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USDA-ARS, U.S. Meat Animal Research Center, P.O. Box 166, Clay Center, NE 68933-0166
* Corresponding author (berry{at}email.marc.usda.gov)
Received for publication March 18, 2004.
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ABSTRACT |
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 TOPNOTES ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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Abbreviations: CFU, colony forming units • FSM, feedlot surface material • SMAC, MacConkey sorbitol agar • STEC, Shiga toxin–producing Escherichia coli • TSB, Trypticase soy broth
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INTRODUCTION |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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Preharvest control strategies that successfully reduce E. coli O157:H7 in cattle and the animal production environment will include measures that interrupt the cycling of pathogens in the production environment and subsequent reinfection of the herd. Horizontal transmission by direct or indirect fecal–oral exposure appears to be the primary means of dissemination of E. coli O157:H7 and other Shiga toxin–producing E. coli (STEC) in cattle. Faith et al. (1996) found that both transmission among cattle and contact with areas previously occupied by cattle shedding the pathogen were important factors in the dissemination of E. coli O157:H7 in a dairy herd. Similarly, Cobbold and Desmarchelier (2002) reported a higher prevalence of an inoculated STEC strain among calves housed as a group than among calves housed in separate pens. These researchers found that contamination of pen floors and hides were important environmental sources for STEC transmission to the animals (Cobbold and Desmarchelier, 2002). Several studies have also suggested that water troughs contaminated with feces serve as a reservoir for E. coli O157 for source cycling in cattle and the production environment (Faith et al., 1996; Hancock et al., 1998; LeJeune et al., 2001; Shere et al., 1998).
Although high prevalence of shedding of this pathogen is seasonal (Hancock et al., 1997; Mechie et al., 1997) and cattle appear to shed the pathogen intermittently (Besser et al., 1997; Rahn et al., 1997; Shere et al., 1998), E. coli O157:H7 can persist for long periods in bovine feces. When inoculated at an initial level of 105 CFU g–1 of feces, E. coli O157:H7 survived up to 70 d at 5°C (Wang et al., 1996). At the higher temperatures of 22 and 37°C, the organism survived in bovine feces for up to 56 and 49 d, respectively, in spite of low moisture content and water activity (Wang et al., 1996). Aerated bovine manure from cattle that were inoculated with E. coli O157:H7 remained culture-positive for 47 d (Kudva et al., 1998). Serotypes of STEC other than O157 can also survive in bovine feces for long periods (Fukushima et al., 1999). However, little or no information is available regarding the survival and growth potential of E. coli O157 in soils at the feedlot pen surface, the medium in which bovine feces is deposited in beef animal feeding operations and in which the fecal matter concentration increases during the finishing period. In addition, the effects of the various environmental factors that can influence the survival of this pathogen in feedlot soils are unknown. The objective of this work was to evaluate the impacts of a range of different moisture contents and manure levels on the survival of E. coli O157:H7, generic E. coli, and coliforms in cattle feedlot soils. In a second study, the effects of repeated cycles of wetting and drying and of different drying rates of feedlot soils on these target bacterial populations in feedlot soils were determined.
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MATERIALS AND METHODS |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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In the second study, the feedlot soils were prepared with bovine manure that was naturally contaminated with E. coli O157. Freshly shed bovine feces from cattle housed in the 6000 head capacity beef feedlot at the Roman L. Hruska U.S. Meat Animal Research Center (MARC) were screened to identify feces containing E. coli O157, using a modification of the nonselective enrichment and immunomagnetic separation (IMS) procedures described by Barkocy-Gallagher et al. (2002). Briefly, 10 g of each fecal sample was measured into a sterile filtered sample bag (Spiral Biotech, Norwood, MA), 90 mL of TSB was added, and the bag contents were mixed using a Stomacher Circulator (200 rpm, 1 min; Model 400; Seward Limited, London, UK). To approximate the concentrations of E. coli O157 in any positive samples, 1 mL of each initial feces–TSB preparation was further serially diluted in tubes containing 9 mL of TSB. Both the initial 10–1 enrichment preparations and the diluted samples were incubated at 37°C for 7 h. One-milliliter volumes of the enrichments were subjected to IMS using Dynabeads anti-E.coli O157 (Dynal Biotech ASA, Oslo, Norway) and 50-µL volumes of the concentrated bead suspensions were spread-plated onto sorbitol MacConkey agar (SMAC) containing 0.05 µg mL–1 cefixime and 2.5 µg mL–1 potassium tellurite (CT-SMAC). The CT-SMAC plates were incubated at 37°C for 24 h before examination for E. coli O157. Sorbitol-negative colonies typical of E. coli O157 growth were tested for agglutination with E. coli O157 latex test reagents (Oxoid Limited, Basingstoke, England). These isolates were further confirmed as E. coli by the demonstration of lactose fermentation with gas production, indole production, inability to utilize citrate as a sole carbon source, negative Voges-Proskauer reaction, and positive methyl red reaction (Hitchins et al., 1998), and as E. coli O157 by polymerase chain reaction screening for the presence of the enterohemorrhagic Escherichia coli (EHEC) and E. coli O157 genes stx1, stx2, eaeA, EHEC hlyA, and rfbEO157 (Paton and Paton, 1998). Immediately following their collection and initial sampling, the bovine fecal samples were frozen at –20°C. Before their use in the second study, the E. coli O157–positive fecal samples were thawed overnight at 4°C.
