Molecular epidemiological analysis of Escherichia coli sequence type ST131 (O25:H4) and blaCTX-M-15 among extended-spectrum-β-lactamase-producing E. coli from the United States, 2000 to 2009

Abstract

Escherichia coli sequence type ST131 (from phylogenetic group B2), often carrying the extended-spectrum-β-lactamase (ESBL) gene bla(CTX-M-15), is an emerging globally disseminated pathogen that has received comparatively little attention in the United States. Accordingly, a convenience sample of 351 ESBL-producing E. coli isolates from 15 U.S. centers (collected in 2000 to 2009) underwent PCR-based phylotyping and detection of ST131 and bla(CTX-M-15). A total of 200 isolates, comprising 4 groups of 50 isolates each that were (i) bla(CTX-M-15) negative non-ST131, (ii) bla(CTX-M-15) positive non-ST131, (iii) bla(CTX-M-15) negative ST131, or (iv) bla(CTX-M-15) positive ST131, also underwent virulence genotyping, antimicrobial susceptibility testing, and pulsed-field gel electrophoresis (PFGE). Overall, 201 (57%) isolates exhibited bla(CTX-M-15), whereas 165 (47%) were ST131. ST131 accounted for 56% of bla(CTX-M-15)-positive- versus 35% of bla(CTX-M-15)-negative isolates (P < 0.001). Whereas ST131 accounted for 94% of the 175 total group B2 isolates, non-ST131 isolates were phylogenetically distributed by bla(CTX-M-15) status, with groups A (bla(CTX-M-15)-positive isolates) and D (bla(CTX-M-15)-negative isolates) predominating. Both bla(CTX-M-15) and ST131 occurred at all participating centers, were recovered from children and adults, increased significantly in prevalence post-2003, and were associated with molecularly inferred virulence. Compared with non-ST131 isolates, ST131 isolates had higher virulence scores, distinctive virulence profiles, and more-homogeneous PFGE profiles. bla(CTX-M-15) was associated with extensive antimicrobial resistance and ST131 with fluoroquinolone resistance. Thus, E. coli ST131 and bla(CTX-M-15) are emergent, widely distributed, and predominant among ESBL-positive E. coli strains in the United States, among children and adults alike. Enhanced virulence and antimicrobial resistance have likely promoted the epidemiological success of these emerging public health threats.

Fig 1

Principal coordinate analysis of virulence genotype data (upper panel) and antimicrobial resistance data (lower panel) among 200 Escherichia coli isolates (collected in 2000 to 2009) in relation to ST131 and bla_CTX-M-15 status. Populations 1 to 4 correspond to the groups shown in the tables (i.e., Table 1, non-ST131 bla_CTX-M-15 negative; Table 2, non-ST131 bla_CTX-M-15 positive; Table 3, ST131 bla_CTX-M-15 negative; Table 4, ST131 bla_CTX-M-15 positive). Upper panel (virulence genotypes): coordinates 1 and 2 capture 58% and 12% of total variation, respectively. Note the marked separation of (overlapping) populations 1 and 2 from (overlapping) populations 3 and 4. Lower panel (antimicrobial resistance): coordinates 1 and 2 capture 32% and 26% of total variation, respectively. Note the marked overlap of all four populations.