Resistant Genes and Multidrug-Resistant Bacteria in Wastewater: A Study of Their Transfer to the Water Reservoir in the Czech Republic

. 2022 Jan 20 ; 12 (2) : . [epub] 20220120

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid35207435

Grantová podpora
SGS09/PřF/2019 University of Ostrava
SGS01/PřF/2020 University of Ostrava
SGS11/PřF/2021 University of Ostrava
UNCE/SCI/006 Center for Geosphere Dynamics
CZ.02.1.01/0.0/0.0/17\_049/0008441 Operational Programme Research, Development and Education

Wastewater is considered the most serious source of the spread of antibiotic resistance in the environment. This work, therefore, focuses on the fate and spread of antibiotic resistance genes (ARGs) in wastewater and the monitoring of multidrug-resistant strains. ARGs were monitored in the nitrification and sedimentation tanks of the wastewater treatment plant (WWTP) and in the dam into which this WWTP flows, at various times. The highest relative abundance was found for the blaTEM > tetW > blaNDM-1 > vanA resistance genes, respectively. An increased concentration of tetracycline (up to 96.00 ng/L) and ampicillin (up to 19.00 ng/L) was found in water samples compared to other antibiotics detected. The increased incidence of seven ARGs and four antibiotics was observed in the November and December sampling times. Isolated ampicillin-resistant strains showed a high degree of resistance to ampicillin (61.2% of the total isolates had a minimum inhibitory concentration (MIC) ≥ 20 mg/mL). In 87.8% of isolates, out of the total number, the occurrence of two or more ARGs was confirmed. These multidrug-resistant strains were most often identified as Aeromonas sp. This strain could represent a significant role in the spread of multidrug resistance through wastewater in the environment.

Zobrazit více v PubMed

Kumar M., Sarma D.K., Shubham S., Kumawat M., Verma V., Nina P.B., Jp D., Kumar S., Singh B., Tiwari R.R. Futuristic Non-antibiotic Therapies to Combat Antibiotic Resistance: A Review. Front. Microbiol. 2021;12:609459. doi: 10.3389/fmicb.2021.609459. PubMed DOI PMC

Pazda M., Kumirska J., Stepnowski P., Mulkiewicz E. Antibiotic resistance genes identified in wastewater treatment plant systems—A review. Sci. Total Environ. 2019;697:134023. doi: 10.1016/j.scitotenv.2019.134023. PubMed DOI

Zhang T., Zhang X.X., Ye L. Plasmid metagenome reveals high levels of antibiotic resistance genes and mobile genetic elements in activated sludge. PLoS ONE. 2011;6:e26041. doi: 10.1371/journal.pone.0026041. PubMed DOI PMC

Amarasiri M., Sano D., Suzuki S. Understanding human health risks caused by antibiotic resistant bacteria (ARB) and antibiotic resistance genes (ARG) in water environments: Current knowledge and questions to be answered. Crit. Rev. Environ. Sci. Technol. 2020;50:2016–2059. doi: 10.1080/10643389.2019.1692611. DOI

Czekalski N., Sigdel R., Birtel J., Matthews B., Bürgmann H. Does human activity impact the natural antibiotic resistance background? Abundance of antibiotic resistance genes in 21 Swiss lakes. Environ. Int. 2015;81:45–55. doi: 10.1016/j.envint.2015.04.005. PubMed DOI

Rizzo L., Manaia C., Merlin C., Schwartz T., Dagot C., Ploy M.C., Michael I., Fatta-Kassinos D. Urban wastewater treatment plants as hotspots for antibiotic resistant bacteria and genes spread into the environment: A review. Sci. Total Environ. 2013;447:345–360. doi: 10.1016/j.scitotenv.2013.01.032. PubMed DOI

Suda K.J., Hicks L.A., Roberts R.M., Hunkler R.J., Taylor T.H. Trends and seasonal variation in outpatient antibiotic prescription rates in the United States, 2006 to 2010. Antimicrob. Agents Chemother. 2014;58:2763–2766. doi: 10.1128/AAC.02239-13. PubMed DOI PMC

