Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates

Salazar González, María Cecilia - Giménez Martínez, Matías - Riera Faraone, Nadia - Parada, Andrés - Puig Boschetti, Josefina - Galiana, Antonio - Grill, Fabio - Vieytes, Mariela - Antelo Gutiérrez, Verónica Beatriz - D’Alessandro, Bruno - Risso, Jimena - Iraola, Gregorio - Mason, Christopher E.

Resumen:

Background: The microbial community composition of urban environments is primarily determined by human activity. The use of metagenomics to explore how microbial communities are shaped in a city provides a novel input that can improve decisions on public health measures, architectural design, and urban resilience. Of note, the sewage system in a city acts as a complex reservoir of bacteria, pharmaceuticals, and antimicrobial resistant (AMR) genes that can be an important source of epidemiological information. Hospital effluents are rich in patient-derived bacteria and can thus readily become a birthplace and hotspot reservoir for antibiotic resistant pathogens which are eventually incorporated into the environment. Yet, the scope to which nosocomial outbreaks impact the urban environment is still poorly understood. Results: In this work, we extensively show that different urban waters from creeks, beaches, sewage spillways and collector pipes enclose discrete microbial communities that are characterized by a differential degree of contamination and admixture with human-derived bacteria. The abundance of human bacteria correlates with the abundance of AMR genes in the environment, with beta-lactamases being the top-contributing class to distinguish low vs.highly-impacted urban environments. Indeed, the abundance of beta-lactamase resistance and carbapenem resistance determinants in the urban environment significantly increased in a 1-year period. This was in line with a pronounced increase of nosocomial carbapenem-resistant infections reported during the same period that was mainly driven by an outbreak-causing, carbapenemase-producing Klebsiella pneumoniae (KPC) ST-11 strain. Genome-resolved metagenomics of urban waters before and after this outbreak, coupled with high-resolution whole-genome sequencing, confirmed the dissemination of the ST-11 strain and a novel KPC megaplasmid from the hospital to the urban environment. City-wide analysis showed that geospatial dissemination of the KPC megaplasmid in the urban environment inversely depended on the sewage system infrastructure. Conclusions: We show how urban metagenomics and outbreak genomic surveillance can be coupled to generate relevant information for infection control, antibiotic stewardship, and pathogen epidemiology. Our results highlight.


Detalles Bibliográficos
2022
ANII: POS_FSA_2019_1_1008860.
Antimicrobial resistance
Urban metagenomics
Nanopore sequencing
Carbapenem resistance
Nosocomial outbreak
KPC
Urban wastewater
Inglés
Universidad de la República
COLIBRI
https://hdl.handle.net/20.500.12008/39941
Acceso abierto
Licencia Creative Commons Atribución (CC - By 4.0)
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author Salazar González, María Cecilia
author2 Giménez Martínez, Matías
Riera Faraone, Nadia
Parada, Andrés
Puig Boschetti, Josefina
Galiana, Antonio
Grill, Fabio
Vieytes, Mariela
Antelo Gutiérrez, Verónica Beatriz
D’Alessandro, Bruno
Risso, Jimena
Iraola, Gregorio
Mason, Christopher E.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author_facet Salazar González, María Cecilia
Giménez Martínez, Matías
Riera Faraone, Nadia
Parada, Andrés
Puig Boschetti, Josefina
Galiana, Antonio
Grill, Fabio
Vieytes, Mariela
Antelo Gutiérrez, Verónica Beatriz
D’Alessandro, Bruno
Risso, Jimena
Iraola, Gregorio
Mason, Christopher E.
author_role author
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collection COLIBRI
dc.contributor.filiacion.none.fl_str_mv Salazar González María Cecilia, Instituto Pasteur (Montevideo).
Giménez Martínez Matías, Instituto Pasteur (Montevideo).
Riera Faraone Nadia, Instituto Pasteur (Montevideo).
Parada Andrés, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.
Puig Boschetti Josefina, Instituto Pasteur (Montevideo).
Galiana Antonio, Hospital Maciel (Montevideo)
Grill Fabio, Hospital Maciel (Montevideo)
Vieytes Mariela, Hospital Maciel (Montevideo)
Antelo Gutiérrez Verónica Beatriz, Instituto Pasteur (Montevideo).
D’Alessandro Bruno, Universidad de la República (Uruguay). Instituto de Higiene, Facultad de Medicina.
Risso Jimena, Intendencia de Montevideo (Uruguay).
Iraola Gregorio, Instituto Pasteur (Montevideo).
