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Poult Sci 2008. 87:992-998. doi:10.3382/ps.2007-00406
© 2008 Poultry Science Association
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PROCESSING, PRODUCTS, AND FOOD SAFETY

The Effect of Chilling in Cold Air or Ice Water on the Microbiological Quality of Broiler Carcasses and the Population of Campylobacter1

M. E. Berrang2, R. J. Meinersmann, D. P. Smith and H. Zhuang

USDA-Agricultural Research Service-Russell Research Center, 950 College Station Rd., Athens, GA 30604

2 Corresponding author: mark.berrang{at}ars.usda.gov


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Cold air or ice water can be used to chill poultry carcasses after slaughter. The objective of this study was to compare the effect of 2 chill methods on broiler carcass bacteria. Broiler carcasses were cut in half along the dorsal-ventral midline; one half was subjected to an ice-water immersion chill in an agitated bath for 50 min, whereas the reciprocal half was subjected to an air chill in a 1°C cold room for 150 min. Total aerobic bacteria, coliforms, Escherichia coli, and Campylobacter were enumerated from half-carcass rinses. Species of Campylobacter isolates was determined by a commercial PCR method, which was followed by molecular subtyping with pulsed-field gel electrophoresis and determination of antimicrobial susceptibility to 9 drugs. Although significantly fewer of each bacterial type were detected per milliliter from immersion-chilled carcasses than from air-chilled carcasses, in each case the difference was less than 1 log10 cfu/mL. Chilling method did not affect species; both Campylobacter jejuni and Campylobacter coli were recovered. Results of pulsed-field gel electrophoresis subtyping did not suggest that either chilling method selected for any specific subtypes; most subtypes were found on carcass halves used for both the air chill and water immersion chill. Resistance to 2 antimicrobial drugs was noted in 9 C. coli isolates, 6 from air-chilled carcass halves and 3 from immersion-chilled carcass halves. These data showed that immersion-chilled carcasses had lower numbers of bacteria; however, the difference was not large and may have been due to simple dilution. Both methods were effective for lowering carcass temperature, and neither chilling method seemed to select for specific species, subtypes, or antimicrobial-resistant Campylobacter.

Key Words: Campylobacter • broiler • air chill • immersion chill


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
In the United States, most broiler processing plants use ice-water immersion to lower carcass temperature at the end of the first processing, whereas in the European Union, most processors use an air-chill method. Both chilling procedures are effective in lowering the temperature of broiler carcasses and have been shown to substantially reduce numbers of carcass-associated total aerobic bacteria, Escherichia coli, and Campylobacter (Blank and Powell, 1995; Allen et al., 2000a,b; Berrang and Dickens, 2000; Bilgili et al., 2002; Stern and Robach, 2003). Lindblad et al. (2006) reported that air chilling can be more effective than immersion chilling to lower the prevalence of Campylobacter on broiler carcasses, suggesting that air chilling can injure or kill Campylobacter by desiccation. Other authors reported no change in Campylobacter numbers on carcasses treated with an air-chill procedure in a commercial processing plant (Fluckey et al., 2003).

Poultry processing may affect the diversity of bacteria found on carcasses. Alter et al. (2005) found lower numbers and less diversity of Campylobacter on turkey carcasses after a commercial chilling procedure. Isolates detected postchilling were determined to be closely related, prompting the conclusion that chilling may have selected for a limited subset of Campylobacter. Sanchez et al. (2002) examined antimicrobial resistance profiles of bacteria from air-chilled and immersion-chilled broiler carcasses. They reported a difference in resistance according to the chill method used; specifically, resistance to tetracycline was found in Campylobacter from air-chilled carcasses, whereas resistance to nalidixic acid was noted in Campylobacter from immersion-chilled carcasses.

Most published studies comparing air chilling with immersion chilling have used different carcasses for each process. Carcass-to-carcass and flock-to-flock variation in microbial populations has been documented (Renwick et al., 1993; Berrang and Dickens, 2000). Carcass-to-carcass variation can be avoided by using paired half carcasses split along the dorsal-ventral midline to examine the effect of various processing treatments on bacterial numbers (Izat et al., 1990; Cason and Berrang, 2002).

