• We are sorry, but NCBI web applications do not support your browser and may not function properly. More information
Logo of aemPermissionsJournals.ASM.orgJournalAEM ArticleJournal InfoAuthorsReviewers
Appl Environ Microbiol. Jun 2005; 71(6): 2824–2831.
PMCID: PMC1151807

Effect of Preslaughter Events on Prevalence of Campylobacter jejuni and Campylobacter coli in Market-Weight Turkeys

Abstract

The effects of events which occur prior to slaughter, such as loading, transport, and holding at an abattoir, on the prevalence of Campylobacter species, including Campylobacter jejuni and Campylobacter coli, were examined. Cloacal swabs from market-weight turkeys in each of five flocks were obtained on a farm prior to loading (time 1; 120 swabs per flock) and after transport and holding at the abattoir (time 2; 120 swabs per flock). A statistically significant increase in the overall prevalence of Campylobacter spp. was observed for cloacal swabs obtained from farm 3 following transport (P < 0.01). At time 2, an increase in the prevalence of C. coli was also noted for cloacal swabs from farms 3, 4, and 5 (P < 0.01). Neither the minimum time off of feed nor the distance transported from the farm to the abattoir was correlated with the increase in C. coli prevalence. Similarly, responses to an on-farm management questionnaire failed to detect any factors contributing to the observed changes in Campylobacter sp. prevalence. A SmaI macrorestriction analysis of Campylobacter sp. isolates recovered from flock 5 indicated that C. coli was more diverse than C. jejuni at both time 1 and time 2 (P < 0.01), based on a comparison of the Shannon indices of diversity and evenness.

Human food-borne campylobacteriosis causes nearly 2 million cases of food-borne illness annually, resulting in ~10,000 hospitalizations and ~100 deaths each year (18). Of the three thermotolerant Campylobacter species, Campylobacter jejuni, C. coli, and C. lari, C. jejuni is the primary human pathogen. C. coli is a commensal of hogs, is occasionally reported in poultry, and is also a human pathogen (1, 14, 31, 32). C. lari, which is present in poultry, hogs, and shellfish, is infrequently associated with human illness (12). The consumption of contaminated undercooked poultry is a major risk factor for human Campylobacter infections (1, 11, 20, 29). The 1997 USDA Food Safety and Inspection Service (FSIS) young turkey baseline study detected Campylobacter jejuni/coli on 90% of turkey carcasses (34). In that national study, FSIS protocols did not require the identification of C. jejuni and C. coli to the species level. Thus, reducing the prevalence of Campylobacter spp. in live birds entering abattoirs may ultimately reduce the occurrence of human campylobacteriosis.

Feed withdrawal, catching, crating, and transport occur within 24 h of slaughter and may influence the intestinal carriage of food-borne pathogens such as Campylobacter spp. Feed withdrawal immediately prior to live hauling evacuates the crop, minimizes the gastrointestinal contents, and thereby reduces fecal contamination of both turkey and broiler carcasses (6, 17, 35). After ~4 h of feed withdrawal, birds may reflexively peck at fecal-contaminated litter, thus increasing crop contamination (6). In a study of broilers, the percentage of crops harboring Campylobacter spp. increased significantly after feed withdrawal (62.4%) compared to the baseline level (25%; P < 0.001) (4). In the same study, the prevalence of Campylobacter spp. in crops (62%) exceeded that of Campylobacter-positive ceca (4%; P < 0.001) after transport and holding, which suggested that the crop may be a critical control point for reducing the entry of Campylobacter into the abattoir (4). The effects of feed withdrawal may be age related, as demonstrated by Northcutt et al., who reported that feed withdrawal increased Campylobacter levels on carcasses of younger birds (42 days), with older animals (49 and 56 days) being unaffected (23).

Whereas the physical exertion during catching may increase intestinal peristalsis in poultry and augment the excretion of food-borne pathogens, the inactivity while cooped during transport slows gut motility (17). Contacts of birds with dirty crates as well as with excrement contaminate the feet and feathers of colonized birds as well as those of previously uncontaminated cagemates (23, 27). The idea that transport crates are a source of contamination was based on a comparison of genotypes of Campylobacter isolates recovered from carcasses with those recovered from transport crates. Crates may already be contaminated prior to loading (21, 27). In a previous study, confinement in a crate significantly increased the prevalence of Campylobacter on broiler carcasses, some of which originated from Campylobacter-negative flocks (27). In that study, the contamination may have originated from either workers crating the birds prior to transport or workers shackling the birds at the abattoir (27).

