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PROCESSING, PRODUCTS, AND FOOD SAFETY |
Department of Poultry Science, The University of Georgia, Athens 30602-2772
1 Corresponding author: srussell{at}uga.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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0.05) reduced on all days of sampling. The average log10 reduction overall was 3.80 and 3.05 for APC and E. coli, respectively. Salmonella prevalence was reduced by an average of 30%. For carcasses that were scalded, picked, and dipped postpick using this sanitizer, APC were significantly P 0.05) reduced on all days of sampling by an average of 1.19 log10. Escherichia coli counts were reduced on all but 2 d of sampling for carcasses scalded, picked, and dipped in this sanitizer, except for d 2 and 10. Averages on these days were higher for controls, but were not significantly different. Salmonella prevalence was not consistently impacted overall. For the shelf-life study, odor scores were significantly (P 0.05) reduced for treated carcasses at d 8 through 14 of storage. The psychrotrophic plate counts were significantly (P 0.05) lower on treated carcasses at d 6 through 14 of storage. This sanitizer suppressed spoilage bacteria with a 99.99% reduction at d 10 and a 99.9% reduction at d 12 of storage. This effect could result in an extension of the shelf life of the poultry carcasses by up to 4 d.
Key Words: Salmonella • Escherichia coli • copper sulfate • scalder • shelf-life
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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Cason et al. (2000) reported that the washing action in commercial immersion scalders removes bacteria from the skin and feathers of the birds. Eventually, the bacterial levels in the scalder reach equilibrium and the number of bacteria entering the scalder is similar to those exiting the scalder. Some of the bacteria may die as a result of the high water temperature. The authors also stated that these bacteria may be a source of contamination later on as processing continues (Cason et al., 2000).
Pathogenic bacteria such as Salmonella and Campylobacter may be transferred from carcass to carcass during scalding and picking (Cason et al., 2000; Hinton et al., 2004; Mulder et al., 1978). Although this transfer may occur infrequently and involve very low numbers of bacteria, Salmonella regulations are enforced based on a carcass being positive for Salmonella. Thus, cross-contamination of only one cell of Salmonella from carcass to carcass may result in regulatory action (Cason et al., 2000). Mikolajczyk and Radkowski (2002) reported that Salmonella prevalence increased between stunning and postevisceration from 6 to 24%. These studies indicate the need for a sanitizer to be used during immersion scalding to prevent cross-contamination of pathogenic bacteria such as Salmonella and Campylobacter from carcass to carcass.
The 3 most important challenges when attempting to use a sanitizer in a scalder are the following: 1) the water is hot and most sanitizers will evolve into the air in the scald room, causing workers to become ill, 2) the water contains a very high organic load and will immediately deactivate oxidizing sanitizers such as chlorine and ozone, and 3) the exposure time is very short at 2 to 3 min. To date, no commercially available sanitizers have been employed effectively to prevent cross-contamination during scalding. Okrend et al. (1986) observed that acetic acid used at a level of 0.2 to 1.2% resulted in reductions of Salmonella. However, use of organic acids at high levels has been reported to cause off-flavors in poultry carcasses.
The purpose of these studies was to determine the efficacy of an acidic, copper sulfate-based commercial sanitizer for eliminating indicator, pathogenic, and spoilage bacteria from the surfaces of broiler chicken carcasses in a model system, during immersion scalding with or without a postpick dip, and to determine the shelf-life of carcasses exposed to this sanitizer when scalded, immersion chilled, and postchill dipped.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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Study I was conducted to evaluate the effect of an acidic, copper sulfate-based commercial sanitizer on pathogenic, indicator, and spoilage bacteria associated with broiler chicken carcasses in a model scald water system. Salmonella Typhimurium (ST), Escherichia coli (EC), Listeria monocytogenes (LM), and Staphylococcus aureus (SA) were obtained from the USDA-Agricultural Research Service’s Poultry Microbiological Safety Unit laboratory. These pathogenic and indicator bacterial isolates were originally collected from commercial broiler carcasses. Each isolate was assayed for gram reaction, cytochrome oxidase activity, and production of catalase and was identified using the Vitek (bioMérieux Vitek Inc., Hazelwood, MO), Biolog (Biolog Inc., Hayward, CA), or Micro-ID (Organon Teknika Corporation, Durham, NC) rapid identification methods.
