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Poult Sci 2006. 85:1821-1828
© 2006 Poultry Science Association
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PROCESSING, PRODUCTS, AND FOOD SAFETY

Growth Depth Effects of Bacteria in Ground Turkey Meat Patties Subjected to High Carbon Dioxide or High Oxygen Atmospheres

R. Dhananjayan, I. Y. Han, J. C. Acton and P. L. Dawson

Department of Food Science and Human Nutrition, Clemson University, SC 29634

1 Corresponding author: pdawson{at}clemson.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Modified atmosphere packaging (MAP) is used to extend the shelf life of ground meats by altering the gas atmosphere surrounding the meat. This study evaluated how deep MAP bactericidal effects penetrate into a ground meat patty. Patties made from freshly ground turkey breasts were subjected to 2 MAP treatments of high CO2 (97%) or high O2 (80% O2, 20% CO2). Total plate and lactic acid bacterial counts were determined for 3 patty depths (top, middle, bottom). Meat surface color and the package gas headspace composition were also measured. All analyses were performed on 0, 3, 6, 9, and 12 d. Changes in gas headspace and meat surface color were also measured at 0, 3, 6, 9, and 12 d. High CO2 atmosphere maintained a better meat surface color than high O2 atmosphere over the whole storage period. Overall counts were lower (P ≤ 0.05) in a high-CO2 atmosphere compared with a high-O2 modified atmosphere. Patties stored under a high-CO2 atmosphere displayed slower bacterial growth in the top layer compared with the middle and bottom layers. Total plate count did not differ (P ≥ 0.05) in layers for patties pack-aged in a high-O2 atmosphere Lactic acid bacterial counts increased in the high-O2 modified atmosphere by d 9 and 12 of storage; no increase was observed in CO2-packaged patties. Thus, high-CO2 MAP slowed the growth of total bacteria as well as lactic acid bacteria. Also, there was slower growth in the top meat layer exposed to CO2 compared with interior layers.

Key Words: modified atmosphere packaging • ground turkey meat • bacterial growth depth meat color


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 REFERENCES
 
Three sensory properties by which consumers judge meat quality are appearance, texture, and flavor. The most important property at the time of purchase is appearance, because texture and flavor cannot be evaluated when the product is packaged. Surface discoloration is inevitable and is used as an indicator of freshness. Both deoxymyoglobin and oxymyoglobin are oxidized to form metmyoglobin, which has a dull, brown color associated with deterioration of quality (Hood and Riordan, 1973). The oxidation of deoxymyoglobin is more rapid than the oxidation of oxymyoglobin (Gill, 1996), and oxidation of myoglobin at low O2 (~5 to 7%) is more rapid than at high concentrations of O (O’Keeffe and Hood, 1982; Gill, 1996). The oxygenation of myoglobin is rapid and reversible, and the fraction of the pigment in the oxygenated form increases with increasing concentrations of O (Forrest et al., 1975). Ground meat color stability is achieved by slowing the reactions associated with pigment oxidation and by increasing the depth of the oxygenated surface layer. Apart from maintaining meat at low temperatures with-out freezing, there are 2 obvious means of preserving muscle tissue color. The atmosphere surrounding the meat can be modified (Rousset and Renerre, 1990) by exposing the meat to high concentrations of O to increase the fraction of oxidation resistant oxymyoglobin or O can be completely excluded to increase deoxymyoglobin levels.

Ledward (1992) stated that a typical modified atmosphere for storing ground red meat was 80% O2 and 20% CO2, in which the high O level serves to increase the depth of the oxymyoglobin layer at the meat surface, and the CO2 level slows microbial growth. Skandamis et al. (2002) reported that 100% CO2 extended fresh meat shelf life compared with air, vacuum, 40% CO2, and 80% CO2 mixtures of modified atmospheres. Similar high-O2 gas compositions have been utilized for ground turkey; however, Baker et al. (1985) reported that high-CO2 modified atmosphere packaging (MAP) improved ground chicken shelf life. Furthermore, Saucier et al. (2000) found that the hue of ground chicken and turkey remained more stable in gas atmospheres devoid of O2. Modification of the atmosphere within the package by reducing the O content and increasing the levels CO2, N2, or both has been shown to significantly extend the shelf life of perishable foods at chill temperatures by suppressing spoilage bacterial growth (Parry, 1993). Carbon dioxide atmospheres have been found to suppress the growth of Pseudomonas spp. (Enfors and Molin, 1980; Molin, 1985a). Pseudomonas spp. has been detected in meat stored in a low-O2 atmosphere containing CO2 but not in an O2-free atmosphere with or without CO2 (Molin, 1985b) This indicated that although CO2 reduced the growth rate of P. spp, the complete inhibition of these organisms can only be achieved by a nearly complete removal of O (Newton and Gill, 1978). Packaging chicken under CO2 reduced growth of total aerobes, psychrotrophs, Enterobacteriaceae, and P. spp (Sawaya et al., 1995).

