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Prevalence of Campylobacter spp. from Skin, Crop, and Intestine of Commercial Broiler Chicken Carcasses at Processing
Prevalence of Campylobacter spp. from Skin, Crop, and Intestine of Commercial Broiler Chicken Carcasses at Processing J. S. Jeffrey,*†1 K. H. Tonooka,† and J. Lozano† *Departments of Population, Health and Reproduction/Veterinary Extension; and †Poultry Health & Food Safety Laboratory, Veterinary Medicine Teaching and Research Center, University of California-Davis, 18830 Road 112, Tulare, California 93274 48% positive, and intestines were 94% positive (n = 202). Based on our results, if the intestine was positive for Campylobacter, the odds of finding a positive crop culture was 8.6 times greater, and the odds of finding a positive skin culture was 35 times greater than if the intestinal culture was negative for Campylobacter. These data suggest that the intestine was the most likely organ of those tested to be positive in postscald broiler carcasses from positive flocks. Further, if only one organ can be sampled, intestinal samples are most likely to reflect the prevalence of Campylobacter in a flock.
(Key words: Campylobacter, broiler chicken, crop, intestine, skin) 2001 Poultry Science 80:1390–1392
INTRODUCTION The presence of Campylobacter in commercial broiler flocks and on processed poultry products has been widely demonstrated (Jacobs-Rietsma, 2000). When a flock of broiler chickens becomes positive for Campylobacter, the prevalence of infection among birds is high, often reaching 100% of birds tested (Gregory et al., 1997; Pokamunski et al., 1986). Campylobacter colonizes the intestinal mucus layer in the crypts of the intestinal epithelium of chickens as a commensal organism (Beery et al., 1988). Fecal contamination of feathers and skin during transport to the slaughter facility, leakage of fecal content from the cloaca, intestinal breakage and contact with contaminated equipment, water, or other carcasses have been cited as probable sources of Campylobacter on poultry products (JacobsRietsma, 2000). Chicken skin has been shown to harbor and support the survival of C. jejuni (Lee et al., 1998). The crop has also been noted as a significant source of Campylobacter, contributing to carcass contamination (Byrd et al., 1998) and posing a greater risk than intestinal content based on the percentage recovery of Campylobacter
2001 Poultry Science Association, Inc. Received for publication November 16, 2001. Accepted for publication May 11, 2001. 1 To whom correspondence should be addressed: jjeffrey@vmtrc. ucdavis.edu. 2 CampyFDA agar, product no. 110122, Remel, Inc., Lenexa, KS 66215.
from each site. Subsequently, others have challenged this conclusion, demonstrating that the intestine was far more likely to be a source of Campylobacter contamination than the crop (Berrang et al., 2000; Newell and Wagenaar, 2000). This study compares the prevalence of positive Campylobacter isolations from skin, crop, and intestine of 202 broiler carcasses from 22 flocks and calculates the correlation between positive intestinal cultures and other positive organ cultures.
MATERIALS AND METHODS Six to 12 broiler carcasses per flock were collected just prior to evisceration at a commercial processing plant. Each carcass was placed in a sterile, sealable, plastic bag. Bagged carcasses were placed on ice in chest freezers and transported to the laboratory. Because the carcasses were hot, transport on ice resulted in cooling, but not freezing, of the carcasses. Culturing for Campylobacter took place within 4 h of collection. Three sites were cultured. Skin swabs were obtained by rubbing a sterile cotton swab on skin over the breast and corresponding interior of a plastic bag following hand massage of the whole bird from the outside of the bag for 45 s. Care was taken to avoid massaging or swabbing near the cloacal area. Swabs were streaked directly onto CampyFDA plates.2 The skin over the crop was incised with a sterile blade and reflected (pulled to the side) to expose the crop. A full thickness piece of crop (i.e., including the mucosal, muscular, and
1390
Downloaded from http://ps.oxfordjournals.org/ at Kainan University on March 18, 2015
ABSTRACT This study describes the prevalence of positive Campylobacter cultures from the skin, crop, and intestine of postscald broiler chicken carcasses at processing. Six to 12 carcasses from 22 flocks were sampled. Skin was cultured by direct plating of a cotton swab, whereas crop and intestine were cultured from tissue that was aseptically harvested and stomached in PBS before plating. Cultures were not enriched prior to plating. The methods used in this report are compared to those used by others. In this study, skin samples were 78% positive; crops were
PREVALENCE OF CAMPYLOBACTER FROM BROILER ORGANS
serosal layers), 3 to 5 cm in diameter, was excised and placed in a 2-oz. whirl-pak bag3 containing 2 mL of sterile PBS. The body cavity was opened, and a 4-to-5 cm piece of proximal ceca and adjacent ileum spanning the ileocecal junction was aseptically removed. The wall of the ceca and ileum were cut longitudinally with a sterile blade to expose the mucosal surface and then placed into a 2oz. whirl-pak bag with 2 mL PBS. Ceca and crop samples were stomached for 30 s in a Seward Stomacher 80.4 A sterile cotton-tipped swab was dipped into the sample bag and rubbed onto a CampyFDA plate that was then streaked with a sterile loop for isolation. Samples were placed in a microaerophilic chamber with a CampyPak microaerophilic system envelope5 and incubated for 48 h at 42 C. Suspect colonies were confirmed by Gram stain, catalase, oxidase, and hippurate tests.
