Sequence type 131 fimH30 and fimH41 subclones amongst Escherichia coli isolates in Australia and New Zealand
Introduction
Using contemporary molecular typing techniques, a broad picture of the genetic diversity of Escherichia coli causing urinary tract infections (UTIs) and other invasive infections is beginning to emerge. Recent studies have demonstrated that collections of E. coli from urine and blood are largely clonal in composition [1], [2], [3], [4]. These clonal components invariably include the global pandemic clone, sequence type 131 (ST131) E. coli, as well as other frequently described uropathogenic E. coli (e.g. ST95, ST69, ST73 and ST127). ST131 E. coli has been implicated as a major contributor to fluoroquinolone-resistant and expanded-spectrum cephalosporin-resistant E. coli (ESC-R-EC) infections globally [5].
Clinical and epidemiological risk factors for colonisation or infection with these clones, in particular ST131, have been difficult to define. Recently identified risk factors for ST131 include long-term care facility (LTCF) residence or bedridden status [6], [7], [8], exposure to antimicrobials [6], ethnicity [9], female sex [8], age [6], [8] and infection characteristics [6], [10].
In Australia and New Zealand, a range of ST131 clones have been identified amongst animals as well as humans from a variety of patient groups [11], [12], [13], [14], [15], [16]. Few facets of epidemiology have been investigated, with one study reporting no difference between the co-morbidities of patients infected with ST131 and non-ST131 E. coli following prostate biopsy [17], and another demonstrating some possible sharing of ST131 clones between human and companion animals [18]. There have been no population estimates of prevalence.
We previously described risk factors for community-onset ESC-R-EC in Australia and New Zealand. These risk factors included healthcare contact, travel to high-risk regions (Indian subcontinent, Southeast Asia, China, Africa and the Middle East), trimethoprim ± sulfamethoxazole and/or expanded-spectrum cephalosporin use (ceftriaxone, ceftazidime or cefepime), UTI in the previous year, and birth on the Indian subcontinent. We also demonstrated that ST131 E. coli was spread broadly in our region, although with a relatively uncommon distribution. It resided almost exclusively amongst ESC-R-EC, where the prevalence was 45% compared with 7% amongst expanded-spectrum cephalosporin-susceptible E. coli (ESC-S-EC) isolates. In addition, there was a non-significant difference in the proportion containing blaCTX-M-9 group and blaCTX-M-1 group enzymes [19].
The aim of this follow-up study was to define the clonal composition and molecular characteristics of community-onset ESC-S-EC and ESC-R-EC infections. A further aim was to understand the subclonality of ST131 and to elucidate factors that may influence the distribution of the ST131 worldwide pandemic in our region. To do this, epidemiological data, collected as part of a case–control study, were combined with genetic characterisation of E. coli isolates from the study patients.
Section snippets
Clinical data and bacterial isolates
All bacterial isolates and clinical data are from The COOEE Study (COmmunity Onset ESBL and AmpC E. coli Study), a multisite case–control study with prospective recruitment of patients and data collection. The study has been described in detail elsewhere [19]. In brief, six geographically dispersed tertiary centres in Australia (n = 5) and New Zealand (n = 1) recruited patients over a 9–12-month period during 2011 and 2012. In total, 182 patients (91 ESC-R-EC cases and 91 ESC-S-EC controls) were
Results
In total, 179 bacterial isolates were included in this study (89 ESC-R-EC and 90 ESC-S-EC). Bacteraemia was detected in 29 patients (16%), with the remainder having isolated urine cultures. All isolates were community-onset, including 2/179 (1.1%) originating from residents of LTCFs.
Discussion
This study provides the first comprehensive molecular epidemiological profile of susceptible and resistant E. coli in our region. Previous studies in our region have investigated selected groups such as fluoroquinolone resistance or particular clonal groups, limiting their ability to ascertain a broad profile [13], [18].
At first glance, the global pandemic clone ST131 appears to be dominant in our population. However, this must be seen in the perspective of local rates of ESC-R-EC (Fig. 4). Our
Conclusion
We delineate a markedly different clonal composition between ESC-S-EC and ESC-R-EC groups in Australia and New Zealand. Overall, ST131 is less frequent than in other regions of the world. The fluoroquinolone-susceptible H41 subclone of ST131 is most prevalent, although the H30 subclone dominates ESC-R-EC. ST131 was significantly associated with upper UTI presentation, suggesting enhanced virulence. We hypothesise that the factors contributing to the low background rate of
Acknowledgments
The authors would like to thank the clinical and microbiology laboratory staff at all sites who have made significant contributions to this study. The authors also thank Anna Sartor and Wan Keat Yam for their laboratory work, Makrina Totsika for advice on fimH typing, and Scott Weissman for provision of reference fimH sequences.
Funding: The laboratory component of this work was supported by a grant from The Royal Brisbane and Women's Hospital Foundation (Herston, Queensland, Australia). Use of
References (39)
- et al.
