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Sodium lactate and storage temperature effects on shelf life of vacuum packaged beef top rounds
Meat Science 53 (1999) 23±29
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Sodium lactate and storage temperature eects on shelf life of vacuum packaged beef top rounds J.V. Maca a, R.K. Miller b,*, M.E. Bigner c, L.M. Lucia b, G.R. Acu b a
b
Nabisco, Inc., Morristown, NJ, USA Texas A&M University, Department of Animal Science, College Station, TX 77843-2471, USA c USDA, ARS, Beltsville, MD, USA Received 19 February 1999; accepted 27 February 1999
Abstract Cooked, vacuum-packaged beef top rounds containing up to 4% sodium lactate (NaL) in the ®nal product were stored at 0, 4, 10 or 16 C for 1, 7, 14 or 21 days. Aerobic plate counts (APCs) were lower for roasts containing 3 or 4% NaL and stored at 10 C for 7 days. At higher temperatures and longer storage times, only those treated with 4% NaL were lower than controls. Lipid oxidation, Hunter L* and b* values decreased and Hunter a* values, cooked yields and Ph increased with NaL addition. Beefy odor decreased with storage but was higher in roasts containing NaL. Roasts with added NaL had lower rancid odor scores. # 1999 Elsevier Science Ltd. All rights reserved. Keywords: Beef; Sodium lactate; Storage; Shelf-life
1. Introduction The economic and quality advantages achieved in recent years in the value-added meat industry, such as higher cooking yields, improved ¯avor, increased palatability, increased shelf-life and decreased microbial growth, have led to more marketable meat products to meet consumer demands for convenient foods. As a result, the delicatessen section was the fastest growing segment of the supermarket (Litwak, 1989); however, recontamination of precooked meat items provide a potential food safety risk, because meat products sold in a delicatessen are often sliced, served and consumed without additional heating. Also, the shelf-life of uncured deli beef is usually less than 45 days. Nitrites have been used extensively to limit microbiological growth and extend shelf-life, however, consumer concerns about nitrosamine formation have increased. Alternative ingredients to maintain shelflife in precooked beef products that are positively perceived by consumers are needed. Sodium lactate (NaL), the sodium salt of lactic acid, has a bacteriostatic eect in uncured, refrigerated precooked roast beef (Anonymous, 1988; Evans, 1992; * Corresponding author. Tel.: +1-409-845-3935; fax: +1-409-8459454. E-mail address: [email protected] (R.K. Miller)
Pagach, 1992; Papadopoulos et al., 1991a; Papadopoulos, Miller, Acu, Vanderzant & Cross, 1991b; Papadopoulos, Miller, Ringer & Cross, 1991c), as well as having an inhibitory eect on growth of Streptococcus faecalis, Staphylococcus aureus and Salmonella typhimurium in other products (Maas, Glass & Doyle, 1989). Control of microbial growth with bacteriostatic ingredients may have adverse eects on a product's color, odor, ¯avor, appearance or palatability, which can be quality indicators to consumers. It is important, therefore, to understand what eect NaL has on color and color deterioration in cooked beef products and if this deterioration is proportionate to microbiological spoilage. Since it is still unknown to what extent NaL is eective in controlling microbial spoilage at various storage temperatures, the objective of this study was to determine the eect of NaL in cooked beef top rounds on microbiological, chemical, color and olfactory sensory attributes and lipid oxidation. 2. Materials and methods 2.1. Processing USDA Select beef top rounds (n=64) were obtained from a commercial beef processor from the same
0309-1740/99/$ - see front matter # 1999 Elsevier Science Ltd. All rights reserved. PII: S0309-1740(99)00032-7
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J.V. Maca et al. / Meat Science 53 (1999) 23±29
processing day and shift to assure consistent age. Top rounds were trimmed to 0 cm external fat and the abductor muscle was removed. Quartered top rounds were injected to 20% of the original (green) weight with an Inject Star B125 (Inject Star Systems, Globus Laboratories, Inc., South Hackensack, NJ) to contain 0.5% sodium chloride, 0.3% sodium tripolyphosphate and either 0, 2, 3 or 4% NaL in the ®nal product (Purac, Inc., Arlington Heights, IL). As NaL is sold on a 60% dry weight basis, 0, 3.33, 5, and 6.6% of the wet based product was added to the ®nal product. Four quartered top rounds from each treatment were processed on each of 4 days, vacuum-tumbled 2 h in a Vortron1 vacuum tumbler (Type 021-333 56-7, Parker CPI, Beloit, WI). Additional brine was added before tumbling, as needed, to insure a 20% total pickup weight. After tumbling, top rounds were submerged in their respective brine solutions and allowed to equilibrate for 36 h at 4 C and retumbled 15 min prior to cooking in vacuum-sealed CN530 cook-in-bags (Cryovac Division, WR Grace and Company, Duncan, SC). Top rounds then were cooked in an Alkar two-truck food processing oven (Model PP024519, DEC International, Lodi, WI). Temperatures were monitored with an Omega Model OM272 temperature recorder using chromel-alumel thermocouples (Omega Engineering, Inc., Stamford, CT) placed in the geometric center of each roast through a Permatex High Silicone RTV gasket (Loctite Corp., Cleveland, OH) on the exterior of the bag. Roasts were cooled in a blast freezer (ÿ20 C) for up to 6 h and transferred to a cooler (4 C) for 12 h or until an internal temperature of 42 C was reached. Cooking juices then were drained and roasts were vacuum-packaged in B540 bags (Cryovac Division, WR Grace and Co., Duncan, SC) and randomly assigned to storage temperatures of either 0, 4, 10 or 16 C and storage times of 1, 7, 14 or 21 days at each storage temperature. Those assigned to 0 day storage were sampled after removal from the cook-in-bags. Cook yield was calculated by dividing the ®nal cooked weight of each quartered top round by the raw weight and multiplying by 100. 2.2. Microbiological evaluation Samples were obtained by aseptically opening vacuum-packaged bags with a sterile scalpel and excising two 10-cm2 surface (2 mm thick) sections using a sterile scalpel and forceps. Samples were combined in a sterile stomacher bag containing 100 ml of 0.1% sterile peptone solution (Difco Laboratories, Detroit, MI) and pummeled for 1 min in a Stomacher 400 (Tekmar Company, Cincinnati, OH). Serial dilutions were surface spread on prepoured and dried tryptic soy agar (TSA; Difco Laboratories, Detroit, MI) plates with a bent sterile glass rod. Plates were counted after incubation (25 C) for 48 h.