The association between Campylobacter in the intestine and Campylobacter in crop or skin was tested using exact conditional logistic regression, stratified by flock (Cytel Software Corp., 1996). Significance of statistical associations was assigned at P ≤ 0.1. To overcome the conservatism of a discrete test without compromising on its significance level, the mid-P-value was calculated instead of the exact P-value (Lancaster, 1961). The likelihood of obtaining a positive crop or skin culture in the case of a positive intestinal culture was expressed as the odds ratio.
RESULTS AND DISCUSSION We sampled a total of 202 broilers from 22 flocks. Table 1 lists the number of positive cultures for each flock and the percentage of cultures that were positive from each organ. Within a flock, recovery of Campylobacter ranged from 0 to 100% for intestinal samples, 17 to 100% for skin samples, and 0 to 100% for crop samples. The highest prevalence of Campylobacter was from the intestine (94%), followed by the skin (78%), and the lowest prevalence was from the crop (48%). These prevalence data suggested that sampling the intestine, as opposed to the skin or crop, would produce the highest prevalence estimate for Campylobacter within a flock. The odds of having a positive skin or crop culture, if the intestine was positive for Campylobacter, was determined by statistical analysis. The results showed that the odds of having a positive skin sample were 35 times greater for carcasses with positive intestines than for carcasses with negative intestines (90% confidence interval, 5.6 to +infinity, mid-P-value = 0.0002). Similarly, the odds of having a positive crop were 8.6 times greater for carcasses with positive intestines than for carcasses that had negative intestines (90% confidence interval, 1.4 to +infinity, mid-P-value = 0.0169). Byrd et
3
Nasco, Inc. Seward Medical, London, SE1 1PP, UK. BBL CampyPak, Becton Dickinson & Co., Sparks, MD 21152.
