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Poult Sci 2006. 85:1570-1575
© 2006 Poultry Science Association
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GENETICS

Bacteriocins Reduce Campylobacter Colonization and Alter Gut Morphology in Turkey Poults1,2

K. Cole*, M. B. Farnell{dagger},1, A. M. Donoghue{dagger},1, N. J. Stern§,1, E. A. Svetoch{ddagger}, B. N. Eruslanov{ddagger}, L. I. Volodina{ddagger}, Y. N. Kovalev{ddagger}, V. V. Perelygin{ddagger}, E. V. Mitsevich{ddagger}, I. P. Mitsevich{ddagger}, V. P. Levchuk{ddagger}, V. D. Pokhilenko{ddagger}, V. N. Borzenkov{ddagger}, O. E. Svetoch{ddagger}, T. Y. Kudryavtseva{ddagger}, I. Reyes-Herrera*, P. J. Blore*, F. Solis de los Santos* and D. J. Donoghue*,3

* Department of Poultry Science, University of Arkansas, Fayetteville 72701;{dagger} Poultry Production and Product Safety Research Unit, USDA-ARS, Fayetteville, AR 72701;{ddagger} State Research Center for Applied Microbiology, Obolensk, Russian Federation; and § Poultry Microbiological Safety Research Unit, Russell Research Center, USDA-ARS, Athens, GA 30604

3 Corresponding author: ddonogh{at}uark.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Campylobacter is a leading cause of foodborne illness in the United States. Recent evidence has demonstrated that bacteriocins produced by Bacillus circulans and Paenibacillus polymyxa reduce cecal Campylobacter colonization in broiler chickens infected with Campylobacter jejuni. As Campylobacter coli is the most prevalent Campylobacter isolate recovered in turkeys, the objectives of the present study were to evaluate the efficacy of these bacteriocins against C. coli colonization and their influence on the gastrointestinal architecture of young turkeys. In 3 separate trials, a total of 135 day-of-hatch poults (n = 45/trial) were orally challenged on d 3 with approximately 106 cfu of a mixture of 3 C. coli isolates. Immediately before bacteriocin treatment (d 10), cecal Campylobacter concentrations averaged 1.1 x 107 cfu/ g of cecal contents (n = 15/trial). On d 10 to 12 posthatch, 2 bacteriocin treatment groups were given free access to feed supplemented with purified, microencapsulated bacteriocins, whereas the positive control treatment group had access to untreated feed (n = 10/treatment group per trial). At the end of the 3-d dosing period, ceca and duodenal loops were collected for analysis. In each of the 3 separate trials, treatment with bacteriocin eliminated detectable ceca Campylobacter concentrations (detection limit, 1 x 102 cfu/g of cecal contents) vs. controls (1.0 x 106 cfu of Campylobacter/g of cecal contents). Duodenum crypt depth and goblet cell numbers were also reduced in turkeys treated with either bacteriocin vs. controls (P < 0.05). The dynamic reduction in crypt depth and goblet cell density in turkeys dosed with bacteriocin may provide clues to how bacteriocins inhibit enteric Campylobacter.

Key Words: Campylobacter • ceca • bacteriocin • turkey • gastrointestinal tract


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Campylobacter is one of the leading bacterial causes of human foodborne illness in the United States (Centers for Disease Control and Prevention, 2005). A substantial number of poultry and retail poultry products are contaminated with Campylobacter, with isolation rates approaching 100% (Stern et al., 2001; Zhao et al., 2001; Newell and Fearnley, 2003). Epidemiological evidence has emphasized the importance of poultry products as a significant source of human Campylobacter infection (Jacobs-Reitsma, 2000; Corry and Attabay, 2001). Therefore, the reduction or elimination of this organism in commercial poultry flocks should greatly reduce the incidence of human Campylobacter infection (Jacobs-Reitsma, 1997; Sahin et al., 2002).