Pseudomonas fluorescens (PF) and Shewanella putrefaciens (SP) spoilage bacterial isolates were obtained by collecting broiler carcasses from processing plants in Georgia, Arkansas, California, and North Carolina. These carcasses were individually bagged in sterile polyethylene bags (3,000 mL O2 at 22.8°C/m2/24 h at 1 atm) and held on ice until arrival at the laboratory. Carcasses were allowed to spoil under controlled conditions at 3 + 0.5°C for 15 d. After spoilage, the carcasses were rinsed with 100 mL of sterile deionized water. The rinse fluid was diluted to 10–6, 10–7, and 10–8 using a sterile 1% solution of Bactopeptone (BBL, Difco Laboratories, Detroit, MI), and 1 mL of the diluent was spread onto duplicate plate count agar (PCA, Difco) plates. Plates were incubated at 25°C for 48 h. Each isolate was assayed for gram reaction, cytochrome oxidase activity, and production of catalase and was identified using one of the same rapid identification methods used to identify the pathogenic and indicator bacterial isolates discussed above. The PF and SP isolates from these spoiled carcasses were obtained and used in this study.
Scalder water was collected from a commercial processing facility after at least 60,000 birds had been processed in the scalder and was autoclaved to eliminate background microflora. The water was then compared with scald water that had not been autoclaved by adding chlorine to the water and measuring the depletion due to reaction with the organic material in the water. Both autoclaved and unautoclaved scald water had the same characteristics with regard to depletion of chlorine. Thus, autoclaved scald water was deemed acceptable as a scald water substitute to provide background organic material for the purposes of this experiment.
To determine the effect of this sanitizer on each isolate or on indicator populations of bacteria, EC, LM, ST, and SA were individually placed into brain heart infusion broth (Difco) at 35°C, and PF and SP were individually placed into brain heart infusion broth at 25°C for 24 h. One 10-µL loopful of each of these actively growing cultures was placed into 10 mL of sterile scalder water as controls or sterile scalder water containing a sanitizer containing ammonium sulfate, sulfuric acid, and copper sulfate (commercially known as Tasker Blue) at a concentration of 38 mg/L with 0.8 mg/L of copper in test tubes, with a pH of 2.0, and allowed to remain for 2 min in a water bath at 54°C to mimic commercial scalder time and temperature.
After the exposure period, 1 mL of the suspension from each individual inoculated tube of scalder water was neutralized using neutralizing buffer (Edge Biological item number EB400NB) and spread plated onto aerobic plate count agar (APC, Difco). The pathogens and EC were incubated at 35°C for 48 h. Spoilage bacteria were incubated at 7°C for 10 d. The experimental design was a 3 x 3 x 6 x 2 of experimental unit, repetition, bacterial species, and treatment (control vs. treated).
The data were analyzed by the Statistical Consulting Group in the Statistics Department at The University of Georgia. The data presented in Table 1
were subjected to a nonparametric test (equivalent to the Mann-Whitney or Wilcoxon Rank Sum Statistic) that provided an exact P-value of P = 0.00002 for each of the bacterial species evaluated individually.
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Study II was conducted to evaluate the efficacy of application of an acidic, copper sulfate-based commercial sanitizer in a poultry scalder alone or in combination with a postpick dip solution as a means of reducing indicator populations of bacteria and Salmonella prevalence on ready-to-cook carcasses.
A study was conducted at a very large commercial poultry processing facility producing 340,000 whole ready-to-cook carcasses per day. The research project was conducted over 10 wk. One set of 10 carcasses was collected postscald (sample point A), and 10 carcasses were collected after scalding, picking, and a tap water postpick dip (sample point B) and evaluated for aerobic plate counts, EC counts, and Salmonella prevalence. On one processing line, no chemicals were added to the scalders, pickers, or in the postpick dip. The carcasses selected from this line were considered the control groups A and B. The scalder on the other identical processing line was dosed with this sanitizer to a target pH range of 2.0 and a target level of 1.0 to 2.0 mg/L of copper sulfate. After the initial dosing to bring the pH down, the third scalder was continually dosed during the process with the sanitizer to achieve a target level pH of 2.0 and 2.0 mg/L of copper sulfate. The overflow water coming out of the third scald tank (counter-current flow scalder) was monitored for pH and free copper, and the level of material added to the incoming fresh water was adjusted based on these measurements, enabling all 3 tanks to be maintained at a pH of 2.0. A postpick dip solution was prepared by filling a sanitized 166.5-L container with tap water and dosing the water with the sanitizer to achieve a pH of 2.0 and a copper content of 2.0 mg/L using copper sulfate. A group of carcasses was collected postscald (sample point A) and postpick and dip (sample point B) on the Tasker treated line and evaluated for aerobic plate counts (APC), EC counts, and Salmonella prevalence. These carcasses were considered treatment groups A and B.