Sun L., Klein E.Y., Laxminarayan R. Seasonality and temporal correlation between community antibiotic use and resistance in the United States. Clin. Infect Dis. 2012;55:687–694. doi: 10.1093/cid/cis509. PubMed DOI

Makowska N., Bresa K., Koczura R., Philips A., Nowis K., Mokracka J. Urban wastewater as a conduit for pathogenic Gram-positive bacteria and genes encoding resistance to β-lactams and glycopeptides. Sci. Total Environ. 2021;765:144176. doi: 10.1016/j.scitotenv.2020.144176. PubMed DOI

Osińska A., Korzeniewska E., Harnisz M., Niestępski S. Quantitative Occurrence of Antibiotic Resistance Genes among Bacterial Populations from Wastewater Treatment Plants Using Activated Sludge. Appl. Sci. 2019;9:387. doi: 10.3390/app9030387. DOI

Karkman A., Do T.T., Walsh F., Virta M.P.J. Antibiotic-resistance genes in waste water. Trends Microbiol. 2018;26:220–228. doi: 10.1016/j.tim.2017.09.005. PubMed DOI

Korzeniewska E., Harnisz M. Relationship between modification of activated sludge wastewater treatment and changes in antibiotic resistance of bacteria. Sci. Total Environ. 2018;639:304–315. doi: 10.1016/j.scitotenv.2018.05.165. PubMed DOI

Zieliński W., Buta M., Hubeny J., Korzeniewska E., Harnisz M., Nowrotek M., Płaza G. Prevalence of Beta Lactamases Genes in Sewage and Sludge Treated in Mechanical-Biological Wastewater Treatment Plants. Ecol. Eng. 2019;20:80–86. doi: 10.12911/22998993/112506. DOI

Mbanga J., Amoako D.G., Abia A.L.K., Allam M., Ismail A., Essack S.Y. Genomic Insights of Multidrug-Resistant Escherichia coli From Wastewater Sources and Their Association With Clinical Pathogens in South Africa. Front. Vet. Sci. 2021;8:636715. doi: 10.3389/fvets.2021.636715. PubMed DOI PMC

Lépesová K., Olejníková P., Mackuľak T., Cverenkárová K., Krahulcová M., Bírošová L. Hospital Wastewater—Important Source of Multidrug Resistant Coliform Bacteria with ESBL-Production. Int. J. Environ. Res. Public Health. 2020;17:7827. doi: 10.3390/ijerph17217827. PubMed DOI PMC

Chia P., Sengupta S., Kukreja A., Ponnampalavanar S.S.L., Ng O.T., Marimuthu K. The role of hospital environment in transmissions of multidrug-resistant gram-negative organisms. Antimicrob. Resist. Infect. Control. 2020;9:29. doi: 10.1186/s13756-020-0685-1. PubMed DOI PMC

Mody L., Washer L.L., Kaye K.S., Gibson K., Saint S., Reyes K., Cassone M., Mantey J., Cao J., Altamimi S., et al. Multidrug-resistant Organisms in Hospitals: What Is on Patient Hands and in Their Rooms? Clin. Infect Dis. 2019;69:1837–1844. doi: 10.1093/cid/ciz092. PubMed DOI PMC

Rodríguez E.A., Garzón L.M., Gómez I.D., Jiménez J.N. Multidrug resistance and diversity of resistance profiles in carbapenem-resistant Gram-negative bacilli throughout a wastewater treatment plant in Colombia. J. Glob. Antimicrob. Resist. 2020;22:358–366. doi: 10.1016/j.jgar.2020.02.033. PubMed DOI

Martinez J.L. The role of natural environments in the evolution of resistance traits in pathogenic bacteria. Proc. Biol. Sci. 2009;276:2521–2530. doi: 10.1098/rspb.2009.0320. PubMed DOI PMC

