life using above treatments.
2. Materials and methods 2.1. Sample preparation and treatment Chicken breast fillets (300 g/fillet) were prepared in a local poultry plant (Pindos SA, Ioannina, Greece) immediately after slaughter, packaged as described below and blast frozen at 40 1C for 3 h. Frozen samples were kept at this temperature for 7 days and allowed to thaw at refrigeration temperature (471 1C for 9 h) where they were kept for an additional period of 9 days (treatments 1 and 2) or 15 days (treatments 3 and 4). Four lots of samples were prepared: 1. chilled at 4 1C without previous freezing; 2. freeze-chilled and thawed as described above; 3. chilled at 4 1C and packaged under modified atmosphere (70% N2:30% CO2); 4. packaged under modified atmosphere (70% N2:30% CO2), freeze-chilled and thawed as described above.
(Ringsted). Fillets to be packaged aerobically were packaged in a polyethylene film, 75 mm in thickness, having an oxygen permeability of 4600 mL/(m2 day atm) at 60% RH/25 1C and a water vapor permeability of 1.75 g/(m2 day atm) at 100% RH/25 1C. 2.1.1. Sample analysis Samples 1 and 2 were tested at sampling days 0, 3, 5, 7, and 9 while samples 3 and 4 were tested at sampling days 0, 3, 5, 7, 9, 12, and 15. 2.2. Microbiological analyses The following groups of microflora were monitored: TVC, Pseudomonads, Enterobacteriaceae, LAB, yeasts and molds as well as Salmonella spp and Listeria monocytogenes. A sample (25 g) was removed aseptically using a scalpel and forceps from the chicken breast fillet, transferred to a stomacher bag (Seward Medical, UK), containing 225 ml of sterile quarterstrength Ringer’s solution, and homogenized using a stomacher (Lab Blender 400, Seward Medical) for 60 s at room temperature. For microbial enumeration, 0.1 mL samples of serial dilutions (1:10, diluent, quarter-strength Ringer’s solution) of chicken homogenates were spread on the surface of dry media. Total viable counts (TVC) were determined using plate count agar (PCA; Merck, Denmark, Germany), after incubation for 3 days at 30 1C. Pseudomonads were determined on cetrimide fusidin cephaloridine agar (oxoid supplemented with selective supplement SR 103, Oxoid, Basingstoke, UK) after incubation at 25 1C for 2 days (Mead and Adams, 1977). For members of the Enterobacteriaceae family, 1.0 mL sample was inoculated into 10 mL of molten (45 1C) violet red bile glucose agar (Oxoid). After setting, a 10 mL overlay of molten medium was added and incubated at 30 1C for 24 h. The large colonies with purple haloes were counted (Mossel et al., 1979). Lactic acid bacteria were determined on de Man Rogosa Sharpe medium (Oxoid) after incubation at 25 1C for 5 days. Yeasts and molds were enumerated using rose bengal chloroamphenicol agar (RBC; Merck) after incubation at 25 1C for 3 days in the dark. All plates were examined visually for typical colony types and morphological characteristics associated with each growth medium. In addition, the selectivity of each medium was checked routinely by Gram staining and microscopic examination of smears prepared from randomly selected colonies from all of the media. Salmonella was determined according to ISO6579, 2002. L. monocytogenes was determined according to ISO11290-1, 1996. 2.3. Chemical analysis The pH value was recorded using a Metrohm, model 691, pH meter. Chicken samples were thoroughly homogenized with 10 ml of distilled water and the homogenate used for pH determination. Total volatile basic nitrogen (TVB-N) was determined according to the method of Malle and Poumeyrol (1989). 2.4. Physical testing
Fillets to be packaged under modified atmosphere were placed in low-density polyethylene/polyamide/low-density polyethylene (LDPE/PA/LDPE) barrier pouches (1 fillet/pouch), 75 mm in thickness having an oxygen permeability of 52.2 mL/(m2 day atm) at 60% RH/25 1C and water vapor permeability of 2.4 g/(m2 day) at 100% RH/25 1C. Gas mixtures were prepared using a PBI-Dansensor model 9000 gas mixer (Ringsted, Denmark). Pouches were heatsealed using a BOSS model N48 vacuum sealer (Boss GmbH, Germany). Gas concentrations in packages were determined using a PBI, model Checkmate 9900 headspace analyzer instrument
Color determination was carried out on the surface of breast chicken meat using a Hunter Lab, model DP-9000, optical sensor colorimeter (Hunter Associates Laboratory, Reston, VA, USA) as described by Du et al. (2002). The quantity of drip released from fillets after storage was measured by removal of the product from the pre-weighed pouch and reweighing. Drip loss was expressed as a percentage of the initial weight of the packaged product (Kotzekidou and Bloukas, 1996).