Mason Christopher E.
dc.creator.none.fl_str_mv Salazar González, María Cecilia
Giménez Martínez, Matías
Riera Faraone, Nadia
Parada, Andrés
Puig Boschetti, Josefina
Galiana, Antonio
Grill, Fabio
Vieytes, Mariela
Antelo Gutiérrez, Verónica Beatriz
D’Alessandro, Bruno
Risso, Jimena
Iraola, Gregorio
Mason, Christopher E.
dc.date.accessioned.none.fl_str_mv 2023-09-18T15:18:52Z
dc.date.available.none.fl_str_mv 2023-09-18T15:18:52Z
dc.date.issued.none.fl_str_mv 2022
dc.description.abstract.none.fl_txt_mv Background: The microbial community composition of urban environments is primarily determined by human activity. The use of metagenomics to explore how microbial communities are shaped in a city provides a novel input that can improve decisions on public health measures, architectural design, and urban resilience. Of note, the sewage system in a city acts as a complex reservoir of bacteria, pharmaceuticals, and antimicrobial resistant (AMR) genes that can be an important source of epidemiological information. Hospital effluents are rich in patient-derived bacteria and can thus readily become a birthplace and hotspot reservoir for antibiotic resistant pathogens which are eventually incorporated into the environment. Yet, the scope to which nosocomial outbreaks impact the urban environment is still poorly understood. Results: In this work, we extensively show that different urban waters from creeks, beaches, sewage spillways and collector pipes enclose discrete microbial communities that are characterized by a differential degree of contamination and admixture with human-derived bacteria. The abundance of human bacteria correlates with the abundance of AMR genes in the environment, with beta-lactamases being the top-contributing class to distinguish low vs.highly-impacted urban environments. Indeed, the abundance of beta-lactamase resistance and carbapenem resistance determinants in the urban environment significantly increased in a 1-year period. This was in line with a pronounced increase of nosocomial carbapenem-resistant infections reported during the same period that was mainly driven by an outbreak-causing, carbapenemase-producing Klebsiella pneumoniae (KPC) ST-11 strain. Genome-resolved metagenomics of urban waters before and after this outbreak, coupled with high-resolution whole-genome sequencing, confirmed the dissemination of the ST-11 strain and a novel KPC megaplasmid from the hospital to the urban environment. City-wide analysis showed that geospatial dissemination of the KPC megaplasmid in the urban environment inversely depended on the sewage system infrastructure. Conclusions: We show how urban metagenomics and outbreak genomic surveillance can be coupled to generate relevant information for infection control, antibiotic stewardship, and pathogen epidemiology. Our results highlight.
dc.description.sponsorship.none.fl_txt_mv ANII: POS_FSA_2019_1_1008860.
dc.format.extent.es.fl_str_mv 12 h.
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dc.identifier.citation.es.fl_str_mv Salazar González, M, Giménez Martínez, M, Riera Faraone, N, [y otros autores]. "Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates". Microbiome. [en línea] 2022, 10: 208. 12 h. DOI: 10.1186/s40168-022-01407-8
dc.identifier.doi.none.fl_str_mv 10.1186/s40168-022-01407-8
dc.identifier.issn.none.fl_str_mv 2049-2618
dc.identifier.uri.none.fl_str_mv https://hdl.handle.net/20.500.12008/39941
dc.language.iso.none.fl_str_mv en_US
eng
dc.publisher.es.fl_str_mv Springer Nature
dc.relation.ispartof.es.fl_str_mv Microbiome, 2022, 10: 208.