Effects of Manure Content and Moisture Level of Feedlot Soils
The feedlot soils were prepared and mixed as described by Miller and Berry (2005). Freshly deposited bovine feces were collected from cattle housed in the MARC feedlot. Hastings silt loam (fine, smectitic, mesic Udic Argiustolls) was collected from surface soil near the feedlot pens. The manure and soil were dried to final water contents of less than 0.1 g H2O g–1 dry matter. Three different manure contents (5, 25, and 75% manure, dry matter basis) were examined at each of six different moisture levels of 0.11, 0.25, 0.43, 0.67, 1.00, and 1.50 g H2O g–1 dry FSM. Powdered urea was mixed into the feedlot soils at a level of 1 g kg–1 dry FSM before the addition of H2O. Urea is the primary form of nitrogen excreted in bovine urine and this level of urea is consistent with that which can be found in fresh manure. Each treatment combination was prepared in triplicate in plastic pans, with each pan receiving approximately 400 g of FSM with added H2O. Moisture levels were maintained by daily weighing and addition of deionized distilled H2O to the feedlot soils, which were held at room temperature. Room temperature was monitored and ranged from 18.2 to 22.3°C, with an average temperature of 19.0°C. To avoid any potential transport of the pathogen by flies or other vectors, the table bearing the experimental pans containing the soils was draped with mosquito bar netting (Cabela's, Sidney, NE). The feedlot soils were stirred thoroughly before removing samples at Days 0, 1, 2, 3, 7, and 14. The samples were analyzed as described below.
Effect of Fluctuating Moisture Levels of Feedlot Soils
The effects of repeated cycles of water addition followed by drying on the growth and survival of indigenous E. coli O157, generic E. coli, and coliforms were examined in cattle feedlot soils containing 25% manure and 75% soil, dry matter basis. Approximately 1.5 kg of the previously frozen E. coli O157–positive bovine feces were supplemented with additional fresh manure for a total mass of 5.5 kg manure. The manure was mixed with additional dried manure, soil, and urea as described above and by Miller and Berry (2005) to obtain feedlot soil of the targeted manure and soil levels. Prepared in this fashion, the initial moisture content of the feedlot soil and manure mixture was 0.78 g H2O g–1 dry FSM. The feedlot soils were distributed in triplicate to the pans in three different amounts, to also examine the effect of three different levels of moisture loss: the fast-drying, or high moisture flux, pans contained 360 g of feedlot soil; the intermediate moisture flux pans contained 900 g of feedlot soil; and the low moisture flux pans contained 1800 g of feedlot soil. The pans were held at room temperature (approximately 19°C) and covered with mosquito bar netting as described above. The pans were weighed daily to determine moisture loss and deionized distilled H2O was added weekly to return the soil to the initial water content of 0.78 g H2O g–1 dry FSM. The feedlot soils were stirred thoroughly before removing samples at 0, 2, 7, 14, 21, 28, 35, 49, 63, 77, 105, and 133 d. The samples were processed and analyzed as described below.
Sample Analyses
In the first study, populations of the inoculated E. coli O157:H7 streptomycin-resistant mutant were enumerated on SMAC containing 250 µg mL–1 streptomycin (SMAC-Str). Five-gram samples of the feedlot soils were mixed with 45 mL of 2% buffered peptone water (BPW) in a filtered stomacher bag as described above. Following mixing, the filtered samples were serially diluted further as needed in BPW and spread-plated in duplicate onto SMAC-Str plates (0.1 mL per 100- x 15-mm Petri plate). The SMAC-Str plates were incubated for 24 h at 37°C and typical E. coli O157 colonies were enumerated.