2.3. Chemical analyses Roasts were cut in half, and the middle steak (2.5 cm thick) was ground for Ph determination. The next sequential steak was used for sensory color and odor evaluation and instrumental color determination. The other half of the roast was ground, placed in Snap-Cap amber vials (Lerner Packaging Corp., Garwood, NJ) and stored at ÿ20 C for lactic acid concentration and at ÿ40 C for 43 days for the 2-thiobarbituric acid test (TBA) test. 2.3.1. 2-Thiobarbituric acid test (TBA) Two 30-g ground samples were used to determine mg malonaldehyde/kg sample using procedures described by Tarladgis, Watts, Younathan, and Dugan (1960) as modi®ed by Rhee (1978). Absorbance was measured at 530 nm using a DU-7 spectrophotometer (Beckman Instruments Inc., Fulerton, CA). 2.3.2. pH Slurries were prepared from equal volumes of sample and distilled water in 100 ml beakers. Fluted ®lter paper was forced into the slurries. After 5 min, a Ph electrode (Model PHH-1X, Omega Engineering, Inc., Stamford, CT) was immersed into the collected solution inside the ¯uted ®lter paper and values were recorded to the nearest tenth of a unit. 2.3.3. Lactic acid concentration Two 5-g samples from each ground steak from processing days 1 and 3 were used to measure l-lactic acid concentration using a test kit (Boehringer Mannheim Corp., Indianapolis, IN). NADH concentration was measured at 340 nm using a DU-7 spectrophotometer (Beckman Scienti®c Instruments Division, Irvine, CA). 2.3.4. Sensory color and odor evaluation Steaks were evaluated by a ®ve-member panel at the Texas A & M University Sensory Testing Facility. Panelists were provided with sample steaks and paint swatches to identify color and anchor points along the scale in the training sessions. An eight-point scale was developed incorporating lean color (1=dark gray; 8=dark red), lean discoloration (1=extremely severe; 8=none), and percentage of two-toned color (1=total surface two-toned color; 8=no two-toned color). Putrid, acid, sour, rancid, beefy, and other aromatics also were evaluated on a nine-point scale (0=none; 8=strong). Sixteen samples were evaluated for color and odor each day in one session. 2.3.5. Instrumental color After sensory evaluation, ®ve randomly selected 1.5cm cubes were cut from the steaks, two from the outer area, two from the middle portion and one from the
J.V. Maca et al. / Meat Science 53 (1999) 23±29
center, and allowed to bloom for 30 min. Color (L*, a* and b*) was evaluated using a JB-1201 M (A) Hunterlab Labscan Spectro Colorimeter (Hunter Associates Laboratories, Inc., Reson, VA) at a wavelength of 525 nm. 2.4. Statistical analysis Data were analyzed by ANOVA using the PROC MIXED procedure of SAS (1994). The design of the experiment was a 444 factorial arrangement in four blocks (processing days) and analyzed as a Randomized Complete Block Design. Sensory data was analyzed as a split plot with panelist as a random eect. NaL level (0, 2, 3 and 4%), storage temperature (0, 4, 10 and 16 C) and storage time (1, 7, 14 and 21 days) were the main eects for all data. Interactions between the main eects also were tested. Signi®cance was established at p <0.05 for ANOVA and mean separation using Tukey's Studentized Range test. 3. Results and discussion 3.1. Cook yields It has been hypothesized that the lactate ion binds to water easily, resulting in higher cook yields (Evans, 1992). Cook yields were lowest for the control roasts and increased in roasts containing up to 3% NaL
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and were not aected by storage time or temperature (Table 1). Papadopoulos et al. (1991b) and Pagach (1992) also found increases in cook yield with NaL addition. 3.2. Microbiological populations The interactions between days of storage and sodium lactate level and between storage temperature and sodium lactate level were signi®cant (p <0.05). APC did not dier among treatments with 1 day storage (Fig. 1) and roasts with 4% NaL had consistently lower APCs than controls through 21 days storage. Addition of 4% NaL also slowed bacterial growth at ``abuse'' temperatures of 16 C (Fig. 2). It was interesting that APCs tended to be lower for roasts with 0, 2 or 3% sodium lactate stored at 4 C when compared to roasts with the same sodium lactate level stored at 0 C. It should be noted that while these dierences were numerically different, APCs did not dier based on Tukey's mean separation technique. This indicates that variation associated with sampling and enumeration of APCs most likely attributed to the numeric eect. NaL may provide a potential protective action for pre-cooked roasts when held at elevated temperatures or when stored for up to 21 days since it slowed microbial growth. Cooked beef roasts injected with 2 to 4% NaL have been reported to exhibit decreased bacterial proliferation when stored at abuse temperatures of up to 25 C (Miller & Acu, 1994; Stillmunkes, Prabhu,
Table 1 Sodium lactate (NaL) level and storage time eects on cooked beef top rounds (least squared means) Hunter color L*
a*
b*
Lactic acid (%)
Cook yield (%)
Sensory color± discolorationa
Sensory odor±acidb
** 50.29ac 47.11b 45.80c 43.90d
** 6.63b 7.89a 7.94a 8.14a
** 10.89a 10.55b 10.10c 9.85c
** 1.85b 2.64b 3.78a 4.69a
** 84.85c 95.87b 98.93a 97.56ab
5.46a 5.41a 5.26a 5.34a
0.91a 0.80a 0.74a 0.80a
* 46.38a 46.25a 47.35a 47.13a
** 7.42b 8.20a 7.88a 7.11b
** 10.54a 10.13b 10.45a 10.28ab
3.42a 3.40a 3.45a 2.69a
93.51a 95.07a 94.00a 94.63a
** 5.85a 5.54b 4.95c 5.13c
** 1.10a 1.00a 0.84a 0.32b
0.94
0.82
0.65
1.67
0.99
1.31
1.98
NaL level (%) 0 2 3 4 Storage time 1 7 14 21 RSDd a b c d *
1=extremely severe; 8=none. 0=none; 8=strong. Means within a column and main eect with similar letters are not dierent (p>0.05). Residual Standard Deviation. p<0.05, **p<0.01.
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J.V. Maca et al. / Meat Science 53 (1999) 23±29
Fig. 1. Total aerobic plate count (log10 CFU/g) for roast beef with dierences due to length of storage and sodium lactate. a±t Means across storage temperatures and storage days followed by dierent superscripts are dierent (p<0.05).
