The emergence of highly resistant and hypervirulent Klebsiella pneumoniae CC14 clone in a tertiary hospital over 8 years.

Klebsiella pneumoniae Antimicrobial resistance Precision epidemiology Whole-genome sequencing

Journal

Genome medicine
ISSN: 1756-994X
Titre abrégé: Genome Med
Pays: England
ID NLM: 101475844

Informations de publication

Date de publication:
18 Apr 2024
Historique:
received: 03 10 2023
accepted: 08 04 2024
medline: 19 4 2024
pubmed: 19 4 2024
entrez: 18 4 2024
Statut: epublish

Résumé

Klebsiella pneumoniae is a major bacterial and opportunistic human pathogen, increasingly recognized as a healthcare burden globally. The convergence of resistance and virulence in K. pneumoniae strains has led to the formation of hypervirulent and multidrug-resistant strains with dual risk, limiting treatment options. K. pneumoniae clones are known to emerge locally and spread globally. Therefore, an understanding of the dynamics and evolution of the emerging strains in hospitals is warranted to prevent future outbreaks. In this study, we conducted an in-depth genomic analysis on a large-scale collection of 328 multidrug-resistant (MDR) K. pneumoniae strains recovered from 239 patients from a single major hospital in the western coastal city of Jeddah in Saudi Arabia from 2014 through 2022. We employed a broad range of phylogenetic and phylodynamic methods to understand the evolution of the predominant clones on epidemiological time scales, virulence and resistance determinants, and their dynamics. We also integrated the genomic data with detailed electronic health record (EHR) data for the patients to understand the clinical implications of the resistance and virulence of different strains. We discovered a diverse population underlying the infections, with most strains belonging to Clonal Complex 14 (CC14) exhibiting dominance. Specifically, we observed the emergence and continuous expansion of strains belonging to the dominant ST2096 in the CC14 clade across hospital wards in recent years. These strains acquired resistance mutations against colistin and extended spectrum β-lactamase (ESBL) and carbapenemase genes, namely bla Overall, these results demonstrate the clinical significance of ST2096 clones and illustrate the rapid evolution of an emerging hypervirulent and MDR K. pneumoniae in a clinical setting.

Sections du résumé

BACKGROUND BACKGROUND
Klebsiella pneumoniae is a major bacterial and opportunistic human pathogen, increasingly recognized as a healthcare burden globally. The convergence of resistance and virulence in K. pneumoniae strains has led to the formation of hypervirulent and multidrug-resistant strains with dual risk, limiting treatment options. K. pneumoniae clones are known to emerge locally and spread globally. Therefore, an understanding of the dynamics and evolution of the emerging strains in hospitals is warranted to prevent future outbreaks.
METHODS METHODS
In this study, we conducted an in-depth genomic analysis on a large-scale collection of 328 multidrug-resistant (MDR) K. pneumoniae strains recovered from 239 patients from a single major hospital in the western coastal city of Jeddah in Saudi Arabia from 2014 through 2022. We employed a broad range of phylogenetic and phylodynamic methods to understand the evolution of the predominant clones on epidemiological time scales, virulence and resistance determinants, and their dynamics. We also integrated the genomic data with detailed electronic health record (EHR) data for the patients to understand the clinical implications of the resistance and virulence of different strains.
RESULTS RESULTS
We discovered a diverse population underlying the infections, with most strains belonging to Clonal Complex 14 (CC14) exhibiting dominance. Specifically, we observed the emergence and continuous expansion of strains belonging to the dominant ST2096 in the CC14 clade across hospital wards in recent years. These strains acquired resistance mutations against colistin and extended spectrum β-lactamase (ESBL) and carbapenemase genes, namely bla
CONCLUSIONS CONCLUSIONS
Overall, these results demonstrate the clinical significance of ST2096 clones and illustrate the rapid evolution of an emerging hypervirulent and MDR K. pneumoniae in a clinical setting.

Identifiants

pubmed: 38637822
doi: 10.1186/s13073-024-01332-5
pii: 10.1186/s13073-024-01332-5
pmc: PMC11025284
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

58

Subventions

Organisme : KAUST
ID : BAS/1/1108-01-01
Organisme : KAUST
ID : BAS/1/1020-01-01

Informations de copyright

© 2024. The Author(s).

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Auteurs

Sharif Hala (S)

Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, 23955-6900, Jeddah, Makkah, Saudi Arabia.
King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.

Mohammed Malaikah (M)

Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, 23955-6900, Jeddah, Makkah, Saudi Arabia.
Laboratory of Infectious Disease Epidemiology, Biological and Environmental Science and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia.

Jiayi Huang (J)

Laboratory of Infectious Disease Epidemiology, Biological and Environmental Science and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia.
KAUST Computational Bioscience Research Center (CBRC), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia.

Wesam Bahitham (W)

King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.

Omniya Fallatah (O)

King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.

Samer Zakri (S)

King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.

Chakkiath Paul Antony (CP)

Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, 23955-6900, Jeddah, Makkah, Saudi Arabia.
International Institute for Zoonosis Control, Hokkaido University, Sapporo, 001-0020, Japan.

Mohammed Alshehri (M)

King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.

Raeece Naeem Ghazzali (RN)

Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, 23955-6900, Jeddah, Makkah, Saudi Arabia.

Fathia Ben-Rached (F)

Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, 23955-6900, Jeddah, Makkah, Saudi Arabia.

Abdullah Alsahafi (A)

King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.

Asim Alsaedi (A)

King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.

Ghadeer AlAhmadi (G)

King Faisal Specialist Hospital and Research Centre, Jeddah, Saudi Arabia.

Mai Kaaki (M)

King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.

Meshari Alazmi (M)

KAUST Computational Bioscience Research Center (CBRC), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia.
College of Computer Science and Engineering, University of Hail, Hail, Saudi Arabia.

Baraa AlhajHussein (B)

King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.

Muhammad Yaseen (M)

King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.

Hosam M Zowawi (HM)

King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.
The University of Queensland, UQ Centre for Clinical Research, Herston, QLD, Australia.

Majed F Alghoribi (MF)

King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.

Abdulhakeem O Althaqafi (AO)

King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.

Abdulfattah Al-Amri (A)

King Saud Bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
Infectious Disease Research Department, King Abdullah International Medical Research Centre, Jeddah, Saudi Arabia.
Ministry of National Guard Health Affairs, Riyadh, Western Region, Saudi Arabia.

Danesh Moradigaravand (D)

Laboratory of Infectious Disease Epidemiology, Biological and Environmental Science and Engineering (BESE) Division, King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia. danesh.moradigaravand@kaust.edu.sa.
KAUST Computational Bioscience Research Center (CBRC), King Abdullah University of Science and Technology (KAUST), Thuwal, Saudi Arabia. danesh.moradigaravand@kaust.edu.sa.

Arnab Pain (A)

Pathogen Genomics Laboratory, Biological and Environmental Sciences and Engineering, King Abdullah University of Science and Technology, 23955-6900, Jeddah, Makkah, Saudi Arabia. arnab.pain@kaust.edu.sa.
The University of Queensland, UQ Centre for Clinical Research, Herston, QLD, Australia. arnab.pain@kaust.edu.sa.

Classifications MeSH