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2.5. Sensory evaluation At all sampling days, samples destined for sensory evaluation were frozen. Chicken breast samples (ca. 100 g) were cooked in a microwave oven at high power (700 W) for 4 min including time of defrosting. An untrained panel of 17 judges experienced in chicken evaluation was used for sensory analysis. Panelists were asked to evaluate taste and odor of cooked samples. Along with the test samples, the panelists were presented with a freshly thawed chicken sample, stored at 40 1C throughout the experiment, this serving as the reference sample. Acceptability of odor and taste was estimated using a scale ranging from 9 to 0, with 9 corresponding to the most liked sample and 0 corresponding to the least liked sample. A score of 5 was taken as the lower limit of acceptability. 2.6. Statistical analysis Experiments were replicated twice on different occasions with different chicken samples. Analyses were run in triplicate for each replicate (n ¼ 2 3). Microbiological data were transformed into logarithms of the number of colony forming units (cfu/g) and were subjected to analysis of variance (ANOVA). Trial results were analyzed as 4 treatments 6 replicates. Means and standard deviations were calculated and when F values were significant at the Po0.05 level, mean differences were separated by the least significant difference (LSD) procedure.
3. Results and discussion 3.1. Microbiological analyses TVC values for the four different treatments as a function of storage time are shown in Fig. 1A. Initial TVC values in the range of 4.3–4.6 log cfu/g are indicative of good quality chicken meat. These values are in excellent agreement with those of Balamatsia et al. (2006) (4.29 log cfu/g) for chicken breast fillets, Chouliara et al. (2007, 2008) (4.28 log cfu/g) for chopped chicken breast meat and Chouliara et al. (2007, 2008) (4.3 log cfu/g) for chunks of chicken breast meat but significantly lower than those of Kakouri and Nychas (1994) (6.74 log cfu/ml) for chicken breast fillet most probably owed to cross contamination during preparation. Chilled fillets reached 7 log cfu/g, related to the upper microbiological limit for fresh poultry meat, as defined by the ICMFS (1986) after 5–6 days while freeze-chilled fillets reached the same value after approximately 8 days of storage. In turn, chilled fillets under MAP reached a TVC of 7 log cfu/g after approximately 10 and 12 days, respectively. It was anticipated that freeze chilling would produce a higher TVC as freezing opens up product structure resulting in more drip than chilling alone (Fagan et al., 2003). However, present data did not support this postulation as freeze-chilled fillets gave a lower TVC (Po0.05) at a given sampling day than chilled fillets. MAP, as expected, delayed microbial growth as a large portion of the spoilage microflora of chicken meat, mainly pseudomonads, are aerobic being inhibited by high CO2 concentrations (Farber, 1991). This statement is supported by data in Fig. 1B. Fagan et al. (2003) reported statistically insignificant differences between TVC for chilled and freeze-chilled whiting fillets (5.54 log cfu/g vs. 5.24 log cfu/g) and mackerel fillets (5.34 log cfu/g vs. 5.14 log cfu/g) after 3 days of storage. Similarly, statistically insignificantly differences between chilled and freeze-chilled salmon portions (7.36 log cfu/g vs. 7.56 log cfu/g) were reported after 5 days of storage at 4 1C. In contrast O’Leary et al. (2000),
