Chicken as Reservoir for Extraintestinal Pathogenic Escherichia coli in Humans, Canada

Catherine Racicot Bergeron¹, Catharine Prussing¹, Patrick Boerlin, Danielle Daignault, Lucie Dutil², Richard J. Reid-Smith, George G. Zhanel, and Amee R. Manges

Author affiliations: McGill University, Montréal, Québec, Canada (C. Racicot Bergeron, C. Prussing, A.R. Manges); University of Guelph, Guelph, Ontario, Canada (P. Boerlin, R.J. Reid-Smith); Public Health Agency of Canada, Saint-Hyacinthe, Québec, Canada (D. Daignault, L. Dutil); Public Health Agency of Canada, Guelph (R.J. Reid-Smith); University of Manitoba, Winnipeg, Manitoba, Canada (G.G. Zhanel)

Abstract

We previously described how retail meat, particularly chicken, might be a reservoir for extraintestinal pathogenic Escherichia coli (ExPEC) causing urinary tract infections (UTIs) in humans. To rule out retail beef and pork as potential reservoirs, we tested 320 additional E. coli isolates from these meats. Isolates from beef and pork were significantly less likely than those from chicken to be genetically related to isolates from humans with UTIs. We then tested whether the reservoir for ExPEC in humans could be food animals themselves by comparing geographically and temporally matched E. coli isolates from 475 humans with UTIs and from cecal contents of 349 slaughtered animals. We found genetic similarities between E. coli from animals in abattoirs, principally chickens, and ExPEC causing UTIs in humans. ExPEC transmission from food animals could be responsible for human infections, and chickens are the most probable reservoir.

Extraintestinal pathogenic Escherichia coli (ExPEC) is the leading cause of community-acquired urinary tract infections (UTIs) in humans, accounting for >85% of UTIs (1). Each year, 6–8 million UTIs are diagnosed in the United States, and 130–175 million are diagnosed worldwide. Estimated direct health care costs related to uncomplicated UTIs in the United States are $1–$2 billion per year (1,2). UTIs also can lead to more severe illnesses, such as pyelonephritis, bacteremia, and sepsis (3). During the past decade, the emergence of drug-resistant E. coli has dramatically increased. As a consequence, the management of UTIs, which was previously straightforward, has become more complicated; the risks for treatment failure are higher, and the cost of UTI treatment is increasing (4).
In the past, extraintestinal E. coli infections have been described as sporadic infections caused by bacteria that originate from the host’s intestinal tract. However, ExPEC strains recently have been associated with possible outbreaks (5). Communitywide outbreaks have been described in south London (E. coli O15:K152:H1) (6); Copenhagen (E. coli O78:H10) (7); Calgary, Alberta, Canada (extended-spectrum β-lactamase–producing E. coli) (8); and California, USA (trimethoprim/sulfamethoxazole–resistant E. coli) (9). These outbreaks suggest that ExPEC can be spread to the intestinal tracts of persons in the community by a common source or vehicle.
We recently described the results of a study that characterized the genetic similarities between E. coli isolates recovered from retail meat, particularly chicken, and ExPEC in humans causing community-acquired UTIs (10). That study oversampled isolates from retail chicken because evidence suggested that chicken was likely to be the primary reservoir of ExPEC in humans (11–16). To exclude the possibility that isolates from other retail meat sources (beef and pork) might also be genetically related to UTI isolates from humans, we first aimed to characterize additional E. coli isolates recovered from retail beef and pork sources. These new isolates from retail meat were added to the preexisting collection of retail meat isolates and compared with the same UTI isolates from humans. Second, we aimed to determine whether transmission was primarily human to human through food or whether an animal source was involved. In the case of human-to-human transmission through food, E. coli strains from humans would be introduced during the meat preparation process by food handlers. In the case of an animal source, the E. coli would derive from the cecal content of the animal itself, and contamination would occur during the slaughtering process. On the basis of previous findings, we hypothesized that a food animal reservoir exits for ExPEC that cause UTIs in humans and that chicken is the primary source. To evaluate this hypothesis, we analyzed isolates from animals entering the food chain. E. coli isolates recovered from the cecal contents of slaughtered food animals (beef cattle, chickens, and pigs) were compared with the preexisting geographically and temporally matched collection of isolates from humans with UTIs.