Effects of modified atmosphere packaging (MAP) on the microbiological quality and shelf life of ostrich meat

Meat Science 88 (2011) 774–785

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Effects of modified atmosphere packaging (MAP) on the microbiological quality and shelf life of ostrich meat Enver Baris Bingol ⁎, Ozer Ergun Istanbul University, Faculty of Veterinary Medicine, Department of Food Hygiene and Technology, 34320 Avcilar, Istanbul, Turkey

a r t i c l e

i n f o

Article history: Received 27 August 2010 Received in revised form 10 March 2011 Accepted 10 March 2011 Keywords: Ostrich meat Microbiological Physico-chemical Sensorial quality MAP Shelf life

a b s t r a c t Effects of various concentrations of O2/CO2 in modified atmosphere packaging on the microbiological quality and shelf-life of ostrich meat was investigated. Nine–12 months old ostriches were used. The iliofibularis muscle was cut into small cubes that were divided into five groups and then separately packaged under various gas mixes: air and O2:CO2:N2 ratios of 80:20:0, 60:20:20, 60:40:0, and 40:40:20, using 2 different headspace ratios (1:1 and 3:1). The packaged meats were kept at 4 °C for 10 days and were analysed microbiologically, physico-chemically and sensorially. As a result, the meat quality and shelf-life of ostrich meat under various gas compositions were improved; microbial growth was delayed due to high CO2 usage and shelf-life was increased by 5–7 days. However, an undesired loss of red colour of the ostrich meat may affect consumer acceptance. © 2011 Elsevier Ltd. All rights reserved.

1. Introduction New trends toward consumption of alternative and healthy red meats have increased and meat from the ostrich (Struthio camelus) is marketed as a healthy red meat due to favourable nutritional properties, low cholesterol and intramuscular fat contents and high contents of polyunsaturated fatty acids (Fisher, Hoffman, & Mellet, 2000; Sales, 1998). Ostrich carcasses are typically chilled for 24–48 h post-mortem, fabricated, and immediately vacuumed and/or chub packaged before marketing (Sales & Horbanczuk, 1998). Ostrich meat processors sell fresh and frozen meat, as well as processed meat products, to a variety of markets generally utilising modern retail packaging practises (Alonso-Calleja, Martinez-Fernandez, Prieto, & Capita, 2004). Modern meat packaging techniques are intended to maintain the microbial and sensory quality of the product. Product shelf-life can be extended by inhibiting or retarding the growth of undesirable microflora. This can be achieved by the manipulation of the meat microenvironment (Hotchkiss, 1988). Modified atmosphere packaging (MAP) is designed to preserve the bright red appearance of meat (Taylor, Down, & Shaw, 1990), although lipid oxidation and microbial growth are also important factors regarding shelf-life and consumer acceptance of fresh meat (Jakobsen & Bertelsen, 2000). MAP is inhibitory to some microorgan-

⁎ Corresponding author. Tel.: +90 212 473 70 70/17152; fax: +90 212 473 72 41. E-mail address: [email protected] (E.B. Bingol). 0309-1740/$ – see front matter © 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.meatsci.2011.03.013

isms, and therefore increases the keeping quality of a variety of foods (Cutter, 2002). The relatively high pH of ostrich meat creates an ideal environment for rapid microbial spoilage in some packaging conditions (Alonso-Calleja et al., 2004; Sales & Mellet, 1996). Even though the nutritional value of ostrich meat is well documented, little information is available on the microbiological aspects and keeping quality of this foodstuff (Alonso-Calleja et al., 2004). Ostrich meat can affect consumer preferences because of its dark visual appearance. The objectives of this study were to investigate the effect of MAP of different gas compositions and headspace to meat volume ratios on ostrich meat quality by comparing pH and oxidative changes, colour stability and microbial quality. 2. Materials and methods The research protocol was approved by the Ethic Committee of the Istanbul University Veterinary Faculty (Approval number: 2005/134). 2.1. Sample preparation Nine−12 month-old ostriches were slaughtered at a commercial abattoir (with GMP and HACCP compliance) using industrial slaughtering techniques. The dietary history and production practises of the ostriches were unknown but all birds were from the same farm, and were thus assumed to have received similar diets and management conditions. Carcasses were chilled at 4 ± 1 °C for a minimum of 24 h post-mortem. Iliofibularis muscles were removed from the carcasses after removal of external fat and epimysial connective tissue

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and were grouped equally for each of the 3 replications of the study. They were immediately transported to a commercial meat company (Bonfilet, Istanbul, Turkey) under hygienic conditions and processed immediately upon arrival. Muscles were cut into pieces, about 2.5 × 2.5 × 2.5 cm cubes. The cubes were divided into five groups and were portioned into 200 ± 5 g samples (randomly distributed, approximately 13 meat cubes per pack).

was determined according to the ISO 16649–2 (ISO, 2001) procedure in Tryptone Bile X-Glucuronide agar (TBX, Oxoid, CM0945); pour plates were incubated at 44 °C for 24 h. Yeast and mould were defined on Dichloran Rose Bengal Chloramphenicol agar with Chloramphenicol Selective supplement (DRBC, Oxoid, CM0727 and SR0078). Spread plates were incubated at 25 °C for 3–5 days (Harrigan, 1998). All microbiological tests were carried out in duplicate, and the results expressed as log10 CFU/g.

2.2. Packaging of samples

2.6. Physico-chemical and sensory analyses

Packs (a total of 50 packs) were prepared by placing samples into either 400 or 800 mm3 inner volume trays to obtain 1:1 and 3:1 headspace ratios. The cubes were packaged in low O2 permeable (8– 12 cm3/m2/24 h at STP) polystyrene/ethylvinylalcohol (EVOH)/polyethylene (PE) trays and were over-wrapped with oxygen permeable (6000–8000 cm3/m2/24 h at STP) polyvinyl-chloride film (Wrap Film Systems Ltd., Shropshire, England) for aerobic packaging. The other ostrich meat samples were heat-sealed with a Multivac packaging unit (Multivac A 300/16, Sepp Haggenmüller, D 87787 Wolfertschwenden, Germany) within these trays using a low O2 permeable (3 cm3/m2/24 h) lidding film (20 mm of a laminate orientated polypropylene (OPP) and a co-extrusion layer (50 mm) of PE/EVOH/ PE) for modified atmosphere packaging using a gas mixture containing either 80:20:0, 60:20:20, 60:40:0 or 40:40:20/O2, CO2, N2 and a gas volume ratio to meat of either 1:1 or 3:1.

2.6.1. pH The pH was determined by blending a 10 g sample with 100 mL deionized water for 2 min. The pH of the resultant suspension was measured after 10 min at room temperature (about 20 ± 2 °C) using a Hanna pH metre (Hanna HI-9321,Woonsocket, RI), equipped with a FC220B electrode (Hanna HI-9321), calibrated with standard buffers of pH 4.0 and 7.0. Three readings were made for each sample and the mean recorded (AOAC, 1984).

