An Overview of Shiga-Toxin Producing Escherichia coli Carriage and Prevalence in the Ovine Meat Production Chain

Abstract

Shiga-toxin producing Escherichia coli (STEC) are zoonotic foodborne pathogens that are capable of causing serious human illness. Ovine ruminants are recognized as an important source of STEC and a notable contributor to contamination within the food industry. This review examined the prevalence of STEC in the ovine food production chain from farm-to-fork, reporting carriage in sheep herds, during abattoir processing, and in raw and ready-to-eat meats and meat products. Factors affecting the prevalence of STEC, including seasonality and animal age, were also examined. A relative prevalence can be obtained by calculating the mean prevalence observed over multiple surveys, weighted by sample number. A relative mean prevalence was obtained for STEC O157 and all STEC serogroups at multiple points along the ovine production chain by using suitable published surveys. A relative mean prevalence (and range) for STEC O157 was calculated: for feces 4.4% (0.2–28.1%), fleece 7.6% (0.8–12.8%), carcass 2.1% (0.2–9.8%), and raw ovine meat 1.9% (0.2–6.3%). For all STEC independent of serotype, a relative mean prevalence was calculated: for feces 33.3% (0.9–90.0%), carcass 58.7% (2.0–81.6%), and raw ovine meat 15.4% (2.7–35.5%). The prevalence of STEC in ovine fleece was reported in only one earlier survey, which recorded a prevalence of 86.2%. Animal age was reported to affect shedding in many surveys, with younger animals typically reported as having a higher prevalence of the pathogen. The prevalence of STEC decreases significantly along the ovine production chain after the application of postharvest interventions. Ovine products pose a small risk of potential STEC contamination to the food supply chain.

Introduction

Shiga-toxin producing Escherichia coli (STEC) are zoonotic foodborne pathogens that are capable of causing serious human illness. More than 8000 STEC infections were reported in Europe in 2018, with more than 37% of those requiring hospitalization and further medical treatment (EFSA and ECDC, 2019). Bovine ruminants are considered the primary STEC reservoir but small ruminants, in particular ovine ruminants, are now recognized as an important reservoir of STEC and a notable contributor to contamination within the food industry (Mughini-Gras et al., 2018).

This review is focused on the carriage and prevalence of STEC (an E. coli that carries the stx gene) in ovine ruminants, indiscriminate of age, breed, and sex. The prevalence of STEC O157 and non-O157 is discussed. STEC O157 when referenced throughout the text is with respect to serogroup O157 and is inclusive of all flagellar antigens, including E. coli O157:H7. This review aims at examining the prevalence rates of this pathogen from farm-to-fork, reporting carriage in domestic sheep herds, during abattoir processing and in raw and ready-to-eat meats and meat products. The impact of decontamination treatments and other intervention processes was not addressed in this study.

Research papers and reports containing relevant data included in this review are discussed in the text. Some studies have also been organized into tables. Data presented in the tables have been limited to studies that include a minimum of 95 samples, and that clearly and unambiguously report the identification of Shiga-toxin positive samples, with no preference for the detection techniques employed or the sample type. Studies published before the year 2001 have not been included. Studies that involve mixed-species samples, such as sheep and goat, have not been included where possible. Smaller studies of relevance are also discussed in the text. Studies that did not meet the criteria for inclusion are listed in Supplementary Table S1.

An indication of the relative prevalence, and the observed range of prevalence rates, of STEC O157 and non-O157 STEC at different stages of production was calculated by using the surveys presented in each of the tables. A relative mean was obtained by calculating the mean prevalence observed over the selected surveys, weighted by the sample number. Hence, the relative mean can be expressed as:

where $\bar{x_{w}}$ is the weighted mean variable, w_i is the allocated weighted value, and x_i is the observed value. A summary of the relative mean calculations is presented in Supplementary Table S2.

Shiga-toxin producing E. coli

STEC are significant enteric pathogens associated with disease, both sporadically and in outbreaks, resulting in the manifestation of serious diarrheal symptoms and the potential onset of hemorrhagic colitis or hemolytic uremic syndrome (Nataro and Kaper, 1998; Petras, 2011; Trachtman et al., 2012). STEC O157 is the most frequently isolated pathogenic STEC serogroup globally, accounting for 36.6% and 41% of STEC infections in the United States and the European Union, respectively, in 2015 (CDC, 2017; EFSA and ECDC, 2018).

Four additional serogroups (O26, O103, O111, O145) are recognized as important adulterants and are collectively referred to, along with E. coli O157:H7, as the “top five” STEC (EFSA BIOHAZ Panel et al., 2020). However, a recent EFSA Scientific opinion (2020) concluded that based on the current available evidence, serogroup cannot be used as a predictor of clinical outcome and that the presence of the intimin gene (eae) is not essential for severe illness and thus that all STEC strains are pathogenic in humans, capable of causing at least diarrhea, and that all STEC subtypes may be associated with severe illness. Ovine ruminants harbor a diverse range of non-O157 STEC, many of which share virulence features with strains recovered from disease-causing outbreaks (Blanco et al., 2003; Aktan et al., 2004; Djordjevic et al., 2004; Cookson et al., 2006; Kalchayanand et al., 2007).

STEC pathogenic factors

STEC are characterized by the production of one or more Shiga toxin(s) (denoted as Stx) that target the globotriaosylceramide (Gb3) receptor found along human renal endothelial cells and monocytes (O'Brien et al., 1982; Phillips et al., 2000; Obrig, 2010; Schüller, 2011; Piérard et al., 2012). Ruminants lack this receptor, possessing a Gb4 receptor variant instead, and can therefore harbor the pathogen asymptomatically for prolonged periods of time (Gyles, 2007). There are two major families of the Stx toxin (Stx1 and Stx2), which share an estimated 55% amino acid sequence homology (Kaper et al., 2004; Caprioli et al., 2005). They are encoded on mobile lysogenic prophages commonly referred to as stx phages (Krüger and Lucchesi, 2015). Strains may express one or both families of the toxins, and several variants of each are known (Melton-Celsa, 2014; EFSA BIOHAZ Panel et al., 2020). Ruminants may preferentially harbor different stx variants (Mora et al., 2012; Bai et al., 2016; Shridhar et al., 2017). The subtypes stx_2d and stx_1c- are strongly associated with sheep, whereas recent reports have highlighted the increasing prevalence of subtype stx_2O118 in ovine ruminants (Koch et al., 2001; Ramachandran et al., 2001; Brett et al., 2003; Alonso et al., 2016).

The ability to adhere to and successfully colonize the lower gastro-intestinal tract of the host is a critical factor in the successful population and persistence of STEC in ovine ruminants (La Ragione et al., 2009). Invading STEC typically induce the formation of attaching and effacing (A/E) lesions to allow intimate adherence between the bacterium and the host intestinal epithelial cells (Cepeda-Molero et al., 2017). The factors responsible for the formation of A/E lesions are encoded on a pathogenicity island (PAI) called the locus of enterocyte effacement (LEE) (Elliott et al., 1998). The major elements encoded include a Type III secretion system (T3SS), the intimin protein, its receptor Tir, and the Esp proteins (Nataro and Kaper, 1998; Garmendia et al., 2005).

STEC may also harbor other important PAIs, including O-island (OI) 122, OI-43/48, and the high pathogenicity island. These encode many important non-LEE encoded (nle) effector genes as well as alternative virulence factors, including the toxin Sen (sen), adhesion factors (efa1, efa2, iha, aid-A1), and antimicrobial resistance genes (ureC, terC) (Schmidt and Hensel, 2004; Bugarel et al., 2010; Ju et al., 2013; Franz et al., 2015; Karama et al., 2019).

STEC and ovine ruminants

Ovine ruminants are recognized as notable contributors to STEC contamination to the food supply chain. Intrinsic factors such as animal age and sex may make an animal more susceptible to STEC infection, whereas extrinsic factors associated with the farm environment are the leading contributors to the animal becoming infected. It has been demonstrated that STEC can survive for extended periods in animal feces and in the farm environment. STEC may persist in drinking troughs, animal feed, soil, or effluent (Soon et al., 2011). The continued exposure to the pathogen results in the indirect infection or re-infection of ovine ruminants from the environment, whereas direct transmission between animals can also occur via the fecal–oral route (Persad and LeJeune, 2014).

Sheep farming is a global practice. Farmers in the northern and southern hemisphere, while still producing ovine meat and wool all year, follow seasonal production times. Both regions observe their busiest lambing period in the spring with seasonal demand peaking toward Easter and Ramadan, whereas the southern hemisphere also observes a second seasonal peak in the early Autumn (MLA Corporate, 2019). Sheep production in the southern hemisphere tends to be more diverse than what is observed in European production systems, with many famers keeping sheep to produce wool and mutton meat as well as lamb production. Slaughtered animals tend to be older in these regions, with lower weaning rates as a result, when compared with other sheep-producing countries in Europe (Behrendt and Weeks, 2019). Lamb producers in countries such as Spain, Greece, or France may have multiple lambing events per annum, and typically slaughter lambs at a much younger age (<3 months of age) than other regions, with consumers preferring younger, preweaned lamb meat (Campo et al., 2016).

A wide variety of ovine sources have been associated with STEC outbreaks. Many of the reported outbreaks are as a result of poor hygiene after interaction with animals at specified events or petting farms or ingestion of fecally contaminated soil (Licence et al., 2001; Bekal et al., 2014; Gobin et al., 2018). Other outbreaks are associated with consumption of contaminated raw meat products or undercooked meat/ready-to-eat ovine produce (Espié et al., 2006; Sekse et al., 2009; Wahl et al., 2011). The diverse range of infection sources highlights the disease-causing potential of ovine ruminants and the importance of obeying good hygiene standards after animal contact and when preparing food (Rowell et al., 2016).

STEC colonization in ovine hosts

STEC have been shown to demonstrate effective colonization at the terminal end of the rectum, termed the recto-anal junction (RAJ), in cattle (Naylor et al., 2003; Low et al., 2005). However, colonization in ovine hosts has been shown to be less specific compared with bovine animals (La Ragione et al., 2009; Vande Walle et al., 2011). Colonization dynamics between ovine hosts and the bacterium are notoriously difficult to investigate due to the absence of a stable ovine colonization model in artificially inoculated animals (Cookson et al., 2002; Sheng et al., 2004; Best et al., 2009).

STEC colonization is dependent on several factors. The intimin protein is essential for A/E lesion formation and subsequent strain colonization in sheep (Cornick et al., 2000). A/E lesions primarily target intestinal epithelial cells (Cepeda-Molero et al., 2017). Colonizing STEC may also secrete other important adherence factors, including a selection of Esp and Nle proteins (La Ragione et al., 2009; Ojo et al., 2010). The secretion of such proteins is suspected to illicit an immune response in the host, which contributes to the removal of the pathogen from the animal (Sanderson et al., 1999; Yekta et al., 2011). Interestingly, an immune response is only seen after natural or artificial oral infection with STEC, with some suggestions that the bacterium must pass through the small intestine to elicit an antibody reaction (Vande Walle et al., 2011). Colonization in ovine ruminants has also been shown to be positively affected if the invading STEC strain possesses either of the lpf adhesion fimbrieae (Farfan and Torres, 2012).

Tissue tropism has been shown to be an important factor in E. coli O157:H7 pathogenesis and successful colonization in human and bovine studies (Naylor et al., 2003; Sheng et al., 2004). In contrast, STEC colonization studies in small ruminants have identified non-preferential selection of different tissues during colonization. La Ragione et al. (2009) demonstrated that E. coli O157:H7 colonization was specific to the distal intestine in young lambs. Interestingly, this study also demonstrated that E. coli O157:H7 had no specific tropism for lymphoid tissue, something that is commonly observed in bovine hosts (Naylor et al., 2003; Bonardi et al., 2007). Other studies have shown that shedding of E. coli O157:H7 for ≥14 days (persistent shedding) is correlated with colonization throughout the entire gastrointestinal (GI) tract of 6-week-old lambs (Cookson et al., 2002; Woodward et al., 2003). Similar colonization patterns have been observed for STEC O26. A nontoxigenic E. coli O26:K60 strain was orally inoculated in young lambs and found to colonize the whole GI tract during high excretion. However, after day 38, A/E lesions could only be recovered from the distal small intestine (Aktan et al., 2007).

To date, no clear evidence has been presented, which would indicate that STEC has a preferred site of colonization in ovine hosts. Instead, it is capable of colonization along the entire GI tract, including the RAJ, but to a lesser degree than that observed in cattle (La Ragione et al., 2009; McPherson et al., 2015).

Super-shedding ruminants

Ovine ruminants are important contributors to the dissemination of STEC among the herd, environment, and, subsequently, in slaughtering facilities (Persad and LeJeune, 2014). It has been demonstrated that bovine ruminants can transiently shed STEC between 10¹ colony-forming unit (CFU)/mL and 10⁹ CFU/mL, a characteristic termed intermittent shedding (Fukushima et al., 1999; Chase-Topping et al., 2008; Menrath et al., 2010; McCabe et al., 2019).

