Dissemination of Extended-Spectrum Beta-Lactamase–Producing Enterobacteriaceae in an Urban Wastewater Treatment Plant and Their Emission to a River
Publication: Journal of Environmental Engineering
Volume 144, Issue 2
Abstract
Several studies have reported that wastewater treatment plants may facilitate the occurrence of resistant bacteria in effluents, creating a growing concern about their impact on animal and human health. For this study, 254 Enterobacteriaceae were isolated from influent wastewater, effluent wastewater, and sludge in a municipal wastewater treatment plant and from river water receiving their effluent, with a predominance of Klebsiella pneumoniae. Susceptibility tests showed that amikacine and ciprofloxacine were the most active antibiotics. High resistance rates () were observed with penicillins and cephalosporins. A set of 143 strains (56.30%) were defined as extended-spectrum beta- lactamase producers. The findings revealed a decrease in the rate of extended-spectrum beta-lactamase (ESBL)–producing Enterobacteriaceae in the effluent wastewater compared to influent wastewater. In addition, nonnegligible levels of these bacteria were found in the river water (17.50%) and sludge (29.41%). This study demonstrated that the municipal sewage may be a reservoir of the dissemination of extended-spectrum beta-lactamase–producing Enterobacteriaceae into the environment, thereby contaminating natural water resources. This survey highlighted the serious negative impact of discharging urban sewage into the environment on public health and suggests that the topic requires further evaluation and appropriate control techniques.
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Acknowledgments
This study was supported by the Ministry of Higher Education and Scientific Research of Algeria under Grant No. D01N01UN120120140002. The authors gratefully acknowledge Prof. Karim Elmahda for kindly supplying the referenced strains. They are also grateful to the operators at the WWTP for their assistance.
References
Al-Jaboobi, M., Bouksaim, M., Tijane, M., and El-Ariqi, S. (2013). “Agricultural quality evaluation of wastewater, used in Yemen vegetables production.” Middle-East J. Sci. Res., 16(5), 667–677.
Andersen, S. R. (1993). “Effects of wastewater treatment on the species composition and antibiotic resistance of coliform bacteria.” Current Microbiol., 26(2), 97–103.
Andersen, S. R., and Sandaa, R. A. (1994). “Distribution of tetracycline resistance among Gram-negative bacteria isolated from polluted and unpolluted marine sediments.” Appl. Environ. Microbiol., 60(3), 908–912.
APHA, AWWA, and WEF (American Public Health Association, American Water Works Association, and Water Environment Federation). (1998). Standard methods for the examination water and wastewater, Washington, DC.
Audic, J. M. (1990). “Evolution des technologies d’élimination des micro-organismes.” IFREMER- actes de colloques, 11, 133–148.
Auerbach, E. A., Seyfried, E. E., and McMahon, K. D. (2007). “Tetracycline resistance genes in activated sludge wastewater treatment plants.” Water Res., 41(5), 1143–1151.
Baba Ahmed, Z., Ayad, A., Mesli, E., Messai, Y., Bakour, R., and Drissi, M. (2012). “CTX-M-15 extended-spectrum β-lactamases in Enterobacteriaceae in the intensive care unit of Tlemcen Hospital, Algeria.” East. Mediterr. Health J., 18(4), 382–386.
Börjesson, S. (2009). “Antibiotic resistance in wastewater: Methicillin-resistant Staphylococcus aureus (MRSA) and antibiotic resistance genes.” Ph.D. dissertation, Division of Medical Microbiology, Linköping Univ., Linköping, Sweden.
Boxall, A. B., et al. (2012). “Pharmaceuticals and personal care products in the environment: What are the big questions?” Environ. Health Perspect., 120(9), 1221–1229.
Bush, K. (2009). “The importance of β-lactamases to the development of new β-lactams.” Antimicrobial drug resistance: Mechanisms of drug resistance, D. L. Mayers, ed., Springer Science and Business Media, Berlin.
CA-SFM (Comité de l”Antibiogramme de la Société Française de Microbiologie) (2012). “Recommandations.” Paris.
Chagas, T. P. G., et al. (2011). “Multiresistance, betalactamase-encoding genes and bacterial diversity in hospital wastewater in Rio de Janeiro, Brazil.” J. Appl. Microbiol., 111(3), 572–581.
Davison, J. (1999). “Genetic exchange between bacteria in the environment.” Plasmid, 42(2), 73–91.
Debabza, M., Mechai, A., and Chettibi, H. (2014). “Prevalence and characterization of extended- spectrum β- lactamase- producing Enterobacteriaceae isolated from hospital environments.” Asian J. Microbiol. Biotech. Environ. Sci., 16(2), 19–27.