Stern et al. reported that transportation and holding increase Campylobacter carcass contamination in broilers (28). In their study, Campylobacter was detected on 12.1% of carcasses of broilers that were slaughtered on the farm (average = log10 2.71 Campylobacter spp. per carcass). After transport and slaughter, 56% of carcasses harbored Campylobacter at higher levels (log10 5.15 CFU per carcass; P < 0.05). Interestingly, no such increases were noted for Campylobacter spp. recovered from the ceca. In addition, Whyte et al. (38) reported that the numbers of Campylobacter present in feces of broilers increased significantly after transportation.

Limited information is available detailing the effects of events which occur prior to slaughter on the prevalence of food-borne pathogens in turkeys. Therefore, based on studies of broilers, the primary goal of this study was to determine if feed withdrawal, transport, and holding at the abattoir collectively influence the prevalence of C. jejuni and C. coli populations in market-weight turkeys.

(Portions of this study were presented at the annual convention of the Midwest Poultry Federation, Minneapolis, Minn., 15 to 17 March 2004.)

MATERIALS AND METHODS

Farm selection.

Five Midwestern premises (farms 1 through 5) were selected on the basis of their scheduled delivery of market-weight turkeys to the abattoir during the summer months of May through August 2003, when sampling was conducted. Four of the five farms utilized a two-stage production system with separate brooder and grow-out houses (~10,000 birds per house). The fifth farm utilized a three-stage production system in which ~6-week-old birds remained in the first grow-out house until ~12 weeks of age, when they were transferred to a second grow-out house until achieving market weight (~40 lbs).

Live hauling.

All producers used the same company for live hauling to a single commercial abattoir. Estimates of the perimarketing interval were based on the drivers' logs, which included the times for loading (catching and crating) at the farm, transport, a resting interval at the processing plant, and the plant's record of the time of slaughter.

Cloacal swabs.

Cloacal swabs were obtained at each farm within 12 h of the beginning of catching and loading into transport cages (time 1; n = 120 per farm) and again at the slaughter facility prior to slaughter (time 2; n = 120 per farm). Six-inch cotton-tipped applicators (Harwood Products, Guilford, Maine) were inserted approximately 3 inches into the cloaca, with care taken to avoid contact with the surrounding feathers and skin. The wooden applicator was broken in half and the upper half was discarded as each swab was placed into a 16- by 125-mm round-bottomed polystyrene tube (Becton-Dickinson, Franklin Lakes, N.J.) containing 13.5 ml blood-free enrichment broth (BFEB), allowing for the requisite headspace air to take up 16 to 17% of the tube's total capacity (33). Tubes were transported to the laboratory, where they were immediately incubated (24 h, 42°C, ambient atmosphere). BFEB, which incorporates activated charcoal as an oxygen quencher, has been shown to be equivalent to the U.S. Food and Drug Administration-approved protocol for Campylobacter isolation (33).

Viscera sampling.

Ceca and crops were analyzed for farms 4 and 5. At the slaughterhouse, organs were placed individually into sterile WhirlPak bags (Nasco, Ft. Atkinson, Wisc.), transported back to the laboratory at ambient temperature, refrigerated within ~6 h of collection, and processed the following morning.

Isolation and identification of Campylobacter spp.

For cloacal swabs, after enrichment in BFEB (24 h, 42°C), an aliquot (50 μl) was streaked onto Campy cefex agar (30) and incubated (48 h, 42°C) microaerobically (5% O2, 10% CO2, 85% N2) in a three-gas incubator (Forma Scientific, Marietta, Ohio).

For crops, sterile phosphate-buffered saline (10 ml) was pipetted into each crop and the contents mixed by hand to achieve a homogeneous suspension. An aliquot of this suspension (1 ml) was placed in BFEB (12.5 ml) and incubated (24 h, 42°C), after which an aliquot (100 μl) was subcultured onto Campy cefex agar and incubated (48 h, 42°C) microaerobically as described above.

The contents from both ceca (~5 g) were squeezed into buffered peptone water (90 ml) and mixed, and an aliquot (1 ml) was placed in BFEB (12.5 ml) and incubated (24 h, 42°C). An aliquot (100 μl) was subcultured onto Campy cefex agar plates (48 h, 42°C) and incubated microaerobically.

Species of Campylobacter were determined as follows. For cloacal swabs and viscera, three presumptive Campylobacter colonies from each Campy cefex agar plate (flat, shiny, and mucoid, with a pink hue) were randomly picked to ensure an even representation of colony types. The colonies were subcultured on brain heart infusion agar (Becton Dickinson, Sparks, Md.) supplemented with 0.6% yeast extract and 10% defibrinated sheep blood and then were incubated microaerobically (24 h, 42°C).

