Rapid Emergence, Subsidence, and Molecular Detection of Escherichia coli Sequence Type 1193- fimH64, a New Disseminated Multidrug-Resistant Commensal and Extraintestinal Pathogen

Abstract

Escherichia coli sequence type 1193 (ST1193) is an emerging multidrug-resistant pathogen. We performed longitudinal and cross-sectional surveillance for ST1193 among clinical and fecal E. coli isolates from Minneapolis Veterans Affairs Medical Center (VAMC) patients and their household members, other Minnesota centers, and national VAMCs and compared these ST1193 isolates with archival human and canine ST1193 isolates from Australia (2008). We also developed and extensively validated a novel multiplex PCR assay for ST1193 and its characteristic fimH64 (type 1 fimbrial adhesin) allele. We found that ST1193-H64 (where "H64" refers to a phylogenetic subdivision within ST1193 that is characterized by the fimH64 allele), which was uniformly fluoroquinolone resistant, appeared to emerge in the United States in a geographically staggered fashion beginning around 2011. Its prevalence among clinical and fecal E. coli isolates at the Minneapolis VAMC rose rapidly beginning in 2013, peaked in early 2017, and then plateaued or declined. In comparison with other ST14 complex (STc14) isolates, ST1193-H64 isolates were more extensively multidrug resistant, whereas their virulence genotypes were less extensive but included (uniquely) K1 capsule and fimH64 Pulsed-field gel electrophoresis separated ST1193-H64 isolates from other STc14 isolates and showed genetic commonality between archival Australian versus recent U.S. isolates, fecal versus clinical isolates, and human versus canine isolates. Three main ST1193 pulsotypes differed significantly in resistance profiles and capsular types; emergent pulsotype 2123 was associated with trimethoprim-sulfamethoxazole resistance and K1 (versus K5) capsule. These findings clarify ST1193-H64's temporal prevalence trends as a fluoroquinolone-resistant pathogen and commensal; document clonal subsets with distinctive geographic, temporal, resistance, and virulence gene associations; and establish a new laboratory tool for rapid and simple detection of ST1193-H64.

Keywords: Escherichia coli; PCR; ST1193; antimicrobial resistance; fluoroquinolone resistance; intestinal colonization; molecular epidemiology; surveillance; veterinary epidemiology; zoonotic infections.

FIG 1

Prevalence of FQ-R E. coli variants among clinical isolates and human volunteers. (A) Clinical isolates (6,569) at the MVAMC. (B) Fecal surveillance subjects (MVAMC veterans and their household members). H30R, prevalence of the ST131-H30R subclone; ST1193, prevalence of ST1193-H64; ST1193/FQ-R, prevalence of ST1194-H64 among FQ-R E. coli clinical isolates (A) or FQ-R E. coli-colonized subjects (B). P values not preceded by Δ are for the respective curve or curve segment’s fit to a chi-squared test for linear trend; those preceded by Δ are for the change in slope at the inflection point, according to multivariable logistic regression analysis. The vertical lines mark inflection points used to define curve segment boundaries (i.e., ST1193 and ST1193/FQ-R) for analyses of segmental slope and change in slope. Curves without a vertical line (i.e., FQ-R and H30R) were analyzed in total. P values are shown where P is less than 0.10. NS, nonsignificant (P ≥ 0.10). Numbers of isolates (top) or subjects (bottom) per year are shown below the x axis.