De Boeck, H., Lunguya, O., Muyembe, J. J., Glupczynski, Y., and Jacobs, J. (2012). “Presence of extended-spectrum beta-lactamase-producing Enterobacteriaceae in waste waters, Kinshasa, the Democratic Republic of the Congo.” Eur. J. Clin. Microbiol. Infect Dis., 31(11), 3085–3088.
Dreschel, P., Scott, C. A., Raschid-Sally, L., Redwood, M., and Bahri, A. (2010). Wastewater irrigation and health-assessing and mitigating risk in low-income countries, Earthscan-IDRC-IWMI, London.
Drieux-Rouzet, L., and Jarlier, V. (2014). “Bactéries multirésistantes dans l’eau: modèles des entérobactéries productrices de bêta-lactamase à spectre étendu.” Revue Francophone des Laboratoires, 2014(460), 75–79.
Ferreira da Silva, M., Vaz-Moreira, I., Gonzalez-Pajuelo, M., Nunnes, O. C., and Manaia, C. M. (2007). “Antimicrobial resistance patterns in Enterobacteriaceae isolated from an urban wastewater treatment plant.” FEMS Microbiol. Ecol., 60(1), 166–176.
Ferro, G., Fiorentino, A., Alferez, M. C., Polo-López, M. I., Rizzo, L., and Fernández-Ibánez, P. (2015). “Urban wastewater disinfection for agricultural reuse: Effect of solar driven AOPs in the inactivation of a multidrug resistant E. coli strain.” Appl. Catal. B Environ., 178, 65–73.
Goni-Urriza, M., Le cardepuy, M., Aprin, C., Raymond, N., Caumette, P., and Quentin, C. (2000). “Impact of an urban effluent on antibiotic resistance of riverine Enterobacteriaceae and Aeromonas spp.” Appl. Environ. Microbiol., 66(1), 125–132.
Guardabassi, L., Petersen, A., Olsen, J. E., and Dalsgaard, A. (1998). “Antibiotic resistance in Acinetobacter spp. isolated from sewers receiving waste effluent from a hospital and a pharmaceutical plant.” Appl. Environ. Microbiol., 64(9), 3499–3502.
Guardabassi, L., Wong, D. M. L. F., and Dalsgaard, A. (2002). “The effects of tertiary wastewater treatment on the prevalence of antimicrobial resistant bacteria.” Water Res., 36(8), 1955–1964.
Iwane, T., Urase, T., and Yamamoto, K. (2001). “Possible impact of treated wastewater discharge on incidence of antibiotic resistant bacteria in river water.” Water Sci. Technol., 43(2), 91–99.
Jarlier, V., Nicolas, M. H., Fournier, G., and Philippon, A. (1988). “Extended broad spectrum β-lactamases conferring transferable resistance to newer β-lactam agents in Enterobacteriaceae: Hospital prevalence and susceptibility patterns.” Rev. Infect. Dis., 10(4), 867–878.
JORA (Journal officiel de la République Algérienne) N° 26. (2006). “Décret exécutif n° 06-141.” 4–9.
Kantachote, D., Dangtago, K., and Siriwong, C. (2009). “Treatment efficiency in wastewater treatment plant of Hat Yai Municipality by quantitative removal of microbial indicators.” Songklanakarin J. Sci. Technol., 31(5), 567–576.
Kelly, B. G., Vespermann, A., and Bolton, D. J. (2009). “Gene transfer events and their occurrence in selected environments.” Food Chem. Toxicol., 47(5), 978–983.
Kim, S., and Aga, D. S. (2007). “Potential ecological and human health impacts of antibiotics and antibiotic-resistant bacteria from wastewater treatment plants.” J. Toxicol. Environ. Health Part B, 10(8), 559–573.
Korzeniewska, E, and Harnisz, M. (2013a). “Extended-spectrum beta-lactamase (ESBL)-positive Enterobacteriaceae in municipal sewage and their emission to the environment.” J. Environ. Manage., 128, 904–911.
Korzeniewska, E., and Harnisz, M. (2012). “Culture-dependent and culture-independent methods in evaluation of emission of Enterobacteriaceae from sewage to the air and surface water.” Water Air Soil Pollut., 223(7), 4039–4046.
Korzeniewska, E., and Harnisz, M. (2013b). “Beta-lactamase-producing Enterobacteriaceae in hospital effluents.” J. Environ. Manage., 123, 1–7.
Korzeniewska, E., Korzeniewska, A., and Harnisz, M. (2013). “Antibiotic resistant Escherichia coli in hospital and municipal sewage and their emission to the environment.” Ecotoxicol. Environ. Saf., 91, 96–102.