Presumptive colonies were identified by use of a multiplex PCR assay for C. jejuni and C. coli, as described previously (5). Templates for PCR were initially prepared (farms 1 and 2) with an InstaGene Matrix (Bio-Rad Laboratories, Hercules, Calif.) according to the manufacturer's directions. For reasons of efficiency, cost of template preparation, number of samples processed, and improved template recovery, DNA templates were ultimately prepared by using boiled sterile distilled water (farms 3, 4, and 5). For the aqueous method of template preparation, bacteria were harvested from a 2- by 4-mm area of growth on blood agar plates, placed in 50 μl of sterile distilled water, and incubated (10 min, 100°C), and the lysate was then centrifuged (11,000 rpm, 3 min; IEC Micromax, Needham Heights, Maine). Multiplex PCR was performed as previously described (5), using either 20 μl of the InstaGene supernatant (farms 1 and 2) or 5 μl of the water template preparation (farms 3 to 5). Presumptive Campylobacter colonies that were not identified as either C. jejuni or C. coli were further subjected to a PCR for the Campylobacter genus and then a PCR for C. lari as described previously (13), using a 5-μl template. All isolates confirmed as Campylobacter spp. were stored in brain heart infusion broth (Becton Dickinson, Sparks, Md.) with 20% glycerol (−80°C).

PFGE.

Farm 5 was randomly selected for a pulsed-field gel electrophoresis (PFGE) analysis of isolates recovered at time 1 and time 2. A macrorestriction analysis of the C. jejuni (n = 88 isolates) and C. coli (n = 71) isolates utilized SmaI and was conducted with a Chef Mapper (Bio-Rad Laboratories, Hercules, Calif.) as described previously (25). Campylobacter coli ATCC 33559, which originated from swine feces, served as the positive control. The lambda cI857 DNA ladder (0.05 to 1 Mb) was used as the size standard (Bio-Rad Laboratories, Hercules, Calif.).

Analysis of PFGE restriction enzyme digestion profiles.

GelCompar II v. 3 software (Applied Maths, Kortrijk, Belgium) was employed for band analysis and dendrogram construction. Patterns were normalized according to the lambda size standard, with a 1% band tolerance using Dice similarity coefficients, as described previously (19). To ensure gel-to-gel consistency for band comparisons, we included the C. coli reference standard thrice in each gel.

Statistical analysis.

Chi-square analysis was used to compare the prevalence of Campylobacter at time 1 (on-farm) and time 2 (after transport). P values of <0.01 were considered significant.

The Shannon indices of diversity (H′) and evenness (E) were used to compare the diversities of C. jejuni and C. coli isolates (16).

The Shannon index of diversity (H′) is defined as follows: H′ = −Σpiln(pi), where pi = ni/N and is the proportion of a strain found in an isolate. The Shannon index of evenness was used to measure the abundance of isolates and is defined as follows: E = H′/ln(S), where S is the number of strains.

The t test was used to statistically compare the H′ values of C. jejuni and C. coli isolates recovered at time 1 and time 2, with significance set at P values of <0.001, as described previously (16). In the absence of a formula for calculating variance, t tests were not done for the E values.

Farm management questionnaire.

A farm management questionnaire was used in a follow-up telephone interview of turkey growers to determine if any management practices were associated with the prevalence of Campylobacter at the time of slaughter. The questionnaire surveyed, for example, the source of poults, the use of growth promoters, the frequency of top dressing litter changes, vaccine strategies, the use of coccidiostats, health problems associated with the flock, and the use of chlorinated water. The interviewer was unaware of individual farm Campylobacter prevalence data when the questionnaire was administered.

RESULTS

Duration of preslaughter events.

The average estimated perimarketing interval, or minimum time off feed, was 7.94 h for the five premises, as shown in Table Table1.1. Although the loading times (mean, 0.79 h) were similar for the five flocks, the transport time did vary from 0.25 h (flock 2) to 3 h (flock 1). Birds rested in the holding shed, where they were cooled by industrial-size fans, for an average of 6 h. Coincidentally, flock 2, which had the shortest transport time, had the longest interval (10 h) in the holding shed.

TABLE 1.
Summary of times for loading, transport, and holding and minimum overall time off feed (feed withdrawal interval) for turkeys sampled from each of five premises

Campylobacter sp. prevalence.

