Molecular analysis of blaSHV, blaTEM, and blaCTX-M in extended-spectrum β-lactamase producing Enterobacteriaceae recovered from fecal specimens of animals

PLoS One. 2021 Jan 7;16(1):e0245126. doi: 10.1371/journal.pone.0245126. eCollection 2021.

Abstract

Colonization of extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae as animal gut microbiota is a substantial global threat. This study aimed to determine the molecular characterization of blaSHV, blaTEM, and blaCTX-M variants in animals, as well as to evaluate the antimicrobial resistance conferred by these genes. We prospectively analyzed 1273 fecal specimens of farm and domestic animals for the isolation of enterobacteria that had the ESBL phenotype by using biochemical methods. The extracted genes were amplified by polymerase chain reaction and sequenced for the characterization of blaSHV, blaTEM, and blaCTX-M variants. The drug-resistance spectrum and hierarchical clusters were analyzed against 19 antibacterial agents. Out of 245 (19.2%) ESBL enterobacteria, 180 (75.5%) Escherichia coli and 34 (13.9%) Klebsiella pneumoniae were prevalent species. A total of 73.9% blaCTX-M, 26.1% blaTEM, and 14.2% blaSHV were found among the enterobacteria; however, their association with farm or domestic animals was not statistically significant. The distribution of bla gene variants showed the highest number of blaCTX-M-1 (133; 54.3%), followed by blaCTX-M-15 (28; 11.4%), blaTEM-52 (40; 16.3%), and blaSHV-12 (22; 9%). In addition, 84.5% of the enterobacteria had the integrons intI1. We observed ±100% enterobacteria resistant to cephalosporin, 7 (2.9%) to colistin (minimum inhibitory concentration breakpoint ≥4 μg/mL), 9 (3.7%) to piperacillin-tazobactam, 11 (4.5%) to imipenem, 14 (5.7%) to meropenem, and 18 (7.3%) to cefoperazone-sulbactam, without statistically significant association. Animal gut microbiota contain a considerable number of blaCTX-M, blaTEM, blaSHV, and integrons, which are a potential source of acquired extensive drug resistance in human strains and leaves fewer therapeutic substitutes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Bacterial Agents / pharmacology
  • Bacterial Proteins / genetics*
  • Drug Resistance, Multiple, Bacterial / genetics*
  • Escherichia coli / classification
  • Escherichia coli / enzymology
  • Escherichia coli / genetics*
  • Escherichia coli / isolation & purification
  • Feces / microbiology*
  • Gastrointestinal Microbiome
  • Humans
  • Klebsiella pneumoniae / classification
  • Klebsiella pneumoniae / enzymology
  • Klebsiella pneumoniae / genetics*
  • Klebsiella pneumoniae / isolation & purification
  • beta-Lactam Resistance / genetics*
  • beta-Lactamases / genetics*

Substances

  • Anti-Bacterial Agents
  • Bacterial Proteins
  • beta-Lactamases

Grants and funding

HE received the award. The study was supported by the Deanship of Scientific Research, Jouf University, Al Jouf, Saudi Arabia, through project No. 47/40. Most of the authors are Jouf University employees, so the study design, data collection, and analysis, decision to publish, or preparation of the manuscript is contributed through the employees. https://www.ju.edu.sa/en/home/.