scholarly journals Variation in Resistance Traits, Phylogenetic Backgrounds, and Virulence Genotypes among Escherichia coli Clinical Isolates from Adjacent Hospital Campuses Serving Distinct Patient Populations

2015 ◽  
Vol 59 (9) ◽  
pp. 5331-5339 ◽  
Author(s):  
Sarah M. Drawz ◽  
Stephen Porter ◽  
Michael A. Kuskowski ◽  
Brian Johnston ◽  
Connie Clabots ◽  
...  

ABSTRACTEscherichia colisequence type 13 (ST131), an emergent cause of multidrug-resistant extraintestinal infections, has important phylogenetic subsets, notably theH30 andH30Rx subclones, with distinctive resistance profiles and, possibly, clinical associations. To clarify the local prevalence of these ST131 subclones and their associations with antimicrobial resistance, ecological source, and virulence traits, we extensively characterized 233 consecutiveE. coliclinical isolates (July and August 2013) from the University of Minnesota Medical Center-Fairview Infectious Diseases and Diagnostic Laboratory, Minneapolis, MN, which serves three adjacent facilities (a children's hospital and low- and high-acuity adult facilities). ST131 accounted for 26% of the study isolates (more than any other clonal group), was distributed similarly by facility, and was closely associated with ciprofloxacin resistance and extended-spectrum β-lactamase (ESBL) production. TheH30 andH30Rx subclones accounted for most ST131 isolates and for the association of ST131 with fluoroquinolone resistance and ESBL production. Unlike ST131per se, these subclones were distributed differentially by hospital, being most prevalent at the high-acuity adult facility and were absent from the children's hospital. The virulence gene profiles of ST131 and its subclones were distinctive and more extensive than those of other fluoroquinolone-resistant or ESBL-producing isolates. Within ST131,blaCTX-M-15was confined toH30Rx isolates and otherblaCTX-Mvariants to non-RxH30 isolates. Pulsed-field gel electrophoresis documented a predominance of globally distributed pulsotypes and no local outbreak pattern. These findings help clarify the epidemiology, ecology, and bacterial correlates of theH30 andH30Rx ST131 subclones by documenting a high overall prevalence but significant segregation by facility, strong associations with fluoroquinolone resistance and specific ESBL variants, and distinctive virulence gene associations that may confer fitness advantages over other resistantE. coli.

2018 ◽  
Vol 62 (10) ◽  
Author(s):  
Shehara M. Mendis ◽  
Shawn Vasoo ◽  
Brian D. Johnston ◽  
Stephen B. Porter ◽  
Scott A. Cunningham ◽  
...  

ABSTRACT Escherichia coli bacteremia is caused mainly by sequence type complex 131 (STc131) and two clades within its fluoroquinolone-resistance-associated H30 subclone, H30R1 and H30Rx. We examined clinical and molecular correlates of E. coli bacteremia in two geographically distinct centers. We retrospectively studied 251 unique E. coli bloodstream isolates from 246 patients (48 from the Mayo Clinic, Rochester, MN [MN], and 198 from Tan Tock Seng Hospital, Singapore [SG]), from October 2013 through March 2014. Isolates underwent PCR for phylogroup, STc, blaCTX-M type, and virulence gene profiles, and medical records were reviewed. Although STc131 accounted for 25 to 27% of all E. coli bacteremia isolates at each site, its extended-spectrum-β-lactamase (ESBL)-associated H30Rx clade was more prominent in SG than in MN (15% versus 4%; P = 0.04). In SG only, patients with STc131 (versus other E. coli STc isolates) were more likely to receive inactive initial antibiotics (odds ratio, 2.8; P = 0.005); this was true specifically for patients with H30Rx (odds ratio, 7.0; P = 0.005). H30Rx comprised 16% of community-onset bacteremia episodes in SG but none in MN. In SG, virulence scores were higher for H30Rx than for H30R1, non-H30 STc131, and non-STc131 isolates (P < 0.02 for all comparisons). At neither site did mortality differ by clonal status. The ESBL-associated H30Rx clade was more prevalent and more often of community onset in SG, where it predicted inactive empirical treatment. The clonal distribution varies geographically and has potentially important clinical implications. Rapid susceptibility testing and clonal diagnostics for H30/H30Rx might facilitate earlier prescribing of active therapy.