The objective of the current study was to determine whether chilling broiler carcasses in cold air or ice water would affect bacteria on the carcasses differently. Numbers of total aerobic bacteria, coliforms, E. coli, and Campylobacter were measured on paired half-carcass samples after air and water chilling. We further examined the possibility that the air-chill and water-chill methods could select for different species, subtypes, or antimicrobial resistance profiles of Campylobacter.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Carcasses

On each of 8 replicate sampling days, 16 broiler carcasses (42 to 56 d of age) were collected from 1 of 2 commercial broiler processing plants. Carcasses were randomly removed from the shackle line after evisceration, before the inside-outside washer. Each carcass was placed in an individual plastic bag and transported to the laboratory without ice. Upon arrival at the pilot processing plant (within 45 min), each carcass was cut in half with a bone saw along the dorsal-ventral midline, resulting in mirror-image halves. The saw blade was sanitized with 70% ethanol to limit cross-contamination. Each carcass half was identified with a sanitized tag (Heartland Animal Health Inc., Fair Play, MO), to facilitate identification of halves from the same carcass, and placed into a separate clean plastic bag. Carcass halves were randomly assigned to a chill treatment. Ten half carcasses were subjected to an immersion chill, and the corresponding halves of each carcass were subjected to an air-chill procedure.

Chilling Procedures

Immersion chilling was conducted in a pilot-scale paddle-agitated chill tank filled with 151 L of ice and tap water (average total chlorine level of 0.5 mg/L). The intramuscular temperature of one extra carcass half and the temperature of the ice-water chill bath were noted before placement of carcass halves by use of a thermocouple thermometer (Barnant Co., Barrington, IL) out-fitted with a hypodermic needle microprobe (Physitemp Instruments Inc., Clifton, NJ). Tagged carcass halves were placed in the pilot chill tank and allowed to agitate for 50 min. One extra carcass half was included for temperature measurement after the chill period was completed.

Air chilling was conducted in a 31.2 m2 refrigerated room (1°C) with a ceiling height of 2.4 m. Ten carcass halves were hung by the leg from shackles, which were attached to a bar and rack. This placed the carcasses approximately 1.5 m above the floor and 5.2 m from a series of 3 circulation fans within the cooling unit. Carcass halves were randomly assigned to shackles, which were arranged in a single line such that all carcasses were exposed to the flowing air. Carcass halves remained in the room for 150 min. The air currents within the room proved to be complex; however, the cooling unit fans were in constant operation, resulting in air moving past the carcasses at approximately 76.2 m/min as measured with a velometer (Alnor Products TSI Inc., Shoreview, MN). Although the air currents were not perfectly uniform within the room, the cooling unit was run the same way in each replication, and airflow was the same for each replication when measured in a set location. A large tub full of water (0.62 x 0.62 x 0.91 m) was maintained in the cooling chamber in an effort to keep the air uniformly humid for each replication. The temperature and RH were measured every 15 min (Cox Recorders, Belmont, NC) during the air-chill treatment. One extra carcass half was included in the sample set and used to measure intramuscular temperature after the air-chill treatment was completed.

