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ANIMAL GROWTH, PHYSIOLOGY, AND REPRODUCTION |
1 Departments of Animal Sciences and Industry and
and
Diagnostic Medicine/Pathobiology Kansas State University, Manhattan 66506
Abstract
A 28-d experiment evaluated the growth, acute-phase response, and bacterial shedding patterns in pigs (n = 96; initially 6.8 ± 1.3 kg) fed mannanoligosaccharides (MANNAN) and sodium chlorate (CHLORATE) before and after oral challenge with Salmonella enterica serotype Typhimurium (ST). The negative control diet contained no antimicrobial (CON), and the positive control contained carbadox (CARB; 55 ppm). Test diets contained (as-fed basis) MANNAN (1,500 ppm) or CHLORATE (800 ppm). Pigs were fed diets for 14 d and then given ST orally. Pigs fed CARB had greater ADG over the entire study than pigs from other treatments (P < 0.05). During wk 1 to 2, before ST challenge, feed intake (as-fed basis) was lower for pigs fed MANNAN and CHLORATE than pigs fed CARB (P < 0.05). During the final 2 wk, pigs fed CARB had greater feed intake than pigs on other treatments (P < 0.05). Gain/feed was greater for pigs fed CARB in the 2 wk before ST (P < 0.05); however, in wk 3 to 4 after ST, gain/feed was reduced for CON pigs compared to pigs on other treatments (P < 0.05). Serum IGF-I was decreased at 2 and 4 d after ST (P < 0.001), and, overall, IGF-I was greater in pigs fed CARB than CON or CHLORATE (P < 0.05). Serum haptoglobin concentrations were greater (P < 0.001) for all treatments at d 6 compared with d 13 after ST. Overall, haptoglobin was greater for MANNAN than for CARB and CHLORATE (P < 0.05) and tended to be increased (P < 0.06) relative to CON. Interleukin-6 was not affected by treatment or day post-ST challenge. Fecal shedding of salmonellae organisms was less for CHLORATE (P < 0.05) than all other treatments at 7 d after ST. Shedding scores decreased from d 7 to 14 after ST (P < 0.05) for the CON, CARB, and MANNAN treatments. We conclude that feeding MANNAN and CHLORATE before acute enteric disease challenge may support improved gut function as evidenced by improved gain/feed, and that CHLORATE may decrease bacterial shedding. But neither MANNAN nor CHLORATE enhanced growth relative to the absence of dietary antimicrobials, nor was either treatment as effective as CARB following ST challenge.
Key Words: Antimicrobial • Mannans • Pigs • Salmonella • Sodium chlorate
Introduction
There are concerns that low-dose antimicrobial feeding for growth promotion of livestock may lead to strains of pathogens that are resistant to antibiotic therapy (Bach Knudsen, 2001
). This study was conducted to evaluate alternative feed additives for their effectiveness in enhancing growth in pigs undergoing Salmonella enterica serovar Typhimurium (ST) challenge.
Mannanoligosaccharides (MANNAN) are derived from yeast (Saccharomyces cerevisiae) cell walls, with approximately 45% of the cell wall consisting of mannose residues (Tizard et al., 1989). Lectins specific for mannose predominate in many intestinal pathogens and mediate adherence of bacteria to the epithelia (Baumler et al., 1997). Gram negative bacteria appear to be agglutinated by MANNAN products by interacting with mannose-specific lectins that appear on the surface of the microbes. The inclusion of MANNAN in pig diets may promote overall health and growth by decreasing pathogenic bacteria (Connolly, 2001) and immunomodulation (Newman, 1994; Pettigrew, 2000).
Sodium chlorate (CHLORATE) has also shown promise as a potential feed additive for pigs. Bacteria belonging to the family Enterobacteriaceae (e.g., Salmonella) possess respiratory nitrate reductase activity (Brenner, 1984) that promotes intracellular reduction of chlorate to cytotoxic chlorite (Pichinoty and Piechaud, 1968). Pigs dosed orally with a CHLORATE solution after oral gavage with ST had reduced cecal populations of salmonellae (Anderson et al., 2000). In addition, pigs treated orally with approximately 0.04 g CHLORATE/kg had reduced intestinal pathogenic organisms (Anderson et al., 2001).