Stachurová T., Piková H., Bartas M., Semerád J., Svobodová K., Malachová K. Beta-lactam resistance development during the treatment processes of municipal wastewater treatment plants. Chemosphere. 2021;280:130749. doi: 10.1016/j.chemosphere.2021.130749. PubMed DOI

Honda R., Tachi C., Yasuda K., Hirata T., Noguchi M., Hara-Yamamura H., Yamamoto-Ikemoto R., Watanabe T. Estimated discharge of antibiotic-resistant bacteria from combined sewer overflows of urban sewage system. npj Clean Water. 2020;3:15. doi: 10.1038/s41545-020-0059-5. DOI

Barancheshme F., Munir M. Strategies to combat antibiotic resistance in the wastewater plants. Front. Microbiol. 2018;8:2603. doi: 10.3389/fmicb.2017.02603. PubMed DOI PMC

SUKL (State Institution of Drug Control) Consumption of Antibiotics in the Czech Republic in the Years 2008–2018—Part 1. [(accessed on 12 January 2022)]. Available online: https://www.sukl.cz/file/92111_1_1.

SUKL (State Institution of Drug Control) Consumption of Antibiotics in the Czech Republic in the Years 2008–2018—Part 2. [(accessed on 12 January 2022)]. Available online: https://www.sukl.cz/file/92415_1_1.

Fouz N., Pangesti K.N.A., Yasir M., Al-Malki A.L., Azhar E.I., Hill-Cawthorne G.A., Abd El Ghany M. The Contribution of Wastewater to the Transmission of Antimicrobial Resistance in the Environment: Implications of Mass Gathering Settings. Trop. Med. Infect. Dis. 2020;5:33. doi: 10.3390/tropicalmed5010033. PubMed DOI PMC

Klančnik A., Piskernik S., Jeršek B., Smole Možina S. Evaluation of diffusion and dilution methods to determine the antibacterial activity of plant extracts. J. Microbiol. Methods. 2010;81:121–126. doi: 10.1016/j.mimet.2010.02.004. PubMed DOI

Svobodová K., Semerád J., Petráčková D., Novotný Č. Antibiotic resistance in Czech urban wastewater treatment plants: Microbial and molecular genetic characterization. Microb. Drug Resist. 2018;24:830–838. doi: 10.1089/mdr.2017.0406. PubMed DOI

Stach J.E.M., Bathe S., Clapp J.P., Burns R.G. PCR-SSCP comparison of 16S rDNA sequence diversity in soil DNA obtained using different isolation and purification methods. FEMS Microbiol. Ecol. 2001;36:139–151. doi: 10.1111/j.1574-6941.2001.tb00834.x. PubMed DOI

Mlynarcik P., Roderova M., Kolar M. Primer Evaluation for PCR and its Application for Detection of Carbapenemases in Enterobacteriaceae. Jundishapur J. Microbiol. 2016;9:e29314. doi: 10.5812/jjm.29314. PubMed DOI PMC

Ribeiro P.C.S., Monteiro A.S., Marques S.G., Monteiro S.G., Monteiro-Neto V., Coqueiro M.M., Marques A.C., de Jesus Gomes Turri R., Santos S.G. Phenotypic and molecular detection of the blaKPC gene in clinical isolates from inpatients at hospitals in São Luis, MA, Brazil. BMC Infect. Dis. 2016;16:737. doi: 10.1186/s12879-016-2072-3. PubMed DOI PMC

Marti E., Jofre J., Balcazar J.L. Prevalence of antibiotic resistance genes and bacterial community composition in a river influenced by a wastewater treatment plant. PLoS ONE. 2013;8:e78906. doi: 10.1371/journal.pone.0078906. PubMed DOI PMC

Rathnayake I.U., Hargreaves M., Huygens F. Antibiotic resistance and virulence traits in clinical and environmental Enterococcus faecalis and Enterococcus faecium isolates. Syst. Appl. Microbiol. 2012;35:326–333. doi: 10.1016/j.syapm.2012.05.004. PubMed DOI