For control groups A and B and treatment groups A and B, the carcasses were collected after at least 2 flocks had traversed the scalder. Ten carcasses were removed postscald (sample point A) on the control and treated lines and 10 carcasses were removed after picking and dipping in tap water or tap water with the sanitizer (sample point B) on the control and treated lines using the following technique to ensure that no bias was introduced. For sample point B, carcasses were removed from the line postpick and dipped into the tap water or water containing the sanitizer solution for 10 to 12 s. For every day of sampling, all 4 groups (control A, treatment A, control B, and treatment B) were selected from one single flock of birds to control for variables associated with bacterial levels and Salmonella prevalence between flocks.
After treatment, a carcass was selected visually on the line postscald or postpick dip, then the next 5 carcasses were counted aloud and the sixth carcass was selected for testing. The individual selecting the carcasses was wearing sterile examination gloves. In this way, no visual cues were used to introduce bias. The 10 carcasses were hung on a sanitized rack and allowed to drip for 2 min. Sterile zip ties were used to cinch the neck of each chicken to prevent leakage of crop contents into the sample bag. Additionally, a sterile, unscented tampon was used to plug the vent of the chickens to prevent leakage of fecal material into the sample bag during shaking as described by Musgrove et al. (1997). In this way, the contents of the intestinal tract were not able to influence the disinfection ability of the sanitizer during scalding or in scalding and postpick dipping. The carcasses were then individually bagged in sterile polyethylene bags and rinsed using 400 mL of sterile Butterfield’s phosphate buffer by conducting the whole carcass rinse method as employed by the USDA inspectors in processing facilities. Numerous test rinsates were evaluated using pH probes to ensure that the Butterfield’s phosphate buffer was sufficiently neutralizing the pH effect of the sanitizer. The rinsate was encoded using a 4-digit number (to prevent identification by employees at the microbiological analysis laboratory and the introduction of bias) and sent via overnight courier to a reference testing laboratory for evaluation for APC, EC counts, and Salmonella prevalence. Aerobic plate counts were determined using The Official Methods of Analysis of the AOAC, method 990.12, and reported in colony-forming units; EC counts were conducted using The Official Methods of Analysis of the AOAC, Method No. 998.08, and reported in colony-forming units; and Salmonella were tested using The Official Methods of Analysis of the AOAC, method 2000.07, and reported as positive or negative.
These tests were conducted for 10 wk and a total of 10 complete data sets were collected. The data sets were analyzed by the Statistical Consulting Group in the Department of Statistics at the University of Georgia. The Statistical Consulting Group had no way of identifying the samples because they were characterized by a 4-digit code that was known only to the researchers. Main effects of control versus treated were evaluated for each bacterial type. The overall experimental design was a 2 x 2 x 10 x 3 x 10 of treatment, location (sample point A or B), day of collection, bacterial type evaluated, and chicken, for a total of 400 chickens and 1,200 tests.
Statistical evaluation was conducted by the Statistical Consulting Group in the Department of Statistics at the University of Georgia. Treatment effects were determined using t-tests and the Statistical Analytical Software (SAS Institute Inc., Cary, NC) program for APC and EC counts. For Salmonella prevalence, Fisher’s exact test was conducted using SAS.
Study III
Study III was conducted to evaluate the effect of an acidic, copper sulfate-based commercial sanitizer applied during immersion scalding, immersion chilling, and post-chill dipping on psychrotrophic spoilage bacteria and subjective odor assessment of broiler chicken carcasses.