Some animals may shed higher numbers of STEC for prolonged periods, in a phenomenon known as “super-shedding,” and these have been shown to pose the greatest risk of contamination to the agri-food chain (Chase-Topping et al., 2008; Karmali, 2017). A super-shedder has many different definitions that are time and study specific (Matthews et al., 2006b; Chase-Topping et al., 2008). However, it is generally accepted that a super-shedding ruminant is any animal that sheds greater than 10⁴ CFU/g feces (Matthews et al., 2006a, 2006b; Munns et al., 2015; McCabe et al., 2019). Ruminants colonized in the RAJ display a higher propensity for super-shedding when compared with non-colonized animals (Lim et al., 2007; Chase-Topping et al., 2008; Persad and LeJeune, 2014). Both E. coli O157 and non-O157 STEC serogroups have been isolated from super-shedding ruminants (Menrath et al., 2010; Paquette et al., 2018; McCabe et al., 2019).

Factors Impacting STEC Carriage in the Host

Age

Several studies investigating STEC shedding in cattle and sheep have reported that as animals age, especially after weaning, the prevalence of STEC decreases (Chapman et al., 1997; Fagan et al., 1999; Menrath et al., 2010; Mir et al., 2016). This has been attributed to the changing composition of the gut microflora as the animal matures (Mir et al., 2016). A year-long study of sheep in the United States found that younger sheep (22.7%) on a feedlot had a significantly higher fecal prevalence of STEC than older animals (0–1.9%) at pasture (Kilonzo et al., 2011). A long-term study of Australian sheep identified newborn lambs (55.2%) as the highest shedders of STEC, and ewes (32.3%) and weaned lambs (25.8%) as the lowest shedders (Djordjevic et al., 2004). A study carried out at a later date in New Zealand also found that the prevalence of STEC in lambs (3.8%) presented at slaughter was much greater than that reported for ewes (0.9%) at pasture (Moriarty et al., 2011).

Other reports have suggested that the impact of an animal's age on STEC prevalence is unclear (Heuvelink et al., 1998; Evans et al., 2011; Mir et al., 2015; EFSA and ECDC, 2018). One Scottish study reported a significantly higher prevalence of the “ top five” STEC serogroups among slaughtered sheep (10%) than lambs (3%), but did not clarify whether adult sheep had a higher overall STEC prevalence than lambs for all stx-positive E. coli serogroups (Evans et al., 2011). An earlier study in Spain also reported a greater prevalence of STEC in ewes (33.1%) than lambs (13.8%) (Orden et al., 2003). However, this study defined lambs as animals younger than 4 weeks of age. Most other studies classify lambs as animals up to 8 and a half months old, which likely influences the reported prevalence rates (Kudva et al., 1997).

Changes in housing arrangements, differences in rearing practices between surveys, and changes to the animals' diet as it matures could account for a large portion of the observed affect (Gunn et al., 2007). Regular contact with other ruminants and wildlife may also increase the risk of herd shedding or increase the likelihood of a herd becoming infected (Venegas-Vargas et al., 2016; Ahlstrom et al., 2017).

Diet

The animals' diet has been shown to influence STEC colonization and subsequent shedding in both bovine and ovine carriers (Kudva et al., 1997; Diez-Gonzalez et al., 1998; Hovde et al., 1999; Cornick et al., 2000; Chaucheyras-Durand et al., 2010; Mir et al., 2016). Food intake and the fiber content of the fodder provided can exert an impact on the bacterial populations of the gut (Grau et al., 1969; Kudva et al., 1995; Chaucheyras-Durand et al., 2010, 2012). Concentrate diets have been shown to correlate with a higher concentration of STEC shedding in lambs and sheep (Kudva et al., 1995; Lema et al., 2001; Gutta et al., 2009). A longitudinal survey investigating STEC prevalence in lambs fed on concentrates or reared at pasture reported a prevalence range of between 15.6% and 40.6% (Djordjevic et al., 2004). This variation can largely be attributed to the pasture-based diets with significant differences observed between lambs finished at grass (15.6%) and on concentrated feed (40.6%).

Seasonality

There is evidence to suggest that seasonal effects are likely to influence prevalence rates, with several surveys observing seasonal peaks in STEC shedding (Franco et al., 2009; Fraser et al., 2013; Kamel et al., 2015). The observed changes are likely due to the associated changes in temperature.

Higher ambient temperatures, as opposed to increased solar exposure, have been linked with elevated STEC shedding rates (Sheng et al., 2004; Milnes et al., 2008; Tahmasby et al., 2014; Williams et al., 2015). Investigations in bovine hosts have suggested that enhanced transmission rates at elevated temperatures are also influenced by the increased activity of flies, animals drinking more water, and hormonal and behavioral changes in the host (Berry and Wells, 2010; Dawson et al., 2018). Kilonzo et al. (2011) reported that STEC is 3.2 times more likely to be isolated during the higher summertime temperatures, despite not recording any significant differences in shedding between seasons. Higher summertime temperatures have been associated with increased STEC isolation rates in sheep in Great Britain, Egypt, Italy, and the United States (Ogden et al., 2002; Franco et al., 2009; Fraser et al., 2013; Kamel et al., 2015). In addition, Evans et al. (2011) observed clear seasonal differences between the shedding of STEC O157 and O26 in Scottish sheep and failed to detect any STEC O157 isolates between January and March during their study.

Prevalence and Carriage of STEC in Ovine Feces

Ovine fecal samples can be collected in different ways. Live animal feces have been collected from pasture, sheds, or lairage floors. Alternatively, the rectum of the animal may be swabbed. Slaughtered animals may also be swabbed at the rectum pre-evisceration, or samples from the colon, rectum, or ileum may be collected post-evisceration. Fecal contents can also be collected from the lower GI tract after evisceration. Selected surveys on the prevalence of STEC in ovine feces are presented in Table 1 and have been arranged in order of sample type.

Table 1.

Selected^a Surveys on the Prevalence of Shiga-Toxin Producing Escherichia coli in Ovine Feces

Country	Year	Source	Sampling point	Serotyping/flagellar antigen	Virulence genotype	n^b	%^c	Detection method	Notes	References
Greece	2008	Fecal pats	Farm	O157	stx, eaeA	361 361	1.9 8.3	Selective agar, latex agglutination, ELISA, PCR, amplicon sequencing	Sheep and lambs, feces collected from pen floors	Pinaka et al. (2013)
New Zealand	2006–2007	Fecal pats	Abattoir	STEC	stx. eaeA, hlyA	220	0.9	Selective agar, IMS, PCR	Flock of sheep in Otago >12 months	Moriarty et al. (2011)
United Kingdom	2003	Fecal pats	Farm	O157	stx, eaeA	676	6.5	Selective agar, latex agglutination, IMS, PCR	Pasture-raised sheep	Ogden et al. (2005)
United Kingdom	2005	Fecal pats	Farm	O157	stx, eaeA	390	5.8	Selective agar, IMS, PCR, latex agglutination, VCA, MLVA	Samples collected from 14 flocks fed on a specific diet	Solecki et al. (2009)
Australia	2014–2016	Feces	Farm	O157:H7	stx, eaeA, ehlyA	115	20.0	Selective plating, probe hybridization, PCR	Dairy sheep	Oporto et al. (2019)
				Non-O157		115	46.1
Australia	—	Mutton feces	Farm	STEC	stx, eaeA	904	73.3	PCR, O antisera	Slaughter-age animals	Djordjevic et al. (2001)
		Lamb feces				719	59.2
Australia	—	Ewe feces	Farm	STEC	stx, eaeA, ehxA	130	32.3	PCR, O antisera	Longitudinal study, ewes sampled once, lambs sampled three times	Djordjevic et al. (2004)
		Lambs <6 weeks				125	55.2
		Preweaning lambs				123	43.9
		Postweaning lambs				97	25.8
		Lamb feces (sampling 2)				285	38.6		A dietary study, lambs sampled four times. Included is sampling 2, 3 and 4.
		Lamb feces (sampling 3)				288	40.6
		Lamb feces (sampling 4)				122	15.6
Brazil	2010	Feces	Farm	O103:H2	stx, eaeA, ehxA	130	0.8	Selective agar, VCA, PCR	STEC isolated from 4-week-old lamb	Martins et al. (2014)
Brazil	—	Feces	Farmhouse	STEC	stx1, stx2, ipaH, ehxA, aaiC, aatA, eae, bfpA, aggR, elt, est, aap, aggR, AA probe	100	6.0	PCR, O antisera	Samples collected from farmhouse housing sheep	Furlan et al. (2019)
China	2015	Feces	Farm	STEC	stx	130	0.8	Latex agglutination, PCR		Chunchun et al. (2017)
Egypt	—	Feces	Farm and wandering flocks	O157:H7	stx, eaeA, hlyA	150	7.3	Selective agar, latex agglutination, PCR	Sheep from three farms and from wandering flocks around Giza were sampled	Kamel et al. (2015)
Italy	2002	Feces	Abattoir	O157	stx, eaeA	643	0.2	Selective agar, latex agglutination, IMS, VCA, PCR	Weaned and suckling lambs	Battisti et al. (2006)
Italy	2005–2006	Feces	Abattoir	O157	stx, eaeA, hlyA	533	7.1	Selective agar, latex agglutination, IMS, PCR	Slaughter-age sheep	Franco et al. (2009)
India	—	Lamb feces	Farm	STEC	stx, eaeA, ehxA, saa	107	10.3	O antisera, PCR	Diarrhegic lambs from high-altitude flocks	Bandyopadhyay et al. (2011)
Ireland	2005–2006	Feces	Abattoir	O157:H7	stx, eaeA, hlyA, katP, espA, espB	400	0.0	Selective agar, IMS, PCR	Positive isolates recovered from fleece and carcass samples	Lenahan et al. (2007)
Jordan	2006	Feces	Abattoir and butchers' premises	STEC	stx, eaeA, ehlyA	233	6.0	Selective agar, IMViC test, PCR, slide agglutination assay	Samples recovered from small farms at five sampling sites	Tarawneh et al. (2009)
Norway	2006–2007	Feces	Farm	O103	stx, eaeA, bfpA, astA	585	0.7	Selective agar, latex agglutination, AIMS-ELISA, O antisera, PCR	Sheep and lambs	Sekse et al. (2013)
Saudi Arabia	2012	Feces	Abattoir	O157:H7	stx, eaeA, fliC-H7	208	2.4	Selective agar, latex agglutination, IMS, PCR	50 samples from the youngest animals in each sampled flock	Bosilevac et al. (2015)
Spain	2003	Sheep feces	Farm	STEC	stx, eaeA, ehxA	576	6.8	Selective agar, VCA, HeLa cell assay, IMS, PCR, O antisera	Longitudinal study carried out over 1 year. 12 ewes from four unrelated flocks were sampled monthly for the duration of the study	Sánchez et al. (2009)
Spain	2003–2005	Feces	Farm	O157:H7	stx, eaeA, hlyA	112	8.7	Selective agar, VIDAS, IMS, PCR	Lambs ≤2 months	Oporto et al. (2008)
				Non-O157		112	50.8
Sweden	2007–2009	Feces	Abattoir	O157:H7	stx, eaeA, ehxA	492	1.8	Selective agar, latex agglutination, IMS, PCR	Diarrhegic lambs	Söderlund et al. (2012)
Switzerland	2004–2005	Feces	Abattoir	O157	stx, eaeA, ehxA, astA, paa, bfpA, EAF plasmid	630	1.1	IMS, PCR, biochemical confirmation	Slaughter-age animals, seasonal sampling	Zweifel et al. (2006)
United Arab Emirates	2017–2018	10 g feces from RAJ	Abattoir	O157:H7	rfbE, fliC-H7, uidA, hlyA, stx	141	0.0	Selective agar, latex agglutination, IMS, PCR		Al-Ajmi et al. (2020)
United Kingdom	1997–2007	Feces	Open farms	O157	stx, phage type	427	28.1	IMS, selective agar, latex agglutination, PCR	Faces collected from rectum, environment, or animal enclosure	Pritchard et al. (2009)
United Kingdom	2005–2008	Feces, small intestine, large intestine, intestinal mucosa, liver	Clinical laboratory	STEC	stx, eaeA	131	12.8	Indole test, cytochrome oxidase test, latex agglutination, PCR	Samples were collected from the VLA regional laboratories across the United Kingdom from animals displaying symptoms of suspected or confirmed E. coli infection	Hutchinson et al. (2011)
Qatar	—	Feces	Abattoir	O157:H7	stx, eaeA	142	23.0	Selective agar, BAX system PCR		Mohammed et al. (2015)
				Non-O157		142	90.0
Brazil	2009	Fecal swabs	Abattoir	STEC	stx, eaeA, aidA, F17, F18, cnf, sfa, papC, iucD, paa, astA, afa, tsh	101	7.9	Colony hybridisation, latex agglutination, PCR	Feces collected from three farms and one abattoir	Maluta et al. (2014)
			Farm			202	13.4
Brazil	2010	Rectal swab	Farm	STEC	stx, eaeA, ehxA, saa, iha, lpfO113, subAB, cdtV	130	50.0	PCR, O antisera	10 farms were visited, lambs and sheep sampled over 6 months	Martins et al. (2015)
Greece	—	RAMS	Farm	O157:H7	stx, eaeA, phage typing	171	0.0	Selective agar, slide agglutination, PCR	Samples collected from different breeding farms in northern Greece	Dontorou et al. (2004)
Iran	2009–2010	Rectal swab samples	Abattoir	O157	stx, eaeA	153	4.6	Selective agar, latex agglutination, PCR	Sheep presented for slaughter at slaughterhouses in Fars province Iran	Tahamtan and Namavari (2014)
				Non-O157		153	29.1
Iran	2010–2011	Sheep RAJ swabs	Farm	STEC	stx, eaeA	192	13.0	Selective plating, PCR, latex agglutination	Fat tailed adult sheep from eight flocks	Ghanbarpour and Kiani (2013)
Ireland	2008–2009	Rectal swab	Abattoir	O157	stx, eaeA	103	5.8	Selective agar, latex agglutination, IMS, PCR	Samples collected from seven primary ovine abattoirs	Prendergast et al. (2011)
New Zealand	2006–2007	Lamb RAJ swabs	Abattoir	STEC	stx. eaeA, hlyA	105	3.8	Selective agar, IMS, PCR	Lambs <12 months	Moriarty et al. (2011)
New Zealand	—	Recto-anal swabs	Farm	STEC	stx, eaeA, ehxA	132	65.9	Selective agar, PCR, O antisera	Lambs 3 months old, ewes and rams	Cookson et al. (2006)
Norway	2002–2003	Fecal swabs	Farm	O157:H7	stx, eaeA	117	17.0	Selective agar, AIMS, PCR, VCA, ELISA	Longitudinal study investigating the persistence of O157 at farm level. Ewes sampled four times over 1 year	Wasteson et al. (2005)
Spain	2000–2001	Lamb fecal swabs	Farms	O157:H7	stx, eaeA, ehxA	697	1.0	Selective agar, VCA, HeLa cell assay, IMS, PCR, O antisera	Lambs ≤2 months	Rey et al. (2003)
				Non-O157		697	35.0	Selective agar, VCA, HeLa cell assay, IMS, PCR, O antisera
Turkey	2012–2013	Rectal swabs	Abattoir	O157:H7	stx, eaeA, fliC-H7	100	2.0	Selective agar, latex agglutination, IMS, PCR		Gencay (2014)
Australia	2006–2007	10 g feces from last 60 cm of rectum	Abattoir	O157	stx, eaeA, ehxA	163	5.0	AIMS, PCR	Two abattoirs, five groups of sheep	Duffy et al. (2010)
Ethiopia	2007–2008	Feces from distal colon	Abattoir	O157:H7	stx, eaeA	112	5.4	Selective agar, agglutination, IMS, PCR	Slaughter-age animals	Mersha et al. (2010)
Switzerland	2002	Cecum	Abattoir	Non-O157	stx1, stx2c, stx2d, eaeA, ehxA, astA	653	10.8	Selective agar, PCR	Slaughter-age animals	Zweifel et al. (2004)
United Kingdom	2003	Feces from distal colon	Abattoir	O157	stx, eaeA	2825	0.7	Selective agar, latex agglutination, VCA, IMS, PCR	Slaughter-age animals	Milnes et al. (2008)
United Kingdom	2005–2006	Sheep rectum	Abattoir	O157	stx	1082	2.9	Selective agar, latex agglutination, IMS, PCR	Slaughter-age animals, recovered a high number of serogroup positive E. coli O103	Evans et al. (2011)
				O26		1082	0.9
United States	2002–2003	Feces	Agricultural fair	O157:H7	stx	251	4.4	Selective agar, latex agglutination, IMS, PCR	Sheep and lambs	Keen et al. (2006)

