Escherichia coli ST131- H 22 as a Foodborne Uropathogen

Abstract

Escherichia coli sequence type 131 (ST131) has emerged rapidly to become the most prevalent extraintestinal pathogenic E. coli clones in circulation today. Previous investigations appeared to exonerate retail meat as a source of human exposure to ST131; however, these studies focused mainly on extensively multidrug-resistant ST131 strains, which typically carry allele 30 of the fimH type 1 fimbrial adhesin gene (ST131-H30). To estimate the frequency of extraintestinal human infections arising from foodborne ST131 strains without bias toward particular sublineages or phenotypes, we conducted a 1-year prospective study of E. coli from meat products and clinical cultures in Flagstaff, Arizona. We characterized all isolates by multilocus sequence typing, fimH typing, and core genome phylogenetic analyses, and we screened isolates for avian-associated ColV plasmids as an indication of poultry adaptation. E. coli was isolated from 79.8% of the 2,452 meat samples and 72.4% of the 1,735 culture-positive clinical samples. Twenty-seven meat isolates were ST131 and belonged almost exclusively (n = 25) to the ST131-H22 lineage. All but 1 of the 25 H22 meat isolates were from poultry products, and all but 2 carried poultry-associated ColV plasmids. Of the 1,188 contemporaneous human clinical E. coli isolates, 24 were ST131-H22, one-quarter of which occurred in the same high-resolution phylogenetic clades as the ST131-H22 meat isolates and carried ColV plasmids. Molecular clock analysis of an international ST131-H22 genome collection suggested that ColV plasmids have been acquired at least six times since the 1940s and that poultry-to-human transmission is not limited to the United States.IMPORTANCEE. coli ST131 is an important extraintestinal pathogen that can colonize the gastrointestinal tracts of humans and food animals. Here, we combined detection of accessory traits associated with avian adaptation (ColV plasmids) with high-resolution phylogenetics to quantify the portion of human infections caused by ST131 strains of food animal origin. Our results suggest that one ST131 sublineage-ST131-H22-has become established in poultry populations around the world and that meat may serve as a vehicle for human exposure and infection. ST131-H22 is just one of many E. coli lineages that may be transmitted from food animals to humans. Additional studies that combine detection of host-associated accessory elements with phylogenetics may allow us to quantify the total fraction of human extraintestinal infections attributable to food animal E. coli strains.

Keywords: Antibiotic resistance; ColV plasmid; Escherichia coli; ExPEC; ST131; UTI; antimicrobial resistance; foodborne; host adaptation; poultry; urinary tract infection.

FIG 1

Whole-genome phylogeny of meat and human clinical Escherichia coli ST131 isolates. (A) A total of 207 ST131 isolates from meat (in red) and human clinical specimens (in yellow) were included in this unrooted phylogeny. The fimH alleles corresponded closely with the phylogenetic groupings and were used to designate the four major lineages: H22, H27, H30, and H41. The ST131-H22 lineage included isolates with other fimH alleles fimH161 or fimH207, both of which are minor sequence variants of fimH22. Most (69%) of the clinical isolates belonged to the ST131-H30 lineage, with the balance falling into the ST131-H41 (16%), ST131-H22 (13%), and ST131-H27 (2%) lineages. In contrast, 93% of the meat isolates belonged to the ST131-H22 lineage. (B) Forty-nine ST131-H22 isolates from meat (in red) and human clinical specimens (in yellow) were included in this rooted high-resolution phylogeny. While some subclades contained only human clinical isolates, two subclades included intermingled meat and human clinical isolates. All ColV plasmid-positive ST131-H22 human clinical isolates fell within the latter two subclades, suggesting that these meat and human clinical isolates were derived from a common source. The scale bar represents the substitution rate in the conserved core genome. The branch leading to the H41 clade is truncated to approximately 20% of its full length for graphic purposes.

FIG 2

Bayesian analysis of 140 global Escherichia coli ST131-H22 genomes. The tree, based on a total of 3,774 SNPs identified in the relaxed core genome of 49 Flagstaff ST131-H22 isolates and 91 international H22 isolates, was obtained using a strict clock model, GTR substitution rate, and the Bayesian Skyline population tree model. The analysis strongly indicates six independent acquisitions of ColV plasmids within the ST131-H22 sublineage. The tips of the tree are constrained by year of isolation, with shaded areas used to represent the time scale (in decades). White arrows and red crosses point to branches associated with putative ColV plasmid acquisitions and losses, respectively.