Koton-Czarnecka, M., and Chróst, R. J. (2003). “Protozoans prefer large and metabolically active bacteria.” Pol. J. Environ. Stud., 12(3), 325–334.
Kruse, H., and Sorum, H. (1994). “Transfer of multiple drug resistance plasmids between bacteria of diverse origins in natural microenvironments.” Appl. Environ. Microbiol., 60(11), 4015–4021.
Li, B., Zhang, T., Xu, Z. Y., and Fang, H. H. P. (2009). “Rapid analysis of 21 antibiotics of multiple classes in municipal wastewater using ultra performance liquid chromatography-tandem mass spectrometry.” Anal. Chim. Acta., 645(1–2), 64–72.
López-Serna, R., Jurado, A., Vázquez-Suñé, E., Carrera, J., Petrović, M., and Barceló, D. (2013). “Occurrence of 95 pharmaceuticals and transformation products in urban ground waters underlying the metropolis of Barcelona, Spain.” Environ. Pollut., 174, 305–315.
Lorenz, M. G., and Wackernagel, W. (1994). “Bacterial gene transfer by natural genetic transformation in the environment.” Microbiol. Rev., 58(3), 563–602.
Mach, P. A., and Grimes, D. J. (1982). “R-plasmid transfer in a wastewater treatment plant.” Appl. Environ. Microbiol., 44(6), 1395–1403.
Manaia, C. M., Novo, A., Coelho, B., and Nunes, O. C. (2010). “Ciprofloxacin resistance in domestic wastewater treatment plants.” Water Air Soil Pollut., 208(1–4), 335–343.
Manivasagan, P., Rajaram, G., Ramesh, S., Ashokkumar, S., and Damotharan, P. (2011). “Occurrence and seasonal distribution of antibiotic resistance heterotrophic bacteria and physico-chemical characteristics of Muthupettai mangrove environment, southeast coast of India.” J. Environ. Sci. Technol., 4(2), 139–149.
Marti, E., Jofre, J., and Balcazar, J. L. (2013). “Prevalence of antibiotic resistance genes and bacterial community composition in a river influenced by a wastewater treatment plant.” PLoS ONE, 8(10), e78906.
Matyar, F., Kaya, A., and Dinçer, S. (2008). “Antibacterial agents and heavy metal resistance in Gram-negative bacteria isolated from seawater, shrimp and sediment in Iskenderun Bay, Turkey.” Sci. Total Environ., 407(1), 279–285.
Meradi, L., Djahoudi, A., Abdi, A., Bouchakour, M., Perrier Gros Claude, J. D., and Timinouni, M. (2011). “Resistance aux quinolones de types qnr, aac (6’)-Ib-cr chez les entérobactéries isolées à Annaba en Algérie.” Pathologie Biologie, 59(4), e73–e78.
Mesa, R. J., et al. (2006). “Extended-spectrum β-lactamase-producing Enterobacteriaceae in different environments (humans, food, animal farms and sewage).” J. Antimicrob. Chemother., 58(1), 211–215.
Mezrioui, N., and Echab, K. (1995). “Drug resistance in Salmonella strains isolated from domestic waste water before and after treatment in stabilization ponds in an arid region (Marrakech, Morocco).” World J. Microbiol. Biotechnol., 11(3), 287–290.
Michael, I., et al. (2013). “Urban wastewater treatment plants as hotspots for the release of antibiotics in the environment: A review.” Water Res., 47(3), 957–995.
Minitab 16 [Computer software]. Minitab, Inc., Paris.
Nedjai, S., et al. (2012). “Prevalence and characterization of extended spectrum β-lactamases in Klebsiella-Enterobacter-Serratia group bacteria, in Algeria.” Médecine et maladies infectieuses, 42(1), 20–29.
Ojer-Usoz, E., Gonzalez, D., Garcia-Jalon, I., and Vitas, A. I. (2014). “High dissemination of extended-spectrum β-lactamase-producing Enterobacteriaceae in effluents from wastewater treatment plants.” Water Res., 56, 37–47.
Passerat, J., and Servais, P. (2008). “Occurrence et origines des bactéries fécales antibiorésistantes (E. coli et entérocoques) dans le bassin de la Seine [Occurrence and origin of antibiotic-resistant fecal bacteria (E. coli and enterococci) in the Seine basin].” Rapport PIREN-Seine 2007.
Prado, T., Pereira, W. C., Silva, D. M., Seki, L. M., Carvalho, A. P., and Asensi, M. D. (2008). “Detection of extended-spectrum beta-lactamase-producing Klebsiella pneumoniae in effluents and sludge of a hospital sewage treatment plant.” Lett. Appl. Microbiol., 46(1), 136–141.
