Rapid emergence, subsidence, and molecular detection of Escherichia coli sequence type 1193-fimH64, a new disseminated multidrug-resistant commensal and extraintestinal pathogen

James R Johnson, Brian D Johnston, Stephen B. Porter, Connie Clabots, Tricia L. Bender, Paul Thuras, Darren J. Trott, Rowland Cobbold, Joanne Mollinger, Patricia Ferrieri, Sarah Drawz, Ritu Banerjee

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Article numbere01664-18
JournalJournal of clinical microbiology
Volume57
Issue number5
DOIs
StatePublished - May 1 2019

Fingerprint

Fluoroquinolones
Veterans
Escherichia coli
Capsules
Virulence
Canidae
Bacterial Adhesins
Trimethoprim Resistance
Alleles
Pulsed Field Gel Electrophoresis
Multiplex Polymerase Chain Reaction
Sulfamethoxazole Drug Combination Trimethoprim
Genotype
Genes

Keywords

  • Antimicrobial resistance
  • Escherichia coli
  • Fluoroquinolone resistance
  • Intestinal colonization
  • Molecular epidemiology
  • PCR
  • ST1193
  • Surveillance
  • Veterinary epidemiology
  • Zoonotic infections

Cite this

Rapid emergence, subsidence, and molecular detection of Escherichia coli sequence type 1193-fimH64, a new disseminated multidrug-resistant commensal and extraintestinal pathogen. / Johnson, James R; Johnston, Brian D; Porter, Stephen B.; Clabots, Connie; Bender, Tricia L.; Thuras, Paul; Trott, Darren J.; Cobbold, Rowland; Mollinger, Joanne; Ferrieri, Patricia; Drawz, Sarah; Banerjee, Ritu.

In: Journal of clinical microbiology, Vol. 57, No. 5, e01664-18, 01.05.2019.

Research output: Contribution to journalArticle

Johnson, James R ; Johnston, Brian D ; Porter, Stephen B. ; Clabots, Connie ; Bender, Tricia L. ; Thuras, Paul ; Trott, Darren J. ; Cobbold, Rowland ; Mollinger, Joanne ; Ferrieri, Patricia ; Drawz, Sarah ; Banerjee, Ritu. / Rapid emergence, subsidence, and molecular detection of Escherichia coli sequence type 1193-fimH64, a new disseminated multidrug-resistant commensal and extraintestinal pathogen. In: Journal of clinical microbiology. 2019 ; Vol. 57, No. 5.
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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.",
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AU - Thuras, Paul

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AB - 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.

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