The antimicrobial effect of a CO2-enriched atmosphere requires continuous contact of CO2 with meat, as short exposure to even high levels of CO2 is ineffective in providing a residual effect (Narasimha and Sachindra, 2002). In one study, residual effect of CO2 on microbial growth observed when chicken meat was stored in 80% CO2, whereas a CO2 concentration of 60% was not sufficient to slow microbial growth compared with chicken stored in ambient air (Baker et al., 1985). Bacteria grow faster in minced meat compared with intact muscle due to the enhanced substrate availability in minced meat (Bhonsack and Hope, 1990). Dissolution of CO2 into the aqueous phase of the meat will likely enhance the inhibition of bacterial growth in meat. Because meat is ground in air and then packaged in a modified atmosphere, the depth of the antimicrobial effect into the meat may be limited by how far the gas penetrates into the meat. The objective of this study was to determine how MAP of ground turkey affected the growth of bacteria at different depths from the meat surface into the ground meat.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 REFERENCES
 
Meat and Packaging
Whole fresh turkey breast meat was purchased from a local retail market. Skin was removed, and meat was cut into small pieces using a sterile knife. Cut meat pieces were thoroughly mixed before grinding. The meat was then ground (American Eagle Food Machinery Inc., Chicago, IL) twice using 2 sieves, 1 with a 1.2-mm diameter, followed by 1 with a 0.4-mm diameter. Patties were prepared from 220 g of ground meat, packaged in expanded polystyrene barrier trays, and sealed with barrier lid stock (Sealed Air Corp., Duncan, SC). Container volume was approximately 880 mL, and 220 g of meat was selected to give approximately a 3:1, package headspace:meat volume ratio. Trays containing patties were packaged in high CO2 (97%) or high O2 (80%) using a preformed tray pack-aging machine (Robert Reiser & Co Inc., Canton, MA). Gas tanks were premixed (National Welders Supply Co. Inc., Greenville, SC) to target high CO2 (100% CO2) or high O2 (80% O2, 20% CO2). Packaged meat was refrigerated at 4°C ± 1°C in a lighted refrigerator. Package gas headspace, meat color, and total plate and lactic acid bacterial (LAB) counts were determined 0, 3, 6, 9, and 12 d after packaging.

Package Headspace Gas Analysis
A 500-µL sample of package gas headspace was drawn by syringe through a silicone septum on the package surface. Gas samples were analyzed by gas chromatography using a thermal conductivity detector (series 580, Gow-Mac Instrument Co., Bethlehem, PA) with a column (catalog number 8700, Alltech Associates Inc., Deerfield, IL) at 30°C. The injector and conductivity detector were 100°C, and He was the carrier gas, with a flow rate of 60 mL/min. Percentage of CO2, O2, and N2 was calculated from the response recorded on a strip recorder.

Color Analysis
Ground turkey patty surface color was measured using a colorimeter (Minolta Chroma Meter Model CR-300, Minolta Corp., Ramsey, NJ) having an 8-mm measuring orifice. The colorimeter was calibrated using a calibration plate (Y = 92.80; x = 0.3134, y = 0.3197). Sample lightness (L*), redness (a*), and yellowness (b*) values were determined using an International Commission on Illumination illuminant incandescent light source. Lightness, a*, and b* are color measurement units quantitating the meat surface lightness-darkness, redness-greenness, and blueness-yellowness, respectively. One patty was taken from each modified atmosphere on d 0, 3, 6, 9, and 12 for color analysis. All 4 sides of the packaging film were cut so that the colorimeter orifice could be pressed smoothly against the package film meat surface. Color measurements were taken through the film, and film color properties were subtracted from the color readings. Three measurements at different locations were taken from each sample. Three measurements were averaged as the sample’s color coordinate value. Hue was calculated using tan–1 (b*/a*; Francis and Clydesdale, 1975) and chroma value was calculated using a2 + b2 (Acton and Dawson, 1994).

