Antibiotic Residues in Final Effluents of European Wastewater Treatment
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Environment International 140 (2020) 105733 Contents lists available at ScienceDirect Environment International journal homepage: www.elsevier.com/locate/envint Antibiotic residues in final effluents of European wastewater treatment plants and their impact on the aquatic environment T ⁎ Sara Rodriguez-Mozaza,b, , Ivone Vaz-Moreirac, Saulo Varela Della Giustinaa,b, Marta Llorcaa,b,d, Damià Barcelóa,b,d, Sara Schuberte, Thomas U. Berendonke, Irene Michael-Kordatouf, Despo Fatta-Kassinosf,g, Jose Luis Martinezh, Christian Elpersi, Isabel Henriquesj, Thomas Jaegerk, Thomas Schwartzk, Erik Paulshusl, Kristin O'Sullivanl, Katariina M.M. Pärnänenm, Marko Virtam, Thi Thuy Don, Fiona Walshn, Célia M. Manaiac a Catalan Institute for Water Research (ICRA), Emili Grahit 101, 17003 Girona, Spain b Universitat de Girona, Girona, Spain c Universidade Católica Portuguesa, CBQF – Centro de Biotecnologia e Química Fina – Laboratório Associado, Escola Superior de Biotecnologia, Rua Diogo Botelho 1327, 4169-005 Porto, Portugal d Water and Soil Quality Research Group, Department of Environmental Chemistry, (IDAEA-CSIC), Jordi Girona 18-26, 08034, Barcelona, Spain e Technische Universität Dresden, Institute of Hydrobiology, Dresden, Germany f Nireas-International Water Research Centre, University of Cyprus, P.O. Box 20537, CY-1678 Nicosia, Cyprus g Department of Civil and Environmental Engineering, University of Cyprus, P.O. Box 20537, CY-1678 Nicosia, Cyprus h Centro Nacional de Biotecnología, CSIC, Darwin 3, 20049 Madrid. Spain i Aquantec GmbH, Am Zwinger 5, 76227 Karlsruhe, Germany j Centre for Environmental and Marine Studies (CESAM, University of Aveiro) and Department of Life Sciences, Faculty of Sciences and Technology, University of Coimbra, Calçada Martin de Freitas, 3000-456 Coimbra, Portugal k Karlsruhe Institute of Technology (KIT) – Campus North, Institute of Functional Interfaces (IFG), P.O. Box 3640, 76021 Karlsruhe, Germany l Norwegian University of Life Sciences, Faculty of Veterinary Medicine, Department of Food Safety and Infection Biology, Section of Microbiology, Immunology and Parasitology, Post Box 8146 Dep., 0033 Oslo, Norway m Department of Microbiology, University of Helsinki, Viikinkaari 9, 00014 University of Helsinki, Finland n Department of Biology, Maynooth University, Maynooth, Co. Kildare, Ireland ARTICLE INFO ABSTRACT Handling Editor: Adrian Covaci A comprehensive monitoring of a broad set of antibiotics in the final effluent of wastewater treatment plants (WWTPs) of 7 European countries (Portugal, Spain, Ireland, Cyprus, Germany, Finland, and Norway) was carried out in two consecutive years (2015 and 2016). This is the first study of this kind performed at an international level. Within the 53 antibiotics monitored 17 were detected at least once in the final effluent of the WWTPs, i.e.: ciprofloxacin, ofloxacin, enrofloxacin, orbifloxacin, azithromycin, clarithromycin, sulfapyridine, sulfamethox- azole, trimethoprim, nalidixic acid, pipemidic acid, oxolinic acid, cefalexin, clindamycin, metronidazole, am- picillin, and tetracycline. The countries exhibiting the highest effluent average concentrations of antibiotics were Ireland and the southern countries Portugal and Spain, whereas the northern countries (Norway, Finland and Germany) and Cyprus exhibited lower total concentration. The antibiotic occurrence data in the final effluents were used for the assessment of their impact on the aquatic environment. Both, environmental predicted no effect concentration (PNEC-ENVs) and the PNECs based on minimal inhibitory concentrations (PNEC-MICs) were considered for the evaluation of the impact on microbial communities in aquatic systems and on the evolution of antibiotic resistance, respectively. Based on this analysis, three compounds, ciprofloxacin, azithromycin and cefalexin are proposed as markers of antibiotic pollution, as they could occasionally pose a risk to the en- vironment. Integrated studies like this are crucial to map the impact of antibiotic pollution and to provide the basis for designing water quality and environmental risk in regular water monitoring programs. ⁎ Corresponding author at: Catalan Institute for Water Research (ICRA), Scientific and Technologic Park of the University of Girona, Emili Grahit 101, E-17003 Girona, Spain. E-mail address: [email protected] (S. Rodriguez-Mozaz). https://doi.org/10.1016/j.envint.2020.105733 Received 27 December 2019; Received in revised form 16 March 2020; Accepted 8 April 2020 Available online 27 April 2020 0160-4120/ © 2020 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/). S. Rodriguez-Mozaz, et al. Environment International 140 (2020) 105733 1. Introduction