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University of Kentucky, Lexington 40546
3 Correspondence:
Dept. of Animal Sciences (phone: 859-257-7534; fax: 859-323-1027; E-mail:
gcromwel{at}uky.edu).
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Abstract |
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 Top Abstract IntroductionExperimental ProceduresResultsDiscussionImplicationsLiterature Cited |
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Key Words: Carbadox • Coliform Bacteria • Mannans • Pigs • Yeasts
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Introduction |
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Mannan oligosaccharides (MOS) from yeast cell walls have been researched with respect to their value in immune modulation (Newman and Newman, 2001; O’Quinn et al., 2001) and in reduction of intestinal pathogen colonization (Newman, 1994). Though results have been somewhat inconsistent, some research suggests that MOS may improve growth performance in young pigs (Davis et al., 1999; Pettigrew, 2000). Considering the possibility of future antibiotic restrictions and potential benefits of MOS, the effects of brewers dried yeast as a source of MOS need to be further researched in pigs. Certain organic acids have been shown to benefit growth in young pigs (Burnell et al., 1988). Whether the efficacy of MOS is influenced by diet acidification is not known.
The objectives of this research were to evaluate the efficacy of brewers dried yeast as a source of MOS, alone and in combination with citric acid, on performance and intestinal health traits of weanling pigs reared in a conventional nursery and to determine if yeast would reduce the colonization of the swine pathogen, E. coli K88, and modulate the immune response in early-weaned pigs.
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Experimental Procedures |
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The brewers dried yeast was a commercial product (Brewtech, International Ingredient Corp., St. Louis, MO), as were the citric acid (Archer Daniels Midland Co., Decatur, IL) and the antibiotic, carbadox (Mecadox-10; Phibro Animal Health, Fairfield, NJ). The yeast contained approximately 43% CP, 2.97% lysine, and 3.13 Mcal ME/kg according to the manufacturer. The yeast was originally assumed to contain approximately 7.8% MOS based on the findings by Brady et al. (1994) that cell walls of Saccharomyces cerevisiae comprise 25% of cell dry mass and contain 31% mannan. However, based on an analysis of the mannose content of the yeast, the MOS content was found to be 5.2%.
Agglutination tests were conducted based on methods described by Mirelman (1980) to confirm that the brewers dried yeast would agglutinate Gram-negative bacteria having Type 1 fimbriae, as described by Firon et al. (1982). Swine pathogenic E. coli K88, two wild-type E. coli (CS1 and CS15) from the same herd from which the pigs in this study originated, Salmonella typhimurium and S. cholerasuis subsp. cholerasuis sero. typhimurium agglutinated with the yeast cells indicating that the yeast cells had the ability to adsorb potential Gram-negative pathogens as has been demonstrated with MOS (Spring et al., 2000).
Experiment 1
Animals, Diets, and Samples.
In a 28-d study, 140 crossbred (Hampshire x Landrace-Yorkshire) barrows and gilts from the University of Kentucky Swine Research herd were used. Pigs from this herd are routinely fed subtherapeutic levels of various antimicrobials, including carbadox (55 mg/kg diet during the postweaning and early growing phase). Pigs were weaned at approximately 21.8 d of age and weighed an average of 6.6 kg initially and 18.0 kg at termination of the 4-wk experiment. Seven pen-replicates of pigs were randomly allotted to four treatments in a randomized complete block design from outcome groups based on initial weight and sex. The pigs were housed five pigs per pen in two environmentally controlled nursery buildings. Elevated, mesh-floor pens measured 0.9 x 2.1 m in one building and 1.2 x 1.2 m in the second building. Each pen was equipped with a nursery-style self-feeder and a nipple waterer for ad libitum provision of feed and water. Pigs were weighed individually and feed consumption was determined at weekly intervals.