In the second study, E. coli O157 in the feedlot soils were enumerated using a most probable number (MPN)–immunomagnetic separation (IMS) technique. Five-gram samples of the feedlot soils were mixed with 45 mL of TSB in filtered stomacher bags as described above. These 10–1 dilutions were split and further diluted 10-fold in TSB as a three-replicate tube MPN. All MPN dilutions were incubated at 37°C for 7 h, after which 1-mL volumes were subjected to IMS and plating onto CT-SMAC as described above. Escherichia coli O157 positive tubes (confirmed as described above) were recorded and the MPN of each soil sample was calculated using the formula of Thomas (1942). After E. coli O157 numbers dropped below levels enumerable by the MPN (less than 1 cell in 3 g of feedlot soil), the entire volumes of the initial 10–1 dilutions were enriched by incubation for 7 h at 37°C and 1-mL volumes were subjected to IMS to determine if low levels of the pathogen were present.
Indigenous generic E. coli and coliforms in the feedlot soils were enumerated in both studies. The initial 10–1 soil sample dilutions in either BPW or TSB were serially diluted further if needed in BPW and 1-mL volumes were plated in duplicate onto Petrifilm E. coli/coliform count plates (3M Microbiology Products, St. Paul, MN). Following incubation at 37°C for 24 h, characteristic E. coli and coliform colonies were counted.
For both studies, water content of feedlot soils was determined by mass loss after drying overnight at 105°C. Additional analyses, including pH determination, organic matter content, and headspace gases composition, were as described in Miller and Berry (2005).
Statistical Analyses
Numbers of bacteria from duplicate plates were averaged and converted to log10 CFU g–1 dry FSM. Least squares means of bacterial populations were analyzed using the general linear model procedure for repeated measurements (SAS Institute, 2001). The unit of observation was the pan. The model included effects of manure level, water content, day, pan (manure level x water content), manure level x water content, manure level x day, water content x day, and manure level x water content x day. The effects of manure level, water content, and manure level x water content were tested using pan (manure level x water content) as the error term. Differences in water loss per drying cycle data were analyzed by Bonferroni's t test (SAS).
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RESULTS AND DISCUSSION |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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0.0001).
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0.01) during the first day or two, then remained stable throughout the remainder of the 14-d study period. Unlike the results seen in feedlot soils of 5% manure, E. coli O157:H7 populations increased in some of the water content treatments of the soils with 25 and 75% manure. In soil with 25% manure at 0.43 g H2O g–1 dry FSM, the E. coli O157:H7 numbers increased by 2 log10 CFU g–1 by Day 3, and persisted at this high level for the remainder of the 14-d study. The reduction of E. coli O157:H7 in the 0.11 g H2O g–1 dry FSM treatment soils containing 25% manure was similar to that seen in 5% manure soils, although the rate was not as rapid. At Day 7, populations had dropped below detectable levels. The response seen at 0.25 g H2O g–1 dry FSM was somewhat between that at 0.11 and 0.43 g H2O g–1; following an initial decline, the E. coli O157:H7 numbers remained steadily high at approximately 5.0 log10 CFU g–1 dry FSM through Day 14. At the higher water contents of 0.67, 1.00, and 1.50 g H2O g–1 dry FSM in the 25% manure soils, levels declined slowly over the course of the experiment to levels of 2.92, 3.21, and 3.62 log10 CFU g–1 of dry FSM, respectively.
Increasing the manure level of the feedlot soils from 25% to 75% shifted the range of soil water content at which the pathogen could grow. In 25% manure soils with water contents of 0.67 and 1.00 g H2O g–1 dry FSM, E. coli O157:H7 populations dropped; however, in feedlot soils of 75% manure and of 0.67 and 1.00 g H2O g–1, the initial populations of 5.9 to 6.0 log10 CFU g–1 dry FSM increased to levels greater than 8.0 log10 CFU g–1 dry FSM by Day 3. And, while the pathogen grew at water content of 0.43 g H2O g–1 in the 25% manure soils, at water content of 0.43 g H2O g–1 in the 75% manure soils, the growth of the organism was inhibited. At 1.50 g H2O g–1 dry FSM and 75% manure, E. coli O157:H7 numbers dropped slowly to 2.65 log10 CFU g–1 dry FSM by Day 14. In 75% manure soils of 0.11 and 0.25 g H2O g–1 dry FSM, E. coli O157:H7 populations were below detectable levels by Day 14.