Microbiological Analysis
Ground turkey breast meat patties were prepared to a height of 3 cm using a petri dish having a depth of 5 cm (dimensions of 50 x 100 mm). These patties were placed in expanded polystyrene trays and subjected to MAP. For patty depth analysis, each patty was divided into 3 layers: top, middle, and bottom. The initial depth of 1 cm starting from the surface of the patty in contact with the modified atmosphere was designated the top layer, followed by the next 1-cm depth as the middle layer, and the last 1-cm depth of the patty, which was in contact with tray, the bottom layer of the patty. For the top layer, 11 g of meat taken from the surface of the patty was used for analysis. For the middle layer, 11 g of meat was taken at a depth of 1 cm from the surface of the patty using a sterile spatula. For this layer, 1 cm was left from the outer rim of the patty in a circumference to avoid any effect of the modified atmosphere from the patty sides when taking the middle layer. For the bottom layer, meat was flipped over a sterile Al foil sheet, and 11 g of sample was taken using a sterile spatula. These depths were chosen after preliminary studies to account for the entire meat patty. The middle and bottom layers did not include the outer 1-cm edge of the patty, so none of these layers were directly exposed to the gas during storage. Meat layers were measured and removed using a sterile stainless steel ruler and spatula, respectively. On 3, 6, 9, and 12 d, 3 layers from 1 patty from each atmosphere were taken for microbiological analysis.

Eleven grams obtained from the different layers were each diluted with 99 mL of 0.1% wt/vol sterile peptone solution (Bacto peptone, Difco Laboratories, Detroit, MI) for a 1:10 dilution. Contents were then homogenized in a stomacher (Seward Ltd., London, UK) for 2 min at 230 rpm. Cell numbers were determined using the pour plate method (Speck, 1984). Total aerobic plate count was determined using plate count agar (Difco Laboratories), and lactobacilli counts were determined using de Man, Rogosa, and Sharpe medium (Difco Laboratories). Total aerobic plates were incubated at 37°C for 48 h before counting. Lactobacilli plates were placed in a CO2 incubator (model 2300, VWR Scientific Products, West Chester, PA) with 5% CO2 injected (35 psi) at 37°C for 48 h. All platings were performed in duplicate. Plated dilutions with 25 to 250 colonies were counted, and then numbers were converted to log10 cfu/g of meat.

Statistical Analysis
The experimental design was a 3 x 2 x 5 randomized complete block design (3 levels of depth, 2 levels of modified atmosphere, and 5 levels of storage time). A GLM was used to determine the ANOVA. When the treatment effect was significant (P ≤ 0.05), the means were separated using the LSMEANS, PDIFF, and STDERR statement using SAS Release 8.0 (SAS Institute, 1999). The experiment was replicated using 3 separate batches of meat. The replications were used as the blocking factor.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
REFERENCES
 
Package Headspace Gas
For the high-O2 treatment (Table 1Go), headspace O concentration was relatively high from d 0 to 6, with a decrease by d 12. The decrease in headspace O2 for the high-O treatment may be due to growth of microorganisms that consumed O2 and produced CO2 (Butler et al., 1953). The decrease in O concentration was accompanied by an increase in total aerobic bacterial count that may have included pseudomonads. Nychas and Arkoudelos (1990) also reported that the composition of the gas phase changed during storage, with a decrease in O concentration and a subsequent increase in the number of pseudomonads and the concentration of gluconate (a product of aerobic metabolism). Some of the reduction in O concentration may be attributed to meat tissue respiration (Lawrie, 1998).


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  		Table 1. Package headspace gas analysis for ground turkey meat pack-aged in high CO2 or high O2 held under refrigeration (4°C) for 12 d
 
In the high-CO2 treatment, CO2 decreased by the d 6 from initial levels. Decrease in headspace CO2 can be attributed to CO2 solubilization in meat and gas production by bacteria. Decrease in headspace CO2 during the storage of MAP meat [d 0 (96%) to d 12 (90%)] was previously attributed to CO2 dissolving in the meat tissue (Baker et al., 1985; Mc Mullen and Stiles, 1991; Gill, 1996). Gill (1988) stated that CO2 is highly soluble in both water and oil, thus it can readily absorb into muscle and fat tissue during storage. Because N2 is an inert gas, the change in N2 in the high-CO2 treatment was likely only a reflection of the changes in CO2 concentration.