2.3. Storage conditions Packages (air and MA packs) were held under refrigerated display conditions (4 °C) using fluorescent light (Osram L30W/76, Natura Delux, Germany) (616 lx) for up to 10 days and examined at 1, 3, 5, 7 and 10 days of storage for microbiological, physico-chemical and sensorial analysis. 2.4. Gas analyses Gas analyses of the internal atmosphere were done in duplicate at 1, 3, 5, 7 and 10 days of storage. Analyses for CO2, O2 and N2 within the packages were monitored by injecting 0.5 mL of gas removed from the headspace with a syringe (B, Braun, Melsungen AG, Deutchland) into a PDI gas chromatograph (PBI-Dansensor A/B, Ronnedevaj 18, DK 410 Ringsted, Denmark) fitted with a thermal conductivity detector. 2.5. Microbiological analyses Ten grammes of ostrich meat from each group was transferred to a sterile bag with 90 mL sterile Peptone water (Oxoid, CM0009, Hampshire, UK), and was homogenised for 90 s using a stomacher (Lab Blender 400, Model BA6021, Steward Lab., London, UK). Serial decimal dilutions were prepared using the same diluent. A 0.1- or 1mL inoculum of appropriate dilution was spread on plate count agar (PCA, Oxoid, CM0325). Plates were incubated at 35 °C for 48 h for determination of total aerobic plate counts (TAPC) and at 7 °C for 10 days for total psychrophilic bacteria (Andrews, June, Sherrod, Hammack, & Amaguana, 1995; Harrigan, 1998). Lactic acid bacteria (LAB) counts were determined by plating with overlay on de Man, Rogosa, Sharpe agar (MRS, Oxoid, CM0361) and incubating at 35 °C for 48 h (Davidson & Cronin, 1973); Pseudomonas spp. were enumerated on Pseudomonas agar with Cetrimid, Fucidin, Cephaloridin supplement (PA with CFC, Oxoid, CM0559 and SR0103); on spread plates were incubated at 25–30 °C for 48 h. Enterobacteria and Coliforms were examined in Violet Red Bile Glucose agar (VRBG, Oxoid, CM0485) and Violet Red Bile agar (VRB, Oxoid, CM0107) respectively by using pour plates with overlay added before incubation, with incubation at 35 °C for 24 h (Harrigan, 1998). E. coli

2.6.2. Thiobarbituric acid reactive substances (TBARS) value The ostrich meat samples were first chopped thoroughly and then homogenised using a Waring blender. Twenty grammes of the sample was mixed with 50 mL of 20% trichloroacetic acid in 2 M phosphoric acid at 4 °C, and then homogenised by ultra-turrax (ART Miccra RT) for 1.5 min. The resulting mixture was diluted with deionised water to a final volume of 100 mL and then filtered through a Whatman filter paper No. 4. Five millilitre of freshly prepared 0.005 M thiobarbituric acid solution was added to 5 mL of filtrate in a stopper fitted glass tube, mixed by inverting the tube several times, and then kept in the dark for 15 h at room temperature. Finally, the absorbance was measured at 530 nm using a UV visual spectrophotometer (Chebios Optimum-One). Results are expressed as the percentage of malondialdehyde (MDA), which has a molecular weight of 72.06 (Shrestha & Min, 2006). The TBARS value was calculated as: TBARS value = ½ðabsorbance−0:0121Þ = 0:1379 × ½72:06 = 94 mg MDA = kg ostrich meat:

2.6.3. Surface colour The surface colour of the samples at five different locations on each meat was averaged at each sampling day, immediately after opening each package in terms of CIE L* (lightness), a* (redness) and b* (yellowness) values. From these coordinates, hue (h*) and chroma (C*) were calculated: Hue = tan

   2 2 1 = 2 b = a Chroma = a + b :

−1 

Samples were placed in a special cup, which fitted within the sample port of the colorimeter. The colour was measured using a Colorflex HunterLab Spectrophotometer (Hunter Associates Laboratory Inc., Reston, VA, USA). Colour was evaluated using diffuse illumination (D65 2° observer) with 8 mm viewing aperture and a 25 mm port size with the specular component excluded (AMSA, 1991). 2.6.4. Sensory scores Eight semi-trained panellists, staff of Istanbul University, Food Hygiene and Technology Department, who had previously participated in training sessions to become familiar with the sensory characteristics of meat (ISO, 1985, 1993), were requested to score the red colour, off-odour and general appearance acceptability on the basis of nine point hedonic rating scales. The scales included 1 =

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CO2 deviations were smaller in packs with a 3:1 headspace than in those with a 1:1 headspace. Seydim, Acton, Hall, and Dawson (2006) reported that the mean headspace compositions of ground ostrich meat packages during storage were 91.2 ± 2.1% N2, 4.5 ± 1.15% O2 and 4.3 ± 1.05% CO2 in air and 9.1 ± 3.1% N2, 76.6 ± 2.7% O2 and 14.3 ±3.2% CO2 in O2 MA packs. Daly and Acton (2004) found minor changes in high O2 MA ground beef over 9 days storage. Similarly, Coventry et al. (1998) reported that the composition of MAP packs remained relatively stable over 6 weeks at − 1 °C; but after at 4 °C an increase in CO2 levels was seen. In addition, Jakobsen and Bertelsen (2000) using a high ratio of headspace to meat (about 9:1) showed that headspace composition remained constant during the entire experiment except for samples stored at 8 °C where reduced oxygen levels (5–10% less) were observed on days 8 and 10, due to microbial metabolism and/or endogenous biochemical reactions. Kennedy, Buckley, and Kerry (2004) reported that oxygen concentrations in 2:1 and 1.5:1 headspace to meat volume ratio packs containing lamb were significantly (P b 0.05) higher than in those in 1:1 ratio packs after 3 days of storage. They reported that in hogget packs with a 2:1 ratio, oxygen concentrations were also significantly (P b 0.001) higher than in packs with 1:1 and 1.5:1 (P b 0.01) ratios after 3, 6, 9, and 12 days of storage. The headspace is dynamic, with CO2 dissolving in the meat and being formed by tissue and bacterial respiration, with the consumption of O2 (Gill, 1996). Thus higher headspaces to meat volume ratios were more effective at buffering against such changes and so maintaining the initial gas mix. The increase in CO2 was correlated with the decrease in O2 concentration in the headspace. Daun, Solberg, Franke, and Gilbert (1971) reported similar results using MA packaged beef, and suggested the initial increase in CO2 was due to tissue utilisation of O2 while the second increase corresponded to microbial growth.

extremely unacceptable, 2 = very much unacceptable, 3 = moderately unacceptable, 4 = slightly unacceptable, 5 = between acceptable and unacceptable, 6 = slightly acceptable, 7 = moderately acceptable, 8 = very much acceptable and 9 = extremely acceptable (Ranganna, 1994). The panellists were trained in three separate sessions approximately 2 h long for each evaluation of the selected attributes. Training sessions were conducted to acquaint panellists with the products and attributes to be evaluated, and were followed by an open-discussion session to familiarise panellists with the attributes and the scale to be used. The panel members were seated in individual booths in a temperature and light-controlled room (fluorescent lighting of 2000 lx; Philips 40 W Cool White), receiving a set of ten samples in a completely randomised order. Each sample was labelled, at random, with a two-digit code number. Unsalted crackers and water were served to panellists to freshen their mouth between each sub-samples assessment (ISO, 1988). Sensory analysis was performed in triplicate in two sessions. 2.7. Statistical analyses Analysis of variance was conducted for each variable to investigate the effect of storage time and packaging type. The trial was performed in triplicate and The General Linear Model procedure (PROC GLM) of SPSS 13.0 was used to analyse the data. The microbiological loads, pH, TBARS, instrumental colour and sensory characteristics were evaluated and significance of differences was defined as P b 0.05 (SPSS, 2001). The model used included the fixed effects of storage time, packaging conditions and headspace ratios. Microbial counts were expressed as log10 CFU/g and mean separations were obtained using Duncan's multiple range tests. 3. Results and discussion

3.2. pH 3.1. Headspace composition The initial pH was 6.24 ± 0.15 and decreased at the end of the storage to 5.97 ± 0.20, and 6.02 ± 0.23 in packs with headspaces of 1:1 and 3:1, respectively. Significant differences were not observed between the various storage conditions until day 5 (P N 0.05), but appeared at days 7 and 10 (P b 0.05) (Fig. 1).