4 5
al. (1998) reported 62% prevalence for Campylobacter from crop samples (n = 359) and 4% from ceca samples. However, when the same analysis was applied to the study by Byrd et al. (1998), a similar trend for higher crop prevalence in carcasses with positive intestines was demonstrated. In flocks in which samples were taken from intestine and crop, the odds of having a positive crop were 5.5 times greater for chickens with positive intestinal samples than for chickens with negative intestinal samples (90% confidence interval, 0.7 to +infinity, mid-P-value = 0.08). Epidemiologic studies suggest that flocks that are positive for Campylobacter have a high infection rate among individuals, evidenced by a high percentage of recovery from cecal droppings or cloacal swabs (Pokamunski et al., 1986; Gregory et al., 1997). It is possible that differences in culture techniques may account for the reduced recovery of Campylobacter in the study by Byrd et al. (1998), as compared to this study and others (Berrang et al., 2000; Newell and Wagenaar, 2000). In the study by Byrd et al. (1998); the ceca were incubated in enrichment media and subcultured onto selective media for Campylobacter. Enrichment culture of the cecal contents can result in overgrowth of Campylobacter colonies, even when subcultured to selective media (Aquino et al., 1996). In the current study, 48% of crops were positive for Campylobacter (n = 202) using a culture technique similar to that reported by Berrang et al. (2000). In contrast, Berrang et al. (2000) found 100% of crop samples (n = 18) were positive for Campylobacter with mean counts of log 3.1 cfu/g of crop tested. A possible explanation is that, in this study, only crop tissue without contents were cultured, whereas Berrang et al. (2000) and Byrd et al. (1998) cultured the entire crop and crop contents. Coprophagy in feed-withdrawn broilers could account for Campylobacterpositive crop contents and more positive cultures. Evidence for actual crop colonization has not been offered in previous studies. In the present study, skin samples from carcasses obtained after scalding and picking were 78% positive for Campylobacter as compared to Berrang et al. (2000), in which carcasses sampled prior to scalding and picking were 100% positive. Processing has been shown to reduce levels of bacterial contamination on carcasses. A 2 log reduction in Campylobacter from neck skin following processing has been observed (Mead et al., 1995), and as much as a 1.4 log reduction between prescald versus postpick broilers has been reported (Izat et al., 1988). Other contrasts in sample collection, size, technique, and culture methods may account for the variability between studies. For example, Byrd et al. (1998) sampled market-age broilers on the farm, diluted samples in distilled water prior to stomaching, and enriched samples in Bolton broth before plating. Berrang et al. (2000) sampled broiler carcasses off the kill line prior to scalding, diluted samples in PBS prior to stomaching, and did not enrich prior to plating. In the present study, broiler carcasses were sampled after scalding and picking, samples were diluted in PBS prior to stomaching, and were not enriched prior to plating.
Downloaded from http://ps.oxfordjournals.org/ at Kainan University on March 18, 2015
Statistical Analysis
1391
1392
JEFFREY ET AL. TABLE 1. Prevalence of positive Campylobacter jejuni cultures from skin, crop, and intestine in flocks that were positive for C. jejuni Skin1
%2
Crop
%
Intestine
%
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 Total
4/12 12/12 12/12 11/12 6/12 11/12 8/12 4/12 5/12 11/12 10/10 8/10 6/8 6/6 6/6 6/6 6/6 6/6 6/6 1/6 6/6 6/6 157/202
(33) (100) (100) (92) (50) (92) (67) (33) (42) (92) (100) (80) (67) (100) (100) (100) (100) (100) (100) (17) (100) (100) (78)
3/12 5/12 12/12 3/12 0/12 6/12 1/12 3/12 5/12 5/12 4/10 6/10 4/8 6/6 6/6 6/6 6/6 4/6 1/6 0/6 5/6 5/6 96/202
(25) (42) (100) (25) (0) (50) (8) (25) (42) (42) (40) (60) (50) (100) (100) (100) (100) (67) (17) (0) (84) (84) (48)
12/12 12/12 12/12 11/12 12/12 11/12 12/12 11/12 8/12 12/12 10/10 10/10 8/8 6/6 6/6 6/6 6/6 6/6 6/6 0/6 6/6 6/6 189/202
(100) (100) (100) (92) (100) (92) (100) (92) (67) (100) (100) (100) (100) (100) (100) (100) (100) (100) (100) (0) (100) (100) (94)
1
Number of positive cultures per total cultures. Percentage positive cultures.
2
In conclusion, it appears that recovery of Campylobacter from the crop may be improved by sampling the crop contents along with the crop. Direct plating appears sufficiently sensitive for identifying positive intestine samples. These data suggest that the intestine (versus crop or skin) is most likely to be positive for Campylobacter in postscald broiler carcasses from positive flocks. Further, if only one organ can be tested, intestinal samples are most likely to reflect the prevalence of Campylobacter in a flock.
ACKNOWLEDGMENTS The authors thank Randall Singer for invaluable assistance with carcass collection and Rob Atwill for his assistance with logistic regression analysis of the data.