A study was conducted in a commercial poultry processing facility. To mimic application of the product in the scalder, scalder water was removed from the tank after 5 h of production to ensure organic loading of the water and placed into two 208.2-L drums (S). To mimic the 3 chillers used in this plant, two 208.2-L gallon drums were filled with water from chiller 1 (CH1), 2 were filled with water from chiller 2 (CH2), and 2 were filled with water from chiller 3 (CH3). To mimic a postchill dip application, two 208.2-L gallon drums were filled with tap water (DIP). One of each of these pairs of drums (S, CH1, CH2, CH3, and DIP) was used as a control and one was dosed with the sanitizer to a pH of 2.0 and copper sulfate content of 2.0 mg/L, except the chiller water drums were dosed to a pH of 3.2 and a copper sulfate content of 2.0 mg/L. Eighteen carcasses each were exposed to the control or treated S for 2 min, CH1 for 17 min, CH2 for 15 min, CH3 for 45 min, and DIP for 10 s, in that order, and were allowed to drip for 1 min, individually placed into sterile bags, sealed, and packed on ice in a cooler. The carcasses were transported to a reference laboratory and held at 4°C. After storage for 6, 8, 10, 12, 14, and 16 d, 3 carcasses each from the control and treated groups, respectively, were evaluated by a 3-member panel for odor score, where 1 = no off odor, 2 = questionable with regard to acceptability, and 3 = unacceptable. The reference laboratory had 3 technicians who routinely conduct quality evaluations on poultry products. Thus, the panel evaluating the chicken was considered a trained panel. Additionally, after odor scores were recorded, psychrotrophic plate counts (PPC) were conducted on each carcass on d 6, 8, 10, 12, 14, and 16 of storage using the method described by Cousin et al. (1992).
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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The results for the effect of the sanitizer on pathogenic, indicator, and spoilage bacteria associated with broiler chicken carcasses in a model scald water system are presented in Table 1
. Exposure of ST, LM, SA, PF, or SP to the sanitizer in scalder water at 54°C for 2 min resulted in complete elimination of these bacterial species. Exposure of EC to the treated scald water resulted in a 4.9 log10 (>99.99%) reduction. These results indicate that one can be 99.99998% sure that the hypothesis that an acidic, copper sulfate-based commercial sanitizer will significantly reduce each of the pathogens, the indicator, and the spoilage bacteria evaluated is true, and that there is a 0.00002% chance that the hypothesis is incorrect. These data strongly suggest that using this sanitizer would be an effective means of controlling cross-contamination of pathogenic, indicator, and spoilage bacteria from carcass to carcass during scalding.
Study II
Results for application of an acidic, copper sulfate-based commercial sanitizer in a poultry scalder alone or in combination with a postpick dip solution as a means of reducing pathogenic and indicator populations of bacteria on ready-to-cook carcasses are presented in Tables 2 and 3. Aerobic plate counts were significantly (P 0.05) reduced on all days of sampling and overall for carcasses scalded in the sanitizer. The average log10 reduction across all days of sampling was 3.80. Escherichia coli counts were significantly (P 0.05) reduced on all days of sampling and overall for carcasses scalded in the sanitizer. The average log10 reduction across all days of sampling was 3.05. Salmonella prevalence was significantly (P 0.05) reduced on 8 of 13 d of sampling and overall (P 0.05) for carcasses scalded in the sanitizer, then picked, then dipped in the sanitizer. On the days that the sanitizer did not significantly reduce Salmonella prevalence, the control samples had higher Salmonella prevalence, but the amount was not found to be significantly higher than treated samples. The average percent reduction across all days of sampling was 30%.
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0.05) reduced on all days of sampling and overall. The average log10 reduction across all days of sampling was 1.19. Escherichia coli counts were significantly (P 0.05) reduced on all but 2 d of sampling and overall for carcasses scalded in the sanitizer, picked, and dipped in a solution containing the sanitizer, except for d 2 and 10. The averages on these days were higher for control samples, but were not found to be significantly different. The average log10 reduction across all days of sampling was 1.2. Salmonella prevalence was not consistently impacted overall for carcasses scalded in the sanitizer, picked, and dipped in the sanitizer. In some cases, the treated samples had a higher prevalence; in one case the controls had a higher prevalence; and in other cases, there were no differences. No real conclusion could be drawn regarding the efficacy of this product on post-picked and dipped Salmonella prevalence values. The reason why bacterial reductions postpicking and dipping were not as great as the reductions observed postscald was that the pickers were causing cross-contamination. The data collected postpicking and dipping are somewhat deceptive in that the full effect of use of an acidic, copper sulfate-based commercial sanitizer in the front end of the process could not be assessed by neutralizing the material in carcass rinses and evaluating them immediately after treatment. The positive effect of exposure time of the product on the carcasses as they ride down the processing line for 15 min until they reach online reprocessing has been shown in later studies (data not presented).
