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      Pathogenic Escherichia coli in Dogs Reveals the Predominance of ST372 and the Human-Associated ST73 Extra-Intestinal Lineages

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          Abstract

          Escherichia coli is a ubiquitous commensal and pathogen that has also been recognized as a multi-sectoral indicator of antimicrobial resistance (AMR). Given that latter focus, such as on resistances to extended-spectrum cephalosporins (ESC) and carbapenems, the reported population structure of E. coli is generally biased toward resistant isolates, with sequence type (ST)131 being widely reported in humans, and ST410 and ST648 being reported in animals. In this study, we characterized 618 non-duplicate E. coli isolates collected throughout France independently of their resistance phenotype. The B2 phylogroup was over-represented (79.6%) and positively associated with the presence of numerous virulence factors (VFs), including those defining the extra-intestinal pathogenic E. coli isolates (presence of ≥2 VFs: papA, sfaS, focG, afaD, iutA, and kpsMTII) and those more specifically related to uropathogenic E. coli ( cnf1, hlyD). The major STs associated with clinical isolates from dogs were by far the dog-associated ST372 (20.7%) and ST73 (20.1%), a lineage that had commonly been considered until now as human-associated. Resistance to ESC was found in 33 isolates (5.3%), along with one carbapenemase-producing isolate, and was mostly restricted to non-B2 isolates. In conclusion, the presence of virulent E. coli lineages may be the issue, rather than the presence of ESC-resistant isolates, and the risk of transmission of such virulent isolates to humans needs to be further studied.

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          Global Extraintestinal Pathogenic Escherichia coli (ExPEC) Lineages

          SUMMARY Extraintestinal pathogenic Escherichia coli (ExPEC) strains are responsible for a majority of human extraintestinal infections globally, resulting in enormous direct medical and social costs. ExPEC strains are comprised of many lineages, but only a subset is responsible for the vast majority of infections. Few systematic surveillance systems exist for ExPEC. To address this gap, we systematically reviewed and meta-analyzed 217 studies (1995 to 2018) that performed multilocus sequence typing or whole-genome sequencing to genotype E. coli recovered from extraintestinal infections or the gut. Twenty major ExPEC sequence types (STs) accounted for 85% of E. coli isolates from the included studies. ST131 was the most common ST from 2000 onwards, covering all geographic regions. Antimicrobial resistance-based isolate study inclusion criteria likely led to an overestimation and underestimation of some lineages. European and North American studies showed similar distributions of ExPEC STs, but Asian and African studies diverged. Epidemiology and population dynamics of ExPEC are complex; summary proportion for some STs varied over time (e.g., ST95), while other STs were constant (e.g., ST10). Persistence, adaptation, and predominance in the intestinal reservoir may drive ExPEC success. Systematic, unbiased tracking of predominant ExPEC lineages will direct research toward better treatment and prevention strategies for extraintestinal infections.
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            Isolation and molecular characterization of nalidixic acid-resistant extraintestinal pathogenic Escherichia coli from retail chicken products.

            Fluoroquinolone use in poultry production may select for resistant Escherichia coli that can be transmitted to humans. To define the prevalence and virulence potential of poultry-associated, quinolone-resistant E. coli in the United States, 169 retail chicken products from the Minneapolis-St. Paul area (1999 to 2000) were screened for nalidixic acid (Nal)-resistant E. coli. Sixty-two (37%) products yielded Nal-resistant E. coli. From 55 products that yielded both Nal-resistant and susceptible E. coli, two isolates (one resistant, one susceptible) per sample were further characterized. Twenty-three (21%) of the 110 E. coli isolates (13 resistant, 10 susceptible) satisfied criteria for extraintestinal pathogenic E. coli (ExPEC), i.e., exhibited >or=2 of pap (P fimbriae), sfa/foc (S/F1C fimbriae), afa/dra (Dr binding adhesins), iutA (aerobactin receptor), and kpsMT II (group 2 capsule synthesis). Compared with other isolates, ExPEC isolates more often derived from virulence-associated E. coli phylogenetic groups B2 or D (74% versus 32%; P < 0.001) and exhibited more ExPEC-associated virulence markers (median, 10.0 versus 4.0; P < 0.001). In contrast, the Nal-resistant and -susceptible populations were indistinguishable according to all characteristics analyzed, including pulsed-field gel electrophoresis profiles. These findings indicate that Nal-resistant E. coli is prevalent in retail poultry products and that a substantial minority of such strains represent potential human pathogens. The similarity of the Nal-resistant and -susceptible populations suggests that they derive from the same source population, presumably the avian fecal flora, with Nal resistance emerging by spontaneous mutation as a result of fluoroquinolone exposure.
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              Escherichia coli isolates that carry vat, fyuA, chuA, and yfcV efficiently colonize the urinary tract.

