Characterization and transmission dynamics of carbapenemase-encoding genes in carbapenem-resistant Enterobacter cloacae isolated from eight teaching hospitals in Guangdong province, China (2022–2024)

The Corona Virus Disease 2019 (COVID-19) pandemic has introduced complex challenges in resistance and transmission. During the COVID-19 pandemic, increased antibiotic use, interruptions in healthcare services, and complex infections in patients can all promote the emergence and spread of drug-resistant bacteria. However, detailed investigations into the characteristics of carbapenemase-encoding genes (CEGs) in carbapenem-resistant Enterobacter cloacae (CREC) and the alterations in their transmission dynamics during the pandemic remain scarce. This study analyzed 54 CREC strains collected from eight teaching hospitals in Guangdong Province, China, between December 2022 and June 2024. The variable temperature Sodium Dodecyl Sulfate (SDS) plasmid elimination method and PCR were used to analyze the samples. The positive rate of CEGs was 85.19% (46/54). Among the 54 CREC isolates, 33.33% (18/54) carried the blaNDM−1 gene on both chromosomes and plasmids. A total of 46.30% (25/54) of the isolates had the blaNDM−1 gene exclusively on plasmids. Additionally, 3.70% (2/54) of the isolates harbored only the blaIMP gene on plasmids. Finally, 1.85% (1/54) of the isolates contained both the blaNDM−1 gene and blaKPC−2 gene on plasmids. The broth microdilution method showed that the resistance rate of CEG-positive group to imipenem, cefepime, gentamicin, ceftazidime/avibactam, ciprofloxacin and levofloxacin were significantly higher than those of CEG-Negative group (P<0.05). Plasmid conjugation experiments and PCR analysis revealed a 95.65% (44/46) success rate for the transfer of CEGs. Among these, the success rates for the blaNDM−1, blaIMP, and blaKPC−2 genes were 95.45% (42/44), 100.00% (2/2) and 0% (0/1) respectively. Six types of mobile genetic elements were identified, with ISEcp1 being the most prevalent (87.04%, 47/54). CREC carrying four types of mobile genetic elements simultaneously was the most prevalent (40.74%, 22/54). ERIC-PCR and NTSYS software categorized the 54 CREC strains into 17 genotypes, with type E and type G showing the highest prevalence (both of them 20.37%, 11/54), originating from different departments in five hospitals. Among the type E isolates, 3.70% (2/54) strains shared a Dice coefficient of 100%. The epidemiology of CEG shows that the detection rates of men, elderly people, respiratory medicine, and sputum samples are the highest in gender, age group, clinical department, and specimen category, accounting for 64.81% (35/54), 72.22% (39/54), 20.37% (11/54) and 33.33% (18/54), respectively. CREC plasmids and chromosomes frequently harbor CEGs, with the blaNDM−1 gene being a predominant example, particularly when located on plasmids. CEG-positive strains demonstrated significant levels of multidrug resistance. Furthermore, CEGs displayed a notable capacity for both horizontal and vertical dissemination. Higher detection frequencies of CEGs were identified in male patients, elderly individuals, within respiratory medicine contexts, and in sputum samples.