Occurrence and genotypes of Campylobacter in broiler flocks, other farm animals, and the environment during several rearing periods on selected poultry farms

On 15 Swiss poultry farms, broiler flocks, other farm animals, and the environment were examined during consecutive rearing periods to investigate the occurrence and genetic diversity of Campylobacter. Of the 5154 collected samples, 311 (6%) from 14 farms were Campylobacter positive by culture. Amongst the positive samples, 228 tested positive for Campylobacter jejuni and 92 for Campylobacter coli. Positive samples originated from broilers, the broiler houses, cattle, pigs, bantams, laying hens, a horse, and a mouse. Feed, litter, flies, and the supply air to the broiler house tested negative. By flagellin gene typing (fla-RFLP) and pulsed-field gel electrophoresis (PFGE), 917 Campylobacter isolates were genotyped. Additionally, amplified fragment length polymorphism (AFLP) analysis was performed on 15 assorted strains. On eight farms, matching genotypes were isolated from broiler flocks and other farm animals: Certain genotypes from cattle (farms H, K, L, and M), pigs (farms D and P), or laying hens (farm L) were subsequently found in the broiler flocks, whereas other genotypes initially present in the broiler flocks turned up in cattle (farms A, D, and O). These results emphasize the importance of other farm animals on poultry farms for broiler flock colonization. Indications of persistent contamination of the broiler house were evident on four farms (C, D, I, and L) where matching genotypes were detected in consecutive broiler flocks, but not concurrently in other samples. By fla-RFLP, PFGE, and confirmed by AFLP, some genotypes proofed to be identical across different farms.     

Distribution of Campylobacter spp. in selected U.S. poultry production and processing operations.

A study was conducted of 32 broiler flocks on eight different farms, belonging to four major U.S. producers. The farms were studied over I complete calendar year. Overall, 28 (87.5%) of the flocks became Campylobacter positive, and only four (12.5%) remained negative throughout the 6- to 8-week rearing period. In the majority of flocks, sampled every 2 weeks throughout production, Campylobacter-positive fecal and cecal samples were not detected until 4 to 8 weeks of age. In only six of the flocks were environmental samples found to be positive before shedding of Campylobacter was detected in the birds. Even in some of the Campylobacter-negative flocks, contamination of the rearing environment was positive for Campylobacter but did not result in the birds subsequently excreting the organism. These findings are discussed in relation to U.S. husbandry practices and present uncertainty about sources of Campylobacter infection for poultry flocks. Birds were often transported to the processing plant in coops that were already contaminated with Campylobacter, and the organisms were sometimes found in samples of scald water and chill water. After chilling, the proportions of Campylobacter-positive carcasses from different producers ranged from 21.0 to 40.9%, which is lower than in other studies, and possible reasons are considered.     

The effects of Campylobacter numbers in caeca on the contamination of broiler carcasses with Campylobacter

For the presence and number of Campylobacter, 18 broiler flocks were sampled over a period of 18 months. A total of 70% of the flocks were positive for Campylobacter, with higher prevalence found in summer and autumn, compared to winter and spring. Positive flocks showed contamination rates above 90%, in negative flocks this was lower, mostly below 50%. The enumeration showed a decrease in Campylobacter during processing of positive flocks. The numbers were highest in carcasses after scalding/defeathering (mean 5.9 log(10) cfu/carcass) and dropped by 0.7 log(10) cfu/carcass after chilling. A positive correlation was observed between the number of Campylobacter present in the caeca and the number of bacteria present on carcasses and cut products. When a negative flock was slaughtered after Campylobacter positive flocks, the number of positive samples was higher compared to the case when a negative flock had been slaughtered previously. C. jejuni was isolated from 73.6% of the poultry samples.     

Pre-harvest surveillance of Campylobacter and Salmonella in Danish broiler flocks: a 2-year study.

