Antibiotic resistance genes in treated wastewater and in the receiving water bodies: a pan-European survey of urban settings

Article

Cacace, D., Fatta-Kassinos, D., Manaia, C., Cytryn, E., Kreuzinger, N., Rizzo, L., Karaolia, P., Schwartz, T., Alexander, J., Merlin, C., Garelick, H., Schmitt, H., de Vries, D., Schwermer, C., Meric, S., Ozkal, C., Pons, M., Kneis, D. and Berendonk, T. 2019. Antibiotic resistance genes in treated wastewater and in the receiving water bodies: a pan-European survey of urban settings. Water Research. 162, pp. 320-330. https://doi.org/10.1016/j.watres.2019.06.039
TypeArticle
TitleAntibiotic resistance genes in treated wastewater and in the receiving water bodies: a pan-European survey of urban settings
AuthorsCacace, D., Fatta-Kassinos, D., Manaia, C., Cytryn, E., Kreuzinger, N., Rizzo, L., Karaolia, P., Schwartz, T., Alexander, J., Merlin, C., Garelick, H., Schmitt, H., de Vries, D., Schwermer, C., Meric, S., Ozkal, C., Pons, M., Kneis, D. and Berendonk, T.
Abstract

There is increasing public concern regarding the fate of antibiotic resistance genes (ARGs) during wastewater treatment, their persistence during the treatment process and their potential impacts on the receiving water bodies. In this study, we used quantitative PCR (qPCR) to determine the abundance of nine ARGs and a class 1 integron associated integrase gene in 16 wastewater treatment plant (WWTP) effluents from ten different European countries. In order to assess the impact on the receiving water bodies, gene abundances in the latter were also analysed. Six out of the nine ARGs analysed were detected in all effluent and river water samples. Among the quantified genes, intI1 and sul1 were the most abundant. Our results demonstrate that European WWTP contribute to the enrichment of the resistome in the receiving water bodies with the particular impact being dependent on the effluent load and local hydrological conditions. The ARGs concentrations in WWTP effluents were found to be inversely correlated to the number of implemented biological treatment steps, indicating a possible option for WWTP management. Furthermore, this study has identified bla as a possible resistance gene for future studies investigating the impact of WWTPs on their receiving water. [Abstract copyright: Copyright © 2019 The Authors. Published by Elsevier Ltd.. All rights reserved.]

KeywordsAntibiotic resistance genes; Wastewater; Freshwater; qPCR; Europe
PublisherElsevier
JournalWater Research
ISSN0043-1354
Electronic1879-2448
Publication dates
Online24 Jun 2019
Print01 Oct 2019
Publication process dates
Deposited23 Jul 2019
Accepted15 Jun 2019
Submitted28 Feb 2019
Output statusPublished
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Copyright Statement

©2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Digital Object Identifier (DOI)https://doi.org/10.1016/j.watres.2019.06.039
Web of Science identifierWOS:000479023000031
LanguageEnglish
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Ellis, J. and Garelick, H. 2009. Multi-criteria analysis for the assessment of options for the mitigation/remediation of arsenic in drinking water. in: Garelick, H. and Jones, H. (ed.) Reviews of environmental contamination and toxicology: an international perspective. New York Springer.
Evaluation study of the IHM project on the evaluation of the accreditation of health and social care managers: a pilot.
Weller, G. and Garelick, H. 2010. Evaluation study of the IHM project on the evaluation of the accreditation of health and social care managers: a pilot. London Middlesex University.
Technical note: effects of arsenate (AS5+) on growth and production of glutathione (GSH) and phytochelatins (PCS) in Chlorella Vulgaris
Jiang, Y., Purchase, D., Jones, H. and Garelick, H. 2011. Technical note: effects of arsenate (AS5+) on growth and production of glutathione (GSH) and phytochelatins (PCS) in Chlorella Vulgaris. International Journal of Phytoremediation. 13 (8), pp. 834-844. https://doi.org/10.1080/15226514.2010.525560
A novel enzymatic composition effective for prion degradation
Okoroma, E., Purchase, D., Garelick, H. and Abiola, O. 2011. A novel enzymatic composition effective for prion degradation. Society for General Microbiology Spring Conference. Harrogate, UK 11 - 14 Apr 2011
European MSc programs in nuclear sciences: to meet the need of stakeholders.