The headspace compositions in the air and MAP stored samples are presented in Table 1. Values were almost constant during storage, only a slight shift was observed after 10 days of storage under MAP conditions. When compared to the applied concentration, the O2 and Table 1 Headspace compositions of the ostrich meat packs. Attribute

Headspace Packed atmosphere

Days of storage 1

3

O2 Headspace 1:1 ratio

3:1

a,b,c

Air 80:20:0/O2: CO2:N2 60:20:20/O2: CO2:N2 60:40:0/O2: CO2:N2 40:40:20/O2: CO2:N2 Air 80:20:0/O2: CO2:N2 60:20:20/O2: CO2:N2 60:40:0/O2: CO2:N2 40:40:20/O2: CO2:N2 SE P

CO2

7

O2

CO2

N2

5.43d 20.53b

76.20a 2.93d

17.33e 74.76a

5.86e 21.50c

76.80a 16.50d 6.33e 3.73c 73.50a 22.23c

19.26bc 22.93b

56.73c

20.03cd 23.23b 56.00b 20.36cd 23.63b 55.53c

20.73de 23.73b

4.76d 61.00b

35.43a

3.56d

59.46b

35.10b

35.76bc 7.56c

33.06b

25.33b 41.06d

36.86a

22.06b

38.56d

36.96a

24.46b 36.36c

36.90a

26.73b 35.56e 38.66a

25.76b

20.66d 3.20f 76.40a 18.23d

76.13a 19.23e 5.36d 74.56a

3.70d 77.06a 18.63bc 6.80c

18.90e 75.10a

3.96f 19.13d

77.13a 18.26d 4.10e 5.76c 72.46a 19.23d

77.63a 16.86f 4.33g 7.30c 73.86a 19.23e

78.80a 6.90c

61.56b 17.73d

20.70c

18.20c

58.23bc 18.36d

23.40b 57.50b 18.76d

23.73b 58.33c

19.06e

22.60b

34.43c

8.13c

75.43a 18.36e 1.93d 76.53a

61.76b 18.33cd 19.90c

41.60c

61.80b 34.56ab 42.96c 3.67 *

57.80c

60.30b

3.63d 59.76ab 35.20a

21.50b

5.03cd 59.70b

5.43c

35.83ab

4.46c

O2

10

N2

61.76b 33.46b

O2

5 CO2

19.50d 5.06e 78.20a 19.86c

N2

41.36d

35.46a

23.16b

40.40d

36.50ab 23.10b 39.60c

2.11 NS

4.92 **

3.61 NS

2.20 NS

4.92 **

3.62 **

*

: Means within a column with different letters are significantly different (P b 0.05), SE: Standard Error. NS: Not significant (*): P b 0.05 (**): P b 0.01 (***): P b 0.001.

4.92

CO2

5.46c

7.96c

56.67c

57.43c

36.43ab 23.96b 40.40d 36.40b

3.59 *

O2

77.16a 15.70f 6.86f 4.26c 68.20b 21.60d

57.80b 34.23b

21.43c

*

N2

57.80b 36.73ab

35.60a

2.19

CO2

2.17 *

4.87 *

3.55 NS

2.17 NS

N2 77.43a⁎ 10.20c

23.20b 4.81 NS

E.B. Bingol, O. Ergun / Meat Science 88 (2011) 774–785

pH of 1:1 headspace ratio packaged ostrich meats

a

6,3

6,2

6,1

6

5,9

5,8 0

1

3

5

7

10

7

10

Time (days)

b pH of 3:1 headspace ratio packaged ostrich meats

Jayasingh, Cornforth, Brennand, Carpenter, and Whittier (2002) stated that the high-oxygen modified atmosphere packaging (80% O2/ 20% CO2) and air packaged samples of ground beef had significant pH differences, especially after 10 days of storage at 2 °C. They observed a pH drop in air packaged samples from 5.7 at days 1 to 5.3 after 10 days of storage, whereas MAP samples showed only a slight decrease from 5.8 to 5.7 over the same period. Seydim et al. (2006) indicated that the pH of ground ostrich packaged under different atmospheres at 4 ± 1 °C did not change significantly due to storage. The initial pH of ground ostrich meat averaged 6.16 ± 0.06, and a final pH of 5.95 and 5.97 for O2 (80% O2/20% CO2) and air packaged samples at day 9, respectively. Fernandez-Lopez et al. (2008) found that pH values showed differences (P b 0.05) due to storage time and storage conditions, in ostrich steaks of initial pH 6.04 ± 0.10. A pH above 6.0 was also found for ostrich carcasses 2–6 h after bleeding (Sales & Horbanczuk, 1998). Berge, Lepetit, Renerre, and Touraille (1997) reported that depletion of glycogen reserves following ante-mortem stress in ratites might be the major reason for the relatively high pH values compared to other meats. The highest decreases were found in 1:1 headspace packaged samples, in accordance with their higher counts of lactic acid bacteria. Meat pH can be affected by many factors; however, growth of lactic acid bacteria resulting in lactic acid production is the major factor causing pH decreases in packaged meats (Gill, 1996). Lower pH values at 10 days were found in the air and N2 packaged samples which would support lactic acid bacteria outgrowth. Similarly, Coventry et al. (1998) reported that steaks in O2–CO2 atmospheres showed a relatively constant pH (5.5–5.6) compared with those in N2–CO2 atmospheres stored at 4 °C which exhibited significant (P b 0.01) decreases in pH (b5.0 after 2– 6 weeks).

777

6,3

6,2

6,1

6

5,9

5,8 0

1

3

5

Time (days) 3.3. Microbiological examination Changes in microbial populations are shown in Fig. 2(a) and (b). Days of storage at 4 °C and meat-to-gas headspace volume ratio in each package were the factors (P b 0.05) affecting each bacterial group. Microbial loads showed differences (P b 0.05) during storage and between packaging conditions. Microbial growth in 3:1 headspace ratio packaged samples was in general lower than in 1:1 headspace packaged ones; thus the 3:1 headspace is more inhibitory than the 1:1. Bacterial inhibition was significantly different (P b 0.001) in 60:40:0/O2:CO2:N2 atmosphere packages, whereas packaging atmosphere was not practically different for the same headspace packs (generally b1–0.5 log10 CFU/g among packaging treatments). Initial microbial counts at day 0 were 4.5± 0.3 log CFU/g for total aerobic plate counts, 4.2 ± 0.2 log CFU/g for total psychrophilic bacteria, 3.1 ± 0.3 log CFU/g for lactic acid bacteria, 3.0 ± 0.4 log CFU/g for Pseudomonas, 3.5 ± 0.2 log CFU/g for Enterobacteriaceae, 3.4± 0.3 for Coliforms, 2.6 ± 0.2 for E. coli and 3.0 ± 0.2 log CFU/g for yeasts and moulds. The high microbial load found in ostrich meat in relation to other red meats has been attributed to the high pH of this meat which creates an ideal environment for rapid microbial spoilage in some packaging conditions (Alonso-Calleja et al., 2004; Fernandez-Lopez et al., 2008; Sales & Mellet, 1996; Seydim et al., 2006). Initial counts for TAPC increased to 6.94–7.36 log CFU/g at day 5 in air packaged samples, which approach spoilage by off-odours and possible slime development (Gill & Newton, 1977; Jay, 1998). Similarly, high initial aerobic counts on fresh ostrich steak surfaces were reported by Alonso-Calleja et al. (2004), 6.5–7.8 log CFU/g. Fernandez-Lopez et al. (2008) and Seydim et al. (2006) also stated that microbial counts were higher than for other red meats. Gill, Jones, Bryant, and Brereton (2000) emphasised that ostrich and emu carcasses had greater numbers of total aerobes than beef carcasses indicating more processing contamination during ostrich slaughter in small slaughter plants.

