Campylobacter succession in broiler chickens

The competitive ability of Campylobacter coli OR12 over C. jejuni OR1 has been examined in experimental broiler chickens following the observation that C. coli replaced an established C. jejuni intestinal colonisation within commercial chicken flocks reared outdoors [El-Shibiny, A., Connerton, P.L., Connerton, I.F., 2005. Enumeration and diversity of campylobacters and bacteriophages isolated during the rearing cycles of free-range and organic chickens. Appl. Environ. Microbiol. 71, 1259-1266]. Co-cultures of C. coli OR12 with C. jejuni OR1, revealed that the two species were able to grow together at similar growth rates in exponential growth phase but if the disparity of the inoculum ratios were >log(10)4 in favour of C. coli OR12, C. jejuni OR1 was observed to prematurely enter decline phase. Chickens were pre-colonised with C. jejuni OR1 at 21-days-old to examine succession in vivo. The birds were inoculated between 2 and 12 days later with C. coli OR12, to determine if the second isolate could efficiently colonise and compete with an established C. jejuni strain. C. coli OR12 were able to co-colonise before replacing C. jejuni OR1 as the dominant species when the birds were more than 27 days of age at the time of administration over a 4-day period. If these criteria were met C. coli OR12 became the dominant isolate otherwise co-colonisation occurred until they were met. C. coli OR12 was also found to displace three alternative C. jejuni strains from pre-colonised chickens challenged with C. coli OR12 at 30 days of age and tested at 40 days. These data raise the possibility of manipulating populations of Campylobacter colonising chickens through competition.     

Colonisation phenotype and colonisation potential differences in Campylobacter jejuni strains in chickens before and after passage in vivo

Campylobacter jejuni strains isolated from chicken faeces and from humans suffering from gastroenteritis were used to determine the colonisation phenotypes and colonisation potential of these strains in chickens. Five different colonisation types were observed ranging from immediate and sustained colonisation to completely non-colonising. Phenotype one showed immediate colonisation with prolonged excretion of viable C. jejuni bacteria. Phenotype two showed delayed colonisation with prolonged excretion of viable C. jejuni bacteria. Phenotype three showed immediate colonisation and delayed clearing of viable C. jejuni bacteria. Phenotype four showed delayed colonisation and delayed clearing of viable C. jejuni bacteria. Strains of phenotype five could not colonise chickens. Inoculum levels to obtain maximum caecal colonisation for each phenotype for strains cultured in vitro and in vivo was also determined. Following passage in vivo through a chicken, the minimum inoculum required for sustained colonisation dropped approximately 1000-fold, however, the colonisation phenotype remained unchanged before and after a passage in vivo.     

Detection of Campylobacter jejuni strains in the water lines of a commercial broiler house and their relationship to the strains that colonized the chickens

Campylobacter jejuni is frequently present in the intestinal tract of commercial broiler chickens, and their drinking water has been proposed to be an initial source of bacteria for newly hatched chicks. We studied three sequential commercial broiler flocks raised in a house from which we had cultured C. jejuni from the nipple waters prior to placement of the first flock. Campylobacter cells were detected by immunofluorescence in the biofilm of the drinking nipples during the weeks when the flock was colonized with C. jejuni but not during weeks when the birds were negative. Campylobacter jejuni was isolated from the drinking water during the growth of the first flock and was present in the birds from all three flocks. Randomly amplified polymorphic DNA (RAPD)-polymerase chain reaction (PCR) typing with primer OPA11 indicated that seven distinct strains were present within the broiler house. One strain found in drinking water was similar to a strain found in birds in the second flock; however, RAPD-PCR with primer HLW85 showed that the strains were not identical. These results suggest that although the watering system is a potential source of C. jejuni in broiler flocks, the waterborne strain in this study was not detected in the birds.     