As shown in Fig. Fig.1,1, the baseline prevalence of Campylobacter spp. in turkeys from the five premises ranged from 65% to 90% on-farm prior to transport (time 1) and from 66% to 95% at the slaughter facility (time 2). Chi-square analysis indicated a statistically significant increase in the prevalence of Campylobacter spp. in flock 3 between time 1 (65%; on-farm) and time 2 (81%; after transport [P < 0.01]). The overall prevalence of Campylobacter spp. did not differ prior to (time 1) and after (time 2) transport for the remaining four of the five flocks examined.

FIG. 1.
Prevalence of Campylobacter spp. in five Midwestern turkey flocks, as determined by use of cloacal swabs. Time 1 represents the prevalence on-farm prior to loading into transport cages. Time 2 represents the prevalence after transport and holding (at ...

As shown in Fig. Fig.2,2, when Campylobacter isolates were identified to the species level, significant differences emerged. For the isolates from flocks 3, 4, and 5, an increase in the prevalence of C. coli was noted for cloacal swabs taken at the holding shed at the slaughter plant (time 2) compared to the on-farm baseline data (time 1). For flock 5, the prevalence of C. coli exceeded that of C. jejuni. This coincided with a lower prevalence of C. jejuni at time 2 (P < 0.01). Birds from which both C. jejuni and C. coli were isolated were scored as concurrently positive and were grouped separately from birds from which either C. jejuni or C. coli was exclusively recovered. A significant increase in the frequency of concurrently positive birds between the two sampling times was observed at time 2 for farms 3 and 4 (P < 0.01) (Fig. (Fig.22).

FIG. 2.
Prevalence of C. jejuni, C. coli, and concurrently positive turkeys in five turkey flocks, as determined by use of cloacal swabs. Birds from which both C. jejuni and C. coli were isolated were scored as “concurrently positive” and were ...

The majority of isolates recovered from cloacal swabs were C. jejuni (69%; 735/1,066), followed by C. coli (30.5%; 325/1,066) and C. lari (0.6%; 6/1,066). In contrast, as shown in Table Table2,2, C. coli was the predominant species recovered from limited sampling of the crop (61/84; 72.6%) and the cecum (96/96; 100%).

TABLE 2.
Recovery of C. jejuni and C. coli from the crop and cecum based on limited sampling of farms 4 and 5

Farm management.

As summarized in Table Table3,3, the flocks differed regarding the source of poults, the mill providing feed, the type of litter, the source of water in the turkey houses, water chlorination, vaccine regimens, and biosecurity practices. All flocks used growth promoters, at minimum moved birds from a brooder house to a grow-out house (two-stage production), top dressed the litter with the introduction of each flock, recorded sparrows or starlings in the houses, and used coccidiostats. However, with this small sample, no single factor emerged to explain the observed shift in C. jejuni and C. coli populations between the two sampling intervals.

TABLE 3.
Summary of on-farm management practices for the farms in this study

PFGE.

Isolates from flock 5 were examined by PFGE to compare the relative diversities of C. coli and C. jejuni recovered at time 1 (n = 80) with those of organisms recovered after transport and holding at time 2 (n = 79). As shown in Fig. Fig.33 (top panel), for the two time points combined, the C. jejuni isolates (n = 88) exhibited seven restriction enzyme patterns (arbitrarily designated J1 to J7). Profile J1 was exhibited by 79.5% of the isolates (31 of 39) at time 1 and by 82% of the isolates (40 of 49) at time 2. Thus, the J1 profile was represented more frequently than the remaining C. jejuni patterns (J2 to J7). As shown in Fig. Fig.33 (bottom panel), for time 1 and time 2 overall, the C. coli isolates (n = 71) exhibited 17 patterns, or nearly 2.4 times more unique profiles (C1 to C17), than a comparable number of C. jejuni isolates (n = 88). In addition, the C. coli isolates collected at time 1 (n = 41 isolates) exhibited more patterns (n = 15) than the isolates collected at time 2 (n = 30 isolates), which exhibited eight patterns.

FIG. 3.
Distribution of SmaI macrorestriction patterns of Campylobacter spp. isolated from cloacal swabs from turkeys in farm 5. Cloacal swabs were collected prior to (time 1) and after (time 2) feed withdrawal, transport, and holding at the abattoir. The frequencies ...

As summarized in Table Table4,4, a comparison of the Shannon indices of diversity (H′) and evenness (E) affirmed that C. coli had more diversity among the isolates, and thus more strains, than did C. jejuni at both time 1 and time 2. For the index of diversity (H′), this difference was statistically significant (P < 0.001). Furthermore, the C. coli isolates recovered at time 1 were more diverse than those collected at time 2 (P < 0.001), based on a comparison of H′ values, which may reflect the smaller number of C. coli recovered at time 2. In contrast, there was no difference in the diversity (H′) of C. jejuni at time 1 (n = 39 isolates [four strains]) and that at time 2 (n = 49 isolates [six strains]; P > 0.4).