Rahal, K. (2005). Standardisation de l’antibiogramme en Médecine Humaine à l’échelle nationale selon les recommandations de l’OMS, 4ème édition, Ministère de la santé, de la population et de la reforme hospitalière, Algérie.
Rizzo, L., et al. (2013). “Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: A review.” Sci. Total Environ., 447, 345–360.
Saddoud, A., Ellouze, M., Dhouib, A., and Sayadi, S. (2007). “Anaerobic membrane bioreactor treatment of domestic wastewater in Tunisia.” Desalination, 207(1–3), 205–215.
Scheierling, S. M., Bartone, C. R., Mara, D. D., and Drechsel, P. (2011). “Towards an agenda for improving wastewater use in agriculture.” Water Int., 36(4), 420–440.
Schlüter, A., et al. (2003). “The 64 508 bp IncP-1beta antibiotic multiresistance plasmid pB10 isolated from a waste-water treatment plant provides evidence for recombination between members of different branches of the IncP-1beta group.” Microbiology, 149(11), 3139–3153.
Schlüter, A., Krause, L., Szczepanowski, R., Goesmann, A., and Pühler, A. (2008). “Genetic diversity and composition of a plasmid metagenome from a wastewater treatment plant.” J. Biotechnol., 136(1–2), 65–76.
Schlüter, A., Szczepanowski, R., Pühler, A., and Top, E. M. (2007). “Genomics of IncP-1 antibiotic resistance plasmids isolated from wastewater treatment plants provides evidence for a widely accessible drug resistance gene pool.” FEMS Microbiol. Rev., 31(4), 449–477.
Silva, J., Castillo, G., Callejas, L., López, H., and Olmos, J. (2006). “Frequency of transferable multiple antibiotic resistance amongst coliform bacteria isolated from a treated sewage effluent in Antofagasta, Chile.” Electron. J. Biotechnol., 9(5), 533–540.
Szczepanowski, R., et al. (2009). “Detection of 140 clinically relevant antibioticresistance genes in the plasmid metagenome of wastewater treatment plant bacteria showing reduced susceptibility to selected antibiotics.” Microbiology, 155(7), 2306–2319.
Thomas, C. M., and Nielsen, K. M. (2005). “Mechanisms of, and barriers to, horizontal gene transfer between bacteria.” Nat. Rev. Microbiol., 3(9), 711–721.
Thomson, K. S., and Sanders, C. C. (1992). “Detection of extended spectrum beta-lactamases in members of the family Enterobacteriaceae: Comparison of the double-disk and three-dimensional tests.” Antimicrob. Agents Chemother., 36(9), 1877–1882.
Touati, A., Medboua, C., Touati, D., Denine, R., Brasme, L., and De Champs, C. (2012). “CTX-M-15-producing Enterobacteriaceae isolates causing bloodstream infections at the Beni-Messous hospital in Algiers (Algeria).” Int. Res. J. Microbiol., 3(5), 181–185.
Wagner, M., Loy, A., Nogueira, R., Purkhold, U., Lee, N., and Daims, H. (2002). “Microbial community composition and function in wastewater treatment plants.” Antonie Van Leeuwenhoek, 81(1–4), 665–680.
Walther-Rasmussen, J., and Hoiby, N. (2004). “Cefotaximases (CTX-M-ases), an expanding family of extended-spectrum β-lactamases.” Can. J. Microbiol., 50(3), 137–165.
Yagoubi, M., Foutlane, A., Bourchich, L., Jellal, J., Wittland, C., and El Yachioui, M. (2000). “Study on the performance of the wastewater stabilisation pond of Boujaad, Morocco.” J. Water Serv. Res. Technol. AQUA, 49(4), 203–209.
Ye, L., and Zhang, T. (2013). “Bacterial communities in different sections of a municipal wastewater treatment plant revealed by 16S rDNA 454 pyrosequencing.” Appl. Microbiol. Biotechnol., 97(6), 2681–2690.
Zhang, Y., Marrs, C. F., Simon, C., and Xi, C. (2009). “Wastewater treatment contributes to selective increase of antibiotic resistance among Acinetobacter spp.” Sci. Total Environ., 407(12), 3702–3706.
Zou, S., Xu, W., Zhang, R., Tang, J., Chen, Y., and Zhang, G. (2011). “Occurrence and distribution of antibiotics in coastal water of the Bohai Bay, China: Impacts of river discharge and aquaculture activities.” Environ. Pollut., 159(10), 2913–2920.
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Published In
Journal of Environmental Engineering
Volume 144 • Issue 2 • February 2018
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©2017 American Society of Civil Engineers.
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Received: Jan 4, 2017
Accepted: Jun 26, 2017
Published online: Nov 23, 2017
Published in print: Feb 1, 2018
Discussion open until: Apr 23, 2018
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