Environment International (Nov 2020)
A global multinational survey of cefotaxime-resistant coliforms in urban wastewater treatment plants
- Roberto B.M. Marano,
- Telma Fernandes,
- Célia M. Manaia,
- Olga Nunes,
- Donald Morrison,
- Thomas U. Berendonk,
- Norbert Kreuzinger,
- Tanel Telson,
- Gianluca Corno,
- Despo Fatta-Kassinos,
- Christophe Merlin,
- Edward Topp,
- Edouard Jurkevitch,
- Leonie Henn,
- Andrew Scott,
- Stefanie Heß,
- Katarzyna Slipko,
- Mailis Laht,
- Veljo Kisand,
- Andrea Di Cesare,
- Popi Karaolia,
- Stella G. Michael,
- Alice L. Petre,
- Roberto Rosal,
- Amy Pruden,
- Virginia Riquelme,
- Ana Agüera,
- Belen Esteban,
- Aneta Luczkiewicz,
- Agnieszka Kalinowska,
- Anne Leonard,
- William H. Gaze,
- Anthony A. Adegoke,
- Thor A. Stenstrom,
- Alfieri Pollice,
- Carlo Salerno,
- Carsten U. Schwermer,
- Pawel Krzeminski,
- Hélène Guilloteau,
- Erica Donner,
- Barbara Drigo,
- Giovanni Libralato,
- Marco Guida,
- Helmut Bürgmann,
- Karin Beck,
- Hemda Garelick,
- Marta Tacão,
- Isabel Henriques,
- Isabel Martínez-Alcalá,
- Jose M. Guillén-Navarro,
- Magdalena Popowska,
- Marta Piotrowska,
- Marcos Quintela-Baluja,
- Joshua T. Bunce,
- Maria I. Polo-López,
- Samira Nahim–Granados,
- Marie-Noëlle Pons,
- Milena Milakovic,
- Nikolina Udikovic-Kolic,
- Jérôme Ory,
- Traore Ousmane,
- Pilar Caballero,
- Antoni Oliver,
- Sara Rodriguez-Mozaz,
- Jose L. Balcazar,
- Thomas Jäger,
- Thomas Schwartz,
- Ying Yang,
- Shichun Zou,
- Yunho Lee,
- Younggun Yoon,
- Bastian Herzog,
- Heidrun Mayrhofer,
- Om Prakash,
- Yogesh Nimonkar,
- Ester Heath,
- Anna Baraniak,
- Joana Abreu-Silva,
- Manika Choudhury,
- Leonardo P. Munoz,
- Stela Krizanovic,
- Gianluca Brunetti,
- Ayella Maile-Moskowitz,
- Connor Brown,
- Eddie Cytryn
Affiliations
- Roberto B.M. Marano
- Department of Agroecology and Plant Health, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel; Department of Soil Chemistry, Plant Nutrition and Microbiology, Institute of Soil Water and Environmental Sciences, Volcani Center, Agricultural Research Organization, Rishon Lezion, Israel
- Telma Fernandes
- Universidade Católica Portuguesa, CBQF – Centro de Biotecnologia e Química Fina – Laboratório Associado, Escola Superior de Biotecnologia, Rua Arquiteto Lobão Vital, 172, 4200-374 Porto, Portugal
- Célia M. Manaia
- Universidade Católica Portuguesa, CBQF – Centro de Biotecnologia e Química Fina – Laboratório Associado, Escola Superior de Biotecnologia, Rua Arquiteto Lobão Vital, 172, 4200-374 Porto, Portugal
- Olga Nunes
- LEPABE, Laboratório de Engenharia de Processos, Ambiente, Biotecnologia e Energia, Faculdade de Engenharia, Universidade do Porto, Rua Dr. Roberto Frias, 4200-465 Porto, Portugal
- Donald Morrison
- School Applied Sciences, Edinburgh Napier University, EH11 4BN, UK
- Thomas U. Berendonk
- Institute of Hydrobiology, TU Dresden, Dresden, Germany
- Norbert Kreuzinger
- Vienna University of Technology, Institute for Water Quality and Resources Management, Vienna, Austria
- Tanel Telson
- Institute of Technology, University of Tartu, Estonia
- Gianluca Corno
- CNR-IRSA Molecular Ecology Group, Largo Tonolli 50, 28922 Verbania, Italy
- Despo Fatta-Kassinos
- Civil and Environmental Engineering Department and Nireas International Water Research Center, University of Cyprus, P.O. Box 20537, CY-1678 Nicosia, Cyprus
- Christophe Merlin
- UMR 7564 University of Lorraine-CNRS (LCPME), France
- Edward Topp
- Agriculture and Agri-Food Canada, London Research and Development Centre (ON), Canada; Department of Biology, University of Western Ontario, London, ON, Canada
