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Poult Sci 2007. 86:394-399
© 2007 Poultry Science Association
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PROCESSING, PRODUCTS, AND FOOD SAFETY

Frequency and Enumeration of Campylobacter Species from Processed Broiler Carcasses by Weep and Rinse Samples

N. J. Stern*,1, F. Georgsson{dagger}, R. Lowman{ddagger}, J.-R. Bisaillon{ddagger}, J. Reiersen§, K. A. Callicott*, M. Geirsdóttir{dagger}, R. Hrolfsdóttir{dagger}, K. L. Hiett* the Campy-on-Ice Consortium2

* USDA-Agricultural Research Service, Poultry Microbiological Safety Research Unit, Athens, GA 30604; {dagger} Food Laboratory, Environment and Food Agency of Iceland, IS-112 Reykjavik, Iceland; {ddagger} Canadian Food Inspection Agency, Ottawa, Ontario, Canada K2H 8P9; and § Agricultural Agency of Iceland, IS-112 Reykjavik, Iceland

1 Corresponding author: norman.stern{at}ars.usda.gov


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Frequency and numbers of Campylobacter spp. were assessed per freshly processed, contaminated broiler carcass. Campylobacter-positive flocks were identified by cecal sample analysis at slaughter. These flocks had been tested as Campylobacter negative at 4.1 ± 0.9 d prior to slaughter. Levels of contamination were estimated using 2 sampling approaches per carcass: (1) free weep fluids and (2) whole-carcass, 100 mL of distilled water rinses. Estimations of counts were determined by directly plating dilutions of weeps and rinses onto Campy-Cefex agar and incubating the plates at 41.5°C under microaerobic atmosphere. Confirmation was provided by latex agglutination to quantify levels per milliliter of weep and per 100 mL of rinse. Thirty-two slaughter groups (~20 carcasses per group) were compared from 2003 to 2004. The Campylobacter-positive weep frequency was 84.8%, whereas the frequency for rinse samples was 74.4% (P < 0.001). Enumeration of Campylobacter spp. on positive samples ranged from 0.70 to 6.13 log10 cfu/mL of weep (geometric mean of 2.84) and from 2.30 to 7.72 log10 cfu/100 mL of rinse (geometric mean of 4.38). The correlations between weep and rinse were 0.814 with 0.5 mL of rinse and 0.6294 when applying 0.1 mL of rinse The quantitative regression analyses for these 2 corresponding tests were log10 rinse (for 0.5 mL of inoculum) = 1.1965 log10 weep + 0.4979, and log10 rinse (for 0.1 mL of inoculum) = 1.322 log10 weep – 0.1521. FlaA SVR sequencing of isolates indicated that the same genotypes were found in weep and rinse samples. Weep and rinse sampling led to different proportions of Campylobacter-positive carcasses detection, but we demonstrated that this difference was reduced by increasing the amount of rinse fluid used for plating.

Key Words: Campylobacter • frequency • enumeration • weep • rinse


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The epidemic outbreak of human campylobacteriosis in Iceland during the late 1990s suggested that novel sources of Campylobacter jejuni had been introduced, causing increased public exposure (Stern et al., 2002). Among the earliest suspects fresh, chilled poultry products appeared to be plausible. In part, this was due to increased consumer demand for such products. Before February 1996, retail stores in Iceland had exclusively sold frozen carcasses to consumers, and no fresh poultry had been available in Iceland. The upsurge in consumer demand for fresh broiler products peaked in 1999, as did the incidence of human campylobacteriosis.

One consequence of selling only frozen carcasses was the reduced exposure to greater numbers of the organism via broilers. Freezing of broiler carcasses resulted in an approximate 2log reduction of C. jejuni numbers (Stern et al., 1985). Among 5 lots of processed broilers, levels of naturally contaminated Campylobacter on carcasses were reduced by log mean values ranging from 0.65 to 2.87 after 31 d of storage under frozen conditions (Georgsson et al., 2006). In 1995, regulations changed in Iceland, along with increased consumer demand for fresh product, and, consequently, the public was exposed to greater amounts of fresh poultry having increased levels of the pathogen.