TABLE 4.
Comparison of C. jejuni and C. coli isolates recovered at time 1 and time 2 by their Shannon indices of diversity (H′) and evenness (E)

DISCUSSION

Feed withdrawal, catching, crating, live hauling, and resting in holding sheds at the slaughterhouse are routinely practiced in the turkey industry. In this study of five independently operated commercial turkey farms, we compared the prevalence of Campylobacter spp. in turkey cloacal swabs collected on-farm (time 1) and after transport to the abattoir (time 2). Turkeys had no access to feed for an average of nearly 8 h, based on the interval from the beginning of loading to the time of slaughter. This was the minimum interval, since the exact time that feed was withdrawn varied for each farm, with some premises allowing access to feed until loading began.

The overall prevalence of Campylobacter spp. in cloacal swabs from tom turkeys sampled during the summer months both on-farm (time 1; 65 to 90%) and immediately prior to slaughter (time 2; 66 to 95%) was comparable to that reported for the southeastern Atlantic states, where Campylobacter spp. were frequently isolated from cecal droppings of hens (70%) and toms (80%) (7).

Compared to the on-farm baseline (time 1), there was a significant increase in the prevalence of Campylobacter spp. after transport and holding (time 2) in cloacal swabs from turkeys in flock 3. The fact that no other flock exhibited a change may be attributed to the already high prevalence of Campylobacter spp. and the resultant need for sampling more birds per flock to detect a statistically significant shift. The impact of perimarketing events, reflected in the dynamics of gut microflora, on Campylobacter sp. prevalence in broilers has been noted earlier (28, 38). For example, the prevalence and mean counts of Campylobacter spp. on carcasses, but not in ceca, increased for broilers slaughtered after feed withdrawal and transport compared with birds slaughtered on-farm (28). In addition, mean counts of Campylobacter spp. in feces increased significantly after the transportation of broilers compared with pretransport levels, although the overall Campylobacter sp. prevalence was unchanged (38).

In the present study, the prevalence of C. coli increased significantly in cloacal swabs taken after the transportation of turkeys originating from three of the five premises compared with the baseline on-farm sampling at time 1 (P < 0.05; flocks 3, 4, and 5). These events coincided with a significant increase in concurrent infections of C. jejuni and C. coli for two of the premises (P < 0.05; flocks 3 and 4). The fact that C. coli was the predominant species recovered after enrichment in a limited study of ceca (96 of 96 [100%]) and crops (61 of 84 [62%]) suggests that these sites may serve as reservoirs for carcass contamination (36). The physiological consequences of feed withdrawal, crating, transport, and holding may have altered the gut microflora and thus preferentially favored the replication and survival of C. coli rather than C. jejuni at detectable levels. For the crops of broilers during the first 12 h of feed withdrawal, a decline in Salmonella and lactic acid bacteria with a concurrent increase in the crop pH has been noted (9). For the ceca of broilers, in contrast, since lactic acid bacteria are present in smaller numbers, their decline generates a modest pH increase only after 12 h of feed withdrawal, with a minimal impact on either Campylobacter or Salmonella (3, 10).

No specific on-farm management practices were clearly associated with the shift in the C. jejuni and C. coli populations, which may have been due to the small number of flocks surveyed. The five premises were independently operated and employed similar overall industry practices. Although three of the premises did not use chlorinated water, this was not associated with the observed change in Campylobacter sp. prevalence either pre- or posttransport. Feed withdrawal compounded with the physical exertion of catching and loading may initially favor voiding of the intestinal tract, thus reducing carcass contamination. However, the limited movement of turkeys after crating slows gut motility (17). For this study, birds were held in transport crates for an average duration of nearly 8 h, which would have favored gut stasis and the subsequent retention of digesta (4). Turkey ceca harbor 2.7 × 106 Campylobacter cells per gram of contents, which surpasses the amounts in other segments of the intestine by up to 5 orders of magnitude (15, 36, 39). Thus, C. coli from the cecum may have been voided into the cloaca, resulting in the observed increase after transport. Although physiological changes in the crops (9) and ceca (10) of broiler chickens have been reported after feed withdrawal and confinement in a transport crate, limited information is available for turkeys. Alternatively, since the individual turkeys swabbed on-farm (time 1) differed from those sampled posttransport (time 2), it is possible that the difference merely reflected a sampling bias, despite the random selection of turkeys.