Sebranek, & Mollins, 1993; Unda, Mollins, & Walker, 1991). Maas et al. (1989) also found delayed toxin production by Clostridium botulinum in cook-in-bag turkey products treated with 3.5% NaL. It has been theorized that NaL lengthens the lag phase and ultimately decreases the maximum growth rate of microorganisms (Woolthuis & Smulders, 1985), but the speci®c mode of action is unknown. Our results indicated that NaL levels are inversely related to microbial growth when used at levels of up to 4%. 3.3. Chemical analyses 3.3.1. 2-Thiobarbituric acid In general, TBA values tended to decrease as NaL levels increased (Figs. 3 and 4). Additionally, TBA
Fig. 2. Total aerobic plate count (log10 CFU/g) for roast beef with dierences due to storage temperature and sodium lactate. a±t Means across storage temperatures and storage days followed by dierent superscripts are dierent (p<0.05).
values were unaected by storage time or temperature when NaL was added at any level, while oxidation of control roasts tended to increase with storage time. This agrees with McVann and Nnanna (1991) who found a decrease in TBA values with the addition of NaL at levels of 1 and 2% in raw beef and pork. Values also are similar to those reported by Stillmunkes et al. (1993) for beef roasts containing up to 3.5% NaL. St. Angelo et al. (1987) reported values of 3.75 and 14.71 mg of malonaldehyde per kg meat for cooked beef and beef with warmed over ¯avor (WOF), respectively. TBA values in our study were lower than would be expected for freshly cooked beef. However, Papadopoulos et al. (1991b) also reported lower values than were expected for up to 84 days storage in roasts containing 0 and 3% NaL.
J.V. Maca et al. / Meat Science 53 (1999) 23±29
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Fig. 5. Ph dierences in roast beef due to length of storage. a±d Means across storage days followed by dierent superscripts are dierent (p<0.05).
Fig. 3. TBA values in roast beef with dierences due to length of storage. a±d Means across storage days followed by dierent superscripts are dierent (p<0.05).
reported by Miller and Acu (1994). Rounds containing 0% NaL had the lowest level of lactic acid, with levels being slightly higher than those normally associated with fresh beef muscle of 9 mg/g (Lawrie, 1979). However, pooling eects of NaL level on % lactic acid across storage temperatures may have in¯uenced these data and the increased level was probably due to lactic acid produced by microorganisms. Papadopoulos et al. (1991b) showed that the predominant micro¯ora was Lactobacillus spp. which produce l-lactate along with other organic acids. 3.4. Color and odor
Fig. 4. TBA values in roast beef with dierences due to storage temperature. a±c Means across storage temperatures followed by dierent superscripts are dierent (p<0.05).
3.3.2. pH With storage of 7 days or longer, Ph was higher in roasts containing 3 or 4% NaL (Fig. 5) than control roasts and was not aected by storage temperature. Sodium ion concentration may have played a role in the increased pH (Childers, Terrell, Craig, Kayfus, & Smith, 1982; Terrell, 1983). Additionally, increased lactic acid production due to microbial growth in control roasts may have contributed to the pH decline that was not as pronounced when increased levels of NaL were present. NaL has been shown to stabilize pH (Maca, Miller, Maca, & Acu, 1997; Papadopoulos 1991b). Our data also showed that pH change with storage was minimized by addition of 3 or 4% NaL. 3.3.3. Lactic acid concentration Lactic acid concentration increased as NaL level increased (Table 1), which is consistent with data
3.4.1. Instrumental color Eects of NaL and storage time are presented in Table 1. Hunter color values were not aected by storage temperature. Papadopoulos et al. (1991c) also reported that increased NaL level decreased L* and b* values and increased a* values. Our results indicated that NaL had a protective eect and acted as a color stabilizer since roasts with NaL were darker and redder than controls and storage time and temperature did not aect color. This may be due to a pH eect on the myoglobin conversion to metmyoglobin in the cooked product. However, the exact mechanism by which NaL aects color is still unknown and future research should be conducted to better understand NaL's mechanism in reducing color changes. 3.4.2. Sensory color Lean color was evaluated because it is the ®rst factor examined for acceptability by consumers. Roasts with 3 or 4% NaL were redder than controls with 14 days storage or longer (Fig. 6), while storage temperature had no eect on lean color. Lean discoloration increased between 1 and 14 days of storage (Table 1). Lean discoloration evaluated the gray intensity changes identi®ed with increased storage times and storage temperatures. For example, at 1 days storage,
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J.V. Maca et al. / Meat Science 53 (1999) 23±29
Fig. 6. Lean color score dierences in roast beef due to length of storage. a±c Means across storage days followed by dierent superscripts are dierent (p<0.05).