In national surveillance programmes of broiler flocks carried out in Denmark during 1998 and 1999, 89,110 samples for Campylobacter representing 8911 broiler flocks were taken at 10 different abattoirs, and 44,550 samples for Salmonella were taken from the same flocks in the broiler houses at the farms. Of the swabs, 42.5% were Campylobacter positive. Most positive samples were found during July, August and September, while the lowest number of positive samples were found during January, February, March and April. Of the flocks, 5.5% were Salmonella positive, but no seasonal variation was observed. For each flock, the presence of Campylobacter and Salmonella was recorded in order to estimate the possible correlation between colonisation with the two pathogens. In conclusion, no significant effects on intensive cleaning and disinfection procedures on Campylobacter occurrence could be demonstrated, and no significant correlation between occurrence of Campylobacter and Salmonella infections in Danish broilers could be demonstrated which is in contrast to previous observations on concurrent colonisation of broilers with these two zoonotic pathogens.     

Use of MIDI-fatty acid methyl ester analysis to monitor the transmission of Campylobacter during commercial poultry processing

The presence of Campylobacter spp. on broiler carcasses and in scald water taken from a commercial poultry processing facility was monitored on a monthly basis from January through June. Campylobacter agar, Blaser, was used to enumerate Campylobacter in water samples from a multiple-tank scalder; on prescalded, picked, eviscerated, and chilled carcasses; and on processed carcasses stored at 4 degrees C for 7 or 14 days. The MIDI Sherlock microbial identification system was used to identify Campylobacter-like isolates based on the fatty acid methyl ester profile of the bacteria. The dendrogram program of the Sherlock microbial identification system was used to compare the fatty acid methyl ester profiles of the bacteria and determine the degree of relatedness between the isolates. Findings indicated that no Campylobacter were recovered from carcasses or scald tank water samples collected in January or February, but the pathogen was recovered from samples collected in March, April, May, and June. Processing generally produced a significant (P < 0.05) decrease in the number of Campylobacter recovered from broiler carcasses, and the number of Campylobacter recovered from refrigerated carcasses generally decreased during storage. Significantly (P < 0.05) fewer Campylobacter were recovered from the final tank of the multiple-tank scald system than from the first tank. MIDI similarity index values ranged from 0.104 to 0.928 based on MIDI-fatty acid methyl ester analysis of Campylobacterjejuni and Campylobacter coli isolates. Dendrograms of the fatty acid methyl ester profile of the isolates indicated that poultry flocks may introduce several strains of C. jejuni and C. coli into processing plants. Different populations of the pathogen may be carried into the processing plant by successive broiler flocks, and the same Campylobacter strain may be recovered from different poultry processing operations. However, Campylobacter apparently is unable to colonize equipment in the processing facility and contaminate broilers from flocks processed at later dates in the facility.     

Detection and diversity of various Arcobacter species in Danish poultry

The prevalence and diversity of different Arcobacter spp. in various poultry species in Denmark were investigated using cultural and multiplex PCR methods. A pool of three fresh droppings obtained at the production site from 70 broiler chicken flocks aged 4-5 weeks was examined. In addition, pools of 10 cloacal swabs taken at the abattoir prior to stunning from each of 15, and 37 duck and turkey flocks, respectively, were analyzed. Thirty fresh broiler chicken carcasses and 29 cloacal swabs from the respective viscera were also examined at the abattoir. Finally, 10 caecal and 10 cloacal swabs from ducks at the abattoir were analyzed individually. In total, 85 Arcobacter isolates were obtained. Of these 45, 20 and 7 were identified as Arcobacter butzleri, Arcobacter cryaerophilus and Arcobacter skirrowii, respectively, using a multiplex PCR. Interestingly, some chicken isolates of A. butzleri showed urease activity, and 6 out of seven A. skirrowi isolates were unable to hydrolyse indoxyl acetate. All chicken carcasses examined were found positive for A. butzleri and/or A. cryaerophilus, whereas 21 (72%) of the 29 chicken cloacal swabs were positive for either A. butzleri (13) or A. cryaerophilus (9). Three (4.3%) out of 70 chicken flocks analyzed were positive only for A. cryaerophilus. Of the ten ducks examined individually, 7 carried A. skirrowii and/or A. cryaerophilus in their cloacae. None of the respective caecal samples were positive. Of the remaining 15 duck flocks, 11 (73%) were positive for A. cryaerophilus (7), A. butzleri (2) or A. skirrowii (2). Four (11%) of the 37 turkey flocks analyzed harboured either A. butzleri or A. cryaerophilus. The carriage rate of Arcobacter was higher in live ducks than those of live broiler chickens and turkeys in the present study. In addition, chicken carcasses slaughtered in Denmark were found to be contaminated with Arcobacter. The presence of Arcobacter spp. both on chicken carcasses and in poultry intestine may be of significance to human health.     

