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Dry-rolled or steam-flaked grain-based diets and fecal shedding of Escherichia coli O157 in feedlot cattle¹

J. T. Fox^*, B. E. Depenbusch, J. S. Drouillard and T. G. Nagaraja^*,2

^* Department of Diagnostic Medicine and Pathobiology, and Department of Animal Sciences and Industry, Kansas State University, Manhattan 66506

	Abstract

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Hindgut is a major colonization site for Escherichia coli O157 in cattle. In this study, diets were formulated to effect changes in hindgut fermentation to test our hypothesis that changes in the hindgut ecosystem could have an impact on fecal shedding of E. coli O157. Feedlot heifers (n = 347) were prescreened for the prevalence of E. coli O157 by fecal and rectoanal mucosal swab cultures. A subset of 40 heifers identified as being positive for fecal shedding of E. coli O157 was selected, housed in individual pens, and randomly allocated to 4 dietary treatments. Treatments were arranged as a 2 x 2 factorial, with factor 1 consisting of grain type (sorghum or wheat) and factor 2 being method of grain processing (steam-flaking or dry-rolling). Four transition diets, each fed for 4 d, were used to adapt the animals to final diets that contained 93% concentrate and 7% roughage. The grain fraction consisted of dry-rolled sorghum, steam-flaked sorghum, a mixture of dry-rolled wheat and steam-flaked corn, or a mixture of steam-flaked wheat and steam-flaked corn. Wheat diets contained 52% wheat and 31% steam-flaked corn (DM basis). Fecal and rectoanal mucosal swab samples were obtained 3 times a week to isolate (enrichment, immunomagenetic separation, and plating on selective medium) and identify (sorbitol negative, indole production, and agglutination test) E. coli O157. The data were analyzed as repeated measures of binomial response (positive or negative) on each sampling day. Method of processing (dry-rolled vs. steam-flaked), sampling day, and the grain type x day interaction were significant (P < 0.05), but not the method of processing x grain type interaction. The average prevalence of E. coli O157 from d 9 was greater (P < 0.001) in cattle fed steam-flaked grains (65%) compared with those fed dry-rolled grains (30%). Average prevalence in cattle fed sorghum (51%) or wheat (43%) were similar (P > 0.10) on most sampling days. Results from this study indicate that feeding dry-rolled grains compared with steam-flaked grains reduced fecal shedding of E. coli O157. Possibly, dry-rolling allowed more substrate to reach the hindgut where it was fermented, thus making the hindgut inhospitable to the survival of E. coli O157. Dietary intervention to influence hindgut fermentation offers a simple and practical mitigation strategy to reduce the prevalence of E. coli O157 in feedlot cattle.

Key Words: Escherichia coli O157 • fecal shedding • finishing cattle • grain processing • preharvest intervention

	INTRODUCTION

Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 
Escherichia coli O157 is an important human foodborne pathogen. The gastrointestinal tract of cattle is the major reservoir of the organism, and cattle feces are the primary source of infection (Bach et al., 2002). Many preharvest intervention strategies aimed at reducing prevalence of E. coli O157 have been tested with varying levels of success (Callaway et al., 2003). Fecal shedding of E. coli O157 in cattle is reflective of the ability of the organism to persist in or colonize the gastrointestinal tract. Evidence suggests that the site of persistence or colonization is in the hindgut and not the rumen (Rasmussen et al., 1993; Brown et al., 1997; Grauke et al., 2002; Van Baale et al., 2004). Although the reasons are not known, it is likely that the ecosystem of the hindgut is relatively more hospitable than the rumen.

Therefore, we hypothesize that dietary factors that promote the supply of substrates (starch, fiber, protein, or lipids) to the hindgut will have a significant effect on the ability of E. coli O157 to survive and colonize and thereby influence shedding in feces. Our objective is to use processed grains to effect changes in hindgut fermentation that will have detrimental effects on the survival, growth, and colonization of E. coli O157. Grains that are less extensively digested within the rumen present more starch to the hindgut, thereby increasing fermentative activity and acid production in the hindgut. Steam-flaking of grains has been shown to enhance ruminal starch digestion compared with dry-rolling, effectively reducing the amount of starch reaching the hindgut (Huntington, 1997).