Isolation and molecular analysis of colonising and non-colonising strains of Campylobacter jejuni and Campylobacter coli following experimental infection of young chickens

Fourteen-day-old chickens were inoculated with selected Campylobacter coli and C. jejuni strains. C. jejuni strains were of two subgroups based on a polymorphism detected using a DNA probe and represented the profiles typical for the majority of strains of either chicken or human origin. All C. coli strains previously isolated from humans colonised chickens, whereas from 4/7 C. jejuni strains of human origin, failed to colonise. Of 12 Campylobacter strains of chicken origin, 10 established a persistent colonisation in the chickens, and 2 strains colonised poorly or not at all. Four strains that failed to colonise chickens were each inoculated into groups of five birds. Three strains again did not colonise any of the chickens and the fourth strain colonised four out of the five chickens, but was poorly excreted. When infected chickens were placed in the same enclosure to facilitate interchange of strains, C. jejunistrain 331 was found to be dominant and colonised all 12 chickens by 21 days, displacing all other strains. C. jejuni strain 331, was then inoculated into groups of five birds with previously established colonisation by C. jejuni and C. coli strains. Strain 331 was able to replace the C. jejuni strain in all five birds but established co-colonisation with C. coli strain. Naturally occurring co-colonisation by two C. jejuni strains was detected in one chicken out of 200 tested. There was no obvious correlation between the type of DNA polymorphism in strains of chicken origin and their ability to colonise chickens.     

Serotype and genotype diversity and hatchery transmission of Campylobacter jejuni in commercial poultry flocks.

We investigated the genotype and serotype diversity of Campylobacter coli and C. jejuni in two parent flocks of adult hens and their offspring over two rotations in order to evaluate the role of hatchery mediated transmission and/or vertical transmission of campylobacters in broiler flocks. In total, 314 C. jejuni and 32 C. coli isolates from parent and broiler flocks and from the surroundings of broiler houses were typed by flagellin gene PCR/RFLP (fla-typing), and selected isolates were also typed by serotyping and macrorestriction profiling using PFGE (MRP/PFGE). The combined typing results showed that the broiler flocks could be colonised by 1-3 different Campylobacter clones and parent flocks could be colonised by 2-6 different clones. C. coli was isolated from up to 36% of birds in one parent flock, whereas only C. jejuni was isolated from broiler flocks. C. jejuni clones from different flocks were clearly discriminated by fla-typing as well as by MRP/PFGE, except for a few cases where individual isolates belonging to two different clones were found to have altered fla-types. Similarly, one C. coli clone showed pronounced fla-type variation. The present results lead to the conclusion that vertical transmission or horizontal transmission via the hatchery are not significant transmission routes of C. jejuni to broiler chickens under Danish conditions. In the cases where more than one Campylobacter clone simultaneously colonised flocks, we found that the different clones coexisted in flocks rather than excluding each other.     

Influence of host lineage on cecal colonization by Campylobacter jejuni in chickens

The resistance to cecal colonization by Campylobacter jejuni was assessed by challenging three crossbred stocks of commercially available broiler chickens. These three stocks, designated A, B, and C, were related as follows: Offspring from four pedigreed grandparent flocks were used as progenitors. Stock B was derived by cross-breeding grandparent 1 with grandparent 3. Stocks A and C were crossbreeds from grandparents 1 and 2 and grandparents 3 and 4, respectively. Campylobacter jejuni were gavaged into 48-hour-old chicks, using the same levels of challenge dose for each of the different chicken stocks. Six days post-challenge, the birds were sacrificed, and cecal contents were plated onto Campylobacter-selective media. Results from two replicate trials with three isolates of C. jejuni indicated that chicken stock A was colonized in only two of 60 ceca, stock B in six of 60, and stock C in 19 of 60 chicken ceca. Statistical analysis of these data indicate that resistance to cecal colonization by C. jejuni was significantly (P less than 0.05) influenced through chicken host lineage.     

Effect of acidified feed on susceptibility of broiler chickens to intestinal infection by Campylobacter and Salmonella

Consumption of poultry meat is associated with human Campylobacter and Salmonella infections. One way to control the presence of these bacteria in broiler flocks is to make chickens less susceptible for colonisation. Acidification of feed may be a tool to reduce the Campylobacter and Salmonella carriage in broiler chickens. In the present experiments an acidified feed with high levels of organic acid, 5.7% lactic acid and 0.7% acetic acid, was applied. In an in vitro experiment the reduction or growth of Campylobacter and Salmonella was measured after addition of 10(7)cfu of these bacteria into a conventional broiler feed, acidified feed and fermented feed, whereas the numbers of Salmonella increased in non-acidified feed. The number of Campylobacter decreased 2-3 (10)log cfu. In the acidified and fermented feed a complete reduction of Campylobacter was observed within 20 min, and a total Salmonella reduction started after 1h, and was complete after 2h. Subsequently, an in vivo experiment with 100 individually housed broiler chickens showed that chickens fed acidified feed were less susceptible to an infection with Campylobacter than were chickens fed conventional feed. The size of reduction was however limited. The susceptibility for Salmonella colonisation was not affected by acidified feed. It is concluded that the role for acidified feed in the control of Campylobacter and Salmonella is limited.     