Reduction in flock prevalence of Campylobacter spp. in broilers in Norway after implementation of an action plan

An action plan against thermophilic Campylobacter spp. in Norwegian broilers was implemented in May 2001. The action plan consists of three parts: a surveillance program including all Norwegian broiler flocks slaughtered before 50 days of age, a follow-up advisory service on farms delivering flocks positive for Campylobacter spp., and surveys of broiler meat products at the retail level. This article presents results covering the inclusive 3-year period between 2002 and 2004. During this period, a total of 10,803 flocks from 562 broiler farms were tested; altogether, 521 (4.8%) of the flocks were identified as positive for Campylobacter spp., primarily Campylobacter jejuni. The positive flocks originated from 257 (45.7%) of the farms. During the period 2002 to 2004, there was a large and steady reduction in flock prevalence, from 6.3% in 2002 to 3.3% in 2004. Also, the proportion of farms producing flocks positive for Campylobacter spp. each year reduced substantially, from 28.4% in 2002 to 17.8% in 2004. The proportion of flocks positive for Campylobacter spp. varied considerably with season and region. The action plan is a successful collaboration between academia, regulatory agencies, and the poultry industry that has resulted in a significant reduction in the number of broiler carcasses positive for Campylobacter spp. on the market. The temporal associations between implementation of the control program and the drop in the number of infected chickens and contaminated carcasses indicate that this collaborative action plan has been instrumental in achieving the goals of enhancing food safety.     

Prevalence of Listeria monocytogenes in poultry production in France

This study aimed to update and create a data set from laying hens and broilers regarding contamination by Listeria monocytogenes. Two hundred laying-hen flocks were sampled, with 88 flocks reared in cages and 112 reared on the floor. One hundred forty-five broiler flocks were sampled, with 85 conventional and 60 free-range flocks. A total of 774 and 725 samples were analyzed from laying hens and broilers, respectively. L. monocytogenes was detected in 31 of 200 flocks, yielding an estimated prevalence of 15.5% in laying-hen flocks. Among positive flocks, there appeared a significant (P = 0.004) difference between caged and floor-reared hens, with a higher detection in dust samples from floor-reared hens. In positive caged hen flocks, significant (P = 0.028) differences between dust and fecal samples appeared, with a higher detection in feces than in dust samples. In broiler flocks, L. monocytogenes was isolated in 46 of 145 flocks, yielding an estimated prevalence of 32% (28% in conventional flocks versus 37% in the free-range flocks). L. monocytogenes was isolated in samples taken from conventional flocks with a lower frequency than in free-range flocks (13 versus 18%, respectively). The serotyping of L. monocytogenes strains showed that the majority belonged to type 1/2a in laying-hen flocks (74.3%) and in broiler flocks (40.5%). A significant difference (P = 0.007) between laying hens and broilers was shown for serogroup 4 and for serovar 1/2b (P = 0.007); these serogroups were more prevalent in broilers (40%) than in laying hens (5.7%).     

Prevalence and comparison of genetic profiles of Campylobacter strains isolated from poultry and sporadic cases of campylobacteriosis in humans.