The objective of this study was to evaluate the effects of grain type (sorghum or wheat) and grain processing (dry-rolled or steam-flaked) in finishing diets on prevalence of E. coli O157 in cattle.

	MATERIALS AND METHODS

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Experimental Animals and Design

Animal management and handling procedures for this study were approved by the Kansas State University Institutional Animal Care and Use Committee. Upon arrival at the Kansas State University Beef Cattle Research Center, feedlot heifers were ear tagged, vaccinated, implanted, and had their BW recorded. Heifers (n = 347) were tested for the prevalence of E. coli O157 by fecal and rectoanal mucosal swab (RAMS) cultures (Greenquist et al., 2005). Heifers positive for fecal shedding of E. coli O157 were retested within a week, and 40 heifers (initial BW = 287 ± 5 kg) were selected for use in the study. Heifers were then grouped based on prescreen E. coli O157-positive samples and within group were randomly assigned to 1 of 4 treatments. Treatments consisted of a 2 x 2 factorial arrangement with factor 1 being grain type (sorghum- or wheat-based diets) and factor 2 being the method of grain processing (steam-flaking or dry-rolling). Within treatment, animals were randomly assigned to 1 of 2 barns and 1 of 20 individual pens within each barn.

A series of transition diets were used to adapt animals to high-concentrate finishing diets consisting of 81.4% (DM basis) dry-rolled or steam-flaked sorghum, or 52.0% (DM basis) dry-rolled or steam-flaked wheat (Table 1). Steam-flaked corn was added to wheat diets to achieve a similar forage:concentrate ratio among all diets. Each transition diet was fed for 4 d to achieve the final diet on d 16 of the study.

Feed samples were collected to determine DM (AOAC, 1990). Bunks were evaluated every morning at approximately 0700 h, and feed was delivered once daily at 0900 h. Heifers were fed amounts sufficient to result in only traces of feed remaining on the following day, and any feed remaining from the previous day was weighed and DM was measured to determine feed intake of each animal.

Fecal and RAMS Samples Collection and E. coli O157 Culture

Fecal and RAMS samples were collected from each heifer 3 times a week for 30 d (d 0, 2, 5, 7, 9, 12, 14, 16, 19, 21, 23, 26, 28, and 30). Fecal samples were deposited into Whirl-pack bags (Nasco, Ft. Atkinson, WI) and placed on ice. Rectoanal mucosal swab samples were placed directly into test tubes containing 3 mL of gram-negative broth (Becton Dickinson Co., Franklin Lakes, NJ) supplemented with cefixime, cefsulodin, and vancomycin (GNccv; Greenquist et al., 2005).

Whirl-pack bags and RAMS test tubes were then transported on ice to the laboratory. Approximately 1 g of feces from each heifer was placed into a test tube containing 9 mL of GNccv. Fecal and RAMS tubes were vortexed for 1 min and incubated at 37°C for 6 h. Following enrichment, tubes were vortexed for 1 min and 1 mL from each tube was subjected to immunomagnetic separation (Dynal Inc., New Hyde Park, NY). After the immunomagnetic separation procedure, samples were plated onto sorbitol MacConkey agar (Becton Dickinson Co.) containing cefixime (50 ng/mL) and potassium tellurite (2.5 µg/mL; CT-SMAC). Plates were incubated overnight (16 to 18 h) and up to 6 sorbitol-negative colonies were grown on blood agar (Remel, Lenexa, KS) for 12 to 18 h at 37°C. Cultures from blood agar were tested for indole production and latex agglutination for the O157 antigen (Oxoid Limited, Basingstoke, Hampshire, UK). The species was confirmed by API (Rapid 20E, Biomerieux Inc., Hazelwood, MO) on prescreening samples and samples collected on d 0, 2, and 5.

