Wastewater treatment plants, an “escape gate” for ESCAPE pathogens

Antibiotics are an essential tool of modern medicine, contributing to significantly decreasing mortality and morbidity rates from infectious diseases. However, persistent misuse of these drugs has accelerated the evolution of antibiotic resistance, negatively impacting clinical practice. The environ...

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Main Authors: Luminita Gabriela Marutescu, Marcela Popa, Irina Gheorghe-Barbu, Ilda Czobor Barbu, Daloha Rodríguez-Molina, Fanny Berglund, Hetty Blaak, Carl-Fredrik Flach, Merel Aurora Kemper, Beate Spießberger, Laura Wengenroth, D. G. Joakim Larsson, Dennis Nowak, Katja Radon, Ana Maria de Roda Husman, Andreas Wieser, Heike Schmitt, Gratiela Pircalabioru Gradisteanu, Corneliu Ovidiu Vrancianu, Mariana Carmen Chifiriuc
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-05-01
Series:Frontiers in Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fmicb.2023.1193907/full
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author Luminita Gabriela Marutescu
Luminita Gabriela Marutescu
Marcela Popa
Irina Gheorghe-Barbu
Irina Gheorghe-Barbu
Ilda Czobor Barbu
Ilda Czobor Barbu
Daloha Rodríguez-Molina
Daloha Rodríguez-Molina
Daloha Rodríguez-Molina
Fanny Berglund
Fanny Berglund
Hetty Blaak
Carl-Fredrik Flach
Carl-Fredrik Flach
Merel Aurora Kemper
Beate Spießberger
Beate Spießberger
Beate Spießberger
Laura Wengenroth
D. G. Joakim Larsson
D. G. Joakim Larsson
Dennis Nowak
Dennis Nowak
Katja Radon
Ana Maria de Roda Husman
Andreas Wieser
Andreas Wieser
Andreas Wieser
Heike Schmitt
Gratiela Pircalabioru Gradisteanu
Gratiela Pircalabioru Gradisteanu
Gratiela Pircalabioru Gradisteanu
Corneliu Ovidiu Vrancianu
Mariana Carmen Chifiriuc
Mariana Carmen Chifiriuc
Mariana Carmen Chifiriuc
author_facet Luminita Gabriela Marutescu
Luminita Gabriela Marutescu
Marcela Popa
Irina Gheorghe-Barbu
Irina Gheorghe-Barbu
Ilda Czobor Barbu
Ilda Czobor Barbu
Daloha Rodríguez-Molina
Daloha Rodríguez-Molina
Daloha Rodríguez-Molina
Fanny Berglund
Fanny Berglund
Hetty Blaak
Carl-Fredrik Flach
Carl-Fredrik Flach
Merel Aurora Kemper
Beate Spießberger
Beate Spießberger
Beate Spießberger
Laura Wengenroth
D. G. Joakim Larsson
D. G. Joakim Larsson
Dennis Nowak
Dennis Nowak
Katja Radon
Ana Maria de Roda Husman
Andreas Wieser
Andreas Wieser
Andreas Wieser
Heike Schmitt
Gratiela Pircalabioru Gradisteanu
Gratiela Pircalabioru Gradisteanu
Gratiela Pircalabioru Gradisteanu
Corneliu Ovidiu Vrancianu
Mariana Carmen Chifiriuc
Mariana Carmen Chifiriuc
Mariana Carmen Chifiriuc
author_sort Luminita Gabriela Marutescu
collection DOAJ
description Antibiotics are an essential tool of modern medicine, contributing to significantly decreasing mortality and morbidity rates from infectious diseases. However, persistent misuse of these drugs has accelerated the evolution of antibiotic resistance, negatively impacting clinical practice. The environment contributes to both the evolution and transmission of resistance. From all anthropically polluted aquatic environments, wastewater treatment plants (WWTPs) are probably the main reservoirs of resistant pathogens. They should be regarded as critical control points for preventing or reducing the release of antibiotics, antibiotic-resistant bacteria (ARB), and antibiotic-resistance genes (ARGs) into the natural environment. This review focuses on the fate of the pathogens Enterococcus faecium, Staphylococcus aureus, Clostridium difficile, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacteriaceae spp. (ESCAPE) in WWTPs. All ESCAPE pathogen species, including high-risk clones and resistance determinants to last-resort antibiotics such as carbapenems, colistin, and multi-drug resistance platforms, were detected in wastewater. The whole genome sequencing studies demonstrate the clonal relationships and dissemination of Gram-negative ESCAPE species into the wastewater via hospital effluents and the enrichment of virulence and resistance determinants of S. aureus and enterococci in WWTPs. Therefore, the efficiency of different wastewater treatment processes regarding the removal of clinically relevant ARB species and ARGs, as well as the influence of water quality factors on their performance, should be explored and monitored, along with the development of more effective treatments and appropriate indicators (ESCAPE bacteria and/or ARGs). This knowledge will allow the development of quality standards for point sources and effluents to consolidate the WWTP barrier role against the environmental and public health AR threats.