One approach to reduce Campylobacter colonization in preharvest poultry is the use of competitive exclusion (CE) cultures (Stern et al., 2001). Competitive exclusion is the administration of nonpathogenic enteric microflora that may compete with and reduce enteric pathogens. Competitive exclusion, first described by Nurmi and Rantala (1973) has been used to successfully control Salmonella contamination in poultry (Corrier et al., 1995; Bielke et al., 2003). Unfortunately, the use of CE cultures has not consistently reduced Campylobacter colonization (Stern et al., 2001; Mead, 2002). Through efforts to improve the effectiveness of CE cultures against Campylobacter, researchers have observed that certain bacteria produce metabolites that are inhibitory to Campylobacter growth in vitro (Schoeni and Doyle, 1992; Newell and Wagenaar, 2000; Svetoch et al., 2005). These metabolites, identified as bacteriocins, are proteins naturally produced by bacteria that kill or inhibit the growth of other bacteria (Cleveland et al., 2001). Unlike antibiotics, bacteriocins have no known toxic effects and have a narrow killing spectrum (Riley and Wertz, 2002). The use of bacteriocins as antimicrobials has already been applied in food preservation; as the bacteriocin nisin is considered a generally recognized as safe compound and is approved for use in foods (Joeger, 2003).

Recently, Svetoch et al. (2005) found that bacteriocins produced by certain strains of Bacillus circulans and Paenibacillus polymyxa were inhibitory to Campylobacter growth in vitro. In a follow-up study, these purified bacteriocins, microencapsulated and administered via feed, reduced cecal Campylobacter colonization in young broiler chickens experimentally infected with Campylobacter jejuni (Stern et al., 2005). However, the efficacy of these bacteriocins in turkeys has not been determined. Furthermore, the influence of bacteriocins on enteric histology has not been evaluated. Therefore, the objectives in the present study were to evaluate the efficacy of these bacteriocins against Campylobacter coli colonization and to evaluate the influence of bacteriocins on the gastrointestinal morphology in turkeys.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Bacteriocins
Bacteria producing the bacteriocins were recovered from the intestinal tracts of broiler chickens. Associated bacteriocin purification and microencapsulation procedures have been previously described in detail (Stern et al., 2005; Svetoch et al., 2005). Briefly, bacteriocin B602 was secreted by the isolate P. polymyxa (NRRL B-30509), whereas bacteriocin OR7 was secreted by the isolate Lactobacillus salivarius (NRRL B-35014; N. J. Stern, E. A. Svetoch, B. V. Eruslanov, V. V. Perelygin, E. V. Mitsevich, I. P. Mitsevich, V. D. Pokhilenko, V. P. Levchuk, and O. E. Svetoch, unpublished data). Each bacteriocin was precipitated with saturated ammonium sulfate, dissolved, dialyzed, and purified by Superose 12HR 16/50 column chromatography (Pharmacia, Uppsala, Sweden), followed by passing the protein over a 300-mL SP Sepharose Fast Flow column (GE Healthcare Bio-Sciences Corp., Piscataway, NJ). The purified bacteriocins were then mixed with polyvinylpyrrolidone powder to produce microencapsulated bacteriocins, which were used to produce a medicated feed. The final concentration of each bacteriocin was 250 mg/kg of feed.

Campylobacter Isolates and Growth Conditions
Poults used in this study were challenged with a solution containing an equal combination of 3 C. coli isolates, 2 wild-type turkey isolates, and an American Type Culture Collection isolate 43481. A frozen culture of each isolate was inoculated into 9.0 mL of Campylobacter enrichment broth and grown individually for 24 h at 42°C in a microaerobic environment (5% O2, 10% CO2, 85% N2), as previously described (Cole et al., 2004). After 24 h, 10 uL of each culture was passed into another 9.0 mL of Campylobacter enrichment broth and grown for 24 h in a microaerophilic environment. After 24 h, each culture was combined in a 50-mL conical tube and used for poult inoculation (see below).

Experimental Design
A total of 135 poults were used in this study. In each of 3 separate trials, 45 day-of-hatch poults were obtained from a local commercial hatchery and randomly allocated to 1 of 3 treatment groups: positive control, bacteriocin B602, or bacteriocin OR7 (n = 15/pen). Each treatment group was housed in an individual floor pen on fresh pine litter and provided water and feed ad libitum. Three days posthatch, all poults in each treatment group were inoculated, via oral gavage, with 0.25 mL of a solution containing a mixture of 3 C. coli isolates (approximately 106 cfu/mL), as described previously (Farnell et al., 2005). Immediately before bacteriocin treatment (d 10), 5 of the 15 birds from each of the 3 treatment pens (n = 15/trial) in each trial were euthanized and ceca was collected for Campylobacter enumeration. On d 10 to 12 posthatch, the 2 bacteriocin treatment groups were given free access to feed supplemented with purified, microencapsulated bacteriocins, whereas the positive controls had access to untreated feed. At the end of the 3-d dosing period, ceca were collected from all remaining turkeys (n = 10/pen; 30/trial) for Campylobacter enumeration, and their duodenal loops were collected for morphometric analysis.