- Edouard Jurkevitch
- Department of Agroecology and Plant Health, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, Israel
- Leonie Henn
- School Applied Sciences, Edinburgh Napier University, EH11 4BN, UK
- Andrew Scott
- Agriculture and Agri-Food Canada, London Research and Development Centre (ON), Canada
- Stefanie Heß
- Institute of Hydrobiology, TU Dresden, Dresden, Germany; Institute of Microbiology, TU Dresden, Dresden, Germany
- Katarzyna Slipko
- Vienna University of Technology, Institute for Water Quality and Resources Management, Vienna, Austria
- Mailis Laht
- Institute of Technology, University of Tartu, Estonia; Estonian Environmental Research Centre, Estonia
- Veljo Kisand
- Institute of Technology, University of Tartu, Estonia
- Andrea Di Cesare
- CNR-IRSA Molecular Ecology Group, Largo Tonolli 50, 28922 Verbania, Italy
- Popi Karaolia
- Civil and Environmental Engineering Department and Nireas International Water Research Center, University of Cyprus, P.O. Box 20537, CY-1678 Nicosia, Cyprus
- Stella G. Michael
- Civil and Environmental Engineering Department and Nireas International Water Research Center, University of Cyprus, P.O. Box 20537, CY-1678 Nicosia, Cyprus
- Alice L. Petre
- Department of Chemical Engineering, University of Alcalá, E-28871 Alcalá de Henares, Madrid, Spain
- Roberto Rosal
- Department of Chemical Engineering, University of Alcalá, E-28871 Alcalá de Henares, Madrid, Spain
- Amy Pruden
- Department of Civil and Environmental Engineering, Virginia Tech, Blacksburg, VA, USA
- Virginia Riquelme
- Department of Civil and Environmental Engineering, Virginia Tech, Blacksburg, VA, USA
- Ana Agüera
- Solar Energy Research Centre (CIESOL), Joint Centre University of Almería-CIEMAT, 04120 Almería, Spain
- Belen Esteban
- Solar Energy Research Centre (CIESOL), Joint Centre University of Almería-CIEMAT, 04120 Almería, Spain
- Aneta Luczkiewicz
- Faculty of Civil and Environmental Engineering, Gdansk University of Technology, G. Narutowicza 11/12 street, 80-233 Gdańsk, Poland
- Agnieszka Kalinowska
- Faculty of Civil and Environmental Engineering, Gdansk University of Technology, G. Narutowicza 11/12 street, 80-233 Gdańsk, Poland
- Anne Leonard
- University of Exeter Medical School, European Centre for Environment and Human Health, Environment and Sustainability Institute, University of Exeter, Penryn campus, TR10 9FE, UK
- William H. Gaze
- University of Exeter Medical School, European Centre for Environment and Human Health, Environment and Sustainability Institute, University of Exeter, Penryn campus, TR10 9FE, UK
- Anthony A. Adegoke
- Institute for Water and Wastewater Technology, Durban University of Technology, Durban South Africa; Department of Microbiology, University of Uyo, Uyo, Nigeria
- Thor A. Stenstrom
- Institute for Water and Wastewater Technology, Durban University of Technology, Durban South Africa
- Alfieri Pollice
- CNR-IRSA Viale F. De Blasio 5, 70132 Bari, Italy
- Carlo Salerno
- CNR-IRSA Viale F. De Blasio 5, 70132 Bari, Italy
- Carsten U. Schwermer
- Norwegian Institute for Water Research, Gaustadalléen 21, N-0349 Oslo, Norway
- Pawel Krzeminski
- Norwegian Institute for Water Research, Gaustadalléen 21, N-0349 Oslo, Norway
- Hélène Guilloteau
- UMR 7564 University of Lorraine-CNRS (LCPME), France
- Erica Donner
- Future Industries Institute, University of South Australia, Adelaide, SA 5001, Australia
- Barbara Drigo
- Future Industries Institute, University of South Australia, Adelaide, SA 5001, Australia
- Giovanni Libralato