              Extraintestinal Escherichia coli (ExPEC), a heterogeneous group of pathogens, encompasses avian, neonatal meningitis, and uropathogenic E. coli strains. While several virulence factors are associated with ExPEC, there is no core set of virulence factors that can be used to definitively differentiate these pathotypes. Here we describe a multiplex of four virulence factor-encoding genes, yfcV, vat, fyuA, and chuA, highly associated with uropathogenic E. coli strains that can distinguish three groups of E. coli: diarrheagenic and animal-associated E. coli strains, human commensal and avian pathogenic E. coli strains, and uropathogenic and neonatal meningitis E. coli strains. Furthermore, human intestinal isolates that encode all four predictor genes express them during exponential growth in human urine and colonize the bladder in the mouse model of ascending urinary tract infection in higher numbers than human commensal strains that do not encode the four predictor genes (P = 0.02), suggesting that the presence of the predictors correlates with uropathogenic potential.
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                Author and article information

                Contributors
                Journal
                Front Microbiol
                Front Microbiol
                Front. Microbiol.
                Frontiers in Microbiology
                Frontiers Media S.A.
                1664-302X
                21 April 2020
                2020
                : 11
                : 580
                Affiliations
                [1] 1Unité Antibiorésistance et Virulence Bactériennes, ANSES Laboratoire de Lyon – Université de Lyon , Lyon, France
                [2] 2Vebio , Arcueil, France
                [3] 3Orbio , Lyon, France
                [4] 4Unité de Bactériologie, BioPôle, Ecole Nationale Vétérinaire d’Alfort , Maisons-Alfort, France
                [5] 5Laboratoire Vétérinaire Départemental , Biot, France
                [6] 6Unité Epidémiologie et Appui à la Surveillance, ANSES Laboratoire de Lyon – Université de Lyon , Lyon, France
                Author notes

                Edited by: Etienne Giraud, Institut National de la Recherche Agronomique de Toulouse, France

                Reviewed by: Tessa LeCuyer, Virginia Tech, United States; Darren Trott, The University of Adelaide, Australia

                *Correspondence: Marisa Haenni, marisa.haenni@ 123456anses.fr

                This article was submitted to Antimicrobials, Resistance and Chemotherapy, a section of the journal Frontiers in Microbiology

                Article
                10.3389/fmicb.2020.00580
                7186358
                32373083
                eb57693f-4425-4883-9ec3-eec42becc593
                Copyright © 2020 Valat, Drapeau, Beurlet, Bachy, Boulouis, Pin, Cazeau, Madec and Haenni.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 13 November 2019
                : 17 March 2020
                Page count
                Figures: 1, Tables: 5, Equations: 0, References: 56, Pages: 12, Words: 0
                Funding
                Funded by: Agence Nationale de Sécurité Sanitaire de l’Alimentation, de l’Environnement et du Travail 10.13039/501100007546
                Categories
                Microbiology
                Original Research

                Microbiology & Virology
                e. coli,uti,dog,esbl,virulence,upec
                Microbiology & Virology
                e. coli, uti, dog, esbl, virulence, upec

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