Enumeration of Campylobacter in Cecal Contents
The cecal contents of each poult were serially diluted 1:9 in buffered phosphate diluent, and 100 uL of each dilution was plated onto Campylobacter Line agar plates (Line, 2001). The plates were incubated for 48 h at 42°C in a microaerobic environment. After incubation, characteristic colonies were confirmed as Campylobacter using a commercial latex agglutination test kit (Panbio Inc., Columbia, MD). The direct counts were converted to log10 colony-forming units per gram of cecal contents. The detection limit for Campylobacter was 1 x 102 cfu/g of cecal contents.

Morphometric Analysis of the Gut
The gastrointestinal morphometric variables evaluated were villus height, villus surface area, lamina propria thickness, villus crypt depth, and goblet cell number per villus from the duodenum. A 1-cm segment of the midpoint of the duodenum was removed and fixed in 10% buffered formalin for 72 h. Each segment was then embedded in paraffin, and a 2-µm section of each sample was placed on a glass slide and stained with hematoxylin and eosin for examination with a light microscope (Sakamoto et al., 2000). Morphological parameters were measured using the Image-Pro Plus Version 4.5 software package (Media Cybernetics Inc., Silver Springs, MD), as previously described (Solis de Los Santos et al., 2005). Ten replicate measurements for each variable studied were taken from each poult. Briefly, the villus height was measured from the top of the villus to the top of the lamina propria. Surface area was calculated using the formula surface area = (2{pi}) (VW/2) (VL) where VW = villus width and VL = villus length (Sakamoto et al., 2000). The lamina propria thickness was measured in the space between the base of the villus and the top of the muscularis mucosa. Crypt depth was measured from the base to the region of transition between the crypt and villus (Aptekmann et al., 2001). Goblet cell number was determined by counting the number of goblet cells in 10 individual histologically well-oriented villi (Yunus et al., 2005).

Statistical Analysis
Data were subjected to ANOVA using the GLM procedure of SAS (SAS Institute, 2003). Treatment means were partitioned by LSMEANS analysis. A probability of P < 0.05 was required for statistical significance.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Campylobacter Colonization
Immediately before bacteriocin treatment (d 10), the 5 birds collected from each of the pens used in this study (n = 15/trial) were colonized with Campylobacter. The average cecal Campylobacter numbers were 2.0 x 107, 8.2 x 104, or 1.3 x 107 cfu/g of cecal contents for the turkeys from trials 1, 2, or 3, respectively. In each of the 3 separate trials, the 3-d treatment with bacteriocins eliminated detectable ceca Campylobacter concentrations in all turkeys (detection limit, 1 x 102 cfu/g of cecal contents) when compared with the unmedicated positive control groups (P < 0.01; Table 1Go).


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  		Table 1. Reduction of cecal Campylobacter concentrations and incidence in commercial turkey poults treated with bacteriocins1
 
Morphometric Analysis of the Gut
Administration of bacteriocins reduced the duodenum crypt depth (Figure 1Go) and number of goblet cells (Figure 2Go) in comparison with the untreated positive control groups in each of the 3 separate trials. Treatment with bacteriocin OR7 produced a greater reduction in goblet cell numbers in all 3 trials when compared with bacteriocin B602 (Figure 2Go). Duodenum villus height did not differ among treatment groups, except in trial 3, in which treatment with bacteriocin OR7 reduced the villus height vs. controls (Table 2Go). Duodenum villus surface area was lower for turkeys treated with bacteriocin OR7 in trials 1 and 2 vs. controls (Table 2Go). Lamina propria thickness was inconsistent among the treatment groups, with lower values for turkeys treated with bacteriocin B602 compared with controls in trials 1 and 3 and for turkeys treated with bacteriocin OR7 in trials 1 and 2 (Table 2Go).


