Genomic Analysis of Hospital Plumbing Reveals Diverse Reservoir of Bacterial Plasmids Conferring Carbapenem Resistance

ABSTRACT The hospital environment is a potential reservoir of bacteria with plasmids conferring carbapenem resistance. Our Hospital Epidemiology Service routinely performs extensive sampling of high-touch surfaces, sinks, and other locations in the hospital. Over a 2-year period, additional sampling...

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Autores principales:	Rebecca A. Weingarten, Ryan C. Johnson, Sean Conlan, Amanda M. Ramsburg, John P. Dekker, Anna F. Lau, Pavel Khil, Robin T. Odom, Clay Deming, Morgan Park, Pamela J. Thomas, David K. Henderson, Tara N. Palmore, Julia A. Segre, Karen M. Frank
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	antimicrobial resistance carbapenem resistant carbapenemase-producing organisms environment infection control plasmid-mediated resistance Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/fcf915979d37441ea9ec74ff7535984d
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spelling	oai:doaj.org-article:fcf915979d37441ea9ec74ff7535984d2021-11-15T15:53:25ZGenomic Analysis of Hospital Plumbing Reveals Diverse Reservoir of Bacterial Plasmids Conferring Carbapenem Resistance10.1128/mBio.02011-172150-7511https://doaj.org/article/fcf915979d37441ea9ec74ff7535984d2018-03-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02011-17https://doaj.org/toc/2150-7511ABSTRACT The hospital environment is a potential reservoir of bacteria with plasmids conferring carbapenem resistance. Our Hospital Epidemiology Service routinely performs extensive sampling of high-touch surfaces, sinks, and other locations in the hospital. Over a 2-year period, additional sampling was conducted at a broader range of locations, including housekeeping closets, wastewater from hospital internal pipes, and external manholes. We compared these data with previously collected information from 5 years of patient clinical and surveillance isolates. Whole-genome sequencing and analysis of 108 isolates provided comprehensive characterization of blaKPC/blaNDM-positive isolates, enabling an in-depth genetic comparison. Strikingly, despite a very low prevalence of patient infections with blaKPC-positive organisms, all samples from the intensive care unit pipe wastewater and external manholes contained carbapenemase-producing organisms (CPOs), suggesting a vast, resilient reservoir. We observed a diverse set of species and plasmids, and we noted species and susceptibility profile differences between environmental and patient populations of CPOs. However, there were plasmid backbones common to both populations, highlighting a potential environmental reservoir of mobile elements that may contribute to the spread of resistance genes. Clear associations between patient and environmental isolates were uncommon based on sequence analysis and epidemiology, suggesting reasonable infection control compliance at our institution. Nonetheless, a probable nosocomial transmission of Leclercia sp. from the housekeeping environment to a patient was detected by this extensive surveillance. These data and analyses further our understanding of CPOs in the hospital environment and are broadly relevant to the design of infection control strategies in many infrastructure settings. IMPORTANCE Carbapenemase-producing organisms (CPOs) are a global concern because of the morbidity and mortality associated with these resistant Gram-negative bacteria. Horizontal plasmid transfer spreads the resistance mechanism to new bacteria, and understanding the plasmid ecology of the hospital environment can assist in the design of control strategies to prevent nosocomial infections. A 5-year genomic and epidemiological survey was undertaken to study the CPOs in the patient-accessible environment, as well as in the plumbing system removed from the patient. This comprehensive survey revealed a vast, unappreciated reservoir of CPOs in wastewater, which was in contrast to the low positivity rate in both the patient population and the patient-accessible environment. While there were few patient-environmental isolate associations, there were plasmid backbones common to both populations. These results are relevant to all hospitals for which CPO colonization may not yet be defined through extensive surveillance.Rebecca A. WeingartenRyan C. JohnsonSean ConlanAmanda M. RamsburgJohn P. DekkerAnna F. LauPavel KhilRobin T. OdomClay DemingMorgan ParkPamela J. ThomasDavid K. HendersonTara N. PalmoreJulia A. SegreKaren M. FrankAmerican Society for Microbiologyarticleantimicrobial resistancecarbapenem resistantcarbapenemase-producing organismsenvironmentinfection controlplasmid-mediated resistanceMicrobiologyQR1-502ENmBio, Vol 9, Iss 1 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	antimicrobial resistance carbapenem resistant carbapenemase-producing organisms environment infection control plasmid-mediated resistance Microbiology QR1-502
