J APPL POULT RES 2008. 17:354-360. doi:10.3382/japr.2008-00024
© 2008 Poultry Science Association
Presence and Numbers of Campylobacter, Escherichia coli, and Salmonella Determined in Broiler Carcass Rinses from United States Processing Plants in the Hazard Analysis and Critical Control Point-Based Inspection Models Project
M. E. Berrang*,1,
J. S. Bailey*,
S. F. Altekruse
and
W. K. Shaw, Jr.
* USDA-Agricultural Research Service, Russell Research Center, Athens GA 30605; and USDA-Food Safety and Inspection Service, Washington, DC 20250-3700
1 Corresponding author: mark.berrang{at}ars.usda.gov
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SUMMARY
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In 1999, the USDA-Food Safety and Inspection Service introduced an inspection system called the Hazard Analysis and Critical Control Point-Based Inspection Models Project (HIMP). The HIMP varies from standard inspection in that the emphasis of Food Safety and Inspection Service inspection program personnel is shifted. Each carcass is still visually inspected according to the Poultry Products Inspection Act, but some responsibility for food safety and identification and removal of defects is shifted from the regulatory agency to the processor, freeing up inspectors to more effectively verify the process and food safety system of the establishment. This survey was conducted in 2 stages: first to examine carcasses collected in HIMP and non-HIMP plants and then to test carcasses from all 20 volunteer plants currently operating under HIMP inspection. Carcasses were collected at rehang and postchill being careful to follow the same flock through processing. Postchill carcasses from HIMP plants were found to have equal bacterial contamination (numbers of Campylobacter and Escherichia coli and presence of Salmonella) as carcasses from standard HACCP plants. Overall, HIMP inspection, which places additional responsibility on the plant for process control, does not affect the microbiological quality of fully processed broiler carcasses.
Key Words: broiler processing • Campylobacter • Escherichia coli • Salmonella • Hazard Analysis and Critical Control Point-Based Inspection Models Project • inspection
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DESCRIPTION OF PROBLEM
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In the United States, commercial young chicken (broiler) processing plants that participate in interstate commerce operate under inspection by the USDA-Food Safety Inspection Service (FSIS). Commercial poultry processing has been shown to significantly lower the numbers and prevalence of bacteria including human pathogens on chicken carcasses [1–3]. However, inspection alone cannot be credited with lowering bacterial numbers; rather, the goal of inspection is to verify that processors are complying with federal regulations and implementing effective food safety systems to ensure a safe and wholesome product. Traditional inspection includes the visual examination of every carcass on the shackle line by FSIS employees to identify and remove defects. In 1996, FSIS inspection of poultry was modified by the Pathogen Reduction Final Rule to include Hazard Analysis and Critical Control Point (HACCP) principles [4]. Although this was a monumental undertaking for the poultry processing industry and new requirements for process control verification and record keeping were instituted, it did not result in a fundamental change in the practice of online carcass inspection.
In 1999, FSIS began the testing phase of a new inspection system called HACCP-Based Inspection Models Project (HIMP). Commercial broiler processing plants that were interested in participating in HIMP were allowed to enroll on a volunteer basis. Twenty broiler processing plants are currently operating under HIMP inspection. Although every carcass is still visually inspected, HIMP differs from standard inspection in some respects. Much of the emphasis is placed on food safety system inspection and verification. Some of the responsibility for carcass-to-carcass inspection is shifted to the processor to provide defect-free carcasses to the FSIS visual inspection personnel, who are placed on the line before the final chiller. This is approached by identifying and removing defects, defining corrective actions, and solving production problems. The result is that FSIS inspectors have greater flexibility to provide food safety system verification and oversight inspection to assure that the process is under control [5].
There have been reports suggesting that after implementation of the pathogen reduction HAC-CP systems final rule in 1996, or due to a combination of processing modifications commonly instituted during the same time period, poultry carcasses had lower prevalence of pathogenic bacteria such as Salmonella and Listeria [4, 6]. Data collected in 1998 and 2000 resulted in a published study comparing the performance of HIMP plants before and after the start of the new inspection system [7]. Much of the data reported by Cates et al. [7] are not microbiological; however, that report and information presented by FSIS on the internet [8] suggest that broiler carcasses from plants under HIMP inspection are not microbiologically different than those from non-HIMP plants. The objective of the current study was to measure the numbers of Campylobacter and Escherichia coli and the prevalence of Salmonella on chicken carcasses from commercial broiler processing plants operating under HIMP inspection in 2004 to 2005 and 2006 and compare the results to those from commercial plants under standard HACCP inspection.