2012 ◽  
Vol 80 (4) ◽  
pp. 1554-1562 ◽  
Author(s):  
James R. Johnson ◽  
Stephen B. Porter ◽  
George Zhanel ◽  
Michael A. Kuskowski ◽  
Erick Denamur

ABSTRACTEscherichia colisequence type ST131 (O25b:H4) has emerged over the past decade as a globally disseminated, multidrug-resistant pathogen. Unlike traditional antimicrobial-resistantE. coli, ST131 derives from virulence-associated phylogenetic group B2 and exhibits extraintestinal virulence factors. This, plus preliminary evidence of virulence in experimental animals, has suggested that ST131's epidemic emergence may be due to high virulence potential, compared with otherE. colitypes. To test this hypothesis, we compared a large number of matched ST131 and non-ST131E. coliclinical isolates, both fluoroquinolone resistant and susceptible, plus isolates from classic extraintestinal pathogenicE. coli(ExPEC) sequence types (STs) and case report ST131 household transmission isolates, for virulence in a mouse subcutaneous sepsis model. Overall, in mice, the study isolates produced a wide range of lethality and clinical illness. However, neither ST131 status nor fluoroquinolone phenotype correlated with this diversity of illness severity, which occurred within each of the 6 study groups. In contrast, multiple known or suspected ExPEC virulence genes, includingpap(P fimbriae),vat(vacuolating toxin),kpsMII (group 2 capsule),ibeA(invasion of brain endothelium), andclbB/N(colibactin synthesis), plus molecularly defined ExPEC status, were significantly associated with virulence. These findings point away from ST131 isolates as having higher virulence potential compared with otherE. colitypes in causing invasive extraintestinal infections and suggest instead that ST131's epidemiological success may reflect enhanced fitness for upstream steps in pathogenesis or in colonization and transmission. Additionally, the extensive within-ST virulence diversity suggests an opportunity to compare closely related strains to identify the responsible genetic determinants.


mBio ◽  
2013 ◽  
Vol 4 (6) ◽  
Author(s):  
Lance B. Price ◽  
James R. Johnson ◽  
Maliha Aziz ◽  
Connie Clabots ◽  
Brian Johnston ◽  
...  

ABSTRACT The Escherichia coli sequence type 131 (ST131) clone is notorious for extraintestinal infections, fluoroquinolone resistance, and extended-spectrum beta-lactamase (ESBL) production, attributable to a CTX-M-15-encoding mobile element. Here, we applied pulsed-field gel electrophoresis (PFGE) and whole-genome sequencing to reconstruct the evolutionary history of the ST131 clone. PFGE-based cluster analyses suggested that both fluoroquinolone resistance and ESBL production had been acquired by multiple ST131 sublineages through independent genetic events. In contrast, the more robust whole-genome-sequence-based phylogenomic analysis revealed that fluoroquinolone resistance was confined almost entirely to a single, rapidly expanding ST131 subclone, designated H30-R. Strikingly, 91% of the CTX-M-15-producing isolates also belonged to a single, well-defined clade nested within H30-R, which was named H30-Rx due to its more extensive resistance. Despite its tight clonal relationship with H30Rx, the CTX-M-15 mobile element was inserted variably in plasmid and chromosomal locations within the H30-Rx genome. Screening of a large collection of recent clinical E. coli isolates both confirmed the global clonal expansion of H30-Rx and revealed its disproportionate association with sepsis (relative risk, 7.5; P < 0.001). Together, these results suggest that the high prevalence of CTX-M-15 production among ST131 isolates is due primarily to the expansion of a single, highly virulent subclone, H30-Rx. IMPORTANCE We applied an advanced genomic approach to study the recent evolutionary history of one of the most important Escherichia coli strains in circulation today. This strain, called sequence type 131 (ST131), causes multidrug-resistant bladder, kidney, and bloodstream infections around the world. The rising prevalence of antibiotic resistance in E. coli is making these infections more difficult to treat and is leading to increased mortality. Past studies suggested that many different ST131 strains gained resistance to extended-spectrum cephalosporins independently. In contrast, our research indicates that most extended-spectrum-cephalosporin-resistant ST131 strains belong to a single highly pathogenic subclone, called H30-Rx. The clonal nature of H30-Rx may provide opportunities for vaccine or transmission prevention-based control strategies, which could gain importance as H30-Rx and other extraintestinal pathogenic E. coli subclones become resistant to our best antibiotics.