REFERENCES Aquino, M. C., J. C. Carvalho, A. Tibana, and R. M. Franco, 1996. Campylobacter jejuni/coli: Methodology of isolation and possible interfering factors in primary culture. J. Food Prot. 59:42–432. Beery, J. T., M. B. Hugdahl, and M. P. Doyle, 1988. Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl. Environ. Microbiol. 54:2365–2370. Berrang, M. E., R. J. Buhr, and J. A. Cason, 2000. Campylobacter recovery from external and internal organs of commercial broiler carcass prior to scalding. Poultry Sci. 79:286–290.
Byrd, J. A., D. E. Corrier, M. E. Hume, R. H. Bailey, L. H. Stanker, and B. M. Hargis, 1998. Incidence of Campylobacter in crops of preharvest market-age broiler chickens. Poultry Sci. 77:1303–1305. Cytel Software Corp., 1996. LogXact for Windows: Logistic Regression Software Featuring Exact Methods, 1996. Cytel Software Corp., Cambridge, MA. Gregory, E., H. Barnhart, D. W. Dreesen, N. J. Stern, and J. L. Corn, 1997. Epidemiological study of Campylobacter spp. in broilers: Source, time of colonization, and prevalence. Avian Dis. 41:890–898. Izat, A. L., F. A. Gardner, J. H. Denton,and F. A. Golan, 1988. Incidence and level of Campylobacter jejuni in broiler processing. Poultry Sci. 67:1568–1572. Jacobs-Rietsma, W., 2000. Campylobacter in the food supply. Pages 467–482 in: Campylobacter. 2nd ed. I. Nachamkin and M. J. Blaser, ed. American Society of Microbiology Press, Washington, DC. Lancaster, H. O., 1961. Significance tests in discrete distributions. J. Am. Stat. Assoc. 56:223–234. Lee, A., S. C. Smith, and P. J. Coloe, 1998. Survival and growth of Campylobacter jejuni after artificial inoculation onto chicken skin as a function of temperature and packaging conditions. J. Food Prot. 61:1609–1614. Mead, G. C., W. R. Hudson, and M. H. Hinton, 1995. Effect of changes in processing to improve hygiene control on contamination of poultry carcasses with Campylobacter. Epidemiol. Infect. 115:495–500. Newell, D. G., J. A. Wagenaar, 2000. Poultry infections and their control at the farm level. Pages 497–510 in: Campylobacter, 2nd ed. I. Nachamkin and M. J. Blaser, ed. American Society of Microbiology Press, Washington, DC. Pokamunski, S., N. Kass, E. Borochovich, B. Marantz, and M. Rogol. 1986. Incidence of Campylobacter spp. in broiler flocks from hatching to slaughter. Avian Pathol. 15:83–92.
Downloaded from http://ps.oxfordjournals.org/ at Kainan University on March 18, 2015
Flock
(Key words: Campylobacter, broiler chicken, crop, intestine, skin) 2001 Poultry Science 80:1390–1392
INTRODUCTION The presence of Campylobacter in commercial broiler flocks and on processed poultry products has been widely demonstrated (Jacobs-Rietsma, 2000). When a flock of broiler chickens becomes positive for Campylobacter, the prevalence of infection among birds is high, often reaching 100% of birds tested (Gregory et al., 1997; Pokamunski et al., 1986). Campylobacter colonizes the intestinal mucus layer in the crypts of the intestinal epithelium of chickens as a commensal organism (Beery et al., 1988). Fecal contamination of feathers and skin during transport to the slaughter facility, leakage of fecal content from the cloaca, intestinal breakage and contact with contaminated equipment, water, or other carcasses have been cited as probable sources of Campylobacter on poultry products (JacobsRietsma, 2000). Chicken skin has been shown to harbor and support the survival of C. jejuni (Lee et al., 1998). The crop has also been noted as a significant source of Campylobacter, contributing to carcass contamination (Byrd et al., 1998) and posing a greater risk than intestinal content based on the percentage recovery of Campylobacter
2001 Poultry Science Association, Inc. Received for publication November 16, 2001. Accepted for publication May 11, 2001. 1 To whom correspondence should be addressed: jjeffrey@vmtrc. ucdavis.edu. 2 CampyFDA agar, product no. 110122, Remel, Inc., Lenexa, KS 66215.
from each site. Subsequently, others have challenged this conclusion, demonstrating that the intestine was far more likely to be a source of Campylobacter contamination than the crop (Berrang et al., 2000; Newell and Wagenaar, 2000). This study compares the prevalence of positive Campylobacter isolations from skin, crop, and intestine of 202 broiler carcasses from 22 flocks and calculates the correlation between positive intestinal cultures and other positive organ cultures.