Fla-DGGE analysis of Campylobacter jejuni and Campylobacter coli in cecal samples of broilers without cultivation

In a commercial broiler flock during rearing multiple genotypes of Campylobacter jejuni may be present as well as in gastrointestinal tracts of individual birds. The aim of this study was to optimize and apply a denaturing gradient gel electrophoresis assay of the flagellin gene (fla-DGGE) for analysis of C. jejuni and Campylobacter coli in cecal samples of broilers without prior cultivation. One C. coli and 21 C. jejuni strains isolated from broiler flocks, of which 14 typed as unique by restriction fragment length polymorphism of flaA and two undefined strains, were clustered into 9 groups when applying fla-DGGE. Spiking of cecal samples revealed that fla-DGGE is able to detect at least 4.55-5.96logCFUCampylobacter/mlcecal material. The presence of 3 strains spiked in cecal material was demonstrated by fla-DGGE as the corresponding bands were visible on the DGGE gel. Naturally contaminated cecal samples were shown to contain different types of C. jejuni and C. coli. Fla-DGGE has some potential as a cultivation-independent fast primary subtyping method for C. jejuni and C. coli in cecal samples of broilers.     

Isolation of Campylobacter Fetus Subsp. Jejuni from Faeces of Norwegian Poultry

Pooled faeces samples from 106 poultry flocks in Norway were examined. Campylobacter fetus subsp. jejuni was isolated from 10 of 100 chicken flocks and from 4 of 6 turkey flocks. Eight of the 14 isolates were classified as biotype C. jejuni, which is frequently associated with human campylobacteriosis. Five strains belonged to the biotype C. coli. One strain was resistant to nalidixic acid but differed from the biotype NARTC in its ability to hydrolyse hippurate. The results indicate that C. fetus subsp. jejuni is widespread among Norwegian poultry.     

Campylobacter jejuni strains of human and chicken origin are invasive in chickens after oral challenge

The aim of the study was to evaluate the colonizing ability and the invasive capacity of selected Campylobacter jejuni strains of importance for the epidemiology of C jejuni in Danish broiler chickens. Four C. jejuni strains were selected for experimental colonization studies in day-old and 14-day-old chickens hatched from specific pathogen free (SPF) eggs. Of the four C. jejuni strains tested, three were Penner heat-stable serotype 2, flaA type 1/1, the most common type found among broilers and human cases in Denmark. The fourth strain was Penner heat-stable serotype 19, which has been shown to be associated with the Guillain Barré Syndrome (GBS) in humans. The minimum dose for establishing colonization in the day-old chickens was approximately 2 cfu, whereas two- to threefold higher doses were required for establishing colonization in the 14-day-old chickens. Two of the C. jejuni strains were shown to be invasive in orally challenged chickens as well as in three different human epithelial cell lines.     

Influence of bird strain on competitive exclusion of Campylobacter jejuni in young chicks

1. Newly hatched chicks of either layer or broiler strain were treated orally at regular intervals with either homologous or heterologous gut-flora preparations from young donor birds, in an attempt to prevent subsequent colonisation with Campylobacter jejuni by 'competitive exclusion' (CE). 2. Donors of 3 to 10 d of age were chosen to correspond with the period in which intensively reared poultry are least likely to become colonised with Campylobacter. 3. In two separate trials, material from donor layer hens (ISA Brown) protected male chicks of the same strain against a low (195 to 360 cfu/bird) Campylobacter challenge, but the same kind of material was ineffective when administered to chicks of a broiler strain (JA957). 4. Two further trials involved treatment preparations from young broilers, which failed to prevent Campylobacter colonisation of broiler chicks, even when colonisation occurred relatively slowly from a challenge of 90 to 94 cfu/bird. 5. It was concluded that any CE effect observed was strongly dependent on bird strain.     