Surveys were selected based on specific criteria; see the Introduction section for details.

Number of samples examined.

Percentage of samples recorded as positive.

AIMS, automated IMS; ELISA, enzyme linked immunoassay; IMS, immunomagnetic separation; IMViC, indole, methyl red, Voges Proskauer and citrate; MLVA, Multi Locus VNTR Analysis; PCR, polymerase chain reaction; RAJ, recto-anal junction; RAMS, recto-anal mucosal swabs; STEC, Shiga-toxin producing E. coli; VCA, vero cell assay; VLA, Veterinary Laboratories Agency.

From the results presented in Table 1, the fecal prevalence of both STEC O157 and non-O157 STEC varies considerably between surveys. The relative prevalence of STEC O157 is 4.4% and ranges from 0.2% to 28.1%, while the relative prevalence of STEC is 33.3% and ranges from 0.9% to 90.0%. The wide range of reported prevalence rates may be influenced by several factors, including study design, the number of samples collected, and the isolation techniques employed. However, it is more likely that a large portion of the variation is due to intrinsic factors associated with the animal, such as their age, sex, and immune status, as well as extrinsic factors such as the season, diet, and climate (Dewell et al., 2005).

Sample type may also be an important factor when estimating STEC prevalence. Some of the lowest prevalence rates reported for both E. coli O157 and non-O157 STEC were observed in surveys conducted in Brazil, Scotland, New Zealand, and Greece. Each of those surveys collected matter from fecal pats or pellets excreted by lambs or sheep in farmhouses, at pasture, or in abattoirs. The STEC have been shown to have a heterogenous distribution in excreted fecal matter collected from pats in bovine enclosures, and there is a risk of underestimating the true STEC prevalence (Pearce et al., 2004; Robinson et al., 2005). In addition, the increased exposure to the environment after excretion may result in some bacterial decay.

Similar investigations have not yet been carried out in ovine ruminants, but it is an important point to consider when assessing the reduced prevalence observed in these studies. In comparison, studies in both ovine and bovine hosts investigating STEC O157 prevalence have shown that fecal samples (collected via fecal palpitation) and recto-anal mucosal swabs are most suitable for the detection of STEC (Rice et al., 2003; McPherson et al., 2015).

Some of the observed variance could also be due to the wide array of STEC detection and characterization techniques employed among the presented surveys. Molecular techniques such as polymerase chain reaction (PCR) may be at risk of potentially overestimating the true prevalence of STEC due to its inability to differentiate live and dead cells, resulting in DNA amplification from dead STEC cells, and interference from background flora present in the sample (Macori et al., 2020). Other methods, such as immunomagnetic separation (IMS), agglutination techniques, and selective agars, may underestimate certain serogroups or atypical strains due to their high degree of specificity and reliance on the expression of typical STEC phenotypes (Noll et al., 2015; Hallewell et al., 2017). In addition, many surveys employ an enrichment step during the STEC detection protocol. The temperature at which this is carried out may be preferential to certain serogroups and mask the presence of others (Wang et al., 2013; Conrad et al., 2016). In general, it is important to employ a multi-hurdle approach during the detection and culture of an STEC isolate to ensure all typical and atypical strains present in a sample are accounted for. The highest rates of STEC carriage have been observed in ovine herds located in the southern hemisphere.

Several surveys have investigated the prevalence of STEC in Australian sheep and lambs and have observed STEC carriage to be higher than the relative mean reported for STEC (33.3%), and it ranges from 15.6% to 73.3% (Djordjevic et al., 2001, 2004; Yang et al., 2017; Oporto et al., 2019). Interestingly, high prevalence rates were observed across all ovine herds and animals tested, regardless of animal age, diet, or sample type. High STEC prevalence rates have also been observed in herds in Brazil and New Zealand from fecal samples collected on farm (Cookson et al., 2006; Martins et al., 2015). The higher prevalence rates may be influenced by the higher ambient temperatures generally observed in these regions in comparison to other sheep-producing regions in the northern hemisphere (Fleury et al., 2006; Carlton et al., 2016; Philipsborn et al., 2016).

The lowest rates of STEC O157 and non-O157 STEC carriage have generally been observed in European herds. Herds sampled in Great Britain reported an STEC O157 prevalence of between 0.7% and 28.1%. Many of the surveys reported STEC O157 carriage to be below the relative mean of 4.4%, with the exception of one long-term study that recorded an STEC O157 prevalence of 28.1% in ovine feces collected on open farms in England and Wales (Pritchard et al., 2009). Studies involving Spanish herds recorded the highest rates of STEC carriage among ovine herds in Europe. It is likely that the higher prevalence rates can in part be attributed to the age of the lambs when slaughtered. Lambs younger than 3 months of age, often preweaned and milk fed, account for many of the slaughtered lambs in Spain (Campo et al., 2016). In other regions of Europe lambs are much older, often between 6 and 8 months old, before they are sent for slaughter.

A small number of surveys have also investigated the prevalence of a selected number of serogroups among sheep and lambs. The prevalence of the “top five” serogroups (O157, O26, O103, O145, O111) in the surveyed herds is generally lower than the relative mean observed for STEC O157 (4.4%). Overall, there are a limited number of surveys investigating the prevalence of non-O157 STEC serogroups, and only a small number of the wider STEC prevalence surveys have proceeded to serotype the isolated STEC colonies.

STEC Prevalence in Ovine Abattoirs

STEC and ovine fleece contamination

The fleece is a major source of STEC and microbial contamination within slaughtering facilities, and carcass de-pelting has been identified as a critical control point (CCP) for carcass contamination (EFSA Panel on Biological Hazards (BIOHAZ), 2013). Fleeces can also be interchangeably referred to as the pelt or hide. They primarily become soiled along the abdomen, rump, and in the area surrounding the hind legs (Lenahan et al., 2007; Hauge et al., 2011; Thomas et al., 2013). A wide variety of materials may contaminate the fleece, including mud, dust, sand, feces, and soil. Contamination may occur on farm, in sheds, or at pasture, during transport, or when the animal is held in lairage (Hauge et al., 2011). Table 2 presents selected surveys describing the prevalence of STEC on ovine fleeces.

Table 2.

Selected^a Surveys on the Reported Prevalence of Shiga-Toxin Producing Escherichia coli on Ovine Pelts, Fleece, or Hides

Country	Year	Source	Area sampled	Serogroup/flagellar antigen	Virulence genotypes	n^b	%^c	Detection method	Notes	References
Australia	2006–2007	Fleece	25 cm² at flank, brisket and mid-loin	O157	stx, eaeA, ehxA	164	3.0	AIMS, PCR	Two abattoirs, five groups of sheep	Duffy et al. (2010)
Ethiopia	2007–2008	Skin with fleece		O157:H7	stx, eaeA	112	8.0	Selective agar, latex agglutination, IMS, PCR	Slaughter-age animals	Mersha et al. (2010)
Ireland	2005–2006	Fleece	Skin sample with fleece attached from 100 cm² area near neck	O157:H7	stx, eaeA, katP, hlyA, etpD, espA, espB, espP, espF, fliC-H7, TIR	400	5.8	Selective agar, IMS, PCR	Five export abattoirs	Lenahan et al. (2007)
Ireland	2008–2009	Fleece	∼10 g fleece from rump	O157O26	stx	500500	0.81.0	Selective agar, latex agglutination, IMS, PCR	Failed to recover any STEC O111, O103 and O145	Thomas et al. (2013)
Saudi Arabia	2012	Hide	∼10 g fleece from rump	O157:H7	stx, eaeA, fliC-H7	207	9.2	Selective agar, latex agglutination, IMS, PCR	Municipal abattoir processing sheep, goats, cattle, and camels	Bosilevac et al. (2015)
United States	2005	Pelt	1000 cm² area over fourth rib1000 cm² area over fourth rib	O157:H7Non-O157	stx, eaeA	851846	12.886.2	Selective agar, latex agglutination, IMS, ProSpect assay	Three abattoirs in the United States	Kalchayanand et al. (2007)

Surveys were selected based on specific criteria; see the Introduction section for details.

Number of samples examined.

Percentage of samples recorded as positive.

AIMS, automated IMS; IMS, immunomagnetic separation; PCR, polymerase chain reaction; STEC, Shiga-toxin producing E. coli.

From the surveys presented in Table 2, the relative prevalence of STEC O157 on the ovine fleece ranged from 0.8% to 12.8% and had a relative mean of 7.6%. It is interesting to note that the relative prevalence of STEC O157 was much higher on the fleece than what was reported for fecal samples and declines considerably after de-pelting. This can in part be attributed to the fact that the fleece is easily soiled and fecal matter may build up over time. A similar trend was observed in a wide-ranging review of pathogens along the bovine production chain (Rhoades et al., 2009).

Only one study investigating STEC carriage on ovine fleeces was suitable for inclusion in this review and reported a non-O157 STEC prevalence of 86.2% from a sample size of 846 sheep (Kalchayanand et al., 2007). One Irish survey report on the prevalence of the “top five” serogroups on the fleece of Irish sheep noted a much lower STEC prevalence of 1.8% (Thomas et al., 2013).

STEC contamination on ovine carcasses

Carcass dressing immediately follows fleece removal or de-pelting. First, the gut contents are discarded during the evisceration process (EFSA Panel on Biological Hazards (BIOHAZ), 2013; FAO, 2018). Evisceration is a major CCP for the transfer of bacteria from the intestines to the carcass, with various reports citing an increase in bacteria, including E. coli, being transferred to the carcass surface at this point (Alonso et al., 2007; Sheridan, 2007; Milios et al., 2011). The carcass may then be subjected to numerous interventions, which differ depending on the legislation employed in each specific region, before it is chilled, boned, and processed into retail cuts (EFSA Panel on Biological Hazards (BIOHAZ), 2016). Selected surveys on the prevalence of STEC on de-pelted ovine carcasses and meat samples collected from abattoirs are presented in Table 3.

Table 3.