Fecal pH

Fecal pH was measured in samples collected on d 9, 16, 23, and 30 of the study. Approximately 5 g of feces from each animal were suspended in 25 mL of distilled water inside a 50-mL polypropylene tube (Becton Dickinson and Co.). The tube was vortexed to make a fecal suspension before pH was measured with an Accumet model AR 10 pH meter (Fisher Scientific International, Pittsburgh, PA).

Statistical Analyses

Mean DM values for each dietary ingredient were calculated and used to determine daily DM intake for each animal. Intake expressed as average daily DM intake from d 9 to the end of the study was analyzed using the MIXED procedure (SAS Inst. Inc., Cary, NC) utilizing grain type, grain processing, and the interaction as fixed effects and barn as a random effect.

The prevalence of E. coli O157, expressed as a binomial response (positive or negative) on each sampling day, was analyzed with animal as the experimental unit. Cattle were considered positive if E. coli O157 was detected by fecal or RAMS culture. Samples collected on d 0, 2, 5, and 7 were not included in the analysis because cattle were being fed transition diets consisting of less than 60% sorghum or less than 40% wheat. Data were analyzed using the GLIMMIX procedure of SAS in a split-split-plot design, with the whole-plot factor being prescreen, positive sample group in a randomized complete block design with barn as block. Grain-type, grain processing method and the 2-way interaction made up the subplot, and the sub-sub-plot was repeated measures over sampling days utilizing first order autoregression.

Fecal pH data were analyzed with the MIXED procedure of SAS in a split-plot design with the whole plot factors being grain type, grain processing method, and the 2-way interaction, with repeated measures as the subplot. Barn was included as a random effect in this analysis.

	RESULTS

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One heifer receiving the steam-flaked sorghum treatment was removed from the study on d 5 of the study due to lameness.

Dry-Matter Intake

Mean daily DM intakes from d 9 to the end of the study for heifers fed steam-flaked sorghum, dry-rolled sorghum, steam-flaked wheat, and dry-rolled wheat diets were 6.12 ± 0.38, 6.79 ± 0.36, 6.14 ± 0.38, and 7.21 ± 0.36 kg, respectively. Grain processing affected (P = 0.026) DMI, but grain type and grain type x grain processing interaction did not (P > 0.10). Dry-matter intake of heifers fed diets with dry-rolled grains (7.00 ± 0.26 kg) was greater (P = 0.026) compared with heifers fed diets containing steam-flaked grains (6.13 ± 0.27 kg).

Prevalence of E. coli O157

Mean prevalence of E. coli O157 in all heifers across all sampling days was 50.0%. Analysis of prevalence data began on d 9 when animals were on the third transition diet. Mean prevalences of E. coli O157 from d 9 in heifers fed the steam-flaked sorghum, dry-rolled sorghum, steam-flaked wheat, and dry-rolled wheat diets were 73, 30, 58, and 29%, respectively. Grain-type did not affect (P = 0.29) prevalence of E. coli O157, but the grain type x sampling day interaction was significant (P = 0.04). It should be noted that the grains (sorghum and wheat) were included in diets at different levels to avoid potential ruminal digestive disorders associated with wheat-based diets. On d 12 and 19 of the study, prevalence of E. coli O157 was greater (P < 0.05) in heifers fed sorghum-based compared with heifers fed wheat-based diets, but the difference was not significant on other sampling days (Figure 1).

View larger version (16K): [in this window] [in a new window]   Figure 1. Least squares means (from logistic regression) for prevalence of Escherichia coli O157 from d 9 of the study in heifers fed sorghum (circles; n = 19) or wheat (squares; n = 20) diets. Error bars represent SEM for the main effect on each sampling day. Main effect of grain type, P = 0.29. Grain type x sampling day interaction, P = 0.04. *Means for a specific day are different (P < 0.05).