Air (1:1)

80:20:0/O2,CO2,N2 (1:1)

60:20:20/O2,CO2,N2 (1:1)

60:40:0/O2,CO2,N2 (1:1)

40:40:20/O2,CO2,N2 (1:1)

Air (3:1)

80:20:0/O2,CO2,N2 (3:1)

60:20:20/O2,CO2,N2 (3:1)

60:40:0/O2,CO2,N2 (3:1)

40:40:20/O2,CO2,N2 (3:1)

Fig. 1. (a) and (b). pH values of ostrich meat packed under different conditions (air and modified atmosphere packaging of 80:20:0, 60:20:20, 60:40:0, 40:40:20/O2:CO2:N2 combinations with headspace ratios of 1:1 and 3:1) during storage at 4 °C.

Air packaged samples showed higher aerobic plate counts than MAP packaged ones (P b 0.001), especially in 3:1 headspace ratio packages. Microbial counts reached 5.66 ± 0.3 log CFU/g in 60:40:0/ O2:CO2:N2 atmosphere packages at day 10, while final counts were between 7.77 and 8.04 log CFU/g for air packaged samples at the end of storage. As expected higher CO2 concentrations reduced the number of aerobic bacteria during storage; counts in MAP samples were always lower (P b 0.05) than in air packaged samples, whatever the storage time. Counts of 7 log CFU/g is the approximate point at which meat would be unacceptable (Dainty & Mackey, 1992). Therefore, the shelflife of ostrich meat stored under aerobic conditions would be 5 days, while ostrich meat stored under modified atmospheres would be more than 10 days. Farber (1991) found that the overall effect of CO2 on microorganisms was an extension of the lag phase of growth and a decrease in growth rate during the logarithmic phase. Increased shelf life has been reported by Kennedy et al. (2004); Kennedy, Buckley, and Kerry (2005) and Insausti et al. (2001) for other red meat packaged under different modified atmospheres. Lactic acid bacteria counts were different (P b 0.05) between air and MAP packaged samples. MAP packaged samples had lower (P b 0.05) counts than air packaged ones, especially in 3:1 headspace ratio packages. Lactic acid bacteria counts increased during storage

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growth was limited when the CO2 concentration increased in the atmosphere. Pseudomonas began to increase in all groups from the 3rd day of storage and reaching 6.13–6.56 log CFU/g and 5.23–6.21 log CFU/g respectively in 1:1 and 3:1 headspace ratio packages at the end of storage (day 10). Seydim et al. (2006) reported that, after 9 days of storage, Pseudomonas growth was less in modified atmosphere packs of the ground ostrich meat, compared with air packaged samples. They noted that there was enough residual oxygen in these packages to support the slow growth of Pseudomonas, leading to higher populations than normally reported. Under aerobic conditions, predominant spoilage organisms are typically Pseudomonas (Gill, 1996; Gill et al., 2000). Alonso-Calleja et al. (2004) reported a range of 5.0–7.2 log CFU/g for Pseudomonas on fresh ostrich steaks. Kennedy et al. (2004) determined that 60:40:0/O2:CO2:N2 was the most effective gas composition in inhibiting growth in agreement with the present study. In O2 depleted atmospheres of N2 or CO2, the anaerobic conditions prevent all growth of Pseudomonas (Gill, 1996).

time for all samples. Initial counts were about 3.1 ± 0.3 log CFU/g and between 6.90 and 7.29 log CFU/g and 5.92–6.14 log CFU/g at day 10 for air and MAP packaged samples, respectively. The increase in growth of LAB in 3:1 headspace ratio packages was lower than in the 1:1 ratio packages, whatever the gas composition. Likewise, Daly and Acton (2004) reported that fresh ground beef in high O2 atmospheres initially had a mean count of 3.72 log CFU/g lactic acid bacteria with growth to 5.4 log CFU/g in 9 days at 4 °C. Seydim et al. (2006) stated that LAB counts were lower than those reported on fresh ostrich steak surfaces (Alonso-Calleja et al., 2004) at day 0 and reached to 5.71 log CFU/g at day 9. Fernandez-Lopez et al. (2008) determined that the evolution of LAB counts in air packaged ostrich steaks was 1 log cycle lower than in vacuum and MAP packs. Pseudomonas growth correlated to the O2 concentration in the packs. The increase was statistically different (P b 0.001) between 1:1 and 3:1 headspace ratio packages, with 3:1 headspace packages showing lower (P b 0.001) counts than 1:1 packs. Pseudomonas

a

9

Lactic acid bacteria (Log CFU/g)

Total aerobic bacteria (Log CFU/g)

8 8

7

6

5

4

0

1

3

5

7

7

6

5

4

3

2

10

0

1

Time (days)

5

7

10

7

10

Time (days) 9

Psychrotrophic bacteria (Log CFU/g)

8

Pseudomonas spp. (Log CFU/g)

3

7

6

5

4

3

2

8

7

6

5

4

3 0

1

3

5

7

10

Time (days)

0

1

3

5

Time (days) Air (1:1)

80:20:0/O2,CO2,N2 (1:1)

60:20:20/O2,CO2,N2 (1:1)

60:40:0/O2,CO2,N2 (1:1)

40:40:20/O2,CO2,N2 (1:1)

Fig. 2. (a) and (b). Microbial changes of ostrich meat packed under different conditions (air and modified atmosphere packaging of 80:20:0, 60:20:20, 60:40:0, 40:40:20/O2:CO2:N2 combinations with 1:1 headspace ratio) during storage at 4 °C. (c) and (d). Microbial changes of ostrich meat packed under different conditions (air and modified atmosphere packaging of 80:20:0, 60:20:20, 60:40:0, 40:40:20/O2:CO2:N2 combinations with 3:1 headspace ratio) during storage at 4 °C.

E.B. Bingol, O. Ergun / Meat Science 88 (2011) 774–785

8

7

7 6

Coliforms (Log CFU/g)

Enterobactericeae (Log CFU/g)

b

5

4

6

5

4

3

0

1

3

5

7

3

10

0

1

Time (days)

3

5

7

10

7

10

Time (days) 7

Yeast and Moulds (Log CFU/g)

6

E.coli (Log CFU/g)

779

5

4

3

6

5

4

3

2

2 0

1

3

5

7

10

0

Time (days)

1

3

5

Time (days) Air (1:1)

80:20:0/O2,CO2,N2 (1:1)

60:20:20/O2,CO2,N2 (1:1)

60:40:0/O2,CO2,N2 (1:1)

40:40:20/O2,CO2,N2 (1:1)

Fig. 2 (continued).

