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Evaluation of an Experimental Chlorate Product as a Preslaughter Feed Supplement to Reduce Salmonella in Meat-Producing Birds¹

United States Department of Agriculture-Agricultural Research Service, Southern Plains Agricultural Research Center, Food and Feed Safety Research Unit, 2881 F & B Road, College Station, TX 77845

² Corresponding author: Allen.Byrd{at}ars.usda.gov

	ABSTRACT

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A study was conducted to evaluate the effect of experimental chlorate product (ECP) feed supplementation on Salmonella Typhimurium (ST) in the crop and ceca of market-age broilers. In trial 1, 160 market-age broilers were randomly assigned to 8 treatment groups and replicated twice, with 20 broilers per pen for 1 wk. Trial 2 used the same design, but used 80 market-age broilers with 10 broilers per pen. Treatments were as follows: 1) control feed + double-distilled drinking water (dd H₂O); 2) control + 18.5% experimental zeolite carrier with dd H₂O; 3 to 7) control feed supplemented with 0.5, 1.0, 5.0, 10.0, or 18.5% of a feed grade ECP + dd H₂O; 8) control feed + 1x ECP (0.16% w/v; containing 15 mM chlorate ion equivalent) added to dd H₂O. Seven-week-old broilers were provided experimental treatments for 7 d, killed, and then ceca and crops were removed and evaluated for ST. Broilers fed 5 to 18.5% ECP or water ECP had a significantly lower (P < 0.05) incidence of ST in the crop (36 to 38% and 14%, respectively) when compared with the control (60%). Broilers fed 10% ECP or water ECP had significantly lower ST crop concentrations (1.03 log₁₀ and 0.38 log₁₀ ST/g, respectively) when compared with broilers fed a control diet (1.54 log₁₀ ST/g). Crop and ceca ST incidence (32 to 48%) and concentration (1.00 to 1.82 log₁₀ ST/g) were significantly lower in broilers fed 5 to 18.5% ECP as compared with the control (78%; 2.84 log₁₀ ST/g). Broilers fed 5% or greater ECP had significantly higher water consumption (380 to 580 mL water/d) and litter moisture (31 to 56%) when compared with the control (370 mL water/d; 23% moisture). Only broilers fed 18.5% ECP had significantly lower 7-wk BW (2.77 kg of BW) when compared with the controls (3.09 kg of BW). Average daily gains were significantly depressed in broilers fed 10 or 18.5% ECP compared with the controls. These results indicate broilers supplemented with feed 5% ECP or water ECP 7 d before slaughter reduced ST without affecting growth parameters.

Key Words: broiler • experimental chlorate product • Salmonella • performance

	INTRODUCTION

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Each year foodborne disease infections are estimated to affect more than 76 million people worldwide (Mead et al., 1999). Salmonella and Campylobacter are common foodborne bacterial pathogens that are responsible for causing more than 1.9 and 1.3 million infections worldwide, respectively (Mead et al., 1999). Salmonella alone cost Americans around one billion dollars a year for medical cost and loss of productivity (Roberts, 1988). In the recent years, the poultry industry has implemented new programs to control these foodborne pathogens. Various methods of eradication have been tested to control Salmonella on poultry and poultry products. These intervention strategies include, but are not limited to, chemical litter treatments (Moore and Miller, 1994; Huff et al., 1996; Moore et al., 1996; Terzich et al., 1998), vaccinations (Hassan and Curtiss, 1997; Zhang-Barber et al., 1999; Sydenham et al., 2000), and chemical disinfection (Mulder et al., 1987; Dickens and Whitemore, 1994; Byrd et al., 2001).

