Occurrence of multi-carbapenemase-producing Enterobacterales in a tertiary hospital in Madrid (Spain): A new epidemiologic scenario

J Glob Antimicrob Resist. 2024 Sep:38:281-291. doi: 10.1016/j.jgar.2024.06.012. Epub 2024 Jul 10.

Abstract

Introduction: Multi-carbapenemase-producing Enterobacterales (M-CPE) are increasingly described. We characterized the M-CPE isolates prospectively recovered in our hospital (Madrid, Spain) over two years (2021-2022).

Methods: We collected 796 carbapenem resistant Enterobacterales (CRE) from clinical and surveillance samples. Carbapenemase production was confirmed with phenotypic (immunochromatographic, disk diffusion) and molecular (PCR, WGS) techniques. Antimicrobial susceptibility was evaluated by a standard broth microdilution method. Clinical and demographic data were collected.

Results: Overall, 23 M-CPE (10 Klebsiella pneumoniae, 6 Citrobacter freundii complex, 3 Escherichia coli, 2 Klebsiella oxytoca, and 2 Enterobacter hormaechei) isolates were recovered from 17 patients (3% with CPE, 0.26-0.28 cases per 1000 admissions). OXA-48 + KPC-3 (7/23) and KPC-3 + VIM-1 (5/23) were the most frequent carbapenemase combinations. All patients had prior antibiotics exposure, including carbapenems (8/17). High resistance rates to ceftazidime/avibactam (14/23), imipenem/relebactam (16/23) and meropenem/vaborbactam (7/23) were found. Ceftazidime/avibactam + aztreonam combination was synergistic in all metallo-β-lactamase producers. Clonal and non-clonal related isolates were found, particularly in K. pneumoniae (5 ST29, 3 ST147, 3 ST307) and C. freundii (3 ST8, 2 ST125, 1 ST563). NDM-1 + OXA-48 was introduced with the ST147-K. pneumoniae high-risk clone linked to the transfer of a Ukrainian patient. We identified four possible nosocomial clonal transmission events between patients of the same clone with the same combination of carbapenemases (KPC-3 + VIM-1-ST29-K. pneumoniae, NDM-1 + OXA-48-ST147-K. pneumoniae and KPC-2 + VIM-1-ST145-K. oxytoca). Carbapenemase-encoding genes were located on different plasmids, except for VIM-1 + KPC-2-ST145-K. oxytoca. Cross-species transmission and a possible acquisition overtime was found, particularly between K. pneumoniae and E. coli producing OXA-48 + KPC-3.

Conclusion: M-CPE is an emerging threat in our hospital. Co-production of different carbapenemases, including metallo-β-lactamases, limits therapeutic options and depicts the need to reinforce infection control measures.

Keywords: Enterobacterales co-producing multiple carbapenemases; K. pneumoniae; KPC; Metallo-β-lactamases; OXA-48.

MeSH terms

  • Adult
  • Aged
  • Aged, 80 and over
  • Anti-Bacterial Agents* / pharmacology
  • Azabicyclo Compounds / pharmacology
  • Bacterial Proteins* / genetics
  • Bacterial Proteins* / metabolism
  • Carbapenem-Resistant Enterobacteriaceae* / drug effects
  • Carbapenem-Resistant Enterobacteriaceae* / genetics
  • Carbapenem-Resistant Enterobacteriaceae* / isolation & purification
  • Carbapenems / pharmacology
  • Ceftazidime / pharmacology
  • Citrobacter freundii / drug effects
  • Citrobacter freundii / enzymology
  • Citrobacter freundii / genetics
  • Citrobacter freundii / isolation & purification
  • Drug Combinations
  • Drug Resistance, Multiple, Bacterial
  • Enterobacter / drug effects
  • Enterobacter / enzymology
  • Enterobacter / genetics
  • Enterobacter / isolation & purification
  • Enterobacteriaceae / drug effects
  • Enterobacteriaceae / enzymology
  • Enterobacteriaceae / genetics
  • Enterobacteriaceae / isolation & purification
  • Enterobacteriaceae Infections* / epidemiology
  • Enterobacteriaceae Infections* / microbiology
  • Escherichia coli / drug effects
  • Escherichia coli / enzymology
  • Escherichia coli / genetics
  • Escherichia coli / isolation & purification
  • Female
  • Humans
  • Klebsiella oxytoca / drug effects
  • Klebsiella oxytoca / enzymology
  • Klebsiella oxytoca / genetics
  • Klebsiella oxytoca / isolation & purification
  • Klebsiella pneumoniae / drug effects
  • Klebsiella pneumoniae / enzymology
  • Klebsiella pneumoniae / genetics
  • Klebsiella pneumoniae / isolation & purification
  • Male
  • Microbial Sensitivity Tests*
  • Middle Aged
  • Prospective Studies
  • Spain / epidemiology
  • Tertiary Care Centers* / statistics & numerical data
  • beta-Lactamases* / genetics
  • beta-Lactamases* / metabolism

Substances

  • beta-Lactamases
  • carbapenemase
  • Bacterial Proteins
  • Anti-Bacterial Agents
  • Drug Combinations
  • Azabicyclo Compounds
  • Ceftazidime
  • avibactam, ceftazidime drug combination
  • Carbapenems

Supplementary concepts

  • Enterobacter hormaechei