View larger version (15K): [in this window] [in a new window]   Figure 2. Least squares means (from logistic regression) for prevalence of Escherichia coli O157 from d 9 of the study in heifers fed diets with dry-rolled grains (closed symbols; n = 20) or steam-flaked grains (open symbols; n = 19). Error bars represent SEM for the main effect on each sampling day. Main effect of grain processing method, P < 0.001. Processing method x sampling day interaction, P = 0.45. *Means for a specific day are different (P < 0.05). Means for a specific day are different (P < 0.10).

Fecal pH was measured on d 9, 16, 23, and 30 as a potential indicator of hindgut fermentative activity. Mean fecal pH over all 4 sampling days in heifers fed the steam-flaked sorghum, dry-rolled sorghum, steam-flaked wheat, and dry-rolled wheat diet was 6.47 ± 0.07, 6.53 ± 0.07, 6.53 ± 0.07, and 6.58 ± 0.07, respectively. Grain type, grain processing, and their interaction had no effect on fecal pH; however, sampling day (P = 0.02) and grain type x sampling day interaction (P = 0.01) affected fecal pH. On d 9 of the study when animals were fed the third transition diet, fecal pH was lower (P = 0.01) in cattle fed sorghum diets (6.38 ± 0.08) compared with cattle fed wheat diets (6.56 ± 0.08), but this difference was not apparent on other sampling days.

	DISCUSSION

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Preharvest intervention strategies to eliminate or reduce E. coli O157 in beef cattle have typically been evaluated using experimentally inoculated cattle (Callaway et al., 2002; Van Baale et al., 2004; Bach et al., 2005), experimental trials utilizing large numbers of animals to compare prevalence of natural infection (Brashears et al., 2003; Berg et al., 2004), or observational studies (Garber et al., 1995; Dargatz et al., 1997; Herriott et al., 1998). Potential limitations to these types of studies include the need to euthanize experimentally inoculated animals, the cost incurred with sampling large numbers of animals, and external factors that are difficult to evaluate effectively in observational studies. For this study, we prescreened a population of cattle and selected a subpopulation that was positive for fecal E. coli O157 to impose treatments. This model proved useful in that prevalence was great enough to detect statistical differences among treatment groups with only 10 animals per treatment. We included RAMS method because RAMS has been shown to be more sensitive than fecal testing in detecting animals that are positive for E. coli O157 (Greenquist et al., 2005).

Fecal shedding of E. coli O157 is reflective of the ability of the organism to persist or colonize the gastrointestinal tract. Published data suggest that the hindgut may be the major site of E. coli O157 persistence. Naylor et al. (2003) suggested that the primary site of E. coli O157 colonization was the rectum, specifically the region approximately 2 to 5 cm proximal to the rectoanal junction. In studies with experimentally inoculated cattle (Grauke et al., 2002, 2003; Van Baale et al., 2004) or prevalence data in gut contents collected from necropsied or slaughtered cattle (Laven et al., 2003; Van Baale et al., 2004), E. coli O157 was detected more frequently in the cecum and colon than in the rumen. Possibly, the conditions in the cecum and colon (greater pH, lower VFA concentrations, absence of ciliated protozoa, slower rate of passage of digesta, etc., compared with the rumen) are more hospitable to the survival and growth of E. coli O157.

Sorghum and wheat grains were chosen for this study because their ruminal digestibilities are substantially different, thus differing in the amount of starch reaching the hindgut (Huntington, 1997). Wheat diets (steam-flaked or dry-rolled) in our study contained only 52.0% wheat, and steam-flaked corn was added to achieve similar forage:concentrate ratio among all diets. Because wheat has one of the fastest rates of ruminal starch digestion (Stock and Britton, 1993) with increased propensity to induce metabolic disorders, such as subacute acidosis, feeding high levels of wheat in cattle diets may increase the likelihood of digestive disorders (Axe et al., 1987; Stock and Britton, 1993).