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reported a higher TVC for freeze-chilled than chilled steamed salmon (3.62 log cfu/g vs. 2.68 log cfu/g) after 5 days of refrigerated storage. Similarly, Redmond et al. (2005) reported a higher TVC for freeze-chilled as compared to chilled beef lasagne (4.03 s, 1.95 log cfu/g) after 7 days of storage at 4 1C. The Pseudomonads (Fig. 1B) were the dominant microbial species in chicken fillets under aerobic packaging conditions. Interestingly, freeze chilling gave a lower (Po0.05) count of Pseudomonads than chilled samples by approximately 0.5–1.5 log cfu/g throughout storage. As mentioned previously, this was not anticipated given the effect of freezing on meat structure. Significantly lower (Po0.05) counts of Pseudomonads by approximately 2–4 log cfu/g of MA-packaged samples as compared to air-packaged samples were recorded throughout the entire storage period. Such a trend was anticipated given the strictly aerobic nature of Pseudomonads (Balamatsia et al., 2007; Chouliara et al., 2007, 2008). After 9 days of storage, freeze-chilled samples under MAP gave a lower Pseudomonads count (Po0.05) than chilled samples under MAP by approximately 1 log cfu/g. This difference remained until day 15 of storage. The reason for such a behavior is not clear requiring further investigation. Above results with regard to the effect of MAP are in good agreement with those of Skandamis and Nychas (2002) who reported a reduction of 3 log cfu/ml in beef stored under MAP after 6 days of storage at 5 1C as compared to control samples. Of the facultative anaerobic bacterial species, LAB constituted a part of the natural microflora of raw chicken meat stored both in air and under MAP (Fig. 1C). Initial (day 0) LAB counts determined were between 3.7 and 4 log cfu/g, increasing progressively with storage time attaining final counts of ca. 6.6 and 7.5 log cfu/g for freeze-chilled and chilled samples stored in air and ca. 6.1 and 7.4 log cfu/g for freeze-chilled and chilled samples stored under MAP, respectively. The behavior exhibited by LAB was fully anticipated given the fact that LAB are facultative anaerobic and are able to grow both in the presence and absence of oxygen. Patsias et al. (2006) reported a small reduction of about 1.7 log cfu/g in LAB populations in pre-cooked chicken products after 12 days of storage at 4 1C under MAP as compared to airpackaged pre-cooked samples. Skandamis and Nychas (2002) reported rapid growth of LAB in beef under MAP at 5 1C with no differences compared to air-packaged samples. Enterobacteriaceae, a large group of facultatively anaerobic bacteria, used as hygiene indicators, were found in low numbers (day 0) and progressively increased to approximately 6.5 log cfu/g in the air-chilled samples after day 9 of storage. In contrast, in freeze-chilled and MA-packaged samples, the population of Enterobacteriaceae remained below or equal to 5.5 log cfu/g throughout the entire storage period. Thus, both freeze chilling and MAP partly inhibited the growth of Enterobacteriaceae. MAP further inhibited Enterobacteriaceae, which reached a population of 3.6 and 5.2 log cfu/g after 15 days of storage for the freezechilled and chilled sample under MAP, respectively. Present results with regard to the effect of MAP are in agreement with those of Chouliara et al. (2007, 2008) who reported a 2–3 log cfu/g reduction of Enterobacteriaceae under various MAP conditions after 6 days of storage at 4 1C. Lastly, most yeasts and molds, aerobic in nature, increased from an initial value of 2.9–3.0 to 6.3 log cfu/g in the chilled airpackaged samples (Fig. 1E). They were, however, substantially inhibited by MAP reaching populations between 3 and 3.6 log cfu/g after 15 days of storage. Interestingly, yeasts and molds were also inhibited by freeze chilling reaching a population of 3.8–3.9 log cfu/g on day 9 of storage. With regard to MAP, present results are in general agreement with those of Balamatsia et al. (2007) who reported a decrease in yeasts by 3.1–4.1 log cfu/g for chicken
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14
16
Fig. 1. (A) Changes in total viable counts of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.17–0.55). (B) Changes in Pseudomonas spp. of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.11–0.61). (C) Changes in lactic acid bacteria of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.12–0.48). (D) Changes in Enterobacteriaceae of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freezechilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.08–0.44). (E) Changes in yeasts and molds of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.09–0.42).