Colomer-Lluch M., Jofre J., Muniesa M. Antibiotic resistance genes in the bacteriophage DNA fraction of environmental samples. PLoS ONE. 2011;6:e17549. doi: 10.1371/journal.pone.0017549. PubMed DOI PMC

Poirel L., Walsh T.R., Cuvillier V., Nordmann P. Multiplex PCR for detection of acquired carbapenemase genes. Diagn. Microbiol. Infect. Dis. 2011;70:119–123. doi: 10.1016/j.diagmicrobio.2010.12.002. PubMed DOI

Heuer H., Krsek M., Baker P., Smalla K., Wellington E.M. Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl. Environ. Microbiol. 1997;63:3233–3241. doi: 10.1128/aem.63.8.3233-3241.1997. PubMed DOI PMC

Novo A., Manaia C. Factors influencing antibiotic resistance burden in municipal wastewater treatment plants. Appl. Microbiol. Biotechnol. 2010;87:1157–1166. doi: 10.1007/s00253-010-2583-6. PubMed DOI

Mukherjee M., Laird E., Gentry T.J., Brooks J.P., Karthikeyan R. Increased Antimicrobial and Multidrug Resistance Downstream of Wastewater Treatment Plants in an Urban Watershed. Front. Microbiol. 2021;12:657353. doi: 10.3389/fmicb.2021.657353. PubMed DOI PMC

Kulkarni P., Olson N.D., Raspanti G.A., Rosenberg Goldstein R.E., Gibbs S.G., Sapkota A., Sapkota A.R. Antibiotic Concentrations Decrease during Wastewater Treatment but Persist at Low Levels in Reclaimed Water. Int. J. Environ. Res. Public Health. 2017;14:668. doi: 10.3390/ijerph14060668. PubMed DOI PMC

Gulkowska A., Leung H.W., So M.K., Taniyasu S., Yamashita N., Yeung L.W.Y., Richardson B.J., Lei A.P., Giesy J.P., Lam P.K.S. Removal of antibiotics from wastewater by sewage treatment facilities in Hong Kong and Shenzhen, China. Water Res. 2008;42:395–403. doi: 10.1016/j.watres.2007.07.031. PubMed DOI

Zhang J., Chen M., Sui Q., Tong J., Jiang C., Lu X., Zhang Y., Wei Y. Impacts of addition of natural zeolite or a nitrification inhibitor on antibiotic resistance genes during sludge composting. Water Res. 2016;91:339–349. doi: 10.1016/j.watres.2016.01.010. PubMed DOI

Hembach N., Alexander J., Hiller C., Wieland A., Schwartz T. Dissemination prevention of antibiotic resistant and facultative pathogenic bacteria by ultrafiltration and ozone treatment at an urban wastewater treatment plant. Sci. Rep. 2019;9:12843. doi: 10.1038/s41598-019-49263-1. PubMed DOI PMC

Rafraf I.D., Lekunberri I., Sànchez-Melsió A., Aouni M., Borrego C.M., Balcázar J.L. Abundance of antibiotic resistance genes in five municipal wastewater treatment plants in the Monastir Governorate, Tunisia. Environ. Pollut. 2016;219:353–358. doi: 10.1016/j.envpol.2016.10.062. PubMed DOI

Hu Z., Chen W., Guo G., Dong C., Shen Y., Qin S., Chen L., Zhang W. An Escherichia coli isolate from hospital sewage carries blaNDM-1 and blaoxa-10. Arch. Microbiol. 2021;203:4427–4432. doi: 10.1007/s00203-021-02431-2. PubMed DOI

Ebomah K.E., Okoh A.I. Enterobacter cloacae harbouring blaNDM-1, blaKPC, and blaOXA-48-like carbapenem-resistant genes isolated from different environmental sources in South Africa. Int. J. Environ. Sci. 2021;78:151–164. doi: 10.1080/00207233.2020.1778274. DOI

Thakali O., Malla B., Tandukar S., Sthapit N., Raya S., Furukawa T., Sei K., Sherchand J.B., Haramoto E. Release of Antibiotic-Resistance Genes from Hospitals and a Wastewater Treatment Plant in the Kathmandu Valley, Nepal. Water. 2021;13:2733. doi: 10.3390/w13192733. DOI

