Human microbiota drives hospital-associated antimicrobial resistance dissemination in the urban environment and mirrors patient case rates
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.
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) |
_version_ | 1807522799383740416 |
---|---|
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. |
dc.format.mimetype.es.fl_str_mv | application/pdf |
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 |
format | article |
id | COLIBRI_6cd9465c79354c260e3054bdabb6b4ab |
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 2049-2618 10.1186/s40168-022-01407-8 |
instacron_str | Universidad de la República |
institution | Universidad de la República |
instname_str | Universidad de la República |
language | eng |
language_invalid_str_mv | en_US |
network_acronym_str | COLIBRI |
network_name_str | COLIBRI |
oai_identifier_str | oai:colibri.udelar.edu.uy:20.500.12008/39941 |
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 |