Whole-genome sequence analysis of CTX-M containing Escherichia coli isolates from retail meats and cattle in the United States

Authors: TADESSE, DANIEL - Food And Drug Administration(FDA); LI, C - Food And Drug Administration(FDA); MUKHERJEE, S - Food And Drug Administration(FDA); HSU, C - Food And Drug Administration(FDA); BODEIS-JONES, S - Food And Drug Administration(FDA); GAINES, S - Food And Drug Administration(FDA); KABERA, C - Food And Drug Administration(FDA); LONERAGAN, G - Texas Tech University; TORRENCE, M - Food And Drug Administration(FDA); Harhay, Dayna; MCDERMOTT, P - Food And Drug Administration(FDA); ZHAO, S - Food And Drug Administration(FDA)

Submitted to: Microbial Drug Resistance
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/1/2018
Publication Date: 9/1/2018
Citation: Tadesse, D.A., Li, C., Mukherjee, S., Hsu, C., Bodeis Jones, S., Gaines, S.A., Kabera, C., Loneragan, G.H., Torrence, M., Harhay, D.M., McDermott, P.F., Zhao, S. 2018. Whole-genome sequence analysis of CTX-M containing Escherichia coli isolates from retail meats and cattle in the United States. Microbial Drug Resistance. 24(7):939-948. https://doi.org/10.1089/mdr.2018.0206.
DOI: https://doi.org/10.1089/mdr.2018.0206

Interpretive Summary: Extended spectrum beta-lactamases (ESBLs) are a group of enzymes that confer resistance to certain medically important antibiotics. One of the most common ESBL enzymes circulating world-wide is blaCTX-M which has rapidly increased in prevalence in clinical populations in the U.S., however few CTX-M ESBLs have been reported from food animals and animal products. The National Antimicrobial Resistance Monitoring System (NARMS) monitors foodborne bacteria associated with animals and animal products, for changes in resistance to medically important antimicrobials. Here we report on the prevalence and genetic characterization of ESBL producing Escherichia coli isolated from cattle and retail meat samples collected through the NARMS program between 2011 and 2015. Screening of 8,721 E. coli isolates resulted in the identification of 17 CTX-M ESBL producing E. coli. Genome sequence analysis revealed that three of these isolates (one each respectively from retail pork, beef and turkey samples) carried rare variants of CTX-M which have not previously been identified in U.S. retail meats. The data presented increase our understanding of CTX-M carrying E. coli isolates in food animals and animal products. They also highlight the rare occurrence of this type of ESBL in E. coli isolated from U.S. food animal and retail meats, with only 0.2% of samples tested found to carry CTX-M.

Technical Abstract: In recent years, there have been increased reports on the detection of extended-spectrum beta-lactamase (ESBL)- producing Escherichia coli and Salmonella strains from food-producing animals and animal products in the United States. We characterized 18 ESBL E. coli isolates from cattle (n = 5), chicken breast (n = 5), ground turkey (n = 6), ground beef (n = 1), and pork chops (n = 1) that were collected by the National Antimicrobial Resistance Monitoring System (NARMS) between 2011 and 2015. In vitro antimicrobial susceptibility testing was done against a panel of 14 antimicrobials followed by a secondary panel of 9 b-lactam agents. Whole-genome sequencing was used to characterize the resistome, plasmids, and the genetic structures of the ESBL genes. All ESBL-producing E. coli isolates were resistant to at least three antimicrobial classes and carried various blaCTX-M genes. Most of the cattle and ground turkey isolates carried blaCTX-M-27. In chicken breast isolates, blaCTX-M-1 was present as part of an ISEcp1 transposition unit carried on a plasmid that shares sequence similarity with the backbone structure of the IncI plasmid. Isolates carrying the blaCTX-M-14 and blaCTX-M-15 genes, widely distributed in human clinical isolates, were also isolated. To our knowledge, this is the first report of the widely distributed blaCTX-M-14 and blaCTX-M-15 in E. coli isolates from retail meat samples in the United States. Different insertional sequences were identified upstream of these blaCTX-Ms, including ISEcp1, IS26, and IS903-D. CTX-Min E. coli from food animals and retail chicken breast were often present on plasmids with other resistance genes. Other resistance genes identified included aadA, strA, strB, aac(3)-IId, aac(3)-VIa, aph(3¢)-Ic, blaTEM, blaHERA-3, floR, sul1, sul2, catA1, tetA, tetB, dfrA, and qacE. These data describe the emergence of CTX-M-carrying E. coli isolates in food animals and animal products monitored by NARMS program.