Association between animal age and the prevalence of Shiga toxin-producing Escherichia coli in a cohort of beef cattle

doi:10.1016/j.vetmic.2014.12.016

Veterinary Microbiology

Volume 175, Issues 2–4, 25 February 2015, Pages 325-331

https://doi.org/10.1016/j.vetmic.2014.12.016 Get rights and content

Highlights

•
Identified animal age as a critical factor that affects the prevalence of STEC.
•
Heifers had lower STEC prevalence than cows, but higher concentrations when present.
•
STEC prevalence peaked in cows that were two years of age.
•
Uniparous showed the highest STEC prevalence, and no difference among multiparous.
•
Findings have clear implications for the development of on-farm STEC mitigation.

Abstract

Even with advancements in pre- and post-harvest food safety, Shiga toxin-producing Escherichia coli (STEC) still present challenges to human health. Since cattle are the primary reservoir for STEC, lowering the prevalence of this pathogen in farm animals may reduce STEC outbreaks in humans. However, because many of the factors that modulate the colonization and persistence of STEC in cattle remain unknown, reducing STEC in this host is challenging. In this study, we evaluated a cohort of beef cattle one to eleven years of age to determine the effect of animal age on the prevalence of STEC. During the first year of sample collection, heifers had significantly lower STEC prevalence than cows (37.5% vs. 70%). In the second year of sample collection, STEC prevalence peaked in cows that were two years of age and tended to decrease as animals became older. In addition, by studying a subset of the animals in both years, we observed an increase in STEC prevalence from 40.6% to 53.1% in heifers, whereas cows had a net decrease in STEC prevalence from 71.4% to 61.9%. The results from this study indicate that animal age is a significant factor that influences the prevalence of STEC in cattle. These findings have implications for the development of on-farm mitigation strategies by targeting animals with the highest risk of shedding; it could be possible to reduce pathogen transmission among cattle and prevent zoonotic or foodborne transmission to humans.

Introduction

Even though progress has been made to reduce the incidence of diseases caused by foodborne pathogens, they remain of great economic and public health concerns. The Centers for Disease Control and Prevention (CDC) has estimated that pathogenic Shiga-toxin producing Escherichia coli (STEC) cause about 269,000 cases of illnesses (including ca. 3700 hospitalizations and 30 deaths) in the United States every year (Scallan et al., 2011). Among STEC serotypes, E. coli O157:H7 is the most well-known and can cause hemorrhagic colitis, bloody diarrhea, and hemolytic uremic syndrome (HUS) in humans (Kaper et al., 2004). Non-O157 STEC serogroups, such as O26, O45, O103, O111, O121, and O145, commonly called the “Big Six” serogroups, accounted for about 71% of non-O157 STEC isolates between 1983 and 2002, and have been also associated with human disease outbreaks in United States (Brooks et al., 2005). As such, the Big Six non-O157 STEC have been declared as food adulterants by the U.S. Department of Agriculture, Food Safety and Inspection Service (U.S. Department of Agriculture, 2012).

Cattle are considered the primary reservoir for STEC with multiple STEC serogroups isolated from both dairy and beef cattle (Cernicchiaro et al., 2013, Murinda et al., 2004, Pradel et al., 2000). Estimates of the prevalence of STEC in herds of cattle vary widely from 4.6% to 55.9% (Cernicchiaro et al., 2013, Jenkins et al., 2003, Renter et al., 2007). A multitude of factors modulates the colonization and persistent shedding of STEC in cattle. These include bacterial factors that affect the colonization of the recto-anal junction (RAJ), which likely allows the persistence and shedding of this pathogen for weeks or months (Jeong et al., 2013, Naylor et al., 2003). Environmental factors, such as precipitation, temperature, soil characteristics, and presence of wild animals and insects are also believed to modulate the presence of STEC in the environment (Ferens and Hovde, 2011, Shere et al., 2002). It has been recently shown that animal factors, including breeds and physiological differences may affect the prevalence of E. coli O157 in cattle (Jeon et al., 2013).

