Bacterial colonization dynamics and antibiotic resistance gene dissemination in the hospital environment after first patient occupancy: a longitudinal metagenetic study

Abstract Background Humans spend the bulk of their time in indoor environments. This space is shared with an indoor ecosystem of microorganisms, which are in continuous exchange with the human inhabitants. In the particular case of hospitals, the environmental microorganisms may influence patient re...

Full description

Bibliographic Details
Main Authors: Tilman E. Klassert, Rasmus Leistner, Cristina Zubiria-Barrera, Magdalena Stock, Mercedes López, Robert Neubert, Dominik Driesch, Petra Gastmeier, Hortense Slevogt
Format: Article
Language:English
Published: BMC 2021-08-01
Series:Microbiome
Online Access:https://doi.org/10.1186/s40168-021-01109-7
id doaj-9c8607ade5b14e08a08c53849621c562
record_format Article
spelling doaj-9c8607ade5b14e08a08c53849621c5622021-08-15T11:10:19ZengBMCMicrobiome2049-26182021-08-019111710.1186/s40168-021-01109-7Bacterial colonization dynamics and antibiotic resistance gene dissemination in the hospital environment after first patient occupancy: a longitudinal metagenetic studyTilman E. Klassert0Rasmus Leistner1Cristina Zubiria-Barrera2Magdalena Stock3Mercedes López4Robert Neubert5Dominik Driesch6Petra Gastmeier7Hortense Slevogt8Jena University Hospital, ZIK Septomics, Host SeptomicsInstitute for Hygiene and Environmental Medicine and Department for Medicine (Gastroenterology, Infectious diseases, Rheumatology), Charité – Universitätsmedizin BerlinJena University Hospital, ZIK Septomics, Host SeptomicsJena University Hospital, ZIK Septomics, Host SeptomicsUniversity Institute of Tropical Diseases and Public Health of the Canary Islands, University of La LagunaJena University Hospital, ZIK Septomics, Host SeptomicsBioControl Jena GmbHInstitute for Hygiene and Environmental Medicine, Charité–UniversitätsmedizinJena University Hospital, ZIK Septomics, Host SeptomicsAbstract Background Humans spend the bulk of their time in indoor environments. This space is shared with an indoor ecosystem of microorganisms, which are in continuous exchange with the human inhabitants. In the particular case of hospitals, the environmental microorganisms may influence patient recovery and outcome. An understanding of the bacterial community structure in the hospital environment is pivotal for the prevention of hospital-acquired infections and the dissemination of antibiotic resistance genes. In this study, we performed a longitudinal metagenetic approach in a newly opened ward at the Charité Hospital (Berlin) to characterize the dynamics of the bacterial colonization process in the hospital environment after first patient occupancy. Results The sequencing data showed a site-specific taxonomic succession, which led to stable community structures after only a few weeks. This data was further supported by network analysis and beta-diversity metrics. Furthermore, the fast colonization process was characterized by a significant increase of the bacterial biomass and its alpha-diversity. The compositional dynamics could be linked to the exchange with the patient microbiota. Over a time course of 30 weeks, we did not detect a rise of pathogenic bacteria in the hospital environment, but a significant increase of antibiotic resistance determinants on the hospital floor. Conclusions The results presented in this study provide new insights into different aspects of the environmental microbiome in the clinical setting, and will help to adopt infection control strategies in hospitals and health care-related buildings. Video Abstracthttps://doi.org/10.1186/s40168-021-01109-7
collection DOAJ
language English
format Article
sources DOAJ
author Tilman E. Klassert
Rasmus Leistner
Cristina Zubiria-Barrera
Magdalena Stock
Mercedes López
Robert Neubert
Dominik Driesch
Petra Gastmeier
Hortense Slevogt
spellingShingle Tilman E. Klassert
Rasmus Leistner
Cristina Zubiria-Barrera
Magdalena Stock
Mercedes López
Robert Neubert
Dominik Driesch
Petra Gastmeier
Hortense Slevogt
Bacterial colonization dynamics and antibiotic resistance gene dissemination in the hospital environment after first patient occupancy: a longitudinal metagenetic study
Microbiome
author_facet Tilman E. Klassert
Rasmus Leistner
Cristina Zubiria-Barrera
Magdalena Stock
Mercedes López
Robert Neubert
Dominik Driesch
Petra Gastmeier
Hortense Slevogt
author_sort Tilman E. Klassert