Color
The gas MAP treatment by storage time interaction for L* value was significant (P ≤ 0.05). A lower L* value and a higher a* value reflected a good meat color stability in patties packaged under a high-CO2 atmosphere (Table 2Go). Boulianne and King (1995) suggested that L* value could be used with high sensitivity and high specificity to distinguish pale, soft, exudative meat from normal meat. Thus, L* value can distinguish differences in L* for intact meat pieces. Ground turkey meat is lighter and, therefore, may show higher L* as compared with ground beef due to lower pigment concentration (Saucier et al., 2000).


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  		Table 2. CIE lightness (L*) and redness (a*) values for ground turkey meat packaged in high CO2 or high O2 under refrigeration (4°C ± 1°C) for 12 d1
 
The meat packaged in high CO2 maintained higher a* values (Table 1Go) and redder color (Figure 1Go) from 6 to 12 d compared with meat packaged in high O2. There was no difference (P ≥ 0.05) between a* values of the patties packaged under a high-CO2 atmosphere and patties packaged under a high-O2 atmosphere until d 6 of storage. This could be due to the limited ability of the poultry meat to bloom (form oxymyoglobin) as compared with beef and pork. Millar et al. (1994) observed little evidence of oxymyoglobin formation when chicken meat was kept at 5°C for 48 h, and no oxymyoglobin was found in chicken meat stored at 23°C. The lack of oxymyoglobin formation in poultry is supported by Millar et al. (1994), who observed that chicken and turkey retail samples appeared to be either purple or purple-brown in color. This is attributed to high metmyoglobin-reducing activity and the high O consumption rate of poultry meat. Mercier et al. (1998) reported that ground poultry meat stored in a gas mixture without O (20% CO2, 80% N2) increased in a* value, indicating the gas mixture maintained myoglobin, probably through metmyoglobin-reducing activity. The decrease in a* value of meat packaged in the high-O2 atmosphere in this study reflects myoglobin oxidation.


Figure 1
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  		Figure 1. Pictures of meat surface color angle for ground turkey meat packaged in high CO2 or high O2 under refrigeration (4°C) for 12 d.

 
Hue Angle
Hue angles of patties kept under a high-O2 atmosphere increased by d 6 of storage. Increase in hue angle (Figure 2Go) indicates a shift in color from red to yellow, which may indicate increased pigment oxidation and the formation of metmyoglobin. Discoloration of meat stored in high O2 by d 6 of storage may be attributed to the high O consumption rate of the meat. Millar et al. (1994) reported that chicken breast muscles had little capacity to form oxymyoglobin when exposed to air, and the high O consumption rate associated with these muscles encouraged the formation of metmyoglobin at the surface. Millar et al. (1994) also demonstrated that, after 24 h at 5°C, chicken muscle tissue oxidized to produce some metmyoglobin at the surface. The relative differences in total myoglobin content between meat from different species and muscle will affect the appearance and intensity of color due to changes in myoglobin state. Saucier et al. (2000) found an increase in hue angle for ground chicken and turkey meat during storage in an atmosphere con- taining O (62% CO2, 8% O2, 30% N2) as compared with an atmosphere without O2 (20% CO2, 80% N2), whereas hue values for ground chicken and turkey meat remained relatively stable in an atmosphere devoid of O. Gill (1996) stated that retail cuts of pork and beef containing 80% O2 and 20% CO2 will slow color deterioration but will only slightly increase the microbiological shelf life compared with packaging in air.


Figure 2
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  		Figure 2. Hue angle for ground turkey meat packaged in high CO2 or high O2 under refrigeration (4°C) for 12 d. Layers with different superscripts are significantly different (P ≤ 0.05); number of observations = 45.