Figure 1
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  		Figure 1. Effect of bacteriocins on duodenal crypt depth in turkey poults after oral challenge with Campylobacter. Values are means ± SEM, representing 10 birds/group and 10 measurements/parameter per bird from 3 separate trials. In each trial, poults were orally challenged 3 d posthatch with approximately 106 cfu of a mixture of 3 Campylobacter coli isolates. On d 10 to 12 posthatch, the 2 treatment groups were fed a commercial diet containing bacteriocins, and the positive control group was fed the same commercial diet without bacteriocins. On d 13 posthatch (10 d postchallenge), turkeys were euthanized, and duodenal loops were collected for morphometric analysis. Means with no common superscripts differ significantly (P < 0.05) between treatments within trials.

 

Figure 2
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  		Figure 2. Effect of bacteriocins on duodenal goblet cell density in turkey poults after oral challenge with Campylobacter. Values are mean ± SEM, representing 10 birds/treatment group and 10 measurements/ parameter per bird from 3 separate trials. In each trial, poults were orally challenged 3 d posthatch with approximately 106 cfu of a mixture of 3 Campylobacter coli isolates. On d 10 to 12 posthatch, the 2 treatment groups were fed a commercial diet containing bacteriocins, and the positive control group was fed the same commercial diet without bacteriocins. On d 13 posthatch (10 d postchallenge), turkeys were euthanized, and duodenal loops were collected for morphometric analysis. Means with no common superscript differ significantly (P < 0.05) between treatments within trials.

 

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  		Table 2. Effects of bacteriocin treatment on duodenal morphology of turkey poults after oral Campylobacter challenge1
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
In the present study, oral administration of the purified microencapsulated bacteriocins eliminated detectable cecal Campylobacter colonization in young turkeys in 3 separate trials. These findings are consistent with previous studies in which treatment with these same bacteriocins eliminated detectable Campylobacter in young broiler chickens infected with C. jejuni (Stern et al., 2005; N. J. Stern, E. A. Svetoch, B. V. Eruslanov, V. V. Perelygin, E. V. Mitsevich, I. P. Mitsevich, V. D. Pokhilenko, V. P. Levchuk, and O. E. Svetoch, unpublished data).

One of the possible mechanisms by which bacteriocins reduce Campylobacter colonization in poultry is by direct bactericidial or bacteriostatic activity. Bacteriocins have been demonstrated to inhibit or kill other foodborne pathogens, such as Listeria, Clostridium, and Salmonella, and are used in food processing and preservation (Daly et al., 1970; Tagg et al., 1976; Natrajan and Sheldon, 2000). Bacteriocin-like compounds have also been shown to have direct antimicrobial activity, in vitro, against Campylobacter (Schoeni and Doyle, 1992; Morency et al., 2001; Chaveerach et al., 2004), including the bacteriocins used in this study (Svetoch et al., 2005; N. J. Stern, E. A. Svetoch, B. V. Eruslanov, V. V. Perelygin, E. V. Mitsevich, I. P. Mitsevich, V. D. Pokhilenko, V. P. Levchuk, and O. E. Svetoch, unpublished data).

Another possible mechanism of action of the bacteriocins is physical or functional alteration of Campylobacter colonization sites. Use of either bacteriocin in this study reduced both duodenal crypt depth and goblet cell numbers. To our knowledge, this is the first study demonstrating that altering the gastrointestinal tract eliminated detectable Campylobacter colonization. Previous research has demonstrated that the mucus layer of intestinal crypts is an important niche for Campylobacter colonization in poultry (Beery et al., 1988; Meinersmann et al., 1991). The ability of Campylobacter to sequester itself within these crypts may be an important strategy to avoid intervention efforts, such as the use of antibiotics or CE cultures (Mead, 2002; Zhang et al., 2003; Bywater, 2004; Mead, 2004; Farnell et al., 2005). The reduction in crypt depth may have multiple effects on Campylobacter colonization. For example, it is possible the smaller crypt size, and subsequent greater exposure to the lumen, may change the nutrient or chemical environment (e.g., increased oxygen tension), limiting Campylobacter growth and colonization. It is also possible that different microflora will colonize these smaller crypts, with the ability to outcompete Campylobacter (CE).