Since several factors modulate the colonization and persistence of STEC in cattle, controlling the prevalence of STEC in cattle to reduce outbreaks of this pathogen in humans is challenging. It may explain why outbreaks of STEC continue despite a great deal of research focusing on improving food safety. Reducing the prevalence of STEC in cattle at the pre-harvest level has been recently highlighted as an intervention point (Arthur et al., 2011, Chase-Topping et al., 2007, Jeong et al., 2011), and it has been suggested that lowering the STEC prevalence on farms may reduce the total number of E. coli O157:H7 outbreaks in humans (Matthews et al., 2013). Recently we have shown that animal physiological differences contribute to the prevalence of E. coli O157 in cattle (Jeon et al., 2013), which lead us to hypothesize that animal age may also play a role in the prevalence of this pathogen. To better understand the effect of cattle age on the prevalence of STEC, a herd of beef cattle, one to eleven years of age, was monitored for two years to determine the prevalence of multiple STEC genotypes over time.

Section snippets

Ethics statement

Standard practices of animal care and use were applied to animals used in this project. Research protocols, including permission for animal care facility in the University of Florida—North Florida Research and Education Center (NFREC, Marianna, Florida, USA), were approved by the University of Florida Institutional Animal Care and Use Committee (IACUC Protocol no.: 201308027).

Animal management and sample collection

Fecal samples were collected with cotton-tipped swabs (Fisher Scientific, USA) to scrape off bacteria from recto-anal

Heifers had lower prevalence of STEC compared to older cows

In the samples collected during the first year (n = 90), the prevalence of STEC in cattle was 55.6%. Among STEC genotypes, stx2 (33.3%) and stx1/stx2 (30.0%) were the most dominant while only 5.6% of cattle shed STEC with stx1. Multiple genotypes of STEC isolates were detected from 11.1% of the animals (Fig. 1A). To test if animal age affects the prevalence of STEC, we categorized the animals into two groups: heifers (at least one year of age) and cows (at least two years old with at least one

Discussion

Our findings provide insight into the prevalence of STEC in cattle that could be used to mitigate transmission to humans by lowering this pathogen at the pre-harvest level. In this study, we demonstrated that animal age is associated with the prevalence of STEC in cattle. Heifers less than two years old had significantly lower STEC prevalence compared to cows that had previously given birth.

We showed that STEC shedding is lower in heifers compared to cows (Fig. 1). It is possible that multiple

Acknowledgements

We are grateful to Drs. Soojin Jeon, Manhwan Oh, Dongjin Park, Seung Cheon Hong, and Ms. Maria B. Cevallos for technical support and helpful discussion. This work was supported by USDA-NIFA-CRIS program (FLA-ANS-005218) and also supported in part by USDA-AFRI Grants program (Nanotechnology for Agricultural and Food Systems, 2014-67021-21597) to KCJ.

References (30)

J. Bai et al.
A multiplex PCR procedure for the detection of six major virulence genes in Escherichia coli O157:H7
J. Microbiol. Methods
(2010)
K.C. Jeong et al.
Prevalent and persistent Escherichia coli O157:H7 strains on farms are selected by bovine passage
Vet. Microbiol.
(2013)
J. Kim et al.
Factors impacting the regrowth of Escherichia coli O157:H7 in dairy manure compost
J. Food Prot.
(2009)
T.M. Arthur et al.
Prevalence and characterization of non-O157 Shiga toxin-producing Escherichia coli on carcasses in commercial beef cattle processing plants
Appl. Environ. Microbiol.
(2002)
T.M. Arthur et al.
Survival of Escherichia coli O157:H7 on cattle hides
Appl. Environ. Microbiol.
(2011)
L. Beutin et al.
Epidemiological relatedness and clonal types of natural populations of Escherichia coli strains producing Shiga toxins in separate populations of cattle and sheep
Appl. Environ. Microbiol.
(1997)
E. Bok et al.
Age as a factor influencing diversity of commensal E. coli microflora in pigs
Pol. J. Microbiol.
(2013)
J.T. Brooks et al.
Non-O157 Shiga toxin-producing Escherichia coli infections in the United States, 1983–2002
J. Infect. Dis.
(2005)
N. Cernicchiaro et al.
Prevalence of Shiga toxin-producing Escherichia coli and associated virulence genes in feces of commercial feedlot cattle
Foodborne Pathog. Dis.
(2013)
M.E. Chase-Topping et al.
Risk factors for the presence of high-level shedders of Escherichia coli O157 on Scottish farms
J. Clin. Microbiol.
(2007)

S. Cho et al.

Cattle-level risk factors associated with fecal shedding of Shiga toxin-encoding bacteria on dairy farms, Minnesota, USA

Can. J. Vet. Res.

(2009)

S.E. Dowd et al.

Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP)

BMC Microbiol.

(2008)

L.M. Durso et al.