Between July 1998 and June 1999, 93 lots of broiler chickens distributed on 57 farms were sampled in two abattoirs of the province of Quebec (Canada). A total of 2,325 samples of cecal material were analyzed to determine the prevalence of campylobacters. Biotyping and pulsed-field gel electrophoresis (PFGE) were done on 20% of the Campylobacter isolates to study the distribution within poultry production. Macrorestriction profiles were compared with profiles of 24 Campylobacter strains isolated from sporadic cases of human diarrheic patients in order to evaluate genetic relationships. Approximately 40% of the broiler chickens in 60% of the lots and 67% of the farms were colonized. Biotypes I and II of Campylobacter jejuni were the most prevalent biotypes in poultry and human isolates. The PFGE dendograms revealed a high genetic diversity among poultry isolates, with 49 different genotypes from the 56 positive lots. More than 75% of these lots were colonized by a unique genotype. All positive lots raised simultaneously on the same farm had common genotype(s). Different genotypes were isolated from lots raised at different grow-out periods on a farm. In some cases, identical genotypes were found at different grow-out periods on a farm and also from different farms. Macrorestriction profiles showed that approximately 20% of human Campylobacter isolates were genetically related to genotypes found in poultry. This genetic relationship and the high prevalence of C. jejuni biotypes I and II in poultry indicated that Campylobacter in broiler production of the province of Quebec could be a potential source of hazard for public health.     

Resistance patterns of Campylobacter spp. strains isolated from poultry carcasses in a big Swiss poultry slaughterhouse

The aim of this study was to determine resistance patterns of strains of Campylobacter spp. isolated from poultry carcasses in one of the two big Swiss poultry slaughterhouses. A variety of antibiotics with clinical relevance in human and/or in veterinary medicine was tested. In addition, the results of the disc diffusion method, E-test and microdilution broth methods were compared. Of the 195 Campylobacter jejuni strains isolated from 195 poultry carcasses from 21 flocks, 134 strains were susceptible in vitro to all tested antibiotics. Sixty-one strains (31.3%, from eight flocks) showed resistance. Forty-one strains were resistant to a single antibiotic-34 to streptomycin, 6 to ampicillin and 1 to ciprofloxacin. Eighteen strains (from two flocks) showed combined resistance to erythromycin and streptomycin, two strains to ciprofloxacin and streptomycin. None of the isolates was resistant to tetracycline. The data of this first study in Switzerland show a favourable resistance situation for C. jejuni strains against erythromycin, tetracycline and ciprofloxacin. The disc diffusion method was found to be a reliable and easy tool for monitoring the prevalence of resistant C. jejuni strains. For surveillance of changes in the susceptibility concentration levels to antimicrobial agents, however, a MIC method should be used. Further investigations along the whole poultry production chain (farm, slaughterhouse and retail levels) are now necessary in order to confirm the resistance situation.     

Campylobacter contamination during poultry slaughter in Belgium

The relation between internal carriage and surface contamination with thermophilic Campylobacter species in broilers was examined by molecular typing methods. Samples from 39 flocks were collected in three Belgian poultry slaughterhouses. From each flock, crop swabs before slaughter and intestines and neck skins during slaughter were collected. A total of 309 isolates were identified at species level and further characterized by flagellin gene A PCR/restriction fragment length polymorphism and pulsed-field gel electrophoresis. Isolates were identified as Campylobacter jejuni (90%), Campylobacter coli (8.7%), and Campylobacter lari (2.2%), and 27 genotypes could be distinguished by combining the two molecular methods. Seventy-two percent of the flocks arriving at the abattoir were colonized with campylobacters. After slaughter, 79% of the flocks had contaminated neck skins. In six flocks, genotypes isolated from the neck skins were also found in the alimentary tract from previously slaughtered flocks. Four of these flocks were initially free of Campylobacter. These four flocks might have had no contaminated carcasses after logistic slaughtering.     