To our knowledge, there are no reports of studies in which MANNAN or CHLORATE was directly added to the feed of weanling pigs provided with an active, enteric disease challenge. The current study evaluated growth, acute-phase responses, and patterns of bacterial shedding in pigs fed MANNAN and CHLORATE both before and after enteric disease challenge with ST.
Materials and Methods
Experimental Design.
The experimental protocol used in this study was approved by the Kansas State University Institutional Animal Care and Use Committee. A total of 96 weaned pigs (initially 6.8 ± 1.3 kg) were blocked by weight and sex, and randomly allotted to one of four treatments in a 28-d study. Treatments had 12 replicates (pens) and were arranged in two identical rooms, with six blocks per room, four pens per block, and two pigs per pen. The four dietary treatments (Table 1) were as follows: a negative control with no added antimicrobial (CON), a positive control containing carbadox (CARB; 55 ppm; as-fed basis), and the test diets containing (as-fed basis) mannanoligosaccharide (MANNAN; 1,500 ppm; SAF-Mannan, LeSaffre Yeast Corp., Milwaukee, WI) or sodium chlorate (CHLORATE; 800 ppm; Sigma Chemical Co., St. Louis, MO). None of the diets contained other antimicrobial agents. Pigs were fed test diets 14 d before ST challenge. The level of MANNAN inclusion was consistent with manufacturer-recommended levels. The level of added CHLORATE was based on a published bactericidal level in pigs (Anderson et al., 2001).
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).
Serum Analyses.
Blood was collected into glass tubes containing no anticoagulant. Blood was allowed to clot at room temperature and stored overnight at 4°C before harvest of serum by centrifugation. An immunoradiometric assay, described previously for use in pigs (Balaji et al., 2000), was utilized to analyze serum IGF-I concentrations. Serum was analyzed for haptoglobin with a colorimetric, enzymatic assay (Smith et al., 1998). A swine-specific ELISA was used for determination of IL-6 (R& D Systems, Minneapolis, MN; Quantikine Porcine IL-6 Immunoassay; Catalog No. P6000).
Bacterial Shedding Analyses.
Fecal samples were evaluated for the presence of salmonellae organisms using a semiquantitative approach. Fecal samples were diluted 1:10 in tryptic soy broth (TSB), incubated overnight at 37°C and then diluted 1:100 in 10 mL of Rappaport Vasiliadis (RV) broth (Difco, Detroit, MI). The RV broth was incubated for 24 h at 42°C. Then seven 200-µL aliquots of the fecal dilution were inoculated onto RV Medium Semisolid (MSRV) plates. The remainder of the fecal dilution in TSB and the MSRV plates were incubated at 42°C. After 24 h, MSRV plates were removed and evaluated for evidence of salmonellae growth. Plates with essentially confluent growth throughout were assigned a fecal shedding score of 3. Plates lacking confluent growth, but with one or more positive areas of growth were scored 2. If MSRV plates were negative, then a score of 1 was later assigned to fecal samples that demonstrated positive growth only after more prolonged incubation in TSB. A score of 0 was later assigned to fecal samples that remained negative for salmonellae growth even after prolonged incubation.
Statistical Analyses.
Data were analyzed by the PROC MIXED procedure of SAS (SAS Inst. Inc., Cary, NC) as a randomized complete block design with repeated measures over time on each experimental unit (individual pens). The model included terms for the fixed effects of disease challenge, dietary treatment, time, and the interactions, and block and pen were considered random effects. Comparisons between dietary treatments and/or sampling times were made only when a significant (P < 0.05 unless noted otherwise) F-test for the main effect or interaction was found using the least significant difference procedure. All means presented are least squares means.
Results
Average daily gain (top panel), feed intake (middle panel), and feed efficiency (bottom panel) data were computed and analyzed for the 2 wk before bacterial challenge (wk 1 to 2), the 2 wk following bacterial challenge (wk 3 to 4), and over the entire experiment (Figure 1). Pigs fed CARB had greater ADG (P < 0.05) than pigs on other treatments, both before and after bacterial challenge (Figure 1, top panel). However, during wk 3 (data not shown in Figure 1), the week immediately following ST challenge, ADG did not differ between CON and MANNAN (0.15 ± 0.04 vs. 0.22 ± 0.04 kg/d), but ADG for pigs fed CHLORATE (0.24 ± 0.04 kg/d) was greater (P < 0.05) than CON, and all treatments were less (P < 0.05) than CARB (0.37 ± 0.04 kg/d). Before bacterial challenge, pigs fed MANNAN and CHLORATE treatments had reduced feed intake compared to CARB (P < 0.05), and pigs fed CHLORATE also had lower feed intake than CON (P < 0.05). During wk 3 to 4, and for the entire study, feed intake was greater for pigs fed CARB than all other treatments (P < 0.05). Feed efficiency was greater before ST challenge in pigs fed CARB than other treatments (P < 0.05). However, after bacterial challenge (wk 3 to 4), gain/feed ratio was similar between pigs fed CARB, MANNAN, and CHLORATE, and all were greater than CON (P < 0.05).