Selected^a Surveys on the Prevalence of Shiga-Toxin Producing Escherichia coli on Ovine Carcasses at Different Stages of Abattoir Processing

Country	Year	Source	Processing stage	Serotype/flagellar antigen	Virulence genotypes	n^b	%^c	Detection method	Notes	References
Algeria	2015	Wet and dry swab of 4 × 100 cm² area of the thigh, flank, large breast, and posterior aspect of the forelegs	—	O26	stx, eaeA	363	1.4	Selective agar, latex agglutination, PCR, API 20E		Ferhat et al. (2019)
Algeria	2015		—	Non-O157	stx, eaeA	363	3.9	Selective agar, latex agglutination, PCR, API 20E		Ferhat et al. (2019)
Australia	2004	25 cm² area from mid-loin, flank, and brisket on both sides of the carcass	Postchill	O157:H7	stx	1117	0.6	IMS, PCR		Phillips et al. (2006)
Australia	2011	900 cm² from leg	Postchill	O157:H7	stx, eaeA, hlyA	613	0.3	IMS, PCR	Abattoirs from five Australian states included	Phillips et al. (2013)
Australia	2011	900 cm² from shoulder	Postchill	O157:H7	stx, eaeA, hlyA	613	0.2	IMS, PCR	Abattoirs from five Australian states included	Phillips et al. (2013)
Australia	2006–2007	5 × 5 cm² area from flank, mid-loin, and brisket	Prechill	O157	stx, eaeA, ehxA	159	0.6	AIMS, PCR		Duffy et al. (2010)
Brazil	2009	25 cm² from rump, flank, and brisket	N. A	STEC	stx, eaeA, aidA, cnf, sfa, papC, iucD, paa, f17, f18	99	2.0	Colony hybridization, latex agglutination, PCR		Maluta et al. (2014)
Ethiopia	2007–2008	6 × 50 cm² from left side of the carcass	Prewash	O157:H7	stx, eaeA	112	9.8	Selective agar, latex agglutination, IMS, PCR		Mersha et al. (2010)
Ethiopia	2007–2008	6 × 50 cm² from left side of the carcass	Postwash	O157:H7	stx, eaeA	112	8.9	Selective agar, latex agglutination, IMS, PCR		Mersha et al. (2010)
Iran	2005	3 × 25 cm² area from neck, shoulder, and abdomen	Postevisceration	O157:H7	stx	152	3.9	Selective agar, latex agglutination, O antisera, PCR	114 lamb, 38 sheep >2 years old	Shekarforoush et al. (2008)
Iran	2005–2006	Swab of sheep carcass surface	N. A	O157:H7	stx, eaeA	200	4.0	Selective agar, latex agglutination, PCR	120 lamb, 80 ewes	Tahamtan et al. (2010)
Iran	2005–2006	Swab of sheep carcass surface	N. A	Non-O157	stx, eaeA	200	5.5	Selective agar, latex agglutination, PCR	120 lamb, 80 ewes	Tahamtan et al. (2010)
Ireland	2008–2009	Full external carcass swab	Postevisceration	O157	stx, eaeA, hlyA	500	5.5	Selective agar, latex agglutination, IMS, PCR	Failed to recover any STEC O111 and O145	Thomas et al. (2013)
				O26		500	0.6
				O103		500	0.4
Ireland	2008–2009	4 × 100 cm² area from flank, lateral thorax, brisket, and breast	Postevisceration	O157	stx, eaeA	103	2.9	Selective agar, latex agglutination, IMS, PCR	Samples collected from the seven major ovine abattoirs	Prendergast et al. (2011)
Ireland	2005–2006	Full external carcass swab	Postevisceration	O157:H7	stx, eaeA, hlyA, katP, espA, espB	400	1.5	Selective agar, IMS, PCR		Lenahan et al. (2007)
Ireland	2005–2006	Full external carcass swab	Postchill	O157:H7	stx, eaeA, hlyA, katP, espA, espB	400	1.0	Selective agar, IMS, PCR		Lenahan et al. (2007)
Turkey	2012–2013	3 × 100 cm² area from flank, brisket, and breast on both sides of the carcass, ventral tail	Postevisceration	O157/O157:H7	stx, eaeA, hlyA, lpfA1	100	8.0	Selective agar, latex agglutination, IMS, PCR		Gencay (2014)
Qatar	—	Swabbed area, including the breast, lateral thorax, brisket, flank, and rump on both sides of the carcass	N. A	O157:H7	stx, eaeA	300	2.0	Selective agar, BAX system PCR		Mohammed et al. (2015)
United States	2005	4000 cm² area of inside and outside leg, breast-foreshank	Pre-evisceration	O157:H7	stx, eaeA, hlyA, fliC-H7	851	1.5	Selective agar, latex agglutination, IMS, PCR		Kalchayanand et al. (2007)
			Pre-evisceration	Non-O157		846	78.6
			Post-treatment	O157:H7		851	2.9
			Post-treatment	Non-O157		846	81.6

Surveys were selected based on specific criteria; see the Introduction section for details.

Number of samples examined.

Percentage of samples recorded as positive.

AIMS, automated IMS; IMS, immunomagnetic separation; N. A, not available; PCR, polymerase chain reaction.

The prevalence of E. coli O157 and non-O157 STEC declines after abattoir processing and the application of suitable interventions. A relative mean prevalence of 2.1% and a range of 0.2% to 9.8% is reported for STEC O157 on ovine carcasses from the studies shown in Table 3. The relative mean prevalence for all STEC on ovine carcasses was 58.7% and ranged from 2.0% to 81.6%.

From the surveys presented in Table 3, the reported prevalence rates were affected in some instances after the application of intervention processes to reduce or arrest the growth and proliferation of STEC and other microbes on the carcass surface. The STEC prevalence rates were largely unchanged after carcass chilling. A small reduction in STEC O157 prevalence was observed in a survey of Ethiopian ovine carcasses after carcass washing (Mersha et al., 2010). Evisceration of the carcass resulted in a marginal increase in both STEC O157 and non-O157 STEC on ovine carcasses sampled during a large survey of lamb carcasses in three American abattoirs, despite the application of antimicrobial interventions (Kalchayanand et al., 2007). However, this study also reported a reduction between 2 and 2.5 log CFU/100 cm² in indictor bacteria and Salmonella after the application of intervention processes and carcass chilling. The reduced interference from background flora likely leads to easier STEC isolation, particularly as the study used molecular methods such as PCR and IMS, and is an important point to consider when analyzing STEC prevalence at different processing stages.

STEC contamination in raw ovine meat

Raw meat products are defined as raw meat mixes composed of muscle meat and sometimes animal fat. The products have not been cured or processed but may occasionally contain nonmeat products, such as flavourings or fruits (FAO, 2018). These products may include trimmings, offal, and butcher cuts such as steaks, mince, and chops (Rhoades et al., 2009). Contamination of raw meat products generally occurs due to carcass contamination and the subsequent dissemination of the pathogen from the kill line to the boning hall. Selected surveys on the prevalence of STEC in raw, unprocessed ovine meat products are presented in Table 4.

Table 4.

Selected^a Surveys on the Prevalence of Shiga-Toxin Producing Escherichia coli in Raw Unprocessed Ovine Meat Products

Country	Year	Source	Sampling point	Region	Serogroup/flagellar antigen	Virulence genotype	n^b	%^c	Detection method	Notes	Literature
Australia	2004	Frozen sheep meat	Abattoir	Five mainland Australian states	O157:H7	stx	560	0.2	IMS, PCR	Frozen meat collected from 20 abattoirs, stored <1 month	Phillips et al. (2006)
China	2013–2014	Retail raw mutton	Supermarkets and farmers markets	Zigong and Beijing	STEC	stx, eaeA, ehxA	126	19.0	Selective agar, O antisera, PCR	Raw, unpacked meat	Bai et al. (2015)
Iran	2010–2011	25 g meat sample from leg, neck, and flank	Farm butchers	Chaharmahal-va-Bakhtiari	STEC	stx2_c	270	2.7	Selective agar, PCR		Tahmasby et al. (2014)
Iran	2012	Lamb carcass	Farm butchers	Four geographically distinct regions in Iran	STEC	stx, eaeA, iha, saa, hlyA, espP, toxB	220	35.5	PCR	10 g meat sample taken from carcass	Momtaz et al. (2013)
					O157O26O103O45O111O113O121O91O128O145		220220220220220220220220220200	6.33.21.84.11.81.40.51.40.90.9
India	2007–2009	Mutton	Abattoir and local abattoir shops		STEC		160	6.3	PCR, biochemical tests, O antisera	Also tested for serogroups O26, O111, O121, O45, O145 and O103 but failed to recover any isolates	Kumar et al. (2014)

Surveys were selected based on specific criteria; see the Introduction section for details.

Number of samples examined.

Percentage of samples recorded as positive.

IMS, immunomagnetic separation; PCR, polymerase chain reaction; STEC, Shiga-toxin producing E. coli.

From the surveys presented in Table 4, STEC O157 had a relative mean prevalence of 1.9% and ranged from 0.2% to 6.3% in raw ovine meat. A relative mean prevalence of 15.4% and a range between 2.7% and 35.5% was reported for STEC. It is interesting to note that the prevalence of STEC O157 on raw ovine products is similar to that observed for ovine carcasses (2.1%), whereas the observed STEC prevalence is much lower. The weighted mean prevalence observed for STEC O157 is likely an inflated rate and may be influenced by the low number of surveys available for inclusion, as well as the variable hygiene standards in the sampled premises. However, the low prevalence rates are indicative of how effective application of postharvest intervention processes in slaughtering facilities has been in stopping the spread of the pathogen to raw meat products and subsequently to the food supply chain.

Overall, the lowest STEC prevalence rates were observed in raw ovine meat and meat products. No significant differences were observed in STEC prevalence between lamb or mutton meat or meat mixes. However, as was the case for the observed fecal prevalence, some of the highest prevalence rates for STEC were observed in the southern hemisphere. One survey in Australia reported an STEC prevalence of 40.0% on lamb cutlets collected from butchers' premises, whereas a later study recorded a prevalence of 55.6% in raw mutton collected from supermarkets and farmers markets in China (Barlow et al., 2006; Bai et al., 2016). Other surveys have reported much lower prevalence rates (2.7–22.3%) for lamb and mutton meat sampled in India and Iran (Momtaz et al., 2013; Kumar et al., 2014; Tahmasby et al., 2014). The detection techniques employed by each research group may influence isolation rates, as molecular techniques may over-estimate the true STEC prevalence. In addition, the sample type may also influence the observed prevalence, with some areas of the carcass being more susceptible to potential STEC contamination than others.

Discussion

It is clear from these data that the prevalence of both STEC O157 and non-O157 STEC generally decreases along the ovine production chain. The highest rates of carriage are observed on the ovine fleece, with the prevalence decreasing on the carcass and in raw ovine meat, after carcass dressing and abattoir processing. However, as previously discussed, the small number of surveys that have investigated STEC prevalence in the ovine fleece, carcass, and raw meat means that these figures should be interpreted with caution.

In general, there is a lack of information regarding the prevalence of STEC among ovine ruminants, as most studies have only investigated the carriage of STEC O157. This is particularly concerning, as it is widely accepted that ovine animals host a broad range of non-O157 STEC. To compound this, many of the studies have employed qualitative methodologies, and though useful, have added little to the understanding of the shedding patterns of ovine ruminants, particularly the “super-shedding” dynamics within ovine herds.

Super-shedding ruminants have been demonstrated to excrete high numbers of STEC and have a higher risk of disseminating the pathogen among the herd and within slaughtering facilities. Studies investigating the shedding of STEC O157 in cattle reported that 8% and 9% of the respective herds were classified as super-shedding individuals, but were responsible for 96% and 99% of the total bacteria shed (Omisakin et al., 2003; Chase-Topping et al., 2007). A quantitative study of a Scottish sheep flock identified some individual animals shedding up to 10⁶ CFU g⁻¹ (Ogden et al., 2005). It is likely that STEC exhibits discrete super-shedding dynamics in ovine ruminants, which are anticipated to be distinct from what is observed in other prominent ruminant hosts. Additional investigations on the quantitative shedding of STEC in ovine ruminants and the risk they may pose to the food supply chain are, therefore, required.

There is a noticeable lack of information regarding the prevalence of STEC within the boning hall and in raw processed ovine meat products, with only five surveys suitable for inclusion in this review. A smaller survey conducted in the Dunedin region of New Zealand reported an STEC prevalence of 17.1% from 37 sampled lamb and mutton meat products from butchers and supermarkets premises (Brooks et al., 2001). An Indian study also reported a high STEC prevalence of 40.0% from 50 mutton meat samples (Kiranmayi, 2010). A number of disease cases have also been linked to the consumption of contaminated ovine produce (Espié et al., 2006; Sekse et al., 2013; Bekal et al., 2014; Wilson et al., 2018). In addition, while compiling this review, only a handful of studies could be found that investigated the prevalence of STEC among ovine ready-to-eat products. These reports were not included in calculations for this review due to the small number of samples tested.

Conclusion

Ovine ruminants are a significant STEC reservoir, and further investigations into the colonization and shedding patterns of STEC within this ruminant population are required to improve our understanding on the shedding dynamics of the pathogen in ovine hosts. Despite the relatively high fecal carriage rate of STEC in ovine ruminants, the prevalence of this pathogen declines significantly along the ovine production chain after the application of suitable postharvest interventions and proper carcass dressing. The small number of surveys investigating the prevalence of STEC in raw ovine products is concerning. However, the low prevalence rates reported in raw meat produce are reassuring as to the potential risk of contamination these products may pose to the food supply chain.

Footnotes

Acknowledgment

The authors thank Paula Reid for assisting with the statistical analysis of the data.

Disclosure Statement

No competing financial interests exist.