In the current study, DMI was affected by grain processing method. Intakes were lower in cattle fed diets with steam-flaked grains. This observation is consistent with those presented in a review by Owens et al. (1997) in which steam-rolling sorghum, wheat, or corn decreased (P < 0.05) daily DMI of feedlot cattle compared with dry-rolling the grains. Dry matter intakes of wheat-based diets have been reported to be lower than DMI of sorghum-based diets (Owens et al., 1997). In our study, we did not observe differences in DMI among heifers fed sorghum or wheat diets. Differences in DMI of diets containing different grain types or grain processing methods are likely a combination of differences in metabolizable energy and ruminal degradation of starch yielding differences in ruminal acid concentrations (Owens et al., 1997).

Previous studies have shown that cattle diets containing grains with lower ruminal starch degradation are associated with lower prevalence of E. coli O157 (Buchko et al., 2000; Berg et al., 2004). This may be due to a greater amount of starch being fermented in the hindgut, ultimately yielding greater organic acid concentrations and reduced pH in the region of the gastrointestinal tract that has been identified as the primary colonization site of E. coli O157 (Grauke et al., 2002; Van Baale et al., 2004). Although starch fermentation was not measured in this study, we believe that increasing hindgut fermentation of starch and consequent acid production will create inhospitable conditions for E. coli O157. Short-chain fatty acids (acetic, propionic, butyric) have been shown to suppress and inhibit growth of E. coli O157 at pH values of 6.0 and 5.5, respectively (Shin et al., 2002). Van Kessel et al. (2002) evaluated differences in pH and microbial populations in cannulated steers with starch hydrolysate infused into the rumen or abomasum. They reported that infusing starch into the abomasum decreased pH and increased total anaerobic bacteria, total aerobic bacteria, and generic E. coli in the hindgut compared with infusing starch into the rumen. Increased availability of substrate in the hindgut increases the accumulation of organic acids (VFA) and reduces pH (Van Kessel et al., 2002). In our study, differences in fecal pH were not consistently detected among dietary treatments. It is possible that fecal pH may not truly reflect the pH of cecum or colon. In addition to grain processing, greater intake of grains allows more starch to reach the hindgut (Owens et al., 1997). The greater intake of DR grains compared with SF grains observed in our study would further enhance the effects of grain processing on E. coli O157 in the hindgut.

It is documented that dry-rolled grains have decreased ruminal degradation of starch compared with steam-flaked grains, thus presenting more starch to the hindgut and possibly increasing fecal starch content (Zinn et al., 1995; Huntington, 1997). Previous studies have shown that fecal pH of cattle fed steam-flaked grains was greater (P < 0.05) than that of cattle fed dry-rolled grains (Oliveira et al., 1995; Barajas and Zinn, 1998). In these studies, cattle fed steam-flaked grains also had reduced fecal starch compared with cattle fed dry-rolled grains. Berg et al. (2004) observed decreased (P < 0.01) fecal pH and lower (P < 0.05) prevalence of E. coli O157 and in cattle fed corn compared with cattle fed barley. Because barley is more digestible than corn in the rumen, corn diets would present more starch to the hindgut and increase organic acid production, thus reducing pH and potentially reducing survivability of E. coli O157.

In conclusion, prescreening and selecting cattle positive for shedding of Escherichia coli O157 is a useful model to evaluate potential preharvest intervention strategies. Because grain processing influences site and extent of starch digestion in ruminants, it offers a simple and effective method of targeting specific regions of the gastrointestinal tract to affect changes in fermentation (acid production, pH, microflora, etc.). Utilizing grains processed by methods that are known to increase the amount of starch reaching the hindgut and enhance fermentation may be useful in reducing E. coli O157 in cattle if fed prior to slaughter.

	Footnotes

 
¹ Contribution No. 06-219-J from the Kansas Agric Exp. Stn., Manhattan. Financial support for this research was provided in part by a USDA grant (2006-34359-06177). Authors extend special thanks to the staff at the KSU Beef Cattle Research Center and KSU College of Veterinary Medicine Preharvest Food Safety Lab.

² Corresponding author: tnagaraj{at}vet.k-state.edu

Received for publication February 13, 2006. Accepted for publication January 2, 2007.

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Top Abstract INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION LITERATURE CITED

 


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