breast fillets under MAP and VP as compared to air-packaged samples stored at 4 1C. A lower reduction effect of MAP on yeasts (0.5–1.0 log cfu/g) was reported by Chouliara et al. (2007, 2008) for chilled chicken breast meat after 6 days of storage at 4 1C. Neither Salmonella spp. or L. monocytogenes were detected in samples.
3.2. Chemical changes Differences in pH between chilled and freeze-chilled samples were not statistically significant (P40.05); pH values ranging between 5.9 and 6.1. Results were somewhat different for MA-packaged samples where statistically significant differences in pH were recorded after day 7 of storage. pH values varied
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between 6.1 and 5.6 for both chilled and freeze-chilled samples stored under MAP which was attributed to the production of lactic acid through LAB metabolism and CO2 dissolution in the aqueous phase of the chicken muscle (Farber, 1991). Present pH values, with regard to the effect of MAP, are in excellent agreement with those of Chouliara et al. (2007, 2008) who reported pH values between 5.9 and 6.4 for air and MA-packaged chopped chicken breast meat stored for 25 days at 4 1C. Results for TVB-N are shown in Fig. 2. The initial TVB-N value of 12 mg/100 g increased sharply in the chilled sample stored in air resulting in high TVB-N values (49 g/100 g) after 9 day of storage. The proposed upper limit of 30 mg/100 g (Bynn et al., 2003) as indicator of meat freshness for pork was exceeded between day 4 and 5 of storage for the chilled sample giving a reasonably good correlation of TVB-N with microbiological data (TVC). In contrast, the freeze-chilled sample stored in air and both the MA-packaged samples gave TVB-N values lower or equal to 25 mg/100 g throughout storage rendering TVB-N an unfit indicator of freeze-chilled chicken meat quality. Present TVB-N values are in general agreement with those of Balamatsia et al. (2006, 2007) who reported TVB-N values in the range of 54.5 mg/100 g for air-packaged chicken breast fillets after 15 days of storage at 4 1C. With regard to the effect of freeze chilling on TVB-N values, Fagan et al. (2003) did not observe statistically significant differences between chilled and freeze-chilled whiting and mackerel fillets after 3 days of storage and salmon portions after 5 days of storage.
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Table 1 Effect of freeze chilling and MAP on % drip loss of chicken breast fillets stored at 4 1C Storage time (days)
Chilled in Chilled under air MAP
Freeze-chilled in air
Freeze-chilled under MAP
0 9 15
0 3.970.2 –
12.070.5 11.570.6 –
11.570.8 – 10.670.5
0 – 5.870.3
Table 2 Effect of freeze chilling and MAP on color parameters of chicken breast fillets stored at 4 1C Storage time (days)
Chilled in Chilled under air MAP
Freeze-chilled in air
Freeze-chilled under MAP
L*-value 0 9 15
51.771.4 56.371.8 –
51.772.0 – 57.871.6
52.771.1 57.371.9 –
52.772.1 – 60.272.8
a*-value 0 9 15
3.970.1 3.970.2 3.270.2 – – 3.470.1
2.970.1 2.670.1 –
2.970.2 – 2.570.1
b*-value 0 9 15
12.670.3 12.670.4 12.970.2 – – 12.170.3
12.270.2 12.670.1 –
12.270.3 – 12.070.2
3.3. Physical testing The effect of specific treatment on % drip loss is shown in Table 1. Drip loss varied between 0% and 3.9% for the chilled product, and between 0% and 5.8% for the chilled product under MAP after 9 days of storage. MAP seemed to enhance moisture loss in the product possibly by decreasing the water holding capacity of proteins through pH drop due to CO2 dissolution in the aqueous phase of the product. As expected, drip loss in the freezechilled and the chilled under MAP product showed a different pattern starting from an initial high value of 11–12% on day 0 (immediately after thawing) attributed to the thawing process and retaining this range of values after 15 days of storage. Obviously, the effect of MAP was negligible as compared to the strong effect of freezing/thawing on drip loss. Present drip loss values are in general agreement with those of Fagan et al. (2003) who reported drip loss values for chilled and freeze-chilled
TVB N (mg/100g)
60 50 40 30 20 10 0
0
2
4
6 8 10 Days of storage
12
14
16
Fig. 2. Changes in TVB-N values of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.33–2.1).
