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J APPL POULT RES 2009. 18:521-529. doi:10.3382/japr.2009-00003
© 2009 Poultry Science Association
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Research Reports

Efficacy testing of a defined competitive exclusion product in combination with fructooligosaccharide for protection against Salmonella Typhimurium challenge in broiler chicks

B. E. Telg* and D. J. Caldwell{dagger},1

* Department of Population Health, Poultry Diagnostic and Research Center, 953 College Station Road, University of Georgia, Athens 30602; and {dagger} Department of Poultry Science, Texas A&M University, College Station 77843-2472

1 Corresponding author: Caldwell{at}poultry.tamu.edu


   SUMMARY
TOP
 SUMMARY
DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Three replicate trials were conducted to evaluate the ability of fructooligosaccharide (FOS), in combination with a defined competitive exclusion (dCE) culture, to reduce cecal colonization of Salmonella Typhimurium in 1-d-old naïve broiler chicks. Fructooligosaccharide is an oligosaccharide that cannot be directly utilized by avian or mammalian species, but that can be fermented and utilized for growth by many bacterial species. For each trial, 4 groups were established, with each group receiving a different treatment (FOS only, FOS + dCE, dCE only, and nontreatment controls). Forty-eight hours after the administration of each group-specific treatment, ceca were harvested from 5 chicks in each group to evaluate the establishment of the competitive exclusion culture through cecal propionate levels. The remaining chicks were challenged with 104 cfu of Salmonella Typhimurium by oral gavage. Body weight gain and feed intake were monitored throughout the trials. Seven days after Salmonella challenge, the ceca and crops were aseptically collected from all chicks. Both direct plating for enumeration and enrichment were performed to assess the level of Salmonella colonization in these chicks. Chicks in the dCE-only and dCE + FOS groups had consistently higher cecal propionate levels than the chicks in the FOS-only and nontreatment control groups. Body weight gain and feed conversion were not consistently different among the 4 treatment groups. However, enriched and direct-plated levels of Salmonella were consistently lower in both the crops and ceca of chicks in the dCE-only and dCE + FOS groups when compared with the FOS-only and non-treatment control groups. No significant differences were consistently observed between the dCE-only and dCE + FOS groups in any measured category.

Key Words: competitive exclusion • Salmonella • fructooligosaccharide • probiotic


   DESCRIPTION OF PROBLEM
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Much of the Salmonella-related food-borne illness in the United States is attributed to the consumption or handling of poultry products contaminated with paratyphoid salmonellae, which includes Salmonella Typhimurium (ST). Salmonella has a dramatic impact on nearly every aspect of the poultry industry, and controlling Salmonella contamination of poultry and poultry products has become a top priority for the industry as a whole. To combat enteric colonization by various Salmonella species, competitive exclusion (CE) cultures have been used in an attempt to reduce the human food safety risk and, as an added benefit, to improve various production parameters such as BW gain and feed conversion. Competitive exclusion cultures are generally a mixture of intestinal bacteria, oftentimes derived from the ceca of mature chickens, which can coexist as a stable community in the intestines of naïve chickens [1, 2]. Competitive exclusion cultures are intended to replace the natural succession and development of the intestinal microbiota by providing the naïve bird with colonizing bacteria [2].

It has been known for many years that young chicks exposed to and colonized with indigenous bacteria from healthy adult chickens will be better protected from deleterious effects upon exposure to enteropathogens [3–8]. Since this discovery, many attempts have been made to unravel the microbiota of the healthy avian intestinal tract and, from these findings, to construct bacterial cultures that can be used as supplements in young or naïve chickens. The purpose of using CE with regard to Salmonella is always the same: to provide the naïve chick with a population of microorganisms that will rapidly colonize the intestinal tract and outcompete or possibly displace Salmonella for space and nutrients, thereby excluding and preventing the Salmonella from establishing itself as a viable organism within the gut of an exposed chicken. Once the Salmonella has become established, the bird itself may show no ill effect, but the likelihood of shedding the offending Salmonella organism and of subsequent carcass contamination increases.

Recently, more characterized or defined CE (dCE) cultures have been used successfully to reduce the level of Salmonella colonization in young chicks [9–14]. Many of these defined or partially defined cultures have been found to consist of microorganisms that produce volatile fatty acids (VFA), and that by measuring cecal propionate levels, the successful establishment of these beneficial bacteria can be assessed. Previous research has shown that higher cecal propionate levels have often been correlated with better protection from subsequent Salmonella challenge and colonization [9, 11, 13]. One such trial, involving a commercial dCE culture of known VFA-producing organisms, revealed that birds given this CE culture orally could be significantly protected from a Salmonella challenge as soon as 4 h after CE administration [11].