2016 ◽  
Vol 61 (2) ◽  
Author(s):  
Toyotaka Sato ◽  
Yuuki Suzuki ◽  
Tsukasa Shiraishi ◽  
Hiroyuki Honda ◽  
Masaaki Shinagawa ◽  
...  

ABSTRACT Tigecycline (TGC) is a last-line drug for multidrug-resistant Enterobacteriaceae. We investigated the mechanism(s) underlying TGC nonsusceptibility (TGC resistant/intermediate) in Escherichia coli clinical isolates. The MIC of TGC was determined for 277 fluoroquinolone-susceptible isolates (ciprofloxacin [CIP] MIC, <0.125 mg/liter) and 194 fluoroquinolone-resistant isolates (CIP MIC, >2 mg/liter). The MIC50 and MIC90 for TGC in fluoroquinolone-resistant isolates were 2-fold higher than those in fluoroquinolone-susceptible isolates (MIC50, 0.5 mg/liter versus 0.25 mg/liter; MIC90, 1 mg/liter versus 0.5 mg/liter, respectively). Two fluoroquinolone-resistant isolates (O25b:H4-ST131-H30R and O125:H37-ST48) were TGC resistant (MICs of 4 and 16 mg/liter, respectively), and four other isolates of O25b:H4-ST131-H30R and an isolate of O1-ST648 showed an intermediate interpretation (MIC, 2 mg/liter). No TGC-resistant/intermediate strains were found among the fluoroquinolone-susceptible isolates. The TGC-resistant/intermediate isolates expressed higher levels of acrA and acrB and had lower intracellular TGC concentrations than susceptible isolates, and they possessed mutations in acrR and/or marR. The MICs of acrAB-deficient mutants were markedly lower (0.25 mg/liter) than those of the parental strain. After continuous stepwise exposure to CIP in vitro, six of eight TGC-susceptible isolates had reduced TGC susceptibility. Two of them acquired TGC resistance (TGC MIC, 4 mg/liter) and exhibited expression of acrA and acrB and mutations in acrR and/or marR. In conclusion, a population of fluoroquinolone-resistant E. coli isolates, including major extraintestinal pathogenic lineages O25b:H4-ST131-H30R and O1-ST648, showed reduced susceptibility to TGC due to overexpression of the efflux pump AcrAB-TolC, leading to decreased intracellular concentrations of the antibiotics that may be associated with the development of fluoroquinolone resistance.


2015 ◽  
Vol 59 (10) ◽  
pp. 6087-6095 ◽  
Author(s):  
Amit Ranjan ◽  
Sabiha Shaik ◽  
Arif Hussain ◽  
Nishant Nandanwar ◽  
Torsten Semmler ◽  
...  

ABSTRACTEscherichia colisequence type 131 (ST131) is a pandemic clone associated with multidrug-resistant, extraintestinal infections, attributable to the presence of the CTX-M-15 extended-spectrum β-lactamase gene and mutations entailing fluoroquinolone resistance. Studies on subclones withinE. coliST131 are critically required for targeting and implementation of successful control efforts. Our study comprehensively analyzed the genomic and functional attributes of theH30-Rx subclonal strains NA097 and NA114, belonging to the ST131 lineage. We carried out whole-genome sequencing, comparative analysis, phenotypic virulence assays, and profiling of the antibacterial responses of THP1 cells infected with these subclones. Phylogenomic analysis suggested that the strains were clonal in nature and confined entirely to a single clade. Comparative genomic analysis revealed that the virulence and resistance repertoires were comparable among theH30-Rx ST131 strains except for the commensal ST131 strain SE15. Similarly, seven phage-specific regions were found to be strongly associated with theH30-Rx strains but were largely absent in the genome of SE15. Phenotypic analysis confirmed the virulence and resistance similarities between the two strains. However, NA097 was found to be more robust than NA114 in terms of virulence gene carriage (draoperon), invasion ability (P< 0.05), and antimicrobial resistance (streptomycin resistance). RT2gene expression profiling revealed generic upregulation of key proinflammatory responses in THP1 cells, irrespective of ST131 lineage status. In conclusion, our study provides comprehensive, genome-inferred insights into the biology and immunological properties of ST131 strains and suggests clonal diversification of genomic and phenotypic features within theH30-Rx subclone ofE. coliST131.


mSphere ◽  
2016 ◽  
Vol 1 (6) ◽  
Author(s):  
James R. Johnson ◽  
Brian Johnston ◽  
Paul Thuras ◽  
Bryn Launer ◽  
Evgeni V. Sokurenko ◽  
...  