whiting (1% vs. 6%) and mackerel (2% vs. 4%) fillets after 3 days of storage and for salmon portions (1.7% vs. 3.2%) after 5 days of storage at 4 1C. They are also in agreement with that of Redmond et al. (2005), who reported centrifugal drip losses of 3.4% vs. 1.56% for freeze-chilled and chilled beef lasagne after 7 days of storage at 4 1C. These authors reported no effect of MAP on drip loss in the freeze-chilled product in accordance to our findings. Higher values of drip loss reported in the present study as compared to those reported for fish are probably justified by the higher final pH of fish (6.2–6.6) as compared to that of chicken (5.6–5.8) at which poultry proteins lose more moisture due to denaturation and aggregation occurring close to their isoelectric point (Lawrie, 1979). In fish, due to a higher final pH, the water holding capacity of the fish muscle suffers less moisture loss and thus drip loss is limited. The effect of specific treatment on color of chicken breast fillets is shown in Table 2. MAP did not affect the redness (a-value) or yellowness (b-value) for the chicken samples while freeze chilling resulted in decreased product redness. With regard to the effect of MAP, present trend of a- and b-values trend is in agreement with that found by Chouliara et al. (2007, 2008) who reported a-values between 3.3 and 5.3 and b-values between 9.2 and 11.4 for chicken breast fillets stored aerobically and under MAP at 4 1C. Lightness (L*-values) increased with time ranging between 51.7 and 60.2 but both MAP and freeze chilling did not affect (Po0.05) this color parameter. Similarly, Ahn and Lee (2004) reported no changes in L*- and a*-values for both aerobically and vacuumpackaged turkey breast meat during 15 days of storage. However, they reported an increase in b*-values in aerobically packaged samples. Such a trend was not observed in the present study. With regard to the effect of freeze chilling, Fagan et al. (2003) reported no differences in both L*- and a*-values between chilled and freeze-chilled whiting and mackerel fillets and only a small increase in yellowness (b-values). Regarding salmon fillets, they reported a slight decrease only in product lightness as compared to the chilled product. O’Leary et al. (2000) reported no significant
ARTICLE IN PRESS A. Patsias et al. / Food Microbiology 25 (2008) 575–581
10
9
9
8
8
Taste score
Odor score
580
7 6 5
6 5 4
4 3
7
0
2
4
6 8 Days of storage
10
12
3
0
2
4 6 Days of storage
8
10
Texture score
9 8.5 8 7.5 7 6.5 6 5.5 5 4.5 4
0
2
4 6 Days of storage
8
10
Fig. 3. (A) Changes in odor scores of chicken breast fillets stored at 4 1C chilled aerobically packaged (E), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.14–0.69). (B) Changes in taste cores of chicken breast fillets stored at 4 1C chilled aerobically packaged (~), chilled packaged under MAP (’), freeze-chilled aerobically packaged (m), freeze-chilled packaged under MAP ( ). Each point is the mean7S.E. of three samples taken from two replicate experiments (n ¼ 3 2 ¼ 6) (S.D. range: 0.13–0.71).
changes in color parameters of freeze-chilled as compared to chilled salmon portions. Finally, Redmond et al. (2005) reported a brighter color (L*/b*) for freeze-chilled as compared to chilled lasagne.
