Sequence type 131 fimH30 and fimH41 subclones amongst Escherichia coli isolates in Australia and New Zealand

https://doi.org/10.1016/j.ijantimicag.2014.11.015Get rights and content

Highlights

  • Escherichia coli causing urinary tract infections may originate from virulent clones.

  • Sequence type 131 (ST131) is a virulent and antimicrobial-resistant clone of E. coli.

  • We have characterised clonality, focusing on ST131 and its subclones, amongst E. coli in Australia and New Zealand.

  • ST131 is prevalent in antimicrobial resistant E. coli in Australia and New Zealand.

  • Characterised by fimH typing, ST131 has a unique epidemiology in Australia and New Zealand.

Abstract

The clonal composition of Escherichia coli causing extra-intestinal infections includes ST131 and other common uropathogenic clones. Drivers for the spread of these clones and risks for their acquisition have been difficult to define. In this study, molecular epidemiology was combined with clinical data from 182 patients enrolled in a case–control study of community-onset expanded-spectrum cephalosporin-resistant E. coli (ESC-R-EC) in Australia and New Zealand. Genetic analysis included antimicrobial resistance mechanisms, clonality by DiversiLab (rep-PCR) and multilocus sequence typing (MLST), and subtyping of ST131 by identification of polymorphisms in the fimH gene. The clonal composition of expanded-spectrum cephalosporin-susceptible E. coli and ESC-R-EC isolates differed, with six MLST clusters amongst susceptible isolates (median 7 isolates/cluster) and three clusters amongst resistant isolates, including 40 (45%) ST131 isolates. Population estimates indicate that ST131 comprises 8% of all E. coli within our population; the fluoroquinolone-susceptible H41 subclone comprised 4.5% and the H30 subclone comprised 3.5%. The H30 subclone comprised 39% of all ESC-R-EC and 41% of all fluoroquinolone-resistant E. coli within our population. Patients with ST131 were also more likely than those with non-ST131 isolates to present with an upper than lower urinary tract infection (RR = 1.8, 95% CI 1.01–3.1). ST131 and the H30 subclone were predominant amongst ESC-R-EC but were infrequent amongst susceptible isolates where the H41 subclone was more prevalent. Within our population, the proportional contribution of ST131 to fluoroquinolone resistance is comparable with that of other regions. In contrast, the overall burden of ST131 is low by global standards.

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

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