Therefore, we wished to determine the frequency and numbers of Campylobacter associated with freshly processed broilers, which represents a measure of consumer risk. Although the regulatory measure used to monitor microbiological quality of broiler carcasses has traditionally been rinse sampling, discussions and presentations at various meetings involving the Food and Drug Administration, Centers for Disease Control, and Health Canada have suggested that poultry weep sampling might serve as a superior measure to assess public exposure to Campylobacter associated with product (R. Lowman, Canadian Food Inspection Agency, personal communications). Musgrove et al. (2003) compared weep and rinse procedures for qualitative detection of the organism and found no significant difference between the methods. The present paper addresses how weep and rinse from poultry carcasses compare qualitatively and quantitatively to one another.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Sampling
In Iceland, regulations require that broiler flocks are sampled for Campylobacter spp. colonization 4.1 ± 0.9 d before slaughter. Those flocks that were determined as colonized were processed at the end of the work week (or day), and such lots were frozen or further processed to reduce subsequent consumer exposure to the pathogen. Some of the flocks that had tested as Campylobacter negative subsequently became colonized before the day of processing. These market-age flocks (36.4 ± 2.5 d of age) were detected by culturing 4 pools of 10 bird ceca obtained at the processing plant. Because it was not known whether the ceca would be positive, 18 to 20 freshly processed carcasses (2 cartons of 9 or 10 whole carcasses each) per lot were stored at –2 to 2°C for <24 h until the test results were determined. When the ceca were positive, the chilled carcasses were then shipped to the laboratory and tested as follows. In total, 32 process lots were colonized and sampled during the course of the study.

Immediately after the lot was processed, carcasses were placed into ready-to-ship commercial containers and held in storage. At up to 30 h after processing, the accumulated free fluids were aspirated by a sterile pipet and surface plated directly. Subsequently, each carcass was aseptically transferred into a new sterile plastic bag, 100 mL of distilled water was added, and each carcass vigorously shaken by hand for ~60 s. After being rinsed, the carcass was aseptically removed, and the rinse suspension was used for subsequent microbiological analysis.

Microbiology
Serial, logarithmic dilutions were made using sodium peptone water for the weep samples and distilled water for the rinse samples and then plated onto Campy-Cefex agar (Stern et al., 1992). Each sample was quantitatively analyzed for Campylobacter. Volumes of 0.1 or 0.5 mL (rinse samples) from the undiluted samples and 0.1 mL of 10–1 to 10–4 dilutions were surface plated onto duplicate Campy-Cefex plates. Before inoculation, plates to receive 0.5 mL were dried for 40 min at 37°C to obtain separated colonies. Other plates were dried for 20 min at 37°C. The inoculated plates were held in zip-sealed plastic bags and incubated at 41.5°C for 48 h. A microaerobic condition was created using gas mixtures of 5 to 10% O2, 70 to 85% N2, and 10 to 20% CO2 expelled through an inserted hose to thoroughly purge the bags of the normal atmosphere. After incubation, suspect colonies, preferentially from plates containing 15 to 150 colonies, were counted, and 3 colonies from each plate were confirmed using colony morphology, Gram stain, biochemical tests, and latex agglutination assays. The results were calculated as colony-forming units of Campylobacter spp. per 100 mL of distilled water rinse fluid or per milliliter of the weep fluid.