roasts varied in color from light gray to grayish-purple. With increased storage time, storage temperature, and amount of NaL injected into each roast, the color of the roasts changed from its initial gray color to either green or light pink similar to Pepto-Bismol1 (Procter and Gamble, Cincinnati, OH). This pink color was distinctly dierent from the desirable pinkish color associated with recently cooked roast beef. Storage of 7 or 14 days tended to increase the % twotoned color of the roast beef slices (Table 2). In general, as storage time increased, the amount of surface gray increased across treatments. This con®rms results reported by Papadopoulos et al. (1991c) who found that increasing NaL beyond 1% did not aect surface gray color signi®cantly. 3.4.3. Sensory odor Putrid is an odor associated with microbial growth of Pseudomonas spp. and subsequent deterioration of the product. Papadopoulos et al. (1991b), found Pseudomonas spp. was a large percentage of the micro¯ora found on roasts containing 1 to 3% NaL. This attribute was identi®ed and evaluated because, at very low levels, putrid can be detected by the average consumer and is considered undesirable or oensive. Putrid aromatic increased from 0.19 on day 1 to 0.26 on day 21 (RSD= 1.20; data not presented). Within NaL level, putrid odor Table 2 Two-toned color scoresa by sodium lactate level and storage time (least squared means)b Days of storage Treatmentc
1
7
14
21
0% NaL 2% NaL 3% NaL 4% NaL
5.86a 5.81a 5.16a 5.04a
4.85ab 5.14a 5.49a 5.29a
4.18b 4.93ab 5.15a 5.45a
4.70b 4.73ab 4.63b 4.74ab
a
1=total surface two-toned color; 8=no two-tone color. RSD=1.47. c NaL=sodium lactate. d Means within a column and rows with similar letters are not different (p>0.005). b
in only control roasts was aected by storage temperature (data not presented), where the odor increased with increased storage temperature (range 0.00±0.91, RSD= 1.20). Putrid odor did not change signi®cantly with increased storage temperature in roasts treated with NaL. This suggests that NaL may be useful in controlling this undesirable aromatic, even at abusive storage temperatures. Lactic acid bacteria that predominate in meat stored under anaerobic conditions produce organic acids which create an acid aromatic. The acid aromatic did not dier by NaL level or storage temperature; however, acid aromatic decreased with storage (Table 1). As the strong putrid aromatic increased with storage time, it most likely masked the less detectable acid component. Meilgaard, Civille, and Carr (1991) described this as the suppression physiological factor, where the presence of one substance decreases the perceived intensity of a mixture of two or more substances. The putrid aromatic was a very strong, dominating aromatic, so as it increased, panelists had diculty detecting other aromatics. Sour aromatic is commonly associated with spoilage by Lactobacillus spp. and is an indication of product deterioration. Papadopoulos et al. (1991b) reported that in cooked beef Lactobacillus spp. increased as storage time increased and became predominant after 84 days of storage. There were dierences between treatments for sour aromatic only at 10 C, where controls smelled more sour than those treated with 4% NaL. It would be expected that roasts stored at 16 C would have similar or higher levels of the sour aromatic, though these trends were not observed in our study. Rancid aromatic is an odor associated with lipid oxidation. A 3-way interaction between NaL level and storage time and temperature was found. Since it is dif®cult to statistically explain dierences in data from a 3way interaction, the 2-way interactions will be discussed (data not presented). Rancid scores ranged from 0.00 to 0.65 (RSD=0.83) for the interaction between NaL level and storage time and from 0.00 to 0.72 for the interaction between storage time and storage temperature. Rancid odor tended to increase with storage time for both interactions and control roasts tended to have more rancid odor than treated roasts with storage of 7 days or longer. Beefy is a positive aromatic associated with the characteristic lean beef aroma and ¯avor. Beefy odor decreased with storage time from 5.50 to 4.86 (RSD=1.45). In treated roasts, beefy odor did not change with increased storage temperature and was higher than controls when stored at 16 C (Fig. 7). Previous research also has shown that cooked beefy/brothy ¯avor increased with the addition of NaL (Evans 1993; Pagach, 1992; Papadopoulos et al., 1991b). However, increasing NaL levels above 2% did not positively increase the beefy aromatic. It can be concluded that the
J.V. Maca et al. / Meat Science 53 (1999) 23±29
Fig. 7. Beefy odor score dierences in roast beef due to storage temperature. a,b Means across storage temperatures followed by dierent superscripts are dierent (p<0.05).
addition of NaL aids in maintaining the beefy aromatic when roasts are stored at elevated temperatures. Hydroperoxides, the initial products of autooxidation, form aldehydes, ketones, alcohols and lactones (Sato & Hegarty, 1971). These short-chain carbon compounds impart o-odors in meat (Fioriti, Kanuk, & Sims, 1974; Gray, 1978). Brewer, McKeith, Martin, Dallmier, and Meyer (1991) reported the addition of 2 or 3% NaL to fresh pork sausage delayed the development of sour- and o-¯avors, which are directly related to o-odors. Our sensory odor data suggests that increasing NaL levels also decreased o-odors in cooked beef. 4. Conclusions NaL has potential value in the meat industry as a bacteriostatic agent and antioxidant to increase shelflife and product quality of cooked beef systems even with temperature abuse storage conditions. Based on the lack of dierence between 3 and 4% NaL, it can be concluded that 3% NaL is the optimum level for use as a bacteriostatic agent, antioxidant and color stabilizer for cooked beef systems using the same processing methods and storage conditions. References Anon (1988). A meaty problem solved. Food Processing, 49, 9. Brewer, S. M., McKeith, F., Martin, S. E., Dallmier, A. W., & Meyer, J. NaL eects on shelf-life, sensory, and physical characteristics of fresh pork sausage. Journal of Food Science, 56, (1991). 1176±1178 Childers, A. B., Terrell, R. N., Craig, T. M., Kayfus, T. J., & Smith, G. C. (1982). Eect of sodium chloride concentration, water activity, fermentation method, and drying time on the viability of Trichinella spiralis in Genoa Salami. Journal of Food Protection, 45, 816±819, 823. Evans, L. L. (1992). l-NaL in cooked beef top rounds: Diering levels of incorporation and cookery. College Station, TX: Texas A & M University.
