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Evolution of Outbreak-Causing Carbapenem-Resistant Klebsiella pneumoniae ST258 at a Tertiary Care Hospital over 8 Years.
MBio 2019; 10(5)MBIO

Abstract

Carbapenem-resistant Klebsiella pneumoniae (CRKP) strains belonging to sequence type 258 (ST258) are frequent causes of hospital-associated outbreaks and are a major contributor to the spread of carbapenemases. This genetic lineage emerged several decades ago and remains a major global health care challenge. In this study, genomic epidemiology was used to investigate the emergence, evolution, and persistence of ST258 carbapenem-resistant K. pneumoniae outbreak-causing lineages at a large tertiary care hospital over 8 years. A time-based phylogenetic analysis of 136 ST258 isolates demonstrated the succession of multiple genetically distinct ST258 sublineages over the 8-year period. Ongoing genomic surveillance identified the emergence and persistence of several distinct clonal ST258 populations. Patterns of multidrug resistance determinants and plasmid replicons were consistent with continued evolution and persistence of these populations. Five ST258 outbreaks were documented, including three that were caused by the same clonal lineage. Mutations in genes encoding effectors of biofilm production and iron acquisition were identified among persistent clones. Two emergent lineages bearing K. pneumoniae integrative conjugative element 10 (ICEKp10) and harboring yersiniabactin and colibactin virulence factors were identified. The results show how distinct ST258 subpopulations have evolved and persisted within the same hospital over nearly a decade.IMPORTANCE The carbapenem class of antibiotics is invaluable for the treatment of selected multidrug-resistant Gram-negative pathogens. The continued transmission of carbapenem-resistant bacteria such as ST258 K. pneumoniae is of serious global public health concern, as treatment options for these infections are limited. This genomic epidemiologic investigation traced the natural history of ST258 K. pneumoniae in a single health care setting over nearly a decade. We found that distinct ST258 subpopulations have caused both device-associated and ward-associated outbreaks, and some of these populations remain endemic within our hospital to the present day. The finding of virulence determinants among emergent ST258 clones supports the idea of convergent evolution of drug-resistant and virulent CRKP strains and highlights the need for continued surveillance, prevention, and control efforts to address emergent and evolving ST258 populations in the health care setting.

Authors+Show Affiliations

Infectious Diseases Epidemiology Research Unit, University of Pittsburgh School of Medicine and Graduate School of Public Health, Pittsburgh, Pennsylvania, USA jwmarsh@pitt.edu.Infectious Diseases Epidemiology Research Unit, University of Pittsburgh School of Medicine and Graduate School of Public Health, Pittsburgh, Pennsylvania, USA.Infectious Diseases Epidemiology Research Unit, University of Pittsburgh School of Medicine and Graduate School of Public Health, Pittsburgh, Pennsylvania, USA.Division of Infectious Diseases, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.Infectious Diseases Epidemiology Research Unit, University of Pittsburgh School of Medicine and Graduate School of Public Health, Pittsburgh, Pennsylvania, USA.Division of Microbiology, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA.Infectious Diseases Epidemiology Research Unit, University of Pittsburgh School of Medicine and Graduate School of Public Health, Pittsburgh, Pennsylvania, USA.Infectious Diseases Epidemiology Research Unit, University of Pittsburgh School of Medicine and Graduate School of Public Health, Pittsburgh, Pennsylvania, USA. Division of Hospital Epidemiology and Infection Control, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA.Division of Hospital Epidemiology and Infection Control, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania, USA.Division of Infectious Diseases, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.Division of Infectious Diseases, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.Department of Microbiology and Molecular Genetics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.Division of Infectious Diseases, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA.Infectious Diseases Epidemiology Research Unit, University of Pittsburgh School of Medicine and Graduate School of Public Health, Pittsburgh, Pennsylvania, USA.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

