Genomic Surveillance of Ceftriaxone-Resistant Escherichia coli in Western New York Suggests the Extended-Spectrum β-Lactamase bla(CTX-M-27) Is Emerging on Distinct Plasmids in ST38

Extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae pose significant treatment and infection prevention challenges. Escherichia coli sequence type (ST) 131 associated with the bla(CTX-M-15) gene has been the dominant lineage of ESBL-producing E. coli in the US and worldwide. In this study, our objective was to determine the β-lactamase profile, means of dissemination, prevalence, and the clonal identity of ESBL-producing E. coli in our region of Western New York. Whole-genome SNP-based phylogenomics was used to assess 89 ceftriaxone-resistant (CTR) E. coli. Isolates were collected from both inpatients and outpatients and from urine and sterile-sites over a 2 month period in 2017 or throughout the year, respectively. ST131 was the predominant ST (46.0%), followed by ST38 (15.7%). The bla(CTX-M-15) gene was commonly found in 53.7% of ST131 isolates, whereas the bla(CTX-M-27) gene was found in 26.8% of ST131, though was significantly associated with ST38, and was found in 71.4% of those strains. When compared to ST131, ST38 E. coli exhibited increased frequency of resistance to nitrofurantoin and decreased frequency of resistance to ciprofloxacin and ampicillin-sulbactam. Using Nanopore long-read sequencing technology, an analysis of the ESBL genetic context showed that the bla(CTX-M-15) gene was chromosomal in 68.2% of ST131, whereas the bla(CTX-M-27) gene was plasmid-borne in all ST131 and 90% of ST38 isolates. Notably, the bla(CTX-M-27) gene in ST38 resided on highly-related (99.0–100.0% identity and 65.0–98.0% query coverage) conjugative IncF plasmids of distinct plasmid multi-locus sequence types (pMLSTs) from those in ST131. Furthermore, ST131 and ST38 were found to harbor different antibiotic resistance gene and virulence factor profiles. These findings raise the possibility of an emerging ESBL-producing E. coli lineage in our region.