Molecular Typing
Isolates collected from broiler ceca, weep sampling, and rinse sampling of 2 broiler flocks were typed using the flaA short variable region (flaA SVR; Meinersmann et al., 1997). DNA was prepared from frozen stocks by placing 10 µL of glycerol stock in 50 µL of sterile, distilled water. Cells were lysed at 100°C for 5 min. Microcentrifuge tubes containing DNA samples were spun briefly to precipitate cellular debris (Hiett et al., 2002). The DNA was prepared for unrecoverable isolates by pipetting 40 µL of Wang’s transport medium into 200 µL of sterile distilled water, boiling these samples at 100°C for 5 min, and spinning to precipitate cellular debris (Callicott et al., 2005). In both cases, the flaA SVR was then amplified using the primers Fla4F (5'-GGA TTT CGT ATT AAC ACA AAT GGT GC-3'; Nachamkin et al., 1993) and FlaA625RU (Meinersmann et al., 1997) with a reaction mix containing 2 mM MgCl2, 0.125 µM of each primer, 0.8 mM each of dNTP, and 2.5 U of AmpliTaq in a 100-µL reaction. Tubes were subjected to 35 cycles of 94°C for 45 s, 55°C for 45 s, and 72°C for 1 min, followed by a 5-min extension at 72°C. Sequencing was performed using degenerate primers Fla106F (5'-GAY GAT GCT TCW GGK ATG-3') and FlaA625RU by BigDye@terminator 3.1 chemistry (Applied Biosystems, Foster City, CA). Sequence data were obtained using a 3730 DNA Analyzer (Applied Biosystems). The 359-nucleotide region between primers FlaA242FU (Meinersmann et al., 1997) and FlaA625RU was used for allelic comparisons.

Statistical Analysis
Statistical analysis of the levels of Campylobacter in the weep vs. the rinse sample was assessed (Microsoft Excel, Microsoft Corp., Seattle, WA). McNemar’s test (95% con-fidence interval) was used to determine whether the proportions of positive tests were different from one sampling method to the other. Regression analyses for weep vs. rinse sample enumeration were determined for 0.1-and 0.5-mL rinse aliquots inoculated per plate.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
In total, 615 carcasses from broilers of flocks, tested for colonization by Campylobacter spp., were compared quantitatively and qualitatively for contamination. Figures 1Go and 2Go provide quantitative comparisons of weep vs. rinse sampling. The regression coefficient of 0.6294 indicated that there was good comparability between these 2 quantitative measurements when only 0.1 mL of rinse was plated from the undiluted rinse. The next year we monitored the weep samples as above, but determined the rinse samples by directly plating 0.5 mL of the undiluted rinse onto Campy-Cefex plates. The regression coefficient of 0.814 indicated that there was substantially improved quantitative comparability between these 2 measurements. The quantitative regression analyses for these 2 corresponding tests were log10 rinse (for 0.1 mL of inoculum) = 1.322 log10 weep + 0.1521 and, log10 rinse (for 0.5 mL of inoculum) = 1.1965 log10 weep + 0.4979.


Figure 1
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  		Figure 1. Regression analysis of rinse and weep log count relations from 330 broiler carcasses contaminated with Campylobacter spp. as measured per milliliter of weep fluids or by enumerating 0.1 of 100 mL of rinse fluids inoculated onto Campy-Cefex agar.

 

Figure 2
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  		Figure 2. Regression analysis of rinse and weep log counts from 374 broiler carcasses contaminated with Campylobacter spp. as measured per milliliter of weep fluids or by enumerating 0.5 of 100 mL of rinse fluids inoculated onto Campy-Cefex agar.

 
The McNemar test was used to compare proportions of positive samples in the paired studies. The McNemar test indicated that qualitative weep sampling detected more Campylobacter-positive carcasses than did the rinse sampling. When weep sampling was compared with 0.1 mL of rinse sampling, the weep sampling detected 18.5% more Campylobacter-positive carcasses with a 95% confidence interval (Table 1Go) on the difference of 14.1 to 22.8%. When weep sampling was compared with 0.5 mL of rinse sampling, the weep sampling detected 3.7% more Campylobacter-positive with a 95% confidence interval of 0.7 to 6.8%. The gap reduction in differences when using more rinse fluid was correlated by the McNemar test. Results indicated the data went from {chi}2 = 57.3 when comparing weep with rinse with 0.1 mL to {chi}2 = 5.8 when comparing weep with rinse with 0.5 mL.