Liu H., Zhou X., Huang H., Zhang J. Prevalence of Antibiotic Resistance Genes and Their Association with Antibiotics in a Wastewater Treatment Plant: Process Distribution and Analysis. Water. 2019;11:2495. doi: 10.3390/w11122495. DOI

Oravcova V., Mihalcin M., Zakova J., Pospisilova L., Masarikova M., Literak I. Vancomycin-resistant enterococci with vanA gene in treated municipal wastewater and their association with human hospital strains. Sci. Total Environ. 2017;609:633–643. doi: 10.1016/j.scitotenv.2017.07.121. PubMed DOI

Kristich C.J., Rice L.B., Arias C.A. Enterococcal infection-treatment and antibiotic resistance. In: Gilmore M.S., Clewell D.B., Ike Y., Shankar N., editors. Enterococci: From Commensals to Leading Causes of Drug Resistant Infection. Massachusetts Eye and Ear Infirmary; Boston, MA, USA: 2014. pp. 1–99. PubMed

Caucci S., Karkman A., Cacace D., Rybicki M., Timpel P., Voolaid V., Gurke R., Virta M., Berendonk T.U. Seasonality of antibiotic prescriptions for outpatients and resistance genes in sewers and wastewater treatment plant outflow. FEMS Microbiol. Ecol. 2016;92:fiw060. doi: 10.1093/femsec/fiw060. PubMed DOI

Obayiuwana A., Ogunjobi A., Yang M., Ibekwe M. Characterization of Bacterial Communities and Their Antibiotic Resistance Profiles in Wastewaters Obtained from Pharmaceutical Facilities in Lagos and Ogun States, Nigeria. Int. J. Environ. Res. Public Health. 2018;15:1365. doi: 10.3390/ijerph15071365. PubMed DOI PMC

Aslan A., Cole Z., Bhattacharya A., Oyibo O. Presence of Antibiotic-Resistant Escherichia coli in Wastewater Treatment Plant Effluents Utilized as Water Reuse for Irrigation. Water. 2018;10:805. doi: 10.3390/w10060805. DOI

Stachurová T., Malachová K., Semerád J., Sterniša M., Rybková Z., Možina S.S. Tetracycline Induces the Formation of Biofilm of Bacteria from Different Phases of Wastewater Treatment. Processes. 2020;8:989. doi: 10.3390/pr8080989. DOI

Harnisz M., Kiedrzyńska E., Kiedrzyński M., Korzeniewska E., Czatzkowska M., Koniuszewska I., Jóźwik A., Szklarek S., Niestępski S., Zalewski M. The impact of WWTP size and sampling season on the prevalence of antibiotic resistance genes in wastewater and the river system. Sci. Total Environ. 2020;741:140466. doi: 10.1016/j.scitotenv.2020.140466. PubMed DOI

Skwor T., Stringer S., Haggerty J., Johnson J., Duhr S., Johnson M., Seckinger M., Stemme M. Prevalence of Potentially Pathogenic Antibiotic-Resistant Aeromonas spp. in Treated Urban Wastewater Effluents versus Recipient Riverine Populations: A 3-Year Comparative Study. Appl. Environ. Microbiol. 2020;86:e02053-19. doi: 10.1128/AEM.02053-19. PubMed DOI PMC

Oliveira H., Pinto G., Oliveira A., Noben J.P., Hendrix H., Lavigne R., Łobocka M., Kropinski A.M., Azeredo J. Characterization and genomic analyses of two newly isolated Morganella phages define distant members among Tevenvirinae and Autographivirinae subfamilies. Sci. Rep. 2017;7:46157. doi: 10.1038/srep46157. PubMed DOI PMC

Luczkiewicz A., Kotlarska E., Artichowicz W., Tarasewicz K., Fudala-Ksiaze S. Antimicrobial resistance of Pseudomonas spp. isolated from wastewater and wastewater-impacted marine coastal zone. Environ. Sci. Pollut. Res. 2015;22:19823–19834. doi: 10.1007/s11356-015-5098-y. PubMed DOI PMC