Carcass Sampling and Bacterial Culture

Carcass halves were sampled by a rinse method. Each half was placed in a separate plastic bag, 100 mL of sterile PBS was added, and the bags were shaken by hand for 60 s. Rinse diluent was used to prepare serial dilutions in PBS, which were plated onto media for enumeration of total aerobic bacteria, coliforms, E. coli, and Campylobacter. Total aerobic bacteria were enumerated by plating 0.1 mL of a serial dilution onto the surface of a plate count agar plate (Becton Dickinson, Sparks, MD). Plate count agar plates were incubated at 35°C for 24 h, and all colonies were counted. Coliform and E. coli numbers were determined by placing 1 mL from a serial dilution onto a Petrifilm E. coli-coliform count plate (3M Microbiology Products, St. Paul, MN). Petrifilm plates were incubated at 35°C for 24 h and counted according to package instructions. Samples were examined for the presence of Campylobacter both by enrichment for detection of injured cells and by enumeration. Enrichment was conducted by placement of 1 mL of carcass rinse into 9 mL of Campylobacter enrichment broth (CEB; Accumedia Manufacturers Inc., Baltimore, MD). Tubes of CEB were incubated in resealable bags flushed with microaerobic gas (5% O2, 10% CO2, 85% N2) for 48 h at 42°C. Incubated CEB was used to streak Campy-Cefex agar (CCA) plates (Stern et al., 1992), which were incubated as described below. Campylobacter were enumerated by plating 0.1 mL of a serial dilution onto each of duplicate CCA plates. Campy-Cefex agar plates were incubated at 42°C in a resealable bag flushed with microaerobic gas. Colonies characteristic of Campylobacter were counted as cfu. Each colony type on each plate was confirmed as Campylobacter by observation of typical cellular morphology and motility on a wet mount under a phase-contrast microscope (Carl Zeiss Microimaging Inc., Thornwood, NY). Each colony type was further confirmed as a member of thermophilic Campylobacter species (jejuni, lari, or coli) by using a latex agglutination kit (Microgen Bioproducts Ltd., Camberly, UK).

Statistical Analysis

Numbers of colonies detected on duplicate plates were recorded as the mean number of cfu per milliliter of carcass rinse. Numbers of cfu were log10-transformed and geometric means for each treatment were calculated. A GLM procedure was conducted for each bacterial count by using a randomized complete block design with replication as the block and chill treatment as the main effect. Significance was assigned at P ≤ 0.01.

Campylobacter Speciation, Subtyping, and Antimicrobial Resistance Testing

In 2 of 3 replications in which Campylobacter was detected, 2 representative colonies from each carcass half subjected to air chill and 2 from the corresponding halves subjected to immersion chill were selected for subtyping. All selected colonies were subcultured on CCA plates to produce pure culture isolates. The species (C. coli or C. jejuni) of each isolate was determined by using an automated PCR system (BAX, Qualicon Inc., Wilmington DE) according to the manufacturer’s instructions.

Isolates were subtyped by using a pulsed-field gel electrophoresis (PFGE) method similar to that described by Centers for Disease Control and Prevention (CDC) PulseNet [One-Day (24–26 h) Standardized Laboratory Protocol for Molecular Subtyping of Campylobacter jejuni by Pulsed Field Gel Electrophoresis (PFGE); http://www.cdc.gov/PULSENET/protocols/campy_protocol.pdf, accessed July 3, 2007] with the addition of a postre-striction incubation. Briefly, bacterial DNA was embedded in 1.0% agarose (SeaKem Gold, Cambrex, Rockland, ME) and restricted with 40 U of SmaI (Roche Molecular Biochemicals, Indianapolis, IN). Control standards were prepared for comparison from Salmonella Braenderup H9812 DNA restricted with XbaI (Roche Molecular Biochemicals, Indianapolis, IN; Hunter et al., 2005). Sliced plugs with embedded DNA were subjected to a 5-min room temperature incubation in 200 µL of 0.5x Tris-borate-EDTA before loading the gel. Deoxyribonucleic acid was separated by using a CHEF Mapper XA PFGE system (Bio-Rad, Hercules, CA) according to the manufacturer’s instructions. Electrophoresis was conducted at 6 V for 18.5 h with an increased pulse time of 6.76 to 35.58 s in 0.5x Tris-borate-EDTA at 14°C. Gels were stained with ethidium bromide and imaging was done by using a Gel Doc 1000 instrument (Bio-Rad). Images were saved as TIFF files and analyzed (BioNumerics software, version 4.0, Applied Maths Scientific Software Development, Sint-Martens-Latem, Belgium). The image from each gel was normalized by using the standard, and bands within the range of the standard (668.9 to 20.5 kB) were marked. Cluster analysis of PFGE subtyping data was conducted using dice coefficient and the unweighted pair-group method analysis (UPGMA, Bio-Numerics software, version 4.0).