Over the years, numerous types of compounds have been evaluated for their ability to enhance the growth and establishment of various bacterial populations present in CE cultures. Of these compounds, several different saccharides have been evaluated for their ability to manipulate or effect the composition of enteric bacterial populations while having no dietary or nutritive effect on the host. This utilization can result in improved bird performance, increased bacterial growth rates, shifts in enteric bacterial populations, changes in intestinal pH, or reduced intestinal colonization with pathogenic bacteria through direct oligosaccharide-pathogen interactions or the ability to enhance CE of pathogenic bacteria [15–29]. Fructooligosaccharide (FOS) is often evaluated in both mammals and poultry, as well as the potential for FOS to enhance the establishment or growth of introduced or native beneficial enteric bacteria. The overall purpose of the present project was to evaluate the ability and efficacy of a dCE culture in combination with FOS-supplemented feed to provide protection against cecal colonization of young broiler chicks after an experimental ST challenge.


   MATERIALS AND METHODS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Experimental Birds
Day-of-hatch Cobb x Cobb broiler chicks [30] were obtained from a local commercial hatchery and were randomly assigned to 1 of 4 experimental groups. Each experimental group within each replicate trial consisted of 40 chicks divided into 2 nearly identical rearing pens (20 chicks/pen) to minimize pen effects and thus increase statistical power of the collected data. Chicks were reared on new pine shavings in floor pens. All birds received water and feed (respective to treatment) ad libitum at the time of placement. A standard broiler chick starter diet with corn and soybean meal was used as the basal diet [31].

Experimental Design
For each of the 3 trials, the 1-d-old chicks were divided into 4 different treatment groups, with the treatment being applied at 1 d of age. These groups consisted of 1) the control group (administered 0.25 mL of water by oral gavage at 1 d of age), 2) the dCE group [32] (administered 1 manufacturer-recommended dose by oral gavage at 1 d of age), 3) the FOS group (with FOS mixed into the basal diet at 100 lb (45.4 kg) of diet plus 1 lb (0.454 kg) of FOS, to attain a 0.99% inclusion rate in the finished feed for the duration of the trial), and 4) the dCE + FOS group (administered both treatments individually, as described above).

Chicks within each experimental group were weighed at the beginning and end of each trial so that estimates of BW gain for each experimental group could be determined. Feed consumption data were also recorded daily so that estimates of FE and FCR could be determined for each experimental group. Chicks, treated with dCE, FOS, or both, were housed in a rearing room separate from the negative control chicks within the same isolation facility. Birds designated to receive the dCE were administered 1 manufacturer-recommended dose at the time of placement.

To assess the cecal establishment of the dCE in experimental birds, cecal propionate levels were determined by removing ceca from 5 birds in each experimental group 48 h after dCE administration. All birds remaining in each pen after this sampling for propionate values were challenged by oral gavage with 0.5 mL of a 104 cfu nalidixic acid-resistant ST. This isolate is a primary poultry isolate that was obtained from the USDA-Animal and Plant Health Inspection Service-National Veterinary Services Laboratory in Ames, Iowa. The ST was grown for challenge in 3 serial passages of 8 h each in tryptic soy broth to achieve an inoculum of bacteria in log-phase growth. Bacteria were spectrophotometrically quantified and diluted to 2x 104 cfu/mL for challenge. In total, 3 replicate trials were performed, using chicks of the same strain but from different hatches. Fresh preparations of the treatment and challenge organisms were used in each trial.

ST Recovery
To assess whether the experimental birds and feed used in each experiment were Salmonella negative at the initiation of each experiment, chick transport materials (liners) and feed were cultured for the presence of Salmonella at the time of placement. Twenty-five grams of liner material from each chick transport container was collected and placed in a sterile stomacher bag. Buffered peptone water (200 mL/bag) was added and samples were stomached for 30 s. Stomached suspensions were then transferred to a sterile sample vessel and all bottles were incubated at 37°C for 18 h. The presence or absence of Salmonella was confirmed by through-plating the incubated suspensions on brillant green agar (BGA) plates, incubating the plates for 18 to 24 h at 37°C, and then evaluating the plates for growth of Salmonella. Before use in each individual experiment, the feed was similarly cultured in triplicate using the procedures above to ensure that it was Salmonella free.