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MATERIALS AND METHODS
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2004 to 2005 Sample Plan
In 2004 to 2005, broiler carcasses were examined from 20 commercial broiler processing plants randomly selected [9] from all large plants in the United States. Test plants were located in 13 states [10] representing 8 integrated broiler companies. Four plants were under HIMP inspection, whereas the other 16 were under standard HACCP inspection plans.
The FSIS personnel traveled to each plant and collected samples 4 times, roughly spaced to represent seasons. Each season was defined as a 10-wk period of time during which 2 plants were visited each week. All processing plants were sampled on Monday or Tuesday morning. Carcasses were collected at rehang to determine the presence and numbers of bacteria on carcasses early in processing for comparison to postchill carcasses. On each sample day from each plant, 10 carcasses were removed from the shackle line or rehang table (depending on safety and convenience) at the point where the change was made from the kill line to the evisceration line. Using plant evisceration line speed (from 70 to 160 carcasses per minute) and timing (including chilling time), the same flock was sampled again by removing an additional 10 carcasses after immersion chilling. The total number of samples was 800 carcass rinses; 80 from HIMP plant at rehang, 320 from standard HACCP plants at rehang, 80 from HIMP plants postchill, and 320 from standard HACCP plants postchill.
2006 Sample Plan
In the fall of 2006, broiler carcasses from all 20 HIMP-inspected commercial broiler processing plants in the United States were examined. The FSIS personnel traveled to each plant once during a 4-wk period (5 plants/wk) to collect samples. Samples were collected using the same sites, timing for flock control, and methods as in the 2004 to 2005 survey, except that only 5 carcasses were collected at each site. The total number of samples in this survey was 200; 100 samples at rehang and 100 postchill.
Sample Collection
All samples were collected by the same group of FSIS personnel, who traveled from plant to plant. Carcasses were removed from the line or table using a clean pair of latex gloves for each carcass. Each carcass was placed directly into a sterile plastic bag with 100 mL of sterile buffered peptone water. Carcass rinses were performed by hand-shaking the bag for 60 s. Carcass rinses were poured into sterile specimen cups and shipped by overnight courier in an insulated container with frozen ice packs. Upon receipt, the temperature of each sample was taken using an infrared thermometer [11] and recorded. If the temperature was below 10°C, the sample was used for culture. In cases in which the rinses were not within acceptable temperature range upon receipt, the plant was resampled. Resampling was required twice in 2004 and once in 2006.
Campylobacter Culture Methods
All samples were examined for Campylobacter by direct plating on Campy Cefex agar [12]. Serial dilutions of the rinsate were prepared in PBS and used to plate on the surface of the agar. To achieve a count for undiluted rinse, 0.25 mL of rinse was plated on each of 4 plates; greater dilutions were achieved by plating 0.1 mL on each of 2 duplicate plates. Plates were placed in sealable bags flushed with microaerobic gas (5% O2, 10% CO2, and 85% N2), bags were sealed, and the plates were incubated at 42°C for 24 to 48 h. Colonies characteristic of Campylobacter were counted. All colony types found in each sample were confirmed as members of the genus Campylobacter by observation of cellular morphology and motility under phase contrast microscopy. All colony types were further confirmed as thermophilic Campylobacter (members of species jejuni, coli, or lari) by means of a positive reaction to a latex agglutination serological test [13].
E. coli Culture Methods
The E. coli numbers were determined by placing 1 mL from a serial dilution onto a Petrifilm E. coli-coliform count plate [14]. Petrifilm plates were incubated at 35°C for 24 h and counted according to package instructions.
Salmonella Culture Methods
Thirty milliliters of rinse sample was aseptically mixed with 30 mL of buffered peptone water and incubated for 24 h at 37°C. Following preenrichment, samples were screened for the presence of Salmonella by an automated PCR assay according to the instructions of the manufacturer [15].