The growth of microorganisms was slowed by increasing CO2 levels in the packs but at the low temperature, cold-resistant bacteria continued their activities. Counts of psychrophilic bacteria showed differences (P b 0.001) among systems, but an increase was observed in all groups during storage (The final bacterial population was between 7.08 and 8.37 log CFU/g in 1:1 headspace ratio packages and 6.26–7.98 log CFU/g in 3:1 headspace ratio samples). The highest (P b 0.001) counts were found in air packaged samples, and the lowest (P b 0.001) in 60:40:0/O2:CO2:N2 and 3:1 headspace ratio packaged ones. Similar results were found by Fernandez-Lopez et al. (2008) who reported that counts of psychrotrophs increased during storage, and that air packaged samples showed the highest (P b 0.05) counts. Higher rates of microbial growth were also reported by Capita, Diaz-Rodriguez, Prieto, and Alonso-Calleja (2006) in ostrich steaks stored under air and vacuum conditions. Coliform and Enterobacteriaceae showed steady growth during storage. Enterobacteriaceae counts increased (P b 0.01) to an average value of 6.08 log CFU/g for 1:1 headspace ratio packs and 5.50 log CFU/ g for 3:1 headspace ratio ones at the end of storage (day 10), while Coliform counts reached (P b 0.01) average values of 6.72 log CFU/g and 6.16 log CFU/g with those two ratios, respectively. Alonso-Calleja et al. (2004) reported a range of 5.4–6.7 log CFU/g for Enterobacter-

iaceae on fresh ostrich steaks while Seydim et al. (2006) reported 2.3 log CFU/g at day 0. Enterobacteriaceae counts increased to approximately 6.5 log CFU/g at day 9, similar to results reported by Fernandez-Lopez et al. (2008), 7.0 ± 0.2 log CFU/g after 18 days. However, Coventry et al. (1998) found that Enterobacteriaceae showed a general decrease during storage in O2–CO2 atmospheres, whereas Insausti et al. (2001) stated that Enterobacteriaceae counts increased continuously during storage of beef steaks for 15 days. E. coli counts also showed slow growth during the entire storage time, but significant differences (P b 0.05) were observed at day 7. E. coli counts reached 5.35–5.78 log CFU/g at day 10 for air packaged samples while E. coli levels were between 4.00 and 5.21 log CFU/g and 3.66–4.71 log CFU/g for 1:1 and 3:1 headspace ratio packaged MAP samples, respectively. The most effective composition for inhibition was again 60:40:0/O2:CO2:N2. Yeast and moulds showed sustained growth during storage. Significant differences (P b 0.001) were observed between air and MAP packs. Ostrich meats reached an average value of 5.36 log CFU/g and 4.87 log CFU/g at day 10 in 1:1 and 3:1 headspace ratio MAP packs, while air packaged samples increased to 6.94 log CFU/g and 6.60 log CFU/g respectively. It was remarkable that the initial counts of yeast and moulds in air packaged samples were about 1 log cycle

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c

9

8

7

6

5

4

7

Lactic acid bacteria (Log CFU/g)

Total aerobic bacteria (Log CFU/g)

8

0

1

3

5

7

6

5

4

3

2

10

0

1

Time (days)

3

5

7

10

7

10

Time (days) 9

Psychrotrophic bacteria (Log CFU/g)

Pseudomonas spp. (Log CFU/g)

8

7

6

5

4

3

8

7

6

5

4

3

2 0

1

3

5

7

10

0

Time (days)

1

3

5

Time (days) Air (3:1)

80:20:0/O2,CO2,N2 (3:1)

60:20:20/O2,CO2,N2 (3:1)

60:40:0/O2,CO2,N2 (3:1)

40:40:20/O2,CO2,N2 (3:1)

Fig. 2 (continued).

higher than in MAP packs. Packs with 60:40:0/O2:CO2:N2 composition performed better than the others, and reached 4.61 log CFU/g and 4.15 log CFU/g at the end of storage depending on headspace ratio. Coventry et al. (1998) determined that the yeast and mould count in N2–CO2 atmospheres was substantially greater than in O2–CO2 atmospheres over the 4th and 6th week of storage and emphasised that yeasts were the predominant organisms in all of yeast and mould counts. 3.4. Thiobarbituric acid (TBA) values Storage time and gas composition were the significant factors for thiobarbituric acid (TBA) values. Thiobarbituric acid reactive substances (TBARS) values showed differences (P b 0.05) with storage time and between storage conditions (Fig. 3). Ostrich meats packaged with air or with high CO2 concentrations had lower mean TBARS values during the 10 days of storage compared to meat in O2 packages.

High O2 concentration led to higher lipid oxidation and modified atmosphere packaging did not extend the shelf-life of ostrich meats compared to air packaged ones. TBARS values of all air packaged ostrich samples remained lower than those of modified atmosphere packaged samples. This was observed during the entire storage time except in 60:40:0/O 2 :CO 2 :N 2 atmosphere and 3:1 headspace packages, which showed at day 10 a difference to 8.78 mg MDA/kg (Fig. 3). Samples in 1:1 headspace ratios had higher (P b 0.01) TBARS values than those with a 3:1 headspace. These results agree with Ordonez and Ledward (1977) who stated that the concentration of oxygen in the atmosphere is the determining factor for the rate of lipid oxidation. Seydim et al. (2006) emphasised that after 6 days of storage, ground meat packaged in O2 and air had increased (P ≤ 0.05) TBA values, whereas no significant changes were observed for meat in N2 and vacuum packs. They observed that TBA values in O2 packaged samples were very high (N20 mg MDA/kg) at the end of storage (day

E.B. Bingol, O. Ergun / Meat Science 88 (2011) 774–785

7

8

7 6

Coliforms (Log CFU/g)

Enterobactericeae (Log CFU/g)

d

5

4

6

5

4

3

0

1

3

5

7

3

10

0

1

Time (days)

3

5

7

10

7

10

Time (days) 7

Yeast and Moulds (Log CFU/g)

6

E.coli (Log CFU/g)

781

5

4

3

6

5

4

3

2

2 0

1

3

5

7

0

10

Time (days)

1

3

5

Time (days) Air (3:1)

80:20:0/O2,CO2,N2 (3:1)

60:20:20/O2,CO2,N2 (3:1)

60:40:0/O2,CO2,N2 (3:1)

40:40:20/O2,CO2,N2 (3:1)

Fig. 2 (continued).

9), while it was 9.76–10.94 mg MDA/kg for 1:1 headspace ratio packs and 8.78–10.77 mg MDA/kg for 3:1 headspace packs in the present study. Fernandez-Lopez et al. (2008) stated that ostrich steaks exposed to air showed the highest (P b 0.05) TBARS values, while steaks in vacuum, MAP (80% CO2 + 20% N2) or MAP + CO (30% CO2 + 69.8% argon + 0.2% CO) packages showed no differences (P N 0.05) in TBARS values. They stated that the reduction in the amount of oxygen in vacuum, MAP and MAP + CO packaged steaks and the barrier characteristics of the packaging film accounted for the lower TBARS values. TBA values for ostrich meat in O2 packages were very high compared to other meats. Spainer (1992) stated that the amount of heme catalyst (from haemoglobin, myoglobin and cytochrome) and the amount of heme and non-heme iron in meat was related to lipid oxidation rate. Ostrich meat has higher heme iron (Sales & Hayes, 1996) and polyunsaturated fatty acid (Sales, Marais, & Kruger, 1996) contents than beef, chicken and pork making ostrich meat more susceptible to oxidation. Jakobsen and Bertelsen (2002) reported that CO2 decreased lipid oxidation rate in meat and this was attributed to pH reduction due to the absorption of CO2.

Kennedy et al. (2004) indicated that even though TBARS values remained below 2.0 mg MDA/kg for lamb and hogget meat, TBARS values were higher in meat packaged in 80:20:0/O2:CO2:N2 than other MAP packs. These results were similar to those reported by Jakobsen and Bertelsen (2000) who found that a reduction in O2 concentration in the headspace from 80% to 55% had little influence on lipid oxidation of MA packaged beef. Jayasingh et al. (2002) determined that after 6 days of storage, high oxygen MAP ground beef samples had much higher mean TBA numbers (1.8 mg MDA/kg) than air packaged ones (0.6 mg MDA/kg). In addition, Linares, Berruga, Bórnez, and Vergara (2007) emphasised that 70:30:0/O2:CO2:N2 atmospheres resulted the highest values of TBARS in lamb meat. High oxygen concentrations favour lipid oxidation in meat, in agreement with Insausti et al. (2001) and Smiddy et al. (2002).