Another potentially important affect on Campylobacter colonization is the reduction in goblet cell numbers following bacteriocin treatment. Mucin glycoproteins are synthesized and secreted from goblet cells, which arise from stem cells at the base of the crypts and migrate toward the villus tip, in which they enter into the lumen (Cheng and Leblond, 1974; Geyra et al., 2001). Previous research has demonstrated that Campylobacter can use mucin as a nutrient source for growth (Hugdahl et al., 1988; Schoeni and Doyle, 1992). This capability may provide a competitive advantage over other microflora. The ability of bacteriocins to reduce goblet cell number and subsequent mucin production may limit Campylobacter colonization. This idea is supported by previous research, reporting that colonization of C. jejuni in chicks can be influenced by diets that alter mucin production and viscosity (Fernandez et al., 2000).

Although bacteriocin treatment eliminated detectable Campylobacter colonization in this study (detection limit, 1 x 102 cfu/g of cecal contents), it is possible that undetectable numbers of Campylobacter may still persist in these birds. Previous research from our laboratory has demonstrated that even if Campylobacter is eliminated from most, but not all, enteric locations, the remaining enteric Campylobacter can recolonize the gut within a few days (Farnell et al., 2005). If, however, bacteriocins are dosed just before marketing, the ability of any possible Campylobacter to recolonize the tract would be reduced or prevented. Furthermore, even if bacteriocin treatment did not totally eliminate Campylobacter, the approximately 4-log reduction in Campylobacter concentrations obtained in the current study would provide a significant benefit to human food safety. Research by Rosenquist et al. (2003) reported that even a 2-log reduction in carcass contamination would reduce the human incidence of Campylobacteriosis in human by 30-fold.

In the present study, the administration of bacteriocins isolated from B. circulans and P. polymyxa was effective in eliminating detectable Campylobacter colonization in young commercial turkeys. The mechanism of bacteriocin action on Campylobacter colonization may be related to the ability of these compounds to reduce crypt depth and goblet cell density in young turkeys. The use of bacteriocins may be an important strategy to reduce Campylobacter colonization in poultry.


   FOOTNOTES
 
1 Mention of a trade name, proprietary product, or specific equipment does not constitute a guarantee or warranty by the USDA and does not imply its approval to the exclusion of other products that may be suitable. Back

2 This research has been supported in part by the Food Safety Consortium, the US Department of State (Washington, DC), the Russian Federation State Research Center for Applied Microbiology (Moscow, Russian Federation), the USDA-ARS, and the International Science and Technology Center project no. 1720. Back

Received for publication March 3, 2006. Accepted for publication April 25, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Aptekmann, K. P., S. M. Baraldi Arton, M. A. Stefanini, and M. A. Orsi. 2001. Morphometric analysis of the intestine of domestic quails (Coturnix coturnix japonica) treated with different levels of dietary calcium. Anat. Histol. Embryol. 30:277–280.[Web of Science][Medline]

Beery, J. T., M. B. Hughdahl, and M. P. Doyle. 1988. Colonization of the gastrointestinal tracts of chicks by Campylobacter jejuni.Appl. Environ. Microbiol. 54:2365–2370.[Abstract/Free Full Text]

Bielke, L. R., A. L. Elwood, D. J. Donoghue, A. M. Donoghue, L. A. Newberry, N. K. Neighbor, and B. M. Hargis. 2003. Approach for selection of individual enteric bacteria for competitive exclusion in turkey poults. Poult. Sci. 82:1378–1382.[Abstract/Free Full Text]

Bywater, R. J. 2004. Veterinary use of antimicrobials and emergence of resistance in zoonotic and sentinel bacteria in the EU. J. Vet. Med. B Infect. Dis. Vet. Public Health 51:361–363.[Web of Science][Medline]

Centers for Disease Control and Prevention. 2005. Preliminary FoodNet data on the incidence of infection with pathogens commonly transmitted through food – 10 sites, United States, 2004. Morb. Mortal. Wkly. Rep. 54:352–356.[Medline]

Chaveerach, P., L. J. Lipman, and F. van Knapen. 2004. Antagonistic activities of several bacteria on in vitro growth of 10 strains of Campylobacter jejuni/coli. Int. J. Food Microbiol. 90:43–50.[Web of Science][Medline]

Cheng, H., and C. P. Leblond. 1974. Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine. IV. Unitarian Theory of the origin of the four epithelial cell types. Am. J. Anat. 141:537–561.[Web of Science][Medline]

Cleveland, J., T. J. Montville, I. F. Nes, and M. L. Chikindas. 2001. Bacteriocins: Safe, natural antimicrobials for food preservation. Int. J. Food Microbiol. 71:1–20.[Web of Science][Medline]