Campylobacter isolates that were subjected to subtyping were also tested for resistance to a panel of 9 antimicrobials, including azithromycin, ciprofloxacin, erythromycin, gentamicin, tetracycline, florfenicol, nalidixic acid, telithromycin, and clindamycin. A commercially available broth microdilution method was used to determine antimicrobial resistance profiles (Sensititre-Campy, Trek Diagnostics Systems Ltd., Cleveland, OH) following the protocol provided by the manufacturer. Breakpoints for resistance to the drugs in the panel, as previously determined for Campylobacter, were ciprofloxacin ≥4 µg/mL, erythromycin ≥32 µg/mL, and tetracycline ≥16 µg/mL (Clinical and Laboratory Standards Institute, 2006.) Breakpoints used for the other drugs in the panel were those used by the National Antimicrobial Resistance Monitoring System (http://www.fda.gov/cvm/NARMSReport2004.htm, accessed June 11, 2007) and are as follows: azithromycin ≥8 µg/mL, clindamycin ≥8 µg/mL, gentamicin ≥8 µg/mL, nalidixic acid ≥64 µg/mL, telithromycin ≥8 µg/mL. Because of a lack of resistant strains, no breakpoint is provided for florfenicol, but any resistance above 4 µg/mL would be considered nonsusceptible.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Mean percent RH in the air-chill chamber ranged from 79.4 to 87.6% RH, with an average of 81.6% RH. Mean temperature in the air-chill chamber ranged from 0.75 to 1°C, with an average of 0.9°C. The temperature of broiler carcasses as measured in the thigh muscle before entering either chill treatment ranged from 27 to 38°C, with an average of 32.4°C. After the air-chill treatment, the mean temperature of broiler carcasses was 1.4°C; the mean temperature after the ice-water immersion-chill treatment was 1.6°C.

Mean numbers of bacteria recovered from carcass rinses in 8 replications of air or ice-water chilling are shown in Table 1Go. Numbers of total aerobic bacteria, coliforms, and E. coli were higher per milliliter of half-carcass rinse after air chilling than after ice-water immersion chilling. In each case, the difference in counts attributable to the chill method was approximately 0.5 log cfu/mL of half-carcass rinse. Campylobacter was detected only in carcass rinses from 3 of the 8 replications conducted (replications 6, 7, and 8); all carcasses in these replications were Campylobacter positive. Similar to the other bacterial populations enumerated, Campylobacter counts were approximately 0.5 log cfu/mL higher on half carcasses subjected to air chilling as compared with those subjected to the ice-water immersion-chilling technique.


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  		Table 1. Mean log cfu (±95% confidence interval) aerobic bacteria, coliforms, and Escherichia coli and Campylobacter per milliliter of rinse of half-broiler carcasses chilled in air or by ice-water immersion
 
In replications 7 and 8, two colonies from each Campylobacter-positive half carcass were used for further characterization of the isolates. The species detected and antimicrobial resistance profiles of those isolates are shown in Table 2Go. Campylobacter jejuni and C. coli were detected in both replications. However, C. jejuni was more prevalent in replication 7 and C. coli was more commonly encountered in the eighth replication. In some cases, both species were found on both halves of the same carcass or even on the same half carcass. For example, C. jejuni was detected on the air-chilled half of carcass 2 in replication 7, whereas C. coli was detected on the immersion-chilled half; both species were found on the water-chilled half of carcass 1 in replication 7. Overall, 2 species of Campylobacter were detected on 12 of the 20 carcasses (60%); it is possible that more of the carcasses had both species, but the sample size of 2 colonies per plate limited the detection.


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  		Table 2. Species of Campylobacter detected and antimicrobial resistance of isolate from carcass halves cooled by means of air chilling or ice-water immersion
 
The results of PFGE subtyping of Campylobacter isolates from replications 7 and 8 are shown in Figures 1Go and 2Go, respectively. No subtype of C. jejuni or C. coli appeared in more than 1 experimental replication. In replication 7 (Figure 1Go), 30 C. jejuni were detected; 1 subtype included 29 isolates. Almost equal numbers (14 and 15) of isolates were from air-chilled and water-chilled carcass halves. Ten C. coli isolates were subdivided into 3 subtypes, and like C. jejuni, subtypes of C. coli included similar numbers of isolates from air- and water-chilled carcass halves. In replication 8 (Figure 2Go), 34 C. coli isolates were subdivided into 4 subtypes; the subtype with the most isolates (22) included 9 C. coli isolates from air-chilled carcass halves and 13 from water-chilled halves. Only 6 C. jejuni isolates were detected in replication 8; these included members of 2 subtypes and both chilling methods. Overall, 4 Campylobacter isolates were subtyped from each of 20 carcasses. Multiple subtypes were recovered from 15 carcasses (75%); 3 subtypes were detected on 4 carcasses, and 4 subtypes were detected on 1 carcass (carcass 3 in replication 8).