Piotrowska M., Kowalska S., Popowska M. Diversity of β-lactam resistance genes in gram-negative rods isolated from a municipal wastewater treatment plant. Ann. Microbiol. 2019;69:591–601. doi: 10.1007/s13213-019-01450-1. DOI

Alam A.N., Sarvari J., Motamedifar M., Khoshkharam H., Yousefi M., Moniri R., Bazargani A. The occurrence of blaTEM, blaSHV and blaOXA genotypes in Extended-Spectrum β-Lactamase (ESBL)-producing Pseudomonas aeruginosa strains in Southwest of Iran. Gene Rep. 2018;13:19–23. doi: 10.1016/j.genrep.2018.08.002. DOI

Mahrouki S., Perilli M., Bourouis A., Chihi H., Ferjani M., Moussa M.B., Amicosante G., Belhadj O. Prevalence of quinolone resistance determinant qnrA6 among broad- and extended-spectrum beta-lactam-resistant Proteus mirabilis and Morganella morganii clinical isolates with sul1-type class 1 integron association in a Tunisian hospital. Scand. J. Infect. Dis. 2013;45:600–605. doi: 10.3109/00365548.2013.795657. PubMed DOI

Obayiuwana A., Ibekwe A.M. Antibiotic Resistance Genes Occurrence in Wastewaters from Selected Pharmaceutical Facilities in Nigeria. Water. 2020;12:1897. doi: 10.3390/w12071897. DOI

Horcajada J.P., Montero M., Oliver A., Sorlí L., Luque S., Gómez-Zorrilla S., Benito N., Grau S. Epidemiology and Treatment of Multidrug-Resistant and Extensively Drug-Resistant Pseudomonas aeruginosa Infections. Clin. Microbiol. Rev. 2019;32:e00031-19. doi: 10.1128/CMR.00031-19. PubMed DOI PMC

Pachori P., Gothalwal R., Gandhi P. Emergence of antibiotic resistance Pseudomonas aeruginosa in intensive care unit; a critical review. Genes Dis. 2019;6:109–119. doi: 10.1016/j.gendis.2019.04.001. PubMed DOI PMC

Devatha C.P., Pavithra N. Isolation and identification of Pseudomonas from wastewater, its immobilization in cellulose biopolymer and performance in degrading Triclosan. J. Environ. Manag. 2019;232:584–591. doi: 10.1016/j.jenvman.2018.11.083. PubMed DOI

Batrich M., Maskeri L., Schubert R., Ho B., Kohout M., Abdeljaber M., Abuhasna A., Kholoki M., Psihogios P., Razzaq T., et al. Pseudomonas Diversity Within Urban Freshwaters. Front. Microbiol. 2019;10:195. doi: 10.3389/fmicb.2019.00195. PubMed DOI PMC

Chang Q., Wang W., Regev-Yochay G., Lipsitch M., Hanage W.P. Antibiotics in agriculture and the risk to human health: How worried should we be? Evol. Appl. 2015;8:240–245. doi: 10.1111/eva.12185. PubMed DOI PMC

Pérez-Etayo L., González D., Leiva J., Vitas A.I. Multidrug-Resistant Bacteria Isolated from Different Aquatic Environments in the North of Spain and South of France. Microorganisms. 2020;8:1425. doi: 10.3390/microorganisms8091425. PubMed DOI PMC

Amador P.P., Fernandes R.M., Prudêncio M.C., Barreto M.P., Duarte I.M. Antibiotic resistance in wastewater: Occurrence and fate of Enterobacteriaceae producers of Class A and Class C β-lactamases. J. Environ. Sci. Health A. 2015;50:26–39. doi: 10.1080/10934529.2015.964602. PubMed DOI

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Bacterial Infections, Antimicrobial Resistance and Antibiotic Therapy

. 2022 Mar 23 ; 12 (4) : . [epub] 20220323

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...