Distribution of phylogenetic groups, sequence type ST131, and virulence-associated traits among Escherichia coli isolates from men with pyelonephritis or cystitis and healthy controls
Clin Microbiol Infect
(2013) - et al.
Clonal composition and community clustering of drug-susceptible and -resistant Escherichia coli isolates from bloodstream infections
Antimicrob Agents Chemother
(2013) - et al.
Molecular epidemiology of extraintestinal pathogenic Escherichia coli isolates from a regional cohort of elderly patients highlights the prevalence of ST131 strains with increased antimicrobial resistance in both community and hospital care settings
J Antimicrob Chemother
(2011) - et al.
Epidemic clonal groups of Escherichia coli as a cause of antimicrobial-resistant urinary tract infections in Canada, 2002 to 2004
Antimicrob Agents Chemother
(2009) - et al.
Escherichia coli sequence type 131 (ST131) subclone H30 as an emergent multidrug-resistant pathogen among US veterans
Clin Infect Dis
(2013) - et al.
Escherichia coli O25b–ST131: a pandemic, multiresistant, community-associated strain
J Antimicrob Chemother
(2011) - et al.
Escherichia coli sequence type 131 is a dominant, antimicrobial-resistant clonal group associated with healthcare and elderly hosts
Infect Control Hosp Epidemiol
(2013) - et al.
Different factors associated with CTX-M-producing ST131 and non-ST131 Escherichia coli clinical isolates
PLOS ONE
(2013) - et al.
Escherichia coli belonging to the worldwide emerging epidemic clonal group O25b/ST131: risk factors and clinical implications
J Antimicrob Chemother
(2014) - et al.
Prevalence of ST131 among fluoroquinolone-resistant Escherichia coli obtained from rectal swabs before transrectal prostate biopsy
Urology
(2013)
Bacteremia caused by extended-spectrum-β-lactamase-producing Escherichia coli sequence type ST131 and non-ST131 clones: comparison of demographic data, clinical features, and mortality
Antimicrob Agents Chemother
Escherichia coli ST131 producing CTX-M-15 in Australia
J Antimicrob Chemother
Clonal group distribution of fluoroquinolone-resistant Escherichia coli among humans and companion animals in Australia
J Antimicrob Chemother
Escherichia coli sequence type 131 as a prominent cause of antibiotic resistance among urinary Escherichia coli isolates from reproductive-age women
J Clin Microbiol
Genotypic and phenotypic characterization of Escherichia coli isolates from children with urinary tract infection and from healthy carriers
Pediatr Infect Dis J
Escherichia coli bloodstream infection after transrectal ultrasound-guided prostate biopsy: implications of fluoroquinolone-resistant sequence type 131 as a major causative pathogen
Clin Infect Dis
Clinical and molecular correlates of virulence in Escherichia coli causing bloodstream infection following transrectal ultrasound-guided (TRUS) prostate biopsy
J Antimicrob Chemother
Commonality among fluoroquinolone-resistant sequence type ST131 extraintestinal Escherichia coli isolates from humans and companion animals in Australia
Antimicrob Agents Chemother
Community-onset Escherichia coli infection resistant to expanded-spectrum cephalosporins in low-prevalence countries
Antimicrob Agents Chemother
Cited by (19)
Extended-spectrum β-lactamase- and AmpC β-lactamase-producing Enterobacterales associated with urinary tract infections in the New Zealand community: a case-control study
2023, International Journal of Infectious DiseasesPhylogenetic and antibiotics resistance in extended-spectrum B-lactamase (ESBL) Uropathogenic Escherichia coli: An update review
2021, Gene ReportsCitation Excerpt :One study demonstrated no significant difference between the co-mortality of patients without ST131 and ST131 E. coli following prostate biopsy (Williamson et al., 2013). Rogers et al. (Rogers et al., 2015) indicated that the H30 and ST131 subclones were higher among ESBL resistant E. coli and expanded-spectrum cephalosporin-resistant (ESC-R-EC) in New Zealand and Australia. UPECs, members of extra-intestinal pathogenic E. coli (EXPE) and classic pandemic EXPEC clones, have been identified via multi-locus sequence typing (MLST), ST69, ST73, ST393, ST131 and ST95 (Riley, 2014).
Extra-intestinal pathogenic Escherichia coli (ExPEC): Disease, carriage and clones
2015, Journal of InfectionCitation Excerpt :ExPEC ST131 was first reported in 2008 and is now considered a pathogen of global importance.85 Recent molecular epidemiological studies have revealed a number of ST131 clonal subgroups associated with variable antimicrobial resistance patterns, the most prevalent being ST131 clonal subgroup H30 (contains the H30 variant of fimH).86–88 A number of ST131 H30 subgroups, mainly H30-R (encodes fluoroquinolone resistance), H30 (non-R) and H30-Rx (encodes fluoroquinolone resistance and produces CTX-M-15 ESBL), have subsequently evolved through a process of clonal selection from a common ST131 H30 ancestor (see Fig. 2).88–90