title Bacterial colonization dynamics and antibiotic resistance gene dissemination in the hospital environment after first patient occupancy: a longitudinal metagenetic study
title_short Bacterial colonization dynamics and antibiotic resistance gene dissemination in the hospital environment after first patient occupancy: a longitudinal metagenetic study
title_full Bacterial colonization dynamics and antibiotic resistance gene dissemination in the hospital environment after first patient occupancy: a longitudinal metagenetic study
title_fullStr Bacterial colonization dynamics and antibiotic resistance gene dissemination in the hospital environment after first patient occupancy: a longitudinal metagenetic study
title_full_unstemmed Bacterial colonization dynamics and antibiotic resistance gene dissemination in the hospital environment after first patient occupancy: a longitudinal metagenetic study
title_sort bacterial colonization dynamics and antibiotic resistance gene dissemination in the hospital environment after first patient occupancy: a longitudinal metagenetic study
publisher BMC
series Microbiome
issn 2049-2618
publishDate 2021-08-01
description Abstract Background Humans spend the bulk of their time in indoor environments. This space is shared with an indoor ecosystem of microorganisms, which are in continuous exchange with the human inhabitants. In the particular case of hospitals, the environmental microorganisms may influence patient recovery and outcome. An understanding of the bacterial community structure in the hospital environment is pivotal for the prevention of hospital-acquired infections and the dissemination of antibiotic resistance genes. In this study, we performed a longitudinal metagenetic approach in a newly opened ward at the Charité Hospital (Berlin) to characterize the dynamics of the bacterial colonization process in the hospital environment after first patient occupancy. Results The sequencing data showed a site-specific taxonomic succession, which led to stable community structures after only a few weeks. This data was further supported by network analysis and beta-diversity metrics. Furthermore, the fast colonization process was characterized by a significant increase of the bacterial biomass and its alpha-diversity. The compositional dynamics could be linked to the exchange with the patient microbiota. Over a time course of 30 weeks, we did not detect a rise of pathogenic bacteria in the hospital environment, but a significant increase of antibiotic resistance determinants on the hospital floor. Conclusions The results presented in this study provide new insights into different aspects of the environmental microbiome in the clinical setting, and will help to adopt infection control strategies in hospitals and health care-related buildings. Video Abstract
url https://doi.org/10.1186/s40168-021-01109-7
work_keys_str_mv AT tilmaneklassert bacterialcolonizationdynamicsandantibioticresistancegenedisseminationinthehospitalenvironmentafterfirstpatientoccupancyalongitudinalmetageneticstudy
AT rasmusleistner bacterialcolonizationdynamicsandantibioticresistancegenedisseminationinthehospitalenvironmentafterfirstpatientoccupancyalongitudinalmetageneticstudy
AT cristinazubiriabarrera bacterialcolonizationdynamicsandantibioticresistancegenedisseminationinthehospitalenvironmentafterfirstpatientoccupancyalongitudinalmetageneticstudy
AT magdalenastock bacterialcolonizationdynamicsandantibioticresistancegenedisseminationinthehospitalenvironmentafterfirstpatientoccupancyalongitudinalmetageneticstudy
AT mercedeslopez bacterialcolonizationdynamicsandantibioticresistancegenedisseminationinthehospitalenvironmentafterfirstpatientoccupancyalongitudinalmetageneticstudy
AT robertneubert bacterialcolonizationdynamicsandantibioticresistancegenedisseminationinthehospitalenvironmentafterfirstpatientoccupancyalongitudinalmetageneticstudy
AT dominikdriesch bacterialcolonizationdynamicsandantibioticresistancegenedisseminationinthehospitalenvironmentafterfirstpatientoccupancyalongitudinalmetageneticstudy
AT petragastmeier bacterialcolonizationdynamicsandantibioticresistancegenedisseminationinthehospitalenvironmentafterfirstpatientoccupancyalongitudinalmetageneticstudy
AT hortenseslevogt bacterialcolonizationdynamicsandantibioticresistancegenedisseminationinthehospitalenvironmentafterfirstpatientoccupancyalongitudinalmetageneticstudy
_version_ 1721207109603819520