3.5. Surface colour measurements Lightness (L*), redness (a*), yellowness (b*), chroma (C*) and hue (h*) values are presented in Tables 2a and 2b.

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Fig. 3. (a) and (b). TBARS values of ostrich meat packed under different conditions (air and modified atmosphere packaging of 80:20:0, 60:20:20, 60:40:0, 40:40:20/O2:CO2: N2 combinations with headspace ratios of 1:1 and 3:1) during storage at 4 °C.

Surface L* values changed only slightly during storage for a given packaging condition, whereas significant differences were observed between the different packaging conditions (P b 0.01). In high O2 packages, initial L* values were between 34.46 and 34.62 and decreased to 30.18–30.79 at day 10. Meat in 60:40:0/O2:CO2:N2 atmosphere packages was generally darker (lower L*) in appearance than meat in the MAP and air systems. Several authors have reported lightness increases in different meat and meat products during refrigerated storage (Fernandez-Lopez, Jimenez, Sayas-Barbera, Sendra & Perez-Alvarez, 2006; Kusmider, Sebranek, Lonergan, & Honeyman, 2002). In a comparison with other meats, Paleari et al. (1998) reported that mean surface L* values for ostrich meat (non-ground) was 36.7, similar to others, 38.85 (Seydim et al., 2006) and 36.11 (Fernandez-Lopez et al., 2006) for ground ostrich meat and 38.4 for ostrich steaks (Fernandez-Lopez et al., 2008). Initial mean surface L* values for ostrich meat in the present study (31.76 ± 1.45) were lower than reported by others. The dark red colour of ostrich meat can be explained by the high heme content and the effect of the high pH on water binding resulting in less light reflection (Seydim et al., 2006). Changes in surface CIE a* values throughout storage are shown in Table 2a. Redness values for air and MAP packaged samples decreased (P b 0.05) during storage. This decrease was higher (P b 0.05) for high

O2 MAP packaged ostrich samples than for air and other MAP packaged ones. In a high oxygen atmosphere, oxymyoglobin is rapidly formed, which provides the typical cherry-red visual colour of ostrich meat (Seydim et al., 2006). Even though the initial surface a* values were higher for high O2 packaged samples; the decrease was significantly more than in the other packs. Statistically significant differences (P b 0.05) were observed only after 5 days of storage. At day 10, CIE a* values were higher in air packs than in any other packages. The loss of redness due to oxidation of myoglobin in packaged meat was expected as a consequence of the high pH of meat (N6.0). At high pH, mitochondrial enzyme systems (cytochrome, succinate and pyruvate-malate oxidase) are active and can consume oxygen (Lawrie, 1998). Bendall and Taylor (1972) reported that the oxygen consumption rate is more important in high pH than in normal pH muscles. Bembers and Satterlee (1975) also noted that the rate of the conversion of myoglobin to metmyoglobin (MMb) was 1.5–2.0 times faster in high pH systems than in muscles of normal pH. Seydim et al. (2006) reported that mean initial surface a* value for ostrich meat in O2 packages was 20.7 and differed (P b 0.05) from air, N2 and vacuum packages with a* values of 15.5, 12.7 and 13.2, respectively. They also noticed a* values decreasing (P b 0.05) rapidly for ground meat in O2 and air packages during the first 3 days, whereas no change was observed until day 9 under vacuum or N2 (P N 0.05). Fernandez-Lopez et al. (2008) determined that changes in surface a* values occurred throughout storage of ostrich steaks in all packages and redness values for air, vacuum and MAP (80% CO2 + 20% N2) packaged samples decreased (P b 0.05) during storage, as in the present study. Surface CIE b* values decreased (P b 0.05) during storage for ostrich meat packaged in air and MAP (Tables 2a and 2b). The smallest yellowness values were in air packaged samples reaching 8.43–8.69 at the end of storage; while MAP packages gave values between 9.60 and 10.88. In all samples, chroma (C*) values decreased during storage (Tables 2a and 2b). Significant differences appeared at day 3 (P b 0.05) and persisted until day 10 with the high O2 packages yielding the lowest values. Changes in hue (h*) values during storage are shown in Table 2b and the influence of atmosphere on surface colour follow the same behaviour observed for the a* values. A remarkable decrease was observed from the 5th day of storage (P b 0.05) for high O2 packaged samples. Fernandez-Lopez et al. (2008) emphasised that changes in hue during storage of ostrich steaks were similar to values observed for a* values. Kennedy et al. (2004) indicated that the 80:20:0/O2:CO2: N2 gas composition and the 2:1 headspace to meat volume ratio was the most effective packaging combination in maintaining and prolonging the attractive red colour of MA packaged lamb and hogget meat. Insausti et al. (1999) determined that beef under MAP (60:30:10/O2:CO2:N2) had higher lightness (L*) and hue (h*) and lower redness (a*) and chroma (C*) than beef under vacuum. Zakrys, Hogan, O'Sullivan, Allen, and Kerry (2007) reported that redness (a*) increased between days 0 and 3 in beef muscles, but instrumental a* values displayed a significant (P b 0.05) negative correlation with days, indicating a decrease in the red colour over time. However, Jayasingh et al. (2002) reported that ground beef, packaged in high oxygen MAP (80:20/O2:CO2) maintained a bright red colour for 10 days. John et al. (2005) determined that steaks packaged under high oxygen (80:20/O2:CO2) had a desirable red colour on day 7 of storage, but some browning was evident by day 14 and steaks were completely brown and unappealing by day 21. 3.6. Sensory evaluation Results of sensory analysis of ostrich meat samples for red colour, off-odour and general appearance are presented in Table 3. The

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783

Table 2a Instrumental colour (CIE L*, a*, b*) of ostrich meat during storage at 4 °C. Attribute

Headspace

Packed atmosphere

Days of storage 1

Lightness (L*)

1:1

3:1

Redness (a*)

1:1

3:1

Yellowness (b*)

1:1

3:1

a,b,c

3 b

Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 P Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 P Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 P

5 b

31.19 ± 0.73 33.60 ± 0.50a 29.19 ± 0.96b 29.82 ± 0.31b 30.56 ± 0.75b 31.17 ± 0.77b 33.36 ± 0.60a 29.71 ± 0.64b 30.08 ± 0.33b 30.29 ± 0.18b *** 12.43 ± 1.15 13.80 ± 0.87 13.86 ± 0.46 13.71 ± 0.41 12.94 ± 0.91 13.39 ± 1.34 14.41 ± 0.86 14.08 ± 1.01 13.97 ± 0.56 13.64 ± 0.93 NS 10.21 ± 0.29d 11.50 ± 0.28c 12.66 ± 0.16a 12.33 ± 0.20ab 11.41 ± 0.16c 10.31 ± 0.27d 11.76 ± 0.35bc 12.89 ± 0.22a 12.38 ± 0.32ab 11.43 ± 0.24c ***

31.55 ± 0.93 34.46 ± 0.64a 30.60 ± 0.62b 30.35 ± 0.24b 31.48 ± 0.50b 31.93 ± 0.88b 34.62 ± 0.70a 30.78 ± 0.61b 31.15 ± 0.20b 30.73 ± 0.27b *** 14.56 ± 0.80 15.80 ± 1.31 15.04 ± 0.96 14.74 ± 0.87 13.95 ± 0.82 14.66 ± 0.82 15.92 ± 1.20 14.96 ± 0.78 14.99 ± 0.93 14.41 ± 0.77 NS 11.42 ± 0.35de 11.87 ± 0.49cde 14.00 ± 0.41a 12.84 ± 0.25bc 11.85 ± 0.26cde 10.86 ± 0.78e 12.73 ± 0.59bc 14.19 ± 0.39a 13.28 ± 0.30ab 12.36 ± 0.21bcd ***

