TY - JOUR
T1 - Secrets of the Hospital Underbelly
T2 - Patterns of Abundance of Antimicrobial Resistance Genes in Hospital Wastewater Vary by Specific Antimicrobial and Bacterial Family
AU - Perry, Meghan R.
AU - Lepper, Hannah C.
AU - McNally, Luke
AU - Wee, Bryan A.
AU - Munk, Patrick
AU - Warr, Amanda
AU - Moore, Barbara
AU - Kalima, Pota
AU - Philip, Carol
AU - de Roda Husman, Ana Maria
AU - Aarestrup, Frank M.
AU - Woolhouse, Mark E.J.
AU - van Bunnik, Bram A.D.
PY - 2021
Y1 - 2021
N2 - 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.
AB - 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.
KW - Antimicrobial resistance
KW - Metagenomics
KW - Hospital waste water
KW - Surveillance
KW - Environmental risk
KW - Resistance dissemination
KW - Antibiotic usage
U2 - 10.3389/fmicb.2021.703560
DO - 10.3389/fmicb.2021.703560
M3 - Journal article
C2 - 34566912
SN - 1664-302X
VL - 12
JO - Frontiers in Microbiology
JF - Frontiers in Microbiology
M1 - 703560
ER -