Skipperud, L., Salbu, B., Priest, N., Garelick, H., Tamponnet, T., Abbott, A. and Mitchell, P. 2011. European MSc programs in nuclear sciences: to meet the need of stakeholders. Nuclear Engineering and Design. 241 (4), pp. 1013-1017. https://doi.org/10.1016/j.nucengdes.2010.03.018
Keratin degradation by proteolytic microorganisms isolated from activated sludge and farmyard manure: possible application in decontamination of prion protein
Purchase, D., Garelick, H., Okoroma, E., Christen, H. and Abiola, O. 2007. Keratin degradation by proteolytic microorganisms isolated from activated sludge and farmyard manure: possible application in decontamination of prion protein. BAGECO 9: 9th Symposium on Bacterial Genetics and Ecology. Wernigerode, Germany
The development of work based learning for sustainable environmental education.
Garelick, H., Rounce, K. and Garnett, J. 2007. The development of work based learning for sustainable environmental education. World Environmental Education Congress 2007. Durban, South Africa 02 - 06 Jul 2007
Remediation technologies for the removal of arsenic from water and wastewater
Garelick, H., Bollinger, J., Bux, K., Caussy, D., Dybowska, A., Ellis, J., Feldmann, J., Jones, H., Priest, N., Shevah, Y., Sneddon, R., Valsami-Jones, E. and Visoottiviseth, P. 2005. Remediation technologies for the removal of arsenic from water and wastewater. 43rd IUPAC General Assembly. Beijing, China 13 - 21 Aug 2005
The development of a doctorate in Professional Studies in Health.
Rounce, K., Garelick, H., Vernon, L. and Portwood, D. 2005. The development of a doctorate in Professional Studies in Health. in: Rounce, K. and Workman, B. (ed.) Work based learning in health care: applications and innovations. Kingsham Press.
Sanitation and disease: health aspects of excreta and wastewater management.
Feachem, R., Bradley, D., Garelick, H. and Mara, D. 1983. Sanitation and disease: health aspects of excreta and wastewater management. Published for the World Bank by Wiley.
Water and health. [Chapter 6 of 'Sustainable water: chemical science priorities summary report']
Green, C., Donner, E., Faulkner, H., Garelick, H., Jones, H., Revitt, D. and Lundy, L. 2007. Water and health. [Chapter 6 of 'Sustainable water: chemical science priorities summary report']. Royal Society of Chemistry.
Safe water.
Garelick, H. 2002. Safe water. in: Dawood, R. (ed.) Travellers' health: how to stay healthy abroad. OUP.
Pollutant biodegradation potentials on airport surfaces.
Revitt, D., Garelick, H. and Worrall, P. 2002. Pollutant biodegradation potentials on airport surfaces. in: Strecker, E. and Huber, W. (ed.) Global solutions for urban drainage. American Society of Civil Engineers.
Existing competence and infrastructure in radiation protection training at postgraduate level within the EU and new entrant states.
Mitchell, P., Bowden, L., Vintro, L., García-Tenorio, R., Garelick, H., Holm, E., Kovacs, T., Kovats, N., Priest, N., Salbu, B., Skipperud, L. and Tamponnet, C. 2005. Existing competence and infrastructure in radiation protection training at postgraduate level within the EU and new entrant states. ETRAP2005 Conference (3rd International Conference on Education and Training in Radiological Protection). Brussels, Belgium 23 - 25 Nov 2005
Keratinase production by proteolytic micro-organisms in activated sludge and farmyard waste.
Okoroma, E., Purchase, D., Garelick, H. and Abiola, O. 2008. Keratinase production by proteolytic micro-organisms in activated sludge and farmyard waste. Society for General Microbiology, Autumn Meeting. Trinity College, Dublin, Ireland 08 - 11 Sep 2008
Bacterial keratinase: prospects for prion degradation.
Okoroma, E., Purchase, D., Garelick, H. and Abiola, O. 2009. Bacterial keratinase: prospects for prion degradation. Society for General Microbiology, Spring Meeting. Harrogate, UK 30 Mar - 02 Apr 2009
Mitigating arsenic pollution: bridging the gap between knowledge and practice
Garelick, H. and Jones, H. 2008. Mitigating arsenic pollution: bridging the gap between knowledge and practice. Chemistry International. 30 (4).