Chlorate acts on the bacterial physiological system, utilizing the respiratory nitrate reductase pathway to kill specific pathogenic bacteria by building up of chlorite within the cell. Salmonella and Escherichia coli respire under anaerobic conditions by converting nitrate to nitrite using a dissimilatory nitrate reductase (Stewart, 1988). Only bacteria that utilize dissimilatory nitrate reductase to breakdown nitrate such as members of the family Enterobacteriaceae, which includes Salmonella and Escherichia, are affected by this compound (Brenner, 1984). This intracellular enzyme does not distinguish between nitrate and chlorate. Within these bacteria, chlorate is reduced to chlorite that builds up to toxic levels, and susceptible bacteria die (Stewart, 1988). Chlorate administered in the drinking water has been effective in controlling Salmonella and E. coli O157:H7 in pigs (Anderson et al., 2001a,b), cattle, and sheep (Callaway et al., 2002). In poultry, water soluble chlorate significantly reduced Salmonella in chickens and turkeys (Byrd et al., 2003; Moore et al., 2006). Furthermore, chlorate was effective in controlling Clostridium perfringens in broilers with necrotic enterititis (McReynolds et al., 2004). The administration of chlorate via the drinking water may lead to many obstacles and will require the broiler farm manager to provide the product at specific time points to achieve the maximum killing effect. To reduce the potential for administration error, providing a chlorate-based product in the feed improves the likelihood of uniform application. Therefore, the objective of the present study was to evaluate the effectiveness of feeding a 0.5 to 18.5% experimental chlorate product (ECP) before slaughter on the efficacy of reducing ST in the crop and ceca of market-age broilers.

	MATERIALS AND METHODS

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Experimental Design and Husbandry

The effect of ECP (EKA Chemicals Inc., Marietta, GA; 1x ECP is equivalent to a 15 mM chlorate ion concentration) on Salmonella contamination of crop and cecal contents was evaluated in 3 replicates. In 3 replicate trials, 5-wk-old broilers were obtained from a commercial producer and divided into 8 groups. In trials 1 and 2, one hundred sixty broilers were divided into 8 groups of 20. In trial 3, 80 broilers were divided into 8 groups of 10. Birds were then placed on 7.6-cm-thick new pine shavings in 2.4 x 1.2 m floor pens, allowing 0.12 m² of pen space per bird. Birds were allowed to acclimate for 1 wk before the start of the experiment. To determine whether or not the broilers were colonized with Salmonella, cloacal swabs were taken from each bird after arrival on the test farm and cultured by selective enrichment procedures described below. Technical procedures of this study were approved by the Institutional Animal Care and Use Committee.

Feed rations for each group were formulated from nonmedicated corn-soybean meal grower ration obtained from Texas A&M University Poultry Research Center. All diets were formulated to meet or exceed National Research Council (1994) specifications. Feed and water were provided for ad libitum consumption. Before broiler placement, ECP was formulated and mixed into the feed and water according to the appropriate treatment. The study design consisted of 2 controls without ECP (normal control and 18.5% ECP-zeolite carrier) and 6 treatments with ECP (0.5, 1.0, 5.0, 10.0, and 18.5% ECP dietary supplementation, along with a 1x ECP (1x ECP is equivalent to a 15 mM chlorate ion concentration drinking water supplementation). Double-distilled drinking water was utilized in each treatment. Feed deprivation occurred approximately 8 to 10 h before euthanasia by cervical dislocation. Broilers were provided the experimental diets at 6 wk of age and continued until 7 wk of age.

Broiler performance parameters for all 3 trials were recorded or determined and included individual BW (kg), weight gain (kg/bird), total water (mL/bird/d) and feed (g/bird/) consumption, feed conversion (weight gain/feed intake), and mortality. At termination of each trial, 5 litter samples from symmetrical locations in each pen were collected for analyses of moisture content and expressed as a percentage. Broilers were weighted as a group and an average weight was calculated for the pen. Water and feed consumption was recorded daily.

Salmonella Culture Procedure

A primary poultry isolate of ST was selected for resistance to novabiocin (NO) and nalidixic acid (NA) at USDA-ARS, College Station, Texas, was used. Media to culture the resistant isolate in experimental studies contained 25 µg of NO and 20 µg of NA per mL. The challenge inoculum was prepared from an overnight culture, which had been previously transferred 3 times in trypticase soy broth. The culture was serially diluted in sterile phosphate-buffered saline to approximately 10⁹ cfu/mL. The viable cell concentration of the challenge inocula was confirmed by colony counts on brilliant green agar (BGA) plates (Oxoid, Unipath Ltd., Basingstoke, Hampshire, UK). Plates were incubated for 24 h at 37°C and expressed as log₁₀ ST to determine colony-forming units per milliliter. Broilers were inoculated via oral gavage at 6 wk of age with 3 mL of the ST culture before administration of ECP. Inoculum cfu titers were 0.7 to 1.8 x 10⁹ cfu/mL.