Seven days after ST challenge, the crop was aseptically removed from each chick, sliced open, and put into a stomacher bag. Immediately, 10 mL of buffered peptone was added to each sample and all bags were stomached for 30 s. Dilutions of the resulting crop suspensions were performed, and all dilution tubes were plated on BGA containing 20 µg/mL of nalidixic acid and 25 µg/mL of sodium novobiocin. Because of the low level of recovery upon direct plating of crop samples that was observed in trials 1 and 2, direct plating of crop samples to recover colony-forming units of ST was not attempted in trial 3. Additionally, in all 3 trials, 10 mL of crop suspension made from each experimental bird was enriched in tetrathionate broth base. All tetrathionate samples were incubated for 24 h at 37°C. All enriched samples were similarly plated on BGA containing 20 µg/mL of nalidixic acid and 25 µg/mL of sodium novobiocin. All plates were incubated at 37°C for 24 h, and typical Salmonella colonies were counted and confirmed serologically.

Seven days after ST challenge, the cecum from each experimental bird was aseptically removed and transferred to a small, preweighed plastic bag. Cecal contents were separated from ceca, individual bags were weighed again, and the weights were recorded. Cecal contents from 1 cecum per chick were then mixed with 9 mL of peptone diluent, 10-fold serial dilutions were performed, and 100 µL of each sample was plated on BGA containing 20 µg/mL of nalidixic acid and 25 µg/mL of sodium novobiocin in duplicate. Similar to the crop culture, the cecal contents of 1 cecum from each chick were also enriched in tetrathionate broth base. All dilutions and enriched samples were streaked on BGA and incubated at 37°C for 24 h, and typical Salmonella colonies were counted and confirmed serologically.

Statistical Analysis
Incidence (positive or negative) of recovery of ST from enriched cecal cultures was compared by using the chi-squared test of independence [33]. Numeric data, including log10 colony-forming units of ST per gram of cecal contents and propionate values, were analyzed using the GLM procedure for ANOVA with SAS software; statistically different means (P < 0.05) were further separated by using Duncan’s multiple range test [34].


   RESULTS AND DISCUSSION
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
In the present investigation, all feed and hatchery samples were observed to be negative for Salmonella contamination; thus, all experiments proceeded, and data derived from each, with regard to Salmonella contamination, should be considered valid. Mortality in trials 1 and 2 was observed to occur at the levels expected for pen studies of this nature. Significantly higher levels of mortality were observed in trial 3. Necropsy of recovered dead birds in trial 3 did not result in an identification of a specific bacterial etiology that may have been responsible for high levels of mortality in the control and FOS experimental groups. The observation of significantly lower levels of mortality in the dCE and dCE + FOS groups is noteworthy and is suggestive of a level of protection conferred to experimental birds in these groups against the pathogenic effects resulting from exposure of birds to the unidentified etiological agent.

A common indicator of the establishment of this particular dCE culture is an overall elevation in the concentration of propionic acid (propionate), a VFA in the cecum of treated birds. In the present investigation, cecal propionate levels were consistently elevated in all trials from birds in the dCE and dCE + FOS groups (Tables 1Go, 2Go, and 3Go). Cecal propionate levels were higher in trials 2 and 3, as compared with trial 1, which may explain the overall higher level of Salmonella protection that was observed in these latter trials. In experimental groups receiving dCE + FOS, there was no observed suggestion that FOS interfered with, or amplified, dCE bacterial establishment in the ceca of treated birds.


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  		Table 1. Trial 1—Effects of defined competitive exclusion (dCE) and fructooligosaccharide (FOS) on BW gain, feed conversion, cumulative mortality, and cecal propionate levels
 

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  		Table 2. Trial 2—Effects of defined competitive exclusion (dCE) and fructooligosaccharide (FOS) on BW gain, feed conversion, cumulative mortality, and cecal propionate levels
 

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  		Table 3. Trial 3—Effects of defined competitive exclusion (dCE) and fructooligosaccharide (FOS) on BW gain, feed conversion, cumulative mortality, and cecal propionate levels
 
Taken together, no significant effect of treatment was observed on BW gain in the present investigation (Tables 1Go, 2Go, and 3Go). When administered alone, FOS did not statistically differ from controls in any experiment. When the dCE culture was administered alone, no statistically significant positive effect was observed when compared with controls in any trial. In trial 1, the mean BW gain in the dCE-only culture group was statistically lower than that of the control group. Despite being numerically suggestive in trial 2, no significant elevations in BW gain were observed in the dCE + FOS group when compared with the control group. However, when compared with groups receiving dCE or FOS alone, the dCE + FOS group had a significantly higher mean BW gain in trial 2 (Table 2Go). Similarly, in trial 3, the BW gain of the dCE + FOS group was statistically higher than that of the FOS group, but was not different from that of the dCE group (Table 3Go).