Funding Information

This project was funded by the Food Institutional Research Measure, administered by the Department of Agriculture, Food and the Marine, Ireland (Grant Number 15/F/629).

Supplementary Material

Supplementary Table S1

Supplementary Table S2

References

Abdul-Raouf

, Ammar

, Beuchat

. Isolation of Escherichia coli O157:H7 from some Egyptian foods. Int J Food Microbiol, 1996; 29:423–426.

Abreham

, Teklu

, Cox

, Sisay Tessema

. Escherichia coli O157:H7: Distribution, molecular characterization, antimicrobial resistance patterns and source of contamination of sheep and goat carcasses at an export abattoir, Mojdo, Ethiopia. BMC Microbiol, 2019; 19:215.

Ahlstrom

, Muellner

, Lammers

, Jones

, Octavia

, Lan

, Heller

. Shiga toxin-producing Escherichia coli O157 shedding dynamics in an Australian beef herd. Front Vet Sci, 2017; 4:200.

Akanbi

, Mbah

, Kerry

. Prevalence of Escherichia coli O157:H7 on hides and faeces of ruminants at slaughter in two major abattoirs in Nigeria. Lett Appl Microbiol, 2011; 53:336–340.

Aktan

, La Ragione

, Woodward

. Colonization, persistence, and tissue tropism of Escherichia coli O26 in conventionally reared weaned lambs. Appl Environ Microbiol, 2007; 73:691–698.

Aktan

, Sprigings

, La Ragione

, Faulkner

, Paiba

, Woodward

. Characterisation of attaching-effacing Escherichia coli isolated from animals at slaughter in England and Wales. Vet Microbiol, 2004; 102:43–53.

Akyol

Development and application of RTi-PCR method for common food pathogen presence and quantity in beef, sheep and chicken meat. Meat Sci, 2018; 137:9–15.

Al-Ajmi

, Rahman

, Banu

. Occurrence, virulence genes, and antimicrobial profiles of Escherichia coli O157 isolated from ruminants slaughtered in Al Ain, United Arab Emirates. BMC Microbiol, 2020; 20:210.

Alonso

, Krüger

, Sanz

, Padola

, Lucchesi

PMA

. Serotypes, virulence profiles and stx subtypes of Shiga toxigenic Escherichia coli isolated from chicken derived products. Rev Argent Microbiol, 2016; 48:325–328.

10.

Alonso

, Mora

, Blanco

, Dahbi

, Ferreiro

, López

, Alberghini

, Albonetti

, Echeita

, Trevisani

, Blanco

. Fecal carriage of Escherichia coli O157:H7 and carcass contamination in cattle at slaughter in northern Italy. Int Microbiol, 2007; 10:109–116.

11.

Amézquita-López

, Quiñones

, Cooley

, León-Félix

, Castro-del Campo

, Mandrell

, Jiménez

, Chaidez

. Genotypic analyses of Shiga toxin-producing Escherichia coli O157 and non-O157 recovered from feces of domestic animals on rural farms in Mexico. PLoS One, 2012; 7:e51565.

12.

Bai

, Hu

, Xu

, Sun

, Zhao

, Ba

, Fu

, Fan

, Jin

, Wang

, Guo

, Xu

, Lu

, Xiong

. Molecular and phylogenetic characterization of non-O157 Shiga toxin-producing Escherichia coli strains in China. Front Cell Infect Microbiol, 2016; 6:143.

13.

Bai

, Wang

, Xin

, Wei

, Tang

, Zhao

, Sun

, Zhang

, Wang

, Xu

, Zhang

, Li

, Xu

, Xiong

. Prevalence and characteristics of Shiga toxin-producing Escherichia coli isolated from retail raw meats in China. Int J Food Microbiol, 2015; 200:31–38.

14.

Bandyopadhyay

, Mahanti

, Samanta

, Dutta

, Ghosh

, Bera

, Bandyopadhyay

, Bhattacharya

. Virulence repertoire of Shiga toxin-producing Escherichia coli (STEC) and enterotoxigenic Escherichia coli (ETEC) from diarrhoeic lambs of Arunachal Pradesh, India. Trop Anim Health Prod, 2011; 43:705–710.

15.

Barlow

, Gobius

, Desmarchelier

. Shiga toxin-producing Escherichia coli in ground beef and lamb cuts: Results of a one-year study. Int J Food Microbiol, 2006; 111:1–5.

16.

Battisti

, Lovari

, Franco

, Di Egidio

, Tozzoli

, Caprioli

, Morabito

. Prevalence of Escherichia coli O157 in lambs at slaughter in Rome, central Italy. Epidemiol Infect, 2006; 134:415–419.

17.

Behrendt

, Weeks

. How Are Global and Australian Sheepmeat Producers Performing? Meat and Livestock Australia Limited, North Sydney, NSW: 2019.

18.

Bekal

, Ramsay

, Rallu

, Pilon

, Gilmour

, Johnson

, Tremblay

. First documented case of human infection with ovine Shiga-toxin-producing Escherichia coli serotype O52:H45. Can J Microbiol, 2014; 60:417–418.

19.

Berry

, Wells

. Chapter 4—Escherichia coli O157:H7: Recent advances in research on occurrence, transmission, and control in cattle and the production environment. In: Advances in Food and Nutrition Research, Volume 60. Taylor SL (ed.). Burlington, MA: Academic Press, 2010, pp. 67–117.

20.

Best

, Clifford

, Crudgington

, Cooley

, Nunez

, Carter

, Weyer

, Woodward

, La Ragione

. Intermittent Escherichia coli O157:H7 colonisation at the terminal rectum mucosa of conventionally-reared lambs. Vet Res, 2009; 40:9.

21.

Blanco

, Blanco

, Mora

, Rey

, Alonso

, Hermoso

, Alonso

, Dahbi

, González

, Bernárdez

, Blanco

. Serotypes, virulence genes, and intimin types of Shiga toxin (verotoxin)-producing Escherichia coli isolates from healthy sheep in Spain. J Clin Microbiol, 2003; 41:1351–1356.

22.

Bonardi

, Foni

, Chiapponi

, Salsi

, Brindani

. Detection of verocytotoxin-producing Escherichia coli serogroups 0157 and 026 in the cecal content and lymphatic tissue of cattle at slaughter in Italy. J Food Prot, 2007; 70:1493–1497.

23.

Bosilevac

, Gassem

, Al Sheddy

, Almaiman

, Al-Mohizea

, Alowaimer

, Koohmaraie

. Prevalence of Escherichia coli O157:H7 and Salmonella in camels, cattle, goats, and sheep harvested for meat in Riyadh. J Food Prot, 2015; 78:89–96.

24.

Brett

, Ramachandran

, Hornitzky

, Bettelheim

, Walker

, Djordjevic

. stx1c is the most common Shiga toxin 1 subtype among Shiga toxin-producing Escherichia coli isolates from sheep but not among isolates from cattle. J Clin Microbiol, 2003; 41:926–936.

25.

Brooks

HJL

, Mollison

, Bettelheim

, Matejka

, Paterson

, Ward

. Occurrence and virulence factors of non-O157 Shiga toxin-producing Escherichia coli in retail meat in Dunedin, New Zealand. Lett Appl Microbiol, 2001; 32:118–122.

26.

Bugarel

, Beutin

, Fach

. Low-density macroarray targeting non-locus of enterocyte effacement effectors (nle genes) and major virulence factors of Shiga toxin-producing Escherichia coli (STEC): A new approach for molecular risk assessment of STEC isolates. Appl Environ Microbiol, 2010; 76:203–211.

27.

Campo

, Mur

, Fugita

, Sañudo

. Current strategies in lamb production in Mediterranean areas. Anim Front, 2016; 6:31–36.

28.

Caprioli

, Morabito

, Brugère

, Oswald

. Enterohaemorrhagic Escherichia coli: Emerging issues on virulence and modes of transmission. Vet Res, 2005; 36:289–311.

29.

Carlton

, Woster

, DeWitt

, Goldstein

, Levy

. A systematic review and meta-analysis of ambient temperature and diarrhoeal diseases. Int J Epidemiol, 2016; 45:117–130.

30.

CDC. Foodborne Diseases Active Surveillance Network (FoodNet): FoodNet 2015 Surveillance Report (Final Data). Atlanta, GA: U. S. Department of Health and Human Services, CDC, 2017.

31.

Cepeda-Molero

, Berger

, Walsham

ADS

, Ellis

, Wemyss-Holden

, Schüller

, Frankel

, Fernández

LÁ

. Attaching and effacing (A/E) lesion formation by enteropathogenic E. coli on human intestinal mucosa is dependent on non-LEE effectors. PLoS Pathog, 2017; 13:e1006706.

32.

Chapman

, Cerdán Malo

, Ellin

, Ashton

, Harkin

. Escherichia coli O157 in cattle and sheep at slaughter, on beef and lamb carcasses and in raw beef and lamb products in South Yorkshire, UK. Int J Food Microbiol, 2001; 64:139–150.

33.

Chapman

, Siddons

, Gerdan Malo

, Harkin

. A 1-year study of Escherichia coli O157 in cattle, sheep, pigs and poultry. Epidemiol Infect, 1997; 119:245–250.

34.

Chapman

, Siddons

, Malo

ATC

, Harkin

. A one year study of Escherichia coli O157 in raw beef and lamb products. Epidemiol Infect, 2000; 124:207–213.

35.

Chase-Topping

, Gally

, Low

, Matthews

, Woolhouse

. Super-shedding and the link between human infection and livestock carriage of Escherichia coli O157. Nat Rev Microbiol, 2008; 6:904–912.

36.

Chase-Topping

, McKendrick

, Pearce

, MacDonald

, Matthews

, Halliday

, Allison

, Fenlon

, Low

, Gunn

, Woolhouse

MEJ

. Risk factors for the presence of high-level shedders of Escherichia coli O157 on Scottish farms. J Clin Microbiol, 2007; 45:1594–1603.

37.

Chaucheyras-Durand

, Chevaux

, Martin

, Forano

Use of yeast probiotics in ruminants: Effects and mechanisms of action on rumen pH, fibre degradation, and microbiota according to the diet. Probiotic Anim 2012:119–152.

38.

Chaucheyras-Durand

, Faqir

, Ameilbonne

, Rozand

, Martin

. Fates of acid-resistant and non-acid-resistant Shiga toxin-producing Escherichia coli strains in ruminant digestive contents in the absence and presence of probiotics. Appl Environ Microbiol, 2010; 76:640–647.

39.

Chunchun

, Bin

, Zhenwang

, Zengqiang

, Ming

, Baoli

, Zhenqiang

. Serotype identification and antibiotic susceptibility of Shiga toxin-producing Escherichia coli in the Weishan area in Shandong Province, China. Chin J Prev Med, 2017; 51:70–75.

40.

Coia

, Johnston

, Steers

, Hanson

. A survey of the prevalence of Escherichia coli O157 in raw meats, raw cow's milk and raw-milk cheeses in south-east Scotland. Int J Food Microbiol, 2001; 66:63–69.

41.

Conrad

, Stanford

, McAllister

, Thomas

, Reuter

. Competition during enrichment of pathogenic Escherichia coli may result in culture bias. FACETS, 2016; 1:114–126.

42.

Cookson

, Taylor

SCS

, Attwood

. The prevalence of Shiga toxin-producing Escherichia coli in cattle and sheep in the lower North Island, New Zealand. N Z Vet J, 2006; 54:28–33.

43.

Cookson

, Wales

, Roe

, Hayes

, Pearson

, Woodward

. Variation in the persistence of Escherichia coli O157:H7 in experimentally inoculated 6-week-old conventional lambs. J Med Microbiol, 2002; 51:1032–1040.

44.

Cornick

, Booher

, Casey

, Moon

. Persistent colonization of sheep by Escherichia coli O157:H7 and other E. coli pathotypes. Appl Environ Microbiol, 2000; 66:4926–4934.

45.

Dawson

, Keung

, Napoles

, Vella

, Chen

, Sanderson

, Lanzas

. Investigating behavioral drivers of seasonal Shiga-Toxigenic Escherichia coli (STEC) patterns in grazing cattle using an agent-based model. PLoS One, 2018; 13:e0205418.

46.

Dewell

, Ransom

, Dewell

, McCurdy

, Gardner

, Hill

, Sofos

, Belk

, Smith

, Salman

. Prevalence of and risk factors for Escherichia coli O157 in market-ready beef cattle from 12 U.S. feedlots. Foodborne Pathog Dis, 2005; 2:70–76.

47.

Diez-Gonzalez

, Callaway

, Kizoulis

, Russell

. Grain feeding and the dissemination of acid-resistant Escherichia coli from cattle. Science, 1998; 281:1666–1668.

48.

Djordjevic

, Hornitzky

, Bailey

, Gill

, Vanselow

, Walker

, Bettelheim

. Virulence properties and serotypes of Shiga toxin-producing Escherichia coli from healthy Australian slaughter-age sheep. J Clin Microbiol, 2001; 39:2017–2021.

49.

Djordjevic

, Ramachandran

, Bettelheim

, Vanselow

, Holst

, Bailey

, Hornitzky

. Serotypes and virulence gene profiles of Shiga toxin-producing Escherichia coli strains isolated from feces of pasture-fed and lot-fed sheep. Appl Environ Microbiol, 2004; 70:3910–3917.

50.