7 b

30.32 ± 0.88 32.48 ± 0.95a 29.78 ± 0.33b 29.39 ± 0.23b 30.23 ± 0.51b 30.48 ± 0.94b 32.82 ± 1.10a 29.77 ± 0.15b 29.35 ± 0.12b 29.46 ± 0.26b ** 12.25 ± 0.82 10.64 ± 1.27 12.93 ± 0.60 12.80 ± 0.68 11.67 ± 0.72 12.58 ± 1.33 11.10 ± 1.35 12.97 ± 0.67 12.72 ± 0.81 11.99 ± 0.68 NS 9.94 ± 0.32e 10.74 ± 0.25cde 12.05 ± 0.33a 11.80 ± 0.38ab 10.95 ± 0.30bcd 10.04 ± 0.28de 10.97 ± 0.13bcd 12.06 ± 0.24a 12.00 ± 0.40a 11.29 ± 0.36abc ***

10 abcd

29.59 ± 0.91 31.25 ± 0.70a 28.16 ± 1.00cd 27.68 ± 0.39d 29.32 ± 0.71bcd 29.99 ± 0.86abc 30.96 ± 0.58ab 28.72 ± 0.10cd 28.28 ± 0.27cd 29.07 ± 0.43cd ** 11.49 ± 0.86ab 7.27 ± 0.69d 10.11 ± 0.29abc 9.80 ± 0.31abc 9.79 ± 0.25abc 11.76 ± 1.50a 7.79 ± 1.19cd 9.17 ± 0.46bcd 10.03 ± 0.51abc 10.01 ± 0.31abc * 9.69 ± 0.22c 9.82 ± 0.56bc 10.92 ± 0.20ab 10.71 ± 0.25abc 10.32 ± 0.07abc 9.98 ± 0.46bc 10.69 ± 0.34abc 10.88 ± 0.23ab 11.33 ± 0.42a 10.53 ± 0.29abc *

28.58 ± 0.23b 30.79 ± 0.49a 25.40 ± 0.20e 26.47 ± 0.12de 28.14 ± 53bc 28.83 ± 0.61b 30.18 ± 0.37a 26.79 ± 0.74d 26.67 ± 1.00d 27.36 ± 0.50cd *** 10.62 ± 0.54a 6.47 ± 0.35c 7.53 ± 0.35bc 6.90 ± 0.21bc 7.36 ± 0.55bc 10.00 ± 0.94a 6.39 ± 0.59c 7.51 ± 0.35bc 7.25 ± 0.15bc 8.22 ± 0.59b *** 8.43 ± 0.32c 9.78 ± 0.45ab 10.38 ± 0.72a 10.28 ± 0.35a 9.60 ± 0.16abc 8.69 ± 0.31bc 10.34 ± 0.44a 10.28 ± 0.18a 10.88 ± 0.85a 9.83 ± 0.18ab **

: Means within a column with different letters are significantly different (P b 0.05), (*): P b 0.05 (**): P b 0.01 (***): P b 0.001.

attributes showed differences for packaged atmosphere and storage time. Even if the shelf-life was prolonged with modified atmosphere packaging; the samples were in general not acceptable after 5 days of storage in respect of panellists' preferences.

For “red colour” evaluation, high oxygen packaged samples performed better than the other groups at days 1 and 3. Significant differences were no longer observed after day 5 (P N 0.05). However, ostrich meat packaged with high O2 and 3:1 headspace ratio

Table 2b Instrumental colour (C*, h*) of ostrich meat during storage at 4 °C. Attribute

Chroma (C*)

Headspace

1:1

3:1

Hue (h*)

1:1

3:1

a,b,c

Packed atmosphere

Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 P Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 P

Days of storage 1

3

5

7

10

171.38 ± 11.36 195.41 ± 25.57 211.15 ± 18.75 191.16 ± 13.76 167.59 ± 11.52 166.50 ± 12.47 207.79 ± 25.87 212.58 ± 15.31 200.62 ± 10.88 180.29 ± 11.23 NS 1.00 ± 0.11 1.07 ± 0.08 0.74 ± 0.07 0.84 ± 0.08 0.88 ± 0.09 1.09 ± 0.08 0.97 ± 0.05 0.72 ± 0.06 0.82 ± 0.12 0.86 ± 0.08 NS

129.49 ± 16.71 161.39 ± 12.77 176.28 ± 4.66 170.08 ± 7.39 148.98 ± 12.61 142.91 ± 18.81 172.97 ± 16.16 182.29 ± 12.12 174.30 ± 5.10 158.51 ± 14.50 NS 0.93 ± 0.10 0.91 ± 0.10 0.77 ± 0.06 0.79 ± 0.03 0.82 ± 0.09 1.03 ± 0.14 0.94 ± 0.04 0.77 ± 0.12 0.82 ± 0.09 0.90 ± 0.08 NS

124.51 ± 9.12ab 114.42 ± 11.52b 156.19 ± 6.19a 151.62 ± 7.47a 128.08 ± 9.74ab 129.65 ± 13.10ab 121.89 ± 15.67ab 156.91 ± 8.53a 152.94 ± 9.75a 135.77 ± 11.56ab * 0.95 ± 0.13 0.63 ± 0.20 0.74 ± 0.09 0.76 ± 0.10 0.73 ± 0.08 0.98 ± 0.21 0.66 ± 0.17 0.75 ± 0.08 0.73 ± 0.12 0.73 ± 0.05 NS

113.07 ± 7.44a 74.67 ± 1.30c 110.80 ± 1.25ab 105.44 ± 2.10ab 101.24 ± 2.58ab 119.02 ± 13.02a 87.52 ± 10.89bc 101.26 ± 6.74ab 114.52 ± 7.12a 105.64 ± 5.97ab ** 0.89 ± 0.15a 0.22 ± 0.24b 0.54 ± 0.06ab 0.52 ± 0.07ab 0.57 ± 0.04ab 0.88 ± 0.26a 0.20 ± 0.24b 0.40 ± 0.04ab 0.47 ± 0.09ab 0.57 ± 0.02ab *

91.96 ± 3.48a 68.80 ± 2.55c 82.28 ± 2.91abc 76.74 ± 5.12abc 73.25 ± 4.64bc 87.82 ± 7.64ab 73.94 ± 1.49bc 81.04 ± 1.73abc 85.50 ± 9.42ab 82.15 ± 5.41abc * 0.98 ± 0.13a 0.06 ± 0.16bc 0.19 ± 0.06bc 0.08 ± 0.05bc 0.27 ± 0.11bc 0.85 ± 0.19a − 0.05 ± 0.26c 0.20 ± 0.02bc 0.07 ± 0.13bc 0.39 ± 0.09b ***

: Means within a column with different letters are significantly different (P b 0.05), (*): P b 0.05 (**): P b 0.01 (***): P b 0.001.