Phase I diets, consisting primarily of corn, dehulled soybean meal, roller-dried whey, and spray-dried animal plasma, were fed during the first 2 wk of the study. Phase II diets, consisting primarily of corn, dehulled soybean meal, roller-dried whey, and spray-dried blood cells, were fed during the last 2 wk (Table 1
). The diets were formulated to contain 1.40 and 1.20% lysine during the two phases, respectively, and were supplemented with amino acids, minerals, and vitamins to meet or exceed NRC (1998) requirements. Treatment 1 was a nonmedicated basal diet. The second treatment was the basal diet plus 55 mg carbadox/kg. Treatments 3 and 4 were the basal diet with 3% brewers dried yeast and the basal diet with 3% yeast and 2% citric acid, respectively. The yeast and citric acid were substituted for corn and adjustments in crystalline L-lysine HCl were made to maintain a consistent lysine level across all treatments. Diets were fed in meal form.
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One pig per pen (median-weight pig in each pen) was killed at the end of the experiment (anesthetized with an i.m. injection of ketamine, then euthanatized with an i.v. injection of sodium pentobarbital) and intestinal samples were taken for morphological observation. Small intestinal sections (1 cm) were sampled approximately one- and two-thirds of the length proximal to the pylorus and placed in small amber bottles containing phosphate-buffered neutral formalin solution.
Microbial Analyses.
Fecal swabs were taken at 2 and 4 wk. At each sampling, the swabs were pooled within each pen. Serial dilutions were made based on countable numbers of bacteria observed from incubation plates according to procedures described by Vanderzant and Spllittstoesser (1992). The weight of fecal samples was determined by weighing a tube containing five clean swabs before and after collection of feces. Each set of five swabs from each pen was placed in phosphate-buffered solution in a 1:10 dilution. Secondary dilutions were 10-3 to 10-5 for both coliforms and E. coli populations, 10-6 to 10-7 for Bifidobacteria spp., 10-5 to 10-7 for lactobacilli and total aerotolerant anaerobes, and 10-2 to 10-3 for Clostridium perfringens. They were plated for total coliforms and E. coli using violet red bile agar with methylumbelliferyl-ß-d-gluceronide (Difco, Detroit, MI) and incubated 24 h at 35°C (FDA, 1998). Lactobacilli were enumerated using Rogosa Agar (Oxoid, Ltd., Basingstoke, Hampshire, England), and incubated microaerophillically for 72 h at 35°C. Bifidobacteria spp. were enumerated using modified liver veal agar (Difco) and incubated in an anaerobic chamber containing 84% N2, 10% CO2, and 6% H2 for 48 h at 37°C (McCann et al., 1996). Total aerotolerant anaerobes were determined by plating on reinforced clostrial medium (Difco) and incubated anaerobically 48 h at 37°C. Clostridium perfringens were enumerated using Perfringes agar (Oxoid) and incubated 48 h at 37°C (FDA, 1998). All microbial enumerations were expressed as log10 colony forming units CFU per gram of feces.
Serum Protein and Immunological Analyses.
Serum proteins were measured using a portable refractometer (Westover, Model RHC-200 ATC, Woodenville, WA). For Ig analyses, serum samples were pooled within pen, and IgA, IgG, and IgM were quantified using Radial Immunodiffusion assay kits (Bethyl Laboratories, Inc., Montgomery, TX). The kits were allowed to incubate undisturbed for 18 h at room temperature. After incubation, IgA, IgM, and IgG were quantified by measuring diameter of Ig/anti-Ig complex using a scale provided in the kits.
Morphological Analyses.
Slides of the intestinal samples were prepared by a commercial laboratory (Histo-Scientific Research Laboratories, Basye, VA). One slide was prepared for each sample with three to five cross sections per sample. Villus height and crypt depth measurements were made similarly to those described by Li et al. (1990). Mounted samples were magnified at 40x using an Olympus BX-50 light microscope and a MTI camera attached to a computer in the laboratory of B. M. Davis (Dept. of Anatomy and Neuroscience, University of Kentucky, Lexington). After calibration, eight average villi and their respective crypt depths at approximate equidistant points in each cross section were measured.
