Persistent colonization of sheep by Escherichia coli O157:H7 and other E. coli pathotypes.

Escherichia coli O157:H7 and other serotypes of Shiga toxin-producing E. coli (STEC) are important causes of food-borne illnesses in people. Most clusters of disease are traced to contaminated food or water, but person-to-person transmissions also occurs (24, 32, 56). Contaminated beef has been the source of several large outbreaks of disease, and cattle are considered to be a reservoir for E. coli O157:H7 and other STEC serotypes (24, 32, 48, 58). Healthy cattle shed E. coli O157:H7 intermittently. Among U.S. cattle the overall individual animal prevalence of E. coli O157:H7 is approximately 2 to 3%, while the herd prevalence is much higher (16, 20, 25, 46, 58, 59). Fecal shedding of E. coli O157:H7 is often seasonal, with increased shedding during the summer (7, 25, 27, 41), which corresponds to an increased incidence of human disease (27, 37). Frequently individual cattle are transiently colonized (<1 month) by one particular strain, but occasional animals excrete multiple strains of E. coli O157:H7 (1, 16, 53). Individual strains of E. coli O157:H7 can be isolated from some herds for as long as 2 years, whereas other herds remain culture negative for several years (53). E. coli O157:H7 has also been isolated from healthy sheep (7, 29, 36), sheep's milk (50), and wild deer (47, 51). Food products from other ruminants, such as venison jerky (33) and goat's milk (3), have also been implicated as sources of human STEC infection. Both cattle and sheep also harbor other serotypes of STEC, usually at a much higher prevalence than serotype O157:H7 (2, 18, 35, 46, 58). In contrast to ruminants, E. coli O157:H7 is isolated much less frequently from other domestic and wild animals (7, 26, 53, 57). This may be partially due to a sampling bias toward cattle. However, in a survey of 4,229 market swine in the United States, the incidence of E. coli O157:H7 was less than 0.07% (5). E. coli O157:H7 was not isolated from 1,000 fecal samples from either swine or poultry in England (7). There are recent reports of E. coli O157:H7 being isolated from swine in Chile (49) and Japan (45). Although E. coli O157:H7 occurs in nonruminant animals such as dogs, horses, birds, and flies, there is no evidence that the agent is as prevalent or as persistent in these animals as it is in ruminants (6, 26, 53, 57). Furthermore, the prevalence of all types of STEC appears to be greater in ruminants than in other types of domestic animals (2). Both calves and adult cattle have been experimentally inoculated with E. coli O157:H7 (4, 11, 28, 30). The magnitude of shedding is greatest during the first 2 weeks postinoculation (p.i.) and decreases thereafter. In general, calves shed higher numbers of E. coli O157:H7 organisms for a longer duration than do mature animals (11). This parallels the results of on-farm studies that show a greater percentage of young animals colonized with E. coli O157:H7 than adults (25, 27, 41, 58). However, there is considerable animal-to-animal variability in both the numbers of bacteria shed and the duration of shedding (4, 11). The infection persists for several months in some cattle and calves (11). Sheep have also been experimentally inoculated with E. coli O157:H7 (34, 37). The quantity and duration of fecal shedding are similar to those for cattle. Diet appears to influence the colonization of E. coli O157:H7 in both cattle and sheep (10, 30, 34, 37). Serum antibody to O157 lipopolysaccharide or Shiga toxin 1 (Stx1) acquired from a prior infection does not protect calves from reinfection (31). Sheep and cattle that have cleared a previous colonization with E. coli O157:H7 can also be reinfected (11, 37). Despite the widespread epidemiological evidence that most ruminants are colonized by STEC, the reasons for this observation are not known. We hypothesized that STEC bacteria are better adapted to colonize and persist in the alimentary tracts of ruminants than are other pathotypes of E. coli. We tested this hypothesis by analyzing the frequency, magnitude, duration, and transmissibility of E. coli O157:H7 colonization compared to those for other pathotypes of E. coli when sheep were inoculated with a cocktail consisting of multiple strains representing three pathotypes of E. coli. We found that the inoculated STEC strains tended to persist longer than the enterotoxigenic (ETEC) and enteropathogenic (EPEC) strains included in the same inoculum. We also found that all of the strains were transmitted to naive animals from infected donors and again that the STEC strains tended to persist longer in the recipient animals than did two of the other strains. (A preliminary report of this work was made at the 99th General Meeting of the American Society for Microbiology, 1999, abstr. D/B 309); at the annual meeting of the Food Research Institute, University of Wisconsin—Madison, 1999; and at the Verocytotoxigenic E. coli in Europe: Pathogenicity and Virulence meeting, Liege, Belgium, 1999.)