dc.rights.license.none.fl_str_mv Licencia Creative Commons Atribución (CC - By 4.0)
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
dc.source.none.fl_str_mv reponame:COLIBRI
instname:Universidad de la República
instacron:Universidad de la República
dc.subject.es.fl_str_mv Antimicrobial resistance
Urban metagenomics
Nanopore sequencing
Carbapenem resistance
Nosocomial outbreak
KPC
Urban wastewater
dc.title.none.fl_str_mv Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates
dc.type.es.fl_str_mv Artículo
dc.type.none.fl_str_mv info:eu-repo/semantics/article
dc.type.version.none.fl_str_mv info:eu-repo/semantics/publishedVersion
description Background: The microbial community composition of urban environments is primarily determined by human activity. The use of metagenomics to explore how microbial communities are shaped in a city provides a novel input that can improve decisions on public health measures, architectural design, and urban resilience. Of note, the sewage system in a city acts as a complex reservoir of bacteria, pharmaceuticals, and antimicrobial resistant (AMR) genes that can be an important source of epidemiological information. Hospital effluents are rich in patient-derived bacteria and can thus readily become a birthplace and hotspot reservoir for antibiotic resistant pathogens which are eventually incorporated into the environment. Yet, the scope to which nosocomial outbreaks impact the urban environment is still poorly understood. Results: In this work, we extensively show that different urban waters from creeks, beaches, sewage spillways and collector pipes enclose discrete microbial communities that are characterized by a differential degree of contamination and admixture with human-derived bacteria. The abundance of human bacteria correlates with the abundance of AMR genes in the environment, with beta-lactamases being the top-contributing class to distinguish low vs.highly-impacted urban environments. Indeed, the abundance of beta-lactamase resistance and carbapenem resistance determinants in the urban environment significantly increased in a 1-year period. This was in line with a pronounced increase of nosocomial carbapenem-resistant infections reported during the same period that was mainly driven by an outbreak-causing, carbapenemase-producing Klebsiella pneumoniae (KPC) ST-11 strain. Genome-resolved metagenomics of urban waters before and after this outbreak, coupled with high-resolution whole-genome sequencing, confirmed the dissemination of the ST-11 strain and a novel KPC megaplasmid from the hospital to the urban environment. City-wide analysis showed that geospatial dissemination of the KPC megaplasmid in the urban environment inversely depended on the sewage system infrastructure. Conclusions: We show how urban metagenomics and outbreak genomic surveillance can be coupled to generate relevant information for infection control, antibiotic stewardship, and pathogen epidemiology. Our results highlight.
eu_rights_str_mv openAccess
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identifier_str_mv Salazar González, M, Giménez Martínez, M, Riera Faraone, N, [y otros autores]. "Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates". Microbiome. [en línea] 2022, 10: 208. 12 h. DOI: 10.1186/s40168-022-01407-8
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publishDate 2022
reponame_str COLIBRI
repository.mail.fl_str_mv mabel.seroubian@seciu.edu.uy
repository.name.fl_str_mv COLIBRI - Universidad de la República
repository_id_str 4771
rights_invalid_str_mv Licencia Creative Commons Atribución (CC - By 4.0)
spelling Salazar González María Cecilia, Instituto Pasteur (Montevideo).Giménez Martínez Matías, Instituto Pasteur (Montevideo).Riera Faraone Nadia, Instituto Pasteur (Montevideo).Parada Andrés, Universidad de la República (Uruguay). Facultad de Ciencias. Instituto de Biología.Puig Boschetti Josefina, Instituto Pasteur (Montevideo).Galiana Antonio, Hospital Maciel (Montevideo)Grill Fabio, Hospital Maciel (Montevideo)Vieytes Mariela, Hospital Maciel (Montevideo)Antelo Gutiérrez Verónica Beatriz, Instituto Pasteur (Montevideo).D’Alessandro Bruno, Universidad de la República (Uruguay). Instituto de Higiene, Facultad de Medicina.Risso Jimena, Intendencia de Montevideo (Uruguay).Iraola Gregorio, Instituto Pasteur (Montevideo).Mason Christopher E.2023-09-18T15:18:52Z2023-09-18T15:18:52Z2022Salazar González, M, Giménez Martínez, M, Riera Faraone, N, [y otros autores]. "Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates". Microbiome. [en línea] 2022, 10: 208. 