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Fioriti, B. A., Kanuk, M. J., & Sims, R. J. (1974). Chemical and organoleptic properties of oxidized fats. Journal of the American Oil Chemist Society, 51, 219±223. Gray, J. I. (1978). Measurement of lipid oxidation: A review. J. Am. Oil Chem. Soc., 55, 539±546. Lawrie, R. A. (1979). Chemical and biochemical constitution of muscle. In Meat science. (p. 76). Elmsford, NY: Pergamon Press. Litwak, D. (1989). Seventh annual operations report: service deli review. Supermarket Business, 44, 1A±4A. Maas, M. R., Glass, K. A., & Doyle, M. P. (1989). NaL delays toxin production by Clostridium botulinum in cook-in-bag turkey products. Applied Environmental Microbiology, 55, 2226±2229. Maca, J. V., Miller, R. K., Maca, J. D., & Acu, G. R. (1997). Microbiological, sensory and chemical characteristics of vacuumpackaged cooked beef top rounds treated with sodium lactate and sodium propionate. Journal of Food Science, 62, 586±590, 596. McVann, K. B., & Nnanna, I. B. (1991). Eects of NaL on lipid oxidation and heme pigment in raw pork. Poster No. 71, presented at 51st Annual Meeting of Inst. of Food Technologists, Dallas, TX, 15 June. Meilgaard, M., Civille, G. V., & Carr, B. T. (1987). Sensory evaluation techniques (2nd ed., p.38). Boca Raton, FL: CRC Press. Miller, R. K., & Acu, G. R. (1994). Sodium lactate aects pathogens in cooked beef. Journal of Food Science, 59, 15±19. Pagach, D. A. (1992). The use of sodium and/or potassium lactate to extend shelf-life and reduce sodium levels in precooked beef systems. M. S. thesis, Texas A & M University, College Station, TX. Papadopoulos, L. S., Miller, R. K., Acu, G. R., Lucia, L. M., Vanderzant, C., & Cross, H. R. (1991a). Consumer and trained sensory comparisons of cooked beef top rounds treated with NaL. Journal of Food Science 56, 1141±1146, 1153. Papadopoulos, L. S., Miller, R. K., Acu, G. R., Vanderzant, C., & Cross, H. R. (1991b). Eect of NaL on microbial and chemical composition of cooked beef during storage. Journal of Food Science, 56, 341±347. Papadopoulos, L. S., Miller, R. K., Ringer, L. J., & Cross, H. R. (1991c). NaL eect on sensory characteristics, cooked meat color and chemical composition. Journal of Food Science 56, 621±626, 635. Rhee, K. S. (1978). Minimization of further lipid peroxidation in the distillation of 2-thiobarabituric acid test of ®sh and meat. Journal of Food Science 48, 1776±78, 81. SAS (1994). SAS/STAT software: Changes and Enhancements. Cary, NC: SAS Institute. Sato, K., & Hegarty, G. R. (1971). Warmed-over ¯avor in cooked meats. Journal of Food Science, 36, 1098±1192. St. Angelo, A. J., Vercellotti, J. R., Legendre, M. G., Vinnett, C. H., Kuan, J. W., James Jr, C., & Dupuy, H. P. (1987). Chemical and instrumental analyses of warmed-over ¯avor in beef. Journal of Food Science, 52, 1163±1168. Stilllmunkes, A. A., Prabhu, G. A., Sebranek, J. G., & Molins, R. A. (1993). Microbiological safety of cooked beef roasts treated with lactate, monolaurin or gluconate. Journal of Food Science, 58, 953± 958. Tarladgis, B. G., Watts, B. M., Younathan, M. T., & Dugan Jr, L. (1960). A distilliation method for the quantitative determination of malonaldehyde in rancid foods. Journal of the American Oil Chemist Society, 37, 44±48. Terrell, R. N. (1983). Reducing the sodium content of processed meats. Food Technol., 37, 66±71. Unda, J. R., Molins, R. A., & Walker, H. W. (1991). Clostridium sporogenes and Listeria monocytogenes: survival and inhibition in microwave-ready beef roasts containing selected antimicrobials. Journal of Food Science, 56, 198±205, 219. Woolthuis, C. H. J., & Smulders, F. J. M. (1985). Microbial decontamination of calf carcasses by lactic acid sprays. Journal of Food Protection, 48, 832±837.
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Sodium lactate and storage temperature eects on shelf life of vacuum packaged beef top rounds J.V. Maca a, R.K. Miller b,*, M.E. Bigner c, L.M. Lucia b, G.R. Acu b a
b
Nabisco, Inc., Morristown, NJ, USA Texas A&M University, Department of Animal Science, College Station, TX 77843-2471, USA c USDA, ARS, Beltsville, MD, USA Received 19 February 1999; accepted 27 February 1999
Abstract Cooked, vacuum-packaged beef top rounds containing up to 4% sodium lactate (NaL) in the ®nal product were stored at 0, 4, 10 or 16 C for 1, 7, 14 or 21 days. Aerobic plate counts (APCs) were lower for roasts containing 3 or 4% NaL and stored at 10 C for 7 days. At higher temperatures and longer storage times, only those treated with 4% NaL were lower than controls. Lipid oxidation, Hunter L* and b* values decreased and Hunter a* values, cooked yields and Ph increased with NaL addition. Beefy odor decreased with storage but was higher in roasts containing NaL. Roasts with added NaL had lower rancid odor scores. # 1999 Elsevier Science Ltd. All rights reserved. Keywords: Beef; Sodium lactate; Storage; Shelf-life
1. Introduction The economic and quality advantages achieved in recent years in the value-added meat industry, such as higher cooking yields, improved ¯avor, increased palatability, increased shelf-life and decreased microbial growth, have led to more marketable meat products to meet consumer demands for convenient foods. As a result, the delicatessen section was the fastest growing segment of the supermarket (Litwak, 1989); however, recontamination of precooked meat items provide a potential food safety risk, because meat products sold in a delicatessen are often sliced, served and consumed without additional heating. Also, the shelf-life of uncured deli beef is usually less than 45 days. Nitrites have been used extensively to limit microbiological growth and extend shelf-life, however, consumer concerns about nitrosamine formation have increased. Alternative ingredients to maintain shelflife in precooked beef products that are positively perceived by consumers are needed. Sodium lactate (NaL), the sodium salt of lactic acid, has a bacteriostatic eect in uncured, refrigerated precooked roast beef (Anonymous, 1988; Evans, 1992; * Corresponding author. Tel.: +1-409-845-3935; fax: +1-409-8459454. E-mail address: [email protected] (R.K. Miller)
Pagach, 1992; Papadopoulos et al., 1991a; Papadopoulos, Miller, Acu, Vanderzant & Cross, 1991b; Papadopoulos, Miller, Ringer & Cross, 1991c), as well as having an inhibitory eect on growth of Streptococcus faecalis, Staphylococcus aureus and Salmonella typhimurium in other products (Maas, Glass & Doyle, 1989). Control of microbial growth with bacteriostatic ingredients may have adverse eects on a product's color, odor, ¯avor, appearance or palatability, which can be quality indicators to consumers. It is important, therefore, to understand what eect NaL has on color and color deterioration in cooked beef products and if this deterioration is proportionate to microbiological spoilage. Since it is still unknown to what extent NaL is eective in controlling microbial spoilage at various storage temperatures, the objective of this study was to determine the eect of NaL in cooked beef top rounds on microbiological, chemical, color and olfactory sensory attributes and lipid oxidation. 2. Materials and methods 2.1. Processing USDA Select beef top rounds (n=64) were obtained from a commercial beef processor from the same
0309-1740/99/$ - see front matter # 1999 Elsevier Science Ltd. All rights reserved. PII: S0309-1740(99)00032-7