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) and feed intake (Figure 3) were measured daily. During the 7 d following ST challenge, there was a significant (P < 0.05) treatment x day interaction for daily RT and a tendency (P < 0.06) for a treatment x day interaction for daily feed intake. Compared to RT on d 0, before ST challenge, pigs assigned to all treatments experienced a uniform febrile response (P < 0.05) within 2 d following oral pathogen treatment. Pigs fed the CON diet had elevated RT within 24 h after infection (P < 0.05), and animals on this treatment did not return to preinfection temperatures until d 4. In contrast, pigs fed CARB only had a single spike in RT on d 2 after treatment (P < 0.05). In general, pigs fed MANNAN and CHLORATE had fever profiles that were similar to CON animals (i.e., 3 d of elevated RT). Rectal temperatures returned to preinfection levels by d 5 postchallenge for all dietary treatments.
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). By d 2, feed intake for all treatments was reduced similarly in response to pathogen challenge. Then, feed intake gradually returned to preinfection levels through the remainder of the week. However, on each day, pigs fed the CARB diet had greater intakes than all other treatments (P < 0.05).
Serum IGF-I concentrations were measured in samples collected on alternate days following ST challenge (Figure 4). There were significant effects of both dietary treatment (P < 0.05) and day postinfection (P < 0.0001) on circulating IGF-I, although the interaction was not significant. As was expected, circulating IGF-I, across all treatments, was reduced (P < 0.001) in response to ST infection on d 2 (25.4 ± 4.5 ng/mL) and 4 (33.7 ± 6.2 ng/mL) relative to d 0 (92.9 ± 12.7 ng/mL; P < 0.001). Dietary treatment also affected circulating levels of IGF-I. In general, IGF-I was greater in pigs fed CARB (89.0 ± 13.8 ng/mL) than CON (38.3 ± 13.8 ng/mL) and CHLORATE (57.3 ± 14.0 ng/mL; P < 0.05), and tended to be greater than MANNAN (42.2 ± 13.8 ng/mL; P < 0.10).
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). Serum haptoglobin concentrations were greater (P < 0.001) for all treatments on d 6 (76.3 ± 3.4 mg/dL) compared to d 13 (47.6 ± 3.4 mg/dL). When averaged across both d 6 and d 13, haptoglobin was greater (P < 0.05) for MANNAN (74.6 ± 5.8 mg/dL) than for CARB (56.2 ± 5.4 mg/dL) and CHLORATE (57.7 ± 5.4 mg/dL) treatments and tended to be increased (P < 0.06) relative to CON (59.3 ± 5.4 mg/dL).
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A significant treatment x day interaction (P < 0.05) was observed for fecal shedding of salmonellae organisms. Relative to all other treatments, CHLORATE fed pigs had lower (P < 0.05) shedding scores on d 7 following ST challenge (Figure 6). Between d 7 and 14 postchallenge, shedding scores decreased (P < 0.001) in all treatments except CHLORATE. At 14 d following ST challenge (d 28 of the study), shedding scores were generally similar between treatments, although pigs fed CARB had lower scores than pigs fed CHLORATE (P < 0.05).
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Growth Performance.