Epidemiology of ovine Campylobacter infection determined by numerical analysis of electrophoretic protein profiles

The relationship of 50 Campylobacter strains isolated from aborted ovine foetuses, and the faeces of sheep, cattle and chickens were determined by numerical analysis of electrophoretic (SDS-PAGE) protein profiles. Comparison of protein patterns by numerical methods revealed differences between C. fetus ssp. fetus, C. jejuni, and C. coli strains as well as heterogeneity among isolates from different outbreaks. Isolates from each farm produced a distinct cluster and flocks from different locations were found to be infected with relatively different strains. In most cases, protein patterns of ovine foetal isolates were very similar to those of ovine faecal isolates. Ovine isolates of C. fetus ssp. fetus, C. jejuni and C. coli gave similar protein patterns to the corresponding Campylobacter species isolated from cattle or chicken, on the same farm. Thus, it was concluded that certain protein types of ovine Campylobacter strains were more likely associated with local areas, and Campylobacter strains causing ovine abortions are distributed in the environment more widely than assumed to date.     

Campylobacter jejuni infection in broiler chickens

Day-old, straight-run broiler chickens were procured from a hatchery located in the Pacific Northwest. The chickens were subdivided individually into nine groups of 20 chickens. The chickens were tagged, housed in isolation chambers on wire, fed commercial broiler feed, and given water ad libitum. Three isolates of Campylobacter jejuni of poultry origin and one of human origin were tested in this study. Various C. jejuni cultures were inoculated into 9-day-old chickens by crop gavage. Four groups of 20 chickens were inoculated at a dose level of 0.5 ml of 1 x 10(2) colony-forming units (CFU)/ml. The other four groups were inoculated with 0.5 ml of 1 X 10(4) CFU/ml. One group of 20 chickens was kept as an uninoculated control group. Four randomly selected chickens from each of the inoculated and uninoculated groups were necropsied at 5, 12, and 19 days postinoculation (DPI). The C. jejuni was cultured and enumerated from a composite of the upper and midintestine and the cecum. Body weights of all chicken groups at 7 days of age and at 5, 12, and 19 DPI were measured and statistically analyzed. No significant differences were present in the mean body weights (MBWs) of 7-day-old, 5 DPI, and 12 DPI male and female broiler chickens inoculated with C. jejuni at both dose levels compared with uninoculated controls. Differences in MBWs of the male and female broilers at 19 DPI were observed in some of the groups. Results of the C. jejuni culture enumeration mean (CEM) of composite intestine samples at 5 DPI from all inoculated chicken groups, irrespective of the dose level, ranged from (2.5 +/- 5.0) x 10(2) to (2.8 +/- 4.8) x 10(5) CFU/g (mean +/- SD). Results of cecum C. jejuni CEM at 5 DPI inoculated at both dose levels ranged from (2.5 +/- 5.0) x 10(6) to (1 +/- 0.0) x 10(7) CFU/g in all treatment groups irrespective of the dose level. CEM results from the composite intestine samples at 12 and 19 DPI increased by 1 log unit, or sometimes more. Results of cecum C. jejuni CEM at 5 DPI inoculated at both dose levels ranged from (2.5 +/- 5.0) x 10(6) to (1 +/- 0.0) x 10(7) CFU/g in all treatment groups irrespective of the dose level. Increases of 2-5 log units in C. jejuni CEM was present in chicken groups inoculated with 1 X 10(2) CFU of C. jejuni, and a 2- to 3-log increase was present in groups inoculated with a higher dose level of C. jejuni at 12 DPI. The results of C. jejuni CEM from cecal samples at 19 DPI were similar to chicken groups at 12 DPI. Campylobacterjejuni was not isolated from the uninoculated control chickens at 5, 12, and 19 DPI. Clinical signs of illness or gross pathologic lesions were not present in any of the chicken groups during this study. No lesions were present on histopathologic evaluations in C. jejuni-inoculated chickens or uninoculated control chickens.     