Few studies have delineated the Campylobacter species recovered from turkeys, perhaps assuming that C. jejuni represents the majority of isolates. For example, the 1997 USDA National Young Turkey Microbial Baseline survey reported the presence of Campylobacter jejuni/C. coli on 90.3% of carcasses and did not further identify isolates to the species level (34). Although regarded as an intestinal commensal of swine, C. coli has been isolated from up to 25% of turkeys (2, 14, 22) and up to 20% of broiler chickens (26). In the present study, C. coli was frequently recovered from turkeys, although hogs were not raised on any of the premises. In a survey of Campylobacter spp. in two turkey processing plants in the upper Midwestern United States, Logue et al. (14) reported that 34.9% of carcasses overall harbored Campylobacter spp., with the contamination rates being similar for the two slaughterhouses. In that study, the proportion of C. jejuni and C. coli on turkey carcasses varied from plant A (51.6% and 40.5%, respectively) to plant B (76.8% and 4.6%, respectively).

Farm 5 was randomly selected for PFGE analysis to gauge the genetic diversity of the isolates. Overall C. jejuni exhibited proportionately fewer macrorestriction profiles by PFGE than did C. coli. The Shannon indices of diversity and evenness also indicated that C. coli was more diverse than C. jejuni. It is possible that C. jejuni encountered in the field may have been preferentially more sensitive to the antimicrobials incorporated in the selective enrichments, thus favoring the recovery of a broader range of C. coli. The fact that a single profile (J1) was overrepresented among the seven unique profiles of C. jejuni may reflect a long-standing colonizing strain introduced early into the flock (24, 37) or preferential strain survival after selective enrichment (21). Limited genomic diversity and thus genetic stability were suggested earlier for C. jejuni isolated from turkey flocks raised simultaneously on individual farms (2) and from broiler chicken carcasses purchased from a single producer (8). In contrast, Rivoal et al. attributed the multiple genotypes of C. coli (4 strains) and C. jejuni (11 strains) within a broiler chicken flock to either multiple origins or genetic drift within the Campylobacter population (26). The multiple genotypes exhibited by the 71 isolates of C. coli from a single farm in this study may reflect its survival advantage in the intestine of the healthy turkey (37).

This constitutes the first report of a shift in C. jejuni and C. coli populations in turkeys associated with perislaughter events, including catching, crating, transport, and resting at the abattoir. These observations concur with a previous analysis of the crop and cecum and suggest that the overall gut microbiota is impacted by feed withdrawal, crating, transport, and holding. Whether these events favor the selection of more virulent strains or of bacteria with enhanced antimicrobial resistance is unknown.

Acknowledgments

Field studies were funded in part by the Midwest Poultry Federation.

We acknowledge the technical assistance of Chris Bouchard, Michelle Anderson, Ellen Harbaugh, Emily Nestor, and V. Alejandra Morales from the Autonomous University of Nuevo Leon, Monterrey, Mexico. We are grateful to Deb Palmquist for performing the statistical analysis of species diversity. We thank Shawn Bearson and Alexandra Scupham for reviewing the manuscript. We are indebted to Sandy Johnson for secretarial support.

Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U.S. Department of Agriculture.