Counts of Campylobacter spp. on U.S. broiler carcasses

Foodborne Campylobacter-associated gastroenteritis remains a public health concern, and the Centers for Disease Control and Prevention suggests that improperly handled poultry is the most important source of this human disease. In response to these concerns, 10 of the largest U.S. poultry integrators cooperatively determined the incidence and counts of Campylobacter on processed broiler carcasses. Prior to conducting the survey, laboratory personnel were trained in a direct Campy-Cefex plating procedure for enumeration of the organism. Before and after the survey enumeration, consistency in reporting was compared among the participating laboratories. Participating laboratories were able to consistently estimate inoculated concentrations of Campylobacter in carcass rinses. Within the central study, we determined the potential exposure of U.S. consumers to Campylobacter spp. associated with broiler carcasses during a 13-month period. Among each of the 13 participating poultry complexes, rinses from 25 randomly selected fully processed carcasses were sampled monthly from individual flocks. Among 4200 samples, approximately 74% of the carcasses yielded no countable Campylobacter cells. Campylobacter spp. were isolated from approximately 3.6% of all commercially processed broiler carcasses at more than 10(5) CFU per carcass. Acceptable counts of these organisms on raw poultry carcasses remain to be determined. Nevertheless, this survey indicates industry recognition of its responsibility to assess and reduce public exposure to Campylobacter through broiler chickens.     

Contamination of carcasses with Salmonella during poultry slaughter

Successively slaughtered poultry flocks were sampled for Salmonella to study the relationship between gastrointestinal colonization of the birds and contamination of the carcasses after slaughter. Samples from 56 broiler flocks and 16 spent layer and breeder flocks were collected in six slaughterhouses. Salmonella isolates were serotyped and further characterized by pulsed-field gel electrophoresis (PFGE). Although only 7 (13%) broiler flocks were colonized with Salmonella at slaughter, carcasses of 31 (55%) broiler flocks were contaminated after slaughter. Concerning the layer and breeder flocks, 11 (69%) flocks were colonized in the gastrointestinal tract, but after slaughter, carcasses of all flocks were contaminated. The Salmonella status determined at the farm did not always correlate to the status at slaughter. On the other hand, the slaughter of Salmonella-colonized flocks did not always result in the contamination of the carcasses with the same PFGE types isolated from the gastrointestinal tract. When only uncolonized flocks were slaughtered, the carcasses of flocks were on some occasions still contaminated with Salmonella. This indicates possible cross-contamination from the slaughter equipment or transport crates. These observations show that it is difficult to reach the benefits of logistic slaughter in commercial poultry slaughterhouses.     

Development of a new protocol for the isolation and quantification of Arcobacter species from poultry products.

None of the presently available selective supplements for the specific isolation of Arcobacter species allows the growth of Arcobacter butzleri, A. cryaerophilus and A. skirrowii and at the same time fully suppresses the accompanying flora present in poultry and poultry products. Furthermore, little is known about the contamination levels of poultry with Arcobacter species. In this study, a new selective supplement comprising amphotericin B (10 mg/l), cefoperazone (16 mg/l), 5-fluorouracil (100 mg/l), novobiocin (32 mg/l) and trimethoprim (64 mg/l) was developed. With a new isolation procedure, including enrichment in Arcobacter broth with the selective supplement, incubated for 24 to 48 h at 28 degrees C under microaerobic conditions, arcobacters were isolated from 100% (n = 34) of neck skin of laying hens and from 90% (n = 71) of similar samples from broilers. Of the broiler breast meat samples examined (n = 52), 65% were found to be contaminated with these bacteria. In 64% of the samples, A. butzleri was the only Arcobacter species isolated. In 9% of the samples, A. cryaerophilus was the only species present, while 11% of the samples were positive for both species simultaneously. Using direct isolation on the selective agar medium developed in this study, incubated for 24 to 48 h under microaerobic conditions at 28 degrees C. 32 out of 45 broiler carcasses and 6 out of 25 broiler breast meat samples carried a bacterial load of arcobacters of 10(2) to 10(3) cfu/g. The prevalence of Arcobacter in Belgian poultry was found higher than the prevalence of thermophilic Campylobacter species in each of the poultry categories examined. The enrichment procedure and the direct plating method were validated for the isolation of A. skirrowii. For this species, growth performance was less than the other two Arcobacter species and it was not isolated nor detected by m-PCR from the naturally contaminated poultry samples examined. This new protocol provides a fast and reliable method for the isolation of Arcobacter species from poultry and can contribute to more comprehensive epidemiological investigations.     

Contamination of meat with Campylobacter jejuni in Saitama, Japan.