31481386

Citation

Marsh, Jane W., et al. "Evolution of Outbreak-Causing Carbapenem-Resistant Klebsiella Pneumoniae ST258 at a Tertiary Care Hospital Over 8 Years." MBio, vol. 10, no. 5, 2019.
Marsh JW, Mustapha MM, Griffith MP, et al. Evolution of Outbreak-Causing Carbapenem-Resistant Klebsiella pneumoniae ST258 at a Tertiary Care Hospital over 8 Years. MBio. 2019;10(5).
Marsh, J. W., Mustapha, M. M., Griffith, M. P., Evans, D. R., Ezeonwuka, C., Pasculle, A. W., ... Harrison, L. H. (2019). Evolution of Outbreak-Causing Carbapenem-Resistant Klebsiella pneumoniae ST258 at a Tertiary Care Hospital over 8 Years. MBio, 10(5), doi:10.1128/mBio.01945-19.
Marsh JW, et al. Evolution of Outbreak-Causing Carbapenem-Resistant Klebsiella Pneumoniae ST258 at a Tertiary Care Hospital Over 8 Years. MBio. 2019 Sep 3;10(5) PubMed PMID: 31481386.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Evolution of Outbreak-Causing Carbapenem-Resistant Klebsiella pneumoniae ST258 at a Tertiary Care Hospital over 8 Years. AU - Marsh,Jane W, AU - Mustapha,Mustapha M, AU - Griffith,Marissa P, AU - Evans,Daniel R, AU - Ezeonwuka,Chinelo, AU - Pasculle,A William, AU - Shutt,Kathleen A, AU - Sundermann,Alexander, AU - Ayres,Ashley M, AU - Shields,Ryan K, AU - Babiker,Ahmed, AU - Cooper,Vaughn S, AU - Van Tyne,Daria, AU - Harrison,Lee H, Y1 - 2019/09/03/ PY - 2019/9/5/entrez PY - 2019/9/5/pubmed PY - 2019/9/5/medline KW - carbapenem-resistant KW - evolution KW - genomics KW - molecular epidemiology KW - outbreaks JF - mBio JO - MBio VL - 10 IS - 5 N2 - Carbapenem-resistant Klebsiella pneumoniae (CRKP) strains belonging to sequence type 258 (ST258) are frequent causes of hospital-associated outbreaks and are a major contributor to the spread of carbapenemases. This genetic lineage emerged several decades ago and remains a major global health care challenge. In this study, genomic epidemiology was used to investigate the emergence, evolution, and persistence of ST258 carbapenem-resistant K. pneumoniae outbreak-causing lineages at a large tertiary care hospital over 8 years. A time-based phylogenetic analysis of 136 ST258 isolates demonstrated the succession of multiple genetically distinct ST258 sublineages over the 8-year period. Ongoing genomic surveillance identified the emergence and persistence of several distinct clonal ST258 populations. Patterns of multidrug resistance determinants and plasmid replicons were consistent with continued evolution and persistence of these populations. Five ST258 outbreaks were documented, including three that were caused by the same clonal lineage. Mutations in genes encoding effectors of biofilm production and iron acquisition were identified among persistent clones. Two emergent lineages bearing K. pneumoniae integrative conjugative element 10 (ICEKp10) and harboring yersiniabactin and colibactin virulence factors were identified. The results show how distinct ST258 subpopulations have evolved and persisted within the same hospital over nearly a decade.IMPORTANCE The carbapenem class of antibiotics is invaluable for the treatment of selected multidrug-resistant Gram-negative pathogens. The continued transmission of carbapenem-resistant bacteria such as ST258 K. pneumoniae is of serious global public health concern, as treatment options for these infections are limited. This genomic epidemiologic investigation traced the natural history of ST258 K. pneumoniae in a single health care setting over nearly a decade. We found that distinct ST258 subpopulations have caused both device-associated and ward-associated outbreaks, and some of these populations remain endemic within our hospital to the present day. The finding of virulence determinants among emergent ST258 clones supports the idea of convergent evolution of drug-resistant and virulent CRKP strains and highlights the need for continued surveillance, prevention, and control efforts to address emergent and evolving ST258 populations in the health care setting. SN - 2150-7511 UR - https://www.unboundmedicine.com/medline/citation/31481386/Evolution_of_Outbreak-Causing_Carbapenem-Resistant_Klebsiella_pneumoniae_ST258_at_a_Tertiary_Care_Hospital_over_8_Years L2 - http://mbio.asm.org/cgi/pmidlookup?view=long&pmid=31481386 DB - PRIME DP - Unbound Medicine ER -