Isolation and identification of enteropathogenic Campylobacter spp. from chicken samples in Taipei

A total of 95 chicken samples that consisted of 34 whole chickens, 32 organs (gizzards and livers), and 29 chicken parts (drumsticks, wings, and breasts), collected from traditional retail markets (no chilling facilities) and supermarkets in Taipei, were examined for the occurrence of enteropathogenic campylobacters. Three selective media, Peterz's charcoal cefoperazone deoxycholate agar, Campy-Cefex agar, and charcoal-based selective medium, were evaluated for their efficacy to isolate Campylobacter spp. from chicken samples. The results showed that there were no differences among the three media to isolate Campylobacter spp. from all chicken samples (P > 0.05). However, there were markedly different isolation rates of campylobacters between supermarket and retail market (P < 0.05). Enteropathogenic campylobacters (C. jejuni and C. coli) were found on 68% of whole chickens, 100% of chicken parts, and 100% of organs from retail markets. In supermarkets, the isolation rates of these campylobacters from whole chickens, chicken parts, and organs were 42%, 53%, and 60%, respectively. The low isolation rates of the two campylobacters isolated from chicken samples in supermarkets differed statistically from those obtained from traditional retail markets (P < 0.10). The API CAMPY test kit also was evaluated for the identification of Campylobacter spp. as compared with the conventional identification method. The results showed that the API CAMPY test kit (Biomerieux, Marcy-l'Etoile, France) could efficiently detect 87 Campylobacter spp. isolates from chicken samples examined, with 100% agreement at the genus level to 94% at the species level as compared with conventional methods.     

Campylobacter spp. in New Zealand raw sheep liver and human campylobacteriosis cases

Sheep liver samples were tested for the presence and numbers of Campylobacter jejuni and C. coli during both spring and autumn. Over the same period, isolates were obtained from human clinical cases from the same geographical area as where the food samples were purchased. A subset of the C. jejuni isolates was typed by both Penner serotyping and pulsed field gel electrophoresis using the restriction enzyme SmaI, to estimate the proportion of liver isolate types that were also isolated from human cases of campylobacteriosis. Of the 272 liver samples tested, 180 (66.2%) contained Campylobacter. Most of the positive samples contained <3 MPN/g of the organism, and only 12 (6.7%) were contaminated at a level exceeding 100 MPN/g. A total of 180 C. jejuni isolates were obtained from sheep liver and another 200 from human faeces. Of these, 212 isolates were randomly selected for typing, half from raw liver and half from human faeces. More than half (61.1%) of the 106 C. jejuni isolates from liver were of subtypes that were also isolated from human cases. While the C. jejuni present in sheep liver were mostly of subtypes also isolated from human cases, the significance of this food as a vehicle of human campylobacteriosis needs to be examined further in respect to other factors such as dose-response information, consumption data, frequency of undercooking and cross contamination.     

Comparison of different sampling techniques and enumeration methods for the isolation and quantification of Campylobacter spp. in raw retail chicken legs

Comparable quantitative data of Campylobacter spp. on chicken products are a major data lack for quantitative risk assessment approaches. The objective of this study was to compare two different sampling techniques for the isolation and enumeration of Campylobacter spp. in chicken and to evaluate a suitable enumeration method comparing the most probable number (MPN) technique to the direct plating method. For this, 90 packages containing at least two raw chicken legs were examined for the comparison of sampling techniques, rinsing one leg and homogenizing 25 g of skin of the other leg of each package; both sample preparation types were examined by direct plating method and MPN technique in 40 out of 90 packages. Of the skin samples, 70% (63/90), and of the rinse samples, 77% (69/90), were Campylobacter-positive. Enumeration of Campylobacter spp. by direct plating revealed a median of log 4 cfu/leg surface in skin samples (S.D.=0.6) and a median of log 4.3 cfu/leg surface in rinse samples (S.D.=0.9) of the rinse samples; 73% (37/51) had higher numbers of Campylobacter spp. than the skin samples although the difference was not significant (p=0.08). The correlation coefficient of Campylobacter counts in skin and rinse samples was 0.43. The prevalence of Campylobacter spp. in rinse samples was 58% (23/40). In 5% (2/40) of the rinse samples, numbers of Campylobacter spp. could be detected only by the MPN technique due to the lower detection limit compared to the direct plating method. The MPN technique turned out to be unsuitable for the enumeration of Campylobacter spp. in skin samples because a layer formation on the top of the incubated MPN-tubes leads to irregular MPN results. Out of 80% (16/20) of the compared rinse samples, the direct plating detected higher numbers of Campylobacter spp., with a median count of log 4.2 cfu/leg surface (S.D.=1) compared the MPN technique where a median of log 4 cfu/leg surface (S.D.=1.1) was obtained. The difference was not significant (p=0.05). A highly positive correlation coefficient of 0.9 was observed between the direct plating and the MPN technique. Both sampling methods, rinsing the chicken leg and homogenizing the skin, are suitable for the detection and quantification of Campylobacter spp.; the direct plating method was superior to the MPN technique for enumerating Campylobacter spp. in raw chicken legs at retail level because enumeration is more rapid and less laborious.     