Animal-to-animal variation in fecal microbial diversity among beef cattle

Appl. Environ. Microbiol.

(2010)

W.A. Ferens et al.

Escherichia coli O157:H7: animal reservoir and sources of human infection

Foodborne Pathog. Dis.

(2011)

J. Frohlich et al.

Maternally and naturally acquired antibodies to Shiga toxins in a cohort of calves shedding Shiga-toxigenic Escherichia coli

Appl. Environ. Microbiol.

(2009)

Cited by (25)

Seasonal effect on Salmonella, Shiga toxin-producing E. coli O157:H7 and non-O157 in the beef industry in Colombia, South America
2021, Heliyon
Citation Excerpt :
The authors suggest that this can be due to a more developed stomach in which high volatile fatty acids suppress the growth of E. coli O157:H7 (Cray and Moon, 1995). Contrary to these results, Mir et al. (2015) found an inverse influence between animal age and STEC shedding in feces. Based on their study, heifers have an STEC prevalence of 37.5% while cows 70%.
This research investigated the variations in the occurrence of Salmonella, STEC O157:H7 and non-O157 in the beef production chain in Colombia affected by seasons, hypothesizing that pathogen prevalence will be highest in the rainy season owing to soil moisture promoting bacteria multiplication and transfer between animals. To test this hypothesis, samples were obtained from five abattoirs, which represent 50% of the beef production in this country. A total of 1017 samples were collected, from which 606 were bovine feces, 206 were hide swabs, and 205 corresponded to carcass post-intervention. From the 1017 samples, 49.9% (n = 507) were collected during dry season, while 50.1% (n = 510) during rainy season. All samples (n = 1017) underwent screening for E. coli O157:H7 and Salmonella, while only a proportion of fecal samples (n = 339) were screened for the big six STEC serogroups and their virulence markers. The effect of season, age of animal and sex of animal were correlated with the prevalence results. A total of 84.7% of fecal samples carried virulence genes associated to STEC (stx or eae), suggesting that testing and control should be increased for the big-six STEC compared to E. coli O157:H7. Pathogen prevalence in feces was found to be 8.3%, 5.0%, and 51.0% for Salmonella, E. coli O157:H7 and STEC non-O157, respectively. Hides had a prevalence of 15.0% and 6.8% of Salmonella and E. coli O157:H7, respectively. Carcasses post-intervention were found to have 4.4% and 2.5% prevalence of Salmonella and E. coli O157:H7, respectively. A seasonal effect was found for fecal samples. E. coli O157 and non-O157 STEC shedding were significantly higher (P ≤ 0.05) during rainy season compared to dry season. In contrast, hides and carcasses were more likely to present lower incidence of pathogens during rainy months compared to dry season; however, it was significant only for Salmonella on carcasses with estimated odds of detection almost six times higher in the dry season relative to the rainy season (OR = 5.90, 95% CI 1.18–29.57).
Recovery rate of cells of the seven regulated serogroups of Shiga toxin-producing Escherichia coli from raw veal cutlets, ground veal, and ground beef from retail stores in the mid-atlantic region of the United States
2021, Journal of Food Protection
A total of 482 veal cutlet, 555 ground veal, and 540 ground beef samples were purchased from retail establishments in the mid-Atlantic region of the United States over a noncontiguous 2-year period between 2014 and 2017. Samples (325 g each) were individually enriched and screened via real-time PCR for all seven regulated serogroups of Shiga toxin–producing Escherichia coli (STEC). Presumptive STEC-positive samples were subjected to serogroup-specific immunomagnetic separation and plated onto selective media. Up to five isolates typical for STEC from each sample were analyzed via multiplex PCR for both the virulence genes (i.e., eae, stx₁ and/or stx₂, and ehxA) and serogroup-specific gene(s) for the seven regulated STEC serogroups. The recovery rates of non-O157 STEC from veal cutlets (3.94%, 19 of 482 samples) and ground veal (7.03%, 39 of 555 samples) were significantly higher (P < 0.05) than that from ground beef (0.93%, 5 of 540 samples). In contrast, only a single isolate of STEC O157:H7 was recovered; this isolate originated from 1 (0.18%) of 555 samples of ground veal. Recovery rates for STEC were not associated with state, season, packaging type, or store type (P > 0.05) but were associated with brand and fat content (P < 0.05). Pulsed-field subtyping of the 270 viable and confirmed STEC isolates from the 64 total samples testing positive revealed 78 pulsotypes (50 to 80% similarity) belonging to 39 pulsogroups, with ≥90% similarity among pulsotypes within pulsogroups. Multiple isolates from 43 (67.7%) of 64 samples testing positive had an indistinguishable pulsotype. STEC serotypes O26 and O103 were the most prevalent serogroups in beef and veal, respectively. These findings support related findings from regulatory sampling studies over the past decade and confirm that recovery rates for the regulated STEC serogroups are higher for raw veal than for raw beef samples, as was observed in the present study of meat purchased at food retailers in the mid-Atlantic region of the United States.
The bacterial biota of laboratory-reared edible mealworms (Tenebrio molitor L.): From feed to frass
2018, International Journal of Food Microbiology
Citation Excerpt :