Despite suggested trends of differences within each trial, feed conversion values did not differ significantly between groups within the individual trials. Estimates of feed conversion adjusted for mortality in trial 1 revealed no effect of treatment on feed conversion because control birds had the lowest overall feed conversion of any experimental group (Table 1Go). In trial 2, a suggestion of an effect of combined treatment (dCE + FOS) was observed when this experimental group had an approximately 8-point reduction in feed conversion as compared with the control group (Table 2Go). Trial 3 offered the best suggestion of an effect of treatment on feed conversion. Although no individual effect of feeding FOS was observed, the dCE and the dCE + FOS groups had lower overall estimates of feed conversion when compared with the control group (Table 3Go). Again, despite suggested trends, these values did not differ (P > 0.05) after statistical analysis. Because statistical significance does not always equate with commercial significance, we feel replication of these experimental parameters on a larger scale, possibly under commercial conditions, is warranted to better understand any influence of these treatments on feed conversion.

Selective enrichment of crop samples in trial 1 for the recovery of ST resulted in 67.5% of samples from the control group being positive for the challenge isolate (Table 4Go). The FOS and dCE groups did not differ from the control group because they had approximately equivalent recovery isolation frequencies. Surprisingly, the dCE + FOS experimental group had a significantly higher isolation frequency of the challenge isolate than did all other experimental groups. When crop samples were direct-plated for enumeration of crop ST, very low levels of crop colonization were observed in all experimental groups. Salmonella Typhimurium was recovered from only 1 bird each in the control, FOS, and dCE experimental groups, suggesting that crop contamination by ST in this experiment was low overall. When cecal samples were enriched for the recovery of the challenge isolate, ST levels were sufficiently high in all experimental groups. Significant reductions associated with treatment were observed in only 1 experimental group, dCE + FOS. Isolation rates from the other experimental groups did not differ from those of the control group. When cecal samples were direct-plated to enumerate ST recovered from birds in all experimental groups, the enumeration of colony-forming units from the dCE and dCE + FOS groups was similar to that of the control group, whereas the FOS group had a higher mean recovery of colony-forming units as compared with the control group (Table 4Go).


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  		Table 4. Trial 1—Effects of defined competitive exclusion (dCE) and fructooligosaccharide (FOS) on crop and cecal Salmonella Typhimurium (ST) recovery
 
In the second trial, effects of treatment were observed in a reduction in both crop and cecal ST colonization. When crop samples were enriched, the administration of dCE alone and of dCE + FOS was associated with a significant reduction (P < 0.001 and P < 0.05, respectively) in crop colonization (Table 5Go). As observed in trial 1, direct plating of crop samples resulted in similarly low levels of ST recovery. As such, significant differences were not observed. When cecal samples were enriched, to provide an estimate of cecal colonization in the birds, significant reductions were observed in all experimental groups [see Table 5Go; P < 0.05 (FOS) and P < 0.025 (dCE and dCE + FOS)] when compared with the nontreatment control group. When cecal samples were direct-plated to enumerate recovered ST from experimental birds in all groups, significant reductions (P < 0.05) in recovery were observed in the dCE and the dCE + FOS groups (Table 5Go).


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  		Table 5. Trial 2—Effects of defined competitive exclusion (dCE) and fructooligosaccharide (FOS) on crop and cecal Salmonella Typhimurium (ST) recovery
 
Similar to trial 2, reductions in crop and cecal ST colonization were associated with specific treatments in trial 3 (Table 6Go). When crop samples were enriched, significant reductions in crop colonization, as compared with the control group, were observed in the dCE (P < 0.025) and dCE + FOS (P < 0.01) groups. When cecal samples from all experimental birds in trial 3 were enriched to estimate levels of cecal colonization by ST, significant reductions were observed in the dCE (P < 0.01) and dCE + FOS (P < 0.001) groups. When cecal contents were direct-plated to enumerate recovered ST, significant reductions (P < 0.05) associated with treatment were observed in the dCE and dCE + FOS groups (Table 6Go).