As noted above, the generic E. coli and coliform populations generally behaved like the E. coli O157:H7 populations in response to the manure levels or water contents of the feedlot soils. The main two divergences in response between E. coli O157 and generic E. coli or coliforms are revealed by visual comparison of the growth and survival curves of the three groupings of bacteria shown in Fig. 1. First, in feedlot soils of all the manure levels examined at water contents of 0.11 g H2O g–1 dry FSM, E. coli O157:H7 populations dropped below detectable levels (<1.0 log10 CFU g–1 of dry FSM) during the course of the study. Populations of generic E. coli and coliforms, on the other hand, remained at detectable levels even though they were reduced substantially at this low water content. Second, generic E. coli and coliforms were capable of growth in some of the feedlot soils in which E. coli O157:H7 did not grow. These results were particularly apparent in the feedlot soils containing 25% manure (Fig. 1). Populations of E. coli O157:H7, generic E. coli, and coliforms all grew readily in the 25% manure soils with water content of 0.43 g H2O g–1 dry FSM. Escherichia coli O157:H7 levels were also stably persistent in the soils with 0.25 g H2O g–1 dry FSM, but declined gradually in the soils with 0.67, 1.00, and 1.50 g H2O g–1 dry FSM. Conversely, generic E. coli and coliforms multiplied in the 25% manure soils of water contents of 0.25 and 0.67 to 1.50 g H2O g–1 dry FSM, although the lag times were extended. In both situations, these differences in responses between the three groupings of bacteria are likely due to variations in the abilities of individual strains of E. coli and/or species of coliform bacteria to grow in the feedlot soils under different conditions of manure or moisture content. Furthermore, these results call attention to the importance of using several strains of the same species or of a closely related group (e.g., generic E. coli or coliforms, respectively) and/or using multiple strains of a specific type (e.g., a mixed cocktail of different isolates of E. coli O157) in such studies.
Miller and Berry (2005) found that three different general environmental conditions occur in feedlot soils based on their water and manure contents and the microbial metabolic activities taking place in the soils (Table 1). By and large, the growth and/or survival of E. coli O157:H7 in the feedlot soils examined in the first study were reflective of these three general environments. At the lowest water contents, in which microbial activity was not detectable or very low, E. coli O157:H7 viability generally was rapidly lost. The feedlot soils of intermediate water contents typically were an aerobic environment; E. coli O157:H7 populations tended to persist at high levels in these soils, and if moisture was adequate, the pathogen could multiply in these soils. At higher water contents, anaerobic, fermentative conditions prevailed. There was an accumulation of lactic acid in these soils and in some cases, soil pH declined. As a rule, the growth of E. coli O157:H7 was inhibited in these soils and populations slowly declined.
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Effect of Fluctuating Moisture Levels of Feedlot Soils
In the first study, relatively constant soil moisture levels were maintained by replenishing water daily. Such constant conditions of hydration would be the exception rather than the rule in nature and in the open feedlot environment. Therefore, the second study was designed to ascertain the effects of repeated cycles of water addition and drying, and therefore the effects of the resultant cycles in soil environment (fermentative, aerobic, and/or dry), on the target bacterial populations. Because water was replenished weekly over the course of the 133-d experiment, there were 19 one-week-long drying cycles. Adding different masses of feedlot soils to the pans was useful for obtaining treatment units with different drying rates (P > 0.05). Mean values of H2O loss per cycle for the high, intermediate, and low moisture flux pans were 0.87, 0.41, and 0.20 g H2O g–1 dry FSM, respectively. Because samples were removed from the pans weekly, the final soil water contents tended to decline over the course of the experiment. However, these water contents for feedlot soils before adding back H2O in the high, intermediate, and low moisture flux pans were generally less than 0.11 g H2O g–1, between 0.25 and 0.43 g H2O g–1, and between 0.43 and 0.67 g H2O g–1 of dry FSM, respectively.