Safety assessment of dairy microorganisms: Propionibacterium and Bifidobacterium

Streptococcus suis present in raw pork meats sold in local retail markets was enumerated by Most Probable Number (MPN)-PCR method. This method combined the conventional MPN technique with a specifically designed PCR assay based on the amplification of a 294-bp S. suis species-specific 16S rRNA gene sequence. A total of 78 raw pork lean meat samples purchased at two different supermarkets (Site A and B) and a wet market (Site C) were tested. Results indicated that S. suis could be detected from the enriched MPN tubes of all, except one, sample homogenates. The concentration of S. suis ranged from <3 to 4600 MPN/g of pork meat, with a total bacterial count (TBC) varying from 3.6 log to 7.4 log CFU/g. Statistical analyses indicated that pork meats purchased from the supermarket at Site B in summer contained significantly higher concentration of S. suis organisms than those from other retailers in any season. A significant correlation existed between log S. suis concentration and log TBC of the samples. This study revealed that raw pork meats available in local supermarkets or wet markets could contain S. suis at concentrations that were usually difficult to detect with traditional culture method. Field application of this method may contribute to a measurable evaluation, and thus the effective control, of human S. suis infection due to raw pork or pig carcass handling.     

Microbiological quality of retail imported unprepared whole lettuces: a PHLS Food Working Group Study. Public Health Laboratory Service.

A study of imported unprepared whole lettuces sampled from supermarkets, greengrocers, shops, and market stalls found that all were of acceptable microbiological quality. Twenty-seven out of 151 (18%) imported lettuce samples had Enterobacteriaceae levels of 10(4) CFU/g or more. However, these bacteria that constitute part of the natural microflora of unprepared vegetables may also be derived from the soil and/or by poor handling. The pathogens, Salmonella spp., Shigella spp., Campylobacter spp., Escherichia coli O157:H7, Vibrio cholerae, Listeria monocytogenes, and also Escherichia coli, an indicator of fecal contamination, were not detected in any imported lettuces, indicating that hygiene, harvesting, and production practices were good. Imported lettuces with Enterobacteriaceae levels of 10(4) CFU/g or more varied with type of retail premises and the temperature at which the lettuces were displayed. Samples from greengrocers, shops, and market stalls were more likely to contain Enterobacteriaceae at levels in excess of 10(4) CFU/g than those from supermarkets.     

Prevalence, numbers, and subtypes of Campylobacter jejuni and Campylobacter coli in uncooked retail meat samples