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  		Table 1. Comparison of qualitative recoveries of Campylobacter jejuni from processed carcasses by using weep and 0.1 or 0.5 mL-rinse sampling procedures1
 
The weep sample enumeration distribution of Campylobacter, by exponential groupings, among the processed carcasses is shown in Figure 3Go. The data represent the distribution for exponential levels of contamination. The actual estimations for levels of Campylobacter per carcass for each process lot, comparing weep and rinse methods, are shown in Table 2Go. Process lot number 25 had the highest levels observed with an average of 104.51 Campylobacter cfu/mL of weep and 105.94 cfu in 100-mL rinses.


Figure 3
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  		Figure 3. Enumeration distribution of Campylobacter by exponential groupings, among known contaminated carcasses as measured by enumeration of free weep and rinse samples from fresh, fully processed, Iceland broiler chickens.

 

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  		Table 2. Enumeration of Campylobacter spp. associated with process lots of fresh, fully processed broiler carcasses as estimated by weep and rinse methods
 
Genetic typing of isolates revealed little difference between sampling by the weep and rinse methods. For 1 flock, all 23 weep isolates, 12 rinse isolates, and 4 cecal isolates had the same flaA SVR allele (A11203). In the second flock, 16 of the 17 weep isolates, 4 of the 5 rinse isolates, and all 4 of the cecal isolates had 1 allele (A15498 [GenBank] ), whereas the remaining weep isolate has an allele (A14898) that differed from the common allele by 1 substitution. The last rinse isolate had an allele (A14875) that differed from A15498 [GenBank] by 74 substitutions. Because we have only 4 preprocessing isolates, we cannot know whether alleles A14898 and A14875 were present in the flock prior to slaughter or if they represented cross-contamination during processing. It did appear that the rinse and weep methods of sampling retail product could identify the predominant allele without difficulty and that both could provide common alleles present on the carcass.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
What monitoring measure should food inspection services use? And what is an acceptable level of risk for Campylobacter carcass contamination? These questions disregard the established understanding that there will, inevitably, be differences in human-virulence expression among specific strains. There will also be differences in human susceptibility to specific strains. Such answers will require additional insight and resource investment to resolve. However, consumers will equally mishandle poultry products, regardless of the unknown levels of pathogen contamination on the product. Weep and rinse sample enumerations (Figure 2Go) were well correlated, and sequence typing of isolates recovered using the 2 methods also gave similar results. The results of studies conducted using one of the sampling regimens would be acceptable to monitor carcass contamination.

Health concerns over the organism are expressed in a recent World Health Organization (2005) surveillance program newsletter article which indicated that qualitative and quantitative occurrence of Campylobacter in broiler chickens along the farm-to-fork continuum should be collected and validated. Pursuant to the question of Campylobacter numbers, Nannapaneni et al. (2005) reported that total colony-forming units of ciprofloxacin-resistant Campylobacter on carcass rinses in Arkansas ranged up to 4.06, 3.95, and to 3.04 log10 cfu/carcass in 2001, 2002, and 2003, respectively. Jorgensen et al. (2002) reported levels of Campylobacter on carcasses from retail outlets in England during the winters of 1998 and 1999. In that study, the log10 colony-forming units of Campylobacter spp. were 2.70 to 4.99 in 18% of the chickens and 5.00 to 6.99 in 20% of the carcasses sampled. In Italy, among 213 carcasses sampled, the overall estimated mean count per carcass was 5.16 ± 0.80, with the greatest level per flock averaging 6.13 log10 cfu/carcass (Manfreda et al., 2006). Stern and Robach (2003) reported the average numbers of Campylobacter spp. per broiler carcass in northern Georgia had decreased from 4.11 to 3.05 log10 cfu from 1995 to 2001. Throughout the United States from September 2003 through September 2004, 4,200 carcasses were sampled, and approximately 3.6% of the commercially processed broiler carcasses had greater than 105 cfu of Campylobacter spp. per carcass (Stern and Pretanik, 2006). In the present study among known contaminated carcasses, the average rinse numbers per carcass lot ranged from 2.95 to 5.94 log10 cfu (Table 2Go) with 41, 38, and 19% of the lots with results between 3 to 4, 4 to 5, and 5 to 6 log10, respectively.