REFERENCES

1. Altekruse, S. F., and L. K. Tollefson. 2003. Human campylobacteriosis: a challenge for the veterinary profession. J. Am. Vet. Med. Assoc. 223:445-452. [PubMed]
2. Borck, B., E. M. Nielsen, and K. Pedersen. 2003. Serotypes and pulsed-field gel electrophoresis profiles of C. jejuni strains obtained from Danish turkeys. CHRO, Aarhus, Denmark.
3. Byrd, J. A., D. E. Corrier, M. E. Hume, R. H. Bailey, L. H. Stanker, and B. M. Hargis. 1998. Effect of feed withdrawal on Campylobacter in the crops of market-age broiler chickens. Avian Dis. 42:802-806. [PubMed]
4. Byrd, J. A., D. E. Corrier, M. E. Hume, R. H. Bailey, L. H. Stanker, and B. Hargis. 1998. Incidence of Campylobacter in crops of preharvest market-age broiler chickens. Poult. Sci. 77:1303-1305. [PubMed]
5. Cloak, O., and P. M. Fratamico. 2002. A multiplex polymerase chain reaction for the differentiation of Campylobacter jejuni and Campylobacter coli from a swine processing facility and characterization of isolates by pulsed-field gel electrophoresis and antibiotic resistance profiles. J. Food Prot. 65:266-273. [PubMed]
6. Corrier, D. E., J. A. Byrd, B. M. Hargis, M. E. Hume, R. H. Bailey, and L. H. Stanker. 1999. Presence of Salmonella in the crop and ceca of broiler chickens before and after preslaughter feed withdrawal. Poult. Sci. 78:45-49. [PubMed]
7. Cox, N. A., N. J. Stern, S. E. Craven, M. E. Berrang, and M. T. Musgrove. 2000. Prevalence of Campylobacter and Salmonella in the cecal droppings of turkeys during production. J. Appl. Poult. Res. 9:542-545.
8. Dickins, M. A., S. Franklin, R. Stefanova, G. E. Schutze, K. D. Eisenach, I. Wesley, and M. D. Cave. 2002. Diversity of Campylobacter isolates from retail poultry carcasses and from humans as demonstrated by pulsed-field gel electrophoresis. J. Food Prot. 65:957-962. [PubMed]
9. Hinton, A., Jr., R. J. Buhr, and K. D. Ingram. 2000. Physical, chemical and microbiological changes in the crop of broiler chickens subjected to incremental feed withdrawal. Poult. Sci. 79:212-218. [PubMed]
10. Hinton, A., Jr., R. J. Buhr, and K. D. Ingram. 2000. Physical, chemical and microbiological changes in the ceca of broiler chickens subjected to incremental feed withdrawal. Poult. Sci. 79:483-488. [PubMed]
11. Kapperud, G., G. Espeland, E. Wahl, A. Walde, H. Herikstad, S. Gustavsen, I. Tveit, O. Natas, L. Bevanger, and A. Digranes. 2003. Factors associated with increased and decreased risk of Campylobacter infection: a prospective case-control study in Norway. Am. J. Epidemiol. 158:234-242. [PubMed]
12. Lastovica, A. J., and M. B. Skirrow. 2000. Clinical significance of Campylobacter and related species other than Campylobacter jejuni and C. coli, p. 89-120. In I. Nachamkin and M. J. Blaser (ed.), Campylobacter, 2nd ed. American Society for Microbiology, Washington, D.C.
13. Linton, D., R. J. Owen, and J. Stanley. 1996. Rapid identification by PCR of the genus Campylobacter and of five Campylobacter species enteropathogenic for man and animals. Res. Microbiol. 147:707-718. [PubMed]
14. Logue, C., S. J. Sherwood, L. M. Elijah, P. A. Olah, and M. R. Dockter. 2003. The incidence of Campylobacter spp. on processed turkey from processing plants in the midwestern United States. J. Appl. Microbiol. 95:234-241. [PubMed]
15. Luechtefeld, N. W., W. L. Wang, M. J. Blaser, and L. B. Reller. 1981. Evaluation of transport and storage techniques for isolation of Campylobacter fetus subsp. jejuni from turkey cecal specimens. J. Clin. Microbiol. 13:438-443. [PMC free article] [PubMed]
16. Magurran, A. E. 1988. Ecological diversity and its measurement. Princeton University Press, Princeton, N.J.
17. May, J. D., and J. W. Deaton. 1989. Digestive tract clearance of broilers cooped or deprived of water. Poult. Digest 68:627-630. [PubMed]
18. Mead, P. S., L. Slutsker, V. Dietz, L. F. McCaig, J. S. Breesee, C. Shapiro, M. Griffin, and R. V. Tauxe. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-625. [PMC free article] [PubMed]
19. Muraoka, W., C. Gay, D. Knowles, and M. Borucki. 2003. Prevalence of Listeria monocytogenes subtypes in bulk milk of the Pacific Northwest. J. Food Prot. 66:1413-1419. [PubMed]
20. Neal, K. R., and R. C. Slack. 1995. The autumn peak in campylobacter gastro-enteritis. Are the risk factors the same for travel- and UK-acquired campylobacter infections? J. Public Health Med. 17:98-102. [PubMed]