A national quantitative survey of Campylobacter jejuni and Campylobacter coli in 1,011 uncooked retail meat samples (beef, unweaned veal, chicken, lamb and mutton, and pork) was undertaken from August 2003 to June 2004 to establish baseline proportionality data. The presence, number, and type of Campylobacter present in each sample was assessed. Prevalences of C. jejuni and C. coli were 89.1% in chicken, 9.1% in pork, 6.9% in lamb and mutton, 3.5% in beef, and 10% in unweaned veal. C. jejuni was identified in the majority of positive samples (246 of 259). In chicken samples positive for C. jejuni, 40.2% had counts of <0.3 most probable number (MPN)/g, 50.5% had 0.3 to 10.0 MPN/g, 8.8% had 10.1 to 50.0 MPN/g, and 0.5% had 110 MPN/g. In other meats (49 samples), Campylobacter counts were < or = 0.3 MPN/g, except for one unweaned veal sample at > 10.9 MPN/g. Penner serotyping and SmaI macrorestriction genotyping using pulsed-field gel electrophoresis with 247 isolates revealed 17 Penner serotypes and 56 electrophoresis profiles. Seven Penner serotypes (HS1 complex, 2, 4 complex, 6, 11, 27, and 42) were represented by 10 or more isolates from chicken. When data from both typing methods were combined, 62 sero-genotypes were generated. In a comparison of these sero-genotypes with historical data for isolates from human cases, 71% of the beef isolates, 50% of the lamb and mutton isolates, 50% of the pork isolates, 41% of the chicken isolates, and 25% of the unweaned veal isolates were common to both sources. These results provide baseline proportionality profiles of Campylobacter in these five meats and will facilitate exposure assessment in combination with other information such as consumption data and subsequent quantitative risk assessment.     

Occurrence and resistance to antibiotics of Campylobacter jejuni and Campylobacter coli in animals and meat in northeastern Italy

A study was carried out in northeastern Italy during 2000 and 2001 to investigate the occurrence of Campylobacter jejuni and Campylobacter coli in animals, cattle, pigs, and broilers, and raw meat, beef, pork, and chicken. Campylobacter spp. were detected in 53.9% of the cattle, 63.5% of the pigs, and 82.9% of the broilers examined. Chicken meat was frequently contaminated (81.3%), while lower rates were found in pork meat (10.3%) and beef (1.3%). The resistance to antibiotics of the strains was also investigated, and compared to that of human clinical isolates. C. coli was generally more resistant than C. jejuni. Resistance to quinolones was frequently observed in C. coli isolated in chicken meat (78.6%); slightly lower rates were found in C. jejuni isolated in broilers (42.2%), chicken meat (52.8%), and humans (38.2%). C. coli was also frequently resistant to tetracycline in all sources, while resistance to streptomycin was most frequently observed in pig isolates (89.4%).     

Quantification of Campylobacter on the surface and in the muscle of chicken legs at retail

The objective of this study was to determine the prevalence and numbers of Campylobacter on the skin and in the muscle of chicken legs at retail to examine the external and internal contamination for an exposure assessment. Furthermore, the study assessed seasonal influence on Campylobacter contamination in chicken legs. Of the 140 examined skin samples, 66% were positive, and the internal contamination of 115 sampled chicken legs was 27%. The enumeration of Campylobacter on the surface of positive chicken legs revealed a median of 2.4 log CFU/g of skin, and the quantification of Campylobacter in the muscle gave results mainly under the detection limit of the most-probable-number method (<0.3 MPN Campylobacter per g). The external contamination was significantly higher than the internal. In both skin and muscle samples, Campylobacter jejuni had a much higher incidence than Campylobacter coli. However, with regard to the specification of Campylobacter on the surface of chicken legs, C. coli was isolated at higher colony counts than C. jejuni. During the 1-year study, two peaks of Campylobacter contamination occurred, one in the early springtime (February and March, 100 and 90%, respectively) and the second during the warmer months in the summer (July and August, both 90%). Furthermore, a positive correlation between prevalence and numbers of Campylobacter on chicken legs was observed.     

Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from raw chicken meat and human stools in Korea