Comprehensive reviews by Hays (1978), Zimmerman (1986), and Cromwell (2002) have all documented the growth-promoting properties of antimicrobials in swine production. These reviews have all contributed to the current dogma that antimicrobials included in swine diets act to improve feed efficiency and rate of growth. In another, more recent compilation of the relevant literature, Dritz et al. (2002), reaffirmed the efficacy of antimicrobials as growth promotants in nursery pigs, but to a lesser degree than depicted in previous reviews. In that review, the authors suggested that improved hygiene in contemporary swine production systems probably accounted for some of the reduced magnitude in growth response of pigs to dietary antimicrobials compared with earlier reports. In the current study, our bacterial challenge set up a controlled experimental model that exposed maximum beneficial effects of CARB relative to the negative control diet. These benefits were especially evident after ST challenge when pigs fed CARB had 50% greater gains, 24% greater intakes, and 38% improvements in efficiency than pigs fed the negative control diet. Over the entire study, CARB improved gain by 37% compared to pigs fed the negative control diet. It should be noted that these effects of CARB could even be greater in similar circumstances under field conditions because institutional animal care policies required that all pens be thoroughly washed daily in the current study, likely minimizing reexposure to pathogens shed in the feces.
Alternatives to antimicrobials are currently being evaluated to determine their effect on the growth performance in young pigs. Various researchers (Pettigrew, 2000; LeMieux et al., 2001; Hancock et al., 2002; Davis et al., 2002) have all reported numerical improvements in ADG, ADFI, and(or) feed efficiency when MANNAN were fed alone or in combination with other antimicrobials. In other studies (Ko et al., 2000; White et al., 2002), researchers reported no response or a negative response when MANNAN was included in the diets of young pigs. Ours is the first report of growth performance in pigs fed CHLORATE in the diet. Over the entire 28 d in the current study, pigs fed MANNAN or CHLORATE performed similarly to pigs fed diets with no added antimicrobial. However, both MANNAN and CHLORATE tended to have improved gain and feed efficiency in the week immediately following ST challenge compared to CON, perhaps suggesting a beneficial effect of these products in protecting gut function in the face of active enteritis.
The effect of CHLORATE to support improved gain in the week immediately following ST challenge, and the lower fecal culture scores observed in this treatment are generally supportive of the demonstrated bactericidal function of CHLORATE in pigs (Anderson et al., 2001). The concentration of CHLORATE in our experimental diet was extrapolated from that published report to achieve a bactericidal level of chlorate in the gut. It is important to note that this concentration may have presented palatability problems as it reduced feed intake in the first 2 wk of the study. In a subsequent study without ST challenge, it was demonstrated that 200 ppm CHLORATE was better than 800 ppm for enhancing gain of nursery pigs and this performance tended to be greater than pigs fed diets free of added antimicrobials (Burkey et al., 2003).
Acute Febrile, Feed Intake, and Insulin-Like Growth Factor-I Effects.
In previous studies, tracking acute febrile and feed intake responses have proven useful measures of the clinical manifestations in pigs with enteric disease (Balaji et al., 2000; Turner et al., 2002a,b). However, responses in control vs. antibiotic-fed pigs were not compared in those studies. In this regard, the advantage of pigs fed CARB was evident in that they had only a single day of elevated temperature (compared to the day of challenge) and intakes were uniformly greater than all other treatments. Thus, in the week following bacterial challenge, benefits noted for pigs fed CHLORATE or MANNAN in gain and efficiency were clearly not reflected in less severe enteritis-associated fever and inappetence.
Circulating IGF-I is sensitive to acute changes in feed intake and has, therefore, provided useful ancillary data as an additional readout of the severity of the enteric disease process (Balaji et al., 2000; Turner et al., 2002a,b). In the present study, reductions in circulating IGF-I following ST were similar to results obtained previously in enteric disease-challenged pigs. Although there was not a significant treatment x day interaction, the effects of both dietary treatment and day postinfection on circulating IGF-I were significant. The greatest depressions in circulating IGF-I were at 24 and 48 h after infection, and this decline in IGF-I was coincident with the aforementioned decline in intake. Averaged across the entire week postchallenge, pigs fed CARB maintained the greatest concentrations of IGF-I and this is undoubtedly associated with their relatively rapid recovery of feed intake.
Acute-Phase Responses: Haptoglobin and IL-6.
We expected serum haptoglobin to be increased by enteric disease and that the concentration would decrease with time as pigs recovered from ST-induced enteritis (Dritz et al., 1996; Turner et al., 2002a,b). We further hypothesized that CARB-fed pigs might have sufficient containment of their gut inflammatory response such that they might have a much-reduced haptoglobin response. This was not the case, however, as the haptoglobin changes from d 6 to 13 after challenge did not differ significantly among treatments. In fact, only when averaged across days did haptoglobin differ among treatments, and even then, contrary to our hypothesis, haptoglobin was slightly elevated in pigs fed MANNAN. The reason for this treatment effect was unexpected given the aforementioned ability of MANNAN to bind bacteria in the gut. At present, we do not have a definitive explanation for this observation.