Prevalence and risk factors for Campylobacter spp. in chicken broiler flocks in Reunion Island (Indian Ocean)

Our objectives were to determine Campylobacter prevalence in broiler chicken flocks in Reunion Island and to define specific practices associated with the presence of Campylobacter spp. Infection in Reunionese broiler flocks. Fifty broiler flocks were studied in Reunion Island from May 2007 to February 2009. A questionnaire was submitted to the farmers and samples of fresh droppings were collected to assess the flock's Campylobacter status. Fifty four percent of the flocks were infected by Campylobacter spp.: 30% (95% CI: 28.71-31.29) were infected with Campylobacter coli and 17% (95% CI: 15.95-18.05) with Campylobacter jejuni; only 7% (95% CI: 6.28-7.72) were infected by both species at the same time. Several poultry houses in the farm (OR=11.2; [1.05-92]) and cleaning without any detergent (OR=13.1; [2.1-78.3]) increased the risk of Campylobacter infection. A distance higher than 500 m between broiler farms (OR=0.27; [0.1-0.8]) and use of disinfectant during the rearing period decreased this risk of infection (OR=0.15; [0.1-0.75]).     

PFGE and PCR/RFLP typing of Campylobacter jejuni strains from poultry

1. Pulsed-field gel electrophoresis (PFGE) and PCR-restriction fragment length polymorphisms of the flagellin gene (fla-RFLP) were used to analyse 92 poultry and 110 human strains of Campylobacter jejuni. 2. Among poultry strains, 11 fla-RFLP and 11 PFGE subtypes were found, while human strains could be divided into 23 fla-RFLP and 32 PFGE subtypes. Altogether, 31 fla-RFLP and 32 PFGE subtypes were found. 3. The results show that individual flocks in farms are mostly infected with a single C. jejuni clone, while during subsequent colonisation their genotypes altered. fla-RFLP and PFGE profiles in poultry and humans were identical in less than 6% of cases. The results found so far confirm previous findings that chicken meat does not represent as important a source of campylobacteriosis as was previously believed. 4. The typing of Campylobacter sp. forms the basis for an evaluation of the current state and risk assessment of various Campylobacter sp. sources in relation to humans. Examination of samples with only one method is insufficient for epidemiology studies, because apparently different clones identified with one method could originate from a single clone, which could be proved with the other method.     

Epidemiologic features of Campylobacter jejuni isolated from poultry broiler houses and surrounding environments as determined by use of molecular strain typing

OBJECTIVE: To genetically type Campylobacter jejuni isolates from broiler houses or the external environment to identify the source of Campylobacter organisms in broiler chickens. SAMPLE POPULATION: Environmental samples associated with broiler chickens, in commercial grow-out houses. PROCEDURE: Polymerase chain reaction (PCR) was used to amplify flaB, and the amplicon was digested with Sau3A to create a restriction fragment length polymorphism assay; PCR was also used to detect a transcribed spacer region in the 23S rRNA gene. RESULTS: Isolates possessing a 23S spacer region were more prevalent outside broiler houses than inside. Houses that had previously contained chickens or lacked biosecurity procedures were more likely to contain isolates possessing the 23S spacer. One house contained only isolates possessing the spacer, whereas an adjacent house contained only isolates lacking the spacer. The flaB type detected in broiler houses was different from the type detected in the environment; however, many isolates within the broiler houses contained untypable flaB genotypes. CONCLUSIONS AND CLINICAL RELEVANCE: Most isolates from within houses were genetically distinct from isolates from outside houses that were examined by bacteriologic culture, suggesting an undetected source of C jejuni. Detection of isolates containing the 23S spacer appeared to be an indicator of environmental contamination of the houses. The observation of completely different C jejuni genetic types simultaneously within adjacent houses suggests that some types do not compete successfully during the grow-out period. In addition, the diversity of genotypes identified within broiler houses indicates the complexity of the ecologic features of C jejuni in the chicken environment.     

安徽省部分地区鸡群禽偏肺病毒感染的血清学调查

为掌握禽偏肺病毒(aMPV)在安徽省鸡群中的感染状况,采用酶联免疫吸附试验(ELISA)对安徽省合肥、亳州、定远、舒城等地区的9个鸡场、7个不同品种(系)鸡群的296份血液样本进行了aMPV血清抗体检测。结果表明,所有被检鸡场均有aMPV感染,鸡场阳性率最高达100%,最低为20%;各品种(系)鸡均有感染,感染率最高的是青脚麻肉鸡,其次分别为科宝肉鸡、海兰蛋鸡、禽粤黄蛋鸡、淮南麻黄鸡、黄羽土鸡和新广麻肉鸡;其中蛋用型鸡血清样本总体阳性率为88.7%,明显高于肉用和兼用型鸡;公鸡和母鸡血清抗体阳性率均较高。研究结果表明,安徽省鸡群aMPV的感染已广泛存在,且不同地区、品种(系)、用途和性别的鸡群均较严重,应根据感染状况尽早制定相应的防控对策。     