Cole, K., A. M. Donoghue, P. J. Blore, J. S. Holliman, N. A. Cox, M. T. Musgrove, and D. J. Donoghue. 2004. Effect of aeration and storage temperature on Campylobacter concentrations in poultry semen. Poult. Sci. 83:1734–1738.[Abstract/Free Full Text]

Corrier, D. E., D. J. Nisbet, C. M. Scanlan, A. G. Hollister, D. J. Caldwell, L. A. Thomas, B. M. Hargis, T. Tomkins, and J. R. Deloach. 1995. Treatment of commercial broiler chickens with a characterized culture of cecal bacteria to reduce salmonellae colonization. Poult. Sci. 74:1093–1101.[Web of Science][Medline]

Corry, J. E., and I. Attabay. 2001. Poultry as a source of Campylobacter and related organisms. J. Appl. Microbiol. 90:96S–114S.

Daly, C., W. E. Sandme, and P. R. Elliker. 1970. Interactions of food starter cultures and food-borne pathogens: Streptococcus diacetylactis versus food pathogens. J. Milk Food Technol. 35:349–357.

Farnell, M. B., A. M. Donoghue, K. Cole, I. Reyes-Herrera, P. J. Blore, and D. J. Donoghue. 2005. Campylobacter susceptibility to ciprofloxacin and corresponding fluoroquinolone concentrations within the gastrointestinal tracts of chickens. J. Appl. Microbiol. 99:1043–1050.[Medline]

Fernandez, F., R. Sharma, M. Hinton, and M. R. Bedford. 2000. Diet influences the colonisation of Campylobacter jejuni and distribution of mucin carbohydrates in the chick intestinal tract. Cell. Mol. Life Sci. 57:1793–1801.[Web of Science][Medline]

Geyra, A., Z. Uni, and D. Sklan. 2001. Enterocyte dynamics and mucosal development in the posthatch chick. Poult. Sci. 80:776–782.[Abstract/Free Full Text]

Hugdahl, M. B., J. T. Berry, and M. P. Doyle. 1988. Chemotactic behavior of Campylobacter jejuni. Infect. Immun. 56:1560–1566.[Abstract/Free Full Text]

Jacobs-Reitsma, W. 1997. Aspects of epidemiology of Campylobacter in poultry. Vet. Q. 19:113–117.[Web of Science][Medline]

Jacobs-Reitsma, W. 2000. Campylobacter in the food supply. Pages 467–481 in Campylobacter. I. Nachamkin and M. J. Blaser, ed. ASM Press, Washington, DC.

Joeger, R. D. 2003. Alternatives to antibiotics: Bacteriocins, antimicrobial peptides and bacteriophages. Poult. Sci. 82:640–647.[Abstract/Free Full Text]

Line, J. E. 2001. Development of a selective differential agar for isolation and enumeration of Campylobacter spp. J. Food Prot. 64:1711–1715.[Web of Science][Medline]

Mead, G. C. 2002. Factors affecting intestinal colonization of poultry by Campylobacter and role of microflora in control. World’s Poult. Sci. J. 58:169–178.

Mead, G. C. 2004. Current trends in the microbiological safety of poultry meats. World’s Poult. Sci. J. 60:112–118.

Meinersmann, R. J., W. E. Rigsby, N. J. Stern, L. C. Kelley, J. E. Hill, and M. P. Doyle. 1991. Comparative study of colonizing and noncolonizing Campylobacter jejuni. Am. J. Vet. Res. 52:1518–1522.[Web of Science][Medline]

Morency, H., M. Mota-Meira, G. Lapointe, C. Lacroix, and M. C. Lavoie. 2001. Comparison of the activity spectra against pathogens of bacteria strains producing a mutacin or a lantibiotic. Can. J. Microbiol. 47:322–331.[Web of Science][Medline]

Natrajan, N., and B. W. Sheldon. 2000. Inhibition of Salmonella on poultry skin using protein- and polysaccharide-based films containing a nisin formulation. J. Food Prot. 63:1268–1272.[Web of Science][Medline]

Newell, D. G., and C. Fearnley. 2003. Sources of Campylobacter colonization in broiler chickens. Appl. Environ. Microbiol. 69:4343–4351.[Free Full Text]

Newell, D. G., and J. A. Wagenaar. 2000. Poultry infections and their control at the farm level. Pages 497–509 in Campylobacter. 2nd ed. J. Nachamkin and M. J. Blaser. ASM Press, Washington, DC.