spellingShingle	antimicrobial resistance carbapenem resistant carbapenemase-producing organisms environment infection control plasmid-mediated resistance Microbiology QR1-502 Rebecca A. Weingarten Ryan C. Johnson Sean Conlan Amanda M. Ramsburg John P. Dekker Anna F. Lau Pavel Khil Robin T. Odom Clay Deming Morgan Park Pamela J. Thomas David K. Henderson Tara N. Palmore Julia A. Segre Karen M. Frank Genomic Analysis of Hospital Plumbing Reveals Diverse Reservoir of Bacterial Plasmids Conferring Carbapenem Resistance
description	ABSTRACT The hospital environment is a potential reservoir of bacteria with plasmids conferring carbapenem resistance. Our Hospital Epidemiology Service routinely performs extensive sampling of high-touch surfaces, sinks, and other locations in the hospital. Over a 2-year period, additional sampling was conducted at a broader range of locations, including housekeeping closets, wastewater from hospital internal pipes, and external manholes. We compared these data with previously collected information from 5 years of patient clinical and surveillance isolates. Whole-genome sequencing and analysis of 108 isolates provided comprehensive characterization of blaKPC/blaNDM-positive isolates, enabling an in-depth genetic comparison. Strikingly, despite a very low prevalence of patient infections with blaKPC-positive organisms, all samples from the intensive care unit pipe wastewater and external manholes contained carbapenemase-producing organisms (CPOs), suggesting a vast, resilient reservoir. We observed a diverse set of species and plasmids, and we noted species and susceptibility profile differences between environmental and patient populations of CPOs. However, there were plasmid backbones common to both populations, highlighting a potential environmental reservoir of mobile elements that may contribute to the spread of resistance genes. Clear associations between patient and environmental isolates were uncommon based on sequence analysis and epidemiology, suggesting reasonable infection control compliance at our institution. Nonetheless, a probable nosocomial transmission of Leclercia sp. from the housekeeping environment to a patient was detected by this extensive surveillance. These data and analyses further our understanding of CPOs in the hospital environment and are broadly relevant to the design of infection control strategies in many infrastructure settings. IMPORTANCE Carbapenemase-producing organisms (CPOs) are a global concern because of the morbidity and mortality associated with these resistant Gram-negative bacteria. Horizontal plasmid transfer spreads the resistance mechanism to new bacteria, and understanding the plasmid ecology of the hospital environment can assist in the design of control strategies to prevent nosocomial infections. A 5-year genomic and epidemiological survey was undertaken to study the CPOs in the patient-accessible environment, as well as in the plumbing system removed from the patient. This comprehensive survey revealed a vast, unappreciated reservoir of CPOs in wastewater, which was in contrast to the low positivity rate in both the patient population and the patient-accessible environment. While there were few patient-environmental isolate associations, there were plasmid backbones common to both populations. These results are relevant to all hospitals for which CPO colonization may not yet be defined through extensive surveillance.
format	article
author	Rebecca A. Weingarten Ryan C. Johnson Sean Conlan Amanda M. Ramsburg John P. Dekker Anna F. Lau Pavel Khil Robin T. Odom Clay Deming Morgan Park Pamela J. Thomas David K. Henderson Tara N. Palmore Julia A. Segre Karen M. Frank
author_facet	Rebecca A. Weingarten Ryan C. Johnson Sean Conlan Amanda M. Ramsburg John P. Dekker Anna F. Lau Pavel Khil Robin T. Odom Clay Deming Morgan Park Pamela J. Thomas David K. Henderson Tara N. Palmore Julia A. Segre Karen M. Frank
author_sort	Rebecca A. Weingarten
title	Genomic Analysis of Hospital Plumbing Reveals Diverse Reservoir of Bacterial Plasmids Conferring Carbapenem Resistance
title_short	Genomic Analysis of Hospital Plumbing Reveals Diverse Reservoir of Bacterial Plasmids Conferring Carbapenem Resistance
title_full	Genomic Analysis of Hospital Plumbing Reveals Diverse Reservoir of Bacterial Plasmids Conferring Carbapenem Resistance
title_fullStr	Genomic Analysis of Hospital Plumbing Reveals Diverse Reservoir of Bacterial Plasmids Conferring Carbapenem Resistance
title_full_unstemmed	Genomic Analysis of Hospital Plumbing Reveals Diverse Reservoir of Bacterial Plasmids Conferring Carbapenem Resistance
title_sort	genomic analysis of hospital plumbing reveals diverse reservoir of bacterial plasmids conferring carbapenem resistance
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/fcf915979d37441ea9ec74ff7535984d
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_version_	1718427315447267328

Genomic Analysis of Hospital Plumbing Reveals Diverse Reservoir of Bacterial Plasmids Conferring Carbapenem Resistance

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