Secrets of the Hospital Underbelly: Patterns of Abundance of Antimicrobial Resistance Genes in Hospital Wastewater Vary by Specific Antimicrobial and Bacterial Family
Background: Hospital wastewater is a major source of antimicrobial resistance (AMR) outflow into the environment. This study uses metagenomics to study how hospital clinical activity impacts antimicrobial resistance genes (ARGs) abundances in hospital wastewater.Methods: Sewage was collected over a...
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Frontiers Media S.A.
2021-09-01
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Series: | Frontiers in Microbiology |
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Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2021.703560/full |
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doaj-fe906ec030a64fd0bc970f26be4e9d15 |
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record_format |
Article |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Meghan R. Perry Meghan R. Perry Meghan R. Perry Hannah C. Lepper Luke McNally Luke McNally Bryan A. Wee Patrick Munk Amanda Warr Barbara Moore Pota Kalima Carol Philip Ana Maria de Roda Husman Frank M. Aarestrup Mark E. J. Woolhouse Bram A. D. van Bunnik |
spellingShingle |
Meghan R. Perry Meghan R. Perry Meghan R. Perry Hannah C. Lepper Luke McNally Luke McNally Bryan A. Wee Patrick Munk Amanda Warr Barbara Moore Pota Kalima Carol Philip Ana Maria de Roda Husman Frank M. Aarestrup Mark E. J. Woolhouse Bram A. D. van Bunnik Secrets of the Hospital Underbelly: Patterns of Abundance of Antimicrobial Resistance Genes in Hospital Wastewater Vary by Specific Antimicrobial and Bacterial Family Frontiers in Microbiology antimicrobial resistance metagenomics hospital waste water surveillance environmental risk resistance dissemination |
author_facet |
Meghan R. Perry Meghan R. Perry Meghan R. Perry Hannah C. Lepper Luke McNally Luke McNally Bryan A. Wee Patrick Munk Amanda Warr Barbara Moore Pota Kalima Carol Philip Ana Maria de Roda Husman Frank M. Aarestrup Mark E. J. Woolhouse Bram A. D. van Bunnik |
author_sort |
Meghan R. Perry |
title |
Secrets of the Hospital Underbelly: Patterns of Abundance of Antimicrobial Resistance Genes in Hospital Wastewater Vary by Specific Antimicrobial and Bacterial Family |
title_short |
Secrets of the Hospital Underbelly: Patterns of Abundance of Antimicrobial Resistance Genes in Hospital Wastewater Vary by Specific Antimicrobial and Bacterial Family |
title_full |
Secrets of the Hospital Underbelly: Patterns of Abundance of Antimicrobial Resistance Genes in Hospital Wastewater Vary by Specific Antimicrobial and Bacterial Family |
title_fullStr |
Secrets of the Hospital Underbelly: Patterns of Abundance of Antimicrobial Resistance Genes in Hospital Wastewater Vary by Specific Antimicrobial and Bacterial Family |
title_full_unstemmed |
Secrets of the Hospital Underbelly: Patterns of Abundance of Antimicrobial Resistance Genes in Hospital Wastewater Vary by Specific Antimicrobial and Bacterial Family |
title_sort |
secrets of the hospital underbelly: patterns of abundance of antimicrobial resistance genes in hospital wastewater vary by specific antimicrobial and bacterial family |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Microbiology |
issn |
1664-302X |
publishDate |
2021-09-01 |
description |
Background: Hospital wastewater is a major source of antimicrobial resistance (AMR) outflow into the environment. This study uses metagenomics to study how hospital clinical activity impacts antimicrobial resistance genes (ARGs) abundances in hospital wastewater.Methods: Sewage was collected over a 24-h period from multiple wastewater collection points (CPs) representing different specialties within a tertiary hospital site and simultaneously from community sewage works. High throughput shotgun sequencing was performed using Illumina HiSeq4000. ARG abundances were correlated to hospital antimicrobial usage (AMU), data on clinical activity and resistance prevalence in clinical isolates.Results: Microbiota and ARG composition varied between CPs and overall ARG abundance was higher in hospital wastewater than in community influent. ARG and microbiota compositions were correlated (Procrustes analysis, p=0.014). Total antimicrobial usage was not associated with higher ARG abundance in wastewater. However, there was a small positive association between resistance genes and antimicrobial usage matched to ARG phenotype (IRR 1.11, CI 1.06–1.16, p<0.001). Furthermore, analyzing carbapenem and vancomycin resistance separately indicated that counts of ARGs to these antimicrobials were positively associated with their increased usage [carbapenem rate ratio (RR) 1.91, 95% CI 1.01–3.72, p=0.07, and vancomycin RR 10.25, CI 2.32–49.10, p<0.01]. Overall, ARG abundance within hospital wastewater did not reflect resistance patterns in clinical isolates from concurrent hospital inpatients. However, for clinical isolates of the family Enterococcaceae and Staphylococcaceae, there was a positive relationship with wastewater ARG abundance [odds ratio (OR) 1.62, CI 1.33–2.00, p<0.001, and OR 1.65, CI 1.21–2.30, p=0.006 respectively].Conclusion: We found that the relationship between hospital wastewater ARGs and antimicrobial usage or clinical isolate resistance varies by specific antimicrobial and bacterial family studied. One explanation, we consider is that relationships observed from multiple departments within a single hospital site will be detectable only for ARGs against parenteral antimicrobials uniquely used in the hospital setting. Our work highlights that using metagenomics to identify the full range of ARGs in hospital wastewater is a useful surveillance tool to monitor hospital ARG carriage and outflow and guide environmental policy on AMR. |