Nurmi, E., and M. Rantala. 1973. New aspects of Salmonella infection in broiler production. Nature 241:210–211.[Medline]

Riley, M., and J. E. Wertz. 2002. Bacteriocins: Evolution, ecology, and application. Annu. Rev. Microbiol. 56:117–137.[Web of Science][Medline]

Rosenquist, H., N. L. Nielsen, H. M. Sommer, B. Norrung, and B. B. Christensen. 2003. Quantitative risk assessment of human campylobacteriosis associated with thermophilic Campylobacter species in chickens. Int. J. Food Microbiol. 83:87–103.[Web of Science][Medline]

Sahin, O., T. Y. Morishita, and Q. Zhang. 2002. Campylobacter colonization in poultry: Sources of infection and modes of transmission. Anim. Health Res. Rev. 3:95–105.[Medline]

Sakamoto, K., H. Hirose, A. Onizuka, M. Hayashi, N. Futamura, Y. Kawamura, and T. Ezaki. 2000. Quantitative study of changes in intestinal morphology and mucus gel on total parenteral nutrition in rats. J. Surg. Res. 94:99–106.[Web of Science][Medline]

SAS Institute. SAS/STAT Users Guide. Version 9. 2003. SAS Inst. Inc., Cary, NC.

Schoeni, J. L., and M. P. Doyle. 1992. Reduction of Campylobacter jejuni colonization of chicks by cecum-colonizing bacteria producing anti-C. jejuni metabolites. Appl. Environ. Microbiol. 58:667–670.

Solis de Los Santos, F., G. Tellez, M. B. Farnell, J. M. Balog, N. B. Anthony, H. O. Pavlidis, and A. M. Donoghue. 2005. Hypobaric hypoxia in ascites resistant and susceptible broiler genetic lines influence gut morphology. Poult. Sci. 84:1495–1498.[Abstract/Free Full Text]

Stern, N. J., N. A. Cox, J. S. Bailey, M. E. Berrang, and M. T. Musgrove. 2001. Distribution of Campylobacter spp. in selected U.S. poultry production and processing operations. Poult. Sci. 80:156–160.[Abstract/Free Full Text]

Stern, N. J., E. A. Svetoch, B. V. Eruslanov, Y. N. Kovalev, L. I. Volodina, V. V. Perelygin, E. V. Mitsevich, I. P. Mitsevich, and V. P. Levchuk. 2005. Paenibacillus polyxma purified bacteriocin to control Campylobacter jejuni in chickens. J. Food Prot. 68:1450–1453.[Web of Science][Medline]

Svetoch, E. A., N. J. Stern, B. V. Eruslanov, Y. N. Kovalev, L. I. Volodina, V. V. Perelygin, E. V. Mitsevich, I. P. Mitsevich, V. D. Pokhilenko, V. N. Borzenkov, V. P. Levchuk, O. E. Svetoch, and T. Y. Kudriavtseva. 2005. Isolation of Bacillus circulans and Paenibacillus polymyxa strains inhibitory to Campylobacter jejuni and characterization of associated bacteriocins. J. Food Prot. 68:11–17.[Web of Science][Medline]

Tagg, J. R., A. S. Dajani, and L. W. Wannamaker. 1976. Bacteriocins of gram-positive bacteria. Bacteriol. Rev. 40:722–756.[Free Full Text]

Yunus, M., Y. Horii, S. Makimura, and L. Smith. 2005. Murine goblet cell hypoplasia during Eimeria pragensis infection is ameliorated by clindamycin treatment. J. Vet. Med. Sci. 67:311–315.[Web of Science][Medline]

Zhang, Q. J. Lin, and S. Pereira. 2003. Fluoroquinolone resistant Campylobacter in animal reservoirs: Dynamics of development, resistance mechanisms and ecological fitness. Anim. Health Res. Rev. 4:63–71.[Medline]

Zhao, C., B. Ge, J. DeVillena, R. Sudler, E. Yeh, S. Zhao, D. G. White, D. Wagner, and J. Meng. 2001. Prevalence of Campylobacter spp., Escherichia coli, and Salmonella serovars in retail chicken, turkey, pork, and beef from the greater Washington, DC area. Appl. Environ. Microbiol. 67:5431–5436.[Abstract/Free Full Text]




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