Spain, Ireland, Cyprus, Germany, Finland, and Norway) was sampled twice (early Spring and early Autumn) in two consecutive years (2015 Antibiotics are a class of pharmaceutical active compounds with and 2016) and was monitored for 53 antibiotic residues belonging to 10 high usage and consumption worldwide. By definition, an antibiotic is a different therapeutic classes. The countries were selected following a chemotherapeutic agent that specifically inhibits, by cell destruction or north-to-south gradient in the use of antibiotics as well as in the pre- growth inhibition, the proliferation of bacteria (Kümmerer, 2009). valence of antibiotic resistance in clinical settings as reported in the According to Kümmerer (2009) over 250 different chemical substances 2017 EARS-Net surveillance report (ECDC European Centre for Disease are registered as antibiotics for human and/or animal health use Prevention and Control, 2017). The specific objectives of the study globally. Based on the analysis of data from scientific literature and were: (i) to provide an overview of the presence and concentration of national and regional surveillance systems from 71 countries over the antibiotics in final effluents of WWTPs located in different European past 10 years, antibiotic use is growing steadily worldwide (30%), countries; (ii) to assess geographical and temporal trends about the driven mainly by rising demand in low- and middle-income countries occurrence of these contaminants; (iii) to infer about the potential en- (Gelband et al. 2015). This increase in the use of antibiotics and the vironmental and human health risk posed by antibiotic residues in final awareness about their side effects have led to increasing concern re- treated wastewater effluents; and (iv) to propose robust analytical tools garding their potentially detrimental effects in the environment. In and indicator compounds to be used in regular water-monitoring pro- particular, it is suspected that their occurrence can accelerate resistance grams, hence making feasible the comparison of country-based studies. spread in the environment (Bengtsson-Palme et al., 2018), with po- tential implications on human health. According to the World Health 2. Materials and methods Organization (WHO), antimicrobial resistance is a major challenge to global human and animal health, food safety, and development today, 2.1. Sampling campaigns with the perspective of aggravation in the upcoming years, if effective measures are not implemented (World Health Organization, 2014). Four sampling campaigns were carried out in early Spring (March Because of the intensive use of antibiotics for human, veterinary and 2015 and 2016) and early Autumn (October 2015 and September agriculture purposes, these compounds are continuously released into 2016), suggested to correspond to the highest and the lowest peaks of the environment from anthropogenic sources. In urban areas, waste- antibiotic consumption, respectively (Caucci et al., 2016; Sun et al., water treatment plants (WWTPs), when available, are among the main 2012). In each of the 4 sampling campaigns, 24-h composite samples receptors of antibiotics, part of which persist after the treatment and were collected in 3 consecutive days (Tuesday, Wednesday, and can be released into various environmental compartments (Michael Thursday) at the outlet of 13 urban WWTPs belonging to 7 European et al., 2013). Several studies about the presence of antibiotics in countries (Portugal, Spain, Cyprus, Ireland, Germany, Finland, and WWTPs have been conducted in the last couple of decades. Most of Norway) (Fig. 1, Table S1). Two WWTPs were monitored in each them have focused on a limited amount of compounds (between 2 and country except in Spain and Norway, where a single WWTP was sam- 33 target antibiotics). Further, studies comparing the situation in dif- pled. In Portugal, due to a problem in the WWTP PT1 in the sampling ferent countries are nearly absent and, in the case that a single country campaign of March 2016, a third WWTP (PT3), located in the same as China, Croatia, Sweden, Portugal, United Kingdom, and Greece is region, was sampled instead. General characteristics of the selected analysed, a limited number of WWTPs, varying between 2 and 19 WWTPs are gathered in Table S2. For every campaign, data concerning within each country has been studied (Gao et al., 2012; Johnson et al., weather conditions were collected for the 3 days of sampling and the 2017; Kosma et al., 2014; Lindberg et al., 2005; Pereira et al., 2015; day before (Table S3). Senta et al., 2013; Wang et al., 2018; Zhang et al., 2019). Among the All participants collected the samples on the same dates and most comprehensive studies so far are those by Gracia-Lor et al. (2011), adopted a common protocol for sampling