Dontorou

, Papadopoulou

, Filioussis

, Apostolou

, Economou

, Kansouzidou

, Levidiotou

. Isolation of a rare Escherichia coli O157:H7 strain from farm animals in Greece. Comp Immunol Microbiol Infect Dis, 2004; 27:201–207.

51.

Duffy

, Small

, Fegan

. Concentration and prevalence of Escherichia coli O157 and Salmonella serotypes in sheep during slaughter at two Australian abattoirs. Aust Vet J, 2010; 88:399–404.

52.

[EFSA and ECDC] European Food Safety Authority and European Centre for Disease Prevention and Control. The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J, 2018; 16:e05500.

53.

EFSA and ECDC. The European Union One Health 2018 Zoonoses Report. EFSA J, 2019; 17:e05926.

54.

EFSA BIOHAZ Panel, Koutsoumanis

, Allende

, Alvarez-Ordóñez

, Bover-Cid

, Chemaly

, Davies

, De Cesare

, Herman

, Hilbert

, Lindqvist

, Nauta

, Peixe

, Ru

, Simmons

, Skandamis

, Suffredini

, Jenkins

, Monteiro Pires

, Morabito

, Niskanen

, Flemming

, Da Silva Felício

, Messans

, Bolton

. Pathogenicity assessment of Shiga toxin-producing Escherichia coli (STEC) and the public health risk posed by contamination of food with STEC. EFSA J, 2020; 18:e05967.

55.

EFSA Panel on Biological Hazards (BIOHAZ). Scientific Opinion on the public health hazards to be covered by inspection of meat from sheep and goats. EFSA J, 2013; 11:3265.

56.

EFSA Panel on Biological Hazards (BIOHAZ). Growth of spoilage bacteria during storage and transport of meat. EFSA J, 2016; 14:e04523.

57.

Elliott

, Wainwright

, McDaniel

, Jarvis

, Deng

, Lai

L-C

, McNamara

, Donnenberg

, Kaper

. The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol Microbiol, 1998; 28:1–4.

58.

Espié

, Grimont

, Vaillant

, Montet

, Carle

, Bavai

, de Valk

, Vernozy-Rozand

. O148 Shiga toxin-producing Escherichia coli outbreak: Microbiological investigation as a useful complement to epidemiological investigation. Clin Microbiol Infect, 2006; 12:992–998.

59.

Evans

, Knight

, Mckendrick

, Stevenson

, Barbudo

, Gunn

, Low

. Prevalence of Escherichia coli O157: H7 and serogroups O26, O103, O111 and O145 in sheep presented for slaughter in Scotland. J Med Microbiol, 2011; 60:653–660.

60.

Fagan

, Hornitzky

, Bettelheim

, Djordjevic

. Detection of Shiga-like toxin (stx1 and stx2), intimin (eaeA), and enterohemorrhagic Escherichia coli (EHEC) hemolysin (EHEC hlyA) genes in animal feces by multiplex PCR. Appl Environ Microbiol, 1999; 65:868–872.

61.

FAO. Guidelines for Slaughtering, Meat Cutting and Further Processing. Rome, Italy: FAO, 2018.

62.

Farfan

, Torres

. Molecular mechanisms that mediate colonization of Shiga toxin-producing Escherichia coli strains. Infect Immun, 2012; 80:903–913.

63.

Ferhat

, Chahed

, Hamrouche

, Korichi-Ouar

, Hamdi

T-M

. Research and molecular characteristic of Shiga toxin-producing Escherichia coli isolated from sheep carcasses. Lett Appl Microbiol, 2019; 68:546–552.

64.

Fleury

, Charron

, Holt

, Allen

, Maarouf

. A time series analysis of the relationship of ambient temperature and common bacterial enteric infections in two Canadian provinces. Int J Biometeorol, 2006; 50:385–391.

65.

Franco

, Lovari

, Cordaro

, Matteo

, Sorbara

, Iurescia

, Donati

, Buccella

, Battisti

. Prevalence and concentration of verotoxigenic Escherichia coli O157:H7 in adult sheep at slaughter from Italy. Zoonoses Public Health, 2009; 56:215–220.

66.

Franz

, van Hoek

AHAM

, Wuite

, van der Wal

, de Boer

, Bouw

, Aarts

HJM

. Molecular hazard identification of non-O157 Shiga toxin-producing Escherichia coli (STEC). PLoS One, 2015; 10:e0120353.

67.

Fraser

, MacRae

, Ogden

, Forbes

, Strachan

NJC

. Effects of seasonality and a diet of brassicas on the shedding of Escherichia coli O157 in sheep. Foodborne Pathog Dis, 2013; 10:649–654.

68.

Fukushima

, Hoshina

, Gomyoda

. Long-term survival of Shiga toxin-producing Escherichia coli O26, O111, and O157 in bovine feces. Appl Environ Microbiol, 1999; 65:5177–5181.

69.

Furlan

JPR

, Gallo

IFL

, de Campos

ACLP

, Passaglia

, Falcão

, Navarro

, Nakazato

, Stehling

. Molecular characterization of multidrug-resistant Shiga toxin-producing Escherichia coli harboring antimicrobial resistance genes obtained from a farmhouse. Pathog Glob Health, 2019; 113:268–274.

70.

Garmendia

, Frankel

, Crepin

. Enteropathogenic and enterohemorrhagic Escherichia coli infections: Translocation, translocation, translocation. Infect Immun, 2005; 73:2573–2585.

71.

Gencay

YE.

Sheep as an important source of E. coli O157/O157:H7 in Turkey. Vet Microbiol, 2014; 172:590–595.

72.

Ghanbarpour

, Kiani

. Characterization of non-O157 Shiga toxin-producing Escherichia coli isolates from healthy fat-tailed sheep in southeastern of Iran. Trop Anim Health Prod, 2013; 45:641–648.

73.

Gobin

, Hawker

, Cleary

, Inns

, Gardiner

, Mikhail

, McCormick

, Elson

, Ready

, Dallman

, Roddick

, Hall

, Willis

, Crook

, Godbole

, Tubin-Delic

, Oliver

. National outbreak of Shiga toxin-producing Escherichia coli O157:H7 linked to mixed salad leaves, United Kingdom, 2016. Euro Surveill, 2018; 23:17-00197.

74.

Grau

, Brownlie

, Smith

. Effects of food intake on numbers of Salmonellae and Escherichia coli in rumen and faeces of sheep. J Appl Bacteriol, 1969; 32:112–117.

75.

Gunn

, McKendrick

, Ternent

, Thomson-Carter

, Foster

, Synge

. An investigation of factors associated with the prevalence of verocytotoxin producing Escherichia coli O157 shedding in Scottish beef cattle. Vet J Lond Engl 1997, 2007; 174:554–564.

76.

Gutta

, Kannan

, Lee

, Kouakou

, Getz

. Influences of short-term pre-slaughter dietary manipulation in sheep and goats on pH and microbial loads of gastrointestinal tract. Small Rumin Res, 2009; 81:21–28.

77.

Gyles

CL.

Shiga toxin-producing Escherichia coli: An overview. J Anim Sci, 2007; 85:E45–E62.

78.

Hallewell

, Alexander

, Reuter

, Stanford

. Limitations of immunomagnetic separation for detection of the top seven serogroups of Shiga toxin–producing Escherichia coli . J Food Prot, 2017; 80:598–603.

79.

Hanlon

, Miller

, Guillen

, Echeverry

, Dormedy

, Cemo

, Branham

, Sanders

, Brashears

. Presence of Salmonella and Escherichia coli O157 on the hide, and presence of Salmonella, Escherichia coli O157 and Campylobacter in feces from small-ruminant (goat and lamb) samples collected in the United States, Bahamas and Mexico. Meat Sci, 2018; 135:1–5.

80.

Hauge

, Nafstad

, Skjerve

, Røtterud

O-J

, Nesbakken

. Effects of shearing and fleece cleanliness on microbiological contamination of lamb carcasses. Int J Food Microbiol, 2011; 150:178–183.

81.

Heuvelink

, van den Biggelaar

, de Boer

, Herbes

, Melchers

, Huis in't Veld

, Monnens

. Isolation and characterization of verocytotoxin-producing Escherichia coli O157 strains from Dutch cattle and sheep. J Clin Microbiol, 1998; 36:878–882.

82.

Heuvelink

, Zwartkruis-Nahuis

JTM

, Beumer

, de Boer

. Occurrence and survival of verocytotoxin-producing Escherichia coli O157 in meats obtained from retail outlets in the Netherlands. J Food Prot, 1999; 62:1115–1122.

83.

Hiko

, Asrat

, Zewde

. Occurrence of Escherichia coli O157:H7 in retail raw meat products in Ethiopia. J Infect Dev Ctries, 2008; 2:389–393.

84.

Hovde

, Austin

, Cloud

, Williams

, Hunt

. Effect of cattle diet on Escherichia coli O157:H7 acid resistance. Appl Environ Microbiol, 1999; 65:3233–3235.

85.

Hutchinson

, Cheney

TEA

, Smith

, Lynch

, Pritchard

. Verocytotoxin-producing and attaching and effacing activity of Escherichia coli isolated from diseased farm livestock. Vet Rec, 2011; 168:536–536.

86.

Johnsen

, Wasteson

, Heir

, Berget

, Herikstad

. Escherichia coli O157:H7 in faeces from cattle, sheep and pigs in the southwest part of Norway during 1998 and 1999. Int J Food Microbiol, 2001; 65:193–200.

87.

, Shen

, Toro

, Zhao

, Meng

. Distribution of pathogenicity islands OI-122, OI-43/48, and OI-57 and a high-pathogenicity island in shiga toxin-producing Escherichia coli . Appl Environ Microbiol, 2013; 79:3406–3412.

88.

Kagambèga

, Martikainen

, Lienemann

, Siitonen

, Traoré

, Barro

, Haukka

. Diarrheagenic Escherichia coli detected by 16-plex PCR in raw meat and beef intestines sold at local markets in Ouagadougou, Burkina Faso. Int J Food Microbiol, 2012; 153:154–158.

89.

Kalchayanand

, Arthur

, Bosilevac

, Brichta-Harhay

, Guerini

, Shackelford

, Wheeler

, Koohmaraie

. Microbiological characterization of lamb carcasses at commercial processing plants in the United States. J Food Prot, 2007; 70:1811–1819.

90.

Kamel

, Abo El-Hassan

, El-Sayed

. Epidemiological studies on Escherichia coli O157:H7 in Egyptian sheep. Trop Anim Health Prod, 2015; 47:1161–1167.

91.

Kaper

, Nataro

, Mobley

. Pathogenic Escherichia coli . Nat Rev Microbiol, 2004; 2:123–140.

92.

Karama

, Mainga

, Cenci-Goga

, Malahlela

, El-Ashram

, Kalake

. Molecular profiling and antimicrobial resistance of Shiga toxin-producing Escherichia coli O26, O45, O103, O121, O145 and O157 isolates from cattle on cow-calf operations in South Africa. Sci Rep, 2019; 9:1–15.

93.

Karmali

MA.

Emerging public health challenges of Shiga toxin-producing Escherichia coli related to changes in the pathogen, the population, and the environment. Clin Infect Dis, 2017; 64:371–376.

94.

Keen

, Wittum

, Dunn

, Bono

, Durso

. Shiga-toxigenic Escherichia coli O157 in agricultural fair livestock, United States. Emerg Infect Dis, 2006; 12:780–786.

95.

Kilonzo

, Atwill

, Mandrell

, Garrick

, Villanueva

, Hoar

. Prevalence and molecular characterization of Escherichia coli O157:H7 by multiple-locus variable-number tandem repeat analysis and pulsed-field gel electrophoresis in three sheep farming operations in California. J Food Prot, 2011; 74:1413–1421.

96.

Kiranmayi

Detection of Escherichia coli O157:H7 prevalence in foods of animal origin by cultural methods and PCR technique. Vet World, 2010; 3:13–16.

97.

Koch

, Hertwig

, Lurz

, Appel

, Beutin

. Isolation of a lysogenic bacteriophage carrying the stx1_OX3 gene, which is closely associated with Shiga toxin-producing Escherichia coli strains from sheep and humans. J Clin Microbiol, 2001; 39:3992–3998.

98.

Krüger

, Lucchesi

PMA

. Shiga toxins and stx phages: Highly diverse entities. Microbiol Read Engl, 2015; 161:451–462.

99.

Kudva

, Hatfield

, Hovde

. Characterization of Escherichia coli O157:H7 and other Shiga toxin-producing E. coli serotypes isolated from sheep. J Clin Microbiol, 1997; 35:892–899.

100.

Kudva

, Hatfield

, Hovde

. Effect of diet on the shedding of Escherichia coli O157:H7 in a sheep model. Appl Environ Microbiol, 1995; 61:1363–1370.

101.

Kumar

, Taneja

, Sharma

. An epidemiological and environmental study of Shiga toxin-producing Escherichia coli in India. Foodborne Pathog Dis, 2014; 11:439–446.

102.

La Ragione

, Best

, Woodward

, Wales

. Escherichia coli O157:H7 colonization in small domestic ruminants. FEMS Microbiol Rev, 2009; 33:394–410.

103.

Lema

, Williams

, Rao

. Reduction of fecal shedding of enterohemorrhagic Escherichia coli O157:H7 in lambs by feeding microbial feed supplement. Small Rumin Res J Int Goat Assoc, 2001; 39:31–39.

104.