Results from a previous study in Iceland by Georgsson et al. (2006) showed among 5 processed broiler lots (50 carcasses), the average carcass rinse per lot ranged from 4.66 to 6.07 log10 and was distributed as 50, 32, 14, and 4% among 4 to 5, 5 to 6, 6 to 7, and 7 to 8 log10, respectively. These earlier results for fresh broilers in Iceland were considerably higher than found in the present study. One explanation for the reduced numbers seen in the present study is that the flocks tested were Campylobacter negative at ~32 d of age and only became colonized during the last 4.1 ± 0.9 d before slaughter, whereas flocks in the previous study were demonstrated as positive prior to ~32 d of age. Colonization levels would be expected to increase with additional rearing time (Stern et al., 2005). An additional conclusion posed is that even though a control program to exclude naturally contaminated broilers from the market (by testing production flocks at ~32 d) cannot assure all fresh broilers are Campylobacter free, our data indicate that such inspection and altering how the product is distributed will reduce the level of public exposure.

The World Health Organization has suggested that weep fluids from processed poultry may provide a superior estimate of consumer exposure to Campylobacter spp. Regulatory Agencies in both Iceland and the United States routinely use rinse methodology to assess the microbiological quality of poultry carcasses in the processing plants. Weep sampling requires packaging and storing the carcasses until the weep fluid accumulates in the packaging material (~24 h). The package must then be aseptically opened and the weep aspirated for microbiological sampling. The quantity of weep materials produced is highly variable among each carcass and is, in part, dependent upon how many abrasions the carcass received during its processing, how well the carcass was drained after chilling, and the length of time the carcass was held in storage.

Weep samples may vary from 0.5 mL to several milliliters per carcass. As a confounder, the Campylobacter enumeration may vary with the amount of weep accumulated. To accomplish their goals, inspectors among regulatory agencies must work in a timely manner and must have a consistent sampling protocol. The variation in weep sample quantity disregards this requirement. Conversely, rinse samples are typically taken at the end of the broiler processing line and consistent quantities of diluent are added to individual carcasses. The carcass rinse agitation is prescribed for a certain arc and duration. This rinse sampling remains the standard and, as shown in this paper, has substantial agreement with the weep sample method. When 0.5 mL of direct plating was used for quantitative rinse analyses, the substantial regression with the weep plating (R2 = 0.814) further supported the traditional sampling approach. When combined with the correlation coefficients indicated, this regression analysis enabled us to conclude that the 2 sample methods were highly predictive of one another. Despite the fact weep and rinse sampling approaches led to different results in terms of the proportion of Campylobacter-positive carcasses, it was demonstrated that this difference was reduced by increasing the amount of fluid used for the rinse method.

Regulatory agencies and the poultry industries are increasingly concerned over what levels of Campylobacter associated with broiler carcasses is a human health hazard. Answers to this question should be made using an acceptable method that can be incorporated into an ongoing regulatory regimen. After a method has been accepted, a rigorous comparison of poultry-borne Campylobacter exposure levels to the risk of human disease will be needed to draw the line between limited risk and substantial risk related to contamination of poultry carcasses.


   ACKNOWLEDGMENTS
 
Acknowledgement is extended to USDA-Cooperative State Research, Education, and Extension Service National Research Initiative for providing financial assistance for project 2002-35212-12369 and USDA-Agricultural Research Service CRIS no. 6612-32000-046-00.


   FOOTNOTES
 
2 Campy-on-Ice Consortium: USDA-Agricultural Research Service; Poultry Microbiological Safety Research Unit, Athens, GA; Agricultural Agency of Iceland, Reykjavik, Iceland; Institute of Experimental Pathology, Reykjavik, Iceland; Environment and Food Agency of Iceland; Landspitali University Hospital; Directorate of Health, Iceland; Swe-Chick AB, Sweden; Public Health Agency of Canada, Guelph, Ontario, Canada; University of Montreal; Decisionalysis Risk Consultants Inc.; and Canadian Food Inspection Agency, Ottawa, Ontario, Canada. Back