Organisational involvement in supporting the learned professional
Weller, G., Garelick, H., Naylor, D. and Sherry, R. 2010. Organisational involvement in supporting the learned professional. Work Based Learning e-Journal International. 1 (1), pp. 106-124.
A biokinetic model to describe the distribution and excretion of arsenic by man following acute and chronic intakes of arsenite/arsenate compounds by ingestion.
Adeyemi, A., Garelick, H. and Priest, N. 2010. A biokinetic model to describe the distribution and excretion of arsenic by man following acute and chronic intakes of arsenite/arsenate compounds by ingestion. Human and Experimental Toxicology. 29 (11), pp. 891-902. https://doi.org/10.1177/0960327110364912
Antimicrobial resistance of campylobacter species isolated from edible bivalve molluscs purchased from Bangkok markets, Thailand
Soonthornchaikul, N. and Garelick, H. 2009. Antimicrobial resistance of campylobacter species isolated from edible bivalve molluscs purchased from Bangkok markets, Thailand. Foodborne Pathogens and Disease. 6 (8), pp. 947-951. https://doi.org/10.1089/fpd.2008.0236
Degradation of scrapie infected brain homogenateby a novel bacterial keratinase
Okoroma, E., Purchase, D., Garelick, H., Jen, A., Morris, R. and Abiola, O. 2009. Degradation of scrapie infected brain homogenateby a novel bacterial keratinase. Prion 2009. Chalkidiki, Greece 23 - 25 Sep 2009
A multi-criteria approach for assessing options to remediate arsenic in drinking water
Ellis, J. and Garelick, H. 2009. A multi-criteria approach for assessing options to remediate arsenic in drinking water. in: Garelick, H. and Jones, H. (ed.) Reviews of environmental contamination: international perspectives on arsenic pollution and remediation New York Springer.
Constructed wetland control of BOD levels in airport runoff
Adeola, S., Revitt, D., Shutes, B., Garelick, H., Jones, H. and Jones, C. 2009. Constructed wetland control of BOD levels in airport runoff. International Journal of Phytoremediation. 11 (1), pp. 1-10. https://doi.org/10.1080/15226510802363220
Work based learning for the development of the chemistry professional.
Garelick, H., Page, A. and Weller, G. 2008. Work based learning for the development of the chemistry professional. 2nd International IUPAC Conference on Green Chemistry. 14 - 19 September 2008
Arsenic pollution sources
Garelick, H., Jones, H., Dybowska, A. and Valsami-Jones, E. 2008. Arsenic pollution sources. in: Garelick, H. and Jones, H. (ed.) Reviews of environmental contamination: international perspectives on arsenic pollution and remediation New York Springer.
Resistance to three antimicrobial agents of Campylobacter isolated from organically- and intensively-reared chickens purchased from retail outlets
Soonthornchaikul, N., Garelick, H., Jones, H., Jacobs, J., Ball, D. and Choudhury, M. 2006. Resistance to three antimicrobial agents of Campylobacter isolated from organically- and intensively-reared chickens purchased from retail outlets. International Journal of Antimicrobial Agents. 27 (2), pp. 125-130. https://doi.org/10.1016/j.ijantimicag.2005.09.020
Remediation technologies for arsenic contaminated drinking waters.
Garelick, H., Dybowska, A., Valsami-Jones, E. and Priest, N. 2005. Remediation technologies for arsenic contaminated drinking waters. Journal of Soils and Sediments. 5 (3), pp. 182-190. https://doi.org/10.1065/jss2005.06.140
An investigation into arsenic(V) removal from aqueous solutions by hydroxylapatite and bone-char.
Sneddon, I., Garelick, H. and Valsami-Jones, E. 2005. An investigation into arsenic(V) removal from aqueous solutions by hydroxylapatite and bone-char. Mineralogical Magazine. 69 (5), pp. 769-780. https://doi.org/10.1180/0026461056950287
Minimum requirements for reporting analytical data for environmental samples.(IUPAC Technical Report).