To determine the source of food contamination with Campylobacter jejuni, we investigated retail meat, a chicken processing plant and a broiler farm. C. jejuni was found in domestic retailed poultry (45.8%) and imported poultry (3.7%), but not in beef or pork. In the poultry processing plant, there is significant contamination with C. jejuni in chicken carcasses, equipment and workers' hands. This contamination increases during the defeathering and evisceration processes. RAPD analysis shows that contamination with C. jejuni is of intestinal origin. In a broiler farm, C. jejuni was first isolated from a faecal sample of broiler chicken after the 20th day of age. Two weeks later, all birds in this farm became C. jejuni positive. RAPD analysis indicated that C. jejuni spread rapidly from one broiler flock to the other flocks on the farm.     

Prevalence and characterization of Campylobacter jejuni isolated from pasture flock poultry

The growing interest in organic and natural foods warrants a greater need for information on the food safety of these products. In this study, samples were taken from 2 pasture flock farms (N = 178; feed, water, drag swabs, and insect traps), pasture flock retail carcasses (N = 48) and 1 pasture flock processing facility (N = 16) over a period of 8 mo. A total of 105 Campylobacter isolates were obtained from 53 (30%), 36 (75%), and 16 (100%) samples from the farms, retail carcasses, and processing facility, respectively. Of the 105 isolates collected, 65 were C. jejuni, 31 were C. coli, and 9 were other Campylobacter spp. Using PCR, the C. jejuni isolates were further analyzed for virulence genes involved in colonization and survival (flaA, flaC, cadF, dnaJ, racR, cbrR), invasion (virB11, ciaB, pldA), protection against harsh conditions (sodB, htrA, clpA), toxin production (cdtA, cdtB, cdtC), siderophore transport (ceuE), and ganglioside mimicry (wlaN). In addition, the short variable region of the flaA locus (flaA SVR) was sequenced to determine the genetic diversity of the C. jejuni isolates. The flaA SVR diversity indices increased along the farm to carcass continuum. PCR-based analysis indicated a low prevalence of 5 genes involved in colonization (dnaJ, ciaB, pldA, racR, virB11). The results of this survey indicate that the prevalence of Campylobacter on organic retail carcasses is similar to prevalence reports of Campylobacter on conventional retail carcasses. However, the genetic diversity of the flaA SVR genotypes increased along the farm to carcass continuum that contrasted with conventional poultry studies. PRACTICAL APPLICATION: Campylobacter jejuni is a leading cause of foodborne illness with poultry and poultry products being leading sources of infection. Free-range and pasture flock chickens are becoming more popular; however, there is an inherent biosecurity risk that can increase the prevalence of foodborne pathogens in these flocks. This study aimed to determine sources and characterize C. jejuni isolated from pasture flocks.     

PCR assay for the detection of Campylobacter in marinated and non-marinated poultry products

During a period of 9 months, 194 marinated and non-marinated poultry products were collected from retail shops in a defined area in Western Finland and tested for Campylobacter spp. using a conventional enrichment culture and Polymerase Chain Reaction (PCR) method. For marinated poultry products, the study involved modification of a commercial DNA isolation method. Using either a conventional culture or PCR method, a total of 25 (12.9%) of all investigated samples were Campylobacter positive. In marinated poultry products, Campylobacter was detected at a prevalence of 21.1% and 9.5% in turkey and chicken products, respectively. In August, there was a peak with 28.9% positive Campylobacter samples. Campylobacter inoculation tests were carried out to test the detection limit of both methods. The PCR method used is faster than microbiological analyses. However, enrichment of the samples is necessary due to the low occurrence of Campylobacter spp. in retail Finnish poultry products.     