To date, STEC has been isolated in a wide variety of vectors, including insects (Amézquita-Lòpez et al., 2017). As reported by Mir et al. (2015), insects are capable of modulating the occurrence of STEC in the environment. Notwithstanding, there is a paucity of scientific literature on the occurrence of STEC in insects.
Tenebrio molitor represents one of the most popular species used for the large-scale conversion of plant biomass into protein and is characterized by high nutritional value. In the present laboratory study, the bacterial biota characterizing a pilot production chain of fresh T. molitor larvae was investigated. To this end, different batches of fresh mealworm larvae, their feeding substrate (wheatmeal) and frass were analyzed by viable microbial counts, PCR-DGGE and Illumina sequencing. Moreover, the occurrence of Coxiella burnetii, Pseudomonas aeruginosa and Shiga toxin-producing E. coli (STEC) was assessed through qualitative real-time PCR assays. Microbial viable counts highlighted low microbial contamination of the wheatmeal, whereas larvae and frass were characterized by high loads of Enterobacteriaceae, lactic acid bacteria, and several species of mesophilic aerobes. Spore-forming bacteria were detected to a lesser extent in all the samples. The combined molecular approach used to profile the microbiota confirmed the low microbial contamination of wheatmeal and allowed the detection of Enterobacter spp., Erwinia spp., Enterococcus spp. and Lactococcus spp. as dominant genera in both larvae and frass. Moreover, Klebsiella spp., Pantoea spp., and Xenorhabdus spp. were found to be in the minority. Entomoplasmatales (including Spiroplasma spp.) constituted a major fraction of the microbiota of one batch of larvae. From the real-time PCR assays, no sample was positive for either C. burnetii or STEC, whereas P. aeruginosa was detected in one sample of frass. Based on the overall results, two sources of microbial contamination were hypothesized, namely feeding with wheatmeal and vertical transmission of microorganisms from mother to offspring. Since mealworms are expected to be eaten as a whole, the overall outcomes collected in this laboratory study discourage the consumption of fresh mealworm larvae. Moreover, microbial loads and the absence of potential pathogens known to be associated with this insect species should be carefully assessed in order to reduce the minimum risk for consumers, by identifying the most opportune processing methods (e.g., boiling, frying, drying, etc.).
Fate of Escherichia coli O157:H7 and bacterial diversity in corn silage contaminated with the pathogen and treated with chemical or microbial additives
2017, Journal of Dairy Science
Citation Excerpt :
The estimated annual cost associated with EC illnesses can be as high as $405 million (Frenzen et al., 2005). Cattle harbor and shed EC in their manure (Lahti et al., 2003; Mir et al., 2015) and are considered the main reservoirs of the pathogen (Cernicchiaro et al., 2013). Up to 30% of all cattle are asymptomatic carriers of EC (Callaway et al., 2006; Reinstein et al., 2007) and livestock feeds are considered to be the vehicle of transmission among livestock (Hancock et al., 2001; Davis et al., 2003).
Inhibiting the growth of Escherichia coli O157:H7 (EC) in feeds may prevent the transmission or cycling of the pathogen on farms. The first objective of this study was to examine if addition of propionic acid or microbial inoculants would inhibit the growth of EC during ensiling, at silo opening, or after aerobic exposure. The second objective was to examine how additives affected the bacterial community composition in corn silage. Corn forage was harvested at approximately 35% dry matter, chopped to a theoretical length of cut of 10 mm, and ensiled after treatment with one of the following: (1) distilled water (control); (2) 1 × 10⁵ cfu/g of EC (ECCH); (3) EC and 1 × 10⁶ cfu/g of Lactobacillus plantarum (ECLP); (4) EC and 1 × 10⁶ cfu/g of Lactobacillus buchneri (ECLB); and (5) EC and 2.2 g/kg (fresh weight basis) of propionic acid, containing 99.5% of the acid (ECA). Each treatment was ensiled in quadruplicate in laboratory silos for 0, 3, 7, and 120 d and analyzed for EC, pH, and organic acids. Samples from d 0 and 120 were also analyzed for chemical composition. Furthermore, samples from d 120 were analyzed for ammonia N, yeasts and molds, lactic acid bacteria, bacterial community composition, and aerobic stability. The pH of silages from all treatments decreased below 4 within 3 d of ensiling. Escherichia coli O157:H7 counts were below the detection limit in all silages after 7 d of ensiling. Treatment with L. buchneri and propionic acid resulted in fewer yeasts and greater aerobic stability compared with control, ECCH, and ECLP silages. Compared with the control, the diversity analysis revealed a less diverse bacterial community in the ECLP silage and greater abundance of Lactobacillus in the ECLP and ECA silages. The ECLB silage also contained greater abundance of Acinetobacter and Weissella than other silages. Subsamples of silages were reinoculated with 5 × 10⁵ cfu/g of EC either immediately after silo opening or after 168 h of aerobic exposure, and EC were enumerated after 6 or 24 h, respectively. All silages reinoculated with EC immediately after silo opening (120 h) had similar low pH values (<4.0) and EC counts were below the detection limit. The ECCH and ECLP silages reinoculated with EC after 168 h of aerobic exposure had relatively high pH values (>5.0) and EC counts (5.39 and 5.30 log cfu/g, respectively) 24 h later. However, those treated with L. buchneri or propionic acid had lower pH values (4.24 or 3.96, respectively) and lower EC counts (1.32 log cfu/g or none, respectively). During ensiling, EC was eliminated from all silages at pH below 4.0. During aerobic exposure, the growth of EC was reduced or prevented in silages that had been treated with L. buchneri or propionic acid at ensiling, respectively.