Figure 1
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  		Figure 1. Pulsed-field gel electrophoresis subtyping of Campylobacter isolated from half carcasses chilled in air or ice water in replication 7.

 

Figure 2
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  		Figure 2. Pulsed-field gel electrophoresis subtyping of Campylobacter isolated from half carcasses chilled in air or ice water in replication 8. All members of clades marked with an asterisk (*) were resistant to ciprofloxacin and nalidixic acid.

 
Antimicrobial resistance was noted only in C. coli isolates. Nine isolates from the eighth replication showed resistance to ciprofloxacin and nalidixic acid. All other isolates were susceptible to all drugs tested. Campylobacter coli isolates exhibiting resistance to ciprofloxacin and nalidixic acid were distributed across 2 subtypes and represented isolates from both chilling methods. The 2 subtypes that included antimicrobial-resistant C. coli were 49.66% similar to each other.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Many published studies have demonstrated a decrease in bacterial numbers on poultry carcasses during chilling (Blank and Powell, 1995; Allen et al., 2000a,b; Berrang and Dickens, 2000; Bilgili et al., 2002; Stern and Robach, 2003; Lindblad et al., 2006). Some researchers (Fluckey et al., 2003), however, have reported that Campylobacter numbers were not reduced during air chilling of broiler carcasses. Differing results relative to bacterial contamination of air-chilled carcasses may be due to differences in the type of system applied (e.g., dry air chilling or evaporative chilling), the amount of air circulation, and application of antimicrobials in the chiller air. Cross-contamination may also play a role and has been noted in both air- and immersion-chilling systems (Fries and Graw, 1999; Mead et al., 2000; Smith et al., 2005). The air-chilled method used in the current study best simulates a small-scale static batch method without application of antimicrobials.

In the current study, some skin surface drying was noted on air-chilled carcasses. Lindblad et al. (2006) suggested that such drying may lead to the death of Campylobacter; we had also hypothesized that rinse samples of air-chilled broiler carcasses would have lower numbers of Campylobacter than those from water-chilled carcasses. However, the current data did not support that hypothesis. In fact, the numbers of bacteria detected per milliliter of rinse were lower for immersion-chilled carcass halves than from air-chilled carcass halves. This difference, although statistically significant, was relatively small and could have been due to dilution of the rinse by chiller water or a washing-off effect in the chill tank (Smith et al., 2005).

Unlike Sanchez et al. (2002), we found no evidence that air chilling selected for different antimicrobial resistance in Campylobacter than immersion chilling. Neither did air chilling select for different subtypes of Campylobacter than immersion chilling. Although immersion chilling did result in slightly lower numbers, the difference was not large enough to be microbiologically important. On the basis of these data and under the conditions of our tests, we see no clear microbiological reason to suggest one chilling method over the other.


   ACKNOWLEDGMENTS
 
The authors gratefully acknowledge expert technical assistance by Eric Adams, V. Allan Savage, Lori Fouche, Steven Lyon, and Beth Savage. We further thank Aphrodite Douris for subtyping Campylobacter isolates, analyzing PFGE data, and providing the associated figures.


