High-Risk International Clones of Carbapenem-Nonsusceptible <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Endemic to Indonesian Intensive Care Units: Impact of a Multifaceted Infection Control Intervention Analyzed at the Genomic Level

ABSTRACT Infection control effectiveness evaluations require detailed epidemiological and microbiological data. We analyzed the genomic profiles of carbapenem-nonsusceptible Pseudomonas aeruginosa (CNPA) strains collected from two intensive care units (ICUs) in the national referral hospital in Jaka...

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Autores principales: Andreu Coello Pelegrin, Yulia Rosa Saharman, Aurélien Griffon, Mattia Palmieri, Caroline Mirande, Anis Karuniawati, Rudyanto Sedono, Dita Aditianingsih, Wil H. F. Goessens, Alex van Belkum, Henri A. Verbrugh, Corné H. W. Klaassen, Juliëtte A. Severin
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:ec905eba151743ea83ae43815448b24d2021-11-15T15:54:46ZHigh-Risk International Clones of Carbapenem-Nonsusceptible <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Endemic to Indonesian Intensive Care Units: Impact of a Multifaceted Infection Control Intervention Analyzed at the Genomic Level10.1128/mBio.02384-192150-7511https://doaj.org/article/ec905eba151743ea83ae43815448b24d2019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02384-19https://doaj.org/toc/2150-7511ABSTRACT Infection control effectiveness evaluations require detailed epidemiological and microbiological data. We analyzed the genomic profiles of carbapenem-nonsusceptible Pseudomonas aeruginosa (CNPA) strains collected from two intensive care units (ICUs) in the national referral hospital in Jakarta, Indonesia, where a multifaceted infection control intervention was applied. We used clinical data combined with whole-genome sequencing (WGS) of systematically collected CNPA to infer the transmission dynamics of CNPA strains and to characterize their resistome. We found that the number of CNPA transmissions and acquisitions by patients was highly variable over time but that, overall, the rates were not significantly reduced by the intervention. Environmental sources were involved in these transmissions and acquisitions. Four high-risk international CNPA clones (ST235, ST823, ST375, and ST446) dominated, but the distribution of these clones changed significantly after the intervention was implemented. Using resistome analysis, carbapenem resistance was explained by the presence of various carbapenemase-encoding genes (blaGES-5, blaVIM-2-8, and blaIMP-1-7-43) and by mutations within the porin OprD. Our results reveal for the first time the dynamics of P. aeruginosa antimicrobial resistance (AMR) profiles in Indonesia and additionally show the utility of WGS in combination with clinical data to evaluate the impact of an infection control intervention. (This study has been registered at www.trialregister.nl under registration no. NTR5541). IMPORTANCE In low-to-middle-income countries such as Indonesia, work in intensive care units (ICUs) can be hampered by lack of resources. Conducting large epidemiological studies in such settings using genomic tools is rather challenging. Still, we were able to systematically study the transmissions of carbapenem-nonsusceptible strains of P. aeruginosa (CNPA) within and between ICUs, before and after an infection control intervention. Our data show the importance of the broad dissemination of the internationally recognized CNPA clones, the relevance of environmental reservoirs, and the mixed effects of the implemented intervention; it led to a profound change in the clonal make-up of CNPA, but it did not reduce the patients’ risk of CNPA acquisitions. Thus, CNPA epidemiology in Indonesian ICUs is part of a global expansion of multiple CNPA clones that remains difficult to control by infection prevention measures.Andreu Coello PelegrinYulia Rosa SaharmanAurélien GriffonMattia PalmieriCaroline MirandeAnis KaruniawatiRudyanto SedonoDita AditianingsihWil H. F. GoessensAlex van BelkumHenri A. VerbrughCorné H. W. KlaassenJuliëtte A. SeverinAmerican Society for MicrobiologyarticlePseudomonas aeruginosaintensive care unitsinfection controlsingle nucleotide polymorphismIndonesiamicrobial drug resistanceMicrobiologyQR1-502ENmBio, Vol 10, Iss 6 (2019)
institution DOAJ
collection DOAJ
language EN
topic Pseudomonas aeruginosa
intensive care units
infection control
single nucleotide polymorphism
Indonesia
microbial drug resistance
Microbiology
QR1-502
spellingShingle Pseudomonas aeruginosa
intensive care units
infection control
single nucleotide polymorphism
Indonesia
microbial drug resistance
Microbiology
QR1-502
Andreu Coello Pelegrin
Yulia Rosa Saharman
Aurélien Griffon
Mattia Palmieri
Caroline Mirande
Anis Karuniawati
Rudyanto Sedono
Dita Aditianingsih
Wil H. F. Goessens
Alex van Belkum
Henri A. Verbrugh
Corné H. W. Klaassen
Juliëtte A. Severin