3.4. Sensory evaluation The effect of specific treatment on sensory attributes (odor and taste) is shown in Fig. 3A and B. Scores for odor (Fig. 3A) showed a pattern of decreasing acceptability with storage time. Until day 3 of storage all four treatments received high scores between 8.4 and 8.8 beyond which odor scores for the chilled samples decreased at a higher rate than the rest of the samples. The limit of acceptability (score of 5) was reached after 8 days for the chilled product 9 days for the chilled MA-packaged product and 8–9 days for both the freeze-chilled products. Respective data for taste are given in Fig. 3B. Taste proved to be a more sensitive sensory attribute for the evaluation of chicken breast fillets with initial scores for the chilled product being higher (8.4–8.7) than those of the freeze-chilled product (7.8–8.0). Until day 3 of storage, all treatments received a similar taste score between 7.6 and 8.0. The limit of acceptability was reached after 6–7 days for the freeze-chilled sample under MAP, after 7 days for the chilled in air sample and after 6–7 days for the chilled sample under MAP and the freeze-chilled sample. MAP did not substantially affect both odor and taste of the product. Jiang and Lee (1985) found no statistically significant differences in preference or acceptability scores between chilled and freeze-chilled salmon portions.
Similarly, Fagan et al. (2003) found no statistical differences in odor scores between chilled and freeze-chilled whiting and mackerel fillets stored for 3 days at 4 1C. However, odor scores were higher for chilled salmon portions as compared to freezechilled counterparts (odor score 5.6 vs. 3.6) after 5 days at 4 1C. Taste scores were similar for all three fish products (chilled and freeze-chilled samples). Finally, Redmond et al. (2005) did not observe differences in sensory acceptability of beef lasagne between chilled and freeze-chilled product stored for 7 days at 4 1C. Sensory data (taste data being the most sensitive) correlate reasonably well with microbiological (TVC) for chilled and chilled under MAP samples. Correlation was poor for the two freezechilled samples. Based primarily on sensory data, it is suggested that the use of freeze chilling did not extend the shelf life of chicken breast fillets but provided the advantage of short-term frozen storage (40 1C, 7 days in the present study) enabling ‘‘chilled’’ products to reach foreign markets more easily. MAP did not substantially affect shelf life of freeze-chilled product. Lastly, an issue that should be addressed is that of freezechilled product safety as the thawed product has a more open structure (due to freezing damage) which along with the excess free moisture (drip loss) could enhance pathogens’ growth during the subsequent chilling phase. In addition freezing does not kill all the bacteria (Forsythe and Hayes, 1998), and psychrophiles will preferentially grow during subsequent chilling. It is, therefore, obligatory to follow the guidelines for chilled foods (Inst., Food Sci. and Tech., 1990) rather than for frozen during the manufacture, distribution, thawing and retailing of freeze-chilled products.
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Use of good manufacturing practices (GMP) and hazard analysis of critical control point (HACCP) should be complementary guidelines during these processes. In addition, routine checks for all potential pathogens should also be made to ensure product safety. Particular attention should be also focused on the thawing step and careful temperature control should be exercised (Fagan et al., 2003). In the use of poultry fillets, tempering can be achieved by transferring packages from the supermarket deep freezer to the chilled retail display cabinets in the evening time, while the thawed product will be obtained the following morning. With respect to labeling, it is desirable for reasons of consumer information to label the product as ‘‘previously frozen’’ given that freeze-chilled meat products cannot be domestically refrozen. An expiration date must also be used and such a label must be attached at the beginning of the thawing stage.
4. Conclusions Chicken breast fillets are a suitable product for freeze chilling. Products stored at 40 1C for 7 days followed by thawing and storage for 6–7 days at 4 1C were still found sensorily acceptable. Modified atmosphere packaging had a small impact on quality of freeze-chilled chicken breast fillets.
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