Fecal Volatile Fatty Acid and pH Analyses.
Feces were mixed with distilled water (3:1, vol:vol), centrifuged for 10 min at approximately 1,400 x g, then 0.8 mL of 25% metaphosphoric acid was added to the supernates to acidify the samples. The supernates were placed in chromatography vials, capped, and analyzed by GLC (Hewlett-Packard 5890 Series II, Wilmington, DE) according to the methods of Erwin et al. (1961). The fecal pH was determined with an electronic pH meter (Accumet Basic, Fisher Scientific, Fairlawn, NJ).
Experiment 2
Isolation Units.
Six isolation chambers were fabricated from fiberglass with windows and side doors comprised of lexan material (General Electric, Pittsburgh, PA). Side doors and windows were surrounded by rubber gaskets to ensure microbial isolation within the chambers. Two arm-length gloves were attached to a window to allow access into the chamber. Individual air hepafilters (Airguard Industries, Louisville, KY) and excreta containers were used in each unit, and doors were tightly closed after pigs entered their chambers to maintain isolation. Feed was dropped through a capped, 12.7 cm (i.d.) PVC pipe into a self-feeder twice daily to minimize contamination. Tap water was provided by plastic water lines equipped with a filter.
Animals, Diets, and Samples.
Two 39-d trials involving a total of 24 pigs were conducted. Hampshire x Landrace-Yorkshire crossbred pigs from the University of Kentucky Swine Research herd were used in each trial. The pigs initially averaged 11 d of age and 4.1 kg BW. The pigs were randomly allotted to three treatments from littermate outcome groups with two pigs penned together in each chamber. The design was a randomized complete block design with two replications (chambers) per treatment per trial, for a total of four replications in the study.
Three diets containing 1.50% lysine (Table 1
) were fed throughout the entire 39-d experiment to maintain a consistent luminal environment for optimal bacterial colonization. Treatments consisted of a nonmedicated basal diet, the basal diet with 55 mg of carbadox/kg, and the basal diet with 3% brewers dried yeast. The yeast was substituted for corn and adjustments in crystalline amino acids were made to maintain constant levels of lysine, methionine + cystine, and threonine in each diet. All diets met or exceeded NRC (1998) requirements for all nutrients and were prepared in meal form. Pigs were allowed to consume their diets and water on an ad libitum basis.
After a 29-d preliminary period, pigs were inoculated with E. coli K88. The inoculum was prepared from a nalidixic acid (NA) resistant mutant of E. coli K88 obtained from the Food Microbiology Laboratory at the University of Kentucky. Stock cultures were maintained in skim milk at -70°C. Prior to inoculation, cultures were transferred two times into fresh brain heart infusion broth (Difco) and incubated 24 h at 35°C. The pigs were orally dosed with approximately 9.5 x 108 CFU of E. coli K88.
Beginning on the day of inoculation, daily fecal swabs were taken from each pig to quantify total, E. coli K88, and carbadox-resistant coliform populations. Swabs were placed in sterile phosphate-buffered diluent and plated within 1 h after collection. All animals were bled on the day of inoculation (d 0) and on the last day of each experiment (d 10). Pigs were weighed and killed (anesthetized with an i.m. injection of ketamine, then euthanatized with an i.v. injection of sodium pentobarbital) at the end of the study. Intestinal contents and tissue from the duodenum, jejunum, ileum, cecum, and colon were obtained in order to enumerate final bacterial counts for estimation of colonization.
On d 9 of the experimental period in the second trial, six pigs in one replicate died from asphyxiation due to an electrical system failure; therefore, data from those pigs were used only for initial serum protein quantifications and for daily fecal swab analysis.
Microbial Analyses.