- Department of Biology, University of Naples Federico II, via Cinthia 21, 80126 Naples, Italy
- Marco Guida
- Department of Biology, University of Naples Federico II, via Cinthia 21, 80126 Naples, Italy
- Helmut Bürgmann
- Eawag, Swiss Federal Institute of Aquatic Science and Technology, 6047 Kastanienbaum, Switzerland
- Karin Beck
- Eawag, Swiss Federal Institute of Aquatic Science and Technology, 6047 Kastanienbaum, Switzerland
- Hemda Garelick
- Department of Natural Sciences, Middlesex University, London NW4 4BT, UK
- Marta Tacão
- CESAM and Department of Biology, University of Aveiro, Campus Universitário de Santiago, 3810-193, Portugal
- Isabel Henriques
- CESAM and Department of Biology, University of Aveiro, Campus Universitário de Santiago, 3810-193, Portugal; University of Coimbra, Department of Life Sciences, Calçada Martim de Freitas, 3000-456 Coimbra, Portugal
- Isabel Martínez-Alcalá
- Department of Civil Engineering, Av. de los Jerónimos, 135, 30107 Guadalupe, Murcia, Spain
- Jose M. Guillén-Navarro
- Department of Civil Engineering, Av. de los Jerónimos, 135, 30107 Guadalupe, Murcia, Spain
- Magdalena Popowska
- Institute of Microbiology, Department of Applied Microbiology, Faculty of Biology, University of Warsaw, Poland
- Marta Piotrowska
- Institute of Microbiology, Department of Applied Microbiology, Faculty of Biology, University of Warsaw, Poland
- Marcos Quintela-Baluja
- School of Engineering, Newcastle University, Newcastle Upon Tyne, UK
- Joshua T. Bunce
- School of Engineering, Newcastle University, Newcastle Upon Tyne, UK
- Maria I. Polo-López
- Solar Energy Research Centre (CIESOL), Joint Centre University of Almería-CIEMAT, 04120 Almería, Spain; Plataforma Solar de Almería – CIEMAT, P.O. Box 22, 04200 Tabernas, Almería, Spain
- Samira Nahim–Granados
- Solar Energy Research Centre (CIESOL), Joint Centre University of Almería-CIEMAT, 04120 Almería, Spain; Plataforma Solar de Almería – CIEMAT, P.O. Box 22, 04200 Tabernas, Almería, Spain
- Marie-Noëlle Pons
- Université de Lorraine, CNRS, LRGP, F-54000 Nancy, France
- Milena Milakovic
- Rudjer Boskovic Institute, Bijenicka 54, Zagreb, Croatia
- Nikolina Udikovic-Kolic
- Rudjer Boskovic Institute, Bijenicka 54, Zagreb, Croatia
- Jérôme Ory
- Laboratoire “Microorganisme: Génome et Environnement”, Université Clermont Auvergne, BP 10448, F-63000 Clermont-Ferrand, France; CNRS, UMR 6023, LMGE, F-63170 Campus Universitaire des Cézeaux, Clermont-Ferrand, France; Service d'hygiène hospitalière, CHU Clermont-Ferrand, Clermont-Ferrand, France
- Traore Ousmane
- Laboratoire “Microorganisme: Génome et Environnement”, Université Clermont Auvergne, BP 10448, F-63000 Clermont-Ferrand, France; CNRS, UMR 6023, LMGE, F-63170 Campus Universitaire des Cézeaux, Clermont-Ferrand, France; Service d'hygiène hospitalière, CHU Clermont-Ferrand, Clermont-Ferrand, France
- Pilar Caballero
- Laboratori EMATSA, Ctra Valls Km 3, 43130 Tarragona, Spain
- Antoni Oliver
- Laboratori EMATSA, Ctra Valls Km 3, 43130 Tarragona, Spain
- Sara Rodriguez-Mozaz
- Catalan Institute for Water Research (ICRA), 17003 Girona, Spain
- Jose L. Balcazar
- Catalan Institute for Water Research (ICRA), 17003 Girona, Spain
- Thomas Jäger
- Institute of Functional Interfaces (IFG), Karlsruhe Institute of Technology (KIT), Eggenstein-Leopoldshafen, Germany
- Thomas Schwartz
- Institute of Functional Interfaces (IFG), Karlsruhe Institute of Technology (KIT), Eggenstein-Leopoldshafen, Germany
- Ying Yang
- School of Marine Sciences, Sun Yat-sen University, Guangzhou, China
- Shichun Zou
- School of Marine Sciences, Sun Yat-sen University, Guangzhou, China