An additional objective of this second study was to determine the effects of these moisture level cycles on E. coli O157 naturally occurring in feedlot soils. Therefore, fresh bovine feces collected from beef cattle that were shedding this pathogen were used to prepare the feedlot soil samples. The prevalence of fecal shedding of E. coli O157:H7 by cattle typically is higher during the summer and early fall (Hancock et al., 1997; Mechie et al., 1997), so the experiment was scheduled in September to improve our chances of obtaining adequate volumes of O157-positive feces. A total of 26 fecal samples were collected and analyzed on two different days, and seven of these samples were positive. Approximate concentrations of E. coli O157 in the fecal samples ranged from 102 to 103 CFU g–1 of fresh feces.
The initial concentrations of the naturally contaminating E. coli O157 in the feedlot soils immediately following their preparation were 2.4 to 2.5 log10 MPN g–1 of dry FSM (Fig. 2) . These low levels of the pathogen declined in soils of all three moisture flux treatments examined. In all flux treatments, E. coli O157 populations were detectable at Day 14, but at Day 21, all were below detectable levels. On Day 35, two of three high moisture flux samples and one of three intermediate moisture flux samples were positive for E. coli O157 by enrichment. Thus, under conditions of moisture cycling and drying, these low initial populations of E. coli O157 were reduced rapidly in the feedlot soils, though their presence could be detected at Day 35.
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Depending on the particular study and the combination of feedlot soil water and/or manure content, all three groups of the target bacteria were observed to be capable of persistence in the feedlot soils. To our knowledge, feedlot soils have not been specifically examined; however, these observations are consistent with survival and persistence reported for E. coli and related bacteria in manure-amended soils. Depending on the date of manure application, Natvig et al. (2002) found that indigenous generic E. coli and Salmonella enterica serovar Typhimurium (at initial levels of 4.5–5.0 log10 CFU g–1 of soil) could be detected and enumerated in manure-fertilized soil by direct plating at 17 weeks after the manure application. In a similar study, Lau and Ingham (2001) reported growth followed by persistence of indigenous E. coli in bovine manure incorporated into either loamy sand or silty clay loam soils (17 g manure per 400 g soil), although soil type did affect survival. Other studies have reported the growth of E. coli O157 in soils amended with bovine manure (Gagliardi and Karns, 2000; Jiang et al., 2002). Gagliardi and Karns (2002) reported that the presence of manure did not appear to affect the persistence of E. coli O157:H7 in soils when 3 g of manure was applied to 500-g soil microcosms. However, they also found that survival of E. coli O157:H7 in soils was improved by the presence of some of the cover crops tested and also by the presence of clay in the soils. Thus, the potential impact of different soil types should be a consideration for the design of similar experiments. The silt-loam soil used in the current work has a high clay content relative to its textural class (B.L. Woodbury, personal communication, 2004), which may have played a role in the high persistence of the pathogen that was observed in the first study. The ability of E. coli O157 to survive for extended periods in soils amended with manure has important implications for the microbial safety of food crops grown in the soils. Recent works have shown that vegetables can be contaminated with this organism during their cultivation in soils amended with manure or compost containing the pathogens, or by irrigation with contaminated water (Islam et al., 2004; Solomon et al., 2002). Furthermore, persistence of E. coli O157 in soils increases the probability of water supply contamination in cases of runoff from fields treated with manures.
The ability of this pathogen to survive for long periods and even grow in feedlot soils suggests that the feedlot pen floor may serve a source of transmission of E. coli O157:H7 to cattle. In their examination of E. coli O157:H7 prevalence in more than 3000 cattle from five Midwestern U.S. feedlots, Smith et al. (2001) found that higher percentages of cattle in muddy pens shed the pathogen than cattle from pens in a normal condition, and they reasoned that the muddy soil environment might facilitate the fecal–oral transmission of pathogens among cattle. A recent work by LeJeune et al. (2004) indicates that the production environment as a reservoir may play a larger role as a source for transmission of the pathogen than do incoming cattle. More work will be needed to determine the role for feedlot soil as a source of E. coli O157:H7 for cattle infection. However, taken together, this information suggests that the soils of the feedlot pen surface may be a potential target for preharvest control measures to reduce E. coli O157:H7 in cattle and the feedlot environment, as well as to reduce the risk of pathogen contamination of water supplies from feedlot runoff. Additional studies are planned to examine other variables, including temperature, that can affect the survival and activities of bacteria in feedlot soils. Future work will also identify specific treatments for the reduction of pathogens in feedlot soils.
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CONCLUSIONS |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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ACKNOWLEDGMENTS |
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NOTES |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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TOPNOTESABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONCONCLUSIONSREFERENCES |
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