ABSTRACT The ever-rising prevalence of resistance to first-line antibiotics among clinical Escherichia coli isolates leads to worse clinical outcomes and higher health care costs, thereby creating a need to discover its basis so that effective interventions can be developed. We found that the H30 subset within E. coli sequence type 131 (ST131-H30) is currently, and has been since at least 2004, the main E. coli lineage contributing to key resistance phenotypes—including extended-spectrum-beta-lactamase (ESBL) production, fluoroquinolone resistance, multidrug resistance, and dual ESBL production-plus-fluoroquinolone resistance—at a United States tertiary care center with a rising prevalence of ESBL-producing E. coli isolates. This identifies ST131-H30 as a target for diagnostic tests and preventive measures designed to curb the emergence of multidrug-resistant E. coli isolates and/or to blunt its clinical impact. The H30 strain of Escherichia coli sequence type 131 (ST131-H30) is a recently emerged, globally disseminated lineage associated with fluoroquinolone resistance and, via its H30Rx subclone, the CTX-M-15 extended-spectrum beta-lactamase (ESBL). Here, we studied the clonal background and resistance characteristics of 109 consecutive recent E. coli clinical isolates (2015) and 41 historical ESBL-producing E. coli blood isolates (2004 to 2011) from a public tertiary care center in California with a rising prevalence of ESBL-producing E. coli isolates. Among the 2015 isolates, ST131, which was represented mainly by ST131-H30, was the most common clonal lineage (23% overall). ST131-H30 accounted for 47% (8/17) of ESBL-producing, 47% (14/30) of fluoroquinolone-resistant, and 33% (11/33) of multidrug-resistant isolates. ST131-H30 also accounted for 53% (8/14) of dually fluoroquinolone-resistant, ESBL-producing isolates, with the remaining 47% comprised of diverse clonal groups that contributed a single isolate each. ST131-H30Rx, with CTX-M-15, was the major ESBL producer (6/8) among ST131-H30 isolates. ST131-H30 and H30Rx also dominated (46% and 37%, respectively) among the historical ESBL-producing isolates (2004 to 2011), without significant temporal shifts in relative prevalence. Thus, this medical center’s recently emerging ESBL-producing E. coli strains, although multiclonal, are dominated by ST131-H30 and H30Rx, which are the only clonally expanded fluoroquinolone-resistant, ESBL-producing lineages. Measures to rapidly and effectively detect, treat, and control these highly successful lineages are needed. IMPORTANCE The ever-rising prevalence of resistance to first-line antibiotics among clinical Escherichia coli isolates leads to worse clinical outcomes and higher health care costs, thereby creating a need to discover its basis so that effective interventions can be developed. We found that the H30 subset within E. coli sequence type 131 (ST131-H30) is currently, and has been since at least 2004, the main E. coli lineage contributing to key resistance phenotypes—including extended-spectrum-beta-lactamase (ESBL) production, fluoroquinolone resistance, multidrug resistance, and dual ESBL production-plus-fluoroquinolone resistance—at a United States tertiary care center with a rising prevalence of ESBL-producing E. coli isolates. This identifies ST131-H30 as a target for diagnostic tests and preventive measures designed to curb the emergence of multidrug-resistant E. coli isolates and/or to blunt its clinical impact.


mBio ◽  
2014 ◽  
Vol 5 (2) ◽  
Author(s):  
Dana Willner ◽  
Serene Low ◽  
Jason A. Steen ◽  
Narelle George ◽  
Graeme R. Nimmo ◽  
...  