   FOOTNOTES
 
1 Mention of trade names or commercial products in this publication is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the US Department of Agriculture. Back

Received for publication October 1, 2007. Accepted for publication January 14, 2008.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Allen, V. M., C. H. Burton, J. E. L. Corry, G. C. Mead, and D. B. Tinker. 2000a. Investigation of hygiene aspects during air chilling of poultry carcasses using a model rig. Br. Poult. Sci. 41:575–583.[CrossRef][Web of Science][Medline]

Allen, V. M., J. E. L. Corry, C. H. Burton, R. T. Whyte, and G. C. Mead. 2000b. Hygiene aspects of modern poultry chilling. Int. J. Food Microbiol. 58:39–48.[CrossRef][Web of Science][Medline]

Alter, T., F. Gaull, A. Froeb, and K. Fehlhaber. 2005. Distribution of Campylobacter jejuni strains at different stages of a turkey slaughter line. Food Microbiol. 22:345–351.[CrossRef][Web of Science]

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]

Bilgili, S. F., A. L. Waldroup, D. Zelenka, and J. E. Marion. 2002. Visible ingesta on prechill carcasses does not affect the microbiological quality of broiler carcasses after immersion chilling. J. Appl. Poult. Res. 11:233–238.[Abstract/Free Full Text]

Blank, G., and C. Powell. 1995. Microbiological and hydraulic evaluation of immersion chilling poultry. J. Food Prot. 58:1386–1388.[Web of Science]

Cason, J. A., and M. E. Berrang. 2002. Variation in numbers of bacteria on paired chicken carcass halves. Poult. Sci. 81:126–133.[Abstract/Free Full Text]

Clinical and Laboratory Standards Institute. 2006. Methods for Antimicrobial Dilution and Disk Susceptibility Testing of Infrequently Isolated or Fastidious Bacteria: Approved Guideline. CLSI Doc. M45-A. Clin. Lab. Stand. Inst., Wayne, PA.

Fluckey, W. M., M. X. Sanchez, S. R. McKee, D. Smith, E. Pendleton, and M. M. Brashears. 2003. Establishment of a microbiological profile for an air-chilling poultry operation in the United States. J. Food Prot. 66:272–279.[Web of Science][Medline]

Fries, R., and C. Graw. 1999. Water and air in two poultry processing plants chilling facilities a bacteriological survey. Br. Poult. Sci. 40:52–58.[Web of Science][Medline]

Hunter, S., P. Vauterin, M. Lambert-Fair, M. Van Duyne, K. Kubota, L. Graves, D. Wrigley, T. Barrett, and E. Ribot. 2005. Establishment of a universal size standard strain for use with the PulseNet standardized pulsed-field gel electrophoresis protocol: Converting the national databases to the new size standard. J. Clin. Microbiol. 43:1045–1050.[Abstract/Free Full Text]

Izat, A. L., R. E. Hierholzer, J. M. Kopek, M. H. Adams, and A. Mauromoustakos. 1990. Research note: The use of carcass halves for reducing the variability in Salmonellae numbers with broiler processing trials. Poult. Sci. 69:864–866.[Web of Science][Medline]

Lindblad, M., I. Hansson, I. Va °gsholm, and R. Lindqvist. 2006. Postchill Campylobacter prevalence on broiler carcasses in relation to slaughter group colonization level and chilling system. J. Food Prot. 69:495–499.[Web of Science][Medline]

Mead, G. C., V. M. Allen, C. H. Burton, and J. E. L. Corry. 2000. Microbial cross contamination during air chilling of poultry. Br. Poult. Sci. 41:158–162.[CrossRef][Web of Science][Medline]

Renwick, S. A., W. B. McNab, H. R. Lowman, and R. C. Clarke. 1993. Variability and determinants of carcass bacterial load at a poultry abattoir. J. Food Prot. 56:694–699.[Web of Science]

Sanchez, M. X., W. M. Fluckey, M. M. Brashears, and S. R. McKee. 2002. Microbial profile and antibiotic susceptibility of Campylobacter spp. and Salmonella spp. in broilers processed in air-chilled and immersion-chilled environments. J. Food Prot. 65:948–956.[Web of Science][Medline]

Smith, D. P., M. E. Berrang, and J. A. Cason. 2005. Effect of fecal contamination and cross contamination on numbers of coliform, Escherichia coli, Campylobacter and Salmonella on immersion chilled broiler carcasses. J. Food Prot. 68:1340–1345.[Web of Science][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.[Web of Science][Medline]

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]




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