Prevalence of Campylobacter in raw chicken meat and human stools and subsequent antibiotic resistance profiles of the pathogenic isolates obtained from 2000 through 2002 were investigated. Campylobacter jejuni and Campylobacter coli were isolated from 570 of the 923 raw chicken meat samples collected from traditional markets, large retail stores, or department stores in Korea, resulting in the isolation rate of 61.8%. A total of 579 Campylobacter isolates were obtained from raw chicken (36.3% for C. jejuni and 26.4% for C. coli) with the average population of 335.6 CFU/g. From 513 human stool samples, 15 isolates of Campylobacter were detected. Seasonal variation in the quantification of C. coli was not noticeable throughout the year, while the isolation rate of C. jejuni was the highest in September through October (840 CFU/g) followed by that of July through August and May through June in decreasing order, showing a significant seasonal effect (P < 0.05). Contamination of Campylobacter was more severe in raw chicken meat sold in traditional markets than in those sold in large retail stores and department stores. Prevalence of Campylobacter in raw chicken sold in traditional markets was significantly influenced by seasonal changes (P < 0.05), whereas the samples obtained from other places was less affected by the seasonal changes. Susceptibilities of the 594 chicken isolates to ciprofloxaxin, chloramphenicol, erythromycin, kanamycin, nalidixic acid, and tetracycline were determined by an E-test. Campylobacter isolates were the most resistant to nalidixic acid (91.4%) followed by ciprofloxaxin (87.9%), tetracycline (87.2%), kanamycin (30.6%), erythromycin (19.4%), and chloramphenicol (1.3%). Human isolates showed a similar resistance to the six antibiotics tested. The proportion of Campylobacter isolates with multidrug resistance to four or more antimicrobials obtained from 2000 through 2002 ranged from 28 to 43.5%, indicating that it could be a serious health-threatening factor. This study suggests that it is prudent to establish an effective National Monitoring Program in Korea for the prevention and control of Campylobacter spp.     

Prevalence of Campylobacter, Salmonella, and Escherichia coli on the external packaging of raw meat

During September and October 2002, 3,662 prepackaged raw meat samples were collected to evaluate the extent and nature of microbiological contamination on external surfaces of the packaging, which could potentially cross-contaminate ready-to-eat foods during and after purchase. Salmonella was detected on two (<1%) samples of external packaging (both from raw chicken), and Campylobacter was detected on 41 (1.1%) samples of external packaging. The external packaging of game fowl exhibited the highest Campylobacter contamination (3.6%), followed by raw chicken (3.0%), lamb (1.6%), turkey (0.8%), pork (0.2%), and beef (0.1%); Campylobacter jejuni and Campylobacter coli accounted for 59% (24 of 41) and 24% (10 of 41) of the contaminating Campylobacter species, respectively. C. coli isolates from the external packaging were more multiresistant to antimicrobial drugs, including quinolones such as ciprofloxacin, than was C. jejuni. Escherichia coli (an indicator of fecal contamination) was isolated from the external packaging on 4% of the raw meat samples at levels of 40 to 10(5) CFU per swab. The external packaging of raw meats is a vehicle for potential cross-contamination by Campylobacter, Salmonella, and E. coli in retail premises and consumers' homes. The external surface of heat-sealed packaging was less frequently contaminated with Campylobacter and E. coli compared with other types of packaging (e.g., overwrapping, bag, and tie tape) (P < 0.0001 to 0.01). In addition, external packaging of raw meats was contaminated less frequently with Campylobacter and E. coli when packaging was intact, packaging and display areas were visually clean, display temperatures were below 8 degrees C, and hazard analysis systems were in place.     

Molecular epidemiology and antimicrobial susceptibility of Campylobacter jejuni and Campylobacter coli isolates of poultry, swine, and cattle origin collected from slaughterhouses in Hungary

Campylobacter spp. are the most common cause of bacterial enteritis in Hungary, and the aim of this study was to identify the distribution, genotypes, and antimicrobial susceptibility of Campylobacter species in the most important food-producing animals at the time of slaughter during 2008 and 2009. Of 1,110 samples, 266 were identified as Campylobacter coli (23.9%) and 143 as C. jejuni (12.9%) by real-time PCR. Resistance to enrofloxacin-ciprofloxacin and nalidixic acid was significant, especially in C. jejuni (73.3%) and C. coli (77.2%) from broilers. Higher erythromycin (P = 0.043) and tetracycline (P = 1.865e-14) resistance rates were found among C. coli isolates (9.7 and 74.1%, respectively) than among C. jejuni isolates (3.1 and 36.6%, respectively). A total of 47 fla short variable region sequences were identified among 73 selected C. coli and C. jejuni isolates, with 35 fla types detected only once. At the nucleotide level, fla types A66 and A21 were the most common. Using the pulsed-field gel electrophoresis method, 66% of strains exhibited unique profiles after Sma I digestion. Forty-two isolates assigned to 18 Sma I clusters were further typed by Kpn I, and of these, 24 were assigned to 10 Kpn I clusters. For isolates in five Kpn I clusters, epidemiological links were observed. Stable C. jejuni and C. coli clones were detected, indicating that further studies involving broiler and human isolates need to be conducted to elucidate the importance of these stable clones in human infections.     

