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J. Anim. Sci. 2003. 81:553-560
© 2003 American Society of Animal Science

Effect of feeding the ionophores monensin and laidlomycin propionate and the antimicrobial bambermycin to sheep experimentally infected with E. coli O157:H7 and Salmonella typhimurium1

T. S. Edrington2, T. R. Callaway, K. M. Bischoff, K. J. Genovese, R. O. Elder, R. C. Anderson and D. J. Nisbet

Food and Feed Safety Research Unit, Southern Plains Agricultural Research Center,USDA, ARS, College Station, TX 77845

2 Correspondence:
2881 F&B Rd. (phone: 979-260-3757; fax: 979-260-9332; E-mail:
edrington{at}ffsru.tamu.edu).


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
Escherichia coli O157:H7 and Salmonella are widely recognized as important agents of food-borne disease with worldwide distribution. The use of ionophores in feeding growing ruminants is widespread in the United States and has attracted recent interest due to the apparent temporal relationship between initial ionophore use and the increase in human E. coli O157:H7 cases. Two experiments were conducted to evaluate the effects of short-term feeding of ionophores on fecal shedding, intestinal concentrations, and antimicrobial susceptibility of E. coli O157:H7 and S. typhimurium in growing lambs. Sixteen lambs were used in each experiment, four lambs per treatment group: monensin, laidlomycin propionate, bambermycin, and a control treatment. Lambs were fed a grain and hay (50:50) diet with their respective ionophore for 12 d before experimental inoculation with E. coli O157:H7 or S. typhimurium. Animals were maintained on their respective diets an additional 12 d, and fecal shedding of inoculated pathogens was monitored daily. Lambs were killed and tissues and contents were sampled from the rumen, cecum, and rectum. No differences (P > 0.05) in fecal shedding of Salmonella or E. coli O157:H7 were observed due to treatment. Occurrence of Salmonella or E. coli in luminal contents and tissue samples from the rumen, cecum, and rectum did not differ (P > 0.05) among treatments. Feeding monensin decreased (P < 0.05) the incidence of scours in sheep infected with Salmonella compared with the other treatments. No differences in antimicrobial susceptibility were found in any of Salmonella or E. coli O157:H7 isolates. Results from these studies indicate that short-term ionophore feeding had very limited effects on E. coli and Salmonella shedding or on antimicrobial susceptibility in experimentally infected lambs.

Key Words: Escherichia coli O157:H7E. coli O157:H7 • Ionophores • Salmonella • Sheep


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 
In the United States, medical and productivity costs associated with bacterial human food-borne illness have been estimated at $2.9 to $6.7 billion per year. Illness caused by Salmonella and E. coli O157:H7 account for almost half of these costs (Buzby et al., 1996). Escherichia coli O157:H7 has been isolated from beef and dairy cattle at all stages of production, and although shedding is intermittent and can be difficult to detect, it appears to be fairly widespread throughout the bovine population (USDA, 1997; Hancock et al., 1998; Elder et al., 2000). Salmonella populate the intestinal tracts of various animal species, including beef and dairy cattle, which represent a major reservoir for human food-borne salmonellosis (Fedorka-Cray et al., 1998).

Ionophores were approved by the U.S. FDA in the mid-1970s as feed additives, and since then, their use has become routine in the feeding of growing ruminants. The use of ionophores has attracted interest, given the apparent temporal relationship between initial ionophore use in the U.S. cattle industry and the increase in E. coli O157:H7 cases (Griffin and Tauxe, 1991; Rasmussen et al., 1999). Researchers have suggested that because E. coli is a gram-negative bacterium, ionophores could increase the incidence of E. coli in cattle by inhibiting competing gram-positive species (Dennis et al., 1981; Henderson et al., 1981; Schelling, 1984). However, survey data and experimentation in cattle have yielded conflicting results (Garber et al., 1995; Dargatz et al., 1997; Herriott et al., 1998). We hypothesize that the ability of ionophores to alter the gut microbiota may give E. coli and/or Salmonella a selective advantage and warrants research. Therefore, two experiments were conducted to evaluate the effects of feeding the ionophores monensin and laidlomycin propionate and the antibiotic bambermycin on E. coli O157:H7 and Salmonella typhimurium in experimentally infected sheep.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 Implications
 Literature Cited
 