Previous studies had shown that ST-induced enteric disease was not accompanied by altered serum TNF
(Balaji et al., 2000). At the time of that study, a swine-specific ELISA for porcine IL-6 was not available, so the current study is the first to evaluate systemic IL-6 in an enteric disease model with live ST. Our failure to find changes in circulating IL-6 is generally consistent with our previous data for systemic TNF in pigs with active enteric disease. However, this observation is significant in light of the haptoglobin data and the view that changes in plasma acute-phase proteins are driven by changes in circulating cytokines, notably IL-1 and IL-6 (Baumann and Gauldie, 1994). Our finding that systemic IL-6 was not altered consistently in the periphery, whereas haptoglobin decreased from d 6 to 13, suggests that cytokines acting locally within the liver, rather than in an endocrine-like systemic fashion, may account for changes in ST-induced hepatic acute-phase proteins (Turner et al., 2002a,b).
Bacterial Shedding.
We hypothesized that MANNAN would affect shedding of salmonellae organisms because MANNAN in the diet of weanling pigs may prevent the attachment of pathogens to the intestinal epithelium and provide a source of attachment for invading bacteria (Newman, 1994). By offering bacteria a surrogate source of attachment other than the gut wall, clearance of the pathogenic organism was predicted to be more rapid. In addition, CHLORATE is reduced to sodium chlorite, which is bactericidal (Anderson et al., 2001), and could potentially reduce shedding because of the cytotoxic nature of the substance within the gastrointestinal tract.
In the present study, pigs fed the diet containing CHLORATE had decreased fecal shedding scores at 7 d postinfection, and, in fact, many CHLORATE-fed pigs were negative for salmonellae (fecal score of 0) at that time. A reduction in gut bacterial load would be suggested by these low fecal culture scores and would be the most likely factor associated with the improved gain and feed efficiency for these pigs (compared with controls) during the week following bacterial challenge. On the other hand, it is interesting to note that even in the face of similar fecal culture scores in pigs fed the CARB diet compared to pigs fed both CON and MANNAN diets (suggesting similar bacterial loads in the gut), pigs fed CARB had substantially increased intakes and growth performance in the week following bacterial challenge. One of the mechanisms by which dietary antimicrobials are assumed to enhance growth in pigs relates to their ability to reduce viable bacterial numbers in the gut. However, our data suggest that this explanation cannot entirely account for these well-known effects on growth. Perhaps one of the effects of CARB may be to reduce epithelial attachment and colonization rather than absolute numbers of viable salmonellae, at least when they are present in very large numbers, as would be the case in our ST challenge model.
Implications
In general, pigs fed both dietary test substances, mannanoligosaccharide and sodium chlorate, performed similarly to pigs fed no added antimicrobial in the negative control diet. None of the additives equaled the growth-promoting effects observed with dietary antibiotic, especially in the presence of the active enteric disease. It is noteworthy, however, that both mannanoligosaccharide and sodium chlorate improved feed efficiency following bacterial challenge, which may suggest some degree of gut protection in the face of the pathogenic insult. Furthermore, sodium chlorate enhanced growth relative to the diet containing no added antimicrobials in the week immediately after bacterial challenge, and pigs fed this diet also had reduced bacterial load (as evidenced by lower shedding scores). Thus, we suggest that further evaluation of sodium chlorate as a feed additive is warranted because the level used in the current study had a negative effect on growth before bacterial challenge.
Footnotes
1 Contribution 04-016-J of the Kansas Agric. Exp. Stn. The authors thank M. R. Barker and C. M. Hill for assistance with animal management and laboratory analyses, respectively. The authors gratefully acknowledge partial support from LeSaffre Yeast Corp., Milwaukee, WI, and from USDA under section 1433 of Public Law 95-113. 
2 Correspondence: 253 Weber Hall (phone: 785-532-1238; fax: 785-532-7059. e-mail: eminton{at}ksu.edu).
Received for publication July 28, 2003. Accepted for publication November 7, 2003.
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