Following inoculation (d 0), daily fecal swabs were collected during the 10-d postinoculation period and were plated using serial dilutions as described for fecal swabs in Exp. 1. The swabs were plated on MacConkey CS agar or MacConkey CS agar with 15 µg of carbadox/mL or 35 µL of NA/mL for quantification of total, carbadox-resistant, and E. coli K88 coliform populations, respectively. Because fecal swab samples were handled differently on d 10 of the experimental period, samples from d 10 were not included in the microbial analyses.
Intestinal samples were plated in the same manner as the fecal swabs. Each tissue sample was diluted with phosphate-buffered solution in a 1:10 dilution, "stomached" for 60 s, and coliforms were enumerated.
Serum Protein and Immunological Analyses.
All samples were centrifuged at approximately 1,000 x g for 20 min at room temperature, and serum was collected. Serum protein concentrations were determined using the same methods as described for Exp. 1. The final IgA, IgG, and IgM levels were quantified using the same procedures as previously described.
Statistical Analysis
Most of the data were analyzed as a randomized complete block design using the GLM procedure of SAS (SAS Inst. Inc., Cary, NC). In most instances (except for feed:gain), there was no building x treatment interaction (P > 0.10) for the traits in Exp. 1, so the data were pooled and considered as seven replicates. Likewise, the data from the two trials in Exp. 2 were pooled and considered as four replicates. The statistical model for the performance, immunological and morphological data, fecal VFA and pH data, and tissue microbial data included the effects of replication, treatment, and replication x treatment (experimental error). Nonorthogonal contrasts were performed between the basal and each of the other treatments. The pen or chamber was considered the experimental unit.
For the microbial data in Exp.1 and the daily fecal swab data in Exp. 2, the PROC MIXED procedure of SAS was used for accurate repeated measures analysis (Littell et al., 1998). Replicate, treatment, day, and treatment x day interaction were included in each model statement, with pen or chamber as the experimental unit or "subject," using the compound symmetry covariance structure in Exp. 1 and autoregressive structure in Exp. 2. For each bacterial analysis, differences from adjusted least squares means were used to separate treatment differences across the entire experimental period for each experiment.
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Results |
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). Pigs fed the two yeast-containing diets consumed less feed (P < 0.05), which resulted in reduced growth rates (P < 0.05) over the 28-d test period. These general trends were evident during each week of the experiment. Feed:gain ratios tended to be inferior in the yeast-fed pigs during the initial phase of the experiment, but were similar to those of controls at the end of the 28-d test. Pigs fed carbadox performed similarly as those fed the nonmedicated basal diet during the first phase of the experiment and overall.
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). However, in samples collected at 28 d, numbers of Bifidobacteria spp. and aerotolerant anaerobes were less (P < 0.05) in pigs fed yeast plus acid compared with the controls. At 28 d, lactobacilli counts were greater (P < 0.05) in pigs fed yeast. Yeast addition to diets tended to reduce total coliforms at 14 and 28 d, but not significantly (P = 0.10).
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). The yeast plus citric acid-fed pigs had substantially higher (P < 0.01) levels of IgG than their basal-fed counterparts, and IgG levels in yeast-fed pigs tended (P < 0.10) to be higher than controls. Serum IgA and IgM levels were not affected by yeast treatment nor by feeding carbadox.
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), but average crypt depth was greater in the carbadox-fed group when contrasted to the controls (P < 0.05). The ratio of villus height:crypt depth, an indicator of overall intestinal health (Zijlstra et al., 1994), was similar for the four treatment groups.
Fecal pH and VFA concentrations were determined in this study because they are indicative of fermentation patterns. However, only minor changes in fecal pH and VFA concentrations occurred in the feces of pigs fed the four diets (Table 5). Valerate concentrations were lower (P < 0.05) in pigs fed carbadox, and isovalerate concentrations were lower (P < 0.05) in pigs fed yeast plus acid compared with controls.
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), but the numbers of observations per treatment were too small to statistically detect if the responses were real.