Animals and Experimental Design.
For each of two experiments, 16 Suffolk wether and ewe lambs (average BW = 35 kg) were housed indoors in individual pens with ad libitum access to Bermudagrass hay and water. A commercial lamb diet was provided to each lamb starting at 0.2 kg/d increasing over a 10-d period to a final feeding level of 1 kg animal-1 d-1 (Table 1Go). Hay intake was slowly decreased over this same time so that lambs were consuming approximately a 50:50 concentrate to hay diet. Lambs were randomly assigned to receive daily in their feed, one of four treatments: 1) control (CON): no ionophore; 2) monensin (MON): 90 mg animal-1 d-1; 3) laidlomycin propionate (LP): 37.5 mg animal-1 d-1; and 4) bambermycin (BBM): 5 mg animal-1 d-1. Lambs continued an additional 4 d on full feed before bacterial challenge as described below and remained on this diet throughout the 12-d experimental period. Sheep were killed (Euthasol, Delmarva Laboratories, Inc., Midlothian, VA) on d 12 of each experiment, and tissue from the rumen, cecum, and rectum, as well as their respective lumen contents (10 to 15 g) were aseptically collected for bacterial enumeration as described below. Care was taken to ensure each tissue and lumen content sample was removed from approximately the same location on each animal. Additionally, ileocecal lymph nodes were collected in Exp. 1. The incidence of scours (no indication of fecal pellet formation) was recorded daily in Exp. 1. The Animal Care and Use Committee of the Food and Feed Safety Research Laboratory, USDA preapproved care, use, and handling of experimental animals.


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  		Table 1. Ingredient composition of grain diet fed to lambs (dry matter basis)
 
Bacterial Cultures.
Salmonella typhimurium strain NVSL 95-1776, which was naturally resistant to novobiocin, was made resistant to nalidixic acid in our laboratory via successive cultivation in tryptic soy broth (TSB) containing up to 20 µg/mL of nalidixic acid. Escherichia coli O157:H7 strain BDMS T4169 (ATCC 700728) was obtained from the American Type Culture Collection (Manassas, VA) and was cultivated in anoxic TSB medium at 37°C. This strain was made resistant to novobiocin and nalidixic acid (20 and 25 µg/mL, respectively) via the same procedures as above. These novobiocin/naladixic resistant phenotypes were stable through multiple unselected transfers in batch culture and through repeated culture vessel turnovers in continuous culture (data not shown). Overnight cultures (1,000 mL) were harvested by centrifugation (7,500 x g, 10 min) and the cell pellets were resuspended in TSB medium (150 mL total volume). Sheep were individually inoculated with 10 mL of TSB containing S. typhimurium (Exp. 1; 1 x 109 cfu) or E. coli O157:H7 (Exp. 2; 4 x 1011 cfu) via oral gavage. Fecal samples were collected 3 d prior to dosing and were screened for the presence of wild-type Salmonella and E. coli O157:H7. The day following dosing (d 1) and on each of the subsequent 11 d, fecal samples were collected and fecal shedding of inoculated Salmonella or E. coli were enumerated as described below. Qualitative enumeration was conducted daily in both experiments and quantitatively on d 3, 4, 5, 6, 7, 8, 10, 11, and 12 in Exp. 1 and on all 12 d in Exp. 2.

Bacterial Enumeration.
Ten to fifteen grams of fecal material was collected from each lamb daily. From each composited fecal sample, 1 g of fecal material was serially diluted (10-fold increments) in sterile PBS and plated on brilliant green agar (for inoculated Salmonella) or MacConkey’s agar (for inoculated E. coli O157:H7); each agar was supplemented with novobiocin (20 µg/mL) and nalidixic acid (25 µg/mL). Plates were incubated 24 h at 37°C and colonies that grew on agar plates were directly counted. In order to qualitatively confirm the presence of inoculated E. coli O157:H7 and S. typhimurium, daily fecal samples, intestinal contents, and epithelial tissue samples were incubated (24 h, 37°C) in 10 mL of tetrathionate broth (Salmonella) or 20 mL of GN Hajna with novobiocin/naladixic acid (E. coli O157:H7) and streaked on agar plates as above. Plates showing colony growth were judged to be positive for their respective bacterial species (qualitative enumeration).