Prevalence of Campylobacter species in meat, milk and other food commodities in Pakistan

A surveillance study was carried out to determine the prevalence of Campylobacter in meat, milk and other food commodities in Pakistan. Over a period of 3 years (January 2002-December 2004), a total of 1636 food samples of meat, milk and other food commodities were procured from three big cities of Pakistan (Faisalabad, Lahore and Islamabad) and were analysed. Among meat samples, the highest prevalence (48%) of Campylobacter was recorded in raw chicken meat followed by raw beef (10.9%) and raw mutton (5.1%). Among other food commodities, the highest prevalence was observed in vegetable/fruit salad (40.9%), sandwiches (32%), cheese (11%) and raw bulk milk samples (10.2%). The overall prevalence of Campylobacter was found to be 21.5%, out of which 70.6% were identified as Campylobacter (C.) jejuni and 29.4% as C. coli. The study reported that the prevalence of Campylobacter spp. was significantly higher in the food commodities, which included raw/undercooked ingredients.     

Comparison of eight phenotypic methods for subspecies characterization of thermophilic Campylobacter spp. isolated from pig liver

Four hundred pork livers from bacon pigs (37 herds) obtained at six pig-processing plants were studied to assess the Campylobacter contamination rate. Deep tissue areas were sampled immediately after evisceration. Approximately 6% of livers were infected with Campylobacter spp., including Campylobacter coli (67%), Campylobacter jejuni (30%), and Campylobacter lari (3%). The 60 resulting isolates (39 C. coli isolates, 19 C. jejuni isolates, and 2 C. lari isolates) employed in this study were characterized at the subspecies level in a comparison of eight phenotyping schemes, including four biotyping, two serotyping, and two phage-typing schemes. The Skirrow-Benjamin biotyping scheme produced two biotypes for C. jejuni, i.e., biotype 2 (95%) and biotype 1 (5%). The Lior biotyping scheme subdivided C. coli into biotype 1 (41%) and biotype 2 (59%), while biotype 4 was the dominant type (95%) for C. jejuni. The Roop scheme allowed further differentiation of C. coli into three biovars, i.e., biovar 1 (57%), biovar 2 (40%), and biovar 3 (3%), and it subdivided C. jejuni into two biotypes, i.e., biovar 1 (95%) and biovar 2 (5%). Preston biotyping produced the largest degree of subspecies differentiation, with 18 C. coli biotypes and 7 C. jejuni biotypes being identified. The most common were biotypes 2650 and 6030, representing 18 and 42% of all C. coli and C. jejuni isolates, respectively. The Penner-Hennessy serotyping scheme successfully serotyped 89% of the isolates, with 10 serotypes being identified; 30% of the serotypeable isolates were accounted for by Penner 23, followed by Penner 20 (16%) and Penner 39 (14%). The Lior serotyping scheme successfully serotyped only 45% of the strains, and eight serogroups were identified, with Lior 36 (31%), Lior 20 (23%), and Lior 5 being the most frequent. The Preston scheme and the Khakhria-Lior phage-typing scheme were able to type 16 and 25% of the isolates, respectively. The Preston scheme produced three phage groups, i.e., 69 (56%), 90 (22%), and 116 (22%), and the Khakhria-Lior scheme also produced three phage types, i.e., 44 (40%), 27 (33%), and 37 (20%), as well as atypical lysis patterns (7%). The results of this study demonstrate the role of Preston biotyping in the phenotyping of isolates, particularly in diagnostic laboratories that have no access or limited access to molecular typing equipment.     