MATERIALS AND METHODS Six to 12 broiler carcasses per flock were collected just prior to evisceration at a commercial processing plant. Each carcass was placed in a sterile, sealable, plastic bag. Bagged carcasses were placed on ice in chest freezers and transported to the laboratory. Because the carcasses were hot, transport on ice resulted in cooling, but not freezing, of the carcasses. Culturing for Campylobacter took place within 4 h of collection. Three sites were cultured. Skin swabs were obtained by rubbing a sterile cotton swab on skin over the breast and corresponding interior of a plastic bag following hand massage of the whole bird from the outside of the bag for 45 s. Care was taken to avoid massaging or swabbing near the cloacal area. Swabs were streaked directly onto CampyFDA plates.2 The skin over the crop was incised with a sterile blade and reflected (pulled to the side) to expose the crop. A full thickness piece of crop (i.e., including the mucosal, muscular, and
1390
Downloaded from http://ps.oxfordjournals.org/ at Kainan University on March 18, 2015
ABSTRACT This study describes the prevalence of positive Campylobacter cultures from the skin, crop, and intestine of postscald broiler chicken carcasses at processing. Six to 12 carcasses from 22 flocks were sampled. Skin was cultured by direct plating of a cotton swab, whereas crop and intestine were cultured from tissue that was aseptically harvested and stomached in PBS before plating. Cultures were not enriched prior to plating. The methods used in this report are compared to those used by others. In this study, skin samples were 78% positive; crops were
PREVALENCE OF CAMPYLOBACTER FROM BROILER ORGANS
serosal layers), 3 to 5 cm in diameter, was excised and placed in a 2-oz. whirl-pak bag3 containing 2 mL of sterile PBS. The body cavity was opened, and a 4-to-5 cm piece of proximal ceca and adjacent ileum spanning the ileocecal junction was aseptically removed. The wall of the ceca and ileum were cut longitudinally with a sterile blade to expose the mucosal surface and then placed into a 2oz. whirl-pak bag with 2 mL PBS. Ceca and crop samples were stomached for 30 s in a Seward Stomacher 80.4 A sterile cotton-tipped swab was dipped into the sample bag and rubbed onto a CampyFDA plate that was then streaked with a sterile loop for isolation. Samples were placed in a microaerophilic chamber with a CampyPak microaerophilic system envelope5 and incubated for 48 h at 42 C. Suspect colonies were confirmed by Gram stain, catalase, oxidase, and hippurate tests.
The association between Campylobacter in the intestine and Campylobacter in crop or skin was tested using exact conditional logistic regression, stratified by flock (Cytel Software Corp., 1996). Significance of statistical associations was assigned at P ≤ 0.1. To overcome the conservatism of a discrete test without compromising on its significance level, the mid-P-value was calculated instead of the exact P-value (Lancaster, 1961). The likelihood of obtaining a positive crop or skin culture in the case of a positive intestinal culture was expressed as the odds ratio.
RESULTS AND DISCUSSION We sampled a total of 202 broilers from 22 flocks. Table 1 lists the number of positive cultures for each flock and the percentage of cultures that were positive from each organ. Within a flock, recovery of Campylobacter ranged from 0 to 100% for intestinal samples, 17 to 100% for skin samples, and 0 to 100% for crop samples. The highest prevalence of Campylobacter was from the intestine (94%), followed by the skin (78%), and the lowest prevalence was from the crop (48%). These prevalence data suggested that sampling the intestine, as opposed to the skin or crop, would produce the highest prevalence estimate for Campylobacter within a flock. The odds of having a positive skin or crop culture, if the intestine was positive for Campylobacter, was determined by statistical analysis. The results showed that the odds of having a positive skin sample were 35 times greater for carcasses with positive intestines than for carcasses with negative intestines (90% confidence interval, 5.6 to +infinity, mid-P-value = 0.0002). Similarly, the odds of having a positive crop were 8.6 times greater for carcasses with positive intestines than for carcasses that had negative intestines (90% confidence interval, 1.4 to +infinity, mid-P-value = 0.0169). Byrd et
3
Nasco, Inc. Seward Medical, London, SE1 1PP, UK. BBL CampyPak, Becton Dickinson & Co., Sparks, MD 21152.