21. Newell, D. G., J. E. Shreeve, T. Toszeghy, G. Domingue, S. Bull, T. Humphrey, and G. Mead. 2001. Changes in the carriage of Campylobacter strains by poultry carcasses during processing in abattoirs. Appl. Environ. Microbiol. 67:2636-2640. [PMC free article] [PubMed]
22. Nielsen, E. M., and N. L. Nielsen. 1999. Serotypes and typability of Campylobacter jejuni and Campylobacter coli isolated from poultry products. Int. J. Food Microbiol. 18:199-205. [PubMed]
23. Northcutt, J. K., M. W. Berrang, J. A. Dickens, D. L. Fletcher, and N. A. Cox. 2003. Effect of broiler age, feed withdrawal, and transportation on levels of coliforms, Campylobacter, Escherichia coli and Salmonella on carcasses before and after immersion chilling. Poult. Sci. 82:169-173. [PubMed]
24. Pearson, A. D., M. H. Greenwood, R. K. A. Feltham, T. D. Healing, J. Donaldson, D. M. Jones, and R. R. Colwell. 1996. Microbial ecology of Campylobacter jejuni in a United Kingdom chicken supply chain: intermittent common source, vertical transmission, and amplification by flock propagation. Appl. Environ. Microbiol. 62:4614-4620. [PMC free article] [PubMed]
25. Ribot, E., C. Fitzgerald, K. Kubota, B. Swaminathan, and T. Barrett. 2001. Rapid pulsed-field gel electrophoresis protocol for subtyping of Campylobacter jejuni. J. Clin. Microbiol. 39:1889-1894. [PMC free article] [PubMed]
26. Rivoal, K., M. Denis, G. Salvat, P. Colin, and G. Ermel. 1999. Molecular characterization of diversity of Campylobacter spp. isolates collected from a poultry slaughterhouse: analysis of cross-contamination. Lett. Appl. Microbiol. 29:370-374. [PubMed]
27. Slader, J., G. Dominique, F. Jorgensen, K. McAlpine, R. J. Owen, F. J. Bolton, and T. J. Humphrey. 2002. Impact of transport crate reuse and of catching and processing on Campylobacter and Salmonella contamination of broiler chickens. Appl. Environ. Microbiol. 68:713-719. [PMC free article] [PubMed]
28. Stern, N. J., M. R. S. Clavero, J. S. Bailey, N. A. Cox, and M. C. Robach. 1995. Campylobacter spp. in broilers on the farm and after transport. Poult. Sci. 74:937-941. [PubMed]
29. Stern, N. J., K. L. Hiett, G. A. Alfredsson, K. G. Kristinsson, J. Reiersen, H. Hardardottir, H. Briem, E. Gunnarsson, F. Georgsson, R. Lowman, E. Berndtson, A. M. Lammerding, G. M. Paoli, and M. T. Musgrove. 2003. Campylobacter spp. in Icelandic poultry operations and human disease. Epidemiol. Infect. 130:23-32. [PMC free article] [PubMed]
30. Stern, N. J., B. Wojton, and K. Kwiatek. 1992. A differential-selective medium and dry ice-generated atmosphere for recovery of Campylobacter jejuni. J. Food Prot. 55:514-517.
31. Tam, C. C., S. J. P. O'Brien, G. K. Adak, S. M. Meakins, and J. A. Frost. 2003. Campylobacter coli—an important foodborne pathogen. J. Infect. 47:28-32. [PubMed]
32. Taylor, D. N. 1992. Infections in developing countries, p. 20-30. In I. Nachamkin, M. J. Blaser, and L. Tompkins, (ed.), Campylobacter jejuni—current status and future trends. American Society for Microbiology, Washington, D.C.
33. Tran, T. T. 1998. A blood-free enrichment medium for growing Campylobacter spp. under aerobic conditions. Lett. Appl. Microbiol. 26:145-148. [PubMed]
34. U.S. Department of Agriculture. www.fsis.usda.gov/ophs/baseline/yngturk1.pdf.
35. Wabeck, C. J. 1972. Feed and water withdrawal time relationship to processing yield and potential fecal contamination of broilers. Poult. Sci. 51:1119-1121.
36. Wallace, J. S., K. N. Stanley, and K. Jones. 1998. The colonization of turkeys by thermophilic campylobacters. J. Appl. Mirobiol. 85:224-230. [PubMed]
37. Wassenaar, T. M., B. Geilhausen, and D. G. Newell. 1998. Evidence of genomic instability in Campylobacter jejuni isolated from poultry. Appl. Environ. Microbiol. 64:1816-1821. [PMC free article] [PubMed]
38. Whyte, P., J. D. Collins, K. McGill, C. Monahan, and H. O'Mahony. 2001. The effect of transportation stress on excretion rates of campylobacters in market-age broilers. Poult. Sci. 80:817-820. [PubMed]
39. Yusufu, H. I., C. Genigeorgis, T. B. Farver, and J. M. Wempe. 1983. Prevalence of Campylobacter jejuni at different sampling sites in two California turkey processing plants. J. Food Prot. 46:868-872.

Articles from Applied and Environmental Microbiology are provided here courtesy of American Society for Microbiology (ASM)
PubReader format: click here to try

Formats:

Related citations in PubMed

See reviews...See all...

Cited by other articles in PMC

See all...

Links

Recent Activity

Your browsing activity is empty.

Activity recording is turned off.

Turn recording back on

See more...