Thermal inactivation of Campylobacter species, Yersinia enterocolitica, and hemorrhagic Escherichia coli O157:H7 in fluid milk

Heat treatment of raw milk in an HTST pasteurizer operated at 60.0 to 72.0 degrees C for a minimum holding time of 16.2 s rapidly inactivated mixtures of hemorrhagic Escherichia coli O157:H7, Yersinia enterocolitica and Campylobacter spp. (C. fetus, C. coli, and C. jejuni). Each of the three genera in the mixture was inoculated at a level of approximately 1.0 x 10(5) cfu/ml. At 60.0 degrees C, hemorrhagic E. coli showed a maximum 2 log10 reduction in counts and no viability at greater than or equal to 64.5 degrees C. Yersinia enterocolitica and Campylobacter spp. showed greater heat sensitivity with a 4 log10 reduction in counts at 60.0 degrees C and absence of viable cells at greater than or equal to 63.0 degrees C. These findings reiterate the need for stringent control of thermal processes in the manufacture of dairy products from raw or heat-treated (non-pasteurized) milk.     

PREVALENCE OF THERMOPHILIC CAMPYLOBACTER SPP. IN RETAIL CHICKEN MEAT IN ANKARA

From May to August 2004, 127 samples of chicken meat for sale on the retail market in Ankara were analyzed for the prevalence of thermophilic Campylobacter spp. Campylobacter spp. were isolated from 83.4% of the samples analyzed. Campylobacter jejuni was found in 74.8% of all samples. A total of 364 thermophilic Campylobacter strains were isolated and the species distribution among these strains was 70.1% C. jejuni, 21.1% Campylobacter coli and 8.6% Campylobacter lari. The results obtained from the study indicate that hygienic and technical compliance is needed in all stages of poultry processing to reduce contamination and to prevent public health hazard. An integrated HACCP plan must be applied from the farm to the table for the prevention of C. jejuni infections.     

Effects of pulsed electric fields on pathogenic microorganisms of major concern in fluid foods: a review

Pathogenic microorganisms such as Escherichia coli O157:H7, Salmonella spp., Listeria monocytogenes, Bacillus cereus, Staphylococcus aureus, Yersinia enterocolitica, and Campylobacter jejuni have been implicated in foodborne diseases and outbreaks worldwide. These bacteria have been associated with the consumption of fresh fruit juices, milk, and dairy products, which are foodstuff, highly demanded by consumers in retails and supermarkets. Nowadays, consumers require high quality, fresh-like, and safe foods. Pulsed electric field (PEF) is a non-thermal preservation method, able to inactivate pathogenic microorganisms without significant loss of the organoleptic and nutritional properties of food. The PEF treatment effectiveness to destroy bacteria such as Listeria innocua, E. coli, Salmonella Typhimurium, E. coli O157:H7 and E. coli 8739 at pasteurization levels (> or = 5.0 log(10) cycles) in some fluid foods was reported. However, data on the inactivation of some microorganisms such as Bacillus cereus, Staphylococcus aureus, Yersinia enterocolitica, and Campylobacter jejuni in fluid foods by PEF processing is very limited. Therefore, future works should be focused toward the inactivation of these pathogenic bacteria in real foods.     

Rapid detection of Campylobacter jejuni in chicken rinse water by melting-peak analysis of amplicons in real-time polymerase chain reaction

Five DNA extraction protocols for the detection of Campylobacter spp. by polymerase chain reaction (PCR) were compared. A method involving Triton X-100 produced template DNA of sufficient quality to allow the detection of Campylobacter jejuni at levels of 100 CFU/ml in pure culture. Primers were designed on the basis of the cadF gene sequence. With a SYBR Green I real-time PCR assay, these primers amplified only sequences present in C. jejuni to produce a product with a melting temperature of 81.5 degrees C. None of the strains of Campylobacter coli, Campylobacter lari, or Campylobacter fetus tested produced this product during the PCR assay. Other noncampylobacter species tested were shown not to possess the cadF sequence. The real-time PCR combined with a rapid, simple Triton X-100 DNA extraction protocol made it possible to detect < 10 CFU of C. jejuni per ml of chicken rinse within 14 h.     