High-Risk International Clones of Carbapenem-Nonsusceptible <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Endemic to Indonesian Intensive Care Units: Impact of a Multifaceted Infection Control Intervention Analyzed at the Genomic Level
description ABSTRACT Infection control effectiveness evaluations require detailed epidemiological and microbiological data. We analyzed the genomic profiles of carbapenem-nonsusceptible Pseudomonas aeruginosa (CNPA) strains collected from two intensive care units (ICUs) in the national referral hospital in Jakarta, Indonesia, where a multifaceted infection control intervention was applied. We used clinical data combined with whole-genome sequencing (WGS) of systematically collected CNPA to infer the transmission dynamics of CNPA strains and to characterize their resistome. We found that the number of CNPA transmissions and acquisitions by patients was highly variable over time but that, overall, the rates were not significantly reduced by the intervention. Environmental sources were involved in these transmissions and acquisitions. Four high-risk international CNPA clones (ST235, ST823, ST375, and ST446) dominated, but the distribution of these clones changed significantly after the intervention was implemented. Using resistome analysis, carbapenem resistance was explained by the presence of various carbapenemase-encoding genes (blaGES-5, blaVIM-2-8, and blaIMP-1-7-43) and by mutations within the porin OprD. Our results reveal for the first time the dynamics of P. aeruginosa antimicrobial resistance (AMR) profiles in Indonesia and additionally show the utility of WGS in combination with clinical data to evaluate the impact of an infection control intervention. (This study has been registered at www.trialregister.nl under registration no. NTR5541). IMPORTANCE In low-to-middle-income countries such as Indonesia, work in intensive care units (ICUs) can be hampered by lack of resources. Conducting large epidemiological studies in such settings using genomic tools is rather challenging. Still, we were able to systematically study the transmissions of carbapenem-nonsusceptible strains of P. aeruginosa (CNPA) within and between ICUs, before and after an infection control intervention. Our data show the importance of the broad dissemination of the internationally recognized CNPA clones, the relevance of environmental reservoirs, and the mixed effects of the implemented intervention; it led to a profound change in the clonal make-up of CNPA, but it did not reduce the patients’ risk of CNPA acquisitions. Thus, CNPA epidemiology in Indonesian ICUs is part of a global expansion of multiple CNPA clones that remains difficult to control by infection prevention measures.
format article
author Andreu Coello Pelegrin
Yulia Rosa Saharman
Aurélien Griffon
Mattia Palmieri
Caroline Mirande
Anis Karuniawati
Rudyanto Sedono
Dita Aditianingsih
Wil H. F. Goessens
Alex van Belkum
Henri A. Verbrugh
Corné H. W. Klaassen
Juliëtte A. Severin
author_facet Andreu Coello Pelegrin
Yulia Rosa Saharman
Aurélien Griffon
Mattia Palmieri
Caroline Mirande
Anis Karuniawati
Rudyanto Sedono
Dita Aditianingsih
Wil H. F. Goessens
Alex van Belkum
Henri A. Verbrugh
Corné H. W. Klaassen
Juliëtte A. Severin
author_sort Andreu Coello Pelegrin
title High-Risk International Clones of Carbapenem-Nonsusceptible <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Endemic to Indonesian Intensive Care Units: Impact of a Multifaceted Infection Control Intervention Analyzed at the Genomic Level
title_short High-Risk International Clones of Carbapenem-Nonsusceptible <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Endemic to Indonesian Intensive Care Units: Impact of a Multifaceted Infection Control Intervention Analyzed at the Genomic Level
title_full High-Risk International Clones of Carbapenem-Nonsusceptible <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Endemic to Indonesian Intensive Care Units: Impact of a Multifaceted Infection Control Intervention Analyzed at the Genomic Level
title_fullStr High-Risk International Clones of Carbapenem-Nonsusceptible <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Endemic to Indonesian Intensive Care Units: Impact of a Multifaceted Infection Control Intervention Analyzed at the Genomic Level
title_full_unstemmed High-Risk International Clones of Carbapenem-Nonsusceptible <named-content content-type="genus-species">Pseudomonas aeruginosa</named-content> Endemic to Indonesian Intensive Care Units: Impact of a Multifaceted Infection Control Intervention Analyzed at the Genomic Level
title_sort high-risk international clones of carbapenem-nonsusceptible <named-content content-type="genus-species">pseudomonas aeruginosa</named-content> endemic to indonesian intensive care units: impact of a multifaceted infection control intervention analyzed at the genomic level
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/ec905eba151743ea83ae43815448b24d
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