ABSTRACTUrinary tract infections (UTIs) are one of the most commonly acquired bacterial infections in humans, and uropathogenicEscherichia colistrains are responsible for over 80% of all cases. The standard method for identification of uropathogens in clinical laboratories is cultivation, primarily using solid growth media under aerobic conditions, coupled with morphological and biochemical tests of typically a single isolate colony. However, these methods detect only culturable microorganisms, and characterization is phenotypic in nature. Here, we explored the genotypic identity of communities in acute uncomplicated UTIs from 50 individuals by using culture-independent amplicon pyrosequencing and whole-genome and metagenomic shotgun sequencing. Genus-level characterization of the UTI communities was achieved using the 16S rRNA gene (V8 region). Overall UTI community richness was very low in comparison to other human microbiomes. We strain-typedEscherichia-dominated UTIs using amplicon pyrosequencing of the fimbrial adhesin gene,fimH. There were nine highly abundantfimHtypes, and each UTI sample was dominated by a single type. Molecular analysis of the corresponding clinical isolates revealed that in the majority of cases the isolate was representative of the dominant taxon in the community at both the genus and the strain level. Shotgun sequencing was performed on a subset of eightE. coliurine UTI and isolate pairs. The majority of UTI microbial metagenomic sequences mapped to isolate genomes, confirming the results obtained using phylogenetic markers. We conclude that for the majority of acute uncomplicatedE. coli-mediated UTIs, single cultured isolates are diagnostic of the infection.IMPORTANCEIn clinical practice, the diagnosis and treatment of acute uncomplicated urinary tract infection (UTI) are based on analysis of a single bacterial isolate cultured from urine, and it is assumed that this isolate represents the dominant UTI pathogen. However, these methods detect only culturable bacteria, and the existence of multiple pathogens as well as strain diversity within a single infection is not examined. Here, we explored bacteria present in acute uncomplicated UTIs using culture-independent sequence-based methods.Escherichia coliwas the most common organism identified, and analysis ofE. colidominant UTI samples and their paired clinical isolates revealed that in the majority of infections the cultured isolate was representative of the dominant taxon at both the genus and the strain level. Our data demonstrate that in most cases single cultured isolates are diagnostic of UTI and are consistent with the notion of bottlenecks that limit strain diversity during UTI pathogenesis.


2015 ◽  
Vol 59 (3) ◽  
pp. 1718-1727 ◽  
Author(s):  
Elisabeth Thulin ◽  
Martin Sundqvist ◽  
Dan I. Andersson

ABSTRACTAmdinocillin (mecillinam) is a β-lactam antibiotic that is used mainly for the treatment of uncomplicated urinary tract infections. The objectives of this study were to identify mutations that confer amdinocillin resistance on laboratory-isolated mutants and clinical isolates ofEscherichia coliand to determine why amdinocillin resistance remains rare clinically even though resistance is easily selected in the laboratory. Under laboratory selection, frequencies of mutation to amdinocillin resistance varied from 8 × 10−8to 2 × 10−5per cell, depending on the concentration of amdinocillin used during selection. Several genes have been demonstrated to give amdinocillin resistance, but here eight novel genes previously unknown to be involved in amdinocillin resistance were identified. These genes encode functions involved in the respiratory chain, the ribosome, cysteine biosynthesis, tRNA synthesis, and pyrophosphate metabolism. The clinical isolates exhibited significantly greater fitness than the laboratory-isolated mutants and a different mutation spectrum. ThecysBgene was mutated (inactivated) in all of the clinical isolates, in contrast to the laboratory-isolated mutants, where mainly other types of more costly mutations were found. Our results suggest that the frequency of mutation to amdinocillin resistance is high because of the large mutational target (at least 38 genes). However, the majority of these resistant mutants have a low growth rate, reducing the probability that they are stably maintained in the bladder. Inactivation of thecysBgene and a resulting loss of cysteine biosynthesis are the major mechanism of amdinocillin resistance in clinical isolates ofE. coli.


2015 ◽  
Vol 59 (4) ◽  
pp. 1962-1968 ◽  
Author(s):  
Sun Hee Park ◽  
Su-Mi Choi ◽  
Dong-Gun Lee ◽  
Sung-Yeon Cho ◽  
Hyo-Jin Lee ◽  
...  

