Spreading of Extended-Spectrum β-Lactamase-Producing Escherichia coli ST131 and Klebsiella pneumoniae ST11 in Patients with Pneumonia: A Molecular Epidemiological Study
Introduction
Extended-spectrum β-lactamase (ESBL)-producing Enterobacteriaceae, particularly Escherichia coli (E. coli) and Klebsiella pneumoniae (K. pneumoniae), are significant pathogens causing pneumonia and pose substantial clinical challenges. The prevalence of ESBL-producing E. coli and K. pneumoniae varies across different geographical regions in China and types of infections. Continuous surveillance on the prevalence of these pathogens is crucial due to their high resistance to antibiotics and the clonal transmission of predominant sub-types such as E. coli ST131 and K. pneumoniae ST11. This study aims to investigate the clinical and molecular epidemiology characteristics of ESBL-producing E. coli and K. pneumoniae causing pneumonia in a large teaching hospital in Hubei province, China.
Methods
Ethical approval for this study was obtained from the Tongji Medical College Ethics Committee, Huazhong University of Science and Technology. Clinical data and ESBL-producing E. coli and K. pneumoniae strains causing pneumonia were collected from December 2015 to June 2016 at a teaching hospital in Hubei province. Community-acquired pneumonia (CAP), hospital-acquired pneumonia (HAP), and ventilator-related pneumonia (VAP) were defined according to established guidelines. Samples were cultured using blood agar medium, and the BD PhoenixTM100 Automated Microbiology System was used for strain identification and antimicrobial susceptibility testing. Confirmation of ESBL production was performed using the double-disc synergy test, and the modified Hodge test was applied to confirm carbapenemase-producing strains. Clonal relationships were analyzed using multi-locus sequence typing (MLST) and enterobacterial repetitive intergenic consensus polymerase chain reaction (ERIC-PCR). ESBL and carbapenemase genes were identified using PCR and sequencing, and the genetic environment of these genes was investigated.
Results
A total of 976 non-reduplicate E. coli and K. pneumoniae strains were collected, with 28.7% confirmed as ESBL producers. Among these, 59 strains (31 E. coli and 28 K. pneumoniae) isolated from patients with pneumonia were analyzed. Most strains were isolated from patients with HAP (62.7%), followed by CAP (22.0%) and VAP (15.3%). The predominant sub-types were E. coli ST131 (29.0%) and K. pneumoniae ST11 (17.9%). The most prevalent ESBL gene was CTX-M-14, followed by SHV-77, CTX-M-3, SHV-11, and CTX-M-27. At least 55.9% of the ESBL-producing strains carried two or more ESBL genes. ISEcp1 and IS26 were found upstream of all blaCTX-M and most blaSHV genes, respectively. Additionally, three ESBL-producing K. pneumoniae ST11 strains resistant to carbapenems carried blaNDM-1 and blaKPC-2, with two also bearing blaOXA-48 and resistant to all antibiotics, including tigecycline.
Discussion
The prevalence of ESBL-producing E. coli and K. pneumoniae in this study was lower than reported in other regions of China. However, the global spread of E. coli ST131 and K. pneumoniae ST11 was evident in patients with pneumonia in the hospital. The majority of ESBL-producing strains were associated with HAP, indicating a higher risk of ESBL producers in hospital settings. Patients with HAP or VAP caused by ESBL producers had higher 28-day mortality rates compared to those with CAP, likely due to the co-existence of multiple ESBL genes, multidrug resistance, and severe complications.
The most predominant ESBL gene, CTX-M-14, aligns with findings from other studies in the Asia-Pacific region. The ISEcp1 insertion sequence, detected upstream of all blaCTX-M genes, underscores its role in the global spread of blaCTX-M. In contrast, SHV-11 was the main blaSHV gene, with SHV-77 also prevalent. The mutation in the coding region of blaSHV-77 may contribute to its encoding of ESBL enzymes. The presence of IS26 upstream of most blaSHV genes highlights its importance in the expression and transmission of blaSHV.
MLST analysis revealed that E. coli ST131 was the most prevalent strain among ESBL-producing E. coli causing pneumonia. This strain, known for its multidrug resistance and global dissemination, was predominantly isolated from patients with HAP. E. coli ST131 strains exhibited higher antimicrobial resistance and were associated with poorer patient outcomes, including acute respiratory failure. The adaptive characteristics and genomic backbone of E. coli ST131 may contribute to its widespread prevalence in hospital environments.
For K. pneumoniae, ST11 was the major type of ESBL-producing strain. This strain, known for its multidrug resistance and high transmissibility, was predominantly isolated from patients with HAP and VAP. Three ESBL-producing K. pneumoniae ST11 strains resistant to carbapenems carried blaNDM-1 and blaKPC-2, with two also bearing blaOXA-48. The presence of these genes in K. pneumoniae ST11 poses a significant threat to public health, emphasizing the need for continuous surveillance to control the spread of these resistant strains.
Conclusion
This study documents the emergence and dissemination of multidrug-resistant E. coli ST131 and K. pneumoniae ST11 causing pneumonia in a Chinese teaching hospital. The findings highlight the significant threat these strains pose to hospitalized patients and underscore the importance of continuous surveillance of multidrug-resistant ESBL-producing E. coli and K. pneumoniae strains in hospital settings. The mobilization of blaCTX-M and blaSHV genes by ISEcp1 and IS26 further emphasizes the need for understanding the genetic mechanisms driving the spread of antibiotic resistance.
doi.org/10.1097/CM9.0000000000000368
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