Positive Salmonella samples by PCR were confirmed by conventional methods. A 0.5-mL amount of PCR-positive preenriched sample was transferred to 10 mL of tetrathionate broth and 0.1 mL to 10 mL of Rappaport-Vassiliadis R10 broth [16]. Both enrichment broths were incubated aerobically at 37°C for 24 h. Each broth was used to streak onto the surface of Modified Lysine Iron Agar [17] and Brilliant Green Sulfa Agar [16] plates that were incubated aerobically at 37°C for 24 h. After incubation, a well-isolated colony with typical Salmonella spp. morphology was picked to Triple Sugar Iron and Lysine Iron Agar slants [16], which were incubated aerobically at 37°C overnight. Isolates with biochemical reactions typical of Salmonella were categorized by somatic surface serology [16] and flagellar antigen latex agglutination [13].
Statistical Analysis
Campylobacter and E. coli counts were transformed into base-10 logarithm colony-forming units per milliliter of carcass rinse. In cases in which no bacteria of interest were detected, the number was set as 0, and geometric means were determined. A Student’s t-test was used to determine effect of sample site within plant, inspection system, or year of sampling. The 
2 test for independence was used to determine the significance of differences in Salmonella prevalence. Significance was assigned at P 
0.05.
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RESULTS AND DISCUSSION
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Results from the 2004 to 2005 study in which 20 commercial broiler plants, 4 under HIMP inspection, were examined are shown in Table 1
. As a result of processing (rehang to postchill), numbers of Campylobacter and E. coli as well as the prevalence of Salmonella on broiler carcasses were effectively lowered (P < 0.05) in both HIMP and non-HIMP plants. Carcass rinses collected at rehang in HIMP plants had 0.4 log cfu/mL less Campylobacter than did those from non-HIMP plants. However, no difference was noted in Campylobacter numbers postchill. Neither were E. coli numbers or Salmonella prevalence affected by the type of inspection system employed at the different plants. From these data, we can conclude that these 4 HIMP plants were performing similarly to the 16 more traditionally inspected non-HIMP plants to lower the numbers and prevalence of bacteria on broiler carcasses.
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Table 1. Mean log colony-forming units per milliliter of Campylobacter and Escherichia coli and prevalence of Salmonella on carcasses from Hazard Analysis and Critical Control Point-Based Inspection Models Project (HIMP) and standard Analysis and Critical Control Point plants in 2004 and 2005
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The reduction in Campylobacter and E. coli between rehung and postchill samples noted in this study was similar to that seen in earlier studies undertaken in commercial broiler plants [1–3]. The broiler processing continuum lowers bacterial numbers and prevalence; inspection itself cannot be expected to have a direct effect. The current data, however, do show that postchill carcasses processed under HIMP inspection have a similar degree of contamination with Campylobacter, E. coli, and Salmonella as those processed under standard inspection.
Table 2 shows data from 4 HIMP plants examined in 2004 to 2005 and more data from the same plants examined again as part of the 2006 survey. This presentation allows comparison between sample years and testing to determine if there was any significant change in the bacterial profile of broiler carcasses between the 2 surveys. We found that the numbers of E. coli and the prevalence of Salmonella on carcasses collected in 2006 were not significantly different than what we detected in 2004. In 2004, twenty-five percent of postchill samples were Salmonella positive compared with just 5% in 2006 (P = 0.06). Overall mean Campylobacter numbers on fully processed broiler carcasses were significantly lower in 2006 compared with 2004. From these data, we conclude that in 2006, these 4 HIMP plants continued to perform at least as well as in 2004.
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Table 2. Mean log colony-forming units per milliliter of Campylobacter and Escherichia coli and prevalence of Salmonella (10 sampled in 2004 and 5 sampled in 2006) in broiler carcass rinses collected from 2 sites within 4 Hazard Analysis and Critical Control Point-Based Inspection Models Project plants in the fall of 2006 and fall of 2004
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The data from all 20 HIMP plants collected in 2006 are shown in Table 3. Comparisons were made using mean values to test the reduction in each type of bacteria due to processing. The numbers of Campylobacter and E. coli were significantly lower postchill than at rehang. Although in 1 plant more carcasses were detected postchill with Salmonella than at rehang, overall Salmonella prevalence was reduced due to broiler processing. Therefore, when considering all plants under HIMP inspection in the year 2006, it is clear that they performed adequately to reduce bacterial contamination on broiler carcasses. These data are in agreement with other studies, which show that poultry processing lowers bacterial contamination on carcasses [1–3]; these data specifically show that plants under HIMP inspection are effective to decrease bacterial contamination.