 
Microbiology
Because of the homogenous nature of the sample, all samples initially started with the same microbial load on d 0 of storage. High concentrations of O are lethal to living cells, causing inactivation of certain enzymes, an increase in intracellular concentration of H2O2, oxidation of membrane lipids, and production of superoxide in the cell (Zeitoun and Debevere, 1993). High concentrationsof CO2 are bacteriocidal, decreasing intracellular pH, inhibiting enzymatically catalyzed reactions and enzyme synthesis, and interacting with the cell membrane. High CO2 MAP has previously been shown to improve the shelf life of chicken carcasses (Sawaya et al., 1995) and ground chicken (Baker et al., 1985). Patties packaged in a high-O2 atmosphere showed higher total aerobic bacterial counts (5.6 log10 cfu/g) compared with patties packaged in high CO2 (4.3 log10 cfu/g).

Total Aerobic Plate Count.
There was a slower bacterial growth rate in patties packaged under a high-CO2 atmosphere compared with a high-O2 atmosphere throughout storage (P < 0.05). The average total aerobic plate count throughout storage for the high-O2 and high-CO2 packaged meat was 5.69 and 4.37 cfu/g, respectively. Furthermore, the bacterial population of CO2-packaged meat in the top layer (3.93 cfu/g) was lower than the middle (4.61 cfu/g) and bottom (4.56 cfu/g) layers. The top layer of meat packaged in high O2 had a higher (P < 0.05) bacterial population (5.58 cfu/g) than the top layer of meat packaged in high CO2 (3.93 cfu/g). This has been attributed to the effect of CO2 in the package headspace, creating anaerobic conditions and reducing meat pH. Carbon dioxide retards the growth of the fast-growing pseudomonads that usually cause the spoilage of meat under aerobic conditions (Wolfe, 1980; Zeitoun and Debevere, 1993; Devlieghere and Debevere, 2000; Luno et al., 2000; Narasimha and Sachindra, 2002). Gram-negative bacteria would also be more susceptible to inhibition by CO2 than the gram-positive bacteria (Sutherland et al., 1997). These results are supported by Erichsen and Molin (1981), who found lower total aerobic bacterial counts for beef in 100% CO2 compared with beef stored in air, a vacuum, or a gas mixture of 78% N2, 20% CO2, and 2% O2 when held at 4°C. Packaging chicken under CO2 compared with air slowed growth of total aerobes, psychrotrophs, and Enterobacteriaceae (Gill, 1996). Carbon dioxide is believed to inhibit the metabolism of Pseudomonas aeruginosa by decreasing isocitrate dehydrogenase and malate dehydrogenase activity (Hammes et al., 1983).

Patties packaged in a high-CO2 atmosphere had lower (P ≤ 0.05) total aerobic bacterial counts in the top layer compared with the middle and bottom layers (Figure 3Go). There was no difference (P ≥ 0.05) in total aerobic bacterial counts between the middle and bottom layers of patties. The reduced bacterial growth in the top layer was probably due to dissolving of CO2 into part of the first 1-cm depth of the patty, which was in constant contact with high-CO2 gas in the package headspace. There was a noticeable collapse of the package observed by d 3 of storage, which may be due to CO2 dissolving in the water and fat phases of the meat (Devlieghere et al., 1998). Devlieghere et al. (1998) demonstrated that concentration of dissolved CO2 determines the growth inhibition of micro-organisms in a modified atmosphere.


Figure 3
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  		Figure 3. Total plate count for 1-cm meat layers [top (t), middle (m), bottom (b)] for ground turkey meat patties packaged in high CO2 or high O2 under refrigeration (4°C) for 12 d. Slopes for the linear regression over 12 d of aerobic bacteria populations with different superscripts are significantly different (P ≤ 0.05); number of observations = 6.

 
There was no difference in total aerobic bacterial counts among the 3 layers for patties packaged in a high-O2 atmosphere after 12 d of storage (Figure 3Go). This result is supported by Borch et al. (1996), who stated that packages containing up to 80% O2 and 20% CO2 will reduce the color deterioration of retail cuts of meat but will only slightly increase the shelf life compared with aerobic storage. Ordonez et al. (1991) and Jackson et al. (1992) showed that Brochothrix thermosphacta, P. spp., Leuconostoc spp., and Lactobacillus spp. are able to grow to high numbers in a high-O2 modified atmosphere.

It has been proposed that CO2 penetrates the bacterial cell membrane, causing intracellular pH changes of a greater magnitude than that would be found in similar external acidification, which can be effectively buffered by the organism (Aickin and Thomas, 1975). Zeitoun and Debevere (1993) stated that CO2 could cause inhibition of cytoplasmic enzymes by affecting the rate at which particular reactions proceeded. Although the mechanisms of inhibition by CO2 are sometimes debated, Young et al. (1998) demonstrated that the 1 result is an increase in the lag phase and generation time, which slows the increase in bacterial populations.