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processing day and shift to assure consistent age. Top rounds were trimmed to 0 cm external fat and the abductor muscle was removed. Quartered top rounds were injected to 20% of the original (green) weight with an Inject Star B125 (Inject Star Systems, Globus Laboratories, Inc., South Hackensack, NJ) to contain 0.5% sodium chloride, 0.3% sodium tripolyphosphate and either 0, 2, 3 or 4% NaL in the ®nal product (Purac, Inc., Arlington Heights, IL). As NaL is sold on a 60% dry weight basis, 0, 3.33, 5, and 6.6% of the wet based product was added to the ®nal product. Four quartered top rounds from each treatment were processed on each of 4 days, vacuum-tumbled 2 h in a Vortron1 vacuum tumbler (Type 021-333 56-7, Parker CPI, Beloit, WI). Additional brine was added before tumbling, as needed, to insure a 20% total pickup weight. After tumbling, top rounds were submerged in their respective brine solutions and allowed to equilibrate for 36 h at 4 C and retumbled 15 min prior to cooking in vacuum-sealed CN530 cook-in-bags (Cryovac Division, WR Grace and Company, Duncan, SC). Top rounds then were cooked in an Alkar two-truck food processing oven (Model PP024519, DEC International, Lodi, WI). Temperatures were monitored with an Omega Model OM272 temperature recorder using chromel-alumel thermocouples (Omega Engineering, Inc., Stamford, CT) placed in the geometric center of each roast through a Permatex High Silicone RTV gasket (Loctite Corp., Cleveland, OH) on the exterior of the bag. Roasts were cooled in a blast freezer (ÿ20 C) for up to 6 h and transferred to a cooler (4 C) for 12 h or until an internal temperature of 42 C was reached. Cooking juices then were drained and roasts were vacuum-packaged in B540 bags (Cryovac Division, WR Grace and Co., Duncan, SC) and randomly assigned to storage temperatures of either 0, 4, 10 or 16 C and storage times of 1, 7, 14 or 21 days at each storage temperature. Those assigned to 0 day storage were sampled after removal from the cook-in-bags. Cook yield was calculated by dividing the ®nal cooked weight of each quartered top round by the raw weight and multiplying by 100. 2.2. Microbiological evaluation Samples were obtained by aseptically opening vacuum-packaged bags with a sterile scalpel and excising two 10-cm2 surface (2 mm thick) sections using a sterile scalpel and forceps. Samples were combined in a sterile stomacher bag containing 100 ml of 0.1% sterile peptone solution (Difco Laboratories, Detroit, MI) and pummeled for 1 min in a Stomacher 400 (Tekmar Company, Cincinnati, OH). Serial dilutions were surface spread on prepoured and dried tryptic soy agar (TSA; Difco Laboratories, Detroit, MI) plates with a bent sterile glass rod. Plates were counted after incubation (25 C) for 48 h.
2.3. Chemical analyses Roasts were cut in half, and the middle steak (2.5 cm thick) was ground for Ph determination. The next sequential steak was used for sensory color and odor evaluation and instrumental color determination. The other half of the roast was ground, placed in Snap-Cap amber vials (Lerner Packaging Corp., Garwood, NJ) and stored at ÿ20 C for lactic acid concentration and at ÿ40 C for 43 days for the 2-thiobarbituric acid test (TBA) test. 2.3.1. 2-Thiobarbituric acid test (TBA) Two 30-g ground samples were used to determine mg malonaldehyde/kg sample using procedures described by Tarladgis, Watts, Younathan, and Dugan (1960) as modi®ed by Rhee (1978). Absorbance was measured at 530 nm using a DU-7 spectrophotometer (Beckman Instruments Inc., Fulerton, CA). 2.3.2. pH Slurries were prepared from equal volumes of sample and distilled water in 100 ml beakers. Fluted ®lter paper was forced into the slurries. After 5 min, a Ph electrode (Model PHH-1X, Omega Engineering, Inc., Stamford, CT) was immersed into the collected solution inside the ¯uted ®lter paper and values were recorded to the nearest tenth of a unit. 2.3.3. Lactic acid concentration Two 5-g samples from each ground steak from processing days 1 and 3 were used to measure l-lactic acid concentration using a test kit (Boehringer Mannheim Corp., Indianapolis, IN). NADH concentration was measured at 340 nm using a DU-7 spectrophotometer (Beckman Scienti®c Instruments Division, Irvine, CA). 2.3.4. Sensory color and odor evaluation Steaks were evaluated by a ®ve-member panel at the Texas A & M University Sensory Testing Facility. Panelists were provided with sample steaks and paint swatches to identify color and anchor points along the scale in the training sessions. An eight-point scale was developed incorporating lean color (1=dark gray; 8=dark red), lean discoloration (1=extremely severe; 8=none), and percentage of two-toned color (1=total surface two-toned color; 8=no two-toned color). Putrid, acid, sour, rancid, beefy, and other aromatics also were evaluated on a nine-point scale (0=none; 8=strong). Sixteen samples were evaluated for color and odor each day in one session. 2.3.5. Instrumental color After sensory evaluation, ®ve randomly selected 1.5cm cubes were cut from the steaks, two from the outer area, two from the middle portion and one from the
J.V. Maca et al. / Meat Science 53 (1999) 23±29
center, and allowed to bloom for 30 min. Color (L*, a* and b*) was evaluated using a JB-1201 M (A) Hunterlab Labscan Spectro Colorimeter (Hunter Associates Laboratories, Inc., Reson, VA) at a wavelength of 525 nm. 2.4. Statistical analysis Data were analyzed by ANOVA using the PROC MIXED procedure of SAS (1994). The design of the experiment was a 444 factorial arrangement in four blocks (processing days) and analyzed as a Randomized Complete Block Design. Sensory data was analyzed as a split plot with panelist as a random eect. NaL level (0, 2, 3 and 4%), storage temperature (0, 4, 10 and 16 C) and storage time (1, 7, 14 and 21 days) were the main eects for all data. Interactions between the main eects also were tested. Signi®cance was established at p <0.05 for ANOVA and mean separation using Tukey's Studentized Range test. 3. Results and discussion 3.1. Cook yields It has been hypothesized that the lactate ion binds to water easily, resulting in higher cook yields (Evans, 1992). Cook yields were lowest for the control roasts and increased in roasts containing up to 3% NaL
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and were not aected by storage time or temperature (Table 1). Papadopoulos et al. (1991b) and Pagach (1992) also found increases in cook yield with NaL addition. 3.2. Microbiological populations The interactions between days of storage and sodium lactate level and between storage temperature and sodium lactate level were signi®cant (p <0.05). APC did not dier among treatments with 1 day storage (Fig. 1) and roasts with 4% NaL had consistently lower APCs than controls through 21 days storage. Addition of 4% NaL also slowed bacterial growth at ``abuse'' temperatures of 16 C (Fig. 2). It was interesting that APCs tended to be lower for roasts with 0, 2 or 3% sodium lactate stored at 4 C when compared to roasts with the same sodium lactate level stored at 0 C. It should be noted that while these dierences were numerically different, APCs did not dier based on Tukey's mean separation technique. This indicates that variation associated with sampling and enumeration of APCs most likely attributed to the numeric eect. NaL may provide a potential protective action for pre-cooked roasts when held at elevated temperatures or when stored for up to 21 days since it slowed microbial growth. Cooked beef roasts injected with 2 to 4% NaL have been reported to exhibit decreased bacterial proliferation when stored at abuse temperatures of up to 25 C (Miller & Acu, 1994; Stillmunkes, Prabhu,
Table 1 Sodium lactate (NaL) level and storage time eects on cooked beef top rounds (least squared means) Hunter color L*
a*
b*
Lactic acid (%)
Cook yield (%)
Sensory color± discolorationa
Sensory odor±acidb
** 50.29ac 47.11b 45.80c 43.90d
** 6.63b 7.89a 7.94a 8.14a
** 10.89a 10.55b 10.10c 9.85c
** 1.85b 2.64b 3.78a 4.69a
** 84.85c 95.87b 98.93a 97.56ab
5.46a 5.41a 5.26a 5.34a
0.91a 0.80a 0.74a 0.80a
* 46.38a 46.25a 47.35a 47.13a
** 7.42b 8.20a 7.88a 7.11b
** 10.54a 10.13b 10.45a 10.28ab
3.42a 3.40a 3.45a 2.69a
93.51a 95.07a 94.00a 94.63a
** 5.85a 5.54b 4.95c 5.13c
** 1.10a 1.00a 0.84a 0.32b
0.94
0.82
0.65
1.67
0.99
1.31
1.98
NaL level (%) 0 2 3 4 Storage time 1 7 14 21 RSDd a b c d *
1=extremely severe; 8=none. 0=none; 8=strong. Means within a column and main eect with similar letters are not dierent (p>0.05). Residual Standard Deviation. p<0.05, **p<0.01.