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shows changes in fecal shedding of total coliforms, E. coli K88, and carbadox-resistant coliforms for the 9-d period after the pigs were orally challenged with E. coli K88. Overall, pigs fed brewers yeast shed fewer (P < 0.05) total coliforms in their feces than those fed the basal diet. Counts of E. coli K88 increased by 2 to 3 log units during the first 2 d after oral inoculation, then returned to baseline levels by 7 d after inoculation. Pigs fed the yeast diet shed fewer E. coli K88 than those fed the basal diet during d 1 and 2 postinoculation. Overall, treatment differences in E. coli K88 counts were not evident (P > 0.10). Carbadox resistant coliforms were 1.5 to 2.5 log units higher than basal in feces of pigs fed carbadox.
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. As expected, all enumerations of coliforms were higher in the cecum and colon compared with the duodenum, jejunum, and ileum. Feeding yeast seemed to reduce colonization of total coliforms in the jejunum (P < 0.01) and the cecum (P < 0.05) with a similar qualitative response in most of the other components of the small and large intestine. Carbadox also reduced colonization of total coliforms in the jejunum (P < 0.01) and cecum (P < 0.01). Colonization of E. coli K88 was not consistently influenced by feeding yeast or carbadox except for an increased colonization in the colon of carbadox-fed pigs (P < 0.05). Colonization of carbadox-resistant coliforms was not affected by diet.
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). At the end of the final 10-d period following E. coli K88 challenge, the initial difference between basal- and yeast-fed pigs had disappeared; however, higher serum protein levels were found in carbadox-fed pigs at the end of the study compared with controls (P < 0.01). In general, serum protein levels were greater following the 10 d postchallenge than before the pigs were challenged. Pigs fed yeast tended to have higher levels of IgG and IgA levels at study termination, but the differences were significant only at P < 0.15. The magnitude of the increases, however, was similar to those observed in Exp. 1.
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Discussion |
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The failure of carbadox to stimulate growth performance in the first experiment was unexpected because carbadox has been found in many studies including those of Roof and Mahan (1982), Cromwell and Stahly (1985), Yen and Pond (1984, 1993), and others (as reviewed by Hays, 1981) to enhance weight gains of young pigs. In Exp. 1, the nursery buildings were cleaned with high pressure water and disinfected, so the pens were exceptionally clean at the beginning of the study, which may have been a contributing factor. One of the most widely accepted modes of action for antibiotics is a disease control effect, which explains why pigs in "dirty" environments respond more to growth promotants than those in "clean" environments (Cromwell, 2001). The exceptionally clean environment in this study probably limited the opportunity for growth stimulation that normally has been observed with carbadox addition to diets. In the second experiment (isolation study), there was evidence that growth rates were enhanced with carbadox supplementation, but numbers of animals per treatment were too few to detect treatment effects if the differences, in fact, were real.
Although diet did not have a major effect on the microbial populations in the gut, pigs fed yeast did have the highest lactobacilli counts at 28 d in Exp. 1 (P < 0.05) and, in most cases, the lowest coliform counts in both experiments. The lower counts of total coliforms in Exp. 2 was consistent throughout the postchallenge period and the overall effect was significant (P < 0.05). Also, reduced coliform numbers on gut tissue and in gut contents from the duodenum, jejunum (P < 0.01), cecum (P < 0.05), and colon occurred in pigs fed yeast. Decreases in coliform concentrations are significant because certain toxins produced by coliforms such as E. coli act in the small intestine and colon to produce intestinal hyperactivity, secretion, and diarrhea. Inhibition of the bacteria responsible for toxin production could prevent or decrease the severity of diarrhea (Giannella, 1983). Muralidhara et al. (1977) first proposed a relationship between lactobacilli and coliforms by expressing the relationship as a lactobacilli:coliform ratio. These authors suggested that higher ratios might be associated with a microbial population that is more desirable and that would result in improved growth in the animal.