Metronidazole resistance in Campylobacter jejuni from poultry meat

The occurrence of metronidazole resistance was investigated among Campylobacter jejuni in raw poultry meat collected from supermarkets. MICs were determined by the agar dilution procedure in the testing range of 3 to 60 microg/ml metronidazole. The MICs showed a bimodal distribution with a significant proportion of metronidazole-resistant isolates among C. jejuni from raw broiler and turkey meat. Metronidazole resistance occurred most frequently among turkey meat isolates (P < 0.005). This is the first report of foodborne bacteria carrying metronidazole resistance.     

Effect of temperature on viability of Campylobacter jejuni and Campylobacter coli on raw chicken or pork skin

To determine growth and survival of Campylobacter jejuni and Campylobacter coli on chicken and pork, Campylobacter spp. (10(4) CFU/cm2) were inoculated on pieces of raw, irradiated chicken or pork skin and exposed to temperatures ranging from -20 to 42 degrees C under either microaerobic or aerobic conditions. Viable counts over 48 h declined 2 to 3 log CFU/cm2 at -20 degrees C and 1 to 2 log CFU/cm2 at 25 degrees C regardless of skin type, species of Campylobacter, or level of oxygen. At 4 degrees C, there was no significant change in the number of Campylobacter over 48 h. At both 37 and 42 degrees C, the number of viable Campylobacter increased significantly (2 to 3 log CFU/cm2, P < 0.0001) under microaerobic conditions but decreased 0.5 to 1.5 log CFU/cm2 in air. Preincubation of skins for 24 h at 42 degrees C under microaerobic conditions to establish Campylobacter on the surface prior to lowering the temperature to -20, 4, or 25 degrees C and incubating in air resulted in a decline in viability for the first 4 h (0.5 to 1 log CFU/cm2). However, after this initial drop in viability, no additional effect on viability was observed compared with incubation at -20, 4, or 25 degrees C in air without microaerobic preincubation at 42 degrees C. Preincubation of inoculated skins at -20, 4, or 25 degrees C in air for 24 h followed by a shift in temperature to 42 degrees C for 4, 8, 24, or 48 h and a shift to microaerobic conditions resulted in an overall decline in viability on raw pork skin but not on raw chicken skin. In contrast, preincubation of inoculated skins at -20, 4, or 25 degrees C for 24 h in air followed by a shift in temperature to 37 degrees C and microaerobic conditions did not result in a decrease in viable counts for either chicken or pork skins. Overall, viability of C. coli and C. jejuni on chicken and pork skins was similar. Therefore, a lower incidence of Campylobacter spp. in pork than in poultry postslaughter, despite a similar prevalence in live animals, is not due to differences in viability of C. coli versus C. jejuni on raw chicken or pork skin.     

Incidence of Salmonella, Campylobacter jejuni, Campylobacter coli, and Listeria monocytogenes in poultry carcasses and different types of poultry products for sale on the Belgian retail market.

From January 1997 to May 1998, 772 samples of poultry carcasses and poultry products for sale on the retail market in Belgium were analyzed for the presence of Salmonella spp., Salmonella Enteritidis, Campylobacter jejuni, C. coli, and Listeria monocytogenes per 100 cm2 or 25 g. Poultry samples were contaminated with Salmonella (36.5%), C. jejuni and C. coli (28.5%), and L. monocytogenes (38.2%). In about 12.3% of the poultry samples, the L. monocytogenes contamination level exceeded 1 CFU per g or cm2. Significant differences in pathogen contamination rates of poultry products were noticed between the poultry products originating from Belgian, French, and U.K. abattoirs. Poultry products derived from broiler chickens running free in pine woods until slaughtering age (12 to 13 weeks) had a significantly (P < 0.05) lower contamination rate of Salmonella than poultry products from enclosed broilers slaughtered at the age of 6 to 8 weeks. A significantly (P < 0.05) lower pathogen contamination rate was noted for Salmonella, C. jejuni, and C. coli for poultry cuts without skin compared to poultry cuts with skin on. An increase in pathogen contamination rate was noticed during cutting and further processing. To diminish C. jejuni, C. coli, Salmonella, and L. monocytogenes contamination rates, hygienic rules of slaughter and meat processing must be rigorously observed. At the moment, zero tolerance for these pathogens is not feasible, and there is a need to establish criteria allowing these pathogens to be present at reasonable levels in the examined poultry samples.