Lactic Acid Bacteria
Lactic acid bacterial counts in ground turkey meat were lower (P ≤ 0.05) in a high-CO2 atmosphere (2.06 log10 cfu/ g) compared with a high-O2 atmosphere (2.77 log10 cfu/ g) after 12 d of storage (Figure 4Go). For the meat stored in high CO2, LAB populations did not increase during the 12-d storage period. Samelis and Georgiadou (2000) found that 100% CO2 slightly retarded LAB growth at 4 and 10°C, and this may explain the lower LAB counts compared with total aerobic bacterial counts observed at high CO2 concentrations. The lack of increase in LAB populations during storage in high CO2 may also be partially because LAB form a diverse group of organisms (homofermentative and heterofermentative) and are dif-ficult to enumerate with 1 growth medium. Pseudomonads may have outgrown the LAB due to their ability to grow in a wide range of CO2 levels. Baker et al. (1985) found that, after 7 d of storage, P. spp. was the predominant bacteria detected in ground chicken, regardless of the concentration of CO2 in the atmosphere. After 14 d of storage, P. spp. represented 50% of the genera in all CO2-treated samples. Pseudomonas spp. are able to grow under near-anaerobic conditions, as shown by Saucier et al. (2000). Furthermore, Saucier et al. (2000) found that the bacterial populations obtained on all-purpose tween agar were significantly higher than those obtained on de Man, Rogosa, and Sharpe medium (standard medium used for LAB) in or from samples stored in an atmosphere containing 62% CO2, 8% O2, and balanced with N2. For meat packaged in a high-O2 gas environment, the LAB growth was biphasic in that from d 0 to 6 there was no increase in their populations; from d 6 through 12, there was a significant increase in the slope of the growth curves.


Figure 4
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  		Figure 4. Lactic acid bacterial (LAB) plate count for 1-cm meat layers [top (t), middle (m), bottom (b)] for ground turkey meat patties packaged in high CO2 or high O2 under refrigeration (4°C) for 12 d. Slopes for the linear regression from d 6 though 12 of LAB populations with different superscripts are significantly different (P ≤ 0.05); number of observations = 6.

 
There was no difference (P > 0.05) in LAB populations from the 3 layers for the patties subjected to a high-O2 or a high-CO2 atmosphere until d 6 of storage, after which an increase in counts was observed for patties stored in a high-O2 atmosphere (Figure 4Go). Ordonez et al. (1991), Jackson et al. (1992), and Pin et al. (2002) showed that B. thermosphacta, P. spp., Leuconostoc spp., and L. spp. are able to grow to high numbers in a high-O2 modified atmospheres. Blickstad et al. (1981) and Greer et al. (1993) stated that the shelf life is extended by using a high-CO2 atmosphere, because some LAB grow more slowly under these conditions. Depending upon the pH and storage temperature, other bacteria, such as Aeromonas spp., B. thermosphacta, and Enterobacteriaceae, may grow (Blickstad and Molin, 1983; McMullen and Stiles, 1993).

A high-CO2 atmosphere helped maintain the color of ground turkey meat, as indicated by higher a* values, constant hue angles, and lower L* values throughout refrigerated storage compared with meat packaged in high O2. The surface color of patties packaged in a high-O2 atmosphere was less stable compared with meat in high CO2. Patties stored in a high-CO2 atmosphere showed lower total aerobic bacterial counts and LAB counts when compared with a high-O2 atmosphere. A layer effect was observed in patties packaged under high CO2 atmosphere, in which the top layer showed lower (P ≤ 0.05) total aerobic bacterial counts compared with the middle and the bottom layers. There was no layer effect observed in the patty packaged under a high-O2 atmosphere. Thus, the high CO2 atmosphere both maintained meat color and inhibited the growth of microorganisms, resulting in lower total aerobic bacterial and LAB counts in ground turkey. The suppression of bacterial growth was greatest in the top surface layer of the patty, where maximum CO2 dissolution occurred.

Received for publication December 17, 2005. Accepted for publication June 17, 2006.


   REFERENCES
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 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
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