The higher lactobacilli counts in yeast-fed pigs in Exp. 1 agrees with results of others who have reported numerically higher lactobacilli and Bifidobacteria spp. counts in dogs and pigs fed oligosaccharides (Mathew et al., 1998; Flickinger et al., 2000; Strickling et al., 2000). Other studies have demonstrated shifts in intestinal microbial populations from dietary oligosaccharide supplementation (Quigley, 1996; Flickinger et al., 2000).
We realize that most of our collections were from fecal swabs representing lower tract microbial populations. Although the utilization of fecal samples has obvious limitations when describing the colonization of the anterior gastrointestinal tract, fecal swabs are excellent indicators of the shedding of this potential pathogen. Also, the total coliform counts collected in the upper tract (duodenum, jejunum) at termination of Exp. 2 gave the same trends as observed in the lower tract (cecum, colon) samples and in fecal swab samples in that experiment.
Morphological changes in the gut wall in Exp. 1 were minor and not consistently affected by dietary treatment. The only difference was that pigs fed carbadox had slightly greater crypt depths, which indicates slightly higher rate of cell proliferation in the gut. The reason for this difference in the antibiotic-fed pigs is not clear and may have been simply due to chance. Average villus height and villus height:crypt depth ratios did not differ among dietary treatments. These results are different from some studies with turkeys (Savage et al., 1996b) and pigs (Spencer et al., 1997), in which feeding of oligosaccharides resulted in increased villus heights and reduced crypt depths.
Fecal pH and VFA concentrations are indicative of fermentation patterns. However, in Exp. 1, there were no consistent trends in fecal pH or fecal VFA concentrations among pigs fed the four diets. Some studies have shown that decreases in pH occur throughout the digestive tract when organic acids such as citric or fumaric acid are fed (Burnell et al., 1988; Radcliffe et al., 1998), but citric acid did not affect fecal pH in our study. The fecal VFA patterns generally followed patterns reported in other experiments (Flickinger et al., 2000; Strickling et al., 2000).
Yeast additions to diets seemed to have an effect on the immune response in both experiments. In Exp. 1, increased IgG (P < 0.01) and IgA (not significant) levels occurred in pigs fed brewers yeast alone or in combinations with citric acid compared with pigs fed the basal diet. Similar trends occurred in Exp. 2 in yeast-fed pigs. While an antigenic response to the yeast product cannot be completely ruled out based on results of this research, an Ig response to the yeast is unlikely. Immune responses to fungi generally include activation of the complement system, resulting in an increase in the response of neutrophils and T-cell mediated mechanisms, including activation of macrophages and direct cytotoxic effects.
The trends resulting from the feeding of yeast in our study are in agreement with studies involving turkeys (Savage et al., 1996a) and sows fed MOS products (Newman and Newman, 2001; O’Quinn et al., 2001). These results suggest that MOS products may affect certain Ig thereby possibly enhancing immune modulation as suggested in recent studies by Newman and Newman (2001) and O’Quinn et al. (2001). More research is needed to ascertain the appropriate level of immune modulation for weanling pigs.
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Footnotes |
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2 Appreciation is extended to International Ingredient Corporation, St. Louis, MO, for providing the brewers dried yeast and for collaboration in this research. Appreciation is also extended to Akey, Lewisburg, OH, for providing the vitamin premix and to Heartland Lysine, Chicago, IL; ADM Bioproducts, Decatur, IL; and Degussa Corp., Kennesaw, GA, for providing the amino acids used in this study. Thanks are given to H. J. Monegue for his assistance and deftness in modifying the isolation units, to D. D. Higginbotham for assistance in mixing the diets, to S. T. Franklin for assistance in the immunological assays, to V. Rupard Barnett and D. K. Aaron for assistance in compiling and statistically analyzing the data, and to S. L. Traylor, S. E. Kitts, T. M. Dubbs, J. I. Zaffarano, A. L. P. de Souza, E. G. Xavier, T. A. Meyer, L. A. Pettey, and J. H. Agudelo for their assistance in conducting the experiments.
Received for publication November 28, 2001. Accepted for publication June 6, 2002.
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