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Fig. 1. Total aerobic plate count (log10 CFU/g) for roast beef with dierences due to length of storage and sodium lactate. a±t Means across storage temperatures and storage days followed by dierent superscripts are dierent (p<0.05).
Sebranek, & Mollins, 1993; Unda, Mollins, & Walker, 1991). Maas et al. (1989) also found delayed toxin production by Clostridium botulinum in cook-in-bag turkey products treated with 3.5% NaL. It has been theorized that NaL lengthens the lag phase and ultimately decreases the maximum growth rate of microorganisms (Woolthuis & Smulders, 1985), but the speci®c mode of action is unknown. Our results indicated that NaL levels are inversely related to microbial growth when used at levels of up to 4%. 3.3. Chemical analyses 3.3.1. 2-Thiobarbituric acid In general, TBA values tended to decrease as NaL levels increased (Figs. 3 and 4). Additionally, TBA
Fig. 2. Total aerobic plate count (log10 CFU/g) for roast beef with dierences due to storage temperature and sodium lactate. a±t Means across storage temperatures and storage days followed by dierent superscripts are dierent (p<0.05).
values were unaected by storage time or temperature when NaL was added at any level, while oxidation of control roasts tended to increase with storage time. This agrees with McVann and Nnanna (1991) who found a decrease in TBA values with the addition of NaL at levels of 1 and 2% in raw beef and pork. Values also are similar to those reported by Stillmunkes et al. (1993) for beef roasts containing up to 3.5% NaL. St. Angelo et al. (1987) reported values of 3.75 and 14.71 mg of malonaldehyde per kg meat for cooked beef and beef with warmed over ¯avor (WOF), respectively. TBA values in our study were lower than would be expected for freshly cooked beef. However, Papadopoulos et al. (1991b) also reported lower values than were expected for up to 84 days storage in roasts containing 0 and 3% NaL.
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Fig. 5. Ph dierences in roast beef due to length of storage. a±d Means across storage days followed by dierent superscripts are dierent (p<0.05).
Fig. 3. TBA values in roast beef with dierences due to length of storage. a±d Means across storage days followed by dierent superscripts are dierent (p<0.05).
reported by Miller and Acu (1994). Rounds containing 0% NaL had the lowest level of lactic acid, with levels being slightly higher than those normally associated with fresh beef muscle of 9 mg/g (Lawrie, 1979). However, pooling eects of NaL level on % lactic acid across storage temperatures may have in¯uenced these data and the increased level was probably due to lactic acid produced by microorganisms. Papadopoulos et al. (1991b) showed that the predominant micro¯ora was Lactobacillus spp. which produce l-lactate along with other organic acids. 3.4. Color and odor
Fig. 4. TBA values in roast beef with dierences due to storage temperature. a±c Means across storage temperatures followed by dierent superscripts are dierent (p<0.05).
3.3.2. pH With storage of 7 days or longer, Ph was higher in roasts containing 3 or 4% NaL (Fig. 5) than control roasts and was not aected by storage temperature. Sodium ion concentration may have played a role in the increased pH (Childers, Terrell, Craig, Kayfus, & Smith, 1982; Terrell, 1983). Additionally, increased lactic acid production due to microbial growth in control roasts may have contributed to the pH decline that was not as pronounced when increased levels of NaL were present. NaL has been shown to stabilize pH (Maca, Miller, Maca, & Acu, 1997; Papadopoulos 1991b). Our data also showed that pH change with storage was minimized by addition of 3 or 4% NaL. 3.3.3. Lactic acid concentration Lactic acid concentration increased as NaL level increased (Table 1), which is consistent with data
3.4.1. Instrumental color Eects of NaL and storage time are presented in Table 1. Hunter color values were not aected by storage temperature. Papadopoulos et al. (1991c) also reported that increased NaL level decreased L* and b* values and increased a* values. Our results indicated that NaL had a protective eect and acted as a color stabilizer since roasts with NaL were darker and redder than controls and storage time and temperature did not aect color. This may be due to a pH eect on the myoglobin conversion to metmyoglobin in the cooked product. However, the exact mechanism by which NaL aects color is still unknown and future research should be conducted to better understand NaL's mechanism in reducing color changes. 3.4.2. Sensory color Lean color was evaluated because it is the ®rst factor examined for acceptability by consumers. Roasts with 3 or 4% NaL were redder than controls with 14 days storage or longer (Fig. 6), while storage temperature had no eect on lean color. Lean discoloration increased between 1 and 14 days of storage (Table 1). Lean discoloration evaluated the gray intensity changes identi®ed with increased storage times and storage temperatures. For example, at 1 days storage,
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J.V. Maca et al. / Meat Science 53 (1999) 23±29
Fig. 6. Lean color score dierences in roast beef due to length of storage. a±c Means across storage days followed by dierent superscripts are dierent (p<0.05).