Salmonella Crop and Cecal Analysis

At 7 wk of age, birds were killed by cervical dislocation, and their crop and cecal contents were aseptically collected. A 0.25-g sample of cecal content was collected, placed in 2.25 mL of Butterfield’s solution, and serially diluted in Butterfield’s 4-fold and spread-plated on BGA. Each crop was placed in 10 mL of Butterfield’s contained in a Stomacher bag with filter (Nasco, Fort Atkinson, WI) and stomached for 30 s in a Teckmar Laboratory Blender-Stomacher 80 (Seward Medical Ltd., London, UK). One milliliter of stomached crop content was serially diluted in Butterfield’s 4-fold and spread-plated on BGA NA/NO agar plate to enumerate ST. Plates were incubated for 24 h at 37°C and expressed as log₁₀ ST to determine cfu/unit of cecal and crop content. Colonies that grew on agar plates after 24 h of incubation were directly counted (quantitative enumeration). To qualitatively confirm the presence of inoculated ST, the remaining minced ceca and 2.5 mL of stomached crop material (10 samples/treatment) were each transferred into their respective polypropylene tube containing 20 mL of Rappaport-Vassiliadis enrichment broth (Difco, Sparks, MD) and incubated for 24 h at 37°C. Enrichments were streaked on BGA NO/NA and incubated for 24 h at 37°C. Suspect Salmonella colonies and colonies showing typical Salmonella morphology were confirmed using Salmonella O (group B; factors 1, 4, 5, and 12) antisera to confirm Salmonella Typhimurium colonies.

Salmonella Cloacal Swab Analysis

To determine if broilers were positive for Salmonella before arrival to our facilities, a cotton-tipped applicator was inserted into the cloaca for 10 s and transferred into a polypropylene tube containing 20 mL of Rappaport-Vassiliadis enrichment broth (Difco) and incubated for 24 h at 37°C. Enrichments were streaked on BGA NO/NA and incubated for 24 h at 37°C. Suspect Salmonella colonies and colonies showing typical Salmonella morphology were confirmed using Salmonella O (Group B; factors 1, 4, 5, and 12) antisera to confirm Salmonella Typhimurium colonies. All broilers were negative for Salmonella before the start of the study (data not shown).

Statistical Analysis

A completely randomized experimental design was utilized. All 3 replicates were combined and differences among groups in BW, weight gain, water and feed consumption, feed conversion, mortality, and litter moisture, along with log₁₀ cfu Salmonella were determined by one-way ANOVA (Snedecor and Cochran, 1967) using the general linear model procedure in the PC SAS version 6.11 statistical software (SAS Institute, 1996). Variable means for treatments showing significant differences in the ANOVA were further separated using Duncan’s multiple range test. Salmonella colonies were logarithmically transformed before analysis to achieve homogeneity of variance were expressed as log₁₀ cfu. Differences among groups in the incidence of Salmonella crop and cecal incidence were analyzed by chi-square analysis. All analyses were conducted using commercial statistical analysis software (Luginbuke and Schlotzhauer, 1987). All statements of significance are based on the P < 0.05 unless noted otherwise.

	RESULTS

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Crop and Ceca Analysis

Table 1 reports the bactericidal effects of the ECP supplemented treatments on crop ST incidence and concentration compared with nonECP-supplemented treatments provided in the feed 7 d before slaughter. There were significant reductions (P < 0.05) in crop ST incidence from broilers fed 5 to 18.5% ECP or water ECP when compared with the broilers fed the control diet. Similarly, crop ST concentrations were significantly reduced in broilers fed 10% ECP (1.03 log₁₀ ST) and water ECP (0.38 log₁₀ ST) when compared with the controls (1.54 log₁₀ ST). Broilers provided ECP in the water had the greatest reduction in both incidence (14% ST positive) and ST crop concentration (0.38 log₁₀ ST/g of crop contents).