Determination of Antimicrobial Susceptibility.
Salmonella and E. coli isolates were collected on d 1, 6, and 12 of each experiment and examined for antimicrobial susceptibility using the National Antimicrobial Resistance Monitoring System (NARMS) 2001 panel. Minimum inhibitory concentrations (MIC) for antimicrobials were determined by broth microdilution according to methods described by the National Committee for Clinical Laboratory Standards (NCCLS, 1999). Susceptibility testing was performed using the Sensititre automated antimicrobial susceptibility system according to the manufacturer’s instructions (Trek Diagnostic Systems, Westlake, OH). The following antimicrobials were assayed: amikacin, amoxicillin/clavulanic acid, ampicillin, apramycin, cefoxitin, ceftiofur, ceftriaxone, cephalothin, chloramphenicol, ciprofloxacin, gentamicin, imipenem, kanamycin, nalidixic acid, streptomycin, sulfamethoxazole, tetracycline, and trimethoprim/sulfamethoxazole. Resistance breakpoints were determined using NCCLS interpretive standards (NCCLS, 1999) unless unavailable, in which case breakpoints in the NARMS 2000 Annual Report (FDA, 2000) were used. Escherichia coli ATCC 25922, E. coli ATCC 35218, and Enterococcus faecalis ATCC 29212 were used as quality control strains for broth microdilution susceptibility testing.

Ionophores, Reagents and Supplies.
Laidlomycin propionate (Cattlyst) was generously provided by Alpharma Inc. (Chicago Heights, IL) and BBM (Gainpro) was provided by Hoechst Roussel Vet (Warren, NJ). Monensin (Rumensin) was from Elanco (Greenfield, IN). Unless otherwise noted, all media and agar were from Difco Laboratories (Detroit, MI). Reagents and antibiotics were obtained from Sigma Chemical Co. (St. Louis, MO).

Statistical Analysis.
Data were analyzed using SAS Version 8.02 (SAS Inst., Inc., Cary, NC). Data for daily fecal shedding of bacteria were analyzed using the Proc Mixed procedure with treatment, day, and lamb included in the model and reported as least squares means ± SEM. Logistic regression was used to analyze the incidence of scours and qualitative bacterial enumeration. Bacterial counts from luminal contents (quantitative) were subjected to ANOVA appropriate for a completely randomized design. Differences among means were considered significant at a 5% level of significance. Power analysis was conducted using GPOWER software (Erdfelder et al., 1996).


   Results
Top
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 Implications
 Literature Cited
 
Experiment 1.
Fecal samples collected prior to inoculation with S. typhimurium were negative for wild-type Salmonella strains (data not shown). Fecal shedding data of S. typhimurium over the 12-d experimental period are presented in Figure 1Go. Data are presented by day, although there was no treatment x day interaction (P > 0.05). Populations of S. typhimurium ranged from 101 to 104 cfu/g of feces throughout the experiment. Overall, S. typhimurium populations tended to decrease by d 4, showed a slight increase on d 5 and 6, and then dropped to low levels by d 12. When examined across days, ionophore feeding had no effect (P > 0.05) on fecal shedding of S. typhimurium.



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  		Figure 1. Fecal shedding (cfu/g feces [log10]) of S. typhimurium in experimentally infected sheep fed a control diet or diets containing monensin, bambermycin, or laidlomycin propionate.

 
Luminal contents from the rumen, cecum, and rectum contained similar (P > 0.05) populations of S. typhimurium, although CON animals had numerically lower counts compared with animals fed ionophores (Table 2Go). Tissue samples from the rumen, cecum, rectum, and lymph nodes were nearly all Salmonella positive after a 24-h enrichment, however there was not a treatment effect (P > 0.05). Contents from the cecum and rectum were positive for generic E. coli, but no treatment differences were noted (P > 0.05; Table 2Go).


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  		Table 2. Lumen contents and tissue samples positive for S. typhimurium and E. coli in sheep experimentally infected with S. typhimurium and fed a control (CON)diet or diets containing monensin (MON), bambermycin (BBM), or laidlomycin propionate (LP) (Exp. 1)
 
The number of lambs per treatment with scours and the number positive for S. typhimurium after enrichment are presented in Table 3Go. The incidence of scours was similar among sheep on the CON, BBM, and LP diets, but was lower (less than half) in MON-fed animals (P < 0.05). When combined over the entire experimental period, the number of sheep shedding S. typhimurium was numerically, but not significantly, higher in all treated groups compared with CON animals. Ionophore treatment had no affect on antimicrobial susceptibility patterns of S. typhimurium isolates at d 1, 6, or 12 of the experimental period (data not shown).