12 h. DOI: 10.1186/s40168-022-01407-82049-2618https://hdl.handle.net/20.500.12008/3994110.1186/s40168-022-01407-8Background: The microbial community composition of urban environments is primarily determined by human activity. The use of metagenomics to explore how microbial communities are shaped in a city provides a novel input that can improve decisions on public health measures, architectural design, and urban resilience. Of note, the sewage system in a city acts as a complex reservoir of bacteria, pharmaceuticals, and antimicrobial resistant (AMR) genes that can be an important source of epidemiological information. Hospital effluents are rich in patient-derived bacteria and can thus readily become a birthplace and hotspot reservoir for antibiotic resistant pathogens which are eventually incorporated into the environment. Yet, the scope to which nosocomial outbreaks impact the urban environment is still poorly understood. Results: In this work, we extensively show that different urban waters from creeks, beaches, sewage spillways and collector pipes enclose discrete microbial communities that are characterized by a differential degree of contamination and admixture with human-derived bacteria. The abundance of human bacteria correlates with the abundance of AMR genes in the environment, with beta-lactamases being the top-contributing class to distinguish low vs.highly-impacted urban environments. Indeed, the abundance of beta-lactamase resistance and carbapenem resistance determinants in the urban environment significantly increased in a 1-year period. This was in line with a pronounced increase of nosocomial carbapenem-resistant infections reported during the same period that was mainly driven by an outbreak-causing, carbapenemase-producing Klebsiella pneumoniae (KPC) ST-11 strain. Genome-resolved metagenomics of urban waters before and after this outbreak, coupled with high-resolution whole-genome sequencing, confirmed the dissemination of the ST-11 strain and a novel KPC megaplasmid from the hospital to the urban environment. City-wide analysis showed that geospatial dissemination of the KPC megaplasmid in the urban environment inversely depended on the sewage system infrastructure. Conclusions: We show how urban metagenomics and outbreak genomic surveillance can be coupled to generate relevant information for infection control, antibiotic stewardship, and pathogen epidemiology. Our results highlight.Submitted by Farías Verónica (vfarias@fcien.edu.uy) on 2023-09-01T18:34:35Z No. of bitstreams: 2 license_rdf: 19875 bytes, checksum: 9fdbed07f52437945402c4e70fa4773e (MD5) 101186s12879022072620.pdf: 2247475 bytes, checksum: 5d0179b2a9e054435af5b346ddcdd5e7 (MD5)Rejected by Faget Cecilia (lfaget@fcien.edu.uy), reason: on 2023-09-18T12:15:49Z (GMT)Submitted by Farías Verónica (vfarias@fcien.edu.uy) on 2023-09-18T12:59:07Z No. of bitstreams: 2 license_rdf: 19875 bytes, checksum: 9fdbed07f52437945402c4e70fa4773e (MD5) 101186s40168022014078.pdf: 4005341 bytes, checksum: deb13e67d58dffb416338a77b817ea57 (MD5)Approved for entry into archive by Faget Cecilia (lfaget@fcien.edu.uy) on 2023-09-18T13:23:56Z (GMT) No. of bitstreams: 2 license_rdf: 19875 bytes, checksum: 9fdbed07f52437945402c4e70fa4773e (MD5) 101186s40168022014078.pdf: 4005341 bytes, checksum: deb13e67d58dffb416338a77b817ea57 (MD5)Made available in DSpace by Seroubian Mabel (mabel.seroubian@seciu.edu.uy) on 2023-09-18T15:18:52Z (GMT). No. of bitstreams: 2 license_rdf: 19875 bytes, checksum: 9fdbed07f52437945402c4e70fa4773e (MD5) 101186s40168022014078.pdf: 4005341 bytes, checksum: deb13e67d58dffb416338a77b817ea57 (MD5) Previous issue date: 2022ANII: POS_FSA_2019_1_1008860.12 h.application/pdfen_USengSpringer NatureMicrobiome, 2022, 10: 208.Las obras depositadas en el Repositorio se rigen por la Ordenanza de los Derechos de la Propiedad Intelectual de la Universidad de la República.(Res. Nº 91 de C.D.C. de 8/III/1994 – D.O. 7/IV/1994) y por la Ordenanza del Repositorio Abierto de la Universidad de la República (Res. Nº 16 de C.D.C. de 07/10/2014)info:eu-repo/semantics/openAccessLicencia Creative Commons Atribución (CC - By 4.0)Antimicrobial resistanceUrban metagenomicsNanopore sequencingCarbapenem resistanceNosocomial outbreakKPCUrban wastewaterHuman microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case ratesArtículoinfo:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionreponame:COLIBRIinstname:Universidad de la Repúblicainstacron:Universidad de la RepúblicaSalazar González, María CeciliaGiménez Martínez, MatíasRiera Faraone, NadiaParada, AndrésPuig Boschetti, JosefinaGaliana, AntonioGrill, FabioVieytes, MarielaAntelo Gutiérrez, Verónica BeatrizD’Alessandro, BrunoRisso, JimenaIraola, GregorioMason, Christopher E.LICENSElicense.txtlicense.txttext/plain; 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- Universidad de la Repúblicafalse
spellingShingle Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates
Salazar González, María Cecilia
Antimicrobial resistance
Urban metagenomics
Nanopore sequencing
Carbapenem resistance
Nosocomial outbreak
KPC
Urban wastewater
status_str publishedVersion
title Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates
title_full Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates
title_fullStr Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates
title_full_unstemmed Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates
title_short Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates
title_sort Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates
topic Antimicrobial resistance
Urban metagenomics
Nanopore sequencing
Carbapenem resistance
Nosocomial outbreak
KPC
Urban wastewater
url https://hdl.handle.net/20.500.12008/39941