ABSTRACTExtended-spectrum β-lactamase-producingEscherichia coli(ESBL-EC) is increasingly identified as a cause of acute pyelonephritis (APN) among patients without recent health care contact, i.e., community-associated APN. This case-control study compared 75 cases of community-associated ESBL-EC APN (CA-ESBL) to 225 controls of community-associated non-ESBL-EC APN (CA-non-ESBL) to identify the risk factors for ESBL-EC acquisition and investigate the impact of ESBL on the treatment outcomes of community-associated APN (CA-APN) caused byE. coliat a Korean hospital during 2007 to 2013. The baseline characteristics were similar between the cases and controls; the risk factors for ESBL-EC were age (>55 years), antibiotic use within the previous year, and diabetes with recurrent APN. The severity of illness did not differ between CA-ESBL and CA-non-ESBL (Acute Physiology and Chronic Health Evaluation [APACHE] II scores [mean ± standard deviation], 7.7 ± 5.9 versus 6.4 ± 5.3;P= 0.071). The proportions of clinical (odds ratio [OR], 1.76; 95% confidence interval [CI], 0.57 to 5.38;P= 0.323) and microbiological (OR, 1.16; 95% CI, 0.51 to 2.65;P= 0.730) cures were similar, although the CA-ESBL APN patients were less likely to receive appropriate antibiotics within 48 h. A multivariable Cox proportional hazards analysis of the prognostic factors for CA-APN caused byE. colishowed that ESBL production was not a significant factor for clinical (hazard ratio [HR], 0.39; 95% CI, 0.12 to 1.30;P= 0.126) or microbiological (HR, 0.49; 95% CI, 0.21 to 1.12;P= 0.091) failure. The estimates did not change after incorporating weights calculated using propensity scores for acquiring ESBL-EC. Therefore, ESBL production did not negatively affect treatment outcomes among patients with community-associatedE. coliAPN.


2014 ◽  
Vol 58 (12) ◽  
pp. 7240-7249 ◽  
Author(s):  
Arif Hussain ◽  
Amit Ranjan ◽  
Nishant Nandanwar ◽  
Anshu Babbar ◽  
Savita Jadhav ◽  
...  

ABSTRACTIn view of the epidemiological success of CTX-M-15-producing lineages ofEscherichia coliand particularly of sequence type 131 (ST131), it is of significant interest to explore its prevalence in countries such as India and to determine if antibiotic resistance, virulence, metabolic potential, and/or the genetic architecture of the ST131 isolates differ from those of non-ST131 isolates. A collection of 126E. coliisolates comprising 43 ST131E. coli, 40 non-ST131E. coli, and 43 fecalE. coliisolates collected from a tertiary care hospital in India was analyzed. These isolates were subjected to enterobacterial repetitive intergenic consensus (ERIC)-based fingerprinting, O typing, phylogenetic grouping, antibiotic sensitivity testing, and virulence and antimicrobial resistance gene (VAG) detection. Representative isolates from this collection were also analyzed by multilocus sequence typing (MLST), conjugation, metabolic profiling, biofilm production assay, and zebra fish lethality assay. All of the 43 ST131E. coliisolates were exclusively associated with phylogenetic group B2 (100%), while most of the clinical non-ST131 and stool non-ST131E. coliisolates were affiliated with the B2 (38%) and A (58%) phylogenetic groups, respectively. Significantly greater proportions of ST131 isolates (58%) than non-ST131 isolates (clinical and stoolE. coliisolates, 5% each) were technically identified to be extraintestinal pathogenicE. coli(ExPEC). The clinical ST131, clinical non-ST131, and stool non-ST131E. coliisolates exhibited high rates of multidrug resistance (95%, 91%, and 91%, respectively), extended-spectrum-β-lactamase (ESBL) production (86%, 83%, and 91%, respectively), and metallo-β-lactamase (MBL) production (28%, 33%, and 0%, respectively). CTX-M-15 was strongly linked with ESBL production in ST131 isolates (93%), whereas CTX-M-15 plus TEM were present in clinical and stool non-ST131E. coliisolates. Using MLST, we confirmed the presence of two NDM-1-positive ST131E. coliisolates. The aggregate bioscores (metabolite utilization) for ST131, clinical non-ST131, and stool non-ST131E. coliisolates were 53%, 52%, and 49%, respectively. The ST131 isolates were moderate biofilm producers and were more highly virulent in zebra fish than non-ST131 isolates. According to ERIC-based fingerprinting, the ST131 strains were more genetically similar, and this was subsequently followed by the genetic similarity of clinical non-ST131 and stool non-ST131E. colistrains. In conclusion, our data provide novel insights into aspects of the fitness advantage ofE. colilineage ST131 and suggest that a number of factors are likely involved in the worldwide dissemination of and infections due to ST131E. coliisolates.


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