Lenahan

, O'Brien

, Kinsella

, Sweeney

, Sheridan

. Prevalence and molecular characterization of Escherichia coli O157:H7 on Irish lamb carcasses, fleece and in faeces samples. J Appl Microbiol, 2007; 103:2401–2409.

105.

Licence

, Oates

, Synge

, Reid

. An outbreak of E. coli O157 infection with evidence of spread from animals to man through contamination of a private water supply. Epidemiol Infect, 2001; 126:135–138.

106.

Lim

, Li

, Sheng

, Besser

, Potter

, Hovde

. Escherichia coli O157:H7 colonization at the rectoanal junction of long-duration culture-positive cattle. Appl Environ Microbiol, 2007; 73:1380–1382.

107.

Little

, Gillespie

, de Louvois

, Mitchell

. Microbiological investigation of halal butchery products and butchers' premises. Commun Dis Public Health, 1999; 2:114–118.

108.

Low

, McKendrick

, McKechnie

, Fenlon

, Naylor

, Currie

, Smith

DGE

, Allison

, Gally

. Rectal carriage of enterohemorrhagic Escherichia coli O157 in slaughtered cattle. Appl Environ Microbiol, 2005; 71:93–97.

109.

Macori

, McCarthy

, Burgess

, Fanning

, Duffy

. Investigation of the causes of shigatoxigenic Escherichia coli PCR positive and culture negative samples. Microorganisms, 2020; 8:587.

110.

Madzingira

Shiga toxin-producing E. coli isolated from sheep in Namibia. J Infect Dev Ctries, 2016; 10:400–403.

111.

Maluta

, Fairbrother

, Stella

, Rigobelo

, Martinez

, de Ávila

. Potentially pathogenic Escherichia coli in healthy, pasture-raised sheep on farms and at the abattoir in Brazil. Vet Microbiol, 2014; 169:89–95.

112.

Martins

, Guth

BEC

, Piazza

, Leão

, Ludovico

, Dahbi

, Marzoa

, Mora

, Blanco

, Pelayo

. Diversity of Shiga toxin-producing Escherichia coli in sheep flocks of Paraná State, southern Brazil. Vet Microbiol, 2015; 175:150–156.

113.

Martins

, Guth

BEC

, Piazza

RMF

, Blanco

, Pelayo

. First description of a Shiga toxin-producing Escherichia coli O103:H2 strain isolated from sheep in Brazil. J Infect Dev Ctries, 2014; 8:126–128.

114.

Matthews

, Low

, Gally

, Pearce

, Mellor

, Heesterbeek

JAP

, Chase-Topping

, Naylor

, Shaw

, Reid

SWJ

, Gunn

, Woolhouse

MEJ

. Heterogeneous shedding of Escherichia coli O157 in cattle and its implications for control. Proc Natl Acad Sci U S A, 2006a;103:547–552.

115.

Matthews

, McKendrick

, Ternent

, Gunn

, Synge

, Woolhouse

MEJ

. Super-shedding cattle and the transmission dynamics of Escherichia coli O157. Epidemiol Infect, 2006b;134:131–142.

116.

McCabe

, Burgess

, Lawal

, Whyte

, Duffy

. An investigation of shedding and super-shedding of Shiga toxigenic Escherichia coli O157 and E. coli O26 in cattle presented for slaughter in the Republic of Ireland. Zoonoses Public Health, 2019; 66:83–91.

117.

McCluskey

, Rice

, Hancock

, Hovde

, Besser

, Gray

, Johnson

. Prevalence of Escherichia coli O157 and other Shiga-toxin-producing E. coli in lambs at slaughter. J Vet Diagn Investig, 1999; 11:563–565.

118.

McPherson

, Dhungyel

, Ward

. Comparison of recto-anal mucosal swab and faecal culture for the detection of Escherichia coli O157 and identification of super-shedding in a mob of Merino sheep. Epidemiol Infect, 2015; 143:2733–2742.

119.

Melton-Celsa

AR.

Shiga toxin (Stx) classification, structure, and function. Microbiol Spectr, 2014; 2:EHEC-0024-2013.

120.

Menrath

, Wieler

, Heidemanns

, Semmler

, Fruth

, Kemper

. Shiga toxin producing Escherichia coli: Identification of non-O157:H7-super-shedding cows and related risk factors. Gut Pathog, 2010; 2:7.

121.

Mersha

, Asrat

, Zewde

, Kyule

. Occurrence of Escherichia coli O157:H7 in faeces, skin and carcasses from sheep and goats in Ethiopia. Lett Appl Microbiol, 2010; 50:71–76.

122.

Milios

, Mataragas

, Pantouvakis

, Drosinos

, Zoiopoulos

. Evaluation of control over the microbiological contamination of carcasses in a lamb carcass dressing process operated with or without pasteurizing treatment. Int J Food Microbiol, 2011; 146:170–175.

123.

Milnes

, Stewart

, Clifton-Hadley

, Davies

, Newell

, Sayers

, Cheasty

, Cassar

, Ridley

, Cook

AJC

, Evans

, Teale

, Smith

, McNally

, Toszeghy

, Futter

, Kay

, Paiba

. Intestinal carriage of verocytotoxigenic Escherichia coli O157, Salmonella, thermophilic Campylobacter and Yersinia enterocolitica, in cattle, sheep and pigs at slaughter in Great Britain during 2003. Epidemiol Infect, 2008; 136:739–751.

124.

Mir

, Weppelmann

, Elzo

, Ahn

, Driver

, Jeong

. Colonization of beef cattle by Shiga toxin-producing Escherichia coli during the first year of life: A cohort study. PLoS One, 2016; 11:e0148518.

125.

Mir

, Weppelmann

, Kang

, Bliss

, DiLorenzo

, Lamb

, Ahn

, Jeong

. Association between animal age and the prevalence of Shiga toxin-producing Escherichia coli in a cohort of beef cattle. Vet Microbiol, 2015; 175:325–331.

126.

MLA Corporate. Lower NZ lamb crop puts pressure on global prices | Meat & Livestock Australia. MLA Corp, 2019. Available at: https://www.mla.com.au/prices-markets/market-news/2019/lower-nz-lamb-crop-puts-pressure-on-global-prices/, accessed October 5, 2020 .

127.

Mohammed

, Stipetic

, Salem

, McDonough

, Chang

, Sultan

. Risk of Escherichia coli O157:H7, Non-O157 Shiga toxin–producing Escherichia coli, and Campylobacter spp. in food animals and their products in Qatar. J Food Prot, 2015; 78:1812–1818.

128.

Momtaz

, Safarpoor Dehkordi

, Rahimi

, Ezadi

, Arab

. Incidence of Shiga toxin-producing Escherichia coli serogroups in ruminant's meat. Meat Sci, 2013; 95:381–388.

129.

Mora

, López

, Dhabi

, López-Beceiro

, Fidalgo

, Díaz

, Martínez-Carrasco

, Mamani

, Herrera

, Blanco

. Seropathotypes, phylogroups, Stx subtypes, and intimin types of wildlife-carried, Shiga toxin-producing Escherichia coli strains with the same characteristics as human-pathogenic isolates. Appl Environ Microbiol, 2012; 78:2578–2585.

130.

Moriarty

, McEwan

, Mackenzie

, Karki

, Sinton

, Wood

. Incidence and prevalence of microbial indicators and pathogens in ovine faeces in New Zealand. N Z J Agric Res, 2011; 54:71–81.

131.

Mughini-Gras

, van Pelt

, van der Voort

, Heck

, Friesema

, Franz

. Attribution of human infections with Shiga toxin-producing Escherichia coli (STEC) to livestock sources and identification of source-specific risk factors, The Netherlands (2010–2014). Zoonoses Public Health, 2018; 65:e8–e22.

132.

Munns

, Selinger

, Stanford

, Guan

, Callaway

, McAllister

. Perspectives on super-shedding of Escherichia coli O157:H7 by cattle. Foodborne Pathog Dis, 2015; 12:89–103.

133.

Muñoz

, Alvarez

, Lanza

, Cármenes

. Role of enteric pathogens in the aetiology of neonatal diarrhoea in lambs and goat kids in Spain. Epidemiol Infect, 1996; 117:203–211.

134.

Nataro

, Kaper

. Diarrheagenic Escherichia coli . Clin Microbiol Rev, 1998; 11:142–201.

135.

Naylor

, Low

, Besser

, Mahajan

, Gunn

, Pearce

, McKendrick

, Smith

DGE

, Gally

. Lymphoid follicle-dense mucosa at the terminal rectum is the principal site of colonization of enterohemorrhagic Escherichia coli O157:H7 in the bovine host. Infect Immun, 2003, 71:1505–1512.

136.

Noll

, Shridhar

, Dewsbury

, Shi

, Cernicchiaro

, Renter

, Nagaraja

. A comparison of culture- and PCR-based methods to detect six major non-O157 serogroups of Shiga toxin-producing Escherichia coli in cattle feces. PLoS One, 2015; 10:e0135446.

137.

O'Brien

, LaVeck

, Thompson

, Formal

. Production of Shigella dysenteriae type 1-like cytotoxin by Escherichia coli . J Infect Dis, 1982; 146:763–769.

138.

Obrig

TG.

Escherichia coli Shiga toxin mechanisms of action in renal disease. Toxins, 2010; 2:2769–2794.

139.

Ogden

, Hepburn

, MacRae

, Strachan

NJC

, Fenlon

, Rusbridge

, Pennington

. Long-term survival of Escherichia coli O157 on pasture following an outbreak associated with sheep at a scout camp. Lett Appl Microbiol, 2002; 34:100–104.

140.

Ogden

, MacRae

, Strachan

NJC

. Concentration and prevalence of Escherichia coli O157 in sheep faeces at pasture in Scotland. J Appl Microbiol, 2005; 98:646–651.

141.

Ojo

, Ajuwape

ATP

, Otesile

, Owoade

, Oyekunle

, Adetosoye

. Potentially zoonotic Shiga toxin-producing Escherichia coli serogroups in the faeces and meat of food-producing animals in Ibadan, Nigeria. Int J Food Microbiol, 2010; 142:214–221.

142.

Omisakin

, MacRae

, Ogden

, Strachan

NJC

. Concentration and prevalence of Escherichia coli O157 in cattle feces at slaughter. Appl Environ Microbiol, 2003; 69:2444–2447.

143.

Oporto

, Esteban

, Aduriz

, Juste

, Hurtado

. Escherichia coli O157:H7 and non-O157 Shiga toxin-producing E. coli in healthy cattle, sheep and swine herds in Northern Spain. Zoonoses Public Health, 2008; 55:73–81.

144.

Oporto

, Ocejo

, Alkorta

, Marimón

, Montes

, Hurtado

. Zoonotic approach to Shiga toxin-producing Escherichia coli: Integrated analysis of virulence and antimicrobial resistance in ruminants and humans. Epidemiol Infect, 2019; 147:e164.

145.

Orden

, Ruiz-Santa-Quiteria

, Blanco

, Mora

, Cid

, González

, Blanco

, de la Fuente

. Prevalence and characterization of Vero cytotoxin-producing Escherichia coli isolated from diarrhoeic and healthy sheep and goats. Epidemiol Infect, 2003; 130:313–321.

146.

Osman

, Mustafa

, Elhariri

, AbdElhamed

. The distribution of Escherichia coli Serovars, virulence genes, gene association and combinations and virulence genes encoding serotypes in pathogenic E. coli recovered from diarrhoeic calves, sheep and goat. Transbound Emerg Dis, 2013; 60:69–78.

147.

Paiba

, Gibbens

, Pascoe

SJS

, Wilesmith

, Kidd

, Byrne

, Ryan

JBM

, Smith

, McLaren

, Futter

, Kay

ACS

, Jones

, Chappell

, Willshaw

, Cheasty

. Faecal carriage of verocytotoxin-producing Escherichia coli O157 in cattle and sheep at slaughter in Great Britain. Vet Rec, 2002; 150:593–598.

148.

Pao

, Patel

, Kalantari

, Tritschler

, Wildeus

, Sayre

. Detection of Salmonella strains and Escherichia coli O157:H7 in feces of small ruminants and their isolation with various media. Appl Environ Microbiol, 2005; 71:2158–2161.

149.

Paquette

S-J

, Stanford

, Thomas

, Reuter

. Quantitative surveillance of Shiga toxins 1 and 2, Escherichia coli O178 and O157 in feces of western-Canadian slaughter cattle enumerated by droplet digital PCR with a focus on seasonality and slaughterhouse location. PLoS One, 2018; 13:e0195880.

150.

Pearce

, Fenlon

, Low

, Smith

, Knight

, Evans

, Foster

, Synge

, Gunn

. Distribution of Escherichia coli O157 in bovine fecal pats and its impact on estimates of the prevalence of fecal shedding. Appl Environ Microbiol, 2004; 70:5737–5743.

151.

Persad

, LeJeune

. Animal reservoirs of Shiga toxin-producing Escherichia coli . Microbiol Spectr, 2014; 2:EHEC-0027-2014.

152.

Petras

RE.

66—Gastrointestinal pathology. In: Pediatric Gastrointestinal and Liver Disease, Fourth Ed. Wyllie R, Hyams JS (eds.). Saint Louis, MO: W.B. Saunders, 2011, pp. 699–716.e5.

153.

Philipsborn

, Ahmed

, Brosi

, Levy

. Climatic drivers of diarrheagenic Escherichia coli incidence: A systematic review and meta-analysis. J Infect Dis, 2016; 214:6–15.

154.