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spelling doaj.art-1d191de9c45243fa84aa7fcc42ff4aba2023-05-24T05:30:34ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-05-011410.3389/fmicb.2023.11939071193907Wastewater treatment plants, an “escape gate” for ESCAPE pathogensLuminita Gabriela Marutescu0Luminita Gabriela Marutescu1Marcela Popa2Irina Gheorghe-Barbu3Irina Gheorghe-Barbu4Ilda Czobor Barbu5Ilda Czobor Barbu6Daloha Rodríguez-Molina7Daloha Rodríguez-Molina8Daloha Rodríguez-Molina9Fanny Berglund10Fanny Berglund11Hetty Blaak12Carl-Fredrik Flach13Carl-Fredrik Flach14Merel Aurora Kemper15Beate Spießberger16Beate Spießberger17Beate Spießberger18Laura Wengenroth19D. G. Joakim Larsson20D. G. Joakim Larsson21Dennis Nowak22Dennis Nowak23Katja Radon24Ana Maria de Roda Husman25Andreas Wieser26Andreas Wieser27Andreas Wieser28Heike Schmitt29Gratiela Pircalabioru Gradisteanu30Gratiela Pircalabioru Gradisteanu31Gratiela Pircalabioru Gradisteanu32Corneliu Ovidiu Vrancianu33Mariana Carmen Chifiriuc34Mariana Carmen Chifiriuc35Mariana Carmen Chifiriuc36Department of Microbiology and Immunology, Faculty of Biology, Research Institute of the University of Bucharest, University of Bucharest, Bucharest, RomaniaEarth, Environmental and Life Sciences Section, Research Institute of the University of Bucharest, University of Bucharest, Bucharest, RomaniaEarth, Environmental and Life Sciences Section, Research Institute of the University of Bucharest, University of Bucharest, Bucharest, RomaniaDepartment of Microbiology and Immunology, Faculty of Biology, Research Institute of the University of Bucharest, University of Bucharest, Bucharest, RomaniaEarth, Environmental and Life Sciences Section, Research Institute of the University of Bucharest, University of Bucharest, Bucharest, RomaniaDepartment of Microbiology and Immunology, Faculty of Biology, Research Institute of the University of Bucharest, University of Bucharest, Bucharest, RomaniaEarth, Environmental and Life Sciences Section, Research Institute of the University of Bucharest, University of Bucharest, Bucharest, RomaniaInstitute and Clinic for Occupational, Social and Environmental Medicine, University Hospital, LMU Munich, Munich, GermanyInstitute for Medical Information Processing, Biometry, and Epidemiology – IBE, LMU Munich, Munich, GermanyPettenkofer School of Public Health, Munich, GermanyDepartment of Infectious Diseases, Institute of Biomedicine, University of Gothenburg, Gothenburg, SwedenCentre for Antibiotic Resistance Research in Gothenburg (CARe), University of Gothenburg, Gothenburg, SwedenCentre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, NetherlandsDepartment of Infectious Diseases, Institute of Biomedicine, University of Gothenburg, Gothenburg, SwedenCentre for Antibiotic Resistance Research in Gothenburg (CARe), University of Gothenburg, Gothenburg, SwedenCentre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, NetherlandsGerman Centre for Infection Research (DZIF), Partner Site Munich, Munich, Germany0Max von Pettenkofer Institute, Faculty of Medicine, LMU Munich, Munich, Germany1Department of Infectious Diseases and Tropical Medicine, LMU University Hospital Munich, Munich, GermanyInstitute and Clinic for Occupational, Social and Environmental Medicine, University Hospital, LMU Munich, Munich, GermanyDepartment of Infectious Diseases, Institute of Biomedicine, University of Gothenburg, Gothenburg, SwedenCentre for Antibiotic Resistance Research in Gothenburg (CARe), University of Gothenburg, Gothenburg, SwedenInstitute and Clinic for Occupational, Social and Environmental Medicine, University Hospital, LMU Munich, Munich, Germany2Comprehensive Pneumology Center Munich (CPC-M), German Center for Lung Research (DZL), Munich, GermanyInstitute and Clinic for Occupational, Social and Environmental Medicine, University Hospital, LMU Munich, Munich, GermanyCentre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, NetherlandsGerman Centre for Infection Research (DZIF), Partner Site Munich, Munich, Germany0Max von Pettenkofer Institute, Faculty of Medicine, LMU Munich, Munich, Germany1Department of Infectious Diseases and Tropical Medicine, LMU University Hospital Munich, Munich, GermanyCentre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, NetherlandsDepartment of Microbiology and Immunology, Faculty of Biology, Research Institute of the University of Bucharest, University of Bucharest, Bucharest, RomaniaEarth, Environmental and Life Sciences Section, Research Institute