These data indicate that an acidic, copper sulfate-based commercial sanitizer was able to reduce APC, EC, and Salmonella during scalding, but due to excessive cross-contamination during picking, much of this effect was mitigated. However, even after picking, then dipping carcasses in the sanitizer, bacteria were reduced significantly in most cases; and although the effect on Salmonella at this stage was inconsistent, the beneficial effect on total Salmonella prevalence at the end of the process has been positive (data not presented). This sanitizer may be an effective means of assisting processors with meeting the USDA-Food Safety Inspection Service Salmonella performance standard in poultry processing facilities.
Study III
Results for the effect of an acidic, copper sulfate-based commercial sanitizer applied during immersion scalding, dipping, and immersion chilling on psychrotrophic spoilage bacteria and subjective odor assessment of broiler chicken carcasses are presented in Table 4. Odor scores were 1, 2, 3, 3, 3, and 3 for controls and 1, 1, 1, 2, 2, and 3 for treated samples on d 6, 8, 10, 12, 14, and 16, respectively. Base-10 logarithm PPC were 7.3, 7.6, 11, 11, 11, and 11 for controls and 5.2, 5.1, 6.8, 7.7, 8.1, and 11 for treated samples on d 6, 8, 10, 12, 14, and 16, respectively. Odor scores were significantly (P 0.05) reduced for treated carcasses at d 8 through 14 of storage. The PPC were significantly (P 0.05) lower on treated carcasses at d 6 through 14 of storage. This sanitizer suppressed the growth of spoilage bacteria with a 99.99% reduction at d 10 and a 99.9% reduction at d 12 of storage. The sanitizer prevented any spoilage defect from occurring on carcasses until d 12 (4 d later than controls) and prevented complete spoilage from occurring until d 16 (6 d later than controls). These data clearly indicate that the sanitizer had a significant impact on spoilage of broiler chicken carcasses. It can be concluded from these data that the sanitizer in the scalder, chiller, and as a postchill dip had a residual effect on the development of psychrotrophic spoilage bacteria during refrigerated storage. This effect could result in an extension of the shelf life of the poultry carcasses by up to 4 d.
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Received for publication August 17, 2007. Accepted for publication September 19, 2007.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONREFERENCES |
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Cousin, M. A., J. M. Jay, and P. C. Vasavada. 1992. Psychrotrophic microorganisms. Pages 156–157 in Compendium of Methods for the Microbiological Examination of Foods. C. Vanderzant and D. F. Splittstoesser, ed. Am. Public Health Assoc., Washington, DC.
Hinton, A., Jr., K. D. Ingram, M. E. Hume, and J. A. Cason. 2004. Use of MIDI-fatty acid methyl ester analysis to monitor the transmission of Campylobacter during commercial poultry processing. J. Food Prot. 67:1610–1616.[Web of Science][Medline]
Mikolajczyk, A., and M. Radkowski. 2002. Salmonella spp. on chicken carcasses in processing plants in Poland. J. Food Prot. 65:1475–1479.[Web of Science][Medline]
Mulder, R. W. A. W., L. W. J. Dorresteijn, and J. Van Der Broek. 1978. Cross-contamination during the scalding and plucking of broilers. Br. Poult. Sci. 19:61–70.[CrossRef][Web of Science]
Musgrove, M. T., N. A. Cox, J. S. Bailey, N. J. Stern, J. A. Cason, and D. L. Fletcher. 1997. Effect of cloacal plugging on microbial recovery from partially processed broilers. Poult. Sci. 76:530–533.
Okrend, A. J., A. B. Moran, and R. W. Johnston. 1986. Effect of acetic acid on the death rates at 52 degrees C of Salmonella newport, Salmonella Typhimurium, and Campylobacter jejuni in poultry scald water. J. Food Prot. 49:500–503.[Web of Science]
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