There were no significant differences (P < 0.05) found with regard to mortality (data not shown). Water consumption was significantly increased in broilers fed 5% ECP or greater (Table 3). Broilers provided the ECP-carrier, water ECP, 1% ECP, or less consumed significantly less water than the controls possibly due to an off flavor to the chickens. Broilers fed 18.5% ECP had the most severely depressed BW of 2.77 kg. The average daily gain was reduced in broilers receiving the ECP-carrier or the highest concentrations of ECP at 10 or 18.5% ECP when compared with broilers fed the control diet. Feed conversions were not significantly affected by any treatment. Litter moisture significantly increased in ECP administered in the feed or the water treatment. Litter in the pens of broilers fed 18.5% ECP had the highest litter moisture content (55.8% moisture) and broilers fed the diet containing ECP-carrier had the lowest litter moisture content (17% moisture).

	DISCUSSION

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Previously, our laboratory has shown that oral administration of ECP significantly reduced Salmonella colonization in the gut of pigs, broilers and turkeys (Anderson et al., 2001a,b, 2004; Byrd et al., 2003; Jung et al., 2003; Moore et al., 2006;). Drinking water or feed administration of ECP has also resulted in significant reductions of generic E. coli, E. coli O157:H7, or both in cattle and sheep gut concentrations (Anderson et al., 2002, 2005; Callaway et al., 2002, 2003; Edrington et al., 2003).

Whereas both E. coli and Salmonella possess respiratory nitrate reductase, evidence from in vitro studies reveals that co-application with nitrate enhanced the bactericidal activity of chlorate against Salmonella but not against E. coli (Anderson et al., 2000, 2007). This observation likely has practical implications as the design of anti-Salmonella products for application in animals may require small amounts of nitrate to achieve optimal efficacy. Nitrate preadaptation may select for nitrate respiring bacteria in situ and allow these bacteria to become more sensitive to chlorate products (Stewart, 1988). Although previous evidence suggest chlorate resistance does not likely develop in mixed populations of gut bacteria and that even when resistant cultures generated in pure culture were added to a mixed population derived from the gastrointestinal tract, the chlorate-resistant bacteria could not compete within the highly competitive environment (Callaway et al., 2001). Recent research examining pharmacokinetic aspects of chlorate metabolism in the mammals and aves indicate that residual chlorate in edible tissue is within established provisional safety limits (Smith et al., 2005a,b, 2006, 2007; Oliver et al., 2007).

Results from the current research suggest that chlorate administered in the feed of broilers is effective in reducing Salmonella in the crop or ceca when fed at concentrations of 5% ECP or greater. At concentrations of 5% ECP or less, ECP did not significantly affect 7-wk BW. Feed conversions were not affected by even the highest concentrations of ECP. Therefore, the ideal concentration of 5% ECP in the feed is the best compromise for the control of Salmonella without the loss of production parameters. Broilers fed ECP had higher litter moisture content than broilers fed a control diet. The reason for increased moisture is the increased sodium intake that accompanies ECP. By increasing the concentration of ECP, sodium concentrations also increase, which causes flushing of water in the gastrointestinal tract and eventually on to the litter. A solution to this problem would be to reformulate the broiler diet or by removal or decreasing the salt content normally added to the diet or by changing the ECP formulation. Sodium could possibly be exchanged with potassium or another cation generally required by the animal.

Government regulations (Pathogen Reduction Rule; USDA-FSIS, 1996) have brought a need for cost-efficient approaches to reducing foodborne pathogens without altering current management techniques. Experimental chlorate product is a cost-effective approach to reducing the prevalence of Salmonella, E. coli, and Clostridium spp. in broilers and could be considered as a component in a program to control or reduce food-borne pathogens. Chlorate-based products would attack these pathogenic bacteria without reducing beneficial bacteria. Furthermore, by selecting for beneficial bacteria, these bacteria will aid the battle against these pathogenic bacteria. The results of the present study suggest that ECP is a cost-efficient means to reduce foodborne pathogens that can be added into the diet and could be incorporated into existing commercial management procedures.

	ACKNOWLEDGMENTS

 
The authors appreciate the expert technical assistance of Earl Munson and Clayton Myers at the US-DA-Agricultural Research Service, Southern Plains Agricultural Research Center, Food and Feed Safety Research Unit, 2881 F & B Road, College Station, Texas.

	FOOTNOTES

 
¹ Use of trade names in this publication does not imply endorsement by the USDA of these products, nor similar ones not mentioned.

³ Present address: Matthew R. Burnham, Jones County Junior College, Department of Biological Sciences, Ellisville, MS 39437.

Received for publication December 13, 2007. Accepted for publication May 7, 2008.

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