topic |
antimicrobial resistance metagenomics hospital waste water surveillance environmental risk resistance dissemination |
url |
https://www.frontiersin.org/articles/10.3389/fmicb.2021.703560/full |
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doaj-fe906ec030a64fd0bc970f26be4e9d152021-09-10T05:27:00ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2021-09-011210.3389/fmicb.2021.703560703560Secrets of the Hospital Underbelly: Patterns of Abundance of Antimicrobial Resistance Genes in Hospital Wastewater Vary by Specific Antimicrobial and Bacterial FamilyMeghan R. Perry0Meghan R. Perry1Meghan R. Perry2Hannah C. Lepper3Luke McNally4Luke McNally5Bryan A. Wee6Patrick Munk7Amanda Warr8Barbara Moore9Pota Kalima10Carol Philip11Ana Maria de Roda Husman12Frank M. Aarestrup13Mark E. J. Woolhouse14Bram A. D. van Bunnik15Usher Institute, University of Edinburgh, Edinburgh, United KingdomNHS Lothian Infection Service, Edinburgh Clinical Infection Research Group, Edinburgh, United KingdomCentre for Inflammation Research, University of Edinburgh, Edinburgh, United KingdomUsher Institute, University of Edinburgh, Edinburgh, United KingdomCentre for Synthetic and Systems Biology, School of Biological Sciences, University of Edinburgh, Edinburgh, United KingdomSchool of Biological Sciences, Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, United KingdomUsher Institute, University of Edinburgh, Edinburgh, United KingdomNational Food Institute, Technical University of Denmark, Kongens Lyngby, DenmarkRoslin Institute, University of Edinburgh, Edinburgh, United KingdomNHS Lothian Infection Service, Edinburgh Clinical Infection Research Group, Edinburgh, United KingdomNHS Lothian Infection Service, Edinburgh Clinical Infection Research Group, Edinburgh, United KingdomNHS Lothian Infection Service, Edinburgh Clinical Infection Research Group, Edinburgh, United KingdomNational Institute for Public Health and the Environment (RIVM), Bilthoven, NetherlandsNational Food Institute, Technical University of Denmark, Kongens Lyngby, DenmarkUsher Institute, University of Edinburgh, Edinburgh, United KingdomUsher Institute, University of Edinburgh, Edinburgh, United KingdomBackground: Hospital wastewater is a major source of antimicrobial resistance (AMR) outflow into the environment. This study uses metagenomics to study how hospital clinical activity impacts antimicrobial resistance genes (ARGs) abundances in hospital wastewater.Methods: Sewage was collected over a 24-h period from multiple wastewater collection points (CPs) representing different specialties within a tertiary hospital site and simultaneously from community sewage works. High throughput shotgun sequencing was performed using Illumina HiSeq4000. ARG abundances were correlated to hospital antimicrobial usage (AMU), data on clinical activity and resistance prevalence in clinical isolates.Results: Microbiota and ARG composition varied between CPs and overall ARG abundance was higher in hospital wastewater than in community influent. ARG and microbiota compositions were correlated (Procrustes analysis, p=0.014). Total antimicrobial usage was not associated with higher ARG abundance in wastewater. However, there was a small positive association between resistance genes and antimicrobial usage matched to ARG phenotype (IRR 1.11, CI 1.06–1.16, p<0.001). Furthermore, analyzing carbapenem and vancomycin resistance separately indicated that counts of ARGs to these antimicrobials were positively associated with their increased usage [carbapenem rate ratio (RR) 1.91, 95% CI 1.01–3.72, p=0.07, and vancomycin RR 10.25, CI 2.32–49.10, p<0.01]. Overall, ARG abundance within hospital wastewater did not reflect resistance patterns in clinical isolates from concurrent hospital inpatients. However, for clinical isolates of the family Enterococcaceae and Staphylococcaceae, there was a positive relationship with wastewater ARG abundance [odds ratio (OR) 1.62, CI 1.33–2.00, p<0.001, and OR 1.65, CI 1.21–2.30, p=0.006 respectively].Conclusion: We found that the relationship between hospital wastewater ARGs and antimicrobial usage or clinical isolate resistance varies by specific antimicrobial and bacterial family studied. One explanation, we consider is that relationships observed from multiple departments within a single hospital site will be detectable only for ARGs against parenteral antimicrobials uniquely used in the hospital setting. Our work highlights that using metagenomics to identify the full range of ARGs in hospital wastewater is a useful surveillance tool to monitor hospital ARG carriage and outflow and guide environmental policy on AMR.https://www.frontiersin.org/articles/10.3389/fmicb.2021.703560/fullantimicrobial resistancemetagenomicshospital waste watersurveillanceenvironmental riskresistance dissemination |