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  		Table 3. Incidence of scours (SC) and fecal shedding of S. typhimurium (ST) in experimentally infected sheep fed a control diet (CON) or diets containing monensin (MON), bambermycin (BBM), or laidlomycin propionate (LP) (Exp. 1)a
 
Experiment 2.
Sheep were examined the day prior to inoculation and found to be negative for E. coli O157:H7 populations capable of growth on novobiocin/naladixic acid supplemented agar, negative for Salmonella, and positive for generic E. coli (data not shown). Fecal shedding of E. coli O157:H7 showed no treatment x day interactions (P > 0.05). Overall, a steady decline in E. coli O157:H7 populations was observed through d 10, after which bacterial numbers began to increase over the last 2 d of the experiment (Figure 2Go). Ionophore treatment had no affect (P < 0.05) on fecal shedding compared with controls when data was pooled across days (3.27 vs. 4.26, 4.49, and 4.58 cfu (log10)/g feces for CON, MON, BBM, and LP treatments, respectively).



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  		Figure 2. Fecal shedding (cfu/g feces [log10]) of E. coli O157:H7 in experimentally infected sheep fed a control diet or diets containing monensin, bambermycin, or laidlomycin propionate.

 
Overall, bacterial populations recovered from lumen contents of the rumen, cecum, and rectum were low with no differences (P > 0.05) observed among treatments (Table 4Go). Salmonella was not recovered from any of the gut samples. Tissue samples enriched for 24 h resulted in at least one E. coli O157:H7-positive tissue sample per treatment; however, no significant differences among treatments were noted (Table 4Go). The total number of sheep shedding E. coli O157:H7 over the 12-d experimental period was numerically higher (P > 0.05) for ionophore treatments when compared with control animals (Table 5Go). Antimicrobial susceptibility was generally unaffected by ionophore treatment at any of the sampling times examined (data not shown). However, the number of isolates resistant to streptomycin appeared to be lower in BBM compared with CON treatments (one vs. three isolates), and collectively, the E. coli isolates from the BBM treatment showed resistance to seven antibiotics compared with four antibiotics for the CON treatment; however, these differences were not significant.


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  		Table 4. Gut contents and tissue samples positive for E. coli O157:H7 and Salmonella spp. in sheep experimentally infected with E. coli O157:H7 and fed a control (CON) diet or diets containing monensin (MON), bambermycin (BMB),or laidlomycin propionate (LP) (Exp. 2)
 

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  		Table 5. Fecal shedding (number of positives by day) of E. coli O157:H7 in experimentally infected sheep fed a control (CON) diet or diets containing monensin (MON), bambermycin (BBM), or laidlomycin propionate (LP) (Exp. 2)
 

   Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
Implications
 Literature Cited
 
Ruminant animals are asymptomatic carriers of E. coli O157:H7 and other enterohemorrhagic E. coli (Rasmussen et al., 1993; Bielaszewska et al., 2000; Cornick et al., 2000), with the majority of human outbreaks linked to contact with ruminant animals or to products derived from them (Gage, 2001). Sheep, like cattle, are naturally colonized by E. coli O157:H7 in a transient and seasonal manner (Chapman et al., 1996; Kudva et al., 1997a,b; Johnsen et al., 2001) and have been documented with populations of E. coli O157:H7 similar to those found in cattle (Zschock et al., 2000). Although the number of human outbreaks of E. coli that are attributed to ovine rather than bovine sources are far fewer, sheep still serve as an effective and economical experimental model of E. coli O157:H7 colonization and infection (Kudva et al., 1995; 1997a; Cornick et al., 2000; Cookson et al., 2001).

Overall, we saw no effect of ionophore treatment on fecal shedding or gut populations of experimentally infected E. coli O157:H7 or S. typhimurium. Previous research, however, has yielded conflicting results. Garber et al. (1995) reported no association between fecal shedding of E. coli O157:H7 and ionophore use in dairy calves. Dargatz et al. (1997) reported no relationship between ionophore use and E. coli O157:H7 in feedlot cattle. In a survey of 100 feedlots in the United States, Losinger et al. (1997) found no difference in the number of fecal samples positive for Salmonella when ionophores were included in the diet. Rather, the prevalence of E. coli O157 was higher in dairy herds that used monensin, lasalocid, and/or decoquinate in their heifer rations compared with herds not using these additives (Herriott et al., 1998).