4 5
al. (1998) reported 62% prevalence for Campylobacter from crop samples (n = 359) and 4% from ceca samples. However, when the same analysis was applied to the study by Byrd et al. (1998), a similar trend for higher crop prevalence in carcasses with positive intestines was demonstrated. In flocks in which samples were taken from intestine and crop, the odds of having a positive crop were 5.5 times greater for chickens with positive intestinal samples than for chickens with negative intestinal samples (90% confidence interval, 0.7 to +infinity, mid-P-value = 0.08). Epidemiologic studies suggest that flocks that are positive for Campylobacter have a high infection rate among individuals, evidenced by a high percentage of recovery from cecal droppings or cloacal swabs (Pokamunski et al., 1986; Gregory et al., 1997). It is possible that differences in culture techniques may account for the reduced recovery of Campylobacter in the study by Byrd et al. (1998), as compared to this study and others (Berrang et al., 2000; Newell and Wagenaar, 2000). In the study by Byrd et al. (1998); the ceca were incubated in enrichment media and subcultured onto selective media for Campylobacter. Enrichment culture of the cecal contents can result in overgrowth of Campylobacter colonies, even when subcultured to selective media (Aquino et al., 1996). In the current study, 48% of crops were positive for Campylobacter (n = 202) using a culture technique similar to that reported by Berrang et al. (2000). In contrast, Berrang et al. (2000) found 100% of crop samples (n = 18) were positive for Campylobacter with mean counts of log 3.1 cfu/g of crop tested. A possible explanation is that, in this study, only crop tissue without contents were cultured, whereas Berrang et al. (2000) and Byrd et al. (1998) cultured the entire crop and crop contents. Coprophagy in feed-withdrawn broilers could account for Campylobacterpositive crop contents and more positive cultures. Evidence for actual crop colonization has not been offered in previous studies. In the present study, skin samples from carcasses obtained after scalding and picking were 78% positive for Campylobacter as compared to Berrang et al. (2000), in which carcasses sampled prior to scalding and picking were 100% positive. Processing has been shown to reduce levels of bacterial contamination on carcasses. A 2 log reduction in Campylobacter from neck skin following processing has been observed (Mead et al., 1995), and as much as a 1.4 log reduction between prescald versus postpick broilers has been reported (Izat et al., 1988). Other contrasts in sample collection, size, technique, and culture methods may account for the variability between studies. For example, Byrd et al. (1998) sampled market-age broilers on the farm, diluted samples in distilled water prior to stomaching, and enriched samples in Bolton broth before plating. Berrang et al. (2000) sampled broiler carcasses off the kill line prior to scalding, diluted samples in PBS prior to stomaching, and did not enrich prior to plating. In the present study, broiler carcasses were sampled after scalding and picking, samples were diluted in PBS prior to stomaching, and were not enriched prior to plating.
Downloaded from http://ps.oxfordjournals.org/ at Kainan University on March 18, 2015
Statistical Analysis
1391
1392
JEFFREY ET AL. TABLE 1. Prevalence of positive Campylobacter jejuni cultures from skin, crop, and intestine in flocks that were positive for C. jejuni Skin1
%2
Crop
%
Intestine
%
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 Total
4/12 12/12 12/12 11/12 6/12 11/12 8/12 4/12 5/12 11/12 10/10 8/10 6/8 6/6 6/6 6/6 6/6 6/6 6/6 1/6 6/6 6/6 157/202
(33) (100) (100) (92) (50) (92) (67) (33) (42) (92) (100) (80) (67) (100) (100) (100) (100) (100) (100) (17) (100) (100) (78)
3/12 5/12 12/12 3/12 0/12 6/12 1/12 3/12 5/12 5/12 4/10 6/10 4/8 6/6 6/6 6/6 6/6 4/6 1/6 0/6 5/6 5/6 96/202
(25) (42) (100) (25) (0) (50) (8) (25) (42) (42) (40) (60) (50) (100) (100) (100) (100) (67) (17) (0) (84) (84) (48)
12/12 12/12 12/12 11/12 12/12 11/12 12/12 11/12 8/12 12/12 10/10 10/10 8/8 6/6 6/6 6/6 6/6 6/6 6/6 0/6 6/6 6/6 189/202
(100) (100) (100) (92) (100) (92) (100) (92) (67) (100) (100) (100) (100) (100) (100) (100) (100) (100) (100) (0) (100) (100) (94)
1
Number of positive cultures per total cultures. Percentage positive cultures.
