Contrasting patterns of longitudinal population dynamics and antimicrobial resistance mechanisms in two priority bacterial pathogens over 7 years in a single center

Abstract Background Two of the most important pathogens contributing to the global rise in antimicrobial resistance (AMR) are Klebsiella pneumoniae and Enterobacter cloacae. Despite this, most of our knowledge about the changing patterns of disease caused by these two pathogens is based on studies w...

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Main Authors: Matthew J. Ellington, Eva Heinz, Alexander M. Wailan, Matthew J. Dorman, Marcus de Goffau, Amy K. Cain, Sonal P. Henson, Nicholas Gleadall, Christine J. Boinett, Gordon Dougan, Nicholas M. Brown, Neil Woodford, Julian Parkhill, M. Estée Török, Sharon J. Peacock, Nicholas R. Thomson
Format: Article
Language:English
Published: BMC 2019-09-01
Series:Genome Biology
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13059-019-1785-1
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author Matthew J. Ellington
Eva Heinz
Alexander M. Wailan
Matthew J. Dorman
Marcus de Goffau
Amy K. Cain
Sonal P. Henson
Nicholas Gleadall
Christine J. Boinett
Gordon Dougan
Nicholas M. Brown
Neil Woodford
Julian Parkhill
M. Estée Török
Sharon J. Peacock
Nicholas R. Thomson
author_facet Matthew J. Ellington
Eva Heinz
Alexander M. Wailan
Matthew J. Dorman
Marcus de Goffau
Amy K. Cain
Sonal P. Henson
Nicholas Gleadall
Christine J. Boinett
Gordon Dougan
Nicholas M. Brown
Neil Woodford
Julian Parkhill
M. Estée Török
Sharon J. Peacock
Nicholas R. Thomson
author_sort Matthew J. Ellington
collection DOAJ
description Abstract Background Two of the most important pathogens contributing to the global rise in antimicrobial resistance (AMR) are Klebsiella pneumoniae and Enterobacter cloacae. Despite this, most of our knowledge about the changing patterns of disease caused by these two pathogens is based on studies with limited timeframes that provide few insights into their population dynamics or the dynamics in AMR elements that they can carry. Results We investigate the population dynamics of two priority AMR pathogens over 7 years between 2007 and 2012 in a major UK hospital, spanning changes made to UK national antimicrobial prescribing policy in 2007. Between 2006 and 2012, K. pneumoniae showed epidemiological cycles of multi-drug-resistant (MDR) lineages being replaced approximately every 2 years. This contrasted E. cloacae where there was no temporally changing pattern, but a continuous presence of the mixed population. Conclusions The differing patterns of clonal replacement and acquisition of mobile elements shows that the flux in the K. pneumoniae population was linked to the introduction of globally recognized MDR clones carrying drug resistance markers on mobile elements. However, E. cloacae carries a chromosomally encoded ampC conferring resistance to front-line treatments and shows that MDR plasmid acquisition in E. cloacae was not indicative of success in the hospital. This led to markedly different dynamics in the AMR populations of these two pathogens and shows that the mechanism of the resistance and its location in the genome or mobile elements is crucial to predict population dynamics of opportunistic pathogens in clinical settings.