roasts varied in color from light gray to grayish-purple. With increased storage time, storage temperature, and amount of NaL injected into each roast, the color of the roasts changed from its initial gray color to either green or light pink similar to Pepto-Bismol1 (Procter and Gamble, Cincinnati, OH). This pink color was distinctly dierent from the desirable pinkish color associated with recently cooked roast beef. Storage of 7 or 14 days tended to increase the % twotoned color of the roast beef slices (Table 2). In general, as storage time increased, the amount of surface gray increased across treatments. This con®rms results reported by Papadopoulos et al. (1991c) who found that increasing NaL beyond 1% did not aect surface gray color signi®cantly. 3.4.3. Sensory odor Putrid is an odor associated with microbial growth of Pseudomonas spp. and subsequent deterioration of the product. Papadopoulos et al. (1991b), found Pseudomonas spp. was a large percentage of the micro¯ora found on roasts containing 1 to 3% NaL. This attribute was identi®ed and evaluated because, at very low levels, putrid can be detected by the average consumer and is considered undesirable or oensive. Putrid aromatic increased from 0.19 on day 1 to 0.26 on day 21 (RSD= 1.20; data not presented). Within NaL level, putrid odor Table 2 Two-toned color scoresa by sodium lactate level and storage time (least squared means)b Days of storage Treatmentc
1
7
14
21
0% NaL 2% NaL 3% NaL 4% NaL
5.86a 5.81a 5.16a 5.04a
4.85ab 5.14a 5.49a 5.29a
4.18b 4.93ab 5.15a 5.45a
4.70b 4.73ab 4.63b 4.74ab
a
1=total surface two-toned color; 8=no two-tone color. RSD=1.47. c NaL=sodium lactate. d Means within a column and rows with similar letters are not different (p>0.005). b
in only control roasts was aected by storage temperature (data not presented), where the odor increased with increased storage temperature (range 0.00±0.91, RSD= 1.20). Putrid odor did not change signi®cantly with increased storage temperature in roasts treated with NaL. This suggests that NaL may be useful in controlling this undesirable aromatic, even at abusive storage temperatures. Lactic acid bacteria that predominate in meat stored under anaerobic conditions produce organic acids which create an acid aromatic. The acid aromatic did not dier by NaL level or storage temperature; however, acid aromatic decreased with storage (Table 1). As the strong putrid aromatic increased with storage time, it most likely masked the less detectable acid component. Meilgaard, Civille, and Carr (1991) described this as the suppression physiological factor, where the presence of one substance decreases the perceived intensity of a mixture of two or more substances. The putrid aromatic was a very strong, dominating aromatic, so as it increased, panelists had diculty detecting other aromatics. Sour aromatic is commonly associated with spoilage by Lactobacillus spp. and is an indication of product deterioration. Papadopoulos et al. (1991b) reported that in cooked beef Lactobacillus spp. increased as storage time increased and became predominant after 84 days of storage. There were dierences between treatments for sour aromatic only at 10 C, where controls smelled more sour than those treated with 4% NaL. It would be expected that roasts stored at 16 C would have similar or higher levels of the sour aromatic, though these trends were not observed in our study. Rancid aromatic is an odor associated with lipid oxidation. A 3-way interaction between NaL level and storage time and temperature was found. Since it is dif®cult to statistically explain dierences in data from a 3way interaction, the 2-way interactions will be discussed (data not presented). Rancid scores ranged from 0.00 to 0.65 (RSD=0.83) for the interaction between NaL level and storage time and from 0.00 to 0.72 for the interaction between storage time and storage temperature. Rancid odor tended to increase with storage time for both interactions and control roasts tended to have more rancid odor than treated roasts with storage of 7 days or longer. Beefy is a positive aromatic associated with the characteristic lean beef aroma and ¯avor. Beefy odor decreased with storage time from 5.50 to 4.86 (RSD=1.45). In treated roasts, beefy odor did not change with increased storage temperature and was higher than controls when stored at 16 C (Fig. 7). Previous research also has shown that cooked beefy/brothy ¯avor increased with the addition of NaL (Evans 1993; Pagach, 1992; Papadopoulos et al., 1991b). However, increasing NaL levels above 2% did not positively increase the beefy aromatic. It can be concluded that the
J.V. Maca et al. / Meat Science 53 (1999) 23±29
Fig. 7. Beefy odor score dierences in roast beef due to storage temperature. a,b Means across storage temperatures followed by dierent superscripts are dierent (p<0.05).
addition of NaL aids in maintaining the beefy aromatic when roasts are stored at elevated temperatures. Hydroperoxides, the initial products of autooxidation, form aldehydes, ketones, alcohols and lactones (Sato & Hegarty, 1971). These short-chain carbon compounds impart o-odors in meat (Fioriti, Kanuk, & Sims, 1974; Gray, 1978). Brewer, McKeith, Martin, Dallmier, and Meyer (1991) reported the addition of 2 or 3% NaL to fresh pork sausage delayed the development of sour- and o-¯avors, which are directly related to o-odors. Our sensory odor data suggests that increasing NaL levels also decreased o-odors in cooked beef. 4. Conclusions NaL has potential value in the meat industry as a bacteriostatic agent and antioxidant to increase shelflife and product quality of cooked beef systems even with temperature abuse storage conditions. Based on the lack of dierence between 3 and 4% NaL, it can be concluded that 3% NaL is the optimum level for use as a bacteriostatic agent, antioxidant and color stabilizer for cooked beef systems using the same processing methods and storage conditions. References Anon (1988). A meaty problem solved. Food Processing, 49, 9. Brewer, S. M., McKeith, F., Martin, S. E., Dallmier, A. W., & Meyer, J. NaL eects on shelf-life, sensory, and physical characteristics of fresh pork sausage. Journal of Food Science, 56, (1991). 1176±1178 Childers, A. B., Terrell, R. N., Craig, T. M., Kayfus, T. J., & Smith, G. C. (1982). Eect of sodium chloride concentration, water activity, fermentation method, and drying time on the viability of Trichinella spiralis in Genoa Salami. Journal of Food Protection, 45, 816±819, 823. Evans, L. L. (1992). l-NaL in cooked beef top rounds: Diering levels of incorporation and cookery. College Station, TX: Texas A & M University.
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