In support of our findings, Dealy and Moeller (1977) reported that calves supplemented with BBM in their feed had similar intestinal E. coli populations compared to control calves. However, these same authors reported that BBM decreased the percentage of E. coli resistant to streptomycin and oxytetracycline and the percentage of E. coli multiply resistant to two and three antibiotics. Sokol et al. (1973) demonstrated that feeding low levels of BBM to swine reduced tetracycline resistance in E. coli. Similar experiments showed that BBM reduced the number of E. coli resistant to streptomycin and sulfonamides (Federic and Sokol, 1973). Our research tends to agree with these reports. The number of isolates resistant to streptomycin appeared to be less in BBM compared to CON treatments (one vs. three isolates). Additionally, E. coli isolates from the BBM treatment showed resistance to seven antibiotics compared to four antibiotics for the CON treatment. The reason these observations were not statistically different may be related to the small sample size since we examined only one isolate per sheep, giving us a total of four isolates per treatment. However, the current concern over the subtherapeutic use of antibiotics in livestock production and the hypothesized connection to an increase in antimicrobial-resistant pathogens isolated from humans (Cohen and Tauxe, 1986) substantiates the importance and the need for continued research in this area.

The use of BBM-supplemented feed reduced the duration and prevalence of S. typhimurium shedding in experimentally infected calves (Dealy and Moeller, 1977). Furthermore, these authors reported that feeding BBM reduced the number of Salmonella resistant to streptomycin, ampicillin and oxytetracycline. Feeding swine BBM, likewise reduced the duration and prevalence of Salmonella shedding and decreased the number of Salmonella resistant to ampicillin, streptomycin, triple sulfa, and tetracycline (Dealy and Moeller, 1976). Salmonella recovery from various tissues was lower in pigs fed BBM compared to control animals leading these authors to conclude that BBM did not increase the carrier state of Salmonella in pigs. In contrast, we did not observe any difference in the duration or levels of Salmonella shedding nor were any differences noted in antimicrobial susceptibility patterns. We also observed no differences in the number of tissue samples positive for Salmonella, indicating BBM neither increased nor decreased the carrier state of Salmonella in our study. The effect of MON on decreasing the incidence of scours is interesting but difficult to explain considering no treatment differences were observed in the number of positive GIT tissue samples, lumen content concentrations or fecal shedding in these same animals.

Research results examining the effects of ionophores on E. coli and Salmonella are conflicting and highlight the complexity of the ruminant animal. While the results of our research typically agree with most reports concerning MON, we did not see the effects of BBM on these pathogens reported by others. Differences may be due to animal species, duration of experiment, BBM concentration fed, or other variables. We conducted a power analysis on our data to determine if more animals per treatment were needed. Results from Exp. 1 indicate that because so little difference was seen between treatments, thousands of animals would be needed (0.80 power). In Exp. 2, power analysis indicated (0.08 power) that tripling the number of animals per treatment may have produced significant differences. Because this was a terminal study, we used a small number of animals to look for major differences in shedding patterns. Increasing animal numbers as the power analysis indicates in Exp. 2, may have detected small significant differences (one-half log) in shedding, however these differences would be meaningless in modern livestock production. It should be noted that although animals were individually penned, there was the chance for horizontal transmission to occur among animals. To support this, fecal shedding of E. coli in Exp. 1 steadily decreased over time until about d 10, at which time numbers began to increase. However, if examined from a practical livestock production standpoint, horizontal transmission would be the norm rather than the exception.


   Implications
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
Literature Cited
 
The overall effect of short-term feeding of ionophores on Salmonella and E. coli O157:H7 in experimentally infected sheep was negligible. The effects of long-term ionophore feeding (i.e., dairy heifers and feedlot cattle) on gut populations and shedding of food-borne pathogens in ruminants warrants further research. Disseminating the factors involved in the carriage and shedding of food-borne pathogens in ruminants is a complex, but necessary task, as long as there is opportunity for contamination of our food supply. Incorporating knowledge from this and other research, along with pre- and postharvest treatment methodologies may help to improve the safety of ruminant derived foods.


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

Received for publication May 28, 2002. Accepted for publication November 14, 2002.


   Literature Cited
Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Implications
 Literature Cited
 


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