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 CesarePopi 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*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

53 Citations (Scopus)


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.

Original languageEnglish
Article number106035
JournalEnvironment International
Publication statusPublished - Nov 2020


  • Antibiotic resistance
  • Coliforms
  • ESBLs
  • Wastewater treatment
  • Water reuse


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