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Table 3 Sensory evaluation (red colour, off-odour, and general appearance) of ostrich meat during storage at 4 °C. Attribute

Headspace

Packed atmosphere

Days of storage 1

Red colour

1:1

3:1

Off-odour

1:1

3:1

Appearance

1:1

3:1

a,b,c

Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 P Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 P Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 Air 80:20:0/O2:CO2:N2 60:20:20/O2:CO2:N2 60:40:0/O2:CO2:N2 40:40:20/O2:CO2:N2 P

3 cx

6.76 ± 0.39 8.36 ± 0.19ax 7.80 ± 0.40abcx 7.50 ± 0.50abcx 7.53 ± 0.57abcx 6.90 ± 0.21bcx 8.50 ± 0.25ax 8.33 ± 0.17abx 7.46 ± 0.73abcx 7.36 ± 0.53abcx * 7.33 ± 0.67x 7.96 ± 0.48x 7.96 ± 0.48x 8.00 ± 0.50x 7.70 ± 0.35x 6.90 ± 0.70x 8.06 ± 0.67x 7.70 ± 0.30x 7.66 ± 0.33x 7.33 ± 0.17x NS 7.43 ± 0.22x 8.33 ± 0.17x 8.00 ± 0.00x 7.86 ± 0.19x 7.26 ± 0.48x 7.26 ± 0.53x 8.43 ± 0.22x 7.86 ± 0.44x 7.53 ± 0.57x 7.13 ± 0.87x NS

5 by

5.86 ± 0.59 8.03 ± 0.48ax 7.43 ± 0.28ax 7.33 ± 0.33ax 6.90 ± 0.77abx 7.00 ± 0.01abx 8.06 ± 0.67ax 7.40 ± 0.45ay 6.96 ± 0.73abx 7.50 ± 0.01ax * 6.93 ± 0.47x 7.70 ± 0.35x 7.66 ± 0.33x 7.33 ± 0.67x 7.43 ± 0.23x 6.83 ± 0.42x 7.56 ± 0.28y 7.90 ± 0.77x 7.86 ± 0.67x 6.93 ± 0.22x NS 7.23 ± 0.12x 8.13 ± 0.67x 8.33 ± 0.33x 8.13 ± 0.44x 7.46 ± 0.23x 7.26 ± 0.23x 8.20 ± 1.00x 7.66 ± 0.33x 7.76 ± 0.13x 7.16 ± 0.43x NS

7 y

5.60 ± 0.60 5.23 ± 0.63y 5.43 ± 1.28y 4.86 ± 0.76y 5.00 ± 1.00y 6.96 ± 0.41x 6.53 ± 0.31y 6.06 ± 0.66z 6.03 ± 0.23y 6.50 ± 0.85y NS 6.83 ± 0.15bcx 7.26 ± 0.40abcx 7.30 ± 0.10abx 6.83 ± 0.29bcy 6.66 ± 0.40cdy 6.70 ± 0.01bcx 7.26 ± 0.77abcy 7.56 ± 0.21ax 6.90 ± 0.36bcy 6.23 ± 0.64dy ** 5.86 ± 0.31y 5.43 ± 0.78y 5.50 ± 1.00y 5.16 ± 0.66y 5.70 ± 1.15y 6.03 ± 0.33y 5.86 ± 0.18y 5.73 ± 0.37y 5.86 ± 0.31y 5.53 ± 0.33y NS

10 z

4.16 ± 0.71 4.10 ± 0.10z 4.10 ± 0.45z 3.90 ± 0.77z 4.00 ± 0.20z 4.73 ± 0.63y 4.33 ± 0.21z 4.16 ± 0.81v 4.26 ± 0.16z 4.13 ± 0.33z NS 3.20 ± 0.65ey 4.83 ± 0.53ay 4.80 ± 0.60ay 5.00 ± 0.90az 4.06 ± 0.66bcz 3.53 ± 0.33dy 4.66 ± 0.57az 4.10 ± 0.95by 4.26 ± 0.81bz 3.80 ± 0.60cz * 3.63 ± 0.63z 4.83 ± 0.33z 4.70 ± 0.65z 4.73 ± 0.73z 4.16 ± 0.16z 4.83 ± 0.58z 4.86 ± 0.31z 4.46 ± 0.31z 4.73 ± 0.73z 4.33 ± 0.33z NS

2.56 ± 0.12v 3.43 ± 0.12v 3.40 ± 0.77v 3.23 ± 0.26v 3.10 ± 0.77v 3.23 ± 0.21z 3.70 ± 0.15v 3.26 ± 0.38t 3.23 ± 0.16v 3.33 ± 0.12v NS 2.50 ± 1.00cy 3.83 ± 0.16abcy 4.40 ± 0.40ay 4.00 ± 0.25abv 3.53 ± 0.81abcz 2.70 ± 0.35bcz 3.46 ± 0.81abcv 2.50 ± 0.35cz 2.93 ± 0.31bcv 2.66 ± 0.33bcv * 2.53 ± 0.53v 3.40 ± 0.40v 3.56 ± 0.47v 3.50 ± 0.65v 3.23 ± 0.48v 3.40 ± 0.35v 3.36 ± 0.16v 3.16 ± 0.16v 3.43 ± 0.63v 2.86 ± 0.21v NS

: Means within a column with different letters are significantly different (P b 0.05), (*): P b 0.05 (**): P b 0.01 (***): P b 0.001. : For each attribute, means within a row with different letters are significantly different (P b 0.05).

x,y,z

atmosphere was more acceptable during the entire storage time. These results fit only partially with the a* values (Tables 2a and 2b). Fernandez-Lopez et al. (2008) stated that MAP + CO (30% CO2 + 69.8% argon + 0.2% CO) packaged ostrich meat showed the best scores (P b 0.05) throughout all the storage time (18 days). Some researchers indicated that, in packaged meat, the presence of oxygen is necessary to have a better perception of the characteristic red colour of fresh meat due to oxymyoglobin pigment (Luño, Beltrán, & Roncalés, 1998; Renerre, Anton, & Gatellier, 1992). Although significant differences were not observed over the entire storage time (P N 0.05), the 1:1 headspace ratio and CO2 atmosphere packaged samples were more acceptable by the panellists. For this reason, “appearance” scores were not in accord with the colour scores. “Off-odour” evaluation showed no differences (P N 0.05) between air and MAP packaged samples up to 5th day of storage. Those packaged with high O2 and 3:1 headspace ratio atmospheres received better scores during the entire storage. Fernandez-Lopez et al. (2008) determined that off-odour evaluation showed differences (P b 0.05) between air and MAP packs. They emphasised that the off-odours were mainly putrefactive and sour, and the air packed samples had the highest scores (P b 0.05) for off-odour. Vergara and Gallego (2001) reported that off-odour developed much more rapidly (from 7 days onwards) in low CO2 packaged lamb meat compared to other MAP packs and also, redness was significantly decreased (P b 0.05). John et al. (2005) stated that steaks packaged in 80% oxygen or CO retained desirable red colours for 14 and 21 days, respectively. Zakrys et al. (2007) emphasised that panellists expressed a preference for steaks

stored in packs containing 50% oxygen, despite detecting oxidised flavours under these conditions. 4. Conclusion Although ostrich meat is perceived as a red meat, the comparison between ostrich and beef may lead to very different bacterial counts because of differences between birds' and mammals' gastrointestinal tracts and the early processes of meat preparation. The relatively high pH of ostrich meat creates an ideal environment for rapid microbial spoilage. The quality and shelf-life of ostrich meat packaged by various gas compositions of modified atmosphere were somewhat improved; microbial growth in the meats was delayed due to high CO2 usage and shelf-life was increased by 5–7 days. The longer the exposure to high CO2 concentration, the more effective the inhibition of microbial growth. Additionally, high O2 concentrations promote the formation of oxymyoglobin (OxyMb), but this may impact negatively on the oxidative stability of muscle lipids and lead to the development of undesirable flavours. The high CO2 contents prevented increased lipid oxidation and increased acceptable shelf-life by more than 5 days. Furthermore, the increase in O2 inside the package causes rapid loss of redness of ostrich meat and thus the desired red-colour is not obtained. The consumer may be adversely affected by this. Acknowledgement The present work was supported by the Research Fund of Istanbul University, Istanbul, Turkey. Project no. T-764/27122005.

E.B. Bingol, O. Ergun / Meat Science 88 (2011) 774–785

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