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Table 3. Mean log colony-forming units per milliliter of Campylobacter and Escherichia coli and prevalence of Salmonella in broiler carcass rinses collected from 2 sites within Hazard Analysis and Critical Control Point-Based Inspection Models Project plants in 2006
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CONCLUSIONS AND APPLICATIONS
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- The HIMP inspection does not interfere with the ability of a broiler slaughter plant to lessen the bacterial contamination on carcasses through processing operations.
- The microbiological quality of broiler carcasses from processing plants operating under HIMP inspection is equivalent to those from standard HACCP plants.
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ACKNOWLEDGMENTS
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We wish to acknowledge expert technical assistance by Eric Adams, Suttawee Thitaram, Debbie Posey, and Steven Lyon (USDA-Agricultural Research Service) and Patricia Bennett, Barbara Dwyer, and Bharat Patel (USDA-Food Safety and Inspection Service).
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REFERENCES AND NOTES
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- Izat, A. L., F. A. Gardner, J. H. Denton, and F. A. Golan. 1988. Incidence and level of Campylobacter jejuni in broiler processing. Poult. Sci. 67:1568–1572.[Web of Science][Medline]
- Berrang, M. E., and J. A. Dickens. 2000. Presence and level of Campylobacter on broiler carcasses throughout the processing plant. J. Appl. Poult. Res. 9:43–47.[Abstract/Free Full Text]
- Rosenquist, H., H. M. Sommer, N. L. Nielsen, and B. B. Christensen. 2006. The effect of slaughter operations on the contamination of chicken carcasses with thermotolerant Campylobacter. Int. J. Food Microbiol. 108:226–232.[CrossRef][Web of Science][Medline]
- Rose, B. E., W. E. Hill, R. Umholtz, G. M. Ransom, and W. O. James. 2002. Testing for Salmonella in raw meat and poultry products collected at federally inspected establishments in the United States, 1998 through 2000. J. Food Prot. 65:937–947.[Web of Science][Medline]
- FSIS. 1998. Slaughter inspection under the HACCP-Based Inspection Models Project–Oversight and verification. http://www.fsis.usda.gov/oa/background/keyover.htm Accessed July 17, 2008.
- Berrang, M. E., C. E. Lyon, D. P. Smith, and J. K. Northcutt. 2000. Incidence of Listeria monocytogenes on pre-scald and post-chill chicken. J. Appl. Poult. Res. 9:546–550.[Abstract/Free Full Text]
- Cates, S. C., D. W. Anderson, S. A. Karns, and P. A. Brown. 2001. Traditional versus hazard analysis and critical control point-based inspection: Results from a poultry slaughter project. J. Food Prot. 64:826–832.[Web of Science][Medline]
- FSIS. 2007. Public health lessons from HACCP-Based Inspection Models Project. http://www.fsis.usda.gov/PDF/Slaughter_LLange.pdf Accessed July 17, 2008.
- All 127 large (i.e., 500 or more employees) USDA-inspected young chicken slaughter establishments in operation in autumn 2004 were eligible for the study. A random sample of 20 establishments (about 1 in 6) was drawn using the SAS Procedure PROC SURVEYSELECT (SAS v 9.1, SAS Institute, Cary, NC).
- Alabama, Arkansas, California, Delaware, Georgia, Indiana, Missouri, North Carolina, South Carolina, Tennessee, Texas, Virginia, West Virginia.
- Cole Parmer Instruments Co., Chicago, IL.
- Stern, N. J., B. Wojton, and K. Kwiatek. 1992. A differential selective medium and dry ice generated atmosphere for recovery of Campylobacter jejuni. J. Food Prot. 55:514–517.[Web of Science]
- Microgen Bioproducts Ltd., Camberly, Surrey, UK.
- 3M Microbiology Products, St. Paul, MN.
- BAX PCR; DuPont Qualicon, Wilmington, DE.
- Becton Dickinson (Difco), Sparks, MD.
- Oxoid, Basingstoke, Hamphire, UK.
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