National survey of Shiga toxin-producing Escherichia coli serotypes O26, O45, O103, O111, O121, O145, and O157 in Australian beef cattle feces
2016, Journal of Food Protection
Escherichia coli O157 and six non-O157 Shiga toxin–producing E. coli (STEC) serotypes (O26, O45, O103, O111, O121, and O145, colloquially referred to as the “big 6”) have been classified as adulterants of raw nonintact beef products in the United States. While beef cattle are a known reservoir for the prototype STEC serotype, E. coli O157, less is known about the dissemination of non-O157 STEC serotypes in Australian cattle. In the present study, 1,500 fecal samples were collected at slaughter from adult (n =628) and young (n =286) beef cattle, adult (n =128) and young (n =143) dairy cattle, and veal calves (n = 315) across 31 Australian export-registered processing establishments. Fecal samples were enriched and tested for E. coli O157 and the big 6 STEC serotypes using BAX System PCR and immunomagnetic separation methods. Pathogenic STEC (pSTEC; isolates that possess stx, eae, and an O antigen marker for O157 or a big 6 serotype) were isolated from 115 samples (7.7%), of which 100 (6.7%) contained E. coli O157 and 19 (1.3%) contained a big 6 serotype. Four of the 115 samples contained multiple pSTEC serotypes. Among samples confirmed for big 6 pSTEC, 15 (1%) contained E. coli O26 and 4 (0.3%) contained E. coli O111. pSTEC of serotypes O45, O103, O121, and O145 were not isolated from any sample, even though genes indicative of E. coli belonging to these serotypes were detected by PCR. Analysis of animal classes revealed a higher pSTEC prevalence in younger animals, including veal (12.7%), young beef (9.8%), and young dairy (7.0%), than in adult animals, including adult beef (5.1%) and adult dairy (3.9%). This study is the largest of its kind undertaken in Australia. In contrast to E. coli O157 and consistent with previous findings, this study reports a relatively low prevalence of big 6 pSTEC serotypes in Australian cattle populations.
Control of Escherichia coli O157:H7 in contaminated alfalfa silage: Effects of silage additives
2016, Journal of Dairy Science
Citation Excerpt :
Escherichia coli O157:H7 is estimated to cause about 75,000 illness cases and 50 deaths yearly in the United States (Mead et al., 1999). Cattle are considered the primary reservoir of E. coli O157:H7 (Cernicchiaro et al., 2013), and they shed the pathogen in their manure (Lahti et al., 2003; Mir et al., 2015). Animal feeds, such as silage, have been suggested to be the vehicle for transmission of the pathogen among livestock (Hancock et al., 2001; Davis et al., 2003).
This study was conducted to examine if adding microbial inoculants or propionic acid to alfalfa silages contaminated with Escherichia coli O157:H7 would inhibit the growth of the pathogen during or after ensiling. Alfalfa forage was harvested at the early bloom stage, wilted to a dry matter concentration of 54%, chopped to 19-mm lengths, and ensiled after treatment with one of the following: (1) distilled water (control); (2) 1 × 10⁵ cfu/g of E. coli O157:H7 (EC); (3) EC and 1 × 10⁶ cfu/g of Lactobacillus plantarum (EC+LP); (4) EC and 1 × 10⁶ cfu/g of Lactobacillus buchneri (EC+LB); and (5) EC and 2.2 g/kg of propionic acid (EC+PA). Each treatment was ensiled in quadruplicate in laboratory silos for 0, 3, 7, 16, and 100 d and analyzed for EC counts, pH, and organic acids. In addition, samples from d 100 were analyzed for chemical composition, ammonia-N, counts of yeasts and molds, and aerobic stability. Escherichia coli O157:H7 was detected in all silages until d 7, but by d 16 it was not detected in those treated with EC+LB and EC+LP, though it was still detected in EC and EC+PA silages. However, by d 100, the pathogen was not detected in any silage. The rate of pH decrease to 5.0 was fastest for the EC+LP silage (7 d), followed by the EC+LB silage (16 d). Nevertheless, all silages had attained a pH of or less than 5.0 by d 100. The rapid decrease in pH in EC+LP and EC+LB silages was observed due to higher lactate and acetate concentrations, respectively, relative to the other silages during the early fermentation phase (d 3–16). Propionic acid was only detected in the EC+PA silage. Yeast counts were lowest in EC+LB and EC+PA silages. Subsamples of all d-100 silages were reinoculated with 1 × 10⁵ cfu/g of EC immediately after silo opening. When the pathogen was subsequently enumerated after 168 h of aerobic exposure, it was not detected in silages treated with EC+PA, EC+LB, or EC+LP, which all had pH values less than 5.0. Whereas the EC silage had a pH value of 5.4 and 2.3 log cfu/g of the pathogen. Certain bacterial inoculants can hasten the inhibition of E. coli O157:H7 during ensiling, such as propionic acid, and they can also prevent its growth on silage contaminated with the pathogen after ensiling.