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spelling doaj.art-f036a345f97748a0b9feb81855d82e3f2022-12-21T23:57:45ZengBMCGenome Biology1474-760X2019-09-0120111610.1186/s13059-019-1785-1Contrasting patterns of longitudinal population dynamics and antimicrobial resistance mechanisms in two priority bacterial pathogens over 7 years in a single centerMatthew J. Ellington0Eva Heinz1Alexander M. Wailan2Matthew J. Dorman3Marcus de Goffau4Amy K. Cain5Sonal P. Henson6Nicholas Gleadall7Christine J. Boinett8Gordon Dougan9Nicholas M. Brown10Neil Woodford11Julian Parkhill12M. Estée Török13Sharon J. Peacock14Nicholas R. Thomson15Public Health England, National Infection Service, Addenbrooke’s HospitalWellcome Sanger Institute, Wellcome Genome CampusWellcome Sanger Institute, Wellcome Genome CampusWellcome Sanger Institute, Wellcome Genome CampusWellcome Sanger Institute, Wellcome Genome CampusWellcome Sanger Institute, Wellcome Genome CampusKEMRI-Wellcome Trust Research Programme, CGMRCPublic Health England, National Infection Service, Addenbrooke’s HospitalWellcome Sanger Institute, Wellcome Genome CampusWellcome Sanger Institute, Wellcome Genome CampusPublic Health England, National Infection Service, Addenbrooke’s HospitalAntimicrobial Resistance and Healthcare Associated Infections (AMRHAI) Reference Unit, National Infection Service, Public Health EnglandWellcome Sanger Institute, Wellcome Genome CampusPublic Health England, National Infection Service, Addenbrooke’s HospitalPublic Health England, National Infection Service, Addenbrooke’s HospitalWellcome Sanger Institute, Wellcome Genome CampusAbstract Background Two of the most important pathogens contributing to the global rise in antimicrobial resistance (AMR) are Klebsiella pneumoniae and Enterobacter cloacae. Despite this, most of our knowledge about the changing patterns of disease caused by these two pathogens is based on studies with limited timeframes that provide few insights into their population dynamics or the dynamics in AMR elements that they can carry. Results We investigate the population dynamics of two priority AMR pathogens over 7 years between 2007 and 2012 in a major UK hospital, spanning changes made to UK national antimicrobial prescribing policy in 2007. Between 2006 and 2012, K. pneumoniae showed epidemiological cycles of multi-drug-resistant (MDR) lineages being replaced approximately every 2 years. This contrasted E. cloacae where there was no temporally changing pattern, but a continuous presence of the mixed population. Conclusions The differing patterns of clonal replacement and acquisition of mobile elements shows that the flux in the K. pneumoniae population was linked to the introduction of globally recognized MDR clones carrying drug resistance markers on mobile elements. However, E. cloacae carries a chromosomally encoded ampC conferring resistance to front-line treatments and shows that MDR plasmid acquisition in E. cloacae was not indicative of success in the hospital. This led to markedly different dynamics in the AMR populations of these two pathogens and shows that the mechanism of the resistance and its location in the genome or mobile elements is crucial to predict population dynamics of opportunistic pathogens in clinical settings.http://link.springer.com/article/10.1186/s13059-019-1785-1Resistance mechanismsPopulation dynamicsIntrinsic resistancePlasmid diversity
spellingShingle Matthew J. Ellington
Eva Heinz
Alexander M. Wailan
Matthew J. Dorman
Marcus de Goffau
Amy K. Cain
Sonal P. Henson
Nicholas Gleadall
Christine J. Boinett
Gordon Dougan
Nicholas M. Brown
Neil Woodford
Julian Parkhill
M. Estée Török
Sharon J. Peacock
Nicholas R. Thomson
Contrasting patterns of longitudinal population dynamics and antimicrobial resistance mechanisms in two priority bacterial pathogens over 7 years in a single center
Genome Biology
Resistance mechanisms
Population dynamics
Intrinsic resistance
Plasmid diversity
title Contrasting patterns of longitudinal population dynamics and antimicrobial resistance mechanisms in two priority bacterial pathogens over 7 years in a single center
title_full Contrasting patterns of longitudinal population dynamics and antimicrobial resistance mechanisms in two priority bacterial pathogens over 7 years in a single center
title_fullStr Contrasting patterns of longitudinal population dynamics and antimicrobial resistance mechanisms in two priority bacterial pathogens over 7 years in a single center
title_full_unstemmed Contrasting patterns of longitudinal population dynamics and antimicrobial resistance mechanisms in two priority bacterial pathogens over 7 years in a single center
title_short Contrasting patterns of longitudinal population dynamics and antimicrobial resistance mechanisms in two priority bacterial pathogens over 7 years in a single center
title_sort contrasting patterns of longitudinal population dynamics and antimicrobial resistance mechanisms in two priority bacterial pathogens over 7 years in a single center
topic Resistance mechanisms
Population dynamics
Intrinsic resistance
Plasmid diversity
url http://link.springer.com/article/10.1186/s13059-019-1785-1
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