Escherichia coli O157:H7 Colonization at the Rectoanal Junction of Long-Duration Culture-Positive Cattle

Abstract

Long-duration consistently Escherichia coli O157:H7 culture-positive cattle were euthanized and necropsied. Tissue and digesta from along the gastrointestinal tract (GIT) were cultured for the bacteria and examined histologically for lymphoid character. E. coli O157:H7 was detected only at the rectoanal junction mucosa and not at any other GIT location.Escherichia coli O157:H7 causes hemorrhagic colitis and the life-threatening sequela hemolytic-uremic syndrome in humans (6). Healthy cattle are the major reservoir for E. coli O157:H7, and contaminated ground beef, direct animal contact, and bovine manure contamination of other foods or water account for the majority of human infections (2, 3). The predominant colonization site of this microorganism in the bovine gastrointestinal tract (GIT) has been identified as the rectoanal junction (RAJ) mucosa (7). Localization to this site is in contrast with other E. coli serotypes that are present in consistent numbers throughout the large intestine without an increase at the RAJ mucosa. This tissue area comprises a clear junction between the stratified squamous epithelium of the anal canal and the columnar epithelial mucosa of the rectum and is a lymphoid follicle-dense mucosa. Although the mechanisms underlying the tropism of this serotype for this lymphoid follicle-rich site are not known, many studies of experimentally and naturally colonized cattle conclude that the RAJ mucosa plays an important role in E. coli O157:H7 bovine carriage of this human pathogen (5,7,8,10,11). Also, application of E. coli O157:H7 at the RAJ mucosa results in carriage of the bacteria similar to that by naturally infected animals (10).Three distinct patterns of E. coli O157:H7 carriage in cattle have been described previously (1, 9, 12). First, animals can be transiently culture positive for short durations of a few days and are considered passive shedders and are likely not colonized at the RAJ mucosa; second, cattle can be colonized and shed the bacteria for an average of 1 month and typically not longer than 2 months; and third, a few rare animals are colonized for a long duration and shed the bacteria from 3 to 12 months or longer. This unique situation in which a few animals develop long-duration colonization (Ͼ2 months) with E. coli O157 is likely due to bacterial association at the RAJ mucosa; however, it may be due to unique colonization by the bacteria at a site(s) in addition to the RAJ mucosa. For example, the gall bladder can harbor Salmonella spp. in carrier animals and a recent investigation reports E. coli O157:H7 in the gall bladders of some cattle at slaughter; however, this report does not provide information about the E. coli O157:H7 culture history of the animals tested, so the duration for which each animal was culture positive is unknown (4). For the first time, the current study investigated the colonization site of E. coli O157:H7 along the GIT of animals for which a documented history of long-duration carriage of E. coli O157:H7 was available. To identify animals t...

Escherichia coli O157:H7-secreted cytotoxins are toxic to enterocytes and increase Escherichia coli O157:H7 colonization of jejunum and descending colon in cattle

“…In contrast, Shiga toxins do not affect either EHEC O157:H7 colonization of the terminal rectum in single strain rectal challenged cattle (Sheng et al 2006) or secretory responses in bovine ileal intestinal loops from older calves (Stevens et al 2002). The terminal rectum studies (Naylor et al 2003;Sheng et al 2004Sheng et al , 2006Low et al 2005;Lim et al 2007) have focused on the role of lymphoid tissue in the EHEC O157:H7 infection process in cattle without comparisons with absorptive epithelium in other intestinal sites despite the reported association of EHEC O157:H7 with small and large intestinal sites in challenged cattle (Cray and Moon 1995;Grauke et al 2002;Van Baale et al 2004). In a previous study, we reported that there were no differences in the dose-dependent colonization of small and large intestinal sites compared with the terminal rectum (Baines et al 2008, manuscript in preparation) and in this study, we add to this by showing that the small and large intestinal tissues also respond to EHEC O157:H7 secreted cytotoxins in a similar manner to that reported for a model system purported to better represent the response of ruminant systems to EHEC O157:H7 colonization (Robinson et al 2006).…”

“…EHEC O157:H7 has been isolated from the small and large intestine of older calves and mature cattle but not necessarily associated with A/E lesions (Cray and Moon 1995;Brown et al 1997;Grauke et al 2002;Naylor et al 2003;van Baale et al 2004). The current model for EHEC O157:H7 colonization in cattle suggests that the lymphoid-follicle dense mucosa in the terminal rectum is the primary colonization site and it is this colonization that is responsible for persistent shedding (Naylor et al 2003Sheng et al 2004Sheng et al , 2006Lim et al 2007). The basic assumption of this model is that cattle are not adversely affected by EHEC O157:H7 virulence factors, and although a reduction in the expression of some EHEC O157:H7 virulence factors has been demonstrated (Rashid et al 2006), it is not true for all virulence factors.…”

Animal Reservoirs of Shiga Toxin-ProducingEscherichia coli

“…The average duration of STEC O157 carriage is 30 days; however, in rare cases animals may be colonized for up to 1 year (28). Animals excreting greater than 10 4 CFU/g feces are termed "super-shedding animals" (29,30).…”

Responses of Cattle to Gastrointestinal Colonization by Escherichia coli O157:H7

“…In this study, extensive histological examination of terminal rectal tissues did not reveal a prominent association between E. coli O157:H7 microcolonies and follicle-associated epithelium. Thus, the reason for the terminal rectum tropism of E. coli O157:H7 is still obscure (19). Two of the main features of this area are a potentially reduced width of the mucous barrier, based on measurements taken with mice over Peyer's patches (33) and the fact that the recto-anal junction is adjacent to the anal sphincter.…”