Phillips

, Navabpour

, Hicks

, Dougan

, Wallis

, Frankel

. Enterohaemorrhagic Escherichia coli O157:H7 target Peyer's patches in humans and cause attaching/effacing lesions in both human and bovine intestine. Gut, 2000; 47:377–381.

155.

Phillips

, Jordan

, Morris

, Jenson

, Sumner

. Microbiological quality of Australian sheep meat in 2004. Meat Sci, 2006; 74:261–266.

156.

Phillips

, Sumner

, Alexander

, Dutton

. Microbiological quality of Australian sheep meat. J Food Prot, 2001; 64:697–700.

157.

Phillips

, Tholath

, Jenson

, Sumner

. Microbiological quality of Australian sheep meat in 2011. Food Control, 2013; 31:291–294.

158.

Piérard

, De Greve

, Haesebrouck

, Mainil

. O157:H7 and O104:H4 Vero/Shiga toxin-producing Escherichia coli outbreaks: Respective role of cattle and humans. Vet Res, 2012; 43:13.

159.

Pinaka

, Pournaras

, Mouchtouri

, Plakokefalos

, Katsiaflaka

, Kolokythopoulou

, Barboutsi

, Bitsolas

, Hadjichristodoulou

. Shiga toxin-producing Escherichia coli in Central Greece: Prevalence and virulence genes of O157:H7 and non-O157 in animal feces, vegetables, and humans. Eur J Clin Microbiol Infect Dis, 2013; 32:1401–1408.

160.

Prendergast

, Lendrum

, Pearce

, Ball

, McLernon

, O'Grady

, Scott

, Fanning

, Egan

, Gutierrez

. Verocytotoxigenic Escherichia coli O157 in beef and sheep abattoirs in Ireland and characterisation of isolates by pulsed-field gel electrophoresis and multi-locus variable number of tandem repeat analysis. Int J Food Microbiol, 2011; 144:519–527.

161.

Pritchard

, Smith

, Ellis-Iversen

, Cheasty

, Willshaw

. Verocytotoxigenic Escherichia coli O157 in animals on public amenity premises in England and Wales, 1997 to 2007. Vet Rec, 2009; 164:545–549.

162.

Rahimi

, Kazemeini

, Salajegheh

. Escherichia coli O157:H7/NM prevalence in raw beef, camel, sheep, goat, and water buffalo meat in Fars and Khuzestan provinces, Iran. Vet Res Forum Int Q J, 2012; 3:15–17.

163.

Ramachandran

, Hornitzky

, Bettelheim

, Walker

, Djordjevic

. The common ovine Shiga toxin 2-containing Escherichia coli serotypes and human isolates of the same serotypes possess a Stx2d toxin type. J Clin Microbiol, 2001; 39:1932–1937.

164.

Rey

, Blanco

, Mora

, Dahbi

, Alonso

, Hermoso

, Alonso

, Usera

, González

, Bernárdez

, Blanco

. Serotypes, phage types and virulence genes of shiga-producing Escherichia coli isolated from sheep in Spain. Vet Microbiol, 2003; 94:47–56.

165.

Rhoades

, Duffy

, Koutsoumanis

. Prevalence and concentration of verocytotoxigenic Escherichia coli, Salmonella enterica and Listeria monocytogenes in the beef production chain: A review. Food Microbiol, 2009; 26:357–376.

166.

Rice

, Sheng

, Wynia

, Hovde

. Rectoanal mucosal swab culture is more sensitive than fecal culture and distinguishes Escherichia coli O157:H7-colonized cattle and those transiently shedding the same organism. J Clin Microbiol, 2003; 41:4924–4929.

167.

Robinson

, Brown

, John Wright

, Bennett

, Hart

, French

. Heterogeneous distributions of Escherichia coli O157 within naturally infected bovine faecal pats. FEMS Microbiol Lett, 2005; 244:291–296.

168.

Roug

, Byrne

, Conrad

, Miller

. Zoonotic fecal pathogens and antimicrobial resistance in county fair animals. Comp Immunol Microbiol Infect Dis, 2013; 36:303–308.

169.

Rowell

, King

, Jenkins

, Dallman

, Decraene

, Lamden

, Howard

, Featherstone

, Cleary

. An outbreak of Shiga toxin-producing Escherichia coli serogroup O157 linked to a lamb-feeding event. Epidemiol Infect, 2016; 144:2494–2500.

170.

Sánchez

, Martínez

, García

, Blanco

, Dahbi

, López

, Mora

, Rey

, Alonso

. Longitudinal study of Shiga toxin-producing Escherichia coli shedding in sheep feces: Persistence of specific clones in sheep flocks. Appl Environ Microbiol, 2009; 75:1769–1773.

171.

Sanderson

, Besser

, Gay

, Hancock

. Fecal Escherichia coli O157:H7 shedding patterns of orally inoculated calves. Vet Microbiol, 1999; 69:199–205.

172.

Schilling

A-K

, Hotzel

, Methner

, Sprague

, Schmoock

, El-Adawy

, Ehricht

, Wöhr

A-C

, Erhard

, Geue

. Zoonotic agents in small ruminants kept on city farms in Southern Germany. Appl Environ Microbiol, 2012; 78:3785–3793.

173.

Schmidt

, Hensel

. Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev, 2004; 17:14–56.

174.

Schüller

Shiga toxin interaction with human intestinal epithelium. Toxins, 2011; 3:626–639.

175.

Sekse

, O'Sullivan

, Granum

, Rørvik

, Wasteson

, Jørgensen

. An outbreak of Escherichia coli O103:H25- bacteriological investigations and genotyping of isolates from food. Int J Food Microbiol, 2009; 133:259–264.

176.

Sekse

, Sunde

, Hopp

, Bruheim

, Cudjoe

, Kvitle

, Urdahl

. Occurrence of potentially human-pathogenic Escherichia coli O103 in Norwegian sheep. Appl Environ Microbiol, 2013; 79:7502–7509.

177.

Shekarforoush

, Tahamtan

, Pourbakhsh

. Detection and frequency of Stx2 gene in Escherichia coli O157 and O157:H7 strains isolated from sheep carcasses in Shiraz-Iran. Pak J Biol Sci, 2008; 11:1085–1092.

178.

Sheng

, Davis

, Knecht

, Hovde

. Rectal administration of Escherichia coli O157:H7: Novel model for colonization of ruminants. Appl Environ Microbiol, 2004; 70:4588–4595.

179.

Sheridan

Sources of contamination during slaughter and measures for control. J Food Saf, 2007; 18:321–339.

180.

Shridhar

, Siepker

, Noll

, Shi

, Nagaraja

, Bai

. Shiga toxin subtypes of non-O157 Escherichia coli serogroups isolated from cattle feces. Front Cell Infect Microbiol, 2017; 7:121.

181.

Sidjabat-Tambunan

, Bensink

. Verotoxin-producing Escherichia coli from the faeces of sheep, calves and pigs. Aust Vet J, 1997; 75:292–293.

182.

Söderlund

, Hedenström

, Nilsson

, Eriksson

, Aspán

. Genetically similar strains of Escherichia coli O157:H7 isolated from sheep, cattle and human patients. BMC Vet Res, 2012; 8:200.

183.

Solecki

, MacRae

, Strachan

, Lindstedt

B-A

, Ogden

. E. coli O157 from sheep in northeast Scotland: Prevalence, concentration shed, and molecular characterization by multilocus variable tandem repeat analysis. Foodborne Pathog Dis, 2009; 6:849–854.

184.

Soon

, Chadd

, Baines

. Escherichia coli O157:H7 in beef cattle: On farm contamination and pre-slaughter control methods. Anim Health Res Rev, 2011; 12:197–211.

185.

Tahamtan

, Hayati

, Namavari

. Contamination of sheep carcasses with verocytotoxin producing Escherichia coli during slaughtering. Transbound Emerg Dis, 2010; 57:25–27.

186.

Tahamtan

, Namavari

. Prevalence of O157:H7 and non-O157 E. coli in Iranian domestic sheep. Pak J Biol Sci, 2014; 17:104–108.

187.

Tahmasby

, Mehrabiyan

, Tajbakhsh

, Farahmandi

, Monji

, Farahmandi

. Molecular detection of nine clinically important non-O157 Escherichia coli serogroups from raw sheep meat in Chaharmahal-va-Bakhtiari province, Iran. Meat Sci, 2014; 97:428–432.

188.

Tarawneh

, Al-Tawarah

, Abdel-Ghani

, Al-Majali

, Khleifat

. Characterization of verotoxigenic Escherichia coli (VTEC) isolates from faeces of small ruminants and environmental samples in southern Jordan. J Basic Microbiol, 2009; 49:310–317.

189.

Thomas

, McCann

, Collery

, Moschonas

, Whyte

, McDowell

, Duffy

. Transfer of verocytotoxigenic Escherichia coli O157, O26, O111, O103 and O145 from fleece to carcass during sheep slaughter in an Irish export abattoir. Food Microbiol, 2013; 34:38–45.

190.

Trachtman

, Austin

, Lewinski

, Stahl

RAK

. Renal and neurological involvement in typical Shiga toxin-associated HUS. Nat Rev Nephrol, 2012; 8:658–669.

191.

Vande Walle

, Yekta

, Verdonck

, De Zutter

, Cox

. Rectal inoculation of sheep with E. coli O157:H7 results in persistent infection in the absence of a protective immune response. Vet Microbiol, 2011; 147:376–382.

192.

Vanderlinde

, Shay

, Murray

. Microbiological status of Australian sheep meat. J Food Prot, 1999; 62:380–385.

193.

Venegas-Vargas

, Henderson

, Khare

, Mosci

, Lehnert

, Singh

, Ouellette

, Norby

, Funk

, Rust

, Bartlett

, Grooms

, Manning

. Factors associated with Shiga toxin-producing Escherichia coli shedding by dairy and beef cattle. Appl Environ Microbiol, 2016; 82:5049–5056.

194.

Vettorato

, Leomil

, Guth

BEC

, Irino

, Pestana de Castro

. Properties of Shiga toxin-producing Escherichia coli (STEC) isolates from sheep in the State of São Paulo, Brazil. Vet Microbiol, 2003; 95:103–109.

195.

Wahl

, Vold

, Lindstedt

, Bruheim

, Afset

. Investigation of an Escherichia coli O145 outbreak in a child day-care centre—Extensive sampling and characterization of eae- and stx1-positive E. coli yields epidemiological and socioeconomic insight. BMC Infect Dis, 2011; 11:238.

196.

Wang

, Yang

, Kase

, Meng

, Clotilde

, Lin

, Ge

. Current trends in detecting non-O157 Shiga toxin-producing Escherichia coli in food. Foodborne Pathog Dis, 2013; 10:665–677.

197.

Wasteson

, Johannessen

, Bruheim

, Urdahl

, O'Sullivan

, Rørvik

. Fluctuations in the occurrence of Escherichia coli O157:H7 on a Norwegian farm. Lett Appl Microbiol, 2005; 40:373–377.

198.

Williams

, Ward

, Dhungyel

, Hall

EJS

. Risk factors for Escherichia coli O157 shedding and super-shedding by dairy heifers at pasture. Epidemiol Infect, 2015; 143:1004–1015.

199.

Wilson

, Dolan

, Aird

, Sorrell

, Dallman

, Jenkins

, Robertson

, Gorton

. Farm-to-fork investigation of an outbreak of Shiga toxin-producing Escherichia coli O157. Microb Genomics, 2018; 4:e000160.

200.

Woodward

, Best

, Sprigings

, Pearson

, Skuse

, Wales

, Hayes

, Roe

, Low

, La Ragione

. Non-toxigenic Escherichia coli O157:H7 strain NCTC12900 causes attaching-effacing lesions and eae-dependent persistence in weaned sheep. Int J Med Microbiol, 2003; 293:299–308.

201.

Yang

, Abraham

, Gardner

, Ryan

, Jacobson

. Prevalence and pathogen load of Campylobacter spp., Salmonella enterica and Escherichia coli O157/O145 serogroup in sheep faeces collected at sale yards and in abattoir effluent in Western Australia. Aust Vet J, 2017; 95:143–148.

202.

Yekta

, Goddeeris

, Vanrompay

, Cox

. Immunization of sheep with a combination of intiminγ, EspA and EspB decreases Escherichia coli O157:H7 shedding. Vet Immunol Immunopathol, 2011; 140:42–46.

203.

Zschöck

, Hamann

, Kloppert

, Wolter

. Shiga-toxin-producing Escherichia coli in faeces of healthy dairy cows, sheep and goats: Prevalence and virulence properties. Lett Appl Microbiol, 2000; 31:203–208.

204.

Zweifel

, Kaufmann

, Blanco

, Stephan

. [Significance of Escherichia coli O157 in sheep at slaughter in Switzerland]. Schweiz Arch Tierheilkd, 2006; 148:289–295.

205.

Zweifel

, Stephan

. Microbiological monitoring of sheep carcass contamination in three Swiss abattoirs. J Food Prot, 2003; 66:946–952.

206.

Zweifel

, Zychowska

, Stephan

. Prevalence and characteristics of Shiga toxin-producing Escherichia coli, Salmonella spp. and Campylobacter spp. isolated from slaughtered sheep in Switzerland. Int J Food Microbiol, 2004; 92:45–53.

Supplementary Material

Please find the following supplemental material available below.

For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.

For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.

0.00 MB

0.08 MB

0.05 MB