View all citing articles on Scopus

View full text

Association between animal age and the prevalence of Shiga toxin-producing Escherichia coli in a cohort of beef cattle

Highlights

Abstract

Introduction

Section snippets

Ethics statement

Animal management and sample collection

Heifers had lower prevalence of STEC compared to older cows

Discussion

Acknowledgements

J. Microbiol. Methods

Vet. Microbiol.

J. Food Prot.

Prevalence and characterization of non-O157 Shiga toxin-producing Escherichia coli on carcasses in commercial beef cattle processing plants

Appl. Environ. Microbiol.

Survival of Escherichia coli O157:H7 on cattle hides

Appl. Environ. Microbiol.

Epidemiological relatedness and clonal types of natural populations of Escherichia coli strains producing Shiga toxins in separate populations of cattle and sheep

Appl. Environ. Microbiol.

Age as a factor influencing diversity of commensal E. coli microflora in pigs

Pol. J. Microbiol.

Non-O157 Shiga toxin-producing Escherichia coli infections in the United States, 1983–2002

J. Infect. Dis.

Prevalence of Shiga toxin-producing Escherichia coli and associated virulence genes in feces of commercial feedlot cattle

Foodborne Pathog. Dis.

Risk factors for the presence of high-level shedders of Escherichia coli O157 on Scottish farms

J. Clin. Microbiol.

Cattle-level risk factors associated with fecal shedding of Shiga toxin-encoding bacteria on dairy farms, Minnesota, USA

Can. J. Vet. Res.

Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP)

BMC Microbiol.

Animal-to-animal variation in fecal microbial diversity among beef cattle

Appl. Environ. Microbiol.

Escherichia coli O157:H7: animal reservoir and sources of human infection

Foodborne Pathog. Dis.

Maternally and naturally acquired antibodies to Shiga toxins in a cohort of calves shedding Shiga-toxigenic Escherichia coli

Appl. Environ. Microbiol.