- Yunho Lee
- School of Earth Sciences and Environmental Engineering, Gwangju Institute of Science and Technology (GIST), Gwangju 61005, Republic of Korea
- Younggun Yoon
- School of Earth Sciences and Environmental Engineering, Gwangju Institute of Science and Technology (GIST), Gwangju 61005, Republic of Korea
- Bastian Herzog
- Chair of Urban Water Systems Engineering, Technical University of Munich (TUM), Germany
- Heidrun Mayrhofer
- Chair of Urban Water Systems Engineering, Technical University of Munich (TUM), Germany
- Om Prakash
- National Centre for Microbial Resource (NCMR), National Centre for Cell Science, Pune 411007, India
- Yogesh Nimonkar
- National Centre for Microbial Resource (NCMR), National Centre for Cell Science, Pune 411007, India
- Ester Heath
- Jozef Stefan Institute, Jamova 39 1000 Ljubljana, Slovenia
- Anna Baraniak
- National Medicines Institute, Department of Molecular Microbiology, Chelmska 30/34, 00-725 Warsaw, Poland
- Joana Abreu-Silva
- Universidade Católica Portuguesa, CBQF – Centro de Biotecnologia e Química Fina – Laboratório Associado, Escola Superior de Biotecnologia, Rua Arquiteto Lobão Vital, 172, 4200-374 Porto, Portugal
- Manika Choudhury
- Department of Natural Sciences, Middlesex University, London NW4 4BT, UK
- Leonardo P. Munoz
- Department of Natural Sciences, Middlesex University, London NW4 4BT, UK
- Stela Krizanovic
- Rudjer Boskovic Institute, Bijenicka 54, Zagreb, Croatia
- Gianluca Brunetti
- Future Industries Institute, University of South Australia, Adelaide, SA 5001, Australia
- Ayella Maile-Moskowitz
- Department of Civil and Environmental Engineering, Virginia Tech, Blacksburg, VA, USA
- Connor Brown
- Department of Civil and Environmental Engineering, Virginia Tech, Blacksburg, VA, USA
- Eddie Cytryn
- Department of Soil Chemistry, Plant Nutrition and Microbiology, Institute of Soil Water and Environmental Sciences, Volcani Center, Agricultural Research Organization, Rishon Lezion, Israel; Corresponding author.
- Journal volume & issue
-
Vol. 144
p. 106035
Abstract
The World Health Organization Global Action Plan recommends integrated surveillance programs as crucial strategies for monitoring antibiotic resistance. Although several national surveillance programs are in place for clinical and veterinary settings, no such schemes exist for monitoring antibiotic-resistant bacteria in the environment. In this transnational study, we developed, validated, and tested a low-cost surveillance and easy to implement approach to evaluate antibiotic resistance in wastewater treatment plants (WWTPs) by targeting cefotaxime-resistant (CTX-R) coliforms as indicators. The rationale for this approach was: i) coliform quantification methods are internationally accepted as indicators of fecal contamination in recreational waters and are therefore routinely applied in analytical labs; ii) CTX-R coliforms are clinically relevant, associated with extended-spectrum β-lactamases (ESBLs), and are rare in pristine environments. We analyzed 57 WWTPs in 22 countries across Europe, Asia, Africa, Australia, and North America. CTX-R coliforms were ubiquitous in raw sewage and their relative abundance varied significantly (<0.1% to 38.3%), being positively correlated (p < 0.001) with regional atmospheric temperatures. Although most WWTPs removed large proportions of CTX-R coliforms, loads over 103 colony-forming units per mL were occasionally observed in final effluents. We demonstrate that CTX-R coliform monitoring is a feasible and affordable approach to assess wastewater antibiotic resistance status.