2
In conclusion, it appears that recovery of Campylobacter from the crop may be improved by sampling the crop contents along with the crop. Direct plating appears sufficiently sensitive for identifying positive intestine samples. These data suggest that the intestine (versus crop or skin) is most likely to be positive for Campylobacter in postscald broiler carcasses from positive flocks. Further, if only one organ can be tested, intestinal samples are most likely to reflect the prevalence of Campylobacter in a flock.
ACKNOWLEDGMENTS The authors thank Randall Singer for invaluable assistance with carcass collection and Rob Atwill for his assistance with logistic regression analysis of the data.
REFERENCES Aquino, M. C., J. C. Carvalho, A. Tibana, and R. M. Franco, 1996. Campylobacter jejuni/coli: Methodology of isolation and possible interfering factors in primary culture. J. Food Prot. 59:42–432. Beery, J. T., M. B. Hugdahl, and M. P. Doyle, 1988. Colonization of gastrointestinal tracts of chicks by Campylobacter jejuni. Appl. Environ. Microbiol. 54:2365–2370. Berrang, M. E., R. J. Buhr, and J. A. Cason, 2000. Campylobacter recovery from external and internal organs of commercial broiler carcass prior to scalding. Poultry Sci. 79:286–290.
Byrd, J. A., D. E. Corrier, M. E. Hume, R. H. Bailey, L. H. Stanker, and B. M. Hargis, 1998. Incidence of Campylobacter in crops of preharvest market-age broiler chickens. Poultry Sci. 77:1303–1305. Cytel Software Corp., 1996. LogXact for Windows: Logistic Regression Software Featuring Exact Methods, 1996. Cytel Software Corp., Cambridge, MA. Gregory, E., H. Barnhart, D. W. Dreesen, N. J. Stern, and J. L. Corn, 1997. Epidemiological study of Campylobacter spp. in broilers: Source, time of colonization, and prevalence. Avian Dis. 41:890–898. Izat, A. L., F. A. Gardner, J. H. Denton,and F. A. Golan, 1988. Incidence and level of Campylobacter jejuni in broiler processing. Poultry Sci. 67:1568–1572. Jacobs-Rietsma, W., 2000. Campylobacter in the food supply. Pages 467–482 in: Campylobacter. 2nd ed. I. Nachamkin and M. J. Blaser, ed. American Society of Microbiology Press, Washington, DC. Lancaster, H. O., 1961. Significance tests in discrete distributions. J. Am. Stat. Assoc. 56:223–234. Lee, A., S. C. Smith, and P. J. Coloe, 1998. Survival and growth of Campylobacter jejuni after artificial inoculation onto chicken skin as a function of temperature and packaging conditions. J. Food Prot. 61:1609–1614. Mead, G. C., W. R. Hudson, and M. H. Hinton, 1995. Effect of changes in processing to improve hygiene control on contamination of poultry carcasses with Campylobacter. Epidemiol. Infect. 115:495–500. Newell, D. G., J. A. Wagenaar, 2000. Poultry infections and their control at the farm level. Pages 497–510 in: Campylobacter, 2nd ed. I. Nachamkin and M. J. Blaser, ed. American Society of Microbiology Press, Washington, DC. Pokamunski, S., N. Kass, E. Borochovich, B. Marantz, and M. Rogol. 1986. Incidence of Campylobacter spp. in broiler flocks from hatching to slaughter. Avian Pathol. 15:83–92.
Downloaded from http://ps.oxfordjournals.org/ at Kainan University on March 18, 2015
Flock