Enumeration of Campylobacter spp. in broiler feces and in corresponding processed carcasses

Twenty north Georgia commercial flocks of broiler chickens sampled in 1995 and 11 flocks sampled in 2001 were tested for Campylobacter spp. Direct plating on Campy-Cefex agar was carried out to determine levels of Campylobacter colonization within each flock through the enumeration of the organism in 50 fresh fecal samples 1 day prior to slaughter. The next morning, these flocks were the first to be processed, and levels of the organism per carcass before the chilling operation (50 carcasses per flock) in 2001 and after the chilling operation (50 carcasses per flock) in both 1995 and 2001 were estimated. Levels of the organism on freshly processed broiler carcasses were estimated by the same methods in 1995 and 2001, and a significant reduction from an average of 10(4.11) CFU per carcass in 1995 to an average of 10(3.05) CFU per carcass in 2001 was observed. Levels of Campylobacter spp. found in production and in processing were not strongly correlative, indicating the existence of complex parameters involving production factors and variables associated with flock transport and the processing of the broilers. The reduction in Campylobacter levels on processed carcasses may have contributed to the reduction in the frequency of human disease observed by the Centers for Disease Control during the same period. These data characterize the distribution of Campylobacter in north Georgia poultry operations and should assist in the development of risk assessment models for Campylobacter spp. The results obtained in this study suggest that the implementation of antimicrobial interventions by the poultry industry has already reduced consumer exposure to the organism.     

Evaluation of logistic processing to reduce cross-contamination of commercial broiler carcasses with Campylobacter spp

Cross-contamination of broiler carcasses with Campylobacter is a large problem in food production. Here, we investigated whether the contamination of broilers carcasses from Campylobacter-negative flocks can be avoided by logistic scheduling during processing. For this purpose, fecal samples were collected from several commercial broiler flocks and enumerated for Campylobacter spp. Based on enumeration results, flocks were categorized as Campylobacter negative or Campylobacter positive. The schedule of processing included the testing of Campylobacter-positive flocks before or after the testing of Campylobacter-negative flocks. During processing, flocks were also sampled for Campylobacter spp. before and after chilling. Campylobacter strains were identified with multiplex PCR and analyzed for relatedness with pulsed-field gel electrophoresis. Our results show that Campylobacter-negative flocks were indeed contaminated with Campylobacter strains originating from previously processed Campylobacter-positive flocks. Campylobacter isolates collected from carcasses originating from different farms processed on the same day showed similar pulsed-field gel electrophoresis patterns, confirming cross-contamination. These findings suggest that a simple logistic processing schedule can preserve the Campylobacter-negative status of broiler carcasses and result in products with enhanced food safety.     

The effect of slaughter operations on the contamination of chicken carcasses with thermotolerant Campylobacter

To evaluate the effect of specific slaughter operations on the contamination of broiler carcasses with naturally occurring thermotolerant Campylobacter, experiments were carried out in two Danish commercial slaughter plants (Plant I and Plant II). Six broiler flocks determined Campylobacter positive prior to slaughter were investigated at four sampling locations within each slaughter plant. Quantification of thermotolerant Campylobacter in 30 neck skin samples per flock per sampling location showed that the evisceration operation in Plant I led to a significant increase in the Campylobacter concentration of 0.5 log(10) cfu/g in average, whereas no significant changes were observed during this operation in Plant II. Air chilling (Plant I) and water chilling (Plant II), both including a carcass wash prior to the chilling operation, caused similar, but significant reductions of 0.83 and 0.97 log(10) cfu/g, respectively. In packed frozen chickens (Plant II) an additional reduction of 1.38 log(10) cfu/g in average was obtained due to the freezing operation. In packed chilled chickens (Plant I), however, the number of thermotolerant Campylobacter per gram remained at the same level as after air chilling. Enumeration of thermotolerant Campylobacter in 30 intestinal samples per flock showed that in two of the six flocks examined the within flock colonization was very low (<3% and 27% positive samples). The remaining four flocks were colonized at percentages of 100 (three flocks) and 97 (one flock) and had intestinal mean counts ranging from 6.65 to 8.20 log(10) cfu/g. A correlation between Campylobacter concentrations in intestinal content and on chicken carcasses after the defeathering operation was documented. This finding indicates that a reduction in the Campylobacter concentration on chicken carcasses may also be obtained by interventions aimed at reducing the concentration of Campylobacter in the intestines of the living birds.