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  		Table 6. Trial 3—Effects of defined competitive exclusion (dCE) and fructooligosaccharide (FOS) on crop and cecal Salmonella Typhimurium (ST) recovery
 
Fructooligosaccharide has been used as a prebiotic for both mammals and avian species in an attempt to enhance or influence the enteric microflora of a given host. In human infants, formula supplemented with FOS appears to stimulate the growth of Bifidobacterium and results in a bacterial fermentation pattern similar to that of breast-fed infants [16, 21]. In 7-d-old chicks, FOS alone, at a 0.75% feed inclusion rate, reduced Salmonella colonization rates by 12%, as compared with control chicks, after a challenge with 109 cells. Fructooligosaccharide in combination with a partially protective CE culture resulted in a 40% reduction in Salmonella colonization under the same challenge conditions [15]. In an experiment by Fukata et al. [18], FOS, in combination with a CE culture, given to 7- and 21-d-old chicks resulted in an apparent reduction in Salmonella colonization, but the combination appeared to have little impact on the overall diversity and population of intestinal microflora. Biggs et al. [25] found that FOS, when fed at 4 g/kg in a dextrose-isolated soy protein diet, reduced the cecal population of Clostridium perfringens. However, cecal bacterial populations of Bifidobacterium, Lactobacillus, C. perfringens, or Escherichia coli were not significantly affected when chicks were fed a corn- and soybean-based diet containing 4 g/kg of FOS.

The data obtained in the present experiment suggest that consistent positive effects of treatment on BW gain or feed conversion were not readily apparent. Larger numbers of birds in each experimental group may yield alternative conclusions. The only possible exception to this trend was observed in trial 3, when an effect of treatment, with dCE alone or dCE + FOS, could be suggested by the collected data (Table 3Go). However, again, these values did not differ significantly (P > 0.05) after statistical analysis.

When effects of the selected treatments on reducing ST crop or cecal colonization were evaluated in the present study, the most consistent effects were observed in the dCE alone and dCE + FOS experimental groups. Fructooligosaccharide alone was associated only with a significant reduction in cecal colonization after selective enrichment of ST in trial 2. This reduction, although significant (P < 0.05), was only 10% lower than the level of recovery observed in the control group. As mentioned above, the dCE alone and dCE + FOS experimental groups were associated with more marked and consistent reductions in ST colonization in the 3 individual trials.

Although several sets of data obtained in the present experiment suggest an added benefit of feeding FOS when birds were administered the dCE on the day of hatch, other sets of data suggest a disadvantage to the addition of FOS. One possible indication of a positive interaction could be observed in trial 1, in which the only group associated with a reduction in crop and cecal ST colonization was the dCE + FOS group. Other suggestions of an effect can be observed in the results of trial 2. Although not statistically different, a numerical suggestion of lower cecal recovery of ST after direct-plating could be seen when the dCE-only group was compared with the dCE + FOS group. Contradicting this trend was the significantly lower rate of recovery of ST from the crops of experimental birds in the dCE-only group, as compared with the dCE + FOS group, when crop samples were selectively enriched (see Table 5Go for both observations). Trial 3 offered similar evidence that a positive interaction, although suggested by some data, appeared to be rebutted by other sets of observations. Taken together, no positive effect of feeding FOS alone was observed in this investigation. Conversely, the experimental groups receiving dCE alone and dCE + FOS were consistently associated with reductions in both crop and cecal colonization by ST in the 3 replicate trials. Suggestions that any of these treatments consistently affected BW gain, feed conversion, and livability in a positive manner are tenuous at best and may require further investigation.


   CONCLUSIONS AND APPLICATIONS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
REFERENCES AND NOTES
 

  1. Throughout all 3 replicate trials, the use of dCE alone or dCE in combination with FOS resulted in a reduced colonization of both the cecum and crop with ST. However, a reduction of ST colonization in either the crop or cecum did not appear to be enhanced by the combination of dCE and FOS compared with that of the dCE alone.
  2. Fructooligosaccharide alone resulted in no reduction of ST in either the cecum or crop as compared with ST in the non-treated control group.
  3. No treatment appeared to have positive and consistent effects on BW gain, feed conversion, or livability.
  4. Further studies are needed to assess the effectiveness of this particular CE culture in combination with other prebiotics.


   REFERENCES AND NOTES
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 

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