Received for publication June 2, 2006. Accepted for publication September 18, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Callicott, K. A., N. J. Stern, K. L. Hiett, and the Campy on Ice Consortium. 2005. Isolation of DNA for PCR assays from noncultivable Campylobacter jejuni isolates. Poult. Sci. 84:1530–1532.[Abstract/Free Full Text]

Georgsson, F., Á. E. Porkelsson, M. Geirsdóttir, J. Reiersen, and N. J. Stern. 2006. The influence of freezing and duration of storage on Campylobacter and indicator bacteria in broiler carcasses. Food Microbiol. 23:677–683.[ISI][Medline]

Hiett, K. L., N. A. Cox, R. J. Buhr, and N. J. Stern. 2002. Genotype analysis of Campylobacter isolated from distinct segments of the reproductive tracts of broiler breeder hens. Curr. Microbiol. 45:400–404.[ISI][Medline]

Jorgensen, F., R. Bailey, S. Williams, P. Henderson, D. R. Wareing, F. J. Bolton, J. A. Frost, L. Ward, and T. J. Humphrey. 2002. Prevalence and numbers of Salmonella and Campylobacter spp. on raw, whole chickens in relation to sampling methods. Int. J. Food Microbiol. 76:151–164.[ISI][Medline]

Meinersmann, R. J., L. O. Helsel, P. I. Fields, and K. L. Hiett. 1997. Discrimination of Campylobacter jejuni isolates by fla gene sequencing. J. Clin. Microbiol. 35:2810–2814.[Abstract]

Manfreda, G., A. De Cesare, V. Bondioli, N. J. Stern, and A. Franchini. 2006. Enumeration and Identity of Campylobacter spp. in Italian broilers. Poult. Sci. 85:556–562.[Abstract/Free Full Text]

Musgrove, M. T., N. A. Cox, M. E. Berrang, and M. A. Harrison. 2003. Comparison of weep and carcass rinses for recovery of Campylobacter from retail broiler carcasses. J. Food Prot. 66:1720–1723.[ISI][Medline]

Nachamkin, I., K. Bohachick, and C. M. Patton. 1993. Flagellin gene typing of Campylobacter jejuni by restriction fragment length polymorphism analysis. J. Clin. Microbiol. 31:1531–1536.[Abstract/Free Full Text]

Nannapaneni, R., R. Story, K. C. Wiggins, and M. G. Johnson. 2005. Concurrent quantitation of total Campylobacter and total ciprofloxacin-resistant Campylobacter loads in rinses from retail raw chicken carcasses from 2001 to 2003 by direct plating at 42°C. Appl. Environ. Microbiol. 71:4510–4515.[Abstract/Free Full Text]

Stern, N. J., K. L. Hiett, G. A. Alfredsson, K. G. Kristinsson, J. Reiersen, H. Hardardottir, H. Briem, E. Gunnarsson, F. Georgsson, R. Lowman, E. Berndtson, A. M. Lammerding, G. M. Paoli, and M. T. Musgrove. 2002. Campylobacter spp. in Icelandic poultry operations and human disease. Epidemiol. Infect. 130:23–32.

Stern, N. J., and S. Pretanik. 2006. Counts of Campylobacter spp. on United States broiler carcasses. J. Food Prot. 69:1034–1039.[ISI][Medline]

Stern, N. J., J. Reiersen, R. Lowman, J.-R. Bisaillon, V. Fridriksdottir, E. Gunnarson, K. L. Hiett, and the Campy-on-Ice Consortium. 2005. Occurrence of Campylobacter spp. in cecal contents among commercial broilers in Iceland. Foodborne Pathog. Dis. 2:82–89.[ISI][Medline]

Stern, N. J., and M. C. Robach. 2003. Enumeration of Campylobacter spp. in broiler feces and in corresponding processed carcasses. J. Food Prot. 66:1557–1563.[ISI][Medline]

Stern, N. J., P. J. Rothenberg, and J. M. Stone. 1985. Enumeration and reduction of Campylobacter jejuni in poultry and red meats. J. Food Prot. 48:606–610.

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.[ISI]

World Health Organization. 2005. Campylobacter Surveillance Program Newslett. 84/85:2.





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