Colonization strategy of Campylobacter jejuni results in persistent infection of the chicken gut

Although poultry meat is now recognized as the main source of Campylobacter jejuni gastroenteritis, little is known about the strategy used by the bacterium to colonize the chicken intestinal tract. In this study, the mechanism of C. jejuni colonization in chickens was studied using four human and four poultry isolates of C. jejuni. The C. jejuni strains were able to invade chicken primary cecal epithelial crypt cells in a predominantly microtubule-dependent way (five out of eight strains). Invasion of cecal epithelial cells was not accompanied by necrosis or apoptosis in the cell cultures, nor by intestinal inflammation in a cecal loop model. C. jejuni from human origin displayed a similar invasive profile compared to the poultry isolates. Invasiveness of the strains in vitro correlated with the magnitude of spleen colonization in C. jejuni inoculated chicks. The C. jejuni bacteria that invaded the epithelial cells were not able to proliferate intracellularly, but quickly evaded from the cells. In contrast, the C. jejuni strains were capable of replication in chicken intestinal mucus. These findings suggest a novel colonization mechanism by escaping rapid mucosal clearance through short-term epithelial invasion and evasion, combined with fast replication in the mucus.     

National surveillance of Campylobacter in broilers at slaughter in Denmark in 1998

A surveillance study for thermophilic Campylobacter spp. in broiler flocks was carried out for the year 1998 in Denmark. The study included examinations of 4286 broiler flocks comprising samples from 57,000 birds. Overall, a flock prevalence of 46.0% was recorded. The species distribution was Campylobacter jejuni 86%, Campylobacter coli 11%, Campylobacter lari 1%, other not further diagnosed species 2%. The prevalence was significantly higher in the period from June to October (3.2 < odds ratio [OR] <1.8, P < 0.0002) and was significantly associated with abattoir (OR < 2.8, P < 0.0001) and the length of the period the broiler houses were left empty between flocks (download period; 6 days or more) (OR = 1.6, P < 0.0198). No association between Campylobacter colonization and the age at slaughter was found. Separating the flocks into batches for slaughter elevated the flock prevalence from 0.41 after the first batch had been slaughtered to 0.46 after all batches had been slaughtered.     

The prevalence and genetic diversity of Campylobacter spp. in domestic 'backyard' poultry in Canterbury, New Zealand

Campylobacteriosis is the most commonly notified illness in New Zealand. Whilst the importance of commercial poultry in campylobacteriosis is well established, little is known about the possible role of chickens kept at home as a direct animal/faecal contact or consumption exposure pathway. The aim of this study was to determine the prevalence and genetic diversity of Campylobacter spp. in domestic backyard chicken flocks in the Canterbury region of New Zealand. Poultry faecal samples were collected from 35 domestic 'backyard' poultry flocks from urban and rural properties around the Canterbury Region of New Zealand. A total of 291 samples were collected and tested for the presence of thermotolerant Campylobacter spp. and positive isolates were analysed using pulsed-field gel electrophoresis (PFGE) using both SmaI and KpnI enzymes. There was a high prevalence of Campylobacter spp. with 86% of flocks testing positive. Campylobacter jejuni alone, Campylobacter coli alone and both C. jejuni and C. coli were detected in 20 (57%), 2 (6%) and 8 (23%) of the flocks respectively. SmaI/KpnI PFGE analysis identified 50 different genotypes across the 35 flocks. Genotype diversity richness was highest on the lifestyle block and farm properties with 43 different genotypes isolated, whilst urban properties displayed the least richness with 12 genotypes isolated. Rural flocks tended to have more different genotypes in a given flock than urban flocks. Comparison of the genotypes with the PulseNet Aotearoa Campylobacter database showed that 28 of the genotypes had previously been isolated from human cases of campylobacteriosis. Many of these were also indistinguishable from Campylobacter spp. previously isolated from retail chicken. Therefore, contact with backyard poultry or their faecal material is a potential additional infection pathway outside of exposure to the established pathways associated with the consumption of Campylobacter-contaminated commercial meat or foods cross-contaminated from contaminated poultry.