of the University of Bucharest, University of Bucharest, Bucharest, Romania3Romanian Academy of Sciences, Bucharest, RomaniaDepartment of Microbiology and Immunology, Faculty of Biology, Research Institute of the University of Bucharest, University of Bucharest, Bucharest, RomaniaDepartment of Microbiology and Immunology, Faculty of Biology, Research Institute of the University of Bucharest, University of Bucharest, Bucharest, RomaniaEarth, Environmental and Life Sciences Section, Research Institute of the University of Bucharest, University of Bucharest, Bucharest, Romania4The Romanian Academy, Bucharest, RomaniaAntibiotics are an essential tool of modern medicine, contributing to significantly decreasing mortality and morbidity rates from infectious diseases. However, persistent misuse of these drugs has accelerated the evolution of antibiotic resistance, negatively impacting clinical practice. The environment contributes to both the evolution and transmission of resistance. From all anthropically polluted aquatic environments, wastewater treatment plants (WWTPs) are probably the main reservoirs of resistant pathogens. They should be regarded as critical control points for preventing or reducing the release of antibiotics, antibiotic-resistant bacteria (ARB), and antibiotic-resistance genes (ARGs) into the natural environment. This review focuses on the fate of the pathogens Enterococcus faecium, Staphylococcus aureus, Clostridium difficile, Acinetobacter baumannii, Pseudomonas aeruginosa, and Enterobacteriaceae spp. (ESCAPE) in WWTPs. All ESCAPE pathogen species, including high-risk clones and resistance determinants to last-resort antibiotics such as carbapenems, colistin, and multi-drug resistance platforms, were detected in wastewater. The whole genome sequencing studies demonstrate the clonal relationships and dissemination of Gram-negative ESCAPE species into the wastewater via hospital effluents and the enrichment of virulence and resistance determinants of S. aureus and enterococci in WWTPs. Therefore, the efficiency of different wastewater treatment processes regarding the removal of clinically relevant ARB species and ARGs, as well as the influence of water quality factors on their performance, should be explored and monitored, along with the development of more effective treatments and appropriate indicators (ESCAPE bacteria and/or ARGs). This knowledge will allow the development of quality standards for point sources and effluents to consolidate the WWTP barrier role against the environmental and public health AR threats.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1193907/fullESCAPE pathogensantibiotic resistancewastewater treatment plantsantibiotic resistance genesESCAPE species disseminationhigh-risk clones
spellingShingle Luminita Gabriela Marutescu
Luminita Gabriela Marutescu
Marcela Popa
Irina Gheorghe-Barbu
Irina Gheorghe-Barbu
Ilda Czobor Barbu
Ilda Czobor Barbu
Daloha Rodríguez-Molina
Daloha Rodríguez-Molina
Daloha Rodríguez-Molina
Fanny Berglund
Fanny Berglund
Hetty Blaak
Carl-Fredrik Flach
Carl-Fredrik Flach
Merel Aurora Kemper
Beate Spießberger
Beate Spießberger
Beate Spießberger
Laura Wengenroth
D. G. Joakim Larsson
D. G. Joakim Larsson
Dennis Nowak
Dennis Nowak
Katja Radon
Ana Maria de Roda Husman
Andreas Wieser
Andreas Wieser
Andreas Wieser
Heike Schmitt
Gratiela Pircalabioru Gradisteanu
Gratiela Pircalabioru Gradisteanu
Gratiela Pircalabioru Gradisteanu
Corneliu Ovidiu Vrancianu
Mariana Carmen Chifiriuc
Mariana Carmen Chifiriuc
Mariana Carmen Chifiriuc
Wastewater treatment plants, an “escape gate” for ESCAPE pathogens
Frontiers in Microbiology
ESCAPE pathogens
antibiotic resistance
wastewater treatment plants
antibiotic resistance genes
ESCAPE species dissemination
high-risk clones
title Wastewater treatment plants, an “escape gate” for ESCAPE pathogens
title_full Wastewater treatment plants, an “escape gate” for ESCAPE pathogens
title_fullStr Wastewater treatment plants, an “escape gate” for ESCAPE pathogens
title_full_unstemmed Wastewater treatment plants, an “escape gate” for ESCAPE pathogens
title_short Wastewater treatment plants, an “escape gate” for ESCAPE pathogens
title_sort wastewater treatment plants an escape gate for escape pathogens
topic ESCAPE pathogens
antibiotic resistance
wastewater treatment plants
antibiotic resistance genes
ESCAPE species dissemination
high-risk clones
url https://www.frontiersin.org/articles/10.3389/fmicb.2023.1193907/full
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