Egli, H., Dassenakis, M., Garelick, H., Grieken, R., Peijnenburg, W., Klasinc, L., Kördel, W., Priest, N. and Tavares, T. 2003. Minimum requirements for reporting analytical data for environmental samples.(IUPAC Technical Report). Pure and Applied Chemistry. 75 (8), pp. 1097-1106. https://doi.org/10.1351/pac200375081097
Hydrocarbon removal in an experimental gravel bed constructed wetland
Shutes, B., Katima, J., Omari, K., Revitt, D. and Garelick, H. 2003. Hydrocarbon removal in an experimental gravel bed constructed wetland. Water Science & Technology. 48 (5), pp. 275-282. https://doi.org/10.2166/wst.2003.0333
An assessment of the toxicity of some pesticides and their metabolites affecting a natural aquatic environment using the Microtox (TM) system
Amoros, I., Connon, R., Garelick, H., Alonso, J. and Carrasco, J. 2000. An assessment of the toxicity of some pesticides and their metabolites affecting a natural aquatic environment using the Microtox (TM) system. Water Science & Technology. 42 (1-2), pp. 19-24. https://doi.org/10.2166/wst.2000.0285
Comparison and recovery of escherichia coli and thermotolerant coliforms in water with a chromogenic medium incubated at 41 and 44.5°C
Alonso, J., Soriano, A., Carbajo, O., Amoros, I. and Garelick, H. 1999. Comparison and recovery of escherichia coli and thermotolerant coliforms in water with a chromogenic medium incubated at 41 and 44.5°C. Applied Environmental Microbiology. 65 (8), pp. 3746-3749.
The microbiology associated with glycol removal in constructed wetlands
Chong, S., Garelick, H., Revitt, D., Shutes, B., Worrall, P. and Brewer, D. 1999. The microbiology associated with glycol removal in constructed wetlands. Water Science & Technology. 40 (3), pp. 99-107. https://doi.org/10.2166/wst.1999.0145
Quantitative determination of escherichia coli in water using CHROMagar® E. coli
Alonso, J., Amoros, I., Chong, S. and Garelick, H. 1996. Quantitative determination of escherichia coli in water using CHROMagar® E. coli. Journal of Microbiological Methods. 25 (3), pp. 309-315. https://doi.org/10.1016/0167-7012(96)00002-4
Preparation and immunogenicity of an inactivated hepatitis A vaccine
Pellegrini, V., Fineschi, N., Matteucci, G., Marsili, I., Nencioni, L., Puddu, M., Garelick, H. and Zuckerman, A. 1993. Preparation and immunogenicity of an inactivated hepatitis A vaccine. Vaccine. 11 (3), pp. 383-387. https://doi.org/10.1016/0264-410X(93)90204-B
Characterization of a hepatitis A virus strain suitable for vaccine production
Fineschi, N., Cavalieri, F., Garelick, H., Prugnola, A., Pellegrini, V. and Zuckerman, A. 1991. Characterization of a hepatitis A virus strain suitable for vaccine production. Journal of Hepatology. 13, pp. S146-S151. https://doi.org/10.1016/0168-8278(91)90048-G
Persistence of hepatitis A virus in fulminant hepatitis and after liver transplantation.
Fagan, E., Yousef, G., Brahm, J., Garelick, H., Mann, G., Wolstenholme, A., Portmann, B., Harrison, T., Mowbray, J., Mowat, A., Zuckerman, A. and Williams, D. 1990. Persistence of hepatitis A virus in fulminant hepatitis and after liver transplantation. Journal of Medical Virology. 30 (2), pp. 131-136. https://doi.org/10.1002/jmv.1890300210
Cytotoxicity of fusobacterium ulcerans
Adriaans, B. and Garelick, H. 1989. Cytotoxicity of fusobacterium ulcerans. Journal of Medical Microbiology. 29 (3), pp. 177-180. https://doi.org/10.1099/00222615-29-3-177
Comparison of edmonston-zagreb and schwarz strains of measles vaccine given by aerosol or subcutaneous injection
Khanum, S., Garelick, H., Nasir, U., Mann, G. and Tomkins, A. 1987. Comparison of edmonston-zagreb and schwarz strains of measles vaccine given by aerosol or subcutaneous injection. The Lancet. 329 (8525), pp. 150-153. https://doi.org/10.1016/S0140-6736(87)91978-7
Concentration of virus from tap water at ambient salt and pH levels using positively charged filter media
Garelick, H. and Scutt, J. 1981. Concentration of virus from tap water at ambient salt and pH levels using positively charged filter media. Water Research. 15 (7), pp. 815-816. https://doi.org/10.1016/0043-1354(81)90134-2